The anuran family Rhinophrynidae today comprises a single species restricted to southernmost Texas and Central America. Three extinct genera allied to this family are known from the Jurassic (Rhadinosteus) and Eocene (Chelomophrynus, Eorhinophrynus), whereas the sole extant genus Rhinophrynus is known from the latest Eocene (Chadronian) of Saskatchewan and the Pleistocene of Mexico. We provide the first records of the Rhinophrynidae from the Oligocene of eastern North America. From two of the oldest terrestrial vertebrate sites on the Florida peninsula (I-75, early Oligocene; Brooksville 2, late Oligocene), we have identified one nearly complete and several partial humeri, two radioulnae, two partial presacral vertebrae, three partial ilia, and one femur that are all referable to the Rhinophrynidae. These specimens are similar in size to the Eocene Rhinophrynus canadensis, smaller than the extant R. dorsalis, and might be distinguishable from both by features of the ilium and humerus. The presence of rhinophrynids during the Oligocene provides the first indication of change in the anuran fauna on the Florida peninsula during the Cenozoic.
The Florida peninsula in the southeastern United States hosts a rich fauna of frogs and toads (Order Anura) with nearly 30 native species representing five families. In addition to the present-day species, fossils of anurans are known from terrestrial deposits in Florida from the Oligocene, Miocene, Pliocene, and Pleistocene (Table 1). These fossils indicate that each of the extant genera, including Acris (Hylidae), Anaxyrus (family Bufonidae), Gastrophryne (Microhylidae), Hyla (or Dryophytes following Duellman et al., 2016; Hylidae), Pseudacris (Hylidae), Rana (Ranidae), and Scaphiopus (Scaphiopodidae) has been present on the Florida peninsula for at least the past 18—and possibly past 30—million years (Pratt, 1989; Morgan, 1993; Table 1). Unlike many other vertebrate groups (Hulbert, 2001), there are no definitive examples of anuran families known from the fossil record of Florida that are not represented among its extant species.
Summary references on fossils of anuran genera native to the Florida peninsula organized by epoch. Note that all toad fossils in Florida have been reported previously as Bufo, though we treat them here as the genus Anaxyrus that is native to North America.
Among North American frogs, the family Rhinophrynidae is among the most morphologically distinctive. This family and the Pipidae together comprise the Pipoidea, which originated in the Jurassic and is among the earliest diverging lineages of extant anurans (Cannatella, 2015; Feng et al., 2017). The single extant species Rhinophrynus dorsalis is today restricted to southernmost Texas, Mexico, and Central America, where it occurs in semiarid and arid areas with loose soils conducive to digging (Dodd, 2013); it has been reported from the Pleistocene of Mexico (Holman, 1969). In addition, extinct taxa that are more closely related to Rhinophrynus than to other pipoid anurans are known from the Mesozoic and Cenozoic of North America, including Rhadinosteus from the Jurassic of Utah (Henrici, 1998), Eorhinophrynus from the Paleocene of Wyoming (Hecht, 1959; Estes, 1975; Krause, 1980), Chelomophrynus from the Eocene of Wyoming (Henrici, 1991; Henrici and Fiorillo, 1993), and the extinct Rhinophrynus canadensis from the Eocene of Saskatchewan (Holman, 1963, 1968, 1969, 1972; Roček and Rage, 2000). To date, there are no Mesozoic or Cenozoic records attributed to the Rhinophrynidae sensu lato from eastern North America (Henrici, 2016).
We report fossils referable to Rhinophrynus from two Oligocene sites in Florida. The majority of the fossils come from Brooksville 2, a site comprised of karst fissure fillings in the Suwanee Limestone near Brooksville, Florida that is one of the earliest terrestrial vertebrate sites in Florida (Arikareean, 26–28 mya; Hayes, 2000). In addition, one humerus comes from the I-75 site (Whitneyean; ∼30 mya; Morgan and Czaplewski, 2003) from which several anurans were briefly listed but never described (Patton, 1969; Meylan, 1984; Hulbert, 2001). We provide the first description of any anuran material from the Oligocene of the Florida peninsula and of the Rhinophrynidae from anywhere in eastern North America. In addition to documenting a formerly more widespread distribution of this family, we discuss the first glimpse into possible faunal turnover of anurans on the Florida peninsula during the Cenozoic.
Materials and Methods
Sampling.—The fossils reported here (Fig. 1) were identified after sorting through anurans isolated after screen-washing matrix from both sites. After comparing these fossils to extant species that are exemplars of all current North American and Caribbean anuran genera, we determined that a subset of these represented a taxon not previously described from the Florida peninsula that we discuss below (Fig. 2). The remainder of the anuran faunas from both the I-75 and Brooksville 2 sites will be described elsewhere. Institutional abbreviations for specimens studied are as follows: CAS, California Academy of Sciences, San Francisco, USA; UF-VP, Division of Vertebrate Paleontology, Florida Museum of Natural History, University of Florida, Gainesville, USA.
CT Scanning.—Following identification, we generated digital three-dimensional models of fossil specimens and comparative material from alcohol-preserved extant specimens using X-ray computed microtomography (CT) at the University of Florida's Nanoscale Research Facility. For this characterization, we used a Phoenix vjtomejx M (GE Measurement & Control, Boston, Massachusetts, USA) scanner with a 240-kV X-ray tube and a tungsten target, modifying X-ray generation and detector settings to optimize resolution and contrast (resolution 4.6–78 µm; see Appendix for details). Raw 2D X-ray data were converted to tomograms using the datosjx software v. 2.3 with postprocessing, analyses (including segmentation and measurement), and visualization conducted using VG StudioMax v. 3.2 (Volume Graphics, Heidelberg, Germany). For comparisons, we generated comparable models for two fluid-preserved specimens (CAS-Herp-71766; UF-Herp-13375-4) of Rhinophrynus dorsalis, as well as exemplars of other North American taxa (Fig. 2). Our anatomical terminology follows Delfino (2017), Gómez and Turazzini (2016), and Trueb et al. (2011). Tomogram data and mesh files for all fossils and comparative specimens are available via morphosource.org (Appendix Tables 1 and 2), which enables users to view all of the discussed elements in additional views (including material not figured here).
Amphibia Linnaeus, 1758
Anura Fischer von Waldheim, 1813
Pipoidea Gray, 1825
Rhinophrynidae Günther, 1859
Rhinophrynus Duméril & Bibron, 1841
Rhinophrynus sp. indet.
Referred Material.—Brooksville 2 Quarry 1A (locality HE003): UF-VP-431013 (right humerus; distal end); 431014 (right proximal ilium; incomplete); 431018–19 (presacral vertebrae); 431020–21 (right humeri; distal end); 431022 (left humerus; distal end); 446628, 446630 (right radioulnae); 446627 (left femur). Brooksville 2 Quarry 1A (locality HE008): 431015 (left proximal ilium; incomplete); 431016 (left proximal ilium; incomplete). I-75 (locality AL018): UF-VP-16714 (right humerus; mostly complete, missing proximal end).
Locality and Age.—The fossils found at the I-75 site—a sinkhole exposed during highway construction near Gainesville, Florida (Alachua County)—come from the first terrestrial vertebrate site known from the Oligocene of Florida (Hulbert, 2001). The I-75 site is likely from the Whitneyean or earliest Arikareean land mammal ages (∼30 mya) as some mammalian taxa restricted to the Arikareean are not present (Hayes, 2000; Morgan and Czaplewski, 2003), making this the oldest terrestrial vertebrate fauna known from the Florida peninsula. Patton (1969) reported both Bufo (possibly corresponding to what is now recognized as Anaxyrus) and Scaphiopus from I-75, and Meylan (1984) also noted that the Ranidae was present (followed by Hulbert, 2001). However, to our knowledge, none of this material has ever been described, figured, or studied further.
The Brooksville site is located near Brooksville, Florida (Hernando County) and is part of the Suwannee Limestone, with at least five clay-filled crevice deposits (Hayes, 2000). The formation lies between the Eocene Ocala limestone to the north and the Miocene Tampa limestone to the south. Based on biochronology, Hayes (2000) dated this site to the Arikareean between 26–28 mya, which was later supported by studies of bats from this site (Czaplewski and Morgan, 2012). The Brooksville 2 local fauna contains a rich diversity of mammals, as well as snakes (Hayes, 2000; Mead, 2013), lizards (Hayes, 2000; Chovanec, 2014), and a kinosternid turtle (Bourque, 2013). In addition, Hayes (2000) reported the presence of three families of anurans, though these were never further identified (simply listed as “Anura: 3 Families present”).
Description.—The presacral vertebrae have ectochordal centra and large triangular neural canals (Fig. 1). One vertebra (UF-VP-431019) likely represents the fifth or sixth presacral vertebra (centrum length: 1.4 mm). It has a large and expanded neural arch that extends posteriorly to overlap with the immediately posterior vertebra, as well as prezygapophyses that are immediately dorsal to the transverse processes, which are directed anteriorly. One vertebra (UF-VP-431018) may represent the eighth presacral vertebra that articulates with the sacrum (centrum length: 1.7 mm). As in the last presacral vertebrae of extant Rhinophrynus dorsalis, this vertebra has a neural arch that does not extend posteriorly beyond its centrum.
The humeri are robust and exhibit a diaphysis that is slightly bowed dorsally, which is especially clear in the most complete specimen from I-75 (UF-VP-16714). The total preserved length is 10.6 mm, though proximally it lacks the ossified articular surface. The distal humerus has a prominent large round distal condyle (3.3 mm in diameter) that is wider than the width of the diaphysis. There is a pronounced cubital fossa proximal to the condyle. A well-developed ulnar epicondyle (entepicondyle) extends to approximately the distal two-thirds of the distal condyle; the radial epicondyle (ectepicondyle) is present but not prominent. There is a weakly developed trochlea between the large distal condyle and the ulnar epicondyle. The ventral crest extends distally beyond the proximodistal midpoint and bears a well-developed medial groove.
The radioulnae are short (distal epiphysis of ulna to tip of olecranon: 6.5 mm in UF-VP-446628; 4.6 mm in the preserved portion of UF-VP-446630), robust, and wide, with the proximal and distal ends having the same width (approximately 3.0 mm in UF-VP-446628; 2.2 mm in UF-VP-446630). The radioulnae are narrow in lateral view with a distinct ridge extending along the ulna. In dorsal view, the radius and ulna have similar widths and form a broad flat shaft. The longitudinal sulcus on the ventral surface between the radius and ulna is short and deep and associated with three large foramina along the sulcus. Several additional small foramina are present along the midline on the dorsal surface but differ in number between the two fossils. There is also a single large foramen—located within a deep fossa on UF-VP-446628—on the medial surface of the shaft close to the olecranon fossa. A short crest extends along the ventromedial surface of the radius beginning near this large foramen and extending to the distal end of the diaphysis. The olecranon has an “S” shape, with the articular surface corresponding to the ulna being larger than that of the radius.
The ilia from Brooksville 2 have a prominent dorsal acetabular expansion that forms a weak right angle with the base of the iliac shaft. Of the three specimens, UF-VP-431015 preserves the largest portion of the iliac shaft (1.3 mm in height), which appears to be almost straight; the maximum dorsoventral dimension of UF-VP-431015 is 6.7 mm (maximum acetabulum dimension: 2.7 mm). The ventral acetabular expansion is not preserved completely in any of these specimens (Fig. 1). The dorsal protuberance is bulbous and located at the anteriormost extent of the dorsal acetabular expansion, which is best preserved on UF-VP-431014, but does not project dorsally beyond the margins of the dorsal acetabular expansion; the maximum dorsoventral dimension of UF-VP-431014 is 5.2 mm (maximum acetabulum dimension: 2.6 mm). The posterior margin of the ilium articulating with the ischium is straight, and the medial surface lacks a tubercle.
The femur is robust, short (7.0 mm in length), and bowed posteriorly. The epiphyseal surface that articulates with the pelvis is not preserved. The diaphysis has a well-developed lateral crest that extends from the diaphysis proximally, reaching its maximum height proximally and terminating 1.3 mm from the proximal head. An oval foramen is located next to the distal end of the lateral crest. Ventrally, an additional crest extends from the distal femur toward the proximal head, and is most pronounced at the middle. Two foramina are located along this auxiliary crest; the larger is found at the distal end of the crest and the smaller at the ventral edge, creating a small canal along its base. Additional smaller foramina are located dorsally along the diaphysis. Distally, the femur has a distinctive distal condyle that articulates with the tibiofibula. This distal condyle is ovoid in shape and surrounded by small foramina along the dorsal, ventral, and posterior surfaces of the diaphysis. In addition, the articular surface of the distal condyle bears distinct articular surfaces extending both posteriorly and posteroventrally.
Remarks.—These specimens all likely represent postmetamorphic individuals because neural arches are fused to the centra, and the distal condyles of the humeri are well ossified and fully synostosed to the diaphyses. However, the lack of a fully ossified proximal articular cartilage may indicate that at least UF-VP-16714 does not represent a fully mature adult. Further, the specimens from Brooksville and I-75 tend to be smaller than elements found in adult specimens of the extant Rhinophrynus dorsalis (Table 2), which reach 50–90-mm snout–vent length as adults (Dodd, 2013).
Comparisons.—The skeletal elements reported here are clearly distinguishable from those of other taxa in North America, including bufonids, hylids, microhylids, and ranids (Fig. 2). The limb elements of Rhinophrynus are all distinguishable from other genera by being stout with prominent crests and articular surfaces. The humerus of Rhinophrynus has a large distal condyle relative to the length of the bone and thick, curved diaphysis bearing a prominent crest. The radioulna similarly has wide distal articular surfaces relative to its total length. Likewise, the femur of Rhinophrynus has relatively large distal articular surfaces, a curved diaphysis, prominent crests, and, uniquely among the taxa considered here, a distal articular surface that extends well onto the posteroventral surface of the diaphysis. The ilium is readily distinguished by a narrow iliac shaft and a tall, angular dorsal acetabular expansion. The vertebrae of Rhinophrynus consistently have ectochordal centra (Fig. 1; Cannatella, 1982) because of the lack of fusion of the centrum to the intervertebral disc (Walker, 1938).
In comparison to other North American taxa, the ilia, vertebrae, humeri, femur, and radioulnae preserved from Brooksville 2 and I-75 all strongly resemble those of the extant Rhinophrynus dorsalis (Holman, 1963; Estes, 1975) and the extinct R. canadensis (Holman, 1963, 2003). There are notable differences between Rhinophrynus and the extinct rhinophrynid genera Rhadinosteus Henrici, 1998, Eorhynophrynus Estes, 1975, and Chelomophrynus Henrici, 1991, especially in the humerus, ilium, and femur. Rhinophrynus differs from Rhadinosteus by having a humerus with a rounded distal condyle and similarly developed ent- and ectepicondyles as well as a femur with well-developed crests (Henrici, 1998). It differs from Chelomophrynus by having a femur that is not dorsoventrally flattened distally, an ilium with a straighter iliac shaft that lacks lateral keel and a more excavated ventral acetabular expansion (Holman, 2003); while not depicted in Henrici (1991), the humerus of Chelomophrynus does have developed ventral and lateral crests separated by a medial groove (A. Henrici, pers. comm.). Last, Rhinophrynus differs from Eorhinophrynus in having a humerus with a less extensive lateral crest and lacking a medial ventral crest that descends towards the distal condyle (Estes, 1975).
The Florida material can be differentiated from the ilia of both R. dorsalis and R. canadensis by having a dorsal protuberance that does not project prominently beyond the dorsal extent of the dorsal acetabular expansion. Although the ventral acetabular expansion is not preserved in the Florida material, the preacetabular region is similar to R. dorsalis by being wider relative to the acetabulum than in R. canadensis. The Brooksville femur is less robust than the two extant specimens and has a less-developed ventral crest, which in the extant specimens extends from the distal epiphysis to the middle part of the diaphysis. The posteroventral surface of the distal condyle is more developed in the extant R. dorsalis than in the fossil. The preserved portions of the humeri are generally similar between R. canadensis and the Florida material by having a prominent ulnar epicondyle, potentially more so than in R. dorsalis, though the trochlea between the large distal condyle and the ulnar epicondyle appears more well developed in the Florida material (see fig. 25 in Holman, 2003). The shaft of the radioulnae from Brooksville is narrower in lateral view than in R. dorsalis and also has an ulnar process of the olecranon that is more elongated. Although other skeletal elements are referred to R. canadensis by Holman (1963, 2003), including radioulnae, tibiofibulae, and vertebrae, because these have not been figured, are only briefly described, and none of the type or referred material can be located today (Holman, 2003; R. McKellar, pers. comm.), further comparisons with the Florida material are not possible.
Comparison of measurements between fossil specimens of Rhinophrynus cited in the text to skeletal elements from two preserved specimens of R. dorsalis. For comparisons to the fossils, the right humerus and radioulna and left femur was measured for R. dorsalis. Measurements in millimeters.
The fossils from Oligocene Brooksville 2 and I-75 are the first example of an anuran family known from fossils in peninsular Florida that is not represented among its modern species. Taken together with the extinct R. canadensis from the Eocene of Saskatchewan (Holman, 1963), this record indicates a larger distribution for the genus Rhinophrynus during the early Cenozoic. Because modern R. dorsalis occupies arid or semiarid regions and there are no known rhinophrynids from the Miocene, Pliocene, or Pleistocene, this Oligocene record of Rhinophrynus in Florida suggests turnover in the anuran fauna associated with climatic cooling and progressive aridification extending from the Oligocene through the Miocene to the present (Böhme, 2003; Anderson et al., 2011; Hansen et al., 2013). Although the Oligocene reptile faunas of Florida from sites such as I-75, White Springs 1A and 3B, and Brooksville 2 remain incompletely documented, it is clear these include taxa such as typhlopid and boid snakes (Patton, 1969; Morgan, 1989; Mead, 2013; Mead and Schubert, 2013) and the kinosternid turtle Xenochelys (Bourque, 2013) that later disappeared from Florida. It also remains unclear whether squamate families documented from the Miocene Thomas Farm site such as Helodermatidae and Xantusiidae (Estes, 1963; Hulbert, 1992, 2001; Bhullar and Smith, 2008) might have been present in the Oligocene as well. Because of the climatic changes from the Oligocene through Miocene and the fact that many genera of amphibians and reptiles appear in the fossil record for the first time in the Oligocene (Hutchison, 1992), the fossil record of the Florida provides a valuable window into origins and transitions in the North American herpetofauna.
Previous research makes clear that other anuran genera previously identified from the fossil record of Florida should be treated with caution. Based on a single ilium from Thomas Farm, an early Miocene site, Holman (1961) described Proacris, which he referred to the Hylidae. However, both Sanchíz (1998) and Roček and Rage (2000) questioned whether Proacris is distinct from Acris or Pseudacris, both of which have been rarely reported in the fossil record of Florida. Holman (1967) reported Acris from Thomas Farm, the same Miocene site as Proacris, based on a fragmentary ilium; the genus is also known from the Pleistocene of Florida (Lynch, 1965). To date, the genus Pseudacris has been reported only from the Pleistocene of Florida (Lynch, 1965; Wilson, 1975). Early on, Lynch (1966) discussed the difficulties in using features such as the position of the dorsal protuberance relative to the acetabulum to discriminate among hylid taxa including Pseudacris and Acris. In this light, the extinct genus Proacris should be considered incertae sedis in the Hylidae.
Two other records of anuran genera from Thomas Farm have been called into doubt by later workers. First, Holman (1964) reported Leptodactylus (family Leptodactylidae) from Thomas Farm. Lynch (1971) later referred this material to Rana, which is well known from this site (Tihen, 1951; Auffenberg, 1956, 1957; Holman, 1964). In addition, Holman (1967) reported Eleutherodactylus (family Eleutherodactylidae) from Thomas Farm, based on a single ilium, but this too has been considered doubtful (Pratt, 1986; Hulbert, 1992). Although it is certainly within the realm of possibility that both Eleutherodactylidae and Leptodactylidae could be found in the fossil record of the Florida peninsula, rigorous study of additional material in the context of a broader taxonomic sampling is needed.
The anuran fauna of the Oligocene of peninsular Florida remains poorly explored. In addition to the I-75 and Brooksville sites (Patton, 1969; this study), anuran fossils have been reported from the Arikareean White Springs site (Morgan, 1989) though never described further. Ongoing research on fossils from these and other Oligocene sites reveals a wealth of anuran material (M. Vallejo-Pareja and D. C. Blackburn, unpubl. data). This period of time is especially interesting for North America in the context of recent time-calibrated molecular phylogenies (e.g., Li et al., 2015; Yuan et al., 2016; Feng et al., 2017; Hutter et al., 2017). At least based on the historical biogeography of extant genera in North America, we might expect to find taxa such as Gastrophryne, Rana, and Hyla. Whereas bufonids such as Anaxyrus may have originated later, time-calibrated molecular phylogenies suggest an earlier origin to the Caribbean Peltophryne (Alonso et al., 2012), which conceivably could turn up in the fossil record of Florida. Connections between the Miocene or Oligocene amphibians and reptiles from the Florida peninsula and the present-day fauna of the Greater Antilles have been repeatedly posited, including for Eleutherodactylus (Goin, 1958; Holman, 1967; but see Hulbert, 1992), “Bufo” praevis (Tihen, 1962), xantusiid and gekkotan lizards, and iguanians referable to families such as Dactyloidae, Iguanidae, and Leiocephalidae (Estes, 1963; Meylan, 1982, 1984; Chovanec, 2014). Further, as our description of Rhinophrynus demonstrates, both extant and extinct genera not currently found in eastern North America might have previously existed on the Florida peninsula. Thorough study of anurans from Oligocene sites on the Florida peninsula may provide important insights into the assembly of the eastern North American frog fauna and its relationship with Caribbean anurans.
The authors thank R. Hulbert for access to fossils in the Division of Vertebrate Paleontology at the Florida Museum of Natural History, and D. Steadman for comments on this manuscript. R. McKellar (Royal Saskatchewan Museum) assisted the authors with attempting to locate material of Rhinophrynus canadensis. Comments from both A. Henrici (Carnegie Museum of Natural History) and R. Gómez (Universidad de Buenos Aires) improved this manuscript. This is University of Florida Contribution to Paleobiology 862.
Appendix Table 1.
Taxonomy and digital object identifiers (DOI) of images of preserved specimens used for comparison. All specimens are complete skeletons and no photographs used a filter. DOIs in MorphoSource repository correspond to TIFF stacks (upper) and STL (lower) image files for each specimen.
Appendix Table 2.
Descriptions and digital object identifiers (DOI) of images of fossil specimens. All specimens are from Rhinophrynus sp. (family Rhinophrynidae) with projection averaging of 3. Digital object identifiers in MorphoSource repository correspond to TIFF stacks (upper) and STL (lower) image files for each specimen.