Abstract
The Neotropical genus Atelopus is the most diverse genus of bufonids comprising 99 species. Tadpoles of these frogs are readily distinguished based on the presence of a belly sucker, used by them to stay attached to rocks in fast-flowing streams. Despite their intriguing biology, information about their anatomy is scarce and many morphological systems are unknown. We describe the buccopharyngeal cavity of five Atelopus species. The Atelopus buccopharyngeal cavity is characterized by (1) presence of a pendulum-like papillae in the prenarial arena, (2) presence of a glandular zone in the prenarial arena, (3) narial vacuities, (4) conical median ridge, (5) absence of buccal roof arena papillae, (6) absence of buccal roof pustulations, (7) single pair of infralabial papillae, (8) absence of lingual papillae, and (9) absence of pustulations in the buccal floor. We propose that characters 1, 2, and 3 are new synapomorphies for the genus. We also propose that the presence of a single pair of infralabial papillae is a synapomorphy for bufonid. Finally, we discuss the convergent evolution of gastromyzophorous and suctorial tadpoles withing anurans.
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Introduction
The Neotropical genus Atelopus currently comprises 99 recognized species—the most diverse genus of bufonids, and several other species have been identified and are awaiting a formal description. At least 131 spices (Lötters et al. 2023) are distributed in Central and South Americas, from Costa Rica to Bolivia, along the Andes, Amazonia, and Guiana Shield, from the sea level to elevations up to 3.600 m.a.s.l. (Frost 2023). Contrasting with its large diversity, Atelopus is one of the most threatened amphibian genera; the last 30 years witnessed an unprecedent populational decline and many species are considered to be extinct (La Marca et al. 2005; Stuart et al. 2008; Wake and Vredenburg 2008; Lötters et al. 2023).
These diurnal, slow-moving frogs are frequently found in association with fast-flowing streams (Lötters 1996). They are popularly known as harlequin frogs due to the bright coloration of many species (Fig. 1a). Also, several species are known to possess tetrodotoxin (TTX) in their skin (Daly et al. 1994; Mebs et al. 1995; Yotsu-Yamashita and Takei 2010), and other compounds have also been reported in Atelopus species (see Pearson and Tarvin 2022). Atelopus frogs are characterized by their heads longer than broader, bearing a long, acuminate snout (McDiarmid 1971; Peters 1973), interdigital webbing well-developed, and by a reduction in size of the first digit that is often associated with the reduction in the number of phalanges (McDiarmid 1971; Lynch 1993; Fig. 1a). The middle ear is lacking in most species (McDiarmid 1971; Cannatella 1981; Lötters et al. 2011; Pereyra et al. 2016), although Atelopus may hear high frequencies, above 1500 Hz, a unique feature among bufonids (Womack et al. 2018).
During breeding season, amplectant pairs can be found in streams in which strings of eggs are laid submerged, beneath rocks and vegetation (Lynch 1986; Lötters 1996; Karraker et al. 2006). The harlequin frog tadpoles may also have bright colors, are gastromyzophorous (Fig. 1), and adapted to live in fast-flowing waters (Altig and Johnston 1989), in which they use their abdominal sucker to attach to rocks (Starrett 1967; Duellman and Lynch 1969; Lynch 1986; Lötters 1996). Tadpoles of 30 species have been described so far (Table 1), but aspects of their internal morphology are restricted to the cranial anatomy of A. tricolor (Lavilla and de Sá 2001; Haas 2003). Herein, we describe for the first time the buccopharyngeal morphology for five Atelopus species (A. balios, A. carrikeri, A. nahumae, A. nanay, and A. subornatus) and discuss the evolutionary and phylogenetic implications of our findings for the systematics of bufonids.
Material and methods
Buccopharyngeal morphology assessment
We studied the buccopharyngeal morphology in the tadpoles of five species of Atelopus. This material is housed at the Instituto de Ciencias Naturales, Universidad Nacional de Colombia (ICN), Bogotá, Colombia, herpetological collection of the Universidad del Magdalena (CBUMAG), Santa Marta, Colombia, and Museo de Zoología de la Pontificia Universidad Católica del Ecuador (QCAZ), Quito, Ecuador. Developmental stages are according to Gosner (1960). Additional bufonids were examined for comparison purposes; we also examined other suctorial and/or gastromyzophorous tadpoles to understand the evolution of buccopharyngeal cavity in these guilds. The complete list of examined material and developmental stages is in the Appendix.
Tadpoles of Atelopus balios and A. nanay used in the present study are part of the lots used in the tadpoles’ original descriptions: Coloma and Lötters (1996) and Coloma (2002), respectively. Tadpoles of A. carrikeri were collected in the same locality as those used in the original description (Rueda-Solano et al. 2015; see also Pérez-Gonzalez et al. 2020). Tadpoles of A. nahumae and A. subornatus were identified by comparisons with the original descriptions (Lynch 1986; Enciso-Calle et al. 2017; Pérez-Gonzalez et al. 2020) and by comparisons with fresh collected tadpoles of both species (M.A. personal observation).
Two tadpoles per species were dissected according to Wassersug (1976) to expose the buccopharyngeal cavity and stained with methylene blue solution. After inspection under the stereoscopic microscope, one individual per species was submitted to a protocol for scanning electron microscopy (SEM) as follows: (1) samples were washed in distilled water, (2) put in ethanol 25% for 2 h, (3) put in ethanol 70% for 24 h, (4) put in ethanol 100%: 2 baths of 15 min, 20 min prior to the critical point, (5) critical point dried in carbon dioxide, (6) mounted in the stubs with double face carbon tape, and (7) covered with a thin layer gold. Terminology for buccopharyngeal cavity follows Wassersug (1976, 1980) and Dias et al. (2018a).
Phylogenetic relationships and character optimization
The monophyly of Atelopus is well supported by molecular and phenotypical evidence (e.g., McDiarmid 1971; Lötters et al. 2011; Jetz and Pyron 2018). Unfortunately, of the five species studied by us, only A. nanay was included in a phylogenetic analysis. Given that the monophyly of the genus is supported, and some characters are invariable within the five species (see “Results”), we discuss the evolution of characters regarding Atelopus and other bufonids and treat apomorphic character states as putative synapomorphies for the genus.
We selected taxa for comparison based on Jetz and Pyron’s (2018) phylogenetic hypothesis that has a dense taxonomic sampling. We personally examined representatives of 11 bufonid genera and complemented our dataset with literature information (e.g., Viertel 1982; Müller 2019). The larva of Frostius erythrophtalmus is not known, but data is available for F. pernambucensis (Dubeux et al. 2023), and we assumed the monophyly of Frostius and the sister relationship between F. erythrophtalmus and F. pernambucensis for optimization purposes. We included representatives of Odontophrynidae larvae, the sister group of Bufonidae in Jetz and Pyron’s (2018) hypothesis, as outgroups. The complete list of examined material and references used is listed in the Appendix.
We propose nine transformation series (Hennig 1966; Grant and Kluge 2004) to account for the variation of the buccopharyngeal morphology in the larvae of Atelopus in comparison with other bufonids. The character matrix was built and edited in Mesquite V. 3.70 (Maddison and Maddison 2021) (Supporting Information), and character optimization was performed in T.N.T. v. 1.5 (Goloboff and Catalano 2016). There is no information for several bufonid genera, but we opt to include them in our optimization to demonstrate which parts of the bufonids tree of life require more studies on larval morphology.
Results
Buccopharyngeal morphology
The buccopharyngeal morphology of the five species is quite similar. A single, condensed, description is provided and differences noted when present.
Buccal roof (Figs. 2a, 4a, 5a, 6a, 7a) triangular
Prenarial arena semi-elliptical, with a pendulum-like papilla (Fig. 3a) and several secretory pits (Fig. 3b, c; absent in A. subornatus); these pits are located immediately posterior to the upper jaw sheath and before the pendulum-like papilla, covering the entire width of that region. The pits are rounded, and a secretion residue can be observed in several pits (Fig. 3c). Internal nares elliptical, transversally oriented; posterior valve free, lacking marginal projection. Vacuities (Fig. 3d, e) present, circumscribed by margins of inner nares, presenting ciliated cells (Fig. 3f). Postnarial arena diamond-shaped, two conical, tall postnarial papillae; first pair shorter than second pair. Lateral ridge papillae short, triangular, bifurcated (not bifurcated in A. carrikeri). Median ridge low, conical (bifurcated in A. carrikeri), papilla-like. Buccal roof arena poorly defined, completely lacking papillae or pustulation. Dorsal velum medially discontinued, devoid of papillae or projections, arch-shaped.
Buccal floor (Figs. 2b, 4b, 5b, 6b, and 7b) triangular
Single pair of flat, wide, infralabial papillae; tip crenulated. Lingual bud poorly defined; lingual papillae absent. Buccal floor arena bell-shaped; buccal floor arena papillae present (10–11 in A. balios; 10–12 in A. carrikeri; 13–14 in A. nahumae; 9–11 in A. nanay; 7–8 in A. subornatus). Buccal floor arena lacking pustulations. Prepocket papillae and pustulation absent. Buccal pockets deep, wide, oblique slit-shaped. Ventral velum present; spicular support inconspicuous; medial notch absent; marginal projections present; secretory pits poorly developed; secretory ridges present. Branchial basket triangular, short, poorly developed, wider than long. Three filter cavities, well-defined, partially covered by ventral velum.
Evolution of characters
Character 1: prenarial arena, pendulum-like papilla: absent (0), present (1)
The prenarial arena is the area between the internal nares and the mouth opening (Wassersug 1976). Several structures have been reported in that region in different anuran larvae, such as crests, ridges, and pustulations, among others (e.g., Wassersug 1980; Vera Candioti 2007; Nascimento et al. 2013; Dias et al. 2018a, b). Atelopus larvae have a pendulum-like papillae (state 1; Fig. 3a).
Taxonomic distribution and optimization
The presence of a pendulum-like papillae was invariable in the five studied Atelopus species and also present in Frostius pernambucensis larvae; current optimization of this character (Fig. 8a) suggests it as a synapomorphy of Atelopus. Additionally, similar papilla was observed in the suctorial tadpoles of Ansonia and Werneria (Fig. 9), but the absence of data for their close related taxa (Ansonia: Pelophryne and Ghatophryne; Werneria: Nectophryne, Didynapius, and Nimbaphrynoides) renders the optimization ambiguous within these lineages.
Character 2: prenarial arena, glandular zone: absent (0), present (1)
In the species of Atelopus, a large portion of the prenarial arena is covered with small pits (Fig. 3b), very similar to secretory pits of the ventral velum of other tadpoles. These pits are rounded, deep, being secreted. The function of these pits in such peculiar region is unknown.
Taxonomic distribution and optimization
Character state 1 was observed only in Atelopus (except in A. subornatus), and we suggest it as a new synapomorphy for the genus (Fig. 8b). As far as we know, it has not been reported in any other anuran larvae.
Character 3: vacuities circumscribed by margins of inner nares: absent (0), present (1)
Van Eeden (1951:9) found what he called “a band of ciliated epithelium” in Ascaphus truei and suggested that the cilia could have some role in the feeding mechanism proposed by Noble (1927). Wassersug (1980) described this “cul de sac” feature in other taxa and suggested that it may have a chemosensory function. Later, vacuities have been reported in several taxa, particularly in Cophomantinae (e.g., Kolenc et al. 2008), Leptodactylidae (e.g., Nascimento et al. 2021), Centrolenidae (e.g., Rada et al. 2019; Dias et al. 2020), and in tadpoles of the Scinax perpusillus species group (e.g., Dias and Pie 2021).
Taxonomic distribution and optimization
We observed the presence of vacuities in all the five Atelopus examined, which suggested it as another synapomorphy for the genus (Fig. 8c). We also observed the presence of vacuities in Ansonia and Werneria (Fig. 9); however, as discussed above (see character 1), the lack of data precludes a non-ambiguous optimization of this character state in those clades.
Character 4: median ridge, shape: triangular (0), conical (1), trapezoidal (2); unordered
The median ridge marks the end of the postnarial arena. It is a feature highly variable among tadpoles. According to Wassersug (1980), due to its central location, the median ridge may play a role in splitting the respiratory current into right and left ones. The shape of the median ridge has been used as a character in the systematics of several groups; for instance, Dias et al. (2019a) suggested a trapezoidal median ridge as a synapomorphy for the Proceratophrys bigibbosa species group. Within examined taxa, three different morphologies were observed for the median ridge: triangular (state 0), as in most of bufonids, conical, as in Atelopus and Ansonia (state 1), and trapezoidal (state 2) in some outgroup taxa (e.g., Odontophrynus).
Taxonomic distribution and optimization
Conical medial ridge was present in all Atelopus examined and also in Ansonia. The absence of median ridge in Osornophryne (inapplicable) and the lack of data for Oreophrynella render the optimization of this character ambiguous (Fig. 8d). It is likely that Oreophrynella will also lack a median ridge due to its endotrophic development—see Wassersug and Duellman (1984) for discussion of buccopharyngeal cavity in endotrophic and direct-developer frogs—which will prevent the optimization of this character in the future as well.
Character 5: buccal roof arena papillae: absent (0), present (1)
The buccal roof arena papillae are usually conical, with one or few bifurcated papillae (Wassersug 1976). Some authors (e.g., Wassersug 1980) suggested that these papillae may contribute to the sorting of food particles in the mouth. These papillae delimitate the buccal roof arena and may be very abundant, as in Hylodes (e.g., Montesinos et al. 2022), or completely absent, as in Atelopus, which renders the buccal roof arena also absent.
Taxonomic distribution and optimization
The optimization of this character is complex (Fig. 10A); we found the buccal roof arena papillae absent in all examined Atelopus, plus in the endotrophic larvae Frostius pernambucensis, in the direct developer tadpole-like Osornophryne occidentalis, in Amazophrynella minuta, and in Ansonia. The optimization of this character is ambiguous in all mentioned taxa. The presence of buccal roof papillae in Dendrophryniscus brevipollicatus and the absence of data for Nannophryne make the optimization of this character difficult at the base of Bufonidae except Melanophryniscus.
Character 6: buccal roof pustulations: absent (0), present (1)
In many anuran taxa, both buccal floor and roof are covered with a field of rounded pustulation. The function of these structures is unknown, but its abundancy seems to be correlated with benthic, lotic species (e.g., Vera Candioti 2007; Dias et al. 2014). The reduction or absence of pustulations has been reported in endotrophic (e.g., Wassersug and Duellman 1984; Wassersug and Heyer 1988), fossorial (e.g., Wassersug 1980; Rada et al. 2019; Dias et al. 2020), macrophagous (e.g., Wassersug 1980; Vera Candioti et al. 2004; Vera Candioti 2005; Dias et al. 2019b), oophagous (e.g., Vera Candioti et al. 2021), and suctorial (e.g., Wassersug and Heyer 1988) tadpoles. In all examined Atelopus, there was no pustulation in the buccal roof.
Taxonomic distribution and optimization
The absence of pustulations followed the exact same pattern as that of the absence of buccal roof arena papillae, being absent in Ansonia, Amazophrynella minuta, Frostius pernambucensis, Osornophryne occidentalis, and Schismaderma carens. Thus, the optimization of this character is highly ambiguous (Fig. 10b).
Character 7: number of infralabial papillae: 2 (0), 4 (1)
The infralabial papillae are the first papillae observed in the buccal floor; they are positioned right after the mouth’s opening and can vary in number, size, and shape—there may be a single pair as in Cycloramphus stejnegeri (Wassersug and Heyer 1983) or up to 12 in tadpoles of Heleophryne natalensis (Wassersug and Heyer 1988); they can be conical (e.g., Vera Candioti 2007) or branched (e.g., Dias et al. 2019a). Wassersug (1980) hypothesized that these papillae play an important role selecting food particles that will enter in the buccal cavity of tadpoles.
Taxonomic distribution and optimization
Atelopus as well as all other bufonids present only a single pair (two papillae) of infralabial papillae, contrasting with the two pairs (four) of papillae in Odontophrynidae. Thus, the presence of two infralabial papillae is a synapomorphy for Bufonidae (Fig. 10c).
Character 8: lingual papillae: absent (0), present (1)
Lingual papillae are located in the tongue anlage (Wassersug 1976) and are likely to have gustatory function (Hammerman and Thomas 1967). Lingual papillae are present in most frogs, although absent by definition in the aglossal pipids and in several other lineages.
Taxonomic distribution and optimization
Atelopus larvae lack lingual papillae (state 0). The same condition was observed in Frostius and Osornophryne. Given the presence of lingual papillae in Melanophryniscus and other bufonids, the optimization of this character was ambiguous (Fig. 10d).
Character 9: buccal floor pustulations: absent (0), present (1)
Pustulations are commonly present in the buccal floor of tadpoles (e.g., Vera Candioti 2007; Nascimento et al. 2013; Dias et al. 2014) and have rarely been reported absent (e.g., Ascaphus truei; Wassersug 1980).
Taxonomic distribution and optimization
Pustulations on the buccal floor were absent in all examined Atelopus. Also, Frostius, Osornophryne, Amazophrynella, and Dendrophryniscus lacked these pustulations, rendering its absence a synapomorphy for all bufonids minus Melanophryniscus (Fig. 11). Pustulations were also absent in Ansonia and Schismaderma carens.
Discussion
Larval morphology and the systematics of bufonids
Atelopus have a distinctive larva within bufonids; their abdominal sucker, wide oral disc, and color pattern (e.g., Duellman and Lynch 1969; Lötters 1996; Pérez-Gonzalez et al. 2020) make these tadpoles easily distinguished from other bufonids. The comparative analysis of the buccopharyngeal cavity of Atelopus revealed a series of new unique, intriguing character states in these tadpoles. The Atelopus buccopharyngeal cavity is characterized by (1) presence of a pendulum-like papillae in the prenarial arena, (2) presence of a glandular zone in the prenarial arena, (3) narial vacuities, (4) conical median ridge, (5) absence of buccal roof arena papillae, (6) absence of buccal roof pustulations, (7) single pair of infralabial papillae, (8) absence of lingual papillae, and (9) absence of pustulations in the buccal floor. We propose that characters 1, 2, and 3 are new synapomorphies for the genus Atelopus.
The prenarial arena of tadpoles is characterized by the presence of several features, ranging from pustulations to crests (e.g., Vera Candioti 2007). These features play an important role in the feeding mechanism of tadpoles; for instance, it has been hypothesized that the presence of an inverted V structure in the prenarial arena of umbelliform tadpoles’ interlocks with the infralabial papillae to prevent large food particles from entering the mouth (Wassersug 1980; Dias et al. 2018b, 2021). The presence of a large, pendulum-like papillae in the larvae of Atelopus is very intriguing; a similar feature is rare among anurans. We speculate two putative functions to it: (1) such large papilla would prevent large particles of reaching the vacuities’ area; (2) it could deviate the water flow to the vacuities. It is important to note that vacuities possibly have a chemosensory function (Wassersug 1980), and both diverting water towards them, as well as preventing them from being obstructed by large particles, seem possible explanations for the presence of this pendulum-like papillae. Nevertheless, further studies are required to test our hypotheses. Interesting to note that a similar, although narrower, feature was described in the prenarial arena of Rhinella quechua (Aguayo et al. 2009), another gastromyzophorous bufonid.
The posterior region of buccal floor is usually marked by secretory tissue in most anurans (Kenny 1969; Wassersug 1980)—secretory tissue, however, may be present in other regions, as in the buccal floor of Rhacophorus vampyrus (Vera Candioti et al. 2021). Usually, secretory cells are organized in pits and ridges (Wassersug and Rosenberg 1979). Many authors agree with the hypothesis that the secretory pits, through the production of mucus strands, may aid in food entrapment (de Jongh 1968; Kenny 1969; Wassersug 1976, 1980; Wassersug and Rosenberg 1979). Although experimental studies testing this hypothesis are lacking, the anatomy and topographical distribution of the secretory pits provide some support to that view. We observed secretory pits in the prenarial arena the Atelopus tadpoles examined, except in A. subornatus that phenotypically resembles the secretory pits of the velum of anuran larvae. The function of these pits is unknown and, as far as we know, this character state has never been reported for other anurans. Further studies are required to understand the biological meaning of these pits, notwithstanding, and we propose their presence in the prenarial arena as a synapomorphy for the genus Atelopus.
Vacuities were originally described in Ascaphus tadpoles (van Eeden 1951) and since then reported in few taxa (e.g., Wassersug 1980; d’Heursel and Haddad 2007; Magalhães et al. 2015; Pezzuti et al. 2015; Dias and Pie 2021). Kolenc et al. (2008) suggested that the presence of vacuities was a synapomorphy for the Cophomantini tribe. Dias et al. (2020; see also Rada et al. 2019) observed this feature in several centrolenids, suggesting its presence as a synapomorphy for glass frogs. However, as more researchers pay attention to this structure, more reports emerge. For instance, recently, Nascimento et al. (2021) reported the presence of vacuities in tadpoles of Lithodytes lineatus and in several species of the Leptodactylus pentadactylus species group; Dias and Pie (2021) reported them in the larvae of S. v-signatus and suggested it as synapomorphy for the S. perpusillus species group. These findings suggest that vacuities are more widely distributed within anurans than previously imagined. We observed vacuities in all examined Atelopus and also in other unrelated bufonids, such as Ansonia, Incilius, and Werneria. Current optimization suggests that the presence of vacuities in Atelopus is a synapomorphy. We also predict that, as more taxa are examined, the presence of vacuities will also optimize as a synapomorphies for Ansonia and Werneria.
The median ridge is highly variable among anuran larvae (e.g., Wassersug 1980; Vera Candioti 2007; Dias et al. 2019a, 2021), but conical median ridge is particularly rare. It has been reported in few taxa, such as the suctorial Heleophryne natalensis (Wassersug and Heyer 1988), and was present in all Atelopus examined, although with ambiguous optimization regarding bufonids.
Lack of pustulations and papillae in the buccal floor and roof is not common in anurans and often associated with endotrophic development (Wassersug and Duellman 1984; Romero-Carvajal et al. 2023). Nevertheless, feeding tadpoles may also present a reduction or lack these features, as in the case of oophagous (e.g., Vera Candioti et al. 2021) and macrophagous (e.g., Dias et al. 2019b, 2023) tadpoles. The diet of Atelopus larvae is poorly unknown—as that of most species (Altig et al. 2007)—but some elements of their anatomy may suggest some degree of macrophagy; the secretory tissues involved in filtering particles are reduced, they lack several papillae and pustulation, lingual papillae are absent, and the presence shortened intestines (PHD, personal observation). In captivity, the larvae of Atelopus flavescent were reported to feed on algae (Gawor et al. 2012), but fish food was also supplemented. Both captivity and field observation as well as detail study of trophic ecology are necessary to better understand what these tadpoles eat.
We observed a single pair of infralabial papillae in Atelopus larvae. This condition differs of that observed in tadpoles of Odontophrynidae that usually present two pairs of infralabial papillae (e.g., Nascimento et al. 2013; Dias 2020). Tadpoles of other closely related lineages, such as centrolenids and leptodactylids, also present two pairs of infralabial papillae, (e.g., Wassersug and Heyer 1988; Vera Candioti et al. 2007; Rada et al. 2019; Dias et al. 2020; Nascimento et al. 2020). Dubeux et al. (2023) suggested that the presence of two infralabial papillae could represent a synapomorphy of Bufonidae, and we provide additional evidence for that hypothesis.
Lingual papillae are also present in most anuran larvae, with some few exceptions (e.g., micohylids and several Dendropsophini; Vera Candioti 2007; Dias et al. 2023). All Atelopus lack lingual papillae, as well as the endotrophic larvae of Frostius (Dubeux et al. 2023) and the direct developer Osornophryne (Romero-Carvajal et al. 2023). The optimization of this character state is ambiguous, but it is interesting noting that absence of it in Frostius and in Osornophryne is probably related to endotrophic development, while Atelopus retained a plesiomorphic state or lost those papillae independently is an interesting evo-devo question.
Convergent evolution in gastromyzophorous and suctorial tadpoles
Convergent evolution is the independent evolution of homoplastic character states in different lineages, usually in association with similar selective pressures (Losos et al. 1998; Losos 2011). Gastromyzophorous tadpoles evolve independently at least eight times in anurans, although highly concentrated in two clades, bufonids and ranids, with one instance in hylids. Gastromyzophorous tadpoles have been reported in Amolops, Huia, Meristogenys, Sumaterana, Wijayarana, and Rana sauteri—(e.g. Kuramoto et al. 1984; Arifin et al. 2021); in three species of the Rhinella veraguensis group (R. chrysophora, R. quechua, and R. veraguensis), in Sabahphrynus maculatus, in Adenomus kandianus, and in Bufo aspinius (Rao and Yang 1994; Matsui et al. 2007; Aguayo et al. 2009; Meegaskumbura et al. 2015); finally, the hylid Phyllodytes gyrinaethes is also gastromyzophorous (Peixoto et al. 2003; Vera Candioti et al. 2017).
Notwithstanding, the development of a belly sucker was not the only solution provided by natural selection to enable tadpoles to adhere to the substrate in fast-flowing waters; suctorial tadpoles also evolved in several lineages (Fig. 12), such as Ansonia, Nasikabatrachus, Odontobatrachus, and many hylids. Gastromyzophorous and suctorial tadpoles, in general, have convergent phenotypic traits, such as enlarged oral discs, depressed bodies with extended and broad snouts, robust and well-keratinized jaw sheaths, strong tails with reduced tail fins, dorsal eyes (Fig. 13), and several modifications in the musculoskeletal system (Gan et al. 2015; Vera Candioti et al. in press).
The buccopharyngeal cavity of gastromyzophorous and suctorial tadpoles also evolved convergently. The buccopharyngeal cavity has been described for few taxa: Amietia ruwenzorica (Viertel et al. 2012) Ansonia longidigita, Ansonia hanitschi, Ansonia minuta (Inger 1985; Haas and Das 2008), Ascaphus truei (Wassersug 1980), Heleophryne natalensis (Wassersug and Heyer 1988), Huia cavitympanum, Meristogenys phaeomerus, Meristogenys poecilus, Meristogenys kinabaluensis (Inger 1985), Nasikabatrachus sahyadrensis (Raj et al. 2012), and Rhinella quechua (Aguayo et al. 2009).
A different combination of the characters described here for Atelopus is present in several of these species (Table 2; Fig. 13). For instance, the presence of a developed element in the prenarial arena is almost invariable within gastromyzophorous and suctorial larvae; similarly, vacuities are present in the many of taxa, suggesting an adaptive value in these traits. Unfortunately, for many of these characters, there are no robust hypotheses about their function and how they might increase fitness in torrent environments is still obscure.
Nevertheless, the fact that some species described as suctorial (e.g., Amietia ruwenzorica) differ phenotypically from that pattern (see Viertel et al. 2012), resembling rheophilous larvae (e.g., Montesinos et al. 2022, 2023), suggests that internal morphology characters should also be included in the studies of ecomorphological guilds of anurans. Moreover, it also suggests that the current structure of ecomorphological guilds might hide ecological, functional, and morphological diversity.
Conclusion and remarks
The buccopharyngeal cavity provided additional information to understand the taxonomy and the evolution of Atelopus. Our study can be added to the growing list of studies about larval morphology of previously poorly known groups in the last 20 years; one important conclusion from those studies is that as more species are investigated, novel and astonishing new morphologies are discovered (e.g., Haas et al. 2006, 2014; Grosjean et al. 2011; Rowley et al. 2012; Vera Candioti et al. 2017, 2021; Dias 2020; Dias et al. 2023). Also, tadpoles have been proven excellent model organism to study evolutionary phenomena; for instance, convergent evolution has been constantly reported in tadpoles of different lineages (e.g., Rada et al. 2019; Grosjean and Preininger 2020) demonstrating how they can be used to better understand the independent evolution of similar phenotypes. This highlights the importance of training new generations of morphologists and evolutionary biologists interested in tadpoles.
References
Acosta-Galvis A, Rueda-Amonacid J, Velásquez-Alvarez AA, Sánchez-Pacheco SJ, Peña-Prieto J (2006) Descubrimiento de una nueva especie de Atelopus (Bufonidae) Para Colombia: ¿Una luz de esperanza o el ocaso de los sapos arlequines? Rev Acad Colomb Cienc 20:271–290
Aguayo R, Lavilla EO, Vera Candioti MF, Camacho T (2009) Living in fast-flowing water: morphology of the gastromyzophorous tadpole of the bufonid Rhinella quechua (R. veraguensis group). J Morph 270:1431–1442. https://doi.org/10.1002/jmor.10768
Aguilar C, Siu-Ting K, Venegas P (2007) The rheophilous tadpole of Telmatobius atahualpai Wiens, 1993 (Anura: Ceratophryidae). S Am J Herpetology 2:165–174
Altig R, Johnston GF (1989) Guilds of anuran larvae: relationships among developmental modes, morphologies, and habitats. Herpetol Monogr 3:81. https://doi.org/10.2307/1466987
Altig R, Whiles MT, Taylor CL (2007) What do tadpoles really eat? Assessing the trophic status of an understudied and imperiled group of consumers in freshwater habitats. Freshwater Biol 52:386–395. https://doi.org/10.1111/j.1365-2427.2006.01694.x
Arifin U, Chan KO, Smart U, Hertwig ST, Smith EN, Iskandar DT, Haas A (2021) Revisiting the phylogenetic predicament of the genus Huia (Amphibia: Ranidae) using molecular data and tadpole morphology. Zool Linn Soc 193:673–699. https://doi.org/10.1093/zoolinnean/zlaa158
Baldo D, Candioti FV, Haad B, Kolenc F, Borteiro C, Pereyra MO, Zank C, Colombo P, Bornschein M, Sisa FN, Brusquetti F, Contes CE, Nogueira-Costa P, Almeida-Santos P, Pie MR (2014) Comparative morphology of pond, stream and phytotelm-dwelling tadpoles of the South American Redbelly Toads (Anura: Bufonidae: Melanophryniscus). Biol J Linn Soc 112(3):417–441
Boistel R, Grosjean S, Lötters S (2005) Tadpole of Atelopus franciscus from French Guyana, with comments on other larvae of the genus (Anura: Bufonidae). J Herpetol 39:148–153. https://doi.org/10.1670/0022-1511(2005)039[0147:TOAFFF]2.0.CO;2
Cannatella DC (1981) A new Atelopus from Ecuador and Colombia. J Herpetol 15:133–138. https://doi.org/10.2307/1563371
Coloma LA (2002) Two new species of Atelopus (Anura: Bufonidae) from Ecuador. Herpetologica 58:229–252. https://doi.org/10.1655/0018-0831(2002)058[0229:TNSOAA]2.0.CO;2
Coloma LA, Lötters S (1996) The tadpole of Atelopus balios (Anura: Bufonidae) from the pacific lowlands of Ecuador. Herpetologica 52:66–70
Coloma LA, Lötters S, Salas AW (2000) Taxonomy of the Atelopus ignescens complex (Anura: Bufonidae): designation of a neotype of Atelopus ignescens and recognition of Atelopus exiguous. Herpetologica 56:303–324
d’Heursel A, Haddad CFB (2007) Anatomy of the oral cavity of hylid larvae from the genera Aplastodiscus, Bokermannohyla, and Hypsiboas (Amphibia, Anura): description and systematic implications. J Herpetol 41:458–468. https://doi.org/10.1670/0022-1511(2007)41[458:AOTOCO]2.0.CO;2
Daly JW, Gusovsky F, Myers CW, Yotsu-Yamashita M, Yasumoto T (1994) First occurrence of tetrodotoxin in a dendrobatid frog (Colostethus inguinalis), with further reports for the bufonid genus Atelopus. Toxicon 32:279–285. https://doi.org/10.1016/0041-0101(94)90081-7
de Jongh HJ (1968) Functional morphology of the jaw apparatus of larval and metamorphosing Rana Temporaria L. Neth J Zool 18:1–133. https://doi.org/10.1163/002829668X00072
Dias PHS (2020) The remarkable larval anatomy of Proceratophrys minuta Napoli, Cruz, Abreu and Del-Grande, 2011 (Amphibia: Anura: Odontophrynidae). J Morphol 281:1086–1097
Dias PHS, Pie MR (2021) Buccopharyngeal morphology of the tadpoles of Scinax v-signatus, with comments on larval characters of the S. perpusillus species group (Amphibia: Anura: Hylidae). Zootaxa 4964:195–200. https://doi.org/10.11646/zootaxa.4964.1.12
Dias PHS, Carvalho-e-Silva AMPT, Carvalho-e-Silva SP (2014) The tadpole of Proceratophrys izecksohni (Amphibia: Anura: Odontophrynidae). Zoolgia 31:181–194. https://doi.org/10.1590/S1984-46702014000200010
Dias PHS, Brandão AP, Grant T (2018a) The buccopharyngeal morphology of the tadpole of Ameerega flavopicta (Anura: Dendrobatidae: Colostethinae), with a redescription of its external morphology. Herpetologica 74:323–328. https://doi.org/10.1655/Herpetologica-D-17-00055.1
Dias PHS, Mongin-Aquino M, Candioti FV, Carvalho-e-Silva AMPT, Baêta (2018b) Internal larval morphology of two species of shining leaf frogs (Anura: Phyllomedusidae: Phasmahyla). S Am J Herpetol 13:44–53. https://doi.org/10.2994/SAJH-D-16-00055.1
Dias PHS, Araujo-Vieira K, Santos RF, Both C (2019a) Review of the internal larval anatomy of the Proceratophrys bigibbosa species group (Anura: Odontophrynidae), with description of the tadpole of P. brauni Kwet and Faivovich, 2001. Copeia 107:417–429. https://doi.org/10.1643/CH-18-138
Dias PHS, Araujo-Vieira K, Carvalho-e-Silva AMPT, Orrico VGD (2019b) Larval anatomy of Dendropsophus decipiens (A. Lutz 1925) (Anura: Hylidae: Dendropsophini) with considerations to larvae of this genus. PLoS One 14:e0219716. https://doi.org/10.1371/journal.pone.0219716
Dias PHS, Anganoy-Criollo M, Rada M, Grant T (2020) Comparative larval buccopharyngeal morphology of two glass frog species (Anura: Centrolenidae: Vitreorana). Zool Anz 289:118–122. https://doi.org/10.1016/j.jcz.2020.10.007
Dias PHS, Anganoy-Criollo M, Rada M, Grant T (2021) The tadpoles of the funnel-mouthed dendrobatids (Anura: Dendrobatidae: Colostethinae: Silverstoneia): external morphology, musculoskeletal anatomy, buccopharyngeal cavity, and new synapomorphies. J Zool Syst Evol Res 59:691–717. https://doi.org/10.1111/jzs.12455
Dias PHS, Marcondes BC, Pezzuti TL, Vera Candioti F, Araújo-Vieira K, Prodocimo MM, Silva HR, Orrico VGD, Haas A (2023) The missing piece of the puzzle: larval morphology of Xenohyla truncata (Anura: Hylidae: Dendropsophini) and its implication to the evolution of Dendropsophini tadpoles. Zoomorphology 142:111–126. https://doi.org/10.1007/s00435-022-00575-3
Dubeux MJM, Nascimento FAC, Dias PHS (2023) Larval morphology of Frostius pernambucensis (Anura): contribution of larval characters for the systematics of the family Bufonidae and evolution of endotrophic tadpoles. Zoomorphology. https://doi.org/10.1007/s00435-023-00623-6
Duellman WE, Lynch JD (1969) Descriptions of Atelopus tadpoles and their relevance to atelopodid classification. Herpetologica 25:231–240
Enciso-Calle MP, Viuche-Lozano A, Anganoy-Criollo M, Bernal HH (2017) Rediscovery of Atelopus subornatus Werner, 1899 (Anura: Bufonidae), with a redescription of the tadpole. Zootaxa 4344:160–162. https://doi.org/10.11646/zootaxa.4344.1.7
Frost DR (2023) Amphibian species of the world: an online reference. Version 6.1 (Accessed at August 10, 2023). Electronic database accessible at https://amphibiansoftheworld.amnh.org/index.php
Gan LL, Hertwig S, Das I, Haas A (2015) The anatomy and structural connectivity of the abdominal sucker in the tadpoles of Huia cavitympanum, with comparisons to Meristogenys jerboa (Lissamphibia: Anura: Ranidae). J Zool Syst Evol Res 54:46–59. https://doi.org/10.1111/jzs.12113
Gascon C (1989) The tadpole of Atelopus pulcher Boulenger (Annura, Bufonidae) from Manaus, Amazonas. Rev Bras Zool 6:235–239. https://doi.org/10.1590/S0101-81751989000200007
Gawor A, Rauhaus A, Karbe D, der Straeten V, Lötters S, Ziegler T (2012) Is there a chance for conservation breeding? Ex situ management, reproduction, and early life stages of the Harlequin toad Atelopus flavescens Duméril & Bibron, 1841 (Amphibia: Anura: Bufonidae). Amphib Reptil Cons 5:29–44
Goloboff PA, Catalano SA (2016) TNT version 1.5, including a full implementation of phylogenetic morphometrics. Cladistics 2016:1–18. https://doi.org/10.1111/cla.12160
Gosner KL (1960) A simplified table for staging anuran embryosand larvae with notes on identification. Herpetologica 5:183–190
Grant T, Kluge AG (2004) Transformation series as an ideographic character concept. Cladistics 20:23–31. https://doi.org/10.1111/j.1096-0031.2004.00003.x
Gray P, Cannatella DC (1985) A new species of Atelopus (Anura, Bufonidae) from the Andes of northern Perú. Copeia 1985:910. https://doi.org/10.2307/1445241
Grosjean S, Preininger D (2020) Description of two Staurois tadpoles from Borneo, Staurois parvus and Staurois tuberilinguis (Anura: Ranidae). Zootaxa 4896:523–534. https://doi.org/10.11646/zootaxa.4896.4.4
Grosjean S, Straus A, Glos J, Randrianiaina RD, Ohler A, Vences M (2011) Morphological and ecological uniformity in the funnel-mouthed tadpoles of Malagasy litter frogs, subgenus Chonomantis. Zool J Linn Soc 162:149–183. https://doi.org/10.1111/j.1096-3642.2010.00667.x
Haas A (2003) Phylogeny of frogs as inferred from primarily larval characters (Amphibia:Anura). Cladistics 19:23–89
Haas A, Das I (2008) Larval identities of Ansonia hanitschi Inger, 1960 (Amphibia: Bufonidae) and Polypedates colletti (Boulenger, 1890) (Amphibia: Rhacophoridae) from East Malaysia (Borneo). Salamndra 44:85–100
Haas A, Hertwig S, Das I (2006) Extreme tadpoles: the morphology of the fossorial megophryid larva, Leptobrachella mjobergi. Zoology 109:26–42. https://doi.org/10.1016/j.zool.2005.09.008
Haas A, Pohlmeyer J, McLeod DS, Kleinteich T, Hertwig ST, Das I, Buchloz DR (2014) (2014) Extreme tadpoles II: the highly derived larval anatomy of Occidozyga baluensis (Boulenger, 1896), an obligate carnivorous tadpole. Zoomorphology 133:321–342. https://doi.org/10.1007/s00435-014-0226-7
Hammerman DL, Thomas RF (1967) Lingual premetamorphic papillae as larval taste structures in frogs. Nature 215:98–99. https://doi.org/10.1038/215098a0
Hennig W (1966) Phylogenetic systematics. University of IllinoisPress, Chicago, IL
Inger RF (1985) Tadpoles of the forested regions of Borneo. Fieldiana 26:1–89. https://doi.org/10.5962/bhl.title.3403
Jetz W, Pyron RA (2018) The interplay of past diversification and evolutionary isolation with present imperilment across the amphibian tree of life. Nat Ecol Evol 2:850–858. https://doi.org/10.1038/s41559-018-0515-5
Karraker NE, Richards CL, Ross HL (2006) Reproductive ecology of Atelopus zeteki and comparisons to other members of the genus. Herpetol Rev 37:284–288
Kenny JS (1969) The amphibia of Trinidad. St Fauna Curaçao Caribbean Islands 29:1–78
Kolenc F, Borteiro C, Alcalde L, Baldo D, Cardozo D, Faivovich J (2008) Comparative larval morphology of eight species of Hypsiboas Wagler (Amphibia, Anura, Hylidae) from Argentina and Uruguay, with a review of the larvae of this genus. Zootaxa 1927:1–66. https://doi.org/10.11646/zootaxa.1927.1.1
Kuramoto M, Wang CS, Yü HT (1984) Breeding, larval morphology and experimental hybridization of Taiwanese brown frogs, Rana longicrus and R. sauteri. J Herpetol 18:387–395. https://doi.org/10.2307/1564101
La Marca E, Lips KR, Lötters S, Puschendorf R, Ibéñez R, Rueda-Almonocid VR, Schulte R, Marty C, Castro F, Manzanilla-Puppo J, Gacía-Pérez JE, Bolaños F, Chaves G, Pounds JA, Toral E, Young BE (2005) Catastrophic population declines and extinctions in neotropical harlequin frogs (Bufonidae: Atelopus). Biotropica 37:190–201. https://doi.org/10.1111/j.1744-7429.2005.00026.x
Lambris AJL (1994) Laryngeal and buccopharyngeal morphology of some South African Bufonidae: new data sets for anuran tax- onomy. Ann Natal Mus 35:261–307
Lavilla EO, de Sá RO (2001) Chondrocranium and visceral skeleton of Atelopus tricolor and Atelophryniscus chrysophorus (Anura, Bufonidae). Amphibia-Reptilia 22:167–177. https://doi.org/10.1163/15685380152030391
Lavilla EO, de Sá RO, de La Riva I (1997) Description of the tadpole of Atelopus tricolor. J Herpetol 31:121–124. https://doi.org/10.2307/1565340
Lescure J (1981) Contribution à l'étude des Amphibiens de Guyane française IX. Le têtard gastromyzophore d'Atelopus flavescens Duméril et Bibron (Anura, Bufonidae). Amphibia-Reptilia 2:209–215
Lindquist J (1981) Contribution à l’étude des Amphibiens de Guyane française IX. Le têtard gastromyzophore d’Atelopus flavescens DUMÉRIL et BIBRON (Anura, Bufonidae). Amphibia-Reptilia 2:209–215. https://doi.org/10.1163/156853881X00032
Lindquist ED, Hetherington TE (1998) Tadpoles and juveniles of the Panamanian golden frog, Atelopus zeteki (Bufonidae), with information on development of coloration and patterning. Herpetologica 54:370–376
Losos JB (2011) Convergence, adaptation, and constraint. Evolution 65:1827–1840. https://doi.org/10.1111/j.1558-5646.2011.01289.x
Losos JB, Jackman TR, Larson A, Queiroz K, Rodríguez-Schettino L (1998) Contingency and determinism in replicated adaptive radiations of island lizards. Science 279:2115–2118. https://doi.org/10.1126/science.279.5359.2115
Lötters S (1996) The Neotropical toad genus Atelopus: Checklist, biology, distribution. Glaw Verlags, Köln, M. Vences & F
Lötters S (2001) Tadpole of Atelopus mindoensis Peters (Anura, Bufonidae) from Northwestern Ecuador. Copeia 2001:276–278. https://doi.org/10.1643/0045-8511(2001)001[0276:TOAMPA]2.0.CO;2
Lötters S, Haas W, Schick S, Böhme W (2002) On the systematics of the harlequin frogs (Amphibia: Bufonidae: Atelopus) from Amazonia. II: Redescription of Atelopus pulcher (Boulenger, 1882) from the eastern Andean versant in Peru. Salamandra 38:165–184
Lötters S, Van der Meijden A, Coloma LA, Boistel R, Cloetens P, Ernst R, Lehr E, Veit M (2011) Assessing the molecular phylogeny of a near extinct group of vertebrates: th Neotropical harlequin frogs (Bufonidae; Atelopus). Syst Biodivers 9:45–57. https://doi.org/10.1080/14772000.2011.557403
Lötters S, Plewnia A, Hönig A, Jung A, Laudor J, Ziegler T (2022) The gastromyzophorous tadpole of the pink harlequin frog from Suriname with comments on the taxonomy of Guianan Clade Atelopus (Amphibia, Bufonidae). Zootaxa 5087:591–598. https://doi.org/10.11646/zootaxa.5087.4.7
Lötters S et al (2023) The amphibian extinction crisis is still an emergency. https://doi.org/10.21203/rs.3.rs-2711241/v1
Lynch JD (1986) Notes on the reproductive biology of Atelopus subornatus. subornatus. J Herpetol 20:126–129. https://doi.org/10.2307/1564145
Lynch JD (1993) A new harlequin frog from Cordillera Oriental of Colombia. Alytes 11:77–87
Lynch JD, Suárez-Mayorga AM (2011) Clave ilustrada de los renacuajos en las tierras bajas al oriente de los Andes, con énfasis en Hylidae. Caldasia 33:235–270
Maddison WP, Maddison DR (2021) Mesquite: a modular system for evolutionary analysis. Version 3.70. Available at http://www.mesquiteproject.org
Magalhães FDM, Mercês EDA, Santana DJ, Juncá FA, Napoli MF, Garda AA (2015) The tadpole of Bokermannohyla flavopicta Leite, Pezzuti and Garcia, 2012 and oral cavity anatomy of the tadpole of B. oxente Lugli and Haddad, 2006 (Anura: Hylidae). S Am J Herpetol 10:211–218. https://doi.org/10.2994/SAJH-D-15-00017.1
Marcillo-Lara A, Coloma LA, Álvarez-Solas S, Terneus E (2020) The gastromyzophorous tadpoles of Atelopus elegans and A. palmatus (Anura: Bufonidae), with comments on oral and suction structures. Neotrop Biodivers 6:1–13. https://doi.org/10.1080/23766808.2019.1709378
Matsui M, Yambun P, Sudin A (2007) Taxonomic relationships of Ansonia anotis Inger, Tan, and Yambun, 2001 and Pedostibes maculatus (Mocquard, 1890), with a description of a new genus (Amphibia, Bufonidae). Zool Res 24:1159–1166
McDiarmid RW (1971) Comparative morphology and evolution of frogs of the neotropical genera Atelopus, Dendrophryniscus, Melanophryniscus and Oreophrynella. Bull Los Angeles County Mus Nat Hist 12:1–66
Mebs D (1980) Zur Fortpflanzung von Atelopus cruciger (Amphibia: Salientia: Bufonidae). Salamandra 16:65–81
Mebs D, Yotsu-Yamashita M, Yasumoto T, Lötters S, Schlüter A (1995) Further report of the occurrence of tetrodotoxin in Atelopus species (family: Bufonidae). Toxicon 33:246–249. https://doi.org/10.1016/0041-0101(94)00149-3
Meegaskumbura M, Senevirathne G, Wijayathilaka N, Jayawardena B, Bandara C, Manamendra-Arachchi K, Pethiyagoda R (2015) The Sri Lankan torrent toads (Bufonidae: Adenominae: Adenomus): species boundaries assessed using multiple criteria. Zootaxa 3911:245–261
Mijares-Urrutia A, La Marca E (2005) Los renacuajos de cuatro especies de Atelopus (Anura: Bufonidae) de los Andes de Venezuela. Croizatia 6:33–47
Montesinos R, Carvalho ALG, Silva HR, Anganoy-Criollo M, Dias PHS (2022) The tadpole of Hylodes perere Silva & Benmaman 2008 (Anura: Hylodidae). Zootaxa 5219:388–396. https://doi.org/10.11646/zootaxa.5219.4.6
Montesinos R, Carvalho ALG, Dias PHS (2023) The tadpole of Hylodes amnicola Pombal, Feio & Haddad 2002 (Anura: Hylodidae): external morphology and buccopharyngeal anatomy. Zootaxa 5380:395–400. https://doi.org/10.11646/zootaxa.5380.4.8
Müller H (2019) Description of the tadpole of the critically endangered Ethiopian toad Altiphrynoides osgoodi (Amphibia: Anura: Bufonidae). J Herpetol 53:218–223. https://doi.org/10.1670/19-047
Nascimento FAC, Mott T, Langone JA, Davis CA, de Sá RO (2013) The genus Odontophrynus (Anura: Odontophrynidae): a larval perspective. Zootaxa 3700:140–158. https://doi.org/10.11646/zootaxa.3700.1.5
Nascimento FAC, de Sá RO, Garcia PCA (2021) Larval anatomy of monotypic painted ant nest frogs Lithodytes lineatus reveals putative homoplasies with the Leptodactylus pentadactylus group (Anura: Leptodactylidae). Zool Anz 290:135–147. https://doi.org/10.1016/j.jcz.2020.12.003
Nascimento FAC, de Sá RO, Garcia PCA (2020) Larval anatomy of monotypic painted ant nest frogs Lithodytes lineatus reveals putative homoplasies with the Leptodactylus pentadactylus group (Anura: Leptodactylidae). Zool Anz 290:135–147
Noble GK (1927) The value of life history data in the study of the evolution of the Amphibia. Ann New York Acad Sci 30:31–128. https://doi.org/10.1111/j.1749-6632.1927.tb55359.x
Oliveira MIRR, Weber LN, de Sá RO, Ferreira JS, Libório AEC, Takazone AMG (2017) Chondrocranium and internal oral morphology of the tadpole of Corythomantis greeningi (Anura: Hylidae). PHyllomedusa 16:71–80
Pearson KC, Tarvin RD (2022) A review of chemical defense in harlequin toads (Bufonidae: Atelopus). Toxicon X 13:100092
Peixoto OL, Caramaschi U, Freire EMX (2003) Two new species of Phyllodytes (Anura: Hylidae) from the state of Alagoas, north- eastern Brazil. Herpetologica 59:235–246. https://doi.org/10.1655/0018-0831(2003)059[0235:TNSOPA]2.0.CO;2
Pereyra MO, Womack MC, Barrionuevo JS, Blotto BL, Baldo D, Targino M, Ospina-Sarria JJ, Guayasamin JM, Coloma LA, Hoke KL, Grant T, Faivovich J (2016) The complex evolutionary history of the tympanic middle ear in frogs and toads (Anura). Sci Rep 6:1–9. https://doi.org/10.1038/srep34130
Pérez-Gonzalez JL, Pérez-Gonzalez JL, Rada M, Vargas-Salinas F, Rueda-Solano LA, Rueda-Solano LA (2020) The tadpoles of two Atelopus species (Anura: Bufonidae) from the Sierra Nevada de Santa Marta, Colombia, with notes on their ecology and comments on the morphology of Atelopus larvae. S Am J Herpetol 2020:47–62. https://doi.org/10.2994/SAJH-D-17-00093.1
Peters J (1973) The frog genus Atelopus in Ecuador (Anura: Bufonidae). Smithson Contrib Zool 145:1–49
Pezzuti TL, Santos MTT, Martins SV, Leite FSF, Garcia PCA, Faivovich J (2015) The tadpoles of two species of the Bokermannohyla circumdata group (Hylidae, Cophomantini). Zootaxa 4048:151–173. https://doi.org/10.11646/zootaxa.4048.2.1
Rada M, Dias PHS, Pérez-Gonzalez JL, Anganoy-Criollo M, Rueda-Solano LA, Pinto-E MA, Quintero LM, Vargas-Salinas F, Grant T (2019) The poverty of adult morphology: bioacoustics, genetics, and internal tadpole morphology reveal a new species of glassfrog (Anura: Centrolenidae: Ikakogi) from the Sierra Nevada de Santa Marta, Colombia. PlosOne 14:e0215349. https://doi.org/10.1371/journal.pone.0215349
Raj P, Vasudevan K, Deepak V, Sharma R, Singh S, Aggarwal RK, Dutta SK (2012) Larval morphology and ontogeny of Nasikabatrachus sahyadrensis Biju & Bossuyt, 2003 (Anura, Nasikabatrachidae) from Western Ghats, India. Zootaxa 3510:65–76
Rao D, Yang D (1994) The study of early development and evolution of Torrentophryne aspinia. Zool Res 15:142–157
Rodriguez LO, Duellman WE (1994) Guide to the frogs of the Iquitos Region, Amazonian Peru. Univ Kansas Nat Hist Mus 22:1–113
Romero-Carvajal A, Negrete L, Salazar-Nicholls MJ, Vizuete K, Debut A, Dias PH, Vera CF (2023) Direct development or endotrophic tadpole? Morphological aspects of the early ontogeny of the plump toad Osornophryne occidentalis (Anura: Bufonidae). J Morphol 284:e21582
Rowley JKL, Tran DTA, Le DTT, Hoang HD, Altig R (2012) The strangest tadpole: the oophagous, tree-hole dwelling tadpole of Rhacophorus vampyrus (Anura: Rhacophoridae) from Vietnam. J Nat Hist 46:2969–2978. https://doi.org/10.1080/00222933.2012.732622
Rueda-Solano LA, Vargas-Salinas F, Rivera-Correa M (2015) The highland tadpole of the harlequin frog Atelopus carrikeri (Anura: Bufonidae) with an analysis of its microhabitat preferences. Salamandra 51:25–32
Savage JM (2002) The amphibians and reptiles of Costa Rica: a herpetofauna between two continents, between two seas. University of Chicago Press
Starrett P (1967) Observations on the life history of frogs of the family Atelopodidae. Herpetologica 23:195–204
Stuart SN, Hoffmann M, Chanson J, Cox NA, Berridge RJ, Young BE (2008) Globally threatened amphibian species. Lynx Edicions, Barcelona, Spain; IUCN, Gland, Switzerland; and Conservation International, Arlington, Virginia, USA
Van Eeden JA (1951) The development of the chondrocranium of Ascaphus truei Stejneger with special reference to the relations of the palatoquadrate to the neurocranium. Acta Zool 32:41–176. https://doi.org/10.1111/j.1463-6395.1951.tb00359.x
Vera Candioti MFV (2005) Morphology and feeding in tadpoles of Ceratophrys cranwelli (Anura: Leptodactylidae). Acta Zool 86:1–11. https://doi.org/10.1111/j.0001-7272.2005.00178.x
Vera Candioti MFV (2007) Anatomy of anuran tadpoles from lentic water bodies: systematic relevance and correlation with feeding habits. Zootaxa 1600:1–175. https://doi.org/10.11646/zootaxa.1600.1.1
Vera Candioti MFV, Lavilla EO, Echeverría DD (2004) Feeding mechanisms in two treefrogs, Hyla nana and Scinax nasicus (Anura: Hylidae). J Morphol 261:206–224. https://doi.org/10.1002/jmor.10239
Vera Candioti M, Brusquetti F, Netto F (2007) Morphological characterization of Leptodactylus elenae tadpoles (Anura: Leptodactylidae: L. fuscus group), from central Paraguay. Zootaxa 1435:1–17. https://doi.org/10.11646/zootaxa.1435.1.1
Vera Candioti F, Haas A, Altig R, Peixoto O (2017) Cranial anatomy of the amazing bromeliad tadpoles of Phyllodytes gyrinaethes (Hylidae: Lophyohylini), with comments about other gastromyzophorous larvae. Zoomorphol 136:61–73. https://doi.org/10.1007/s00435-016-0334-7
Vera Candioti MFV, Dias PHS, Rowley JJL, Hertwig S, Haas A, Altig R (2021) Anatomical features of the phytotelma dwelling, egg-eating, fanged tadpoles of Rhacophorus vampyrus (Anura: Rhacophoridae). J Morphol 282:769–778. https://doi.org/10.1002/jmor.21348
Vera Candioti F, Dias PHS, Haas A (in press) Chapter 8: musculoskeletal system. In Viertel, B. (ed.) Anuran Larvae. Chimaira, Frankfurt am Main
Viertel B (1982) The oral cavities of central European anuran larvae (Amphibia). Morphology, ontogenesis and generic diagnosis. Amphibia-Reptilia 3:327–360. https://doi.org/10.1163/156853882X00059
Viertel B, Channing A (2017) The larva of Schismaderma carens (Smith, 1849) (Anura: Bufonidae) - a redescription. Alytes 33:38–46
Viertel B, Veith M, Schick S, Channing A, Kogoolo S, Baeza-Urrea O, Sinsch U, Lötters S (2012) The stream-dwelling larva of the Ruwenzori River Frog, Amietia ruwenzorica, its buccal cavity and pathology of chytridiomycosis. Zootaxa 3400:43–57. https://doi.org/10.11646/zootaxa.3400.1.3
Wake DB, Vredenburg VT (2008) Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proc Natl Acad Sci USA 105:11466–11473. https://doi.org/10.1073/pnas.0801921105
Wassersug RJ (1976) Oral morphology of anuran larvae: terminology and general description. Occ Pap Mus Nat Hist Kansas Univ 48:1–23
Wassersug RJ (1980) Internal oral features of larvae from eight anuran families: functional, systematic, evolutionary and ecological considerations. Univ Kansas Publ Museum Nat Hist 68:1–146. https://doi.org/10.5962/bhl.title.16230
Wassersug RJ, Duellman WE (1984) Oral structures and their development in egg-brooding hylid frog embryos and larvae: evolutionary and ecological implications. J Morphol 182:1–37. https://doi.org/10.1002/jmor.1051820102
Wassersug RJ, Heyer WR (1983) Morphological correlates of subaerial existence in leptodactylid tadpoles associated with flowing water. Can J Zool 61:761–769. https://doi.org/10.1139/z83-101
Wassersug RJ, Heyer WR (1988) A survey of internal oral features of Leptodactyloid larvae (Amphibia: Anura). Contrib Zool 457:1–99. https://doi.org/10.5479/si.00810282.457
Wassersug RJ, Rosenberg K (1979) Surface anatomy of branchial food traps of tadpoles: a comparative study. J Morphol 159:393–425. https://doi.org/10.1002/jmor.1051590307
Womack MC, Christensen J, Hoke KL (2018) Sensitive high-frequency hearing in earless and partially eared harlequin frogs (Atelopus). J Exp Biol 221: jeb169664. https://doi.org/10.1242/jeb.169664
Yotsu-Yamashita, Takei E (2010) First report on toxins in the Panamanian toads Atelopus limosus, A. glyphus and A. certus. Toxicon 55:153–156. https://doi.org/10.1016/j.toxicon.2009.07.003
Acknowledgements
Pedro H. Dias thanks the Marie Sklodowska-Curie Actions (MSCA-IF-2020, MEGAN; 101030742) and the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP Procs. 2013/20420–4 and 2015/11239-0). Marvin Anganoy-Criollo thanks the Fundación Centro de Estudios Interdisciplinarios Básicos y Aplicados (CEIBA, 2016). We are grateful to Stefan Lötters and an anonymous reviewer for their valuable comments, but we stress that any remaining errors are ours. We thank David Kizirian (AMNH), Ana Maria Paulino Telles de Carvalho-e-Silva (UNIRIO), Hélio Ricardo Silva (EI), Roberto Rueda-Solano (CBUMAG), John D. Lynch (ICN), Santiago Ron (QCAZ), Filipe A.C. Nascimento (MUFAL), Gerardo Chaves (UCR), Gregory Schneider (UMMZ), Dennis Rödder (ZFMK), Alexander Haas (ZMH), Mark-Oliver Rödel (ZMB), and Frank Glaw (ZSM) for the access to material housed under their care.
Funding
Open Access funding enabled and organized by Projekt DEAL.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
This work was supported by the Marie Sklodowska-Curie Actions (MSCA-IF-2020, MEGAN; 101030742) and by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP Procs. 2013/20420–4 and 2015/11239–0).
Additional information
Communicated by: Matthias Waltert
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Appendix. Examined material
Appendix. Examined material
All the material used in the present study is housed at American Museum of Natural History (AMNH), Amphibians’ Collection, Universidade Federal do Estado do Rio de Janeiro (UNIRIO), Eugenio Izecksohn, deposited at Universidade Federal Rural do Rio de Janeiro (EI), Herpetological Collection of the Universidad del Magdalena (CBUMAG), Instituto de Ciencias Naturales, Universidad Nacional de Colombia (ICN), Museo de Zoología de la Pontificia Universidad Católica del Ecuador (QCAZ), Museu de História Natural, Universidade Federal de Alagoas (MUFAL), Universidad de Costa Rica (UCR), University of Michigan Museum of Zoology (UMMZ), Zoologisches Forschungsinstitut und Museum Alexander Koenig (ZFMK), Zoological Museum Hamburg (ZMH), Zoologisches Museum Berlin (ZMB), and Zoologische Staatssammlung München (ZSM).
Taxa | Buccopharyngeal cavity |
Amazophrynella minuta | ICN 54915 |
Anaxyrus americanus | UMMZ 139255 |
Ansonia hanitschi | ZMH A08803 |
Atelopus balios | QCAZ 2670 |
Atelopus carrikeri | CBUMAG 0892 |
Atelopus nahumae | ICN 33202 |
Atelopus nanay | QCAZ 3672 |
Atelopus subornatus | ICN 31435 |
Barbarophryne brongersmai | ZMH 12162 |
Bufo bufo | Viertel 1982 |
Dendrophryniscus brevipollicatus | UNIRIO 3394 |
Duttaphrynus melanostictus | ZMH 13591 |
Frostius pernambucensis | EI 7253 |
Incilius coniferus | UCR 18999 |
Ingerophrynus divergens | Inger 1985 |
Melanophryniscus klappenbachi | Baldo et al. 2014 |
Osornophryne occidentalis | Romero-Carvajal et al. 2023 |
Peltophryne peltocephala | AMNH 38451 |
Poyntonophrynus fenoulheti | Lambris 1994 |
Rentapia hosii | Inger 1985 |
Rhaebo glaberrimus | ICN 49629 |
Rhinella marina | ICN 53853 |
Schismaderma carens | |
Sclerophrys maculatus | ZMH 11955 |
Vandijkophrynus gariepensis | Lambris 1994 |
Werneria mertensiana | ZMB 79695 |
Other taxa | |
Amolops cremnobatus | ZFMK 95596 |
Ascaphus truei | ZFMK 44444 |
Astylosternus robustus | ZMB 82040 |
Boophis schubae | ZSM 817–2004 |
Heleophryne hewitti | ZMB 74986 |
Huia cavitympanum | ZMH13441 |
Macrogenioglottus alipioi | MUFAL 10811 |
Meristogenys jerboa | ZMH10164 |
Odontobatrachus fouta | ZMB 88109 |
Odontophrynus cultripes | UFMG 937 |
Phyllodytes gyrinaethes | MUFAL |
Proceratophrys appendiculata | UNIRIO 4036 |
Sumaterana dabulescens | ZMH12654 |
Werneria mertensiana | ZMB 79695 |
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
dos Santos Dias, P.H., Anganoy-Criollo, M. Harlequin frog tadpoles—comparative buccopharyngeal morphology in the gastromyzophorous tadpoles of the genus Atelopus (Amphibia, Anura, Bufonidae), with discussion on the phylogenetic and evolutionary implication of characters. Sci Nat 111, 3 (2024). https://doi.org/10.1007/s00114-024-01889-6
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00114-024-01889-6