Epipedobates, Myers, 1987

GRANT, TARAN, FROST, DARREL R., CALDWELL, JANALEE P., GAGLIARDO, RON, HADDAD, CÉLIO F. B., KOK, PHILIPPE J. R., MEANS, D. BRUCE, NOONAN, BRICE P., SCHARGEL, WALTER E. & WHEELER, WARD C., 2006, PHYLOGENETIC SYSTEMATICS OF DART-POISON FROGS AND THEIR RELATIVES (AMPHIBIA: ATHESPHATANURA: DENDROBATIDAE), Bulletin of the American Museum of Natural History 299 (299), pp. 1-262 : 1-262

Epipedobates :

• Group 1 (giant types [‘‘Riesenarten’’]): E. bassleri , E. planipaleae , E. silverstonei , E. trivittatus

• Group 2 ( petersi / pictus ): petersi subgroup: E. cainarachi , E. labialis , E. macero , E. petersi , E. pongoensis , E. smaragdinus , E. zaparo ; pictus subgroup: E. bolivianus , E. hahneli , E. pictus , E. rubriventris

• Group 3 ( azureiventris ): E. azureiventris , Phyllobates [i.e., Phyllobates sensu Myers et al., 1978 ]

• Group 4 ( femoralis ): E. femoralis , E. ingeri , E. labialis , E. myersi , E. zaparo

• Group 5 ( parvulus ): E. espinosai , E. parvulus

• Group 6 ( tricolor ): E. anthonyi , E. espinosai , E. parvulus , E. subpunctatus , E. tricolor

Rather than detail exhaustively the relationships Schulte (1999) proposed, we limit ourselves to pointing out a few of his more heterodox hypotheses. Without comment he transferred Prostherapis subpunctatus from Colostethus (where it had been placed by Edwards, 1971) to Epipedobates as sister species to E. anthonyi and E. tricolor . Also without comment, he referred Dendrobates steyermarki and Minyobates virolinensis — both of which had been in Minyobates (Myers, 1987; Ruiz-Carranza and Ramírez-Pinilla, 1992)—to Dendrobates , but he did not discuss the relationships of the remaining species of Minyobates . Further, according to his own diagrams he rendered Epipedobates paraphyletic by grouping E. azureiventris with species of Phyllobates . Schulte redefined the histrionicus group to include D. mysteriosus , but he excluded most of the species Myers et al. (1984) —and even Silverstone (1975a) and Myers and Daly (1976b) —had referred to that group, and he once again placed D. leucomelas in that group (as had Silverstone, 1975a). Relationships among most groups were not specified, but some groups (e.g., Groups 1 and 7) were paraphyletic in Schulte’s own diagrams, and some species (e.g., D. labialis and D. zaparo ; E. parvulus and E. espinosai ) were included in multiple groups, with their relationships to each other being different in each group. No new character systems were added in this study, and, although Schulte provided limit- ed group diagnoses and details on natural history, behavior, coloration and color patterns, and external morphology, no explicit synapomorphies were provided for any of his groups.

Grant (1998) named Colostethus lynchi and argued that it was part of the C. edwardsi group on the basis of the occurrence of a cloacal tube (he did not address the occurrence of this character in Nephelobates ). More specifically, he argued that C. lynchi was the sister species to the group of C. edwardsi + C. ruizi .

The first attempt to address phylogenetic relationships among dendrobatids with DNA sequence data was published by Summers et al. (1997), although that paper only included the distantly related Dendrobates pumilio , Dendrobates claudiae (as Minyobates sp. ), and Phyllobates lugubris (plus C. talamancae , used as the root). Since 1999, nearly a dozen phylogenetic studies of differing scales, scopes, and datasets have appeared ( Summers et al., 1999b; Clough and Summers, 2000; Vences et al., 2000, 2003a; Widmer et al., 2000; Symula et al., 2001, 2003; La Marca et al., 2002; Santos et al., 2003). The cladograms that resulted from those studies are redrawn in figures 5–13 . Interpretation of these studies is complicated by their use of different methods, nonoverlapping taxon samples, and heterogeneous datasets, but their findings can be summarized as follows:

• Colostethus : Found to be either para- or polyphyletic by all authors who tested its monophyly.

• Epipedobates : Found to be monophyletic by Clough and Summers (2000) (with femoralis placed outside in Allobates ) but polyphyletic by Vences et al. (2000, 2003a; see also Santos et al., 2003).

• Phobobates : Found to be monophyletic by Vences et al. (2000) but paraphyletic by Clough and Summers (2000), Santos et al. (2003), and Vences et al. (2003a).

• Allobates : This small genus fell out in a clade with species of Colostethus in Vences et al. (2000, 2003a) and Santos (2003). ( Jungfer and Böhme, 2004 added the enigmatic Dendrobates rufulus to Allobates , but that species has not been included in any analysis.)

• Phyllobates : Without exception, this genus was found to be monophyletic. The optimal topology found by Widmer et al. (2000) was (( vittatus lugubris ) ( aurotaenia ( bicolor terribilis ))) (outgroup taxa were Epipedobates azureiventris and Dendrobates sylvaticus , and the tree was rooted on E. azureiventris ). In their more inclusive study, Vences et al. (2003a) found P. aurotaenia to be the sister of the remainder, and P. bicolor to be sister to the Central American species, giving the topology ( aurotaenia ( terribilis ( bicolor ( lugubris vittatus )))).

• Minyobates : Both Clough and Summers (2000) and Vences et al. (2000) found Minyobates to be nested within Dendrobates . Because each analysis used only one species of Minyobates , they did not test the monophyly of Minyobates itself. Vences et al. (2003a) included M. steyermarki (type species), M. minutus , and M. fulguritus and found Minyobates to be paraphyletic with respect to all other Dendrobates . Santos et al. (2003) included M. minutus and M. fulguritus and found them to be the monophyletic sister to the D. quinquevittatus group (i.e., they recovered a monophyletic minutus group sensu Silverstone, 1975b).

• The Dendrobates histrionicus group is monophyletic in all studies that test its monophyly.

• The Dendrobates quinquevittatus group is potentially monophyletic. Although the tree presented by Clough and Summers (2000: 524) indicates that Minyobates minutus is the sister species of a monophyletic D. quinquevittatus group, there is in fact no evidence to support this assertion, given that these nodes collapse in the strict consensus. Symula et al. (2003) found Dendrobates leucomelas to be sister to part of the D. quinquevittatus group, with a D. quinquevittatus + D. castaneoticus clade in a basal trichotomy (they rooted the network with D. histrionicus , so it is unknown from their results if D. quinquevittatus + D. castaneoticus or D. histrionicus is more closely related to the D. leucomelas + other D. quinquevittatus group clade).

• Nephelobates and Mannophryne were both found to be monophyletic by La Marca et al. (2002) and Vences et al. (2003a).

Lötters et al. (2000) erected the new genus Cryptophyllobates for Phyllobates azureiventris (which was placed in Epipedobates by Myers and Burrowes, 1987). The justification for this monotypic genus is somewhat convoluted. On pp. 235–236, the authors stated that ‘‘from the genetic point of view, it is apparent that azureiventris is more closely related to Epipedobates than to Phyllobates ’’, but that ‘‘the species is not a member of Epipedobates , from which it differs by at least one apomorphy.’’ However, they also asserted that ‘‘[i]t shares more—but not all— characters with Phyllobates from which it appears genetically well separated.’’ Similarly, although Vences et al. (2000) found this species to be the sister of Colostethus bocagei, Lötters et al. (2000) stated that they ‘‘negate that both species are representatives of the same genus for C. bocagei is cryptically coloured, lacking dorsal stripes at all, and possesses webbed feet.’’ Insofar as this change did not fix the nonmonophyly of Epipedobates , the creation of this monotypic genus did little to improve matters. Recently, Caldwell (2005) described a new species and referred it to this genus based on the sister-species relationship between the new species and azureiventris recovered in an independent phylogenetic study, despite noting that these species ‘‘were nested in a clade of Ecuadorian and Peruvian Colostethus .’’

Morales (2002 ‘‘2000’’) combined Rivero’s Groups II ( brunneus ) and III ( alagoanus ) into a newly defined trilineatus group (which excluded C. kingsburyi and C. peruvianus ) on the basis of an analysis of 12 characters. However, in addition to problems of character individuation (e.g., characters 6, ‘‘línea lateral oblicua’’, and 10, ‘‘lista oblicua anteroinguinal’’, are logically dependent; see Grant and Rodríguez, 2001), the monophyly of the group was assumed (the cladogram was rooted on an unspecified ‘‘ Hylodes ’’ and no other dendrobatids were included), and the putatively derived states of all 12 characters are well known to occur in many dendrobatids.

In the most recent contribution to dendrobatid phylogenetics, Graham et al. (2004) added 12S, tRNA val, and 16S mtDNA sequences from a specimen collected near the type locality of Epipedobates tricolor and analyzed them with the data from Santos et al. (2003). Graham et al. reported that the E. tricolor sample from southern Ecuador was more closely related to Colostethus machalilla than to true E. tricolor , and, as such, they resurrected E. anthonyi from synonymy with E. tricolor . However, the Bremer support value 1 reported for the critical node is 0, meaning that this relationship is not recovered in other, equally parsimonious solutions.

PART III: 1926– PRESENT, RELATIONSHIPS BETWEEN DENDROBATIDAE AND OTHER FROGS

Noble (1931) summarized his research on the evolutionary relationships of anurans. He considered the three genera of dendrobatids, which he had grouped together in his earlier paper ( Noble, 1926), to be a subfamily of Brachycephalidae . The other subfamilies were Rhinodermatinae ( Geobatrachus , Sminthillus , and Rhinoderma ) and Brachycephalinae ( Atelopus , Brachycephalus , Dendrophryniscus , and Oreophrynella ). Noble (1931: 505; see Grant et al., 1997: 31, footnote 18) maintained his curious view that independently derived groups may constitute natural assemblages:

Each subfamily has arisen from a different stock of bufonids, but as all the ancestral stocks were bufonids residing in the same general region, Brachycephalidae may be considered natural, even though a composite, family.

1 Graham et al. (2004) did not define the numbers on the nodes in their cladogram, but C. H. Graham (personal commun.) informed us that they are bootstrap frequencies (above) and Bremer values (below).

Particularly, Noble (1931; see also Noble, 1926) reiterated that Dendrobatinae evolved from the elosiine bufonid genus Crossodactylus . Brachycephalidae was included in the suborder Procoela , which also contained Bufonidae and Hylidae , as well as the extinct Palaeobatrachidae .

Noble was aware that his placement of Brachycephalidae in Procoela instead of Diplasiocoela could be viewed as problematic. He ( Noble, 1931: 514) pointed out that the frogs he referred to Diplasiocoela ‘‘differ strikingly from most other Salientia except Brachycephalidae’’, but he reasoned that ‘‘[t]he latter are purely neotropical, and as the genera of Brachycephalidae are well defined, they should not be confused with the Diplasiocoela.’’ He also observed that both Dendrobatinae and the African ranid Petropedetinae (nested well within Diplasiocoela) had ‘‘apparently identical’’ ( Noble, 1931: 520) dermal scutes on the upper surface of each digit, but he explained away this similarity as adding ‘‘one more to the many cases of parallel evolution in the Salientia’’.

Although Noble’s general scheme was widely accepted as the standard for decades (e.g., Dunlap, 1960), it attracted extensive criticism almost immediately. For example, Trewavas (1933: 517) concluded that the hyolaryngeal apparatus provided ‘‘little support for the inclusion of Dendrobates in the family [ Brachycephalidae ]’’ and recommended that the relationships of the family be reconsidered. Davis (1935: 91) criticized Noble’s belief that independently derived taxa could be grouped naturally, and he raised each of Noble’s (1931) brachycephalid subfamilies (i.e., Brachycephalinae, Dendrobatinae , and Rhinodermatinae) to family rank. Laurent (1942: 18; translated, italics as in original) concluded that the similarities in the initial phases of parental care of larvae in dendrobatids (tadpoles are transported on the male’s back) and rhinodermatids (tadpoles are transported in the male’s mouth) ‘‘constituted a weighty argument in favor of the common ancestry of the Rhinodermatinae and the Dendrobatinae ’’, and he included both in Dendrobatidae . Orton (1957; see also Orton, 1953) was highly critical of Noble’s system because it conflicted with larval morphology; but, beyond her rejection of suborder rank within Salientia, dendrobatids were unaffected. Likewise, Reig (1958) incorporated evidence from a variety of previous studies (e.g., Trewavas, 1933; Davis, 1935; Walker, 1938; Taylor, 1951; Griffiths, 1954) and his own fossil work to provide an extensively modified higher taxonomy, but the placement of Dendrobatidae was unaffected (i.e., Reig’s neobatrachian ‘‘Superfamily A’’ [now Hyloidea, 5 Bufonoidea auctorum] was identical to Noble’s Procoela with the exclusion of Palaeobatrachidae ).

Griffiths (1959, 1963) provided the first major challenge to Noble’s placement of Dendrobatidae . Griffiths (1959) reviewed Noble’s (1922, 1926, 1931) evidence that dendrobatids were part of Procoela and related to Crossodactylus , and, arguing that (1) ‘‘vertebral pattern has not the exact taxonomic validity vested in it by Noble’’ (p. 481); (2) path of insertion of the m. semitendinosus is ranoid in Hyloxalus ; (3) ‘‘Noble’s claim that Phyllobates has an arciferal stage cannot be held’’ (p. 482); (4) the bursa angularis oris is found only in firmisternal genera; (5) dermal scutes (which he claimed to be ‘‘glandulo-muscular organs’’) on the digits occur in petropedetid ranids (as well as Crossodactylus ); and (6) the breeding habits of dendrobatids ‘‘are found in no other Salientia except in the arthroleptid ranids’’ (p. 483), proposed ‘‘that the Dendrobatinae be redefined as a Neotropical subfamily of the Ranidae’’ (p. 483). Subsequent reviews either explicitly endorsed (e.g., Hecht, 1963: 31) or did not address (e.g., Tihen, 1965; Inger, 1967; Kluge and Farris, 1969) Griffiths’s hypothesis of the relationships of dendrobatids.

However, Lynch (1971: 164; see also Lynch, 1973) supported Noble’s hypothesis, arguing that elosiines (including Crossodactylus ) and dendrobatids ‘‘agree in cranial morphology, vertebral columns, the Tshaped terminal phalanges, the dermal glandular pads on top of the digital pads, and in the presence, in at least some species of each group, of toxic skin secretions’’ (see fig. 14 ).

Lynch (1971: 164) also asserted that Crossodactylus and dendrobatids exhibit the ranoid pattern of thigh musculature, which ‘‘mitigates the importance of one of the criteria used by Griffiths (1963) to associate the dendrobatids as a Neotropical subfamily the Ranidae .’’ Interestingly, Lynch (1971: 210–211) also indicated that there was ‘‘considerable similarity in myology and osteology’’ between the Neotropical leptodactyloid Elosiinae and Dendrobatidae and the African ranid subfamily Petropedetinae . Further, although he cautioned that his examination of the African taxa was not exhaustive, he stated that ‘‘[t]he similarities are quite striking and probably reflect a community of ancestry rather than parallelism.’’

Lynch’s (1971, 1973) resurrected version of Noble’s (1926) hypothesis stood for 15 years. For example, although Savage (1973) adopted Starrett’s (1973) scheme of higher level relationships and did not discuss dendrobatid phylogeny per se, he followed Lynch (1971) in considering Dendrobatidae to be a South American, tropical, leptodactyloid derivative. Bogart (1973: 348) conjectured that ‘‘ Dendrobatidae may be derived chromosomally from a 26-chromosome ancestor, such as the leptodactylid Elosia ’’ (although he did not examine any African

Figures

Fig. 5. Hypothesized phylogeny of Dendrobates, redrawn from Summers et al. (1999b: 261, fig. 1), based on parsimony analysis of cytochrome oxidase I, cytochrome b, and 16S DNA sequences aligned with Clustal W (Thompson et al., 1994) (parameters not specified) and modified manually, excluding ambiguously aligned regions. Numbers are bootstrap frequencies (unlabeled nodes present in fewer than 50% of replicates).

Fig. 6. Hypothesized phylogeny of dendrobatids, redrawn from Clough and Summers (2000: 342, fig. 1), based on parsimony analysis of 12S, 16S, and cytochrome b DNA sequences aligned with Clustal W (Thompson et al., 1994) (parameters not specified) and modified by eye and excluding ambiguously aligned regions. Numbers are bootstrap frequencies (unlabeled nodes present in fewer than 50% of replicates).

Fig. 7. Hypothesized phylogeny of dendrobatids, redrawn from Vences et al. (2000: 37, fig. 1), based on neighbor-joining analysis of 16S DNA sequences aligned manually and excluding highly variable regions. Numbers are bootstrap frequencies (unlabeled nodes present in fewer than 50% of replicates).

Fig. 8. Hypothesized phylogeny of dendrobatids, redrawn from Widmer et al. (2000: 561, fig. 2), based on parsimony analysis of cytochrome b sequences aligned with Clustal W (Thompson et al., 1994) (parameters not specified). Numbers are parsimony/maximum likelihood/neighbor-joining bootstrap frequencies.

Fig. 14. Hypothesized phylogeny of anurans, redrawn from Lynch (1973).