Rhinella
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publication ID |
https://doi.org/ 10.1206/0003-0090.447.1.1 |
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persistent identifier |
https://treatment.plazi.org/id/AC6D87D2-FFD3-1558-FF89-FC287FAAF91C |
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treatment provided by |
Felipe |
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scientific name |
Rhinella |
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DIAGNOSIS: The long third pair of external gills (char. 79.2) optimizes as the only phenotypic synapomorphy of Rhinella in all the MPTs, which reverts to short third pair of external gills, the plesiomorphic bufonid condition, in the R. granulosa Group. An unequivocal diagnosis of this genus is obscured by the large phenotypic variation within Rhinella that overlaps with the diversity of many of the related bufonid genera. Nevertheless, this genus can be diagnosed from most of the related bufonids by the combination of the following phenotypic characters: (1) nasals and frontoparietal heavily ornamented with pits, striations, and rugosities (char. 9.2); (2) presence of a row of dorsolateral tubercles on skin (char. 57.1); and (3) nucleolar organizer regions (NORs) located on interstitial position of the short arms of the chromosome pair 7 (char. 89.4).
SISTER CLADE: The well-supported clade composed of Anaxyrus + Incilius (JGC = 96%, JAF = 97%).
DISTRIBUTION: Mostly Neotropical, ranging from the southern United States to southern South America. Rhinella marina is a highly invasive species introduced in many countries and islands outside its native distribution (e.g., Antilles, Australia, Hawaii, Philippines, Taiwan, etc.; see Frost, 2020; IUCN, 2020).
COMMENTS: The exclusion of the former Bufo ceratophrys renders Rhinella monophyletic. The two large clades of Rhinella were not recovered in previous phylogenetic analyses (e.g., Pramuk, 2006: fig. 4; Chaparro et al., 2007; Pramuk et al., 2008; van Bocxlaer et al., 2010: suppl. information S1; Pyron and Wiens, 2011; Pyron, 2014: supp. information “amph_shl.tre”; Portik and Papenfuss, 2015; Pereyra et al., 2016a; Jetz and Pyron, 2018: suppl. information “amph_shl_new. tre”). Vera Candioti et al. (2016) proposed the long third pair of external gills as a putative synapomorphy of Rhinella in the context of a review of embryonic morphology of Bufonidae . Our TE analysis supports this character state as synapomorphy of the genus, although the embryonic morphology of many genera of Bufonidae and species of the R. margaritifera Clade (see below) is unknown. This synapomorphy of Rhinella reverts to the plesiomorphic state (short third pair of external gills) in the R. granulosa Group.
As a result of our TE analysis (also see ML result), we define two major clades, the Rhinella marina Clade and the R. margaritifera Clade, composed of eight species groups within Rhinella . The R. marina Clade includes (1) the R. arunco Group (new species group); (2) the R. crucifer Group; (3) the R. granulosa Group; (4) the R. marina Group; and (5) the R. spinulosa Group as redefined here. The second clade, the R. margaritifera Clade, is composed of (1) R. sternosignata , a species unassigned to any group; (2) the R. festae Group as redefined here; (3) the R. margaritifera Group as redefined here; and (4) the R. veraguensis Group as redefined here. Below, we provide diagnoses, content, and comments on the distribution and systematics of each of the newly defined major clades and all species groups of Rhinella . The clades and species group are presented in the order described above and correspond to the sequence in which they appear in the TE tree (figs. 10–14) from base to tip and top to bottom.
THE RHINELLA MARINA CLADE (figs. 11, 12)
DIAGNOSIS: This clade is moderately supported (JGC = 88%, JAF = 92%) and diagnosed by a phenotypic synapomorphy: larval otic capsule with poorly developed processus anterolateralis with a rounded aspect (char. 76.1), with one instance of homoplasy in Sclerophrys regularis .
SISTER CLADE: The Rhinella margaritifera Clade (figs. 13, 14).
CONTENTS: The Rhinella marina Clade is composed of the R. crucifer , R. granulosa , and R. marina Groups , the R. spinulosa Group as redefined here, and the R. arunco Group, a new group defined here (see below). Moreover, we found a divergent mitochondrial lineage introgressed into R. horribilis (hereafter referred to as GIM [ghost introgressed mitochondrion], see below and discussion) that does not seem to belong to any recognized extant species of Rhinella and was recovered as sister clade of the R. marina + R. crucifer Groups (see fig. 12), although with poor support (see below).
DISTRIBUTION: The species of this clade naturally occur in all main biogeographic regions of the Neotropics.
COMMENTS: The Rhinella marina Clade is composed of two subclades. One is poorly supported (JGC = 68%, JAF = 82%) and includes the R. arunco + R. spinulosa Groups (fig. 11). It is diagnosed by four phenotypic synapomorphies: (1) the supraorbital flange on frontoparietal does not extend laterally beyond the lateral margin of the sphenethmoid (char. 17.0, with instances of homoplasy in R. quechua and some outgroups); (2) the m. extensor digitorum on the metacarpophalangeal joint of digiti III (char. 44.1, with instances of homoplasy in Anaxyrus woodhousii [polymorphic], Rhinella hoogmoedi , R. jimi , and R. rumbolli ); (3) parotoid gland round to ovoid, mostly symmetrical (char. 56.2, with instances of homoplasy in R. bergi and several species of the R. margaritifera Clade); and (4) vocal sac absent in adult males (char. 58.0, with instances of homoplasy within Rhinella and outgroups). The other subclade is well supported (JGC and JAF = 99%) and includes the R. crucifer , R. granulosa , and R. marina Groups , and the GIM (figs. 11, 12). Three phenotypic synapomorphies are recovered for this subclade: (1) occurrence of a well-developed supraorbital crest (char. 1.2, with instances of homoplasy in several bufonids); (2) occipital artery pathway completely covered with bone (char. 10.2, with instances of homoplasy in bufonids); and (3) general pattern of coloration of caudal musculature of larvae uniformly dark except an unpigmented longitudinal stripe along the inferior edge (char. 69.1, with instances of homoplasy in R. quechua , R. veraguensis , and some outgroups).
Previous phylogenetic studies including less complete sampling of Rhinella (Pramuk, 2006; Pramuk et al., 2008; van Bocxlaer et al., 2010; Pyron and Wiens, 2011; Pyron, 2014; Portik and Papenfuss, 2015; Pereyra et al., 2016a; Jetz and Pyron, 2018) never found a sister relation between the clade composed of the R. arunco + R. spinulosa Groups and the clade composed of the R. granulosa + (R. crucifer + R. marina ) Groups. Instead, these studies found the R. arunco and R. spinulosa Groups as: (1) the sister clade of the species of the R. margaritifera Clade as defined here (Pramuk, 2006), (2) as sister clade of the remaining species of Rhinella (Pramuk et al., 2008; Pereyra et al., 2016a), or (3) as successive sister clades of the remaining species of Rhinella (van Bocxlaer et al., 2010; Pyron and Wiens, 2011; Pyron, 2014; Portik and Papenfuss, 2015; Jetz and Pyron, 2018). In contrast to all these analyses, our ML analysis recovers the R. arunco Group as the sister clade of the remain- der of the R. marina Clade, whereas the R. spinulosa Group is the sister taxon of the clade composed of R. granulosa + (R. crucifer + R. marina ) Groups. This last clade has always been recovered as monophyletic in previous phylogenetic analyses (Pramuk, 2006; van Bocxlaer et al., 2010; Pyron and Wiens, 2011; Pyron, 2014; Portik and Papenfuss, 2015; Pereyra et al., 2016a; Jetz and Pyron, 2018).
THE RHINELLA ARUNCO GROUP
DIAGNOSIS: Two phenotypic synapomorphies diagnose this strongly supported (JGC and JAF = 100%) species group: (1) jaw articulation opposite to the fenestra ovalis (char. 16.1, with instances of homoplasy in some species of the Rhinella granulosa Group, the R. margaritifera Clade, and in Nannophryne variegata ); and (2) anterior edge of sacral diapophyses perpendicular to the midline axis of the vertebral column (char. 30.1, with instances of homoplasy in R. crucifer , R. quechua , R. rubescens , R. spinulosa , and R. vellardi ). The presence of an insertion of the m. extensor digitorum longus on metatarsophalangeal joint of digit V (char. 40.1) and the presence of an insertion of the m. extensor digitorum on metacarpophalangeal joint of digiti V (char. 45.1) could represent two additional synapomorphies of this group or an internal clade. Moreover, species of the R. arunco Group can be distinguished from members of the other species groups of Rhinella by the following combination of character states: (1) preorbital crest weak (char. 0.1), (2) occipital artery pathway uncovered with bone (char. 10.0), (3) frontoparietal that does not extend laterally beyond the lateral margin of the sphenethmoid (char. 17.0), (4) medial ramus of the pterygoid fused with the anterolateral margin of the parasphenoid (char. 21.1), (5) m. extensor digitorum longus with an insertion on the metatarsophalangeal joint of the digit IV (char. 39.1), (6) m. extensor digitorum with an insertion on the metacarpophalangeal joint of digiti III (char. 44.1), (7) inguinal fat bodies present (char. 51.1), (8) row of dorsolateral tubercles absent (char. 57.0), (9) vocal sac absent in adult males (char. 58.0), and (10) eggs biserially disposed in strings (char. 87.1).
SISTER CLADE: The Rhinella spinulosa Group.
CONTENTS (3 SPECIES): Rhinella arunco (Molina, 1782) , R. atacamensis ( Cei, 1962) , and R. rubropunctata ( Guichenot, 1848).
DISTRIBUTION: Species of the Rhinella arunco Group are distributed in Argentina and Chile: Rhinella arunco and R. atacamensis in the Atac- ama Desert region, R. rubropunctata in the Austral Temperate Forest region ( Cei, 1962, 1980; Correa et al., 2013). See map 1 (available at https://doi.org/10.5531/sd.sp.46) for type localities and sampled localities.
COMMENTS: Pramuk (2006) found the Rhinella spinulosa Group (sensu Duellman and Schulte, 1992) as nonmonophyletic and excluded the species now placed in Nannophryne (i.e., N. apolobambica, N. cophotis , N. corynetes, and N. variegata ; see Frost et al., 2006; Frost, 2020). The remaining species constituted a well-supported clade in her combined (morphological and molecular) analysis, being the sister taxon to all the remaining species of Rhinella . A subsequent molecular phylogeny (Pramuk et al., 2008) considering a similar taxon sampling and mitochondrial genes, but several different nuclear genes with respect to Pramuk (2006; cxcr4 and rag1 -a vs pomc and rag1 -a), recovered this redelimited group as monophyletic with poor support. Previous and subsequent analyses with slightly increased taxon and gene sampling, however, found this group as paraphyletic with respect to all remaining species groups of Rhinella ( Frost et al., 2006; van Bocxlaer et al., 2010; Pyron and Wiens, 2011; Pyron, 2014; Portik and Papenfuss, 2015; Jetz and Pyron, 2018), or as the (poorly supported) sister taxon of all other species of Rhinella (Pereyra et al., 2016a) . In our TE analysis, the former R. spinulosa Group (including R. gallardoi , see below) was recovered as monophyletic but poorly supported (JGC = 68%, JAF = 82%). Moreover, the individual monophyly of its sister subclades is strongly supported (both with JGC and JAF = 100%) and can be diagnosed by phenotypic synapomorphies (see Diagnosis of both groups). Our ML analysis found the former R. spinulosa Group paraphyletic with respect to the remaining species groups of the R. marina Clade (supplementary data 4.2). Based on these observations, we restrict the R. spinulosa Group to the strongly supported clade containing most species of the former R. spinulosa Group (and including R. gallardoi ), and exclude the extra- Andean species R. arunco , R. atacamensis , and R. rubropunctata that constitute another well-supported clade, herein recognized as the R. arunco Group. The southernmost distributed species R. arunco and R. rubropunctata are recovered as sister taxa, although with poor support (JGC = 25, JAF <50%). The three species of this group show a high genetic differentiation in comparison to other species groups of the R. marina Clade (see tables 3–6). Natural hybridization between R. arunco and R. atacamensis was reported by Correa et al. (2012, 2013), but they did not find mitochondrial and nuclear introgression outside a narrow hybrid zone.
THE RHINELLA SPINULOSA GROUP
DIAGNOSIS: The following character states optimize as phenotypic synapomorphies of this strongly supported group (JGC and JAF = 100%) in our TE analysis: (1) pretympanic crest absent or indistinguible (char. 2.0, with instances of homoplasy in Rhinella arunco , R. castaneotica , R. festae , and some outgroups); (2) nasal and frontoparietal bones articulating only laterally (char. 8.1, homoplastic in R. quechua , R. rubropunctata, R. veraguensis , R. yanachaga , Rhinella sp. 14, and some outgroups); (3) lightly exostosed dermal roofing bones (char. 9.1, homoplastic in the R. festae Group, in several species of the R. marina Group, and outgroups); and (4) slightly enlarged otic ramus of squamosal, overlapping with the dorsal surface of the crista parotica (char. 11.1). In addition, species of the R. spinulosa Group can be distinguished from members of the other species groups of Rhinella by the following combination of character states: (1) occipital artery pathway not covered by bone (char. 10.0), (2) frontoparietal that does not extend laterally beyond the lateral margin of the sphenethmoid (char. 17.0), (3) medial ramus of the pterygoid fused with the anterolateral margin of the parasphenoid (char. 21.1), (4) m. extensor digitorum longus with an insertion on metatarsophalangeal joint of digiti IV (char. 39.1), (5) m. extensor digitorum with an insertion on the metacarpophalangeal joint of digiti III (char. 44.1), (6) inguinal fat bodies present (char. 51.1), (7) mul- tiserial configuration of eggs in the jelly string (char. 87.2), (8) tarsal fold present (char. 65.1), and (9) adhesive gland divided after fusion of the operculum in embryo (char. 82.2).
SISTER CLADE: The Rhinella arunco Group.
CONTENTS (9 SPECIES): Rhinella achalensis ( Cei, 1972b) , R. altiperuviana ( Gallardo, 1961) new status, R. amabilis (Pramuk and Kadivar, 2003) , R. gallardoi ( Carrizo, 1992) , R. limensis (Werner, 1901) , R. papillosa (Philippi, 1902), new status, R. spinulosa (Wiegmann, 1834) [including R. arequipensis (Vellard, 1959) , new synonymy, see below], R. trifolium (Tschudi, 1845) new status, and R. vellardi (Leviton and Duellman, 1978) .
DISTRIBUTION: This species group is mostly distributed in arid regions along the Andes of Argentina, Bolivia, Ecuador, Chile, and Peru, except Rhinella gallardoi that inhabits the humid subandean forest of Argentina (Vellard, 1959; Córdova, 1999; Pramuk and Kadivar, 2003; Lavilla and Cei, 2001). Rhinella achalensis and R. limensis are the only species of this group with an extra-Andean distribution in the Sierras Pampeanas Centrales in the Pampas region of Argentina and Atacama Desert of Peru respectively (Vellard, 1959; Cei, 1972b). See map 2 (available at https://doi.org/10.5531/sd.sp.46) for type localities and sampled localities.
COMMENTS: The Rhinella spinulosa Group as redelimited here is composed of some taxa with controversial taxonomies that are discussed in the context of our results. The widespread, polytypic, and poorly defined species R. spinulosa is recovered as nonmonophyletic, with R. achalensis , R. gallardoi , and R. arequipensis nested within it (fig. 11). Based on our results and considering that “ Peru ” is the type locality of R. spinulosa (and putatively confined to southern Peru, see Vellard, 1959), we restrict the species R. spinulosa s.s. to the well-supported lineage (JGC = 95%, JAF = 97%), composed of the populations from southern Peru and northern Bolivia. The lineage containing these populations of R. spinulosa also includes the sampled specimen of R. arequipensis from Departamento Arequipa, Peru. Rhinella arequipensis was originally described as a subspecies of R. spinulosa based only on differences in coloration and density of granular formations in the dorsal tegument (Vellard, 1959). Morrison (1992, 1994), Córdova (1999), and Aguilar and Gamarra (2004) did not find morphological, osteological, karyological, or larval differences that could discriminate between R. spinulosa and R. arequipensis . According to these observations and our results, we consider Bufo spinulosus arequipensis Vellard, 1959 , a junior synonym of Rhinella spinulosa (Wiegmann, 1834) . Thus, the species R. spinulosa is restricted to the populations distributed mainly along the Andean Puna of Peru and adjacent Bolivia.
Populations of Rhinella spinulosa that had been considered as R. s. trifolium were recovered as a distinct and strongly supported lineage (JGC and JAF = 98%) sister to a poorly supported clade (JGC <25%, JAF <50%) containing R. spinulosa s.s. and several other species of the group (see below). There are several morphological differences between R. s. trifolium and R. spinulosa s.s. Vellard (1959) pointed out the disposition of the dorsal glands (longitudinal rows in R. s. trifolium and a uniform distribution in R. s. spinulosa ) and the occurrence of a middorsal vertebral line in R. s. trifolium , as the main distinguishing characters. Morrison (1992, 1994), Sinsch (1986), Haas (2002), and Pramuk and Kadivar (2003) considered R. spinulosa s.s. and R. s. trifolium (and also R. s. flavolineata) as variations of a single species (see below), although all but Haas failed to provide detailed justification. The morphological comparisons were some superficial and a detailed reevaluation of the specimens and comparisons with topotypes is needed. Córdova (1999) and Aguilar and Gamarra (2004) did not find karyological or larval differences between R. s. spinulosa and R. s. trifolium ; however, these character systems are conserved in related species of Rhinella (see Tolledo and Toledo, 2010; Kolenc et al., 2013; Blotto et al., 2014). The UPDs between the specimens of R. s. trifolium and R. spinulosa s.s. are relatively high for this species group (1.11%–1.30%, see table 4). Consequently, the differences in adult morphology proposed by Vellard (1959) and their genetic divergence support the recognition of Rhinella trifolium (Tschudi, 1845) as a distinct species.
Some populations currently assigned to Rhinella spinulosa s.l. from Jujuy ( Argentina) and La Paz ( Bolivia) were recovered as another distinct and strongly supported lineage ( JGC and JAF = 100%; see fig. 4) with a low UPD between them (0.18%). In the intermediate area of Puna between these localities (~ 800 km) lays the type locality of R. s. altiperuviana ( Challapata , Oruro, Bolivia). Gallardo (1961) described this subspecies from two adult females ; the characters used to differentiate it from R. spinulosa s.l. (i.e., tubercles structure, head shape, tarsal fringe development) show considerable variation, at least, in the studied female specimens from northwestern Argentina. Thus, we tentatively assign these populations to R. s. altiperuviana. In addition to the phylogenetic position, these specimens differ in UPDs (see table 4) and adult and larval external morphology (B.L.B., D.B., M.O.P., personal obs.) from other species of the group. For these reasons, these populations should be considered as a distinctive species, R. altiperuviana ( Gallardo, 1961) from the Andean Puna of Argentina and Bolivia. A detailed taxonomic revision is beyond the scope of this work but will be discussed in a subsequent contribution (B.L.B. and M.O.P., in prep.) .
Populations of Rhinella spinulosa that had been considered as R. s. papillosa are recovered as a strongly supported lineage (JGC and JAF = 100%), sister taxon of R. achalensis . Both taxa differ in UPDs (1.10 to 1.47%, see table 4), and are morphologically differentiable from R. spinulosa s.s. (B.L.B. and M.O.P., in prep.). Thus, we consider R. papillosa (Philippi, 1902), a valid species from the austral Andes of Argentina and Chile.
Rhinella gallardoi is deeply nested within the R. spinulosa Group. In the original description, Carrizo (1992) highlighted the “broad skull” of this species over the general morphological similarity with the species of the R. spinulosa Group and assigned it to the “ Bufo veraguensis-typho-
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Departamento de Geologia, Universidad de Chile |
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