Systematics of the Hyloxalus bocagei complex (Anura: Dendrobatidae), description of two new cryptic species, and recognition of H. maculosus

Abstract

The bocagei clade is a species complex of dendrobatid frogs evidenced from recent molecular systematic studies. This lineage is endemic to the eastern Andean slopes and adjacent Amazonian lowlands in southern Colombia, Ecuador and northern Peru. Herein, we analyze the taxonomy of the bocagei clade by means of qualitative and quantitative morphological characters and call parameters. We recognize and provide accounts for six species: Hyloxalus bocagei, H. faciopunctulatus, H. maculosus, H. sauli and two new species. We also provide phylogeographic data. We formally assign the name of Hyloxalus bocagei only to populations from the surroundings of Volcán Reventador (Provincia Napo, Ecuador). Additionally, we describe the tadpoles of Hyloxalus bocagei, H. maculosus, and two new species, plus vocalizations of H. bocagei, H. maculosus, H. sauli, and two new species. Morphological variation was estimated from 16 morphometric characters using multivariate analysis. Adults of the two new species were indistinguishable using quantitative and qualitatively morphological characters. Nevertheless, molecular data, call parameters (dominant frequency, note repetition rate), and tadpole morphology supported the recognition of these two species as cryptic taxa. A current phylogenetic tree using molecular characters of five species of the bocagei clade is also provided including the maximum likelihood (ML) phylogeny and a chronogram of the group. Our phylogeny confirms the close relationship of members of the bocagei clade with Andean relatives of Hyloxalus and recurrent dispersal events from the Andes to the Amazon Basin in the late Miocene (< 10 MYA). Our data also corroborate that the sister lineage of bocagei clade includes the Andean H. subpunctatus clade. We anticipate that further detailed morphological and molecular data will be necessary to reveal the existence of additional cryptic species within the bocagei clade.

Species limits within the widespread Amazonian treefrog Dendropsophus parviceps with descriptions of two new species (Anura, Hylidae)

“…In the last decade, the use of genetic characters in amphibian taxonomy has helped to discover a large number of cryptic species through the upper and lower Amazon Basin (e.g., Almendáriz et al 2014; Brown et al 2008; Brown and Twomey 2009; Caminer and Ron 2014; Elmer and Cannatella 2008; Fouquet et al 2015; Moravec et al 2014; Páez-Vacas et al 2010; Rivera-Correa and Orrico 2013; Rojas et al 2015; Rojas et al 2016; Ron et al 2012; Twomey and Brown 2008). The use of genetic characters in combination with morphological and bioacoustic evidence allows unambiguous delimitation of species under the evolutionary species concept (de Queiroz 1998; de Queiroz 2007; Padial et al 2009).…”

Una nueva rana nodriza de los bosques de niebla asociados a la cuenca del Orinoco de Colombia

“…En Hyloxalus sanctamariensis sp. nov. este rasgo es estable durante el desarrollo ontogénico (Figura 12) con un patrón de manchas (melanóforos) irregulares (condición 1, sensu Grant et al, 2006) que a priori es descrito en Hyloxalus pulchellus (sensu Coloma, 1995), Hyloxalus bocagei (Páez-Vacas et al, 2010), Hyloxalus edwardsi ( sensu Lynch, 1982) e Hyloxalus subpunctatus (sensu Anganoy-Criollo, 2013, cuya variación incluye condiciones 1 y 2).…”

“…Hyloxalus sauli (Edwards, 1974) Duellman 1978Edwards 1974Grant et al 2006 Hyloxalus subpuntactus (Cope,1899) Navas, 1996a, Fandiño et al 1997, Navas y Bevier 2001, Stebbins y Hendrickson 1959, Fandiño et al 1997, Anganoy-Criollo 2013, Sánchez 2013Vences et al 2003, Páez-Vacas et al 2010, Pyron y Wiens 2011, Grant et al 2006, Muñoz et al 2015, Grant et al 2017 Hyloxalus vergeli (Hellmich, 1940) - Sánchez 2013Grant et al 2017 Cont. Tabla 3.…”

“…Durante los últimos 20 años, significativos avances en el desarrollo de hipótesis filogenéticas alrededor de las ranas dendrobátidas han permitido en parte evaluar, delimitar, direccionar y entender las relaciones evolutivas de este complejo grupo bioló-gico (Coloma, 1995;Vences et al, 2000;Grant y Rodríguez, 2001;Vences et al, 2003;Santos et al, 2003;Grant et al, 2006;Páez-Vacas et al, 2010;Pyron y Wiens, 2011;Santos et al, 2014;Grant et al, 2017).…”

Evolution of larval characteres in Dendrobatoidea Cope, 1865 (Amphibia; Anura; Dendrobatidae & Aromobatidae)

“…Tadpoles are frequently poorly described in only few lines of text; in many cases, the described specimens are not illustrated (e.g., Paruwrobates erythromos; Vigle and Miyata 1980) and taxonomic errors permeate the literature (e.g., Dunn 1924), with misleading comparisons and generalizations. Only 157 tadpoles have been described to date (e.g., Savage 1968;Silverstone 1975;Coloma 1995;Mijares-Urrutia and La Marca 1997;Páez-Vacas et al 2010;Grant and Myers 2013; in press)-corresponding to less than 50% of the clade`s diversity-and aspects of the internal morphology are known to c.a. 15 species (e.g., Wassersug 1980;Carr and Altig 1992;Haas 1995).…”