Monday, July 9, 2018

[Herpetology • 2018] A Pan-Amazonian Species Delimitation: High Species Diversity within the Genus Amazophrynella (Anura: Bufonidae)


 (A–B) Amazophrynella minuta; (C–D) Ateko sp. nov.; (E–F) A. siona sp. nov.; (G–H) A. xinguensis sp. nov.;


(O) A. matses; (Q) A. javierbustamantei; (S) Avote; (U) A. moisesii sp. nov.

Rojas, Fouquet, Ron, Hernández-Ruz, Melo-Sampaio, et al​., 2018. 
photos by Rommel R. Rojas, Antoine Fouquet, Santiago R. Ron, Emil Hernándes-Ruz, Juan Carlos Chapparro,  Robson W. Ávila & Paulo R. Melo-Sampaio.

Abstract
Amphibians are probably the most vulnerable group to climate change and climate-change associate diseases. This ongoing biodiversity crisis makes it thus imperative to improve the taxonomy of anurans in biodiverse but understudied areas such as Amazonia. In this study, we applied robust integrative taxonomic methods combining genetic (mitochondrial 16S, 12S and COI genes), morphological and environmental data to delimit species of the genus Amazophrynella (Anura: Bufonidae) sampled from throughout their pan-Amazonian distribution. Our study confirms the hypothesis that the species diversity of the genus is grossly underestimated. Our analyses suggest the existence of eighteen linages of which seven are nominal species, three Deep Conspecific Lineages, one Unconfirmed Candidate Species, three Uncategorized Lineages, and four Confirmed Candidate Species and described herein. We also propose a phylogenetic hypothesis for the genus and discuss its implications for historical biogeography of this Amazonian group.



Amazophrynella teko sp. nov.
 Amazonella sp. Guianas (Fouquet et al., 2012a: 829, French Guiana [in part])
Amazophrynella sp. Guianas (Fouquet et al., 2012b: 68, French Guiana [in part])
Amazophrynella sp. Guianas (Rojas et al., 2015: 85, French Guiana [in part])
Amazophrynella sp1. (Fouquet et al., 2015: 365, French Guiana [in part])
Amazophrynella sp. aff. manaos (Rojas et al., 2016: 49, French Guiana [in part])

Diagnosis. An Amazophrynella with (1) SVL12.9–15.8 mm in males, 17.9–21.5 mm in females; (2) snout acute in lateral view; upper jaw, in lateral view, protruding beyond lower jaw; (3) texture of dorsal skin granular; (4) cranial crest, vocal slits and nuptial pads absent; (5) dorsum covered by abundant rounded granules; (6) abundance of granules on tympanic area, on edges of upper arms and on dorsal surface of arms; (7) ventral skin highly granular; (8) fingers slender, basally webbed; (9) finger III relatively short (HAL/SVL 0.2–0.22 mm, n = 30); (10) finger I shorter than finger II; (11) palmar tubercle protruding and elliptical; (12) hind limbs relatively short (TAL/SVL 0.48–0.49, n = 30); (13) toes slender, basally webbed; in life: (14) venter cream; small blotches on venter.

Distribution and natural history. Amazophrynella teko sp. nov. have been recorded from the district of Saint Laurent du Marioni, Saint Georges and Camopi, French Guiana, the state of Amapá, Brazil and in the southern region of Suriname (A Fouquet, pers. obs., 2017). It occurs at elevations ranging from 70 m a.s.l. to 350 m a.s.l. The species is diurnal and crepuscular but is also active at night during peak breeding period, which normally occurs at the beginning of the rainy season (January–February). This species shows a conspicuous sexual dimorphism, with males being much smaller than females. The conservation status of this species remains unknown. The habitat destruction and pollution must affect their populations; however, due to its abundance we believe that this species probably needs not be classified above Least Concern category.

Etymology. The specific epithet is a noun in apposition and refers to the name of the Teko Amerindians who occupy the southern half of French Guiana; the area occupied by the Teko tribe also encompasses the type locality.


Amazophrynella siona sp. nov.
 Atelopus minutus: (Duellman & Lynch, 1969: 238, Sarayacu [Ecuador])
Dendrophryniscus minutus (Duellman, 1978: 120, Santa Cecilia [Ecuador])
Dendrophryniscus minutus (Duellman & Mendelson III 1995: 336, vicinities of San Jacilllo and Teniente Lopez [Peru])
Amazonela cf. minutus “western Amazonia” (Fouquet et al., 2012a: 829, “western Amazonia”, Ecuador [in part])
Amazophrynella cf. minutus “western Amazonia” (Fouquet et al., 2012a: 68, “western Amazonia”, Ecuador [in part])
Amazophrynella aff. minuta “western Amazonia” (Rojas et al., 2015: 84, “western Amazonia”, Ecuador [in part])
Amazophrynella aff. minuta (Rojas et al., 2016: 49, “western Amazonia”, Ecuador [in part])

Diagnosis. An Amazophrynella with (1) SVL 11.5–14.7 mm in males, 16.1–20.0 mm in females; (2) snout acute in lateral view; upper jaw, in lateral view, protruding beyond lower jaw; (3) texture of dorsal skin finely granular; (4) cranial crests, vocal slits and nuptial pads absent; (5) small granules from the outer edge of the mouth to upper arm; (6) ventral skin granular; (7) tiny granules on ventral surfaces; (8) fingers slender, basally webbed; (9) finger III relative short (HAL/SVL 0.20–0.21, n = 62); (10) finger I shorter than finger II; (11) palmar tubercle rounded; (12) hind limbs relatively large (TAL/SVL 0.5–0.52, n = 62); (13) toes lacking lateral fingers; in life: (14) venter reddish brown; yellow blotches on venter.

Distribution and natural history. Amazophrynella siona sp. nov. have been recorded from Ecuador, in Provinces of Orellana, Sucumbíos and Pastaza and Peru in the Province Andoas, northern Loreto Department. It occurs at elevations ranging from 200–900 m a.s.l. The species is found in the leaf litter of primary and secondary forest, terra firme or flooded forest, and swamps. It is active during the day; at night individuals rest on leaves, usually less than 50 cm above ground. It breeds throughout the year (Duellman, 1978). This species shows conspicuous sexual dimorphism, with males being much smaller than females. The amplexus is axillar. Eggs are pigmented; males call from amidst leaf litter. Duellman & Lynch (1969) reported that this species deposited its eggs in gelatinous strands 245–285 mm long, with 245–291 eggs. It can be abundant at some sites (e.g., Cuyabeno reserve; SR Ron, pers. obs., 2018) Given its large distribution range (>20,000 km2) which also includes vast protected areas and locally abundant populations, we suggest assignment this species to the Least Concern category.

Etymology. The specific epithet is a noun in apposition and refers to the Siona, a western Tucanoan indigenous group that inhabits the Colombian and Ecuadorian Amazon. The Siona inhabit the Cuyabeno Lakes region, an area where Amazophrynella siona sp. nov. is be abundant. While working in his undergraduate thesis in the early 1990s, SRR lived with the Siona at Cuyabeno. The Siona chief, Victoriano Criollo, had an encyclopedic knowledge of the natural history of the Amazonian forest, superior in extent and detail to that of experienced biologists. His death, a few years ago, represents one of many instances of irreplaceable loss of traditional knowledge triggered by cultural change among Amazonian Amerindians.

  (C–D) Amazophrynella teko sp. nov. photo by Antoine Fouquet; 
(E–F) A. siona sp. nov. photo by Santiago R. Ron;
(G–H)
 A. xinguensis sp. nov. photo by Emil Hernándes-Ruz; 
(U–V)
 A. moisesii sp. nov. photo by Paulo R. Melo-Sampaio.

Amazophrynella xinguensis sp. nov.

Diagnosis. An Amazophrynella with (1) SVL 17.0–20.0 mm in males, 22.4–26.3 mm in females; (2) snout pointed in lateral view; (3) upper jaw, in lateral view, protruding beyond lower jaw; 4) tympanums, vocal sac, parotid gland and cranial crest not evident; (5) texture of dorsal skin highly granular; (6) abundance of small tubercles on dorsum, on upper arm and on arms; (7) texture of ventral skin granular; (8) fingers I and II basally webbed; (9) finger III relative short (HAL/SVL = 0.20–0.22, n = 18); (10) thumb larger and robust; (11) finger I larger or equal than finger II, FI = 2.1 vs. FII = 2.1 in adult males, n = 5 and FI = 2.8 mm, vs. FII = 2.9 mm, in adult females, n = 13; (12) palmar tubercle ovoid; (13) toes slender, basally webbed; in life: (14) venter greyish; black dots on venter.

Distribution and natural history. Amazophrynella xinguensis sp. nov. have been recorded from State of Pará, Brazil, at three localities: PDS Virola Jatoba, municipality of Anapú, Fazenda Paraiso, municipality of Senador José Porfirio (right bank of Xingu River) and Ramal dos Cocos, municipality of Altamira (left bank of Xingu River), all of them in area of influence of the Belo Monte dam. It occurs in elevations of 86–106 m a.s.l. This species is found amidst leaf litter. The amplexus is axillar (Fig. 18C). Reproduction occurs in the rainy season in tiny puddles. Males were found hidden in the leaf litter. Tadpoles and advertisement call are unknown. The conservation status of this species remains unknown, but the recent construction of the Belo Monte hydroelectric complex on the Xingu River represents a threat to the population status of this species.

Etymology. The specific epithet refers to geographic distribution of the species within the lower Xingu River basin, Brazil.

Amazophrynella moisesii sp. nov.
Dendrophryniscus minutus (Bernarde et al. 2011: 120 plate 2, Fig. d)
Amazophrynella minuta (Bernarde et al. 2013: 224, 227 plate 7 Fig. c; Miranda et al. 2015: 96)

Diagnosis. An Amazophrynella with (1) SVL 12.2–15.8 mm in males, 16.4–20.9 mm in females; (2) snout acuminate in lateral view, upper jaw, in lateral view, protruding beyond lower jaw; (3) snout length protuberant, large for the genus (SL/HL = 0.48–0.5); (4) cranial crest, vocal slits and nuptial pads absent; (5) small tubercles on upper arms and posterior area of tympanums; (6) texture of dorsal skin tuberculate; (7) texture of ventral skin highly granular (8) finger III relative large (HAL/SVL 0.23–0.25, n = 28); (9) fingers slender, basally webbed; (10) finger I shorter than finger II; (11) palmar tubercle elliptic; (12) hind limbs relatively large (TAL/SVL 0.51–0.53, n = 28); (13) toes slender basally webbed; in life: (14) venter pale yellow; small irregular dots on venter.

Distribution and natural history. Amazophrynella moisesii sp. nov. have been recorded from Brasil. State of Acre: municipalities of Cruzeiro do Sul, Mâncio Lima, Porto Walter and Tarauacá; State of Amazonas: municipality of Envira. Peru: Department of Huanuco, Panguana, Rio Llullapichis. Due to its abundance and presence in conservation units of Brazil (Floresta Estadual do Gregório, Reserva Extrativista do Alto Juruá and Parque Nacional da Serra do Divisor) we recommend the IUCN Least Concern category.

Etymology. The specific epithet refers to Dr. Moisés Barbosa de Souza, a Brazilian biologist, professor and friend at the Universidade Federal do Acre (UFAC), to whom we dedicate this species in recognition of his contributions to herpetological research and amphibian conservation in the state of Acre, Brazil.



Figure 25: Confirmed candidate species (CCS) of Amazophrynella. (A–B) Amazophrynella minuta photo by Rommel R. Rojas; (C–D) Ateko sp. nov. photo by Antoine Fouquet; (E–F) A. siona sp. nov. photo by Santiago R. Ron; (G–H) A. xinguensis sp. nov. photo by Emil Hernándes-Ruz; (I–J) A. bokermanni photo by Marcelo Gordo; (K–L) A. manaos photo by Rommel R. Rojas. (M–N) A. amazonicola photo by Rommel R. Rojas. (O–P) A. matses photo by Rommel R. Rojas; (Q–R) A. javierbustamantei photo by Juan Carlos Chapparro; (S–T) A. vote photo by Robson W. Ávila; (U–V) A. moisesii sp. nov. photo by Paulo R. Melo-Sampaio.

Rommel R. Rojas, Antoine Fouquet, Santiago R. Ron, José Hernández-Ruz, Paulo R. Melo-Sampaio, Juan C. Chaparro, Richard C. Vogt, Vinicius Tadeu de Carvalho, Leandra Cardoso Pinheiro, Robson W. Avila, Izeni Pires Farias, Marcelo Gordo and Tomas Hrbek​. 2018. A Pan-Amazonian Species Delimitation: High Species Diversity within the Genus Amazophrynella (Anura: Bufonidae). PeerJ. 6:e4941  DOI: 10.7717/peerj.4941