Thursday, August 4, 2022

[Herpetology • 2022] Allobates kamilae • A New Nurse Frog of the Allobates tapajos Species Complex (Anura: Aromobatidae) from the upper Madeira River, Brazilian Amazonia


Allobates kamilae 
Ferrão​, Hanken & Lima, 2022
 

Abstract 
Cryptic diversity is extremely common in widespread Amazonian anurans, but especially in nurse frogs of the genus Allobates. There is an urgent need to formally describe the many distinct but unnamed species, both to enable studies of their basic biology but especially to facilitate conservation of threatened environments in which many are found. Here, we describe through integrative taxonomy a new species of the Allobates tapajos species complex from the upper Madeira River, southwestern Amazonia. Species delimitation analyses based on molecular data are congruent and delimit five candidate species in addition to A. tapajos sensu stricto. The new species is recovered as sister to A. tapajos clade F, a candidate species from Teles-Pires River, southeastern Amazonia. The new species differs from nominal congeners in adult and larval morphology and in male advertisement call. Egg deposition sites differ between east and west banks of the upper Madeira River, but there is no evidence of corresponding morphologic or bioacoustic differentiation. The new species appears to be restricted to riparian forests; its known geographic range falls entirely within the influence zone of reservoirs of two large dams, which underscores the urgent need of a conservation assessment through long-term monitoring. This region harbors the richest assemblage of Allobates reported for Brazilian Amazonia, with six nominal species and four additional candidate species awaiting formal description.

Color in life of adult Allobates kamilae sp. nov.
(A, B) Female from the Abunã Direito sampling module, INPAH 42958, SVL = 16.1 mm.
 (C, D) Male from the Abunã Direito sampling module, INPAH 42932, SVL = 15.8 mm.
 (E, F) Male from the Abunã Esquerdo sampling module, INPAH 42881, SVL = 16.4 mm.

 Live tadpoles (lot INPAH 42851) of Allobates kamilae sp. nov., Gosner stages 39–40,
from the Jirau Direito sampling module.

Allobates kamilae sp. nov. 

Allobates sp. 1: Dias-Terceiro et al. (2015), Dayrell et al. (2021).
Allobates tapajos “Allobates_63”: Vacher et al. (2020), SupInfo 4.
Allobates aff. tapajos: Moraes & Lima (2021), Silva et al. (2022).
Allobates aff. tapajos “3”: Réjaud et al. (2020), Fig. 1 and Figs. S1–S3.

Generic placement: The new species is assigned unambiguously to the genus Allobates because the tip of finger IV does not reach the distal subarticular tubercle of finger III, toe IV with basal webbing and lateral fringe on its preaxial side, pale paracloacal marks (characters 5, 43 and 50 of Grant et al., 2017), respectively) and its phylogenetic relationship as assessed by molecular data.

Diagnosis: A small-bodied species of Allobates characterized by the following combination of characters: SVL 14.5–17.4 mm in males (n = 49) and 15.2–17.8 mm in females (n = 26); finger III not swollen in males; one subarticular tubercle on finger IV; basal webbing between toes II and III absent; EN/WFD = 2.67–3.67 in females; WFD/WTD = 0.67–1.00 and HANDIV/WFD = 3.58–5.60 in males; dorsal surface of thigh lacks red or yellow marks; pale dorsolateral stripe absent in preservative; white ventrolateral stripe absent in life; belly without dark and white marbling; throat in males bright yellow with scattered melanophores; throat in females with scattered melanophores; dorsal surface of fingers brown to orange-brown; advertisement calls predominantly arranged in groups of 2–5 unpulsed notes; first (135 ms ± 24) and last (142 ms ± 31) inter-note intervals are of similar duration and longer than note duration; dominant frequency 5,211–6,201 Hz; tadpoles have an oral disc and spiracle; five short papillae on each side of the lateral margin of the anterior labium; long papillae on the posterior labium; a “V”-shaped lower jaw sheath; and labial tooth rows P-3 and P-1 of similar length.

Etymology: The specific epithet kamilae honors Kamila Xavier Amaral, a very young and enthusiastic biologist who passed away prematurely after battling cancer. While an undergraduate student, Kamila was being trained in Allobates taxonomy by A. P. Lima. She was the first person to study the new species described in this study.


Allobates kamilae sp. nov. mating in the Abunã Esquerdo sampling module.
(A) Female climbing over a previously deposited clutch to approach the male. (B) Male approaching the female to embrace her in a lateral cephalic amplexus (C). (D) Female depositing eggs. (E) Female moments before she left the egg deposition site. (F) The freshly deposited clutch has merged with a previously deposited clutch one day after deposition. Male (♂), INPAH 42944, SVL 16.9 mm; female (♀), uncollected. Numbers denote the temporal sequence of clutch deposition from newest (1) to oldest (3).

Conclusions: 
The Allobates tapajos species complex comprises six species distributed in southwestern, southeastern, eastern and northeastern Amazonia. Yet, sampling remote and poorly explored areas will likely reveal additional candidate species (e.g., Silva et al., 2022). Although A. kamilae resembles A. tapajos sensu stricto in morphology, these species nevertheless are easily diagnosed. Acoustic differentiation between these species, however, is achieved mainly through detailed comparisons of temporal traits within the same call arrangement. Recognition of additional candidate species in the A. tapajos species complex—as well as other species complexes in the genus—will likely require such fine-scale analyses. Allobates kamilae is known only from riparian forests in the impact zone of two large dams in the upper Madeira River, underscoring the urgent need for comprehensive assessments of its geographic distribution and conservation status.


Miquéias Ferrão​, James Hanken and Albertina P. Lima. 2022. A New Nurse Frog of the Allobates tapajos Species Complex (Anura: Aromobatidae) from the upper Madeira River, Brazilian Amazonia. PeerJ. 10:e13751 DOI: 10.7717/peerj.13751