Adenomera gridipappi, Carvalho & Moraes & Lima & Fouquet & Peloso & Pavan & Drummond & Rodrigues & Giaretta & Gordo & Neckel-Oliveira & Haddad, 2021

Carvalho, Thiago R. D., Moraes, Leandro J. C. L., Lima, Albertina P., Fouquet, Antoine, Peloso, Pedro L. V., Pavan, Dante, Drummond, Leandro O., Rodrigues, Miguel T., Giaretta, Ariovaldo A., Gordo, Marcelo, Neckel-Oliveira, Selvino & Haddad, Célio F. B., 2021, Systematics and historical biogeography of Neotropical foam-nesting frogs of the Adenomera heyeri clade (Leptodactylidae), with the description of six new Amazonian species, Zoological Journal of the Linnean Society 191, pp. 395-433 : 424-426

ADENOMERA GRIDIPAPPI , SP. NOV.

GRIDI- PAPP’ S TERRESTRIAL NEST- BUILDING FROG

( FIGS 2A, 3–4, 5J, 6J, 7J, 10E–F, 12E–F;

TABLES 1-3)

lsid urn:lsid:zoobank.org:act:0F9B3F8A-DE7D-4680-9F72-315A74C93F64

Holotype: INPA-H 40512 (field # APL 19992), adult male, BRAZIL, Rondônia, Porto Velho , 9.414418°S, 64.429558°W, 121 m, 9-xi-2013, A.P. Lima (Collector).

Paratypes: INPA-H 40511 , 40513–40514 (field # APL 19984, 19993 , 21136 , respectively) , CFBH 44470– 44472 (field # APL 21175, 21797 , 21799 , respectively), adult males, collected at the type locality between 2013–2016, A.P. Lima (Collector) .

Referred specimens: Genetic vouchers assigned to the clade G3 of the lineage Adenomera sp. G of Fouquet et al. (2014) from the north-west portion of the Brazilian state of Mato Grosso (PMJ08, PMJ154, #968179).

Additional material: MZUSP 80593 , 80595–96 , 87830 (adult males), and MZUSP 80592 , 80594 (adult females): BRAZIL, Mato Grosso, Aripuanã , MZUSP 151906 (adult female): BRAZIL, Mato Grosso, Juína .

Etymology: The specific epithet is a patronymic name for Marcos Gridi-Papp for his invaluable research efforts to advance the knowledge on the anuran vocal system from a functional evolutionary perspective. The honoured scientist trained the leading author of this study in acoustics and vocal anatomy during his Ph.D. program and as part of his current project dedicated to understanding the diversity and patterns of evolution of the acoustic mating signals in leptodactylid frogs. The acoustic characterization of Adenomera frogs has been instrumental to elucidate the species diversity of the genus.

Diagnosis: A. gridipappi is characterized by the following combination of character states: (1) large size (adult male SVL = 25.4–27.7 mm); (2) robust body shape; (3) toe tips fully expanded into small discs (character state D); (4) distal antebrachial tubercle on underside of forearm; (5) belly immaculate; (6) two possible chromotypes (presence/absence) of dorsolateral stripe; (7) multi-note advertisement call composed of two- to four-note calls; (8) call notes formed by 2–4 partly fused pulses; (9) note duration varying from 50–75 ms; (10) note dominant frequency coinciding with the second harmonic (3553–4027 Hz); and (11) fundamental frequency ranging from 1820–1970 Hz.

Comparisons with congeners: A. gridipappi (SVL = 25.4–27.7 mm; Table 2) has adult males larger than those of A. ajurauna , A. amicorum , A. araucaria , A. aurantiaca , A. engelsi , A. inopinata , A. kayapo , A. kweti , A. nana and A. phonotriccus [combined SVL 15.4–24.0 mm ( Kwet, 2007; Berneck et al., 2008; Kwet et al., 2009; Carvalho et al., 2019b, c)]. A. gridipappi has a robust body shape ( Fig. 12E– F), whereas A. diptyx , A. martinezi and A. saci have a slender body. A. gridipappi has toe tips that are fully expanded into small discs (character state D), differing from congeners with unexpanded, slightly or moderately expanded toe tips (character states A–C) as in A. bokermanni , A. coca , A. diptyx , A. hylaedactyla , A. martinezi , A. saci and A. thomei . A. gridipappi is distinguished from congeners (except A. amicorum , A. aurantiaca , A. cotuba , A. inopinata , A. kayapo , A. lutzi , A. phonotriccus and A. tapajonica ) by having an antebrachial tubercle on underside of forearm. A. gridipappi differs from A. araucaria , A. bokermanni , A. heyeri , A. kweti , A. lutzi and A. nana by having belly cream-coloured ( Fig. 10F), this is yellow or sometimes has yellowish tints in the other species. A. gridipappi is larger than its nearest relative A. tapajonica ( Table 2) and can have a dorsolateral stripe (never present in A. tapajonica ); however, they are more easily distinguished by their calls.

A. gridipappi can be distinguished from all congeners, either with multi-note and single-note calls ( Table 3), by its unique calling emission pattern: multi-note calls are made up of two- to four-note calls ( Fig. 5J)—multi-note calls of all other Adenomera species are composed of individual notes ( Fig. 5). The other five Adenomera species with multi-note calls are A. amicorum ( Fig. 5E), A. aurantiaca ( Fig. 5G), A. cotuba ( Fig. 5B), A. inopinata ( Fig. 5H) and A. simonstuarti (T.R. de Carvalho, pers. obs.). A. gridipappi is also distinguished from A. aurantiaca ( Figs 6G, 7G) and A. inopinata ( Figs 6H, 7H), which have call notes formed by complete pulses, by having call notes formed by partly fused pulses ( Figs 6J, 7J). A. gridipappi is distinguished from A. amicorum and A. cotuba by the shorter note duration and/or fewer pulses per note ( Table 3). A. gridipappi can only be acoustically distinguished from A. simonstuarti by its unique emission pattern of multi-note calls composed of two- to four-note calls (multi-note calls of A. simonstuarti are composed of individual notes; T.R. de Carvalho, pers. obs.).

Description of holotype ( Fig. 12E–F): Body robust. Snout subovoid to rounded in dorsal view, acuminate in lateral view. Nostril closer to the snout tip than to the eye, fleshy ridge on snout tip, canthus rostralis not marked, loreal region slightly concave, supratympanic fold from the posterior corner of the eye to the base of the arm, postcommissural gland ovoid, vocal sac subgular with a fold from jaw extending to forearm, vocal slit present, vomerine teeth in two straight rows medial and posterior to choanae and oblique to sagittal plane. Tongue elongated, free from the posterior half. Relative finger lengths IV <I <II <III, fingers without ridges or fringes, finger tips rounded, slightly expanded, especially in fingers I and V, inner metacarpal tubercle ovoid, outer metacarpal tubercle nearly rounded. Subarticular tubercles nearly rounded to subconical, supernumerary tubercles rounded. Antebrachial tubercle on underside of forearm rounded, single. Dorsum glandular, flank warty. Dorsal surface of shank and posterior surface of tarsus with whitetipped tubercles. Ventral surface of body and limb mostly smooth, underside of thigh areolate/granular. Posterior surface of thigh with ovoid paracloacal gland. Relative toe lengths I <II <V <III <IV, lateral fringing and webbing absent, tips of toes II–IV fully expanded (character state D), tip of toe I unexpanded, tip of toe V slightly expanded. Inner and outer metatarsal tubercles ovoid. Tarsal fold extending 2/3 of tarsus length, from the inner metatarsal tubercle towards the heel. Subarticular tubercles nearly rounded, supernumerary tubercles nearly rounded. Measurements (in mm): SVL 26.7, HL 8.1, HW 9.7, ED 1.9, TD 1.5, EN 1.9, IND 2.4, HAL 5.6, TL 12.4, THL 11.6, FL 12.9.

Snout tip with a faded white coloration (coincident with the fleshy ridge). Blotches on the upper lip offwhite. Postcommissural gland pale yellow. Tympanum light brown. Dorsum freckled brown, lighter on limbs. Interorbital bar dark brown, outlined by a light greyish brown line, dark brown blotches and stains on dorsum, blackish brown spot coinciding with the lumbar gland. Transverse bars and blotches on limbs dark brown. Flank finely light-brown mottled on a light grey background. Posterior surface of thigh finely mottled in shades of brown and yellow. Mid-dorsal longitudinal line and dorsolateral stripe absent. Posterior surface of thigh cream-coloured and covered with brown spots and dots. Paracloacal gland pale yellow. Ventral surface of belly and limbs partially translucent, cream-coloured. Throat browndotted, more densely coloured laterally, chest and belly immaculate. Underside of forearm (outer margin) brown-speckled, ventral surface of hand, foot and digits mostly brown interspersed with lighter sections, subarticular tubercles partly pigmented, light grey, and tips of fingers and toes non-pigmented.

Variation in type specimens: Dorsal coloration varies from light brown to dark solid blackish brown. Dorsolateral stripe (light grey) present in CFBH 44470. Mid-dorsal longitudinal stripe, restricted to pelvic region, present in CFBH 44470-71. Shape and size of antebrachial tubercles are variable among type specimens, sometimes low and flattened (hardly detected even under magnification). Variation in toe tip development of toes II–IV varies from modestly expanded to fully expanded (character states C and D, respectively). The holotype was not photographed in life, but colours in life of a paratype are shown in Fig. 10E–F.

Advertisement call: Description based on calls of four males (N = 73 notes and 250 pulses quantified; Table 3). The call ( Figs 5J, 6J, 7J) consists of pulsed notes grouped into two levels of temporal organization: two-note (c. 75% of calls), three-note (c. 25%) and fournote (a single case) calls that are given in bouts (4–8, 5 ± 1 calls per bout; N = 13). The only exception was the emission of single-note calls at the beginning of a call bout (= multi-note call) given by one male. Multinote calls are composed of 9–16 (12 ± 3; N = 13) notes given at a rate of 2–3 (3 ± 1; N = 4) per second. Notes are formed by 2–4 (3 ± 1) partly fused pulses given at a rate of 35–98 (68 ± 11) per second and varying in duration from 8–40 (21 ± 4) ms. Note duration varies from 50–75 (64 ± 8) ms and note rise time from 7–74 (42 ± 4)% of note duration. The note frequencies are harmonically structured and the dominant frequency coincides with the second harmonic (3553–4027, 3856 ± 105 Hz). The note fundamental frequency ranges from 1820–1970 (1887 ± 13) Hz. Frequency modulation is upward, when present, ranging from 0–732 (342 ± 52) Hz.

Habitat and natural history: Males were heard calling hidden under the leaf litter of an old-growth nonflooded forest during the daytime at the onset of rainy season (November and December). No individual was recorded in calling activity in the rainy season later than early January. A. andreae and A. hylaedactyla are sympatric congeners with A. gridipappi at the type locality.

Distribution: A. gridipappi is distributed in the interfluvial region delimited by the upper Madeira and Aripuanã rivers, in southern Brazilian Amazonia ( Fig. 2A).

Remarks: Genetic vouchers associated with lineage sp. G from the lower Madeira and Tapajós rivers still require acoustic data for a precise taxonomic assessment. Specimens from Borba [genetic vouchers MTR 12832 (MZUSP 158074) and MTR 12900 (without an associated museum number)] formed a clade with the type series of A. gridipappi ; however, we do not have associated calls that could confirm that they are conspecific to each other. Besides, these populations are separated geographically by almost 800 km and genetic divergence in COI coincides with the 5% threshold of interspecific variation defined in our species delimitation analysis ( Table 1). Until additional data are obtained, we provisionally assign both genetic vouchers from Borba to A. cf. gridipappi . All four genetic vouchers from Nova Olinda do Norte [MTR 12711 (MZUSP 158073) and MTR 13034, 13067, SMS 639 (without associated museum numbers)] form a clade sister of A. gridipappi + A. tapajonica with full support in our analyses ( Fig. 3; Supporting Information, Fig. S2). These two new sister species are categorically distinguished from each other based on their calls, whereas minor differences in morphology and coloration did not help much to their discrimination. We only had access to one genetic voucher of the ‘Nova Olinda do Norte lineage’, an adult female that shares phenotypic traits with both A. gridipappi and A. tapajonica , and calls from this lineage remain unknown. Therefore, we refrain from naming the Nova Olinda do Norte lineage as a new species while acoustic data can be acquired. For that reason, we provisionally assign it to Adenomera sp. of the A. heyeri clade. It is noteworthy that one of the genetic vouchers of Adenomera sp. and one of A. cf. gridipappi were collected from opposite margins of the Abacaxis River, and the collection points are separated one from the other by less than 5 km. Based on the interfluve-associated species distributions in the A. heyeri clade, this could be a piece of evidence pointing to the existence of two unnamed species on opposite river banks ( A. cf. gridipappi and Adenomera sp. ) associated with the Abacaxis River, a tributary of the Amazon River in the Madeira-Tapajós interfluve. If true, this would be a case similar to that of the nearest relatives and assumedly allopatric A. aurantiaca and A. inopinata , distributed on opposite banks of another smaller river (Jamanxim River) in the Amazon Basin ( Fig. 2B).