Adenomera kayapo, 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 : 411-413

ADENOMERA KAYAPO , SP. NOV.

KAYAPÓ TERRESTRIAL NEST- BUILDING FROG

( FIGS 2B, 3–4, 5D, 6D, 7D, 9A–B, 11A–B;

TABLES 1-3)

lsid urn:lsid:zoobank.org:act:98FCDF08-BD14-46BF-BC3A-0C609EE9887B

Holotype: CFBH 43885 (formerly AAG-UFU 6243; field # TRC 124 ), adult male, BRAZIL, Pará , Palestina do Pará, 5.701950°S, 48.235240°W, 121 m, 8-i-2018, T. R. de Carvalho, A.A. Giaretta and P. Marinho (Collectors).

Paratypes: CFBH 43886 (formerly AAG-UFU 6244; field # TRC 125 ) and AAG-UFU 6245‒6246 (field # TRC 126‒127 , respectively), adult males; all with the same collection data as the holotype . MPEG 41619 (field # LOD 1042 ), adult male, BRAZIL, Pará, Parauapebas, Floresta Nacional ( FLONA) de Carajás , 6.076241°S, 50.074451°W, 661 m, 19-i-2018, L.O. Drummond and F.M. Borges (Collectors) . MPEG 41620 (field # LOD 1428 ), adult female, BRAZIL, Pará, Parauapebas , FLONA de Carajás, 6.049913°S, 50.265324°W, 701 m, 23-i-2018, L.O. Drummond and F.M. Borges (Collectors) . MPEG 41692 (field # LOD 799 ), adult male, BRAZIL, Pará, São Félix do Xingu, Serra do Jaguar , Bacia Carapanãzinho , 6.480099°S, 51.249726°W, 236 m, 29-x-2011, L.O. Drummond (Collector) . MPEG 41694 (field # LOD 828 ), adult male, BRAZIL, Pará, São Félix do Xingu, Serra do Jaguar , Bacia Carapanãzinho , 6.456122°S, 51.197732°W, 255 m, 3-xi-2011, L.O. Drummond (Collector) . INPA-H 40523‒40524 , 40526 (field # APL 22299‒300 , 22302 , respectively), adult males, and INPA-H 40525 (field # APL 22301), adult female, BRAZIL, Tocantins, Araguaína , 7.103700°S, 48.197800°W, 227 m, 18-xi- 2018, A.P. Lima (Collector) .

Referred specimens: Adenomera sp. F , in part ( Fouquet et al., 2014: specimens assigned to the lineage F 1 in appendices S1a, S3a): MCP 11384 (genetic voucher TG3259), subadult specimen, BRAZIL, Pará, FLONA dos Carajás; MZUSP 140174 (genetic voucher T314),

adult male, BRAZIL, Pará, Reserva Biológica (REBIO) Tapirapé.

Additional material: MZUSP 92765, 92784 (adult males) and MZUSP 92774, 92778 (adult females): BRAZIL, Mato Grosso, Vila Rica; MZUSP 140172– 73 (adult males; genetic vouchers T220 and T265, respectively): BRAZIL, Pará, REBIO Tapirapé.

Etymology: The name kayapo is given as homage to the Kayapó people (sometimes also spelled as Caiapó). The Kayapó is a large group of Jê speaking people living in the south-eastern portion of Brazilian Amazonia. It is thought that the Kayapó, who name themselves mebêngôkre, once inhabited a vast region between the Araguaia and Tocantins rivers, but were pushed westward by the early colonizers in the 19 th century ( Turner, 1998). The Kayapó are known to be fierce protectors of their rights and lands.

Diagnosis: A. kayapo is characterized by the following combination of character states: (1) small size (adult male SVL = 17.5–21.0 mm); (2) robust body shape; (3) toe tips unexpanded or slightly expanded (character states B–C); (4) distal antebrachial tubercle on underside of forearm; (5) two possible chromotypes (presence/absence) of dorsolateral stripe; (6) singlenote advertisement call; (7) call note formed by 12–16 partly fused pulses; (8) note duration varying from 116–156 ms; and (9) note dominant frequency coinciding either with the fundamental harmonic (2304 Hz; N = 1 male) or the second harmonic (4570– 4992 Hz; N = 3 males).

Comparisons with congeners: A. kayapo has adult males (SVL = 17.5–21.0 mm; Table 2) that are smaller than those (if not otherwise stated, specimens measured are listed in Supporting Information, Appendix S1) of A. bokermanni (21.3–22.8 mm), A. coca [23.6–25.6 mm ( Angulo & Reichle, 2008)], A. heyeri [22.5–25.8 mm ( Boistel et al., 2006)], A. hylaedactyla (21.5–26.5 mm), A. lutzi [25.7–33.5 mm ( Kok et al., 2007)], A. martinezi [21.9–24.2 mm ( Carvalho & Giaretta, 2013b)] and A. simonstuarti [25.9–26.2 mm ( Angulo & Icochea, 2010)]. A. kayapo has a robust body shape ( Fig. 11A– B), whereas A. diptyx , A. martinezi and A. saci have a slender body ( Carvalho & Giaretta, 2013b). A. kayapo has unexpanded or slightly expanded toe tips (character states B–C), differing from congeners having toe tips fully expanded into small discs, character state D ( A. ajurauna , A. andreae , A. chicomendesi , A. heyeri , A. marmorata , A. lutzi , A. nana and A. simonstuarti ). A. kayapo is distinguished from all congeners (except A. cotuba , A. lutzi , and A. phonotriccus ) by having an antebrachial tubercle on underside of forearm. A. kayapo differs from A. cotuba , which does not have a dorsolateral stripe, by the occurrence of two possible chromotypes (presence/absence) of the stripe. A. kayapo and the closest related A. phonotriccus are morphologically cryptic species with sympatric distribution (syntopic occurrence at their type locality; Fig. 2B). In contrast, these sister species markedly differ in their advertisement calls.

The advertisement call of A. kayapo ( Figs 5D, 6D, 7D; Table 3) consists of single notes formed by partly fused pulses. These acoustic characteristics distinguish the new species from the two congeners with multi-note calls, A. cotuba ( Fig. 5B) and A. simonstuarti (T.R. de Carvalho, pers. obs.), and from eight congeners with non-pulsed calls ( Table 3). From congeners also having single-note, pulsed calls, A. kayapo is distinguished from A. andreae , A. coca , A. diptyx , A. heyeri , A. hylaedactyla and A. martinezi by a longer note duration and/or higher fundamental frequency ( Table 3). The call of A. kayapo is formed by partly fused pulses ( Figs 6D, 7D), whereas that of A. phonotriccus is formed by complete pulses ( Figs 6F, 7F). The call of A. kayapo most closely resembles those of A. juikitam ( Figs 5C, 6C, 7C), A. araucaria and A. thomei ( Almeida & Angulo, 2006; Carvalho et al., 2019b). The calls of the four species cannot be distinguished from each other in any of the call traits analysed ( Table 3). Both Atlantic Forest species ( A. araucaria and A. thomei ) are distantly related and allopatric in relation to the Amazonian A. kayapo (Supporting Information, Fig. S1). In contrast, A. juikitam and A. kayapo have sympatric populations in the Cerrado-Amazonia ecotone ( Figs 1B, 2B), but they occupy distinct habitats (preferentially open formations and forests, respectively). Even so, A. kayapo differs from the other three species by the presence of antebrachial tubercles (see morphological comparisons in the previous paragraph).

Description of holotype ( Fig. 11A–B): Body robust. Snout subovoid 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, unexpanded; inner metacarpal tubercle ovoid; outer metacarpal tubercle rounded. Subarticular tubercles nearly rounded; supernumerary tubercles rounded. Antebrachial tubercles on underside of forearm rounded. Anterior dorsum and forelimbs smooth; posterior dorsum and flank warty; tubercles on posterior dorsum, dorsal surface of hindlimb, and posterior surface of tarsus. Dorsolateral fold absent. Paracloacal gland poorly defined. Ventral surface of body and limbs mostly smooth; underside of thigh granular. Relative toe lengths I <II <V <III <IV; lateral fringing and webbing absent; tips of toes II–III slightly expanded (character states B–C), tip of toe I unexpanded, tips of toes IV–V desiccated. Inner metatarsal tubercle nearly rounded, outer metatarsal tubercle ovoid, inner tubercle twice in maximum diameter than outer tubercle. Tarsal fold extending 2/3 of tarsus length, from the inner metatarsal tubercle towards the heel. Subarticular and supernumerary tubercles nearly rounded or subconical. Measurements (in mm): SVL 17.6, HL 5.6, HW 6.6, ED 1.6, TD 1.3, EN 1.1, IND 1.5, HAL 3.7, TL 7.7, THL 7.3, FL 6.9.

Snout tip with a faded white coloration (coincident with the fleshy ridge). Dots and flecks on the upper lip off-white. Postcommissural gland off-white medially and surrounded by dark brown coloration. Tympanum light brown. Dorsal surfaces mostly dark brown intermingled with lighter shades of brown. Flecks on dorsal surface of forelimb and foot off-white, hand partially off-white. Mid-dorsal longitudinal stripe and dorsolateral stripe absent. Flank mottled. Posterior surface of thigh finely mottled in shades of brown and yellow. Ventral surface of belly and thigh partially translucent, light cream. Blotches on lower jaw offwhite. Throat and anterior chest finely dark-mottled, especially following the lateral expansion of the vocal sac. Belly brown-dotted, more densely coloured laterally. Underside of forearm dark brown. Ventral surface of hand, foot and digits brown, subarticular and supernumerary tubercles and tips of fingers and toes cream-coloured. Thigh brown-dotted.

Colour of holotype in life ( Fig. 9A–B): Dorsum nearly solid dark brown intermingled with lighter shades of brown. Base of arm, postcommissural gland and glands on dorsum and flank in varying shades of orange. Snout tip with a faded white coloration. Flecks on upper and lower lips light grey, extending posteriorly to the base of arm. Mid-dorsal longitudinal stripe absent, even though there is an indication as a row of orange-coloured spots arranged longitudinally. Iris deep copper. Tympanum greyish brown. Ventral surfaces mottled dark brown and off-white varying in colour prevalence. Throat finely brown-mottled; belly sparsely brown-dotted medially on a white and cream background, white and brown mottled laterally. Groin with yellow tints. Ventral surface of forelimb and hindlimb partially translucent, violet.

Variation in type specimens: Snout shape in dorsal view subovoid tending to subelliptical ( MPEG 41692 ) or rounded ( MPEG 41619 ). In the female ( MPEG 41620 ), nearly rounded from above, rounded in profile; snout tip lacks a fleshy ridge or a faded white coloration; postcommissural gland nearly rounded and canthus rostralis rounded; more evident than in male specimens. MPEG 41620 and 41694 have a single, rounded antebrachial tubercle on underside (distal edge) of forearm (at least two tubercles in other specimens). In life, ventral coloration of specimens from São Félix do Xingu (photographs not directly associated with preserved specimens) vary from white-and-grey mottled to bright yellow, especially in one female. In preserved specimens, dorsolateral stripe and mid-dorsal longitudinal stripe, pale brown or grey, in CFBH 43886 , MPEG 41620 and MPEG 41692 . Indication of mid-dorsal longitudinal stripe in AAG-UFU 6245–6246 and MPEG 41619 . Paratypes have the dorsal surface of limbs dark brown crossbanded on a lighter brown background colour. Paracloacal gland absent in MPEG 41620 and 41694, well developed in MPEG 41619 , yellowish cream bordered by dark coloration of posterior surface of thigh. AAG-UFU 6245 and MPEG 41619 have lighter belly coloration, with brown dots sparsely distributed, rather than the speckled pattern (densely distributed laterally) .

Advertisement call: Description based on calls of four males (N = 50 notes and 712 pulses quantified; Table 3). The call ( Figs 5D, 6D, 7D) consists of a single-note, pulsed signal given at a low rate of 23–33 (28 ± 4; N = 4) notes per minute. Notes are formed by 12–16 (14 ± 1.0) partly fused pulses given at a rate of 89–131 (108 ± 16) per second and varying in duration from 3–25 (10 ± 1) ms. Note duration varies from 116–156 (139 ± 15) ms and note rise time from 37–74 (54 ± 8)% of note duration. The note frequencies are harmonically structured and the dominant frequency may coincide either with the fundamental harmonic (2304 Hz; N = 1 male) or the second harmonic (4570–4992, 4789 ± 137 Hz; N = 3 males). Frequency modulation, when present, is upward, ranging from 0–938 (553 ± 162) Hz.

Habitat and natural history: A. kayapo is usually associated with non-flooded forest habitats (terra firme forests) in eastern Brazilian Amazonia, although calling males have also been heard at the egde of forest clearings. Males call exposed or under the leaf litter and have calling activity concentrated during the daytime, especially in late afternoon. A. kayapo is sympatric with two other species of Adenomera at its type locality: A. phonotriccus is partly syntopic with A. kayapo at the type locality ( Palestina do Pará), although they have been heard, in almost all cases, in two distinct forest fragments split by a strip of pasture land; A. hylaedactyla , different from A. kayapo and A. phonotriccus , occupies open areas (e.g. pastures and open vegetational types alongside with dirt roads). A. andreae has never been sampled at the type locality of A. kayapo , but they are syntopic species at Serra do Jaguar (São Félix do Xingu).

Distribution: The occurrence of A. kayapo is associated with the Xingu-Tocantins interfluve, comprising the type locality and some other localities on the west bank of the middle-lower Araguaia River in eastern Pará and north-eastern Mato Grosso, and single localities on the opposite bank of the river in northern Tocantins and on the east bank of the lower Xingu River ( Fig. 2B). Given that the closely related A. kayapo and A. phonotriccus are morphologically cryptic species, we based their distribution ranges on acoustic and molecular data; A. kayapo is more widely distributed in the interfluvial region, whereas A. phonotriccus is restricted to two nearby localities on the west bank of the lower Araguaia River in eastern Pará ( Carvalho et al., 2019c).

Remarks: We had access to calls of one individual from Altamira (FNJV 11208) that are similar to the call of A. kayapo . However, there is a issue related to the municipal limits of Altamira, which encompass both margins of the Xingu River. Due to the lack of a specific location or coordinates, it is impossible to ascertain whether A. kayapo was recorded within the Xingu-Tocantins interfluve or on its opposite margin, on the west bank of the Xingu River. A field expedition to the lower Xingu River should focus on a systematic sampling on both west and east banks of the river in order to confirm the westernmost distribution range of A. kayapo and the potential occurrence of other species of the A. heyeri clade.