Adenomera albarena, Martins & Tamanini Mônico & Mendonça & Dantas & Souza & Hanken & Lima & Ferrão, 2024

Martins, Bryan da Cunha, Tamanini Monico, Alexander, Mendonca, Cianir, Dantas, Silionama P., Souza, Jesus R. D., Hanken, James, Lima, Albertina Pimentel & Ferrao, Miqueias, 2024, A new species of terrestrial foam-nesting frog of the Adenomera simonstuarti complex (Anura, Leptodactylidae) from white-sand forests of central Amazonia, Brazil, Zoosystematics and Evolution 100 (1), pp. 233-253 : 233

Adenomera albarena sp. nov.

, Figs 4 , 5 , 6 , 7 , 9B-D

Chresonymy.

Adenomera gr. heyeri (Lima et al. 2021).

Type material.

Holotype. INPA-H 44867, an adult male collected at km 26 of the AM-352 highway, Rio Negro Sustainable Development Reserve (03°05'35"S, 60°40'36"W; 76 m a.s.l.), Municipality of Iranduba, State of Amazonas, Brazil, on 11 December 2020 by M. Ferrão, A. P. Lima and W. E. Magnusson.

Paratypes. Twenty-four adults collected at the same locality as the holotype; eight males MPEG 44649, INPA-H 44868-73 and ZUEC-AMP 25694 collected on 11 December 2020 by M. Ferrão, A. P. Lima and W. E. Magnusson; four females INPA-H 44874-75, ZUEC-AMP 25695 and MPEG 44650 collected on 10 December 2021 by M. Ferrão, A. P. Lima and B. Martins; four males INPA-H 44876-77 and MPEG 44651-52 collected on 11 December 2021 by M. Ferrão, A. P. Lima and B. Martins; four males INPA-H 44878-80 and ZUEC-AMP 25696 collected on 12 December 2021 by M. Ferrão, A. P. Lima and B. Martins; a male INPA-H 44881 collected on 19 January 2022 by B. Martins; a male INPA-H 44882 collected on 3 February 2022 by B. Martins; a male ZUEC-AMP 25697 and a female INPA-H 44883 collected on 14 May 2022 by B. Martins. One adult male INPA-H 44885, collected at km 50 of the AM-352 Highway, Rio Negro Sustainable Development Reserve (2°50'10.0"S, 60°50'20.0"W), Municipality of Iranduba, State of Amazonas, Brazil, on 12 January 2023 by B. Martins.

Etymology.

The specific epithet albarena is formed by the combination of two Latin words: “alba” (white) and “arena” (sand). This is a reference to the white-sand forests of central Amazonia, the distinctive environment inhabited by this species.

Vernacular names.

White-sand terrestrial foam-nesting frog (English), rana terrestre de arena blanca (Spanish) and rãzinha da areia branca (Portuguese).

Diagnosis.

The species Adenomera albarena is recognised by the following combination of characters. (1) Medium size (adult male SVL = 21.2-23.0 mm, n = 21; adult female SVL 22.1-24.3, n = 5); (2) snout of males subovoid in dorsal view and acuminate in lateral view; (3) absence of antebrachial tubercle; (4) toe tips moderately to fully expanded (character states C, D sensu Heyer (1973)); (5) throat in males with condensed melanophores near the jaw and scattered melanophores on the central portion; 6) nearly solid dark-coloured stripe present on the underside of the forearm; (7) Advertisement call composed of a single pulsed note; (8) notes formed by 11-21 pulses; (9) pulses incomplete; (10) dominant frequency 3,448-4,349 Hz; (11) dominant frequency coinciding with the second harmonic; (12) Endotrophic tadpoles; (13) with labial teeth absent; (13) spiracle present; and (14) internarial distance 44-52% of IOD.

Interspecific comparisons.

Adenomera albarena differs from all congeners, except A. simonstuarti by having a nearly solid dark-coloured stripe on the underside of the forearm ( Heyer 1973, 1975; Kwet and Angulo 2002; Almeida and Angulo 2006; Kok et al. 2007; Kwet 2007; Angulo and Reichle 2008; Berneck et al. 2008; Kwet et al. 2009; Angulo and Icochea 2010; Carvalho and Giaretta 2013a, 2013b; Carvalho et al. 2019a, 2019b, 2019c, 2019d, 2020a, 2020c, 2021; Cassini et al. 2020; Zaracho et al. 2023).

Amongst Amazonian congeners, adult male Adenomera albarena have SVL 21.2-23.0 mm, which is smaller than A. glauciae (SVL 27.6-30.4; Carvalho et al. (2020b)), A. gridipappi (SVL 25.4-27.7 mm; Carvalho et al. (2021)), A. lutzi (SVL 25.7-33.5 mm; Kok et al. (2007)) and A. simonstuarti (SVL 23.4-26.2 mm; Angulo and Icochea (2010); Carvalho et al. (2020b); present study), but larger than A. kayapo (SVL 17.5-21.0 mm; Carvalho et al. (2021)). Adenomera albarena has a snout rounded in dorsal view, which differs from A. martinezi (snout pointed in dorsal view; Carvalho & Giaretta (2013b)). The absence of an antebrachial tubercle distinguishes A. albarena from A. amicorum , A. aurantiaca , A. cotuba , A. glauciae , A. gridipappi , A. inopinata , A. kayapo , A. lutzi , A. tapajonica and A. phonotriccus (antebrachial tubercle present; Kok et al. (2007); Carvalho and Giaretta (2013b), Carvalho et al. (2019b, 2020c, 2021)). Adenomera albarena has toe tips moderately to fully expanded (states C and D, sensu Heyer (1973)), which differs from A. cotuba , A. hylaedactyla and A. martinezi (toe tips pointed to poorly expanded, states A and B, respectively; Carvalho et al. (2019c); Carvalho and Giaretta (2013a, 2013b)). Adenomera albarena differs from A. heyeri by having white ventral colouration (yellow colouration; Carvalho et al. (2021)). Although A. albarena differs morphologically from A. andreae , A. chicomendesi and A. guarayo only by having a nearly solid dark-coloured stripe on the underside of the forearm (absence in A. andreae , A. chicomendesi and A. guarayo ; Carvalho et al. (2019a, 2019b, 2019c)), it also differs acoustically from these species (see below).

The advertisement call of Adenomera albarena is composed of incomplete pulses, which differs from A. aurantiaca , A. guarayo , A. inopinata and A. phonotriccus (complete pulses; Carvalho et al. (2019b, 2020a, 2021)). Amongst those with incomplete pulses, calls of A. albarena sp. nov. differ from A. amicorum , A. glauciae , A. gridipappi and A. simonstuarti sensu stricto by having a single note (multi-note calls; Angulo and Icochea (2010); Carvalho et al. (2020b, 2021)). Adenomera albarena has calls composed of 11-21 pulses, which differ from A. amicorum (4-10 pulses; Carvalho et al. (2021)), A. andreae (3-10 pulses; Carvalho et al. (2019c)), A. chicomendesi (22-35 pulses; Carvalho et al. (2019a)), A. gridipappi (2-4 pulses; Carvalho et al. (2021)), A. heyeri (4-12 pulses; Carvalho et al. (2021)), A. hylaedactyla (4-10 pulses; Carvalho et al. (2019c)), A. tapajonica (3-5 pulses; Carvalho et al. (2021)), A. glauciae (unpulsed; Carvalho et al. (2020b)) and A. simonstuarti sensu stricto (2-6 pulses; this study). Adenomera albarena has a dominant frequency of 3,448-4,349 Hz, which differs from A. kayapo (4,570-4,990 Hz; Carvalho et al. (2021)) and A. simonstuarti sensu stricto (1,851-2,224 Hz; this study). The dominant frequency of Adenomera albarena sp. nov. is placed in the second harmonic, which differs from A. simonstuarti sensu stricto (dominant frequency in the fundamental harmonic).

Lack of labial teeth distinguishes tadpoles of Adenomera albarena from exotrophic tadpoles of A. guarani , A. saci and A. thomei (present in all mentioned species; De la Riva (1995); Almeida and Angulo (2006); Carvalho and Giaretta (2013a)). Endotrophic tadpoles of A. albarena differ from those of A. hylaedactyla and A. andreae by the presence of a spiracle (absent in all mentioned species; Menin et al. (2009); Menin and Rodrigues (2013)); from A. marmorata by an internarial distance 44-52% of IOD (IND/IOD = 74%; Heyer et al. (1990)).

Description of the holotype.

Adult male (Figs 4A, B, C , 5A, C ). Dorsal skin glandular, warty on flank. Dorsolateral fold indistinct. Sacral region, dorsal surface of tibia and posterior surface of tarsus with white-tipped tubercles. Vertebral stripe in sacral region. Throat, belly and ventral surface of limbs smooth. Pair of lumbar glands. Posterior surface of thigh with a pair of paracloacal glands. Snout subovoid in dorsal view and acuminate in profile. Nostril closer to the snout tip than to the eye and orientated dorsolaterally; fleshy ridge on the snout tip. Eye nostril distance 83% of eye diameter, eye diameter equals internarial distance. Head wider than long. Internarial distance> 25% of head width. Canthus rostralis defined; loreal region slightly concave. Triangular interorbital blotch. Tympanum distinct, nearly 60% of eye diameter; black-coloured supratympanic fold well developed, extending from posterior corner of eye to base of arm. Postcommissural gland ovoid. Subgular vocal sac; vocal slits present. Vomerine teeth in two straight rows posterior to choanae and arranged in transverse series parallel to choanae. Tongue lanceolate (sensu Duellman (1970)) and free behind. Relative finger lengths IV <I ≈ II <III; fringes or webbing on fingers absent; finger tips rounded, slightly expanded, but without disc; inner metacarpal tubercle elliptical; outer metacarpal tubercle rounded; distinct rounded greyish subarticular tubercles on the underside of fingers; supernumerary tubercles rounded; antebrachial tubercle absent. Elliptical axillary gland. Tibia slightly longer than thigh (TL/THL = 1.01). Relative toe lengths I <II <V <III <IV; toe tips flattened or slightly flattened, with visible expansions (character states C and D, sensu Heyer (1973)); fringes or webbing absent; inner metatarsal tubercle elliptical; outer metatarsal tubercle rounded. Tarsal fold from the inner metatarsal tubercle extends 2/3 of tarsus length. Subarticular tubercles elliptical or rounded, supernumerary tubercles rounded.

Colour of the holotype in life. Snout tip Cinnamon-drab (cc 50), with a fleshy ridge Pale neutral grey (cc 296). Blotches on upper and lower lips Light sky blue (cc 191). Postcommissural gland with melanophores. Tympanum Dark carmine (cc 61) at its edge and Buff (cc 5) in the centre. Supratympanic fold Vandyke brown (cc 281). Thoracic dorsal surface of body Prout’s brown (cc 47); lumbar region Cinnamon-drab with white-tipped tubercles. Interorbital region Sepia (cc 286). Flank Dark spectrum yellow (cc 78). Triangular blotch Sepia. Dorsal surface of forelimbs Tawny (cc 60) with Raw umber (cc 280) blotches. Dorsal surface of hind-limbs True cinnamon (cc 260) with transverse Raw umber bars. Vertebral stripe in sacral region Medium chrome orange (cc 75). Paracloacal region and lumbar glands Sepia. Throat Pale mauve (cc 204) with low density of melanophores around the jaw; belly Light buff (cc 2) and chest and underside of limbs the same colour as throat. Underside of forearm with Dark greyish-olive (cc 275) nearly solid stripe. Palm of hand, sole of foot, digits and subarticular tubercles almost completely covered with melanophores. Metatarsal, proximal and medial phalanx have a Fuscous (cc 283) ventral stripe, which is not present in distal phalanx and toe tip.

Colour of the holotype in preservative. See Figs 4A-C , 5A, C . Iris chrome orange (colour code [cc] 74). Snout tip Pale neutral grey (cc 296), as well as the fleshy ridge. Blotches on upper and lower lips Pale neutral grey. Postcommissural gland with melanophores. Tympanum Dark grey (cc 45). Supratympanic fold Vandyke brown (cc 281). Thoracic dorsal surface of body Hair brown (cc 277); lumbar region Cinnamon-drab (cc 50) with white-tipped tubercles. Interorbital region Sepia (cc 279). Flank Pale buff (cc 1). Triangular interorbital blotch Dark greyish-brown (cc 284). Dorsal surface of forelimbs Pale buff (cc 1) with Drab (cc 19) blotches. Dorsal surface of hind-limbs Tawny olive (cc 17); transverse bars Sepia with white-tipped tubercles. Vertebral stripe Pale buff in sacral region. Paracloacal region and lumbar glands Sepia. Throat Light buff (cc 2) with melanophores and a greater density around the jaw; belly Light buff and chest and underside of limbs pale Pinkish buff (cc 3). Underside of forearm with nearly solid Brownish-olive (cc 276) stripe. Palm of hand, sole of foot, digits and subarticular tubercles almost completely covered with melanophores. Stripe in metatarsal and proximal and medial phalanx Fuscous (cc 283) (Figs 5C, D ).

Intraspecific variation.

Morphometric variation of the new species is summarised in Table 3 . The type series shows three dorsal colour patterns: dark blotches few or absent (Figs 6A , 7A ); many dark blotches (Figs 6B , 7D ); and a dorsolateral stripe (Figs 6C , 7G ). Sixty-eight percent of the type series (including the holotype) has the first pattern, 20% have many dark blotches and only 12% have a dorsolateral stripe. A sacral stripe is present in 64% of specimens. About 52% of paratypes have a toe tip shape in stage D (sensu Heyer (1973)), while 48% have an intermediate shape, stages C or D. All individuals have a triangular mark on the head (Fig. 6 ), which is less visible in individuals that lack dorsal blotches. Texture of the dorsum varies from rough to smooth, with few to many glandules. Throat and belly show slight variation in melanophore density (Fig. 7B, E, H ).

Advertisement call.

The advertisement call of Adenomera albarena consists of a single note with partially fused pulses. Pulse number varies from 11 to 21; pulse duration from 4 to 23 ms; and pulse repetition rate from 94 to 138 pulses per second. Note duration varies from 100 to 199 ms and note repetition rate from 0.6 to1.2 notes per minute. The fundamental frequency of the note coincides with the first harmonic and varies from 1,765 to 2,239 Hz; the dominant frequency varies from 3,746 to 4,349 Hz and corresponds to the second harmonic (Table 4 ; Fig. 8 ).

Tadpole.

Body elliptical in dorsal and ventral views, globular in lateral view (Fig. 9A-C ); BH 86-96% and 51-58% of BW and BL, respectively (Table 5 ). Body length 36-41% of TL, with a well-marked constriction in the postorbital region (Fig. 9A ) that is more pronounced in dorsal than ventral view and less marked in some tadpoles. Snout rounded in dorsal and lateral views; eye-nostril distance 6-7% of BL. Internarial region convex; internarial distance 44-52% of IOD. Nostrils small, rounded, located and directed anterolaterally; visible in lateral view, poorly visible in dorsal view; closer to snout than to eyes. Border of external nares without fleshy marginal rim; border smooth, slightly below the level of marginal region. Eyes large, diameter 34-39% and 139-190% of IOD and END, respectively; located laterally, but directed anterolaterally. Interorbital region slightly concave; interorbital distance 46-50% of BW. Spiracle very small, single, sinistral; directed posterodorsally, located immediately above the edge of the lateral body surface at the level of the hind-limb insertion; poorly visible in dorsal and lateral views. Spiracular opening elliptical; aperture small, narrower than spiracle width, inner wall fused to the body wall. Widely coiled intestines positioned ventrally, perpendicular to main body axis, concealing other internal organs. Vent tube medial with sinistral displacement; comma-shaped, directed upwards; opening very small, rounded, directed dorsally; mostly free from the ventral fin, dorsal wall attached only near the body junction. Tail moderately long, length 142-178% and 59-64% of BL and TL, respectively; low, maximum tail height 83-94% of BH; tip rounded. Musculature moderately robust with strongly acuminate tip, which reaches the tail tip; higher than wide near the tail-body junction, tail muscle width 70-79% of TMH; tail muscle height 43-49% of MTH. Dorsal fin external margin slightly convex, originating from posterior third of body; higher than body, slightly higher than ventral fin, with maximum height at its central portion. Ventral fin external margin poorly arched; maximum height at mid-tail; same height as or shorter than body. Oral disc small, ODW 29-33% of BW; unemarginated; located and directed anteroventrally (Fig. 9D ). Upper and lower labium present; upper labium with 4-6 short, rounded papillae on lateral region, interleaved by a large medial gap, but arranged in a straight line; posterior labium projected posteriorly, with 3-6 short rounded papillae laterally, interleaved by a medial gap, but arranged in a straight line; anterior gap larger than posterior. Submarginal papillae absent. Jaw sheath keratinised only at the external borders; upper jaw sheath arch-shaped, lower jaw sheath V-shaped. Serrations on each sheath extend its entire length. Labial teeth absent; two labial ridges on the upper labium and three on the lower, formulae 2(2)/3(1).

In preservative, dorsal surface of body brown; anterior half of body darker and with more melanophores than posterior half, with very fine translucent vermiculation on posterior half. Dorsal hind-limbs translucent with numerous melanophores. Tail mostly translucent grey, brown at the tail/body junction; caudal musculature whitish-grey; fins translucent grey; small melanophores on the caudal musculature. Vent tube translucent grey. Ventral surface of body translucent grey with numerous melanophores anteriorly; posterior portion translucent, except for lateral regions, which are light brown.

Distribution, habitat and natural history.

Adenomera albarena is known only from the white-sand ecosystems between West Negro and the Solimões Rivers, specifically in the RDS Rio Negro and nearby localities, Municipalities of Iranduba and Manacapuru, Amazonas, Brazil, where these ecosystems are dominant (Figs 1 , 10A ). Two other species of Adenomera occur in sympatry: A. hylaedactyla and A. andreae . Although these species occur in the same region, their habitat is not the same; A. andreae mainly inhabits non-flooded forests, while A. hylaedactyla occurs in open areas. On the other hand, Adenomera albarena inhabits white-sand forests subject to flooding regimes close to streams. At the type locality, A. andreae and the new species occur in syntopy at the border between forests subject to flooding regimes and those that do not flood.

Males call from the ground, above or hidden in the leaf litter (Fig. 10B ). They start calling at ~ 16:00 h and continue calling until ~ 19:00 h. Isolated individuals sometimes call later, but it is unusual.

Adult males are found easily and juveniles are also not difficult to observe, but females are very secretive (Fig. 10C ). Males excavate underground chambers in which foam nests are built and females deposit their eggs (Fig. 10D ). The chambers are very difficult to find when they are located under leaf litter amongst the roots of palm trees and ferns.

Conservation.

The known geographic distribution of Adenomera albarena comprises an area of approximately 150 km2 within the RDS Rio Negro and nearby localities. Although the species is known only from a small area, it is very common there and likely occurs in other parts of the RDS Rio Negro and, potentially, in the nearby Jaú National Park. Despite its abundance, the new species occurs exclusively in white-sand forests subject to flooding regimes, which are highly vulnerable to anthropogenisation (e.g. from pollution, deforestation, mining, free-ranging livestock, irregular occupation and recreational use of water). Indeed, several riverine areas in this environment at RDS Rio Negro, including the type locality, have already been impacted by some of these anthropogenic drivers. Long-term monitoring that compares populations between pristine and anthropogenised areas is essential to evaluate whether and how these drivers impact the conservation status of A. albarena .

Figures

Figure 1. Geographic distribution of the Adenomera simonstuarti species complex (left) and a detailed view of the geographic distribution of the new species in central Amazonia, Amazonas, Brazil (right). Green area: Rio Negro Sustainable Development Reserve. Numbers: permanent sampling modules at (1) km 18, (2) km 26 and (3) km 50 along the AM- 352 highway; (4) Vale da Bencao Community, Ramal do 25, Manacapuru. South American countries: ARG, Argentina; BOL, Bolivia; CHL, Chile; COL, Colombia; ECU, Ecuador; PAR, Paraguay; PER, Peru; VEN, Venezuela.

Figure 4. Male holotype and female paratype of Adenomera albarena. A-C. Male holotype, INPA-H 44867; D-F. Female paratype INPA-H 44875. Scale bar: 5 mm.

Figure 5. Ventral views of the hands and feet of Adenomera albarena. A, C. Male holotype INPA-H 44867; B, D. Female paratype, INPA-H 44875. Scale bars: 5 mm.

Figure 6. Three dorsal colour patterns of Adenomera albarena in life. A. Dark blotches few or absent; B. Many dark blotches; and C. Dorsolateral stripe. Unvouchered specimens.

Figure 7. Dorsal, ventral and lateral views of the three colour patterns of Adenomera albarena in preservative. Paratypes: A-C. (INPA-H 44869, male); D-F. (INPA-H 44870, male) and G-I (INPA-H 44877, male). Photographs: L. R. Mendonca. Scale bar: 5 mm.

Figure 8. Advertisement call of Adenomera albarena (A, B) and A. simonstuarti sensu stricto (C, D). A, B. INPA-H 44876 (FNJV 59564), Rio Negro Sustainable Development Reserve, Iranduba, Amazonas, Brazil. C, D. INPA-H 44904 (FNJV 59568), Tarauaca, Acre, Brazil.

Figure 9. Preserved tadpole of Adenomera albarena, Gosner stage 35. Dorsal (A), lateral (B) and ventral views of the body (C) and ventral view of the oral disc (D). E. Detailed view of the spiracle, with its shape and aperture highlighted by dotted lines. Scale bar: 2 mm (A-D); 1 mm (E).

Figure 10. Natural history of Adenomera albarena. A. Example of the species' habitat; B. Unvouchered male vocalising on leaf litter; C. Unvouchered female hiding in the leaf litter; D. Foam nest, artificially exposed for illustration purpose. Scale bar: ~ 5 mm.