Ameerega berohoka, Vaz-Silva, Wilian & Maciel, Natan Medeiros, 2011

Vaz-Silva, Wilian & Maciel, Natan Medeiros, 2011, A new cryptic species of Ameerega (Anura: Dendrobatidae) from Brazilian Cerrado, Zootaxa 2826, pp. 57-68 : 58-67

publication ID	https://doi.org/ 10.5281/zenodo.205958
DOI	https://doi.org/10.5281/zenodo.5684261
persistent identifier	https://treatment.plazi.org/id/03993850-FFF4-FFF1-FF0C-FA4EFF72063E
treatment provided by	Plazi
scientific name	Ameerega berohoka
status	sp. nov.

Treatment

Ameerega berohoka View in CoL sp. nov.

( Figs. 1–2 View FIGURE 1 View FIGURE 2 )

Allobates femoralis View in CoL (non Boulenger, 1884)— Silva Jr. et al. 2007: 1081 Epipedobates femoralis (non Boulenger, 1884)— Souza et al. 2001: 270

Holotype. Brazil, State of Goiás, Arenópolis Municipality (16o 26' 41"S, 51o 23' 37"W, 416 m above sea level), MNRJ 67263, adult male, Sheila P. Andrade and Edmar P. Vitor col., 22 February 2010.

Paratypes. MNRJ 67262, MNRJ 67264 and MNRJ 67265, three adult males, collected along with the holotype; State of Goiás, Arenópolis Municipality, CEPB 6954, CEPB 6955, two adult males, 27 September 2005, CEPB 6956−59, four adult males, and CEPB 6960, adult female, Ariramba Faunal Rescue Team col., November 2006; State of Goiás, Mineiros Municipality, ZUFG 4043−4044, two adult males, Alessandro R. de Morais, Luciana Signorelli and Rogério P. Bastos col., 0 9 November 2008.

Diagnosis. A member of the Ameerega genus based on the combination of characters proposed by Grant et al. (2006) and Lötters et al. (2007) such as dorsal skin slightly granular; finger I> finger II when adpressed; toe and finger web absent and presence of bright flash marks; and absence of ventrolateral line. The new species is defined by the combination of: (1) a medium sized species (adult SVL 15.5–24.3 mm SVL, sexes grouped); (2) snout subelliptical in dorsal view ( Fig. 1 View FIGURE 1 A); (3) snout rounded in lateral view ( Fig. 1 View FIGURE 1 C); (4) hand small (HAL/SVL=0.2) ( Fig. 1 View FIGURE 1 E); (5) dark dorsum with pale spots in life ( Fig. 2 View FIGURE 2 A −B); (6) in life, bright-orange spots in axillae, on groin, and on medial surface of thighs ( Fig. 2 View FIGURE 2 B); (7) dorsolateral stripes cream to pale yellow in life ( Fig. 2 View FIGURE 2 A −B); (8) venter and flank with white and black reticulation ( Fig 1 View FIGURE 1 B); (9) tympanic annulus well visible, supratympanic fold absent ( Figs. 1 View FIGURE 1 C −2A); (10) finger discs well developed ( Fig. 1 View FIGURE 1 E); (11) pulses per note of the advertisement call ( Fig. 3 View FIGURE 3 A; Table 2); (12) genetic divergence of the 16S rRNA fragment gene among other Ameerega species ( HQ891922 View Materials ; Genbank accession number) (Table 3).

Comparisons with related species. Ameerega berohoka can be distinguished from A. braccata , A. flavopicta and A. boehmei by dark dorsal coloration with irregular cream spots (versus dark brown dorsum with golden, yellow or white spots in A. braccata and bright yellow spots in the two other species mentioned). It further differs from A. braccata by larger adult size and by bluish marbling on venter (versus pattern absent in A. braccata ). Also differs from A. flavopicta by its smaller adult size (SVL= 21.9 mm in A. berohoka and SVL= 26.7 mm in A. flavopicta ). The new species is distinguished from A. picta by smaller size of hands (HAL/SVL = 0.2 versus 0.3 in A. picta ), snout sub-elliptical in dorsal view (versus truncate in A. picta ) and rounded in lateral view (versus protruding in A. picta ), dorsal irregular spots (versus spots absent in A. picta ). Ameerega berohoka differs from A. yungicola by the absence of maxillary teeth (versus teeth present in A. yungicola, Lötters et al. 2005 ) and from A. hahneli and A. altamazonica by the presence of bright-orange spots in axillae, in groin and on medial surface of thighs (versus yellow in A. hahlneli and A. altamazonica, Twomey & Brown 2008 ). The new species is distinguishable from A. boliviana , A. picta , A. petersi and A. pulchripectus by the presence of cream to pale yellow dorsolateral stripes (versus yellowish or green in the respective taxa mentioned). It differs from A. rubriventris by its white and blue ventral coloration (versus reddish-orange in A. rubriventris ).

Description of holotype. Adult male, snout-vent length 19.7 mm ( Fig. 1 View FIGURE 1 ). Dorsal skin of body and hindlimbs slightly granular and dorsal skin of head, both sides of head, forelimbs, and ventral surfaces smooth ( Fig. 1 View FIGURE 1 A). Dorsal surface blackish ( Fig. 1 View FIGURE 1 A). In life and preservative, cream dorsolateral stripe present on either side of the body from tip of snout, passing over eyelid continuing towards inguinal region and cream labial stripe from tip of lower jaw to forelimbs ( Fig. 1 View FIGURE 1 A). Flanks black from groin to snout, ventrolaterally cream fading to white ventrally. In life and preservative, upper arm dorsally brown and ventrally cream ( Fig. 1 View FIGURE 1 A −B); forearm dorsally brown and ventrally white with black reticulation ( Fig. 1 View FIGURE 1 A −B). In life and preservative, hind limbs brown, dorsally with irregular black markings and ventrally white with black reticulation. In life, bright-orange spots present in axillae, groin and on medial surface of thighs, in preservative changed to white. In life and preservative, ventral surfaces of limbs, venter and head with coarse reticulation of irregular black lines. Gular region blackish ( Fig. 1 View FIGURE 1 B). In life and preservative, hands and feet dorsally brown ( Fig. 1 View FIGURE 1 A). In life, iris black. Oval tongue. Premaxillary and maxillary teeth absent. Vocal slits absent. Snout narrow sloping in lateral, sub-elliptical in dorsal view and truncate in ventral view. Nares situated and directed posterolaterally to tip of snout; nares visible from front and in ventral view but not in dorsal view. Canthus rostralis sloped, slightly concave; loreal region nearly vertical, slightly concave. Eye large and prominent with diameter 15 % of SVL; pupil rounded, horizontally elliptical. Tympanum circular, posterodorsally concealed, tympanic annulus well visible ( Fig. 1 View FIGURE 1 C); diameter less than 50% of ED; supratympanic fold absent. Hands relatively small, length 30% of SVL ( Fig. 1 View FIGURE 1 E). Relative length of adpressed fingers: II ≈ IV <I <III ( Fig. 1 View FIGURE 1 E). Finger discs moderately expanded, most evident in finger III ( Fig. 1 View FIGURE 1 E). A large, circular outer metacarpal tubercle on median base of palm ( Fig. 1 View FIGURE 1 E); a smaller inner metacarpal tubercle on base of finger I ( Fig. 1 View FIGURE 1 E); one prominent and well developed subarticular tubercle on fingers I and II, two well developed subarticular tubercles on fingers III and IV ( Fig. 1 View FIGURE 1 E). Hind limbs relatively short with heel reaching shoulder when adpressed forward along body Fig. 1 View FIGURE 1 A −B). Shank length 47% of SVL. Relative lengths of adpressed toes: I <II <V <III <IV ( Fig. 1 View FIGURE 1 D); outer metatarsal tubercle rounded and well developed ( Fig. 1 View FIGURE 1 D); outer metatarsal tubercle smaller than inner ( Fig. 1 View FIGURE 1 D); inner metatarsal tubercle with ovoid shape ( Fig. 1 View FIGURE 1 D). One subarticular tubercle on each toes I and II, two supranumerary subarticular tubercules on toes III and IV ( Fig. 1 View FIGURE 1 D). Hands and feet lacking lateral fringes and webbing ( Fig. 1 View FIGURE 1 D −E). No basal webbing on toes fringes. Tarsal tubercles absent ( Fig. 1 View FIGURE 1 D).

Measurements of holotype (in mm). SVL 19.7; HL 6.8; HW 6.1; IND 2.0; END 2.7; ED 2.9; TD 1.5; HAL 6.0; THL 9.7; TBL 9.3; FL 13.7.

Variation. We found interpopulational coloration variation in the reticulated pattern of dorsum and venter and the transversal spots of hindlimbs. Variation of morphological measurements between males and females are shown in Table 1 View TABLE 1 .

Male (N = 9) Female (N =4)

Coloration. Dorsum dark with pale reticulate spots, bright-orange spots present under axillae, dorsally over groin, and on medial surface of thighs. Dorsolateral stripes cream to pale yellow. Venter white or blueish and flanks with black reticulation. Dorsal hindlimbs light brown with dark spots ( Fig. 2 View FIGURE 2 ). The coloration of preserved specimens resembles the coloration in life. The reticulate spots of dorsum are more in life. Dorsolateral stripes are cream and the venter white with black reticulation on flanks.

Advertisement call. Oscillogram and spectrogram of the advertisement of Ameerega berohoka are shown in Figure 3 View FIGURE 3 . Acoustic parameters of the call and comparisons to other species of the A. picta group are summarized in Table 2. The advertisement call of the new species (n = 201 recorded from one specimen) is composed of a single note and pulsed with average duration of 82.5 ms (SD = 14.2) ( Fig. 3 View FIGURE 3 A). The mean of the dominant frequency is 4.2 kHz ( Fig. 3 View FIGURE 3 B) and frequency ranges from 4.0 to 4.3 kHz ( Fig. 3 View FIGURE 3 B −C). The advertisement call of A. berohoka resembles those of other species in the A. picta group, mainly in dominant and frequency range ( Table 2). However, some features of advertisement call (note duration and frequency range) of the new species are more similar to closely geographically Ameerega species: A. flavopicta , A. braccata , and A. picta ( Table 2). The advertisement call is even more similar to A. flavopicta by a combination of parameters: note duration (82.5 ms in A. berohoka and 110 ms in A. flavopicta ), frequency range frequency (4.0−4.3 kHz in A. berohoka and 3.2−4.2 kHz in A. flavopicta ), and pulses per note range (10 in A. berohoka and 6 in A. flavopicta ) ( Table 2).

notes (ms) (kHz)

A. braccata View in CoL 1 65.8 1 3.5−4.2 Forti et al. (2010) A. flavopicta View in CoL 6 110 6 3.2–4.2 Haddad & Martins (1988) A. picta View in CoL 4 50 4 3.4–4.3 Haddad & Martins (1988) A. hahneli View in CoL 6 15 6 2.5–7.0 Haddad & Martins (1988) A. altamazonica View in CoL - 70* - 4.1−4.3 Twomey & Brown (2008) A. boehmei View in CoL 1 145Ψ 2−3 2.63.2 Lötters et al. (2009) A. berohoka View in CoL 1 82. 5 10 4.0−4.3 Present work

*Obtained from the mean of the ranges data provided by Twomey & Brown (2008). Ψ Mean note duration provided by Lötters et al. (2009).

DNA barcoding. We produced an alignment of 358 base pairs. The average uncorrected p-distances of 16S rRNA sequences of the species described herein towards the other Ameerega View in CoL species analyzed range from 5.31% to 8.10% (Table 3). This is remarkably higher than that within - species variation, for instance, in Ameerega altamazonica View in CoL (0.83%) and A. hahneli View in CoL (1.39%). The new species is genetically most similar to A. flavopicta View in CoL (ca. 5.3%), followed by A. boehmei View in CoL and A. braccata View in CoL , both (ca. 6.4%) (Table 3).

Natural history. The calling male was recorded in late afternoon in cerrado sensu stricto (see Ribeiro & Walter 1998) ( Fig. 4 View FIGURE 4 A). In the wet season males were found calling in bare soil or partially hidden in vegetation and under rocks. The climate of Cerrado areas has two well-defined seasons characterized by wet/warm (approximately September to March) and dry/mild (approximately April to August) cycles ( Ribeiro & Walter 1998). In the dry season, adults and juveniles were found active on the ground during day-time in justafluvial environments of riparian and gallery forests ( Fig. 4 View FIGURE 4 B). The new species is common where it occurs. Apparently the new species is adapted to open and forested areas and it also occurs in cultivated anthropic areas (associated with Brachiara). Sympatric anuran species recorded in Piranhas Municipality include Lithobates palmipes View in CoL , Eupemphix nattereri , Ischnocnema View in CoL sp., Rhinella schneideri View in CoL , Rhinella mirandaribeiroi View in CoL , Rhinella ocellata View in CoL , Barycholos ternetzi , Phyllomedusa azurea , Dendropsophus minutus View in CoL , D. rubicundulus View in CoL , D. cruzi View in CoL , D. nanus View in CoL , Hypsiboas lundii View in CoL , H. raniceps View in CoL , H. paranaiba View in CoL , Scinax fuscovarius View in CoL , Trachycephalus venulosus View in CoL , Physalaemus cuvieri , P. centralis , Pseudopaludicola saltica , Leptodactylus View in CoL aff. latrans, L. fuscus View in CoL , L. labyrinthicus View in CoL , L. martinezi View in CoL , L. mystaceus View in CoL , L. podicipinus View in CoL , Chiasmocleis albopunctata View in CoL and Elachistocleis cesarii View in CoL ( Oliveira et al. 2010; W. Vaz-Silva, unpubl. data).

Distribution. Ameerega berohoka are known to occur in western and southewestern regions in the state of Goiás ( Fig. 5 View FIGURE 5 ). The species seems to be associated with sub-basins that drain the Araguaia River.

Consevation status. The areas in Cerrado are severely threatened by increasing deforestation, charcoal production, and large hydroelectric dams. As a result the Cerrado was recognized as one of the world’s biodiversity hotspots ( Myers et al. 2000). However, most areas in Cerrado are still poorly sampled and the new species are currently recognized for only three localities. Based on this criterion we suggested considering Ameerega berohoka being ‘Data Deficient’ (DD) in IUCN Red List.

Etymology. The specific epithet is derived from the Karajás indigenous term " Berohokã ", meaning “big river”. Ameerega berohoka occurs in sub-basins related to the Araguaia River ( Fig. 5 View FIGURE 5 ). So, the specific name is in recognition of this important Brazilian river. It is used as a noun in apposition.

Remarks. Souza et al. (2001) extended the distribution of the Allobates femoralis complex based on tadpoles and juveniles from the municipality of Piranhas, state of Goiás. We will not rule out that the tadpoles and juveniles found were those of A. berohoka , as we never recorded A. femoralis in the region. Silva Jr. et al. (2007) recorded what they called A. femoralis in the Basin of Caiapó River. Our comparison of voucher specimens confirmed that the specimens correspond to A. berohoka .

The uncorrected p-distances analysis of the 16S mitochondrial rRNA fragment gene revealed higher degrees of divergence among the Ameerega species than previous studies (e.g. Lötters et al. 2009). Probably, this incongruence is related to difference in the matrix size of both works. We produced an alignment of 358 base pair (excluding indels from the alignment due to ambiguous alignments) that is smaller than the analysis performed by Lötters et al. (2009) that selected (564 bp). Probably, we selected a part of the 16S fragment relatively more variable than Lötters et al. (2009), reflecting directly in the results.

Ameerega berohoka is poison frog endemic to Brazilian Cerrado biome and distinguishable from other species in the Ameerega picta group by a combination of features such as: sized; snout shape; patterns of coloration in different parts of the body; patterns of tympanic annulus and supratympanic fold; development of foot and finger discs; pulses per note of the advertisement call; and the genetic divergence of the 16S rRNA fragment gene among other Ameerega species. The new species resembles A. picta , A. flavopicta , A. braccata , and A. boehmei by the features examined such as adult morphology, advertisement call parameters and genetic divergence. However, this arrangement may not reflect phylogenetic relationships. A phylogenetic study including all or at least most species in the A. picta group is necessary to test the monophyly and the relationships among the species in the A. picta group.

Character	Mean (± SD)	Range	Mean (± SD)	Range
SVL	20.8 (± 1.2)	19.2–23.4	23.0 (± 1.1)	21.9–24.3
HW	6.4 (± 0.3)	6.0–7.0	7.0 (± 0.4)	6.5–7.4
HEL	6.9 (± 0.5)	6.2–7.8	7.3 (± 0.4)	6.9–7.8
THL	9.8 (± 0.2)	9.6–10.2	11.0 (± 0.6)	10.2–11.5
TIL	9.9 (± 0.4)	9.3–10.6	10.6 (± 0.4)	10.0–11.1
FL	14.1 (± 0.6)	13.4–15.3	15.1 (± 0.8)	14.3–15.7
HAL	5.6 (± 0.5)	5.0–6.1	5.8 (± 1.0)	4.4–6.4
ED	2.8 (± 0.2)	2.6–3.1	2.7 (± 0.3)	2.5–3.1
TD	1.6 (± 0.1)	1.4–1.7	1.5 (± 0.2)	1.3–1.8
EM	2.4 (± 0.5)	2.0–3.1	2.4 (± 0.3)	2.1–2.9
ID	2.2 (± 0.4)	1.6–2.7	2.8 (± 0.2)	2.5–3.0