Dendropsophus kamagarini, Rivadeneira, C. Daniel, Venegas, Pablo J. & Ron, Santiago R., 2018

Rivadeneira, C. Daniel, Venegas, Pablo J. & Ron, Santiago R., 2018, Species limits within the widespread Amazonian treefrog Dendropsophusparviceps with descriptions of two new species (Anura, Hylidae), ZooKeys 726, pp. 25-77 : 38-46

Dendropsophus kamagarini sp. n. Figs 1, 7B, 10, 11

Holotype.

CORBIDI 5246, an adult male from Peru, Madre de Dios Department, Tambopata Province, Inotawa Lodge (12.8092°S, 69.3182°W), 192 m above sea level, collected on 9 October 2009 by P. J. Venegas.

Paratypes.

CORBIDI 5259, an adult male from Peru, Madre de Dios Department, Tambopata Province, La Habana (12.6537°S, 69.1796°W), 192 m above sea level, collected on 18 October 2009 by V. Duran and M. Cuyos. Thirty-three adult males and seven adult females from Peru, Cusco Department, La Convencion Province: Comunidad Ochigoteni (12.5758°S, 73.0900°W), 1696 m above sea level, CORBIDI 5392, adult female, collected on 19 October 2009 by G. Chavez; Pongo de Mainique (12.2581°S, 72.8425°W), 670 m above sea level, CORBIDI 5471, 5473, 5480, 5484, adult males, collected on 23 April 2010 by G. Chavez; Megantoni (12.2581°S, 72.8425°W), 670 m above sea level, CORBIDI 6659, 6664, 6679, 6685, 6687 88, 6698, adult males, CORBIDI 6692, 6694, adult females; Comunidad Nativa Chokoriari (11.9569°S; 72.9409°W), 434 m above sea level, CORBIDI 8067 68, 8070, adult males, CORBIDI 8069, adult female, collected on 8 December 2010 by D. Vasquez; Comunidad Nativa Poyentimari (12.1885°S, 73.0009°W), 725 m above sea level, CORBIDI 8150 51, 8153, 8228?36, 8285 86, 8305, 8476, adult males, CORBIDI 8152, 8463, adult females, collected on 28 November 2010 by G. Chavez; Puyantimari (12.1861°S, 73.0004°W), 710 m above sea level, CORBIDI 9762, adult male, collected on 8 September 2011 by D. Vasquez and K. Garcia; Pagoreni norte (11.7115°S, 73.8967°W), 402 m above sea level, CORBIDI 10018, adult female, CORBIDI 10019, adult male, collected on 22 November 2011 by V. Duran; Palmeiras-Alto Shima (12.5453°S, 73.1350°W), 1500 m above sea level, CORBIDI 10585, adult female, collected on 7 February 2012 by G. Chavez and D. Vasquez; Chokoriari (11.9569°S, 72.9409°W), 413 m above sea level, CORBIDI 10628, adult male, collected on 19 February 2012 by G. Chavez and D. Vasquez.

Referred specimens.

Two adults from Bolivia, Cochabamba Department, Ayopaya Province: confluence of the Altamachi and Ipiri rivers (16.0543°S, 66.6667°W), 600 m above sea level, MHNC-A 427, 429, collected on 15 September 2004 by A. Munoz and G. Rey. An adult from Bolivia, Cochabamba Department, Carrasco Province: Valle del Sacta (17.118°S, 64.767°W), 230 m above sea level, MHNC-A 2116, collected on 18 April 2014 by G. Callapa, A. Munoz, D. Ercken, S. Barron, and M. Careaga.

Etymology.

The specific name kamagarini is a noun derived from the Matsigenka language, which means demon or devil ( Snell et al. 2011). The Matsigenka language is spoken by the Matsigenka people who inhabit the highlands and lowlands of southeastern Peru, in the departments of Cusco and Madre de Dios. Judeo-Christian religions depict the demon as a human figure with horns. The species name is in allusion to the prominent horn-like tubercles on the upper eyelid of D. kamagarini .

Diagnosis.

Throughout the species description, coloration refers to preserved specimens unless otherwise noted. The new species is assigned to the genus Dendropsophus based on our phylogenetic results (Fig. 1) and the overall similarity with D. parviceps and other species of the genus (Figs 10 11). Dendropsophus kamagarini is a medium-sized species, relative to other species in the D. parviceps group and is characterized by the following combination of traits: (1) size sexually dimorphic; mean SVL 19.9 mm in males (range 17.6 22.7; n = 35), 26.1 mm in females (range 24.0 28.1; n = 7); (2) throat brown mottled with white flecks posteriorly in males vs. white blotch with flecks or with stripes posteriorly in females (Fig. 11); (3) snout is short and truncate in dorsal and lateral views; (4) nostrils slightly protuberant; (5) tympanum visible, tympanic membrane non-differentiated, annulus distinct; (6) one prominent conical tubercle on the distal edge of the upper eyelid; (7) thoracic fold indistinct to barely evident; (8) ulnar tubercles and outer tarsal tubercles distinct; (9) axillary membrane present; (10) skin on dorsal surfaces smooth with scattered tubercles; skin on chest, belly, posterior surfaces of thighs, and subcloacal area coarsely areolate; skin on throat grooved with scattered tubercles; (11) dark brown markings on dorsum (Fig. 11); (12) thenar tubercle distinct; (13) hand webbing formula II1- 2+III1- 1-IV, feet webbing formula I11/2 2+II1- 1III1- 2-IV2 1V; (14) in life, dorsum tan, brown or reddish brown; (15) orange to amber blotch on the proximal ventral surface of shanks and under arms, from the axillae to near the elbow, in life (white to creamy white in preserved); (16) one suborbital white bar present both in life and preserved; (17) thighs black to dark brown with two or three spots on the anterodorsal surfaces both in life and preserved; (18) iris in life creamy white with brown to reddish brown reticulations and a cream ring around pupil.

Comparisons with other species.

Dendropsophus kamagarini is most similar to D. parviceps and D. kubricki sp. n. It can be distinguished from D. parviceps by having a prominent conical tubercle on the distal edge of the upper eyelid (tubercle absent in D. parviceps ; Fig. 12) and a blunt and short snout in lateral view (slightly inclined posteroventrally in profile in D. parviceps ; Fig. 12). Dendropsophus kamagarini is larger than D. parviceps (Fig. 2; see Morphological comparisons) and has a throat with white flecks posteriorly in males both in life and preserved (dark flecks posteriorly in males both in life and preserved in D. parviceps ). Advertisement calls of D. kamagarini also have lower dominant frequency than those of D. parviceps (Fig. 4A D; see Bioacoustic comparisons) and more pulses in the advertisement call (less pulses in D. parviceps ; Fig. 4A D; see Bioacoustic comparisons). Dendropsophus kamagarini differs from D. kubricki sp. n. by having a prominent conical tubercle on the distal edge of the upper eyelid (scattered low tubercles in D. kubricki ; Fig. 12).

Dendropsophus kamagarini differs from other species of the D. parviceps group (sensu Fouquet et al. 2015) by having an orange or amber blotch on the proximal ventral surface of shanks and arms in life and a prominent conical tubercle on the distal edge of the upper eyelid (orange blotches and tubercle absent in D. bokermanni [ Goin 1960; Duellman and Crump 1974], in D. brevifrons [ Duellman and Crump 1974], in D. counani [ Fouquet et al. 2015], in D. frosti [ Motta et al. 2012] and in D. koechlini [ Duellman and Trueb 1989]). Dendropsophus kamagarini also resembles D. pauiniensis , but it can be distinguished by the presence of an orange or amber blotch on the proximal ventral surface of shanks and a prominent conical tubercle on the distal edge of the upper eyelid (blotch and tubercle are absent in D. pauiniensis ; Heyer 1977).

Description of holotype.

Adult male (Fig. 7B), SVL 19.6 mm. Head as wide as body, wider than long, widest below eyes; snout truncate and short in dorsal view, slightly inclined posteroventrally in lateral view; loreal region flat; lips thin; internarial region slightly concave; nostrils slightly protuberant dorsally and laterally; interorbital area flat; tympanum rounded distinct, tympanic annulus evident, tympanic membrane non-differentiated, supratympanic fold thin, restricted to upper edge of tympanum. Arms slender, not hypertrophied; axillary membrane extending to one third of upper arm; ulnar fold distinct, low ulnar tubercles present; fingers short, bearing small, round discs; relative length of fingers I <II <IV <III; subarticular tubercles small, round on fingers I and II, bifid on finger III, and divided on finger IV; supernumerary tubercles small, slightly evident; thenar tubercle distinct; palmar tubercle flat, round; webbing basal between fingers I and II; webbing formula of fingers II1- 2III11/2 1-IV. Hindlimbs long, slender; tarsal fold absent, outer tarsal tubercles present, low; calcar and heel tubercles absent; toes bearing round discs, smaller than those of fingers; relative length of toes I <II <III <V <IV; subarticular tubercles small, round; supernumerary tubercles indistinct; inner metatarsal tubercle small, flat, elliptical; outer metatarsal tubercle absent; webbing formula of toes I11/2 1-II1- 1III1- 2IV2 1-V. Skin on dorsum, dorsal surfaces of limbs, flanks, and groin smooth; skin on head smooth with scattered tubercles and one prominent conical tubercle on the distal edge of the upper eyelid; skin on venter, chest, posterior surfaces of thighs, and subcloacal area coarsely areolate; skin on throat and ventral surfaces of limbs smooth. Cloacal opening directed posteriorly at upper level of thighs; cloacal sheath short; cloacal folds and tubercles absent. Tongue cordiform, barely free posteriorly; dentigerous process of vomers small, prominent, narrowly separated, each bearing three and two vomerine teeth (left/right), positioned obliquely to choanae; choanae small, rounded; vocal slits long, extending from midlateral base of tongue to angle of jaws; vocal sac single, median, subgular.

Color of holotype in preservative.

Figure 7B. Dorsal surfaces of head, body, and limbs brown, grayish tan dorsolaterally with dark brown markings on dorsum consisting of median blotch anteriorly, transverse bars posteriorly; dark brown broad transverse bars on the forelimbs and shanks; anterodorsal surfaces of thighs black with three white spots; white suborbital bar. Ventral surface of belly white anteriorly, creamy mottled posteriorly with dark brown scattered flecks; chest white, throat brown anteriorly and white with brown flecks posteriorly; ventral surfaces of limbs creamy.

Measurements of holotype (in mm).

SVL 19.6, HW 6.3, HL 5.9, END 2.1, IN 2.0, FL 10.4, TL 10.7, FL 8.6.

Variation.

Morphometric variation in the paratype series is given in Table 3. Variation in dorsal and ventral coloration of preserved specimens is shown in Figure 11. Dorsal coloration in preservative varies from gray (e.g., CORBIDI 8305, 10019) to grayish tan (e.g., CORBIDI 8232, 8234), brown (e.g., CORBIDI 5471, 5480), dark brown (e.g., CORBIDI 6694, 8229), reddish brown (e.g., CORBIDI 8463) or creamy tan (e.g., CORBIDI 8151) with dark brown markings (Fig. 11); some specimens have a blotch in occipital region, a blotch in scapular region, and a transverse blotch extending onto flanks in sacral region (e.g., CORBIDI 8234) or two)(shaped stripes beginning on the upper eyelids, extending onto the flanks, and reaching the sacral region; an indistinct creamy middorsal line extends from the occipital region to the sacral region (e.g., CORBIDI 6694, 8151); some specimens have brown, creamy or grayish tan stripes around the dark brown markings (e.g., CORBIDI 10018). The dorsum has scattered tubercles, mainly on head and upper eyelid (e.g., CORBIDI 5471, 6694), but in some specimens the dorsum is smooth (e.g., CORBIDI 8069, 10018). The prominent conical tubercle on the upper eyelid in live individuals becomes smaller in preserved specimens (based on comparisons between photographs and their specimens; Fig. 10).

The venter of preserved specimens (Fig. 11) varies from grayish tan (e.g., CORBIDI 8234), to dark brown (e.g., CORBIDI 5471, 8305), and black (e.g., CORBIDI 8463, 10018) with white scattered flecks. The throat (Fig. 11) varies from gray (e.g., CORBIDI 8305), grayish tan (e.g., CORBIDI 8229), brown (e.g., CORBIDI 5480, 6694), to dark brown (e.g., CORBIDI 5471, 10018) anteriorly, with white flecks (e.g., CORBIDI 5471, 10019), one white blotch (e.g., CORBIDI 10018) or stripes (e.g., CORBIDI 6694) posteriorly. The subcloacal area is white in most specimens (e.g., CORBIDI 6694, 8229, 8232, 10018), but in some specimens the subcloacal area is black (e.g., CORBIDI 8463).

Color in life.

Based on digital photographs (Fig. 10): dorsum varies from tan to brown or reddish brown; creamy tan or mustard brown dorsolaterally; dorsal markings are dark brown, some individuals have brown, creamy, or grayish tan stripes around markings; some individuals also have scattered dark brown flecks dorsolaterally; the flanks are white with black vertical bars; dorsal surfaces of forelimbs and shanks have dark brown transversal bars; the thighs are black with two or three spots on the anterodorsal surfaces. The single suborbital bar is white. The venter is white anteriorly and dark brown or black mottled with translucent gray posteriorly, with white scattered flecks; chest is white and mottled with brown anteriorly; throat is brown or dark brown anteriorly and spotted with white flecks posteriorly in males (posterior part of throat with white blotch with or without stripes in females); the ventral surfaces of the limbs are translucent gray, thighs are mottled with black or dark brown anteriorly and posteriorly the thighs are black with white flecks; the ventral surface of shanks, from the knee to one third or on half the length of the shank, and arms, from the axillae to near the elbow, have a bright amber or orange blotch. Vocal sac in males is olive tan. The iris is creamy white with brown to reddish brown reticulations or reddish brown with creamy white reticulations and a cream ring around pupil.

Calls

(Fig. 4C?D). Descriptive statistics of acoustic variables are provided in Table 6. We analyzed recordings from: (1) three males from Tambopata (13.1343°S, 69.6090°W, 233 m) on 5 March 2016, at 19:00h, 21:40h and 24:47h; (2) one male from Reserva Comunal Amarakaeri (12.7834°S, 70.9548°W, 365 m, Madre de Dios Department, Manu Province, Peru) recorded on 5 February 2015; (3) one male from Chontachaka (12.0405°S, 71.7230°W, 630 m, Cusco Department, Paucartambo Province, Peru); and (4) one male from Rio Madeira (8.8482°S, 64.0689°W, 110 m, Rondonia State, Brazil) ( Lima et al. 2012). Recorded males were not collected.

The advertisement call is a pulsed note (Fig. 4C?D). The amplitude of the advertisement call gradually increases until three-quarters of the note duration to decrease abruptly until the end. The advertisement call may be followed or not by secondary click notes. Nonetheless, the click notes are occasionally vocalized alone. The click notes are pulsed except for the last note.

One recording from Cobija, Bolivia (Pando Department, Nicolas Suarez Province) by Marquez et al. (2002) falls within the range of variation of advertisement calls of Dendropsophus kamagarini from Peru (Table 6). In addition, the number of pulses (15) and the dominant frequency (4150 Hz) of the call described by Duellman (2005) fall within the range for calls of D. kamagarini (Table 6).

Distribution and ecology.

Dendropsophus kamagarini occurs in the Amazon basin of southeastern Peru (Cusco and Madre de Dios regions; Fig. 9), northwestern Brazil (Acre and Rondonia states; Fig. 9), and northeastern Bolivia, from the Andean slopes to lowland tropical rainforest (Fig. 9). Localities with known elevation range from 150 m (Acre) to 1696 m (Ochigoteni) above sea level.

Bolivian records are partly based on De la Riva et al. (2000) report of Dendropsophus parviceps in central northeastern Bolivia, Departments of Beni, Cochabamba, La Paz, Pando, and Santa Cruz. One photograph from Puerto Almacen (Santa Cruz Department; pp. 102 in De la Riva et al. 2000) and two photographs from Tahuamanu and El Negro (both from Pando Department; Fig. 10) show the conical tubercle on the upper eyelid characteristic of D. kamagarini . Dendropsophus parviceps distribution range is at a distance of over 1500 km, which make very unlikely that Bolivian records are conspecific. Thus, we propose that all historic records of Dendropsophus parviceps from Bolivia are assigned to D. kamagarini .

The call from Cobija (Pando Department) falls within the range of advertisement call of D. kamagarini (Table 6). The localities of El Negro, Tahuamanu, and Cobija are at a distance of 89 km, 158 km, and 203 km, respectively, to the type locality of D. kamagarini (Inotawa). In addition, specimens from Museo de Historia Natural Alcide d Orbigny, Cochabamba, Bolivia, also have a prominent conical tubercle on the distal edge of the upper eyelid. These specimens are from Valle del Sacta and the confluence of the Altamachi and Ipiri rivers (both from Cochabamba Department; see Appendix 1). There is also one record from Santa Elena (16.6791°S, 66.6791°W, 600 m, Cochabamba Department, Ayopaya Province; Fig. 9) based on a locality record from Museo de Historia Natural Alcide d Orbigny, Cochabamba, Bolivia. Additionally, the records from Acre, Brazil, of D. kamagarini are also supported by Cochran and Goin (1970) who examined one specimen (WCAB 2511) and report the presence of the conical tubercle on the upper eyelid.

Dendropsophus kamagarini congregates for breeding at temporary and permanent ponds in flooded forest and Terra Firme forest; it is an opportunistic breeder ( Duellman 2005). Adults of both sexes were found at night perching on leaves of bushes and trees, on branches and on palm fronds. Males were calling perched from 2?3 m above the water.

Conservation status.

Extent of occurrence (B1) is 637,800 km2. Dendropsophus kamagarini occurs in the following protected areas from Peru: Otishi National Park, Megantoni National Sanctuary, Amarakaeri Communal Reserve, Manu National Park, Tambopata National Reserve and Bahuaja-Sonene National Park, and protected areas from Bolivia: Manuripi-Heath Amazonian Wildlife National Reserve and Isiboro Secure National Park and Indigenous Territory. Because its distribution range is large and occurs in several protected areas we suggest that D. kamagarini is assigned to the Least Concern category, following IUCN (2001) criteria.

Remarks.

The specimens from Cochabamba Department (Appendix 1) are assigned as referred specimens because we lack genetic data. Marquez et al. (1993) report a maximum SVL = 24.6 for males from Puerto Almacen. This value is slightly above the maximum SVL of males of D. kamagarini (see Table 3). Marquez et al. (1993) also report the dominant frequency range of the advertisement calls (2476 3144 Hz), which is lower than the dominant frequency range of D. kamagarini (3164.1?4306.6 Hz). Therefore, further data is needed to determine the status of that population. We tentatively assign those specimens to D. kamagarini as referred material. Schluter (1979) described the advertisement calls of males from Panguana (Huanaco Department, Peru; Fig. 9), where he reported a dominant frequency range of 3200 4700 Hz and a call duration less than 0.2 s. The frequency range from Panguana is relatively closer to the range of D. kamagarini (3164.1?4306.6 Hz) and D. kubricki sp. n. (3542.2?4394.5 Hz); however, the call duration (less than 0.2 s) is within the range of calls of D. kamagarini (0.09?0.2 s) while the maximum value (0.3 s) of call duration of D. kubricki sp. n. exceeds the call duration reported by Schluter (1979). Thus, we consider the population from Panguana as an unconfirmed register of D. kamagarini unless specimen examination demonstrates otherwise. The population from Rio Madeira (Rondonia State, Brazil) is also unconfirmed until specimens are examined.