Dendropsophus parviceps (Boulenger, 1882)

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 : 33-38

Dendropsophus parviceps (Boulenger, 1882) Figs 1, 6, 7A, 8

Hyla parviceps Boulenger, 1882: 393. Holotype BMNH 1947.2.13.51, an adult female from Sarayacu, Pastaza Province, Ecuador.

Hyla parviceps Duellman and Crump 1974: 19; Duellman 1978: 156.

Dendropsophus parviceps Faivovich et al. 2005: 93.

Diagnosis.

Throughout the species account, coloration refers to preserved specimens unless otherwise noted. Dendropsophus parviceps is characterized by: (1) small size, mean SVL 16.4 mm in males (range 14.3 18.7; n = 65), 22.5 mm in females (range 20.3 24.4; n = 30); (2) throat sexually dimorphic, dark flecks posteriorly in males vs. white blotch with two or three longitudinal stripes or without stripes posteriorly in females (Fig. 8); (3) snout truncate in dorsal and lateral views, slightly inclined posteroventrally in lateral view; (4) nostrils slightly prominent; (5) tympanum visible, concealed posterodorsally, tympanic membrane differentiated and annulus evident; (6) conical tubercles on upper eyelid absent; (7) thoracic fold absent; (8) ulnar tubercles and outer tarsal tubercles indistinct; (9) axillary membrane present; (10) skin on dorsal surfaces smooth with scattered small tubercles; skin on chest areolate; skin on belly, posterior surfaces of thighs, and subcloacal area coarsely areolate; skin on throat and other surfaces smooth; (11) dark brown markings on dorsum (Fig. 8); (12) thenar tubercle is distinct; (13) hand webbing formula II11/2 2III2- 2-IV, feet webbing formula I1-?2-II1-?2-III1- 2IV2?1-V; (14) in life, dorsal surfaces brown, tan or grayish tan; (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 preservative); (16) one suborbital white bar present both in life and preservative; (17) thighs are black to dark brown with two or three white spots on the anterodorsal surfaces both in life and preservative; (18) iris in life is creamy white to reddish brown with brow or dark brown reticulations.

Comparisons with other species.

Dendropsophus parviceps is most similar to D. kamagarini sp. n. and D. kubricki sp. n. The three species differ from other species of the D. parviceps group sensu Fouquet et al. 2015 (characters of other species of the group in parenthesis) by lacking dorsolateral light stripes [present in D. bokermanni (from Goin 1960) and in D. brevifrons (see Duellman and Crump 1974 and Read and Ron 2011)] and having, in life, an orange or amber blotch on the proximal ventral surface of shanks and under arms, from the axillae to near the elbow [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 parviceps is also similar to D. pauiniensis (Heyer, 1977), but it can be distinguished by the presence of an orange or amber blotch on the proximal ventral surfaces of shanks in life (absent in D. pauiniensis ).

Dendropsophus parviceps , D. kamagarini sp. n., and D. kubricki sp. n. further differ from species of the D. parviceps group (traits of other species of the D. parviceps group in parenthesis) as follows: from D. koechlini by having a white chest both in life and preserved [white with black flecks both in life and preserved (see Duellman and Trueb 1989)]; from D. bokermanni , D. brevifrons , D. counani , and D. frosti by having a mottled ventral coloration both in life and preserved [plain coloration both in life and preserved in D. bokermanni (from Goin 1960), in D. brevifrons (from Duellman and Crump 1974), in D. counani (from Fouquet et al. 2015), and in D. frosti (from Motta et al. 2012)]; from D. bokermanni , D. brevifrons , and D. counani by having a single suborbital bar [two suborbital bars (data of D. bokermanni and D. brevifrons from Duellman and Crump 1974, and of D. counani from Fouquet et al. 2015)] and two or three white spots on the anterior dorsal surfaces of the black thighs in life [cream or yellow spots in life (data of D. bokermanni and D. brevifrons from Duellman and Crump 1974, and of D. counani from Fouquet et al. 2015)]. The absence of canthal and rostral stripes also differentiates D. parviceps , D. kamagarini sp. n., and D. kubricki sp. n. from D. bokermanni , D. brevifrons , D. frosti , and D. koechlini [both stripes present in D. bokermanni and D. brevifrons (data of both species from Duellman and Crump 1974), canthal stripes in D. frosti (see Motta et al. 2012), and rostral stripes in D. koechlini (see Duellman and Trueb 1989)].

Dendropsophus parviceps differs from both new species by the absence of tubercles on the upper of eyelid (present). Dendropsophus parviceps also differs from D. kamagarini sp. n. and D. kubricki sp. n. by having translucent gray on the ventral surface of the thighs with dark brown flecks posteriorly in males, in life (black posteriorly in males, in life, in D. kamagarini sp. n. and in D. kubricki sp. n.).

Variation.

Morphometric variation is shown in Table 3. Variation in dorsal and ventral coloration of preserved specimens is depicted on Figure 8. Dorsal coloration varies from brown (e.g., QCAZ 52026, 52816) to dark brown (e.g., QCAZ 52755, CORBIDI 1059), gray (e.g., QCAZ 52017), grayish tan (e.g., QCAZ 44441, 51230), or grayish brown (e.g., QCAZ 44736, 52026) with dark brown markings with varying shapes (Fig. 8). The specimens with gray, grayish tan, and grayish brown coloration have scattered iridophores. The dorsum is smooth (e.g., QCAZ 51108, 52755), but some specimens have scattered small tubercles (e.g., QCAZ 53181, CORBIDI 1046).

The chest is white to cream (Fig. 8) with throat and belly varying from creamy white (e.g., QCAZ 51230), grayish brown (e.g., QCAZ 48929, 52017) to dark brown (e.g., QCAZ 44440) with dark brown or black flecks. The subcloacal area is areolate, its coloration is white (e.g., QCAZ 44441, 48929), but in some specimens is dark brown (e.g., QCAZ 52755).

Color in life.

Based on digital photographs (Fig. 6): dorsum varies from brown, tan, grayish tan to reddish brown, some individuals have few scattered dorsolateral dark brown flecks; dorsal markings are dark brown; flanks are white or creamy yellow with black or dark brown diagonal bars; dorsal surfaces of forelimbs and shanks have dark brown transversal bars; anterodorsally, thighs are black or dark brown with two or three white spots. The single suborbital bar is white. The venter is translucent gray mottled with black or dark brown; in some females venter is black; chest is white; in adult males, throat is olive tan mottled with dark brown flecks anteriorly and translucent gray posteriorly; in adult females, throat is grayish tan or olive brown, dark brown, or black anteriorly with a white blotch with stripes posteriorly; the ventral surfaces of the limbs are translucent gray or translucent white, thighs are mottled with dark brown posteriorly; there is one bright orange or amber blotch in ventral surface of shank next to the knee, and in the posterior arm, from the axillae to near the elbow. The iris is creamy white to reddish brown with brown or dark brown reticulations.

Calls

(Fig. 4A?B). Descriptive statistics of acoustic variables are provided in Table 5. Calls from ten individuals were analyzed. Three individuals (two of them unvouchered specimens and QCAZ 52753) were recorded at the type locality, Sarayaku, Pastaza Province, at night, on 6 April 2012 (QCAZ 52753 was recorded at 01:00h, temperature 22.4°C). Three individuals (QCAZ 52820, 52837 and one individual not collected) were recorded at Canelos, Pastaza Province, on 11 April 2012 (QCAZ 52820 recorded at 01:00h, 23.4°C). Two individuals (QCAZ 52017, 52918) were recorded at Rio Verde, Tungurahua Province, on 19 September 2011 (QCAZ 52018, air temperature = 15.6°C). Finally, two individuals, not collected, were recorded at PUCE s Yasuni? Research Station, Orellana Province, on 1 June 2011. We obtained one recording (unvouchered specimen) from the sound archives of Museo de Zoologi?a, Pontificia Universidad Cato?lica del Ecuador, made by Morley Read, at Pompeya-Iro road, km. 38, Yasuni National Park, Orellana Province.

The advertisement call is a pulsed note (Fig. 4A?B). The amplitude increases gradually at the beginning and falls sharply towards the end. The advertisement call may be emitted alone or followed by one or more click notes. However, the click notes occasionally are emitted alone. The click notes may be non-pulsed or pulsed.

Call comparisons between populations. The advertisement calls from Rio Verde separate along PC II from the calls of other populations (Fig. 5; Table 8). Mean dominant frequency is 5364.7 Hz (SD = 167) at Rio Verde and 6498.1 Hz (SD = 239) at the other populations. Mean pulse rate is 86.1 pulses/s (SD = 11.79) at Rio Verde and 127.6 pulses/s (SD = 15.5) at others. Mean rise time is 0.1 (SD = 0.02) and mean advertisement call duration is 0.19 s (SD = 0.04) at Rio Verde, while mean rise time is 0.06 (SD = 0.01) and mean advertisement call duration is 0.12 s (SD = 0.03) at the other populations.

Distribution and ecology.

Dendropsophus parviceps is known from 39 localities in the Ecuadorian Amazon basin (Napo, Orellana, Pastaza, Sucumbios, and Tungurahua provinces; Fig. 9), few localities in the Peruvian Amazon basin at northwest Loreto (Andoas and San Jacinto; Fig. 9), the Colombian Amazon (Rio Apaporis, Vaupes Department, and Ceilan, Caqueta Department; Cochran and Goin 1970; Fig. 9), and northern Brazil (Taracua [= Taracuaca], Rio Uaupes, Amazonas State; Melin 1941; see Remarks section). Elevation range is 151 m (Andoas) to 1600 m above sea level (Rio Verde). Our Colombian records are unverified and are based on Cochran and Goin (1970) who examined three specimens (MLS 54 and MCZ 28058 59) and explicitly mention the absence of tubercles on the upper eyelids. Moreover, the SVL for a gravid female from Ceilan (MLS 54, 21.8 mm) falls outside the known size range of D. kubricki sp. n. and D. kamagarini sp. n. (Table 3). Ecuadorian localities from Sucumbios province are close to the Colombian border further suggesting the presence of D. parviceps in Colombia. In addition, there is an unconfirmed register of D. parviceps from Ramal do Purupuru, km 34 on the BR-319 highway (3.3535°S, 59.8557°W, 35 m, Amazonas State, Brazil; Fig. 9).

Dendropsophus parviceps inhabits Amazonian lower montane forest, Amazonian foothill forest, and Amazonian evergreen lowland rainforest (habitat types based on Ron et al. 2017). Dendropsophus parviceps is an opportunistic breeder and can be found in primary and secondary forest, temporary ponds, flooded areas, swamps, and artificial open areas. Calling activity starts at dusk (17 18h), but it is mainly nocturnal. According to Lynch (2005), D. parviceps is a canopy species that visits the lower forest strata for breeding.

Conservation status.

Its extent of occurrence is 256,944 km2. There is habitat degradation and fragmentation within its distribution as result of human activities, especially cattle rising, agriculture, and oil exploitation. Its presence in artificial open areas suggests that is tolerant of at least some level of habitat modification ( Azevedo-Ramos et al. 2004). Its distribution range is large and includes extensive undisturbed areas (Ministerio de Ambiente Ecuador 2013). Therefore, we propose that D. parviceps should be assigned to the Least Concern category, following IUCN (2001) criteria.

Remarks.

The advertisement call from Rio Verde differs from other population calls (Fig. 5; Table 5). However, low genetic and morphological differences between Rio Verde and the other populations indicate that they are conspecific. The Brazilian record from Tarauaca, Rio Uaupes (Amazonas State) is based on Melin (1941) who reported a juvenile specimen with SVL = 21 mm. This specimen could be an adult male because the throat is mottled with brown, characteristic of all adult males of Dendropsophus parviceps . Nevertheless, the SVL of the male from Taracua falls above the range of variation of males of D. parviceps (14.3?18.7 mm) and it has a thoracic fold (fold absent in D. parviceps ; see above in Diagnosis section). Therefore, the record from Tarauaca requires verification.

The holotype has SVL = 26.5 mm (adult female; Fig. 7A). This value is above the range of variation of females of D. parviceps reported in Table 3 (20.3?24.4 mm). To confirm that the holotype falls within the range of variation of D. parviceps from Ecuador, we measured the SVL of the largest adult females from the QCAZ collection. We found three specimens with size close to the holotype: QCAZ 4340 (SVL = 26.13 mm) from La Selva (Sucumbios Province), QCAZ 27028 (SVL = 26.03 mm) from Ahuano (Napo Province), and QCAZ 59772 (SVL 26.26 mm) from Comunidad Zarentza (Pastaza Province; Appendix 1). Although the holotype is the largest specimen known for D. parviceps , other specimens are smaller by just ~1% of SVL. Other characteristics of the external morphology of the holotype fall within the known variation of the Ecuadorian populations confirming that they are conspecific (Figs 7A, 8).