Chiasmocleis hudsoni Parker, 1940

Peloso, Pedro L. V., Sturaro, Marcelo José, Forlani, Mauricio C., Gaucher, Philippe, Motta, Ana Paula & Wheeler, Ward C., 2014, Phylogeny, Taxonomic Revision, And Character Evolution Of The Genera Chiasmocleis And Syncope (Anura, Microhylidae) In Amazonia, With Descriptions Of Three New Species, Bulletin of the American Museum of Natural History 2014 (386), pp. 1-1 : 46-52

Chiasmocleis hudsoni Parker, 1940 Figures 28–29 , plate 6

Chiasmocleis jimi: ( Caramaschi and Cruz, 2001) . Holotype, MNRJ 14549 , figure 28C–D, new synonymy.

Syncope jimi: ( de Sá et al., 2012) .

Syncope hudsoni: ( de Sá et al., 2012) .

HOLOTYPE (fig. 28A–B): BM 1939.1.1.3; adult male (according to the original publi-

cation: Parker, 1940) in very good state of preservation (examined from photographs).

TYPE LOCALITY: The type locality was given in the original publication as New River, British Guiana —no geographic coor- dinates given ( Parker, 1940). Frost (1985), based on a personal communication from M.S. Hoogmoed, reported that the locality is in SW Suriname. The New River, however, is in an area of territorial dispute (the New River Triangle) between the Co-operative Republic of Guyana (former British Guiana) and the Republic of Suriname (former Dutch Guiana). The issue is unresolved at present, but historical documents indicate the British Guiana should have precedence over the territory ( Donovan, 2003). Although irrelevant to the species distribution, based on the interpretation of ancient and current resolutions (see Donovan, 2003, for a historical perspective), we consider the type locality to be New River, Co-operative Republic of Guyana.

DIAGNOSIS: A small species for the genus; SVL in males 14.1–23.4 mm (N 5 20); in females 17.2–28.4 mm (N 5 40). Body ovoid, robust; head much narrower than body, snout rounded in dorsal and lateral views. Four distinctive fingers; all but FI slightly fringed, less fringed in females; fingers not webbed; FI reduced with a rounded or slightly pointed tip, lacking subarticular tubercle; finger tips of FII–IV rounded, tips of FII and III swollen, may present discs; adpressed FI does not reach subarticular tubercle of FII; adpressed FIV reach middle or distal margin of distal tubercle on FIII; palmar tubercles protuberant, divided; relative finger lengths I,IV,III,II. Five distinctive toes, first slightly reduced; toes slightly fringed, less distinct in females; toes not webbed in either sex; TI usually without subarticular tubercle (limited to a swelling in some specimens but also may be only slightly visible in few others); adpressed TI does not touch subarticular tubercle of TII; adpressed TV does not touch or reaches only up to the middle of the subarticular tubercle of TIV; TII–IV with terminal discs; relative toe lengths I,II,V,III,IV. Some males with few well-developed dermal spines on chin. Color pattern given in under the variation section.

VARIATION: Ventral pattern (throat, chest, and belly) varies between almost completely unpigmented (fig. 29A) to having different amounts of mottling that can extend from the anterior portion of the chin to the hind limbs (fig. 29B–E). Throat is usually more heavily pigmented in males, sometimes completely pigmented. Ventral pigmentation varies from brown to grayish. Most of the variation in this species is with coloration. The rostral region may vary from a completely uniform brown (fig. 29E) to showing a conspicuous pigmentation of orange (fig. 29B, D), cream (fig. 29C, F), or whitish (fig. 29A) extending from the snout to above the eye. In some specimens the colored pigmentation can extend posteriorly to the eye to the inguinal region (fig. 29B–D) becoming more (fig. 29C) or less (fig. 29B, D) faint posteriorly. Dorsal surface of the hind limbs and sometimes the posterior surface of the dorsum may show a variable amount of minute spots of mottling that vary in color among white, golden, purple, and bright orange (fig. 29).

Some males possess few, but large, dermal spines on the chin.

CALL AND TADPOLE: The advertisement call and a sporadic call of Chiasmocleis hudsoni were described by Rodrigues et al. (2008). The advertisement calls described here (fig. 30) are based on the combined calls of three specimens each belonging to a different population, including one specimen also analyzed by Rodrigues et al. (2008). The call is composed of a repetitive series of multipulsed notes. An introductory note was observed in three calls, with more pulses per note (mean 17.3 ± 2.6 pulses per note, 15–20, N 5 3) and longer duration (427.3 ± 81.6 ms, 360.0–518, N 5 3) than subsequent call notes. The introductory note had a mean dominant frequency of 4249.2 ± 263.1 Hz (3962.1– 4478.9, N 5 3), and pulse duration was 7.6 ± 1.8 ms (4.0–11.0, N 5 50). The chorus notes are shorter (mean 5.6 ± 0.6 pulses per note, 5–10, N 5 1108), emitted at a rate of 498.0 notes/min. Mean note duration was 95.4 ± 2.2 ms (7.0–19.8, N 5 1108) and mean interval between notes was 24.8 ± 3.9 ms (15.0–72.0, N 5 1106). Mean dominant frequency was 4845.2 ± 379.0 Hz (3962.1– 6373.8, N 5 1108), and the pulse duration was 7.2 ± 2.9 ms (2.0–14.0, N 5 357). Harmonics could be observed in one call, one with a lower frequency than the dominant frequency (2584.0 ± 114.3 Hz, 1894.9– 2756.2, N 5 51) and two with frequencies higher than the dominant.

The sporadic call is also composed of a repetitive series of multipulsed notes (mean 11.8 ± 4.7 pulses per note, 7–30, N 5 107) emitted at a rate of 294.5 notes/minute. Mean note duration was 158.3 ± 27.8 ms (121.0– 292.0, N 5 108) and mean interval between notes was 32.3 ± 9.0 ms (22.0–78.0, N 5 105). Mean dominant frequency was 4726.1 ± 928.5 Hz (3789.8–6373.8, N 5 108), and the pulse duration was 6.8 ± 1.5 ms (3.0– 12.0, N 5 282).

The tadpole of Chiasmocleis hudsoni was described by Rodrigues et al. (2008) and the external morphology is similar to that of other tadpoles described in the genus. The absence of an arc shape around the interocular region, a light line between the eyes, and a flagellated tail tip differentiate the tadpole of C. hudsoni from those of C. royi ( Schlüter and Salas, 1991) .

REMARKS: The status of Chiasmocleis jimi Caramaschi and Cruz, 2001 . Caramaschi and Cruz (2001) described C. jimi based on a series of preserved specimens from Humaitá, Amazonas, and Parque Nacional da Amazônia, Pará, both in Brazil. Caramaschi and Cruz (2001) likely did not examine any specimens of C. hudsoni — no list of specimens examined is provided—and therefore based their comparisons solely on the description by Parker (1940). The authors considered C. jimi to differ from C. hudsoni by the swollen tips of fingers III and IV and toes II–V and by color pattern ( Caramaschi and Cruz, 2001: 6). We find that additional discussion of both of these characters is warranted.

Swollen digital tips. Caramaschi and Cruz (2001) argue that ‘‘tips of all digits not expanded in the other [ Chiasmocleis anatipes , C. bassleri , C. hudsoni , C. shudikarensis , C. ventrimaculata ] species,’’ but this statement is inaccurate. The original descriptions of C. anatipes , C. bassleri , C. hudsoni , C. shudikarensis all report discs on at least some digits ( Parker, 1940; Dunn, 1949; Walker and Duellman, 1974). This was confirmed by our observations of larger series of specimens, including a large series of specimens of both C. hudsoni and C. jimi (including both holotypes). We found no differences in the morphology of hands and feet of the types of C. hudsoni and C. jimi (fig. 28).

Color in life. The description of the color in life of Chiasmocleis jimi was based on field notes by Celso Morato de Carvalho ( Caramaschi and Cruz 2001: 7). Considering only the original descriptions of both species ( Parker 1940; Caramashi and Cruz, 2001), they can be distinguished only by (1) ‘‘dorsum purple brown with some fine lighter stipplings white forming an indefinite light zone from the tip of snout above canthus rostralis, along the edge of upper eyelid… flanks and limbs with large areas of light pink stippling’’ in C. hudsoni ( Parker, 1940) , while ‘‘dorsum of body, arms and legs uniform reddish brown with minute irregular white dots’’ in C. jimi ( Caramaschi and Cruz, 2001) ; (2) ‘‘under surfaces white with brown stippling on gular region’’ in C. hudsoni ( Parker, 1940) , while ‘‘ventrolateral region and venter cream, heavily grayish spotted’’ in C. jimi ( Caramaschi and Cruz, 2001) . Apparently the specimen described by Carvalho lacks the ‘‘light zone on the snout’’ (hereinafter, white snout). Color pattern is a variable character and examination of recently collected specimens assigned to both C. jimi or C. hudsoni showed a great degree of variation in the color of live specimens and that the snout may or not be white (pl. 6). The ventrolateral and ventral regions of a C. jimi population from Parque Nacional do Amazonas, Pará, Brazil (where some of the paratypes were collected), are brownish and

TABLE 9 Uncorrected pairwise distances between 16S sequences of Chiasmocleis hudsoni

not grayish (M.S. Hoogmoed, field notes), therefore agreeing with the description of C. hudsoni by Parker (1940).

Advertisement calls. The call of Chiasmocleis hudsoni was described by Rodrigues et al. (2008) from Reserva Florestal Adolpho Ducke, in Manaus, state of Amazonas, Brazil. The authors recognized two call types for C. hudsoni , and named them an advertisement call and a sporadic call ( Rodrigues et al., 2008). We had access to two calls of Chiasmocleis from Rondônia, Brazil, that are referable to C. jimi (based on the original description of the species). In the recording, we detect both the advertisement and sporadic call types and all acoustic parameters are very similar to those of C. hudsoni from Amazonas ( Rodrigues et al., 2008). Unfortunately, no calls of topotypes of C. jimi are available.

Phylogenetic evidence. The phylogenetic analysis did not recover monophyly of specimens identified (by the collectors) as Chiasmocleis jimi or C. hudsoni . Despite uncertainty about the relationships among populations, together all specimens form a well-corroborated clade, sister to C. haddadi , sp. nov. The amount of uncorrected genetic distance between populations is considerably variable (0 % –11.4 %), with up to 2.3 % distance between syntopic species. Genetic distance values between all specimens of C. hudsoni included in the phylogenetic analysis are given in table 9.

THE STATUS OF CHIASMOCLEIS JIMI : Given the above discussion and character analyses, we feel that the present evidence is overwhelming and our conclusion is that C. jimi Caramaschi and Cruz, 2001 , must be regarded a junior synonym of C. hudsoni Parker, 1940 .

DISTRIBUTION (fig. 31): Most of the Amazon basin in Brazil, west of the Rio Tocantins. Although we have not examined specimens from several populations in the Guiana Shield countries, there are known records of the species in Colombia, Venezuela, Guyana, Surinam, and French Guiana ( Barrio-Amorós and Schargel, 2003; Rodrigues et al., 2004a). Possibly present in Peru, although we are unaware of any records.

Chiasmocleis magnova Moravec and Köhler, 2007 Figures 32 , plate 6G–H

Syncope magnova: ( de Sá et al., 2012) .

HOLOTYPE: MHNSM 19993 , not examined.

TYPE LOCALITY: The type locality is 31 km on the road from Iquitos to Nauta, ca. 40 km straight SW of Iquitos (04 ° 009 S, 73 ° 269 W), Departamento Loreto, Peru.

DIAGNOSIS: A small species for the genus; SVL in females 16.7–18.3 mm ( Moravec and Köhler, 2007). We had no access to male specimens. Body slender, snout rounded in dorsal and lateral views. FI much reduced without subarticular tubercle, tip slightly pointed; FII and FIII well developed with hardly visible subarticular tubercles, one on FII and two on FIII; FIV reduced, without subarticular tubercles; fingers only slightly fringed according to Moravec and Köhler (2007), not fringed in the sole specimen examined (AMNH 103550); palmar tubercles not present; relative finger lengths I,IV,II,III. Five distinctive toes present; TI reduced, tip does not reach tubercle of TII by a wide margin; toes only slightly fringed, not webbed; tips of TI pointed, TII–IV rounded with terminal discs present. Relative toe lengths I,II,V,III,IV. Dermal spines present on dorsum, posterior surface of thighs, toes, and tarsus; absent on fingers. No femoral stripe present. Venter (belly and undersurfaces of thighs) beige with small light spots. Few large unpigmented eggs ( Moravec and Köhler, 2007).

CALL AND TADPOLES: Unknown.

REMARKS: Moravec and Köhler (2007), when describing the species, suggested that this species might be associated with the genus Syncope (all former members of Syncope are now included in our Chiasmocleis hudsoni clade). This was based mostly on the basis of the presence of few large eggs (a condition also present in Syncope: Krügel and Richter, 1995 ; Silva and Meinhardt, 1999) and the significant digit reduction.

In our analysis, the sole specimen of Chiasmocleis magnova (sequence from de Sá et al., 2012) is well supported as the sister to a clade containing C. antenori , C. carvalhoi , and C. tridactyla while they all form the sister clade to C hudsoni plus C. haddadi , sp. nov. Studies on the ecology of C. magnova can provide useful insights on the evolution of the group as a whole, as it seems C. magnova can be a transitional form between the more general Chiasmocleis body plan, and the miniaturized C. antenori , C. carvalhoi , and C. tridactyla .

DISTRIBUTION (fig. 27): Known from the vicinities of the type locality, in Iquitos, Departamento Loreto, Peru.

Figures

Fig. 28. Holotypes of (A–B) Chiasmocleis hudsoni (BMNH 1939.1.1.3: photos: G. Bitencourt), in dorsal and ventral views respectively; and (C–D) Chasmocleis jimi (MNRJ 15459: photos I. Nunes), in dorsal and ventral views respectively.

Fig. 29. Variation of ventral color pattern in Chiasmocleis hudsoni. (A–C) Parque Nacional da Amazônia, Itaituba, Pará, Brazil (MPEG 18479, MPEG 18511, and MPEG 18554, respectively). (D) Berbice River 18 mi SW Kwakwani, Guyana (AMNH 166437). (E) Estação Ecológica Grão Pará, Alenquer, Pará, Brazil (CN 1881).

Fig. 32. Chiasmocleis magnova (AMNH 103550) from Iquitos, Peru, in (A) dorsal, and (B) ventral views. SVL 5 16.7 mm.