Chiasmocleis royi, Peloso & Sturaro & Forlani & Gaucher & Motta & Wheeler, 2014

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 : 69-76

Chiasmocleis royi , new species Figures 46–47 , plates 12–13

HOLOTYPE (fig. 46): USNM 343266 (field number USNM-FS 153416 ), an adult male, collected by R. B. Cocroft on December 12 1990.

TYPE LOCALITY: Explorer’s Inn , 30 km southwest of Tambopata Reserve (12 ° 509S / 69 ° 179W; 280 m. a.s.l.), Puerto Maldonado, Departamento Madre de Dios, Peru .

PARATYPES: USNM 269000 , adult male, collected by R. B. Cocroft and K. Hambler on 12 July 1986 ; USNM 269001 , adult male ,

collected by K. Hambler; USNM 346267– 346268 , two adult males, collected with the holotype ; USNM 343033 , adult female, collected by R.W. McDiarmid , in January 10, 1989 ; USNM 247432 , juvenile, anonymous native inhabitant (information taken from label), in August 28, 1983 ; USNM 247433 , juveniles, collected by R. B. Cocroft, on September 13, 1984. All paratypes collected at type locality .

Additional referred (nontype) material listed in appendix 1.

DIAGNOSIS: A medium-sized Chiasmocleis ; SVL in males 18.8–23.1 mm (N 5 24); females 20.7–29.1 mm (N 5 16). Body ovoid and relatively slender; snout rounded in dorsal and lateral views. Four distinctive fingers present; all but FI fringed in males, less so in females; fingers not webbed; FI well developed with a subarticular tubercle usually present between the proximal phalanges; distinct subarticular tubercles present on all fingers; palmar tubercles protuberant, divid- ed; relative finger lengths I,II,IV,III. Five distinctive, well-developed toes present; toes fringed, less so in female; toes basally webbed in both sexes; TI with a distinct welldeveloped subarticular tubercle; adpressed TI does not reach or barely reaches subarticular tubercle of TII; adpressed TV does not reach or reaches only to the middle of the middle subarticular tubercle of TIV; TII–IV with terminal discs, usually more developed in females, but also present in males; relative toe lengths I,II,V,III,IV. Males with dermal spines on fingers and toes; both sexes with dermal spines on dorsum and toes, more numerous and more developed in males. Males with few spines on anterior portion of chin (may be absent in some specimens). Vocal sac well developed, black, directed anteriorly when males are actively calling (pl. 12G). The femoral line is always present.

COMPARISONS: Chiasmocleis royi differs from C. antenori by having four externally evident fingers (FI not evident externally in C. antenori ), five externally evident toes (TI not evident), rounded toe tips (toe tips pointed), and a reticulated venter (dark with scattered light spots). It differs from C. albopunctata by the absence of white blotches on the snout and dorsum (present in C. albopunctata ), its light venter with dark mottling (dark with white dots and blotches in C. albopunctata ), and its advertisement call (see text for details). It differs from C. anatipes by having basal webbing on toes of males (extensive webbing in males C. anatipes ) and by its mottled venter (dark spots in C. anatipes ). The new species is distinguished from C. avilapiresae by its smaller size (mean SVL of C. avilapiresae 32.0 mm in females), its having basally webbed feet in males (extensively webbed in C. avilapiresae ), a mottled venter (usually blotched in C. avilapiresae ), and a slender body (robust in C. avilapiresae ), and by its advertisement call (table 2). The new species differs from C. bassleri in having a mottled venter (large dark spots over a light venter in C. bassleri ), by the absence of an inguinal blotch (present in C. bassleri ) and the presence of the femoral line (absent in C. bassleri ), and by its advertisement call (table 2). The new species differs from C. carvalhoi in having four externally evident fingers (FI not evident externally in C. carvalhoi ) and five externally evident toes (TI not evident). Chiasmocleis royi differs from C. devriesi by its smaller size (SVL of the holotype C. devriesi 42.2 mm), its mottled venter (large dark spots over a light venter in C. devriesi ), presence of a femoral line (absent in C. devriesi ), and its slender body (robust in C. devriesi ). It is distinguished from C. hudsoni by a round finger I tip (tip slightly pointed in C. hudsoni ), the presence of a femoral line (absent in C. hudsoni ), its having a vocal sac protruding forward when calling (vocal sac round, not protruding forward in C. hudsoni ), and by its advertisement call (table 2). Chiasmocleis royi differs from C. magnova in having all fingers fully developed (fingers I and IV reduced in C. magnova ) and by containing many small, pigmented, eggs in oviduct (few large, unpigmented, eggs in C. magnova ; Moravec and Köhler, 2007). Chiasmocleis royi is distinguished from C. shudikarensis by its basal webbing in toes of males (extensive webbing in C. shudikarensis ), the absence of an inguinal blotch (present in C. shudikarensis ), a vocal sac protruding forward when calling (vocal sac round, not protruding forward in C. shudikarensis : see pl. 14A–B), and its advertisement call (table 2). Chiasmocleis royi differs from C. supercilialba by the absence of inguinal blotches (present in C. supercilialba ), by the mottled venter (with large dark spots), and by its advertisement call (table 2). Finally, it differs from C. tridactyla in having four externally evident fingers (FI not evident externally in C. tridactyla ), five externally evident toes (TI not evident), rounded toe tips (toe tips pointed), and a reticulated venter (dark with scattered light spots).

The new species has been historically confused with Chiasmocleis ventrimaculata ( Cocroft and Hambler, 1989; De la Riva, 1995; Schlüter, 2005; Peloso and Sturaro, 2008), from which it differs by having a smaller, more slender body (usually more robust in C. ventrimaculata ), ventral pattern usually reticulated, becoming more densely reticulated on ventral thigh (brown spots in C. ventrimaculata ), longer finger IV, with tip reaching distal tubercle of finger III (finger shorter in C. ventrimaculata , finger tip does not pass the distal margin of the proximal tubercle on finger III), and a femoral line present (femoral line not visible in the photos of the holotype and lacking according to M.S. Hoogmoed personal notes: ‘‘back of thighs without light line’’; also lacking in all other specimens examined).

DESCRIPTION OF THE HOLOTYPE (fig. 46): Body ovoid, relatively slender. Head short, wider than long (HW 1.2 × HL); head slightly narrower than body; snout rounded in dorsal and lateral profiles; nostrils not protuberant, positioned anterolaterally, directed laterally. IOD 2.2 × IND. Canthus rostralis poorly defined, round in cross section; loreal region slightly convex. Eyes small. No occipital fold present, supratympanic fold visible; tympanum not apparent externally. Upper jaw projecting beyond lower; lower lip with truncate, trilobed anterior margin; few spicules on chin present; tongue large, elongated, with free lateral and posterior edges; vocal slits present, extended through most of the extent of the jaw, choanae small, rounded, widely separated, just anterior to eye; vomerine teeth absent. Vocal sac large and prominent, dark colored, directed forward.

Forelimb slender; all fingers developed, nearly round in cross section; no webbing between fingers; relative finger lengths I,IV,II,III; tips rounded, without discs. Subarticular tubercle usually not visible in FI; subarticular tubercles on remaining fingers present but not very developed and not prominent; one subarticular tubercle on FII and FIV, two on FIII; proximal tubercle more prominent than distal, which is hardly visible; no supranumerary tubercles; palmar tubercle not visible, thenar tubercle present, large, round not very prominent; outer metacarpal tubercle present. All fingers with many dermal spicules laterally.

Legs short (combined THL, TBL and FL 1.57 × SVL); relatively robust, lacking tubercles, tibial and tarsal ridges or warts; toes not webbed (a very rudimentary vestige of web between TIII–TIV and TIV–TV is present and may be considered as basal webbing by some observers); TI weakly developed (tip fails to reach subarticular tubercle of TII), without a visible subarticular tubercle; toe tips rounded with small discs on all but TI. Subarticular tubercles present in all toes except TI; no outer metatarsal tubercle. TI barely reaches proximal margin of the tubercle of TII; TV reaches distal margin of proximal subarticular tubercle of TIV; relative toe lengths I,II,V,III,IV. Toes with few lateral dermal spicules.

Skin mostly smooth dorsally and ventrally, with scattered spines, especially on dorsum, hind limbs, fingers, and toes.

MEASUREMENTS OF THE HOLOTYPE: SVL 20.6 , HL 4.0, HW 5.3, ED 1.5, IOD 3.2, IND 1.4, END 1.4, THL 9.0, TBL 8.4 , FL2 13.5, 4TD 0.7.

VARIATION: Throat in males is dark brown or black and a vocal sac can be easily observed in adult male specimens. Ventral patterns usually consist of dense grayish or dark brown vermiculations against a light background (figs. 46, 47, pl. 12B), but in some specimens it consists of numerous small dark spots and stains (fig. 47B).

Color in life seems to be variable. Dorsal color varies from brown to blackish or reddish (pl. 12). Dorsum is not uniformly colored and may show white, orange, or black mottling. A middorsal line is present in most specimens examined, but it may be absent, while the femoral line is always present. Dorsal portion of forelimbs either has the same overall pattern as dorsum, or is either orange or reddish.

ETYMOLOGY: The specific epithet is used as a noun in the genitive case and honors Roy McDiarmid, friend and researcher at the USGS Patuxent Wildlife Research Center and National Museum of Natural History, Washington, DC. Roy has been actively studying frogs in South America for a long time. He was the first one to call the attention of P.L.V.P. to the possibility of a species complex within Chiasmocleis ventrimaculata and continuously encouraged us to describe this new form, which he first collected, along with other colleagues, over 20 years ago.

CALL AND TADPOLES: Schlüter (2005) described a call of Chiasmocleis ventrimaculata from Panguana, Madre de Dios, Peru. The specimens are actually representatives of C. royi . The range of the dominant frequency is 5000–7000 Hz. We had access to additional calls of the species, deposited at the USNM collection, made at Tambopata, Peru, by R. Cocroft (fig. 48). The call is composed of a repetitive series of multipulsed notes (mean 14.6 ± 0.7 pulses per note, 12–16, N 5 109) emitted at a rate of 503.2 notes/minute. Mean note duration is 89.5 ± 5.2 ms (77.0–104.0, N 5 109) and mean interval between notes 21.9 ± 4.4 ms (15.0–41.0, N 5 107). Pulse duration was 4.0 ± 0.8 ms (3.0–7.0, N 5 201). Mean dominant frequency, belonging to the second harmonic, was 7629.1 ± 1204.0 Hz (5512.5–13953.5, N 5 109). The fundamental frequency is 3729.9 ± 526.1 (3273.0–4823.4). Two harmonics with frequencies higher than the dominant frequency could be seen.

Tadpoles are unknown.

REMARKS: Chiasmocleis royi has been historically confounded with C. ventrimaculata ( De la Riva, 1995; Morales and McDiarmid, 1996; Peloso and Sturaro, 2008; Von May et al., 2009), and most of the data on ecology published on the latter actually refers to the new taxon named here ( Cocroft and Hambler, 1989; Schlüter and Salas, 1991). The two are not, to our knowledge found in sympatry (fig. 41) with C. ventrimaculata showing a more septentrional distribution than C. royi .

Genetic distances between the three specimens of C. royi included in the phylogenetic analysis are given in table 13.

DISTRIBUTION (fig. 41): Known from eastern and southern Peru, northern Bolivia, and western Brazil.

DISCUSSION SYSTEMATICS

We provide an overview of the current knowledge and taxonomy of Chiasmocleis in the Amazon and Guiana Shield regions. Given the geographical scope we attempted to cover, we regret that many topics and populations could not be included. Nonetheless, this is, by far, the most complete sampling for Chiasmocleis systematics in the study area. Our findings are consistent with the recognition of 16 species: C. albopunctata , C. anatipes , C. antenori , C. avilapiresae , C. bassleri , C. carvalhoi , C. devriesi , C. haddadi (described and named here), C. hudsoni , C. magnova , C. papachibe (described and named

TABLE 13

Uncorrected pairwise distances between 16S

sequences of Chiasmocleis royi

here), C. royi (described and named here), C. shudikarensis , C. supercilialba , C. tridactyla , and C. ventrimaculata . Chiasmocleis jimi is considered a junior synonym of C. hudsoni . See table 14 for a summary of all taxonomic rearrangements proposed in the present study.

A few new questions and problems arose during this study, and we particularly point to the problematic taxonomy of Chiasmocleis bassleri (and its putative relative, C. supercilialba ), and to the need for further sampling and ecological studies in the C. hudsoni clade. It is extremely important that future work on Chiasmocleis account for variation among populations and that effort is directed to the collection of tadpoles, the recording of advertisement calls, documentation of reproductive behavior, and the collection of tissue samples to improve coverage of populations in phylogenetic studies. These data are essential for further exploration of systematics, geographical variation, and character evolution in the group.

The Chiasmocleis bassleri Clade; a Complex of Species?

Although we assign several populations to C. bassleri , this is done tentatively. Some populations referred to C. bassleri remain

TABLE 14

Summary of nominal taxa associated with Chiasmocleis Review of names associated with Chiasmocleis and dealt with in this study. Original author and publication date is given for all specific names related to current and former members of Chiasmocleis is given, followed by combination after the review and a justification of taxonomic action taken, if any.

with their status undefined because our observations, particularly given the degree of morphological variation observed, do not allow reliable conclusions regarding their taxonomic status. Moreover, sampling included in the phylogenetic analysis is too small for any conclusive observations. Here, we briefly comment on some of these populations and highlight the importance of a directed effort to study variation in the C. bassleri complex. Specimens included in what we refer to as the C. bassleri complex are easily recognized by the combination of the following characters: presence of an inguinal blotch; venter white or cream with black or dark brown spots or stains; toes usually not fully webbed (webbing basal or absent); and femoral line absent. As described earlier (variation section under C. bassleri ), the dorsal and ventral color pattern vary extensively (see fig. 23 and pl. 4), and some variation in body shape and measurements also exists (e.g., relative lengths of FIII and IV, and toes I and V; fig. 23). Populations from southern Brazilian Amazonia (Amazonas, Mato Grosso), and some from Colombia and Ecuador show a much more reticulated venter than other populations, including the holotype, which has large black spots on the venter ( Dunn, 1949). The variable nature of this character (as observed in sympatric specimens from Peru) complicates any accurate assessments. It is possible that distinct species are syntopic in western Amazonia, further complicating the delimitation of species, but our current approach could not detect any obvious pattern.

Our phylogenetic analysis recovered two well-defined clades within C. bassleri (with arguably additional clades found within them; fig. 7). Genetic distances in the 16S between the specimens of C. bassleri are, however, relatively low (up to 4.5 %: table 7).

A more detailed, integrative approach to taxonomy (including additional morphological, acoustic, and molecular data) is needed to resolve the taxonomic status of the populations here assigned to Chiasmocleis bassleri and C. supercilialba , as well as of additional populations for which we examined a very limited amount of material (i.e., from Colombia and Ecuador).

When describing Chiasmocleis supercilialba, Morales and McDiarmid (2009) proposed the recognition of a ‘‘ Chiasmocleis bassleri group’’ on the basis of ‘‘flanks with one or two dark spots, but if the spots are not present, the flanks show a fine clear line at the junction of the ventral and dorsal pattern coloration; ventral patters with dark spots on a light background.’’ We find the diagnosis provided by Morales and McDiarmid (2009) for the C. bassleri species group inadequate. By their definition, C. shudikarensis could be included in the group on the basis that specimens show one dark spot in the inguinal region. The line at the juncture of the ventral and dorsal pattern coloration is what we refer to as a split stripe, but several specimens of C. bassleri have neither spots nor a split line on their flanks.

We were unable to sample C. supercilialba for our phylogenetic analysis, and although we think that a close relationship exist between C. bassleri and C. supercilialba , kinship can only be assumed. Nonetheless, the diagnostic characters suggested by Morales and McDiarmid (2009) do not hold, given the material we analyzed.

Figures

Fig. 46. Holotype of Chiasmocleis royi, sp. nov. (USNM 343266), in (A) dorsal and (B) ventral views. SVL 5 20.6 mm.

Fig. 47. Variation of ventral color pattern in Chiasmocleis royi, sp. nov. (A) Male, from Parque Ambiental Chico Mendes, Rio Branco, Acre, Brazil (UFAC-RB 3539). (B) Male, paratype, from Puerto Maldonado, Madre de Dios, Peru (USNM 343268, paratype). (C–D) Females, Guajará-Mirim, Rondônia, Brazil (CHUNB 23547, 25555, respectively).