Craugastor bitonium, Jameson & Streicher & Manuelli & Head & Smith, 2022

Jameson, Tom J. M., Streicher, Jeffrey W., Manuelli, Luigi, Head, Jason J. & Smith, Eric N., 2022, Miniaturization in Direct-Developing Frogs from Mexico with the Description of Six New Species, Herpetological Monographs 36 (1), pp. 1-48 : 13-16

Craugastor bitonium sp. nov.

Holotype. — UTA A-64254 (field ID: JAC 22117; Fig. 22A ), adult female from road between Yerba Santa and Yextla (HWY 196), Guerrero, Mexico, 17.52666°N, 99.9579°W, 2071 m, collected by J.A. Campbell and colleagues on 10 June 2002 .

Paratypes (5). —MZFC-HE-35600–01 and UTA A- 66117– 18 adult females, and UTA A-66119 adult male ( Fig. 22B–D ), all same collection data as holotype .

Diagnosis. —A species of Craugastor distinguished by the following combination of characters: (1) small adult size (maximum SVL ¼ 16.7 mm); (2) full ossification of skeletal elements in adults; (3) absence of posterolateral projection of frontoparietal; (4) absence of vomerine odontophores; (5) presence of raised tubercles on eyelids; (6) supratympanic fold absent or poorly developed; (7) face flank barred or with supralabial pale stripe, and with or without dark canthal stripe; (8) single postrictal tubercle; (9) gular region peppered with melanocytes; (10) dorsal surface two-toned, usually with a dark suprascapular ^ shape, or almost unicolored; (11) pale or ground color middorsal ridge; (12) scattered fine tubercles on dorsum; (13) body flank barred darker anteriorly, slightly shagreened to smooth; (14) inguinal glands present and axillary glands absent in adults; (15) when leg adpressed to body, heel reaches middle of eye to slightly beyond snout; (16) outer tarsal ridge with 1–6 small mostly round tubercles, no raised fringe; (17) finger and toe tips round, slightly lanceolated, slightly expanded; (18) inner metatarsal tubercle larger than outer metatarsal tubercle.

Comparisons. — Craugastor bitonium can be differentiated from C. mexicanus , C. montanus , C. omiltemanus , and C. saltator by their large adult body sizes of SVL> 20 mm (<20 mm in C. bitonium ), the presence of vomerine odontophores (absent in C. bitonium ), and the presence of three palmar tubercles (one palmar tubercle in C. bitonium ). Craugastor bitonium can be differentiated from C. candelariensis , C. cueyatl , C. hobartsmithi , and C. portilloensis by the presence of metatarsal tubercles of similar sizes (different sizes in C. bitonium ). Craugastor bitonium can be differentiated from C. rubinus by the presence of posterolateral projections of the frontoparietal (absent in C. bitonium ). Craugastor bitonium can be differentiated from C. polaclavus by its shorter eye–nostril distance with an eye–nostril distance 9–10% SVL in C. bitonium and 10–13% SVL in C. polaclavus . Craugastor bitonium is most similar to C. pygmaeus (in morphology, osteology, and genetic distance), but may be differentiated from this taxon by the condition of the outer tarsal ridge; 1–6 small tubercles in C. bitonium versus no tubercles (¼ smooth) in C. pygmaeus .

Holotype description. — Holotype small female with unpigmented developing ova ( SVL ¼ 15.8 mm); snout rounded and short (0.9 mm naris–snout; 6% SVL); short eye–nostril distance (1.42 mm; 9% SVL); tympanum 1.4 mm (8.9% SVL); small supratympanic fold terminating in shoulder tubercle; finger length formula III < IV < II <I; single palmar tubercle; single prepollical tubercle; subarticular tubercles present on all fingers; no supernumerary tubercles present on hands; toe length formula IV < III < V < II <I; innermetatarsal tubercle larger than outer metatarsal tubercle; subarticular tubercles present on all toes; supernumerary tubercles present on plantar surface; small dark supracloacal fold present; white lip bar in life ( Fig. 22 A ), still evident in preservative ( Fig. 19 A ); 2–3 incomplete bands on each arm; one leg removed for genetic analysis and 4 bands on thigh of remaining leg; dorsum brown and mottled on head and anterior-most third of body, eclipsed by lighter coloration on posterior two-thirds of body; ventral surface lightly colored in preservative; skull of holotype lacks vomerine odontophores (although vomers present).

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Variations in paratypes. —Body sizes ( SVL) 15.8 mm (MZFC-HE-35600), 15.2 mm (MZFC-HE-35601), 16.9 mm ( UTA A- 66117), 16.7 mm ( UTA A- 66118), 12.3 mm ( UTA A- 66119); eye–nostril distance 9–10% SVL; tympanic ratios 7– 9%; dorsal color patterns variable, often with two distinctive patches of differing ground coloration ranging from orange to tan.

Etymology. —The specific epithet is a combination of the Latin prefix bi- meaning two and tonium meaning tone. It is a reference to the two distinctive patches of color found on the holotype and several paratypes that create the appearance of a ‘‘two-tone’’ dorsal coloration.

Distribution. —This species is known only from the Sierra Madre del Sur of central Guerrero (~ 2071 m). The closest named places to the type locality are Izotepec to the north and Los Bajos to the southwest. The habitat at the type locality is montane pine–oak forest.

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Diet. —CT-scan of the holotype revealed the presence of a small millipede (Diplopoda) in the stomach. We also noted the presence of a small red ant ( Formicidae ) in the mouth of the holotype.

Phylogenetics. — Craugastor bitonium was inferred to be the sister taxon of C. pygmaeus , with high support in the concatenated analyses (ML ¼ 99; BAYES ¼ 1.0; Fig. 3 ). This sister relationship was also recovered in both mtDNA and nDNA analyses, although with lower support in the nDNAonly analyses (ML ¼ 54, BAYES ¼ 0.67; Figs. 4 and 5 ). Craugastor bitonium is separated from C. pygmaeus by a P - distance of 4.7% ( Table 4 ).

Remarks. —The skull of C. bitonium is similar to C. hobartsmithi , C. montanus , and C. pygmaeus . Craugastor bitonium displays a developmental pattern similar to C. pygmaeus (with high levels of ossification at small sizes), suggesting small adult body sizes ( Fig. 11 ). This species likely co-occurs with C. pygmaeus , C. omiltemanus , and C. saltator in central Guerrero ( Figs. 6 and 8 ). The specimen UTA A-66132 is referred with some hesitation because it was collected from a lower elevation than the type locality and has a Finger Ilength nearing C. pygmaeus (which also occurs in Guerrero). Six of the specimens were adult females containing unpigmented ovaries with yolked eggs and thick oviducts, the seventh (UTA A-66119; Fig. 22C , far left) was an adult male with pigmented testes.

Figures

FIG. 22.—Female holotype of Craugastor bitonium (A, UTA A-64254, SVL ¼ 15.8 mm); female paratype (B, UTA A-66117, SVL ¼ 16.9 mm); (B); one male and two female paratypes (C, left to right, UTA A-66119, SVL ¼ 12.3 mm; MZFC-HE-35600, SVL ¼ 15.8 mm; MZFC-HE-35601, SVL ¼ 15.2 mm); female paratype (D, UTA A-66118, SVL ¼ 16.7 mm). Note two-tone dorsal color pattern in A, B, and C. All collected from the road between Yextla and Vuelta del Sur, Guerrero, Mexico, 2071 m. A color version of this figure is available online.

FIG. 19.—Lateral surface of the head in representative specimens of the Craugastor mexicanus series. Female holotype of C. bitonium (A, UTA A-64254, SVL ¼ 15.8 mm); female paratype of C. candelariensis (B, UTA A-55247, SVL ¼ 18.6 mm); male holotype of C. cueyatl (C, UTA A-62348, SVL ¼ 13.0 mm); female C. hobartsmithi (D, UMMZ 94230, SVL ~12 mm, photo by J. David Curlis); female C. mexicanus (E, UTA A-28754, SVL ¼ 35.9 mm); male C. montanus (F, UMMZ 88002, SVL ¼ 21.8 mm); female C. omiltemanus (G, UTA A-66140, SVL ¼ 30.9 mm); female holotype of C. polaclavus (H, UTA A- 62392, SVL ¼ 14.7 mm); female holotype of C. portilloensis (I, UTA A-62393, SVL ¼ 11.4 mm); female C. pygmaeus (J, UTA A-54809, SVL ¼ 17.3 mm); male holotype of C. rubinus (K, UTA A-62345, SVL ¼ 12.6 mm); male C. saltator (L, UTA A-54931, SVL ¼ 18.4 mm). A color version of this figure is available online.

FIG. 3.—Concatenated Maximum Likelihood analyses of two mitochondrial (12S and 16S) and two nuclear (RAG1 and TYR) gene fragments sequenced from the Craugastor mexicanus series (total of 2230 base pairs). Node values correspond to bootstrap support from Maximum Likelihood analysis and posterior probabilities from a Bayesian analysis of the same data set, respectively. Support values are not reported for nodes that had,50/0.50. NS indicates no support in the Bayesian analysis for a depicted relationship. Locality abbreviations are as follows: COL ¼ Colima, HID ¼ Hidalgo, GRO ¼ Guerrero, JAL ¼ Jalisco, MEX ¼ Estado de México, OAX ¼ Oaxaca, PUE ¼ Puebla, and VER ¼ Veracruz.

FIG. 4.—Maximum Likelihood analyses of mitochondrial DNA (mtDNA) markers sequenced from the Craugastor mexicanus series (total of 1047 base pairs). Black circles indicate nodes receiving bootstrap support values.90 from the Maximum Likelihood analysis and 0.90 posterior probabilities in corresponding Bayesian analyses. Where posterior probabilities were.0.90 but Maximum Likelihood bootstrap support was,90, a number indicates the bootstrap support. NS indicates no support in the Bayesian analysis for a depicted relationship. Locality abbreviations are as follows: COL ¼ Colima, HID ¼ Hidalgo, GRO ¼ Guerrero, JAL ¼ Jalisco, MEX ¼ Estado de México, OAX ¼ Oaxaca, PUE ¼ Puebla, and VER ¼ Veracruz.

FIG. 5.—Maximum Likelihood analysis of nuclear DNA (nDNA) markers sequenced from the Craugastor mexicanus series (total of 1183 base pairs). Black circles indicate nodes receiving bootstrap support values.90 from the Maximum Likelihood analysis and 0.90 posterior probabilities in corresponding Bayesian analyses. Where posterior probabilities were.0.90 but Maximum Likelihood bootstrap support was,90, a number indicates the bootstrap support. NS indicates no support in the Bayesian analysis for a depicted relationship. Locality abbreviations are as follows: COL ¼ Colima, GRO ¼ Guerrero, JAL ¼ Jalisco, MEX ¼ Estado de México, OAX ¼ Oaxaca, PUE ¼ Puebla, and VER ¼ Veracruz.

FIG. 11.—Ossification levels within the Craugastor mexicanus series compared with body size (estimated as log centroid size). Ossification scores are based on the six-stage ontogenetic sequence described in Table 3.

FIG. 6.—Distribution of Craugastor mexicanus, C. montanus, C. pygmaeus, and C. saltator in Mexico and Guatemala. Dots inside symbols indicate individuals used in the molecular analyses in this study. Relevant type localities are indicated by text and arrows.

FIG. 8.—Distribution of Craugastor hobartsmithi, C. cf. hobartsmithi, C. omiltemanus and six new species from Mexico. Dots inside symbols indicate individuals used in the molecular analyses in this study. Inset depicts region of Oaxaca where three of the new species exist in near sympatry. A question mark indicates uncertain georeferencing. Relevant type localities are indicated by text and arrows.