Miniaturization in Direct-Developing Frogs from Mexico with the Description of Six New Species Author Jameson, Tom J. M. Author Streicher, Jeffrey W. Author Manuelli, Luigi Author Head, Jason J. Author Smith, Eric N. text Herpetological Monographs 2022 2022-04-04 36 1 1 48 http://dx.doi.org/10.1655/0733-1347-36.1.1 journal article 10.1655/0733-1347-36.1.1 6518587 Craugastor candelariensis sp. nov. Holotype . — UTA A-64253 (field ID: JAC 21885), male collected by E.N. Smith and colleagues Nof Candelaria on the road to Oaxaca ; Sierra Madre del Sur, Oaxaca , Mexico , 15.94960°N , 96.47110°W , 668 m , on 21 January 2002 between 1130 and 1200 h, near stream bordering coffee plantation and secondary forest . Downloaded From: https://bioone.org/journals/Herpetological-Monographs on 04 May 2022 FIG. 17.—Dorsal surface of the head in representative specimens of the Craugastor mexicanus series. Female paratype of C. bitonium (A, UTA A-66118, SVL ¼ 16.7 mm); female paratype of C. candelariensis (B, UTA A-55247, SVL ¼ 18.6 mm); female paratype of C. cueyatl (C, MZFC-HE-35614. SVL ¼ 17.2 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); female C. montanus (F, UMMZ 87970, SVL ¼ 25.8 mm); male C. omiltemanus (G, UTA A-66139, SVL ¼ 18.1 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). Acolor version of this figure is available online. Paratypes (3). —MZFC-HE-35617 (formerly UTA A-64252 ; field ID : JAC 21873 ; Fig. 23 ) , male with heavily pigmented testes, same data as holotype except collected 1.2 mi on rough road toward Pluma Hidalgo on the Candelaria – Portillo road, 15.95610°N , 96.44930°W , 1051 m , on 21 January 2002 at 1000 h in leaf litter of coffee plantation. UTA A- 66116 ( Field ID : JAC 21851 ) , male with pigmented testes collected by E.N. Smith and colleagues from San Gabriel Mixtepec, Puente de Hamaca, Oaxaca , Mexico , 16.10510°N , 97.06310°W , 710 m , on 20 January 2002 at 1520 h on forest floor. UTA A- 55247 ( Field ID : ENS 9698 ) , female with unpigmented gonads and extended oviducts collected by Karin S. Castaneda along the Carretera San Gabriel Mixtepec–Miahuatlán of the Sierra Madre del Sur, Oaxaca , Mexico , 16.160556°N , 97.00111°W , 1270–1350 m , on 15 March 1998 at 1630 h from pine forest habitat . Downloaded From: https://bioone.org/journals/Herpetological-Monographs on 04 May 2022 FIG. 18.—Ventral surface of the head in representative specimens of the Craugastor mexicanus series. Female paratype of C. bitonium (A, UTA A-66118, SVL ¼ 16.7 mm); female paratype of C. candelariensis (B, UTA A-55247, SVL ¼ 18.6 mm); female paratype of C. cueyatl (C, MZFC-HE-35614. SVL ¼ 17.2 mm); male C. hobartsmithi (D, UMMZ 94231, SVL ~11 mm, photo by J. David Curlis); male C. mexicanus (E, UTA A-6907, SVL ¼ 22.3 mm); female C. montanus (F, UMMZ 87970, SVL ¼ 25.8 mm); male C. omiltemanus (G, UTA A-66139, SVL ¼ 18.1 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); male C. pygmaeus (J, UTA A-64414, SVL ¼ 10.3 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). Acolor version of this figure is available online. Diagnosis. —A species of Craugastor distinguished by the following combination of characters: (1) small adult size (maximum SVL ¼ 18.6 mm ); (2) full ossification of most skeletal elements in adults, lacking ossification only of Stage 6 ( Table 3 ); (3) absence of posterolateral projection of frontoparietal; (4) presence of vomerine odontophores; (5) absence of raised tubercles on eyelids; (6) supratympanic fold absent or poorly developed; (7) face flank with nostril– canthal–supratympanic stripe, lips colored as dorsum; (8) two postrictal tubercles; (9) gular region uniformly pale to slightly evenly peppered with melanocytes; (10) dorsal surface unicolored pale; (11) pale middorsal ridge, sometimes with few tiny spots; (12) evenly fine tubercles on dorsum; (13) body flank unicolored pale, shagreened with fine tuberculation; (14) inguinal glands present and axillary glands absent in adults; (15) when leg adpressed to body, heel reaches between eye and tip of snout; (16) outer tarsal ridge with 3–8 tiny and pointed tubercles on slightly raised fringe; (17) finger and toe tips lanceolate to mucronate (toes and outer two fingers); (18) similar sizes of inner and outer metatarsal tubercles. Downloaded From: https://bioone.org/journals/Herpetological-Monographs on 04 May 2022 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. montanu s (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). Acolor version of this figure is available online. Comparisons. — Craugastor candelariensis can be differentiated from C. bitonium , C. mexicanus , C. montanus , C. omiltemanus , C. polaclavus , C. pygmaeus , C. rubinus , and C. saltator by a larger innermetatarsal tubercle (inner and outer metatarsal tubercles are similar sizes in C. candelariensis ). Craugastor candelariensis can be differentiated from C. cueyatl and C. hobartsmithi by the absence of vomerine odontophores (present in C. candelariensis ). It can be differentiated from C. portilloensis by the presence of posterolateral projections of the frontoparietal (absent in C. candelariensis ). Description of holotype . — Holotype small male (SVL ¼ 13.3 mm ); snout rounded and short ( 0.5 mm naris–snout; 4% SVL); long eye–nostril distance ( 1.7 mm ; 13% SVL); tympanum 1.2 mm (7.6% SVL); no supratympanic fold and no shoulder tubercle; finger length formula III <IV <II ¼ I; single palmar tubercle; single prepollical tubercle; subarticular tubercles present on all fingers; supernumerary tubercles present on Finger III; toe length formula IV <III <V <II <I; inner metatarsal tubercle and outer metatarsal tubercle equal size; subarticular tubercles present on all toes; supernumerary tubercles present on plantar surface; unable to verify supracloacal fold state because posterior end damaged when removing leg for genetic analysis; entire body lightly colored in preservative (appears some saponification may have occurred). Downloaded From: https://bioone.org/journals/Herpetological-Monographs on 04 May 2022 FIG. 20.—Ventral surface of the hand in representative specimens of the Craugastor mexicanus series. Female paratype of C. bitonium (A, UTA A-66118, SVL ¼ 16.7 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 Craugastor montanu s (F, UMMZ 88002, SVL ¼ 21.8 mm); female C. omiltemanus (G, UTA A-66140, SVL ¼ 30.9 mm); female C. polaclavus (H, UTA A-66097, SVL ¼ 16.0 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). Acolor version of this figure is available online. Variations in paratypes . —Body sizes (SVL) 12.4 mm (MZFC-HE-35617), 14.3 mm (UTA A-66116), 18.6 mm (UTA A-55247); eye–nostril distance 10–13% SVL (males), 9% SVL (female); tympanic ratios 7–10%. Etymology. —The name is an abbreviated allusion to the municipality of Candelaria Loxicha (near the type locality) and the Latin suffix - ensis meaning place. It is simultaneously a reference to the Latin noun candēla meaning a fire or light made of wax, given the translucent yellow appearance of several type specimens in preservative, as if someone were shining a candle through them. Downloaded From: https://bioone.org/journals/Herpetological-Monographs on 04 May 2022 FIG. 21.—Ventral surface of the foot in representative specimens of the Craugastor mexicanus series. Female paratype of C. bitonium (A, UTA A-66118, SVL ¼ 16.7 mm); female paratype of C. candelariensis (B, UTA A-55247, SVL ¼ 18.6 mm); female paratype of C. cueyatl (C, MZFC-HE-35614. SVL ¼ 17.2 mm); male C. hobartsmithi (D, UMMZ 94231, SVL ~11 mm, photo by J. David Curlis); male C. mexicanus (E, UTA A-6907, SVL ¼ 22.3 mm); male Craugastor montanu s (F, UMMZ 88002, SVL ¼ 21.8 mm); male C. omiltemanus (G, UTA A-66139, SVL ¼ 18.1 mm); female holotype of C. polaclavus (H, UTA A-62392, SVL ¼ 14.7 mm); female paratype of C. portilloensis (I, MZFC-HE-35581, SVL ¼ 12.1 mm); female C. pygmaeus (J, UTA A-54809, SVL ¼ 17.3 mm); male paratype of C. rubinus (K, MZFC-HE-35616, SVL ¼ 10.8 mm); female C. saltator (L, UTA A-55239, SVL ¼ 38.2 mm). Acolor version of this figure is available online. Distribution. —This species is known from intermediate elevations of southern Oaxaca ( 668–1350 m ), an area that mostly consists of Sierra Madre del Sur pine–oak forest habitat. Phylogenetics. — Craugastor candelariensis was strongly supported as monophyletic in the concatenated analysis (ML ¼ 100; BAYES ¼ 1.0; Fig. 3 ). In this analysis, the sister taxon of C. candelariensis was inferred to be C. polaclavus (ML ¼ 80; BAYES ¼ 0.99). We also observed this sister relationship in the nDNA-only analysis ( Fig. 5 ); however, in the mtDNAonly analysis C. candelariensis was inferred to be the sister taxon of a clade containing C. bitonium þ C. pygmaeus ( Fig. 4 ). In terms of genetic distances, Craugastor candelariensis is most similar to C. polaclavus and C. pygmaeus (both 6.4%; Table 4 ). Downloaded From: https://bioone.org/journals/Herpetological-Monographs on 04 May 2022 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. Acolor version of this figure is available online. Remarks. —The skull of C. candelariensis is similar to C. bitonium , C. hobartsmithi , C. montanus , and C. pygmaeus , with more posteriorly placed anterior suture of the frontoparietal and prootic than in other species. Two type specimens appear white-yellowish in preservative (possibly having been saponified). This species likely co-occurs with C. pygmaeus , C. polaclavus , and C. portilloensis in southcentral Oaxaca ( Figs. 6 and 8 ). In terms of body size and ossification level it is the smallest member of the C. mexicanus series to complete Stage 5 of our ontogenetic sequence.