Craugastormexicanus ( Brocchi 1877 )

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 : 27-29

Craugastormexicanus ( Brocchi 1877)

Leiuperus mexicanus Brocchi 1877:184 . Holotype unsexed ( MNHNP 6218 ) from ‘‘ Mexico ’’ (¼ Cerro San Felipe, Oaxaca, Mexico [ Smith and Taylor 1950]). [Examined].

Paludicola mexicana (Brocchi) : Boulenger 1882:237; Neiden 1923:513.

Pleurodema mexicana (Brocchi) : Parker 1927:475.

Microbatrachylus oaxacae Taylor 1940:505 . Holotype male ( FMNH 100001) from ‘‘Cerro San Flipe, near Oaxaca, Oaxaca, Mexico.’’ [Examined].

Microbatrachylus lineatissimus Taylor 1941:87 . Holotype male ( FMNH 1000036) from ‘‘Cerro San Flipe, near Oaxaca, Oaxaca, Mexico.’’ [Examined].

Microbatrachylus fuscatus Davis and Dixon 1957:146. Holotype female ( TCWC 12171) from ‘‘ 20 miles east of Tulancingo, Hidalgo, Mexico.’’ [Not examined; neartopotypic specimen from Hidalgo examined ( UTA A-66138)].

Eleutherodactylus oaxacae (Taylor) : Lynch 1965:3.

Eleutherodactylus lineatissimus (Taylor) : Lynch 1965:3.

Eleutherodactylus mexicanus (Brocchi) : Gorham 1966:86.

Craugastor mexicanus (Brocchi) : Crawford and Smith 2005:536.

Diagnosis. —Based on 26 specimens. Aspecies of Craugastor distinguished by the following combination of characters: (1) large adult size (maximum SVL ¼ 40.5 mm); (2) full ossification of the skeleton in adults; (3) presence of posterolateral projection of frontoparietal ( Fig. 26B ); (4) presence of vomerine odontophores (in larger individuals); (5) presence or absence of raised tubercles on eyelids, <4 smooth to round and only slightly protruding tubercles; (6) supratympanic fold developed; (7) face flank, labium barred with or without distinctive canthal stripe; (8) one (or two fused) postrital tubercles; (9) gular region peppered with melanocytes; (10) dorsal surface extremely variable, ranging from dark or light stripes, dark hourglass, dark or pale dorsal stripe of different widths, being unicolored dark or pale brown, to bird-dropping coloration (black peppered grayish dorsum with a dirty white medial streak and bright-white heels), all color morphologies have variable presence of interocular band and suprascapular or rump blotching or stripping; in most snout colored as rest of body but sometimes pale; (11) variable middorsal ridge; (12) dorsal skin smooth or tubercular and may have hourglass and/or vertebral and/or paravertebral ridges; (13) body flank unicolored pale, slightly darker anteriorly, or spotted posteriorly and or anteriorly, supratympanic dark coloration sometimes reaching posterior axillary area; smooth to shagreened; (14) inguinal gland present and axillary gland sometimes present in adults; (15) when leg adpressed to body, heel reaches snout tip or beyond; (16) outer tarsal ridge with 0–5 rounded tubercles; smooth or with thick but only slightly raised fringe; (17) finger and toe tips round and expanded (rarely slightly spatulate or barely expanded and somewhat pointed); (18) inner metatarsal tubercle larger than outer metatarsal tubercle.

Comparisons. — Craugastor mexicanus can be differentiated from C. candelariensis , C. cueyatl , C. hobartsmithi , and C. portilloensis by the equal sizes of the inner and outer metatarsal tubercles (unequal sizes in C. mexicanus ). It can be differentiated from C. bitonium and C. pygmaeus by the absence of a posterolateral projection of the frontoparietal (present in C. mexicanus ). It can be differentiated from C. polaclavus and C. rubinus by the absence of vomerine odontophores (present in C. mexicanus ). It can be differentiated from C. montanus by the condition of supratympanic folds in adults; developed in C. mexicanus versus moderate to poorly developed in C. montanus . It can be differentiated from C. omiltemanus by ventral skin texture in life; smooth to granular in C. mexicanus versus areolate in C. omiltemanus . Craugastor mexicanus is most similar to C. saltator . We were unable to identify any reliable morphological characters to differentiate C. mexicanus and C. saltator ; however, they have nonoverlapping geographic distributions, with C. saltator only occurring in western Guerrero ( Fig. 6 ).

Description. —In previous literature, described as largebodied, long-legged with row of small tubercles on outer edge of the tarsus ( Taylor 1941); variable palmar tubercle arrangements (palmar tubercle divided, single, or evaginated; Lynch 1965); inner metatarsal tubercle larger than outer metatarsal tubercle; lack of tarsal tubercles ( Lynch 2000).

Holotype (MNHNP 6318) is large (~ 40 mm SVL); owing to poor preservation, columella of holotype partially ruptured the tympana on both sides ( Fig. 1B ); finger lengths III> IV> II> I; toe length IV> V ¼ III> II> I.

Distribution. —This species is widespread throughout eastern Mexico in high-elevation habitats (1554–2700 m) of Oaxaca, Puebla, Hidalgo, and Veracruz ( Fig. 6 ). These habitats span the Sierra Madre Oriental and Sierra Madre del Sur. Canseco Márquez and Gutiérrez Mayén (2010) report that C. mexicanus occurs in the forests adjacent to the Tehuacán-Cuicatlán Valley in Puebla and Oaxaca. It is likely this species occurs in Guerrero; however, most specimens resembling C. mexicanus we examined from Guerrero are referrable to C. saltator .

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Phylogenetics. —The concatenated data set placed C. mexicanus as the sister taxon to a clade of C. omiltemanus þ C. saltator with high support in the BAYES analysis (0.98) but moderate support in the ML analysis (75; Fig. 3 ). This appears to be a relationship supported exclusively by the mtDNA data set because separate analysis of the nDNA markers did not confidently infer a sister taxon of C. mexicanus ( Figs. 4 and 5 ). Although BAYES analyses strongly supported the monophyly of C. mexicanus (> 0.90), the ML analyses recovered variable support ranging from 79 (concatenated analysis) to 54 (nDNA-only analysis). In terms of genetic distances ( Table 4 ), C. mexicanus was most similar to C. omiltemanus (4.9%), followed by similarity to C. saltator (5.1%).

Intraspecific variation. —We examined over 220 specimens of C. mexicanus for this revision (Appendix I), and briefly provide some patterns of intraspecific variation that we observed. Many populations have substantial colorpattern polymorphism ( Fig. 27 ), similar to what is observed in the C. rhodopis series ( Lynch 1966; Streicher et al. 2014). In some northern populations (Hidalgo and Puebla), the canthal mask is broken into a black spot posterior to the tympanum (often with a thin yet distinctive white margin). Specimens throughout Oaxaca varied in whether they had a single or divided palmar tubercle (as reported by Lynch 1965, see his Fig. 2 ); in six specimens we examined there was asymmetry with a single palmar tubercle on one hand and divided on the other.

Patterns of dorsal ridging and coloration often coincide, with observations of the following morphs: (1) straight raised ridges that are tubercular and darker in coloration than the rest of the dorsum; (2) straight raised dorsal ridges that are tubercular but of the same color as the rest of the dorsum; (3) straight lines of color that are dark but with no tubercular raised ridges; (4) ridges that are not straight but form an hourglass shape and are tubercular; (5) ridges that are not straight but form an hourglass shape and are not tubercular; (6) scattered tubercles on the dorsum, which are sometimes dark and sometimes same color as the background; (7) pale or dark unicolored dorsum; (8) a unicolored dorsum with a pale median stripe that can be ridged or smooth; (9) a wide dark band on the dorsum, which usually co-occurs with a pale upper labium; and, (10) white hills of coloration and a peppered grayish dorsum sometimes with a diffused lighter cream color, a pattern that may mimic bird droppings (appearing superficially as a smear of uric acid and digestive waste).

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Remarks. —The skull of C. mexicanus is similar to that of C. omiltemanus and C. saltator , with more anteriorly placed anterior suture of the frontoparietal and prootic than in other species. We noticed that the ‘‘ M. lineatissimus ’’ morphotype (raised and parallel ridges on the dorsum) occurs widely throughout the range of C. mexicanus . Interestingly, the examined paratype of ‘‘ M. lineatissimus ’’ has a unique skull shape for C. mexicanus . The shape is similar to that of C. hobartsmithi , C. montanus , and C. pygmaeus , with a more posteriorly placed anterior suture of the frontoparietal and prootic than in other species, coupled with a narrower back of the skull than in any other species ( Fig. 27A ). This unique condition likely explains the specimen as an outlier in several of our statistical analyses ( Figs. 9 , 11 , and 12). However, we were unable to CT-scan other individuals with the ‘‘ M. lineatissimus ’’ morphotype (or the holotype of M. lineatissmus ), so future investigation is necessary to determine whether the examined paratype (FMNH 104548) is an aberrant individual of C. mexicanus or represents a valid taxon.

Lynch (1965) reports that ‘‘ E. oaxacae ’’ has parotoid glands. However, we saw no evidence of these glands in the two type specimens that we examined (FMNH 100001 and FMNH 126638), nor are we aware of any species of Craugastor that possess parotoid glands (¼ large poison glands on the nuchal region). Craugastor mexicanus likely co-occurs with C. omiltemanus at high-elevation localities of central Oaxaca ( Figs. 6 and 8 ). At intermediate elevation localities in Veracruz and Oaxaca, it may overlap with C. pygmaeus ( Fig. 7 ). Male C. mexicanus have significantly larger tympana than do female C. mexicanus ( Fig. 13 ).

Figures

FIG. 26.—Skulls of ‘Microbatrachylus lineatissimus’ (A, paratype, FMNH 104548), Craugastor mexicanus (B, UTA A-56558) and C. pygmaeus (C, UTA A- 64272) in dorsal and lateral views. Posterolateral projection of the frontoparietal on C. mexicanus (B) is indicated by an arrow and grey shading. A color version of this figure is available online.

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. 1.—Male holotype of Eleutherodactylus hobartsmithi Taylor (A, FMNH 100114, SVL ¼ 14.4 mm); female holotype of Leiuperus mexicanus Brocchi (B, MNHNP 6318, SVL ~ 40 mm); male holotype of Microbatrachylus oaxacae Taylor (C, FMNH 100001, SVL ¼ 18.1 mm); male holotype of Microbatrachylus lineatissimus Taylor (D, FMNH 100036, SVL ¼ 20.0 mm); female holotype of Microbatrachylus montanus Taylor (E, USNM 115507, SVL ¼ 27.0 mm); female holotype of Eleutherodactylus pygmaeus Taylor (F, UIMNH 16125, SVL ¼ 17.0 mm); female holotype of Microbatrachylus albolabris Taylor (G, FMNH 100071, SVL ¼ 16.5 mm); male holotype of Microbatrachylus minimus Taylor (H, FMNH 100323, SVL ¼ 15.0 mm); female holotype of Microbatrachylus imitator Taylor (I, USNM 115508, SVL ¼ 14.2 mm); male lectotype of Syrrhaphus omiltemanus Günther (J, BMNH 1947.2.16.62, SVL ¼ 19.8 mm); female lectotype of Hylodes calcitrans Günther (K, BMNH 1947.2.16.47, SVL ¼ 34.9 mm); female holotype of Eleutherodactylus saltator Taylor (L, FMNH 100166, SVL ¼ 44.0 mm). Symbols correspond to current taxonomic assignments (square ¼ C. hobartsmithi, triangle ¼ C. mexicanus, crossedsquare ¼ C. montanus, pentagon ¼ C. omiltemanus, circle ¼ C. pygmaeus, rotated-triangle ¼ C. saltator). 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. 27.—Examples of intraspecific polymorphism in Craugastor mexicanus from Mexico; female (A, UTA A-56558, SVL ¼ 37.3 mm) from Putla de Guerrero municipality; Oaxaca, female (B, UTA A-64415, SVL ¼ 28.3 mm) from Carretera Sola de Vega–Juquila, Oaxaca; subadult (C, UTA A-64271, SVL ¼ 11.9 mm) from Carretera Sola de Vega–Juquila, Oaxaca; subadult and adult (D, UTA A-64258, SVL ¼ 13.6 mm and MZFC-HE-35584, SVL ¼ unavailable) both from 8.1 mi south of Sola de Vega, Oaxaca; adult (E, UTA A-66107, SVL ¼ unavailable) from Carretera Sola de Vega–Juquila, Oaxaca; subadult (F, UTA A-64260, SVL ¼ 16.6 mm) from Carretera Sola de Vega–Juquila, Oaxaca; female (G, UTA A-64413, SVL ¼ 23.5) from Sierra Miahuatlán, Oaxaca; female (H, UTA A-56579, SVL ¼ 21.3 mm) from Sierra Negra, Puebla; female (I, UTA A-56559, SVL ¼ 35.4 mm) from Sierra Mazateca, Puerto Soledad, Oaxaca; subadult (J, UTA A-64257, SVL ¼ 17.6 mm) from Sierra Mixe, Carretera Ayutla–Zacatepec, Oaxaca; subadult (K, UTA A-64259, SVL ¼ 10.9 mm) from 6.1 mi south of San Miguel Suchixtepec, Oaxaca; subadult (L, UTA A-66138, SVL ¼ unavailable) from 20 mi east of Tulancingo, Hidalgo. A color version of this figure is available online.

FIG. 2.—Skull of Craugastor mexicanus (USNM 47905) in anterior, dorsal, lateral, and ventral views showing placements of landmarks. Landmarks are (1) anterior midline tip premaxilla, (2) maxilla–premaxilla suture, (3) anterior tip nasal, (4) anterior tip frontoparietal, (5) posterior lateral tip frontoparietal, (6) posterior dorsal tip squamosal, (7) anterior frontoparietal prootic suture, (8) lateral tip nasal, (9) squamosal maxillary suture, (10) posterior tip maxilla, (11) anterior tip parasphenoid (12) posterior tip parasphenoid, (13) lateral tip parasphenoid, and, (14) pterygoid maxillary suture. A color version of this figure is available online.

FIG. 9.—Body size and shape variation within the Craugastor mexicanus series as depicted by principal components analysis of 15 linear measurements. Principal component scores for the first two components (left) are depicted along with their residuals (right). Large-bodied species are those with an adult body size.20 mm SVL (C. mexicanus, C. montanus, C. omiltemanus, C. saltator), and small-bodied species are those with adult body sizes,20 mm (C. bitonium, C. candelariensis, C. cueyatl, C. hobartsmithi, C. polacalvus, C. portilloensis, C. pygmaeus, and C. rubinus).

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. 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.

FIG. 7.—Box plots depicting elevational distribution of Craugastor mexicanus and C. pygmaeus inferred from locality data associated with museum specimens. Results are shown for both specimens used in the molecular analysis (Molecules þ Morphology) and for specimens assigned to species using only morphology. Asterisks represent potential outliers, which are.1.5 times the interquartile range (¼ range inside the box).

FIG. 13.—Evidence of sexual dimorphism of tympanum width in Craugastor mexicanus (left) and C. pygmaeus (right). Sex was determined by directly examining gonads for select specimens of C. mexicanus and is implied by scaling patterns in those specimens where sex was not directly determined. Downloaded From: https://bioone.org/journals/Herpetological-Monographs on 04 May 2022