Distributional Data for Bolitoglossa (Amphibia, Caudata, Plethodontidae) from Nicaragua and Costa Rica

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Herpetological Review, 2012, 43(4), 560–564. © 2012 by Society for the Study of Amphibians and Reptiles Distributional Data for Bolitoglossa (Amphibia, Caudata, Plethodontidae) from Nicaragua and Costa Rica

The genus Bolitoglossa is the largest and most widely distrib- (MHUL), Universidad Nacional Autónoma de Nicaragua-León, uted group of neotropical lungless salamanders (Parra-Olea et León, Nicaragua. We also report information on a Costa Rican al. 2004). There are 121 species (AmphibiaWeb 2012) of small to specimen of B. indio in the British Museum of Natural History large, relatively robust salamanders distributed from northeast- (BMNH), London, UK. Figure 1 depicts collection localities dis- ern Mexico to southern Amazonian Brazil (Savage 2002; Wake cussed below. Geocoordinates are based on datum WGS84. and Lynch 1976). Although most species in the genus occur in Middle America, there are only four species in Nicaragua (the Bolitoglossa indio: COSTA RICA: ALAJUELA: Cantón de San largest and most centrally located country in Central America; Carlos: Boca de Arenal, 68 m elev. First country record. On 20 Sunyer and Köhler 2010): B. indio, B. insularis, B. mombachoen- September 2011, D. B. Wake examined specimen number BMNH sis, and B. striatula. Bolitoglossa indio is a species known only 96.10.8.77 (Fig. 2a) collected by C. F. Underwood in 1890. This from the holotype, collected at 25 m elevation in Dos Bocas de specimen has had a long history. It was first mentioned (but not Río Indio, Dept. Río San Juan (Sunyer et al. 2008). The remaining illustrated) by Günther (1885–1902) as Spelerpes variegatus (a three species, B. insularis, B. mombachoensis, and B. striatula, composite of species in which he included specimens now as- are presumed closely related (S. M. Rovito, pers. comm.) and signed to Bolitoglossa alberchi, B. mexicana, B. mulleri, B. pla- allopatric. Bolitoglossa striatula is a relatively widespread spe- tydactyla, and B. salvinii) and reported it to have been obtained cies with a distributional range from northeastern Honduras to from “San Carlos, Costa Rica.” Dunn (1926) discussed the speci- southeastern Costa Rica, primarily on the Atlantic versant, from men briefly in an addendum to his monograph on the Plethod- near sea level to 1052 m elevation (Savage 2002). Bolitoglossa ontidae. At the time Dunn worked, only 30 species of tropical mombachoensis and B. insularis are species endemic to higher salamanders were known (today there are 121 species of Boli- elevations of cloud forest habitat on two forested and isolated toglossa alone, AmphibiaWeb 2012); many of them were com- volcanoes of the Pacific versant of Nicaragua. Bolitoglossa mom- posites of sometimes unrelated species. Under the heading “Oe- bachoensis is a locally abundant species (Jansen and Köhler 2001) dipus platydactylus” Dunn (1926:440–441) listed six specimens restricted to higher altitudes (950–1345 m elevation) of Reserva in the British Museum of Natural History that he had examined, Natural Volcán Mombacho, Dept. Granada (Köhler and McCra- one from British Honduras, two from Guatemala, the specimen nie 1999; Köhler 2011); and B. insularis is known only from the in question from Costa Rica, and two specimens from Colom- holotype, collected at 800 m elevation in Reserva Natural Volcán bia. While Dunn noted that this Costa Rican specimen might Maderas on Isla de Ometepe in Lago de Nicaragua, Dept. Rivas represent an undescribed form, he stated forcefully that of then- (Sunyer et al. 2008). recognized species it fit only into O. platydactylus. None of these During fieldwork conducted in October and November 2009 six specimens is today considered a member of Bolitoglossa in Nicaragua we collected several specimens that extend the platydactyla, and as early as 1952 Taylor questioned the identi- known vertical distribution of Bolitoglossa insularis, B. momba- fication of the San Carlos specimen. However, in the absence choensis, and B. striatula. All referred specimens were verified of additional specimens, Taylor took no formal action. When by Theodore J. Papenfuss and Sean M. Rovito and are deposited Taylor (1954) described B. alvaradoi and B. arborescandens (the in the Museum of Vertebrate Zoology (MVZ), University of Cali- latter synonymized with B. alvaradoi by Savage 2002), he made fornia, USA, and in the Museo Herpetológico de la UNAN-León no mention of the specimen in question. Wake and Brame (1962) assigned the specimen to B. alvaradoi, and Savage (2002) ac- cepted this decision. However, Savage added more exact geo- JAVIER SUNYER* graphic information “Alajuela: San Carlos: Boca de Arenal.” Sav- Museo Herpetológico de la UNAN-León (MHUL), Departamento de Biología, age (in litt. to DBW, 22 February 2012) explained his reasoning. Facultad de Ciencias y Tecnología, Universidad Nacional Autónoma de Nicaragua-León, León, Nicaragua Underwood was a well-known ornithologist and general natural- DAVID B. WAKE ist, and he is known to have traveled with the ornithologist M. A. Museum of Vertebrate Zoology and Department of Integrative Biology, 3101 Carikker, Jr. (Carriker 1910). The locality “San Carlos” may seem VLSB, University of California, Berkeley, California 94720-3160, USA vague, because the name in its most general sense refers to the LENIN A. OBANDO Cantón de San Carlos in the Provincia de Alajuela. The Canton Museo Herpetológico de la UNAN-León (MHUL), Departamento de Biología, is the largest of the 81 cantons in Costa Rica, and includes terri- Facultad de Ciencias y Tecnología, Universidad Nacional Autónoma de tory between the Cordillera Central and the Nicaraguan border, Nicaragua-León, León, Nicaragua with the San Carlos River a central feature. Savage (1974) consid- *Corresponding author; e-mail: [email protected] ers Underwood’s “San Carlos” to refer to the village known today as Boca de Arenal, following Carriker’s (1910) statement that the

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name as used by collectors refers to the head of navigation up base, although differing from the holotype of B. indio in having a the Río San Carlos (above the Río San Juan) and the beginning bifurcated transverse process of the first caudal vertebra. While of the old land route to the Meseta Central. The site, then known this is the usual beta pattern, absence of the bifurcation is also as the Comandancia de San Carlos, is today’s Boca de Arenal found occasionally in specimens of other species belonging to (see Fig. 1). If we accept this reasoning, the assignment of this the above subgenera, and what is most important is the cross- specimen to B. indio extends the known geographical range of ing of the transverse processes of the adjacent last caudosacral the species approximately 87 km to the southwest from the type and first caudal vertebrae. We do not know the condition of the locality (see Fig. 1), along the San Carlos River south of the San vertebrae in the Rara Avis population, but specimens assigned to Juan River. Therefore, this species is no longer considered a Ni- B. alvaradoi have invariably had the complex tail base, with bi- caraguan endemic. furcated transverse processes on the first caudal vertebra. In ad- BMNH 96.10.8.77 is an adult male that has the following di- dition, some specimens of B. alvaradoi from Rara Avis showed a mensions (in mm): Standard length (SL, snout to posterior end striking change in coloration between day and night time (Twan of vent) 46.8, tail approximately 42, head width 7.3, forelimb Leenders, pers. comm.). In contrast, the holotype of B. indio was length 10.7, hind limb length 12.9, width of pes 4.9. There are 3 kept living for several days and showed no significant change in premaxillary teeth and 68 maxillary teeth. The vomerine teeth coloration. Resolving the question of relationships between B. were not countable, but were in a long, strongly curved row. The indio and what we now consider its likely closest relative B. al- foot is especially broad and the fifth digit of the pes is large and varadoi will require additional specimens and research. stout. Although rather desiccated, color preservation is good. The moderately dark ground color of the dorsal surfaces is cov- Bolitoglossa insularis: NICARAGUA: RIVAS: Reserva Natural ered with extensive light patches that appear to lie superficially Volcán Maderas (11.45643°N, 85.50845°W), Isla de Ometepe, above the ground color. These patches are sharply demarcated 1050 m elev. (see Fig. 1). 13 November 2009. J. Sunyer and L. A. from the ground color. Light pigmentation is marked on the Obando. Adult female (MVZ 264228; Fig. 3). The specimen was back of the head and over the shoulders. Small, isolated spots found active on a fern’s leaf 1.5 m above the ground at night time of pigment are found in the mid-dorsal region, where they form (2030 h) near a rather windy ridge along the trail from Finca Mag- two vaguely defined rows that coalesce over the pelvic region. dalena to the top of the volcano in pristine Premontane Moist Only 5–6 spots are clearly isolated, with the others partly joined. Forest formation (Holdridge 1967). At the time it was found, Spotting is extensive on the tail, with the spots usually slightly to the coloration of MVZ 264228 was homogeneously immaculate extensively connected. Assignment to B. indio is based on close yellowish to brownish dorsally and immaculate white ventrally similarity in morphology (see below) and in color pattern (see Fig. 2a), therefore BMNH 96.10.8.77 constitutes the second pub- lished record of this species (Sunyer et al. 2008). Because of the rarity of the species, we present here detailed comparisons of the specimens. They are both exactly the same size (46.8 SL), but the holotype is female. The holotype has a slightly broader head and a substantially shorter tail (34.8), but the posterior 40% of the tail of the holotype appears to be regenerated, accounting at least in part for its shorter length. The pes is about the same width (5.1 in holotype) and the hind limbs about the same length (10.9). There are substantially more maxillary teeth in the Costa Rican specimen than in the holotype (68 vs. 48). On the whole the two specimens are similar and measurement differences may relate at least in part to preservation artifacts. Some further comments on Bolitoglossa indio are in order. It is possible that a population of salamanders at Rara Avis (see Fig. 2b), adjacent to and upslope from the La Selva Biological Station, Costa Rica, is attributable to B. indio (compare Fig. 2b with Fig. 1b in Sunyer et al. 2008). If this is the case, there are several implications. First, the elevational record for this species would extend upwards to 710 m elev. Second, the species is mis- assigned to the subgenus Bolitoglossa and instead is a member of the subgenus Pachymandra, based on the fact that a speci- men from Rara Avis was used by Parra-Olea et al. (2004) as their representative of B. alvaradoi. An x-ray of the holotype of B. indio indicates that the transverse processes of the first caudal verte- brae are not branched, as are those of other members of Pachy- mandra (B. alvaradoi and B. dofleini). These processes arise at the very anterior end of the vertebra, are very long, and overlap the processes on the last caudosacral vertebra. This qualifies as a “complex” tail base, characteristic of Bolitoglossa beta of Wake Fig. 1. Map of Nicaragua and Costa Rica showing the localities men- and Lynch (1976), which characterizes the subgenera Magna- tioned in text. Water surfaces are colored blue. Areas below 600 m digita, Nanotriton, Mayamandra, Oaxakia, and Pachymandra. green. Areas above 600 m brown. Areas above 1200 m dark brown. We have x-rayed BMNH 96.10.8.77 and it too, has a complex tail

Herpetological Review 43(4), 2012 562 ARTICLES PHOTO BY T. LEENDERS T. BY PHOTO COLOR REPRODUCTION SUPPORTED BY THE THOMAS BEAUVAIS FUND FUND BEAUVAIS THOMAS THE REPRODUCTION BY SUPPORTED COLOR

Fig. 2. (a) Preserved adult male Bolitoglossa indio (BMNH 96.10.8.77) from Boca de Arenal, Cantón de San Carlos, Provincia de Alajuela, Costa Rica, 68 m elevation (see text), and (b) adult specimen of B. alvaradoi from Rara Avis, Provincia de Heredia, Costa Rica, 710 m elevation.

Fig. 3. Adult female Bolitoglossa insularis (MVZ 264228) from Reserva Natural Volcán Maderas, Dept. Rivas, Nicaragua, 1050 m elevation. Compare color change between (a) the moment it was found, and (b) after manipulation.

Fig. 4. (a, b) Non-collected adult specimens of Bolitoglossa mombachoensis from Reserva Natural Volcán Mombacho, Dept. Granada, Nicara- gua, 875–900 m elevation. These and few other specimens were found at day time around the small pond created by rains in the apex of the water-filled tank of the bromeliad-like leaves of Dracaena fragans, a plant locally used to delimit coffee plantation parcels.

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elevation, roughly the total extent of the core of the protected area on Volcán Mombacho.

Bolitoglossa striatula: NICARAGUA: MATAGALPA: Finca Monimbó (13.03173°N, 85.88682°W), 1380 m elev. (see Fig. 1). 18 October 2009. J. Sunyer and L. A. Obando. Adult female (MVZ 264227; Fig. 5). The specimen was found active at night along a trail inside the coffee plantation property in Lower Montane Moist Forest formation (Holdridge 1967). It was found 0.5 m above the ground on a leaf of a red ornamental introduced plant locally used to delimit coffee plantation parcels, which domi- nate the area. This record extends the known altitudinal range of Bolitoglossa striatula in Nicaragua by 610 m (Sunyer and Köhler 2010; Villa 1972) and in its whole distributional range by 328 m (Köhler 2011; Savage 2002); the species is currently known to oc- cur from about sea level to 1380 m elevation.

Acknowledgments.—All specimens were collected under the reg- Fig. 5. Adult female Bolitoglossa striatula (MVZ 264227) from Finca Monimbó, Dept. Matagalpa, Nicaragua, 1380 m elevation. ulations of permit No. 006–062009 and exported under regulations of permit No. DGPN/DB-002-2010 provided by the personnel of MARE- NA (Ministerio del Ambiente y los Recursos Naturales), Managua, (Fig. 3a). Immediately after manipulation, the specimen quickly Nicaragua. For logistic support, we thank Danilo J. Marenco (Finca Monimbó), José M. Zolotoff and Enoc Pineda (Fundación Cocibol- developed two pairs (one lateral and one dorsolateral) of non- ca), Januar López (Guía turístico Mombacho), Gian M. Palazio (Haci- delimited and weakly defined dark brown shadings (Fig. 3b). enda El Progreso), Salvadora Morales (Fauna y Flora Internacional), Dorsal surfaces of the head and limbs also turned slightly darker, and Carlos Flores (Hotel Villa Paraíso). This research was carried out coming to resemble the coloration of the holotype, which differs thanks to the ‘‘Memorandum of agreement between the UNAN-León from MVZ 264228 by having a considerably greater number of and the MVZ’’ and was entirely funded by the MVZ (Museum of Ver- small, dark brown spots, giving a mottled appearance to the en- tebrate Zoology, University of California, Berkeley, USA). We thank tire dorsal and ventral surfaces of the head, body, and tail (see Barry Clarke for help at the Natural History Museum, Jay M. Savage Fig. 2 in Sunyer et al. 2008). This color change was not observed for information and discussion, Josiah H. Townsend and Theodore J. in the holotype, which was collected by day; accordingly, we sus- Papenfuss for commenting on the manuscript, and Twan Leenders pect the species presents alternative coloration by night (Fig. 3a) for field observations and allowing us to use his excellent photo- graph (Fig. 2b). and day, being slightly darker by day as well as under stressful conditions (Fig. 3b). We additionally observed MVZ 264228 using its prehensile tail proficiently as a fifth limb. MVZ 264228 con- Literature Cited stitutes the second published specimen of Bolitoglossa insularis and extends the known altitudinal range of the species by 250 m AmphibiaWeb 2012. Information on Amphibian Biology and Conser- (Köhler 2011; Sunyer and Köhler 2010; Sunyer et al. 2008), thus vation. University of California, Berkeley (http://amphibiaweb. with a total elevational range of 800–1050 m. Unconfirmed sight org/). Accessed 29 June 2012. records of local rangers and tourist guides indicate the presence Carriker, M. A., Jr. 1910. An annotated list of the birds of Costa Rica including Cocos Island. Ann. Carnegie Mus. 6(3):314–970. of this species at even higher altitudes, and the species likely oc- Dunn, E. R. 1926. The Salamanders of the Family Plethodontidae. curs all over the upper portions of this 1394 m elevation, humid Smith College Fiftieth Ann. Publ. 7. Smith College, Northampton, and forested volcano. Massachusetts. 441 pp. Günther, A. C. L. G. 1885–1902. Biologia Centrali-Americana: Reptilia Bolitoglossa mombachoensis: NICARAGUA: GRANADA: and Batrachia. Taylor and Francis, London. 329 pp., Plates 1–76. Reserva Natural Volcán Mombacho (11.83831°N, 85.99277°W), Holdridge, L. R. 1967. Life Zone Ecology. Rev. ed. Tropical Science 875 m elev. (see Fig. 1). 18 November 2009. J. Sunyer and L. A. Center, San José. 206 pp. Obando. Adult female (MHUL 007). The specimen was found Jansen, M., and G. Köhler. 2001. Ökologie des Mombacho-Salaman- during the day in the central-most portion of Dracaena fragans ders, Bolitoglossa mombachoensis Köhler & McCranie, 1999, am (a plant locally used to delimit coffee plantation parcels), 1.5 m Volcán Mombacho, Nicaragua (Caudata: Plethodontidae). Sala- mandra 37(2):83–98. above the ground. It was collected along the road from Hacienda Köhler, G. 2011. Amphibians of Central America. Herpeton, Offen- El Progreso to the top of the volcano, at exactly the transitional bach. 379 pp. area between the coffee plantation and the reserve’s forest, in –––––, and J. R. McCranie. 1999. A new species of salamander from Premontane Moist Forest formation (Holdridge 1967). While Volcán Mombacho, Nicaragua, formerly referred to Bolitoglossa manipulating MHUL 007 we observed it could proficiently use striatula (Amphibia, Caudata, Plethodontidae). Sencken. Biol. its prehensile tail as a fifth limb. Although the species is, at this 79(1):89–93. premontane elevation, not as abundant as at higher altitudes, Parra-Olea, G., M. García-París, and D. B. Wake. 2004. Molecular diver- several other specimens were observed during the day in the sification of salamanders of the tropical American genus Bolito- same general area (875–900 m elevation) hidden in the apex of glossa (Caudata: Plethodontidae) and its evolutionary and biogeo- these plants (Fig. 4). This record extends the known altitudinal graphical implications. Biol. J. Linn. Soc. 81:325–346. Savage, J. M. 1974. Type localities for species of amphibians and rep- range of Bolitoglossa mombachoensis by 75 m (Köhler 2011), so tiles described from Costa Rica. Rev. Biol. Trop. 22(1):71–122. that the species is currently known to occur from 875–1345 m

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–––––. 2002. The Amphibians and Reptiles of Costa Rica: A Herpeto- Taylor, E. H. 1952. The salamanders and caecilians of Costa Rica. fauna between Two Continents, between Two Seas. Univ. Chicago Univ. Kansas Sci. Bull. 34(12):695–791. Press, Chicago, Illinois. 934 pp. –––––. 1954. Additions to the known herpetological fauna of Costa Sunyer, J., and G. Köhler. 2010. Conservation status of the herpetofau- Rica with comments on other species. No. I. Univ. Kansas Sci. Bull. na of Nicaragua. In L. D. Wilson, J. H. Townsend, and J. D. Johnson 36(9):597–639. (eds.), Conservation of Mesoamerican Amphibians and Reptiles, Villa, J. D. 1972. Anfibios de Nicaragua: Introducción a su Sistemáti- pp. 489–509. Eagle Mountain Publ., Eagle Mountain, Utah. ca, Vida y Costumbres. Instituto Geográfico Nacional & Banco –––––, S. Lotzkat, A. Hertz , D. B. Wake, B. M. Alemán, S. J. Robleto, and Central de Nicaragua, Managua. 216 pp. G. Köhler. 2008. Two new species of salamanders (genus Bolito- Wake, D. B., and J. F. Lynch. 1976. The distribution, ecology, and evolu- glossa) from southern Nicaragua (Amphibia, Caudata, Plethodon- tionary history of plethodontid salamanders in tropical America. tidae). Sencken. Biol. 88(2):319–328. Sci. Bull. Nat. Hist. Mus. Los Angeles Co. 25:1–65.

Herpetological Review, 2012, 43(4), 564–568. © 2012 by Society for the Study of Amphibians and Reptiles Morphometric Analyses and Ontogenetic Variation in a Neotropical Toad (Amphibia, Anura, Cycloramphidae)

The genus Proceratophrys, in the family Cycloramphidae or modified over time (Bartoletti et al. 1999; Jolicoeur 1963) and (Frost et al. 2006), was first described by Miranda-Ribeiro (1920) have greatly contributed to phylogenetic studies, by facilitating and comprises a group of generally similar anuran species (small descriptions of these structures and in identifying correspond- toads known locally as “horned frogs” or “bullfrogs”) that are of- ing body parts and organs that might otherwise have been con- ten confused with species of the genus Ceratophrys and Odon- sidered structurally independent and not homologous (Houck tophrynus (Amaro et al. 2009; Hoogmoed 1990; Izecksohn et 1990; Wiley 1981). Morphological studies generally focus on fac- al. 1979; Izecksohn and Peixoto 1981). Proceratophrys currently tors or structures that appear to have a significant importance comprises 24 species distributed throughout various morphocli- in the evolution of the structural or functional characteristics matic regions in South America (Frost 2011; Martins and Giaretta of animal, and ontogenetic studies often focus on allometric 2011; Napoli et al. 2011) and the species P. cristiceps (Fig. 1) stud- relationships and their ecological implications (Di Cerbo and ied here is found in the large Brazilian domain of semi-arid in- Biancardi 2010; Strauss and Altig 1992; Tejedo et al. 2010; With- termontane and interplain depressions known as the “Caatinga” ers and Hillman 2001)—thus extending the scope of descriptive (Ab’Saber 1977; Vieira et al. 2008). morphology. Very little information about Proceratophrys cristiceps is cur- As such, the current work contributes to our knowledge of rently available beyond its original description, although works the species Proceratophrys cristiceps by analyzing proportional- by Lynch (1971) and Vieira et al. (2007, 2008) focused on the os- ity in this species, describing the differences between the prin- teology of this species and provided descriptions of its tadpole cipal ontogenetic categories during the terrestrial phase of this phase and its morphometric variations. anuran, and discussing the probable ecomorphological signifi- Ontogenetic studies examining allometric variability in an- cance of the variations encountered. This information should be uran amphibians are not very common, and are practically useful in further studies of the systematics and ecology of this non-existent for the genus Proceratophrys, with publications genus, as well as other taxa of Neotropical toads. concerning this taxon being largely restricted to descriptions of their morphology (Giaretta and Sazima 1993; Izecksohn and Peixoto 1980; Martins and Giaretta 2011; Mercadal de Barrio and Barrio 1993; Napoli et al. 2011; Prado and Pombal 2008) or, more rarely, their ecology and natural history (Boquimpani-Freitas et al. 2002; Giaretta et al. 1998; Izecksohn and Peixoto 1996; Sazima 1978). Allometric studies of different body parts and organs have VIEIRA WASHINGTON BY PHOTO been used in mathematical models, which have been adapted

KLEBER S. VIEIRA* Programa de Pós-Graduação em Ciências Biológicas (Área de concentração em zoologia), Departamento de Sistemática e Ecologia, Universidade Federal da Paraíba, Campus I, Caixa Postal 5021, Cep 58051-970, João Pessoa, Paraíba, Brazil WASHINGTON L. S. VIEIRA Laboratório de Ecofisiologia Animal, Departamento de Sistemática e Ecologia, Universidade Federal da Paraíba, Campus I, Caixa Postal 5021, Cep 58051-970, João Pessoa, Paraíba, Brazil

*Corresponding author; e-mail: [email protected] Fig. 1. Adult individual of Proceratophrys cristiceps.

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