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NATURE NOTES Amphibia: Anura Shrinking behavior in Pristimantis pardalis (Amphibia: Anura: Craugastoridae) from Costa Rica

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NATURE NOTES Amphibia: Anura Shrinking behavior in Pristimantis pardalis (Amphibia: Anura: Craugastoridae) from Costa Rica Toledo et al. (2010) defined two main defensive behaviors in amphibians, depending
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NATURE NOTES Amphibia: Anura Shrinking behavior in Pristimantis pardalis (Amphibia: Anura: Craugastoridae) from Costa Rica Toledo et al. (2010) defined two main defensive behaviors in amphibians, depending upon the response of the prey to a certain aggressive stimulus by the predator. The most common and well known of these behaviors is death feigning (thanatosis), which is used as a defensive strategy by many species of amphibians, reptiles, and mammals to avoid predation by assuming a dead posture (Edmunds, 1974; Caro, 2014). For anurans, thanatosis can be defined as follows: the posture is motionless, even when the animal is touched, the limbs are loose, and the eyes usually are open. This behavior mostly is used by non-toxic terrestrial and semi-arboreal anurans. Another passive defensive behavior is what Toledo et al. (2010) called shrinking, which is used mostly by toxic terrestrial and arboreal anurans and can be defined as: the posture is motionless and the eyes usually remain closed, the arms and forelimbs are bent and maintained close to the body, and generally contracted against the belly. The genus Pristimantis is the largest known genus of terrestrial vertebrates (Padial et al. 2014). To date, passive or aggressive behaviors (thanatosis or shrinking) have not been reported for any species in this genus (Toledo et al. 2010; L. Toledo, pers. comm.). Herein we report a case of shrinking behavior in Pristimantis pardalis (Barbour, 1928), which entailed some peculiarities. This species is little known and almost no data is available on its biology and habitat, other than it is nocturnal and found on low vegetation within dense forest in the Premontane Rainforest zone, and that it occurs from southern Costa Rica to eastern Panama at elevations from 50 to 1,450 m (Savage, 2002; Leenders, 2016). In appearance this frog is small (males up to 19 mm, females up to 29 mm) with a dark gray to black dorsum and dark brown venter (according to Savage, 2002; but see ventral coloration in images below), with white and black flash markings on the groin (Savage 2002, Leenders 2016). Recently, an individual in Panama was found infected with carnivorous fly larvae that were in the process of consuming its intestines (Leenders, 2016). While walking in Premontane Wet Forest (Savage, 2002) at Casa Tordesillas, Socorro de Platanares, Provincia de San José, Costa Rica (9 12'30 N, 83 41'01 W; elev. 988 m), we observed five individuals of P. pardalis. Two of them were females, and both acted in a similar fashion. The first female was perched vertically on a dry leaf at a height of 1.5 m (Fig. 1A). After photographing the frog for less than 1 min it appeared to release its grip and fell into the leaf litter, where it remained motionless with the limbs contracted against the body (Fig. 1B, C). This behavior lasted for several minutes, and at that point we placed the frog on a leaf to take more photographs. During this time it also remained motionless. We did not detect any specific odor during the encounter. Soon after we came across another female that displayed similar behavior. This individual was perched horizontally on a green leaf, and when we approached it contracted its body and remained motionless but did not fall into the leaf litter. Subsequently, we encountered three males, and none displayed death-feigning or shrinking behavior. After accidentally contacting one of these frogs with the lens of a camera, it jumped for at least 1 m; however, we could not locate the animal to see if he had undergone any apparent physical changes. The other two males we came across were difficult to photograph because they kept walking away slowly (Fig. 1D), and neither displayed shrinking behavior. We cannot provide a clear explanation as to why only the two females displayed this behavior, whereas the three males escaped by jumping or walking away. The proposed shrinking behavior described by Toledo et al. (2010) normally is used by toxic species such as bufonids, and some hylids and phyllomedusids. In this case we do not have information on the toxicity of P. pardalis, although the black and white flash markings on the groin area of this species might be used to deter predators. The individuals that underwent the shrinking behavior, however, did not show their flash markings. Further, the two female P. pardalis did not close their eyes when displaying the shrinking behavior, as occurs with most species known to use this type of defensive mechanism (Toledo et al, 2010). Mesoamerican Herpetology 410 Nature Notes Fig. 1. Adult individuals of Pristimantis pardalis found at Casa Tordesillas, Socorro de Platanares, Provincia de San José, Costa Rica. (A) An adult female found in a vertical position on a dry leaf; (B) the same individual after falling to the ground, displaying shrinking behavior; (C) the second female displaying shrinking behavior; and (D) an adult male on a leaf prior to leaving the scene. ' Cesar Barrio-Amorós Literature Cited Caro, T Antipredator deception in terrestrial vertebrates. Current Biology 60: Edmunds, M Defence in Animals: A Survey of Anti- Predator Defences. Longmans, London, United Kingdom. Leenders. T Amphibians of Costa Rica: A Field Guide. A Zona Tropical Publication, Comstock Publishing Associates, Cornell University Press, Ithaca, New York, United States. Padial, J. M, T. Grant, and D. Frost Molecular systematics of terraranas (Anura; Brachycephaloidea) with an assessment of the effects of alignment and optimality criteria. Zootaxa 3,825: Savage, J. M The Amphibians and Reptiles of Costa Rica: A Herpetofauna between Two Continents, between Two Seas. The University of Chicago Press, Chicago, Illinois, United States. Toledo, L. F., I. Sazima, and C. F. B. Haddad Is it all death feigning? Case in Anurans. Journal of Natural History 44: 1,979 1,988. César L. Barrio-Amorós and Esther Barrio-Amorós Doc Frog Expeditions, Uvita, Costa Ballena, Costa Rica. Mesoamerican Herpetology 411 Nature Notes Amphibia: Caudata Clutch size of Ambystoma velasci (Dugès, 1888) in situ, from Guanajuato, Mexico. The genus Ambystoma in Mexico is represented by 18 species, of which 17 are country endemics (Wilson et al., 2013; Parra-Olea et al., 2014). The Plateau Tiger Salamander (A. velasci), one of these endemics, is distributed in northwestern Chihuahua along the eastern flanks of the Sierra Madre Occidental, southern Nuevo León to Hidalgo in the Sierra Madre Oriental, west to Zacatecas, and south into the Trans-Mexican Volcanic Belt (Frost, 2017), at elevations from 1,200 to 3,600 m (Lemos-Espinal and Dixon, 2013; Ramírez-Bautista et al., 2014; and references therein). Unfortunately, little information is available on the reproductive biology of this species, and here we provide information on a clutch of eggs and the larvae of A. velasci observed in the wild. On 7 January 2017 at 1653 h, two of us (BDLCB, ALM) found a cluster of eggs of A. velasci that apparently were deposited by a single female in a permanent pond (Fig. 1) in the village of El Ocotero, Municipio de Xichú, Guanajuato, Mexico ( N, W; WGS 84; elev. 2,341 m). The pond is elongated in shape (4 1.5 m) with an average depth of 60 cm, and is located in an area containing remnants of pine-oak forest. A total of 53 eggs were observed, of which some had embryos in the last stage of development (Fig. 2) and others were in the process of hatching. The eggs were found approximately 12 cm from the surface in vegetation at the edge of the pond; the water temperature was 9.4 C. Ramírez-Bautista, et al. (2014) indicated the clutch size of A. velasci as fewer than 100 eggs; these records, however, were obtained from captive individuals (A. Ramírez-Bautista, pers. comm.). Conversely, Lemos-Espinal and Dixon (2013: 23) noted that, some 5,000 eggs are deposited a few centimeters under the water, singly, in rows, or in small clusters, which hatch in about two weeks. It is unclear, however, if these eggs were from a single clutch or from clutches deposited by several females. Fig. 1. The pond where the eggs of Ambystoma velasci were found, at El Ocotero, Municipio de Xichú, Guanajuato, Mexico. ' Adrian Leyte-Manrique The number of eggs for A. mexicanum, A. granulosum, and A. lermaense has been reported to range from 300 to 900, 64 to 1,182, and 111 to 1,691, respectively (Salthe, 1969; Kaplan 1980; Aguilar-Miguel et al., 2009). These numbers, however, were based on captive individuals. Our observation provides a precise number for an egg clutch of A. velasci that presumably was deposited by a single female in the wild. From the conservation perspective, this species has been negatively affected by the loss of habitat and contamination resulting from human settlements Mesoamerican Herpetology 412 Nature Notes (Ramírez-Bautista et al., 2014), and these threats also are present in Guanajuato. Currently, this species is regarded as Least Concern by the IUCN (Shaffer et al., 2010), as Subject to Special Protection by SEMARNAT (2010), and Wilson et al. (2013) assessed it an Environmental Vulnerability Score (EVS) of 10, placing it in the lower portion of the medium vulnerability category. Fig. 2. A close-up of the developing eggs deposited by an Ambystoma velasci. ' Kevin Herroz-Hiriart Acknowledgments. We are grateful to Kevin Herroz-Hiriart for field assistance, and for providing photographic material. Literature Cited Aguilar-Miguel, X., G. Legorreta B., and G. Casas-Andreu Reproducción ex situ en Ambystoma granulosum y Ambystoma lermaense (Amphibia: Ambystomatidae). Acta Zoológica Mexicana 25: Frost, D. R Amphibian Species of the World: an Online Reference. Version 6.0 American Museum of Natural History. New York, United States. (www.research.amnh.org/ herpetology/amphibia/index.html; accessed 19 April 2017). Kaplan, R. H The implications of ovum size variability for offspring fitness and clutch size within several populations of salamanders (Ambystoma). Evolution Lemos-Espinal J. A., and J. R. Dixon Amphibians and Reptiles of San Luis Potosí. Eagle Mountain Publishing, LC, Eagle Mountain, Utah, United States. Parra-Olea G., O. Flores-Villela, and C. Mendoza-Almeralla Biodiversidad de anfibios en México. Revista Mexicana de Biodiversidad 85: S460 S466. Ramírez-Bautista, A., U. Hernández-Salinas, R. Cruz-Elizalde, C. Berriozabal-Islas, D. Lara-Tufiño, I. G. Mayer-Goyenechea, and J. M. Castillo-Cerón Los Anfibios y Reptiles de Hidalgo, México: Diversidad, Biogeografía y Conservación. Sociedad Herpetológica Mexicana, A.C., Mexico. Salthe, S. E Reproductive modes and the number and sizes of ova in the Urodeles. The American Midland Naturalist 81: Shaffer, B., G. Parra-Olea, D. Wake, and P. Ponce-Campos Ambystoma velasci. The IUCN Red List of Threatened Species 2010: e.t59073a (www.iucnredlist.org; accessed 22 April 2017). SEMARNAT (Secretaría de Medio Ambiente y Recursos Naturales) Norma Oficial Mexicana NOM-059- SEMARNAT-2010, protección ambiental-especies nativas de México de flora y fauna silvestre-categorías de riesgo y especificaciones para su inclusión, exclusión o cambio-lista de especies en riesgo. Diario Oficial de la Federación. Ciudad de México, Mexico. Wilson, L. D., J. D. Johnson, and V. Mata-Silva A conservation reassessment of the amphibians of Mexico based on the EVS measure. Amphibian and Reptile Conservation 7: Mesoamerican Herpetology 413 Nature Notes Belinda De La Cruz-Beltrán 1, Adrian Leyte-Manrique 2, and Vicente Mata-Silva 3 1 Facultad de Ciencias Naturales, Universidad Autónoma de Querétaro, Avenida de las Ciencias S/N. Col. Juriquilla, Querétaro, Mexico. 2 Laboratorio de Biología, Tecnológico Nacional de México, Campus Salvatierra. Manuel Gómez Morín 300, C.P , Janicho, Salvatierra, Guanajuato, Mexico. 3 Department of Biological Sciences, The University of Texas at El Paso, El Paso, Texas , United States. Bolitoglossa yucatana. (Peters, 1882). Troglodytism. The Yucatan Mushroom-tongued Salamander, Bolitoglossa yucatana, is endemic to the Yucatan Peninsula and often is associated with limestone sinks called cenotes (Lee, 2000). Lee (1996) noted that in spite of its fully webbed feet this appeared to be a terrestrial species, but an adult individual later was found inside a large tank bromeliad (Aechmea bracteata) at a height of 4 m above the ground (Calderón et al., 2003; Galindo-Leal et al., 2003), suggesting that its habits are arboreal as well. Lee (2000) indicated that surface activity in B. yucatana likely is restricted to the rainy season. Known records correspond to specimens found in terrestrial situations: in shallow soil at the base of tree stump, beneath surface debris in thorn forest, on roads at night in tropical evergreen forest, and beneath a log at the edge of a cenote (see Lee, 1996, and references therein). Lee (1996: 45) also noted that, these salamanders probably sequester themselves deep within the recesses of the karsted limestone that abounds throughout their range. On 13 August 2015 at 1230 h, while conducting a tour one of us (CCC) found an adult B. yucatana (Fig. 1) on limestone about 150 m from the entrance of a cave system called Pool Tunich or Cavernas del Río Secreto, Municipio de Solidaridad, Quintana Roo, Mexico (20 35'19.87 N; 87 08'05.67 W; WGS 84; elev. 8 m). A photographer who continually was exploring the site in those days mentioned that this individual had spent at least 15 days in the same location. The surrounding habitat at the entrance of the cave is a combination of tropical evergreen forest and secondary vegetation. Fig. 1. An adult Bolitoglossa yucatana observed about 150 m from the entrance of the cave system called Cavernas del Río Secreto, Municipio de Solidaridad, Quintana Roo, Mexico. ' Cecilia Cahum-Cahum Mesoamerican Herpetology 414 Nature Notes To date 14 species of amphibians, all Nearctic salamanders from the United States (genera: Ensatina, Eurycea, Gyrinophilus, Hydromantes, Plethodon and Pseudotriton), are known to temporally or exclusively inhabit caves or live in groundwater (Fenolio, 2016). To our knowledge, this is the first confirmed report of troglodytism in B. yucatana, a Neotropical species. Acknowledgments. We thank Louis Porras for comments that helped improve the manuscript. Literature Cited Calderon, R., Cedeño-Vázquez, J. R., and C. Pozo Geographic Distribution. New distributional records for amphibians and Reptiles from Campeche, México. Herpetological Review 34: Fenolio, D Life in the Dark. Johns Hopkins University Press, Baltimore, Maryland, United States. Galindo-Leal, C., Cedeño-Vázquez, J. R., Calderón, R., and J. Augustine Arboreal frogs, tank bromeliads and disturbed seasonal tropical forest. Contemporary Herpetology 2003: 1 8. Lee, J. C The Amphibians and Reptiles of the Yucatán Peninsula. Comstock Publishing Associates, Cornell University Press, Ithaca, New York, United States. Lee, J. C A Field Guide to the Amphibians and Reptiles of the Maya World: The Lowlands of Mexico, Northern Guatemala, and Belize. Comstock Publishing Associates, Cornell University Press, Ithaca, New York, United States. J. Rogelio Cedeño-Vázquez 1 and Cecilia Cahum-Cahum 2 1 El Colegio de la Frontera Sur, Unidad Chetumal, Av. Centenario Km. 5.5, C.P Chetumal, Quintana Roo, Mexico. s: and (Corresponding author) 2 Centro Recreativo Río Secreto. Carr. Federal Chetumal-Puerto Juárez Km. 283, Ejido Sur, C.P Playa del Carmen, Quintana Roo, Mexico. Reptilia: Crocodylia Crocodylus acutus (Cuvier, 1807). Ectoparasitism. Crocodylus acutus is the most widely distributed crocodylian in the New World, as it inhabits coastal and lowland wetlands from Florida to the limits of mangrove forest in Peru (Thorbjarnarson et al., 2006). This species is listed as Vulnerable by the International Union for Conservation and Nature (IUCN), and in Appendix I of the Convention on International Trade in Endangered Species (CITES). Belize once was a stronghold for the overall regional population of this species, but habitat destruction and pollution have become a threat. Consequently, the national status of C. acutus is under government review for listing this species as Endangered. In Belize, C. acutus primarily is found along the coast, as well as throughout the cayes and offshore atolls (Thorbjarnarson et al., 2006), but development along the coast (prime habitat for C. acutus) keeps pushing this species farther inland into historical C. moreletii territory (M. Tellez, unpublished). As C. acutus keeps dispersing it likely will encounter a new array of prey and parasites, and thus alter the existing host parasite dynamics of inland aquatic ecosystems. Leeches are generalist parasites of crocodylians that commonly are found in or around the mouth of their hosts; a few records of these ectoparasites, however, have been observed on the neck, legs, or abdomen of individuals (Tellez, 2013). The majority of the documented leeches are from the family Glossiphoniidae, a group of freshwater ectoparasites characterized by using their proboscis to feed off the blood of their vertebrate hosts (Sawyer, 1986). Species from this family of leeches are known vectors of such blood parasites as Placobdella multilineata, which Mesoamerican Herpetology 415 Nature Notes is known to infect Alligator mississippiensis with the blood parasite Haemogregarina crocodilinorum (Cherry and Ager, 1982). To date, leeches and the blood parasites they transmit have not been documented to have ill effects on wild crocodylians. On 6 Jan 2017, the reptile keepers at The Belize Zoo noticed leeches inside and outside the mouth of Brutus, a 3.3 m (total length) male C. acutus (Fig. 1A, B). The crocodile enclosure measures approximately 11 m 6 m and about 3 m deep at its deepest point, and gradually becomes shallower near the banks. The water in the enclosure consists of a combination of rainwater and water pumped in from a freshwater holding pond located approximately 0.4 km west of the zoo. The substrate of the enclosure consists primarily of nutrient poor clay soils and natural vegetation. Through inspection via binoculars and photographs, the leech appears to be from the family Glossiphoniidae; however, we did not retrieve the ectoparasites, and thus this identification is tentative. To date, this is the first record of leeches parasitizing a crocodile in Belize, and the second record of leeches observed on a C. acutus from throughout its range (García-Grajales and Buenrostro-Silva (2011). Fig. 1. (A) Leeches (circled) parasitizing the mouth of a Crocodylus acutus at the Belize Zoo, located 47 km west of Belize City; and (B) mouth a close-up of a leech parasitizing the lower jaw of the animal. ' Danni Brianne Mesoamerican Herpetology 416 Nature Notes Acknowledgments. We thank The Belize Zoo Animal Management Supervisors Tim Sho and Humberto Wohlers for discovering the leeches, and collaborating with the Crocodile Research Coalition on this finding. Literature Cited Cherry, R. H., and A. L. Ager Parasites of American Alligators (Alligator mississippiensis) in south Florida. Journal of Parasitology 68: García-Grajales, J. and A. Buenrostro-Silva Infestación y distribución corporal de sanguijuelas en el Cocrodrilo Americano (Crocodylus acutus Cuvier 1807) del Estero La Ventanilla, Oaxaca, México. Acta Zoológica Mexicana (n.s.) 27: Sawyer, R. T Leech Biology and Behaviour: Volume II, Feeding Biology, Ecology, and Systematics. Oxford University Press, Oxford, England, United Kingdom. Tellez, M A Checklist of Host-Parasite Interactions of the Order Crocodylia. University of California Publications in Zoology, Volume 136, University of California Press, Berkeley, California, United States. Thorbjarnarson, J., F. Mazzotti, E. Sanderson, F. Buitrago, M. Lazcano, K. Minkowski, M. Muñiz, P. Ponce, L. Sigler, R. Soberon, A. M. Trelancia Regional habitat conservation priorities for the American Crocodile. Biological Conservation 128: Marisa Tellez 1, Sharon Matola 2, and Danni B
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