Herpetology Notes, volume 12: 721-723 (2019) (published online on 07 July 2019)

First record of the predation on Bell’s False Brook Salamander Isthmura belli (Gray, 1850) by the Yellow-throated Gartersnake Thamnophis pulchrilatus (Cope, 1885) in Western Mexico

Armando de Jesús Fraustros-Sandoval1, Aldo Dávalos-Martínez1, Verónica Carolina Rosas-Espinoza1, Ana Luisa Santiago-Pérez1,*, Paulino Ponce-Campos2, and Eliezer Iñiguez Ochoa3

The Yellow-throated Gartersnake (Thamnophis soil was extracted with heavy machinery. Thamnophis pulchrilatus) (Cope, 1885) is an endemic Mexican snake pulchrilatus is terrestrial with diurnal or twilight habits (Dixon and Lemos-Espinal, 2010; IUCN, 2019) that can (González-Hernández et al., 2016, Fernández-Badillo et reach 772 mm as total length (Rossman et al., 1996). al., 2016). Although, González-Hernández et al. (2016) Their populations are disjunct throughout its distribution: registered two individuals inactive on oak tree branches the northeastern-most ones are located in western and at 2.10 m and 4.96 m, respectively. It has been suggested southeastern Durango along the Sierra Madre Occidental, that it may prey on fish, anuran tadpoles and adults and Sierra Madre Oriental and the Trans-Mexican Volcanic other invertebrates like crabs, leeches, and earthworms Belt (Flores-Villela, 2007). Additionally, there are (Dixon and Lemos-Espinal, 2010). records of the species in isolated localities in Zacatecas, Bell’s False Brook Salamander (Isthmura bellii) (Gray, Aguascalientes, Guanajuato (Flores-Villela, 2007), San 1850) is a Mexican endemic salamander (Parra-Olea et Luis Potosí (Ramírez-Bautista et al., 2009), Tlaxcala al., 2010). It is classified as Threatened in the Mexican (Fernández et al., 2006) and Hidalgo (Fernández- law (SEMARNAT, 2010) and Vulnerable (VU) in the Badillo et al., 2016). It is associated to fir, pine (Dixon IUCN Red List (IUCN, 2019). It is the largest lungless and Lemos-Espinal, 2010), oak and pine-oak forest salamander with a maximum size of 360 mm in total (Dixon and Lemos-Espinal, 2010; González-Hernández length (Parra-Olea et al., 2005). Its main distribution is et al., 2016), tropical scrub forest ecotone and grassland along the highlands in western and southern margins (Carbajal-Marquez et al., 2014). This snake can tolerate of the Mexican plateau through Trans-Mexican some disturbance, given that Fernández-Badillo et al. Volcanic Belt, with numerous isolated populations (2016) registered an individual under a rock at the edge from the border area of Sonora and Chihuahua, and of a crop field next to an oak forest, and Ponce-Campos from central Tamaulipas, to the mountains of central (October 23, 2005) observed and individual under a Guerrero (Parra-Olea et al., 2005). According to rock in an altered pine-oak forest at northern edge of Bryson et al. (2018) Isthmura bellii show evidence Sierra de Tapalpa, where vegetation was removed, and to be paraphyletic and may comprise several cryptic species along its distribution, where the denominated I. sierraoccidentalis is part of the western clade which include Jalisco populations. It is associated to pine and pine-oak forest at high elevation, as well as forest edges 1 Universidad de Guadalajara, Centro Universitario de Ciencias and grazed areas (Parra-Olea et al., 2010; Bryson et al., Biológicas y Agropecuarias, C.P. 45200 Zapopan, Jalisco, 2018). It is diurnal (Ramírez-Bautista et al., 2014) and México. can be seen active near the water or hiding in humid 2 Bosque Tropical, Investigación para la Conservación de la microhabitat as under rocks and trunks or inside dead Naturaleza, A. C. Misión San Antonio, Torre 4a, depto. 2, logs (Santiago-Pérez et al., 2012; Quintero-Díaz et al., C.P. 45030 Zapopan, Jalisco, México. 2014; Bryson et al., 2018). 3 UMA San Javier. Prolongación Morelos # 107, Tapalpa, Jalisco, México. As part of the project titled “Checklist of the * Corresponding author. E-mail: herpetofauna in the Sierra de Tapalpa, Jalisco, Mexico”, [email protected] we conducted diurnal and nocturnal monthly surveys 722 Armando de Jesús Fraustros-Sandoval et al. on an elevational gradient looking for amphibians and 1854) tadpoles and frogs (Carbajal-Márquez et al., reptiles. On June 9, 2018 at 10:30 h we flipped a fallen 2014; Ramírez-Bautista et al., 2014) and Dryophytes dead trunk on the ground and observed an adult T. plicatus (Brocchi, 1877) (Ramírez-Bautista et al., 2014). pulchrilatus (MZFZ-IMG-179) (Fig. 1A). The habitat In Tapalpa, we recorded 11 anuran species (10 frogs was pine-oak forest on a humid slope with north-west and one toad). We registered tadpoles of Lithobates exposure (20.011365°N, -103.813137°W, 2,335 m neovolcanicus (Hillis & J. S. Frost, 1985), Lithobates a.s.l.). When the snake was found, it was immediately psilonota (Webb, 2001), Dryophytes arenicolor Cope captured with the hand. It tried to flee and secreted musk 1866 and D. eximius in the streams at the pine oak but did not bite. We kept it temporarily in a cloth bag to forest. It is possible that T. pulchrilatus prey on the take measurements and photographs. Later, inside the tadpoles of all these anurans. Dryophytes eximius has cloth bag, the snake regurgitated a partially digested been reported previously as part of the diet of this I. bellii without a tail (MZFZ-IMG-180) (Fig. 1B). Gartersnake (Carbajal-Márquez et al., 2014; Ramírez- Measurements of T. pulchrilatus included a Snout–vent Bautista et al., 2014), so it could be part of the diet in length (SVL) of 510 mm, Tail length = 150 mm, Head Tapalpa, but in our records this frog was not abundant width = 15 mm, Head height = 10 mm, Head length = 21 at the pine oak forest. Thamnophis pulchrilatus preying mm and Mass = 63 g. The I. bellii had SVL = 84.4 mm, on I. belli is related to the fact that this salamander is Head width = 11.1 mm, Head height = 5.5 mm, Head distributed from 750 to 3,300 m a.s.l. (Parra-Olea et al., length = 12.8 mm and Mass = 4 g. The Thamnophis 2010; Bryson et al., 2018) and associated to a variety pulchrilatus individual was released by the night of that of habitats including temperate forest what makes it day in the same place of capture. an available prey. Although, this salamander is not In Sierra de Tapalpa, T. pulchrilatus was observed in abundant in temperate forest in Sierra de Tapalpa. Over pine-oak forests at 2,335 m a.s.l. This record is similar a year, we observed a total of seven individuals (two to others, where this snake was reported in a grassland adults and five juveniles) in the pine oak forest and oak with patches of oak forest and tropical scrub forest forest from 1,938 to 2,497 m a.s.l. They were registered ecotone at 2,002 m a.s.l. (Fernández-Badillo et al., under stones and trunks, inside tree bark, on rock with 2016), in the edge of a crop field near oaks at 2,332 moss and in a puddle, but an individual of Isthmura m a.s.l. (Carbajal-Márquez et al., 2014) and on an oak bellii was found under the bark of a tree prostrated one tree at 3,054 m a.s.l. (González-Hernández et al., 2016), meter above the ground at the edge of a spring. So, it although it can be observed from 1,372 m a.s.l. (Dixon could be possible that T. pulchrilatus look for prey not and Lemos-Espinal, 2010). only on the ground but on trees. This behaviour was Dixon and Lemos-Espinal (2010) suggested that T. mentioned by González-Hernández et al. (2016) to pulchrilatus may eat anurans among other prey. The explain the arboreal habit of this snake. species is known to feed on Dryophytes eximius (Baird,

Figure 1. (A) Thamnophis pulchrilatus adult in Sierra de Tapalpa, Jalisco State, México. (B) Isthmura bellii partially digested, without tail. Photos by Aldo Dávalos. First record of the predation on Isthmura belli by Thamnophis pulchrilatus 723

In the study area, we also recorded two other snakes González-Hernández, A. Moro-Hernández, D.M., Cruz, that can prey on I. bellii, the Black-necked Snake J.A. (2016): Distribución y uso de hábitat de Thamnophis Thamnophis cyrtopsis (Kennicott, 1860) that inhabits pulchrilatus (Cope, 1855) en Chignahuapan, Puebla, México. Acta Zoologica Mexicana Acta Zoológica Mexicana (n.s.) pine-oak and oak forests between 1,850 and 2,000 m 32(3): 390–392. a.s.l. and a snake of the genus Rhadinaea in the pine IUCN (2019): Isthmura bellii. The IUCN Red List of Threatened forest at 2,450 m a.s.l. However, T. cyrtopsis has also Species. Version 2018-2. Available at: http://www.iucnredlist. been reported at higher elevations from 1,900 to 2,300 org Accessed on 6 January 2019. m a.s.l. (Santiago-Pérez et al., 2012) and it is known Parra-Olea, G., García-Paris, M., Papenfuss, T. J., Wake, D. B. that it includes in its diet tadpoles and adults of toads (2005): Systematics of the Pseudoeurycea bellii (Caudata: Plethodontidae) Species Complex. Herpetologica 61(2): 145– Anaxyrus punctatus (Baird and Girard, 1852) and frogs 158. D. arenicolor and Lithobates yavapaiensis (Platz and Parra-Olea, G., Wake, D., Hanken, J., Ponce-Campos, P. (2010): J. S. Frost, 1984). Also Mendoza-Quijano et al. (1995) Isthmura bellii (errata version published in 2016). The IUCN recorded a Pine-Oak Snake Rhadinaea taeniata (Peters, Red List of Threatened Species 2010: e.T59371A89371275. 1863) that fed on I. bellii. Available at: http://dx.doi.org/10.2305/IUCN.UK.2010- 2.RLTS.T59371A11923949.en. Accessed on 6 January 2019. Acknowledgments. We are grateful to Sierra Mazati A.C. Mendoza-Quijano, F., Loeza-Corichi, A., Flores-Villela, O. (1995): for funding support to Fraustos-Sandoval bachelor thesis; Pseudoerycea bellii belli (NCN). Predation. Herpetological U. O. García-Vázquez for depositing the photographs in the Review 26(3): 142. herpetological collection del Museo de Zoología Facultad de Quintero-Díaz, G.E.; Carbajal-Márquez, R.A., Sigala-Rodríguez, Estudios Superiores Zaragoza, Universidad Nacional Autónoma J. (2014): Pseudoerycea bellii (Bell’s Salamander). Geographic de México (MZFZ-UNAM); L. Canseco-Márquez for the distribution. Herpetological Review 45(4): 651. taxonomic support and E. F. Fanti-Rodríguez for the opportunity Ramírez-Bautista, A., Hernández-Salinas U., García-Vázquez to visit his land in Tapalpa. Permits for specimen handling were U.O., Leyte-Manríquez, A., Canseco-Márquez, L. (2009): issued by the Mexican Wildlife Agency, Dirección General de Herpetofauna del Valle de México: Distribución y Conservación. Vida Silvestre of the Secretaría de Medio Ambiente y Recursos Universidad Autónoma del Estado de Hidalgo – CONABIO, Naturales (permit number: SGPA/DGVS/01148/16). México. 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