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(Amphibia: Eleutherodactylidae) As Prey Of Use the following type of citation: North-western Journal of Zoology 2021: e217505 Paper Submitted to The North-Western Journal of Zoology 1 *Handling editor: Yurii Kornilev 2 *Manuscript Domain: Herpetology of the Americas 3 *Manuscript code: NwJZ_21_HA_04 4 *Submission date: 02_03_2021 5 *Revised: 09_06_2021 6 *Accepted: 05_08_2021 7 *No. of words (without abstract, acknowledgement, references, tables, captions): 1330 8 (papers under 700 words are not accepted) 9 *Editors only: 10 11 Title of the paper: Molecular identification of the Jalisco Trilling Frog Eleutherodactylus 12 jaliscoensis (Amphibia: Eleutherodactylidae) as prey of theZoology Garter Snake Thamnophis of 13 cyrtopsis (Squamata: Colubridae) proofing 14 Journal 15 Running head: Eleutherodactylus jaliscoensis as preyuntil of Thamnophis cyrtopsis 16 paper 17 Authors (First LAST - without institution name!): Raquel HERNÁNDEZ-AUSTRIA, Ángel Fernando 18 SOTO-POZOS, Omar BECERRA-SORIA, Abigail MORA-REYES, Gabriela PARRA- 19 OLEA North-western Accepted 20 21 Key Words (at least five keywords): Mexico, endemism, relationship predator-prey, diet, 22 mtDNA16S. 23 24 No. of Tables: 0 25 No. of Figures: 3 26 No. of Files (landscape tables should be in separate file): 1 Use the following type of citation: North-western Journal of Zoology 2021: e217505 nwjz-2 27 Molecular identification of the Jalisco Trilling Frog Eleutherodactylus jaliscoensis 28 (Amphibia: Eleutherodactylidae) as prey of the Garter Snake Thamnophis cyrtopsis 29 (Squamata: Colubridae) 30 Raquel HERNÁNDEZ-AUSTRIA1,2, Ángel Fernando SOTO-POZOS1,2, Omar BECERRA- 31 SORIA1,2, Abigail MORA-REYES3 and Gabriela PARRA-OLEA1,* 32 33 1. Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de 34 México, A.P. 70-153, Ciudad Universitaria, C.P. 04510, Mexico City, Mexico. 35 2. Posgrado en Ciencias Biológicas, Unidad de Posgrado, Edificio A, 1° Piso, Circuito de 36 Posgrados, Ciudad Universitaria, Coyoacán, C.P. 04510, Mexico City, Mexico. Zoology 37 3. Universidad Veracruzana, Facultad de Ciencias Biológicas y Agropecuarias, Campus of 38 Peñuela, camino Peñuela-Amatlán, S/N Peñuela Amatlán de los Reyes, C.P. 94945, Veracruz, proofing 39 Mexico. Journal 40 until 41 *Corresponding author, Gabriela Parra-Olea, E-mail: [email protected] paper 42 43 Abstract. We report the predation of the recently described and poorly know frog 44 Eleutherodactylus jaliscoensisNorth-western by the snake Thamnophis cyrtopsis employing a mitochondrial Accepted 45 marker molecular and morphological evidence. We discuss the importance of frogs in food 46 webs and the use of sequences de DNA in the identification of frogs. 47 48 Key Words: Mexico, endemism, predator-prey relationship, diet, mtDNA16S. 49 Running title: Eleutherodactylus jaliscoensis as prey of Thamnophis cyrtopsis 50 Use the following type of citation: North-western Journal of Zoology 2021: e217505 nwjz-3 51 Direct developing frogs of genus Eleutherodactylus are one of the most diverse groups of 52 vertebrates in the Neotropics with more than 200 species described (Lynch & Duellman 1997, 53 AmphibiaWeb 2021, Frost 2021), which are distributed from the southern USA to northern 54 Argentina (Padial et al. 2014). In Mexico, there are 37 described species of Eleutherodactylus 55 classified in the subgenus Syrrhophus (Hedges et al. 2008, Grünwald et al. 2021), with most 56 of them having a restricted distribution. 57 The Jalisco Trilling Frog Eleutherodactylus (Syrrhophus) jaliscoensis is an endemic species 58 to the state of Jalisco, Mexico. This species is distributed in pine-oak forests in the Sierra 59 Mascota, Sierra Cuale, and Sierra Cacoma within the Transmexican Volcanic Belt 60 biogeographic province, ranging from 1,700 to 2,300 m a.s.l. (Grünwald et al. 2018). This Zoology 61 species has been collected at ground level among oaks, pines, and herbaceous plants of 62 (Grünwald et al. 2018). Eleutherodactylus jaliscoensis is an endangered species according to proofing 63 the IUCN Red List of Threatened Species (2021); but it is not included in the list of species at Journal 64 risk of the Norma Oficial Mexicana NOM-059-SEMARNAT-2010.until Being a recently 65 described species, little is known about the biotic interactions and its natural history, as well paper 66 as its predators and prey, and other aspects of basic biology. 67 The distribution of E. jaliscoensis is immersed in the distribution of the Black-necked Garter 68 Snake Thamnophis cyrtopsisNorth-western, a widely distributed snake from the southern United States, Accepted 69 through Mexico to Guatemala, in vast types of environments ranging from tropical, 70 temperate, to arid climates, and elevations from sea level to 3,000 m a.s.l. (Wilson & Johnson 71 2010). In the highlands, T. cyrtopsis prefers mountain streams but in summer rains sometimes 72 it is found some distances from permanent water (Stebbins 1954). This species is considered 73 an aquatic-foraging generalist and feeds on a wide variety of prey, including semi-aquatic and 74 terrestrial organisms (Jones 1990). Amphibian prey reported for T. cyrtopsis included adult 75 and larvae of Lithobates catesbeianus, possibly some larvae of L. pipiens (Fleharty 1967), Use the following type of citation: North-western Journal of Zoology 2021: e217505 nwjz-4 76 adult of L. chiricahuensis, L. yavapaiensis, and Dryophytes arenicolor (Jones 1990, McCall et 77 al. 2017). 78 Here we report both the first record of consumption of E. jaliscoensis by the snake T. 79 cyrtopsis, and in turn, some prey items consumed by this species of frog. Our observation 80 provides an important addition to the natural history and knowledge of predator-prey 81 relationships of E. jaliscoensis and T. cyrtopsis. 82 During a nocturnal field survey in August 2019 to collect individuals of E. jaliscoensis in the 83 type locality (Sierra Mascota, 20°41'51.52” N, 104°52'0.72” W, datum WGS84, 2,083 m 84 a.s.l.; Fig. 1), Jalisco, Mexico, we collected a E. jaliscoensis (IBH32593) and a T. cyrtopsis 85 (IBH32595). The E. jaliscoensis was found on the forest floor devoid of bushes, while T. Zoology 86 cyrtopsis was found under a rock amongst many bushes around. We obtained liver tissue from of 87 each specimen and stored in RNAlaterTM Tissue Storage Reagent. The specimens were proofing 88 killed with an overdose of sodium pentobarbital, fixed in 10% formalin solution, and Journal 89 preserved in 70% ethanol and deposited in the Colecciónuntil Nacional de Anfibios y Reptiles 90 (CNAR), Instituto de Biología, Universidad Nacional Autónoma de México. paper 91 We found the remains of a frog in the T. cyrtopsis' stomach (Fig. 2A). The posterior region of 92 the frog was in good condition; therefore, we obtained a sample of muscle tissue from the 93 thigh, which we molecularlyNorth-western analyzed for taxonomic identification. Additionally, we Accepted 94 reviewed the remaining parts using a Carl Zeiss (model 2004017913) dissecting microscope. 95 We extracted DNA from the thigh tissue using phenol-chloroform protocol (Sambrook & 96 Russell 2006) and sequenced a region of the 16S mitochondrial gene with the primers 16Sar 97 and 16Sbr (Palumbi et al. 1991). We aligned the new sequence with sequences of 18 98 Eleutherodactylus species including the sequence of the E. jaliscoensis type specimen 99 (accession number MG857003) from the GenBank online repository, using the MAFFT v.7 100 online (Katoh et al. 2019). We obtained the best nucleotide substitution models with Use the following type of citation: North-western Journal of Zoology 2021: e217505 nwjz-5 101 PartitionFinder v.1.1 (Lanfear et al. 2012), resulting in the GTR + I + G as the best. We 102 performed a Bayesian inference analysis in the MrBayes 3.2.3 program (Ronquist et al. 2012), 103 with two independents runs of 10,000 million generations each that were sample every 1,000 104 generations. We discarded the first 25% (2,500,000) of trees as burn-in and used the 105 remaining trees to estimate the majority consensus tree. We made the analysis on the Cipres 106 Science Gateway (Miller et al. 2010). We visualized and edited the generated tree in FigTree 107 v.1.4.3 (Rambaut 2007). Additionally, we used the Basic Local Alignment Search Tool 108 (BLAST) to compare the generated sequence against other Eleutherodactylus sequences. The 109 sequence obtained was deposited in the GenBank repository (accession number MW605049). 110 The Bayesian phylogenetic tree grouped the new sequence with a series of sequences of E. Zoology 111 jaliscoensis; this clade is supported by a high nodal value in our analysis (Pp = 0.95) (Fig. 3). of 112 Moreover, the 16S gene sequence obtained, matched with E. jaliscoensis sequences with a proofing 113 99.64% identity and an e-value of 3e-139. Our results confirm that the specimen (IBH32594) Journal 114 found in the stomach of T. cyrtopsis belongs to E. jaliscoensisuntil . Additionally, some phenotypic 115 characteristics that were observed in the undigested posterior region of the specimen paper 116 (crossbars present in the thighs and legs, and the inner surface of the thigh red) (Fig. 2A, B) 117 coincide with diagnostic characters reported by Grünwald et al. (2018) for E. jaliscoensis. 118 Furthermore, we wereNorth-western able to rescue and identify some prey in the E. jaliscoensis' stomach. Accepted 119 All preys were arthropods of the orders Araneae (family Anyphaenidae), Acari (family 120 Oribatellidae), and Coleoptera, the latter both in its larval (not identified family) and adult 121 stages (including the family Elateridae and another not identified); and remains of 122 unidentified material (Fig. 2C). 123 The encounter of a second individual of E. jaliscoensis but in T. cyrtopsis' stomach was quite 124 unexpected. The two specimens reported in this study (IBH32593 and IBH32594) plus three 125 specimens reported by Grünwald et al. (2018) represent a total of five specimens of E. Use the following type of citation: North-western Journal of Zoology 2021: e217505 nwjz-6 126 jaliscoensis collected at the type locality, which suggests this species may not be abundant in 127 the Sierra Mascota.
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