Lemos-Espinal, J. A.

Smith, Geoffrey R.

Woolrich-Pina, G. A.

English

Denison University

Denison University Denison Digital Commons Denison Faculty Publications 2015 Diet of Larval Ambystoma altamiranoi from Llano de los Axolotes, Mexico J. A. Lemos-Espinal Geoffrey R. Smith G. A. Woolrich-Pina Follow this and additional works at: https://digitalcommons.denison.edu/facultypubs  Part of the Biology Commons Recommended Citation Lemos-Espinal, J. A., Smith, G. R., & Woolrich-Pina, G. A. (2015). Diet of Larval Ambystoma altamiranoi from Llano de los Axolotes, Mexico. Current Herpetology, 34(1), 75-79. doi:10.5358/hsj.34.75 This Article is brought to you for free and open access by Denison Digital Commons. It has been accepted for inclusion in Denison Faculty Publications by an authorized administrator of Denison Digital Commons. Current Herpetology 34(1): 75–79, February 2015© 2015 by The Herpetological Society of Japandoi 10.5358/hsj.34.75Diet of Larval Ambystoma altamiranoi from Llano de los Axolotes, MexicoJǊǂƿǄ A. LEMOS-ESPINAL1*, GƻǄƼƼǇƻǎ R. SMITH2, Ƶǃƺ  GǊƿǂǂƻǇǑǄ A. WOOLRICH-PIÑA31Laboratorio de Ecología—UBIPRO, Facultad de Estudios Superiores Iztacala, Av. Los Barrios 1, Los Reyes Iztacala, Tlalnepantla, Estado de México, 54090, MEXICO2Department of Biology, Denison University, Granville, Ohio 43023, USA3Laboratorio de Paleontología y Geobiología, ESIA Ticomá–IPN, Av. Ticomán 600, Col. Ticomán, Mexico, D.F. 07340, MEXICOAbstract:  Ambystoma altamiranoi is an endangered endemic salamander found in the Transvolcanic Belt of Mexico.  Unfortunately, relatively little is known about its ecology.  Here we report on the diet of larval A. altamiranoi from a population in Llano de los Axolotes, Sierra de las Cruces, State of México, Mexico.  Empty stomachs were found in 13.3% of individuals.  Ostracods and gastropods dominated the diet of A. altamiranoi, together  accounting for 89.9% of prey items consumed.  The remainder of the diet consisted primarily of insects.  Our observations suggest that the diet of A. altamiranoi is relatively narrow and that resources may be limited (relatively high frequency of empty stomachs), suggesting that factors that could impact the availability of ostracods and gastropods might have serious consequences for these endangered salamanders.Key words:  Ambystomatidae; Diet; Mexico; Salamanders; Transvolcanic BeltIǃǉǇǄƺǊƹǉƿǄǃAmbystoma altamiranoi is an endemic spe-cies of salamander found in the Transvolcanic Belt of Mexico (Taylor and Smith, 1945; Lemos-Espinal et al., 1999).  It is currently considered to be Endangered by the IUCN and Threatened by the Mexican government (Frías-Alvarez et al., 2010).  Many of the sites where A. altamira-noi are found, as well as other Mexican Ambystoma, are being impacted by humans, especially by the encroachment of residential areas, pollution, conversion to agriculture, and SGDHMSQNCTBSHNMNEëRGDF+DLNR$ROHM@KDS@K&QHîSGRDS@K%Qp@R KU@QDYDSal., 2010).  In addition, A. altamiranoi has been found to be infected with Batrachochytrium dendrobatidis (Frías-Alvarez et al., 2008). Genetic studies of A. altamiranoi populations ENTMCDUHCDMBDENQKNVKDUDKRNEFDMDìNV@MClow population sizes, and suggest that popula-tions of this species could be particularly  susceptible to extinction due to isolated popu-lations within its broader distribution range (Parra-Olea et al., 2011).  Unfortunately, rela-tively little is known about the ecology or nat-ural history of this rare and endangered sala-mander, beyond a few published anecdotal * Corresponding author.  Tel: +01–52–55–563–1333 ex7914; FAX: +1–740–587–5634; E-mail address: lemos@unam.mx76 Current Herpetol. 34(1) 2015observations (e.g., Taylor, 1938; Taylor and Smith, 1945; Maldonado Koerdell, 1947; Lemos-Espinal et al., 1999) and studies on their eggs and larval growth (Campbell and Simmons, 1962; Brandon and Altig, 1973).  What is known suggests that breeding may take place throughout the year (Campbell and Simmons, 1962; Brandon and Altig, 1973), with larvae taking six months (in lab; Brandon and Altig, 1973) to at least a year to metamorphose (J. Lemos-Espinal, pers. comm).  Once individu-als metamorphose, they remain in, or along the edges of, the aquatic habitat (Lemos-Espinal et al., 1999).  Such a lack of knowledge L@XGHMCDQBNMRDQU@SHNMDðNQSRHere we report on the diet of larval A. altamiranoi from a population in Llano de los Axolotes, Sierra de las Cruces, State of México, Mexico.  Diets of Ambystoma from Mexico G@UD ADDM RGNVM SN CHðDQ ADSVDDM RSQD@LR@MCK@JDR@ðDBSDCNQMNS@ðDBSDCAX@MSGQN-pogenic disturbance (e.g., Chaparro-Herrera et al., 2013; Ruíz-Martínez et al., 2014).  In addition, population growth in some Mexican Ambystoma HRLNRS @ðDBSDCAX SGD DFF@MClarval stages (Zambrano et al., 2007), so an understanding of the ecology of the larval stage may be critical to conserving these species.MƵǉƻǇƿƵǂǈƵǃƺ MƻǉƾǄƺǈOur study was conducted at Llano de los Axolotes, Mpio. Isidro Fabela, Sierra de las Cruces, State of México (19°32'19''N; 99°29'97.8''W; 3475 m a.s.l).  This area is an alpine grassland surrounded by coniferous forest.  In the middle of this grassland runs a small permanent stream.  The grassland extends on the sides of the stream for 100–150 m on the south side and 350–400 m on the north side.  This grassland is grazed by cows and sheep.  The stream is inhabited by a popula-tion of A. altarmiranoi, and most individuals (both adults and larvae) of this population aggregate in the portion of the stream that runs through the grassland, although we have seen some individuals in the parts of the stream that run through the  forest.  At this site breeding takes place in July, and larvae appear to take at least a year to reach meta-morphosis (J. Lemos-Espinal, pers. comm.). Adults remain in the stream after metamor-phosis.  The smallest adults observed were >70 mm and were only found in July.  There @QDMNëRGDR ONRRHAKD OQDC@SNQR NE SGD R@K@-manders), and infection with Batrachochytrium dendrobatidis has never been documented in this population.We visited the study site monthly from ca. 10:00 to 15:00 h from January through July 2014.  Individuals of A. altamiranoi were observed in all months except January. During each visit we searched a 1 km section of the stream that runs in the grassland for 5 h per visit.  All individuals detected were caught by hand or dipnet.  We captured a total of 45 CHðDQDMS K@QU@D 4RHMF SGD RSNL@BGìTRGHMFtechnique (Legler and Sullivan, 1979; Cecala et al., 2007), we obtained stomach contents for individuals of at least 35 mm SVL or larger (smaller individuals were too small to stomach ìTRG.MBDVDNAS@HMDCSGDRSNL@BGBNMSDMSRindividuals were released at the site of their capture.  Stomach contents were preserved in DSG@MNK@MCVDQDK@SDQHCDMSHëDCSNSGDKNVDRStaxonomic level possible and counted.  We calculated diet breadth using Levin’s B (Krebs, 1989), as well as the standardized Levin’s B, which ranges from 0 (specialist) to 1 (general-ist) (Hurlbert, 1978).RƻǈǊǂǉǈƵǃƺ DƿǈƹǊǈǈƿǄǃOf the 45 larvae caught, 39 (89.7%) con-tained stomach contents, and 6 (13.3%) had empty stomachs.  Mean (±SE) SVL for exam-ined larvae was 52.7±1.4 mm (n=45, range= 35–67 mm).  The proportion of empty stom-achs that we observed is higher than many previously published reports.  McCoy and Savitzky (2004) found that 2% of the larval A. mabee that they examined had empty stom-achs.  Tyler and Buscher (1980) also found that 2% of A. tigrinum larvae that they exam-ined had empty stomachs.  Other studies reported 2.5% empty stomachs in larval A. LEMOS-ESPINAL ET AL.—LARVAL SALAMANDER DIET 77cingulatum (Whiles et al., 2004) and 6% in larval  HC÷CPQMLG?LSK (Bardwell et al., 2007).Numerically, ostracods dominated the diets of A. altamiranoi, making up 68.3% of the prey items consumed (Table 1).  Gastropods were the next most frequently consumed prey item, making up 21.7% of the prey recovered. The remainder of the diet consisted primarily of insects, many of which were adults that probably fell into the water and were con-sumed by the salamander larvae.  Ostracods and gastropods were found in every stomach that contained food items (Table 1).  Adult dipterans (92.3%), lepidopterans (64.1%), and trichopterans (71.8%) were found in the majority of stomachs.  The dominance of ostracods and gastropods in the diet relative to the other prey taxa is evident (Table 1).  We observed numerous gastropods and ostracods among the aquatic vegetation on the stream bottom at the study site; however, we did not quantify their availability (J.A. Lemos-Espinal, pers. comm.).  Levin’s B value for the diet was 1.94, and the standardized Levin’s B value was 0.078.  These values suggest a narrow diet.Ostracods are a frequent, important com-ponent of the diets of larval Ambystoma (e.g., Lannoo and Bachmann, 1984; McWilliams and Bachmann, 1989; Nyman, 1991; Ghioca-Robrecht and Smith, 2008).  However, ostra-cods are not important prey items for all larval Ambystoma (e.g., Bardwell et al., 2007).  In particular, Ruíz-Martínez et al. (2014) found that ostracods were the most important prey item for A. ordinarium in undisturbed stream sections in the Transvolcanic Belt of Mexico, but were less important in stream sections showing human disturbance.  Our observa-tions suggest that if ostracods are an indica-tion of relatively undisturbed streams, as  suggested by the results of Ruíz-Martínez et al. (2014), then the streams that we sampled for A. altamiranoi may presently be suitable for the success of these salamanders.In our study, gastropods were also an impor-tant prey item in the diet of A. altamiranoi. This result contrasts with the observation that gastropods are infrequent and relatively uncommon prey items for larval Ambystoma (e.g., Tyler et al., 1980; Lannoo and Bachmann, 1984; McWilliams and Bachmann, 1989; Ghioca-Robrecht and Smith, 2008).  However, there are some species and populations that regularly consume snails or other molluscs (e.g., Dodson and Dodson, 1971; Brophy, 1980; Holomuzki and Collins, 1987; Benoy et al., 2002).  Variation among populations in predation on snails by larval Ambystoma MDDCR ETQSGDQ DW@LHM@SHNM ATS L@X QDìDBSvariation in the availability of snails in the environment, as well as larval size.  Indeed, diet composition in larval Ambystoma can vary with environmental availability of prey items (McWilliams and Bachmann, 1989), and the importance of molluscs in the diet can increase with larval size (Dodson and Dodson, 1971).  In our case the size of salamander  larvae with snails ranged from 35–67 mm TƵƸǂƻ 1.  Stomach contents of Ambystoma  altamiranoi (N=39 stomachs) from Llano de los Axolotes, Sierra de las Cruces, Estado de México, Mexico.  Unless otherwise indicated, prey items were adults.  Percentages are given in parentheses.Prey taxa Number of ItemsNumber of  stomachsAnnelida 4 (0.07) 4 (10.26)Arachnida Acari 36 (0.63) 10 (25.64) Araneae 6 (0.10) 6 (15.38)Crustacea Ostracoda 3873 (68.25) 39 (100.00)Insecta Coleoptera  Larvae 8 (0.14) 5 (12.82)  Adult 95 (1.67) 12 (30.77) Diptera 310 (5.50) 36 (92.31) Hemiptera 1 (0.02) 1 (2.56) Heteroptera 1 (0.02) 1 (2.56) Lepidoptera 42 (0.74) 25 (64.10) Orthoptera 2 (0.04) 2 (5.13) Trichoptera 65 (1.14) 28 (71.79)Mollusca Gastropoda 1231 (21.69) 39 (100.00)Total 5674 3978 Current Herpetol. 34(1) 2015SVL (i.e., the entire range of sizes of larvae we examined); thus larval size does not appear to @ðDBS SGDONSDMSH@K SNBNMRTLDRM@HKR HMNTQpopulation.The relatively high frequency of empty stomachs suggests that resources may be  limiting in this population.  This observation, when taken together with our other diet results, suggests a relatively narrow diet and limited prey availability for A. altamiranoi and further suggests that factors that impact the availability of the two most frequently consumed prey items, ostracods and gastro-pods, might have serious consequences for these endangered salamanders.  Studies con-ëQLHMF SGD QDK@SHUD @U@HK@AHKHSX @MC U@KTD NEU@QHNTR OQDX HSDLR HM CHðDQDMS G@AHS@SR HDthose that have been impacted by human activities vs. those that are undisturbed) would be valuable for understanding the link between diet and habitat quality.  In addition, data on the growth rates of larval Ambystoma from natural populations in streams would be very enlightening.  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Animal Conservation 10: 297–303.Accepted: 12 December 2014Copyright of Current Herpetology is the property of Herpetological Society of Japan and itscontent may not be copied or emailed to multiple sites or posted to a listserv without thecopyright holder's express written permission. However, users may print, download, or emailarticles for individual use.

Diet of Larval Ambystoma altamiranoi from Llano de los Axolotes, Mexico

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Diet of Larval Ambystoma altamiranoi from Llano de los Axolotes, Mexico

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