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Stream use and population characteristics of the endangered salamander, Ambystoma altamirani, from the arroyo los axolotes, state of Mexico, Mexico.

In Mexico, 8 of the 18 (44%) species of salamanders in the genus Ambystoma are critically endangered, and another 3 species are considered endangered by the International Union for Conservation of Nature (The International Union for Conservation of Nature Red List of Threatened Species, Version 2014.2; www.iucnredlist. org). One of these endangered species of Ambystoma is A. altamirani. Ambystoma altamirani is currently considered to be endangered by the International Union for Conservation of Nature and threatened by the Mexican government (Frias-Alvarez et al., 2010; Secretaria de Medio Ambiente y Recursos Naturales, 2010). The Environmental Vulnerability Score (range = 3-19) of A. altamirani is 13; this score places it between medium and high vulnerability primarily because of its relatively restricted geographic and ecological distribution (Wilson et al., 2013), which consists of isolated populations at altitudes from 2,700 m to 3,450 m in the mountains of central Mexico (Lemos-Espinal, 2003). In addition, populations of A. altamirani are subject to many of the same anthropogenic threats as other Mexican Ambystoma, such as urbanization and suburbanization, pollution, conversion to agriculture, and the introduction of fish (e.g., Lemos-Espinal et al., 1999; Griffiths et al., 2004; Contreras et al., 2009; Frias-Alvarez et al., 2010). Additional threats include infection with Batrachochytrium dendrobatidis (Frias-Alvarez et al., 2008; see also Mendoza-Almeralla et al., 2015) and small, isolated populations that are likely more prone to extinction (see Parra-Olea et al., 2012). Of particular concern is that the expansion of Mexico City is a potential threat to populations of Ambystoma in the natural areas surrounding it (e.g., Monroy-Vilchis et al., 2015), especially given recent degradation of the forest in the vicinity (Garcia-Romero, 2002).

As with many other species of Ambystoma in Mexico, little is known about the natural history of A. altamirani. Previously published information includes anecdotal observations (e.g., Taylor, 1938; Taylor and Smith, 1945; Maldonado Koerdell, 1947; Lemos-Espinal et al., 1999), studies on eggs and larval growth (Campbell and Simmons, 1962; Brandon and Altig, 1973), and diet (Lemos-Espinal et al., 2015). It appears breeding potentially takes place throughout the year (Campbell and Simmons, 1962; Brandon and Altig, 1973), with larvae taking 6 months (in lab; Brandon and Altig, 1973) to [greater than or equal to] 1 year to metamorphose (J. Lemos-Espinal, pers. obser.). Metamorphosed individuals stay in or near the aquatic habitat (Lemos-Espinal et al., 1999). Additional information on A. altamirani is needed to better understand its conservation and management. Here we report on aspects of the natural history of A. altamirani from the Arroyo Los Axolotes, Sierra de las Cruces, State of Mexico.

MATERIALS AND METHODS--Study Site--The study area was the Arroyo Los Axolotes, Isidro Fabela, Sierra de las Cruces, state of Mexico (19[degrees]32'12.2"N; 99[degrees]29'52.7", 3,479 m). Arroyo Los Axolotes is the locality from which Duges collected the type specimen of A. altamirani in 1895. No other species of salamander is found in the Arroyo Los Axolotes. The Arroyo Los Axolotes is a permanent stream that runs along the southern edge of the Llano las Navajas, an extensive grassland of [approximately equal to]100 ha surrounded by a Pinus hartwegii forest. Although the Arroyo Los Axolotes is permanent, between December and April it is restricted to a single main channel with shallow pools ([less than or equal to] 3.5 m diameter, [less than or equal to] 1 m depth) and slow-moving water. In contrast, between May and November, the stream is wide and deep with fast-moving water, deep pools, and several swampy areas and a number of small streams along the northwestern side of the grassland. Local residents graze livestock on the grassland. Recreational visitors from Mexico City are numerous on the weekend, but most people concentrate their activities away from the stream and do not go to the stream or spend only a few minutes in short sections of it. However, the stream appears relatively unaffected by these activities. There has been a dramatic increase in the number of trout (Oncorhynchus) farms in the Sierra de las Cruces over the past 30 years (J.A. Lemos-Espinal, pers. obser.). However, the Arroyo Los Axolotes is not suitable for the establishment of trout farms because of its topography, which precludes the presence of running water all year around.

Study Methods--We visited the Arroyo Los Axolotes monthly from January 2014 through September 2015. On each visit, we surveyed either 10 (January 2014 to May 2014) or 25 (June 2014 to September 2015) arbitrarily selected sites along the stream. Site selection during one visit was independent of site selection in other visits. Thus, we may have sampled some sites more than once across the entire study period, but we did not repeatedly sample specific sites over the course of the study. Each site consisted of a 3-m linear section of the stream. Within each site, we carefully searched the stream section visually and by using a snake hook along the bottom of the stream and in depression in the side of the stream to induce movement by any salamanders, thus making them obvious. We also looked under all rocks or other objects in the stream section. Using these methods to thoroughly search every site, we were confident that we detected any salamander within each site. We captured salamanders with a net and we measured snout-vent length (SVL; tip of snout to anterior margin of vent) and body mass of each individual. We also determined the sex of salamanders based on the presence of swelling of the cloacal region on both sides of the tail in males and a lack of swelling in females (Brandon and Altig, 1973). We released salamanders at the point of capture after measurements were made.

We measured the width and depth of the stream at the site to the nearest cm. We measured the dissolved oxygen and water temperature using a YSI model 85 meter (YSI Incorporated, Yellow Springs, Ohio). Beginning in July 2014, we measured water speed at the surface and at the middle of the water column using a Global Water Flow Probe Hand-held Flowmeter (Xylem Inc., White Plains, New York). We also characterized the vegetation at each site as emergent grass and forbs, submerged aquatic plants and algae, or no vegetation. We arbitrarily categorized the substrate color as black, white-yellow, or tanbrown to assess potential background matching by the salamanders; and the substrate bottom type as mud, mud with gravel, gravel, bedrock, or sand. We also recorded the microhabitat (near water surface [i.e., within 15 cm of surface], in algae, in crevice in stream wall, or under rocks) of each individual salamander.

We used analysis of variance to compare the stream characteristics of sites with and without A. altamirani. We compared the use of vegetation type, substrate color, and substrate type of sites used by A. altamirani to all sites surveyed using chi-square tests. We compared SVL between the sexes and between individuals with and without gills using an analysis of variance. We compared body mass between the sexes using an analysis of covariance with SVL as covariate after log transformation of both variables. Statistical analyses were performed using JMP Pro 10.0.0 (SAS Institute, Cary, North Carolina). Means are given [+ or -] 1 SE.

RESULTS--We made 306 salamander observations across the entire study. We observed salamanders in all months of the study except January and December 2014, and January 2015 (see Table 1).

Egg Observations--We observed egg masses in June 2015. One egg mass was in the middle of the stream channel in a section of stream that was 40 cm wide and 10 cm deep. The egg mass had 21 eggs. The egg mass was attached to aquatic plants. The water speed was 0.012 m [s.sup.-1], dissolved oxygen was 5.92 mg [L.sup.-1], and water temperature was 15.28C. The eggs were near the surface of the water (2 cm deep). We also observed two other egg masses, one with 23 eggs and one with 19 eggs. These egg masses were in the same section of stream and were attached to aquatic plants. The water speed near these egg masses was 0 m [s.sup.-1]. The stream where the two egg masses were found was 53 cm wide and 25 cm deep. Dissolved oxygen was 5.81 mg [L.sup.-1].

Stream Use--Stream sites with A. altamirani were significantly wider than sites without A. altamirani ([F.sub.1,447] = 6.83, P = 0.0093), deeper than sites without A. altamirani ([F.sub.1,447] = 25.8, P < 0.0001), and dissolved oxygen levels were significantly higher at sites where A. altamirani were observed than at sites where they were not observed ([F.sub.1,447] = 46.0, P < 0.0001; Table 2). Sites with and without A. altamirani did not have significantly different mean water temperature (Table 2; [F.sub.1,447] = 0.066, P = 0.80). Surface water speed and middle water speed were significantly greater at sites in the stream where A. altamirani were seen than in sites where A. altamirani were not seen ([F.sub.1,372] = 63.1, P < 0.0001 and [F.sub.1,372] = 10.4, P = 0.0014, respectively; Table 2).

Ambystoma altamirani used sites with mud bottoms more than expected and sites with gravel and bedrock substrates less than expected (96 mud, 9 mud with gravel, 0 gravel, 0 bedrock, 9 sand) relative to the total number of sites with each bottom type (272 mud, 56 mud with gravel, 15 gravel, 57 bedrock, 45 sand; [[chi square].sub.4] = 27.97, P < 0.0001). Ambystoma altamirani used sites with emergent grass and forbs whenever it was available and rarely used sites with no vegetation (16 emergent grass and forbs, 92 submerged aquatic plants and algae, 4 no vegetation) relative to the proportion of each vegetation type in all surveyed sites (16 emergent grass and forbs, 317 submerged aquatic plants and algae, 116 no vegetation; [[chi square].sub.2] = 14.72, P = 0.0006). Ambystoma altamirani used sites with black substrates more than expected (104 black, 1 white-yellow, 7 tan-brown), and rarely used sites with white-yellow substrates (total number of sites: 334 black, 73 white-yellow, 42 tan-brown; [[chi square].sub.2] = 20.95, P < 0.0001). Pooled across all microhabitat observations on individual salamanders, A. altamirani were near the surface the most (136); then, in order of decreasing use, they were hidden in algae (42), in crevices in the stream wall (40), on bottom of the stream (35), and rarely under rocks (2).


Body Size and Sexual Dimorphism--The largest A. altamirani we found was 90 mm SVL. Male A. altamirani had a significantly longer mean SVL than females (66.3 [+ or -] 1.35 mm [n = 75] vs. 61.0 [+ or -] 1.50 mm [n = 73]; [F.sub.1,146] = 6.99, P = 0.009). Male and female A. altamirani did not differ in body mass after SVL was accounted for (analysis of covariance: [F.sub.1,144] = 1.50, P = 0.22). Body mass increased with SVL ([F.sub.1,144] = 2718.5, P < 0.0001). Males gained mass faster with an increase of SVL than females (Fig. 1; sex x SVL interaction, [F.sub.1,144] = 5.31, P = 0.023; Males: logMass = -4.36 + 2.98logSVL, n = 75, [r.sup.2] = 0.95 P < 0.0001; Females: logMass = -3.89 + 2.73logSVL, n = 73, [r.sup.2] = 0.95, P < 0.0001).

Metamorphosis--Salamanders without gills were significantly longer than salamanders with gills (74.6 [+ or -] 1.02 mm [n = 64] vs. 47.4 [+ or -] 1.09 mm [n = 231]; [F.sub.1,192] = 25 4.1, P< 0.0001). No salamanders with a SVL <62 mm lacked gills, and no salamander with a SVL >70 mm had gills. Thus, metamorphosis appears to take place between 62 and 70 mm SVL.

DISCUSSION--Our observations suggest that egg laying by A. altamirani takes place in June, which is similar to the timing of egg laying in A. rosaceum (Anderson, 1961; Anderson and Webb, 1978). We observed egg masses attached to aquatic vegetation. Brandon and Altig (1973) also observed eggs attached to vegetation in A. altamirani. The attachment of eggs to vegetation by A. altamirani differs from observations that A. rosaceum and A. rivulare place their eggs under rocks or logs (Brandon and Altig, 1973; Anderson and Webb, 1978). However, A. ordinarium attach their eggs to vegetation (Anderson and Worthington, 1971) and A. rivulare have been observed to attach their eggs to twigs and pine needles (Bille, 2009). It therefore appears that the specific sites where Mexican Ambystoma deposit their eggs may be plastic or vary from species to species or even from population to population.

Ambystoma altamirani in our study area used stream sites that likely held a greater volume of water, had higher dissolved oxygen levels, and had faster moving water. Ambystoma altamirani appeared to use sites with emergent grass and forbs and avoid sites with no vegetation; to avoid sites with gravel or bedrock bottoms, and use mud and sand sites more; and to use sites with black-colored substrates. They also are most often found within 15 cm of the surface of the water. Previous studies have shown that adult A. altamirani are found in streams and under logs or rocks near the water (Taylor and Smith, 1945; Brandon and Altig, 1973; Lemos-Espinal et al., 1999). In particular, A. altamirani are found in small pools with cold and well-oxygenated water (Maldonado Koerdell, 1947). Other species of Mexican Ambystoma show similar habitat use along streams. Ambystoma rivulare are found in "small, slow moving streams" that are 60-100 cm wide and 10-40 cm deep, with rocky bottoms covered in mud (Bille, 2009:157), as well as in and near pools (Brandon and Altig, 1973). Ambystoma rosaceum occurs in streams, often associated with meadow habitats (Anderson, 1961; Anderson and Webb, 1978). Ambystoma leorae are found in pools along streams where the water is slow moving, the substrate is sandy or rocky, and the water is relatively cold and with dissolved oxygen levels around 6.25 mg [L.sup.-1] (Sunny et al., 2014; Monroy-Vilchis et al., 2015).

The largest A. altamirani we found was 90 mm SVL. This is similar to the maximum body size of 93 mm SVL found in A. altamirani by Brandon and Altig (1973). This is smaller than the maximum body size of 103 mm SVL for A. leorae (Lemos-Espinal and Ballinger, 1994).

We found that male A. altamirani were longer than females. Previous published reports of sexual dimorphism in Mexican Ambystoma have found either females larger than males (A. rosaceum, Anderson, 1961) or no significant sexual dimorphism (A. andersoni, Krebs and Brandon, 1984; A. granulosum, Aguilar-Miguel et al., 2009; A. lermaense, Aguilar-Miguel et al., 2009). The reason different species exhibit different degrees of sexual dimorphism is unclear, but suggests further examination of sexual dimorphism in Mexican Ambystoma would be worthwhile, especially exploration of a potential relationship between habitat type (pond or lake vs. stream) and sexual dimorphism.

Our maximum size of an A. altamirani with gills (70 mm) was substantially smaller than the 93-mm SVL individual that Brandon and Altig (1973) observed. However, the 62-70-mm SVL for metamorphosis we observed is within the range of metamorphic sizes Brandon and Altig (1973) found when they observed A. altamirani without gills of 75 and 80 mm SVL. Our observations were also in the range of SVLs for metamorphosis of A. altamirani (48-65 mm SVL) reported by Campbell and Simmons, 1962). The variation among studies does suggest there could be some variation between populations in the timing of metamorphosis. Further study that examines the possible causes of such variation would be informative.

Conclusions--The endangered salamander Ambystoma altamirani uses particular areas or microhabitats within the Arroyo Los Axolotes, in particular areas with faster flowing, oxygenated, vegetated areas with greater volumes of water. Males are larger than females, and metamorphosis takes place at a SVL of between 62 and 70 mm SVL. These observations indicate that the Arroyo Los Axolotes must be managed such that the conditions and water flow amenable to the persistence of A. altamirani are maintained, especially in the face of likely increased water use by an expanding Mexico City and increased use of similar streams for trout farms. In addition, there are some differences in sexual dimorphism and metamorphic size between our study population of A. altamirani and other populations that suggest additional study on interpopulation variation is needed to determine how much among population variation in natural history and ecology exists. Such information is critical to develop any conservation plans for this or related species.

Support for this study was provided by Direction General del Personal Academico--Programa de Apoyo a Proyectos de Investigation e Innovation Technologica (DGAPA--PAPIIT), through the project IN200114. This research conformed with all regulations in place in Mexico at the time the research was conducted. We thank three anonymous reviewers for their helpful comments on a previous version of this manuscript.


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Submitted 8 October 2015.

Acceptance recommended by Associate Editor, Felipe de Jesus Rodriguez Romero, 11 January 2016.

Julio A. Lemos-Espinal, * Geoffrey R. Smith, Angeles Hernandez Ruiz, Raymundo Montoya Ayala

Laboratorio de Ecologia--UBIPRO, Facultad de Estudios Superiores Iztacala, Av. Los Barrios 1, Los Reyes Iztacala, Tlalnepantla, Estado de Mixico, 54090--Mexico (JALE, AHR)

Department of Biology, Denison University, Granville, OH 43023 (GRS)

Laboratorio de Cimputo--UBIPRO, Facultad de Estudios Superiores Iztacala, Av. Los Barrios 1, Los Reyes Iztacala, Tlalnepantla, Estado de Meixico, 54090--Meixico (RMA)

* Correspondent:
Table 1--Number of Ambystoma altamirani observed along the Arroyo los
Axolotes, State of Mexico, Mexico, in each month of the study. Number
of sites surveyed is given in parentheses. '--' indicates no data.

Year   January   February   March     April     May

2014   0 (10)    1 (10)     8 (10)    8 (10)    11 (10)
2015   0 (25)    2 (25)     15 (25)   14 (25)   14 (25)

Year   June      July      August    September

2014   24 (25)   29 (25)   26 (25)   16 (25)
2015   67 (25)   58 (25)   4 (24)    6 (25)

Year   October   November   December

2014   2 (25)    1 (25)     0 (25)
2015   --        --         --

Table 2--Mean ([+ or -]1 SE) of characteristics of stream locations
along the Arroyo los Axolotes, State of Mexico, Mexico, with and
without Ambystoma altamirani pooled across all months and years
(January 2014 through September 2015). Sample size (n) is given in
parentheses. Asterisks mark those characteristics that were
significantly different.

characteristic          With A. altamirani   Without A. altamirani

Stream width * (cm)     84.8 [+ or -]        71.0 [+ or -]
                          3.90 (112)           2.75 (337)
Stream depth * (cm)     43.0 [+ or -]        34.5 [+ or -]
                          1.62 (112)           0.80 (337)
Dissolved oxygen *      5.44 [+ or -]        4.34 [+ or -]
  (mg [L.sup.-1])         0.44 (112)           0.081 (337)
Water temperature       16.7 [+ or -]        16.6 [+ or -]
  ([degrees]C)            0.28 (112)           0.21 (337)
Surface water speed *   0.15 [+ or -]        0.040 [+ or -]
  (m [s.sup.-1])          0.020 (85)           0.005 (289)
Middle water speed *    0.034 [+ or -]       0.015 [+ or -]
  (m [s.sup.-1])          0.006 (85)           0.002 (289)
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Author:Lemos-Espinal, Julio A.; Smith, Geoffrey R.; Ruiz, Angeles Hernandez; Ayala, Raymundo Montoya
Publication:Southwestern Naturalist
Article Type:Report
Geographic Code:1MEX
Date:Mar 1, 2016
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