Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e59832, enero-diciembre 2024 (Publicado Nov. 15, 2024)

Distribution of Ambystoma altamirani (Caudata: Ambystomatidae)

in relation to biotic and abiotic factors in its habitat

Ana Citlali Vargas-Gómez1; https://orcid.org/0000-0003-4273-1023

Diego J. Chaparro-Herrera2*; https://orcid.org/0009-0002-2451-4703

1. Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, Unidad de Posgrado, Edificio D, 1° Piso,

Circuito de Posgrados, Ciudad Universitaria, Coyoacán, C.P. 04510, CDMX, México; anacit.gomez@gmail.com

2. División de Investigación y Posgrado, Universidad Nacional Autónoma de México, Facultad de Estudios Superiores

Iztacala, Laboratorio de Microecología Ambiental UIICSE-CyMA, Av De los Barrios S/N, Los Reyes Iztacala

Tlalnepantla de Baz, Estado de México; diego.chaparro.herrera@gmail.co (*Correspondence)

Received 06-V-2024. Corrected 19-VIII-2024. Accepted 30-X-2024.

ABSTRACT

Introduction: The mountain stream axolotl (Ambystoma altamirani) is an endemic amphibian of Mexico

cataloged as a priority species for conservation with a very restricted distribution in the Sierra de las Cruces.

Anthropogenic activities currently endanger it.

Objective: To determine the habitat factors most associated with its presence to propose conservation strategies.

Methods: Four sites in Villa del Carbon, State of Mexico, were sampled monthly for one year (September 2022 to

August 2023) with the presence and absence of A. altamirani. Environmental, physicochemical, bacteriological,

physicochemical, and biotic parameters of the water were randomly analyzed.

Results: A total of 1 186 organisms were censused, and it was determined with a CCA that the variables most

related to the populations were solar radiation, total coliforms, percentage of oxygen saturation, UV radiation,

fecal coliforms, and temperature. It was observed that the habitat is not being adequately conserved. The popu-

lations studied showed a decline during the study. The sites with the highest population abundance showed an

increase in the presence of adults, mainly females. It is essential to focus conservation actions on this umbrella

species and maintain the variables mentioned above with little disturbance to allow the prevalence of the species.

Conclusion: This information can be useful in developing conservation actions for the habitat, which it shares

with other endemic and endangered amphibians. 1) It is urgent to protect this species due to the fragility of its

populations and rapid decline; 2) It is necessary to propose conservation strategies that are adapted to the locali-

ties studied and 3) This will help to prioritize the protection of microendemic species in local environments.

Key words: Ambystoma altamirani; endemic amphibian; water quality; wildlife conservation; extinction risk.

RESUMEN

Distribución de Ambystoma altamirani (Caudata: Ambystomatidae)

en relación con factores bióticos y abióticos en su hábitat

Introducción: El ajolote arroyero de montaña (Ambystoma altamirani) un anfibio endémico de México es cata-

logado como una especie prioritaria para la conservación y tiene una distribución muy restringida en la Sierra

de las Cruces. Actividades antropogénicas actualmente suponen un riesgo para la especie.

Objetivo: Determinar los factores de su hábitat más asociados a su presencia para plantear estrategias de

conservación.

https://doi.org/10.15517/rev.biol.trop..v72i1.59832

VERTEBRATE BIOLOGY

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e59832, enero-diciembre 2024 (Publicado Nov. 15, 2024)

INTRODUCTION

Mexico is positioned as the fifth country

in amphibian richness with a very high level of

endemism; however, amphibians are the most

endangered vertebrates worldwide (Hoffmann

et al., 2010) and are currently suffering the

worst extinction crisis in their history; 43 % of

Mexican species are considered threatened or

critically endangered (Parra-Olea et al., 2014),

as is the case of amphibians of the genus

Ambystoma (Parra-Olea et al., 2011). In an

analysis carried out by the IUCN, it was deter-

mined that the most important factor for the

decrease in Mexican amphibian populations is

deforestation and transformation of vegetation;

this problem is affecting areas such as the Villa

del Carbón mountain range, which is the cur-

rent habitat of Ambystoma altamirani (Deme-

trio & Martínez, 2020). However, more studies

are needed to have the necessary information to

qualify the degree of threat to many species of

Ambystomidae in Mexico and propose appro-

priate conservation strategies (Frías-Álvarez et

al., 2010; Heredia-Bobadilla & Sunny, 2021).

Amphibians, specifically ambystomas, play

an important role in the stability of all the eco-

systems they inhabit. It has been pointed out

that they can act as emblematic species and bio-

indicators of environmental changes, especially

in aquatic environments since they require

these spaces for reproduction and develop-

ment of early life stages (Monroy-Vilchis, 2015;

Oropeza-Sánchez et al., 2022). The aquatic

habitat inhabited by ambystomas may appear

identical, but it certainly presents characteris-

tics that influence the presence of specific spe-

cies (Franco et al., 2022; Rohman et al., 2020;

Venâncio et al., 2022). Water quality is among

the essential parameters for the adequate main-

tenance of amphibians (Odum & Zippel, 2008),

as are feeding and ecological interactions with

their prey (Arribas et al., 2014). The causes

of amphibian population decline in the genus

Ambystoma are complex and are generally

shared by all aquatic animal taxa (Chaparro-

Herrera et al., 2013; Grant et al., 2019). While

the global decline of amphibians is alarm-

ing, ambystomids are not alone in facing an

uncertain future unless we are able to conduct

appropriate conservation efforts at local scales

rather than pursuing generalities and increas-

ing capacity to test and implement manage-

ment strategies at appropriate levels, especially

for vulnerable and endemic species with small

geographic distributions (Grant et al., 2019;

Heredia-Bobadilla & Sunny, 2021).

Very few natural history studies have been

developed for wild species in Mexico. For

some groups they are practically nonexistent,

Métodos: Se muestrearon mensualmente por un año (septiembre 2022 a agosto 2023) cuatro sitios con presencia

y ausencia de la especie A. altamirani, en Villa del Carbón, Estado de México. Se analizaron aleatoriamente pará-

metros ambientales, fisicoquímicos, bacteriológicos y bióticos del agua.

Resultados: Se censó un total de 1 186 organismos y se determinó mediante un ACC que las variables que

más se relacionaron con las poblaciones fueron: radiación solar, coliformes totales, porcentaje de saturación de

oxígeno, radiación UV, coliformes fecales y temperatura. Se observo que el hábitat de los organismos no se está

conservando adecuadamente y las poblaciones estudiadas mostraron declive durante el estudio. Los sitios con

mayor abundancia poblacional mostraron un incremento en la presencia de adultos, principalmente de hembras.

Es fundamental enfocar las acciones de conservación en esta especie sombrilla, y mantener las variables antes

mencionadas con poca perturbación, para permitir la prevalencia de la especie.

Conclusión: Esta información puede resultar útil para desarrollar acciones de conservación del hábitat, que ade-

más comparte con otros anfibios endémicos y en peligro. 1) Urge proteger esta especie debido a la fragilidad de sus

poblaciones y rápido decrecimiento 2) Se necesita proponer estrategias de conservación que se adecuen a las loca-

lidades estudiadas; y 3) Esto ayudará a priorizar la protección de especies micro endémicas en ambientes locales.

Palabras clave: Ambystoma altamirani; anfibio endémico; calidad del agua; conservación de vida silvestre; riesgo

de extinción.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e59832, enero-diciembre 2024 (Publicado Nov. 15, 2024)

as is the case for the caudates in general and

more specifically for the family Ambystoma-

tidae (Lemos-Espinal et al., 2016). This family

is represented by a single genus comprising 33

species, of which 18 are distributed in Mex-

ico, 17 are endemic, and are listed in NOM-

059-SEMARNAT-2010 (Frías-Álvarez et al.,

2010). We studied the mountain stream axolotl

(Ambystoma altamirani); due to its high level of

endemism, it is listed as threatened in the offi-

cial Mexican standard (Diario Oficial [DOF],

2010) and in the endangered category accord-

ing to the IUCN (Shaffer et al., 2008). In addi-

tion, its distribution is limited to the west and

south of the Valley of Mexico in the Sierra de las

Cruces in the states of Morelos, State of Mexico,

and Mexico City (Fig. 1) (Lemos-Espinal et al.,

2016). Currently, this species shows a drastic

decrease in its population (González-Martínez

et al., 2014; Shaffer et al., 2008), and it has been

shown that this species is susceptible to distur-

bance (Cosentino et al., 2011; Lemos-Espinal et

al., 2016) and there is limited ecological infor-

mation on it.

Because this species presents very particu-

lar characteristics for its presence, the objective

of this study was to determine the biotic and

abiotic factors that are associated with the dis-

tribution of A. altamirani in the wild, contrast-

ing them with sites with historical presence and

local extinction of the species. These popula-

tions present different characteristics of human

disturbance, which can help us determine what

factors are influencing the distribution of this

species in its natural habitat in contrast to

the monitored sites of absence. This study is

relevant since there are no clear conservation

strategies to be applied for this group of endem-

ic amphibians, and it is important to propose

strategies applicable at a local scale.

Fig. 1. A juvenile axolotl is shown on the left side and on the right side a usual site where this species is present in the Sierra

de las Cruces.

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e59832, enero-diciembre 2024 (Publicado Nov. 15, 2024)

MATERIALS AND METHODS

Study area: Villa del Carbon is located in

the Sierra de las Cruces, a mountain range with

a maximum elevation of 3 800 meters above sea

level that is part of the Trans-Mexican Volca-

nic Belt and is the border between the Mexico

Basin and the Toluca Basin. In this Sierra, there

are abundant altitudinal contrasts over rela-

tively short distances, which is associated with

the development of abundant ravines and val-

leys (García-Palomo et al., 2008). This area is

vital for the recharge of other aquifers; there are

more than 50 wells that supply water to vari-

ous populations, and this represents a growing

threat (Mejía, 2012).

The oak-pine forest in Villa del Carbon is

well preserved, covering 57 % of the municipal-

ity’s surface, of which 25 % of the flora has some

type of use, including timber (Rubio-Licona et

al., 2011). Villa del Carbon is a municipality

that still has a significant natural value, and

there is a recent interest in seeking alternatives

to help reduce environmental impact levels,

as well as to conserve and contribute to the

permanence of natural resources (Hernández-

Ramírez & Rosas-Roa, 2010).

For these reasons, Villa del Carbon was

selected to study the distribution of Ambystoma

altamirani; for this purpose, we selected four

sites that represent different populations of

this species with particular characteristics and

different degrees of disturbance, as well as sites

with local extinction of the species to contrast

them. A small tributary of water represents site

one in a sparsely populated rural area. Live-

stock farming activities are carried out on the

slopes of this body of water. It was observed

that human and domestic waste from these

settlements could reach the said body of water

through leachates. Site two is a river located

in an ecotourism park where tourist activities

such as fishing, camping, outdoor grills, and

swimming pools are carried out with a con-

stant flow of tourists. Site three is located near

human settlements and cattle and sheep grazing

was observed, as well as people visiting the site

in order to wash clothes in that body of water.

Finally, site four is a body of water close to a

mine that is no longer active and there is also

cattle grazing. Occasional vehicular traffic was

also identified near all sites (Fig. 2).

Habitat characterization and sampling

design: One visit per month during one year

(September 2022 to August 2023) was made

for each site, alternating the time and day of

Fig. 2. Map showing the main rivers and the four sites located to study the mountain stream siredon in the Sierra de las

Cruces; in yellow are the sites where the species is present, and in red are the sites where it is absent in the locality of Villa

del Carbon. The red star represents the municipal seat of the municipality of Villa del Carbon.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e59832, enero-diciembre 2024 (Publicado Nov. 15, 2024)

sampling, for which a 1 000 m2 transect, was

drawn parallel to the river. Each transect was

sampled by direct search and visual encounter

in the opposite direction to the river cur-

rent to avoid counting the same individual

twice for approximately one hour (Pineda &

Rodríguez-Mendoza, 2010). The stage of each

specimen was recorded, considering gilled

organisms as adults, and the sex was deter-

mined when possible.

Transparency was determined in situ as

well as physicochemical factors of the water: pH,

temperature, dissolved oxygen, and percentage

of oxygen saturation using a HANNA HI98194

multiparametric probe. Solar and UV radia-

tion were also recorded at the water level using

APOGEE MQ-500 and MU-200, respectively.

A surface water sample was taken with

500 ml amber bottles to determine nutrients

(nitrates, phosphates, and ammonium) and

heavy metals (copper, arsenic, and chromium)

in the laboratory using colorimetric tests in a

YSI EcoSense 9 500 Photometer.

A bacteriological sample was taken in

NASCO WHIRL-PAK sterile bags and trans-

ferred to the laboratory to determine fecal and

total coliforms using the most probable num-

ber technique according to NMX-AA-042-SC-

FI-2015 (DOF, 2015).

Using a fine mesh fish net number five

Azul brand, a trawl was performed at each site,

and the zooplankton organisms captured were

fixed in 5 % formalin (Guerly, 2022). Samples

were processed by identifying each organism

to a taxa level using QUASAR stereo microsco-

py Science Qm15 80X. Subsequently, monthly

zooplankton abundance data were analyzed by

obtaining the Shannon-Weaver index using the

PAST program version 4.03 (Chávez-Veintemi-

lla et al., 2021).

Statistical analyses: One-way ANOVA

tests were performed for each factor evalu-

ated, and Tukey’s test was used to determine

differences between sites using SigmaPlot soft-

ware V. 13 3.1. p = 0.05 was used to deter-

mine differences between groups (D’Cruze &

Kumar, 2011).

To analyze the relationship between the

parameters mentioned above and axolotl popu-

lations, a canonical correspondence analysis

(CCA) was performed using CANOCO 5.0

software, which allows us to show the relation-

ship in terms of environmental characteris-

tics (physicochemical parameters, temperature,

etc.) and biological variables (species), only

that in this case it will be adapted considering

populations as species for the purposes of this

study (Kostov, 2008).

RESULTS

Four localities with different characteris-

tics were sampled with the presence of the spe-

cies in Villa del Carbon from September 2022

to August 2023. Populations one and three are

close to rural towns; population two is associ-

ated with a place with ecotourism activity close

to axolotls. On the other hand, the population

four are associated with a site with abandoned

mining activity. A total of 1 199 salamanders

were recorded at these sites, of which sites one

and two had the greatest number of organisms,

with 639 and 374, respectively, and showed

the greatest number of adult specimens. Sites

three and four showed the lowest numbers of

specimens with 166 and 20, respectively. No

eggs were recorded at site four during the year

of sampling (Fig. 3). Similarly, the proportion of

females and males was higher in sites one and

two than in the others (Fig. 4).

The environmental, physicochemical, bac-

teriological, and biotic parameters of the water

showed differences in the sites with the pres-

ence and absence of Ambystoma altamirani

(Table 1). Of the 16 parameters analyzed, eight

showed significant differences: water tempera-

ture, transparency, UV radiation, fecal coli-

forms, total coliforms, nitrates, phosphates, and

zooplankton diversity.

The biotic parameters of the water, such

as zooplankton, were composed of numerous

taxa, of which the most numerous were cope-

pods, followed by larvae of Ephemeroptera,

Diptera, Ostracoda, and Coleoptera, among

others. Predation by A. altamirani on anuran

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e59832, enero-diciembre 2024 (Publicado Nov. 15, 2024)

larvae and various larvae and insects such as

Coleoptera was observed.

The canonical correspondence analysis

showed that the variables most associated with

the presence of the populations were solar

radiation (64.61 %), followed by total coli-

forms, oxygen saturation, fecal coliforms, and

UV radiation, which together explained 97.76

% of the variability of the data (Fig. 5). Each

population showed different associations with

environmental, physicochemical, bacteriologi-

cal, and biotic parameters of the water; popu-

lation one showed an inverse correlation with

zooplankton and fecal coliforms, as well as a

close relationship with ammonium and solar

radiation. Population two showed a strong

interaction with dissolved oxygen, as well as

an inverse relationship with temperature and

Fig. 4. The proportion of females and males in each of the four populations.

Fig. 3. The number of organisms sampled by life stage, categorized into adults, juveniles, larvae, and eggs in each of the four

populations.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e59832, enero-diciembre 2024 (Publicado Nov. 15, 2024)

Table 1

The environmental, physicochemical, bacteriological, and biotic parameters of the water of each population of Ambystoma altamirani.

Parameter Population Absence Min- Max+ p

1234

pH 6.945+ 6.973- 7.191+ 6.945 7.295 6.10 7.92 0.334

Dissolved oxygen (mg/l) 5.400- 6.852+- 6.030 6.295 5.540 3.44 8.22 0.298

Oxygen saturation (%) 88.713- 92.100+ 87.450 92.500 74.000 44.7 103.2 0.075

Temperature (°C) * 15.479 12.093- 16.004 16.704+ 14.625 8.1 21 0.012

Transparency (cm)* 2.917 0.000 3.333+ 0.000 23.000 0 40 < 0.001

Solar radiation (µmol m-2 s-1)1 152.50+ 575.60 212.900 410.500 625.000 0 1 725 0.147

UV radiation (µmol)* 35.250+ 6.250 21.200 26.400 30.000 0 189 0.020

Fecal coliforms

(NMP/100 ml) *

12.050 6.050 13.500+ 4.500 38.500 0 290 0.001

Total coliforms (NMP/100 ml) * 115 000 13 000 58 500 27 000+ 185 000 01 100 0.023

Nitrates (mg/l) * 0.0910 0.0960 0.0635+ 0.0625 0.400 0 0.840 0.009

Phosphates (mg/l) * 0.0390+ 0.01000 0.01000 0.000 0.650 0 1.8 0.002

Ammonium (mg/l) 0.0300+ 0.0250 0.0200 0.0250 0.0350 0 0.07 0.703

Arsenic (PPB) 10.000 0.000+ 10.000 10.000 10.000 0 30 0.600

Chromium (mg/l) 0.0450+ 0.0150 0.0390 0.0300 0.000 0 0.65 0.444

Copper (mg/l) 0.000 0.0750 0.000+ 0.000 0.000 0 0.4 0.092

Zooplankton diversity (H’) * 0.912- 1.126+ 1.338 0.983 0.791 0.4826 1.852 0.002

Parameters that showed a significant difference with respect to the control are shown with the symbol *. The + symbol represents the site with the highest value recorded for the

parameter, and the - symbol represents the lowest value recorded in the year of sampling.

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e59832, enero-diciembre 2024 (Publicado Nov. 15, 2024)

pH. Population three did not show a close

association with the variables. Population four

maintained a relationship with fecal coliforms,

zooplankton, and some heavy metals.

DISCUSSION

Several studies on A. altamirani and other

ambystomatids have reported a higher abun-

dance of females (1.0 versus 0.6 males) (Guer-

rero de la Paz et al., 2020); in our study, we

found that in populations one and two, the

proportion of females was higher than 60 %.

Likewise, these sampling points have a higher

proportion of eggs and the presence of adults,

so we could consider them more stable and

healthier compared to the other sampling sites.

A. altamirani has been reported under

very particular habitat characteristics for its

persistence; abundance has been associated

mainly with physicochemical factors, with lim-

ited influence of terrestrial factors (Franco et

al., 2022). Although each population from the

different sampling sites showed different asso-

ciations to environmental, physicochemical,

bacteriological, and biotic parameters of the

water, the CCA showed that among the most

important characteristics that we should main-

tain in the environments to maintain popula-

tions with the highest number of organisms

include terrestrial factors, such as solar and UV

radiation in the ranges found.

On the other hand, coliforms in low

amounts (fecal and total) are the preferred sites

for these amphibians in relation to the absence

sites. The presence sites showed values below

13.5 and 115 NMP/100 mL, respectively (Table

1). Fecal and total coliforms are below the

Fig. 5. CCA biplot of the Ambystoma altamirani sites sampled in which the dots represent the four populations studied.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e59832, enero-diciembre 2024 (Publicado Nov. 15, 2024)

permissible limits for rivers, lakes, and lagoons,

according to NOM-001-SEMARNAT-2021

(DOF, 2022).

Otherwise, according to the CCA, high

oxygen saturation (6.852 mg/l) is also funda-

mental to maintaining the species populations

(Table 1).It has been reported that higher lev-

els of dissolved oxygen have been shown to be

preferable for organisms (Lemos-Espinal et al.,

2016). In this case, population two showed the

highest levels of dissolved oxygen; However,

population one could be defined as the healthi-

est, and it also presented the lowest levels of

dissolved oxygen saturation. We know that

dissolved oxygen can be reduced by increasing

temperature (Bello et al., 2017), and based on

the data, the temperature of population one is

higher than population two. On the other hand,

fecal coliforms, total coliforms, phosphates,

ammonium, and chromium presented higher

levels at this site compared to population two

and even other sites. It has been reported that

the decomposition of nutrients also consumes

dissolved oxygen (Liu et al., 2022). These fac-

tors cause the reduced reading of oxygen satu-

ration and dissolved oxygen in population one

compared to population two, which is also

more stable compared to the others.

Although it has generally been reported

that high oxygen concentration is preferable for

axolotls, it has also been seen that the species

is usually found at levels of 5.44 ± 0.44 mg/l

(Lemos-Espinal et al., 2016). It should be noted

that levels above 5 mg/L of dissolved oxygen

are healthy for aquatic life (Prasad et al., 2014).

Transparency was among the values that

showed the difference between presence and

absence sites, highlighting that organisms

prefer good water transparency. This may be

explained by the fact that the genus Ambysto-

ma has low visibility compared to other aquatic

organisms such as fish; therefore, environments

with greater transparency may benefit it in its

hunting behavior and competition for food

against other organisms (Chaparro-Herrera et

al., 2020). On the other hand, it cannot be ruled

out that low transparency may be a factor inter-

fering with the observation of this species, and

this aspect should be studied with other types

of population censuses.

Nutrients in the water, such as nitrates and

phosphates, were also different in the absence

and presence of amphibians. However, all sites

are well below the permissible limits according

to NOM-001-SEMARNAT-2021 to not affect

aquatic fauna (DOF, 2022).

One of the most striking parameters has

been UV radiation since it has recently been

identified as one of the stressors that most

threaten amphibians at all stages of their lives

and can have sublethal effects, as well as inter-

act with pollutants to enhance their effects

(Blaustein et al., 2003). However, the popula-

tion with the highest number of organisms and

the sites of absence also showed the highest

value of UV radiation, which could indicate

that the effects of UV radiation may be due

to the sum of several related factors, such as

synergy with pollutants, or may be evidence

of the tolerance of these organisms to the rays.

Tolerance in amphibians to UV radiation has

been documented as a local adaptation, and it

has been inferred that organisms at high alti-

tudes may show greater tolerance (Pahkala et

al., 2002). It has also been shown that exposure

to UV radiation is reaching lethal levels in con-

junction with cold temperatures, increasing the

thermal limits of organisms as plasticity (Kern

et al., 2015), which is consistent with our data.

Although the temperature of population

one was not the lowest, in general, these organ-

isms are characterized by preferring cold tem-

peratures, even showing activity close to the

freezing point (Sánchez-Sánchez et al., 2022).

The temperature difference between sites is

due to factors such as flow volume, flow speed,

riparian vegetation, and human use of the

aquatic system. This species, like other ambys-

tomatids, presents high genetic variability, find-

ing genetic subpopulations with a significant

level of genetic structure and variability within

the same population (Heredia-Bobadilla et al.,

2017). Due to this condition, the four popula-

tions studied showed different relationships

with the variables analyzed. Each population

is behaving differently to the variables which

10 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e59832, enero-diciembre 2024 (Publicado Nov. 15, 2024)

makes it very difficult to define conservation

actions applicable to the species and even more

so to the genus Ambystoma.

This species, like other ambystomatids,

presents high values of heterozygosity, inbreed-

ing, and reduction of the effective population

size probably caused by bottlenecks, which

may be reducing its genetic variability, which

is fundamental for the species to adapt to envi-

ronmental changes (Heredia-Bobadilla et al.,

2017). The reduction of genetic quality can be

a factor that leads species to extinction since it

reduces their plasticity; in ambystomas, there

is a low flow, and genetic knowledge is insuf-

ficient, which greatly hinders their conserva-

tion (Parra-Olea et al., 2011). We know that

amphibians and ambystomes are susceptible

to water quality and the characteristics of their

habitat, so we should focus conservation efforts

on both (Piñon-Flores et al., 2021), in addition

to further study of site contamination, which

may be presenting effects that are not yet visible

in the organisms and although they do not yet

show alarming values.

This species of salamander does not show

a clear relationship with zooplankton diversity,

according to the CCA, but we could assume that

they prefer environments with greater diversity

(Table 1). There needs to be more information

on the feeding of these organisms; in the case of

larvae, it has been reported mainly ostracods,

gastropods, and insects (Lemos-Espinal et al.,

2015), although, in the adult stage, there is no

precise information. A greater abundance of

prey could benefit organisms in all stages of

their life.

Although some studies have suggested that

habitat variables show no influence on the pres-

ence or absence of this species (Guerrero de la

Paz et al., 2020), the CCA shows the variables

that we can pay attention to for the conserva-

tion of amphibians in these environments.

Several studies on this species have proposed

conservation strategies to maintain favorable

water conditions for its persistence, among

which are good water flow and volume, low

temperature, good stream width, shallow water

depth, high dissolved oxygen level (Franco et

al., 2022; Lemos-Espinal et al., 2016) suggest-

ing that critical stream characteristics for A.

altamirani include sites that do not dry out,

presence of mud substrates and absence of fish

(Hernández et al., 2020a). It is also highlighted

that it is crucial to minimize the expansion of

human influence on aquatic habitats where A.

altamirani specimens are found (Franco et al.,

2022) as desiccation due to the likely increased

water use by Mexico City, which may be a cru-

cial factor for the decline of this species (Franco

et al., 2022; Lemos-Espinal et al., 2016).

The favorable water temperature for

this species has been reported in low ranges,

between 12.32 °C and 17.44 °C (Camacho et

al., 2020), even observing organisms with water

temperature activity at 6.4 °C (Sánchez-Sánchez

et al., 2022). The temperature at sites one and

two, which had the highest number of organ-

isms, was between 12.093 and 15.497 °C, and at

the sites with the lowest number of organisms,

it was higher than 16 °C. Water temperature

has been one of the most relevant factors for

the study and maintenance of Ambystoma; it

has also been shown that high temperatures

(27 °C) represent a higher risk of mortality

than cool and dry conditions (Rohr & Palmer,

2013). Temperature is a factor that cannot be

ruled out, as the synergistic effects of climate

change, emerging diseases, and exotic species

will continue to increase pressure on remnant

populations (Hernández et al., 2020b).

This species responds differently to season-

al environmental variations at different stages

of development (Martínez-Ugalde et al., 2022),

which should be studied further, and each pop-

ulation may respond differently to the environ-

ment, which complicates the establishment of

generalized conservation actions. The causes of

amphibian population declines are multifaceted

and context-dependent; they include complex

effects of abiotic and biotic factors that can be

stressful and lead to population losses (Blaus-

tein et al., 2018). We conclude that it is urgent

to protect this species due to the fragility of

its populations and rapid decline; in addition,

we know that the organisms of this group are

emblematic species of which conserving their

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e59832, enero-diciembre 2024 (Publicado Nov. 15, 2024)

habitat can be beneficial to preserve numer-

ous species (Oropeza-Sánchez et al., 2022).

We propose conservation strategies to avoid

contamination by heavy metals and other com-

pounds to maintain water quality in good con-

dition as reported in this study, maintain water

transparency to not interfere with the behavior

of organisms, as mentioned above, avoid reduc-

ing the water level to avoid reducing dissolved

oxygen, which is important for these organisms

(Oropeza-Sánchez et al., 2022).

We know that the fragility of populations

and rapid decline of amphibians is alarming; we

need more specialized and possibly experimen-

tal studies to propose conservation strategies

that are appropriate to the localities studied,

although each population may act differently to

the factors of their environment to generalize

some vital aspects that could ensure the con-

servation of the species at least in a particular

area. It is essential to prioritize the protection of

microendemic species in local environments, as

this ensures the persistence of the habitat of all

the species and the community associated with

these habitats.

Ethical statement: the authors declare that

they all agree with this publication and made

significant contributions; that there is no con-

flict of interest of any kind; and that we fol-

lowed all pertinent ethical and legal procedures

and requirements. All financial sources are fully

and clearly stated in the acknowledgments sec-

tion. A signed document has been filed in the

journal archives.

ACKNOWLEDGMENTS

This paper is part of the requirements

for obtaining a Master’s Science degree in

the Posgrado en Ciencias Biologicas UNAM.

Vargas-Gómez Ana Citlali thanks Posgrado

en Ciencias Biológicas (PCBiol) by Univer-

sidad Nacional Autónoma de México (UNAM)

for its support in carrying out this project

andConsejo Nacional de Humanidades, Cien-

cias y Tecnologías (CONAHCYT) for a master

scholarship (CVU 1190591). Vargas-Gómez

Ana Citlali thanks the support provided by the

Consejo Mexiquense de Ciencia y Tecnología

(COMECYT) through the research stay of

the Programa Investigadoras e Investigadores

COMECYT 2024 (EESP2024-0136).

REFERENCES

Arribas, R., Díaz-Paniagua, C., & Gómez-Mestre, I. (2014).

Ecological consequences of amphibian larvae and

their native and alien predators on the community

structure of temporary ponds. Freshwater Biology,

59(9), 1996–2008. https://doi.org/10.1111/fwb.12402

Bello, A. D., Hashim, N., & Haniffah, M. M. (2017). Predic-

ting impact of climate change on water temperature

and dissolved oxygen in tropical rivers. Climate, 5(3),

58. https://doi.org/10.3390/cli5030058

Blaustein, A. R., Romansic, J. M., Kiesecker, J. M., &

Hatch, A. A. C. (2003). Ultraviolet radiation, toxic

chemicals and amphibian population declines. Diver-

sity and Distributions, 9(2), 123–140. https://doi.

org/10.1046/j.1472-4642.2003.00015.x

Blaustein, A. R., Urbina, J., Snyder, P. W., Reynolds, E.,

Dang, T. D., Hoverman, J. T., Han, B. A., Olson, D. H.,

Searle, C., & Hambalek, N. M. (2018). Effects of emer-

ging infectious diseases on amphibians: A review of

experimental studies. Diversity (Basel. Online), 10(3),

81. https://doi.org/10.3390/d10030081

Camacho, Z. A. V., Smith, G. R., Ayala, R. M., & Lemos-

Espinal, J. A. (2020). Distribution and Popula-

tion Structure of Ambystoma altamirani from the

Llano de Lobos, State of México, Mexico. Western

North American Naturalist, 80(2), 228. https://doi.

org/10.3398/064.080.0210

Chaparro-Herrera, D. de J., Nandini, S., & Sarma, S. (2013).

Effect of water quality on the feeding ecology of

axolotl Ambystoma mexicanum. Journal of Limnology,

72(3), 555–565. https://doi.org/10.4081/jlimnol.2013.

e46

Chaparro-Herrera, D. de J., Nandini, S., & Sarma, S. S. S.

(2020). Turbidity effects on feeding by larvae of the

endemic Ambystoma mexicanum and the introduced

Oreochromis niloticus in Lake Xochimilco, Mexi-

co. Ecohydrology and Hydrobiology, 20(1), 91–101.

https://doi.org/10.1016/j.ecohyd.2019.07.002

Chávez-Veintemilla, C. A., Pezo-Díaz, R., & Vásquez, E.

(2021). Diversidad planctónica de los cuerpos de agua

en la Reserva Nacional Allpahuayo Mishana, Loreto–

Perú. Folia Amazónica, 29(2), 353–370. https://doi.

org/10.24841/fa.v29i2.536

Cosentino, B. J., Schooley, R. L., & Phillips, C. A. (2011).

Spatial connectivity moderates the effect of preda-

tory fish on salamander metapopulation dynamics.

12 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e59832, enero-diciembre 2024 (Publicado Nov. 15, 2024)

Ecosphere, 2(8), 1–14. https://doi.org/10.1890/

es11-00111.1

D’Cruze, N., & Kumar, S. (2011). Effects of anthropogenic

activities on lizard communities in northern Mada-

gascar. Animal Conservation, 14(5), 542–552. https://

doi.org/10.1111/j.1469-1795.2011.00459.x

Demetrio, W. G., & Martínez, D. V. (2020). Procesos locales

de transformación que detonan el cambio de uso de

suelo y vegetación en un área natural protegida de

la Región Centro de México. Acta Universitaria, 30,

1–21. https://doi.org/10.15174/au.2020.2864

Diario Oficial. (2010). Norma Oficial Mexicana NOM-

059-SEMARNAT-2010, Protección ambien-

tal-Especies nativas de México de flora y fauna

silvestres-Categorías de riesgo y especificaciones para

su inclusión, exclusión o cambio-Lista de especies

en riesgo. México: Secretaría de Medio Ambiente

y Recursos Naturales. https://dof.gob.mx/nota_deta-

lle_popup.php?codigo=5173091

Diario Oficial. (2015). Norma Oficial Mexicana NMX-

AA-042-SCFI-2015, Water Analysis - Enumeration

Of Total Coliform Organisms, Thermotolerant Fecal

Coliform Organisms And Escherichia Coli- Multiple

Tube (Most Probable Number) Method. México:

Secretaría de Economía. https://www.dof.gob.mx/

nota_detalle.php?codigo=5645374&fecha=11/03/202

2#gsc.tab=0

Diario Oficial. (2022). Norma Oficial Mexicana NOM-

001-SEMARNAT-2021, que establece los límites per-

misibles de contaminantesen las descargas de aguas

residuales en cuerpos receptores propiedad de la

nación. México: Diario Oficial. Secretaría del Traba-

jo y Previsión Social. https://www.dof.gob.mx/nota_

detalle.php?codigo=5645374&fecha=11/03/2022#

Franco, W. G., Smith, G. R., & Lemos-Espinal, J. A. (2022).

The effects of livestock, proximity to trees, and aqua-

tic characteristics on the abundance of Ambystoma

altamirani within a stream. Journal of Herpetology,

56(1), 56–59. https://doi.org/10.1670/20-118

Frías-Álvarez, P., Zúñiga-Vega, J. J., & Flores-Villela, O.

(2010). A general assessment of the conservation

status and decline trends of Mexican amphibians.

Biodiversity and Conservation, 19(13), 3699–3742.

https://doi.org/10.1007/s10531-010-9923-9

García-Palomo, A., Zamorano, J. J., López-Miguel, C.,

Galván-García, A., Carlos-Valerio, V., Ortega, R.,

& Macías, J. L. (2008). El arreglo morfoestructural

de la Sierra de Las Cruces, México central. Revis-

ta Mexicana de Ciencias Geológicas, 25(1). https://

www.scielo.org.mx/scielo.php?pid=S1026-

87742008000100010&script=sci_arttext

González-Martínez T., Ávila-Akerberg, V., & Galicia-Val-

dés, A. (2014). Conservación del Ajolote de Montaña

(Ambystoma altamirani) en Bosques Templados con

Alta Presión Antrópica. Caso: Establecimiento de un

Centro de Educación y Reproducción en Cautiverio

en México [Memorias del Simposio Internacional

Biodiversidad]. Ibarra, Ecuador. https://repositorio.

utn.edu.ec/handle/123456789/3728

Grant, E. H. C., Muths, E., Schmidt, B. R., & Petrovan, S. O.

(2019). Amphibian conservation in the Anthropoce-

ne. Biological Conservation, 236, 543–547. https://doi.

org/10.1016/j.biocon.2019.03.003

Guerly, Á. P., Dueñas-Ramírez, P. R., Sánchez-García,

R., & Miguel, V. F. (2022). Manual de zooplancton.

hdl:20.500.12010/25810. https://expeditiorepositorio.

utadeo.edu.co/handle/20.500.12010/25810

Guerrero de la Paz, J. G., Mercado-Silva, N., Alcalá, R.

E., & Zambrano, L. (2020). Signals of decline of

flagship species Ambystoma altamirani Dugès, 1895

(Caudata, Ambystomatidae) in a Mexican natural

protected area. Herpetozoa, 33, 177–183. https://doi.

org/10.3897/herpetozoa.33.e56588

Heredia-Bobadilla, R. L., & Sunny, A. (2021). Análisis

de la categoría de riesgo de los ajolotes de arro-

yos de alta montaña (Caudata: Ambystoma). Acta

Zoológica Mexicana, 1–19. https://doi.org/10.21829/

azm.2021.3712315

Heredia-Bobadilla, R., Monroy-Vilchis, O., Zarco-Gonzá-

lez, M. M., Martínez-Gómez, D., Mendoza-Martínez,

G. D., & Sunny, A. (2017). Genetic variability and

structure of an isolated population of Ambystoma

altamirani, a mole salamander that lives in the mou-

ntains of one of the largest urban areas in the

world. Journal of Genetics, 96(6), 873–883. https://doi.

org/10.1007/s12041-017-0823-6

Hernández, V. V., Smith, G. R., Ayala, R. M., & Lemos-

Espinal, J. A. (2020a). Abundance, distribution, popu-

lation structure, and substrate use of Ambystoma

altamirani along the arroyo los axolotes, State of

Mexico, Mexico. Herpetological Conservation and

Biology, 15(1), 188–197.

Hernández, V. V., Lemos-Espinal, J. A., Smith, G. R., &

Montoya-Ayala, R. (2020b). Natural history obser-

vations of Ambystoma altamirani and Dryophytes pli-

catus at sierra de las cruces, State of Mexico, Mexico.

The Southwestern Naturalist, 64(2), 35–137. https://

doi.org/10.1894/0038-4909-64-2-135

Hernández-Ramírez, N., & Rosas-Roa, J. (2010). Ecotu-

rismo e infraestructura vial como detonante de la

economía local, caso de estudio: Villa del Carbón,

2009. Quivera Revista de Estudios Territoriales, 12(2),

37–57. https://quivera.uaemex.mx/article/view/10188

Hoffmann, M., Hilton-Taylor, C., Angulo, A., Böhm, M.,

Brooks, T. M., Butchart, S. H. M., Carpenter, K. E.,

Chanson, J., Collen, B., Cox, N. A., Darwall, W.,

Dulvy, N. K., Harrison, L. R., Katariya, V., Pollock, C.

M., Quader, S., Richman, N. I., Rodrigues, A. S. L.,

Tognelli, M. F., Vié, J.C., ... & Stuart, S. N. (2010). The

impact of conservation on the status of the world’s

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e59832, enero-diciembre 2024 (Publicado Nov. 15, 2024)

vertebrates. Science, 330(6010), 1503–1509. https://

doi.org/10.1126/science.1194442

Kern, P., Cramp, R. L., Seebacher, F., Kazerouni, E. G., &

Franklin, C. E. (2015). Plasticity of protective mecha-

nisms only partially explains interactive effects of

temperature and UVR on upper thermal limits. Com-

parative Biochemistry and Physiology Part A: Molecu-

lar & Integrative Physiology, 190, 75–82. https://doi.

org/10.1016/j.cbpa.2015.09.007

Kostov, B. A. (2008). Aportación del análisis canónico de

correspondencias al análisis textual [Tesis de bachi-

ller]. Universitat Politècnica de Catalunya, España.

http://creativecommons.org/licenses/by-nc-nd/3.0/

es/

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

Lemos-Espinal, J. A., Smith, G. R., Ruíz, Á. H., & Ayala, R.

M. (2016). Stream use and population characteristics

of the endangered salamander, Ambystoma altami-

rani, from the Arroyo Los Axolotes, State of Mexi-

co, Mexico. Southwestern Naturalist, 61(1), 28–32.

https://doi.org/10.1894/0038-4909-61.1.28

Liu, S., He, G., Fang, H., Xu, S., & Bai, S. (2022). Effects of

dissolved oxygen on the decomposers and decompo-

sition of plant litter in lake ecosystem. Journal of Clea-

ner Production, 372, 133837. https://doi.org/10.1016/j.

jclepro.2022.133837

Martínez-Ugalde, E., Ávila-Akerberg, V., Martínez, T. M.

G., Trejo, M. V., Hernández, D. Z., Anaya-Morales, S.

L., & Rebollar, E. A. (2022). The skin microbiota of

the axolotl Ambystoma altamirani is highly influenced

by metamorphosis and seasonality but not by patho-

gen infection. Animal Microbiome, 4(1). https://doi.

org/10.1186/s42523-022-00215-7

Mejía, H. B. (2012). Deterioro socioambiental en la Sierra

de las Cruces.Diseño y Sociedad, (32), 40–49.

Monroy-Vilchis, O. (2015). Análisis de algunos paráme-

tros ecológicos de 2 vertebrados indicadores de con-

servación en el monte Tláloc. http://ri.uaemex.mx/

handle/20.500.11799/49687

Odum, R. A., & Zippel, K. C. (2008). Amphibian water

quality: approaches to an essential environmental

parameter. International Zoo Yearbook, 42(1), 40–52.

https://doi.org/10.1111/j.1748-1090.2008.00053.x

Oropeza-Sánchez, M. T., Suazo-Ortuño, I., Benítez-Mal-

vido, J., Monroy-Hernández, E., & Munguía-Steyer,

R. (2022). Amphibian richness along modified ripa-

rian areas of central Mexico: conservation priorities.

Ecological Processes, 11(1). https://doi.org/10.1186/

s13717-022-00408-7

Pahkala, M., Laurila, A., & Merilä, J. (2002). Effects of

ultraviolet-B radiation on common frog Rana tem-

poraria embryos from along a latitudinal gradient.

Oecologia, 133(4), 458–465. https://doi.org/10.1007/

s00442-002-1058-6

Parra-Olea, G., Flores-Villela, O., & Mendoza-Almeralla, C.

(2014). Biodiversidad de anfibios en México. Revista

Mexicana de Biodiversidad, 85, 460–466. https://doi.

org/10.7550/rmb.32027

Parra-Olea, G., Zamudio, K. R., Recuero, E., Aguilar-

Miguel, X., Huacuz, D., & Zambrano, L. (2011).

Conservation genetics of threatened Mexican axolotls

(Ambystoma). Animal Conservation, 15(1), 61–72.

https://doi.org/10.1111/j.1469-1795.2011.00488.x

Pineda, E., & Rodríguez-Mendoza, C. A. (2010). Distribu-

ción y abundancia de Craugastor vulcani: Una especie

de rana en riesgo de Los Tuxtlas, Veracruz, México.

Revista Mexicana de Biodiversidad, 81(1), 133–141.

https://doi.org/10.22201/ib.20078706e.2010.81.1.1431

Piñon-Flores, M. A., Suazo-Ortuño, I., Ramírez-Herrejón,

J. P., Moncayo-Estrada, R., & del-Val, E. (2021). Habi-

tat, water quality or geomorphological degradation in

the streams: Which is most important for conserving

an endemic amphibian of Central Mexico? Jour-

nal for Nature Conservation, 64, 126063. https://doi.

org/10.1016/j.jnc.2021.126063

Prasad, B. S. R. V., Srinivasu, P. D. N., Varma, P. S., Raman,

A. V., & Ray, S. (2014). Dynamics of dissolved oxygen

in relation to saturation and health of an aquatic body:

a case for Chilka Lagoon, India. Journal of Ecosystems,

2014, 1–17. https://doi.org/10.1155/2014/526245

Rohman, F., Permana, H., Akhsani, F., Wangkulangkul,

S., & Priambodo, B. (2020). The amphibians diver-

sity as bioindicator of aquatic ecosystem at Sumber

Taman, Malang, East Java. AIP Conference Procee-

dings, 2231(1). https://doi.org/10.1063/5.0002503

Rohr, J. R., & Palmer, B. D. (2013). Climate change, multiple

stressors, and the decline of ectotherms. Conserva-

tion Biology, 27(4), 741–751. https://doi.org/10.1111/

cobi.12086

Rubio-Licona, L. E., Romero-Rangel, S., & Rojas-Zenteno,

E. C. (2011). Structure and floristic composition

of two oak (Fagaceae) communities in the State of

Mexico. Revista Chapingo Serie Ciencias Forestales y

del Ambiente, 17(1), 77–90. https://doi.org/10.5154/r.

rchscfa.2010.03.014

Sánchez-Sánchez, R., Méndez-Méndez, O., Smith, G. R.,

Ayala, R. M., Woolrich-Piña, G. A., & Lemos-Espinal,

J. A. (2022). Field observations of Ambystoma altami-

rani at near-freezing conditions in the Sierra de las

Cruces, Mexico. Phyllomedusa: Journal of Herpetolo-

gy, 21(1), 67–69. https://doi.org/10.11606/issn.2316-

9079.v21i1p67-69

14 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e59832, enero-diciembre 2024 (Publicado Nov. 15, 2024)

Shaffer, H. B., Parra-Olea, G., Wake, D., & Flores-Villela, O.

(2008). Ambystoma altamirani. The IUCN Red List

of Threatened Species 2008: e.T59049A11875320.

https://doi.org/10.2305/IUCN.UK.2008.RLTS.

T59049A11875320.en

Venâncio, C., Gabriel, A., Oliveira, M. E. D. E. S., & Lopes,

I. (2022). Feeding exposure and feeding behaviour as

relevant approaches in the assessment of the effects

of micro(nano)plastics to early life stages of amphi-

bians. Environmental Research, 212, 113476. https://

doi.org/10.1016/j.envres.2022.113476