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Corresponding author: Aníbal H. Díaz de la Vega-Pérez ( anibal.helios@gmail.com ) Academic editor: Anthony Herrel
© 2019 Aníbal H. Díaz de la Vega-Pérez, Víctor H. Jiménez-Arcos, Eric Centenero-Alcalá, Fausto R. Méndez-de la Cruz, Andre Ngo.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Díaz de la Vega-Pérez AH, Jiménez-Arcos VH, Centenero-Alcalá E, Méndez-de la Cruz FR, Ngo A (2019) Diversity and conservation of amphibians and reptiles of a protected and heavily disturbed forest of central Mexico. ZooKeys 830: 111-125. https://doi.org/10.3897/zookeys.830.31490
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The high loss rate of forest ecosystem by deforestation in the Trans-Mexican Volcanic Belt is one of the principal ecological problems of central Mexico, even in natural protected areas. We compiled a checklist and determined β-diversity indexes of amphibians and reptiles of the highly disturbed protected area, La Malinche National Park (LMNP) in Mexico, to determine the principal habitats for herpetofaunal conservation. After our extensive eight-year field sampling, we documented 28 species (nine amphibians and 19 reptiles), representing 11 families and 18 genera; four of these species are new records for LMNP. Of the species, 89% are endemic to Mexico. The IUCN Red List considers 22 species as Least Concern, one as Near Threatened, and four as Vulnerable. Meanwhile, the Environmental Viability Scores categorize three species as low vulnerability, 15 as medium, and 10 as high. According to the Mexican list of protected species, eight species are under Special Protection and nine are considered Vulnerable. The dissimilarity index between habitat types (βsør) in both groups is high, principally due to the environmental gradient generated by the altitudinal range. Abies and Pine forest are high diversity areas for amphibians and reptiles, respectively, and must be considered for special protection. LMNP hosts more than 60% of the herpetofauna of Tlaxcala and is the principal “conservation island” for this state. Therefore, based on the percentage of state species represented, endemism and the current social and ecological problems, additional efforts that involve the local communities to protect the biodiversity of this National Park are necessary.
Herpetofauna, natural protected area, high mountain ecosystem, β-diversity
Mexico presents the highest richness of amphibians and reptile species in Mesoamerica (Mexico, Belize, Guatemala, El Salvador, Honduras, Nicaragua, Costa Rica, and Panama) not solely due to the sheer size of the country (
This volcano and the surrounding area were designated La Malinche National Park (LMNP) in 1938. Despite this designation, this protected natural area is still subject to numerous ecological and social problems; nearly 60% of its original vegetation has been removed by local communities for crops and to expand their urban settlements (
Previous studies in LMNP have documented 23 reptile and amphibian species (15 and eight species, respectively) in the area. In 1978, Sánchez-de Tagle performed the first herpetofaunal assessment of LMNP, reporting two amphibian species and seven reptile species. Two years later, in a study of Tlaxcala´s herpetofauna,
Checklist of amphibians and reptiles of La Malinche National Park, Mexico. We provide the state presence, habitat type (Cropland = C, Pine-Oak forest = POF, Pine forest = PF, Abies forest = AF, Alpine grassland = AG, Oak forest = OF, Human constructions = HC, Pine-Alnus forest = PAF), IUCN status (Least Concern = LC, Near Threatened = NT, Vulnerable = V, Endangered = E, Critically Endangered = CE) according to the IUCN Red List, the Environmental Vulnerability Score (The EVS range is broken into the following three categories: low (3–9), medium (10–13), and high vulnerability (14–19) from
State | Habitat type | IUCN status | EVS score | NOM 059 2010 | Source | |
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Class Amphibia | ||||||
Order Caudata | ||||||
Family Ambistomatidae | ||||||
Ambystoma velasci* | P/T | C, HC | LC | 10 | Pr | 6,7 |
Family Plethodontidae | ||||||
Aquiloeurycea cephalica* | P/T | AF | NT | 14 | A | 4, 7 |
Chiropterotriton orculus* | P/T | AF | VU | 18 | NL | 4,5,7 |
Isthmura bellii* | T | – | VU | 12 | A | 4 |
Pseudoeurycea gadovii* | P/T | AF | VU | 13 | Pr | 1,2,4,7 |
Pseudoeurycea leprosa* | P/T | POF, PF, AF, PAF | LC | 16 | A | 1,2,4,6,7 |
Order Anura | ||||||
Family Hylidae | ||||||
Dryophytes eximius * | P/T | C, POF, PF, PAF | LC | 10 | NL | 6,7 |
Dryophytes plicatus* | P/T | C, PF, HC | LC | 11 | A | 7 |
Family Scaphiopodidae | ||||||
Spea multiplicata | P/T | C, OF, PF, HC, PAF | LC | 6 | NL | 4,6,7 |
Class Reptilia | ||||||
Order Squamata | ||||||
Suborder Lacertilia | ||||||
Family Anguidae | ||||||
Barisia imbricata* | P/T | C, POF, PF, AF, AG, OF, PAF | LC | 14 | Pr | 1,4,6,7 |
Family Phrynosomatidae | ||||||
Phrynosoma orbiculare* | P/T | C, POF, PF, AG | LC | 12 | A | 1,4,6,7 |
Sceloporus aeneus* | P/T | C, POF, PF, AG, HC, PAF | LC | 13 | NL | 2,4,6,7 |
Sceloporus bicanthalis* | P/T | PF, AG, PAF | LC | 13 | NL | 1,4,6,7 |
Sceloporus grammicus | P/T | C, POF, PF, AF, AG, OF, HC, PAF | LC | 9 | Pr | 1,2,4,6,7 |
Sceloporus megalepidurus* | T | C | VU | 14 | Pr | 2,4 |
Sceloporus scalaris* | T | AG | LC | 12 | NL | 4,6 |
Sceloporus spinosus* | T | C, HC | LC | 12 | NL | 7 |
Family Scincidae | ||||||
Plestiodon brevirostris* | P/T | C, POF, PF, AF, HC | LC | 11 | NL | 2,4,6,7 |
Plestiodon lynxe* | T | – | LC | 10 | Pr | 4 |
Family Teiidae | ||||||
Aspidoscelis costata* | T | C, OF, HC | LC | 11 | Pr | 2,3,7 |
Order Squamata | ||||||
Suborder Serpentes | ||||||
Family Colubridae | ||||||
Conopsis lineata* | P/T | C, POF, PF | LC | 13 | NL | 7 |
Pituophis deppei* | P/T | C | LC | 14 | A | 7 |
Salvadora bairdi* | T | C | LC | 15 | Pr | 7 |
Family Natricidae | ||||||
Storeria storerioides* | P/T | C, POF, OF, PF | LC | 11 | NL | 4,5,7 |
Thamnophis eques | T | C, PF | LC | 8 | A | 6 |
Thamnophis scalaris* | P/T | C, POF, PF, AF, AG, OF, HC, PAF | LC | 14 | A | 1,2,4,6,7 |
Family Viperidae | ||||||
Crotalus ravus* | P/T | C, POF, PF, AG, HC, PAF | LC | 14 | A | 1,2,4,6,7 |
Crotalus triseriatus* | P/T | POF, PF, AF, AG, OF, PAF | LC | 16 | NL | 1,2,4,6,7 |
Amphibians and reptiles are ideal bio-indicators of the ecosystem health due to their high sensitivity to environmental change; nevertheless, they are not the most common study groups (
LMNP is found between the Mexican states of Tlaxcala (70%) and Puebla (19.240195N; -98.034472W). It covers an area of 46,112 ha, ranges in elevation from 2400 to 4461 m, and is largest national park in the TMVB (
We generated this list of the amphibians and reptiles of the LMNP from: 1) available herpetofaunal literature:
We performed an average of seven-field visits per year for five days (four to five people per visit). We included dry and wet seasons all around the volcano slopes and in eight different habitat types (community vegetation and human modification types, see Results section). We made at least one visit to each community vegetation and human modification type each season every year. The sampling was homogeneous among slopes and vegetation types. We used direct capture methods with diurnal and nocturnal searching (nocturnal surveys were less frequent because LMNP is highly insecure). All species previously reported in the literature from field sampling efforts were included in the present list, even if we could not confirm the record by direct observation or by vouchers in a scientific collection. We deposited images of vouchers of new species records in the Instituto de Biología, UNAM (CNAR-IB) scientific collection.
We included the conservation status of each species according to: 1) the IUCN Red List 2018; 2) environmental viability scores (EVS) from
We use the Sørensen dissimilarity index (βsør) as our approach to determine beta-diversity (Sørensen 1948). The βsør quantifies the proportion of species shared between two communities incorporating both true spatial turnover (i.e. taxonomic turnover) and differences in richness by nesting (
The herpetofauna of LMNP includes 28 species: nine amphibians (six caudates and three anurans) and 19 reptiles (11 lizards and eight snakes). These taxa represent 11 families (four amphibians and seven reptiles) and 18 genera (seven amphibians and 11 reptiles). All the species of the present list were found in Tlaxcala, and eight of these species were only recorded from this state (one amphibian and seven reptiles) (Table
We added four previously undocumented species from LMNP. Three of these new records, the frog, Dryophytes plicatus (CNAR-IB-RF 515-516), the lizard, Sceloporus spinosus (CNAR-IB-RF 517-518), and the snake Salvadora bairdi (observation), were made by direct capture or observations in the field (Table
Four of the reptile and amphibian species found in LMNP are considered Vulnerable according to the IUCN Red List (three amphibians and one reptile); one Near Threatened (the salamander Aquiloeurycea cephalica); and 23 Least Concern (five amphibians and 18 reptiles) (Table
We identified eight different habitats (community vegetation and human modification types) occupied by amphibians and reptiles in LMNP: Oak forest (OF), Pine forest (PF), Abies forest (AF), Pine-Oak forest (POF), Pine-Alnus forest (PAF), Alpine grassland (AG), Human constructions (HC), and Cropland (C). We excluded the AG habitats from amphibian βsør analysis, because, no species were recorded at those elevations. The vegetation communities inhabited by the most amphibians were Abies forest, Pine forest, and croplands (four species each). While, the most commonly occupied habitats for reptiles were croplands (15 species), Pine forest (13), and Pine-Oak forest (10) (Fig.
The average dissimilarity for amphibians, was 0.60±0.29 (mean ± 1SD). The highest average of taxonomic replacement was recorded in AF (0.86±0.16), where three plethodontid salamander species were found exclusively in this habitat. In contrast, PF had the lowest dissimilarity (0.42±0.23) among habitat types, with no species unique to the habitat (Table
Sørensen pairwise dissimilarity (βsør) among vegetation types for the amphibians of LMNP. The average βsør for vegetation types and regional βsør values are shown with one standard deviation. Note that the Alpine grassland was excluded because no amphibian species were recorded in this habitat.
Habitat (unique species) | Pine-Oak forest | Pine forest | Abies forest | Oak forest | Human constructions | Pine-Alnus forest | Cropland |
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Pine-Oak forest (0) | |||||||
Pine forest (0) | 0.33 | ||||||
Abies forest (3) | 0.67 | 0.75 | |||||
Oak forest (0) | 1.00 | 0.60 | 1.00 | ||||
Human constructions (0) | 1.00 | 0.43 | 1.00 | 0.50 | |||
Pine-Alnus forest (0) | 0.20 | 0.14 | 0.71 | 0.50 | 0.67 | ||
Cropland (0) | 0.67 | 0.25 | 1.00 | 0.60 | 0.14 | 0.43 | |
Average βsør | 0.64 (±0.33) | 0.42 (±0.23) | 0.86 (±0.16) | 0.70 (±0.24) | 0.62 (±0.34) | 0.44 (±0.24) | 0.51 (±0.31) |
Regional βsør | 0.60 (±0.29) |
Sørensen pairwise dissimilarity (βsør) among vegetation types for the reptiles of LMNP. The average βsør for vegetation types and regional βsør values are showed with one standard deviation.
Habitat (unique species) | Pine-Oak forest | Pine forest | Abies forest | Alpine grassland | Oak forest | Human constructions | Pine-Alnus forest | Cropland |
Pine-Oak forest (0) | ||||||||
Pine forest (0) | 0.09 | |||||||
Abies forest (0) | 0.33 | 0.41 | ||||||
Alpine grassland (1) | 0.26 | 0.24 | 0.43 | |||||
Oak forest (0) | 0.38 | 0.44 | 0.27 | 0.47 | ||||
Human constructions (0) | 0.41 | 0.47 | 0.50 | 0.50 | 0.54 | |||
Pine-Alnus forest (0) | 0.38 | 0.33 | 0.45 | 0.20 | 0.50 | 0.54 | ||
Cropland (3) | 0.28 | 0.26 | 0.60 | 0.50 | 0.52 | 0.36 | 0.62 | |
Average βsør | 0.30 (±0.11) | 0.32 (±0.14) | 0.43 (±0.11) | 0.37 (±0.13) | 0.45 (±0.09) | 0.47 (±0.07) | 0.43 (±0.14) | 0.45 (±0.15) |
Regional βsør | 0.40 (±0.13) |
Sørensen pairwise dissimilarity (βsør) among vegetation types for the herpetofauna of LMNP. The average βsør for vegetation types and regional βsør values are showed with one standard deviation.
Habitat (unique species) | Pine-Oak forest | Pine forest | Abies forest | Alpine grassland | Oak forest | Human constructions | Pine-Alnus forest | Cropland |
---|---|---|---|---|---|---|---|---|
Pine-Oak forest (0) | ||||||||
Pine forest (0) | 0.14 | |||||||
Abies forest (3) | 0.43 | 0.52 | ||||||
Alpine grassland (1) | 0.33 | 0.36 | 0.56 | |||||
Oak forest (0) | 0.47 | 0.48 | 0.50 | 0.50 | ||||
Human constructions (0) | 0.55 | 0.46 | 0.68 | 0.58 | 0.53 | |||
Pine-Alnus forest (0) | 0.33 | 0.28 | 0.56 | 0.33 | 0.50 | 0.58 | ||
Cropland (1) | 0.35 | 0.26 | 0.71 | 0.57 | 0.54 | 0.31 | 0.57 | |
Average βsim | 0.37 (±0.13) | 0.36 (±0.14) | 0.56 (±0.10) | 0.46 (±0.11) | 0.50 (±0.02) | 0.53 (±0.12) | 0.45 (±0.13) | 0.47 (±0.17) |
Regional βsim | 0.46 (±0.13) |
Mexico has 864 species of reptiles and 376 species of amphibians (
LMNP plays an important role in Tlaxcala’s herpetofaunal preservation. First, this small area (~8.3% of the total length of the state) hosts more than 60% of the herpetofauna known from the entire state. Second, it is the largest protected area in the state (
Analysis of herpetofaunal habitat use provides insight to determine high diversity sites in LMNP that may warrant special attention. Abies forest has the highest level of taxonomic replacement in addition to hosting the greatest diversity of plethodontid species (four) in LMNP, highlighting the importance of this forest in future conservation plans. Also, the protection of Pine-Oak forest, Pine forest, and Oak forest communities is very important, due to presented high taxonomic turnovers in the two groups of organisms and in the interaction as herpetofaunal analysis. In addition, these habitats are under degradation and pressure from illegal logging, cattle grazing, and fire. According to
This study evaluates the richness and diversity of both protected and disturbed areas in the highly diverse central Mexico region; it provides valuable information on biodiversity to determine priority areas to consider for future management protection. More than 17% of the species (five) registered in LMNP are listed in the IUCN Red List, and 35% have a high EVS vulnerability score (10); despite this, only 60% of these amphibians and reptiles are protected by Mexican law. Paradoxically, 88% of amphibians and 89% of reptiles inhabiting this heavily disturbed and protected area are endemic to Mexico.
In addition, after three studies focusing on the herpetofauna of LMNP since 1978, we found four species previously unreported from the protected area; but, were unable to find another five species previously reported from there. The absence of vouchers, photos, or precise information makes it difficult to determine if these are legitimate records or if it was a case of misidentification of these five species. The worst-case scenario would be that these are incidents of short-term local extinctions (40 years) in a natural protected area. LMNP was decreed a protected area 80 years ago; nevertheless, the issues mentioned previously still have an impact on the biodiversity and the natural environment. In addition, the lack of security in LMNP limits research activities in the most important “conservation island” in Tlaxcala. Urgent actions to promote protection and preservation of the diversity in LMNP are necessary. We feel that these protective actions must involve the lowland communities, offering options to stop the high exploitation of natural resources and to demystify and promote the ecological importance of these two groups of vertebrates. Also, any policies should preserve the geographical connectedness of protected areas (biological corridors) to increase the possibility of exchange of the different vertebrates and vegetation from area to area.
We are grateful to Cátedras CONACyT program (project 883), Volkswagen-Por amor al planeta, project: “Estación Científica La Malinche: Investigación integrativa para la conservación y la Educación Ambiental”, and the Mohamed Bin Zayed Conservation Fund (project 162513838) for supporting financially this work. We are grateful to Martínez-Gómez M. and La Malinche Scientific Station for logistical support and to Secretaría de Medio Ambiente y Recursos Naturales for providing the collecting permits (SGPA/DGVS/15396/15 and SEMARNAT FAUT-074). We also thank to García-Vázquez U. and Lemos-Espinal J. for comments that greatly improved the manuscript.
Tables S1–S6
Data type: measurement