Natural Protected Areas (NPAs) includes important species richness, and it is assumed that these are the best areas for biodiversity conservation. There are certain doubts, however, about the effectiveness of the NPAs in developing countries, where economic resources for conservation are scarce and NPAs are not monitored and managed efficiently. In the present study we assessed the species richness, diversity, abundance, and functional guilds of amphibians and reptiles inside and outside of the NPA Reserva Estatal de la Biósfera Sierra San Juan (REBSSJ), Nayarit, Mexico. Our results showed that species numbers of amphibian and reptiles were higher outside than inside the reserve, as well the individual number distributed among species, except for lizard species. Analyses of functional guilds showed that both richness and functional dispersion were greater in amphibians and reptiles outside the reserve. Likewise, outside the reserve we recorded a higher species number with some category of risk at the national level (NOM-059), international level (IUCN), and also by using the Environmental Vulnerability Score (EVS) algorithm. The results suggest that areas outside of the reserve are crucial to the maintenance of regional biodiversity, due to high complementarity with species composition inside of the reserves. These data can be used to implement conservation measures that include a new demarcation of the reserve and the consideration of surrounding areas to include a great number of species.

Amphibians, abundance, conservation, diversity, natural protected area, reptiles

Worldwide, the creation of Natural Protected Areas (NPAs) has been one of the major measures to conserve biodiversity (Rodrigues et al. 2004). Under certain scenarios, however, it has been found that parks may not be the optimal governance structure for promoting local conservation, primarily because economic and human resources are scarce (Hayes 2006) and such areas become only paper parks (Rife et al. 2013, Blackman et al. 2015). Mexico has 182 NPAs decreed under different categories, such as national parks, biosphere reserves, and natural monuments, among others (CONANP 2017).

In spite of the high number of NPAs registered currently, most of them have been established in an arbitrary way, because in most cases there is a lack of basic biological information of the species that are in these areas (Ervin 2003). As such, it is important to assess the efficiency of the decreed NPAs, because in most cases not all components of the biodiversity are preserved, e.g., species, vegetation types, ecosystems, homogeneity, and heterogeneity (Chape et al. 2005). On the other hand, these areas are damaged by anthropic effects, such as illegal looting of flora and fauna, pollution, deforestation, landscape fragmentation, and land-use change (Ervin 2003, Figueroa and Sánchez-Cordero 2008). This disturbance has been consistently evident in tropical areas of developing countries (Román-Cuesta and Martínez-Villalta 2006, Urbina-Cardona et al. 2006). For example, in Sierra San Juan, in Nayarit, Mexico there is a Reserva Estatal de la Biosfera Sierra San Juan (REBSSJ), which was declared in 1987 with the objective to stop the exploitation of banks of materials (González 2010). At the time of being declared as an NPA, however, government officials did not have available accurate information on diversity and abundance of the species, as well as the values of elements of biodiversity of landscape or the most outstanding natural processes; instead, it used as a criterion for its delimitation surface which is comprised up of 980 m a.s.l. (González 2010).

The REBSSJ is located at the westernmost extreme of the Mexican Transvolcanic Belt, in Sierra San Juan, which constitutes a geomorphological unit separated of this biogeographic province (Luhr 2000). Due to this isolation, the study of biological diversity in the REBSSJ is very interesting because it illustrates several vegetation types, which are semi-deciduous tropical forest, cloud forest, oak forest, pine forest, oak-pine forest, and secondary scrubland (Téllez 1995). In this area, there are at least 1250 species of plants and ferns (30% of the flora reported for Nayarit), of which 31 are endemic to Mexico (Téllez 1995), and at least 370 species of birds (44.9% reported from Nayarit; Espinosa 2000).

The amphibians and reptiles from this region have been poorly studied. The only previous study for the site is a catalogue of the species of this group by Bojórquez (2003). In this work, 36 species were reported from Sierra San Juan and 12 for the REBSSJ. In this catalogue is included the Mexican Spiny-tailed Iguana (Ctenosaura acanthura) and Tehuantepec Striped Snake (Geagras redimitus). Natural distribution of these species occurs quite far from REBSSJ, because the former species occurs in states bordering the Gulf of Mexico and the latter in the southeastern portion of the country (Ramírez-Bautista and Hernández-Ibarra 2004, Canseco-Márquez 2007); therefore, these two species suggest an erroneous of species identification from REBSSJ. Recently, Woolrich-Piña et al. (2016) published an article on the herpetofauna of Nayarit, in which they included a limited analysis of diversity in NPAs including REBSSJ. This revision was made based on literature reviews and opportunistic fieldwork only, so the authors did not conduct systematic fieldwork and the data presented on this paper concerning the REBSSJ should be taken with caution.

In order to assess the effectiveness of this NPA, the objectives of this study are: (i) to determine species richness, abundance, functional richness, functional equality, and functional dispersion of amphibians and reptiles inside and outside of the REBSSJ, and (ii) to compare diversity patterns inside and outside of the REBSSJ. This work is important because in spite of being a protected area, diverse anthropic activities are conducted within its boundaries, such as coffee and avocado cultivation, without supervised regulation or estimation of the impact on biodiversity. Thus our hypothesis of work is that because the natural protected area is surrounded by zones highly transformed; therefore there will be a different number of species and communities composition of amphibians and reptiles, with low number of species outside of reserve.

The herpetofauna of Nayarit had been ignored for a long time (Flores-Villela et al. 2004). Currently, however, it is known that the state has 154 species, including 34 anurans, two salamanders, one crocodylian, 107 squamates, and 10 turtles (Woolrich-Piña et al. 2016). In this study we recorded for the entire Sierra San Juan a total of 55 species, representing 35.5% of the state herpetofauna. Of this number of species, the area corresponding to REBSSJ has a herpetofauna of 34 species. Woolrich-Piña et al. (2016) mentioned that the herpetofauna of REBSSJ is composed by 73 species of amphibians and reptiles (19 anurans, 52 squamates, and two turtles). This number of species, however, was taken from the literature; only occasionally one of the authors visited the REBSSJ. Our results are the product of 39 months of fieldwork, which shows that the herpetofauna inside REBSSJ is composed of seven species of anurans, 25 squamates, and two tortoises. Our accumulation curves shows that our inventory of amphibians is complete and for reptiles between nine and 17 species are expected to be recorded in order to achieve the asymptote and completeness of the inventory. Thus, Woolrich-Piña et al. (2016) results overestimated the herpetological biodiversity inside the reserve because they did not conduct a systematic field sampling. In this sense, monitoring and field studies in natural protected area, as well as its surrounding areas represent the best strategies for documenting species richness, as well as diverse aspects of the recorded species, such as natural history, population density, and communities structure (Ervin 2003, Rodrigues et al. 2004). In addition to the bibliographic review and revision of data bases are important sources for evaluating and the decree of the natural protected areas (Ervin 2003).

Inside of REBSSJ was found a lower species number than outside of this NPA. This pattern is similar to that seen in other studies that analyzed species richness and abundance of species from different biological groups inside and outside of a NPA as mammals (Decher and Bahian 1999, Caro 2001), birds (Herremans 1998), and fungi (Bhagwat et al. 2005). In this study we recorded a remarkable increase in species richness and abundance of the herpetofauna outside the reserve. This difference could be explained by environmental heterogeneity among areas, which generates edge effect (Schlaepfer and Gavin 2001), and modification of the environment toward agro-ecosystems, such as shade coffee plantations (Pineda et al. 2005), and land-use change involving grazing areas (Gardner et al. 2007). For example, in two different studies by Bell and Donnelly (2006) and Berriozabal-Islas et al. (2017), with amphibians and reptiles in the former, and with lizard in the last; in both studies the composition of communities was different to those preserved environments. These studies found a decrease in species richness and diversity to transformed environments. These results show a remarkable difference in species richness and composition of communities among areas (Gardner et al. 2007, Berriozabal-Islas et al. 2017).

Inside the REBSSJ we recorded a lower species number of amphibian and reptiles, with Craugastor of the former group the dominant genus. Species of this genus are associated with temperate environments, such as pine forest and pine-oak forest, which were dominant in this area of the reserve (Meza-Parral and Pineda 2015). This pattern is promoted by the vegetation cover of the area, as shown in other studies (Urbina-Cardona et al. 2006, Cruz-Elizalde et al. 2016). Although inside the reserve there exists a higher portion of preserved forest, without apparent agricultural modification, in this area only a species of hylid frog (Sarcohyla bistincta) occurs; in contrast, outside of the reserve we recorded five species of hylid frogs (Agalychnis dacnicolor, E. smaragdina, S. bistincta, Smilisca baudinii, and Tlalocohyla smithii). These results, in the former case, might be associated with the fact that inside the reserve there are no permanents water bodies, which provide the necessary requirements for these kind of species (Wiens et al. 2006), although inside of the reserve there is a high proportion of tree coverage, mainly oak-pine forest and cloud forest (Téllez 1995) in which these species are distributed (Wiens et al. 2006, Cruz-Elizalde et al. 2016). In the latter case, the result might be due to the fact that outside the reserve there exist patches of tropical vegetation, such as semi-deciduous rainforest and cloud forest with temporary streams that provide the necessary requirements for species reproduction, and therefore, a high species diversity of this group (Pineda et al. 2005, Wiens et al. 2006). This pattern is similar to those reported for tropical environments from low elevations, where the species diversity of the family Hylidae was high (Pineda et al. 2005, Cruz-Elizalde et al. 2016).

It is well known that the NPAs are important for nature conservation (Ervin 2003). This study showed that places outside the reserve are represented by cultivated zones of mango and avocado, grazing areas, and shade coffee plantations, which maintain a high species richness and abundance for both amphibians and reptiles. In this sense it has been reported that the surrounding matrix of the protected areas plays an important role in the protection of some species (Halpin 1997, Hannah et al. 2002), in particular for those species with high mobility (Estrada et al. 1994, Caro 2001). Halpin (1997) and Hannah et al. (2002) coincide that climate change affect the structure and dynamics of the landscape, mainly in natural protected areas. These authors pointed out that due to climatic change, diverse species can change their range of migration at large scale (Peters and Darling 1985), and at local scale, their altitudinal distribution in a linear way, mainly in mountains (Peters and Darling 1985, Halpin 1997, Hannah et al. 2002), modify species composition inside and outside of reserves or preserved environments (Halpin 1997). These patterns of variation of species among areas have been tested in mammals of rain forest in Los Tuxtlas, Mexico (Estrada et al. 1994), or inside and outside of natural protected area from Tanzania (Caro 2001). Among reptiles, lizards and snakes showed two patterns in richness and abundance between sites. Lizards, both inside and outside the reserve showed similar species number (11 species); however, inside of the reserve a high number of individuals occurred than outside. In this sense, species that occurred in both inside and outside of the reserve were of the genus Sceloporus, which showed tolerance for the transformed environments due to physiological advantages as impermeable skin or high tolerance to aridity, use a high diversity of environments, and diversity of habits (e.g., saxicolous, arboreal; Macip-Ríos and Muñoz-Alonso 2008). These patterns have been promoted by heterogeneous environments that are reflected in a high number of microhabitats, such as logs, rocks, holes, accumulated rocks, left litter, open areas, which in turn will generate perch sites (Luja et al. 2008). These conditions are favorable to S. utiformis and A. nebulosus because they were dominant species in both inside and outside the reserve. This dominant pattern has been reported in lizard species from tropical environments (Gardner et al. 2007, Vitt et al. 2007).

Among snakes, a high number of species and individuals were found outside of the reserve. This phenomenon is explained by the high dispersal capacity of this group of reptiles, species of which have a larger home range than do lizard species (Vitt et al. 2007). In addition, most of the recorded snakes are nocturnal; therefore, the occurrence outside of the reserve might be related to the presence of water bodies, where abundance of the amphibians is high, with these snakes feeding on this group (Cadle and Greene 1993, França et al. 2008).

Studies on fragmented tropical environments show that the transformation of environments reduces the alpha diversity, but increase the diversity at a landscape level (Vitt and Caldwell 2001). This pattern is similar to our results, because species composition for both communities (inside and outside) was complementary. For example, inside the reserve, the amphibian C. augusti was the exclusive species, and Incilius mazatlanensis and Rhinella marina were exclusive outside of the reserve. Similar patterns occurred in lizards and snakes; places outside the reserve had a higher number of exclusive species, such as Drymobius margaritiferus, Oxybelis aeneus, and A. bilineatus inhabiting tropical environments (França et al. 2008).

In addition to remarkable differences in species richness and abundance of amphibian and reptiles between sites, outside the reserve we recorded higher scores of functional diversity in both amphibians and reptiles. Such differences suggest a more complex network of interactions among the components of biodiversity outside the reserve. Outside the reserve there is a more heterogeneous landscape, which gives the species the opportunity to diversify in terms of guilds (habitat, food, or habits). Therefore, if these sites are not considered within the measures of conservation, biodiversity will be severely eroded. Finally, outside the reserve we found a major species number under some category of protection of the IUCN (2016), NOM-059, as well a high species number under the category of medium environmental vulnerability (Table 4). This reserve belongs to an important region in the context of biodiversity, because currently new forms of amphibian species have been recognized there (Caviedes-Solís et al. in preparation), which suggests that species richness for this area will increase in the future.

Our results suggest that in addition to protecting the area designated as NPA’s, studies in surrounding areas should be carried out to consider the possibility of protecting a greater amount of habitat that should include semi-deciduous tropical forest and cloud forest to conserve a higher number of species (Toledo and Fernades Batista 2012). In this sense, the analyzed areas require a good programs of plans and management for conservation of the reserve and its boundaries (Herremans 1998, Caro 2001, Bhagwat et al. 2005, Becker et al. 2010).

Thanks go to Jorge Chaparro and family for their help in the field, and to Paul López, the owner of “La Noria” ranch, for his logistic support. Several people donated via crowdfunding to support the last part of the fieldwork: Beatriz Luja, Beatriz Molina, Azucena Loza, Jesús Loc, Jacobo Reyes; thank you very much all. We also thank Larry David Wilson for his language review and comments to improve the manuscript, and Christian Berriozabal for his help with some data analysis. We thank two anonymous reviewers for their comments that improved our manuscript.