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Determining Priority Areas for an Endangered Cold-Adapted Snake on Warming Mountaintops

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Determining Priority Areas for an Endangered Cold-Adapted Snake on Warming Mountaintops Determining priority areas for an Endangered cold-adapted snake on warming mountaintops E DVÁRD M IZSEI,MÁRTON S ZABOLCS,LORÁND S ZABÓ,ZOLTÁN B OROS K UJTIM M ERSINI,STEPHANOS A. ROUSSOS,MARIA D IMAKI Y ANNIS I OANNIDIS,ZSOLT V ÉGVÁRI and S ZABOLCS L ENGYEL Abstract Spatial prioritization in systematic conservation areas for the conservation of single species. Our study planning has traditionally been developed for several to demonstrates that spatial prioritization for single umbrella, many species and/or habitats, and single-species applica- flagship or keystone species is a promising approach for the tions are rare. We developed a novel spatial prioritization conservation of species for which few data are available. model based on accurate estimates of remotely-sensed data Keywords Climate change, habitat suitability, land use, and maps of threats potentially affecting long-term species protected area, range shift, reptile, spatial conservation persistence. We used this approach to identify priority areas planning, Vipera graeca for the conservation of the Endangered Greek meadow viper Vipera graeca, a cold-adapted species inhabiting mountain- Supplementary material for this article is available at tops in the Pindos Mountains of Greece and Albania. We doi.org/./S transformed the mapped threats into nine variables to esti- mate conservation value: habitat suitability (climate suitabil- ity, habitat size, occupancy, vegetation suitability), climate change (future persistence, potential for altitudinal range Introduction shift) and land-use impact (habitat alteration, degradation, iological diversity has experienced significant losses as disturbance). We applied the Zonation systematic conserva- a result of a number of factors that directly or indi- tion planning tool with these conservation value variables as B rectly affect species. Amphibians and reptiles are among biodiversity features to rank the areas currently occupied by the groups most affected (Böhm et al., ; Ceballos et al., the species and to identify priority areas where the chances ). Reptiles are specifically threatened by habitat loss, for population persistence are highest. We found that % degradation and fragmentation, introduction of invasive of current habitats will become unsuitable by the s and species, pollution, pathogens and climate change, resulting that conservation actions need to be implemented to avoid in global population declines (Cox & Temple, ). extinction as this is already a threatened species with a nar- Global climate change plays a key role in the biodiversity row ecological niche. If threats are appropriately quantified crisis (Butchart et al., ), as it causes a redistribution of and translated into variables of conservation value, spatial biodiversity patterns (Pecl et al., ). Many species are conservation planning tools can successfully identify priority predicted to shift their range, mostly towards the poles or higher altitudes (Hickling et al., ;Chenetal.,). Spe- EDVÁRD MIZSEI (Corresponding author, orcid.org/0000-0002-8162-5293) cies adapted to high altitude habitats are thus particularly MÁRTON SZABOLCS ( orcid.org/0000-0001-9375-9937) and ZSOLT VÉGVÁRI threatened by climate change because they often have low ( orcid.org/0000-0002-2804-9282) Department of Tisza Research, Danube Research Institute, Centre for Ecological Research, Bem tér 18/C, 4026, dispersal ability, a high level of habitat specialization and Debrecen, Hungary. E-mail [email protected] fragmented distributions, all of which predict low probabil- LORÁND SZABÓ ( orcid.org/0000-0001-7105-715X) Department of Physical ity of range shift (Davies et al., ). Ectothermic animals Geography and Geoinformatics, University of Debrecen, Debrecen, Hungary such as reptiles are further threatened by climate change ZOLTÁN BOROS ( orcid.org/0000-0003-4364-9056) Bio Aqua Pro Ltd., because of their sensitivity to changes in the thermal Debrecen, Hungary landscape and low dispersal ability (Sinervo et al., ). KUJTIM MERSINI Protection and Preservation of Natural Environment in Albania, Mountain-dwelling species usually escape the changing Tirana, Albania thermal landscape by shifting their distributions to higher STEPHANOS A. ROUSSOS Department of Biological Sciences, University of North altitudes (Haines et al., ) but this is possible only if Texas, Denton, USA the local topography allows this (Şekercioğlu et al., ). MARIA DIMAKI Goulandris Natural History Museum, Kifissia, Greece Meadow vipers (Vipera ursinii complex) are among the YANNIS IOANNIDIS Biosphere, Ymittos, Greece most threatened reptiles of Europe. The Greek meadow SZABOLCS LENGYEL ( orcid.org/0000-0002-7049-0100) GINOP Sustainable viper Vipera graeca, a small venomous snake endemic to Ecosystems Group, Department of Tisza Research, Danube Research Institute, Centre for Ecological Research, Debrecen, Hungary the Pindos mountain range of Greece and Albania that Received December . Revision requested January . has recently been recognized as a separate species (Mizsei Accepted April . First published online March . et al., ), is the least known meadow viper in Europe This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, Downloaded fromdistribution, https://www.cambridge.org/core and reproduction in any medium,. IP address: provided 170.106.35.93 the original, work on 30 is Sep properly 2021 cited. at 00:45:17, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/termsOryx, 2021, 55(3),. https://doi.org/10.1017/S0030605319000322 334–343 © The Author(s), 2020. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605319000322 Priority areas for a cold-adapted snake 335 and is categorized as Endangered on the IUCN Red List been found despite extensive searches. To account for po- (Mizsei et al., ). The species has only known popula- tential spatial biases in sampling effort among sites, we re- tions, inhabiting alpine–subalpine meadows above , m sampled the presence dataset to obtain a spatially balanced on isolated mountaintops (Mizsei et al., ). The occupied subset of presence records, which represented all known habitats are the highest and coldest in the region; as the spe- populations (Fig. ). We used BIOCLIM climate variables, cies is adapted to cold environments it is sensitive to climate which have been successfully used to model the distribution change. These alpine habitats are threatened by overgraz- of several European reptiles, including vipers (Scali et al., ; ing and habitat degradation, which simplify vegetation struc- Martínez-Freiria, ; Mizsei et al., ). To ensure com- ture and reduce cover against potential predators. The spe- patibility with our previous work (Mizsei et al., ), we cies is strictly insectivorous, specializing on bush crickets used the same set of predictors: annual mean temperature and grasshoppers (Mizsei et al., ), and thus it is vulner- (BIO), temperature seasonality (BIO), annual precipita- able to changes in its primary prey resource caused by land tion (BIO) and precipitation seasonality (BIO). These use. Shepherds are known to intentionally kill these snakes, variables had high predictive performance and low in- which are held responsible for –% of lethal bites to sheep tercorrelations (r , .). We obtained these variables for annually in Albania (E. Mizsei, unpubl. data). current climatic conditions (mean of –) from Here we identify priority areas that could facilitate the the WorldClim . database at arc seconds resolution long-term persistence of V. graeca. We performed single (Hijmans et al., ). We generated the habitat suitability species spatial prioritization to identify areas based on model using ensemble modelling (Thuiller et al., ) in the conservation value attributes of the currently suitable BIOMOD package in R .. (R Core Team, ). We used landscape. We aimed to identify any populations likely to two linear model algorithms (Generalized Linear Models, disappear by the s and any populations likely to be GLM; Generalized Additive Models, GAM) and three strongholds where the species could benefit from targeted machine learning algorithms (Artificial Neural Networks, management and conservation. To provide guidelines for ANN; Random Forest, RF; Maximum Entropy, MaxEnt). conservation, we studied the overlap between priority areas Default settings were used to build the models (Thuiller and protected areas and explored the interrelationships et al., ). To increase model accuracy we generated da- of the conservation value variables to identify opportuni- tasets of pseudo-absences, which included real absence data ties for potential interventions. and random points at least km from the presence local- ities (a total of , points per dataset). We ran repli- cates with each of the five modelling algorithms for the Methods pseudo-absence datasets, which resulted in habitat suit- ability model replicates. In each model replicate we random- Approach We used spatial prioritization, an approach ly divided the presence data into training ( %) and testing rarely applied to single species (Adam-Hosking et al., subsets ( %). We used the four BIOCLIM variables as pre- ), which is based on quantifying known threats and dictors. We scored all individual model replicates by the transforming them into variables describing conservation true skill statistic (TSS;
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