diversity Article What Makes a Hot-Spring Habitat “Hot” for the Hot-Spring Snake: Distributional Data and Niche Modelling for the Genus Thermophis (Serpentes, Colubridae) Sylvia Hofmann 1,* , Peter Fritzsche 2, Tsering Dorge 3, Georg Miehe 4 and Michael Nothnagel 5,6 1 Centre of Taxonomy and Evolutionary Research, Zoological Research Museum Alexander Koenig, Adenauerallee 160, 53113 Bonn, Germany 2 Institute of Zoology, Martin-Luther University, Domplatz 4, 06108 Halle, Germany; [email protected] 3 Department of Biology, Faculty of Science, Tibet University, Lhasa 850000, China; [email protected] 4 Department of Geography, Philipps-Universität Marburg, Deutschhausstrasse 12, 35032 Marburg, Germany; [email protected] 5 Statistical Genetics and Bioinformatics, Cologne Center for Genomics, University of Cologne, Weyertal 115b, 50931 Cologne, Germany; [email protected] 6 Faculty of Medicine, The Cologne University Hospital, Kerpener Str. 62, 50937 Cologne, Germany * Correspondence: [email protected] Abstract: Knowledge about species’ distributions is central to diverse applications in ecology, bio- geography, and conservation science. Hot-spring snakes of the genus Thermophis share a distribution restricted to geothermal sites at the Tibetan Plateau (T. baileyi) and in the Hengduan Mountains Citation: Hofmann, S.; Fritzsche, P.; (T. zhaoermii, T. shangrila). Although the suture zones of these regions are widely covered with hot Dorge, T.; Miehe, G.; Nothnagel, M. springs, Thermophis populations are restricted to only a few of these habitats. Here, we use bioclimatic, What Makes a Hot-Spring Habitat topographic, and land cover data to model the potential distribution of the genus. Moreover, using “Hot” for the Hot-Spring Snake: logistic regression on field survey data of T. zhaoermii, we test whether hot-spring water parameters Distributional Data and Niche and landscape features correlate with the species’ presence or absence. Hot springs with temperatures Modelling for the Genus Thermophis between 45 and 100 ◦C and winter precipitation showed the most predictive power. At small scale, (Serpentes, Colubridae). Diversity our data support the relevance of the hot-spring temperature on the species’ occurrence and indicate 2021, 13, 325. https://doi.org/ 10.3390/d13070325 that also the along-valley distance from the hot-spring site to the major river might influence the distribution of Thermophis species. Our findings contribute to better understand factors shaping the Academic Editor: Luca Luiselli current distribution of the genus and will aid in setting priorities in applied conservation biology for the hot-spring snakes. Received: 5 July 2021 Accepted: 14 July 2021 Keywords: hot-spring keel-back; distribution; habitat suitability; Hengduan Mountains; Qinghai- Published: 16 July 2021 Tibet-Plateau Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affil- 1. Introduction iations. Understanding the factors underlying the distribution patterns of species is one of the major tasks of ecology and biogeography [1,2]. It is, moreover, of prime concern for biodiversity conservation. The Tibetan Plateau and the Hengduan Mountains pose as unique biogeographic Copyright: © 2021 by the authors. zones since they are among the world’s ecologically most diverse areas [3,4]. The Hengduan Licensee MDPI, Basel, Switzerland. Mountains comprise more than 500,000 km2 of temperate and alpine ecosystems that run This article is an open access article along a north–south orientation at the eastern margin of the Himalayan range, in the distributed under the terms and southeastern corner of the Tibetan Plateau. Its southeastern quarter is one of the world’s conditions of the Creative Commons most important biodiversity hotspots characterized by high levels of species richness and Attribution (CC BY) license (https:// endemism [5]. Similarly, the Tibetan Plateau supports high species diversity. With an area creativecommons.org/licenses/by/ of 2.5 million km2 and an average elevation of 4500 m above sea level (a.s.l.), the highlands 4.0/). Diversity 2021, 13, 325. https://doi.org/10.3390/d13070325 https://www.mdpi.com/journal/diversity DiversityDiversity2021 2021, 13, 13, 325, x FOR PEER REVIEW 2 2of of 12 11 compriseWith an area 95% of of 2.5 the million Earth’s km surface2 and an above average 4400 elevation m [6]. It of encompasses 4500 m above the sea world’s level (a.s.l.), largest subnivalthe highlands and alpine comprise ecosystems, 95% of the and Earth’s a multitude surface of above temperate 4400 m and [6]. subtropical It encompasses mountain the forestworld’s ecosystems largest subnival [7,8]. and alpine ecosystems, and a multitude of temperate and sub- tropicalTheir mountain biodiversity forest facesecosystems major [7,8]. threats from biotope destruction, habitat loss, hy- dropowerTheir projectsbiodiversity and pollutionfaces major due threats to urbanization from biotope and destruction, economic development,habitat loss, hydro- illegal wildlifepower projects trade, and and from pollution the consequences due to urbani ofzation global climateand economic warming development, [9–11]. Among illegal the mostwildlife critical trade, conservation and from the actions consequences needed forof global the flora climate and faunawarming of both [9–11]. regions Among are the the identification,most critical conservation establishment, actions and protection needed for of the areas flora that and are fauna important of both for regions species are popula- the tionsidentification, to mitigate establishment, a loss of biodiversity and protection [12–14]. of Information areas that are on species’important distribution for species patterns popu- andlations ecological to mitigate niches a loss is crucial of biodiversity for these [12– tasks.14]. Information on species’ distribution pat- ternsThe and rare ecological hot-spring niches snakes is crucialThermophis for these zhaoermii tasks. , GUO, LIU, FENG, and HE, 2008, and T.The shangrila rare hot-spring, PENG, LU, snakes HUANG, Thermophis GUO, zhaoermii and ZHANG,, GUO, 2014, LIU, are FENG, geographically and HE, 2008, sepa- ratedand T. from shangrila their, sisterPENG, species, LU, HUANG, namely GUO, the Tibetan and ZHANG, hot-spring 2014, snake are T.geographically baileyi, WALL, sepa- 1907. Allrated species from their share sister a strong species, association namely the with Tibetan geothermal hot-spring sites snake in high T. baileyi elevation, WALL, areas 1907. and, thus,All species also a severeshare a threatstrong from association habitat with destruction geothermal due tosites the in construction high elevation of geothermalareas and, powerthus, also stations a severe or otherthreat commercial from habitat establishments destruction due at to the the hot construction springs [15 of,16 geothermal]. A major deficiencypower stations in knowledge or other commercial about these establishments species is the at extent the hot of springs their geographic [15,16]. A major range, de- es- peciallyficiency within knowledge respect to aboutT. zhaoermii these speciesand T. is shangrila the extent. While of their a patchy geographic distribution range, espe- along thecially main with part respect of the to Yarlung T. zhaoermii suture and zone T. inshangrila southern. While central a patchy Tibet hasdistribution been suggested along the for T.main baileyi part[17 of], theT. zhaoermii Yarlung hassuture only zone been in recordedsouthern fromcentral its Tibet type has locality been insuggested Litang County, for T. Sichuanbaileyi [17], Province T. zhaoermii [18,19 ],has while onlyT. been shangrila recordedis known from its from type two locality localities in Litang in Shangri-La, County, YunnanSichuan province Province (Figure [18,19],1 ;[while20,21 T.]). shangrila is known from two localities in Shangri-La, Yunnan province (Figure 1; [20,21]). FigureFigure 1.1. MapMap of the currently known known distribution distribution of of ThermophisThermophis baileyi baileyi, ,T.T. zhaoermii zhaoermii, and, and T.T. shangrila shangrila. Records are according to [17,18,21] and based on our survey data. Locations where we did not find Records are according to [17,18,21] and based on our survey data. Locations where we did not find Thermophis are included in the map (absence). Hot-spring sites are drawn according to the “Atlas of Thermophis are included in the map (absence). Hot-spring sites are drawn according to the “Atlas of Tibet” [22]. Type localities of the three species are imprecise in the original descriptions and cannot Tibet”be mapped [22]. Typeexactly– localitiesT. baileyi of: the “Thibet”; three species T. shangrila are imprecise: “Shangri-La, in the Northern original Yunnan, descriptions China” and but cannot co- beordinates mapped match exactly– Yulong,T. baileyi Lijian: “Thibet”;g, YunnanT. Province, shangrila: China; “Shangri-La, T. zaoermii Northern: Litang Yunnan, County, China” Sichuan, but coordinatesChina (probably match locality Yulong, no. Lijiang,12 according Yunnan to [20]). Province, The extension China; T. ofzaoermii the Hengduan: Litang Mountains County, Sichuan, region China(HMR) (probably is roughly locality reflected no. by 12 its according typical te tomperate [20]). The coniferous extension forests of the ecoregion Hengduan [23]. Mountains region (HMR) is roughly reflected by its typical temperate coniferous forests ecoregion [23]. Diversity 2021, 13, 325 3 of 11 Compared with the Tibetan