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Ecological Observations on Hybrid Populations of European Plethodontid Salamanders, Genus Speleomantes

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Ecological Observations on Hybrid Populations of European Plethodontid Salamanders, Genus Speleomantes diversity Article Ecological Observations on Hybrid Populations of European Plethodontid Salamanders, Genus Speleomantes Enrico Lunghi 1,2,3,4,* , Fabio Cianferoni 2,5 , Stefano Merilli 6, Yahui Zhao 1,* , Raoul Manenti 7,8 , Gentile Francesco Ficetola 7,9 and Claudia Corti 2 1 Key Laboratory of the Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beichen West Road 1, Beijing 100101, China 2 Museo di Storia Naturale dell’Università di Firenze, Museo “La Specola”, Via Romana 17, 50125 Firenze, Italy; [email protected] (F.C.); claudia.corti@unifi.it (C.C.) 3 Natural Oasis, Via di Galceti 141, 59100 Prato, Italy 4 Unione Speleologica Calenzano, Piazza della Stazione 1, Calenzano, 50041 Firenze, Italy 5 Istituto di Ricerca sugli Ecosistemi Terrestri (IRET), Consiglio Nazionale delle Ricerche (CNR), Sesto Fiorentino, 50019 Firenze, Italy 6 Speleo Club Firenze via Guardavia 8, 50143 Firenze, Italy; [email protected] 7 Department of Environmental Science and Policy, Universitòà degli Studi di Milano, Via Celoria, 26, 20133 Milan, Italy; [email protected] (R.M.); francesco.fi[email protected] (G.F.F.) 8 Laboratorio di Biologia Sotterranea “Enrico Pezzoli”, Parco Regionale del Monte Barro, 23851 Galbiate, Italy 9 Université Grenoble Alpes, Université Savoie Mont Blanc, CNRS, LECA, Laboratoire d’Ecologie Alpine, F-38000 Grenoble, France * Correspondence: [email protected] (E.L.); [email protected] (Y.Z.) Citation: Lunghi, E.; Cianferoni, F.; Abstract: Speleomantes are the only plethodontid salamanders present in Europe. Multiple studies Merilli, S.; Zhao, Y.; Manenti, R.; have been performed to investigate the trophic niche of the eight Speleomantes species, but none Ficetola, G.F.; Corti, C. Ecological of these studies included hybrid populations. For the first time, we studied the trophic niche of Observations on Hybrid Populations five Speleomantes hybrid populations. Each population was surveyed twice in 2020, and stomach of European Plethodontid flushing was performed on each captured salamander; stomach flushing is a harmless technique that Salamanders, Genus Speleomantes. allows stomach contents to be inspected. We also assessed the potential divergence in size and body Diversity 2021, 13, 285. https:// condition between natural and introduced hybrids, and their parental species. Previously collected doi.org/10.3390/d13070285 data on Speleomantes were included to increase the robustness of these analyses. In only 33 out of 134 Academic Editors: sampled hybrid Speleomantes we recognized 81 items belonging to 11 prey categories. The frequency Salvidio Sebastiano and of empty stomachs was higher in females and individuals from natural hybrid populations, whereas Michael Wink the largest number of prey was consumed by males. We compared the total length and body condition of 685 adult salamanders belonging to three types of hybrids and three parental (sub)species. Three Received: 25 May 2021 group of salamanders (one hybrid and two parental species) showed significantly larger size, whereas Accepted: 17 June 2021 no difference in body condition was observed. This study provided novel ecological information on Published: 23 June 2021 Speleomantes hybrid populations. We also provided insights into the potential divergence between hybrids and parental species in terms of size and body condition. We discuss our findings, and Publisher’s Note: MDPI stays neutral formulate several hypotheses that should be tested in the future. with regard to jurisdictional claims in published maps and institutional affil- Keywords: Speleomantes; Hydromantes; trophic niche; body condition; cave biology; biospeleology; iations. parental species; diet; size; capture-mark-recapture Copyright: © 2021 by the authors. 1. Introduction Licensee MDPI, Basel, Switzerland. European cave salamanders of the genus Speleomantes are the only plethodontids This article is an open access article living in the Europe, and are almost all endemic to Italy [1]. Seven of the eight Speleomantes distributed under the terms and S. ambrosii S. italicus S. flavus S. supramontis S. imperialis S. sarrabusensis S. conditions of the Creative Commons species ( , , , , , , Attribution (CC BY) license (https:// genei) live exclusively in Italy, while the range of one species (S. strinatii) extends to part creativecommons.org/licenses/by/ of French Provence [1]. Each species is distributed in a well-defined area, and no range 4.0/). overlap exists; Speleomantes distribution is likely shaped by geomorphology [2,3]. For S. Diversity 2021, 13, 285. https://doi.org/10.3390/d13070285 https://www.mdpi.com/journal/diversity Diversity 2021, 13, x FOR PEER REVIEW 2 of 8 French Provence [1]. Each species is distributed in a well-defined area, and no range overlap exists; Speleomantes distribution is likely shaped by geomorphology [2,3]. For S. ambrosii, the river Magra marks the separation of the two allopatric subspecies: the western S. ambrosii ambrosii and the eastern S. a. bianchii [1,4]. Although some phenotypic variability can be observed among Speleomantes [5–7], a valid method to phenotypically Diversity 2021, 13, 285 distinguish among species/subspecies is still lacking, thus their identification is based 2 of 7 mostly on geography [1,3]. The southern distribution of the latter reaches the norther limit of S. italicus, creating a narrow contact zone in which viable hybrid populations are found [1,8] (see Figureambrosii 1 ,of the Ref.8) river MagraThese marksnatural the hybrid separation populations of the two exhibit allopatric some subspecies: genetic the western divergence, S.which ambrosii is mainly ambrosii influencedand the eastern by theS. relative a. bianchii abundance[1,4]. Although of individuals some phenotypic of each variability parental species:can be in observed the northern among partSpeleomantes of the range[5 –there7], a validare populations method to phenotypicallyof S. a. bianchii distinguish introgressedamong with S. species/subspecies italicus, whereas isin stillthe lacking,southern thus area, their theidentification opposite occurs is based [8]. mostly on However, hybridsgeography do not [1, 3show]. The a southernclear divergence distribution of phenotypic of the latter characters reaches from the norther their limit of S. parental species;italicus therefore,, creating ahybrids narrow can contact also zone only in be which recognized viable hybridon the populations basis of their are found [1,8] geographic distribution(see Figure1 [8,9].of Ref. In [ addition8]) These to natural this natural hybrid hybrid populations zone, exhibithybrids some between genetic S. divergence, ambrosii andwhich S. italicus is mainly are also influenced related to by a thehuman-mediated relative abundance translocation. of individuals In 1983, of for each parental scientific purposesspecies: individuals in the northern of both part S. of italicus the range and thereS. a. ambrosii are populations were introduced of S. a. bianchii into aintrogressed natural cavewith in southernS. italicus Tuscany,, whereas outside in the southernthe natural area, range the oppositeof Speleomantes occurs [1,10]. [8]. However, Thirty hybrids do years after itsnot introduction, show a clear the divergence population of phenotypicwas genetically characters characterized from their and parental none of species; the therefore, individuals hybridshad a pure can genotype. also only beFor recognized 77% of individuals, on the basis the of majority their geographic of alleles distribution (>75%) [8,9]. In matched allelesaddition specific to this to S. natural a. ambrosii hybrid; for zone, 6% hybridsof individuals, between theS. ambrosiimajorityand of allelesS. italicus are also matched thoserelated of S. to italicus a human-mediated; and for 16% of translocation. individuals, In alleles 1983, of for S. scientific a. ambrosii purposes and of individualsS. of italicus wereboth recombinedS. italicus and[11].S. However, a. ambrosii thewere lack introduced of ecological into a naturalinformation cave inon southern this Tuscany, population outsideprevents the us naturalfrom evaluating range of Speleomantes the potential[1 ,10difference]. Thirty between years after these its introduction,non- the natural hybridspopulation and the washybrids genetically living in characterized the natural hybrid and none zone, of and the individualsto assess the had trophic a pure genotype. relationshipsFor between 77% of these individuals, populations the and majority the local of alleles fauna (>75%)[8,12]. Here matched we provide alleles specificthe to S. a. first assessmentambrosii of ;the for size, 6% ofbody individuals, condition, the and majority diet of of both alleles natural matched and thoseintroduced of S. italicus ; and hybrid populationsfor 16% of of Speleomantes individuals,. alleles of S. a. ambrosii and of S. italicus were recombined [11]. However, the lack of ecological information on this population prevents us from evaluating 2. Materials theand potential Methods difference between these non-natural hybrids and the hybrids living in the natural hybrid zone, and to assess the trophic relationships between these populations and In 2020 we surveyed five hybrid populations of Speleomantes that inhabit natural the local fauna [8,12]. Here we provide the first assessment of the size, body condition, and caves (Figure 1); each population was surveyed twice, once before (29 June–14 July) and diet of both natural and introduced hybrid populations of Speleomantes. after (3–10 September)
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