Species distribution modelling leads to the discovery of new populations of one of the least known European snakes, Vipera ursinii graeca, in Albania

in Amphibia-Reptilia
Restricted Access
Get Access to Full Text
Rent on DeepDyve

Have an Access Token?



Enter your access token to activate and access content online.

Please login and go to your personal user account to enter your access token.



Help

Have Institutional Access?



Access content through your institution. Any other coaching guidance?



Connect

Vipera ursinii graeca is a restricted-range, endemic snake of the Pindos mountain range in the southwestern Balkans. The subspecies was previously reported from eight localities in Greece and one locality in southern Albania. We used species distribution modelling based on climate data from known localities in Greece to estimate the potential distribution of the subspecies. The model predicted suitable areas for eleven mountains in southern Albania, which we visited in ten field expeditions in four years. Based on 78 live individuals and 33 shed skins, we validated the presence of the snake on eight of the eleven mountains. Six populations (Dhëmbel, Llofiz, Griba, Shendelli, Tomorr and Trebeshinë Mountains) are reported here for the first time. Morphological characters undoubtedly supported that all individuals found at these new localities belong to V. u. graeca. Genetic analysis of mitochondrial DNA sequences also confirmed the identity of the snakes as V. u. graeca and a low number of identified haplotypes suggested low genetic variability among populations despite significant spatial isolation. All localities were subalpine-alpine calcareous meadows above 1600 m. These high montane habitats are separated by deep valleys and are threatened by overgrazing, soil erosion, and a potential increase in the elevation of the tree line due to climate change. Our surveys increased the number of known populations by 60% and the known geographical range of the subspecies by approximately 30%. Our study serves as a baseline for further ecological research and for conservation measures for one of the least known European viperid snakes.

Species distribution modelling leads to the discovery of new populations of one of the least known European snakes, Vipera ursinii graeca, in Albania

in Amphibia-Reptilia

Sections

References

BandeltH.J.ForsterP.RöhlA. (1999): Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16: 36-48.

BaronJ.P.FerrièreR.ClobertJ.Saint GironsH. (1996): Life history of Vipera ursinii ursinii at Mont-Ventoux (France). Comptes rendus de l’Acadèmie des sciences. Sèrie 3 Sciences de la vie 319: 57-69.

BatesD.MächlerM.BolkerB.M.WalkerS. (2014): lme4: Linear mixed-effects models using Eigen and S4. R package version 1.0-5. Available at http://CRAN.R-project.org/package=lme4.

BeeverE.A.BrussardP.F. (2004): Community- and landscape-level responses of reptiles and small mammals to feral-horse grazing in the Great Basin. J. Arid. Environ. 59: 271-297.

BoakesE.H.McGowanP.J.K.FullerR.A.Chang-qingD.ClarkN.E.O’ConnorK.MaceG.M. (2010): Distorted views of biodiversity: spatial and temporal bias in species occurrence data. PLoS Biol. 8: e1000385.

BrooksT.KennedyE. (2004): Conservation biology: biodiversity barometers. Nature 431: 1046-1047.

BrunoS. (1989): Introduction to a study of the herpetofauna of Albania. Herpetol. Bull. 29: 16-41.

BusbyJ.R. (1991): BIOCLIM: a bioclimate analysis and prediction system. Plant Protection Quarterly (Australia).

ChondropoulosB.P. (1989): A checklist of Greek reptiles. II. The snakes. Herpetozoa 2: 3-36.

DimitropoulosA. (1985): First records of Orsini’s viper, Vipera ursinii (Viperidae) in Greece. Ann. Mus. Goulandris 7: 319-323.

EdgarP.BirdD.R. (2005): Action plan for the conservation of the meadow viper (Vipera ursinii) in Europe. Convention on the Conservation of European Wildlife and Natural Habitats Standing Commitee Council of Europe Strasbourg 32 pp.

EhrichD.GaudeulM.AssefaA.KochM.A.MummenhoffK.NemomissaS.ConsortiumI.BrochmannC. (2007): Genetic consequences of Pleistocene range shifts: contrast between the Arctic, the Alps and the east African mountains. Mol. Ecol. 16: 2542-2559.

ElithJ.GrahamC.H.AndersonR.P.DudíkM.FerrierS.GuisanA.HijmansR.J.HuettmannF.LeathwickJ.R.LehmannA.LiJ.LohmannL.G.LoiselleB.A.ManionG.MoritzC.NakamuraM.NakazawaY.OvertonJ.M.M.Townsend PetersonA.PhillipsS.J.RichardsonK.Scachetti-PereiraR.SchapireR.E.SoberónJ.WilliamsS.WiszM.S.ZimmermannN.E. (2006): Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29: 129-151.

ElithJ.PhillipsS.J.HastieT.DudíkM.CheeY.E.YatesC.J. (2011): A statistical explanation of MaxEnt for ecologists. Divers. Distrib. 17: 43-47.

FerchaudA.-L.UrsenbacherS.CheylanM.LuiselliL.JelićD.HalpernB.MajorÁ.KotenkoT.KeyanN.Crnobrnja-IsailovićJ.TomovićL.GhiraI.IoannidisY.ArnalV.MontgeraldC. (2012): Phylogeography of the Vipera ursinii complex (Viperidae): mitochondrial markers reveal an east-west disjunction in the Palaearctic region. J. Biogeogr. 39: 1836-1847.

FieldingA.H.BellJ.F. (1997): A review of methods for the assessment of prediction errors in conservation presence/absence models. Environ. Cons. 24: 38-49.

FilippiE.LuiselliL. (2004): Ecology and conservation of the meadow viper, Vipera ursinii, in three protected mountainous areas in central Italy. Ital. J. Zool. Suppl. 2: 159-161.

FranklinJ.MillerJ.A. (2009): Mapping Species Distributions: Spatial Inference and Prediction. Cambridge University PressCambridge, England.

GalbreathK.E.HafnerD.J.ZamudioK.R. (2009): When cold is better: climate-driven elevation shifts yield complex patterns of diversification and demography in an alpine specialist (American pika, Ochotona princeps). Evolution 63: 2848-2863.

GraceJ.BerningerF.NagyL. (2002): Impacts of climate change on the tree line. Ann. Bot. 90: 537-544.

GvoždikV.JandzikD.CordosB.RehákI.KotlíkP. (2012): A mitochondrial DNA phylogeny of the endangered vipers of the Vipera ursinii complex. Mol. Phylogenet. Evol. 62: 1019-1024.

HaxhiuI. (1998): The reptilia of Albania: species composition, distribution, habitats. Bonn. zool. Beitr. 48: 35-57.

HernandezP.A.GrahamC.H.MasterL.L.AlbertD.L. (2006): The effect of sample size and species characteristics on performance of different species distribution modeling methods. Ecography 29: 773-785.

HijmansR.J.CameronS.E.ParraJ.L.JonesP.G.JarvisA. (2005): Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25: 1965-1978.

JohnsonC.J.GillinghamM.P. (2005): An evaluation of mapped species distribution models used for conservation planning. Environ. Cons. 32: 1-12.

KéryM. (2002): Inferring the absence of species: a case study of snakes. J. Wildl. Manage. 66: 330-338.

KopsteinF.WettsteinO. (1920): Reptilien und Amphibien aus Albanien. Weh. Zool.-Bot. Ges. 70: 387-457.

KorsósZ.BarinaZ.PifkóD. (2008): First record of Vipera ursinii graeca in Albania (Reptilia: Serpentes, Viperidae). Acta Herpetol. 3: 167-173.

KotenkoT.Morozov-LeonovS.Y.MezhzherinS.V. (1999): Biochemical genetic differentiation of the steppe viper (Vipera ursinii group) in Ukraine and Romania. In: 10th Ordinary General Meeting of the Societas Europaea Herpetologica p. 88-90. Natural History Museum of Crete Irakleio.

LyetA.CheylanM.ProdonR.BesnardA. (2009): Prescribed fire and conservation of a threatened mountain grassland specialist: a capture-recapture study on the Orsini’s viper in the French Alps. Anim. Conserv. 12: 238-248.

LyetA.ThuillerW.CheylanM.BesnardA. (2013): Fine-scale regional distribution modelling of rare and threatened species: bridging GIS tools and conservation in practice. Divers. Distrib. 19: 651-663.

MacKenzieD.I.NicholsJ.D.LachmanG.B.DroegeS.Andrew RoyleJ.LangtimmC.A. (2002): Estimating site occupancy rates when detection probabilities are less than one. Ecology 83: 2248-2255.

MalcolmJ.R.LiuC.NeilsonR.P.HansenL.HannahL. (2006): Global warming and extinctions of endemic species from biodiversity hotspots. Conserv. Biol. 20: 539-548.

MariniL.FontanaP.ScottonM.KlimekS. (2009): Vascular plant and Orthoptera diversity in relation to grassland management and landscape composition in the European Alps. J. Appl. Ecol. 45: 361-370.

MerowC.SmithM.J.SilanderJ.A. (2013): A practical guide to MaxEnt for modeling species’ distributions: what it does, and why inputs and settings matter. Ecography 36: 1058-1069.

MizseiE.ÜvegesB. (2012): Novel defensive behaviours of both sexes of Vipera ursinii graeca (Serpentes: Viperidae). Herpetol. Notes 5: 481-483.

MonasterioC.SalvadorA.IraetaP.DíazJ.A. (2009): The effects of thermal biology and refuge availability on the restricted distribution of an alpine lizard. J. Biogeogr. 36: 1673-1684.

NilsonG.AndrénC. (1988): A new subspecies of the subalpine meadow viper, Vipera ursinii (Bonaparte) (Reptilia, Viperidae), from Greece. Zool. Scr. 17: 311-314.

NilsonG.AndrénC.JogerU. (1993): A re-evaluation of the taxonomic status of the Moldavian steppe viper based on immunological investigations, with a discussion of the hypothesis of secondary intergradation between Vipera ursinii rakosiensis and Vipera (ursinii) renardi. Amphib.-Reptil. 14: 45-57.

NilsonG.AndrénC. (2001): The meadow and steppe vipers of Europe and Asia – the Vipera (Acridophaga) ursinii complex. Acta Zool. 47: 87-267.

PhillipsS.J.AndersonR.P.SchapireR.E. (2006): Maximum entropy modeling of species geographic distributions. Ecol. Model. 190: 231-259.

R Core Team (2014): R: a Language and Environment for Statistical Computing. R Foundation for Statistical ComputingVienna, Austria.

RasbandW. (2012): ImageJ. Version 1.47t. Available at http://imagej.nih.gov/ij/ (accessed 25 April 2013).

ReussT. (1927): Sechs europäische Giftschlangengattungen. Zool. Anz. 73: 124-129.

ScaliS.MangiacottiM.SacchiR.GentilliA. (2011): A tribute to Hubert Saint Girons: niche separation between Vipera aspis and V. berus on the basis of distribution models. Amphib.-Reptil. 32: 223-233.

StohlgrenT.J.MaP.KumarS.RoccaM.MorisetteJ.T.JarnevichC.S.BensonN. (2010): Ensemble habitat mapping of invasive plant species. Risk Anal. 30: 224-235.

SweetsJ.A. (1988): Measuring the accuracy of diagnostic systems. Science 240: 1285-1293.

ÚjváriB.MadsenT.KotenkoT.OlssonM.ShineR.WittzellH. (2002): Low genetic diversity threatens imminent extinction for the Hungarian meadow viper (Vipera ursinii rakosiensis). Biol. Conserv. 105: 127-130.

WilsonS.D. (1994): The contribution of grazing to plant diversity in alpine grassland and heath. Aust. J. Ecol. 19: 137-140.

WiszM.S.HijmansR.J.PetersonA.T.GrahamC.H.GuisanA. (2008): Effects of sample size on the performance of species distribution models. Divers. Distrib. 14: 763-773.

ZinenkoO.StümpelN.MazanaevaL.BakievA.ShiryaevK.PavlovA.KotenkoT.KukushkinO.ChikinY.DuisebayevaT.NilsonG.OrlovN.L.TuniyevS.AnanjevaN.B.MurphyR.W.JogerU. (2015): Mitochondrial phylogeny shows multiple independent ecological transitions and northern dispersion despite of Pleistocene glaciations in meadow and steppe vipers (Vipera ursinii and Vipera renardi). Mol. Phylogenet. Evol. 84: 85-100.

Figures

  • View in gallery

    Geographic area and presence points of Vipera ursinii graeca used in species distribution modelling. Grey shading indicates the area for model training, black outline indicates projection area. The distribution of V. u. macrops is also presented due to its proximity to the study taxon.

  • View in gallery

    The prediction of MaxEnt model for Vipera ursinii graeca throughout the range and in southern Albania (inset). Field surveys were conducted on all mountains shown. Filled acronyms indicate mountains where the subspecies was found, open letters indicate those where no evidence of presence was found. Abbreviations: Bureto (BU), Çika (CI), Dhëmbel (DH), Griba (GR), Kulmak (KU), Llofiz (LL), Lunxhërisë (LU), Nemerçkë (NE), Shendelli (SH), Tomorr (TO), Trebeshinë (TR).

  • View in gallery

    Median-joining haplotype network of Vipera ursinii graeca based on mitochondrial ND4 sequences. Numbers 222 and 384 indicate the relative positions of single nucleotide substitutions. See table 2.

Information

Content Metrics

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 29 29 9
Full Text Views 77 77 56
PDF Downloads 9 9 2
EPUB Downloads 0 0 0