A study of climate niche modeling of the Eurasian Nuthatch (Sitta europaea) in theAlborz and Zagros mountains

Document Type : Research Paper


1 Department of Environmental Science - Faculty of Natural Resources - University of Tehran

2 Department of Environmental Science - Faculty of Natural Resources - University of tehran

3 CEFE UMR 5175, CNRS-EPHE, Laboratoire Biogéographie et écologie des vertèbres, 1919 route de Mende, 34293 Montpellier cedex 5, Montpellier, France

4 Department of Environment of Iran, Isfahan province

5 University of Tehran


Two opposing questions concerning differences among ecological niches of closely-related taxa in similar or adjacent habitats have long been a subject of debate. Did different populations of a species inhabit different ecological niches and undergo speciation due to the interruption of gene flow, or did speciation occur earlier, which later on caused closely-related taxa to inhabit similar habitats? In this study, we investigated the differences between the ecological niche climate of two subspecies of the Eurasian nuthatch (rubiginosa and persica), and the impact such differences had on speciation of these subspecies over different time scales, from the past to the present. To do so, we performed tests of niche equivalency and modeled niche similarities in geographical and environmental spaces of the Alborz and Zagros Mountains. Results revealed that the ecological niche climate overlap between clades of the Alborz and Zagros is insignificant, and tests of niche similarity and niche equivalency between the two subspecies of these mountain ranges were significant. Thus, niche conservatism could be inferred for these subspecies, highlighting the speciation of each subspecies in geographically allopatric regions, prior to their migration to the Alborz and Zagros Mountains. Our results suggest that each population of the Eurasian nuthatch in these ranges could be regarded as an evolutionary significant unit, and each subspecies requires proper conservation management.


Akhani, H., Djamali, M., Ghorbanalizadeh, A., and Ramezani, E. 2010. Plant biodiversity of Hyrcanian relict forests, N Iran: an overview of the flora, vegetation, palaeoecology and conservation. Pakistan Journal of Botany, 42(Special Issue), 231-258.‏
Alai-Taleghani, M. 2015. Geomorphology of Iran, Tehran: Publication Ghomes, 155 pp.
Araújo, M.B., and Peterson, A.T. 2012. Uses and misuses of bioclimatic envelope modeling. Ecology, 93(7), 1527-1539.‏
Arif, I.A., and Khan, H.A. 2009. Molecular markers for biodiversity analysis of wildlife animals: a brief review. Animal Biodiversity and Conservation, 32(1), 9-17.‏
Arteaga, M.C., McCormack, J.E., Eguiarte, L.E., and Medellín, R.A. 2011. Genetic admixture in multidimensional environmental space: asymmetrical niche similarity promotes gene flow in armadillos (Dasypus novemcinctus). Evolution, 65(9), 2470-2480.‏
Ashrafzadeh, M.R., Kaboli, M., and Naghavi, M.R. 2016. Mitochondrial DNA analysis of Iranian brown bears (Ursus arctos) reveals new phylogeographic lineage. Mammalian Biology-Zeitschrift für Säugetierkunde, 81(1), 1-9.‏
Baguette, M., Freville, H., Legrand, D., Ducatez, S. 2012. Dispersal Ecology and Evolution, Chapter: 30, pp.381-391.
Benítez‐Benítez, C., Escudero, M., Rodríguez‐Sánchez, F., Martín‐Bravo, S. and Jiménez‐Mejías, P., 2018. Pliocene‐Pleistocene ecological niche evolution shapes the phylogeography of a Mediterranean plant group. Molecular ecology, 27(7), 1696-1713.
Bianconi, M., Ferraro, L., Traina, G.C., Zanoli, G., Antonelli, T., Guberti, A., Ricci, R., and Massari, L. 2003. Pharmacokinetics and efficacy of ropivacaine continuous wound instillation after joint replacement surgery. British Journal of Anaesthesia, 91(6), 830-835.‏
Bianconi, R., Battisti, C., and Zapparoli, M. 2003. Pattern of richness, abundance and diversity of four interior bird species in a hilly landscape in Central Italy: a contribution to assess their sensitivity to habitat fragmentation. Journal of Mediterranean Ecology, 4, 37-44.‏
Blair, M.E., Sterling, E.J., Dusch, M., Raxworthy, C.J., and Pearson, R.G. 2013. Ecological divergence and speciation between lemur (Eulemur) sister species in Madagascar. Journal of evolutionary biology, 26(8), 1790-1801.‏
Broennimann, O., Fitzpatrick, M.C., Pearman, P.B., Petitpierre, B., Pellissier, L., Yoccoz, N. G., Zimmermann, N. E.,  and Graham, C. H. 2012. Measuring ecological niche overlap from occurrence and spatial environmental data. Global ecology and biogeography, 21(4), 481-497.‏
Brown, J.L. 2014. SDMtoolbox: a python‐based GIS toolkit for landscape genetic, biogeographic and species distribution model analyses. Methods in Ecology and Evolution, 5(7), 694-700.‏
Buermann, W., Saatchi, S., Smith, T.B., Zutta, B. R., Chaves, J.A., Milá, B., and Graham, C.H. 2008. Predicting species distributions across the Amazonian and Andean regions using remote sensing data. Journal of Biogeography, 35(7), 1160-1176.‏
Burbrink, F.T. 2002. Phylogeographic analysis of the cornsnake (Elaphe guttata) complex as inferred from maximum likelihood and Bayesian analyses. Molecular Phylogenetics and Evolution, 25(3), 465-476.‏
Carnaval, A.C., Hickerson, M.J., Haddad, C.F., Rodrigues, M.T., and Moritz, C. 2009. Stability predicts genetic diversity in the Brazilian Atlantic forest hotspot. Science, 323(5915), 785-789.‏
Clements, J. F., Schulenberg, T.S., Iliff, M.J., Sullivan, B. L., Wood, C. L., and Roberson, D. 2014. The eBird/Clements checklist of birds of the world: Version 6.9. Avaliable: http://www.birds.cornell. edu/clementschecklist/download.
Coyne, J.A., and Orr, H.A. 2004. Speciation. Sinauer. Sunderland, MA.‏
Darvish, J., Mohammadi, Z., Mahmoudi, A., and Siahsarvie, R. 2015. Faunistic and taxonomic study of Rodents from northwestern Iran. Iranian Journal of Animal Biosystematics, 10(2), 119-136.‏
Guisan, A. and Thuiller, W. 2005. Predicting species distribution: offering more than simple habitat models. Ecology letters, 8(9), 993-1009.‏
Holt, R.D. 2009. Bringing the Hutchinsonian niche into the 21st century: ecological and evolutionary perspectives. Proceedings of the National Academy of Sciences, 106 (Supplement 2), 19659-19665.‏
Hung, C.M., Drovetski, S.V., and Zink, R.M. 2012. Multilocus coalescence analyses support a mtDNA-based phylogeographic history for a widespread Palearctic Passerinr bird, Sitta europaea. Evolution, 66(9), 2850-2864.‏
Hutchinson, G.E. 1957. Cold spring harbor symposium on quantitative biology. Concluding remarks, 22, 415-427.‏
Jiménez Valverde, A. 2012. Insights into the area under the receiver operating characteristic curve (AUC) as a discrimination measure in species distribution modelling. Global Ecology and Biogeography, 21(4), 498-507.‏
Kaboli, M., Aliabadian, M., Tohidifar, M., and Hashemi, A. 2012. Atlas of birds of Iran. Department of Environment Islamic Republic of Iran, 628.
Khosroshahi, F. B., Shabani, A. A., Kaboli, M., Karami, M., Najafabadi, M. S., and Ahmadi-Mamaqani, Y. 2011. A probabilistic model for presence of Eurasian Nuthatch (Sitta europaea) in the Alborz mountains, northern Iran. The Wilson Journal of Ornithology, 123(4), 741-747.‏
Knouft, J.H., Losos, J.B., Glor, R.E., and Kolbe, J.J. 2006. Phylogenetic analysis of the evolution of the niche in lizards of the Anolis sagrei group. Ecology, 87, 29–38.
Kozak, K.H., Graham, C.H., and Wiens, J.J. 2008. Integrating GIS-based environmental data into evolutionary biology. Trends in ecology and evolution, 23(3), 141-148.‏
Levins, R. 1968. Evolution in changing environments: some theoretical explorations. Princeton University Press, Princeton, New Jersey, 132 pp.
Makowsky, R., Marshall Jr,J.C., McVay, J., Chippindale, P.T., and Rissler, L.J. 2010. Phylogeographic analysis and environmental niche modeling of the plain-bellied watersnake (Nerodia erythrogaster) reveals low levels of genetic and ecological differentiation. Molecular phylogenetics and evolution, 55(3), 985-995.‏
Matthysen, E., Adriaensen, F., and Dhondt, A.A. 1995. Dispersal distances of nuthatches, Sitta europaea, in a highly fragmented forest habitat. Oikos, 72, 375-381.‏
Matthysen, E., and Currie, D. 1996. Habitat fragmentation reduces disperser success in juvenile nuthatches Sitta europaea: evidence from patterns of territory establishment. Ecography, 19(1), 67-72.‏
Mayr, E., and Provine, W.B. 1998. The evolutionary synthesis: perspectives on the unification of biology. Harvard University Press, Massachusetts, 487 pp.‏
McCormack, J.E., Zellmer, A.J., and Knowles, L.L. 2010. Does niche divergence accompany allopatric divergence in Aphelocoma jays as predicted under ecological speciation? insights from tests with niche models. Evolution, 64(5), 1231-1244.‏
Mortelliti, A., Fagiani, S., Battisti, C., Capizzi, D., and Boitani, L. 2010. Independent effects of habitat loss, habitat fragmentation and structural connectivity on forest dependent birds. Diversity and Distributions, 16(6), 941-951.‏
Naderi, G., Kaboli, M., Koren, T., Karami, M., Zupan, S., Rezaei, H.R., and Krystufek, B. 2014. Mitochondrial evidence uncovers a refugium for the fat dormouse (Glis glis Linnaeus, 1766) in Hyrcanian forests of northern Iran. Mammalian Biology-Zeitschrift für Säugetierkunde, 79(3), 202-207.‏
Nazarizadeh, M., Kaboli, M., Rezaie, H.R., Harisini, J.I., and Pasquet, E. 2016. Phylogenetic relationships of Eurasian Nuthatches (Sitta europaea Linnaeus, 1758) from the Alborz and Zagros Mountains, Iran. Zoology in the Middle East, 62(3), 217–226.
Pearman, P.B., Guisan, A., Broennimann, O., and Randin, C.F. 2008. Niche dynamics in space and time. Trends in Ecology and Evolution, 23(3), 149-158.‏
Peterson, A.T., Soberón, J., and Sánchez-Cordero, V. 1999. Conservatism of ecological niches in evolutionary time. Science, 285(5431), 1265-1267.‏
Philips, Z., Ginnelly, L., Sculpher, M., Claxton, K., Golder, S., Riemsma, R., Glanville, J. 2004. Review of guidelines for good practice in decision-analytic modeling in health technology assessment, 8(36), 1-158.
Phillips, S.J., Anderson, R.P., and Schapire, R.E. 2006. Maximum entropy modeling of species geographic distributions. Ecological modeling, 190(3-4), 231-259.‏
Pianka, E. 1975. Niche relations of desert lizards. Ecology and evolution of communities, 292-314.‏
Pravosudov, V.V. 1993. Social organization of the Nuthatch Sitta europaea asiatica. Ornis Scandinavica, 44 (24), 290-296.‏
Price, T. 2008. Speciation in Birds. Roberts, Boulder, CO, USA.
R Development Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, 2011. Available in: <http://www.r-project.org>. Access in: 31 Jan. 2011.
Raxworthy, C.J., Ingram, C.M., Rabibisoa, N. and Pearson, R.G. 2007. Applications of ecological niche modeling for species delimitation: a review and empirical evaluation using day geckos (Phelsuma) from Madagascar. Systematic Biology, 56(6), 907-923.
Rissler, L.J. and Apodaca, J.J. 2007. Adding more ecology into species delimitation: ecological niche models and phylogeography help define cryptic species in the black salamander (Aneides flavipunctatus). Systematic Biology, 56(6), 924-942.
Rödder, D. and Lötters, S. 2009. Niche shift versus niche conservatism? Climatic characteristics of the native and invasive ranges of the Mediterranean house gecko (Hemidactylus turcicus). Global Ecology and Biogeography, 18(6), 674–687.
Schluter, D. 2009. Evidence for ecological speciation and its alternative. Science, 323(5915),737–741.
Schoener, T.W. 1968. The Anolis lizards of Bimini: resource partitioning in a complex fauna. Ecology, 49(4), 704–726.
Soberón, J. 2007. Grinnellian and Eltonian niches and geographic distributions of species. Ecology letters, 10(12), 1115-1123.‏
Soberon, J. and Nakamura, M. 2009. Niches and distributional areas: concepts, methods, and assumptions. Proceedings of the National Academy of Sciences, 106(Supplement 2), 19644-19650.
Thorpe, R.S., Surget-Groba, Y. and Johansson, H. 2008. The relative importance of ecology and geographic isolation for speciation in anoles. Philosophical Transactions of the Royal Society B: Biological Sciences, 363(1506), 3071-3081.
Thorpe, R.S., Surget-Groba, Y. and Johansson, H., 2008. The relative importance of ecology and geographic isolation for speciation in anoles. Philosophical Transactions of the Royal Society B: Biological Sciences, 363(1506), pp.3071-3081.
Waltari, E., Hijmans, R. J., Peterson, A. T., Nyári, Á. S., Perkins, S. L., and Guralnick, R. P. 2007. Locating Pleistocene refugia: comparing phylogeographic and ecological niche model predictions. PLoS one, 2(7), e563.‏
Wang, Z. L., Zhang, D. Y., and Wang, G. 2005. Does spatial structure facilitate coexistence of identical competitors?. Ecological Modelling, 181(1), 17-23.
Warren, D. L., Glor, R. E., and Turelli, M. 2008. Environmental niche equivalency versus conservatism: quantitative approaches to niche evolution. Evolution, 62(11), 2868-2883.
Wiens, J. J., and Graham, C. H. 2005. Niche conservatism: integrating evolution, ecology, and conservation biology. Annual Review of Ecology, Evolution, and Systematics, 36, 519-539.
Wooten, J. A., and Gibbs, H. L. 2012. Niche divergence and lineage diversification among closely related Sistrurus rattlesnakes. Journal of evolutionary biology, 25(2), 317-328.‏
Zink, R. M. 2014. Homage to Hutchinson, and the role of ecology in lineage divergence and speciation. Journal of biogeography, 41(5), 999-1006.
Zink, R. M., Drovetski, S. V., and Rohwer, S. 2006. Selective neutrality of mitochondrial ND2 sequences, phylogeography and species limits in Sitta europaea. Molecular phylogenetics and evolution, 40(3), 679-686.
Zuckerberg, B., Carling, M., Dor, R., Ferree, E., Spellman, G., and Townsend, A. 2014. Differential relationships between habitat fragmentation and within-population genetic diversity of three forest-dwelling birds. bioRxiv, 004903.‏