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The relationships between land cover, climate and cave copepod spatial distribution and suitability along the Carpathians


The distribution of subterranean copepods may reflect the persistence of cave assemblages in relation to the environmental health of the overlying landscape. Areas supporting groundwater fauna were established by modelling the persistence of seven copepod species using a geographical information system (GIS). Environmental drivers were found to influence subterranean copepod distribution in the caves of the Romanian Carpathians. Habitat-based modelling, using ordinary least squares regression and geographically-weighted regression to identify the significant predictors explaining copepod habitat suitability, predicted suitable areas for the selected taxa. The most constant predictor was land cover, a measure of human impact and climate change, followed by precipitation and altitude. The model performed well for the majority of analysed taxa, and the areas predicted as suitable for narrowly distributed taxa overlapped with observed distributions. GIS facilitated the prediction of suitable habitat, and also enabled spatial autocorrelation to be tested. The results of this study demonstrate the importance of sustainable management of the terrestrial surface in limestone areas in conserving copepod biodiversity.

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*Correspondence: Dr Ioana Nicoleta Meleg e-mail:
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Akaike, H. (1974) A new look at the statistical model identification. IEEE Transactions on Automatic Control 19: 716723.
Bacaro, G., Santi, E., Rocchini, D., Pezzo, F., Puglisi, L. & Chiarucci, A. (2011) Geostatistical modelling of regional bird species richness: exploring environmental proxies for conservation purpose. Biodiversity and Conservation 20: 16771694.
Bio, A.M.F., De Becker, P., De Bie, E., Huybrechts, W. & Wassen, M. (2002) Prediction of plant species distribution in lowland river valleys in Belgium: modelling species response to site conditions. Biodiversity and Conservation 11: 21892216.
Bennett, G. (2002) Ecoregion-Based Conservation: The Carpathians: Final Reconnaissance Report. Vienna, Austria: WWF-International Danube–Carpathian Programme.
Boulton, A.J., Fenwick, G.D., Hancock, P.J. & Harvey, M.S. (2008) Biodiversity, functional roles and ecosystem services of groundwater invertebrates. Invertebrate Systematics 22: 103116.
Brotons, L., Mañosa, S. & Estrada, J. (2004) Modelling the effects of irrigation schemes on the distribution of steppe birds in Mediterranean farmland. Biodiversity and Conservation 13: 10391058.
Cardoso, P., Borges, P.A.V., Triantis, K.A., Ferrández, M.A. & Martín, H.L. (2010) Adapting the IUCN Red List criteria for invertebrates. Biological Conservation 144: 24322440.
Castany, G. (1982) Principes et méthodes de l'hydrogéologie. Paris, France: Dunod Université. Ed. Bordas.
Castellarini, F., Malard, F., Dole-Olivier, M.-J. & Gibert, J. (2007) Modelling the distribution of stygobionts in the Jura Mountains (eastern France). Implications for the protection of ground waters. Diversity and Distributions 13: 213224.
Costa, G.C., Wolfe, C., Shepard, D.B., Caldwell, J.P. & Vitt, L.J. (2008) Detecting the influence of climatic variables on species distributions: a test using GIS niche-based model along a steep longitudinal environmental gradient. Journal of Biogeography 35: 637646.
Damian-Georgescu, A. (1963) Copepoda. Fam. Cyclopidae (forme de apă dulce). Fauna Republicii Populare Romîne. Crustacea 4(6). Bucureşti, Romînia: Academia Republicii Populare Romînia.
Damian-Georgescu, A. (1970) Copepoda. Harpacticoida (forme de apă dulce). Fauna Republicii Populare Romîne. Crustacea 4(11). Bucureşti, Romînia: Academia Republicii Populare Romînia.
Danielopol, D.L., Artheau, M. & Marmonier, P. (2009) Site prioritisation for the protection of rare subterranean species: the cases of two ostracods from south-western France. Freshwater Biology 54: 877884.
Danielopol, D.L., Pospisil, P. & Rouch, R. (2000) Biodiversity in groundwater: a large-scale view. Trends in Ecology and Evolution 15: 223224.
Davin, E.L. & de Noblet-Ducoudré, N. (2010) Climatic Impact of Global-Scale Deforestation: Radiative versus Nonradiative Processes. Journal of Climate 23: 97112.
Deharveng, L., Stoch, F., Gibert, J., Bedos, A., Galassi, D., Zagmajster, M., Brancelj, A., Camacho, A., Fiers, F., Martin, P., Giani, N., Magniez, G. & Marmonier, P. (2009) Groundwater biodiversity in Europe. Freshwater Biology 54: 709726.
Di Lorenzo, T., Stoch, F., Fiasca, B., Gattone, E., De Laurentiis, P., Ranalli, F. & Galassi, D.M.P. (2005) Environmental quality of the groundwater in the Lessinian Massif (Italy): signposts for sustainability. In: Proceedings of an International Symposium on World Subterranean Biodiversity, ed. Gibert, J., pp. 115124. Villeurbanne, France: University of Lyon.
Dole-Olivier, M.-J., Marmonier, P., Creuzé des Châtelliers, M. & Martin, D. (1994) Interstitial fauna associated with the alluvial floodplains of the Rhône river (France). In: Groundwater Ecology, ed. Gibert, J., Danielopol, D.L. & Stanford, J.A., pp. 313346. San Diego, CA, USA: Academic Press.
Dussart, B. & Defaye, D. (2006) World Directory of Crustacea Copepoda of Inland Waters. II - Cyclopiformes. Leiden, the Netherlands: Backhuys Publishers.
Elith, J., Graham, C.H., Anderson, R.P., Dudik, M., Ferrier, S., Guisan, A., Hijmans, R.J., Huettmann, H., Leathwick, J.R., Lehmann, A., Li, J., Lohmann, L.G., Loiselle, B.A., Manion, G., Moritz, C., Nakamura, M., Nakazawa, Y., Overton, J.C., Peterson, A.T., Phillips, S.J., Richardson, K., Scachetti-Pereira, R., Schapire, R.E., Soberón, J., Williams, S., Wisz, M.S. & Zimmermann, N.E. (2006) Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29: 129151.
Elith, J., Phillips, S.J., Hastie, T., Dudik, M., Chee, Y.E. & Yates, C.J. (2011) A statistical explanation of MaxEnt for ecologists. Diversity and Distributions 17: 4357.
ESRI (2010) ArcGIS 9.3.1. Environmental Systems Research Institute, Inc., USA.
European Commission (2013) The Habitats Directive [www document]. URL
European Council (1980) Council Directive 80/68/EEC of 17 December 1979 on the protection of groundwater against pollution caused by certain dangerous substances as amended by Council Directive 91/692/EEC (further amended by Council Regulation 1882/2003/EC) [www document]. URL–19911223-en.pdf
European Council (2006) Directive 2006/118/EC of the European Parliament and of the Council of 12 December 2006 on the protection of groundwater against pollution and deterioration [www document]. URL
Fiers, F. & Moldovan, O.T. (2008) Redescription of Spelaeocamptus spelaeus (Chappuis 1925), a subterranean copepod endemic to the Apuseni Mountains in Romania (Copepoda Harpacticoida). Subterranean Biology 6: 5164.
Finch, J.M., Samways, M.J., Hill, T.R., Piper, S.E. & Taylor, S. (2006) Application of predictive distribution modelling to invertebrates: Odonata in South Africa. Biodiversity and Conservation 15: 42394251.
Fotheringham, A., Brunsdon, C. & Charlton, M. (2002) Geographically weighted regression: the analysis of spatially varying relationships. Chichester, England: John Wiley & Sons Ltd.
Galassi, D.M.P., Huys, R. & Reid, J. (2009). Diversity, ecology and evolution of groundwater copepods. Freshwater Biology 54: 691708.
Gibert, J., ed. (2005) World Subterranean Biodiversity. Proceedings of an International Symposium. Lyon, France: Université Claude Bernard.
Gibert, J. & Deharveng, L. (2002) Subterranean ecosystems: a truncated functional biodiversity. BioScience 52: 473481.
Gibert, J., Culver, D.C., Dole-Olivier, M.-J., Malard, F., Christman, M.C. & Deharveng, L. (2009) Assessing and conserving groundwater biodiversity: synthesis and perspectives. Freshwater Biology 54: 930941.
Goodchild, F.M. (1986) Spatial Autocorrelation. Norwich, UK: Geo Books: 57 pp.
Griebler, C., Stein, H., Kellermann, C., Berkhoff, S., Brielmann, H., Schmidt, S., Selesi, D., Steube, C., Fuchs, A & Hahn, H.J. (2010) Ecological assessment of groundwater ecosystems. Vision or illusion? Ecological Engineering 36: 11741190.
Guisan, A. & Thuiller, W. (2005) Predicting species distribution: offering more than simple habitat models. Ecology Letters 8: 9931009.
Hancock, P.J., Boulton, A.J. & Humphreys, W.F. (2005) Aquifers and hyporheic zones: towards an ecological understanding of groundwater. Hydrogeology Journal 13: 98111.
Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P.G. & Jarvis, A. (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25: 19651978 [www document]. URL
Iepure, S. & Defaye, D. (2008) The Acanthocyclops kieferi complex (Copepoda, Cyclopoida) from south-eastern Europe, with description of a new species. Crustaceana 81: 611630.
Kenneth, R.S., Strager, M.P. & Welsh, S.A. (2013) Advantages of geographically weighted regression for modeling benthic substrate in two Greater Yellowstone ecosystem streams. Environmental Modeling and Assessment 18: 209219.
Kopp, D., Santoul, F., Poulet, N., Compin, A. & Céréghino, R. (2010) Patterning the distribution of threatened crayfish and their exotic analogues using self-organizing maps. Environmental Conservation 37: 147154.
Lefébure, T., Douady, C.J., Gouy, M., Trontelj, P., Briolay, J. & Gibert, J. (2006) Phylogeography of a subterranean amphipod reveals cryptic diversity and dynamic evolution in extreme environments. Molecular Ecology 15: 17971806.
Linkie, M., Chapron, G., Martyr, D.J., Holden, J. & Leader-Williams, N. (2006) Assessing the viability of tiger subpopulations in a fragmented landscape. Journal of Applied Ecology 43: 576586.
Malard, F., Reygrobellet, J.-L. & Laurent, R. (1998) Spatial distribution of epigean invertebrates in an alluvial aquifer polluted by iron and manganese, Rhône River, France. Verhandlungen der Internationalen Vereinigung für Limnologie 26: 15901594.
Malard, F., Reygrobellet, J.-L., Mathieu, J. & Lafont, M. (1994) The use of invertebrate communities to describe groundwater flow and contaminant transport in a fractured rock aquifer. Archiv für Hydrobiologie 131: 93110.
Martínez-Freiría, F., Sillero, N., Lizana, M. & Brito, J.C. (2008) GIS-based niche models identify environmental correlates sustaining a contact zone between three species of European vipers. Diversity and Distributions 14: 452461.
Meleg, I.N., Moldovan, O.T., Iepure, S., Fiers, F. & Brad, T. (2011) Diversity patterns of fauna in dripping water of caves from Transylvania. Annales de Limnologie - International Journal of Limnology 47: 185197.
Meleg, I.N., Fiers, F., Robu, M. & Moldovan, O.T. (2012) Distribution patterns pf subsurface copepods and the impact of environmental parameters. Limnologica 42: 156164.
Mitchell, A. (2005) The ESRI guide to GIS analysis: spatial measurements and statistics. Redlands, CA, USA: ESRI Press.
Moldovan, O.T., Iepure, S. & Perşoiu, A. (2005) Biodiversity and protection of Romanian karst areas: the example of interstitial fauna. In: Water Resources and Environmental Problems in Karst. Proceedings International Conference and Field Seminary, ed. Stevanoviæ, Z. & Milanoviæ, P., pp. 831836. Belgrade, Serbia & Montenegro: Belgrade & Kotor.
Moldovan, O.T., Pipan, T., Iepure, S., Mihevc, A. & Mulec, J. (2007) Biodiversity and ecology of fauna in percolating water in selected Slovenian and Romanian caves. Acta Carsologica 36: 493501.
Moldovan, O.T., Levei, E., Banciu, M., Banciu, H.L., Marin, C., Pavelescu, C., Brad, T., Cîmpean, M., Meleg, I., Iepure, S. & Povară, I. (2011) Spatial distribution patterns of the hyporheic invertebrate communities in a polluted river in Romania. Hydrobiologia 669: 6382.
Moldovan, O.T., Meleg, I.N. & Perşoiu, A. (2012) Habitat fragmentation and its effects on groundwater populations. Ecohydrology 5: 445452.
Moldova, O.T., Meleg, I.N., Levei, E. & Terente, M. (2013) A simple method for assessing biotic indicators and predicting biodiversity in the hyporheic zone of a river polluted with metals. Ecological Indicators 24: 412420.
Mösslacher, F. & Notenboom, J. (1999) Groundwater biomonitoring. In: Biomonitoring of Polluted Water, ed. Gerhardt, A., pp. 119140. Zürich, Switzerland: Trans Tech Publications.
Năpăruş, M. & Kuntner, M. (2012) A GIS model predicting global distributions of a lineage: a test case on hermit spiders (Nephilidae: Nephilengys). PLoS ONE 7: e30047. doi:10.1371 /journal.pone.0030047
Neilson, R.P. (1995) A model for predicting continental-scale vegetation distribution and water balance. Ecological Applications 5: 362385.
Osborne, P.E., Foody, G.M. & Suárez-Seoane, S. (2007) Non-stationarity and local approaches to modeling the distributions of wildlife. Diversity and Distributions 13: 313323.
Paran, F., Malard, F., Mathieu, J., Lafont, M., Galassi, D.M.P. & Marmonier, P. (2005) Distribution of groundwater invertebrates along an environmental gradient in a shallow water-table aquifer. In: World Subterranean Biodiversity, Proceedings of an International Symposium, ed. Gibert, J., pp. 99105. Lyon, France: Université Claude Bernard.
Pipan, T., Blejec, A. & Brancelj, A. (2006) Multivariate analysis of copepod assemblages in epikarstic waters of some Slovenian caves. Hydrobiologia 559: 213223.
Rodríguez, J.P., Brotons, L., Bustamante, J. & Seoane, J. (2007) The application of predictive modelling of species distribution to biodiversity conservation. Diversity and Distributions 13: 243251.
Schmidt, S.I. & Hahn, H.S. (2012) What is groundwater and what does this mean to fauna? An opinion. Limnologica 42: 16.
Schmitt, T. & Rákosy, L. (2007) Changes of traditional agrarian landscapes and their conservation implications: a case study of butterflies in Romania. Diversity and Distributions 13: 855862.
Segurado, P. & Araújo, M. (2004) An evaluation of methods for modelling species distributions. Journal of Biogeography 31: 15551568.
Simpson, M. & Prots, B. (2013) Predicting the distribution of invasive plants in the Ukrainian Carpathians under climatic change and intensification of anthropogenic disturbances: implications for biodiversity conservation. Environmental Conservation 40: 167181.
Stein, H., Kellermann, C., Schmidt, S.I., Brielmann, H., Steube, C., Berkhoff, S.E., Fuchs, A., Hahn, H.J., Thulin, B. & Griebler, C. (2010) The potential use of fauna and bacteria as ecological indicators for the assessment of groundwater quality. Journal of Environmental Monitoring 12: 242254.
Stoch, F. & Galassi, D.M.P. (2010) Stygobiotic crustacean species richness: a question of numbers, a matter of scale. Hydrobiologia 653: 217234.
United Nations Environment Programme (2007) Carpathians Environment Outlook. Bielsko-Biala, Poland: Dimograf Printing House.
Vandewalle, M., de Bello, F., Berg, M.P., Bolger, T., Dolédec, S., Duds, F., Feld, C.K., Harrington, R., Harrison, P.A., Lavorel, S., da Silva, P.M., Moretti, M., Niemelä, J., Santos, P., Sattler, T., Sousa, J.P., Sykes, M.T., Vanbergen, A.J. & Woodcock, B.A. (2010) Functional traits as indicators of biodiversity response to land use changes across ecosystems and organisms. Biodiversity and Conservation 19: 29212947.
Wells, J.B.J. (2007) An annotated checklist and keys to the species of Copepoda Harpacticoida (Crustacea). Zootaxa 1568: 1872.
Williams, P.W. (2004) The epikarst: evolution of understanding. In: Proceedings of the Symposium on Epikarst, ed. Jones, W.K., Culver, D.C. & Herman, J.S., pp. 815. Charles Town, WV, USA: Karst Waters Institute Special Publication 9.
Whittaker, R.H., Araújo, M.B., Jepson, P., Ladle, R.J., Watson, J.E.M. & Willis, K.J. (2005) Conservation Biogeography: assessment and prospect. Diversity and Distributions 11: 323.
Yates, C.J., Elith, J., Latimer, A.M., Le Maitre, D., Midgley, G.F., Schurr, F.M. & West, A.G. (2010) Projecting climate change impacts on species distributions in megadiverse South African Cape and Southwest Australian Floristic Regions: opportunities and challenges. Austral Ecology 35: 374391.
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