Abstract
According to ecological theory, the coexistence of competitors in patchy environments may be facilitated by hierarchical spatial segregation along axes of environmental variation, but empirical evidence is limited. Cabrera and water voles show a metapopulation-like structure in Mediterranean farmland, where they are known to segregate along space, habitat, and time axes within habitat patches. Here, we assess whether segregation also occurs among and within landscapes, and how this is influenced by patch-network and matrix composition. We surveyed 75 landscapes, each covering 78 ha, where we mapped all habitat patches potentially suitable for Cabrera and water voles, and the area effectively occupied by each species (extent of occupancy). The relatively large water vole tended to be the sole occupant of landscapes with high habitat amount but relatively low patch density (i.e., with a few large patches), and with a predominantly agricultural matrix, whereas landscapes with high patch density (i.e., many small patches) and low agricultural cover, tended to be occupied exclusively by the small Cabrera vole. The two species tended to co-occur in landscapes with intermediate patch-network and matrix characteristics, though their extents of occurrence were negatively correlated after controlling for environmental effects. In combination with our previous studies on the Cabrera-water vole system, these findings illustrated empirically the occurrence of hierarchical spatial segregation, ranging from within-patches to among-landscapes. Overall, our study suggests that recognizing the hierarchical nature of spatial segregation patterns and their major environmental drivers should enhance our understanding of species coexistence in patchy environments.
Similar content being viewed by others
References
Amarasekare P (2003) Competitive coexistence in spatially structured environments: a synthesis. Ecol Lett 6:1109–1122
Amarasekare P, Nisbet R (2001) Spatial heterogeneity, source-sink dynamics and the local coexistence of competing species. Am Nat 158:572–584
Barbosa S, Pauperio J, Searle JB, Alves PC (2013) Genetic identification of Iberian rodent species using both mitochondrial and nuclear loci: application to noninvasive sampling. Mol Ecol Resour 13:43–56
Barr DJ, Levy R, Scheepers C, Tily HJ (2013) Random effects structure for confirmatory hypothesis testing: keep it maximal. J Mem Lang 68:255–278
Barton K (2014) Package ‘MuMIn’. Model selection and model averaging based on information criteria. R package version 1.10.5 Available at: http://cran.r-project.org/web/packages/MuMIn/MuMIn.pdf
Basset A (1995) Body size-related coexistence: an approach through allometric constraints on home-range use. Ecology 76:1027–1035
Basset A, De Angelis DL (2007) Body size mediated coexistence of consumers competing for resource in space. Oikos 116:1363–1377
Beja P, Schindler S, Santana J, Porto M, Morgado R, Moreira F, Pita R, Mira A, Reino L (2014) Predators and livestock reduce bird nest survival in intensive Mediterranean farmland. Eur J Wildl Res 60:249–258
Bennett AF, Radford JQ, Haslem A (2006) Properties of land mosaics: implications for nature conservation in agricultural environments. Biol Conserv 133:250–264
Biswas SR, Wagner HH (2012) Landscape contrast: a solution to hidden assumptions in the metacommunity concept? Landscape Ecol 27:621–631
Boeye J, Kubisch A, Bonte D (2014) Habitat structure mediates spatial segregation and therefore coexistence. Landscape Ecol 29:593–604
Brunner JL, Duerr S, Keesing F, Killilea M, Vuong H, Ostfeld RS (2013) An experimental test of competition among mice, chipmunks, and squirrels in deciduous forest fragments. PLoS One 8:e66798
Centeno-Cuadros A, Román J, Delibes M, Godoy JA (2011) Prisoners in their habitat? Generalist dispersal by habitat specialists: a case study in southern water vole (Arvicola sapidus). PLoS One 6:e24613
Chase JM, Liebold MA (2003) Ecological niches: linking classical and contemporary approaches. University of Chicago Press, Chicago
Chesson P (2000) General theory of competitive coexistence in spatially-varying environments. Theor Popul Biol 58:211–237
Durant SM (1998) Competition refuges and coexistence: and example from Serengeti carnivores. J Anim Ecol 67:370–386
Fedriani JM, Delibes M, Ferreras P, Román J (2002) Local and landscape habitat determinants of water vole distribution in a patchy Mediterranean environment. Ecoscience 9:12–19
Fernández N, Román J, Delibes M (2016) Variability in primary productivity determines metapopulation dynamics. P R Soc B Biol Sci 283:20152998
Garrido-García JA, Soriguer RC (2014) Topillo de Cabrera Iberomys cabrerae (Thomas, 1906) In: Calzada J, Clavero M, Fernández A (eds) Guía virtual de los indicios de los mamíferos de la Península Ibérica, Islas Baleares y Canarias. Sociedad Española para la Conservación y Estudio de los Mamíferos (SECEM). http://www.secem.es/guiadeindiciosmamiferos/
Gelman A (2006) Prior distributions for variance parameters in hierarchical models. Bayesian Anal 1:515–533
Gilbert B, Srivastava DS, Kirby KR (2008) Niche partitioning at multiple scales facilitates coexistence among mosquito larvae. Oikos 117:944–950
Gillies CS, Hebblewhite M, Nielsen SE, Krawchuk MA, Aldridge CL, Frair JL, Saher DJ, Stevens CE, Jerde CL (2006) Application of random effects to the study of resource selection by animals. J Anim Ecol 75:887–898
Ginger SM, Hellgren EC, Kasparian MA, Levesque LP, Engle DM, Leslie DM Jr (2003) Niche shift by Virgina opossum following reduction of a putative competitor, the raccoon. J Mammal 84:1279–1291
Guillaumet A, Leotard G (2015) Annoying neighbors: multi-scale distribution determinants of two sympatric sibling species of birds. Curr Zool 61:10–22
Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw 33:1–22
Hadfield JD (2012) MCMCglmm Course Notes. Available online at: http://cran.r-project.org/web/packages/MCMCglmm/vignettes/CourseNotes.pdf
Hanski I (1983) Coexistence of competitors in patchy environments. Ecology 64:493–500
Hanski I (2008) Spatial patterns of coexistence of competing species in patchy habitat. Theor Ecol 1:29–43
Hanski I, Ranta E (1983) Coexistence in a patchy environment: three species of Daphnia in rock pools. J Anim Ecol 52:263–280
Holt RD (2001) Species coexistence. Encycl Biodiv 5:413–426
Inouye BD (1999) Integrating nested spatial scales: implications for the coexistence of competitors on a patchy resource. J Anim Ecol 68:150–162
Johnson PCD (2014) Extension of Nakagawa & Schielzeth’s \(R_{{_{\text{GLMM}} }}^{ 2}\) to random slopes models. Method Ecol Evol 5: 44–946
Jorgenson EE (2004) Small mammal use of microhabitat reviewed. J. Mamm 85:531–539
Kleinbaum DG, Kupper LL, Muller KE, Nizam A (1998) Applied regression analysis and other multivariate models. Duxbury Press, California
Kneitel JM (2012) Are trade-offs among species’ ecological interactions scale dependent? A test using pitcher-plant inquiline species. PLoS One 7:e41809
Kneitel JM, Chase JM (2004) Trade-offs in community ecology: linking spatial scales and species coexistence. Ecol Lett 7:69–80
Laporta GZ, Sallum AAM (2014) Coexistence mechanisms at multiple scales in mosquito assemblages. BMC Ecol 14:30
László Z, Tóthmérész B (2013) Landscape and local effects on multiparasitoid coexistence. Insect Cons Divers 6:354–364
Leibold MA, McPeek MA (2006) Coexistence of the niche and neutral perspectives in community ecology. Ecology 87:1399–1410
MacKenzie DI, Royle JA (2005) Designing efficient occupancy studies: general advice and allocating survey effort. J Appl Ecol 42:1105–1114
Morris DW (1987) Ecological scale of habitat use. Ecology 68:362–369
Nowakowski AJ, Hyslop NL, Watling JI, Donnelly MA (2013) Matrix type alters structure of aquatic vertebrate assemblages in cypress domes. Biodivers Conserv 22:497–511
Oliver M, Luque-Larena JJ, Lambin X (2009) Do rabbits eat voles? Apparent competition, habitat heterogeneity and large-scale coexistence under mink predation. Ecol Lett 12:1201–1209
Palomo LJ, Gisbert J, Blanco JC (2007) Atlas y Libro Rojo de los Mamíferos Terrestres de España. Dirección General de Conservación de la, Naturaleza-SECEM-SECEMU
Peralta D, Leitão I, Ferreira A, Mira A, Beja P, Pita R (2016) Factors affecting southern water vole (Arvicolas sapidus) detection and occupancy probabilities in Mediterranean farmland. Mamm Biol 81:123–129
Pita R, Beja P, Mira A (2007) Spatial population structure of the Cabrera vole in Mediterranean farmland: the relative role of patch and matrix effects. Biol Conserv 134:383–392
Pita R, Mira A, Moreira F, Morgado R, Beja P (2009) Influence of landscape characteristics on carnivore diversity and abundance in Mediterranean farmland. Agric Ecosyst Environ 132:57–65
Pita R, Mira A, Beja P (2010) Spatial segregation of two vole species (Arvicola sapidus and Microtus cabrerae) within habitat patches in a highly fragmented farmland landscape. Eur J Wildlife Res 56:651–662
Pita R, Mira A, Beja P (2011a) Assessing habitat differentiation between coexisting species: the role of spatial scale. Acta Oecol 37:124–132
Pita R, Mira A, Beja P (2011b) Circadian activity rhythms in relation to season, sex, and interspecific interactions in two Mediterranean voles. Anim Behav 81:1023–1030
Pita R, Mira A, Beja P (2013) Influence of land mosaic composition and structure on patchy populations: the case of the water vole (Arvicola sapidus) in Mediterranean farmland. PLoS One 8(7):e69976
Plummer M, Best N, Cowles K, Vines K (2006) CODA: convergence diagnosis and output analysis for MCMC. R News 6:7–11
Pocock MJO, White PVL, McClean CJ, Searle JB (2003) The use of accessibility in defining sub-groups of small mammals from point sampled data. Comput Environ Urban syst 27:71–83
Poiani KA, Richter BD, Anderson MG, Richter HE (2000) Biodiversity conservation at multiple scales: functional sites, landscapes, and networks. Bioscience 50:133–146
R Development Core Team. (2014) R: a language and environment for statistical computing, 3.0.2. R Foundation for Statistical Computing, Vienna, Austria
Richter-Boix A, Llorente GA, Montori A (2007) Structure and dynamics of an amphibian metacommunity in two regions. J Anim Ecol 76:607–618
Román J (2007) Historia natural de la rata de agua (Arvicola sapidus) en Doñana. PhD dissertation, Facultad de Ciencias, Universidad Autonoma de Madrid
Román J (2014) Rata de agua Arvicola sapidus Miller, 1908. In: Calzada J, Clavero M, Fernández A. (eds). Guía virtual de los indicios de los mamíferos de la Península Ibérica, Islas Baleares y Canarias. Sociedad Española para la Conservación y Estudio de los Mamíferos (SECEM). http://www.secem.es/guiadeindiciosmamiferos/
Rosário IT, Cardoso PE, Mathias ML (2008) Is habitat selection by the Cabrera vole (Microtus cabrerae) related to food preferences? Mamm Biol 73:423–429
Schippers P, Hemerik L, Baveco JM, Verboom J (2015) Rapid diversity loss of competing animal species in well-connected landscapes. PLoS One 10(7):e0132383
Schmidt MH, Thies C, Nentwig W, Tscharntke T (2008) Contrasting responses of arable spiders to the landscape matrix at different spatial scales. J Biogeogr 35:157–166
Soriguer RC, Amat JA (1988) Feeding of Cabrera vole in west-central Spain. Acta Theriol 33:589–593
Sutherland CS, Elston DA, Lambin X (2014) A demographic, spatially explicit patch occupancy model of metapopulation dynamics and persistence. Ecology 95:3149–3160
Swihart RK, Atwood TC, Goheen JR, Scheiman DM, Munroe KE, Gehring TM (2003) Patch occupancy of North American mammals: is patchiness in the eye of the beholder? J Biogeogr 30:1259–1279
Szabó P, Meszéna G (2006) Spatial ecological hierarchies: coexistence on heterogeneous landscapes via scale niche diversification. Ecosystems 9:1009–1016
Telfer S, Piertney SB, Dallas JF, Stewart WA, Marshall F, Gow JL, Lambin X (2003) Parentage assignment detects frequent and large-scale dispersal in water voles. Mol Ecol 12:1939–1949
Tscharntke T, Tylianakis JM, Rand TA, Didham RK, Fahrig L, Batáry P, Bengtsson J, Clough Y, Crist TO, Dormann CF, Ewers RM, Fründ J, Holt RD, Holzschuh A, Klein AM, Kleijn D, Kremen C, Landis DA, Laurance W, Lindenmayer D, Scherber C, Sodhi N, Steffan-Dewenter I, Thies C, van der Putten WH, Westphal C (2012) Landscape moderation of biodiversity patterns and processes—eight hypotheses. Biol Rev 87:661–685
Valladares F, Bastias CC, Godoy O, Granda E, Escudero A (2015) Species coexistence in a changing world. Front Plant Sci 6:866
Westphal C, Steffan-Dewenter I, Tscharntke T (2006) Bumblebees experience landscapes at different spatial scales: possible implications for coexistence. Oecologia 149:289–300
Whittaker RJ, Willis KJ, Field R (2001) Scale and species richness: towards a general, hierarchical theory of species diversity. J Biogeogr 28:453–470
Wilson AJ, Réale D, Clements MN, Morrissey MM, Postma E, Walling CA, Kruuk LEB, Nussey DH (2010) An ecologist’s guide to the animal model. J Anim Ecol 79:13–26
Yu DW, Wilson HB, Pierce NE (2001) An empirical model of species coexistence in a spatially structured environment. Ecology 82:1761–1771
Zuur AF, Leno EN, Elphic CS (2010) A protocol for data exploration to avoid common statistical problems. Method Ecol Evol 1:3–14
Acknowledgments
This study was financed by FEDER funds through the Programa Operacional Factores de Competitividade—COMPETE, and National funds through the Portuguese Foundation for Science and Technology—FCT, within the scope of the projects PERSIST (PTDC/BIA-BEC/105110/2008), NETPERSIST (PTDC/AAG-MAA/3227/2012), and MateFrag (PTDC/BIA-BIC/6582/2014). RP was supported by the FCT grant SFRH/BPD/73478/2010 and SFRH/BPD/109235/2015. PB was supported by EDP Biodiversity Chair. We thank Rita Brito and Marta Duarte for help during field work. We thank Chris Sutherland, Douglas Morris, William Morgan, and Richard Hassall for critical reviews of early versions of the paper. We also thank two anonymous reviewers for helpful comments to improve the paper.
Authors contribution statement
RP, AM, PB conceived and designed the experiments. RP performed the experiments. RP, XL, AM, and PB analyzed the data. RP, XL, AM and PB wrote the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Janne Sundell.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Pita, R., Lambin, X., Mira, A. et al. Hierarchical spatial segregation of two Mediterranean vole species: the role of patch-network structure and matrix composition. Oecologia 182, 253–263 (2016). https://doi.org/10.1007/s00442-016-3653-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-016-3653-y