Measuring the extent to which a species is specialized is a major challenge in ecology, with important repercussions for fundamental research as well as for applied ecology and conservation. Here, we develop a multidimensional index of specialization based on five sets of ecological characteristics of breeding bird species. We used two recent databases of species traits of European birds based on foraging ecology, habitat, and breeding characteristics. The indices of specialization were calculated by applying the Gini coefficient, an index of inequality. The Gini coefficient is a measure of statistical dispersion on a scale between 0 and 1, reflecting a gradient from low to high specialization, respectively. Finally, we tested the strength of the phylogenetic signal of each specialization index to understand how the variance of such indices is shared throughout the phylogeny. The methods for constructing and evaluating a multidimensional index of bird specialization could also be applied to other taxa and regions, offering a simple but useful tool, particularly suited for global or biogeographic studies, as a contribution to comparative estimates of the degree of specialization of species.

Department of Applied Geoinformatics and Spatial Planning Faculty of Environmental Sciences Czech University of Life Sciences Prague Czech Republic

Ecologie Systématique Evolution Université Paris Sud CNRS AgroParisTech Université Saclay Orsay Cedex France

Faculty of Biological Sciences University of Zielona Góra Zielona Góra Poland

School of Biological Sciences The University of Queensland St Lucia Queensland Australia

Zobrazit více v PubMed

Allan, J. R. , Watson, J. E. M. , Di Marco, M. , O'Bryan, C. J. , Possingham, H. P. , Atkinson, S. C. , & Venter, O. (2019). Hotspots of human impact on threatened terrestrial vertebrates. PLoS Biology, 17, 1–18. 10.1371/journal.pbio.3000158 PubMed DOI PMC

Barnagaud, J. Y. , Devictor, V. , Jiguet, F. , & Archaux, F. (2011). When species become generalists: On‐going large‐scale changes in bird habitat specialization. Global Ecology and Biogeography, 20, 630–640. 10.1111/j.1466-8238.2010.00629.x DOI

Barr, L. M. , Pressey, R. L. , Fuller, R. A. , Segan, D. B. , McDonald‐Madden, E. , & Possingham, H. P. (2011). A new way to measure the World's Protected Area Coverage. PLoS ONE, 6(9), e24707. PubMed PMC

Blomberg, S. P. , & Garland, T. (2003). Tempo and mode in evolution: Phylogenetic inertia, adaptation and comparative methods. Journal of Evolutionary Biology, 15, 899–910. 10.1046/j.1420-9101.2002.00472.x DOI

Blomberg, S. P. , Garland, T. J. , & Ives, A. R. (2003). Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution, 57, 717–745. 10.1111/j.0014-3820.2003.tb00285.x PubMed DOI

Bowler, D. E. , Heldbjerg, H. , Fox, A. D. , de Jong, M. , & Böhning‐Gaese, K. (2019). Long‐term declines of European insectivorous bird populations and potential causes. Conservation Biology, 1–11. 10.1111/cobi.13307 PubMed DOI

Breiner, F. T. , Guisan, A. , Nobis, M. P. , & Bergamini, A. (2017). Including environmental niche information to improve IUCN Red List assessments. Diversity and Distributions, 23, 484–495. 10.1111/ddi.12545 DOI

Castiglione, S. , Mondanaro, A. , Carotenuto, F. , & Passaro, F. (2017). The many shapes of diversity: Ecological and evolutionary determinants of biodiversity through time. Evolutionary Ecology Research, 18, 25–39.

Chazdon, R. L. , Chao, A. , Colwell, R. K. , Lin, S. Y. , Norden, N. , Letcher, S. G. , … Arroyo, J. P. (2011). A novel statistical method for classifying habitat generalists and specialists. Ecology, 92, 1332–1343. 10.1890/10-1345.1 PubMed DOI

Clavel, J. , Julliard, R. , & Devictor, V. (2011). Worldwide decline of specialist species: Toward a global functional homogenization? Frontiers in Ecology and the Environment, 9, 222–228. 10.1890/080216 DOI

Clavero, M. , Brotons, L. , & Herrando, S. (2011). Bird community specialization, bird conservation and disturbance: The role of wildfires. Journal of Animal Ecology, 80, 128–136. 10.1111/j.1365-2656.2010.01748.x PubMed DOI

Colles, A. , Liow, L. H. , & Prinzing, A. (2009). Are specialists at risk under environmental change? Neoecological, paleoecological and phylogenetic approaches. Ecology Letters, 12, 849–863. 10.1111/j.1461-0248.2009.01336.x PubMed DOI PMC

Colwell, F. A. (2011). Measuring Inequality. Oxford, UK: Oxford University Press.

Combes, C. (2004). Parasitism: The ecology and evolution of intimate interactions. Chicago: University of Chicago Press.

Damgaard, C. , & Weiner, J. (2000). Describing inequality in plant size or fecundity. Ecology, 81, 1139–1142. 10.1890/0012-9658(2000)081[1139:DIIPSO]2.0.CO;2 DOI

de Bello, F. , Lavorel, S. , Gerhold, P. , Reier, Ü. , & Pärtel, M. (2010). A biodiversity monitoring framework for practical conservation of grasslands and shrublands. Biological Conservation, 143, 9–17. 10.1016/j.biocon.2009.04.022 DOI

Devictor, V. , Clavel, J. , Julliard, R. , Lavergne, S. , Mouillot, D. , Thuiller, W. , … Mouquet, N. (2010). Defining and measuring ecological specialization. Journal of Applied Ecology, 47, 15–25. 10.1111/j.1365-2664.2009.01744.x DOI

Devictor, V. , Julliard, R. , & Jiguet, F. (2008). Distribution of specialist and generalist species along spatial gradients of habitat disturbance and fragmentation. Oikos, 117, 507–514. 10.1111/j.0030-1299.2008.16215.x DOI

Dondina, O. , Orioli, V. , D'Occhio, P. , Luppi, M. , & Bani, L. (2016). How does forest species specialization affect the application of the island biogeography theory in fragmented landscapes? Journal of Biogeography, 1–12. 10.1111/jbi.12827 DOI

Ducatez, S. , Clavel, J. , & Lefebvre, L. (2015). Ecological generalism and behavioural innovation in birds: Technical intelligence or the simple incorporation of new foods? Journal of Animal Ecology, 84, 79–89. 10.1111/1365-2656.12255 PubMed DOI

Ducatez, S. , & Lefebvre, L. (2014). Patterns of research effort in birds. PLoS ONE, 9, e89955. PubMed PMC

Dufrene, M. , & Legendre, P. (1997). Species Assemblages and indicator species: The need for a flexible asymmetrical approach. Ecological Monographs, 67, 345–366. 10.2307/2963459 DOI

Ericson, P. G. P. , Anderson, C. L. , Britton, T. , Elzanowski, A. , Johansson, U. S. , Källersjö, M. , … Mayr, G. (2006). Diversification of Neoaves: Integration of molecular sequence data and fossils. Biology Letters, 2, 543–547. 10.1098/rsbl.2006.0523 PubMed DOI PMC

Fraser, H. , Pichancourt, J.‐B. , & Butet, A. (2016). Tiny terminological disagreements with far reaching consequences for global bird trends. Ecological Indicators, 73, 79–87. 10.1016/j.ecolind.2016.09.033 DOI

Futuyma, D. J. , & Agrawal, A. A. (2009). Evolutionary history and species interactions. Proceedings of the National Academy of Sciences of the United States of America, 106, 18043–18044. 10.1073/pnas.0910334106 PubMed DOI PMC

Futuyma, D. J. , & Moreno, G. (1988). The evolution of ecological specialization. Annual Review of Ecology and Systematics, 19, 207–233. 10.1146/annurev.es.19.110188.001231 DOI

Garamszegi, L. Z. , & Møller, A. P. (2012). Untested assumptions about within‐species sample size and missing data in interspecific studies. Behavioral Ecology and Sociobiology, 66, 1363–1373. 10.1007/s00265-012-1370-z DOI

Gastwirh, J. (1972). The estimation of the Lorenz curve and Gini index. The Review of Economics and Statistics, 54, 306–316. 10.2307/1937992 DOI

Gini, C. (1921). Measurement of inequality and incomes. The Economic Journal, 31, 124–126.

Gregory, R. D. , van Strien, A. , Voříšek, P. , Gmelig Meyling, A. W. , Noble, D. G. , Foppen, R. P. B. , & Gibbons, D. W. (2005). Developing indicators for European birds. Philosophical Transactions of the Royal Society of London B – Biological Sciences, 360, 269–288. 10.1098/rstb.2004.1602 PubMed DOI PMC

Grinnell, J. (1917). The niche relationships of the California Thrasher. The Auk, 34, 427–433. 10.2307/4072271 DOI

Hammond, T. T. , Palme, R. , & Lacey, E. A. (2018). Ecological specialization, variability in activity patterns and response to environmental change. Biology Letters, 14, 20180115 10.1098/rsbl.2018.0115 PubMed DOI PMC

Harvey, P. H. , & Purvis, A. (1991). Comparative methods for explaining adaptations. Nature, 351, 619–624. 10.1038/351619a0 PubMed DOI

Hatfield, J. H. , Orme, C. D. L. , Tobias, J. A. , & Banks‐Leite, C. (2018). Trait‐based indicators of bird species sensitivity to habitat loss are effective within but not across data sets. Ecological Applications, 28, 28–34. 10.1002/eap.1646 PubMed DOI

Henle, K. , Davies, K. F. , Kleyer, M. , Margules, C. , & Settele, J. (2004). Predictors of species sensitivity to fragmentation. Biodiversity and Conservation, 13, 207–251. 10.1023/B:BIOC.0000004319.91643.9e DOI

Irschick, D. , Dyer, L. , & Sherry, T. W. (2005). Phylogenetic methodologies for studying specialization. Oikos, 110, 404–408. 10.1111/j.0030-1299.2005.13927.x DOI

Julliard, R. , Clavel, J. , Devictor, V. , Jiguet, F. , & Couvet, D. (2006). Spatial segregation of specialists and generalists in bird communities. Ecology Letters, 9, 1237–1244. 10.1111/j.1461-0248.2006.00977.x PubMed DOI

Julliard, R. , Jiguet, F. , & Couvet, D. (2004). Common birds facing global changes: What makes a species at risk? Global Change Biology, 10, 148–154. 10.1111/j.1365-2486.2003.00723.x DOI

Kamilar, J. M. , & Cooper, N. (2013). Phylogenetic signal in primate behaviour, ecology and life history. Philosophical Transactions of the Royal Society B, 368, 20120341 10.1098/rstb.2012.0341 PubMed DOI PMC

Keck, F. , Rimet, F. , Bouchez, A. , & Franc, A. (2016). Phylosignal: An R package to measure, test, and explore the phylogenetic signal. Ecology and Evolution, 6, 2774–2780. 10.1002/ece3.2051 PubMed DOI PMC

Lerman, R. I. , & Yitzhaki, S. (1984). A note on the calculation and interpretation of the Gini index. Economic Letters, 15, 363–368. 10.1016/0165-1765(84)90126-5 DOI

Luck, G. W. , Carter, A. , & Smallbone, L. (2013). Changes in bird functional diversity across multiple land uses: Interpretations of functional redundancy depend on functional group identity. PLoS ONE, 8, e63671 10.1371/journal.pone.0063671 PubMed DOI PMC

McKenzie, A. J. , & Robertson, P. A. (2015). Which species are we researching and why? A Case Study of the Ecology of British Breeding Birds. PLoS ONE, 10, e0131004 10.1371/journal.pone.0131004 PubMed DOI PMC

McKinney, M. (1997). Extinction vulnerability and selectivity: Combining ecological and paleontological views. Annual Review of Ecology and Systematics, 28, 495–516. 10.1146/annurev.ecolsys.28.1.495 DOI

Moreira, F. , Ferreira, P. G. , Rego, F. C. , & Bunting, S. (2001). Landscape changes and breeding bird assemblages in northwestern Portugal: The role of fire. Landscape Ecology, 16, 175–187.

Münkemüller, T. , Lavergne, S. , Bzeznik, B. , Dray, S. , Jombart, T. , Schiffers, K. , & Thuiller, W. (2012). How to measure and test phylogenetic signal. Methods in Ecology and Evolution, 3, 743–756. 10.1111/j.2041-210X.2012.00196.x DOI

Paradis, E. , Claude, J. , & Strimmer, K. (2004). APE: Analyses of phylogenetics and evolution in R language. Bioinformatics, 20, 289–290. 10.1093/bioinformatics/btg412 PubMed DOI

Pearman, P. B. , Lavergne, S. , Roquet, C. , Wüest, R. , Zimmermann, N. E. , & Thuiller, W. (2014). Phylogenetic patterns of climatic, habitat and trophic niches in a European avian assemblage. Global Ecology and Biogeography, 23, 414–424. 10.1111/geb.12127 PubMed DOI PMC

R Development Core Team . (2017). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.

Reif, J. , Hořák, D. , Krištín, A. , Kopsová, L. , & Devictor, V. (2016). Linking habitat specialization with species' traits in European birds. Oikos, 125, 405–413. 10.1111/oik.02276 DOI

Reif, J. , Jiguet, F. , & Šťastný, K. (2010). Habitat specialization of birds in the Czech Republic: Comparison of objective measures with expert opinion. Bird Study, 57, 197–212. 10.1080/00063650903477046 DOI

Revell, L. J. , & Chamberlain, S. A. (2014). Rphylip: An R interface for PHYLIP R package.

Schliep, K. P. (2011). phangorn: Phylogenetic analysis in R. Bioinformatics, 27, 592–593. 10.1093/bioinformatics/btq706 PubMed DOI PMC

Schluter, D. (2000). The ecology of adaptive radiation. Oxford, UK: OUP Oxford.

Signorell, A. , Aho, K. , Alfons, A. , Anderegg, N. , Aragon, T. , Arppe, A. , … Zeileis, A. (2019). DescTools: Tools for descriptive statistics. R package version 0.99.28.

Storchová, L. , & Hořák, D. (2018). Life‐history characteristics of European birds. Global Ecology and Biogeography, 27, 400–406. 10.1111/geb.12709 DOI

Triola, M. F. (2012). Elementary statistics (12th ed.). London, UK: Pearson International.

Vázquez, D. P. , & Simberloff, D. (2002). Ecological specialization and susceptibility to disturbance: Conjectures and refutations. The American Naturalist, 159, 606–623. 10.1086/339991 PubMed DOI

Villéger, S. , Mason, N. W. H. , & Mouillot, D. (2008). New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology, 89, 2290–2301. 10.1890/07-1206.1 PubMed DOI

Violle, C. , Navas, M.‐L.‐L. , Vile, D. , Kazakou, E. , Fortunel, C. , Hummel, I. , & Garnier, E. (2007). Let the concept of trait be functional!. Oikos, 116, 882–892. 10.1111/j.2007.0030-1299.15559.x DOI

Webb, G. J. W. (2008). The dilemma of accuracy in IUCN Red List categories, as exemplified by hawksbill turtles Eretmochelys imbricata. Endangered Species Research, 6, 161–172. 10.3354/esr00124 DOI

Human pressures threaten diet-specialized mammal communities

Ecological filtering shapes the impacts of agricultural deforestation on biodiversity

Forest structure determines nest box use by Central European boreal owls

Diet specialization and brood parasitism in cuckoo species