Abstract
Body size is intrinsically linked to metabolic rate and life-history traits, and is a crucial determinant of food webs and community dynamics1,2. The increased temperatures associated with the urban-heat-island effect result in increased metabolic costs and are expected to drive shifts to smaller body sizes3. Urban environments are, however, also characterized by substantial habitat fragmentation4, which favours mobile species. Here, using a replicated, spatially nested sampling design across ten animal taxonomic groups, we show that urban communities generally consist of smaller species. In addition, although we show urban warming for three habitat types and associated reduced community-weighted mean body sizes for four taxa, three taxa display a shift to larger species along the urbanization gradients. Our results show that the general trend towards smaller-sized species is overruled by filtering for larger species when there is positive covariation between size and dispersal, a process that can mitigate the low connectivity of ecological resources in urban settings5. We thus demonstrate that the urban-heat-island effect and urban habitat fragmentation are associated with contrasting community-level shifts in body size that critically depend on the association between body size and dispersal. Because body size determines the structure and dynamics of ecological networks1, such shifts may affect urban ecosystem function.
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References
Woodward, G. et al. Body size in ecological networks. Trends Ecol. Evol. 20, 402–409 (2005).
Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. & West, G. B. Toward a metabolic theory of ecology. Ecology 85, 1771–1789 (2004).
Scheffers, B. R. et al. The broad footprint of climate change from genes to biomes to people. Science 354, aaf7671 (2016).
Alberti, M., Marzluff, J. & Hunt, V. M. Urban driven phenotypic changes: empirical observations and theoretical implications for eco-evolutionary feedback. Phil. Trans. R. Soc. Lond. B 372, 20160029 (2017).
Cheptou, P. O., Hargreaves, A. L., Bonte, D. & Jacquemyn, H. Adaptation to fragmentation: evolutionary dynamics driven by human influences. Phil. Trans. R. Soc. Lond. B 372, 20160037 (2017).
Chown, S. L. & Gaston, K. J. Body size variation in insects: a macroecological perspective. Biol. Rev. Camb. Philos. Soc. 85, 139–169 (2010).
Kalinkat, G. et al. Body masses, functional responses and predator–prey stability. Ecol. Lett. 16, 1126–1134 (2013).
Brose, U. et al. Predicting the consequences of species loss using size-structured biodiversity approaches. Biol. Rev. Camb. Philos. Soc. 92, 684–697 (2017).
Horne, C. R., Hirst, A. G. & Atkinson, D. Seasonal body size reductions with warming covary with major body size gradients in arthropod species. Proc. R. Soc. B 284, 20170238 (2017).
Seto, K. C., Güneralp, B. & Hutyra, L. R. Global forecasts of urban expansion to 2030 and direct impacts on biodiversity and carbon pools. Proc. Natl Acad. Sci. USA 109, 16083–16088 (2012).
Youngsteadt, E., Dale, A. G., Terando, A. J., Dunn, R. R. & Frank, S. D. Do cities simulate climate change? A comparison of herbivore response to urban and global warming. Glob. Chang. Biol. 21, 97–105 (2015).
Ward, K., Lauf, S., Kleinschmit, B. & Endlicher, W. Heat waves and urban heat islands in Europe: a review of relevant drivers. Sci. Total Environ. 569-570, 527–539 (2016).
Niemelä. J. Urban Ecology: Patterns, Processes, and Applications (Oxford Univ. Press, Oxford, 2011).
Atkinson, D. Temperature and organism size: a biological law for ectotherms? Adv. Ecol. Res 25, 1–58 (1994).
Bonte, D. & Dahirel, M. Dispersal: a central and independent trait in life history. Oikos 126, 472–479 (2017).
Piano, E. et al. Urbanization drives community shifts towards thermophilic and dispersive species at local and landscape scales. Glob. Chang. Biol. 23, 2554–2564 (2017).
Concepción, E. D., Moretti, M., Altermatt, F., Nobis, M. P. & Obrist, M. K. Impacts of urbanisation on biodiversity: the role of species mobility, degree of specialisation and spatial scale. Oikos 124, 1571–1582 (2015).
Arnfield, A. J. Two decades of urban climate research: a review of turbulence, exchanges of energy and water, and the urban heat island. Int. J. Climatol. 23, 1–26 (2003).
Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B Stat. Methodol. 57, 289–300 (1995).
Forster, J., Hirst, A. G. & Atkinson, D. Warming-induced reductions in body size are greater in aquatic than terrestrial species. Proc. Natl Acad. Sci. USA 109, 19310–19314 (2012).
Dahirel, M., Dierick, J., De Cock, M. & Bonte, D. Intraspecific variation shapes community-level behavioral responses to urbanization in spiders. Ecology 98, 2379–2390 (2017).
McDonnell, M. J. & Hahs, A. K. Adaptation and adaptedness of organisms to urban environments. Annu. Rev. Ecol. Evol. Syst. 46, 261–280 (2015).
Alberti, M. et al. Global urban signatures of phenotypic change in animal and plant populations. Proc. Natl Acad. Sci. USA 114, 8951–8956 (2017).
Johnson, M. T. J. & Munshi-South, J. Evolution of life in urban environments. Science 358, eaam8327 (2017).
Schramski, J. R., Dell, A. I., Grady, J. M., Sibly, R. M. & Brown, J. H. Metabolic theory predicts whole-ecosystem properties. Proc. Natl Acad. Sci. USA 112, 2617–2622 (2015).
Malerba, M. E., White, C. R. & Marshall, D. J. Eco-energetic consequences of evolutionary shifts in body size. Ecol. Lett. 21, 54–62 (2018).
Osmond, M. M. et al. Warming-induced changes to body size stabilize consumer–resource dynamics. Am. Nat. 189, 718–725 (2017).
Gianuca, A. T., Pantel, J. H. & De Meester, L. Disentangling the effect of body size and phylogenetic distances on zooplankton top-down control of algae. Proc. R. Soc. B 283, 20160487 (2016).
Agosta, S. J. & Janzen, D. H. Body size distributions of large Costa Rican dry forest moths and the underlying relationship between plant and pollinator morphology. Oikos 108, 183–193 (2005).
Biesmeijer, J. C. et al. Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313, 351–354 (2006).
Duffy, J. E. Biodiversity loss, trophic skew and ecosystem functioning. Ecol. Lett. 6, 680–687 (2003).
Webb, C. T., Hoeting, J. A., Ames, G. M., Pyne, M. I. & LeRoy Poff, N. A structured and dynamic framework to advance traits-based theory and prediction in ecology. Ecol. Lett. 13, 267–283 (2010).
Threlfall, C. G. et al. Increasing biodiversity in urban green spaces through simple vegetation interventions. J. Appl. Ecol. 54, 1874–1883 (2017).
IBZ. Bevolkingscijfers per Provincie en per Gemeente op 1 Januari 2017 http://www.ibz.rrn.fgov.be/fileadmin/user_upload/fr/pop/statistiques/population-bevolking-20170101.pdf (Federale Overheidsdienst Binnenlandse Zaken, 2017).
De Saeger, S. et al. Biologische Waarderingskaart en Natura 2000 Habitatkaart (Instituut voor Natuur en Bosonderzoek, Brussels, 2016).
Packet, J. et al. Watervlakken Versie 1.0: Polygonenkaart van Stilstaand Water in Vlaanderen. Inhoud en Metadata van een Nieuw Instrument voor Water-, Milieu- en Natuurbeleid (Instituut voor Natuur en Bosonderzoek, Brussels, 2017).
Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference: a Practical Information-Theoretic Approach (Springer Science & Business Media, New York, 2003).
R Development Core Team. R: A Language and Environment for Statistical Computing https://www.r-project.org/ (R Foundation for Statistical Computing, Vienna, 2015).
Bink, F. A. Ecologische Atlas van de Dagvlinders van Noordwest-Europa (Schuyt & Co, Haarlem, 1992).
Sekar, S. A meta-analysis of the traits affecting dispersal ability in butterflies: can wingspan be used as a proxy? J. Anim. Ecol. 81, 174–184 (2012).
Stevens, V. M., Trochet, A., Van Dyck, H., Clobert, J. & Baguette, M. How is dispersal integrated in life histories: a quantitative analysis using butterflies. Ecol. Lett. 15, 74–86 (2012).
Stevens, V. M. et al. A comparative analysis of dispersal syndromes in terrestrial and semi-terrestrial animals. Ecol. Lett. 17, 1039–1052 (2014).
Manley, C. British Moths and Butterflies: a Photographic Guide (A & C Black, London, 2008).
Nieminen, M., Rita, H. & Uuvana, P. Body size and migration rate in moths. Ecography 22, 697–707 (1999).
Slade, E. M. et al. Life-history traits and landscape characteristics predict macro-moth responses to forest fragmentation. Ecology 94, 1519–1530 (2013).
Reinhardt, K., Köhler, G., Maas, S. & Detzel, P. Low dispersal ability and habitat specificity promote extinctions in rare but not in widespread species: the Orthoptera of Germany. Ecography 28, 593–602 (2005).
Roberts, M. J. The Spiders of Great Britain and Ireland: Compact Edition (Apollo Books, Vester Skerninge, 2009).
Turin, H. De Nederlandse Loopkevers: Verspreiding en Ecologie (KNNV, Zeist, 2000).
Duff, A. G. et al. Beetles of Britain and Ireland 4 (A. G. Duff, West Runton, 2016).
Donner, J. Ordnung Bdelloidea. Bestimmungsbücher zur Bodenfauna Europas (Akademie-Verlag, Berlin, 1965).
Fontaneto, D. Biogeography of Microscopic Organisms: is Everything Small Everywhere? (Cambridge Univ. Press, Cambridge, 2011).
Meisch, C. Freshwater Ostracoda of Western and Central Europe (Spektrum Akademischer, Heidelberg, 2000).
Bilton, D. T., Freeland, J. R. & Okamura, B. Dispersal in freshwater invertebrates. Annu. Rev. Ecol. Syst. 32, 159–181 (2001).
De Bie, T. et al. Body size and dispersal mode as key traits determining metacommunity structure of aquatic organisms. Ecol. Lett. 15, 740–747 (2012).
Brans, K. I. et al. Eco-evolutionary dynamics in urbanized landscapes: evolution, species sorting and the change in zooplankton body size along urbanization gradients. Phil. Trans. R. Soc. Lond. B 372, 20160030 (2017).
Gianuca, A. T. et al. Taxonomic, functional and phylogenetic metacommunity ecology of cladoceran zooplankton along urbanization gradients. Ecography 41, 183–194 (2018).
Acknowledgements
We thank M. De Cock, J. Dierick, P. Limbourg, E. van den Berg, M. Van Kerckvoorde and P. Vantieghem for help with sampling and identification of species. This is publication BRC419 of the Biodiversity Research Centre (UCL/ELI). This research is part of the SPEEDY-project, funded by the Interuniversity Attraction Poles program of the Belgian Science Policy Office BELSPO (IAP-grant P7/04).
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T.M., L.D.M. and H.V.D. conceived the study. C.S. and L.D.M. coordinated the consortium. T.M., C.S., A.K., L.F.B., T.B., D.B., K.I.B., M.C., M.D., N.D., K.D.W., J.M.T.E., D.F., A.T.G., L.G., F.H., J.H., L.L., K.M., E.M., E.P., R.S., I.S. and K.V.D. contributed to sampling and data collection. T.M. and A.K. performed the analyses. H.M. selected study plots, calculated fragmentation variables and designed the study area map. T.M. wrote the first draft of the manuscript with all authors contributing substantially to revisions.
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Extended data figures and tables
Extended Data Fig. 1 Micro-climatic urban-heat-island effect strengths.
a, b, Slopes of the urban-heat-island effects (measured as the increase in temperature (°C) per 1% increase in percentage BUC) as a function of spatial scale (the radius at which urbanization was quantified) with 95% confidence intervals (CI). Separate measurements are shown for summer (red) and winter (blue) using merged readings for pond, grassland and woodland habitats (n = 104 sites). a, Diurnal measurements. b, Nocturnal measurements. Data points are offset from one another horizontally to improve clarity.
Extended Data Fig. 2 Correlations between urbanization and habitat fragmentation.
Correlations between urbanization (measured as the percentage BUC) and three habitat fragmentation variables: habitat coverage (a, b), mean size of habitat patches (c, d), and mean nearest-neighbour distance among habitat patches (e, f). Separate plots are shown for terrestrial (that is, all types of (semi-)natural habitat, a, c, e) and aquatic (that is, all pond types, b, d, f) habitats (n = 27 landscape-scale sampling plots). Pearson’s r coefficients and P values are indicated; not significant (NS), P > 0.1; *P < 0.05; ***P < 0.001.
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Merckx, T., Souffreau, C., Kaiser, A. et al. Body-size shifts in aquatic and terrestrial urban communities. Nature 558, 113–116 (2018). https://doi.org/10.1038/s41586-018-0140-0
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DOI: https://doi.org/10.1038/s41586-018-0140-0
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