Body-size shifts in aquatic and terrestrial urban communities

Thomas Merckx, Caroline Souffreau, Aurélien Kaiser, Lisa F. Baardsen, Thierry Backeljau, Dries Bonte, Kristien I. Brans, Marie Cours, Maxime Dahirel, Nicolas Debortoli, Katrien De Wolf, Jessie M.T. Engelen, Diego Fontaneto, Andros T. Gianuca, Lynn Govaert, Frederik Hendrickx, Janet Higuti, Luc Lens, Koen Martens, Hans MatheveErik Matthysen, Elena Piano, Rose Sablon, Isa Schön, Karine Van Doninck, Luc De Meester, Hans Van Dyck

Résultats de recherche: Contribution à un journal/une revueArticle

Résumé

Body size is intrinsically linked to metabolic rate and life-history traits, and is a crucial determinant of food webs and community dynamics 1,2. The increased temperatures associated with the urban-heat-island effect result in increased metabolic costs and are expected to drive shifts to smaller body sizes 3. Urban environments are, however, also characterized by substantial habitat fragmentation 4 , 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 settings 5. 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 networks 1 , such shifts may affect urban ecosystem function. Body size is a fundamental species trait relating to space use and key life-history features such as longevity and fecundity 6. It also drives interspecific relationships, thus affecting ecological network dynamics 1. Size-biased species loss has profound effects on ecosystem function 7,8. Ectotherms rely on ambient conditions to achieve operational body temperatures 9. Because higher ambient temperature increases metabolic rates and the associated costs for a given body size 2 , global climatic warming is expected to drive shifts to communities consisting of smaller species 3. Our planet is urbanizing quickly 10 , which is a primary example of human-induced rapid environmental change. Cities are urban heat islands characterized by increased temperatures that are decades ahead of global averages 11. Not only are cities warmer than surrounding areas, but they also experience extensive fragmentation of (semi-)natural habitats , and both of these effects increase with percentage built-up cover (BUC; a proxy for urbanization) 12,13. This provides an opportunity to study the opposing effects of size-dependent thermal tolerance and dispersal capacity, as larger body size favours dispersal in some, but not all, taxa. Here we test the hypothesis that urbanization causes shifts in community level body size, and that these shifts are dictated by the community specific association between body size and dispersal. We generally expect the urban-heat-island effect to drive shifts to species with smaller body sizes in communities of ectothermic species, in line with Atkinson's temperature-size rule 14. For taxa characterized by a positive association between body size and dispersal, however, we also expect a filtering in favour of larger-bodied species associated with habitat fragmentation 5,15. Filtering for increased mobility has been demonstrated for urban ground beetle and plant communities 16,17. Hence, for taxa characterized by a positive body-size-dispersal link, we predict that the general community-level pattern of smaller species with increasing urbanization may be neutralized or even reversed. To test our hypothesis, we engaged in an analysis of community-level shifts in body size across a broad range of both terrestrial and aquatic taxa along the same systematically sampled urbanization gradients. We studied the direction of change of community-level body size in ten taxa using a replicated, highly standardized and nested sampling design that covers urbanization gradients at seven spatial scales (50-3,200 m radii; Fig. 1). We sampled each taxon at up to 81 sites, sampling 95,001 individuals from 702 species, with species-specific body size varying by a factor of 400 (0.2-80 mm; Extended Data Table 1). Three of the ten groups are characterized by a positive association between body size and dispersal capacity (see Extended Data Table 1). We show that the local temperature of pond, grassland and woodland habitats significantly increases with urbanization (linear mixed regression models, P <0.002; Extended Data Table 2). The intensity of these urban-heat-island effects is consistently larger during night and summer, in accordance with slower night-time city cooling and higher irradiation levels in summer 18 (Fig. 2, Extended Data Fig. 1, Extended Data Table 2). We also show that increased urbanization is linked to significant declines in habitat amount and the patch size of terrestrial habitats, and significant increases in distances among patches for both terrestrial and aquatic habitats (Pearson's r correlations, P ≤ 0.020; Extended Data Fig. 2). Confirming our metabolism-based prediction that interspecific mean body size decreases with increasing temperature, urban communities for four out of the seven taxa (ground spiders, ground beetles, weevils and cladocerans) that did not have a positive size-dispersal link display reduced community-weighted mean body size (CWMBS). For ostracods, bdelloid rotifers and web spiders, no relationship with urbanization is found. By contrast, all three taxa with positive size-dispersal links display increased CWMBS in response to urbanization
langue originaleAnglais
Pages (de - à)113-116
Nombre de pages4
journalNature
Volume558
Numéro de publication7708
Les DOIs
étatPublié - 7 juin 2018

Empreinte digitale

body size
urbanization
habitat fragmentation
habitats
Carabidae
temperature
life history
ecosystems
summer
aquatic habitat
heat tolerance
Rotifera
sampling
Curculionidae
body temperature
global warming
food webs
Araneae
woodlands
plant communities

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Merckx, T., Souffreau, C., Kaiser, A., Baardsen, L. F., Backeljau, T., Bonte, D., ... Van Dyck, H. (2018). Body-size shifts in aquatic and terrestrial urban communities. Nature, 558(7708), 113-116. https://doi.org/10.1038/s41586-018-0140-0
Merckx, Thomas ; Souffreau, Caroline ; Kaiser, Aurélien ; Baardsen, Lisa F. ; Backeljau, Thierry ; Bonte, Dries ; Brans, Kristien I. ; Cours, Marie ; Dahirel, Maxime ; Debortoli, Nicolas ; De Wolf, Katrien ; Engelen, Jessie M.T. ; Fontaneto, Diego ; Gianuca, Andros T. ; Govaert, Lynn ; Hendrickx, Frederik ; Higuti, Janet ; Lens, Luc ; Martens, Koen ; Matheve, Hans ; Matthysen, Erik ; Piano, Elena ; Sablon, Rose ; Schön, Isa ; Van Doninck, Karine ; De Meester, Luc ; Van Dyck, Hans. / Body-size shifts in aquatic and terrestrial urban communities. Dans: Nature. 2018 ; Vol 558, Numéro 7708. p. 113-116.
@article{8e542f4e739a4154949f456d87021217,
title = "Body-size shifts in aquatic and terrestrial urban communities",
abstract = "Body size is intrinsically linked to metabolic rate and life-history traits, and is a crucial determinant of food webs and community dynamics 1,2. The increased temperatures associated with the urban-heat-island effect result in increased metabolic costs and are expected to drive shifts to smaller body sizes 3. Urban environments are, however, also characterized by substantial habitat fragmentation 4 , 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 settings 5. 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 networks 1 , such shifts may affect urban ecosystem function. Body size is a fundamental species trait relating to space use and key life-history features such as longevity and fecundity 6. It also drives interspecific relationships, thus affecting ecological network dynamics 1. Size-biased species loss has profound effects on ecosystem function 7,8. Ectotherms rely on ambient conditions to achieve operational body temperatures 9. Because higher ambient temperature increases metabolic rates and the associated costs for a given body size 2 , global climatic warming is expected to drive shifts to communities consisting of smaller species 3. Our planet is urbanizing quickly 10 , which is a primary example of human-induced rapid environmental change. Cities are urban heat islands characterized by increased temperatures that are decades ahead of global averages 11. Not only are cities warmer than surrounding areas, but they also experience extensive fragmentation of (semi-)natural habitats , and both of these effects increase with percentage built-up cover (BUC; a proxy for urbanization) 12,13. This provides an opportunity to study the opposing effects of size-dependent thermal tolerance and dispersal capacity, as larger body size favours dispersal in some, but not all, taxa. Here we test the hypothesis that urbanization causes shifts in community level body size, and that these shifts are dictated by the community specific association between body size and dispersal. We generally expect the urban-heat-island effect to drive shifts to species with smaller body sizes in communities of ectothermic species, in line with Atkinson's temperature-size rule 14. For taxa characterized by a positive association between body size and dispersal, however, we also expect a filtering in favour of larger-bodied species associated with habitat fragmentation 5,15. Filtering for increased mobility has been demonstrated for urban ground beetle and plant communities 16,17. Hence, for taxa characterized by a positive body-size-dispersal link, we predict that the general community-level pattern of smaller species with increasing urbanization may be neutralized or even reversed. To test our hypothesis, we engaged in an analysis of community-level shifts in body size across a broad range of both terrestrial and aquatic taxa along the same systematically sampled urbanization gradients. We studied the direction of change of community-level body size in ten taxa using a replicated, highly standardized and nested sampling design that covers urbanization gradients at seven spatial scales (50-3,200 m radii; Fig. 1). We sampled each taxon at up to 81 sites, sampling 95,001 individuals from 702 species, with species-specific body size varying by a factor of 400 (0.2-80 mm; Extended Data Table 1). Three of the ten groups are characterized by a positive association between body size and dispersal capacity (see Extended Data Table 1). We show that the local temperature of pond, grassland and woodland habitats significantly increases with urbanization (linear mixed regression models, P <0.002; Extended Data Table 2). The intensity of these urban-heat-island effects is consistently larger during night and summer, in accordance with slower night-time city cooling and higher irradiation levels in summer 18 (Fig. 2, Extended Data Fig. 1, Extended Data Table 2). We also show that increased urbanization is linked to significant declines in habitat amount and the patch size of terrestrial habitats, and significant increases in distances among patches for both terrestrial and aquatic habitats (Pearson's r correlations, P ≤ 0.020; Extended Data Fig. 2). Confirming our metabolism-based prediction that interspecific mean body size decreases with increasing temperature, urban communities for four out of the seven taxa (ground spiders, ground beetles, weevils and cladocerans) that did not have a positive size-dispersal link display reduced community-weighted mean body size (CWMBS). For ostracods, bdelloid rotifers and web spiders, no relationship with urbanization is found. By contrast, all three taxa with positive size-dispersal links display increased CWMBS in response to urbanization",
author = "Thomas Merckx and Caroline Souffreau and Aur{\'e}lien Kaiser and Baardsen, {Lisa F.} and Thierry Backeljau and Dries Bonte and Brans, {Kristien I.} and Marie Cours and Maxime Dahirel and Nicolas Debortoli and {De Wolf}, Katrien and Engelen, {Jessie M.T.} and Diego Fontaneto and Gianuca, {Andros T.} and Lynn Govaert and Frederik Hendrickx and Janet Higuti and Luc Lens and Koen Martens and Hans Matheve and Erik Matthysen and Elena Piano and Rose Sablon and Isa Sch{\"o}n and {Van Doninck}, Karine and {De Meester}, Luc and {Van Dyck}, Hans",
year = "2018",
month = "6",
day = "7",
doi = "10.1038/s41586-018-0140-0",
language = "English",
volume = "558",
pages = "113--116",
journal = "Nature",
issn = "0028-0836",
publisher = "Nature Publishing Group",
number = "7708",

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Merckx, T, Souffreau, C, Kaiser, A, Baardsen, LF, Backeljau, T, Bonte, D, Brans, KI, Cours, M, Dahirel, M, Debortoli, N, De Wolf, K, Engelen, JMT, Fontaneto, D, Gianuca, AT, Govaert, L, Hendrickx, F, Higuti, J, Lens, L, Martens, K, Matheve, H, Matthysen, E, Piano, E, Sablon, R, Schön, I, Van Doninck, K, De Meester, L & Van Dyck, H 2018, 'Body-size shifts in aquatic and terrestrial urban communities', Nature, VOL. 558, Numéro 7708, p. 113-116. https://doi.org/10.1038/s41586-018-0140-0

Body-size shifts in aquatic and terrestrial urban communities. / Merckx, Thomas; Souffreau, Caroline; Kaiser, Aurélien; Baardsen, Lisa F.; Backeljau, Thierry; Bonte, Dries; Brans, Kristien I.; Cours, Marie; Dahirel, Maxime; Debortoli, Nicolas; De Wolf, Katrien; Engelen, Jessie M.T.; Fontaneto, Diego; Gianuca, Andros T.; Govaert, Lynn; Hendrickx, Frederik; Higuti, Janet; Lens, Luc; Martens, Koen; Matheve, Hans; Matthysen, Erik; Piano, Elena; Sablon, Rose; Schön, Isa; Van Doninck, Karine; De Meester, Luc; Van Dyck, Hans.

Dans: Nature, Vol 558, Numéro 7708, 07.06.2018, p. 113-116.

Résultats de recherche: Contribution à un journal/une revueArticle

TY - JOUR

T1 - Body-size shifts in aquatic and terrestrial urban communities

AU - Merckx, Thomas

AU - Souffreau, Caroline

AU - Kaiser, Aurélien

AU - Baardsen, Lisa F.

AU - Backeljau, Thierry

AU - Bonte, Dries

AU - Brans, Kristien I.

AU - Cours, Marie

AU - Dahirel, Maxime

AU - Debortoli, Nicolas

AU - De Wolf, Katrien

AU - Engelen, Jessie M.T.

AU - Fontaneto, Diego

AU - Gianuca, Andros T.

AU - Govaert, Lynn

AU - Hendrickx, Frederik

AU - Higuti, Janet

AU - Lens, Luc

AU - Martens, Koen

AU - Matheve, Hans

AU - Matthysen, Erik

AU - Piano, Elena

AU - Sablon, Rose

AU - Schön, Isa

AU - Van Doninck, Karine

AU - De Meester, Luc

AU - Van Dyck, Hans

PY - 2018/6/7

Y1 - 2018/6/7

N2 - Body size is intrinsically linked to metabolic rate and life-history traits, and is a crucial determinant of food webs and community dynamics 1,2. The increased temperatures associated with the urban-heat-island effect result in increased metabolic costs and are expected to drive shifts to smaller body sizes 3. Urban environments are, however, also characterized by substantial habitat fragmentation 4 , 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 settings 5. 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 networks 1 , such shifts may affect urban ecosystem function. Body size is a fundamental species trait relating to space use and key life-history features such as longevity and fecundity 6. It also drives interspecific relationships, thus affecting ecological network dynamics 1. Size-biased species loss has profound effects on ecosystem function 7,8. Ectotherms rely on ambient conditions to achieve operational body temperatures 9. Because higher ambient temperature increases metabolic rates and the associated costs for a given body size 2 , global climatic warming is expected to drive shifts to communities consisting of smaller species 3. Our planet is urbanizing quickly 10 , which is a primary example of human-induced rapid environmental change. Cities are urban heat islands characterized by increased temperatures that are decades ahead of global averages 11. Not only are cities warmer than surrounding areas, but they also experience extensive fragmentation of (semi-)natural habitats , and both of these effects increase with percentage built-up cover (BUC; a proxy for urbanization) 12,13. This provides an opportunity to study the opposing effects of size-dependent thermal tolerance and dispersal capacity, as larger body size favours dispersal in some, but not all, taxa. Here we test the hypothesis that urbanization causes shifts in community level body size, and that these shifts are dictated by the community specific association between body size and dispersal. We generally expect the urban-heat-island effect to drive shifts to species with smaller body sizes in communities of ectothermic species, in line with Atkinson's temperature-size rule 14. For taxa characterized by a positive association between body size and dispersal, however, we also expect a filtering in favour of larger-bodied species associated with habitat fragmentation 5,15. Filtering for increased mobility has been demonstrated for urban ground beetle and plant communities 16,17. Hence, for taxa characterized by a positive body-size-dispersal link, we predict that the general community-level pattern of smaller species with increasing urbanization may be neutralized or even reversed. To test our hypothesis, we engaged in an analysis of community-level shifts in body size across a broad range of both terrestrial and aquatic taxa along the same systematically sampled urbanization gradients. We studied the direction of change of community-level body size in ten taxa using a replicated, highly standardized and nested sampling design that covers urbanization gradients at seven spatial scales (50-3,200 m radii; Fig. 1). We sampled each taxon at up to 81 sites, sampling 95,001 individuals from 702 species, with species-specific body size varying by a factor of 400 (0.2-80 mm; Extended Data Table 1). Three of the ten groups are characterized by a positive association between body size and dispersal capacity (see Extended Data Table 1). We show that the local temperature of pond, grassland and woodland habitats significantly increases with urbanization (linear mixed regression models, P <0.002; Extended Data Table 2). The intensity of these urban-heat-island effects is consistently larger during night and summer, in accordance with slower night-time city cooling and higher irradiation levels in summer 18 (Fig. 2, Extended Data Fig. 1, Extended Data Table 2). We also show that increased urbanization is linked to significant declines in habitat amount and the patch size of terrestrial habitats, and significant increases in distances among patches for both terrestrial and aquatic habitats (Pearson's r correlations, P ≤ 0.020; Extended Data Fig. 2). Confirming our metabolism-based prediction that interspecific mean body size decreases with increasing temperature, urban communities for four out of the seven taxa (ground spiders, ground beetles, weevils and cladocerans) that did not have a positive size-dispersal link display reduced community-weighted mean body size (CWMBS). For ostracods, bdelloid rotifers and web spiders, no relationship with urbanization is found. By contrast, all three taxa with positive size-dispersal links display increased CWMBS in response to urbanization

AB - Body size is intrinsically linked to metabolic rate and life-history traits, and is a crucial determinant of food webs and community dynamics 1,2. The increased temperatures associated with the urban-heat-island effect result in increased metabolic costs and are expected to drive shifts to smaller body sizes 3. Urban environments are, however, also characterized by substantial habitat fragmentation 4 , 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 settings 5. 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 networks 1 , such shifts may affect urban ecosystem function. Body size is a fundamental species trait relating to space use and key life-history features such as longevity and fecundity 6. It also drives interspecific relationships, thus affecting ecological network dynamics 1. Size-biased species loss has profound effects on ecosystem function 7,8. Ectotherms rely on ambient conditions to achieve operational body temperatures 9. Because higher ambient temperature increases metabolic rates and the associated costs for a given body size 2 , global climatic warming is expected to drive shifts to communities consisting of smaller species 3. Our planet is urbanizing quickly 10 , which is a primary example of human-induced rapid environmental change. Cities are urban heat islands characterized by increased temperatures that are decades ahead of global averages 11. Not only are cities warmer than surrounding areas, but they also experience extensive fragmentation of (semi-)natural habitats , and both of these effects increase with percentage built-up cover (BUC; a proxy for urbanization) 12,13. This provides an opportunity to study the opposing effects of size-dependent thermal tolerance and dispersal capacity, as larger body size favours dispersal in some, but not all, taxa. Here we test the hypothesis that urbanization causes shifts in community level body size, and that these shifts are dictated by the community specific association between body size and dispersal. We generally expect the urban-heat-island effect to drive shifts to species with smaller body sizes in communities of ectothermic species, in line with Atkinson's temperature-size rule 14. For taxa characterized by a positive association between body size and dispersal, however, we also expect a filtering in favour of larger-bodied species associated with habitat fragmentation 5,15. Filtering for increased mobility has been demonstrated for urban ground beetle and plant communities 16,17. Hence, for taxa characterized by a positive body-size-dispersal link, we predict that the general community-level pattern of smaller species with increasing urbanization may be neutralized or even reversed. To test our hypothesis, we engaged in an analysis of community-level shifts in body size across a broad range of both terrestrial and aquatic taxa along the same systematically sampled urbanization gradients. We studied the direction of change of community-level body size in ten taxa using a replicated, highly standardized and nested sampling design that covers urbanization gradients at seven spatial scales (50-3,200 m radii; Fig. 1). We sampled each taxon at up to 81 sites, sampling 95,001 individuals from 702 species, with species-specific body size varying by a factor of 400 (0.2-80 mm; Extended Data Table 1). Three of the ten groups are characterized by a positive association between body size and dispersal capacity (see Extended Data Table 1). We show that the local temperature of pond, grassland and woodland habitats significantly increases with urbanization (linear mixed regression models, P <0.002; Extended Data Table 2). The intensity of these urban-heat-island effects is consistently larger during night and summer, in accordance with slower night-time city cooling and higher irradiation levels in summer 18 (Fig. 2, Extended Data Fig. 1, Extended Data Table 2). We also show that increased urbanization is linked to significant declines in habitat amount and the patch size of terrestrial habitats, and significant increases in distances among patches for both terrestrial and aquatic habitats (Pearson's r correlations, P ≤ 0.020; Extended Data Fig. 2). Confirming our metabolism-based prediction that interspecific mean body size decreases with increasing temperature, urban communities for four out of the seven taxa (ground spiders, ground beetles, weevils and cladocerans) that did not have a positive size-dispersal link display reduced community-weighted mean body size (CWMBS). For ostracods, bdelloid rotifers and web spiders, no relationship with urbanization is found. By contrast, all three taxa with positive size-dispersal links display increased CWMBS in response to urbanization

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UR - http://www.mendeley.com/research/bodysize-shifts-aquatic-terrestrial-urban-communities

U2 - 10.1038/s41586-018-0140-0

DO - 10.1038/s41586-018-0140-0

M3 - Article

VL - 558

SP - 113

EP - 116

JO - Nature

JF - Nature

SN - 0028-0836

IS - 7708

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Merckx T, Souffreau C, Kaiser A, Baardsen LF, Backeljau T, Bonte D et al. Body-size shifts in aquatic and terrestrial urban communities. Nature. 2018 juin 7;558(7708):113-116. https://doi.org/10.1038/s41586-018-0140-0