Cryptic eco-evolutionary feedback in the city: Urban evolution of prey dampens the effect of urban evolution of the predator.
Daphnia
Ischnura
cryptic urban eco-evolutionary feedbacks
heatwaves
predator-prey interactions
thermal adaptation
Journal
The Journal of animal ecology
ISSN: 1365-2656
Titre abrégé: J Anim Ecol
Pays: England
ID NLM: 0376574
Informations de publication
Date de publication:
03 2022
03 2022
Historique:
received:
30
03
2021
accepted:
23
09
2021
pubmed:
5
10
2021
medline:
19
3
2022
entrez:
4
10
2021
Statut:
ppublish
Résumé
Most research on eco-evolutionary feedbacks focuses on ecological consequences of evolution in a single species. This ignores the fact that evolution in response to a shared environmental factor in multiple species involved in interactions could alter the net cumulative effect of evolution on ecology. We empirically tested whether urbanization-driven evolution in a predator (nymphs of the damselfly Ischnura elegans) and its prey (the water flea Daphnia magna) jointly shape the outcome of predation under simulated heatwaves. Both interactors show genetic trait adaptation to urbanization, particularly to higher temperatures. We cross-exposed common-garden reared damselflies and Daphnia from replicated urban and rural populations, and quantified predation rates and functional response traits. Urban damselfly nymphs showed higher encounter and predation rates than rural damselflies when exposed to rural prey, but this difference disappeared when they preyed on urban Daphnia. This represents a case of a cryptic evo-to-eco feedback, where the evolution of one species dampens the effects of the evolution of another species on their interaction strength. The effects of evolution of each single species were strong: the scenario in which only the predator or prey was adapted to urbanization resulted in a c. 250% increase in encounter rate and a c. 25% increase in predation rate, compared to the rural predator-rural prey combination. Our results provide unique evidence for eco-evolutionary feedbacks in cities, and underscore the importance of a multi-species approach in eco-evolutionary dynamics research. Onderzoek naar eco-evolutionaire terugkoppelingen focust vaak op de ecologische gevolgen van evolutie in één soort. Bijgevolg negeert men de mogelijkheid dat evolutionaire veranderingen van meerdere interagerende soorten als respons op een gedeelde omgevingsverandering met elkaar kunnen interfereren en zo het netto effect van evolutie op ecologische processen kan veranderen. We testten empirisch of door verstedelijking gedreven evolutie in een predator (larven van de waterjuffer Ischnura elegans) en zijn prooi (de watervlo Daphnia magna) de uitkomst van predatie onder gesimuleerde hittegolven beïnvloedt. Beide interactoren vertonen genetische adaptatie aan de stadsomgeving, meer specifiek de daar voorkomende hogere temperaturen. We stelden waterjuffers en watervlooien, afkomstig van gerepliceerde stedelijke en rurale populaties en opgegroeid in een gestandaardiseerde laboratoriumomgeving, bloot aan elkaar volgens een experimenteel design waarbij alle combinaties van herkomst van prooi en predator werden getest. We kwantificeerden telkens de predatiesnelheid en functionele respons-kenmerken. Stedelijke waterjufferlarven vertoonden een hogere ontmoetings- en predatiesnelheid dan larven afkomstig uit rurale gebieden wanneer ze blootgesteld werden aan rurale Daphnia, maar niet wanneer ze blootgesteld werden aan Daphnia afkomstig uit de stad. Deze bevinding wijst op een cryptische evo-naar-eco terugkoppeling, waarbij evolutie in één van de soorten het effect van evolutie van de andere soort op de sterkte van hun interactie dempt. De effecten van evolutie in elke soort apart waren sterk: de scenario's waarin enkel de predator of de prooi aangepast was aan de stadsomgeving resulteerde in een c. 250% stijging van de ontmoetingssnelheid en een c. 25% verhoging van de predatiesnelheid, in vergelijking met een situatie waarbij een rurale predator met een rurale prooi was gecombineerd. Deze resultaten leveren uniek bewijs voor een eco-evolutionaire terugkoppeling in steden en onderlijnen het belang van een multi-soorten benadering in het onderzoek naar eco-evolutionaire dynamieken.
Autres résumés
Type: Publisher
(dut)
Onderzoek naar eco-evolutionaire terugkoppelingen focust vaak op de ecologische gevolgen van evolutie in één soort. Bijgevolg negeert men de mogelijkheid dat evolutionaire veranderingen van meerdere interagerende soorten als respons op een gedeelde omgevingsverandering met elkaar kunnen interfereren en zo het netto effect van evolutie op ecologische processen kan veranderen. We testten empirisch of door verstedelijking gedreven evolutie in een predator (larven van de waterjuffer Ischnura elegans) en zijn prooi (de watervlo Daphnia magna) de uitkomst van predatie onder gesimuleerde hittegolven beïnvloedt. Beide interactoren vertonen genetische adaptatie aan de stadsomgeving, meer specifiek de daar voorkomende hogere temperaturen. We stelden waterjuffers en watervlooien, afkomstig van gerepliceerde stedelijke en rurale populaties en opgegroeid in een gestandaardiseerde laboratoriumomgeving, bloot aan elkaar volgens een experimenteel design waarbij alle combinaties van herkomst van prooi en predator werden getest. We kwantificeerden telkens de predatiesnelheid en functionele respons-kenmerken. Stedelijke waterjufferlarven vertoonden een hogere ontmoetings- en predatiesnelheid dan larven afkomstig uit rurale gebieden wanneer ze blootgesteld werden aan rurale Daphnia, maar niet wanneer ze blootgesteld werden aan Daphnia afkomstig uit de stad. Deze bevinding wijst op een cryptische evo-naar-eco terugkoppeling, waarbij evolutie in één van de soorten het effect van evolutie van de andere soort op de sterkte van hun interactie dempt. De effecten van evolutie in elke soort apart waren sterk: de scenario's waarin enkel de predator of de prooi aangepast was aan de stadsomgeving resulteerde in een c. 250% stijging van de ontmoetingssnelheid en een c. 25% verhoging van de predatiesnelheid, in vergelijking met een situatie waarbij een rurale predator met een rurale prooi was gecombineerd. Deze resultaten leveren uniek bewijs voor een eco-evolutionaire terugkoppeling in steden en onderlijnen het belang van een multi-soorten benadering in het onderzoek naar eco-evolutionaire dynamieken.
Identifiants
pubmed: 34606084
doi: 10.1111/1365-2656.13601
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
514-526Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2021 British Ecological Society.
Références
Alberti, M., Marzluff, J., & Hunt, V. M. (2017). Urban driven phenotypic changes: Empirical observations and theoretical implications for eco-evolutionary feedback. Philosophical Transactions of the Royal Society B: Biological Sciences, 372. https://doi.org/10.1098/rstb.2016.0029
Bassar, R. D., Marshall, M. C., López-Sepulcre, A., Zandonà, E., Auer, S. K., Travis, J., Pringle, C. M., Flecker, A. S., Thomas, S. A., Fraser, D. F., & Reznick, D. N. (2010). Local adaptation in Trinidadian guppies alters ecosystem processes. Proceedings of the National Academy of Sciences of the United States of America, 107, 3616-3621. https://doi.org/10.1073/pnas.0908023107
Bates, D., Machler, M., Bolker, B., & Walker, S. C. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67, 1-48. https://doi.org/10.18637/jss.v067.i01
Begon, M., Townsend, C. R., & Harper, J. L. (2005). Ecology: From individuals to ecosystems. Wiley-Blackwell.
Brans, K. I., Govaert, L., Engelen, J. M. T., Gianuca, A. T., Souffreau, C., & De Meester, L. (2017). Eco-evolutionary dynamics in urbanized landscapes: Evolution, species sorting and the change in zooplankton body size along urbanization gradients. Philosophical Transactions of the Royal Society B: Biological Sciences, 372(1712), 20160030. https://doi.org/10.1098/rstb.2016.0030
Brans, K. I., Stoks, R., & De Meester, L. (2018). Urbanization drives genetic differentiation in physiology and structures the evolution of pace-of-life syndromes in the water flea Daphnia magna. Proceedings of the Royal Society B: Biological Sciences, 285(1883), 20180169. https://doi.org/10.1098/rspb.2018.0169
Brans, K. I., Govaert, L., & De Meester, L. (2020). Evolutionary dynamics of meta communities in urbanized landscapes. In M. Szulkin, J. Munshi-South, & A. Charmantier (Eds.), Urban Evolutionary Biology (pp. 175-196). Oxford University Press.
Brans, K. I., Tüzün, N., Sentis, A., De Meester, L., & Stoks, R. (2021). Data from: Cryptic eco-evolutionary feedback in the city: Urban evolution of prey dampens the effect of urban evolution of the predator. figshare, https://doi.org/10.6084/m9.figshare.14252948
Brans, K. I., & De Meester, L. (2018). City life on fast lanes: Urbanization induces an evolutionary shift towards a faster lifestyle in the water flea Daphnia. Functional Ecology, 32(9), 2225-2240. https://doi.org/10.1111/1365-2435.13184
Brans, K. I., Engelen, J. M. T., Souffreau, C., & De Meester, L. (2018). Urban hot-tubs: Local urbanization has profound effects on average and extreme temperatures in ponds. Landscape and Urban Planning, 176, 22-29. https://doi.org/10.1016/j.landurbplan.2018.03.013
Brans, K. I., Jansen, M., Vanoverbeke, J., Tüzün, N., Stoks, R., & De Meester, L. (2017). The heat is on: Genetic adaptation to urbanization mediated by thermal tolerance and body size. Global Change Biology, 23, 5218-5227. https://doi.org/10.1111/gcb.13784
Cheptou, P.-O., Hargreaves, A. L., Bonte, D., & Jacquemyn, H. (2017). Adaptation to fragmentation: Evolutionary dynamics driven by human influences. Philosophical Transactions of the Royal Society B: Biological Sciences, 372, 20160037. https://doi.org/10.1098/rstb.2016.0037
Chislock, M. F., Sarnelle, O., Jernigan, L. M., & Wilson, A. E. (2013). Do high concentrations of microcystin prevent Daphnia control of phytoplankton? Water Research, 47, 1960-1971. https://doi.org/10.1016/j.watres.2012.12.038
Cortez, M. H. (2018). Genetic variation determines which feedbacks drive and alter predator-prey eco-evolutionary cycles. Ecological Monographs, 88, 353-371. https://doi.org/10.1002/ecm.1304
Daufresne, M., Lengfellner, K., & Sommer, U. (2009). Global warming benefits the small in aquatic ecosystems. Proceedings of the National Academy of Sciences of the United States of America, 106, 12788-12793. https://doi.org/10.1073/pnas.0902080106
De Block, M., Pauwels, K., Van Den Broeck, M., De Meester, L., & Stoks, R. (2013). Local genetic adaptation generates latitude-specific effects of warming on predator-prey interactions. Global Change Biology, 19, 689-696. https://doi.org/10.1111/gcb.12089
De Meester, L., Brans, K. I., Govaert, L., Souffreau, C., Mukherjee, S., Vanvelk, H., Korzeniowski, K., Kilsdonk, L., Decaestecker, E., Stoks, R., & Urban, M. C. (2019). Analysing eco-evolutionary dynamics-The challenging complexity of the real world. Functional Ecology, 33(1), 43-59. https://doi.org/10.1111/1365-2435.13261
Decaestecker, E., Gaba, S., Raeymaekers, J. A. M., Stoks, R., Van Kerckhoven, L., Ebert, D., & De Meester, L. (2007). Host-parasite ‘Red Queen’ dynamics archived in pond sediment. Nature, 450, 870-873. https://doi.org/10.1038/nature06291
Dell, A. I., Pawar, S., & Savage, V. M. (2014). Temperature dependence of trophic interactions are driven by asymmetry of species responses and foraging strategy. Journal of Animal Ecology, 83, 70-84. https://doi.org/10.1111/1365-2656.12081
Des Roches, S., Brans, K. I., Lambert, M. R., Rivkin, L. R., Savage, A. M., Schell, C. J., Correa, C., De Meester, L., Diamond, S. E., Grimm, N. B., Harris, N. C., Govaert, L., Hendry, A. P., Johnson, M. T. J., Munshi-South, J., Palkovacs, E. P., Szulkin, M., Urban, M. C., Verrelli, B. C., & Alberti, M. (2021). Socio-eco-evolutionary dynamics in cities. Evolutionary Applications, 14, 248-267. https://doi.org/10.1111/eva.13065
Diamond, S. E., Chick, L., Perez, A., Strickler, S. A., & Martin, R. A. (2017). Rapid evolution of ant thermal tolerance across an urban-rural temperature cline. Biological Journal of the Linnean Society, 121, 248-257. https://doi.org/10.1093/biolinnean/blw047
Ellner, S. P., Geber, M. A., & Hairston, N. G. (2011). Does rapid evolution matter? Measuring the rate of contemporary evolution and its impacts on ecological dynamics. Ecology Letters, 14, 603-614. https://doi.org/10.1111/j.1461-0248.2011.01616.x
Engelen, J. M. T. (2017). The impact of urbanization on ponds and their zooplankton communities (PhD dissertation). KU Leuven.
Gerritsen, J., & Strickler, J. R. (1977). Encounter probabilities and community structure in zooplankton: A mathematical model. Journal of the Fisheries Research Board of Canada, 34, 73-82. https://doi.org/10.1139/f77-008
Gianuca, A. T., Pantel, J. H., & De Meester, L. (2016). Disentangling the effect of body size and phylogenetic distances on zooplankton top-down control of algae. Proceedings of the Royal Society B: Biological Sciences, 283, 20160487. https://doi.org/10.1098/rspb.2016.0487
Grimm, N. B., Foster, D., Groffman, P., Grove, J. M., Hopkinson, C. S., Nadelhoffer, K. J., Pataki, D. E., & Peters, D. P. C. (2008). The changing landscape: Ecosystem responses to urbanization and pollution across climatic and societal gradients. Frontiers in Ecology and the Environment, 6, 264-272. https://doi.org/10.1890/070147
Hairston, N. G., Ellner, S. P., Geber, M. A., Yoshida, T., & Fox, J. A. (2005). Rapid evolution and the convergence of ecological and evolutionary time. Ecology Letters, 8, 1114-1127. https://doi.org/10.1111/j.1461-0248.2005.00812.x
Hendry, A. P. (2017). Eco-evolutionary dynamics. Princeton University Press.
Hendry, A. P., & Kinnison, M. T. (1999). Perspective: The pace of modern life: Measuring rates of contemporary microevolution. Evolution, 53(6), 1637-1653. https://doi.org/10.1111/j.1558-5646.1999.tb04550.x
IBZ. (2021). Bevolkingscijfer per provincie en per gemeente op 1 Januari 2021, Koninkrijk België - Chiffres de la population par province et par commune, a la date du 1er Janvier 2021, Royaume de Belgique. Retrieved from www.ibz.rrn.fgov.be
Jeschke, J. M., Kopp, M., & Tollrian, R. (2002). Predator functional responses: Discriminating between handling time and digesting prey. Ecological Monographs, 72(1), 95-112. https://doi.org/10.1890/0012-9615(2002)072[0095:pfrdbh]2.0.co;2
Johnson, M. T. J., & Munshi-South, J. (2017). Evolution of life in urban environments. Science, 358. https://doi.org/10.1126/science.aam8327
Kinnison, M. T., Hairston Jr, N. G., & Hendry, A. P. (2015). Cryptic eco-evolutionary dynamics. Annals of the New York Academy of Sciences, 1360, 120-144. https://doi.org/10.1111/nyas.12974
Kuznetsova, A., Brockhoff, P. B., & Christensen, R. H. B. (2017). lmerTest package: Tests in linear mixed effects models. Journal of Statistical Software, 82(13). https://doi.org/10.18637/jss.v082.i13
Lauwaet, D., De Ridder, K., Maiheu, B., Hooyberghs, H., & Lefebre, F. (2018). Uitbreiding en validatie indicator hitte-eilandeffect, studie uitgevoerd in opdracht van de Vlaamse Milieumaatschappij, MIRA, MIRA/2018/01, VITO.
Lenth, R. (2020). emmeans: Estimated marginal means, aka least-squares means. R Package version 1.15-15. Retrieved from https://github.com/rvlenth/emmeans
LRD. (2013). Large-scale Reference Database, an object-oriented reference map of Flanders. Flanders Information Agency. Retrieved from https://overheid.vlaanderen.be/en/producten-diensten/large-scale-reference-database-lrd
McCauley, E., Wilson, W. G., & de Roos, A. M. (1993). Dynamics of age-structured and spatially structured predator-prey interactions: Individual-based models and population-level formulations. The American Naturalist, 142, 412-442. https://doi.org/10.1086/285547
Nadeau, C. P., & Urban, M. C. (2019). Eco-evolution on the edge during climate change. Ecography, 42, 1280-1297. https://doi.org/10.1111/ecog.04404
Novak, M., & Wootton, J. T. (2008). Estimating nonlinear interaction strengths: An observation-based method for species-rich food webs. Ecology, 89(8), 2083-2089. https://doi.org/10.1890/08-0033.1
Okuyama, T. (2010). Prey density-dependent handling time in a predator-prey model. Community Ecology, 11, 91-96. https://doi.org/10.1556/ComEc.11.2010.1.13
Op de Beeck, L., Verheyen, J., & Stoks, R. (2017). Integrating both interaction pathways between warming and pesticide exposure on upper thermal tolerance in high- and low-latitude populations of an aquatic insect. Environmental Pollution, 224, 714-721. https://doi.org/10.1016/j.envpol.2016.11.014
Palkovacs, E. P., & Post, D. M. (2008). Eco-evolutionary interactions between predators and prey: Can predator-induced changes to prey communities feed back to shape predator foraging traits? Evolutionary Ecology Research, 10, 699-720.
Pantel, J. H., Duvivier, C., & Meester, L. D. (2015). Rapid local adaptation mediates zooplankton community assembly in experimental mesocosms. Ecology Letters, 18, 992-1000. https://doi.org/10.1111/ele.12480
Pawar, S., Dell, A. I., & Savage, V. M. (2012). Dimensionality of consumer search space drives trophic interaction strengths. Nature, 486, 485-489. https://doi.org/10.1038/nature11131
Piano, E., Souffreau, C., Merckx, T., Baardsen, L. F., Backeljau, T., Bonte, D., Brans, K. I., Cours, M., Dahirel, M., Debortoli, N., Decaestecker, E., De Wolf, K., Engelen, J. M. T., Fontaneto, D., Gianuca, A. T., Govaert, L., Hanashiro, F. T. T., Higuti, J., Lens, L., … Hendrickx, F. (2020). Urbanization drives cross-taxon declines in abundance and diversity at multiple spatial scales. Global Change Biology, 26, 1196-1211. https://doi.org/10.1111/gcb.14934
Pickett, S. T. A., Cadenasso, M. L., Childers, D. L., Mcdonnell, M. J., & Zhou, W. (2016). Evolution and future of urban ecological science: Ecology in, of, and for the city. Ecosystem Health and Sustainability, 2, e01229. https://doi.org/10.1002/ehs2.1229
R Core Team. (2018). R: A language and environment for statistical computing. Retrieved from https://www.R-project.org
Réale, D., Garant, D., Humphries, M. M., Bergeron, P., Careau, V., & Montiglio, P.-O. (2010). Personality and the emergence of the pace-of-life syndrome concept at the population level. Philosophical Transactions of the Royal Society B: Biological Sciences, 365, 4051-4063. https://doi.org/10.1098/rstb.2010.0208
Sentis, A., Hemptinne, J.-L., & Brodeur, J. (2013a). Effects of simulated heat waves on an experimental plant-herbivore-predator food chain. Global Change Biology, 19, 833-842. https://doi.org/10.1111/gcb.12094
Sentis, A., Hemptinne, J.-L., & Brodeur, J. (2013b). Parsing handling time into its components: Implications for responses to a temperature gradient. Ecology, 94, 1675-1680. https://doi.org/10.1890/12-2107.1
Sentis, A., Hemptinne, J.-L., & Brodeur, J. (2017). Non-additive effects of simulated heat waves and predators on prey phenotype and transgenerational phenotypic plasticity. Global Change Biology, 23, 4598-4608. https://doi.org/10.1111/gcb.13674
Shama, L. N. S., Campero-paz, M., Wegner, K. M., De Block, M., & Stoks, R. (2011). Latitudinal and voltinism compensation shape thermal reaction norms for growth rate. Molecular Ecology, 20, 2929-2941. https://doi.org/10.1111/j.1365-294X.2011.05156.x
Sinclair, B. J., Williams, C. M., & Terblanche, J. S. (2012). Variation in thermal performance among insect populations. Physiological and Biochemical Zoology, 85, 594-606. https://doi.org/10.1086/665388
Stoks, R., Verheyen, J., Van Dievel, M., & Tüzün, N. (2017). Daily temperature variation and extreme high temperatures drive performance and biotic interactions in a warming world. Current Opinion in Insect Science, 23, 35-42. https://doi.org/10.1016/j.cois.2017.06.008
Szulkin, M., Munshi-South, J., & Charmantier, A. (2020). Urban evolutionary biology. Oxford University Press.
Thompson, D. J. (1978). Prey size selection by larvae of the damselfly Ischnura elegans (Odonata). Journal of Animal Ecology, 47, 769-785. https://doi.org/10.2307/3670
Thompson, J. N. (2005). The geographic mosaic of coevolution. University of Chicago Press.
Thompson, P. L., & Fronhofer, E. A. (2019). The conflict between adaptation and dispersal for maintaining biodiversity in changing environments. Proceedings of the National Academy of Sciences of the United States of America, 116, 21061-21067. https://doi.org/10.1073/pnas.1911796116
Tüzün, N., Op de Beeck, L., Brans, K. I., Janssens, L., & Stoks, R. (2017). Microgeographic differentiation in thermal performance curves between rural and urban populations of an aquatic insect. Evolutionary Applications, 10, 1067-1075. https://doi.org/10.1111/eva.12512
Tüzün, N., & Stoks, R. (2018). Evolution of geographic variation in thermal performance curves in the face of climate change and implications for biotic interactions. Current Opinion in Insect Science, 29, 78-84. https://doi.org/10.1016/j.cois.2018.07.004
Tüzün, N., & Stoks, R. (2021). Lower bioenergetic costs but similar immune responsiveness under a heatwave in urban compared to rural damselflies. Evolutionary Applications, 14, 24-35. https://doi.org/10.1111/eva.13041
Twardochleb, L. A., Treakle, T. C., & Zarnetske, P. L. (2020). Foraging strategy mediates ectotherm predator-prey responses to climate warming. Ecology, 101, e03146. https://doi.org/10.1002/ecy.3146
Urban, M. C., Bocedi, G., Hendry, A. P., Mihoub, J.-B., Peer, G., Singer, A., Bridle, J. R., Crozier, L. G., De Meester, L., Godsoe, W., Gonzalez, A., Hellmann, J. J., Holt, R. D., Huth, A., Johst, K., Krug, C. B., Leadley, P. W., Palmer, S. C. F., Pantel, J. H., … Travis, J. M. J. (2016). Improving the forecast for biodiversity under climate change. Science, 353. https://doi.org/10.1126/science.aad8466
Urban, M. C., Strauss, S. Y., Pelletier, F., Palkovacs, E. P., Leibold, M. A., Hendry, P. A., De Meester, L., Carlson, S. M., Angert, A. L., & Giery, S. T. (2020). Evolutionary origins for ecological patterns in space. Proceedings of the National Academy of Sciences of the United States of America, 117, 17482-17490. https://doi.org/10.1073/pnas.1918960117
Vanoverbeke, J., Urban, M. C., & Meester, L. (2016). Community assembly is a race between immigration and adaptation: Eco-evolutionary interactions across spatial scales. Ecography, 39, 858-870. https://doi.org/10.1111/ecog.01394
Waajen, G. W. A. M., Faassen, E. J., & Lürling, M. (2014). Eutrophic urban ponds suffer from cyanobacterial blooms: Dutch examples. Environmental Science and Pollution Research, 21, 9983-9994. https://doi.org/10.1007/s11356-014-2948-y
Werner, E. E., & Anholt, B. R. (1993). Ecological consequences of the trade-off between growth and mortality rates mediated by foraging activity. The American Naturalist, 142, 242-272. https://doi.org/10.1086/285537
Whitehead, A., Clark, B. W., Reid, N. M., Hahn, M. E., & Nacci, D. (2017). When evolution is the solution to pollution: Key principles, and lessons from rapid repeated adaptation of killifish (Fundulus heteroclitus) populations. Evolutionary Applications, 10(8), 762-783. https://doi.org/10.1111/eva.12470
Wouters, H., De Ridder, K., Poelmans, L., Willems, P., Brouwers, J., Hosseinzadehtalaei, P., Tabari, H., Vanden Broucke, S., van Lipzig, N. P. M., & Demuzere, M. (2017). Heat stress increase under climate change twice as large in cities as in rural areas: A study for a densely populated midlatitude maritime region. Geophysical Research Letters, 44, 8997-9007. https://doi.org/10.1002/2017GL074889
Yoshida, T., Ellner, S. P., Jones, L. E., Bohannan, B. J. M., Lenski, R. E., & Hairston, N. G. (2007). Cryptic population dynamics: Rapid evolution masks trophic interactions. PLoS Biology, 5, 1868-1879. https://doi.org/10.1371/journal.pbio.0050235