Habitat amount, temperature and biotic interactions drive community structure, life-history traits, and performance traits of cavity-nesting bees and wasps and their natural enemies in cities

Urban ecosystems are associated with socio-ecological conditions that can filter and promote taxa. However, the strength of the effect of ecological filtering on biodiversity could vary among biotic and abiotic factors. Here, we investigate the effects of habitat amount, temperature, and host-enemy biotic interactions in shaping communities of cavity-nesting bees and wasps (CNBW) and their natural enemies. We installed trap-nests in 80 sites distributed along urban intensity gradients in 5 European cities (Antwerp, Paris, Poznan, Tartu and Zurich). We quantified the species richness and abundance of CNBW hosts and their natural enemies, as well as two performance traits (survival and parasitism) and two life-history traits (sex ratio and number of offspring per nest for the hosts). We analysed the importance of the abiotic and biotic variables using generalized linear models and multi-model inference. We found that habitat amount and temperature were the main drivers of CNBW host responses, with larger habitat amounts resulting in higher species richness and abundance, and a larger total number of brood cells per nest for both bees and wasps, as well as a larger probability of survival for bees. Conversely, higher local temperatures decreased species richness, abundance, survival rate, number of brood cells per nest, and proportion of females in CNBW hosts. Biotic interactions with natural enemies shaped wasp species richness, with higher levels of parasitism resulting in more wasp species. Similarly, our results showed direct density-dependence between CNBW hosts and their natural enemies. Overall, our study highlights the importance of habitat amount and temperature in shaping urban food webs, through direct effects on hosts responses and the subsequent consequences for their natural enemies. As cities prepare to tackle the future consequences of global change, strategies that make it possible to maintain available habitat and mitigate urban overheating emerge as a key urban adaptation for biodiversity conservation.

[1]  L. Marini,et al.  Temperature and not landscape composition shapes wild bee communities in an urban environment , 2022, Insect Conservation and Diversity.

[2]  P. Theodorou.  The effects of urbanisation on ecological interactions. , 2022, Current opinion in insect science.

[3]  C. Ginzler,et al.  Applying predictive models to study the ecological properties of urban ecosystems: A case study in Zürich, Switzerland , 2021 .

[4]  R. Tinghitella,et al.  Anthropogenic noise affects insect and arachnid behavior, thus changing interactions within and between species. , 2021, Current opinion in insect science.

[5]  R. Samson,et al.  A dataset of the flowering plants (Angiospermae) in urban green areas in five European cities , 2021, Data in brief.

[6]  C. Kueffer,et al.  Promoting wildflower biodiversity in dense and green cities: The important role of small vegetation patches , 2021, Urban Forestry & Urban Greening.

[7]  M. Woyciechowski,et al.  Red mason bee (Osmia bicornis) thermal preferences for nest sites and their effects on offspring survival , 2021, Apidologie.

[8]  Indrajeet Patil,et al.  performance: An R Package for Assessment, Comparison and Testing of Statistical Models , 2021, J. Open Source Softw..

[9]  Eliza M. Grames,et al.  Insect decline in the Anthropocene: Death by a thousand cuts , 2021, Proceedings of the National Academy of Sciences.

[10]  Alice C Hughes,et al.  Global Patterns and Drivers of Bee Distribution , 2020, Current Biology.

[11]  D. Boscolo,et al.  Green patches among a grey patchwork: the importance of preserving natural habitats to harbour cavity-nesting bees and wasps (Hymenoptera) and their natural enemies in urban areas , 2020, Biodiversity and Conservation.

[12]  Xia Li,et al.  High-spatiotemporal-resolution mapping of global urban change from 1985 to 2015 , 2020, Nature Sustainability.

[13]  I. Steffan‐Dewenter,et al.  Climate and food resources shape species richness and trophic interactions of cavity‐nesting Hymenoptera , 2020, Journal of Biogeography.

[14]  M. Moretti,et al.  The origin of urban communities: From the regional species pool to community assemblages in city , 2020, Journal of Biogeography.

[15]  D. Blumstein,et al.  Opinion: Urban Biodiversity and the Importance of Scale. , 2020, Trends in ecology & evolution.

[16]  N. Buchmann,et al.  Multiple plant diversity components drive consumer communities across ecosystems , 2019, Nature Communications.

[17]  I. Perfecto,et al.  Changes in adult sex ratio in wild bee communities are linked to urbanization , 2019, Scientific Reports.

[18]  J. Terborgh,et al.  Tropical forests can maintain hyperdiversity because of enemies , 2018, Proceedings of the National Academy of Sciences.

[19]  Paul R. Martin,et al.  Species interactions limit the occurrence of urban-adapted birds in cities , 2018, Proceedings of the National Academy of Sciences.

[20]  Ulrich Brose,et al.  The biggest losers: habitat isolation deconstructs complex food webs from top to bottom , 2018, bioRxiv.

[21]  S. Frank,et al.  Urban plants and climate drive unique arthropod interactions with unpredictable consequences. , 2018, Current opinion in insect science.

[22]  A. Klein,et al.  Trap nests for bees and wasps to analyse trophic interactions in changing environments—A systematic overview and user guide , 2018, Methods in Ecology and Evolution.

[23]  J. Forrest,et al.  Nesting aggregation as a predictor of brood parasitism in mason bees (Osmia spp.) , 2018 .

[24]  D. Kleijn,et al.  Managing trap‐nesting bees as crop pollinators: Spatiotemporal effects of floral resources and antagonists , 2018 .

[25]  N. Butt,et al.  Opportunities for biodiversity conservation as cities adapt to climate change , 2018 .

[26]  S. Murphy,et al.  Bottom-up vs. top-down effects on terrestrial insect herbivores: a meta-analysis. , 2018, Ecology letters.

[27]  M. Fellowes,et al.  Does urbanization explain differences in interactions between an insect herbivore and its natural enemies and mutualists? , 2018, Urban Ecosystems.

[28]  Casper W. Berg,et al.  glmmTMB Balances Speed and Flexibility Among Packages for Zero-inflated Generalized Linear Mixed Modeling , 2017, R J..

[29]  M. Vilà,et al.  Honeybee spillover reshuffles pollinator diets and affects plant reproductive success , 2017, Nature Ecology & Evolution.

[30]  Mark A. Goddard,et al.  Biodiversity in the city: key challenges for urban green space management , 2017 .

[31]  I. Kühn,et al.  Semi‐natural habitats mitigate the effects of temperature rise on wild bees , 2017 .

[32]  Julia M. Burks,et al.  Local and Landscape Drivers of Parasitoid Abundance, Richness, and Composition in Urban Gardens , 2017, Environmental Entomology.

[33]  A. Klein,et al.  Spillover of trap-nesting bees and wasps in an urban–rural interface , 2014, Journal of Insect Conservation.

[34]  Rudolf P. Rohr,et al.  Plant diversity in a nutshell: testing for small‐scale effects on trap nesting wild bees and wasps , 2014 .

[35]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[36]  Lenore Fahrig,et al.  Rethinking patch size and isolation effects: the habitat amount hypothesis , 2013 .

[37]  W. Kuttler,et al.  Counteracting urban climate change: adaptation measures and their effect on thermal comfort , 2013, Theoretical and Applied Climatology.

[38]  Damaris Zurell,et al.  Collinearity: a review of methods to deal with it and a simulation study evaluating their performance , 2013 .

[39]  T. Oke,et al.  Local Climate Zones for Urban Temperature Studies , 2012 .

[40]  Carsten F. Dormann,et al.  Landscape elements as potential barriers and corridors for bees, wasps and parasitoids , 2011 .

[41]  David R. Anderson,et al.  AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons , 2011, Behavioral Ecology and Sociobiology.

[42]  Alain F. Zuur,et al.  A protocol for data exploration to avoid common statistical problems , 2010 .

[43]  J. Anderies,et al.  Invasion, Competition, and Biodiversity Loss in Urban Ecosystems , 2010 .

[44]  M. Symonds,et al.  A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion , 2010, Behavioral Ecology and Sociobiology.

[45]  Hadley Wickham,et al.  ggplot2 - Elegant Graphics for Data Analysis (2nd Edition) , 2017 .

[46]  T. Tscharntke,et al.  Canopy vs. understory: Does tree diversity affect bee and wasp communities and their natural enemies across forest strata? , 2009 .

[47]  Martine Maron,et al.  Do arthropod assemblages display globally consistent responses to intensified agricultural land use and management , 2008 .

[48]  I. Steffan‐Dewenter,et al.  Do resources or natural enemies drive bee population dynamics in fragmented habitats? , 2008, Ecology.

[49]  Johan Colding,et al.  'ecological land-use complementation' for building resilience in urban ecosystems , 2007 .

[50]  C. Violle,et al.  Let the concept of trait be functional , 2007 .

[51]  Carlos J. Melián,et al.  Food web structure and habitat loss , 2002 .

[52]  Michael P. Hassell,et al.  Host–parasitoid population dynamics , 2000 .

[53]  J. Lawton,et al.  Why More Productive Sites Have More Species: An Experimental Test of Theory Using Tree‐Hole Communities , 1998, The American Naturalist.

[54]  J. Rosenheim.  Density-Dependent Parasitism and the Evolution of Aggregated Nesting in the Solitary Hymenoptera , 1990 .

[55]  M. Hassell.  Patterns of parasitism by insect parasitoids in patchy environments , 1982 .

[56]  Thomas W. Schoener,et al.  Resource Partitioning in Ecological Communities , 1974, Science.

[57]  G. E. Hutchinson,et al.  Homage to Santa Rosalia or Why Are There So Many Kinds of Animals? , 1959, The American Naturalist.