Large uncertainty in trait responses across insects among overall declines in a subtropical city
Corresponding Author
Nicholas A. Federico
Florida Museum of Natural History, University of Florida, Gainesville, Florida, USA
Herbert Wertheim College of Engineering, University of Florida, Gainesville, Florida, USA
Correspondence
Nicholas A. Federico and Michael W. Belitz, Florida Museum of Natural History, University of Florida, Dickinson Hall, Museum Road, Gainesville, FL 32611, USA.
Email: [email protected] and [email protected]
Contribution: Conceptualization, Investigation, Funding acquisition, Writing - original draft, Writing - review & editing, Visualization, Validation, Methodology, Software, Formal analysis, Project administration, Resources, Data curation
Search for more papers by this authorRobert P. Guralnick
Florida Museum of Natural History, University of Florida, Gainesville, Florida, USA
Contribution: Writing - review & editing, Resources, Supervision, Conceptualization
Search for more papers by this authorCorresponding Author
Michael W. Belitz
Florida Museum of Natural History, University of Florida, Gainesville, Florida, USA
Correspondence
Nicholas A. Federico and Michael W. Belitz, Florida Museum of Natural History, University of Florida, Dickinson Hall, Museum Road, Gainesville, FL 32611, USA.
Email: [email protected] and [email protected]
Contribution: Conceptualization, Investigation, Writing - original draft, Writing - review & editing, Visualization, Validation, Methodology, Software, Formal analysis, Project administration, Supervision, Data curation
Search for more papers by this authorCorresponding Author
Nicholas A. Federico
Florida Museum of Natural History, University of Florida, Gainesville, Florida, USA
Herbert Wertheim College of Engineering, University of Florida, Gainesville, Florida, USA
Correspondence
Nicholas A. Federico and Michael W. Belitz, Florida Museum of Natural History, University of Florida, Dickinson Hall, Museum Road, Gainesville, FL 32611, USA.
Email: [email protected] and [email protected]
Contribution: Conceptualization, Investigation, Funding acquisition, Writing - original draft, Writing - review & editing, Visualization, Validation, Methodology, Software, Formal analysis, Project administration, Resources, Data curation
Search for more papers by this authorRobert P. Guralnick
Florida Museum of Natural History, University of Florida, Gainesville, Florida, USA
Contribution: Writing - review & editing, Resources, Supervision, Conceptualization
Search for more papers by this authorCorresponding Author
Michael W. Belitz
Florida Museum of Natural History, University of Florida, Gainesville, Florida, USA
Correspondence
Nicholas A. Federico and Michael W. Belitz, Florida Museum of Natural History, University of Florida, Dickinson Hall, Museum Road, Gainesville, FL 32611, USA.
Email: [email protected] and [email protected]
Contribution: Conceptualization, Investigation, Writing - original draft, Writing - review & editing, Visualization, Validation, Methodology, Software, Formal analysis, Project administration, Supervision, Data curation
Search for more papers by this authorAbstract
- Continued and rapid development of urban environments presents many challenges to organisms living in and around cities. Insects are among the most abundant and diverse class of animals but surprisingly little is known about how most species respond to urbanisation across clades with varying life histories, especially in the subtropics and tropics.
- In this study, we sample insect abundance and diversity across an urbanisation gradient in a subtropical region to assess the impact of urbanisation on 43 phototactic species of insects representing eight distinct orders. We also attempted to determine which life history traits best explain how species respond to urbanisation.
- We predicted an overall loss of abundance and richness with increasing urbanisation, with smaller, generalist species being the least impacted. We also predicted that species with above ground larval habitats would be less affected by urbanisation.
- Overall, urban development decreased both species richness and the abundance of individuals per order, with abundance being most reduced for Hymenoptera but least reduced for Coleoptera. At a species-specific level, urban development negatively impacted most but not all species, although uncertainty around these estimates was high. We did not identify key traits that determined a species' sensitivity to urbanisation.
- Our results showcase that urbanisation may impact ecosystem function given overall reduction in the number of individual insects per order, despite wide variability in species-specific responses. Our study also emphasises the importance of species selection when designing studies that examine responses of multiple taxa across an environmental gradient.
CONFLICT OF INTEREST STATEMENT
The authors declare no conflicts of interest.
Open Research
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are openly available in InsectUrbanization: Code for Manuscript Re-Submission at https://doi.org/10.5281/zenodo.10419482.
Supporting Information
Filename | Description |
---|---|
icad12731-sup-0001-TableS1.xlsxExcel 2007 spreadsheet , 16.9 KB | Table S1. Order abundance, species abundance, urbanization levels, and traits. |
icad12731-sup-0002-Supinfo01.docxWord 2007 document , 1.2 MB | Figure S1. Graphical posterior predictive checks of species richness model. Figure S2. Graphical posterior predictive checks of mode estimating order-specific abundance. Figure S3. Graphical posterior predictive checks of model estimating species-specific abundance. Figure S4. Estimated response of total abundance across an urban development gradient. Figure S5. Community and order-level effects of urban development on abundance per order after removing the most abundant species from the dataset. A) The community-level effect of urban development on abundance per order is shown by the grey vertical line with grey dotted lines showing 95% BCI. The posterior distribution of order-specific responses to urban development are shown with the dot representing the mean estimate and the error bars displaying 95% BCI. B) Community response of pooled abundance per order to urban development with 95% BCI. Each coloured point represents the abundance of an order at a site. Figure S6. Posterior distributions of Bayesian hierarchical model estimating species-specific abundance per site when the most abundant species is removed from the dataset. The left panel of the figure shows response of insect abundance to life-history traits. The right panel of the figure shows the response of insect abundance to urban development (last row) and the interactions between development and traits. Coefficient estimates with 95% Bayesian credible intervals that encompass zero are shaded in grey, while those with 95% BCI that do not encompass zero are purple. Table S2.1. Richness model coefficient estimates. Table S2.2. Fixed effect coefficient estimates of model estimating order-specific abundance. Table S2.3. Fixed effect coefficient estimates of model estimating species-specific abundance. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- Altermatt, F. & Ebert, D. (2016) Reduced flight-to-light behaviour of moth populations exposed to long-term urban light pollution. Biology Letters, 12, 20160111.
- Baeumler, A., D'Aoust, O., Das, M.B., Gapihan, A., Soraya, G., Lakovits, C. et al. (2021) Demographic trends and urbanization. Washington, DC: World Bank.
- Baldock, K.C.R., Goddard, M.A., Hicks, D.M., Kunin, W.E., Mitschunas, N., Osgathorpe, L.M. et al. (2015) Where is the UK's pollinator biodiversity? The importance of urban areas for flower-visiting insects. Proceedings of the Royal Society B: Biological Sciences, 282, 20142849.
- Belitz, M.W., Sawyer, A., Hendrick, L., Kawahara, A. & Guralnick, R.P. (2023) Substantial urbanization-driven declines of larval and adult moths in a subtropical environment. biorRxiv.
- Betts, M.G., Wolf, C., Pfeifer, M., Banks-Leite, C., Arroyo-Rodríguez, V., Ribeiro, D.B. et al. (2019) Extinction filters mediate the global effects of habitat fragmentation on animals. Science, 366, 1236–1239.
- Bürkner, P.-C. (2017) brms: an R package for Bayesian multilevel models using Stan. Journal of Statistical Software, 80, 1–28.
- Callaghan, C.T., Bowler, D.E. & Pereira, H.M. (2021) Thermal flexibility and a generalist life history promote urban affinity in butterflies. Global Change Biology, 27, 3532–3546.
- Camacho, L.F., Barragán, G. & Espinosa, S. (2021) Local ecological knowledge reveals combined landscape effects of light pollution, habitat loss, and fragmentation on insect populations. Biological Conservation, 262, 109311.
- Chatelain, M., Rüdisser, J. & Traugott, M. (2023) Urban-driven decrease in arthropod richness and diversity associated with group-specific changes in arthropod abundance. Frontiers in Ecology and Evolution, 11, 1–16.
- Chust, G., Pretus, J.L., Ducrot, D. & Ventura, D. (2004) Scale dependency of insect assemblages in response to landscape pattern. Landscape Ecology, 19, 41–57.
- Clergeau, P., Jokimaki, J. & Snep, R. (2006) Using hierarchical levels for urban ecology. Trends in Ecology & Evolution, 21, 660–661.
- Coleman, D., Gallagher, R.V., Falster, D., Sauquet, H. & Wenk, E. (2023) A workflow to create trait databases from collections of textual taxonomic descriptions. Ecological Informatics, 78, 102312.
- Cranshaw, W. & Shetlar, D. (2017) Garden insects of North America: the ultimate guide to backyard bugs. New Jersey: Princeton University Press.
10.2307/j.ctt1qft28g Google Scholar
- Di Cecco, G.J., Barve, V., Belitz, M.W., Stucky, B.J., Guralnick, R.P. & Hurlbert, A.H. (2021) Observing the observers: how participants contribute data to iNaturalist and implications for biodiversity science. Bioscience, 71, 1179–1188.
- Diamond, S.E., Bellino, G. & Deme, G.G. (2023) Urban insect bioarks of the 21st century. Current Opinion in Insect Science, 57, 101028.
- Faeth, S.H., Bang, C. & Saari, S. (2011) Urban biodiversity: patterns and mechanisms. Annals of the New York Academy of Sciences, 1223, 69–81.
- Fenoglio, M.S., Rossetti, M.R. & Videla, M. (2020) Negative effects of urbanization on terrestrial arthropod communities: a meta-analysis. Global Ecology and Biogeography, 29, 1412–1429.
- Fick, S.E. & Hijmans, R.J. (2017) WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology, 37, 4302–4315.
- Gaona, F.P., Iñiguez-Armijos, C., Brehm, G., Fiedler, K. & Espinosa, C.I. (2021) Drastic loss of insects (Lepidoptera: Geometridae) in urban landscapes in a tropical biodiversity hotspot. Journal of Insect Conservation, 25, 395–405.
- GBIF.org. (10 May 2022) GBIF occurrence download. https://doi.org/10.15468/dl.azpa7m
10.15468/dl.azpa7m Google Scholar
- Geslin, B., Le Féon, V., Folschweiller, M., Flacher, F., Carmignac, D., Motard, E. et al. (2016) The proportion of impervious surfaces at the landscape scale structures wild bee assemblages in a densely populated region. Ecology and Evolution, 6, 6599–6615.
- González-Césped, C., Alaniz, A.J., Vergara, P.M., Chiappa, E., Zamorano, J. & Mandujano, V. (2021) Effects of urban environmental conditions and landscape structure on taxonomic and functional groups of insects. Urban Forestry & Urban Greening, 58, 126902.
- Grenis, K., Nufio, C., Wimp, G. & Murphy, S. (2023) Does artificial light at night alter moth community composition? Philosophical Transactions of the Royal Society B: Biological Sciences, 378, 20220365.
- Grimm, N.B., Faeth, S.H., Golubiewski, N.E., Redman, C.L., Wu, J., Bai, X. et al. (2008) Global change and the ecology of cities. Science, 319, 756–760.
- Hahs, A.K., Fournier, B., Aronson, M.F.J., Nilon, C.H., Herrera-Montes, A., Salisbury, A.B. et al. (2023) Urbanisation generates multiple trait syndromes for terrestrial animal taxa worldwide. Nature Communications, 14, 4751.
- Hölker, F., Wolter, C., Perkin, E.K. & Tockner, K. (2010) Light pollution as a biodiversity threat. Trends in Ecology & Evolution, 25, 681–682.
- Homer, C., Dewitz, J., Jin, S., Xian, G., Costello, C., Danielson, P. et al. (2020) Conterminous United States land cover change patterns 2001–2016 from the 2016 National Land Cover Database. ISPRS Journal of Photogrammetry and Remote Sensing, 162, 184–199.
- Iserhard, C.A., Duarte, L., Seraphim, N. & Freitas, A.V.L. (2019) How urbanization affects multiple dimensions of biodiversity in tropical butterfly assemblages. Biodiversity and Conservation, 28, 621–638.
- Jackson, H.B. & Fahrig, L. (2012) What size is a biologically relevant landscape? Landscape Ecology, 27, 929–941.
- Kay, M. (12 August 2023) tidybayes: tidy data and geoms for Bayesian models. Zenodo.
- Lagucki, E., Burdine, J.D. & McCluney, K.E. (2017) Urbanization alters communities of flying arthropods in parks and gardens of a medium-sized city. PeerJ, 5, e3620.
- Larson, D.J., Alarie, Y., Roughley, R.E. & Nilsson, A.N. (2001) Predaceous diving beetles (Coleoptera: Dytiscidae) of the Nearctic region, with emphasis on the fauna of Canada and Alaska. Annals of the Entomological Society of America, 94, 769–770.
10.1603/0013-8746(2001)094[0769:PDBCDO]2.0.CO;2 Google Scholar
- Li, D. & Ives, A.R. (2017) The statistical need to include phylogeny in trait-based analyses of community composition. Methods in Ecology and Evolution, 8, 1192–1199.
- Liao, W. & Lin, H. (2024) Urbanisation drivers inter- and intraspecific variation in flight-related morphological traits of aquatic insects at different landscape scales. Insect Conservation and Diversity, 17, 287–303.
- Lizée, M.-H., Mauffrey, J.-F., Tatoni, T. & Deschamps-Cottin, M. (2011) Monitoring urban environments on the basis of biological traits. Ecological Indicators, 11, 353–361.
- Magura, T., Nagy, D. & Tóthmérész, B. (2013) Rove beetles respond heterogeneously to urbanization. Journal of Insect Conservation, 17, 715–724.
- McDonnell, M.J. & Hahs, A.K. (2015) Adaptation and adaptedness of organisms to urban environments. Annual Review of Ecology, Evolution, and Systematics, 46, 261–280.
- Menberg, K., Bayer, P., Zosseder, K., Rumohr, S. & Blum, P. (2013) Subsurface urban heat islands in German cities. The Science of the Total Environment, 442, 123–133.
- Merckx, T., Kaiser, A. & Van Dyck, H. (2018) Increased body size along urbanization gradients at both community and intraspecific level in macro-moths. Global Change Biology, 24, 3837–3848.
- Merckx, T., Souffreau, C., Kaiser, A., Baardsen, L.F., Backeljau, T., Bonte, D. et al. (2018) Body-size shifts in aquatic and terrestrial urban communities. Nature, 558, 113–116.
- Merckx, T. & Van Dyck, H. (2019) Urbanization-driven homogenization is more pronounced and happens at wider spatial scales in nocturnal and mobile flying insects. Global Ecology and Biogeography, 28, 1440–1455.
- Möglich, J.M., Lampe, P., Fickus, M., Younis, S., Gottwald, J., Nauss, T. et al. (2023) Towards reliable estimates of abundance trends using automated non-lethal moth traps. Insect Conservation and Diversity, 16, 539–549.
- Montgomery, G.A., Dunn, R.R., Fox, R., Jongejans, E., Leather, S.R., Saunders, M.E. et al. (2020) Is the insect apocalypse upon us? How to find out. Biological Conservation, 241, 108327.
- Pagel, M. (1999) Inferring the historical patterns of biological evolution. Nature, 401, 877–884.
- Piano, E., De Wolf, K., Bona, F., Bonte, D., Bowler, D.E., Isaia, M. et al. (2017) Urbanization drives community shifts towards thermophilic and dispersive species at local and landscape scales. Global Change Biology, 23, 2554–2564.
- Piano, E., Souffreau, C., Merckx, T., Baardsen, L.F., Backeljau, T., Bonte, D. et al. (2020) Urbanization drives cross-taxon declines in abundance and diversity at multiple spatial scales. Global Change Biology, 26, 1196–1211.
- R Core Team. (2021) R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
- Raupp, M.J., Shrewsbury, P.M. & Herms, D.A. (2010) Ecology of herbivorous arthropods in urban landscapes. Annual Review of Entomology, 55, 19–38.
- Rocha-Ortega, M. & Castaño-Meneses, G. (2015) Effects of urbanization on the diversity of ant assemblages in tropical dry forests, Mexico. Urban Ecosystems, 18, 1373–1388.
- Rocha-Ortega, M., Rodriguez, P. & Córdoba-Aguilar, A. (2021) Geographical, temporal and taxonomic biases in insect GBIF data on biodiversity and extinction. Ecological Entomology, 46, 718–728.
- Schmitt, L. & Burghardt, K.T. (2021) Urbanization as a disrupter and facilitator of insect herbivore behaviors and life cycles. Current Opinion in Insect Science, 45, 97–105.
- Schowalter, T.D., Noriega, J.A. & Tscharntke, T. (2018) Insect effects on ecosystem services—introduction. Basic and Applied Ecology, 26, 1–7.
- Secondi, J., Davranche, A., Théry, M., Mondy, N. & Lengagne, T. (2020) Assessing the effects of artificial light at night on biodiversity across latitude—current knowledge gaps. Global Ecology and Biogeography, 29, 404–419.
- Shirey, V., Belitz, M.W., Barve, V. & Guralnick, R. (2021) A complete inventory of North American butterfly occurrence data: narrowing data gaps, but increasing bias. Ecography, 44, 537–547.
- Simkin, R.D., Seto, K.C., McDonald, R.I. & Jetz, W. (2022) Biodiversity impacts and conservation implications of urban land expansion projected to 2050. Proceedings of the National Academy of Sciences, 119, e2117297119.
- Slade, E.M. & Ong, X.R. (2023) The future of tropical insect diversity: strategies to fill data and knowledge gaps. Current Opinion in Insect Science, 58, 101063.
- Stork, N.E. (2018) How many species of insects and other terrestrial arthropods are there on earth? Annual Review of Entomology, 63, 31–45.
- Straka, T.M., von der Lippe, M., Voigt, C.C., Gandy, M., Kowarik, I. & Buchholz, S. (2021) Light pollution impairs urban nocturnal pollinators but less so in areas with high tree cover. The Science of the Total Environment, 778, 146244.
- Theodorou, P. (2022) The effects of urbanisation on ecological interactions. Current Opinion in Insect Science, 52, 100922.
- Theodorou, P., Radzevičiūtė, R., Lentendu, G., Kahnt, B., Husemann, M., Bleidorn, C. et al. (2020) Urban areas as hotspots for bees and pollination but not a panacea for all insects. Nature Communications, 11, 576.
- United Nations. (2018) World economic situation and prospects 2018.
- Vaz, S., Manes, S., Khattar, G., Mendes, M., Silveira, L., Mendes, E. et al. (2023) Global meta-analysis of urbanization stressors on insect abundance, richness, and traits. Science of the Total Environment, 903, 165967.
- Wagner, D.L., Grames, E.M., Forister, M.L., Berenbaum, M.R. & Stopak, D. (2021) Insect decline in the Anthropocene: death by a thousand cuts. Proceedings of the National Academy of Sciences, 118, e2023989118.
- Weisser, W., Blüthgen, N., Staab, M., Achury, R. & Müller, J. (2023) Experiments are needed to quantify the main causes of insect decline. Biology Letters, 19, 20220500.
- Wenzel, A., Grass, I., Belavadi, V.V. & Tscharntke, T. (2020) How urbanization is driving pollinator diversity and pollination—a systematic review. Biological Conservation, 241, 108321.
- White, P.J.T., Glover, K., Stewart, J. & Rice, A. (2016) The technical and performance characteristics of a low-cost, simply constructed, black light moth trap. Journal of Insect Science, 16, 25.
- Wickham, H., Averick, M., Bryan, J., Chang, W., McGowan, L.D., François, R. et al. (2019) Welcome to the tidyverse. Journal of Open Source Software, 4, 1686.
10.21105/joss.01686 Google Scholar