Microhabitat conditions remedy heat stress effects on insect activity.
animal movement
habitat composition
heat extremes
homogenization
microclimate
microhabitat variability
radio frequency identification
temperature increase
warming
Journal
Global change biology
ISSN: 1365-2486
Titre abrégé: Glob Chang Biol
Pays: England
ID NLM: 9888746
Informations de publication
Date de publication:
07 2023
07 2023
Historique:
revised:
10
03
2023
received:
23
09
2022
accepted:
28
03
2023
medline:
7
6
2023
pubmed:
15
5
2023
entrez:
15
5
2023
Statut:
ppublish
Résumé
Anthropogenic global warming has major implications for mobile terrestrial insects, including long-term effects from constant warming, for example, on species distribution patterns, and short-term effects from heat extremes that induce immediate physiological responses. To cope with heat extremes, they either have to reduce their activity or move to preferable microhabitats. The availability of favorable microhabitat conditions is strongly promoted by the spatial heterogeneity of habitats, which is often reduced by anthropogenic land transformation. Thus, it is decisive to understand the combined effects of these global change drivers on insect activity. Here, we assessed the movement activity of six insect species (from three orders) in response to heat stress using a unique tracking approach via radio frequency identification. We tracked 465 individuals at the iDiv Ecotron across a temperature gradient up to 38.7°C. In addition, we varied microhabitat conditions by adding leaf litter from four different tree species to the experimental units, either spatially separated or well mixed. Our results show opposing effects of heat extremes on insect activity depending on the microhabitat conditions. The insect community significantly decreased its activity in the mixed litter scenario, while we found a strong positive effect on activity in the separated litter scenario. We hypothesize that the simultaneous availability of thermal refugia as well as resources provided by the mixed litter scenario allows animals to reduce their activity and save energy in response to heat stress. Contrary, the spatial separation of beneficial microclimatic conditions and resources forces animals to increase their activity to fulfill their energetic needs. Thus, our study highlights the importance of habitat heterogeneity on smaller scales, because it may buffer the consequences of extreme temperatures of insect performance and survival under global change.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3747-3758Subventions
Organisme : Deutsche Forschungsgemeinschaft
ID : FOR 2716
Organisme : Deutsche Forschungsgemeinschaft
ID : 202548816
Organisme : Deutsche Forschungsgemeinschaft
ID : BR 2315/16-1
Organisme : Deutsche Forschungsgemeinschaft
ID : FZT 118
Organisme : Deutsche Forschungsgemeinschaft
ID : GRK 2118/1
Organisme : Deutsche Forschungsgemeinschaft
ID : HO 3952/3-2
Organisme : Deutsche Forschungsgemeinschaft
ID : RA 2339/2-1
Organisme : Deutsche Forschungsgemeinschaft
ID : SCHL 2259/1-1
Informations de copyright
© 2023 The Authors. Global Change Biology published by John Wiley & Sons Ltd.
Références
Alexander, R. M. (2005). Models and the scaling of energy costs for locomotion. The Journal of Experimental Biology, 208, 1645-1652. https://doi.org/10.1242/jeb.01484
Barker, K. R. (1985). Nematode extraction and bioassays. In K. R. Barker, C. C. Carter, & J. N. Sasser (Eds.), An advanced treatise on Meloidogyne: Methodology (pp. 19-35). North Carolina State University Graphics.
Barlow, S. E., & O'Neill, M. A. (2020). Technological advances in field studies of pollinator ecology and the future of e-ecology. Current Opinion in Insect Science, 38, 15-25. https://doi.org/10.1016/j.cois.2020.01.008
Beck, M. W. (2000). Separating the elements of habitat structure: Independent effects of habitat complexity and structural components on rocky intertidal gastropods. Journal of Experimental Marine Biology and Ecology, 249, 29-49. https://doi.org/10.1016/S0022-0981(00)00171-4
Bell, S. S., McCoy, E. D., & Mushinsky, H. R. (1991). Habitat structure: The physical arrangement of objects in space. Springer Netherlands.
Bennett, A. F. (2004). Thermoregulation in African chameleons. International Congress Series, 1275, 234-241. https://doi.org/10.1016/j.ics.2004.09.035
Black, I. R. G., Berman, J. M., Cadena, V. C., & Tattersall, G. J. (2019). Behavioral thermoregulation in lizards: Strategies for achieving preferred temperature. In V. L. Bels, & A. P. Russell (Eds.), Behavior of lizards. Evolutionary and mechanistic perspectives (pp. 13-46). CRC Press.
Bonte, D., & Dahirel, M. (2017). Dispersal: A central and independent trait in life history. Oikos, 126, 472-479. https://doi.org/10.1111/oik.03801
Brooks, M. E., Kristensen, K., van Benthem, K. J., Magnusson, A., Berg, C. W., Nielsen, A., Skaug, H. J., Machler, M., & Bolker, B. M. (2017). glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. The R Journal, 9, 378-400. https://doi.org/10.3929/ETHZ-B-000240890
Byrne, L. B. (2007). Habitat structure: A fundamental concept and framework for urban soil ecology. Urban Ecosystem, 10, 255-274. https://doi.org/10.1007/s11252-007-0027-6
Cecchetto, N. R., Medina, S. M., & Ibargüengoytía, N. R. (2020). Running performance with emphasis on low temperatures in a Patagonian lizard, Liolaemus lineomaculatus. Scientific Reports, 10, 14732. https://doi.org/10.1038/s41598-020-71617-3
Chomel, M., Guittonny-Larchevêque, M., Fernandez, C., Gallet, C., DesRochers, A., Paré, D., Jackson, B. G., & Baldy, V. (2016). Plant secondary metabolites: A key driver of litter decomposition and soil nutrient cycling. Journal of Ecology, 104(6), 1527-1541. https://doi.org/10.1111/1365-2745.12644
Dainese, M., Martin, E. A., Aizen, M. A., Albrecht, M., Bartomeus, I., Bommarco, R., Carvalheiro, L. G., Chaplin-Kramer, R., Gagic, V., Garibaldi, L. A., Ghazoul, J., Grab, H., Jonsson, M., Karp, D. S., Kennedy, C. M., Kleijn, D., Kremen, C., Landis, D. A., Letourneau, D. K., … Steffan-Dewenter, I. (2019). A global synthesis reveals biodiversity-mediated benefits for crop production. Science Advances, 5, eaax0121. https://doi.org/10.1126/sciadv.aax0121
de Souza, P., Marendy, P., Barbosa, K., Budi, S., Hirsch, P., Nikolic, N., Gunthorpe, T., Pessin, G., & Davie, A. (2018). Low-cost electronic tagging system for bee monitoring. Sensors, 18, 2124. https://doi.org/10.3390/s18072124
Dell, A. I., Bender, J. A., Branson, K., Couzin, I. D., de Polavieja, G. G., Noldus, L. P. J. J., Pérez-Escudero, A., Perona, P., Straw, A. D., Wikelski, M., & Brose, U. (2014). Automated image-based tracking and its application in ecology. Trends in Ecology & Evolution, 29, 417-428. https://doi.org/10.1016/j.tree.2014.05.004
Deutscher Wetterdienst. (2019). Monatlicher Klimastatus Deutschland. Datenteil für August 2019. DWD, Geschäftsbereich Klima und Umwelt.
Deutscher Wetterdienst. (2020a). Klimastatusbericht Deutschland Jahr 2018. DWD, Geschäftsbereich Klima und Umwelt.
Deutscher Wetterdienst. (2020b). Klimastatusbericht Deutschland Jahr 2019. DWD, Geschäftsbereich Klima und Umwelt.
Ehnes, R. B., Rall, B. C., & Brose, U. (2011). Phylogenetic grouping, curvature and metabolic scaling in terrestrial invertebrates: Invertebrate metabolism. Ecology Letters, 14, 993-1000. https://doi.org/10.1111/j.1461-0248.2011.01660.x
Ferlian, O., Wirth, C., & Eisenhauer, N. (2017). Leaf and root C-to-N ratios are poor predictors of soil microbial biomass C and respiration across 32 tree species. Pedobiologia, 65, 16-23. https://doi.org/10.1016/j.pedobi.2017.06.005
Fischer, E. M., & Knutti, R. (2015). Anthropogenic contribution to global occurrence of heavy-precipitation and high-temperature extremes. Nature Climate Change, 5, 560-564. https://doi.org/10.1038/nclimate2617
Fox, J., & Sandford, W. (2019). An R companion to applied regression (3rd ed.). Sage.
Gols, R., Ojeda-Prieto, L. M., Li, K., van der Putten, W. H., & Harvey, J. A. (2021). Within-patch and edge microclimates vary over a growing season and are amplified during a heatwave: Consequences for ectothermic insects. Journal of Thermal Biology, 99, 103006. https://doi.org/10.1016/j.jtherbio.2021.103006
Goossens, S., Wybouw, N., Van Leeuwen, T., & Bonte, D. (2020). The physiology of movement. Movement Ecology, 8, 5. https://doi.org/10.1186/s40462-020-0192-2
Güsewell, S., & Gessner, M. O. (2009). N:P ratios influence litter decomposition and colonization by fungi and bacteria in microcosms. Functional Ecology, 23, 211-219. https://doi.org/10.1111/j.1365-2435.2008.01478.x
Halsey, L. G. (2016). Terrestrial movement energetics: Current knowledge and its application to the optimising animal. The Journal of Experimental Biology, 219, 1424-1431. https://doi.org/10.1242/jeb.133256
Harvey, J. A., Heinen, R., Gols, R., & Thakur, M. P. (2020). Climate change-mediated temperature extremes and insects: From outbreaks to breakdowns. Global Change Biology, 26, 6685-6701. https://doi.org/10.1111/gcb.15377
Harvey, J. A., Tougeron, K., Gols, R., Heinen, R., Abarca, M., Abram, P. K., Basset, Y., Berg, M., Boggs, C., Brodeur, J., Cardoso, P., de Boer, J. G., De Snoo, G. R., Deacon, C., Dell, J. E., Desneux, N., Dillon, M. E., Duffy, G. A., Dyer, L. A., … Chown, S. L. (2022). Scientists' warning on climate change and insects. Ecological Monographs, 93, 1553. https://doi.org/10.1002/ecm.1553
Herrmann, S., Grams, T. E. E., Tarkka, M. T., Angay, O., Bacht, M., Bönn, M., Feldhahn, L., Graf, M., Kurth, F., Maboreke, H., Mailander, S., Recht, S., Fleischmann, F., Ruess, L., Schädler, M., Scheu, S., Schrey, S., & Buscot, F. (2016). Endogenous rhythmic growth, a trait suitable for the study of interplays between multitrophic interactions and tree development. Perspectives in Plant Ecology, Evolution and Systematics, 19, 40-48. https://doi.org/10.1016/j.ppees.2016.02.003
Hillebrand, H., Cowles, J. M., Lewandowska, A., Van de Waal, D. B., & Plum, C. (2014). Think ratio! A stoichiometric view on biodiversity-ecosystem functioning research. Basic and Applied Ecology, 15, 465-474. https://doi.org/10.1016/j.baae.2014.06.003
Hof, C. (2021). Towards more integration of physiology, dispersal and land-use change to understand the responses of species to climate change. The Journal of Experimental Biology, 224, jeb238352. https://doi.org/10.1242/jeb.238352
Hof, C., Levinsky, I., Araújo, M. B., & Rahbek, C. (2011). Rethinking species' ability to cope with rapid climate change: Biodiversity and rapid climate change. Global Change Biology, 17, 2987-2990. https://doi.org/10.1111/j.1365-2486.2011.02418.x
Horton, R. M., Mankin, J. S., Lesk, C., Coffel, E., & Raymond, C. (2016). A review of recent advances in research on extreme heat events. Current Climate Change Reports, 2, 242-259. https://doi.org/10.1007/s40641-016-0042-x
Huey, R. B., & Kingsolver, J. G. (2019). Climate warming, resource availability, and the metabolic meltdown of ectotherms. The American Naturalist, 194, E140-E150. https://doi.org/10.1086/705679
IPCC. (2021). Climate change 2021: The physical science basis. In V. Masson-Delmotte, P. Zhai, A. Pirani, S. L. Connors, C. Péan, S. Berger, N. Caud, Y. Chen, L. Goldfarb, M. I. Gomis, M. Huang, K. Leitzell, E. Lonnoy, J. B. R. Matthews, T. K. Maycock, T. Waterfield, O. Yelekçi, R. Yu, & B. Zhou (Eds.), Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change (pp. 1513-1767). Cambridge University Press. https://doi.org/10.1017/9781009157896
Jochum, M., Barnes, A. D., Ott, D., Lang, B., Klarner, B., Farajallah, A., Scheu, S., & Brose, U. (2017). Decreasing stoichiometric resource quality drives compensatory feeding across trophic levels in tropical litter invertebrate communities. The American Naturalist, 190, 131-143. https://doi.org/10.1086/691790
Jochum, M., Barnes, A. D., Weigelt, P., Ott, D., Rembold, K., Farajallah, A., & Brose, U. (2017). Resource stoichiometry and availability modulate species richness and biomass of tropical litter macro-invertebrates. The Journal of Animal Ecology, 86, 1114-1123. https://doi.org/10.1111/1365-2656.12695
Kalinkat, G., Brose, U., & Rall, B. C. (2013). Habitat structure alters top-down control in litter communities. Oecologia, 172, 877-887. https://doi.org/10.1007/s00442-012-2530-6
Kearney, M., Shine, R., & Porter, W. P. (2009). The potential for behavioral thermoregulation to buffer “cold-blooded” animals against climate warming. Proceedings of the National Academy of Sciences of the United States of America, 106, 3835-3840. https://doi.org/10.1073/pnas.0808913106
Kearney, M. R., Porter, W. P., & Huey, R. B. (2021). Modelling the joint effects of body size and microclimate on heat budgets and foraging opportunities of ectotherms. Methods in Ecology and Evolution, 12, 458-467. https://doi.org/10.1111/2041-210X.13528
Kissling, W. D., Pattemore, D. E., & Hagen, M. (2014). Challenges and prospects in the telemetry of insects. Biological Reviews, 89, 511-530. https://doi.org/10.1111/brv.12065
Laenderdaten.info. (2022). Sonnenaufgang und Untergang in Deutschland. https://www.laenderdaten.info/Europa/Deutschland/sonnenuntergang.php
Luber, G., & McGeehin, M. (2008). Climate change and extreme heat events. American Journal of Preventive Medicine, 35, 429-435. https://doi.org/10.1016/j.amepre.2008.08.021
Ma, C.-S., Ma, G., & Pincebourde, S. (2021). Survive a warming climate: Insect responses to extreme high temperatures. Annual Review of Entomology, 66, 163-184. https://doi.org/10.1146/annurev-ento-041520-074454
Ma, G., Bai, C.-M., Wang, X.-J., Majeed, M. Z., & Ma, C.-S. (2018). Behavioural thermoregulation alters microhabitat utilization and demographic rates in ectothermic invertebrates. Animal Behaviour, 142, 49-57. https://doi.org/10.1016/j.anbehav.2018.06.003
Nakano, S., Kitano, F., & Maekawa, K. (1996). Potential fragmentation and loss of thermal habitats for charrs in the Japanese archipelago due to climatic warming. Freshwater Biology, 36, 711-722. https://doi.org/10.1046/j.1365-2427.1996.d01-516.x
Ott, D., Digel, C., Klarner, B., Maraun, M., Pollierer, M., Rall, B. C., Scheu, S., Seelig, G., & Brose, U. (2014). Litter elemental stoichiometry and biomass densities of forest soil invertebrates. Oikos, 123, 1212-1223. https://doi.org/10.1111/oik.01670
Ott, D., Rall, B. C., & Brose, U. (2012). Climate change effects on macrofaunal litter decomposition: The interplay of temperature, body masses and stoichiometry. Philosophical Transactions of the Royal Society B: Biological Sciences, 367, 3025-3032. https://doi.org/10.1098/rstb.2012.0240
Peck, L. S., Clark, M. S., Morley, S. A., Massey, A., & Rossetti, H. (2009). Animal temperature limits and ecological relevance: Effects of size, activity and rates of change. Functional Ecology, 23, 248-256. https://doi.org/10.1111/j.1365-2435.2008.01537.x
Perkins, S. E. (2015). A review on the scientific understanding of heatwaves-Their measurement, driving mechanisms, and changes at the global scale. Atmospheric Research, 164-165, 242-267. https://doi.org/10.1016/j.atmosres.2015.05.014
Perkins, S. E., Alexander, L. V., & Nairn, J. R. (2012). Increasing frequency, intensity and duration of observed global heatwaves and warm spells. Geophysical Research Letters, 39, 2012GL053361. https://doi.org/10.1029/2012GL053361
R Core Team. (2022). R: A language and environment for statistical computing. R Foundation for Statistical Computing.
Rahmstorf, S., & Coumou, D. (2011). Increase of extreme events in a warming world. Proceedings of the National Academy of Sciences of the United States of America, 108, 17905-17909. https://doi.org/10.1073/pnas.1101766108
Rezende, E. L., & Bozinovic, F. (2019). Thermal performance across levels of biological organization. Philosophical Transactions of the Royal Society B: Biological Sciences, 374, 20180549. https://doi.org/10.1098/rstb.2018.0549
Rillig, M. C., Ryo, M., Lehmann, A., Aguilar-Trigueros, C. A., Buchert, S., Wulf, A., Iwasaki, A., Roy, J., & Yang, G. (2019). The role of multiple global change factors in driving soil functions and microbial biodiversity. Science, 366, 886-890. https://doi.org/10.1126/science.aay2832
Roberts, C. M. (2006). Radio frequency identification (RFID). Computers & Security, 25, 18-26. https://doi.org/10.1016/j.cose.2005.12.003
Rosenblatt, A. E., & Schmitz, O. J. (2016). Climate change, nutrition, and bottom-up and top-down food web processes. Trends in Ecology & Evolution, 31, 965-975. https://doi.org/10.1016/j.tree.2016.09.009
Sage, R. F. (2020). Global change biology: A primer. Global Change Biology, 26, 3-30. https://doi.org/10.1111/gcb.14893
Scheffers, B. R., Edwards, D. P., Diesmos, A., Williams, S. E., & Evans, T. A. (2014). Microhabitats reduce animal's exposure to climate extremes. Global Change Biology, 20, 495-503. https://doi.org/10.1111/gcb.12439
Schmidt, A., Hines, J., Türke, M., Buscot, F., Schädler, M., Weigelt, A., Gebler, A., Klotz, S., Liu, T., Reth, S., Trogisch, S., Roy, J., Wirth, C., & Eisenhauer, N. (2021). The iDiv Ecotron-A flexible research platform for multitrophic biodiversity research. Ecology and Evolution, 11, 15174-15190. https://doi.org/10.1002/ece3.8198
Seebacher, F., & Post, E. (2015). Climate change impacts on animal migration. Climate Change Responses, 2, 5. https://doi.org/10.1186/s40665-015-0013-9
Somero, G. N. (2010). The physiology of climate change: How potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’. The Journal of Experimental Biology, 213, 912-920. https://doi.org/10.1242/jeb.037473
Sterner, R. W., & Elser, J. J. (2002). Ecological stoichiometry: The biology of elements from molecules to the biosphere. Princeton University Press.
Suggitt, A. J., Wilson, R. J., Isaac, N. J. B., Beale, C. M., Auffret, A. G., August, T., Bennie, J. J., Crick, H. Q. P., Duffield, S., Fox, R., Hopkins, J. J., Macgregor, N. A., Morecroft, M. D., Walker, K. J., & Maclean, I. M. D. (2018). Extinction risk from climate change is reduced by microclimatic buffering. Nature Climate Change, 8, 713-717. https://doi.org/10.1038/s41558-018-0231-9
Terblanche, J. S., Hoffmann, A. A., Mitchell, K. A., Rako, L., le Roux, P. C., & Chown, S. L. (2011). Ecologically relevant measures of tolerance to potentially lethal temperatures. The Journal of Experimental Biology, 214, 3713-3725. https://doi.org/10.1242/jeb.061283
Terlau, J., Brose, U., Antunes, A. C., Berti, E., Boy, T., Gauzens, B., Pawar, S., Pinsky, M., Ryser, R., & Hirt, M. R. (2022). Integrating trait-based movement into mechanistic predictions of thermal performance. Preprint from Research Square. https://doi.org/10.21203/rs.3.rs-1815379/v1
Terlau, J. F., Brose, U., Eisenhauer, N., Amyntas, A., Boy, T., Dyer, A., Gebler, A., Hof, C., Liu, T., Scherber, C., Schlägel, U. E., Schmidt, A., & Hirt, M. R. (2023). Data for: Microhabitat conditions remedy heat stress effects on insect activity [Data set]. Zenodo. https://doi.org/10.5281/zenodo.7784702
Thakur, M. P., Bakker, E. S., (Ciska) Veen, G. F., & Harvey, J. A. (2020). Climate extremes, rewilding, and the role of microhabitats. One Earth, 2, 506-509. https://doi.org/10.1016/j.oneear.2020.05.010
Thakur, M. P., Reich, P. B., Hobbie, S. E., Stefanski, A., Rich, R., Rice, K. E., Eddy, W. C., & Eisenhauer, N. (2018). Reduced feeding activity of soil detritivores under warmer and drier conditions. Nature Climate Change, 8, 75-78. https://doi.org/10.1038/s41558-017-0032-6
Travis, J. M. J. (2003). Climate change and habitat destruction: A deadly anthropogenic cocktail. Proceedings of the Royal Society of London - Series B: Biological Sciences, 270, 467-473. https://doi.org/10.1098/rspb.2002.2246
Wikelski, M., Kays, R. W., Kasdin, N. J., Thorup, K., Smith, J. A., & Swenson, G. W. (2007). Going wild: What a global small-animal tracking system could do for experimental biologists. The Journal of Experimental Biology, 210, 181-186. https://doi.org/10.1242/jeb.02629
Wilson, E. O. (1987). The little things that run the world (the importance and conservation of invertebrates). Conservation Biology, 1, 344-346. https://doi.org/10.1111/j.1523-1739.1987.tb00055.x
Yeates, G. W., Bongers, T., De Goede, R. G., Freckman, D. W., & Georgieva, S. S. (1993). Feeding habits in soil nematode families and genera - an outline for soil ecologists. Journal of Nematology, 25(3), 315-331.