More stories

  • in

    Reply to: Fire activity as measured by burned area reveals weak effects of ENSO in China

    Resco de Dios et al. claim that the modulation of ENSO on fire in China is weak. They base their claim on the insignificant correlations they find between gridded area and ENSO indices on individual grid points in China. Unlike their analysis of individual grid points, our analyses were based on the covariance of data on these grid points. Combining all grid points, our correlation analysis increases the degree of freedom, raises the likelihood of a significance test, and therefore is reliable and robust. Fire in individual grid points can be noisy on a local scale, while climate plays a more critical role in modulating large-scale fires.Many previous studies revealed the dominant impacts of ENSO in different regions of China7, 8. Resco de Dios et al. stated that the ENSO could only influence the ignitions and thus has little effect on fire activity. In fact, fuel availability and flammability are also key factors in fire occurrence, particularly for large-scale fires9. This is evidenced by the strong correlations between fire occurrence and interannual climate variability.China’s fire policy not only suppresses existing fires but also prevents human-ignited fire occurrences. As revealed in previous studies, the fire suppression policy since 1987 decreased not only burnt areas but also fire occurrences10.The study by Resco de Dios et al. was based on MODIS-derived annual area burned, which differs from our ground-truthed WFAC fire occurrence dataset. The MODIS cannot sufficiently distinguish the wildfire from the frequent crop fires and thus vastly misinterrupt the crop fires as wildfire, especially over the northern plains where forests are rare. Here, we show that the EOF analyses of the WFAC can also reveal the dipole fire pattern between southwestern and southeastern China. We highlight that the dipole fire pattern and ENSO modulation are on large scales. The fire control policy not only suppresses existing fires but also prevents human-ignited fire occurrences, and thus plays an effective role in reducing five activities in China. More

  • in

    Global economic costs of herpetofauna invasions

    Seebens, H. et al. Projecting the continental accumulation of alien species through to 2050. Glob. Change Biol. 27(5), 970–982 (2021).ADS 

    Google Scholar 
    Bellard, C., Cassey, P. & Blackburn, T. M. Alien species as a driver of recent extinctions. Biol. Lett. 12(2), 20150623 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Walsh, J. R., Carpenter, S. R. & Vander Zanden, M. J. Invasive species triggers a massive loss of ecosystem services through a trophic cascade. Proc. Natl. Acad. Sci. 113(15), 4081–4085 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Linders, T. E. W. et al. Direct and indirect effects of invasive species: Biodiversity loss is a major mechanism by which an invasive tree affects ecosystem functioning. J. Ecol. 107(6), 2660–2672 (2019).
    Google Scholar 
    Diagne, C., Ballesteros-Mejia, L., Bodey, T., Cuthbert, R., Fantle-Lepczyk, J., Angulo, E., Dobigny, G., & Courchamp, F. Economic costs of invasive rodents worldwide: The tip of the iceberg (2021).Schaffner, F., Medlock, J. M. & Van Bortel, A. W. Public health significance of invasive mosquitoes in Europe. Clin. Microbiol. Infect. 19(8), 685–692 (2013).CAS 
    PubMed 

    Google Scholar 
    Schaffner, U. et al. Biological weed control to relieve millions from Ambrosia allergies in Europe. Nat. Commun. 11(1), 1–7 (2020).
    Google Scholar 
    Shackleton, R. T., Shackleton, C. M. & Kull, C. A. The role of invasive alien species in shaping local livelihoods and human well-being: A review. J. Environ. Manag. 229, 145–157 (2019).
    Google Scholar 
    Clavero, M. & García-Berthou, E. Invasive species are a leading cause of animal extinctions. Trends Ecol. Evol. 20(3), 110 (2005).PubMed 

    Google Scholar 
    Crystal-Ornelas, R. & Lockwood, J. L. The ‘known unknowns’ of invasive species impact measurement. Biol. Invasions 22(4), 1513–1525 (2020).
    Google Scholar 
    Florencio, M., Lobo, J. M. & Bini, L. M. Biases in global effects of exotic species on local invertebrates: A systematic review. Biol. Invasions 21(10), 3043–3061 (2019).
    Google Scholar 
    Measey, J. et al. Why have a pet amphibian? Insights from YouTube. Front. Ecol. Evol. 7, 52 (2019).
    Google Scholar 
    Ossiboff, R. J. et al. Differentiating Batrachochytrium dendrobatidis and B. salamandrivorans in amphibian chytridiomycosis using RNAScope in situ hybridization. Front. Vet. Sci. 6, 304 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    Kraus, F. Alien Reptiles and Amphibians: A Scientific Compendium and Analysis, vol. 4. (Springer Science & Business Media, 2009).Kraus, F. Impacts from invasive reptiles and amphibians. Annu. Rev. Ecol. Evol. Syst. 46, 75–97 (2015).
    Google Scholar 
    Ramsay, N. F., Ng, P. K. A., O’Riordan, R. M., & Chou, L. M. The red-eared slider (Trachemys scripta elegans) in Asia: A review. Biological invaders in inland waters: Profiles, distribution, and threats 161–174 (2007).Lindsay, M. K., Zhang, Y., Forstner, M. R. & Hahn, D. Effects of the freshwater turtle Trachemys scripta elegans on ecosystem functioning: An approach in experimental ponds. Amphibia-Reptilia 34(1), 75–84 (2013).
    Google Scholar 
    Phillips, B. L. & Shine, R. An invasive species induces rapid adaptive change in a native predator: Cane toads and black snakes in Australia. Proc. R. Soc. B Biol. Sci. 273(1593), 1545–1550 (2006).
    Google Scholar 
    Shanmuganathan, T. et al. Biological control of the cane toad in Australia: A review. Anim. Conserv. 13, 16–23 (2010).
    Google Scholar 
    Smart, A. S., Tingley, R. & Phillips, B. L. Estimating the benefit of quarantine: Eradicating invasive cane toads from islands. NeoBiota 60, 117 (2020).
    Google Scholar 
    Reaser, J. K. et al. Ecological and socioeconomic impacts of invasive alien species in island ecosystems. Environ. Conserv. 34, 98–111 (2007).
    Google Scholar 
    Fritts, T. H. Economic costs of electrical system instability and power outages caused by snakes on the island of Guam. Int. Biodeterior. Biodegrad. 49(2–3), 93–100 (2002).
    Google Scholar 
    Rodda, G. H., Fritts, T. H. & Chiszar, D. The disappearance of Guam’s wildlife. Bioscience 47(9), 565–574 (1997).
    Google Scholar 
    Kraus, F. Reptiles and amphibians. In Encyclopedia of Biological Invasions 590–594. (University of California Press, 2011).Kraus, F. Global trends in alien reptiles and amphibians. Aliens Invasive Species Bull. 28, 13–18 (2009).
    Google Scholar 
    Capinha, C., Marcolin, F. & Reino, L. Human-induced globalization of insular herpetofaunas. Glob. Ecol. Biogeogr. 29(8), 1328–1349 (2020).
    Google Scholar 
    Reed, R. N. & Kraus, F. Invasive reptiles and amphibians: Global perspectives and local solutions. Anim. Conserv. 13, 3–4 (2010).
    Google Scholar 
    Wasserman, R. J., Dick, J. T., Welch, R. J., Dalu, T. & Magellan, K. Site and species selection for religious release of non-native fauna. Conserv. Biol. 33(4), 969–971 (2019).PubMed 

    Google Scholar 
    Li, X., Liu, X., Kraus, F., Tingley, R. & Li, Y. Risk of biological invasions is concentrated in biodiversity hotspots. Front. Ecol. Environ. 14(8), 411–417 (2016).
    Google Scholar 
    Bellard, C. & Jeschke, J. M. A spatial mismatch between invader impacts and research publications. Conserv. Biol. 30(1), 230–232 (2016).CAS 
    PubMed 

    Google Scholar 
    Diagne, C. et al. InvaCost, a public database of the economic costs of biological invasions worldwide. Sci. Data 7(1), 1–12 (2020).
    Google Scholar 
    Diagne, C. et al. High and rising economic costs of biological invasions worldwide. Nature 592(7855), 571–576 (2021).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Cuthbert, R. N., Diagne, C., Haubrock, P. J., Turbelin, A. J., & Courchamp, F. Are the “100 of the world’s worst” invasive species also the costliest? Biol. Invasions 1–10 (2021).Cuthbert, R. N. et al. Global economic costs of aquatic invasive alien species. Sci. Total Environ. 775, 145238 (2021).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Haubrock, P. J. et al. Biological invasions in Singapore and Southeast Asia: Data gaps fail to mask potentially massive economic costs. NeoBiota 67, 131–152 (2021).
    Google Scholar 
    Van Wilgen, N. J., Gillespie, M. S., Richardson, D. M. & Measey, J. A taxonomically and geographically constrained information base limits non-native reptile and amphibian risk assessment: A systematic review. PeerJ 6, e5850 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    Cuthbert, R. et al. Economic costs of biological invasions in the United Kingdom. Neobiota 67, 299–328 (2021).
    Google Scholar 
    Heringer, G. et al. The economic costs of biological invasions in Central and South America: A first regional assessment. NeoBiota 67, 401 (2021).
    Google Scholar 
    Paini, D. R. et al. Global threat to agriculture from invasive species. Proc. Natl. Acad. Sci. 113(27), 7575–7579 (2016).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Capinha, C. et al. Diversity, biogeography and the global flows of alien amphibians and reptiles. Divers. Distrib. 23(11), 1313–1322 (2017).
    Google Scholar 
    Kumschick, S. et al. How repeatable is the Environmental Impact Classification of Alien Taxa (EICAT)? Comparing independent global impact assessments of amphibians. Ecol. Evol. 7(8), 2661–2670 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    Diagne, C., Catford, J. A., Essl, F., Nuñez, M. A. & Courchamp, F. What are the economic costs of biological invasions? A complex topic requiring international and interdisciplinary expertise. NeoBiota 63, 25 (2020).
    Google Scholar 
    Diagne, C. et al. The economic costs of biological invasions in Africa: A growing but neglected threat?. NeoBiota 67, 11–51 (2021).
    Google Scholar 
    Bradshaw, C. J. et al. Detailed assessment of the reported economic costs of invasive species in Australia. NeoBiota 67, 511–550 (2021).
    Google Scholar 
    Dorcas, M. E. et al. Severe mammal declines coincide with proliferation of invasive Burmese pythons in Everglades National Park. Proc. Natl. Acad. Sci. 109(7), 2418–2422 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Mazzotti, F. J. et al. Implications of the 2013 Python Challenge® for ecology and management of Python molorus bivittatus (Burmese Python) in Florida. Southeast. Nat. 15(sp8), 63–74 (2016).
    Google Scholar 
    Smith, B. J. et al. Betrayal: Radio-tagged Burmese pythons reveal locations of conspecifics in Everglades National Park. Biol. Invasions 18(11), 3239–3250 (2016).
    Google Scholar 
    Easteal, S. The history of introductions of Bufo marinus (Amphibia: Anura); A natural experiment in evolution. Biol. J. Lin. Soc. 16(2), 93–113 (1981).
    Google Scholar 
    Haubrock, P. J., Bernery, C., Cuthbert, R. N., Liu, C., Kourantidou, M., Leroy, B., Turbelin, A., Kramer, A. M., Verbrugge, L., Diagne, C., Courchamp, F., & Gozlan, R. E. What is the recorded economic cost of alien invasive fishes worldwide? (2021).Angulo, E., Hoffmann, B., Ballesteros-Mejia, L., Taheri, A., Balzani, P., Renault, D., Cordonnier, M., Bellard, C., Diagne, C., Ahmed, D. A., Watari, Y., & Courchamp, F. Economic costs of invasive alien ants worldwide. (2021).Kouba, A., Oficialdegui, F., Cuthbert, R., Kourantidou, M., Tricarico, E., Leroy, B., Gozlan, R., Courchamp, F., & Haubrock, P. Feeling the pinch: Global economic costs of crayfish invasions and comparison with other aquatic crustaceans (2021).Dufresnes, C. et al. Cryptic invasion of Italian pool frogs (Pelophylax bergeri) across Western Europe unraveled by multilocus phylogeography. Biol. Invasions 19(5), 1407–1420 (2017).
    Google Scholar 
    Kumschick, S. et al. Impact assessment with different scoring tools: How well do alien amphibian assessments match?. NeoBiota 33, 53 (2017).
    Google Scholar 
    Crystal-Ornelas, R. et al. Economic costs of biological invasions within North America. NeoBiota 67, 485 (2021).
    Google Scholar 
    Angulo, E. et al. Non-English languages enrich scientific knowledge: The example of economic costs of biological invasions. Sci. Total Environ. 775, 144441 (2021).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Taylor, R., & Edwards, G. A review of the impact and control of cane toads in Australia with recommendations for future research and management approaches. A report to the Vertebrate Pests Committee from the National Cane Toad Taskforce (2005).Burnett, K., Pongkijvorasin, S. & Roumasset, J. Species invasion as catastrophe: The case of the brown tree snake. Environ. Resour. Econ. 51(2), 241–254 (2012).
    Google Scholar 
    Haubrock, P. J., Cuthbert, R. N., Ricciardi, A., Diagne, C., & Courchamp, F. Massive economic costs of invasive bivalves in freshwater ecosystems (2021).Pimentel, D., Zuniga, R. & Morrison, D. Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol. Econ. 52(3), 273–288 (2005).
    Google Scholar 
    Fantle-Lepczyk, J. E. et al. Economic costs of biological invasions in the United States. bioRxiv 89, 89 (2021).
    Google Scholar 
    European Environment Agency. The impacts of invasive alien species in Europe. Publications Office of the European Union (2013).Measey, J. et al. Invasive amphibians in southern Africa: A review of invasion pathways. Bothalia-Afr. Biodivers. Conserv. 47(2), 1–12 (2017).
    Google Scholar 
    Anton, A., Geraldi, N. R., Ricciardi, A. & Dick, J. T. Global determinants of prey naiveté to exotic predators. Proc. R. Soc. B 287(1928), 20192978 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    Rico-Sánchez, A. E. et al. Economic costs of invasive alien species in Mexico. NeoBiota 67, 459–483 (2021).
    Google Scholar 
    McNeely, J. Invasive species: A costly catastrophe for native biodiversity. Land Use Water Resour. Res. 1(1732-2016-140260) (2001).Sax, D. F. & Gaines, S. D. Species invasions and extinction: The future of native biodiversity on islands. Proc. Natl. Acad. Sci. 105, 11490–11497 (2008).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Christie, M., Fazey, I., Cooper, R., Hyde, T. & Kenter, J. O. An evaluation of monetary and non-monetary techniques for assessing the importance of biodiversity and ecosystem services to people in countries with developing economies. Ecol. Econ. 83, 67–78 (2012).
    Google Scholar 
    Essl, F. et al. Socioeconomic legacy yields an invasion debt. Proc. Natl. Acad. Sci. 108(1), 203–207 (2011).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Seebens, H. et al. No saturation in the accumulation of alien species worldwide. Nat. Commun. 8(1), 1–9 (2017).
    Google Scholar 
    Ahmed, D. A., Hudgins, E. J., Cuthbert, R. N., Kourantidou, M., Diagne, C., Haubrock, P. J., et al. Managing biological invasions: The cost of inaction. Biol. Invasions. 1–20. (2022).Leung, B. et al. An ounce of prevention or a pound of cure: Bioeconomic risk analysis of invasive species. Proc. R. Soc. Lond. Ser. B Biol. Sci. 269(1508), 2407–2413 (2002).
    Google Scholar 
    Haubrock, P. J. et al. Geographic and taxonomic trends of rising biological invasion costs. Sci. Total Environ. 817, 152948 (2022).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Kopecký, O., Kalous, L. & Patoka, J. Establishment risk from pet-trade freshwater turtles in the European Union. Knowl. Manag. Aquat. Ecosyst. 410, 02 (2013).
    Google Scholar 
    Mohanty, N. P. & Measey, J. The global pet trade in amphibians: Species traits, taxonomic bias, and future directions. Biodivers. Conserv. 28(14), 3915–3923 (2019).
    Google Scholar 
    Altherr, S. & Lameter, K. The rush for the rare: Reptiles and amphibians in the European pet trade. Animals 10, 2085 (2020).PubMed Central 

    Google Scholar 
    Cuthbert, R. N. et al. Biological invasion costs reveal insufficient proactive management worldwide. Sci. Total Environ. 819, 153404 (2022).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Ricciardi, A. Invasive species. In Ecological Systems 161–178. (Springer, 2013).Leroy, B., Kramer, A. M., Vaissière, A. C., Courchamp, F., & Diagne, C. Analysing global economic costs of invasive alien species with the invacost R package. bioRxiv (2020). More

  • in

    Weak effects on growth and cannibalism under fluctuating temperatures in damselfly larvae

    Vázquez, D. P., Gianoli, E., Morris, W. F. & Bozinovic, F. Ecological and evolutionary impacts of changing climatic variability. Biol. Rev. 92, 22–42. https://doi.org/10.1111/brv.12216 (2017).Article 
    PubMed 

    Google Scholar 
    Marshall, K. E. & Sinclair, B. J. The impacts of repeated cold exposure on insects. J. Exp. Biol. 215, 1607–1613. https://doi.org/10.1242/jeb.059956 (2012).Article 
    PubMed 

    Google Scholar 
    Bale, J. & Hayward, S. Insect overwintering in a changing climate. J. Exp. Biol. 213, 980–994 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    Kingsolver, J. G. Feeding, growth, and the thermal environment of cabbage white caterpillars, Pieris rapae L. Physiol. Biochem. Zool. 73, 621–628 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    Stange, E. E. & Ayres, M. P. Climate change impacts: Insects (JohnWiley & Sons, 2010).
    Google Scholar 
    Chapman, A. D. Numbers of Living Species in Australia and the World: Report for the Department of the Environment and Heritage Canberra, Australia (Department of the Environment and Heritage, 2006).
    Google Scholar 
    Colinet, H., Sinclair, B. J., Vernon, P. & Renault, D. Insects in fluctuating thermal environments. Annu. Rev. Entomol. 60, 123–140. https://doi.org/10.1146/annurev-ento-010814-021017 (2015).CAS 
    Article 
    PubMed 

    Google Scholar 
    Hickling, R., Roy, D. B., Hill, J. K. & Thomas, C. D. A northward shift of range margins in British Odonata. Glob. Change Biol. 11, 502–506. https://doi.org/10.1111/j.1365-2486.2005.00904.x (2005).ADS 
    Article 

    Google Scholar 
    Rumpf, S. B., Hülber, K., Zimmermann, N. E. & Dullinger, S. Elevational rear edges shifted at least as much as leading edges over the last century. Glob. Ecol. Biogeogr. 28, 533–543. https://doi.org/10.1111/geb.12865 (2019).Article 

    Google Scholar 
    Halsch, C. A. et al. Insects and recent climate change. Proc. Natl. Acad. Sci. 118, e2002543117. https://doi.org/10.1073/pnas.2002543117 (2021).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    McCain, C. M. & Garfinkel, C. F. Climate change and elevational range shifts in insects. Curr. Opin. Insect Sci. 47, 111–118. https://doi.org/10.1016/j.cois.2021.06.003 (2021).Article 
    PubMed 

    Google Scholar 
    Angilletta, M. J. Jr. & Angilletta, M. J. Thermal Adaptation: A Theoretical and Empirical Synthesis (Oxford University Press, 2009).Book 

    Google Scholar 
    Angilletta, M. J. & Dunham, A. E. The temperature-size rule in ectotherms: Simple evolutionary explanations may not be general. Am. Nat. 162, 332–342. https://doi.org/10.1086/377187 (2003).Article 
    PubMed 

    Google Scholar 
    Jensen, J. L. W. V. Sur les fonctions convexes et les inégalités entre les valeurs moyennes. Acta Math. 30, 175–193 (1906).MathSciNet 
    MATH 
    Article 

    Google Scholar 
    Ruel, J. J. & Ayres, M. P. Jensen’s inequality predicts effects of environmental variation. Trends Ecol. Evol. 14, 361–366 (1999).CAS 
    PubMed 
    Article 

    Google Scholar 
    Kingsolver, J. G. & Woods, H. A. Thermal sensitivity of growth and feeding in Manduca sexta Caterpillars. Physiol. Zool. 70, 631–638. https://doi.org/10.1086/515872 (1997).CAS 
    Article 
    PubMed 

    Google Scholar 
    Gillooly, J. F., Brown, J. H., West, G. B., Savage, V. M. & Charnov, E. L. Effects of size and temperature on metabolic rate. Science 293, 2248–2251 (2001).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Bale, J. S. et al. Herbivory in global climate change research: Direct effects of rising temperature on insect herbivores. Glob. Change Biol. 8, 1–16 (2002).ADS 
    Article 

    Google Scholar 
    Robinet, C. & Roques, A. Direct impacts of recent climate warming on insect populations. Integr. Zool. 5, 132–142 (2010).PubMed 
    Article 

    Google Scholar 
    García-Robledo, C., Kuprewicz, E. K., Staines, C. L., Erwin, T. L. & Kress, W. J. Limited tolerance by insects to high temperatures across tropical elevational gradients and the implications of global warming for extinction. Proc. Natl. Acad. Sci. 113, 680–685. https://doi.org/10.1073/pnas.1507681113 (2016).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Vasseur, D. A. et al. Increased temperature variation poses a greater risk to species than climate warming. Proc. R. Soc. B Biol. Sci. 281, 20132612 (2014).Article 

    Google Scholar 
    Sandehson, D. E. The relation of temperature to the growth of insects. J. Econ. Entomol. 3, 113–140 (1910).Article 

    Google Scholar 
    Cook, W. C. Some Effects of Alternating Temperatures on the Growth and Metabolism of Cutworm Larvae (Oxford University Press, 1927).
    Google Scholar 
    Kingsolver, J. G., Ragland, G. J. & Diamond, S. E. Evolution in a constant environment: Thermal fluctuations and thermal sensitivity of laboratory and field populations of Manduca sexta. Evolution 63, 537–541. https://doi.org/10.1111/j.1558-5646.2008.00568.x (2009).Article 
    PubMed 

    Google Scholar 
    Eldridge, W. H., Sweeney, B. W. & Law, J. M. Fish growth, physiological stress, and tissue condition in response to rate of temperature change during cool or warm diel thermal cycles. Can. J. Fish. Aquat. Sci. 72, 1527–1537 (2015).CAS 
    Article 

    Google Scholar 
    Bernhardt, J. R., Sunday, J. M., Thompson, P. L. & O’Connor, M. I. Nonlinear averaging of thermal experience predicts population growth rates in a thermally variable environment. Proc. R. Soc. B Biol. Sci. 285, 20181076. https://doi.org/10.1098/rspb.2018.1076 (2018).Article 

    Google Scholar 
    Morissette, J., Swart, S., Maccormack, T. J., Currie, S. & Morash, A. J. Thermal variation near the thermal optimum does not affect the growth, metabolism or swimming performance in wild Atlantic salmon Salmo salar. J. Fish Biol. 98, 1585–1589. https://doi.org/10.1111/jfb.14348 (2021).CAS 
    Article 
    PubMed 

    Google Scholar 
    Bozinovic, F. et al. The mean and variance of environmental temperature interact to determine physiological tolerance and fitness. Physiol. Biochem. Zool. 84, 543–552 (2011).PubMed 
    Article 

    Google Scholar 
    Boggs, C. L. The fingerprints of global climate change on insect populations. Curr. Opin. Insect Sci. 17, 69–73. https://doi.org/10.1016/j.cois.2016.07.004 (2016).Article 
    PubMed 

    Google Scholar 
    Lemoine, N. P., Drews, W. A., Burkepile, D. E. & Parker, J. D. Increased temperature alters feeding behavior of a generalist herbivore. Oikos 122, 1669–1678. https://doi.org/10.1111/j.1600-0706.2013.00457.x (2013).Article 

    Google Scholar 
    Vangansbeke, D. et al. Prey consumption by phytoseiid spider mite predators as affected by diurnal temperature variations. Biocontrol 60, 595–603 (2015).Article 

    Google Scholar 
    Davies, C., Coetzee, M. & Lyons, C. L. Effect of stable and fluctuating temperatures on the life history traits of Anopheles arabiensis and An. quadriannulatus under conditions of inter-and intra-specific competition. Parasit. Vectors 9, 1–9 (2016).Article 

    Google Scholar 
    Delava, E., Fleury, F. & Gibert, P. Effects of daily fluctuating temperatures on the Drosophila-Leptopilina boulardi parasitoid association. J. Therm. Biol. 60, 95–102 (2016).PubMed 
    Article 

    Google Scholar 
    Amarasekare, P. & Coutinho, R. M. Effects of temperature on intraspecific competition in ectotherms. Am. Nat. 184, E50–E65. https://doi.org/10.1086/677386 (2014).Article 
    PubMed 

    Google Scholar 
    Jiang, L. & Morin, P. J. Temperature-dependent interactions explain unexpected responses to environmental warming in communities of competitors. J. Anim. Ecol. 73, 569–576 (2004).Article 

    Google Scholar 
    Novich, R. A., Erickson, E. K., Kalinoski, R. M. & DeLong, J. P. The temperature independence of interaction strength in a sit-and-wait predator. Ecosphere 5, 1–9 (2014).Article 

    Google Scholar 
    Fox, L. R. Cannibalism in natural populations. Annu. Rev. Ecol. Syst. 6, 87–106 (1975).Article 

    Google Scholar 
    Polis, G. A. The evolution and dynamics of intraspecific predation. Annu. Rev. Ecol. Syst. 12, 225–251 (1981).Article 

    Google Scholar 
    Nishimura, K. & Isoda, Y. Evolution of cannibalism: Referring to costs of cannibalism. J. Theor. Biol. 226, 293–302. https://doi.org/10.1016/j.jtbi.2003.09.007 (2004).ADS 
    MathSciNet 
    Article 
    PubMed 
    MATH 

    Google Scholar 
    Crumrine, P. W. Body size, temperature, and seasonal differences in size structure influence the occurrence of cannibalism in larvae of the migratory dragonfly, Anax junius. Aquat. Ecol. 44, 761–770 (2010).Article 

    Google Scholar 
    Reglero, P., Urtizberea, A., Torres, A. P., Alemany, F. & Fiksen, Ø. Cannibalism among size classes of larvae may be a substantial mortality component in tuna. Mar. Ecol. Prog. Ser. 433, 205–219 (2011).ADS 
    Article 

    Google Scholar 
    Nilsson-Örtman, V., Stoks, R. & Johansson, F. Competitive interactions modify the temperature dependence of damselfly growth rates. Ecology 95, 1394–1406. https://doi.org/10.1890/13-0875.1 (2014).Article 
    PubMed 

    Google Scholar 
    Pritchard, G. & Leggott, M. Temperature, incubation rates and the origins of dragonflies. Adv. Odonatol. 3, 121–126 (1987).
    Google Scholar 
    Hassall, C. & Thompson, D. J. The effects of environmental warming on Odonata: A review. Int. J. Odonatol. 11, 131–153 (2008).Article 

    Google Scholar 
    Johansson, F. & Crowley, P. H. Larval cannibalism and population dynamics of dragonflies. In Aquatic Insects: Challenges to Populations 36–54 (CABI, 2008).Rudolf, V. H. W. & Rasmussen, N. L. Ontogenetic functional diversity: Size structure of a keystone predator drives functioning of a complex ecosystem. Ecology 94, 1046–1056 (2013).PubMed 
    Article 

    Google Scholar 
    Hyeun-Ji, L. & Johansson, F. Compensating for a bad start: Compensatory growth across life stages in an organism with a complex life cycle. Can. J. Zool. 94, 41–47 (2016).Article 

    Google Scholar 
    Sokolovska, N., Rowe, L. & Johansson, F. Fitness and body size in mature odonates. Ecol. Entomol. 25, 239–248. https://doi.org/10.1046/j.1365-2311.2000.00251.x (2000).Article 

    Google Scholar 
    Karl, T. R. Modern global climate change. Science 302, 1719–1723. https://doi.org/10.1126/science.1090228 (2003).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Meehl, G. A. et al. Climate Change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (Cambridge University Press, 2007).
    Google Scholar 
    Meehl, G. A. More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305, 994–997. https://doi.org/10.1126/science.1098704 (2004).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Khelifa, R. Spatiotemporal Pattern of Phenology Across Geographic Gradients in Insects, in Chapter 1 (Geographic Gradients in Climate Change Response Explained by Non-linear Thermal-Performance Curves) (University of Zurich, 2017).
    Google Scholar 
    Boudot, J. P. & Kalkman, V. Atlas of the European Dragonflies and Damselflies (KNNV Publishing, 2015).
    Google Scholar 
    Norling, U. Growth, winter preparations and timing of emergence in temperate zone Odonata: Control by a succession of larval response patterns. Int. J. Odonatol. 24, 1–36 (2021).Article 

    Google Scholar 
    Sniegula, S. & Johansson, F. Photoperiod affects compensating developmental rate across latitudes in the damselfly Lestes sponsa. Ecol. Entomol. 35, 149–157. https://doi.org/10.1111/j.1365-2311.2009.01164.x (2010).Article 

    Google Scholar 
    Sniegula, S., Golab, M. J. & Johansson, F. Size-mediated priority and temperature effects on intra-cohort competition and cannibalism in a damselfly. J. Anim. Ecol. 88, 637–648. https://doi.org/10.1111/1365-2656.12947 (2019).Article 
    PubMed 

    Google Scholar 
    Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675. https://doi.org/10.1038/nmeth.2089 (2012).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Benke, A. C. A method for comparing individual growth rates of aquatic insects with special reference to the Odonata. Ecology 51, 328–331 (1970).Article 

    Google Scholar 
    Nilsson-Örtman, V., Stoks, R., De Block, M. & Johansson, F. Generalists and specialists along a latitudinal transect: Patterns of thermal adaptation in six species of damselflies. Ecology 93, 1340–1352. https://doi.org/10.1890/11-1910.1 (2012).Article 
    PubMed 

    Google Scholar 
    Eklund, A. et al. Sveriges Framtida Klimat: Underlag Till Dricksvattenutredningen (SMHI, 2015).
    Google Scholar 
    McPeek, M. A. Determination of species composition in the Enallagma damselfly assemblages of permanent lakes. Ecology 71, 83–98. https://doi.org/10.2307/1940249 (1990).Article 

    Google Scholar 
    Kirillin, G. et al. FLake-global: Online lake model with worldwide coverage. Environ. Model. Softw. 26, 683–684. https://doi.org/10.1016/j.envsoft.2010.12.004 (2011).Article 

    Google Scholar 
    SMHI. Advanced Climate Change Scenario Service. https://www.smhi.se.R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2019).Suhling, F., Suhling, I. & Richter, O. Temperature response of growth of larval dragonflies–An overview. Int. J. Odonatol. 18, 15–30 (2015).Article 

    Google Scholar 
    Padfield, D., O’Sullivan, H. & Pawar, S. rTPC and nls.multstart: A new pipeline to fit thermal performance curves in R. Methods Ecol. Evol. 1, 1. https://doi.org/10.1111/2041-210X.13585 (2021).Article 

    Google Scholar 
    Kleiber, M. Body size and metabolism. Hilgardia 6, 315–353 (1932).CAS 
    Article 

    Google Scholar 
    Hemmingsen, A. Reports of the Steno Memorial Hospital and Nordisk Insulin Laboratorium. Energy Metab. Relat. Body Size Respir. Surf. Evol. 9, 6–110 (1960).
    Google Scholar 
    Dell, A. I., Pawar, S. & Savage, V. M. Systematic variation in the temperature dependence of physiological and ecological traits. Proc. Natl. Acad. Sci. 108, 10591–10596 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Logan, J. D., Wolesensky, W. & Joern, A. Temperature-dependent phenology and predation in arthropod systems. Ecol. Model. 196, 471–482. https://doi.org/10.1016/j.ecolmodel.2006.02.034 (2006).Article 

    Google Scholar 
    Pink, M. & Abrahams, M. V. Temperature and its impact on predation risk within aquatic ecosystems. Can. J. Fish. Aquat. Sci. 73, 869–876. https://doi.org/10.1139/cjfas-2015-0302 (2016).Article 

    Google Scholar 
    DeAngelis, D., Cox, D. & Coutant, C. Cannibalism and size dispersal in young-of-the-year largemouth bass: Experiment and model. Ecol. Model. 8, 133–148 (1980).Article 

    Google Scholar 
    Fagan, W. F. & Odell, G. M. Size-dependent cannibalism in praying mantids: Using biomass flux to model size-structured populations. Am. Nat. 147, 230–268 (1996).Article 

    Google Scholar 
    Dong, Q. & Deangelis, D. L. Consequences of cannibalism and competition for food in a smallmouth bass population: An individual-based modeling study. Trans. Am. Fish. Soc. 127, 174–191 (1998).Article 

    Google Scholar 
    Verheyen, J. & Stoks, R. Temperature variation makes an ectotherm more sensitive to global warming unless thermal evolution occurs. J. Anim. Ecol. 88, 624–636. https://doi.org/10.1111/1365-2656.12946 (2019).Article 
    PubMed 

    Google Scholar 
    Starr, S. M. & McIntyre, N. E. Effects of water temperature under projected climate change on the development and survival of Enallagma civile (Odonata: Coenagrionidae). Environ. Entomol. 49, 230–237. https://doi.org/10.1093/ee/nvz138 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    Culler, L. E., McPeek, M. A. & Ayres, M. P. Predation risk shapes thermal physiology of a predaceous damselfly. Oecologia 176, 653–660. https://doi.org/10.1007/s00442-014-3058-8 (2014).ADS 
    Article 
    PubMed 

    Google Scholar 
    Dokulil, M. T. et al. Increasing maximum lake surface temperature under climate change. Clim. Change https://doi.org/10.1007/s10584-021-03085-1 (2021).Article 

    Google Scholar 
    Merritt, R. W. & Cummins, K. W. An Introduction to the Aquatic Insects of North America 2nd edn. (Kendall/Hunt Publishing Company, 1984).
    Google Scholar 
    Verdonschot, R. & Peeters, E. T. Preference of larvae of Enallagma cyathigerum (Odonata: Coenagrionidae) for habitats of varying structural complexity. Eur. J. Entomol. 109, 229–234 (2012).Article 

    Google Scholar 
    McCarty, J. P., Wolfenbarger, L. L. & Wilson, J. A. eLS 1–13 (Wiley, 2017).Book 

    Google Scholar 
    Holzmann, K. L. Challenges in a Changing Climate: The Effect of Temperature Variation on Growth and Competition in Damselflies Independent thesis Advanced level (degree of Master (Two Years) thesis, Uppsala University. http://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-467582 (2022). More

  • in

    Multidecadal, continent-level analysis indicates agricultural practices impact wheat aphid loads more than climate change

    El Bilali, H., Callenius, C., Strassner, C. & Probst, L. Food and nutrition security and sustainability transitions in food systems. Food Energy Secur 8, e00154 (2019).Article 

    Google Scholar 
    De Raymond, A. B. & Goulet, F. Science, technology and food security: An introduction. Sci. Technol. Soc. 25, 7–18 (2020).Article 

    Google Scholar 
    Wang, C. et al. Occurrence of crop pests and diseases has largely increased in China since 1970. Nat. Food 3, 57–65 (2022).Article 

    Google Scholar 
    Deutsch, C. A. et al. Increase in crop losses to insect pests in a warming climate. Science 361, 916–919 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Verger, P. J. P. & Boobis, A. R. Reevaluate pesticides for food security and safety. Science 341, 717–718 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    Humann‐Guilleminot, S. et al. A nation‐wide survey of neonicotinoid insecticides in agricultural land with implications for agri‐environment schemes. J. Appl. Ecol. 56, 1502–1514 (2019).Article 
    CAS 

    Google Scholar 
    Haynes, K. J., Allstadt, A. J. & Klimetzek, D. Forest defoliator outbreaks under climate change: Effects on the frequency and severity of outbreaks of five pine insect pests. Glob. Change Biol. 20, 2004–2018 (2014).Article 

    Google Scholar 
    Sheppard, L., Bell, J. R., Harrington, R. & Reuman, D. C. Changes in large-scale climate alter spatial synchrony of aphid pests. Nat. Clim. Change 6, 610–613 (2016).Article 

    Google Scholar 
    Skendžić, S. et al. The impact of climate change on agricultural insect pests. Insects 12, 440 (2021).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    WASDE. World Agricultural Supply and Demand Estimates 1554–9089 (World Agricultural Outlook Board, 2012).FAOSTAT. Food and agriculture organisation of the United Nations. http://faostat.fao.org/ (2018).Bellard, C. et al. Impacts of climate change on the future of biodiversity. Ecol. Lett. 15, 365–377 (2012).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bebber, D. P. Range-expanding pests and pathogens in a warming world. Annu. Rev. Phytopathol. 53, 335–356 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Jactel, H., Koricheva, J. & Castagneyrol, B. Responses of forest insect pests to climate change: Not so simple. Curr. Opin. Insect Sci. 35, 103–108 (2019).PubMed 
    Article 

    Google Scholar 
    Stephane, A. P., Derocles, D. H., Lunt Sophie, C. F. & Moss., B. Climate warming alters the structure of farmland tritrophic ecological networks and reduces crop yield. Mol. Ecol. 27, 4931–4946 (2018).Article 

    Google Scholar 
    Nechols, J. R. The potential impact of climate change on non-target risks from imported generalist natural enemies and on biological control. Bio. Control 66, 37–44 (2021).
    Google Scholar 
    Tian, B. et al. Elevated temperature reduces wheat grain yield by increasing pests and decreasing soil mutualists. Pest Manag. Sci. 75, 466–475 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Lehmann, P. et al. Complex responses of global insect pests to climate warming. Front. Ecol. Environ. 18, 141–150 (2020).Article 

    Google Scholar 
    Zhao, F., Zhang, W., Hoffmann, A. A. & Ma, C. Night warming on hot days produces novel impacts on development, survival, and reproduction in a small arthropod. J. Anim. Ecol. 83, 769–778 (2014).PubMed 
    Article 

    Google Scholar 
    Marini, L. et al. Climate drivers of bark beetle outbreak dynamics in Norway spruce forests. Ecography 40, 1426–1435 (2017).Article 

    Google Scholar 
    Bale, J. S. et al. Herbivory in global climate change research: Direct effects of rising temperature on insect herbivores. Glob. Change Biol. 8, 1–16 (2002).Article 

    Google Scholar 
    Jamieson, M. A., Trowbridge, A. M., Raffa, K. F. & Lindroth, R. L. Consequences of climate warming and altered precipitation patterns for plant-insect and multitrophic interactions. Plant Physiol. 160, 1719–1727 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Gagic, V. et al. Better outcomes for pest pressure, insecticide use, and yield in less intensive agricultural landscapes. Proc. Natl Acad. Sci. USA 118, 1–6 (2021).Article 
    CAS 

    Google Scholar 
    Paredes, D. et al. Landscape simplification increases vineyard pest outbreaks and insecticide use. Ecol. Lett. 24, 73–83 (2021).PubMed 
    Article 

    Google Scholar 
    Brattsten, L. B., Holyoke, C. W., Leeper, J. R. & Raffa, K. F. Insecticide resistance: Challenge to pest management and basic research. Science 231, 1255–1260 (1986).CAS 
    PubMed 
    Article 

    Google Scholar 
    Haddi, K. et al. Rethinking biorational insecticides for pest management: Unintended effects and consequences. Pest Manag. Sci. 76, 2286–2293 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Gould, F., Brown, Z. S. & Kuzma, J. Wicked evolution: Can we address the sociobiological dilemma of pesticide resistance? Science 360, 728–732 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Wei, N. et al. Transcriptome analysis and identification of insecticide tolerance-related genes after exposure to insecticide in Sitobion avenae. Genes 1012, 951 (2019).Article 
    CAS 

    Google Scholar 
    Gong, X. et al. Feasibility of reinforced post-endogenous denitrification coupling with synchronous nitritation, denitrification and phosphorus removal for high-nitrate sewage treatment using limited carbon source in municipal wastewater. Chemosphere 269, 128687 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Tilman, D. et al. Agricultural sustainability and intensive production practices. Nature 418, 671–677 (2002).CAS 
    PubMed 
    Article 

    Google Scholar 
    Geiger, F. et al. Persistent negative effects of pesticides on biodiversity and biological control potential on European farmland. Basic Appl. Ecol. 11, 97–105 (2010).CAS 
    Article 

    Google Scholar 
    Muneret, L. et al. Evidence that organic farming promotes pest control. Nat. Sustain 1, 361–368 (2018).Article 

    Google Scholar 
    Lu, Y. et al. Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487, 362–365 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Chaplin‐Kramer, R., O’Rourke, M. E., Blitzer, E. J. & Kremen, C. A meta‐analysis of crop pest and natural enemy response to landscape complexity. Ecol. Lett. 14, 922–932 (2011).PubMed 
    Article 

    Google Scholar 
    Baillod, A. B., Tscharntke, T., Clough, Y. & Batary, P. Landscape‐scale interactions of spatial and temporal cropland heterogeneity drive biological control of cereal aphids. J. Appl. Ecol. 54, 1804–1813 (2017).Article 

    Google Scholar 
    Gagic, V. et al. Combined effects of agrochemicals and ecosystem services on crop yield across Europe. Ecol. Lett. 20, 1427–1436 (2017).PubMed 
    Article 

    Google Scholar 
    Zhang, W. et al. Multidecadal, county-level analysis of the effects of land use, Bt cotton, and weather on cotton pests in China. Proc. Natl Acad. Sci. USA 115, 700–7709 (2018).
    Google Scholar 
    Horgan, F. G. et al. Population development of rice black bug, Scotinophara latiuscula (Breddin), under varying nitrogen in a field experiment. Entomol. Gen. 37, 19–33 (2018).Article 

    Google Scholar 
    Butler, J., Garratt, M., & Leather, S. Fertilisers and insect herbivores: A meta‐analysis. Ann. Appl. Biol. 161, 223–233 (2012).Article 

    Google Scholar 
    Aqueel, M. A. et al. Effect of plant nutrition on aphid size, prey consumption, and life history characteristics of green lacewing. Insect Sci. 21, 74–82 (2014).PubMed 
    Article 

    Google Scholar 
    Benton, T. G., Vickery, J. A. & Wilson, J. D. Farmland biodiversity: Is habitat heterogeneity the key? Trends Ecol. Evol. 18, 182–188 (2003).Article 

    Google Scholar 
    Winqvist, C. et al. Mixed effects of organic farming and landscape complexity on farmland biodiversity and biological control potential across Europe. J. Appl. Ecol. 48, 570–579 (2011).Article 

    Google Scholar 
    Tscharntke, T. et al. Landscape perspectives on agricultural intensification and biodiversity-ecosystem service management. Ecol. Lett. 8, 857–874 (2005).Article 

    Google Scholar 
    Meehan, T. D., Werling, B. P., Landis, D. A. & Gratton, C. Agricultural landscape simplification and insecticide use in the Midwestern United States. Proc. Natl Acad. Sci. USA 108, 11500–11505 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Macfadyen, S. et al. Do differences in food web structure between organic and conventional farms affect the ecosystem service of pest control? Ecol. Lett. 12, 229–238 (2009).PubMed 
    Article 

    Google Scholar 
    Liu, J., Ning, J., Kuang, W. & Xu, X. Spatio-temporal patterns and characteristics of land-use change in China during 2010-2015. J. Geogr. Sci. 73, 789–802 (2018).
    Google Scholar 
    Ma, C., Ma, G. & Zhao, F. Impact of global warming on cereal aphids. Chin. J. Appl. Entomol. 51, 1435–1443 (2014).
    Google Scholar 
    Han, Z. et al. Effects of simulated climate warming on the population dynamics of Sitobion avenae (Fabricius) and its parasitoids in wheat fields. Pest Manag. Sci. 75, 3252–3259 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Meisner, M. H., Harmon, J. P. & Ives, A. R. Temperature effects on long‐term population dynamics in a parasitoid-host system. Ecol. Monogr. 84, 457–476 (2014).Article 

    Google Scholar 
    Xiao, H. et al. Exposure to mild temperatures decreases overwintering larval survival and post-diapause reproductive potential in the rice stem borer Chilo suppressalis. J. Pest Sci. 90, 117–125 (2017).Article 

    Google Scholar 
    Senior, V. L. et al. Phenological responses in a sycamore-aphid-parasitoid system and consequences for aphid population dynamics: A 20 year case study. Glob. Change Biol. 26, 2814–2828 (2020).Article 

    Google Scholar 
    Chiu, M. C., Chen, Y. H. & Kuo, M. H. The effect of experimental warming on a low‐latitude aphid, Myzus varians. Entomol. Exp. Appl. 142, 216–222 (2012).Article 

    Google Scholar 
    Adler, L. S., De Valpine, P., Harte, J. & Call, J. Effects of long-term experimental warming on aphid density in the field. J. Kans. Entomol. Soc. 80, 156–169 (2007).Article 

    Google Scholar 
    Clement, S. L., Husebye, D. S. & Eigenbrode, S. D. Aphid Biodiversity under Environmental Change 107–129 (Springer, 2010).Van der Putten, W. H., Macel, M. & Visser, M. E. Predicting species distribution and abundance responses to climate change: why it is essential to include biotic interactions across trophic levels. Philos. T. Roy. Soc. B. 365, 2025–2034 (2010).Article 

    Google Scholar 
    Evans, E. W. Multitrophic interactions among plants, aphids, alternate prey and shared natural enemies—a review. Eur. J. Entomol. 105, 369–380 (2013).Article 

    Google Scholar 
    Sigsgaard, L. A survey of aphids and aphid parasitoids in cereal fields in Denmark, and the parasitoids’ role in biological control. J. Appl. Entomol. 126, 101–107 (2002).Article 

    Google Scholar 
    Diehl, E., Sereda, E., Wolters, V. & Birkhofer, K. Effects of predator specialization, host plant and climate on biological control of aphids by natural enemies: a meta‐analysis. J. Appl. Ecol. 50, 262–270 (2013).Article 

    Google Scholar 
    Hopper, K. R. et al. Natural enemy impact on the abundance of Diuraphis noxia (Homoptera: Aphididae) in wheat in Southern France. Environ. Entomol. 24, 402–408 (1995).Article 

    Google Scholar 
    Latham, D. R. & Mills, N. J. Quantifying aphid predation: The mealy plum aphid Hyalopterus pruni in California as a case study. J. Appl. Ecol. 47, 200–208 (2010).Article 

    Google Scholar 
    Östman, Ö., Ekbom, B. & Bengtsson, J. Yield increase attributable to aphid predation by ground-living polyphagous natural enemies in spring barley in Sweden. Ecol. Econ. 45, 149–158 (2003).Article 

    Google Scholar 
    Snyder, W. E. & Ives, A. R. Interactions between specialist and generalist natural enemies: Parasitoids, predators, and pea aphid control. Ecology 84, 91–107 (2003).Article 

    Google Scholar 
    Freier, B., Triltsch, H., Möwes, M. & Moll, E. The potential of predators in natural control of aphids in wheat: results of a ten-year field study in two German landscapes. Biocontrology 52, 775–788 (2007).Article 

    Google Scholar 
    Barczak, T., Dębek-Jankowska, A. & Bennewicz, J. Primary parasitoid and hyperparasitoid guilds (Hymenoptera) of grain aphid (Sitobion avenae F.) in northern Poland. Arch. Biol. Sci. 66, 1141–1148 (2014).Article 

    Google Scholar 
    Sánchez-Bayo, F. & Wyckhuys, K. A. G. Worldwide decline of the entomofauna: A review of its drivers. Biol. Conserv. 232, 8–27 (2019).Article 

    Google Scholar 
    Seibold, S. et al. Arthropod decline in grasslands and forests is associated with landscape-level drivers. Nature 574, 671–674 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Zhang, W., Jiang, F. & Ou, J. Global pesticide consumption and pollution: With China as a focus. P. Intern. Acad. Ecol. Environ. Sci. 1, 125–144 (2011).CAS 

    Google Scholar 
    El-Wakeil, N., Gaafar, N., Sallam, A. & Volkmar, C. Side Effects of Insecticides on Natural Enemies and Possibility of their Integration in Plant Protection Strategies. Insecticides: Development of Safer and More Effective Technologies Agricultural and Biological Sciences (ed Trdan, S.) 1–56 (Intech Open Access Publisher, 2013).Peshin, R. & Dhawan, A. K. Integrated Pest Management: Innovation-Development Process (Springer Science & Business Media, 2009).Jia, B., Hong, S., Zhang, Y. & Cao, Y. Toxicity and safety of 12 insecticides to Diadegma semiclausum. J. Shanxi Agric. Sci. 43, 999–1002 (2015).
    Google Scholar 
    Emery, S. E. et al. High agricultural intensity at the landscape scale benefits pests, but low intensity practices at the local scale can mitigate these effects. Agric. Ecosyst. Environ. 306, 107199 (2021).Article 

    Google Scholar 
    Aqueel, M. A. & Leather, S. R. Effect of nitrogen fertilizer on the growth and survival of Rhopalosiphum padi (L.) and Sitobion avenae (F.)(Homoptera: Aphididae) on different wheat cultivars. Crop. Prot. 30, 216–221 (2011).Article 

    Google Scholar 
    Gao, J., Guo, H. J., Sun, Y. C. & Ge, F. Juvenile hormone mediates the positive effects of nitrogen fertilization on weight and reproduction in pea aphid. Pest Manag. Sci. 74, 2511–2519 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Barnett, K. L. & Facey, S. L. Grasslands, invertebrates, and precipitation: A review of the effects of climate change. Front. Plant. Sci. 7, 1196 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Yu, X. et al. Engineering plants for aphid resistance: Current status and future perspectives. Theor. Appl. Genet. 127, 2065–2083 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    Martin, E. A. et al. The interplay of landscape composition and configuration: New pathways to manage functional biodiversity and agroecosystem services across Europe. Ecol. Lett. 22, 1083–1094 (2019).PubMed 
    Article 

    Google Scholar 
    Steckel, J. et al. Landscape composition and configuration differently affect trap-nesting bees, wasps and their antagonists. Biol. Conserv. 172, 56–64 (2014).Article 

    Google Scholar 
    Lu, Y. H. et al. Major ecosystems in China: Dynamics and challenges for sustainable management. Environ. Manag. 48, 13–27 (2011).Article 

    Google Scholar 
    Wood, G. A. et al. Real-time measures of canopy size as a basis for spatially varying nitroge applications to winter wheat sown at different seed rates. Biosyst. Eng. 84, 513–531 (2003).Article 

    Google Scholar 
    NOAA. https://www.ncdc.noaa.gov/cdo-web/ (2018).WORLD BANK GROUP. https://climateknowledgeportal.worldbank.org/download-data (2018). More

  • in

    Post-foraging in-colony behaviour of a central-place foraging seabird

    Naef-Daenzer, B. Patch time allocation and patch sampling by foraging great and blue tits. Anim. Behav. 59, 989–999 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    Kotler, B. P., Brown, J. S. & Bouskila, A. Apprehension and time allocation in gerbils: The effects of predatory risk and energetic state. Ecology 85, 917–922 (2004).Article 

    Google Scholar 
    Wajnberg, E., Bernhard, P., Hamelin, F. & Boivin, G. Optimal patch time allocation for time-limited foragers. Behav. Ecol. Sociobiol. 60, 1–10 (2006).Article 

    Google Scholar 
    Embar, K., Kotler, B. P. & Mukherjee, S. Risk management in optimal foragers: The effect of sightlines and predator type on patch use, time allocation, and vigilance in gerbils. Oikos 120, 1657–1666 (2011).Article 

    Google Scholar 
    Lima, S. L. & Bednekoff, P. A. Temporal variation in danger drives antipredator behavior: The predation risk allocation hypothesis. Am. Nat. 153, 649–659 (1999).PubMed 
    Article 

    Google Scholar 
    Beauchamp, G. & Ruxton, G. D. A reassessment of the predation risk allocation hypothesis: A comment on Lima and Bednekoff. Am. Nat. 177, 143–146 (2011).PubMed 
    Article 

    Google Scholar 
    Ferrari, M. C. O., Sih, A. & Chivers, D. P. The paradox of risk allocation: A review and prospectus. Anim. Behav. 78, 579–585 (2009).Article 

    Google Scholar 
    Wolf, L. L. & Hainsworth, F. R. Foraging efficiencies and time budgets in nectar-feeding birds. Ecology 56, 117–128 (1975).Article 

    Google Scholar 
    Litzow, M. A. & Piatt, J. F. Variance in prey abundance influences time budgets of breeding seabirds: Evidence from pigeon guillemots Cepphus columba. J. Avian Biol. 34, 54–64 (2003).Article 

    Google Scholar 
    Rishworth, G. M., Tremblay, Y. & Green, D. B. Drivers of time-activity budget variability during breeding in a pelagic seabird. PLoS One 9, e116544 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Stephens, D. W., Brown, J. S. & Ydenberg, R. C. Foraging: Behavior and Ecology. (The University of Chicago Press, 2007).Orians, G. & Pearson, N. On the theory of central place foraging. In Analysis of Ecological Systems (eds. Horn, D., Mitchell, R. & Stairs, G.) 154–177 (The Ohio State University Press, 1979).Chaurand, T. & Weimerskirch, H. The regular alternation of short and long foraging trips in the blue petrel Halobaena caerulea: A previously undescribed strategy of food provisioning in a pelagic seabird. J. Anim. Ecol. 63, 275–282 (1994).Article 

    Google Scholar 
    Weimerskirch, H. et al. Alternate long and short foraging trips in pelagic seabird parents. Anim. Behav. 47, 472–476 (1994).Article 

    Google Scholar 
    Welcker, J., Beiersdorf, A., Varpe, Ø. & Steen, H. Mass fluctuations suggest different functions of bimodal foraging trips in a central-place forager. Behav. Ecol. 23, 1372–1378 (2012).Article 

    Google Scholar 
    Welcker, J. et al. Flexibility in the bimodal foraging strategy of a high Arctic alcid, the little auk Alle alle. J. Avian Biol. 40, 388–399 (2009).Article 

    Google Scholar 
    Jakubas, D., Wojczulanis-Jakubas, K., Iliszko, L. M. & Kidawa, D. Flexibility of little auks foraging in various oceanographic features in a changing Arctic. Sci. Rep. https://doi.org/10.1038/s41598-020-65210-x (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Shoji, A. et al. Dual foraging and pair coordination during chick provisioning by Manx shearwaters: Empirical evidence supported by a simple model. J. Exp. Biol. 218, 2116–2123 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    Phillips, R. A., Wakefield, E. D., Croxall, J. P., Fukuda, A. & Higuchi, H. Albatross foraging behaviour: No evidence for dual foraging, and limited support for anticipatory regulation of provisioning at South Georgia. Mar. Ecol. Prog. Ser. 391, 279–292 (2009).ADS 
    Article 

    Google Scholar 
    Brown, Z. W., Welcker, J., Harding, A. M. A., Walkusz, W. & Karnovsky, N. J. Divergent diving behavior during short and long trips of a bimodal forager, the little auk Alle alle. J. Avian Biol. 43, 215–226 (2012).Article 

    Google Scholar 
    Baduini, C. L. & Hyrenbach, K. D. Biogeography of procellariiform foraging strategies: Does ocean productivity influence provisioning?. Mar. Ornithol. 31, 101–112 (2003).
    Google Scholar 
    Navarro, J. & González-Solís, J. Environmental determinants of foraging strategies in Cory’s shearwaters Calonectris diomedea. Mar. Ecol. Prog. Ser. 378, 259–267 (2009).ADS 
    CAS 
    Article 

    Google Scholar 
    Ochi, D., Oka, N. & Watanuki, Y. Foraging trip decisions by the streaked shearwater Calonectris leucomelas depend on both parental and chick state. J. Ethol. 28, 313–321 (2010).Article 

    Google Scholar 
    Congdon, B. C., Krockenberger, A. K. & Smithers, B. V. Dual-foraging and co-ordinated provisioning in a tropical Procellariiform, the wedge-tailed shearwater. Mar. Ecol. Prog. Ser. 301, 293–301 (2005).ADS 
    Article 

    Google Scholar 
    Peck, D. R. & Congdon, B. C. Colony-specific foraging behaviour and co-ordinated divergence of chick development in the wedge-tailed shearwater Puffinus pacificus. Mar. Ecol. Prog. Ser. 299, 289–296 (2005).ADS 
    Article 

    Google Scholar 
    Weimerskirch, H. How can a pelagic seabird provision its chick when relying on a distant food resource? Cyclic attendance at the colony, foraging decision and body condition in sooty shearwaters. J. Anim. Ecol. 67, 99–109 (1998).Article 

    Google Scholar 
    Stempniewicz, L. BWP update. Little Auk (Alle alle). J. Birds West. Palearct. 3, 175–201 (2001).
    Google Scholar 
    Wojczulanis-Jakubas, K. & Jakubas, D. When and why does my mother leave me? The question of brood desertion in the Dovekie (Alle Alle). Auk 129, 632–637 (2012).Article 

    Google Scholar 
    Harding, A. M. A., Van Pelt, T. I., Lifjeld, J. T. & Mehlum, F. Sex differences in little auk Alle alle parental care: Transition from biparental to paternal-only care. Ibis (Lond. 1859). 146, 642–651 (2004).Article 

    Google Scholar 
    Wojczulanis-Jakubas, K. et al. Duration of female parental care and their survival in the little auk Alle alle—Are these two traits linked ?. Behav. Ecol. Sociobiol. 74, 1–11 (2020).Article 

    Google Scholar 
    Wojczulanis, K., Dariusz, J. & Lech, S. The Little Auk Alle alle: An ecological indicator of a changing Arctic and a model organism. Polar Biol. https://doi.org/10.1007/s00300-021-02981-7 (2021).Article 

    Google Scholar 
    Steen, H., Vogedes, D., Broms, F., Falk-Petersen, S. & Berge, J. Little auks (Alle alle) breeding in a High Arctic fjord system: Bimodal foraging strategies as a response to poor food quality?. Polar Res. 26, 118–125 (2007).Article 

    Google Scholar 
    Wojczulanis-Jakubas, K., Jakubas, D., Karnovsky, N. J. & Walkusz, W. Foraging strategy of little auks under divergent conditions on feeding grounds. Polar Res. 29, 22–29 (2010).Article 

    Google Scholar 
    Jakubas, D., Wojczulanis-Jakubas, K., Iliszko, L., Darecki, M. & Stempniewicz, L. Foraging strategy of the little auk Alle alle throughout breeding season—switch from unimodal to bimodal pattern. J. Avian Biol. 45, 551–560 (2014).Article 

    Google Scholar 
    Jakubas, D., Iliszko, L., Wojczulanis-Jakubas, K. & Stempniewicz, L. Foraging by little auks in the distant marginal sea ice zone during the chick-rearing period. Polar Biol. 35, 73–81 (2012).Article 

    Google Scholar 
    Jakubas, D. et al. Intra-seasonal variation in zooplankton availability, chick diet and breeding performance of a high Arctic planktivorous seabird. Polar Biol. 391, 1547–1561 (2016).Article 

    Google Scholar 
    Jakubas, D. et al. Foraging closer to the colony leads to faster growth in little auks. Mar. Ecol. Prog. Ser. 489, 263–278 (2013).ADS 
    Article 

    Google Scholar 
    Stempniewicz, L. Predator-prey interactions between Glaucous Gull Larus hyperboreus and Little Auk Alle alle in Spitsbergen. Acta Ornithol. 29, 155–170 (1995).
    Google Scholar 
    Wojczulanis-Jakubas, K., Jakubas, D. & Stempniewicz, L. Changes in the glaucous gull predatory pressure on little auks in Southwest Spitsbergen. Waterbirds 28, 430–435 (2005).Article 

    Google Scholar 
    Kharitonov, S. Methods and Theoretical Aspects of Seabird Studies. (Proc 5 All-Russian Mar Biol School, Marine Biological Institute, 2007).Wojczulanis-Jakubas, K., Jakubas, D. & Stempniewicz, L. Avifauna of Hornsund area, SW Spitsbergen: Present state and recent changes. Polish Polar Res. 29, 187–197 (2008).
    Google Scholar 
    Keslinka, K. L., Wojczulanis-Jakubas, K., Jakubas, D. & Neubauer, G. Determinants of the little auk (Alle alle) breeding colony location and size in W and NW coast of Spitsbergen. PLoS One 14, 1–20 (2019).
    Google Scholar 
    Kidawa, D., Barcikowski, M. & Palme, R. Parent-offspring interactions in a long-lived seabird, the Little Auk (Alle alle): Begging and provisioning under simulated stress. J. Ornithol. 158, 145–157 (2017).Article 

    Google Scholar 
    Welcker, J., Beiersdorf, A., Varpe, Ø. & Steen, H. Mass fluctuations suggest different functions of bimodal foraging trips in a central-place forager. Behav. Ecol. https://doi.org/10.1093/beheco/ars131 (2012).Article 

    Google Scholar 
    Jakubas, D. & Wojczulanis, K. Predicting the sex of Dovekies by discriminant analysis. Waterbirds 30, 92–96 (2007).Article 

    Google Scholar 
    Grissot, A. et al. Parental coordination of chick provisioning in a planktivorous arctic seabird under divergent conditions on foraging grounds. Front. Ecol. Evol. 7, 349 (2019).Article 

    Google Scholar 
    Stoffel, M. A., Nakagawa, S. & Schielzeth, H. rptR: Repeatability estimation and variance decomposition by generalized linear mixed-effects models. Methods Ecol. Evol. 8, 1639–1644 (2017).Article 

    Google Scholar 
    R Core Team. R: A Language and Environment for Statistical Computing. R. (2019).Wojczulanis-Jakubas, K., Jakubas, D. & Stempniewicz, L. Sex-specific parental care by incubating Little Auks (Alle alle). Ornis Fenn. 86, 140–148 (2009).
    Google Scholar 
    Welcker, J., Steen, H., Harding, A. M. A. & Gabrielsen, G. W. Sex-specific provisioning behaviour in a monomorphic seabird with a bimodal foraging strategy. Ibis (Lond. 1859). 151, 502–513 (2009).Article 

    Google Scholar 
    Kidawa, D. et al. Parental efforts of an Arctic seabird, the little auk Alle alle under variable foraging conditions. Mar. Biol. Res. 11, 349–360 (2015).Article 

    Google Scholar 
    Wickham, H. Hadley Wickham. Media 35, 211 (2009).
    Google Scholar 
    Karnovsky, N. J. et al. Inter-colony comparison of diving behavior of an Arctic top predator: Implications for warming in the Greenland Sea. Mar. Ecol. Prog. Ser. 440, 229–240 (2011).ADS 
    Article 

    Google Scholar 
    Karnovsky, N. et al. Foraging distributions of little auks Alle alle across the Greenland Sea: Implications of present and future Arctic climate change. Mar. Ecol. Prog. Ser. 415, 283–293 (2010).ADS 
    Article 

    Google Scholar 
    Gremillet, D. et al. Little auks buffer the impact of current Arctic climate change. Mar. Ecol. Prog. Ser. 454, 197–206 (2012).ADS 
    Article 

    Google Scholar 
    Harding, A. M. A. et al. Flexibility in the parental effort of an Arctic-breeding seabird. Funct. Ecol. 23, 348–358 (2009).Article 

    Google Scholar 
    Jakubas, D. et al. Foraging effort does not influence body condition and stress level in little auks. Mar. Ecol. Prog. Ser. 432, 277–290 (2011).ADS 
    Article 

    Google Scholar 
    Jakubas, D., Wojczulanis-Jakubas, K., Iliszko, L. M., Strøm, H. & Stempniewicz, L. Habitat foraging niche of a High Arctic zooplanktivorous seabird in a changing environment. Sci. Rep. 7, 1–14 (2017).CAS 
    Article 

    Google Scholar  More

  • in

    Increased incompatibility of heterologous algal symbionts under thermal stress in the cnidarian-dinoflagellate model Aiptasia

    Sylvan, J. How to protect a coral reef: the public trust doctrine and the law of the sea recommended citation. Sustain. Dev. Law Policy 7, 12 (2006).
    Google Scholar 
    LaJeunesse, T. C. et al. Systematic revision of symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr. Biol. 28, 2570–2580.e6 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Kopp, C. et al. Highly dynamic cellular-level response of symbiotic coral to a sudden increase in environmental nitrogen. mBio 4, e00052–13 (2013).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Muscatine, L. The role of symbiotic algae in carbon and energy flux in reef corals. Coral Reef. 25, 75–87 (1990).
    Google Scholar 
    Dubinsky, Z. & Stambler, N. Coral reefs: an ecosystem in transition. (Springer, 2011).Wiedenmann, J. et al. Nutrient enrichment can increase the susceptibility of reef corals to bleaching. https://doi.org/10.1038/NCLIMATE1661 (2012).Suggett, D. J., Warner, M. E. & Leggat, W. Symbiotic dinoflagellate functional diversity mediates coral survival under ecological crisis. Trends Ecol. Evolution 32, 735–745 (2017).Article 

    Google Scholar 
    Morris, L. A., Voolstra, C. R., Quigley, K. M., Bourne, D. G. & Bay, L. K. Nutrient availability and metabolism affect the stability of coral–symbiodiniaceae symbioses. Trends Microbiol. 27, 678–689 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Lehnert, E. M. et al. Extensive differences in gene expression between symbiotic and aposymbiotic cnidarians. G3 (Bethesda) 4, 277–95 (2014).CAS 
    Article 

    Google Scholar 
    Dubinsky, Z. & Berman-Frank, I. Uncoupling primary production from population growth in photosynthesizing organisms in aquatic ecosystems. in. Aquat. Sci. 63, 4–17 (2001).CAS 
    Article 

    Google Scholar 
    Burriesci, M. S., Raab, T. K. & Pringle, J. R. Evidence that glucose is the major transferred metabolite in dinoflagellate–cnidarian symbiosis. J. Exp. Biol. 215, 3467–3477 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Davy, S. K., Allemand, D. & Weis, V. M. Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol. Mol. Biol. Rev. 76, 229–61 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rädecker, N., Pogoreutz, C., Voolstra, C. R., Wiedenmann, J. & Wild, C. Nitrogen cycling in corals: the key to understanding holobiont functioning? Trends Microbiol. 23, 490–497 (2015).PubMed 
    Article 
    CAS 

    Google Scholar 
    Cui, G. et al. Host-dependent nitrogen recycling as a mechanism of symbiont control in Aiptasia. PLOS Genet. 15, e1008189 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rädecker, N. et al. Heat stress destabilizes symbiotic nutrient cycling in corals. Proc. Natl Acad. Sci. USA 118, https://doi.org/10.1073/pnas.2022653118 (2021).Weis, V. M. Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. J. Exp. Biol. 211, 3059–3066 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    Wooldridge, S. A. Breakdown of the coral-algae symbiosis: towards formalising a linkage between warm-water bleaching thresholds and the growth rate of the intracellular zooxanthellae. Biogeosciences Discuss. 9, 8111–8139 (2012).
    Google Scholar 
    Cziesielski, M. J., Schmidt‐Roach, S. & Aranda, M. The past, present, and future of coral heat stress studies. Ecol. Evol. https://doi.org/10.1002/ece3.5576 (2019).Leggat, W. et al. Differential responses of the coral host and their algal symbiont to thermal stress. PLoS ONE 6, e26687 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Pinzón, J. H. et al. Whole transcriptome analysis reveals changes in expression of immune-related genes during and after bleaching in a reef-building coral. R. Soc. Open Sci. 2, 140214 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Ziegler, M., Seneca, F. O., Yum, L. K., Palumbi, S. R. & Voolstra, C. R. Bacterial community dynamics are linked to patterns of coral heat tolerance. Nat. Commun. 8, 14213 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bang, C. et al. Metaorganisms in extreme environments: do microbes play a role in organismal adaptation? Zoology 127, 1–19 (2018).PubMed 
    Article 

    Google Scholar 
    Berkelmans, R. & van Oppen, M. J. H. The role of zooxanthellae in the thermal tolerance of corals: a “nugget of hope” for coral reefs in an era of climate change. Proc. Biol. Sci./R. Soc. 273, 2305–12 (2006).
    Google Scholar 
    Sampayo, E. M., Ridgway, T., Bongaerts, P. & Hoegh-Guldberg, O. Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proc. Natl Acad. Sci. 105, 10444–10449 (2008).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Howells, E. J. et al. Coral thermal tolerance shaped by local adaptation of photosymbionts. Nat. Clim. Change https://doi.org/10.1038/nclimate1330 (2011).Cziesielski, M. J. et al. Multi-omics analysis of thermal stress response in a zooxanthellate cnidarian reveals the importance of associating with thermotolerant symbionts. Proc. Biol. Sci. 285, 20172654 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    Baker, A. C., Starger, C. J., McClanahan, T. R. & Glynn, P. W. Corals’ adaptive response to climate change. Nature 430, 741–741 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    Thornhill, D. J., LaJeunesse, T. C., Kemp, D. W., Fitt, W. K. & Schmidt, G. W. Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Mar. Biol. 148, 711–722 (2006).Article 

    Google Scholar 
    Palumbi, S. R., Barshis, D. J., Traylor-Knowles, N. & Bay, R. A. Mechanisms of reef coral resistance to environmental stress,making its relative ability to acclimate or adapt extremely important to the to future climate change. Science 344, 895–898 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    Herrera, M. et al. Temperature transcends partner specificity in the symbiosis establishment of a cnidarian. ISME J. 15, 141–153 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Howells, E. J. et al. Corals in the hottest reefs in the world exhibit symbiont fidelity not flexibility. Mol. Ecol. 29, 899–911 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Hume, B. C. C., Mejia-Restrepo, A., Voolstra, C. R. & Berumen, M. L. Fine-scale delineation of Symbiodiniaceae genotypes on a previously bleached central Red Sea reef system demonstrates a prevalence of coral host-specific associations. Coral Reefs 1–19 https://doi.org/10.1007/s00338-020-01917-7 (2020).Perez, S. F., Cook, C. B. & Brooks, W. R. The role of symbiotic dinoflagellates in the temperature-induced bleaching response of the subtropical sea anemone Aiptasia pallida. J. Exp. Mar. Biol. Ecol. 256, 1–14 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    Mieog, J. C. et al. The roles and interactions of symbiont, host and environment in defining coral fitness. PLoS ONE 4, e6364 (2009).Cantin, N. E., van Oppen, M. J. H., Willis, B. L., Mieog, J. C. & Negri, A. P. Juvenile corals can acquire more carbon from high-performance algal symbionts. Coral Reefs 28, 405–414 (2009).Article 

    Google Scholar 
    Herrera, M. et al. Unfamiliar partnerships limit cnidarian holobiont acclimation to warming. Glob. Change Biol. 26, 5539–5553 (2020).Article 

    Google Scholar 
    LaJeunesse, T. et al. Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Mar. Ecol. Prog. Ser. 284, 147–161 (2004).Article 

    Google Scholar 
    Parkinson, J. E. & Baums, I. B. The extended phenotypes of marine symbioses: ecological and evolutionary consequences of intraspecific genetic diversity in coral-algal associations. Front. Microbiol. 5, 445 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Coffroth, M. A., Poland, D. M., Petrou, E. L., Brazeau, D. A. & Holmberg, J. C. Environmental symbiont acquisition may not be the solution to warming seas for reef-building corals. PLoS ONE 5, e13258 (2010).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Bellantuono, A. J., Granados-Cifuentes, C., Miller, D. J., Hoegh-Guldberg, O. & Rodriguez-Lanetty, M. Coral thermal tolerance: tuning gene expression to resist thermal stress. PLoS ONE 7, e50685 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Sunagawa, S. et al. Generation and analysis of transcriptomic resources for a model system on the rise: the sea anemone Aiptasia pallida and its dinoflagellate endosymbiont. BMC Genomics 10, 258 (2009).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Baumgarten, S. et al. The genome of Aiptasia, a sea anemone model for coral symbiosis. Proc. Natl Acad. Sci. 112, 201513318 (2015).
    Google Scholar 
    Matthews, J. L. et al. Menthol-induced bleaching rapidly and effectively provides experimental aposymbiotic sea anemones (Aiptasia sp.) for symbiosis investigations. J. Exp. Biol. jeb.128934 https://doi.org/10.1242/JEB.128934 (2015).Kenkel, C. D. et al. Evidence for a host role in thermotolerance divergence between populations of the mustard hill coral (Porites astreoides) from different reef environments. Mol. Ecol. 22, 4335–4348 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    Polato, N. R., Altman, N. S. & Baums, I. B. Variation in the transcriptional response of threatened coral larvae to elevated temperatures. Mol. Ecol. 22, 1366–1382 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    DeSalvo, M., Sunagawa, S., Voolstra, C. R. & Medina, M. Transcriptomic resonses to heat stress and bleaching in the elkhorn coral Acropora palmata. Mar. Ecol. Prog. Ser. 402, 97–113 (2010).CAS 
    Article 

    Google Scholar 
    Maor-Landaw, K. & Levy, O. Gene expression profiles during short-term heat stress; branching vs. massive Scleractinian corals of the Red Sea. PeerJ 4, e1814 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Yamamoto, K. et al. Control of the heat stress-induced alternative splicing of a subset of genes by hnRNP K. Genes Cells 21, 1006–1014 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    Seneca, F. O. & Palumbi, S. R. The role of transcriptome resilience in resistance of corals to bleaching. Mol. Ecol. 24, 1467–1484 (2015).PubMed 
    Article 

    Google Scholar 
    Meyer, E. & Weis, V. M. Study of cnidarian-algal symbiosis in the “omics” age. Biol. Bull. 223, 44–65 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Oakley, C. A. et al. Thermal shock induces host proteostasis disruption and endoplasmic reticulum stress in the model symbiotic Cnidarian Aiptasia. J. Proteome Res. 16, 2121–2134 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    Robbart, M. L., Peckol, P., Scordilis, S. P., Curran, H. A. & Brown-Saracino, J. Population recovery and differential heat shock protein expression for the corals Agaricia agaricites and A-tenuifolia in Belize. Mar. Ecol. Prog. Ser. 283, 151–160 (2004).Article 

    Google Scholar 
    Barshis, D. J. et al. Genomic basis for coral resilience to climate change. Proc. Natl Acad. Sci. 110, 1387–1392 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Traylor-Knowles, N., Rose, N. H. & Palumbi, S. R. The cell specificity of gene expression in the response to heat stress in corals. J. Exp. Biol. 220, 1837–1845 (2017).PubMed 

    Google Scholar 
    Benchimol, S. p53-dependent pathways of apoptosis. Cell Death Differ. 8, 1049–1051 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    Moya, A. et al. Functional conservation of the apoptotic machinery from coral to man: The diverse and complex Bcl-2 and caspase repertoires of Acropora millepora. BMC Genomics 17, 62 (2016).Elmore, S. Apoptosis: a review of programmed cell death. Toxicol. Pathol. 35, 495–516 (2007).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Karim, W., Nakaema, S. & Hidaka, M. Temperature effects on the growth rates and photosynthetic activities of symbiodinium cells. J. Mar. Sci. Eng. 3, 368–381 (2015).Article 

    Google Scholar 
    Cunning, R. & Baker, A. C. Excess algal symbionts increase the susceptibility of reef corals to bleaching. Nat. Clim. Change 3, 259–262 (2013).Article 

    Google Scholar 
    Rehman, A. U. et al. Symbiodinium sp. cells produce light-induced intra- and extracellular singlet oxygen, which mediates photodamage of the photosynthetic apparatus and has the potential to interact with the animal host in coral symbiosis. N. Phytologist 212, 472–484 (2016).CAS 
    Article 

    Google Scholar 
    Lesser, K. B. & Garcia, F. A. Association between polycystic ovary syndrome and glucose intolerance during pregnancy. J. Matern. Fetal Med. 6, 303–307 (1997).CAS 
    PubMed 
    Article 

    Google Scholar 
    Dunn, S. R., Schnitzler, C. E. & Weis, V. M. Apoptosis and autophagy as mechanisms of dinoflagellate symbiont release during cnidarian bleaching: every which way you lose. Proc. R. Soc. Lond. B: Biol. Sci. 274, 3079–3085 (2007).
    Google Scholar 
    DeSalvo, M. K. et al. Coral host transcriptomic states are correlated with Symbiodinium genotypes. Mol. Ecol. 19, 1174–1186 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    Levin, R. A. et al. Engineering strategies to decode and enhance the genomes of coral symbionts. Front. Microbiol. https://doi.org/10.3389/fmicb.2017.01220 (2017).Yuyama, I., Ishikawa, M., Nozawa, M., Yoshida, M. & Ikeo, K. Transcriptomic changes with increasing algal symbiont reveal the detailed process underlying establishment of coral-algal symbiosis. Sci. Rep. 8, 16802 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Sproles, A. E. et al. Sub-cellular imaging shows reduced photosynthetic carbon and increased nitrogen assimilation by the non-native endosymbiont Durusdinium trenchii in the model cnidarian Aiptasia. Environ. Microbiol. 22, 3741–3753 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Rädecker, N. et al. Using Aiptasia as a model to study metabolic interactions in Cnidarian-Symbiodinium symbioses. Front. Physiol. 9, 214 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Falkowski, P. G., Dubinsky, Z., Muscatine, L. & McCloskey, L. Population control in symbiotic corals. BioScience 43, 606–611 (1993).Article 

    Google Scholar 
    Wang & Douglas. Nitrogen recycling or nitrogen conservation in an alga-invertebrate symbiosis? J. Exp. Biol. 201, 2445–53 (1998).Loram, J. E., Trapido-Rosenthal, H. G. & Douglas, A. E. Functional significance of genetically different symbiotic algae Symbiodinium in a coral reef symbiosis. Mol. Ecol. 16, 4849–4857 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    Karako-Lampert, S. et al. Transcriptome analysis of the scleractinian coral Stylophora pistillata. PLoS One 9, e88615 (2014).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Hillyer, K. E., Tumanov, S., Villas-Bôas, S. & Davy, S. K. Metabolite profiling of symbiont and host during thermal stress and bleaching in a model cnidarian-dinoflagellate symbiosis. J. Exp. Biol. 219, 516–27 (2016).PubMed 

    Google Scholar 
    Bertucci, A., Forêt, S., Ball, E. E. & Miller, D. J. Transcriptomic differences between day and night in Acropora millepora provide new insights into metabolite exchange and light-enhanced calcification in corals. Mol. Ecol. 24, 4489–4504 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Matthews, J. L. et al. Optimal nutrient exchange and immune responses operate in partner specificity in the cnidarian-dinoflagellate symbiosis. Proc. Natl Acad. Sci. 114, 13194–13199 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Lin, M.-F., Takahashi, S., Forêt, S., Davy, S. K. & Miller, D. J. Transcriptomic analyses highlight the likely metabolic consequences of colonization of a cnidarian host by native or non-native Symbiodinium species. Biol. Open 8, bio038281 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Medrano, E., Merselis, D. G., Bellantuono, A. J. & Rodriguez-Lanetty, M. Proteomic Basis of Symbiosis: A Heterologous Partner Fails to Duplicate Homologous Colonization in a Novel Cnidarian– Symbiodiniaceae Mutualism. Front. Microbiol. 10, 1153 (2019).Schoepf, V., Stat, M., Falter, J. L. & McCulloch, M. T. Limits to the thermal tolerance of corals adapted to a highly fluctuating, naturally extreme temperature environment. Sci. Rep. 5, 17639 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Xiang, T., Hambleton, E. A., DeNofrio, J. C., Pringle, J. R. & Grossman, A. R. Isolation of clonal axenic strains of the symbiotic dinoflagellate Symbiodinium and their growth and host specificity1. J. Phycol. 49, 447–458 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    Bray, N. L., Pimentel, H., Melsted, P. & Pachter, L. Near-optimal probabilistic RNA-seq quantification. Nat. Biotechnol. 34, 525–527 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    Pimentel, H., Bray, N. L., Puente, S., Melsted, P. & Pachter, L. Differential analysis of RNA-seq incorporating quantification uncertainty. Nat. Methods 14, 687–690 (2017).CAS 
    PubMed 
    Article 

    Google Scholar  More

  • in

    The response of wheat and its microbiome to contemporary and historical water stress in a field experiment

    IPCC. Summary for policymakers. In: Climate change 2021: the physical science basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Masson-Delmotte, V, Zhai P, Pirani A, Connors S L, Péan C, Berger S, et al. Editors. Cambridge, UK and New York, NY, USA: Cambridge University Press. 2021. https://doi.org/10.1017/9781009157896.Zhang J, Zhang S, Cheng M, Jiang H, Zhang X, Peng C, et al. Effect of drought on agronomic traits of rice and wheat: a meta-analysis. Int J Environ Res Public Health. 2018;15:839.Article 

    Google Scholar 
    FAO. Global agriculture towards 2050, high-level expert forum, how to feed the world 2050. Rome: Food and Agriculture Organization of United Nations FAO. 2009.Agoussar A, Yergeau E. Engineering the plant microbiota in the context of the theory of ecological communities. Curr Opin Biotechnol. 2021;70:220–5.CAS 
    Article 

    Google Scholar 
    Quiza L, St-Arnaud M, Yergeau E. Harnessing phytomicrobiome signaling for rhizosphere microbiome engineering. Front Plant Sci. 2015;6:507.Article 

    Google Scholar 
    Mitter B, Pfaffenbichler N, Flavell R, Compant S, Antonielli L, Petric A, et al. A new approach to modify plant microbiomes and traits by introducing beneficial bacteria at flowering into progeny seeds. Front Microbiol. 2017;8. https://doi.org/10.3389/fmicb.2017.00011.Li X, Jousset A, de Boer W, Carrión VJ, Zhang T, Wang X, et al. Legacy of land use history determines reprogramming of plant physiology by soil microbiome. ISME J. 2019;13:738–51.CAS 
    Article 

    Google Scholar 
    Nelson EB, Simoneau P, Barret M, Mitter B, Compant S. Editorial special issue: the soil, the seed, the microbes and the plant. Plant Soil. 2018;422:1–5.CAS 
    Article 

    Google Scholar 
    Trivedi P, Leach JE, Tringe SG, Sa T, Singh BK. Plant–microbiome interactions: from community assembly to plant health. Nat Rev Microbiol. 2020;18:607–21.CAS 
    Article 

    Google Scholar 
    Moroenyane I, Tremblay J, Yergeau E. Soybean microbiome recovery after disruption is modulated by the seed and not the soil microbiome. Phytobiomes J. 2021;5:418–31.Article 

    Google Scholar 
    Xiong C, Zhu Y-G, Wang J-T, Singh B, Han L-L, Shen J-P, et al. Host selection shapes crop microbiome assembly and network complexity. New Phytol. 2021;229:1091–104.CAS 
    Article 

    Google Scholar 
    Schimel J, Balser TC, Wallenstein M. Microbial stress-response physiology and its implications for ecosystem function. Ecology. 2007;88:1386–94.Article 

    Google Scholar 
    Allison SD, Martiny JBH. Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci USA. 2008;105:11512–9.CAS 
    Article 

    Google Scholar 
    Bouskill NJ, Lim HC, Borglin S, Salve R, Wood TE, Silver WL, et al. Pre-exposure to drought increases the resistance of tropical forest soil bacterial communities to extended drought. ISME J. 2013;7:384–94.CAS 
    Article 

    Google Scholar 
    Evans SE, Wallenstein MD. Soil microbial community response to drying and rewetting stress: does historical precipitation regime matter? Biogeochemistry. 2012;109:101–16.Article 

    Google Scholar 
    Meisner A, Snoek BL, Nesme J, Dent E, Jacquiod S, Classen AT, et al. Soil microbial legacies differ following drying-rewetting and freezing-thawing cycles. ISME J. 2021;15:1207–21.CAS 
    Article 

    Google Scholar 
    Azarbad H, Constant P, Giard-Laliberté C, Bainard LD, Yergeau E. Water stress history and wheat genotype modulate rhizosphere microbial response to drought. Soil Biol Biochem. 2018;126:228–36.CAS 
    Article 

    Google Scholar 
    Jones DL, Nguyen C, Finlay RD. Carbon flow in the rhizosphere: carbon trading at the soil–root interface. Plant Soil. 2009;321:5–33.CAS 
    Article 

    Google Scholar 
    Sasse J, Martinoia E, Northen T. Feed your friends: do plant exudates shape the root microbiome? Trends Plant Sci. 2018;23:25–41.CAS 
    Article 

    Google Scholar 
    Holz M, Zarebanadkouki M, Kuzyakov Y, Pausch J, Carminati A. Root hairs increase rhizosphere extension and carbon input to soil. Ann Bot. 2018;121:61–9.CAS 
    Article 

    Google Scholar 
    Marasco R, Rolli E, Ettoumi B, Vigani G, Mapelli F, Borin S, et al. A drought resistance-promoting microbiome is selected by root system under desert farming. PLoS ONE. 2012;7:e48479.CAS 
    Article 

    Google Scholar 
    Moroenyane I, Mendes L, Tremblay J, Tripathi B, Yergeau É. Plant compartments and developmental stages modulate the balance between niche-based and neutral processes in soybean Microbiome. Microb Ecol. 2021;82:416–28. https://doi.org/10.1007/s00248-021-01688-w.Chaparro JM, Badri DV, Vivanco JM. Rhizosphere microbiome assemblage is affected by plant development. ISME J. 2014;8:790–803.CAS 
    Article 

    Google Scholar 
    Azarbad H, Tremblay J, Giard-Laliberté C, Bainard LD, Yergeau E. Four decades of soil water stress history together with host genotype constrain the response of the wheat microbiome to soil moisture. FEMS Microbiol Ecol. 2020;96. https://doi.org/10.1093/femsec/fiaa098.Chen S, Cade-Menun BJ, Bainard LD, St. Luce M, Hu Y, Chen Q. The influence of long-term N and P fertilization on soil P forms and cycling in a wheat/fallow cropping system. Geoderma. 2021;404:115274.CAS 
    Article 

    Google Scholar 
    Smith EG, Zentner RP, Campbell CA, Lemke R, Brandt K. Long-term crop rotation effects on production, grain quality, profitability, and risk in the northern great plains. Agron J. 2017;109:957–67.Article 

    Google Scholar 
    Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. J Stat Softw. 2015;67:1–48.Article 

    Google Scholar 
    Kuznetsova A, Brockhoff PB, Christensen RHB. lmerTest package: tests in linear mixed effects models. J Stat Softw. 2017;82:1–26.Article 

    Google Scholar 
    Yang S. otuSummary: summarizing OTU table regarding the composition, abundance and beta diversity of abundant and rare biospheres. 2018.Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. vegan: community ecology package. R package version 2.5-6. 2019. Available online at: https://CRAN.R-project.org/package=vegan.Wagner MR, Lundberg DS, del Rio TG, Tringe SG, Dangl JL, Mitchell-Olds T. Host genotype and age shape the leaf and root microbiomes of a wild perennial plant. Nat Commun. 2016;7:12151.CAS 
    Article 

    Google Scholar 
    Hardoim PR, Hardoim CCP, Overbeek LS, van, Elsas JD. Dynamics of seed-borne rice endophytes on early plant growth stages. PLoS ONE. 2012;7:e30438.CAS 
    Article 

    Google Scholar 
    Grady KL, Sorensen JW, Stopnisek N, Guittar J, Shade A. Assembly and seasonality of core phyllosphere microbiota on perennial biofuel crops. Nat Commun. 2019;10:4135.Article 

    Google Scholar 
    Walsh CM, Becker-Uncapher I, Carlson M, Fierer N. Variable influences of soil and seed-associated bacterial communities on the assembly of seedling microbiomes. ISME J. 2021;15:2748–62.Morales Moreira ZP, Helgason BL, Germida JJ Environment has a Stronger Effect than Host Plant Genotype in Shaping Spring Brassica napus Seed Microbiomes. Phytobiomes J. 2021:PBIOMES-08-20-0059-R.Abdullaeva Y, Ambika Manirajan B, Honermeier B, Schnell S, Cardinale M. Domestication affects the composition, diversity, and co-occurrence of the cereal seed microbiota. J Adv Res. 2021;31:75–86.CAS 
    Article 

    Google Scholar 
    Chandrasekaran M, Chanratana M, Kim K, Seshadri S, Sa T. Impact of arbuscular mycorrhizal fungi on photosynthesis, water status, and gas exchange of plants under salt stress–a meta-analysis. Front Plant Sci. 2019;10. https://doi.org/10.3389/fpls.2019.00457.Begum N, Qin C, Ahanger MA, Raza S, Khan MI, Ashraf M, et al. Role of arbuscular mycorrhizal fungi in plant growth regulation: implications in abiotic stress tolerance. Front Plant Sci. 2019;10. https://doi.org/10.3389/fpls.2019.01068.Rashid MI, Mujawar LH, Shahzad T, Almeelbi T, Ismail IMI, Oves M. Bacteria and fungi can contribute to nutrients bioavailability and aggregate formation in degraded soils. Microbiol Res. 2016;183:26–41.CAS 
    Article 

    Google Scholar 
    Crowther TW, Thomas SM, Maynard DS, Baldrian P, Covey K, Frey SD, et al. Biotic interactions mediate soil microbial feedbacks to climate change. Proc Natl Acad Sci USA. 2015;112:7033–8.CAS 
    Article 

    Google Scholar 
    Evans SE, Wallenstein MD. Climate change alters ecological strategies of soil bacteria. Ecol Lett. 2014;17:155–64.Article 

    Google Scholar 
    Santos-Medellín C, Edwards J, Liechty Z, Nguyen B, Sundaresan V. Drought stress results in a compartment-specific restructuring of the rice root-associated microbiomes. mBio. 2017;8:e00764–17.Article 

    Google Scholar 
    Naylor D, Coleman-Derr D. Drought stress and root-associated bacterial communities. Front Plant Sci. 2018;8:2223.Article 

    Google Scholar 
    Zhou C, Ma Z, Zhu L, Xiao X, Xie Y, Zhu J, et al. Rhizobacterial Strain Bacillus megaterium BOFC15 induces cellular polyamine changes that improve plant growth and drought resistance. Int J Mol Sci. 2016;17:E976.Article 

    Google Scholar 
    Bokhari A, Essack M, Lafi FF, Andres-Barrao C, Jalal R, Alamoudi S, et al. Bioprospecting desert plant Bacillus endophytic strains for their potential to enhance plant stress tolerance. Sci Rep. 2019;9:18154.CAS 
    Article 

    Google Scholar 
    Xu L, Naylor D, Dong Z, Simmons T, Pierroz G, Hixson KK, et al. Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria. Proc Natl Acad Sci USA. 2018;115:E4284–93.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Na X, Cao X, Ma C, Ma S, Xu P, Liu S, et al. Plant stage, not drought stress, determines the effect of cultivars on bacterial community diversity in the rhizosphere of broomcorn millet (Panicum miliaceum L.). Front Microbiol. 2019;10. https://doi.org/10.3389/fmicb.2019.00828. More

  • in

    Pupal size as a proxy for fat content in laboratory-reared and field-collected Drosophila species

    Parker, J. & Johnston, L. A. The proximate determinants of insect size. J. Biol. 5, 15 (2006).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Honěk, A. Intraspecific variation in body size and fecundity in insects: A general relationship. Oikos 66, 483 (1993).Article 

    Google Scholar 
    Kingsolver, J. G. & Huey, R. B. Size, temperature, and fitness: Three rules. Evol. Ecol. Res. 10, 251–268 (2008).
    Google Scholar 
    Beukeboom, L. W. Size matters in insects—An introduction. Entomol. Exp. Appl. 166, 2–3 (2018).Article 

    Google Scholar 
    West, S. A., Flanagan, K. E. & Godfray, H. C. J. The relationship between parasitoid size and fitness in the field, a study of Achrysocharoides zwoelferi (Hymenoptera: Eulophidae). J. Anim. Ecol. 65, 631–639 (1996).Article 

    Google Scholar 
    Sagarra, L. A., Vincent, C. & Stewart, R. K. Body size as an indicator of parasitoid quality in male and female Anagyrus kamali (Hymenoptera: Encyrtidae). Bull. Entomol. Res. 91, 363–367 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    Ellers, J., Alphen, J. J. M. V. & Sevenster, J. G. A field study of size–fitness relationships in the parasitoid Asobara tabida. J. Anim. Ecol. 67, 318–324 (1998).Article 

    Google Scholar 
    Armbruster, P. & Hutchinson, R. A. Pupal mass and wing length as indicators of fecundity in Aedes albopictus and Aedes geniculatus (Diptera: Culicidae). J. Med. Entomol. 39, 699–704 (2002).PubMed 
    Article 

    Google Scholar 
    Tantawy, A. O. & Vetukhiv, M. O. Effects of size on fecundity, longevity and viability in populations of Drosophila pseudoobscura. Am. Nat. 94, 395–403 (1960).Article 

    Google Scholar 
    Lefranc, A. & Bundgaard, J. The influence of male and female body size on copulation duration and fecundity in Drosophila melanogaster. Hereditas 132, 243–247 (2004).Article 

    Google Scholar 
    Atkinson, D. Temperature and organism size: A biological law for ectotherms? Adv. Ecol. Res. 25, 1–58 (1994).Article 

    Google Scholar 
    Poças, G. M., Crosbie, A. E. & Mirth, C. K. When does diet matter? The roles of larval and adult nutrition in regulating adult size traits in Drosophila melanogaster. J. Insect Physiol. 139, 104051. https://doi.org/10.1016/j.jinsphys.2020.104051 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    Tammaru, T. Determination of adult size in a folivorous moth: constraints at instar level? Ecol. Entomol. 23, 80–89 (1998).Article 

    Google Scholar 
    Miller, R. S. & Thomas, J. L. The effects of larval crowding and body size on the longevity of adult Drosophila melanogaster. Ecology 39, 118–125 (1958).Article 

    Google Scholar 
    Nijhout, H. F. The control of body size in insects. Dev. Biol. 261, 1–9 (2003).CAS 
    PubMed 
    Article 

    Google Scholar 
    Shingleton, A. W., Mirth, C. K. & Bates, P. W. Developmental model of static allometry in holometabolous insects. Proc. R. Soc. B 275, 1875–1885 (2008).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Koenraadt, C. J. M. Pupal dimensions as predictors of adult size in fitness studies of Aedes aegypti (Diptera: Culicidae). J. Med. Entomol. 45, 331–336 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    Stillwell, R. C., Dworkin, I., Shingleton, A. W. & Frankino, W. A. Experimental manipulation of body size to estimate morphological scaling relationships in Drosophila. JoVE 56, 3162. https://doi.org/10.3791/3162 (2011).Article 

    Google Scholar 
    Shin, S.-M., Akram, W. & Lee, J.-J. Effect of body size on energy reserves in Culex pipiens pallens females (Diptera: Culicidae). Entomol. Res. 42, 163–167 (2012).Article 

    Google Scholar 
    Mirth, C. K. & Riddiford, L. M. Size assessment and growth control: How adult size is determined in insects. BioEssays 29, 344–355 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    Chown, S. L. & Gaston, K. J. Body size variation in insects: A macroecological perspective. Biol. Rev. 85, 139–169 (2010).PubMed 
    Article 

    Google Scholar 
    Beadle, G. W., Tatum, E. L. & Clancy, C. W. Food level in relation to rate of development and eye pigmentation in Drosophila melanogaster. Biol. Bull. 75, 447–462 (1938).Article 

    Google Scholar 
    Gayon, J. History of the concept of allometry1. Am. Zool. 40, 748–758 (2000).
    Google Scholar 
    Takken, W. et al. Larval nutrition differentially affects adult fitness and Plasmodium development in the malaria vectors Anopheles gambiae and Anopheles stephensi. Parasit. Vectors 6, 345 (2013).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Briegel, H. Metabolic relationship between female body size, reserves, and fecundity of Aedes aegypti. J. Insect Physiol. 36, 165–172 (1990).Article 

    Google Scholar 
    Ellers, J. Fat and eggs: An alternative method to measure the trade-off between survival and reproduction in insect parasitoids. Neth. J. Zool. 3, 227–235 (1996).
    Google Scholar 
    González-Tokman, D. et al. Energy storage, body size and immune response of herbivore beetles at two different elevations in Costa Rica. Rev. Biol. Trop. 67, 608–620 (2019).
    Google Scholar 
    Timmermann, S. E. & Briegel, H. Larval growth and biosynthesis of reserves in mosquitoes. J. Insect Physiol. 45, 461–470 (1999).CAS 
    PubMed 
    Article 

    Google Scholar 
    Strohm, E. Factors affecting body size and fat content in a digger wasp. Oecologia 123, 184–191 (2000).PubMed 
    Article 
    ADS 

    Google Scholar 
    Lease, H. M. & Wolf, B. O. Lipid content of terrestrial arthropods in relation to body size, phylogeny, ontogeny and sex. Physiol. Entomol. 36, 29–38 (2011).CAS 
    Article 

    Google Scholar 
    Arrese, E. L. & Soulages, J. L. Insect fat body: Energy, metabolism, and regulation. Annu. Rev. Entomol. 55, 207–225 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kühnlein, R. P. Lipid droplet-based storage fat metabolism in Drosophila. J. Lipid Res. 53, 1430–1436 (2012).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Church, R. B. & Robertson, F. W. A biochemical study of the growth of Drosophila melanogaster. J. Exp. Zool. 162, 337–351 (1966).Article 

    Google Scholar 
    Merkey, A. B., Wong, C. K., Hoshizaki, D. K. & Gibbs, A. G. Energetics of metamorphosis in Drosophila melanogaster. J. Insect Physiol. 57, 1437–1445 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    Nestel, D., Tolmasky, D., Rabossi, A. & Quesada-Allué, L. A. Lipid, carbohydrates and protein patterns during metamorphosis of the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae). Ann. Entomol. Soc. Am. 96, 237–244 (2003).CAS 
    Article 

    Google Scholar 
    Lee, K. P. & Jang, T. Exploring the nutritional basis of starvation resistance in Drosophila melanogaster. Funct. Ecol. 28, 1144–1155 (2014).Article 

    Google Scholar 
    Hahn, D. A. & Denlinger, D. L. Meeting the energetic demands of insect diapause: Nutrient storage and utilization. J. Insect Physiol. 53, 760–773 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    Tejeda, M. T. et al. Effects of size, sex and teneral resources on the resistance to hydric stress in the tephritid fruit fly Anastrepha ludens. J. Insect Physiol. 70, 73–80 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    Hoffmann, A. A., Hallas, R., Anderson, A. R. & Telonis-Scott, M. Evidence for a robust sex-specific trade-off between cold resistance and starvation resistance in Drosophila melanogaster. J. Evol. Biol. 18, 804–810 (2005).CAS 
    PubMed 
    Article 

    Google Scholar 
    Alaux, C., Ducloz, F., Crauser, D. & Le Conte, Y. Diet effects on honeybee immunocompetence. Biol. Lett. 6, 562–565 (2010).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bryk, B., Hahn, K., Cohen, S. M. & Teleman, A. A. MAP4K3 regulates body size and metabolism in Drosophila. Dev. Biol. 344, 150–157 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    Gasser, M., Kaiser, M., Berrigan, D. & Stearns, S. C. Life-history correlates of evolution under high and low adult mortality. Evolution 54, 1260–1272 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    Chippindale, A. K., Chu, T. J. F. & Rose, M. R. Complex trade-offs and the evolution of starvation resistance in Drosophila melanogaster. Evolution 50, 753 (1996).PubMed 
    Article 

    Google Scholar 
    Kristensen, T. N., Overgaard, J., Loeschcke, V. & Mayntz, D. Dietary protein content affects evolution for body size, body fat and viability in Drosophila melanogaster. Biol. Lett. 7, 269–272 (2011).PubMed 
    Article 

    Google Scholar 
    Juarez-Carreño, S. et al. Body-fat sensor triggers ribosome maturation in the steroidogenic gland to initiate sexual maturation in Drosophila. Cell Rep. 37, 109830 (2021).PubMed 
    Article 
    CAS 

    Google Scholar 
    Markow, T. A. The secret lives of Drosophila flies. Elife 4, e06793 (2015).PubMed Central 
    Article 

    Google Scholar 
    Choma, M. A., Suter, M. J., Vakoc, B. J., Bouma, B. E. & Tearney, G. J. Physiological homology between Drosophila melanogaster and vertebrate cardiovascular systems. Dis. Model. Mech. 4, 411–420 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    Morgan, T. H., Sturtevant, A. H., Muller, H. J. & Bridges, C. B. The Mechanism of Mendelian Heredity (H. Holt, 1923).
    Google Scholar 
    Dobzhansky, T. The influence of the quantity and quality of chromosomal material on the size of the cells in Drosophila melanogaster. Wilhelm Roux Arch. Entwickl Mech. Org. 115, 363–379 (1929).PubMed 
    Article 

    Google Scholar 
    Musselman, L. P. & Kühnlein, R. P. Drosophila as a model to study obesity and metabolic disease. J. Exp. Biol. 221, 163881 (2018).Article 

    Google Scholar 
    DiAngelo, J. R. & Birnbaum, M. J. Regulation of fat cell mass by insulin in Drosophila melanogaster. Mol. Cell. Biol. 29, 6341–6352 (2009).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rovenko, B. M. et al. High sucrose consumption promotes obesity whereas its low consumption induces oxidative stress in Drosophila melanogaster. J. Insect Physiol. 79, 42–54 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Hardy, C. M. et al. Obesity-associated cardiac dysfunction in starvation-selected Drosophila melanogaster. Am. J. Physiol.-Regul. Integr. Compar. Physiol. 309, R658–R667 (2015).CAS 
    Article 

    Google Scholar 
    Hardy, C. M. et al. Genome-wide analysis of starvation-selected Drosophila melanogaster—A genetic model of obesity. Mol. Biol. Evol. 35, 50–65 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Musselman, L. P. et al. A high-sugar diet produces obesity and insulin resistance in wild-type Drosophila. Dis. Model. Mech. 4, 842–849 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Henry, Y., Renault, D. & Colinet, H. Hormesis-like effect of mild larval crowding on thermotolerance in Drosophila flies. J. Exp. Biol. 221, 169342 (2018).Article 

    Google Scholar 
    Bulletin, E. P. P. O. Drosophila suzukii. EPPO Bull. 43, 417–424 (2013).Article 

    Google Scholar 
    Bächli, G., Vilela, C. R., Escher, S. A. & Saura, A. The Drosophilidae (Diptera) of Fennoscandia and Denmark (Brill Academic Publishers, 2004).Book 

    Google Scholar 
    Markow, T. A. & O’Grady, P. M. Drosophila: A Guide to Species Identification and Use (Elsevier, 2006).
    Google Scholar 
    Schindelin, J. et al. Fiji: An open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Visser, B. et al. Variation in lipid synthesis, but genetic homogeneity, among Leptopilina parasitic wasp populations. Ecol. Evol. 8, 7355–7364 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Williams, C. M., Thomas, R. H., MacMillan, H. A., Marshall, K. E. & Sinclair, B. J. Triacylglyceride measurement in small quantities of homogenised insect tissue: Comparisons and caveats. J. Insect Physiol. 57, 1602–1613 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    R Core Team. R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, 2020).Fox, J. & Weisberg, S. An R Companion to Applied Regression 2nd edn. (Sage, 2011).
    Google Scholar 
    Lenth, R., Singmann, H., Love, J., Buerkner, P. & Herve, M. Emmeans: Estimated marginal means, aka least-squares means. R Package Version 1, 3 (2018).
    Google Scholar 
    Burnham, K. P. & Anderson, D. R. A practical information-theoretic approach. In Model Selection and Multimodel Inference (ed. Burnham, K. P.) (Springer, 2002).MATH 

    Google Scholar 
    Crawley, M. J. The R Book (Wiley, 2007).MATH 
    Book 

    Google Scholar 
    Borash, D. J. & Ho, G. T. Patterns of selection: Stress resistance and energy storage in density-dependent populations of Drosophila melanogaster. J. Insect Physiol. 47, 1349–1356 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    Klepsatel, P., Procházka, E. & Gáliková, M. Crowding of Drosophila larvae affects lifespan and other life-history traits via reduced availability of dietary yeast. Exp. Gerontol. 110, 298–308 (2018).PubMed 
    Article 

    Google Scholar 
    Henry, Y., Overgaard, J. & Colinet, H. Dietary nutrient balance shapes phenotypic traits of Drosophila melanogaster in interaction with gut microbiota. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 241, 110626 (2020).CAS 
    Article 

    Google Scholar 
    Ireland, S. & Turner, B. The effects of larval crowding and food type on the size and development of the blowfly, Calliphora vomitoria. Forensic Sci. Int. 159, 175–181 (2006).PubMed 
    Article 

    Google Scholar 
    Saunders, D. S. & Bee, A. Effects of larval crowding on size and fecundity of the blow fly, Calliphora vicina (Diptera: Calliphoridae). EJE 92, 615–622 (2013).
    Google Scholar 
    Ziegler, R. Changes in lipid and carbohydrate metabolism during starvation in adult Manduca sexta. J. Comp. Physiol. B 161, 125–131 (1991).CAS 
    PubMed 
    Article 

    Google Scholar 
    Ojeda-Avila, T., Arthur Woods, H. & Raguso, R. A. Effects of dietary variation on growth, composition, and maturation of Manduca sexta (Sphingidae: Lepidoptera). J. Insect Physiol. 49, 293–306 (2003).CAS 
    PubMed 
    Article 

    Google Scholar 
    Borash, D. J., Gibbs, A. G., Joshi, A. & Mueller, L. D. A genetic polymorphism maintained by natural selection in a temporally varying environment. Am. Nat. 151, 148. https://doi.org/10.1086/286108 (1998).CAS 
    Article 
    PubMed 

    Google Scholar 
    Klepsatel, P., Knoblochová, D., Girish, T. N., Dircksen, H. & Gáliková, M. The influence of developmental diet on reproduction and metabolism in Drosophila. BMC Evol. Biol. 20, 93 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Matzkin, L. M., Johnson, S., Paight, C., Bozinovic, G. & Markow, T. A. Dietary protein and sugar differentially affect development and metabolic pools in ecologically diverse Drosophila. J. Nutr. 141, 1127–1133 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    Musselman, L. P. et al. Role of fat body lipogenesis in protection against the effects of caloric overload in Drosophila. J. Biol. Chem. 288, 8028–8042 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Reeve, M. W., Fowler, K. & Partridge, L. Increased body size confers greater fitness at lower experimental temperature in male Drosophila melanogaster. J. Evol. Biol. 13, 836–844 (2000).Article 

    Google Scholar 
    Lounibos, L. P. et al. Does temperature affect the outcome of larval competition between Aedes aegypti and Aedes albopictus?. J. Vector Ecol. 27, 86–95 (2002).CAS 
    PubMed 

    Google Scholar 
    Bergland, A. O., Genissel, A., Nuzhdin, S. V. & Tatar, M. Quantitative trait loci affecting phenotypic plasticity and the allometric relationship of ovariole number and thorax length in Drosophila melanogaster. Genetics 180, 567–582 (2008).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Holm, S. et al. A comparative perspective on longevity: The effect of body size dominates over ecology in moths. J. Evol. Biol. 29, 2422–2435 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    Nunney, L. The response to selection for fast larval development in Drosophila melanogaster and its effect on adult weight: An example of a fitness trade-off. Evolution 50, 1193–1204 (1996).PubMed 
    Article 

    Google Scholar 
    Partridge, L. & Farquhar, M. Lifetime mating success of male fruitflies (Drosophila melanogaster) is related to their size. Anim. Behav. 31, 871–877 (1983).Article 

    Google Scholar 
    Markow, T. A. & Ricker, J. P. Male size, developmental stability, and mating success in natural populations of three Drosophila species. Heredity 69, 122–127 (1992).PubMed 
    Article 

    Google Scholar 
    Wikelski, M. & Romero, L. M. Body size, performance and fitness in galapagos marine iguanas. Integr. Comp. Biol. 43, 376–386 (2003).PubMed 
    Article 

    Google Scholar 
    van Buskirk, J. & Crowder, L. B. Life-history variation in marine turtles. Copeia 1994, 66–81 (1994).Article 

    Google Scholar 
    Broderick, A. C., Glen, F., Godley, B. J. & Hays, G. C. Variation in reproductive output of marine turtles. J. Exp. Mar. Biol. Ecol. 288, 95–109 (2003).Article 

    Google Scholar 
    Wauters, L. A. et al. Effects of spatio-temporal variation in food supply on red squirrel Sciurus vulgaris body size and body mass and its consequences for some fitness components. Ecography 30, 51–65 (2007).Article 

    Google Scholar 
    Lindström, J. Early development and fitness in birds and mammals. Trends Ecol. Evol. 14, 343–348 (1999).PubMed 
    Article 

    Google Scholar 
    Reim, C., Teuschl, Y. & Blanckenhorn, W. U. Size-dependent effects of temperature and food stress on energy reserves and starvation resistance in yellow dung flies. Evol. Ecol. Res. 8, 1215–1234 (2006).
    Google Scholar 
    Kölliker-Ott, U. M., Blows, M. W. & Hoffmann, A. A. Are wing size, wing shape and asymmetry related to field fitness of Trichogramma egg parasitoids? Oikos 100, 563–573 (2003).Article 

    Google Scholar 
    Knapp, M. Relative importance of sex, pre-starvation body mass and structural body size in the determination of exceptional starvation resistance of Anchomenus dorsalis (Coleoptera: Carabidae). PLoS ONE 11, e0151459 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Lue, C.-H. et al. DROP: Molecular voucher database for identification of Drosophila parasitoids. Mol. Ecol. Resour. 21, 2437–2454 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Visser, B. et al. Loss of lipid synthesis as an evolutionary consequence of a parasitic lifestyle. Proc. Natl. Acad. Sci. 107, 8677–8682 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 
    ADS 

    Google Scholar 
    Visser B et al. Why do
    many parasitoids lack adult triglyceride accumulation, despite functioning fatty acid biosynthesis machinery? EcoEvoRxiv:
    https://doi.org/10.32942/osf.io/zpf4jArakawa, R., Miura, M. & Fujita, M. Effects of host species on the body size, fecundity, and longevity of Trissolcus mitsukurii (Hymenoptera: Scelionidae), a solitary egg parasitoid of stink bugs. Appl. Entomol. Zool. 39, 177–181 (2004).Article 

    Google Scholar 
    Visser, B., Alborn, H.T., Rondeaux, S. et al. Phenotypic plasticity explains apparent reverse evolution of fat synthesis in parasitic
    wasps. Sci Rep 11, 7751 (2021). https://doi.org/10.1038/s41598-021-86736-8.Krüger, A. P. et al. Effects of irradiation dose on sterility induction and quality parameters of Drosophila suzukii (Diptera: Drosophilidae). J. Econ. Entomol. 111, 741–746 (2018).PubMed 
    Article 

    Google Scholar 
    Nikolouli, K. et al. Sterile insect technique and Wolbachia symbiosis as potential tools for the control of the invasive species Drosophila suzukii. J. Pest Sci. 91, 1–15 (2017).
    Google Scholar 
    Nikolouli, K., Sassù, F., Mouton, L., Stauffer, C. & Bourtzis, K. Combining sterile and incompatible insect techniques for the population suppression of Drosophila suzukii. J. Pest Sci. 93, 647–661 (2020).CAS 
    Article 

    Google Scholar 
    Calkins, C. O. & Parker, A. G. Sterile insect quality. In Sterile Insect Technique (eds Dyck, V. A. et al.) 269–296 (Springer, 2005).Chapter 

    Google Scholar  More