Herbivory in global climate change research: direct effects of rising temperature on insect herbivores

Bale, Jeffery S.; Masters, Gregory J.; Hodkinson, Ian D.; Awmack, Caroline; Bezemer, T. Martijn; Brown, Valerie K.; Butterfield, Jennifer; Buse, Alan; Coulson, John C.; Farrar, John; Good, John E. G.; Harrington, Richard; Hartley, Susane; Jones, T. Hefin; Lindroth, Richard L.; Press, Malcolm C.; Symrnioudis, Ilias; Watt, Allan D.; Whittaker, John B.

doi:10.1046/j.1365-2486.2002.00451.x

Cited by 2,775Physiological and biochemical adaptationsEntomological Studies and EcologyInsect-Plant Interactions and Control

Herbivory in global climate change research: direct effects of rising temperature on insect herbivores

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Bale, Jeffery S., Masters, Gregory J., Hodkinson, Ian D., Awmack, Caroline, Bezemer, T. Martijn, Brown, Valerie K., Butterfield, Jennifer, Buse, Alan +11 more·2002·Global Change Biology

DOI 10.1046/j.1365-2486.2002.00451.x

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Abstract

This review examines the direct effects of climate change on insect herbivores. Temperature is identified as the dominant abiotic factor directly affecting herbivorous insects. There is little evidence of any direct effects of CO 2 or UVB. Direct impacts of precipitation have been largely neglected in current research on climate change. Temperature directly affects development, survival, range and abundance. Species with a large geographical range will tend to be less affected. The main effect of temperature in temperate regions is to influence winter survival; at more northerly latitudes, higher temperatures extend the summer season, increasing the available thermal budget for growth and reproduction. Photoperiod is the dominant cue for the seasonal synchrony of temperate insects, but their thermal requirements may differ at different times of year. Interactions between photoperiod and temperature determine phenology; the two factors do not necessarily operate in tandem. Insect herbivores show a number of distinct life‐history strategies to exploit plants with different growth forms and strategies, which will be differentially affected by climate warming. There are still many challenges facing biologists in predicting and monitoring the impacts of climate change. Future research needs to consider insect herbivore phenotypic and genotypic flexibility, their responses to global change parameters operating in concert, and awareness that some patterns may only become apparent in the longer term.

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Factors limiting the distribution of Acyrthosiphon svalbardicum (Hemiptera: Aphididae) on Spitsbergen
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The Maintenance of Annual Life-Cycles in two Species of Tipulidae (Diptera); A Field Study Relating Development, Temperature and Altitude
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EXPERIMENTAL BACKGROUND TO THE STUDY OF THE DISTRIBUTION AND ABUNDANCE OF INSECTS: III. The relation between innate capacity for increase and survival of different species of beetles living together on the same food
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The response of beetles to Quaternary climate changes
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Influence of inter‐tree variation in time of budburst of white spruce on herbivory and the behaviour and survivorship of Zeiraphera canadensis
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Life strategies of arctic terrestrial arthropods
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The Past as a Key to the Future: The Use of Palaeoenvironmental Understanding to Predict the Effects of Man on the Biosphere
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Variation in resource exploitation along an altitudinal gradient: the willow psyllids ( Cacopsylla spp.) on Salix lapponum
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Activité Saisonnière de vol des Pucerons [Hom. Aphididae] Dans l'Ouest de la France. Résultats de Neuf Années de Piégeage (1967-1975)
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The TIGER Programme
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Effects of photoperiod and raised winter temperatures on egg development and timing of oviposition in the willow psyllid Cacopsylla moscovita
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Forecasting of periodic fluctuations in annual abundance of the bean aphid: the role of density dependence and weather
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The biogeography and regional biodiversity of the British seed bugs (Hemiptera: Lygaeidae)
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Monitoring and forecasting for BYDV control - the way forward?
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The diapause syndrome in the seed‐eating caterpillar of Coleophora alticolella
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The rate of development in the overwintering eggs of Tipula pagana Meigen
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A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests
Allen, C. D., Macalady, A. K., Chenchouni, H., Bachelet, D., McDowell, N., Vennetier, M., Kitzberger, T., Rigling, A., Breshears, D. D., Hogg, E. H. (., et al. (2010) · Forest Ecology and Management · doi:10.1016/j.foreco.2009.09.001 · Cited by 7,763 · see citing works
Ecological and Evolutionary Responses to Recent Climate Change
Parmesan, C. (2006) · Annual Review of Ecology, Evolution, and Systematics · doi:10.1146/annurev.ecolsys.37.091305.110100 · Cited by 8,652 · see citing works
Climate change impacts, adaptive capacity, and vulnerability of European forest ecosystems
Lindner, M., Maroschek, M., Netherer, S., Kremer, A., Barbati, A., García-Gonzalo, J., Seidl, R., Delzon, S., Corona, P., Kolström, M., et al. (2009) · Forest Ecology and Management · doi:10.1016/j.foreco.2009.09.023 · Cited by 2,289 · see citing works
Abiotic and biotic stress combinations
Suzuki, N., Rivero, R. M., Shulaev, V., Blumwald, E., & Mittler, R. (2014) · New Phytologist · doi:10.1111/nph.12797 · Cited by 2,153 · see citing works
The interaction of plant biotic and abiotic stresses: from genes to the field
Atkinson, N. J., & Urwin, P. E. (2012) · Journal of Experimental Botany · doi:10.1093/jxb/ers100 · Cited by 1,880 · see citing works
Crops that feed the world 6. Past successes and future challenges to the role played by maize in global food security
Shiferaw, B. A., Prasanna, B. M., Hellin, J., & Bänziger, M. (2011) · Food Security · doi:10.1007/s12571-011-0140-5 · Cited by 1,676 · see citing works
Resilience in Agriculture through Crop Diversification: Adaptive Management for Environmental Change
Lin, B. B. (2011) · BioScience · doi:10.1525/bio.2011.61.3.4 · Cited by 1,570 · see citing works
The Impact of Climate Change on Agricultural Insect Pests
Skendžić, S., Zovko, M., Živković, I. P., Lešić, V., & Lemić, D. (2021) · Insects · doi:10.3390/insects12050440 · Cited by 1,439 · see citing works
Climate Change and Bark Beetles of the Western United States and Canada: Direct and Indirect Effects
Bentz, B., Régnière, J., Fettig, C. J., Hansen, E. M., Hayes, J. L., Hicke, J. A., Kelsey, R. G., Negrón, J. F., & Seybold, S. J. (2010) · BioScience · doi:10.1525/bio.2010.60.8.6 · Cited by 1,294 · see citing works
Impacts and adaptation of European crop production systems to climate change
Olesen, J. E., Trnka, M., Kersebaum, K. C., Skjelvåg, A. O., Seguin, B., Peltonen-Sainio, P., Rossi, F., Kozyra, J., & Micale, F. (2011) · European Journal of Agronomy · doi:10.1016/j.eja.2010.11.003 · Cited by 1,215 · see citing works
The potential for behavioral thermoregulation to buffer “cold-blooded” animals against climate warming
Kearney, M., Shine, R., & Porter, W. P. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0808913106 · Cited by 1,149 · see citing works
Climate Change and Global Food Systems: Potential Impacts on Food Security and Undernutrition
Myers, S. S., Smith, M. R., Guth, S., Golden, C. D. W., Vaitla, B., Mueller, N. D., Dangour, A. D., & Huybers, P. (2017) · Annual Review of Public Health · doi:10.1146/annurev-publhealth-031816-044356 · Cited by 1,140 · see citing works
Terrestrial insects along elevation gradients: species and community responses to altitude
Hodkinson, I. D. (2005) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1017/s1464793105006767 · Cited by 1,095 · see citing works
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Crop pests and pathogens move polewards in a warming world
Bebber, D. P., Ramotowski, M. A. T., & Gurr, S. J. (2013) · Nature Climate Change · doi:10.1038/nclimate1990 · Cited by 1,116 · see citing works
Climate Change Effects on Plant Disease: Genomes to Ecosystems
Garrett, K. A., Dendy, S. P., Frank, E., Rouse, M. N., & Travers, S. E. (2006) · Annual Review of Phytopathology · doi:10.1146/annurev.phyto.44.070505.143420 · Cited by 1,003 · see citing works
Eco-physiological phases of insect diapause
Košťál, V. (2005) · Journal of Insect Physiology · doi:10.1016/j.jinsphys.2005.09.008 · Cited by 988 · see citing works
Assessing the future global impacts of ozone on vegetation
ASHMORE, M. R. (2005) · Plant Cell & Environment · doi:10.1111/j.1365-3040.2005.01341.x · Cited by 920 · see citing works
Insect overwintering in a changing climate
Bale, J. S., & Hayward, S. A. L. (2010) · Journal of Experimental Biology · doi:10.1242/jeb.037911 · Cited by 872 · see citing works
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Predicting species distribution and abundance responses to climate change: why it is essential to include biotic interactions across trophic levels
van der Putten, W. H., Macel, M., & Visser, M. E. (2010) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0037 · Cited by 833 · see citing works
Crop and pasture response to climate change
Tubiello, F. N., Soussana, J., & Howden, M. S. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0701728104 · Cited by 815 · see citing works
Impacts of climate change on the livestock food supply chain; a review of the evidence
Godde, C., Mason-D’Croz, D., Mayberry, D., Thornton, P. K., & Herrero, M. (2021) · Global Food Security · doi:10.1016/j.gfs.2020.100488 · Cited by 850 · see citing works
Impact of Extreme Temperatures on Parasitoids in a Climate Change Perspective
Hance, T., van Baaren, J., Vernon, P., & Boivin, G. (2006) · Annual Review of Entomology · doi:10.1146/annurev.ento.52.110405.091333 · Cited by 711 · see citing works
Changes to the elevational limits and extent of species ranges associated with climate change
Wilson, R. J., Gutiérrez, D., Illán, J. G., Martínez, D. R., Agudo, R., & Monserrat, V. J. (2005) · Ecology Letters · doi:10.1111/j.1461-0248.2005.00824.x · Cited by 697 · see citing works
Adapt or disperse: understanding species persistence in a changing world
Berg, M. P., Kiers, E. T., Driessen, G., van der Heijden, M. G. A., Kooi, B. W., Kuenen, F. J. A., Liefting, M., Verhoef, H. A., & Ellers, J. (2009) · Global Change Biology · doi:10.1111/j.1365-2486.2009.02014.x · Cited by 613 · see citing works
Forecasting the Effects of Global Warming on Biodiversity
Botkin, D. B., Saxe, H., Araújo, M. B., Betts, R., Bradshaw, R., Cedhagen, T., Chesson, P., Dawson, T. P., Etterson, J. R., Faith, D. P., et al. (2007) · BioScience · doi:10.1641/b570306 · Cited by 603 · see citing works
EXPANSION OF GEOGRAPHIC RANGE IN THE PINE PROCESSIONARY MOTH CAUSED BY INCREASED WINTER TEMPERATURES
Battisti, A., Stastny, M., Netherer, S., Robinet, C., Schopf, A., Alain Roques, B., & Larsson, S. (2005) · Ecological Applications · doi:10.1890/04-1903 · Cited by 611 · see citing works
Agroecosystem responses to combinations of elevated CO2, ozone, and global climate change
Fuhrer, J. (2003) · Agriculture Ecosystems & Environment · doi:10.1016/s0167-8809(03)00125-7 · Cited by 608 · see citing works
Unraveling the drivers of intensifying forest disturbance regimes in Europe
Seidl, R., Schelhaas, M., & Lexer, M. J. (2011) · Global Change Biology · doi:10.1111/j.1365-2486.2011.02452.x · Cited by 609 · see citing works
Anticipating the consequences of climate change for Canada’s boreal forest ecosystems
Price, D. T., Alfaro, R. I., Brown, K. J., Flannigan, M., Fleming, R. A., Hogg, E. H., Girardin, M. P., Lakusta, T., Johnston, M., McKenney, D. W., et al. (2013) · Environmental Reviews · doi:10.1139/er-2013-0042 · Cited by 605 · see citing works
Scientists' warning on climate change and insects
Harvey, J. A., Tougeron, K., Gols, R., Heinen, R., Abarca, M., Abram, P. K., Basset, Y., Berg, M. P., Boggs, C. L., Jacques Brodeur, B., et al. (2022) · Ecological Monographs · doi:10.1002/ecm.1553 · Cited by 599 · see citing works
Insect responses to heat: physiological mechanisms, evolution and ecological implications in a warming world
González‐Tokman, D., Córdoba‐Aguilar, A., Dáttilo, W., Lira‐Noriega, A., Sánchez‐Guillén, R. A., & Villalobos, F. (2020) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12588 · Cited by 581 · see citing works
Integrating pests and pathogens into the climate change/food security debate
Gregory, P. J., Johnson, S. N., Newton, A. C., & Ingram, J. S. I. (2009) · Journal of Experimental Botany · doi:10.1093/jxb/erp080 · Cited by 583 · see citing works
Physiological Diversity in Insects: Ecological and Evolutionary Contexts
Chown, S. L., & Terblanche, J. S. (2006) · Advances in insect physiology · doi:10.1016/s0065-2806(06)33002-0 · Cited by 573 · see citing works
Shared and unique responses of plants to multiple individual stresses and stress combinations: physiological and molecular mechanisms
Pandey, P., Ramegowda, V., & Senthil‐Kumar, M. (2015) · Frontiers in Plant Science · doi:10.3389/fpls.2015.00723 · Cited by 579 · see citing works
Health effects from stratospheric ozone depletion and interactions with climate change
Caldwell, M. M., Ballaré, C. L., Bornman, J. F., Flint, S. D., Björn, L. O., Teramura, A. H., Kulandaivelu, G., & Tevini, M. (2003) · Photochemical & Photobiological Sciences · doi:10.1039/b211159b · Cited by 571 · see citing works
Phenology of Forest Caterpillars and Their Host Trees: The Importance of Synchrony
van Asch, M., & Visser, M. E. (2006) · Annual Review of Entomology · doi:10.1146/annurev.ento.52.110405.091418 · Cited by 563 · see citing works
Drought as an Inciting Mortality Factor in Scots Pine Stands of the Valais, Switzerland
Bigler, C., Bräker, O. U., Bugmann, H. K. M., Dobbertin, M., & Rigling, A. (2006) · Ecosystems · doi:10.1007/s10021-005-0126-2 · Cited by 553 · see citing works
Agriculture and climate change are reshaping insect biodiversity worldwide
Outhwaite, C. L., McCann, P., & Newbold, T. (2022) · Nature · doi:10.1038/s41586-022-04644-x · Cited by 563 · see citing works
Winter forest soil respiration controlled by climate and microbial community composition
Monson, R. K., Lipson, D. L., Burns, S. P., Turnipseed, A. A., Delany, A. C., Williams, M. W., & Schmidt, S. K. (2006) · Nature · doi:10.1038/nature04555 · Cited by 542 · see citing works
Increasing liana abundance and biomass in tropical forests: emerging patterns and putative mechanisms: Increasing lianas in tropical forests
Schnitzer, S. A., & Bongers, F. (2011) · Ecology Letters · doi:10.1111/j.1461-0248.2011.01590.x · Cited by 543 · see citing works
Autumn, the neglected season in climate change research
Gallinat, A. S., Primack, R. B., & Wagner, D. L. (2015) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2015.01.004 · Cited by 533 · see citing works
Responses of insect pests, pathogens, and invasive plant species to climate change in the forests of northeastern North America: What can we predict?This article is one of a selection of papers from NE Forests 2100: A Synthesis of Climate Change Impacts on Forests of the Northeastern US and Eastern Canada.
Dukes, J. S., Pontius, J. A., Orwig, D. A., Garnas, J. R., Rodgers, V. L., Brazee, N. J., Cooke, B. J., Theoharides, K. A., Stange, E. E., Harrington, R. A., et al. (2009) · Canadian Journal of Forest Research · doi:10.1139/x08-171 · Cited by 516 · see citing works
Self-citation
Higher predation risk for insect prey at low latitudes and elevations
Roslin, T. V., Hardwick, B., Novotný, V., Petry, W. K., Andrew, N. R., Asmus, A. L., Barrio, I. C., Basset, Y., Boesing, A. L., Bonebrake, T. C., et al. (2017) · Science · doi:10.1126/science.aaj1631 · Cited by 511 · see citing works
Consequences of simultaneous elevation of carbon dioxide and temperature for plant–herbivore interactions: a metaanalysis
Zvereva, E. L., & Kozlov, M. V. (2005) · Global Change Biology · doi:10.1111/j.1365-2486.2005.01086.x · Cited by 505 · see citing works
Insects and low temperatures: from molecular biology to distributions and abundance
Bale, J. S. (2002) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2002.1074 · Cited by 500 · see citing works
Self-citation
Climatic warming increases voltinism in European butterflies and moths
Altermatt, F. (2009) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2009.1910 · Cited by 496 · see citing works
NAC transcription factors in plant multiple abiotic stress responses: progress and prospects
Shao, H., Wang, H., & Tang, X. (2015) · Frontiers in Plant Science · doi:10.3389/fpls.2015.00902 · Cited by 488 · see citing works
Predicting the effects of climate change on natural enemies of agricultural pests
Thomson, L. J., Macfadyen, S., & Hoffmann, A. A. (2009) · Biological Control · doi:10.1016/j.biocontrol.2009.01.022 · Cited by 481 · see citing works
TROPHIC LEVELS ARE DIFFERENTIALLY SENSITIVE TO CLIMATE
Voigt, W., Perner, J., Davis, A., Eggers, T., Schumacher, J., Bährmann, R., Fabian, B., Heinrich, W., Köhler, G., Lichter, D., et al. (2003) · Ecology · doi:10.1890/02-0266 · Cited by 476 · see citing works
Insects at low temperatures: an ecological perspective
Sinclair, B. J., Vernon, P., Klok, C. J., & Chown, S. L. (2003) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(03)00014-4 · Cited by 470 · see citing works
Plants in a warmer world
Walther, G. (2003) · Perspectives in Plant Ecology Evolution and Systematics · doi:10.1078/1433-8319-00076 · Cited by 449 · see citing works
Direct impacts of recent climate warming on insect populations
ROBINET, C., & ROQUES, A. (2010) · Integrative Zoology · doi:10.1111/j.1749-4877.2010.00196.x · Cited by 438 · see citing works
Modelling natural disturbances in forest ecosystems: a review
Seidl, R., Fernandes, P. M., Fonseca, T., Gillet, F., Jönsson, A. M., Merganičová, K., Netherer, S., Arpaci, A., Bontemps, J., Bugmann, H. K. M., et al. (2010) · Ecological Modelling · doi:10.1016/j.ecolmodel.2010.09.040 · Cited by 445 · see citing works
Distribution, diversity and ecology of aerobic CO-oxidizing bacteria
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Authors: Bale, J. S., Masters, G. J., Hodkinson, I. D., Awmack, C., Bezemer, T. M., Brown, V. K., Butterfield, J., Buse, A., Coulson, J. C., Farrar, J., Good, J. E. G., Harrington, R., Hartley, S., Jones, T. H., Lindroth, R. L., Press, M. C., Symrnioudis, I., Watt, A. D., & Whittaker, J. B.
Affiliations: CAB International (GB)
Liverpool John Moores University (GB)
Rothamsted Research (GB)
Durham University (GB)
Bangor University (GB)
Imperial College London (GB)
University of Wisconsin System (US)
University of Sheffield (GB)
Natural Environment Research Council (GB)
Lancaster University (GB)
ORCID: Hodkinson, Ian D.
Farrar, John
Jones, T. Hefin
Lindroth, Richard L.
Watt, Allan D.
Whittaker, John B.
Venue: Global Change Biology
Publisher: Wiley
Published: 2002-01
Volume: 8
Issue: 1
Pages: 1-16
ISSN: 1354-1013 (ISSN-L)
1365-2486
DOI: 10.1046/j.1365-2486.2002.00451.x
OpenAlex: W2149928193
Cited by: 2,775
References: 142
Citations by year: 2026: 131 · 2025: 133 · 2024: 137 · 2023: 154 · 2022: 203 · 2021: 235 · 2020: 177 · 2019: 135 · 2018: 140 · 2017: 154 · 2016: 142 · 2015: 136 · 2014: 153 · 2013: 129 · 2012: 118
FWCI: 34.06
Type: journal article
Language: en
Open access: green
figshare.com
Licence: cc-by
onlinelibrary.wiley.com/termsAndConditions#vor (vor, 22 d)
Locations: Global Change Biology (publishedVersion)
Rothamsted Repository (Rothamsted Repository) (submittedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion)
Lancaster EPrints (Lancaster University) (submittedVersion)
Figshare (submittedVersion, cc-by)
University of Birmingham Research Portal (University of Birmingham) (submittedVersion)
KNAW research portal (Royal Academy of Art and Sciences (KNAW)) (submittedVersion)
Funders: Natural Environment Research Council
Topics: Physical Sciences › Environmental Science › Ecology › Physiological and biochemical adaptations
Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Entomological Studies and Ecology
Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect-Plant Interactions and Control
Keywords: climate change, phytophagous insects, temperature rise, insect development, winter survival, phenology, photoperiod, thermal budget, seasonal synchrony, life history strategies, precipitation effects, CO2 effect, range expansion, temperate insects, phenotypic flexibility

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Herbivory in global climate change research: direct effects of rising temperature on insect herbivores

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