{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,9]],"date-time":"2026-05-09T17:25:00Z","timestamp":1778347500139,"version":"3.51.4"},"reference-count":202,"publisher":"Walter de Gruyter GmbH","issue":"18","license":[{"start":{"date-parts":[[2025,5,6]],"date-time":"2025-05-06T00:00:00Z","timestamp":1746489600000},"content-version":"unspecified","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["J. Insects Food Feed"],"published-print":{"date-parts":[[2025,5,6]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Insect mass-rearing is a rapidly expanding industry for the production of protein for food and feed. These highly productive artificial rearing environments can expose insects to a range of biotic and abiotic stressors, including insect pathogens, which may result in population crashes. Interactions between insect pathogens with multiple stressors can exacerbate the effects of individual pathogens on host insects. However, reliable predictions on the combined effects of individual stressors based on mechanisms of action are lacking within the field of insect pathology. We review how ecotoxicological modelling of multiple stressors can be applied to mass-reared insect systems and discuss the importance of standardization across research fields investigating multiple stressors. Important considerations in multiple stressor terminology, experimental design, endpoints and analysis of results are discussed to improve understanding of multiple stressors and their impact on insects for food and feed. This is essential for ensuring optimal rearing conditions for mass-reared insect populations.<\/jats:p>","DOI":"10.1163\/23524588-bja10203","type":"journal-article","created":{"date-parts":[[2025,5,7]],"date-time":"2025-05-07T23:28:13Z","timestamp":1746660493000},"page":"561-578","source":"Crossref","is-referenced-by-count":1,"title":["BugBook: Determining multiple stressor interactions in mass-reared insects based on principles of ecotoxicology"],"prefix":"10.1163","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-5268-9554","authenticated-orcid":true,"given":"E.","family":"Dearlove","sequence":"first","affiliation":[{"name":"https:\/\/dx.doi.org\/41865UK Centre for Ecology and Hydrology, Maclean Building, Benson Lane, Crowmarsh Gifford, Wallingford, Oxfordshire OX10 8BB, UK"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5651-0208","authenticated-orcid":true,"given":"C.A.M.","family":"Van\u00a0Gestel","sequence":"additional","affiliation":[{"name":"Amsterdam Institute for Life and Environment (A-LIFE), Faculty of Science, https:\/\/dx.doi.org\/1190Vrije Universiteit Amsterdam, De Boelelaan 1108, 1081 HZ Amsterdam, The Netherlands"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5393-9623","authenticated-orcid":true,"given":"S.","family":"Loureiro","sequence":"additional","affiliation":[{"name":"https:\/\/dx.doi.org\/56062University of Aveiro, Centre for Environmental and Marine Studies, Department of Biology, 3810-193 Aveiro, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7281-647X","authenticated-orcid":true,"given":"C.","family":"Svendsen","sequence":"additional","affiliation":[{"name":"https:\/\/dx.doi.org\/41865UK Centre for Ecology and Hydrology, Maclean Building, Benson Lane, Crowmarsh Gifford, Wallingford, Oxfordshire OX10 8BB, UK"}]},{"ORCID":"https:\/\/orcid.org\/0009-0000-8153-8029","authenticated-orcid":true,"given":"M.","family":"Lloyd","sequence":"additional","affiliation":[{"name":"https:\/\/dx.doi.org\/4508Wageningen University and Research, Department of Virology, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands"},{"name":"Department of Genetics, University Institute of Biotechnology and Biomedicine (BIOTECMED), https:\/\/dx.doi.org\/16781Universitat de Vale\u0300ncia, 46100 Valencia, Spain"}]},{"ORCID":"https:\/\/orcid.org\/0009-0008-6553-8457","authenticated-orcid":true,"given":"L.","family":"Mugo-Kamiri","sequence":"additional","affiliation":[{"name":"Institut de Recherche sur la Biologie de l\u2019Insecte, UMR 7261, CNRS \u2013 University of Tours, 37200 Tours, France"},{"name":"Centre for Ecology and Conservation, Penryn Campus, College of Life and Environmental Science, https:\/\/dx.doi.org\/151673University of Exeter, Penryn, Cornwall TR10 9FE, UK"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2190-1401","authenticated-orcid":true,"given":"J.M.","family":"Petersen","sequence":"additional","affiliation":[{"name":"https:\/\/dx.doi.org\/4508Wageningen University and Research, Department of Virology, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands"},{"name":"Institut de Recherche sur la Biologie de l\u2019Insecte, UMR 7261, CNRS \u2013 University of Tours, 37200 Tours, France"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7005-7182","authenticated-orcid":true,"given":"E.","family":"Bessette","sequence":"additional","affiliation":[{"name":"Living Systems Institute, Biosciences, College of Life and Environmental Sciences, https:\/\/dx.doi.org\/151673University of Exeter, Stocker Road, Exeter EX4 4QD, UK"},{"name":"Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2796-8527","authenticated-orcid":true,"given":"S.","family":"Edwards","sequence":"additional","affiliation":[{"name":"Living Systems Institute, Biosciences, College of Life and Environmental Sciences, https:\/\/dx.doi.org\/151673University of Exeter, Stocker Road, Exeter EX4 4QD, UK"},{"name":"Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2650-7518","authenticated-orcid":true,"given":"F.S.","family":"Lim","sequence":"additional","affiliation":[{"name":"Department of Genetics, University Institute of Biotechnology and Biomedicine (BIOTECMED), https:\/\/dx.doi.org\/16781Universitat de Vale\u0300ncia, 46100 Valencia, Spain"},{"name":"Julius K\u00fchn-Institut (JKI), Institute of Biological Control, Schwabenheimerstrasse 101, 69221 Dossenheim, Germany"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8358-9636","authenticated-orcid":true,"given":"P.","family":"Herren","sequence":"additional","affiliation":[{"name":"https:\/\/dx.doi.org\/41865UK Centre for Ecology and Hydrology, Maclean Building, Benson Lane, Crowmarsh Gifford, Wallingford, Oxfordshire OX10 8BB, UK"},{"name":"Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark"},{"name":"Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, UK"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4910-4583","authenticated-orcid":true,"given":"L.","family":"Herna\u0301ndez\u00a0Pelegr\u0131\u0301n","sequence":"additional","affiliation":[{"name":"https:\/\/dx.doi.org\/4508Wageningen University and Research, Department of Virology, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands"},{"name":"Department of Genetics, University Institute of Biotechnology and Biomedicine (BIOTECMED), https:\/\/dx.doi.org\/16781Universitat de Vale\u0300ncia, 46100 Valencia, Spain"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8797-9420","authenticated-orcid":true,"given":"R.D.","family":"Pienaar","sequence":"additional","affiliation":[{"name":"Department of Genetics, University Institute of Biotechnology and Biomedicine (BIOTECMED), https:\/\/dx.doi.org\/16781Universitat de Vale\u0300ncia, 46100 Valencia, Spain"},{"name":"Institut de Recherche sur la Biologie de l\u2019Insecte, UMR 7261, CNRS \u2013 University of Tours, 37200 Tours, France"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4278-1197","authenticated-orcid":true,"given":"H.","family":"Huditz","sequence":"additional","affiliation":[{"name":"https:\/\/dx.doi.org\/4508Wageningen University and Research, Department of Virology, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands"},{"name":"Centre for Ecology and Conservation, Penryn Campus, College of Life and Environmental Science, https:\/\/dx.doi.org\/151673University of Exeter, Penryn, Cornwall TR10 9FE, UK"},{"name":"Insect Pest Control Laboratory, Joint FAO\/IAEA Programme of Nuclear Techniques in Food and Agriculture, International Atomic Energy Agency, Vienna International Centre, P.O. Box 100, 1400 Vienna, Austria"}]},{"given":"A.","family":"Mostafaie","sequence":"additional","affiliation":[{"name":"https:\/\/dx.doi.org\/56062University of Aveiro, Centre for Environmental and Marine Studies, Department of Biology, 3810-193 Aveiro, Portugal"}]},{"given":"J.","family":"Pinto","sequence":"additional","affiliation":[{"name":"https:\/\/dx.doi.org\/56062University of Aveiro, Centre for Environmental and Marine Studies, Department of Biology, 3810-193 Aveiro, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8581-4737","authenticated-orcid":true,"given":"A.","family":"Roman","sequence":"additional","affiliation":[{"name":"Centre for Ecology and Conservation, Penryn Campus, College of Life and Environmental Science, https:\/\/dx.doi.org\/151673University of Exeter, Penryn, Cornwall TR10 9FE, UK"},{"name":"https:\/\/dx.doi.org\/4508Wageningen University and Research, Department of Entomology, Droevendaalsesteeg 1, 6708 PB Wageningen, Netherlands"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6600-8126","authenticated-orcid":true,"given":"C.","family":"Savio","sequence":"additional","affiliation":[{"name":"https:\/\/dx.doi.org\/4508Wageningen University and Research, Department of Entomology, Droevendaalsesteeg 1, 6708 PB Wageningen, Netherlands"},{"name":"Universite\u0301 Paris-Saclay, INRAE, AgroParisTech, Micalis Institute, Domaine de Vilvert, 78350 Jouy-en-Josas, France"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3079-3868","authenticated-orcid":true,"given":"A.R.","family":"Slowik","sequence":"additional","affiliation":[{"name":"https:\/\/dx.doi.org\/41865UK Centre for Ecology and Hydrology, Maclean Building, Benson Lane, Crowmarsh Gifford, Wallingford, Oxfordshire OX10 8BB, UK"},{"name":"Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark"},{"name":"Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, UK"}]},{"given":"J.","family":"Takacs","sequence":"additional","affiliation":[{"name":"https:\/\/dx.doi.org\/4508Wageningen University and Research, Department of Virology, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands"},{"name":"Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8325-4262","authenticated-orcid":true,"given":"J.K.","family":"Upfold","sequence":"additional","affiliation":[{"name":"Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark"},{"name":"Universite\u0301 Paris-Saclay, INRAE, AgroParisTech, Micalis Institute, Domaine de Vilvert, 78350 Jouy-en-Josas, France"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1794-7658","authenticated-orcid":true,"given":"H.","family":"Hesketh","sequence":"additional","affiliation":[{"name":"https:\/\/dx.doi.org\/41865UK Centre for Ecology and Hydrology, Maclean Building, Benson Lane, Crowmarsh Gifford, Wallingford, Oxfordshire OX10 8BB, UK"}]}],"member":"374","reference":[{"key":"R000001","series-title":"Journal of Experimental Biology","first-page":"1997","article-title":"Some like it hot: the effects of climate change on reproduction, immune function and disease resistance in the cricket Gryllus texensis","volume":"214","author":"Adamo, S.A.","unstructured":"Adamo, S.A. and Lovett, M.M.E., 2011. Some like it hot: the effects of climate change on reproduction, immune function and disease resistance in the cricket Gryllus texensis. Journal of Experimental Biology 214: 1997-2004. https:\/\/doi.org\/10.1242\/JEB.056531"},{"key":"R000002","series-title":"Frontiers in Nutrition","article-title":"The nutritional profiles of five important edible insect species from west Africa \u2014 an analytical and literature synthesis","volume":"8","author":"Anankware, J.P.","unstructured":"Anankware, J.P., Roberts, B.J., Cheseto, X., Osuga, I., Savolainen, V. and Collins, C.M., 2021. The nutritional profiles of five important edible insect species from west Africa \u2014 an analytical and literature synthesis. 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Part A, Molecular and Integrative Physiology 156: 57-66. https:\/\/doi.org\/10.1016\/J.CBPA.2009.12.018"},{"issue":"11","key":"R000004","series-title":"Viruses","article-title":"A systematic review on viruses in mass-reared edible insect species","volume":"13","author":"Bertola, M.","unstructured":"Bertola, M. and Mutinelli, F., 2021. A systematic review on viruses in mass-reared edible insect species. Viruses 13(11): 2280. https:\/\/doi.org\/10.3390\/V13112280\/S1"},{"key":"R000005","series-title":"Insects","article-title":"Protists in the Insect Rearing Industry: Benign Passengers or Potential Risk?","volume":"13","author":"Bessette, E.","unstructured":"Bessette, E. and Williams, B., 2022. Protists in the Insect Rearing Industry: Benign Passengers or Potential Risk? Insects 13: 482. https:\/\/doi.org\/10.3390\/INSECTS13050482\/S1"},{"key":"R000006","series-title":"Journal of Insect Physiology","first-page":"89","article-title":"Role of temperature on growth and metabolic rate in the tenebrionid beetles Alphitobius diaperinus and Tenebrio molitor","volume":"107","author":"Bj\u00f8rge, J.D.","unstructured":"Bj\u00f8rge, J.D., Overgaard, J., Malte, H., Gianotten, N. and Heckmann, L.H., 2018. Role of temperature on growth and metabolic rate in the tenebrionid beetles Alphitobius diaperinus and Tenebrio molitor. Journal of Insect Physiology 107: 89-96. https:\/\/doi.org\/10.1016\/j.jinsphys.2018.02.010"},{"key":"R000007","series-title":"Annals of Applied Biology","first-page":"585","article-title":"The toxicity of poisons applied jointly","volume":"26","author":"Bliss, C.I.","unstructured":"Bliss, C.I., 1939. The toxicity of poisons applied jointly. Annals of Applied Biology 26: 585-615. https:\/\/doi.org\/10.1111\/J.1744-7348.1939.TB06990.X"},{"key":"R000008","series-title":"Frontiers in Marine Science","article-title":"A response-surface approach into the interactive effects of multiple stressors reveals new insights into complex responses","volume":"10","author":"Brooks, P.R.","unstructured":"Brooks, P.R., Browne, M.A., Benedetti-Cecchi, L., Lyons, D.A. and Crowe, T.P., 2023. A response-surface approach into the interactive effects of multiple stressors reveals new insights into complex responses. 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PLoS ONE 12: e0177301. https:\/\/doi.org\/10.1371\/JOURNAL.PONE.0177301"},{"key":"R000015","series-title":"Science of the Total Environment","article-title":"Edible insects: understanding benzo(a)pyrene toxicokinetics in yellow mealworms for safe and sustainable consumption","volume":"946","author":"Cardoso, D.N.","unstructured":"Cardoso, D.N., Duarte, R.M.B.O., Silva, A.R.R., Prodana, M., Go\u0301is, A., Silva, P.V., Mostafaie, A., Pinto, J., Branda\u0303o, P.F., Lopes, I.G., Brooks, B.W. and Loureiro, S., 2024. Edible insects: understanding benzo(a)pyrene toxicokinetics in yellow mealworms for safe and sustainable consumption. 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Quantifying synergy: a systematic review of mixture toxicity studies within environmental toxicology. PLoS ONE 9: e96580. https:\/\/doi.org\/10.1371\/JOURNAL.PONE.0096580"},{"key":"R000018","series-title":"Nature Immunology","first-page":"81","article-title":"Entry is a rate-limiting step for viral infection in a Drosophila melanogaster model of pathogenesis","volume":"5","author":"Cherry, S.","unstructured":"Cherry, S. and Perrimon, N., 2004. Entry is a rate-limiting step for viral infection in a Drosophila melanogaster model of pathogenesis. Nature Immunology 5: 81-87. https:\/\/doi.org\/10.1038\/NI1019"},{"key":"R000019","series-title":"Perspectives in Science","first-page":"3","article-title":"One hundred years of Michaelis-Menten kinetics","volume":"4","author":"Cornish-Bowden, A.","unstructured":"Cornish-Bowden, A., 2015. One hundred years of Michaelis-Menten kinetics. Perspectives in Science 4: 3-9. https:\/\/doi.org\/10.1016\/J.PISC.2014.12.002"},{"key":"R000020","series-title":"Scientific Reports","article-title":"Improved control of Trialeurodes vaporariorum using mixture combinations of entomopathogenic fungi and the chemical insecticide spiromesifen","volume":"14","author":"Dearlove, E.L.","unstructured":"Dearlove, E.L., Chandler, D., Edgington, S., Berry, S.D., Martin, G., Svendsen, C. and Hesketh, H., 2024. Improved control of Trialeurodes vaporariorum using mixture combinations of entomopathogenic fungi and the chemical insecticide spiromesifen. Scientific Reports 14: 15259. https:\/\/doi.org\/10.1038\/s41598-024-66051-8"},{"key":"R000021","series-title":"Multiple stressor effects in biological pest control; improving efficacy in challenging environments","author":"Dearlove, E.L.","unstructured":"Dearlove, E.L., 2022. Multiple stressor effects in biological pest control; improving efficacy in challenging environments. University of Warwick, Warwick. Available online at http:\/\/wrap.warwick.ac.uk\/170366"},{"key":"R000022","series-title":"Journal of Insects as Food and Feed","first-page":"1685","article-title":"Standardising black soldier fly larvae feeding experiments: an initial protocol and variability estimates","volume":"10","author":"Deruytter, D.","unstructured":"Deruytter, D., Gasco, L., Yakti, W., Katz, H., Coudron, C.L., Gligorescu, A., Frooninckx, L., Noyens, I., Meneguz, M., Grosso, F., Oddon, S.B., Biasato, I., Mielenz, M., Veldkamp, T., van Loon, J.J.A., Spranghers, T., Vandenberg, G.W., Oonincx, D.G.A.B. and Bosch, G., 2024. Standardising black soldier fly larvae feeding experiments: an initial protocol and variability estimates. Journal of Insects as Food and Feed 10: 1685-1694. https:\/\/doi.org\/10.1163\/23524588-20230008"},{"key":"R000023","series-title":"Journal of Animal Ecology","first-page":"448","article-title":"Immune priming specificity within and across generations reveals the range of pathogens affecting evolution of immunity in an insect","volume":"87","author":"Dhinaut, J.","unstructured":"Dhinaut, J., Chogne, M. and Moret, Y., 2018. Immune priming specificity within and across generations reveals the range of pathogens affecting evolution of immunity in an insect. Journal of Animal Ecology 87: 448-463. https:\/\/doi.org\/10.1111\/1365-2656.12661"},{"key":"R000024","series-title":"Frontiers in Marine Science","article-title":"Assessing population-level effects of anthropogenic disturbance on a marine mammal population","volume":"8","author":"Dunlop, R.A.","unstructured":"Dunlop, R.A., Braithwaite, J., Mortensen, L.O. and Harris, C.M., 2021. 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