Review Article
Vol. 37 No. 1 (2020): Revista de Ciencias Agrícolas - First semester, January - June 2020
Multiple mechanisms in which agricultural insects respond to environmental stressors: canalization, plasticity and evolution
Centro de Bioinformática y Biología Computacional de Colombia - BIOS
Abstract
Insects are a paramount component of biodiversity in terms of taxonomic richness, ecological functions and ecosystem services. However, many human activities have negative consequences on such organisms, causing changes in their morphology, physiology, behaviour, and even causing mass deaths leading to the well-recognized insect decline phenomenon. Although the effects of some environmental stressors (e.g. global warming and pesticides) on insect biology are fairly well understood, there is a plethora of stressors that that have only recently been considered. Additionally, although the exposure to multiple stressors is a common scenario in natural conditions, our knowledge on insect responses in this regard is still incipient. Knowledge that is in much need to inform policy makers in the fight against global change. Here, a short review on prominent environmental stressors, and the known responses that insects may exhibit, which are summarized as canalization, plasticity and evolution is provided. Furthermore, an outlook and recommendation for future studies aiming to elucidate the effects of environmental stressors (both lone and mixed) on insect biology is given. This manuscript advocates for controlled (lab or semi-field) manipulative experiments that implement realistic environmental conditions and that ideally combine several stressors.
References
- Adamo, S.A.; Kovalko, I.; Mosher, B. (2013). The behavioural effects of predator-induced stress responses in the cricket (Gryllus texensis): the upside of the stress response. J Exp Biol. 216: 4608-4614.
- Angert, A.L.; Crozier, L.G.; Rissler, L.J.; Gilman, S. E.; Tewksbury, J. J.; Chunco, A. J. (2011). Do species’ traits predict recent shifts at expanding range edges? Ecol Lett. 14: 677-689. https://doi.org/10.1111/j.1461-0248.2011.01620.x
- Baird, D.J.; Van den Brink, P.J. (2007). Using biological traits to predict species sensitivity to toxic substances. Ecotoxicol Environ Saf. 67:296–301.
- Barsics, F.; Caparros Megido, R.; Brostaux, Y.; Barsics, C.; Blecker, C.; Haubruge, E.; Francis, F. (2017). Could new information influence attitudes to foods supplemented with edible insects? Br Food J. 119: 2027-2039.
- Bebber, DP.; Holmes, T.; Gurr, S.J. (2014) The global spread of crop pests and pathogens. Glob Ecol Biogeogr. 23: 1398-1407.
- Bernhardt, E.S.; Rosi, E.J.; Gessner, M.O. (2017) Synthetic chemicals as agents of global change. Front Ecol Environ. 15: 84-90.
- Bidart-Bouzat, M.G.; Imeh-Nathaniel, A. (2008) Global change effects on plant chemical defenses against insect herbivores. J Integr Plant Biol. 50: 1339-54. doi: https://doi.org/10.1111/j.1744-7909.2008.00751.x
- Bijlsma, R.; Loeschcke, V. (2005). Environmental stress, adaptation and evolution: an overview. J. Evol. Biol. 18:744-749.
- Boersma, M.; Spaak, P.; De Meester, L. (1998) Predator-mediated plasticity in morphology, life history, and behavior of Daphnia: the uncoupling of responses. Am Nat. 152: 237-248.
- Bohnenblust, E.; Egan, J.F.; Mortensen, D.; Tooker, J. (2013). Direct and indirect effects of the synthetic-auxin herbicide dicamba on two lepidopteran species. Environ Entomol. 42: 586-594.
- Breitburg, D.L.; Baxter, J.W.; Hatfield, C.A.; Howarth, R. W.; Jones, C. G.; Lovett, G. M.; Wigand, C. (1998). Understanding effects of multiple stressors: ideas and challenges. In: Pace M.L., Groffman P.M. (eds). Successes, Limitations, and Frontiers in Ecosystem Science. New York, NY: Springer. doi: https://doi.org/10.1007/978-1-4612-1724-4_17
- Callahan, H.S.; Pigliucci, M.; Schlichting, CD. (1997) Developmental phenotypic plasticity: where ecology and evolution meet molecular biology. Bioessays. 19: 519-525.
- Cardinale, B.J., Duffy, J.E.; Gonzalez A.; Hooper, D.; Perrings, C., Venail, P.; Narwani, A.; Mace, G.; Tilman, D.; Wardle, D.; Kinzig, A.; Daily, G.; Loreau, M.; Grace, J.; Larigauderie, A.; Srivastava, D.; Naeem, S. (2012). Biodiversity loss and its impact on humanity. Nature. 486:59
- Christensen, M.R.; Graham, M.D.; Vinebrooke, R.D.; Findlay, D. L.; Paterson, M. J.; Turner, M. A. (2006). Multiple anthropogenic stressors cause ecological surprises in boreal lakes. Glob Chang Biol. 12: 2316-2322. doi: https://doi.org/10.1111/j.1365-2486.2006.01257.x
- Costanza, R.; Kubiszewski, I.; Ervin D.; Bluffstone, R.; Boyd, J.; Brown, D.; Chang, H.; Dujon, V.; Granek, E.; Polasky, S.; Shandas, V.; Yeakley, A. (2011). Valuing ecological systems and services. F1000 Biol Rep. 3: 14.
- Côté, I.M.; Darling, E.S.; Brown, C.J. (2016) Interactions among ecosystem stressors and their importance in conservation. Proc R Soc B Biol Sci. 283: 20152592.
- Coustau, C.; Chevillon, C. (2000) Resistance to xenobiotics and parasites: can we count the cost? Trends Ecol Evol. 15: 378-383.
- Craig, L.S.; Olden, J.D.; Arthington, A.H.; Entrekin, S.; Hawkins, C.P.; Kelly, J.J.; Kennedy, T.; Maitland, B.;, Rosi, E.; Roy, A.; Strayer, D.; Tank, J.; West, A.; Wooten, M. (2017). Meeting the challenge of interacting threats in freshwater ecosystems: A call to scientists and managers. Elem Sci Anth. 5: 72. doi: http://doi.org/10.1525/elementa.256
- Davies, J.; Davies, D. (2010). Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev. 74: 417-433.
- Davis, A.J.; Jenkinson, L.S.; Lawton, J.H.; Shorrocks, B.; Wood, S. (1998) Making mistakes when predicting shifts in species range in response to global warming. Nature. 391: 783 -786. doi: https://doi.org/10.1038/35842
- De Laender, F.; Rohr, J.R.; Ashauer, R.; Baird, D. J.; Berger, U.; Eisenhauer, N.; Grimm, V.; Hommen, U.; Maltby, L.; Meliàn, C.; Pomati, F.; Roessink, I.; Radchuk, V.; Van, P.; Brink, V. (2016) Reintroducing environmental change drivers in biodiversity–ecosystem functioning research. Trends in ecology & evolution. 31(12): 905-915. https://doi.org/10.1016/j.tree.2016.09.007
- Debat, V.; David, P. (2001). Mapping phenotypes: canalization, plasticity and developmental stability. Trends in Ecology & Evolution. 16: 555-561. doi: https://doi.org/10.1016/S0169-5347(01)02266-2
- DeWitt, T.J.; Sih, A.; Wilson, D.S. (1998). Costs and limits of phenotypic plasticity. Trends in ecology & evolution. 13:77-81. https://doi.org/10.1016/S0169-5347(97)01274-3
- Diamond, S.E.; Frame, A.M.; Martin, R.A.; Buckley, L.B. (2011). Species’ traits predict phenological responses to climate change in butterflies. Ecology. 92:1005-1012. doi: https://doi.org/10.1890/10-1594.1
- Ffrench-Constant, R.; Park, Y.; Feyereisen, R. (1999). Molecular biology of insecticide resistance. Mol Biol Toxic Response Taylor Fr Ciudad. 533–551: 83-90. doi: https://doi.org/10.1016/0378-4274(95)03470-6
- Freedman, B. (2015). Ecological Effects of Environmental Stressors. USA: Environmental Science, Oxford University Press. doi: 10.1093/acrefore/9780199389414.013.1
- Gabriel, W. (2005). How stress selects for reversible phenotypic plasticity. J Evol Biol. 18: 873-883.
- Gutiérrez, Y.; Bacca, T.; Zambrano, L.S.; Pineda, M.; Guedes, R. N. (2019). Trade‐off and adaptive cost in a multiple‐resistant strain of the invasive potato tuber moth Tecia solanivora. Pest management science. 75(6): 1655-1662. doi: https://doi.org/10.1002/ps.5283
- Gutiérrez, Y.; Fresch, M.; Ott, D.; Brockmeyer, J.; Scherber, C. (2020a) Diet composition and social environment determine food consumption, phenotype and fecundity in an omnivorous insect. R Soc Open Sci. 7(4): 200100. doi: https://doi.org/10.1098/rsos.200100
- Gutiérrez, Y.; Ott, D.; Scherber, C. (2020b). Direct and indirect effects of plant diversity and phenoxy herbicide application on the development and reproduction of a polyphagous herbivore. Sci Rep. 10: 7300. doi: https://doi.org/10.1038/s41598-020-64252-5
- Gutiérrez, Y.; Ramos, G.S.; Tomé, H.V.; Oliveira, E. E.; Salaro, A. L. (2017a). Bti-based insecticide enhances the predatory abilities of the backswimmer Buenoa tarsalis (Hemiptera: Notonectidae). Ecotoxicology. 26(8): 1147-1155. doi: https://doi.org/10.1007/s10646-017-1840-1
- Gutiérrez, Y.; Santos, H.P.; Serrão, J.E.; Oliveira, E.E. (2016). Deltamethrin-mediated toxicity and cytomorphological changes in the midgut and nervous system of the mayfly Callibaetis radiatus. PLoS One. 11(3): e0152383. doi: https://doi.org/10.1371/journal.pone.0152383
- Gutiérrez, Y.; Tomé, H.V.; Guedes, R,N.C.; Oliveira, E.E. (2017b). Deltamethrin toxicity and impaired swimming behavior of two backswimmer species. Environ Toxicol Chem. 36:1235-1242. doi: https://doi.org/10.1002/etc.3645
- Haddad, N.M.; Holyoak, M.; Mata, T.M.; et al (2008) Species’ traits predict the effects of disturbance and productivity on diversity. Ecology letters. 11(4): 348-356. doi: https://doi.org/10.1111/j.1461-0248.2007.01149.x
- Hall, D.M.; Steiner, R. (2019). Insect pollinator conservation policy innovations: Lessons for lawmakers. Environ Sci Policy. 93:118-128. doi: https://doi.org/10.1016/j.envsci.2018.12.026
- Hallmann, C.A.; Sorg, M.; Jongejans, E.; Siepel, H.; Hofland, N.; Schwan, H.; Stenmans, W.; Müller, A.; Sumser, H.; Hörren, T.; Goulson, D.; de Kroon, H. (2017). More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PloS one. 12(10): e0185809. doi: https://doi.org/10.1371/journal.pone.0185809
- Haubruge, E.; Arnaud, L. (2001). Fitness consequences of malathion-specific resistance in red flour beetle (Coleoptera: Tenebrionidae) and selection for resistance in the absence of malathion. Journal of economic entomology. 94(2): 552-557. doi: https://doi.org/10.1603/0022-0493-94.2.552
- Jackson, M.C.; Loewen, C.J.G.; Vinebrooke, R.D.; Chimimba, C.T. (2016). Net effects of multiple stressors in freshwater ecosystems: a meta‐analysis. Glob Chang Biol. 22:180-189. doi: https://doi.org/10.1111/gcb.13028
- Kassahn, K.S.; Crozier, R.H.; Pörtner, H.O.; Caley, M.J. (2009). Animal performance and stress: responses and tolerance limits at different levels of biological organisation. Biol Rev. 84(2): 277-92. doi: https://doi.org/10.1111/j.1469-185X.2008.00073.x
- Kaunisto, S.; Ferguson, L.V.; Sinclair, B.J. (2016). Can we predict the effects of multiple stressors on insects in a changing climate? Current opinion in insect science. 17: 55-61. doi: https://doi.org/10.1016/j.cois.2016.07.001
- Klein, S.; Cabirol, A.; Devaud, J.M.; Barron, A. B.; Lihoreau, M. (2017). Why bees are so vulnerable to environmental stressors. Trends in ecology & evolution. 32(4): 268-278. doi: https://doi.org/10.1016/j.tree.2016.12.009
- Koolhaas, J.M.; Bartolomucci, A.; Buwalda, B.; de Boer, S. F., Flügge, G., Korte, S. M.; Meerloa, P.; Murisong, R.; Olivieri, B.; Palanzak, P.; Richter-Levine, G.; Sgoifok, A.; Steimerj, T.; Stiedlf, O.; van Dijkh, G.; Wöhrd, M.; Fuchsb, E. (2011). Stress revisited: a critical evaluation of the stress concept. Neurosci Biobehav Rev. 35(5): 1291-1301. doi: https://doi.org/10.1016/j.neubiorev.2011.02.003
- Lexer, C.; Fay, MF. (2005). Adaptation to environmental stress: a rare or frequent driver of speciation? J Evol Biol. 18:893-900. doi: https://doi.org/10.1111/j.1420-9101.2005.00901.x
- Losey, J.E.; Vaughan, M. (2006). The economic value of ecological services provided by insects. AIBS Bull. 56(4): 311-323. doi: https://doi.org/10.1641/0006-3568(2006)56[311:TEVOES]2.0.CO;2
- Luque, G.M.; Bellard, C.; Bertelsmeier, C.; Bonnaud, E.; Genovesi, P.; Simberloff, D.; Courchamp, F. (2014). The 100th of the world’s worst invasive alien species. Biol Invasions. 16: 981-985. doi: https://doi.org/10.1007/s10530-013-0561-5
- McCauley, S.J.; Rowe, L.; Fortin, M-J. (2011). The deadly effects of “nonlethal” predators. Ecology. 9(11): 2043-2048. doi: https://doi.org/10.1890/11-0455.1
- Megido, R.C.; Gierts, C.; Blecker, C.; Brostaux, Y.; Haubruge, É.; Alabi, T.; Francis, F. (2016) Consumer acceptance of insect-based alternative meat products in Western countries. Food Qual Prefer. 52: 237–243. doi: https://doi.org/10.1016/j.foodqual.2016.05.004
- Metcalfe, N.B.; Monaghan, P. (2001). Compensation for a bad start: grow now, pay later? Trends Ecol Evol. 16(5): 254-260.
- Miner, B.G.; Sultan, S.E.; Morgan, S.G.; Padilla, D. K.; Relyea, R. A. (2005). Ecological consequences of phenotypic plasticity. Trends Ecol Evol 20(12): 685-692. doi: https://doi.org/10.1016/j.tree.2005.08.002
- Musolin, D.L. (2007). Insects in a warmer world: ecological, physiological and life‐history responses of true bugs (Heteroptera) to climate change. Global Change Biology. 13(8): 1565-1585. doi: https://doi.org/10.1111/j.1365-2486.2007.01395.x
- Oerke, E-C. (2006). Crop losses to pests. The Journal of Agricultural Science. 144(1): 31-43. doi:
- https://doi.org/10.1017/S0021859605005708
- Padilla, D.K.; Adolph, S.C. (1996). Plastic inducible morphologies are not always adaptive: the importance of time delays in a stochastic environment. Evol Ecol 10:105–117. doi: https://doi.org/10.1007/BF01239351
- Pimentel, D. (1995). Amounts of pesticides reaching target pests: environmental impacts and ethics. Journal of Agricultural and environmental Ethics. 8(1): 17-29. doi: https://doi.org/10.1007/BF02286399
- Pimentel, D. (1994). Insect population responses to environmental stress and pollutants. Environmental Reviews. 2(1): 1-15. doi: https://doi.org/10.1139/a94-001
- Pimentel, D.; Zuniga, R.; Morrison, D. (2005). Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ. 52(3): 273-288. doi: https://doi.org/10.1016/j.ecolecon.2004.10.002
- Potts, S.G.; Biesmeijer, J.C.; Kremen, C.; Neumann, P.; Schweiger, O.; Kunin, W. E. (2010). Global pollinator declines: trends, impacts and drivers. Trends in ecology & evolution. 25(6): 345-353. doi: https://doi.org/10.1016/j.tree.2010.01.007
- Romero, L.M. (2004). Physiological stress in ecology: lessons from biomedical research. Trends Ecol Evol. 19(5): 249-255. doi: https://doi.org/10.1016/j.tree.2004.03.008
- Sánchez-Bayo, F.; Wyckhuys, K.A.G. (2019). Worldwide decline of the entomofauna: A review of its drivers. Biol Conserv. 232: 8–27. doi: https://doi.org/10.1016/j.biocon.2019.01.020
- Schäfer, R.B.; Caquet, T.; Siimes, K.; Mueller, R.; Lagadic, L.; Liess, M. (2007). Effects of pesticides on community structure and ecosystem functions in agricultural streams of three biogeographical regions in Europe. Science of the Total Environment. 382(2-3): 272-285. doi: https://doi.org/10.1016/j.scitotenv.2007.04.040
- Scherber, C.; Gladbach, D.J.; Stevnbak, K.; Karsten, R. J.; Schmidt, I. K.; Michelsen, A.; Rost, K.; Klaus, A.; Larsen Teis, S.; Mikkelsen, N.; Beier, C.; Christensen, S. (2013). Multi‐factor climate change effects on insect herbivore performance. Ecology and evolution. 3(6): 1449-1460. doi: https://doi.org/10.1002/ece3.564
- Schulte, P.M. (2014). What is environmental stress? Insights from fish living in a variable environment. Journal of Experimental Biology. 217(1): 23-34. doi: https://doi.org/10.1242/jeb.089722
- Sinclair, B.J.; Vernon, P.; Klok, C.J.; Chown, S.L. (2003). Insects at low temperatures: an ecological perspective. Trends in Ecology & Evolution. 18(5): 257-262. doi: https://doi.org/10.1016/S0169-5347(03)00014-4
- Smith, K.G. (1973). Insects and other arthropods of medical importance. London: British Museum (Natural History).
- Stearns, S.C.; Kawecki, T.J. (1994). Fitness sensitivity and the canalization of life‐history traits. Evolution (N Y). 48(5): 1438-1450. doi: https://doi.org/10.1111/j.1558-5646.1994.tb02186.x
- Steinberg, C.E.W. (2012). Multiple stressors as environmental realism: synergism or antagonism. In: Stress Ecology. pp. 295-309. Dordrecht: Springer. doi: https://doi.org/10.1007/978-94-007-2072-5_11
- Tanaka, S.; Harano, K.; Nishide, Y.; Sugahara, R. (2016). The mechanism controlling phenotypic plasticity of body color in the desert locust: some recent progress. Curr Opin insect Sci. 17: 10-15. doi: https://doi.org/10.1016/j.cois.2016.05.011
- Tchounwou, P.B.; Yedjou, C.G.; Patlolla, A.K.; Sutton, D.J. (2012). Heavy metal toxicity and the environment. In: Luch A. (eds). Molecular, Clinical and Environmental Toxicology. Experientia Supplementum, vol 101. Basel: Springer. doi: https://doi.org/10.1007/978-3-7643-8340-4_6
- Todgham, A.E.; Stillman, J.H. (2013). Physiological responses to shifts in multiple environmental stressors: relevance in a changing world. Integr Comp Biol. 53: 539-544.
- Urban, M.C.; Bocedi, G.; Hendry, AP.; Mihoub, J.-B.; Pe’er, G.; Singer, A.; Bridle, J. R.; Crozier, L. G.; De Meester, L.; Godsoe, W.;. Gonzalez, A.; Hellmann, J. J.; Holt, R. D.; Huth, A.; Johst, K.; Krug, C. B.; Leadley, P. W.; Palmer, S. C. F.; Pantel, J. H.; Schmitz, A.; Zollner, P. A.; Travis, J.M.J. (2016). Improving the forecast for biodiversity under climate change. Science. (80) 353:aad8466. doi: 10.1126/science.aad8466
- Van Huis, A. (2013). Potential of insects as food and feed in assuring food security. Annu Rev Entomol. 58: 563-583. doi: https://doi.org/10.1146/annurev-ento-120811-153704
- Waddington, C.H. (1942). Canalization of development and the inheritance of acquired characters. Nature. 150: 563- 565. doi: https://doi.org/10.1038/150563a0
- Wagner, G.P.; Booth, G.; Bagheri‐Chaichian, H. (1997) A population genetic theory of canalization. Evolution (N Y). 51(2): 329-347. doi: https://doi.org/10.1111/j.1558-5646.1997.tb02420.x
- Ware, G.W. (1980). Effects of pesticides on nontarget organisms. In: Gunther, F.A.; Gunther J.D. (eds) Residue Reviews. vol 76. New York, NY:.Springer. doi: https://doi.org/10.1007/978-1-4612-6107-0_9
- Weisser, W.W.; Siemann, E. (2008). The various effects of insects on ecosystem functioning. In: In: Weisser W.W., Siemann E. (eds) Insects and Ecosystem Function. Ecological Studies (Analysis and Synthesis), vol 173. Berlin, Heidelberg: Springer. https://doi.org/10.1007/978-3-540-74004-9_1
- Wingfield, J.C. (2013). Ecological processes and the ecology of stress: the impacts of abiotic environmental factors. Funct Ecol. 27:37–44.
- Zabinsky, R.A.; Mason, G.A.; Queitsch, C.; Jarosz, DF. (2018). It’s not magic–Hsp90 and its effects on genetic and epigenetic variation. Seminars in cell & developmental biology. doi: https://doi.org/10.1016/j.semcdb.2018.05.015
- Zalucki, MP.; Shabbir, A.; Silva, R.; Adamson, D.; Shu-Sheng, L.; Furlong, M. J. (2012). Estimating the economic cost of one of the world’s major insect pests, Plutella xylostella (Lepidoptera: Plutellidae): just how long is a piece of string? J Econ Entomol. 105(4): 1115-1129.
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