Multiple mechanisms in which agricultural insects respond to environmental stressors: canalization, plasticity and evolution

Keywords: decline, global change, insecticide resistance, pesticides, plasticity, pollinators, pollution

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, agricultural pesticides and metal pollutants) 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, I provide a short review on prominent environmental stressors, and the known responses that insects may exhibit, which are summarized as canalization, plasticity and evolution. Furthermore, I provide an outlook and recommendation for future studies aiming to elucidate the effects of environmental stressors (both singly and in combination) on insect biology. I advocate for controlled (lab or semi-field) manipulative experiments that implement realistic environmental conditions and that ideally combine several stressors.

Downloads

Download data is not yet available.

References

Adamo SA, 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 AL, Crozier LG, Rissler LJ, et al (2011) Do species’ traits predict recent shifts at expanding range edges? Ecol Lett 14:677–689
Bacca T, Haddi K, Pineda M, et al (2017) Pyrethroid resistance is associated with a kdr‐type mutation (L1014F) in the potato tuber moth Tecia solanivora. Pest Manag Sci 73:397–403

Baird DJ, Van den Brink PJ (2007) Using biological traits to predict species sensitivity to toxic substances. Ecotoxicol Environ Saf 67:296–301

Barsics F, Caparros Megido R, Brostaux Y, et al (2017) Could new information influence attitudes to foods supplemented with edible insects? Br Food J 119:2027–2039
Bebber DP, Holmes T, Gurr SJ (2014) The global spread of crop pests and pathogens. Glob Ecol Biogeogr 23:1398–1407

Bernhardt ES, Rosi EJ, Gessner MO (2017) Synthetic chemicals as agents of global change. Front Ecol Environ 15:84–90

Bidart-Bouzat MG, Imeh-Nathaniel A (2008) Global change effects on plant chemical defenses against insect herbivores. J Integr Plant Biol 50:1339–54. doi: 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 JF, 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 DL, Baxter JW, Hatfield CA, et al (1998) Understanding effects of multiple stressors: ideas and challenges. In: Successes, limitations, and frontiers in ecosystem science. Springer, pp 416–431

Callahan HS, Pigliucci M, Schlichting CD (1997) Developmental phenotypic plasticity: where ecology and evolution meet molecular biology. Bioessays 19:519–525

Cardinale BJ, Duffy JE, Gonzalez A, et al (2012) Biodiversity loss and its impact on humanity. Nature 486:59

Christensen MR, Graham MD, Vinebrooke RD, et al (2006) Multiple anthropogenic stressors cause ecological surprises in boreal lakes. Glob Chang Biol 12:2316–2322

Costanza R, Kubiszewski I, Ervin D, et al (2011) Valuing ecological systems and services. F1000 Biol Rep 3:

Côté IM, Darling ES, Brown CJ (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 LS, Olden JD, Arthington AH, et al (2017) Meeting the challenge of interacting threats in freshwater ecosystems: A call to scientists and managers. Elem Sci Anth 5:

Davies J, Davies D (2010) Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev 74:417–433

Davis AJ, Jenkinson LS, Lawton JH, et al (1998) Making mistakes when predicting shifts in species range in response to global warming. Nature 391:783

De Laender F, Rohr JR, Ashauer R, et al (2016) Reintroducing environmental change drivers in biodiversity–ecosystem functioning research. Trends Ecol Evol 31:905–915

Debat V, David P (2001) Mapping phenotypes: canalization, plasticity and developmental stability. Trends Ecol Evol 16:555–561

DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81

Diamond SE, Frame AM, Martin RA, Buckley LB (2011) Species’ traits predict phenological responses to climate change in butterflies. Ecology 92:1005–1012

Ffrench-Constant R, Park Y, Feyereisen R (1999) Molecular biology of insecticide resistance. Mol Biol Toxic Response Taylor Fr Ciudad 533–551

Freedman B (2015) Ecological Effects of Environmental Stressors. In: Environmental Science - Oxford Research Encyclopedias. Oxford University Press

Gabriel W (2005) How stress selects for reversible phenotypic plasticity. J Evol Biol 18:873–883

Gutiérrez Y, Bacca T, Zambrano LS, et al (2019) Trade‐off and adaptive cost in a multiple‐resistant strain of the invasive potato tuber moth Tecia solanivora. Pest Manag Sci 75:1655–1662

Gutiérrez Y, Fresch M, Ott D, et al (2020a) Diet composition and social environment determine food consumption, phenotype and fecundity in an omnivorous insect. R Soc Open Sci 7:200100

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 10:1–11

Gutiérrez Y, Ramos GS, Tomé HV V, et al (2017a) Bti-based insecticide enhances the predatory abilities of the backswimmer Buenoa tarsalis (Hemiptera: Notonectidae).
Ecotoxicology 26:1147–1155

Gutiérrez Y, Santos HP, Serrão JE, Oliveira EE (2016) Deltamethrin-mediated toxicity and cytomorphological changes in the midgut and nervous system of the mayfly Callibaetis radiatus. PLoS One 11:e0152383

Gutiérrez Y, Tomé HV V, Guedes RNC, Oliveira EE (2017b) Deltamethrin toxicity and impaired swimming behavior of two backswimmer species. Environ Toxicol Chem 36:1235–1242

Haddad NM, Holyoak M, Mata TM, et al (2008) Species’ traits predict the effects of disturbance and productivity on diversity. Ecol Lett 11:348–356

Haddi K, Valbon WR, Jumbo LOV, et al (2018) Diversity and convergence of mechanisms involved in pyrethroid resistance in the stored grain weevils, Sitophilus spp. Sci Rep 8:1–15

Hall DM, Steiner R (2019) Insect pollinator conservation policy innovations: Lessons for lawmakers. Environ Sci Policy 93:118–128

Hallmann CA, Sorg M, Jongejans E, et al (2017) More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS One 12:e0185809

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. J Econ Entomol 94:552–557

Jackson MC, Loewen CJG, Vinebrooke RD, Chimimba CT (2016) Net effects of multiple stressors in freshwater ecosystems: a meta‐analysis. Glob Chang Biol 22:180–189

Kassahn KS, Crozier RH, Pörtner HO, Caley MJ (2009) Animal performance and stress: responses and tolerance limits at different levels of biological organisation. Biol Rev 84:277–292
Kaunisto S, Ferguson L V, Sinclair BJ (2016) Can we predict the effects of multiple stressors on insects in a changing climate? Curr Opin insect Sci 17:55–61

Klein S, Cabirol A, Devaud J-M, et al (2017) Why bees are so vulnerable to environmental stressors. Trends Ecol Evol 32:268–278

Koolhaas JM, Bartolomucci A, Buwalda B d, et al (2011) Stress revisited: a critical evaluation of the stress concept. Neurosci Biobehav Rev 35:1291–1301

Lexer C, Fay MF (2005) Adaptation to environmental stress: a rare or frequent driver of speciation? J Evol Biol 18:893–900

Losey JE, Vaughan M (2006) The economic value of ecological services provided by insects. AIBS Bull 56:311–323

Luque GM, Bellard C, Bertelsmeier C, et al (2014) The 100th of the world’s worst invasive alien species. Biol Invasions 16:981–985

McCauley SJ, Rowe L, Fortin M-J (2011) The deadly effects of “nonlethal” predators. Ecology 92:2043–2048

Megido RC, Gierts C, Blecker C, et al (2016) Consumer acceptance of insect-based alternative meat products in Western countries. Food Qual Prefer 52:237–243

Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260

Miner BG, Sultan SE, Morgan SG, et al (2005) Ecological consequences of phenotypic plasticity. Trends Ecol Evol 20:685–692

Musolin DL (2007) Insects in a warmer world: ecological, physiological and life‐history responses of true bugs (Heteroptera) to climate change. Glob Chang Biol 13:1565–1585

Oerke E-C (2006) Crop losses to pests. J Agric Sci 144:31–43

Padilla DK, Adolph SC (1996) Plastic inducible morphologies are not always adaptive: the importance of time delays in a stochastic environment. Evol Ecol 10:105–117

Pimentel D (1995) Amounts of pesticides reaching target pests: environmental impacts and ethics. J Agric Environ Ethics 8:17–29

Pimentel D (1994) Insect population responses to environmental stress and pollutants. Environ Rev 2:1–15

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 52:273–288

Potts SG, Biesmeijer JC, Kremen C, et al (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353

Romero LM (2004) Physiological stress in ecology: lessons from biomedical research. Trends Ecol Evol 19:249–255

Sánchez-Bayo F, Wyckhuys KAG (2019) Worldwide decline of the entomofauna: A review of its drivers. Biol Conserv 232:8–27

Schäfer RB, Caquet T, Siimes K, et al (2007) Effects of pesticides on community structure and ecosystem functions in agricultural streams of three biogeographical regions in Europe. Sci Total Environ 382:272–285

Scherber C, Gladbach DJ, Stevnbak K, et al (2013) Multi‐factor climate change effects on insect herbivore performance. Ecol Evol 3:1449–1460

Schulte PM (2014) What is environmental stress? Insights from fish living in a variable environment. J Exp Biol 217:23–34

Sinclair BJ, Vernon P, Klok CJ, Chown SL (2003) Insects at low temperatures: an ecological perspective. Trends Ecol Evol 18:257–262

Smith KG V (1973) Insects and other arthropods of medical importance. Insects other arthropods Med importance

Stearns SC, Kawecki TJ (1994) Fitness sensitivity and the canalization of life‐history traits. Evolution (N Y) 48:1438–1450

Steinberg CEW (2012) Multiple stressors as environmental realism: synergism or antagonism. In: Stress Ecology. Springer, pp 295–309

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

Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Heavy metal toxicity and the environment. In: Molecular, clinical and environmental toxicology. Springer, pp 133–164

Todgham AE, Stillman JH (2013) Physiological responses to shifts in multiple environmental stressors: relevance in a changing world. Integr Comp Biol 53:539–544

Tschoeke PH, Oliveira EE, Dalcin MS, et al (2019) Botanical and synthetic pesticides alter the flower visitation rates of pollinator bees in Neotropical melon fields. Environ Pollut 251:591–599

Urban MC, Bocedi G, Hendry AP, et al (2016) Improving the forecast for biodiversity under climate change. Science (80- ) 353:aad8466

Valbon WR, Haddi K, Souza RA, et al (2019) “Armed to the teeth”: The multiple ways to survive insecticidal and predatory challenges in Aedes aegypti larvae. Pestic Biochem Physiol 156:87–95

Van Huis A (2013) Potential of insects as food and feed in assuring food security. Annu Rev Entomol 58:563–583

Waddington CH (1942) Canalization of development and the inheritance of acquired characters. Nature 150:563

Wagner GP, Booth G, Bagheri‐Chaichian H (1997) A population genetic theory of canalization. Evolution (N Y) 51:329–347

Ware GW (1980) Effects of pesticides on nontarget organisms. In: Residue reviews. Springer, pp 173–201

Weisser WW, Siemann E (2008) The various effects of insects on ecosystem functioning. In: Insects and ecosystem function. Springer, pp 3–24

Wingfield JC (2013) Ecological processes and the ecology of stress: the impacts of abiotic environmental factors. Funct Ecol 27:37–44

Zabinsky RA, Mason GA, Queitsch C, Jarosz DF (2018) It’s not magic–Hsp90 and its effects on genetic and epigenetic variation. In: Seminars in cell & developmental biology. Elsevier

Zalucki MP, Shabbir A, Silva R, et al (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 105:1115–1129
Published
2020-06-20
How to Cite
Gutiérrez, Y. (2020). Multiple mechanisms in which agricultural insects respond to environmental stressors: canalization, plasticity and evolution. Revista De Ciencias Agrícolas, 37(1). Retrieved from https://revistas.udenar.edu.co/index.php/rfacia/article/view/5728