Trends in Ecology & Evolution, Journal Year: 2022, Volume and Issue: 37(9), P. 789 - 802

Published: June 16, 2022

Wildlife are exposed to an increasing number and diversity of chemical pollutants.Chemical pollutants can elicit a range sublethal effects on individual organisms, but research how these contaminants affect social interactions animal groups is severely lacking.It imperative that perspectives from behavioural ecology ecotoxicology integrated, increase our understanding contaminant individuals might cascade group-level processes.We present conceptual framework for researchers practitioners guide the study emergence, organisation, function groups. Chemical pollution among fastest-growing agents global change. Synthetic chemicals with diverse modes-of-action being detected in tissues wildlife pervade entire food webs. Although such lacking. Here we synthesise two related, largely segregated fields – examine pathways by which could disrupt processes govern self-organisation, collective Our review provides roadmap prioritising within context sociality highlights important methodological advancements future research. Pollution arising production consumption synthetic now outpaces other environmental megatrends (e.g., rising CO2 emissions [1.Bernhardt E.S. et al.Synthetic as change.Front. Ecol. Environ. 2017; 15: 84-90Crossref Scopus (377) Google Scholar]). Increasing human reliance, coupled world population growth insufficient regulation, has driven exponential rise products marketed globally (>350 000 [2.Wang Z. al.Toward pollution: first comprehensive analysis national regional inventories.Environ. Sci. Technol. 2020; 54: 2575-2584Crossref PubMed (332) Scholar]), corresponding surge infiltrating environment [3.Landrigan P.J. al.Pollution health agenda prevention.Environ. Health Perspect. 2018; 126084501Crossref (52) Scholar]. Ecosystems worldwide staggering array compounds agrochemicals [4.Tang F.H.M. al.Risk pesticide at scale.Nat. Geosci. 2021; 14: 206-210Crossref (293) Scholar] metals [5.Briffa J. al.Heavy metal their toxicological humans.Heliyon. 6e04691Abstract Full Text PDF (1161) Scholar], pharmaceuticals [6.Wilkinson J.L. al.Pharmaceutical world's rivers.Proc. Natl. Acad. U. S. A. 2022; 119e2113947119Crossref (328) personal care [7.Dey al.1 - Pharmaceuticals product (PPCP) contamination—a discharge inventory.in: Prasad M.N.V. Personal Care Products: Waste Management Treatment Technology. Butterworth-Heinemann, 2019: 1-26Crossref (84) Many degrade slowly remain highly persistent environment, while others released near-constant rate thus considered be 'pseudo-persistent'. Consequently, have been wide [8.Li Y. al.Neonicotinoids decline bird biodiversity United States.Nat. Sustain. 3: 1027-1035Crossref (70) Scholar,9.Garcia-Cegarra A.M. al.Persistence, bioaccumulation vertical transfer long-finned pilot whales stranded Chilean Patagonia.Sci. Total 770145259Crossref (8) pervading webs [10.Richmond E.K. al.A suite contaminates stream riparian webs.Nat. Commun. 9: 1-9Crossref (165) Scholar,11.Yamamuro M. aquatic decrease fishery yields.Science. 2019; 366: 620-623Crossref (145) A wealth dating back Rachel Carson's seminal 1962 publication Silent Spring [12.Carson R. Spring. Fawcett Publications, 1962Google documented adverse impacts wildlife. Besides causing mortality acutely lethal levels, animals, even minute concentrations including disrupting behaviour. Such may hidden drivers declines ecological instability [13.Saaristo al.Direct indirect behaviour, evolution wildlife.Proc. Soc. B Biol. 28520181297PubMed fuelling calls better integration indicators into risk assessment [14.Ford A.T. al.The role behavioral protection.Environ. 55: 5620-5628Crossref (83) However, nearly all (see Glossary) focused behaviours little consideration emergent group functions. This critical oversight because many animals engage over lifetime live structured societies or form loosely (Figure 1). These coordinate conspecifics provide protection against predation, gain reproductive opportunities, find food, reduce energy expenditure [15.Krause al.Living Groups. Oxford University Press, 2002Google Collective behaviour directly affects both fitness. Here, novel outlines instrumental emergence self-organisation We formulate predictions disruptions ultimately outcomes, detail themselves exacerbate buffer contamination, species Importantly, presents timely opportunity integrate key step towards improving threat posed influence impacting units compose (i.e., individuals) and/or those sociality). manifest across local spatial scales change formation 2, Key figure ). integrates mechanisms underlie different types systems, dynamic fission–fusion relatively stable To predict groups, need understand they environmentally realistic exposure levels. Documented severe physiological physical impairment, subtler not stress escape response. focus examples cascading implications level (Box 1).Box 1Can make generalised certain classes will impact groups?Chemical unique challenge due sheer classes, existence numerous between classes. The species-specific, contingent several factors, degree homology non-target intended target species. Further, do primary mode-of-action conventionally associated disruption antibiotics, antihistamines), specifically designed metals, surfactants), yet still so. makes generating difficult. biological targets, disruption, general valuable directing studies sociality. In Table I, outline series individual-level induced expected consequences, identify predicted induce effects.Table IGeneral consequencesIndividual-level effectsChemical classesaFor each class, use example subgroup narrow specific targets. class 1–8.Group formationGroup dynamicsRefsAntisocial behaviour1,2,3,4,5Reduced tendency accept Higher rejection potential members.Increased conflict amongst members weaker networks. Altered structure.[33.Whitlock S.E. al.Environmentally relevant antidepressant alters courtship songbird.Chemosphere. 211: 17-24Crossref (18) Scholar,34.Hubená P. al.Prescribed aggression fishes: modify concentrations.Ecotoxicol. Saf. 227112944Crossref Scholar,92.Santos M.E.S. al.Traces tramadol water native European fish.Ecotoxicol. 212111999Crossref (9) Scholar, 93.Brodin T. al.Dilute psychiatric drug alter behavior fish natural populations.Science. 2013; 339: 814-815Crossref (602) 94.Fenske L. al.17-α-Ethinylestradiol modulates endocrine responses zebrafish.Environ. Pollut. Res. Int. 27: 29341-29351Crossref (14) Scholar]Reduced anxiety perception1,2,6Decrease propensity join (particularly if grouping primarily antipredator strategy).Slow response times actions. Less coordination cohesion. risk-taking poorer predator evasion.[30.Cerveny D. al.Bioconcentration four benzodiazepines mixture wild fish.Sci. 702134780Crossref (20) Scholar,57.Martin J.M. psychoactive pollutant fluoxetine compromises fish.Environ. 222: 592-599Crossref (90) Scholar,93.Brodin Scholar]Hyperactivity3,4Higher interaction rates, lower capacity adjust formation.Faster movement, altering cohesion polarisation. Hyperactive rejected unimpaired groups.[95.Horký al.Methamphetamine elicits addiction fish.J. Exp. 224jeb242145Crossref (23) Scholar,96.De Serrano A.R. al.Paternal common pharmaceutical (Ritalin) transgenerational Trinidadian guppies.Sci. Rep. 11: 3985Crossref (6) Scholar]Lower activity/compromised locomotion1,5,6,7,8Inability impaired join, move between, groups.Slower Impaired likely groups.[42.Eng M.L. al.Imidacloprid chlorpyrifos insecticides impair migratory ability seed-eating songbird.Sci. 7: 15176Crossref (105) Scholar,97.Ložek F. al.Behaviour cardiac signal crayfish tramadol.Aquat. Toxicol. 213105217Crossref (17) 98.Almeida C.H.S. al.Sublethal agrochemical exposures honey bees' neotropical stingless color preferences, respiration locomotory responses.Sci. 779146432Crossref 99.Bachour R.-L. al.Behavioral citalopram, tramadol, binary zebrafish (Danio rerio) larvae.Chemosphere. 238124587Crossref (39) 100.Matus G.N. al.Behavior histopathology biomarkers evaluation paracetamol propranolol Phalloceros harpagos.Environ. 25: 28601-28618Crossref Scholar]Altered cognition4,7,8Reduced process information cues formation.Reduced competence inappropriate partners. Poorer decision-making coordination.[16.Bókony V. al.Effects little-studied early development anurans.Environ. 260114078Crossref (15) Scholar,95.Horký Scholar,101.Siviter H. al.Quantifying pesticides learning memory bees.J. Appl. 2812-2821Crossref (94) Scholar]Sensory disruption3,8Inability attract discriminate members. Reduced assortment.Poor communication Uncoordinated increased failure actions.[20.Besson al.Anthropogenic stressors sensory survival via thyroid disruption.Nat. 1-10Crossref (26) Scholar,23.Ankley G.T. androgenic promoter 17-β-trenbolone fecundity endocrinology fathead minnow.Environ. Chem. 2003; 22: 1350-1360Crossref Scholar,60.Tomkins al.An endocrine-disrupting agricultural sequential female mate choice 237: 103-110Crossref (28) Scholar]1-Antidepressants selective serotonin reuptake inhibitors)2- Anxiolytics benzodiazepines)3-Steroids androgens)4- Psychostimulants central nervous system stimulants)5- Analgesics opioids)6- Beta-blockers nonselective blockers)7- Anticonvulsants dibenzazepines)8- Insecticides neonicotinoids)a For 1–8. Open table new tab 1-Antidepressants inhibitors) 2- benzodiazepines) 3-Steroids androgens) 4- stimulants) 5- opioids) 6- blockers) 7- dibenzazepines) 8- neonicotinoids) Exposure lead dramatic morphological alterations, changes body size [16.Bókony colouration [17.Chatelain al.Do trace visual signals? Effects iridescent melanic feather feral pigeon.Oikos. 126: 1542-1553Crossref sex [18.Kidd K.A. al.Collapse after estrogen.Proc. 2007; 104: 8897-8901Crossref (1577) Perhaps most fundamental interfere anatomy involved visual, auditory, olfactory, tactile senses). Various surfactants pesticides, herbicides damage chemoreceptors olfactory [19.Razmara al.Mechanism copper nanoparticle toxicity rainbow trout mucosa.Environ. 284117141Crossref (13) Scholar,20.Besson amphibians [21.Sievers al.Contaminant mixtures interact predator-avoidance larval amphibian.Ecotoxicol. 161: 482-488Crossref (44) insects [22.Williamson S.M. 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