Table 1.
Research in behavioural ecotoxicology has increased markedly in ecological realism, especially in recent years. This includes studies conducted within each of the key areas for future research identified in Fig. 1, although such studies are still relatively rare. Examples of these studies are provided here, grouped by research area
| Research area | Compound(s)/stressor(s) | Species | Major result(s) | Reference |
|---|---|---|---|---|
|
Personality Behavioural differences between individuals that are consistent over time and across contexts (see Montiglio & Royauté, 2014; Jacquin et al., 2020) |
Phosmet (organophosphate insecticide) | Jumping spider (Eris militaris) | Repeatability of personality traits declined in the exposed group, mostly mediated by an increase in within‐individual variance. | Royauté, Buddle & Vincent (2015) |
| Esfenvalerate (pyrethroid insecticide) | Damselfly (Coenagrion puella) | Exposure changed average activity and behavioural covariation (activity and boldness) but not behavioural repeatability. | Tüzün et al. (2017) | |
| Mixture of metals, mainly lead, copper, and zinc | Great tit (Parus major) | Exploration behaviour and aggressiveness during nest defence were repeatable across years. Birds with high levels of lead in their blood and high levels of multiple metals in their feathers exhibited slower exploration behaviour but no effect of exposure was seen on aggressiveness. | Grunst et al. (2019) | |
| Fluoxetine (antidepressant pharmaceutical) | Guppy (Poecilia reticulata) | Homogenised individuals' activity (i.e. reduced consistent variation between individuals). | Tan et al. (2020) | |
| Fluoxetine (antidepressant pharmaceutical) | Guppy (Poecilia reticulata) | Homogenised individuals' activity (i.e. reduced variation between but not within individuals). | Polverino et al. (2021) | |
|
Pace‐of‐life syndrome The correlation between an individual's average behaviour (e.g. activity) and averages of its other phenotypic traits (e.g. metabolic rate, growth rate), with all traits significantly repeatable after repeated measures. |
Chlorpyrifos (organophosphate insecticide) | Ischnura damselfly species (I. elegans, I. genei, I. graellsii and I. pumilio) | Exposure affected covariation of life‐history and boldness in the most fast‐lived species (I. pumilio). | Debecker et al. (2016) |
| Zinc (heavy metal) | Blue‐tailed damselfly (Ischnura elegans) | Fast pace‐of‐life was associated with higher zinc sensitivity. Zinc exposure made larvae less active, less exploratory, and less risk‐taking. Exposure to zinc did not change the covariation patterns between traits (behavioural and physiological). | Debecker & Stoks (2019) | |
| Fluoxetine (antidepressant pharmaceutical) | Fairy shrimp (Branchipodopsis wolf) | Fluoxetine disrupted sex‐specific relationships between body size (proxy for growth rate) and activity. | Thoré, Brendonck & Pinceel (2021b) | |
|
Collective behaviour A form of social behaviour involving the coordinated behaviour of groups of similar individuals, and the emergent properties of these groups. |
4‐nonylphenol (endocrine‐disrupting chemical) | Banded killifish (Fundulus diaphanus) | Unexposed fish oriented away from dosed conspecifics. Shoals of all exposed fish had larger nearest‐neighbour distances (less‐tight shoals). | Ward et al. (2008) |
| Imidacloprid (neonicotinoid insecticide) | Bumblebee (Bombus impatiens) | Impaired nursing behaviour and altered social and spatial dynamics of workers within nests. | Crall et al. (2018) | |
| Crude oil | Atlantic croaker (Micropogonias undulatus) | Reduced shoal cohesion in shoals with all exposed fish and in shoals with only one exposed fish. | Armstrong et al. (2019) | |
| Benzo[a]pyrene (polycyclic aromatic hydrocarbon; PAH) | Zebrafish (Danio rerio) | Increased inter‐individual distances in exposed shoals. Exposed shoals moved less overall. | Hamilton et al. (2021) | |
| Oxazepam (anxiolytic pharmaceutical) | Brown trout (Salmo trutta) | Fish were less aggressive at higher doses and subordinate fish became more competitively successful at low doses (dominant and subordinate fish affected differently). | McCallum et al. (2021) | |
|
Species interactions Behavioural interactions between individuals of different species, such as predator–prey and competitive interactions (see Saaristo et al., 2018; Fleeger, 2020; Fisher et al., 2021) |
Carbaryl (carbamate insecticide), malathion (organophosphate insecticide) | Amphibian prey (gray treefrog, Hyla versicolor; green frog, Rana clamitans; American bullfrog, R. catesbeiana) and a predator (red‐spotted newt, Notophthalmus viridescens) | Exposure to either insecticide reduced the activity of all three tadpole prey species, and reduced the predation rate of newts on one tadpole species. | Relyea & Edwards (2010) |
| Urban and industrial contamination, including polychlorinated biphenyls (PCBs), polycyclic aromatic hydrocarbons (PAHs), dioxins, and metals (e.g. copper, lead, zinc) | Killifish (Fundulus heteroclitus), bluefish (Pomatomus saltatrix), fiddler crab (Uca pugnax), blue crab (Callinectes sapidus), grass shrimp (Palaemonetes pugio) | At contaminated sites, all five species showed reduced activity and feeding. Complex behavioural changes were also seen within species due to contamination, including reduced predator avoidance in killifish but increased predator avoidance in fiddler crabs and blue crabs. | Weis et al. (2011) | |
| Trifloxystrobin (TFS, strobilurin fungicide) | Eel (Synbranchus marmoratus), four anuran prey species (Rhinella arenarum, Physalaemus santafecinus, Leptodactylus latrans, Elachistocleis bicolor) | Exposure altered the outcome of eel–tadpole interactions by decreasing prey movement and prey detection, increasing tadpole survival. Eels preyed selectively upon non‐exposed tadpoles. | Junges et al. (2012) | |
| 17β‐oestradiol (E2, oestrogen steroid hormone) | Fathead minnow (Pimephales promelas), bluegill sunfish (Lepomis macrochirus) | Exposure reduced anti‐predator escape behaviour of larval minnows and they were more likely to be predated by a sunfish predator. | Rearick et al. (2018) | |
| Dichlorodiphenyltrichloroethane (DDT, organochlorine insecticide) | African clawed frog (Xenopus laevis), mosquito (Culex sp.) | Significant exposure × prey cue interaction. Exposure reduced frog foraging behaviour towards live prey cues, although no effect was seen in response to olfactory prey cues. Mosquito larvae exhibited reduced antipredator behaviour. | South et al. (2019) | |
|
Host–pathogen interactions The interactions between microbes (e.g. parasites, bacteria, viruses) and their host organism(s), which may alter the behaviour of the host. |
Imidacloprid (neonicotinoid insecticide), entomopathogenic fungi (Metarhizium robertsii and Beauveria bassiana) | Citrus root weevil (Diaprepes abbreviatus) | Application of either fungus had no effect on the movement of larvae in soil, although insecticide exposure was found to impair larval movement. Moreover, exposure to both imidacloprid and a fungus acted synergistically to produce more severe impairment to larval movement. | Quintela & McCoy (1998) |
| Chlorpyrifos (organophosphate insecticide), trematode parasite (Euhaplorchis californiensis) | California killifish (Fundulus parvipinnis) | Insecticide exposure reduced activity and decreased average swimming speed following a simulated predator attack. No singular or interactive effects of parasite infection were observed. | Renick et al. (2016) | |
| Mixture of metals (cadmium, copper, and zinc), immune challenge (antigen mixture mimicking a parasite infection) | Gudgeon (Gobio occitaniae) | Single stressors increased immune defences and oxidative stress at the expense of body mass (metal contamination) or swimming activity (immune challenge). Multiple stressors produced fewer interactive effects than expected but primarily resulted in antagonistic effects on swimming activity. | Petitjean et al. (2021) | |
|
Multiple stressors The potentially interacting effects of combined exposure to multiple contaminants (within and/or across contaminant classes), or to contaminants and other external stressors (e.g. temperature, light, noise) (see Halfwerk & Slabbekoorn, 2015; Hale, Piggott & Swearer, 2017; Jacquin et al., 2020) |
Copper (heavy metal), imidacloprid (insecticide) | Spotted marsh frog (Limnodynastes tasmaniensis) | Copper increased erratic swimming at the lower imidacloprid concentration. Limited overall evidence for interactive effects (both stressors produced independent effects). | Sievers et al. (2018) |
| Chlorpyrifos (organophosphate insecticide), flow speed | California killifish (Fundulus parvipinnis), polychaete worm (Polydora cornuta) | Contamination and differing flow speeds resulted in complex effects on predator–prey interactions, including reducing prey‐patch selection in contaminated killifish and reducing feeding behaviour in worms. | Hayman et al. (2019) | |
| 17β‐trenbolone (androgenic steroid), temperature | Eastern mosquitofish (Gambusia holbrooki) | Contamination increased boldness, with effects of exposure on some behaviours (i.e. exploration and predator‐escape behaviour) being dependent on temperature. | Lagesson et al. (2019) | |
| Fluoxetine (antidepressant pharmaceutical), acute temperature stress | Guppy (Poecilia reticulata) | No evidence for interactive effects on reproductive behaviours and activity levels (both stressors produced independent effects). | Wiles et al. (2020) | |
| Chlorpyrifos (organophosphate insecticide), acute, developmental, and transgenerational warming | Mosquito (Culex pipiens) | Particularly developmental and transgenerational warming reduced larvae antipredator behaviours. Contamination decreased heat tolerance and antipredator behaviours. | Meng et al. (2021) | |
|
Laboratory to field Using paired laboratory‐ and field‐based approaches to investigate potentially behaviour‐modifying effects of contaminants. Note: also included here are semi‐field and field‐based studies without a paired laboratory component (see Hellström et al., 2016b; Saaristo et al., 2018) |
Urban and industrial contamination, including copper, cadmium, and polycyclic aromatic hydrocarbons (PAHs). | Round goby (Neogobius melanostomus) | In the laboratory, fish collected from contaminated sites exhibited reduced activity and exploration, although this was not reflected in distance moved in a mark–recapture field study. | Marentette et al. (2012) |
| Neonicotinoid insecticide mixture (thiamethoxam and imidacloprid) | European honey bee (Apis mellifera) | Individual honeybees near treated fields disappeared more quickly but this was buffered by the colonies' demographic regulation response. | Henry et al. (2015) | |
| Oxazepam (anxiolytic pharmaceutical) | Atlantic salmon (Salmo salar) | Promoted downward migratory behaviour in the laboratory and in a natural river tributary. | Hellström et al. (2016a) | |
| Oxazepam (anxiolytic pharmaceutical) | European perch (Perca fluviatilis) | Increased boldness and activity both in the laboratory and in a lake ecosystem. | Klaminder et al. (2016) | |
| Clothianidin (neonicotinoid insecticide) | Bumblebee (Bombus terrestris audax) | In a semi‐field experiment, exposure produced subtle changes in patterns of foraging activity and pollen foraging, with a colony census at the end of the experiment revealing that treated colonies had fewer adults (workers, drones, and gynes) compared to control colonies. | Arce et al. (2017) | |
|
Long‐term exposure Examining potential behavioural effects of long‐term exposure to contaminants, including chronic, transgenerational, and multigenerational exposures. |
Carbamazepine (anticonvulsant pharmaceutical), gemfibrozil (blood lipid‐regulating pharmaceutical) | Zebrafish (Danio rerio) | Parental exposure to either drug reduced male courtship behaviour in unexposed offspring. Effects on courtship displays were compound‐specific. | Galus et al. (2014) |
| Fluoxetine (antidepressant pharmaceutical) | Zebrafish (Danio rerio) | Developmental exposure produced hypocortisolism and reduced exploratory behaviours in two consecutive generations of unexposed descendants. | Vera‐Chang et al. (2018) | |
| Lambda‐cyhalothrin (LCT, pyrethroid insecticide) | Mustard leaf beetle (Phaedon cochleariae) | Parental exposure altered aspects of mating behaviour in both the parental generation and unexposed offspring. | Müller, Römer & Müller (2019) | |
| Urban contaminant mixture, including bisphenol‐A (BPA, xenoestrogen), N,N‐diethyl‐meta‐toluamide (DEET, insect repellent), and 4‐nonylphenol (xenoestrogen) | Fathead minnow (Pimephales promelas) | Exposure for three generations altered the behaviour (foraging, courtship, boldness) of larvae and adults, which were magnified in the F1 and F2 generations. | Swank et al. (2021) | |
| Fluoxetine (antidepressant pharmaceutical) and 3,4‐dichloroaniline (pesticide) | Turquoise killifish (Nothobranchius furzeri) | Behavioural effects differed in single‐chemical versus mixture exposure treatments, and across two successive generations. | Thoré et al. (2021) |