Researchers from Sweden, the United States and Austria have collaborated to understand the impacts of chemical pollutants on wildlife. Here are their perspectives on how animal behavioural ecology is influenced by pharmaceuticals.
Synthetic chemical pollutants such as pharmaceuticals have made their way into the environment, the animals that inhabit them and their food web. This under-researched form of pollution has been previously studied in the context of how it
impacts the way social animals establish groups. However, until now, there has been little research into how pharmaceutical pollutants may impact collective behaviour of highly social animals over their lifetime.
Research shows the number of orthologs (same genes across species) and sequence similarities. Orthologs for 1,292 drug targets were identified in mice with a similarity of 87%, chickens (1,151) was 70% and aquatic vertebrates was above
60%. Figure redrawn from Gunnarsson L., et al. (2008) Environ. Sci. Technol. with permission. | Gunnarsson L. 2008 / ACS
Publications
The big question is: how are our pharmaceuticals reaching animals in their natural environments? Many drugs are designed to resist becoming inactive. Therefore, when drug residues are excreted by our bodies, they can persist for a long time
in wastewater sewage and reach water systems.
So, how do these drugs affect animals when they were intended to treat humans? The answer to this is linked to how certain drugs reach their target receptors in human tissue in the first place. Most of these receptors in human cells are
evolutionarily conserved, meaning that our receptors share very similar structures with those across the animal kingdom.
How do chemical pollutants impact individuals?
Previous research on this topic has focused on chemical pollution, with impacts ranging from psychological stress, to physical impairment, to death. Studies on agile frogs (Rana dalmatina) and common toads (Bufo bufo) found
that the drug carbamazepine, which is used to treat epilepsy, can reduce their average adult body size. However, the ecological implications of these changes are not well understood.
Another study found that exposure to trace metals can affect feral pigeons’ (Columba livia) feather coloration by reducing the iridescence brightness, which could in turn have implications for sexual selection.
Chemicals can also disturb animal behaviour neurologically, through the alteration of hormones and neurotransmitters. Male zebra finches (Taeniopygia guttata) exposed to lead during development had shrunken key neural circuits and
song nuclei, affecting song learning ability that is crucial to attract females.
The window of opportunity for a male zebra finch to learn song chirping is sensitive for development. As a result, song, as well as colouration, is vulnerable to adverse environmental conditions—consequently influencing the species
reproductive success.
A further study found evidence that fluoxetine antidepressants in the environment may interfere with the neurotransmission or endocrine systems of some aquatic species, such as by inducing tentacle contraction and reducing swimming ability.
Thus, these unintentional impairments can affect reproductive behaviour and therefore indirectly limit an individual’s ability to join and form groups.
Epilepsy drugs have been known to reduce the body sizes of agile frogs (shown in image) and common toads | Angelo Casto / Unsplash
Formation of animal groups
In order to increase their survival, social animals gravitate towards forming, joining and maintaining a group. For example, hierarchical macaque social groups can comprise 50 or more individuals of all ages and both sexes. Other animals
form fission–fusion societies, which are highly dynamic groups such as swarms of insects, schools of fish or flocks of birds.
In these social groups, members can split (fission) or merge (fusion) as needed. Chemical pollution can interfere with these group formation processes by altering individual phenotypes or removing phenotypes from a population, affecting
population densities over time.
Macaques live in complex social groups and their survival depends on maintaining the group structure. | Olivier
GRYSON / Flickr
In another instance, fish rely on group formation to find food, potential mates, and minimise risk from predators. A study investigated the effects of the psychoactive drug Prozac on guppy populations (Poecilia reticulata) from
Alligator Creek, in Bowling Green Bay National Park, Australia.
They found evidence that this pharmaceutical chemical pollution was associated with a decline in individual behavioural variation, such as repeatability and reduced risk-taking, which lead to reduced predator-avoidance and reproduction. The
population consequently also suffered from reduced genetic variation.
‘Chemical pollution can also interfere with these group formation processes.’
Antidepressants have also been known to alter social behaviour, even impacting the individual’s decision to join a group. Turquoise killifish (Nothobranchius furzeri) that are exposed to fluoxetine, an SSRI that is often found in
surface waters worldwide, are more prone to join a group and reproduce.
On the other hand, Siamese fighting fish (Betta splendens) exposed to a sunscreen filter known as benzophenone-3 (BP3) had the opposite effect; the individual’s preference to join a group was attenuated. This is because the chemical
decreased the fish's courtship behaviours, which impeded successful mating.
Either way chemical exposure comes at a cost; pharmaceuticals trigger diverse biochemical pathways influencing the body’s physiological demands. An animal having a decreased propensity to join a group will lead to a higher overall energetic
cost without the assistance of additional group members and will need more resources to meet this increased demand.
Guppies exposed to antidepressant drugs can affect behaviours such as predator-avoidance and reproduction at a genetic level. | George
Wong / Unsplash
Chemicals can influence entire groups of animals, such as those that depend on collective behaviours that arise due to feedback and social interactions. Schools of fish or flocks of birds can travel in synchrony by individuals collectively
matching each other's speeds and movements.
The chronic exposure to pharmaceuticals is affecting animal behaviour in ways we do not yet fully understand. More worrying, is the fact that these effects can be transgenerational, with phenotypic changes being passed down through
generations.
Coupled with non-pharmaceutical pollution, such as metal from mining, oil and carbon emissions from the fossil fuel industry and transportation, and pesticides from agriculture, it is clear both animals and humans are at risk.
Robaire B., Delbes G., Head J., et al. (2022) A cross-species comparative approach to assessing multi- and transgenerational effects of endocrine disrupting chemicals.
Environmental Research. Volume 204, Part B, Page 112063.
Bókony V., Verebélyi V. and Ujhegyi N. (2020) Effects of two little-studied environmental pollutants on early development in anurans.Environmental Pollution. Volume 260, Issue
114078.
Chatelain M., Pessato A., Frantz A., et al. (2017) Do trace metals influence visual signals? Effects of trace metals on iridescent and melanic feather colouration in the feral pigeon. Oikos. Volume 126, Issue 11, pages
1542-1553.
Goodchild C.G., Bec M.L., VanDiest I., et al. (2021) Male zebra finches exposed to lead (Pb) during development have reduced volume of song nuclei, altered sexual traits, and received less attention from females as adults.
Ecotoxicology and Environmental Safety. Volume 210, Issue 111850.
Perez C., Moye J., Cacela D., et al. (2017) Homing pigeons externally exposed to Deepwater Horizon crude oil change flight performance and behavior. Environmental Pollution. Volume 230, Pages 530-539.
Gunnarsson L., Jauhiainen A., Kristiansson E., et al. (2008) Evolutionary Conservation of Human Drug Targets in Organisms used for Environmental Risk Assessments. Environmental Science & Technology. Volume 42, Issue 15,
Pages 5807-5813.
Michelangeli M., Martin J.M., Pinter-Wollman N., et al. (2022) Predicting the impacts of chemical pollutants on animal groups. Cell Trends in Ecology & Evolution. Volume 37, Issue 9, Pages 789-802.
Polverino G., Martin J., Bertram M., et al. (2021) Psychoactive pollution suppresses individual differences in fish behaviour. Proc. R. Soc. B. Volume 288, Issue 1944, 20202294.
Portrais K., Stevens M., Trask C., et al. (2019)Exposure to the ultraviolet filter benzophenone-3 (BP3) interferes with social behaviour in male Siamese fighting fish. Animal Behaviour. Volume 158, Pages
175-182.
Sankey D., Shepard E., Biro D., et al. (2019) Speed consensus and the ‘Goldilocks principle’ in flocking birds (Columba livia). Animal Behaviour. Volume 157, Pages 105-119.
Thoré E.S.J., Philippe C., Brendonck L, et al. (2020) Antidepressant exposure reduces body size, increases fecundity and alters social behavior in the short-lived killifish Nothobranchius furzeri. Environmental Pollution.
Volume 265, Part A, Page 115068.