Polluted waterways may alter fish behavior

By Doug Johnson, Canadian writer, editor, and journalist. Originally published in Undark.

The world’s aquatic habitats are an intoxicating brew of pollutants. An estimated 14 million tons of plastic enter the ocean as waste each year. Inside, more than 40 percent of the world’s rivers contain human pharmacopoeia, including antidepressants and pain relievers. Heavy metals such as mercury can also appear from industrial waste. Agricultural fertilizers can seep from the soil into rivers, eventually reaching the ocean.

There are an estimated 20,000 species of fish in the world – possibly many more. They and many other organisms that live in “contaminated systems polluted with a mixture of chemicals,” said Michael Bertram, a behavioral ecologist at the Swedish University of Agricultural Studies.

Bertram and other researchers are finding that these compounds may alter fish behavior. In some experiments, the pollutants appear to alter how fish communicate, either by exposing them to psychoactive drugs or by altering their normal development, which may alter the way they swim together and mate. Others seem to make the fish take more risks which, in the wild, can increase their odds of being caught by predators.

The effects of pollution, according to researchers working in this field, are still unknown. This is partly due to the huge number of variables in real ecosystems, which can limit scientists’ abilities to infer how pollutants affect fish in the wild, said Quentin Petijian, a postdoctoral researcher in environmental sciences at the Sophia Agrobiotic Institute in France. – Author of a 2020 paper that looked at the existing literature on pollution and fish behavior. “In the wild, fish and other organisms are exposed to a large number of stressors,” he said.

However, these changing behaviors can have significant effects, according to Bertram. Like many organisms, fish are important parts of their ecosystems, and changing their behavior can hinder or alter their roles in unexpected ways. For example, one study suggests that various chemical pollutants and microplastics can affect the boldness of predatory fish species. Although the authors note that this is unlikely to lead to a population collapse, these “minor modifications in behavior” can reduce the fish’s biomass, alter their size, and ultimately harm predators as well. This single effect, they add, “may be a hidden mechanism behind ecosystem structure changes in both freshwater and marine ecosystems.”

But humans have a funny way of showing their appreciation. One example: People regularly eliminate psychoactive substances, which then find their way into aquatic ecosystems. In 2021, Bertram and a team of researchers published a paper on how the common antidepressant, fluoxetine, better known by the brand name Prozac, affects the tendency of guppies to wallow, or to swim in groups. Over the course of two years, the team exposed groups of guppies to different concentrations of fluoxetine: a low concentration (usually seen in the wild), a high concentration (representing a highly polluted ecosystem), and no fluoxetine at all.

At the higher concentration of exposure, the guppies appeared to be more social, spending more time in the shallows. However, this was only the case in male-female pairs, not when the fish swam singly. Previous research by Bertram and colleagues showed that the drug increases the amount of time males spend chasing females. “Through intense courtship” by males, females will preferentially choose the larger school to distract them and “to avoid persistent mating behaviour,” said Bertram.

While drugs like Prozac are designed to alter brain function, there are other, perhaps less obvious, ways in which pollution can alter behavior. For example, contaminants may alter the microbiome, the collection of microscopic organisms such as fungi and bacteria that reside on or in an organism. In humans, disturbances of microbial life have been linked to disorders such as autism spectrum disorder, dementia, or even simply cognitive impairment. Research published in 2022 suggests that fish brains may also depend on the host of microorganisms.

In the study, the researchers worked with two groups of zebrafish embryos that they rendered germ-free, functionally stripping them of their microbes. In the containers containing a single set of embryos, the team immediately introduced water from a tank of full-grown zebrafish to give the purified population a microbiome. A week later, they did the same thing with the other group.

After another week, the researchers ran a series of experiments, placing two fish from the same group in adjacent tanks to see if they would swim side by side, a previously identified behavior.

Fish deprived of their early-life microbiome spent significantly less time doing this behavior than those in the control group. Of the 54 control fish, nearly 80 percent spent their time near the barrier between tanks, compared to about 65 percent of 67 in the other group. Exposure to microbes early in life is important for the development of social behavior, said Judith Eisen, a neuroscientist and one of the paper’s authors.

The researchers also looked at the fish’s brains using powerful microscopes. Typically, cells called microglia move from the gut to the brain early in a fish’s life, around the time their microbiome begins to develop, Eisen said. She and her team found that fish that lived without their microbiomes for a week had fewer microglia in a specific area of ​​the brain previously associated with shallow behavior. In normal brains (including human brains), these cells perform synaptic pruning, removing weaker or less used connections.

Of course, such a germ-free state of zebrafish would not exist in nature, said Eisen. However, some human pollutants such as pesticides, microplastics, and metals such as cadmium appear to alter fish microbiota. Looking into shallow water is often a protective behavior, and the diminished response to shallow water can cause problems in the wild. “If she doesn’t want to hang out with other fish — that might open her up to predation,” Eisen said.

Pollutants can affect behavior beyond shallow waters, and saltwater ecosystems as well. In a 2020 study, researchers took ambon damselfish larvae into the lab and exposed some of them to microplastic beads. Then they returned the baby fish to different areas of the Great Barrier Reef—some deteriorated, others still healthy—and observed how they behaved. The team also tagged the fish with small fluorescent markers, and they went back to the reef several times over the course of three days to check their survival rate.

Fish exposed to microplastics showed more risky behavior and lived less time before being eaten, according to the study. Almost all tagged fish exposed to microplastics and released near dead corals died after approximately 50 hours. Meanwhile, about 70 percent of uncovered fish released near live corals survived after 72 hours. According to the paper, while the health of the corals was a factor in the risky behavior, the survival rate of fish exposed to plastic was six times lower than those not exposed to the compounds.

According to Alexandra Goulizia, one of the paper’s authors, who has a Ph.D. student at James Cook University, more work is needed to look at the ingredients in plastics and how they affect fish. For example, bisphenol A, better known as BPA, is a common additive to make plastics more flexible. It is also seen in natural habitats and research indicates that it can reduce aggressiveness in fish. “I think we’re only touching the surface of the chemical effects that microplastics have on the behavior of fish and fish,” Giulizia added.

It is difficult to assess how all this would happen in the wild. Eisen noted that other factors that can influence the microbiome include nutrients in the water, water temperature, diet, and salt concentration. Another complication is perhaps more direct: Pollutants can appear simultaneously and in different amounts, Petijian said. For example, one 2016 paper showed that 13 percent of the 426 pollutants in European rivers were found to be neuroactive.

Another complication is that organisms simply won’t function the same way – even within the same species. According to Eisen, model organisms, such as zebrafish, are chosen to represent a wide range of species, just as mice are often used to study human health in medical research. But changes in pollutants and other factors can vary from species to species. Bertram noted that using model organisms saves researchers the trouble of studying each species separately, but that more studies should also be done on different fish.

On the face of it, some behavioral changes may not seem so bad. Increased mating behavior – as in the case of guppies exposed to fluoxetine – may seem like a boon to the species. However, one species that thrives on another tends to throw off its natural habitat, Bertram said. His previous work indicates that Prozac similarly increases the mating behavior of the invasive eastern mosquito. This can help it thrive and outpace native species. Additionally, at some concentrations, cadmium can increase fish activity, which may help them find food. However, Petijian said the more they ate, the more they were exposed to microplastics.

Under these conditions, he added, in-lab experiments need to inject as much complexity into their methods as possible to better replicate real wild systems. Some research is trying that. Bertram’s work showed the tested guppies to be either predatory or similarly sized and non-predatory fish prior to her experiments, while Julizia and her team conducted parts of their experiment in the wild. Some studies also expose fish species to water taken from the environment — and the pollutants that come with it.

Despite the unknowns, Bertram said changes to how fish socialize, mate or find food are unlikely to be good. He continued, “At the end of the day, any change in the expression of normal behaviors will have unintended negative consequences.”

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