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We know terrifyingly little about how our bodies respond to pollutants, but that's changing

Fish DNA can change in response to pollution. What about the rest of us?

Anna Robuck

Marine Science

University of Rhode Island

Bad news: unless you live in a bubble, you are full of contaminants. Somewhat more reassuring news: every other living creature on Earth seems to share this condition with you.

Both terrifying and unifying, widespread contamination in humans and wildlife arises due to the slow and constant accumulation of chemicals in living creatures from their surrounding environment and diet, in a pathway known as bioaccumulation. Virtually everything you or any other living creature do contributes to this buildup: consumer products, food, textiles, building materials, household dust, drinking water, surface water, deep water, soil, and even air have all been found to contain multitudes of human-created chemicals. A recent study has even found microplastic fibers in municipal drinking water supplies across the country and globe.

Despite our chemical-laden lifestyles, we have almost no comprehensive idea how the accumulation of these compounds impacts living creatures, particularly wildlife, beyond acute effects. Yes, some chemicals have been shown to cause cancer or seriously mess up hormone production in humans or wildlife. But most chemicals in the environment primarily act by changing or weakening organisms' overall health in ways that don’t outright kill them.

This poor understanding stems from the fact that it is difficult to pin down definitive or causal relationships between pollution and its consequences when so many other factors could be at play in complex living systems. When a human gets cancer or a bird is having trouble laying eggs, it is nearly impossible to parse out how contaminants contributed in conjunction with variables like age, genetic inclination, nutritional state, and other environmental stressors.

Yet the challenging nature of the problem hasn’t dissuaded researchers from broaching it, and we are slowly starting to better understand how contaminants impact living beings. One recent study in particular helps highlight just how far we’ve come in understanding the sub-lethal metabolic effects contaminants have on wildlife.

Adapting to pollution, but at what cost?

The international team, led by Nishad Jayasundara of the University of Maine at Orono, focused on the mummichog, a common and well-studied fish that primarily lives in estuaries, marshes, and coastal environments. Mummichogs have long demonstrated a unique ability to adapt to polluted environments, with various lab and field research documenting genetic and physical adaptions to a variety of contaminants like heavy metals, pesticides, and other organic chemicals.

Apparently, this is a mummichog.

Brain Graitwicke

The team built upon this prior research by taking advantage of a natural experiment ongoing in the Elizabeth River along the coast of Virginia. Mummichog populations in the Elizabeth inhabit differently contaminated sub-environments within the larger river system. The team collected live fish from sites known to contain high, medium, and low levels of polyaromatic hydrocarbons (PAHs), a toxic and carcinogenic pollutant. The fish were then allowed to acclimate to environmental conditions in captivity before undergoing comprehensive evaluation.

After the acclimation period, the researchers first focused on genetics, and used previously existing work to identify genes that are different in contaminated and uncontaminated fish. They specifically looked at genes related to metabolism. From there, it was time for fish “Olympics.” The researchers made the fish swim until tired while measuring their oxygen consumption, metabolic rate, swimming ability, and tolerance to increased temperatures. The results of these measurements were fed into a statistical model to extrapolate how differential fish physical fitness impacts how the fish moves and responds within its environment.

So, this is a fish treadmill.

Using this multi-tiered strategy, the researchers described how pollution had cumulative effects at the levels of DNA, animal, and ecosystem. They found something surprising. Mummichogs deal with PAH exposure by changing their gene makeup.

Let that sink in a minute: fish DNA actually changes to cope with polluted environments. This alters metabolism and energy allocation, thereby compromising the fish’s ability to deal with other stressors in their environment. In this study, fish from polluted environments were less able to cope with increased temperatures; this has huge implications in a warming world where climate change is at work to increase water temperatures around the globe.

This is also troubling because mummichogs are considered extremely habitat-flexible, dealing with wide ranges in temperature and salinity. If any creature should be able to cope with thermal stress, it's these guys. Additionally, the modeling work suggested the compounded effects of altered genes, metabolism, and coping ability translates to fish being less capable of finding and traveling to an optimum environment, meaning contaminant exposure has the potential to alter the very way fish interact with the surrounding environment.

How does pollution effect the rest of us?

But what about all the wildlife that’s bigger than the size of a finger? How do contaminants sublethally impact cats, pigs, sharks, weasels, deer, or seabirds? Unfortunately, when larger creatures are factored into the conversation, we are reminded that we understand close to zilch when it comes to sublethal impacts of contaminants in wildlife.

A recent study focusing on Arctic seabirds embodies such existing gaps and highlights how tough it is to figure out how contaminants are undermining wildlife processes and function. Few studies have tackled contaminant impacts on metabolism in birds, thanks to how hard it is to compare features of very different species, as well as the fact that studying live creatures in the wild is much harder than analyzing samples. Those that have forged ahead looking at bird hormone production and metabolism have seen conflicting results.

So there is scant consensus regarding how birds metabolically respond to contaminant burdens. An international team led by biologist Pierre Blévin, of the Centre d'Etudes Biologiques de Chizé in France, recognized this uncertainty and implemented a study in an effort to better understand how contaminants are related to energy use in live birds. The team captured black-legged kittiwakes, a type of Arctic seabird, during their chick rearing season on Svalbard in Norway and took blood samples from captured birds for contaminant and hormone analysis. The birds were then rushed back to the lab via boat to take respirometry measurements. Respirometry essentially measures carbon dioxide respiration and oxygen consumption over time, allowing calculation of metabolic rate.

Hey look, it's a black-legged kittiwacke

Mikesegeln

Unfortunately, no clear picture emerged. The researchers found that different groups of contaminants were associated with variable metabolic rate and hormone levels. Increased concentrations of banned chlorine-based compounds, like pesticides or PCBs, were associated with decreased metabolic rate and hormone levels, while currently used perfluorinated chemicals, used as water repellants, were associated with an increased metabolic rate only in females.

These inconsistent results provide more questions than answers in terms of parsing out the greater impact of contaminants on birds. If organochlorine and perfluorinated compounds have opposite effects on metabolism, does this mean they cancel each other out? What is the net effect on bird energy use and what does this mean for bird migration? These birds migrate thousands of miles; do contaminant metabolic artifacts impact these feats?

It's hard to say: wild animals that live longer lives come with a history full on unknown events that may easily confound snapshots of metabolic rate or contaminant signature obtained within a study. In terms of methodology, transporting large wild animals alive for metabolism measurements is extremely time-consuming, expensive, and location-dependent, not to mention a permitting nightmare depending on the study location. This contrasts starkly with research solely measuring contaminant body burdens, which just uses tissue from dead animals. This is exponentially more straightforward, and cheaper, hence the abundance of reports describing contaminant levels in animals with little indication of how found chemicals are impacting the animal or its day to day function.

Still, these sorts of studies should not be avoided, but rather viewed as a challenge. The need to comprehend contaminant impacts in humans and wildlife only continues to grow, as thousands of chemicals are introduced each year to replace banned compounds or for novel applications, adding to the inundating chemical soup surrounding us.

Comment Peer Commentary

We ask other scientists from our Consortium to respond to articles with commentary from their expert perspective.

Kelsey Lucas

Physiology, Marine Biology, and Ecology

University of Michigan

Contamination is a serious problem in all sorts of environments, as captured in the mummichog and bird studies described here. We should also remember that these problems can exist over multiple scales: in time based on the rate of spreading or breakdown of chemicals, in size based on who takes in contaminants how these are passed through a food chain, and in space, like how plastics in the ocean surface are being concentrated and passed to the seafloor. 

The confusing results from the Arctic birds provide a great example of the difficulties in interpreting what exactly contaminants are doing, but answering the questions that emerged will likewise be a challenge. The ethics of giving animals contaminants is dicey at best, making it difficult to tease apart the individual outcomes of multiple contaminants working in tandem. The work presented here is fundamental to our understanding of these processes, and I hope that we'll be able to find acceptable ways to build upon it – and ultimately, find ways to mitigate the damage.

Kevin Pels

Chemical Biology

Dana-Farber Cancer Institute

It would be interesting to know, in a species-specific fashion (not practical, I know), what contaminants have longer in vivo half-lives. I'd guess the polychloro/fluoro compounds, which are relatively inert, stick around in circulation in many species, but the endocrine effects would vary. Birds present a more complicated study as they could sequester contaminants on their feathers/skin and ingest or absorb them. Additionally, they represent a more direct route for contaminants into the human food chain than one might think – gull eggs are considered a delicacy in the UK. If short-sighted people don't care about ecology, maybe their interest is piqued when it circles back to human health.