In the movie “Arrival,” one of the latest films to depict extraterrestrial creatures visiting Earth, a team of scientists takes along a canary in a cage when visiting an alien spaceship. The purpose of the canary is never disclosed, but one assumes it serves as a sentinel—as the bird once did in coal mines—to alert the team if environmental conditions in the spaceship turn unfavorable.
Canaries are the most familiar example of a sentinel species, which are animals and plants that serve as harbingers of danger to human health and the environment. In the case of canaries, if odorless carbon monoxide were present in a high enough concentration in a coal mine, the small bird would die first and give miners time to escape.
Cats, too, have been sentinels. In the 1950s, people in the town of Minamata, Japan, began to notice that local cats were acting strangely: The cats were unable to walk straight and uncontrollably jumped about. After some time, people began to act similarly. The cause of “dancing cat fever” was quickly connected to the release of methylmercury in the wastewater of a local chemical factory. The discharge fed into the city’s harbor, where it bioaccumulated in fish and shellfish. Although several thousand people were affected with what became known as Minamata disease, the outcome could have been worse were it not for the warning from the dancing cats.
Scientists have identified dozens of animals and plants that can function as environmental sentinels. Among them, iconic informants of environmental conditions include species such as polar bears, bald eagles, and dolphins. But these creatures, what scientists in the trade call “charismatic megafauna” because environmental advocates often use them to champion their missions, are difficult to sample for comprehensive monitoring studies.
For a plant or animal to be considered a good sentinel species, it must be relatively common, be easily handled, and have consistent and regularly measurable responses to environmental changes. Species that meet those qualifications on land include lichen growing on rocks and trees and herd animals such as caribou. In freshwater, there’s the tiny crustacean Daphnia and prized game fish such as lake trout. In coastal areas, mussels are a leading sentinel species, whereas in the open ocean it’s birds such as herring gulls and marine mammals like seals.
“A simple reason why birds are sentinels can be told from the DDT story,” says Kurunthachalam Kannan, who uses sentinel data to track organic pollutants for the New York State Department of Health. “Populations of bald eagles and many species of birds declined when the insecticide was heavily used, and the populations are recovering after the 1972 U.S. ban on DDT,” Kannan points out. There’s a similar story to tell about a whole lot of other sentinel species, he says. “Understanding environmental sources, pathways, distribution, dynamics, and fate of chemical pollutants is crucial if we are to devise solutions to current and future environmental problems.”
Besides DDT, researchers have been using sentinels to study other persistent organic pollutants such as polychlorinated biphenyls (PCBs), polycyclic aromatic hydrocarbons (PAHs), brominated flame retardants, and fluoroalkylated substances. They are also checking for toxic metals such as lead, cadmium, and mercury. In addition to tracking contaminant trends, these studies look at natural and human-induced cyclical changes in nitrogen and phosphorus nutrients, as well as dietary shifts that could be the result of climate change or invasive species.
Sentinel species aren’t a replacement for other types of sampling or lab research. For example, researchers have been on a decades-long campaign to chemically and spectroscopically evaluate pollutants in air and water samples, as well as in soil, sediment, and ice cores. Those tests help diagnose which pollutants are present, how much is present, where they come from, and how widespread they are. They also reveal how fast the concentrations of banned substances are decreasing, and for some of the most persistent ones, if they will ever go away. Sentinel species provide the same types of results, but they go further by providing physical evidence of how pollutants are damaging ecological systems.
New technologies are changing the way scientists go about monitoring sentinel species. For example, researchers are now using microsensors fitted to the backs of honeybees as a kind of Fitbit to analyze their ability to pollinate. And others are using drones to snatch snot samples from the blowholes of whales at sea to evaluate their well-being.
The next big thing in sentinel science is the field of evolutionary and ecological functional genomics, says Joseph R. Shaw of Indiana University, who studies Daphnia. In biomedical research, scientists have long relied on fruit flies and the nematode Caenorhabditis elegans in their research because the model animals’ genetic features are well-known, Shaw notes. With the rapid rise in genomic technologies, ecologists, evolutionary biologists, toxicologists, and environmental chemists are now able to expand their research. For example, they can study how symbiotic relationships that bacteria, viruses, and fungi have with plants and animals, including people, contribute to biodiversity and, in turn, how human activities impact those relationships.
“This push is driven by the need to understand how genomes respond to the environment,” Shaw says. “Even with the best annotated genomes, we don’t know the functions of up to one-third of the genes because they have never been expressed in the lab. It’s a call to arms for more researchers to enter the genome era to develop tools for ecological models and at the same time to better study the ecology of traditional models in order to figure out the environmental conditions that control these unknown genes.”
Indeed, scientists think new approaches to monitoring the environment with sentinel species will have a lot to offer. As a primer, on the pages that follow, C&EN provides snapshots of a few key sentinel species and the roles they are playing.
Daphnia are tiny crustaceans about the size of the equal sign on a computer keyboard. They live in ponds and lakes, where their color, size, and abundance serve as a sentinel of good water quality and environmental health. Naturalists began studying the creatures, commonly known as water fleas, in the 1600s. They found early on that Daphnia are a keystone species, providing a link between the algae, bacteria, and protozoans that they eat and the fish that prey on them for food. In the early 1900s, during a period of rapid growth in human use of pharmaceuticals, pesticides, petroleum products, and munitions, Daphnia became important tools for toxicological screening—studies of the chemical limits tolerated by Daphnia helped policy-makers develop food and drug safety laws.
Among Daphnia’s more fascinating features is that they generate two types of eggs, one of which can remain dormant for centuries in sediments. Scientists have learned how to hatch the dormant eggs and use the resurrected Daphnia to study the effects of synthetic chemicals that didn’t exist when the eggs were produced.
Daphnia have more genes (~31,000) than humans do (~20,000).
With the aid of the latest genomic technologies, researchers are now using DNA and RNA sequencing to track how gene expression in Daphnia changes over time. This ability allows scientists to compare how different generations of Daphnia adapt to natural and human-induced shifts in nitrogen and phosphorus nutrient levels, the influx of synthetic chemicals in the environment, and climate change. The results are helping researchers extrapolate the toxicity of existing chemicals and new chemical substances to other animal and plant species, all the way up to humans.
Sources: Lawrence J. Weider, University of Oklahoma; Joseph R. Shaw, Indiana University.
—Lawrence J. Weider, University of Oklahoma
When Daphnia from a Minnesota lake were screened against exposure to the pesticide chlorpyrifos, which was introduced commercially in 1965, researchers found that samples of the crustaceans originating from preindustrial times (1301–1646) were 2.7 times as sensitive (judged by their mobility level) to chlorpyrifos as samples originating just after the chemical began to be used (1967–1977). These results indicate that the creatures evolved some tolerance to chlorpyrifos exposure. Daphnia originating more recently (2007–2011), when chlorpyrifos was no longer detected in the lake, seem to be losing that tolerance (Ecotoxicology 2014, DOI: 10.1007/s10646-014-1397-1).
When it comes to monitoring some of the most problematic synthetic chemicals dispersed in the environment, scientists have given the expression “for the birds” a whole new—and more significant—meaning. Herring gulls (Larus argentatus), for example, have a long history of serving as a sentinel species, providing data on pollutants in the Great Lakes region of the U.S. and Canada since the 1970s. Although researchers do collect birds as samples, their primary sampling target is bird eggs.
Scientists also turn to Arctic-breeding seabirds such as thick-billed murres (Uria lomvia), northern fulmars (Fulmarus glacialis), black-legged kittiwakes (Rissa tridactyla), glaucous gulls (Larus hyperboreus), and black guillemots (Cepphus grylle). And they’ve carried out long-term investigations of sea eagles in the Baltic Sea. The choice of species to sample often depends on accessibility to remote colonies and the ability to compare data among species around the globe. In addition to tracking contaminant trends, other work has looked at dietary shifts in the birds that could be the result of climate change or invasive species.
Seabirds commonly drink seawater, removing the salt with special glands above their eyes and excreting the salt through ducts on their bills.
The number one finding from bird studies is that concentrations of most monitored contaminants, such as DDT, polychlorinated biphenyls (PCBs), and dioxins, have declined as a result of bans and other regulations implemented in the 1970s and 1980s. Among newer pollutants, brominated flame retardant concentrations increased exponentially from 1975 to 2003, then rapidly declined as industry began to replace them. Levels of long-chain fluorinated alkyl compounds increased between 1975 and 2009, then began to decline after an agreement by chemical companies in 2008 to phase them out. Mercury levels increased in seabird eggs from 1975 to 1993 and have mostly plateaued since then.
Sources: Birgit M. Braune, Shane R. de Solla, Robert J. Letcher, and Derek C. G. Muir, Environment & Climate Change Canada
—Derek C. G. Muir, Environment & Climate Change Canada
The total concentration of perfluorinated carboxylates, F3C(CF2)nCOOH (n = 5–14), as measured in bird eggs in the Canadian Arctic is starting to decline (Organohalogen Compd. 2014, 76, 138–141).
In the late 1960s, U.S. scientists discovered that chlorinated pesticides, mercury, and petroleum-derived hydrocarbons were becoming a serious threat to coastal oceans and estuaries. Researchers attempted to study the severity of the pollution problem by using different animal species in different locations: fish in the Chesapeake Bay, lobsters in New England, crabs in Florida, and different crab species in California and Alaska. But the varying habitats, lifestyles, food webs, and metabolic activities of the disparate species rendered the comparative results questionable.
Prompted by a concerned public, federal agencies then called for comprehensive global monitoring aimed at measuring nearly all potentially problematic chemicals in almost all sectors of the environment. But those efforts were considered too costly and a logistical nightmare. To avoid inaction, in 1975, marine geochemist Edward D. Goldberg of Scripps Institution of Oceanography proposed something simple: a “mussel watch” program as a first step to monitor persistent organic pollutants and heavy metals in coastal waters.
Mussels attach to rocks by a bundle of sticky filaments known as a byssus and can filter 50 L of seawater per day.
Mussels, both marine and freshwater species, along with oysters and clams, are ideal for pollution monitoring because they are common and easy to collect. Plus, marine mussels are now grown commercially in estuaries, offering controlled sites for monitoring, and they are easily transplanted to remote test sites.
Mytilus and Perna marine mussels harvested for food feed mainly on phytoplankton by siphoning and filtering large volumes of seawater across their mucus-coated ciliated gills. Like most animals, they didn’t evolve the enzymatic capacity needed to readily metabolize organic pollutants such as polychlorinated biphenyls (PCBs) and hydrocarbons, so they tend to concentrate pollutants from the surrounding seawater, making detection easier. Mussel watch programs are now used globally to identify the sources and distribution of chemical pollutants and assess human health risks.
Sources: John W. Farrington, Woods Hole Oceanographic Institution; Dennis Apeti, National Oceanic & Atmospheric Administration
—John W. Farrington, Woods Hole Oceanographic Institution
NOAA’s mussel watch program has tracked concentrations of pollutants such as DDT along U.S. coastlines for decades. On the West Coast (shown) values have dropped steadily, whereas on the East Coast the concentrations are about twice as much and have remained flat in recent years.
Lake trout (Salvelinus namaycush) are the largest member of the char family and occupy the top of the food web in deep, cold lakes across the upper reaches of North America. Prized by anglers, lake trout often live up to 20 years, reaching more than 60 cm in length and 10 kg in weight with high body-fat content. All these characteristics make lake trout perfect for biomonitoring because they accumulate pollutants in their bodies at levels indicative of their environmental exposure.
In the Great Lakes, the world’s largest freshwater system, lake trout have been under surveillance for more than 40 years by the U.S. Environmental Protection Agency and Environment & Climate Change Canada. At the onset of monitoring in the 1970s, the focus was on the “dirty dozen” persistent organic pollutants listed by the 2001 Stockholm Convention. These recognizable compounds, now banned from production and use, include the pesticides DDT and lindane as well as industrial chemicals such as polychlorinated biphenyls (PCBs). Although the levels of most of these chemicals of concern as measured in lake trout have decreased significantly, demonstrating the desired effects of global restrictions, some are still present at easily detectable and potentially detrimental concentrations.
Trout can be aged from their ear bones, called otoliths, which have growth rings like trees do.
In the past 15 years, monitoring has evolved to include newer classes of chemicals like polybrominated diphenyl ether flame retardants and fluorinated alkyl substances used for their stain-resistant, water-repellent, and nonstick properties. The lake trout data and data from other fish species sampled globally help facilitate risk assessments of chemicals in the environment and measure the effectiveness of risk-management regulatory actions.
Sources: Thomas M. Holsen and Chuanlong Zhou, Clarkson University; Daryl McGoldrick, Environment & Climate Change Canada
—Thomas M. Holsen, Clarkson University and EPA’s Great Lakes Fish Monitoring & Surveillance Program
Canadian-U.S. monitoring of lake trout in the Great Lakes since the 1970s has tracked changes in the concentrations of legacy pollutants and emerging pollutants of concern. These graphs provide a snapshot of the recent trends for two of them (Environ. Sci. Technol. 2017, DOI: 10.1021/acs.est.7b00982).
Lichens are composite organisms assembled from fungi fused with algae or cyanobacteria and come in many colors and sizes. They look like plants, with some having leaflike structures or leafless branches and others forming flakes that look like peeling paint. Yet they don’t have roots, instead growing on trees, rocks, and concrete and absorbing nutrients from fog, wind, and rain. Because lichens have no specialized protective barriers, they also readily absorb contaminants and are among the first organisms to die when pollution increases, making them good sentinels for air quality.
Lichens have been used to identify pollution hot spots since the 1860s, when botanists in Paris discovered that lichens thrive in areas where the air is clean and suffer in areas where it’s dirty. Early investigations focused on the direct effects of sulfur dioxide stemming from burning coal. Over time, scientists discovered that lichens are also good indicators of the regional effects of acid rain caused by longer range transport of sulfur dioxide and other industrial emissions. Lichens are also sensitive to ammonia and nitrates that drift from agricultural areas where fertilizer is used, and they accumulate metals such as mercury from power plant emissions and lead and zinc from mining ore smelters.
Hummingbirds use lichens to camouflage their nests.
In the 1980s, the U.S. Forest Service started a lichen biomonitoring program in which scientists record census data on the diversity and abundance of lichens in thousands of designated survey plots across the country. They collect some samples and send them off to a lab for elemental analysis to identify the type and amount of pollutants. The data help federal agencies set pollution targets and map out areas where the targets are not being met, and they also help state and federal agencies that review emissions permit applications and existing regulations.
Sources: Linda H. Geiser and Sarah Jovan, U.S. Forest Service; Peter R. Nelson, U.S. Forest Service/University of Maine, Fort Kent
—Linda H. Geiser, U.S. Forest Service air-quality programs
U.S. Forest Service lichen surveys enable scientists to map out relative air quality in various regions, as seen here in the Pacific Northwest; green is the best, darker red the worst (Environ. Pollut. 2007, DOI: 10.1016/j.envpol.2006.03.024).
Caribou (Rangifer tarandus), and its subspecies reindeer, are favored as sentinels for their large size and for the migrations of their herds that cover well-trodden annual routes near the top of the world. The animals feed on grasses in summer but eat mostly lichens during the long winters. Because lichens, another key sentinel, absorb a variety of contaminants from the atmosphere, caribou accumulate the pollutants too. And people who live in the far north eat caribou—researchers often rely on Arctic indigenous peoples to provide test samples from annual hunts.
As sentinels, caribou have a niche role in providing some of the longest data sets for radioactive contaminants, such as 137Cs, from the fallout of nuclear weapons testing. Monitoring radioisotopes in caribou took on additional significance after the Chernobyl nuclear reactor accident in Ukraine in 1986 and the Fukushima reactor accident in Japan in 2011.
A caribou’s wide, concave-shaped hooves are adapted for deep snow, functioning like snowshoes.
Besides caribou, polar bears, seals, dolphins, and whales are important mammal sentinels. Polar bears are better Arctic sentinels than caribou because they are at the top of the marine food chain and accumulate persistent pollutants that don’t show up in terrestrial ecosystems. But researchers have few opportunities to conduct long-term studies with bears because they are widely dispersed in winter. Seals, on the other hand, are useful for tracking such pollutants as flame retardants and mercury in large estuaries like San Francisco Bay, where they are year-round residents.
Sources: Mary Gamberg, Canada’s Northern Contaminants Program; Margaret D. Sedlak, San Francisco Estuary Institute; Derek C. G. Muir, Environment & Climate Change Canada
—Mary Gamberg, Canada’s Northern Contaminants Program
By examining caribou, researchers can study how pollutant concentrations vary over time and how they might affect animal health and herd survival, in particular as climate change alters the caribou habitat. In one case, scientists studying caribou livers in Greenland noticed that caribou with higher mercury levels appear less likely to become pregnant (Sci. Total Environ. 2016, DOI: 10.1016/j.scitotenv.2016.02.154).
Honeybees (Apis mellifera) are one of nature’s often underappreciated heroes. While they busily go about their business of foraging, collecting pollen, and producing honey, they also serve as unwitting pollinators to help humans produce much of the food we eat. Because bees are often managed by beekeepers and moved around, they would normally make poor sentinel species. But they still qualify as valuable sentinels by virtue of contaminants that show up in the honey they produce.
Honeybees and other pollinators such as bumblebees and monarch butterflies are under threats from dangers that include loss of habitat and the use of agricultural insecticides. In particular, neonicotinoids used to kill crop-damaging insects have unintended effects on bee neurological function and are one of the prime suspects for causing recent declines in bee populations. Exposure to neonicotinoids affects honeybee olfactory learning, memory, and navigation, which together impair their foraging efficiency and could lead to problems for people by affecting food availability, quality, and cost.
Honeybees are the only insects that produce food for humans.
Although emerging studies on the effects of neonicotinoids in vertebrates show some impaired immune functioning, it’s not clear whether the problems bees and other insects have with neonicotinoids are also human health problems. To help monitor bee health scientists have started using microsensing devices fitted to their backs (shown), which identify individual bees and record their movements around hives to analyze their ability to pollinate.
Sources: Christopher N. Connolly, University of Dundee; Edward A. D. Mitchell and Alexandre Aebi, University of Neuchâtel; Paulo de Souza, Commonwealth Scientific & Industrial Research Organisation
—Christopher N. Connolly, University of Dundee
A recent study of nearly 200 honey samples from around the world found traces of at least one of the five main neonicotinoids in 75% of the samples and two or more neonicotinoids in 45% of the samples. The measured concentrations fell below the residue levels typically permitted for human consumption in the European Union, but about one-third of the samples had high enough concentrations to harm bees (Science 2017, DOI: 10.1126/science.aan3684).