A growing body of research shows how air pollution, fertilizers, and fungicides are altering the chemical signals that plants and animals use to communicate. Scientists warn that insect reproduction, foraging, navigation, and even the pollination of crops could be affected.
Across the globe, human activities are changing the way our planet smells. In Egypt, increasing temperatures are shrinking yields of aromatic jasmine flowers; in France, extreme drought has reduced the production of fragrant, night-blooming tuberose, a major ingredient in many perfumes; in Italy, climactic extremes are altering the characteristic floral, citrusy scent of bergamot.
But anthropogenic factors are also reshaping environmental smellscapes, a word coined in the 1980s to describe the totality of scents in a given geographic area, in ways that are far more subtle — and potentially much more harmful.
While humans largely rely on sight and sound in our interactions with each other and with the world around us, many other creatures rely on smells. Ants, for example, require scents for colony cohesion; turkey vultures let scent guide them to far-away carrion; and male moths use scent to find females hundreds of meters away. “Scent is very important because it mediates so many interactions within an ecosystem,” says James Blande, a chemical ecologist at the University of Eastern Finland.
These scent-based interactions are crucial for the maintenance of ecosystem services that directly benefit humans, from the bees and moths that pollinate crops to the flies and dung beetles that recycle the nutrients from dead and decomposing matter. Intact channels of scent communication are likely also important for the preservation of biodiversity. For example, many rare orchid species use scent to attract the co-evolved pollinators they need in order to reproduce, and scent helps guide monarch butterflies to the single type of plant on which they lay their eggs.
A growing number of scientists are documenting how humans are changing the chemical signals of plants and animals.
But just as we are discovering how important these chemical communication channels are to the fabric of the natural world — and the many benefits we reap from it — we are also learning how drastically they can be disrupted by our activities, including climate change and air pollution.
Now, scientists are working to document human-induced changes in smellscapes across the planet — to understand how these changes affect communication between different organisms, and to try to figure out which systems are capable of adaptation and which may be at risk of failure.
Historically, researchers in the field of sensory pollution have been largely focused on noise and light, says Jeff Riffell, a sensory biologist at the University of Washington. Odor pollution, on the other hand, “is really hard to get a handle on because you need these big chemical analysis devices that [cost] hundreds of thousands of dollars in order to characterize it.” Plus, he says, “we’re just not very olfactory.”
Despite these challenges, a growing number of scientists are documenting how humans are changing the chemical signals of plants and animals. For example, researchers have discovered that air pollution degrades many of the volatile organic compounds (VOCs) that make up lavender’s characteristic scent, and increasing temperatures dramatically decrease the floral perfumes released by strawberry plants and wild white petunias. Agricultural chemicals, like fertilizers and fungicides, add additional VOCs to the air in fields and orchards around the world.
A bee pollinates lavender in Eynsford, England. Researchers have found air pollution degrades the compounds that give lavender its characteristic scent.Dan Kitwood / Getty Images
But figuring out how these changes affect communication between organisms — and whether this impairs their ability to pollinate, procreate, or otherwise survive — can be a tricky task, as objective differences in the chemical makeup of a scent don’t always predict differences in how they are perceived.
To get inside the mind of a pollinator and parse how much a smell has to change before it becomes unrecognizable, researchers often use a simple test called the proboscis extension response — a sort of Pavlov’s dog for bees. While Pavlov taught dogs to associate food with the sound of a bell, triggering them to drool, researchers teach bees to associate particular scents with the taste of sugar. Once they learn the association, the bees stick out their proboscis — the insect equivalent of a tongue.
Using this paradigm, Stony Brook University pollination biologist Jordanna Sprayberry and her colleagues taught bumblebees to recognize a particular floral odor, then tested how three different fungicides affected the bees’ ability to recognize this odor. “We found negative effects of every fungicide we tested,” she says. One fungicide was disruptive at every concentration tested. This could be especially problematic for fruit and vegetable production, since these crops generally require insect pollination and are often heavily treated with fungicides.
In heavily polluted regions, the distance from which a moth can sense a flower is a quarter of what it was in preindustrial times.
A team of researchers in the United Kingdom has also used this type of test to investigate the impact of oxidizing air pollutants — like ozone and nitrate radicals (NO3) — on honeybees’ ability to recognize scents. These pollutants are naturally present in the air at low levels but are dramatically increased by emissions from cars, power plants, and oil and gas production. Instead of just adding new odor molecules on top of an existing scent, oxidizing pollutants react with different components of floral perfumes, degrading their scents.
After researchers taught honeybees to recognize a floral odor blend, they released that scent into a wind tunnel of ozone-polluted air. At six meters from the source, only about 30 percent of bees could still recognize the scent. This kind of pollution could seriously impair honeybees’ ability to find flowers, which is concerning because honeybees are estimated to be responsible for about half of crop pollination worldwide.
While daytime pollinators get the most attention, nocturnal pollinators are also important for crops and wild plant species. To find out if night-time pollination was similarly affected by pollutants, Riffell turned his attention to a fragrant, night-blooming wildflower called the pale evening primrose and its hawkmoth pollinators.
A farmer in Dürmentingen-Heudorf, Germany, sprays fungicide on his potato field. Fungicides may be making it harder for bees to recognize floral odors.Thomas Warnack / picture alliance via Getty Images
He and his team measured how compounds in the primrose scent changed when exposed to NO3, which increases at night. While some types of odor compounds were relatively resistant to these pollutants, others, like β-Pinene, a woodsy-green scent, and β-Ocimene, which is more floral and herbaceous, began to degrade within seconds.
Next, researchers set up scent traps at their field site in eastern Washington. Over the course of the night, they recorded how often pollinators visited a real flower, a paper cone releasing a simulated floral scent, and a cone releasing floral scent degraded by NO3 exposure. Pollinators stopped by the real flower and the floral-scented cone at similar rates, but the degraded scent received about 70 percent fewer visits. That’s bad news for both players: As natural scents degrade, pollinators may have less access to food while plants may have a lower chance of reproducing.
Using a model of atmospheric conditions that included pollution levels and weather conditions and combining it with data on how quickly oxidizing pollutants can degrade key floral odors, Riffell and his colleagues mapped distances at which a moth would be able to detect a primrose in different locations on Earth. In more heavily polluted regions of the world, the team found, the distance from which a moth can sense a flower has fallen to just a quarter of what it was during preindustrial times. Similar modeling strategies could be used to identify croplands and valuable ecosystems at greatest risk for communication breakdown and the loss of crucial pollination services.
Studies reveal that ozone pollution breaks down pheromones, with serious consequences for insects looking to mate.
Much of the work on the ecology of shifting smells has focused on pollination — and with good reason. “When you go to the grocery store in, say, Canada or the United States, almost 70 percent of the food is actually a result of pollination,” says Riffell. The vast majority of wild flowering plants also depend on pollination by insects and other animals.
But plant-pollinator interaction is just a tiny part of how scents structure our world. How human activities affect other types of chemical messages is largely unexplored, but the few existing studies suggest concerning disruptions. Markus Knaden, a researcher at the Max Planck Institute for Chemical Ecology, is exploring how ozone alters chemical communication between insects. “The problem is that [scent] molecules are very sensitive to oxidants,” he says. “Which was not a problem for the last millions of years but is becoming an increasing problem due to us.”
Knaden’s studies revealed that ozone pollution breaks down pheromones, with serious consequences for insects looking to mate. For example, ozone-altered pheromones made male flies less appealing to females of their species and increased male-male courtship behaviors. The mating process leaves insects vulnerable to predation, Knaden says, so if a male wastes time courting other males, he might get eaten before he can reproduce.
Pheromone breakdown can mess with mating in other ways, too: When Knaden’s team exposed flies to ozone-enriched air, females were much more likely to mate with males of a different species, producing hybrid offspring that were often infertile.
A tobacco hawkmoth visits a paper cone emitting the scent of pale evening primrose as part of an experiment into how pollution degrades floral odors.Charles Hedgcock / University of Washington
Insect populations are already in decline globally, a phenomenon known to be driven by habitat loss and the widespread use of pesticides, but Knaden says it’s possible that oxidizing pollutants could accelerate this decline. “If you take down the population by 30 percent or 50 percent, it is already harder for [insects] to locate each other,” he says. “But if you then take down their communications channel by oxidizing their pheromones, that might be an additional effect.”
What does a future of altered smellscapes look like for organisms that rely on scent to communicate?
“Depending on the relationship, some of the plants and animals can handle these changes,” says Shannon Olsson, who runs the Naturalist-Inspired Chemical Ecology lab at the Tata Institute of Fundamental Research, in India. “We have seen robustness in the system, but we’ve also seen failures in the system.”
Some insects are quick learners: Bumblebees and honeybees can learn attraction to new scents after just a handful of training runs. And while pollinating hoverflies seem to be innately attracted to certain floral scents and colors, Olsson’s research shows that they can also learn to avoid them, demonstrating that some insects are highly adaptable to changes in the environment.
Pollution can change the scent of a Mediterranean fig enough that it is no longer attractive to its only pollinator, the fig wasp.
But some insects may not live long enough for meaningful learning to occur. Researchers found that ozone pollution can change the scent of a Mediterranean fig enough that it is no longer attractive to its only pollinator, the fig wasp. In the wild, the wasp lives only about two days — likely not enough time to learn an odor that’s different from the tree that it evolved with over millions of years.
Learning may not help buffer insects against pollution-altered sexual signals, either. “People that work on insect mating and on insect pheromones,” Knudsen says, “usually think that this is a really hard-wired system.”
The good news, says Riffell, is that air quality regulations implemented in recent decades have had a substantial impact on reducing oxidizing air pollutants. In the U.S., levels of ozone and nitrogen oxides — which are also harmful to human health — have been falling slowly but steadily since 1980. Even so, many places in the U.S. and Europe still regularly experience unhealthy levels of these pollutants, and ozone exposure is estimated to be increasing globally.
“I am hopeful that things are getting better,” says Riffell. “But I am very mindful that things can change really dramatically and very quickly. We’ve all experienced this — especially in the U.S., in the last year or two.” To prevent these anthropogenic pollutants from further affecting animal communication systems, he adds, “we need enhanced regulations.”
For agricultural chemicals, like fungicides, Sprayberry says more research is needed to determine when and how much to use them to minimize the loss of crops to disease while also producing the smallest amount of bee-disturbing olfactory pollution. Ultimately, says Olsson, “We have to learn how to coexist in a way that’s minimally destructive to our plants and animals.”



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