November 21, 2016 — County public health officials in South Carolina weren’t thinking about bees in August, when they realized that four residents in a single town had returned from travel abroad infected with Zika. Like health officials around the world, they were thinking of the babies born with heartbreaking birth defects in Brazil. And they were thinking about mosquitoes.
After reports emerged in January that thousands of Brazilian infants had been born with microcephaly, a debilitating neurodevelopmental condition marked by severely stunted head and brain growth, the World Health Organization declared an international public health emergency to figure out why. Scientists thought Zika might be a cause, and within months the U.S. Centers for Disease Control and Prevention confirmed that it was.
In the U.S., the primary Zika-transmitting mosquito species, Aedes aegypti, have been known to inhabit areas ranging from California through the Midwest and Southeast and as far north as Connecticut. When travel-related cases showed up in South Carolina, health officials had one thing in mind: prevent those mosquitoes from biting an infected person and passing Zika to someone else. So they quickly launched an aerial spraying campaign against mosquitoes using the insecticide naled.
Naled, it turns out, is highly toxic to bees.
Officials acknowledged the unintended casualties — more than 2.5 million bees, according to local beekeepers — and apologized. They also determined that no rules had been violated in efforts to prevent a mosquito-borne public health threat.
And for this mosquito species, which can carry several deadly viruses, that threat is formidable. Besides Zika, Ae. aegypti can also transmit yellow fever, chikungunya and dengue. There is a vaccine for yellow fever, but not for Zika, chikungunya or dengue, which is a leading cause of death in tropical and subtropical climates. And there’s reason to believe that the range of these mosquitoes and diseases could change, and possibly expand, as the climate warms.
But the death of millions of honeybees — at a time when wild bees, butterflies and other beneficial insects are declining — highlights an increasingly urgent problem: How do you minimize collateral damage in the war against disease-carrying mosquitoes?
Unintended Targets
U.S. public health officials announced the first human trial for a Zika vaccine in August, and expect initial results by early next year. For now, however, mosquito control remains the best defense. County or city agencies usually manage mosquitoes, but they rarely coordinate with environmental agencies. Ecologist Scott Hoffman Black calls that lack of coordination “highly problematic.”
Mosquito-abatement experts typically aren’t trained to understand the impacts of control measures, only how to do them, says Black, executive director of the Xerces Society for Invertebrate Conservation. And the U.S. Environmental Protection Agency, which evaluates pesticide safety, doesn’t monitor the measures after they’ve been approved.
EPA’s role stops at registration, says Black. “If the vector control agencies are using registered pesticides according to the label, EPA has no authority to step in.”
Yet federal officials have recently recognized the need for better coordination. Representatives of health and environmental agencies have been meeting over the past year to identify ways to minimize environmental harm in the age of Zika.
The first priority, says Patricia Bright, senior science advisor for the U.S. Geological Survey, is to determine what’s known about mosquito-control insecticides’ impacts on butterflies and other imperiled species and what happens to the chemicals after they get into the environment. “We’re just at the beginning stages, trying to figure out what we need to focus on,” Bright says.
For years, beekeepers have been the default monitors of the effects of spraying insecticides to protect public health, says Michele Colopy, program director for the Pollinator Stewardship Council. But many beekeepers have stopped reporting their losses to government agencies because nothing happens when they do, she says. “We have a big gap about the impacts of pesticides because beekeepers have given up.”
Scientists are trying to fill that gap. Six years ago, the U.S. Fish and Wildlife Service asked Tham Hoang and his team to figure out whether mosquito insecticides could be driving the decline of native butterflies found only in South Florida. “We found that, yes, the mosquito control compounds can kill the butterfly and the caterpillars,” says Hoang, an ecotoxicologist at the Institute of Environmental Sustainability at Loyola University Chicago.
Hoang and his team also found that several butterfly species are even more sensitive than bees are to naled and other insecticides. That’s partly because butterfly wings have more surface area, Hoang says, but also because the veins in their wings can deliver oxygen as well as chemicals through the body. And caterpillars get a double dose, contending with exposure through the skin and also through their gut when they eat pesticide-laden leaves. Making matters worse, naled breaks down to dichlorvos, which is even more toxic to some butterflies.
South Florida alone has over 30 species of rare or endangered butterflies. To help safeguard them, Hoang says, mosquito control agents should spray less frequently and only at dusk and dawn, when butterflies are less likely to be on the wing and caterpillars aren’t out foraging. “In the long run,” he says, “we need to think about better ways to control mosquitoes than applying chemicals.”
Bryn Phillips came to the same conclusion after studying the effects of mosquito control on aquatic organisms in California.
A few years ago, the California State Water Resources Control Board reviewed its West Nile virus vector control permits, which require testing for the presence but not toxicity of pesticides. The board asked Phillips, an ecotoxicologist at the University of California at Davis, to conduct toxicity tests to see if the requirements should be changed.
Phillips ran tests by exposing water fleas and other tiny crustaceans, workhorses of the ecotoxicology lab, to water samples taken from field sites around California before and after spraying. He also surveyed field sites for signs of toxic effects on these freshwater invertebrates, which provide a critical food source for fish and birds.
When Phillips went out in the field the morning after naled applications, all the insects he’d seen swimming around the day before were gone. “That’s anecdotal evidence,” he says. “But I also have the laboratory evidence, which shows that concentrations of the chemicals we were seeing in the water samples can kill those animals.”
It wasn’t the naled that killed the animals, he says, but its breakdown product, dichlorvos. He also found, in keeping with a previous study, that the insecticides can interact with other chemicals in the environment to enhance toxicity. “I’m convinced that there’s potential for collateral damage in the environment from using these chemicals to kill mosquitoes,” he says.
Phillips advised the water board to include toxicity testing in its permit requirements. The board did not take his advice. If they protected public health at the expense of some very small organisms in the environment, he says, “they considered it worth it.”
Reducing Collateral Damage
It’s not that public health officials don’t worry about unintended mosquito control causalities. “As a public health official, you have to take all that into account,” says Duane Gubler, who headed vector-borne divisions in the CDC for nearly 25 years and now chairs the Global Dengue and Aedes-transmitted Diseases Consortium. But weighing environmental risks against public health is a bigger policy issue, he says. “If you left that decision to public health officials, they would consider the life of a child as more important than killing a bird.”
Even so, he allows that public health officials could do a better job of coordinating with beekeepers, ecologists and others to monitor potential environmental effects. But people in the community should also be doing more, he says, by making sure their backyards aren’t prime mosquito habitat. For mosquitoes that can breed in as little as a teaspoon of water, that means patrolling your yard for even the smallest pool of stagnant water and dumping it out. If you have bird baths, empty the water every few days and scrub out the insides to remove larvae as well as eggs that cling to surfaces with the tenacity of a gecko.
The Zika-carrying mosquito Ae. aegypti is an invasive species, says Steve Lindsay, a medical entomologist at Durham University, “and we humans have created the perfect environment for it to spread.”
This mosquito species evolved in African forests, laying eggs in tree holes and feeding on monkeys. Scientists think it came to the New World aboard slave ships in the 1600s, then started breeding in discarded containers, feeding on humans and spreading yellow fever, dengue and other diseases once confined to monkeys.
For an urban mosquito that breeds in our backyard garbage and rests in our closets, Lindsay says, “broad spraying beyond cities and towns makes no sense.”
There’s also no reliable evidence that it works. In a review of 35 years of studies related to controlling Ae. aegypti to stop dengue transmission, vector-control expert Philip McCall found no conclusive evidence of spraying’s effectiveness because no one had done randomized controlled trials. “This does not mean there is absolutely no indication that fogging can work, but that a correctly designed trial has not been done,” says McCall, a professor of medical entomology at the Liverpool School of Tropical Medicine.
Gubler suspects aerial spraying could actually be counterproductive, since it can make people think government agencies are controlling mosquitoes so they don’t have to. “It creates a false sense of security,” he says.
Instead of sending in the aerial sprayers during a crisis, he says, official need to do more to prevent mosquitoes’ spread. And that means larval control. “Find out where they’re breeding, map them, and have well-trained inspectors who know where to look and how to get rid of them.” That can often be done without insecticides, he says.
In fact, Ae. aegypti had once been eliminated from most of Latin America, including Brazil, using simple targeted tools to kill mosquito larvae. The campaign benefited from a military-style operation during the era of dictatorships. That sort of top-down effort is not likely in the United States, where distrust of government runs high.
Plus, the chemical used to kill larvae, called Paris Green, proved highly toxic to humans, though a more environmentally friendly alternative called Bti is available today. Bti, which is derived from bacteria, is the primary insecticide used to kill mosquitoes in Germany, where naled is not approved for use.
Gubler allows that the hurdles for implementing such a prevention program today are high. For one thing, he says, policy-makers are more apt to spend money to control impending epidemics rather than to support ongoing programs to prevent them. In the absence of a well-funded prevention program, he says, “We need new tools. Badly.”
Among those in development are genetically modified male mosquitoes that mate with wild females and transfer a gene that kills their offspring before they reach adulthood, and the use of Wolbachia bacteria to interfere with reproduction or disease transmission. But GM mosquito trials have been met with public resistance, and the Wolbachia mosquitoes aren’t ready for widespread deployment.
For Gerry Killeen, an expert on malaria control at the Ifakara Health Institute in Tanzania who recently turned his attention to Zika, the most promising tool relies on something called autodissemination of insect growth regulators — a fancy term for using the mosquito to kill its own. It’s been tested in three countries and has shown good results, Killeen says.
“It’s basically a hormone mimic that stops the mosquito from emerging from its pupa,” he explains. The idea is that a mosquito comes in contact with the chemical, carries it to its larval habitat, then lays eggs while also depositing the insecticide that will kill its own, and other mosquitoes’, offspring.
Toxicity tests suggest this approach may have fewer unintended impacts than insecticides like naled. Although aquatic insects are sensitive to the hormone mimic, the effects are not fatal. And though it produced deformities in certain insects, it showed no effects on bees.
One thing is clear: As public health experts struggle to find less toxic ways to contain the spread of mosquitoes harboring a changing roster of emerging viruses, community action will become more important. At the very least, Killeen says, people should look around their houses. “We’ve just got too much junk these days,” he says. “The consumer society has been very good for Aedes aegypti.”
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