Controversial pesticides linked to catastrophic honeybee declines in North America and Europe may also kill other creatures, posing ecological threats even graver than feared, say some scientists.

According to a report by the American Bird Conservancy, the dangers of neonicotinoid pesticides to birds, and also to stream- and soil-dwelling insects accidentally exposed to the chemicals, have been underestimated by regulators and downplayed by industry.

"The environmental persistence of the neonicotinoids, their propensity for runoff and for groundwater infiltration, and their cumulative and largely irreversible mode of action in invertebrates raise environmental concerns that go well beyond bees," stated the report, which was co-authored by pesticide policy expert Cynthia Palmer and pesticide toxicologist Pierre Mineau, both from the American Bird Conservancy.

Chemical and pharmaceutical company Bayer, a major neonicotinoid manufacturer, said the criticisms lack solid evidence. "This report relies on theoretical calculations and exposure estimates that differ from accepted risk assessment methodologies, while disregarding relevant data that are at odds with its claims," the company said in a statement.

The Bees

Neonicotinoids became popular in the late 1990s, largely replacing earlier insecticides that posed blatant health and environmental risks. Derived from nicotine, which short-circuits the nervous systems of insects that try to eat tobacco plants, neonicotinoids at first seemed both effective and safe.

They now account for some one-quarter of global insecticide sales, used on hundreds of crops and also in gardens and cities. In the last several years, though, it's become evident that regulators, especially the Environmental Protection Agency, overlooked the extreme toxicity of neonicotinoids to honeybees and other pollinators. Regulatory approvals were partly based on industry studies now considered unreliable, and sometimes despite the concerns of the EPA's own scientists.

Neonicotinoids subsequently emerged as a prime suspect in colony collapse disorder, the unexplained malady that since 2005 has annually killed about one-third of the nation's commercial honeybees, and may also affect bumblebee populations. The pesticides are blamed for triggering collapses outright or making bees vulnerable to to diseases and parasites.

A group of beekeepers and environmental groups have sued the EPA, which now plans to review evidence of neonicotinoid harms. Yet amidst the honeybee furor, far less attention has been paid to what the pesticides may do to other creatures.

Early toxicity studies suggested the risks were relatively small: Vertebrates don't have precisely the same receptors to which neonicotinoids bind so tightly in insects, so higher doses are needed to cause harm.

It was also assumed that neonicotinoids wouldn't accumulate in the environment at levels capable of harming either vertebrates or non-pest, non-pollinator invertebrates – the countless insect species that are the foundation of terrestrial and aquatic food webs.

Since then, however, researchers have found widespread evidence of neonicotinoids spreading beyond their crop targets, and the methodologies used to establish neonicotinoid safety have come under question.

"The more studies I see, the more I think the preponderance of evidence is leaning towards neonicotinoids being tremendously bad for lower animals in the food chain, especially all the invertebrates," said Scott Black, executive director of the Xerces Society, an invertebrate conservation group.

The Birds

Seeds used to grow crops like corn, sunflowers and canola are routinely coated in neonicotinoids, which then spread through plants as they grow. Many species of birds eat seeds. In the absence to date of studies directly observing farmland birds and their day-by-day fates, the question of whether neonicotinoids harm them quickly becomes an argument over methods used to set toxicological guidelines.

In the American Bird Conservancy report, Mineau and Palmer note that the EPA typically sets guidelines for bird exposures using laboratory tests on just two species, mallard ducks and bobwhite quail. Their results become the basis of standards for other birds, but this elides widely varying sensitivities among hundreds of species.

For example, the LD50 – a standard toxicological measure for a dose that kills half of exposed animals – for bobwhite and mallards consuming imidacloprid, the most common neonicotinoid formulation, are 152 and 283 milligrams per kilogram of body weight. For canaries, that number drops to about 35 mg/kg, and for gray partridge it's just 15 mg/kg.

Were the guidelines calculated more carefully, say Mineau and Palmer, drawing broadly on peer-reviewed literature and accounting for heightened sensitivity in certain species, they'd be very different. What are now considered safe exposure levels would be recognized as poisonous – and many birds could reach them by eating just a few seeds.

Asked for comment, the Environmental Protection Agency said the report "uses a method to compare risks across chemicals that differs from the long-standing peer-reviewed approach EPA uses. The agency will carefully consider the report’s studies, analytic methods and conclusions."

David Fischer, director of environmental toxicology and risk assessment in Bayer's CropScience division, said the report misrepresented industry testing. "We tested a lot of species. We did tests beyond what was required by the EPA," Fischer said. If neonicotinoids really were killing birds, said Fischer, it would already have been reported, as were die-offs from the earlier, more-toxic chemicals that neonicotinoids largely replaced.

"There have been few instances of mortality in the field. They're extremely rare," Fischer said. "I don't know of any incidents in North America." Mineau responded that, even with earlier chemicals, researchers didn't find evidence of bird deaths until they actively looked for them. That hasn't yet happened with neonicotinoids, he said, and poisoned birds don't immediately and visibly drop dead on fields. They may die hours or days later in a tree or bush, making it unlikely that anyone will even notice.

The report also notes that chronic toxicity – effects that don't kill animals outright, but over time cause health, reproductive and behavioral problems – has largely been overlooked. Preliminary studies suggest a potential for embryo development disorders and decreased immune responses, but guidelines were again set by reference to bobwhite and mallards. Tests only measured obvious birth defects, ignoring the many other ways that animals can be impaired.

Mineau thinks neonicotinoids are at least playing a role in the precipitous decline of birds that live in or migrate through agricultural areas. "I believe this is happening right now," he said. Yet that, said Mineau, may be just a prelude to other problems. "I think the aquatic and soil impacts are even greater," he said. "We're going to see profound changes in aquatic and terrestrial ecosystems."

Sope Creek near Marietta, Georgia, where high levels of neonicotinoids have been detected in the water. Image: Timothy J Carroll/Flickr

Soil and Streams

Neonicotinoids are what's known as "systemic" pesticides, which spread through plant tissue, suffusing it from root to tip. For any given dose, a large proportion of any dose ends up in soil, carried there by roots or plant debris. Depending on conditions, neonicotinoids can remain active for weeks or even months.

What this does to soil-dwelling insects, which would generally be extremely sensitive to exposure, is uncertain. Fischer said neonicotinoids bind to particles of clay, effectively removing them from circulation and making keeping them from being absorbed by other insects. Black said some invertebrates, such as earthworms, do pick up neonicotinoids, and that the pesticides are re-absorbed by subsequent generations of plants, creating new and unintentional exposures.

Soil-bound neonicotinoids also leach into groundwater, ending up in streams and waterways. The danger to fish appears low, if not negligible, but is much higher for aquatic invertebrates. Not only are they neurologically vulnerable to neonicotinoids, said environmental scientist Jeroen van der Sluijs of Utrecht University in the Netherlands, but each exposure builds on the last. Damage caused by neonicotinoids their nervous systems is irreversible, producing compounded effects from multiple exposures.

The EPA's own reviews state that imidacloprid is "acutely very highly toxic" to aquatic invertebrates, with lethality to common creatures seen at concentrations of .05 parts per million, and chronic damage at even lower concentrations. In the United States, where just one-fifth of all streams are considered healthy, systematic watershed testing for neonicotinoids hasn't been conducted, but concentrations well above those levels have been measured in multiple locations.

Surface water measurements of neonicotinoids in the Netherlands. Green dots correspond to levels at or below European standards of acceptable risk. Image: Jeroen van der Sluijs

Over a six-month period at waterways near Marietta and Whitesburg, Georgia, for example, imidacloprid levels averaged 7.13ppm, or some 142 times higher than what the EPA had considered highly toxic. Neonicotinoids have also been detected in water in California, Wisconsin, New York and Quebec.

According to Bayer, their own laboratory tests show that, even at the reported concentrations, effects are not significant. "We've tested entire aquatic communities, in microcosm tests," with no decline in biomass until well beyond routinely measured concentrations, said Fischer.

Yet van der Sluijs argues that real-world effects are visible. Large-scale neonicotinoid in the Netherlands started around 2004, and preliminary research from his own laboratory has correlated neonicotinoid levels in Dutch waterways with large drops in insect populations. "This will likely have an impact on insect-feeding birds," said van der Sluijs.

Insect-eating birds are indeed declining in the Netherlands and elsewhere, a trend that dates to the 1960s and is blamed on a variety of factors, including earlier generations of pesticides, habitat alteration and climate change. Neonicotinoids represent a fairly new threat, but van der Sluijs is not alone in his concerns.

Ecotoxicologist Christy Morrissey of the University of Saskatchewan said there is "considerable circumstantial evidence that these chemicals are causing large-scale reductions in insect abundance. At the same time, we are observing serious declines in many species of birds in Canada, particularly aerial insectivores, swifts and swallows for example, that are highly dependent on insects to raise their young."

Like the EPA, Canada's Pest Management Regulatory Agency is also reviewing neonicotinoids. Morrissey's research is still preliminary, but in most of the wetlands she's sampled, she's found neonicotinoids. "It is moving off the seeds in the fields and into the water," Morrissey said. There appear to be fewer insects in heavily agricultural sites than elsewhere, she said, and birds nesting nearby have lower body weights.

The Future

Concerning as these observations may be, correlations are not proof of causation. Still, the American Bird Conservancy and Xerces Society think there's concern enough for the EPA to accelerate their neonicotinoid review, which is expected to finish in 2018, and consider limiting some uses of the pesticides immediately.

Though prompted by concerns over pollinators, the EPA's review "is not limited to evaluating potential impacts on bees," but will include comprehensive ecological assessments, said the agency. Companies will be required to monitor the environmental presence of neonicotinoids.

Bayer argues that neonicotinoids have become invaluable to farming, and trying to replace them could backfire. "Without these products, an additional three million acres of corn would need to be planted to compensate for the lost productivity," the company said in the statement. "There would be pressure to convert land currently set aside for nature to farmland."

Black said that integrated pest management, or IPM, which combines precisely targeted chemical use with other, non-chemical means of pest control, can deliver industrial-scale yields in an environmentally sustainable way. "We've moved away from IPM, from scouting your farm, putting in habitat for beneficial insects, and spraying only if there's damage," he said. "With neonicotinoids, you don't do that any more."

In coming months, more studies are expected to be published on the ecological effects of neonicotinoids. These may provide a more conclusive diagnosis of what's happening. For Black, the situation resembles what happened with the pesticide classes they replaced, which were rushed to market to replace environmentally toxic DDT. Only later were their dangers recognized. "We've gone full circle here," he said. "We seem to approve these products before we have all the information."