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As children, we learn about one of Nature’s most beautiful and ingenious inventions:  the seed. We learn that the coat of a seed provides both protection and nutrition for the fledging plant inside. We learn later in life about the less beautiful truth of commercial seeds. Our modern-day seeds are often covered in a layer of synthetic chemicals, designed to protect the plant from pests like weeds and insects. While these chemicals can increase the efficiency of farming, there are negative environmental consequences of widespread and intensive use of herbicides and pesticides, some of which are just being elucidated. The most common seed treatments are chemicals from a family of compounds called neonicotinoids. As the name implies, these compounds are structurally related to nicotine, the naturally occurring alkaloid stimulant found in tobacco leaves. Seeds from an array of crops, including cereals, corn, sugar beets, rice and cotton, are treated with neonicotinoids, which serve as highly effective insecticides.

The most widespread neonicotinoid is imidacloprid. Imidacloprid was developed in the 1980s, and was approved for use in the United States by the Environmental Protection Agency in 1994. (1) Imidacloprid kills insects by disrupting the nervous system through binding of the nicotinic acetylcholine receptor (nAChR). While all animals have this receptor, the protein has different forms in different organisms, and imidacloprid is highly specific for the nAChR found in insects.

Persistent pesticide

Figure 1 ~ The lifecycle of imidacloprid, from plant treatment, insect exposure, and its ultimate spread through the environment. 

Despite its selective and acute toxicity for the insects that farmers would like to rid from their crops, imidacloprid use has been linked to several negative environmental impacts. The driving factors for imidacloprid’s environmental effects are its physical characteristics (Figure 1). Imidacloprid has a polar, or non-greasy, structure, making it very soluble in water. This physical characteristic allows the chemical to be distributed throughout the tissue of seed-treated plants via the plant vasculature. Thus, a flowering plant seed-treated with imidacloprid will contain the chemical in its pollen. Furthermore, imidacloprid that isn’t taken up by plants will be carried in the water run-off from the field. In addition to its water solubility, imidacloprid has a half-life in soils greater than 1000 days, meaning that after nearly three years, half of the initial concentration of imidacloprid will still remain in a given area (2). The long lifetime and water solubility of imidacloprid mean that it can be widely dispersed from areas where it was first applied and it can accumulate in soils and water over time. Imidacloprid’s physical traits have negative and unintended consequences for organisms not targeted by the insecticide, including pollinators like bees and, as new research suggests, even birds.

Pollinators at risk

If you’ve gone shopping at an organic grocery store recently, you may have noticed signs for certain products that support pollinator health. Pollinators like bees are incredibly important for agriculture, contributing to the growth of plants that make up about a third of the food we consume each year, including blueberries and almonds. In 2006, beekeepers started noticing that bees were abandoning their hives. The sudden loss of bee colonies in Europe and the US is a disturbing phenomenon that has been named “colony collapse disorder” (CCD, see previous Signal to Noise article). The causative agent of CCD has not been unequivocally identified (3). However, research has identified several possible causes, including infection of bees with the intestinal fungal parasite Nosema apis (4).  Imidacloprid is often found in bee hives, and research suggests that exposure may negatively affect bees’ resistance to the diseases implicated in CCD. In addition, imidacloprid exposure adversely affects bees’ ability to navigate and collect food.

Due to the connection between neonicotinoid exposure and pollinator health, the European Commission issued a two-year ban on specific uses of three different neonicotinoids–including imidacloprid (5). The ban includes seed and foliar, or leaf, treatments of crops including cereals, corn and sunflowers. The dust kicked up from planting imidacloprid-treated seeds and the chemically-contaminated nectar and pollen were cited as exposure routes for bees. However, the extent of imidacloprid’s environmental impact remains unclear. Are other organisms, beyond insects, affected?

Imidacloprid affects the bees… and the birds?

New research published in the journal Nature in July 2014 suggests that imidacloprid may negatively impact birds, in addition to insect pollinators (6). Led by Eelke Jongejans from the Radboud University Nijmegen in the Netherlands, the researchers hypothesized that imidacloprid has a negative impact on populations of birds that eat insects. Specifically, they asked whether there was a significant correlation between the concentration of imidacloprid in water sources and bird populations in those areas.

To investigate their hypothesis, they analyzed data from two long-term studies conducted in the Netherlands. The first study, called the Dutch Common Breeding Bird Monitoring Scheme, is an extensive monitoring program of birds that has been ongoing since 1984. Jongejans and colleagues selected fifteen species of bird that are common on farms and that eat insects during the breeding season. For each geographic location where the birds were monitored, they calculated the intrinsic rate of increase in these bird populations over the period 2003-2009. The intrinsic rate of increase is essentially a measurement of the number of births minus deaths in a given group of organisms over a given period of time.

The second dataset came from the Dutch Pesticide Atlas, a database of measurements from routine monitoring of over 700 chemicals, including imidacloprid, in surface waters throughout the Netherlands. From these data, they could make a map of the average imidacloprid concentration measured in different locations in the time period from 2003-2009.

Figure 2 ~ In the 2014 Nature paper from Jongejans and co-workers, the concentration of imidacloprid in surface water was shown to be negatively associated with insectivorous bird populations in the Netherlands. 

Using both datasets described above, the researchers were able to compare the rate of change in the populations of birds and the concentration of imidacloprid in a given area. They found a negative relationship between the concentration of imidacloprid and the rate of population increase in 14 of the 15 species of birds studied. In other words, in places where the average concentration of imidacloprid was high, the rate of population growth of birds in those areas decreased. (Figure 2) Specifically, they found that when the concentration of imidacloprid in local surface waters exceeded a threshold concentration, bird populations started shrinking, with an average annual population decrease of 3.5%. The imidacloprid concentration threshold determined is nearly 1000 times lower than the concentration set by the EPA to prevent chronic toxicity to insects in water. The EPA’s guideline, called the Aquatic Life Benchmark, may therefore be insufficient to prevent the environmental impacts of imidacloprid (7).

The researchers suggest that the association of bird population decline and imidacloprid could arise from the simple fact that intensive use of imidacloprid on farmlands will deplete insect populations, and insect-eating birds rely on these bugs for food. While birds may not be killed directly by consumption of imidacloprid, decimation of their resources will affect their ability to reproduce and feed their young. The researchers emphasize that more studies should be done on the trophic, or food-related, interactions between pesticides and animals. In conclusion, this study shows that there is a significant correlation, or association, between the concentration of imidacloprid in water and the populations of birds in these same areas, but more studies are needed to pinpoint the direct causes for these effects on bird populations.

What does the association of imidacloprid and bird populations mean for the future of neonicotinoid use? In terms of creating new regulations for pesticides, an important question is, how we can measure the environmental impacts of pesticides beyond their lethal dose for different animals? Can we regulate the use of imidacloprid to minimize its effects on non-targeted organisms? Where and how often should we measure the concentrations of imidacloprid and other persistence pesticides? Our increasing understanding of the connections between bees, birds and imidacloprid points to the complexity and far-reaching effects of the chemical and biological interactions that occur when we add another chemical layer to Nature’s simple seed.

Carolyn Brotherton is a Ph.D candidate in the Balskus lab in the Department of Chemistry and Chemical Biology at Harvard University. 

References

  1.  “Imidacloprid Technical Fact Sheet National Pesticide Information Center http://npic.orst.edu/factsheets/imidacloprid.pdf
  2. Van der Sluijs, J. P., et al. “Conclusions of the Worldwide Integrated Assessment on the risks of neonicotinoids and fipronil to biodiversity and ecosystem functioning.” Environmental Science and Pollution Research 1-7 (2014).
  3. Watanabe, M.E. “Colony Collapse Disorder: Many suspects no smoking gun.” The Xerces Society for Invertebrate Conservation
  4. Hopwood, J., Vaughan, M., Shepherd, M., Biddinger, D., Mader, E., Black, S. B., Mazzacano, C. “Are neonicotinoids killing bees?” The Xerces Society for Invertebrate Conservation http://www.xerces.org/neonicotinoids-and-bees
  1. “Colony Collapse Disorder: European Bans on Neonicotinoid Pesticides” United States Environmental Protection Agency http://www.epa.gov/pesticides/about/intheworks/ccd-european-ban.html
  2. Hallmann, C. A.; Foppen, R. P. B.; van Turnhout, C. A. M.; de Kroon, H.; Jongejans, E. Nature 511, 341-343 (2014).
  3.  “Office of Pesticide Programs’ Aquatic Life Benchmarks” United States Environmental Protection Agency http://www.epa.gov/oppefed1/ecorisk_ders/aquatic_life_benchmark.htm

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