Editor's Choice: Silent Spring redux? Insecticides cascade up a food chain to poison carnivores

February 2015 (Issue 52:1)

Douglas, M. R., Rohr, J. R., Tooker, J. F. (2014), Neonicotinoid insecticide travels through a soil food chain, disrupting biological control of non-target pests and decreasing soya bean yield. Journal of Applied Ecology. doi: 10.1111/1365-2664.12372

Note: This article was first written by Ian Kaplan as a post for The Applied Ecologist's Blog.

Despite being published >50 years ago, almost everyone is familiar with Rachel Carson’s Silent Spring – a cautionary tale of the environmental risks posed by indiscriminate pesticide use, in this case DDT. The example is still frequently cited in science classes throughout the world to illustrate a phenomenon known as biomagnification, whereby the concentration of substances such as chemical pollutants amplify in animal tissues as they transfer up the food chain to apex predators. This results in a more convoluted pathway than pesticides harming non-target species due to direct contact toxicity. It necessitates a food web approach that tracks who eats whom.

Recently in Journal of Applied Ecology, Margaret Douglas and colleagues at Penn State University describe an analogous process by which neonicotinoid insecticides (hereafter, abbreviated as ‘neonics’) poison predaceous insects by consuming intoxicated prey along a soil food chain (Douglas et al. 2014). Much like their DDT predecessor in the mid-1900s, neonics experienced an exponential rise in use on farmland since their discovery nearly two decades ago and are now the most widely used insecticide in the world. Neonics are typically added as a prophylactic seed coating onto soybean, the focal crop of this research, as well as other large acreage field crops that dominate land use in many regions (e.g., corn, canola and cotton). From there, the insecticide is absorbed by the roots of newly emerged seedlings and expressed throughout all plant parts, creating a toxic barrier to insect pests.

Despite their sudden rise to dominance, neonics are also highly controversial, due in large part to pollinator-related concerns such as their connection to localized honeybee kills (e.g., Krupke et al. 2012) and interference with bumblebee reproduction at low doses (Whitehorn et al. 2012). More recently, however, the focus has shifted to include detrimental effects on other non-target species in natural communities (Goulson 2013) such as birds (Hallmann et al. 2014) and aquatic invertebrates (Van Dijk et al. 2013). Douglas and co-authors focus their research on the impact of neonics on a key ecosystem service provided by insect predators and parasites – natural pest suppression, or biological control. Surprisingly, the consequences of neonics for biocontrol and routes of exposure for beneficial pest-killing carnivores are poorly understood (Hopwood et al. 2013).

In their study system, slugs are a dominant pest – more so than insects – where they reduce soybean establishment, particularly in no-till management systems that are increasingly common and promoted due to their agronomic benefits (e.g., reduced soil erosion). Slugs, in turn, are attacked and consumed by predatory insects including voracious ground-foraging beetles in the family Carabidae. Interestingly, in this crop–pest–predator chain linking soybeans, slugs, and beetles, Douglas and colleagues convincingly demonstrate that neonic seed treatments have no direct impact on slug survival, growth, or feeding damage (perhaps to be expected since neonics are insecticides, not molluscicides), but indirectly benefit slugs and reduce soybean yield by poisoning beetles. Essentially, slugs serve as a conduit for neonics, creating pesticide-infused toxic prey that impair or kill their natural control agents. This exposure route is critical as ground beetles do not feed on soybean plants and thus require slugs to pass along the poison. While neonics have previously been shown to induce outbreaks of non-target crop pests (Szczepaniec et al. 2013), this study reveals a novel mechanistic pathway the authors describe as ‘trophic transfer’. In this process neonics decrease in concentration up the food chain, as opposed to biomagnification where it would increase; however, strong effects were still apparent because neonics are extremely toxic even at low doses (i.e., only a little of the insecticide needs to be present in a slug to influence beetle behavior and physiology). This also provides among the first field data illustrating that neonic applications can decrease crop yield and integrates a specific mechanism by which this yield reduction occurs.

This work is especially timely because the Biological and Economic Analysis Division (BEAD) of the U.S. Environmental Protection Agency recently released a report entitled Benefits of Neonicotinoid Seed Treatments to Soybean Production, in which they state: “BEAD concludes that these seed treatments provide negligible overall benefits to soybean production in most situations.” Given this lack of yield enhancement and emerging data on the environmental risks of prophylactic neonic use on large acreage crops, change seems inevitable. Whether this means the U.S. follows the lead of the E.U. in imposing greater restrictions on neonic use or industry takes a proactive stance in facilitating change from within, remains unclear. However, entomologists have been pushing for a return to IPM principles that began decades ago and this study is an outstanding example of why.

Ian Kaplan
ikaplan@purdue.edu
Associate Editor

References

Douglas, M.R., Rohr, J.R., Tooker, J.F. (2015) Neonicotinoid insecticide travels through a soil food chain, disrupting biological control of non-target pests and decreasing soybean yield. Journal of Applied Ecology doi: 10.1111/1365-2664.12372

Goulson, D. (2013) An overview of the environmental risks posed by neonicotinoid insecticides. Journal of Applied Ecology, 50, 977–987

Hallmann, C.A., Foppen, R.P.B., van Turnhout, C.A.M., de Kroon, H. & Jongejans, E. (2014) Declines in insectivorous birds are associated with high neonicotinoid concentrations. Nature, 511: 341–343

Hopwood, J., Black, S.H., Vaughan, M. & Lee-Mäder, E. (2013) Beyond the Birds and the Bees: Effects of Neonicotinoid Insecticides on Agriculturally Important Beneficial Invertebrates. 32 pp. Portland, OR: The Xerces Society for Invertebrate Conservation

Krupke, C.H., Hunt, G.J., Eitzer, B.D., Andino, G. & Given, K. (2012) Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLoS ONE, 7(1): e29268

Szczepaniec, A., Raupp, M.J., Parker, R.D., Kerns, D. & Eubanks, M.D. (2013) Neonicotinoid insecticides alter induced defenses and increase susceptibility to spider mites in distantly related crop plants. PLoS ONE, 8(5): e62620

Van Dijk, T.C., Van Staalduinen, M.A. & Van der Sluijs, J.P. (2013) Macro-invertebrate decline in surface water polluted with imidacloprid. PLoS ONE, 8(5): e62374

Whitehorn, P.R., O’Connor, S., Wäckers, F.L. & Goulson, D. (2012) Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science, 336, 351–352

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