NOTE: Full lecture and slides available here: http://www.organic-center.org/science.pest.php?action=view&report_id=140
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Prevention, not profit, should drive pest management
Rachel Carson Memorial Lecture
Given by Chuck Benbrook
Systemic pest management
Pesticides News 82, December 2008

Summary points by GMWatch

In 2006, Florida's 33,000 acres of sweet corn were sprayed on average 13 times with 2.3 different insecticides, amounting to 3.7 pounds of active ingredient per acre. Almost nine applications were made per acre with carbamate methomyl. Few organisms would survive summer in such a corn field.

In south-central Florida in 2008, an experienced grower, producing several thousand acres of conventional vegetables, harvested 25 acres of organic sweet corn treated only with the natural insecticides Bt and diatomaceous earth. This sweet corn suffered less pest damage than most conventional corn in the region. In the State of Oregon in 2006, about three-quarters of the sweet corn acres (mostly conventional) were not treated with insecticide.

Why are a dozen or more applications of relatively toxic, broad-spectrum insecticides required on some sweet corn but not others?

The answer lies in the differences between integrated pest management (IPM), in contrast to management systems dependent on a few control tactics, especially those that are treatment-oriented and 'systemic' in nature.

'Systemic' approaches to pest management rest upon the incorporation in plants of chemicals or toxins which prevent pest damage. Taken to an extreme, the goal of systemic pest management is to eliminate any further need for the farmer to worry about pest management. The agribusiness industry favours systemic pest management, through patented GM seeds and systemic insecticides that are incorporated into the entire plant and persist for its whole lifespan. This approach encourages the emergence of pests that are resistant to the insecticides in question, because they are exposed over a longer period.

The systemic approach stands in stark contrast to integrated pest management (IPM), which relies on multiple tactics and practices to prevent pests from gaining a foothold in the field. The goal is to keep populations of pests below damage thresholds, so that more intrusive, costly, and often risky interventions are not necessary.

The systemic approach to pest management relies on costly inputs. The IPM approach relies on farmer knowledge.

Some farmers in the US have converted to IPM and, in general, have thrived as a result. In many crops and regions, organic farmers are at the forefront of IPM-innovation. For example, a significant share of the tree-fruit industry in Washington State has converted, or is transitioning to organic production, in part because of the organic price premium, but also because prevention-based IPM is working. It has dramatically lowered risks to farm workers and non-target organisms, and costs no more, in most years, than chemical-intensive management.

For decades farmers have relied on a series of seed treatments (a coating of pesticides on a seed) to help assure healthy germination and robust early growth of plants. The insecticides used for seed treatments have, until recent years, killed certain soil borne insects by contact, but since the late 1990s, systemic nicotinyl insecticides (also known as neonicotinoids) have taken over most of the seed treatment market around the world.

Nicotinyls kill sucking and chewing insects by disrupting the nervous system. In addition to moving to a new chemical family (nicotinyls), seed treatment delivery has also dramatically changed. Today, treated seeds are coated with a material that encapsulates the seed treatment chemical(s), and releases them slowly. This extends the time period during which the root systems of newly germinated plants receive a measure of protection, but it also extends the time during which residues from seed treatments persist in treated plants.

In the US, and to a lesser extent in Europe, public policies have created or reinforced incentives that are driving agribusiness toward systemic approaches to pest management. Few farmers, scientists, and regulators understand the consequences of the shift that is occurring. The research required to serve as an early warning system of major problems is not being done. Our failure to ask ecologically-grounded questions, coupled with the economic power behind the private sector push toward high-cost systemic, genetic engineering and proprietary pest management technology, has set the stage for a series of train wrecks.

Moreover, we are ill-equipped to deal with the unravelling of today’s pest management technology because too many eggs are in one technological basket, and investment in alternatives has waned. This is a sad state of affairs in an era of great scientific and technical progress, during which safe and sustainable pest management alternatives are emerging all over the world.

Nicotinyl insecticides are emerging as the most important class of systemic pesticides and on conventional farms they are now the backbone of most insect pest management systems, especially in high-value fruit and vegetable crops. In apples, 25% of the total crop acres in the US in 2007 were treated with imidacloprid, another 37% with acetamiprid, and 8% with thiamethoxam. These three nicotinyls were used on 70% of apple acres in 2007, 79% of pears in 2005, and in 2006, 54% of broccoli and 40% of cauliflower.

In 2003, as problems worsened with corn rootworm, Monsanto introduced Cry 3bB Bt corn, engineered to express a Bt toxin active against corn rootworms and other soil borne insects. In 2008 nearly one-third of corn acres were planted to Bt corn for corn rootworm control, and several million acres were planted to ‘stacked’ varieties expressing two Bt toxins, and conferring resistance to the herbicide glyphosate.

All major corn seed companies are moving rapidly toward the day when most seed comes with at least a three-trait stack two Bts and resistance to glyphosate. In addition, virtually all of this GM-corn seed will be treated with a systemic nicotinyl seed treatment, and some 30% of the acres will likely still be treated with an insecticide.

Accordingly, in the next few years, the average acre of field corn in the US will contain 26,000 to 32,000 plants with over three insecticides moving through plant tissues two Bt toxins manufactured in the plant, a nicotinyl seed treatment, and on perhaps 15% to 20% of the acres, a systemic insecticide.

Contrast today's need for over three systemic insecticides to the ability of corn farmers in the early 1990s to get by with less than 0.3 systemic insecticide applications per acre. The approximate ten-fold increase in reliance on systemic insecticidal toxins over about a decade marks a new high gear on the corn insect pest management treadmill. It also is imposing on several insect species tremendous selection pressure for resistance. The corn rootworm is notorious for its genetic plasticity, and now, we are selecting for resistant variants to two Bt toxins and the whole class of nicotinyl insecticides, all at the same time.

New risks?

We are entering uncharted waters in the assessment of farm animal, human, and ecological impacts associated with the trend toward systemic solutions to corn insect management challenges. Millions of acres of corn silage are grown and harvested at a stage when there remain relatively high levels of Bt toxins, and perhaps even nicotinyls, in plant tissues. The impacts on animal health and reproduction of the toxin cocktail now in corn silage has not been researched.

No one in the US has carried out the studies necessary to determine whether Bt toxins or nicotinyl insecticides concentrate in corn kernels, or certain products made from corn, such as fructose corn syrup.

Honey bees in peril

Because of the vital role played by bees in crop pollination, honey bee Colony Collapse Disorder (CCD) threatens the production of crops that produce about one-third of the UK and American diets, including nearly 100 fruits and vegetables. The value of crops pollinated by bees exceeds $15 billion in the US alone. Populations of native pollinators are in decline worldwide, heightening the importance of reversing CCD. A survey of US beekeepers was conducted between September and March 2007 and reported an average bee loss of 37.6%, about triple the norm, with over half of respondents reporting 'abnormally heavy' losses. One in three bee colonies have been lost in the UK since autumn, 2007.

Progress has been made in identifying possible causes of CCD, which are likely to include complex combinations of pesticides, weakened immune systems, varroa mite, and viruses. Still, the epidemiology of CCD remains puzzling. One team found an average of 3.7 pathogens in bees from CCD hives, compared to 2.1 pathogens in non-CCD hives. Two possible CCD risk factors have received much attention GM crops and nicotinyl insecticides (such as imidacloprid, thiamethoxam, clothianidin, acetamiprid).

The Bt toxins in GM corn are not known to be active against bees, nor do CCD symptoms match the mode of action of Bt toxins. Several studies have found no adverse acute or subacute effects following the feeding of bees on pollen from Bt corn plants, nor pollen cakes spiked with purified Bt endotoxins4. Plus, the geographic distribution of Bt corn in the US is heavily concentrated in a few regions and clearly differs from the distribution of CCD.

Still, the potential for horizontal gene transfer from GM-crop pollen to microorganisms in the bee gut has been demonstrated; pollination deficits have been recorded in canola fields planted to GM herbicide-tolerant varieties, compared to ‘moderate deficits’ in fields planted to conventional seed and no deficit in fields under organic management; and behavioural effects linked to CCD have been demonstrated in bees exposed to high levels of Bt corn toxins.

Evidence in support of an impact on bee hive health by the systemic nicotinyl insecticides is far more convincing and well beyond the threshold needed to justify decisive action to prevent future losses.

Nicotinyls are moderately persistent in the soil and are the most acutely toxic pesticides ever registered to bees. Major bee kills have occurred from foliar applications, leading to binding pesticide product label restrictions (such as, ‘Do not spray when bees are actively foraging in the field’).

These insecticides are also known to cause chronic and sublethal effects in bees at very low doses measured in parts per billion or even parts per trillion. Such effects include impaired foraging ability, failure to return to the hive, and other neurobehavioural impacts.

Concern over the extreme toxicity of nicotinyls to bees in Europe in the late 1990s led to questions about routes and levels of bee exposure, and possible chronic and subacute effects. While most of the initial focus was on standard agricultural applications of nicotinyls in the field, exposures linked to the seed treatments have emerged as possibly the missing piece in the CCD puzzle.

Focus on seed treatments

Most conventional corn seed, and virtually all Bt corn, is now treated with a nicotinyl seed treatment to protect just-germinated corn plants from soil borne insects. Corn plants grown from seed treated with the typical commercial rate of 1mg imidacloprid per seed produced pollen with an average level of 2.1 ug/kg (ppb) imidacloprid. A bee ingesting just 6 mg of such pollen per day would have a PEC/PNEC (probable exposure concentration/predicted no effect concentration) ratio of between 500 and 600 for chronic mortality after 10 days of exposure. [NB: A PEC/PNEC ratio greater than 1 indicates a risk. The higher the value, the higher the risk] This leads to the conclusion that imidacloprid ‘is one of the major factors contributing to the weakening of bee colonies.'

Levels found in sunflower pollen and flowers, from plants sown with imidacloprid-treated seed, were 3 ug/kg and 8 ug/kg, levels high enough to kill bees. Chronic and sublethal effects have been reported at levels between 0.1-10 ug/kg (ppb) in a bee food source. Neurobehavioural problems in bees have been reported from exposures to imidacloprid and other nicotinyls at levels routinely found in crops grown from seeds treated with nicotinyls.

Plant tissues known to sometimes contain damaging levels of nicotinyls from seed treatments include corn foliage, silk, and pollen, and rapeseed and sunflower pollen and nectar.

The finding of neurobehavioural disruption is significant given that a hallmark of CCD is that foraging bees leave the hive but cannot find their way back. Still, if nicotinyl insecticides in corn silk, pollen or nectar are a major cause of CCD, the epicenters of CCD should include the American Midwest and the Canadian prairies where corn and canola seed treated with nicotinyls are widely planted.

This does not appear to be the case. In the US colony collapse disorder appears to disproportionally impact large, commercial bee keepers who often move their hives long distances in the late winter. Transporting hives is a source of stress, and also tends to bring multiple populations together, where pathogens from many areas and bee strains are readily exchanged. It is also known that CCD tends to happen early in the season during the first spring flights from a hive, suggesting that something in the winter feeding and management of the bees may be a CCD risk factor.

Other notable pieces of the CCD puzzle include the fact that a significant portion of commercial bee keepers leave inadequate stores of honey in their hives to sustain the bees through the winter, and instead feed bees a cheaper high fructose corn syrup (HFCS) supplement. Starting in about 2004, and roughly coinciding with the emergence of CCD, corn seed companies in the US began marketing seeds treated with a 5-X rate of nicotinyls (1.25 mg/seed, compared to the traditional 0.25 mg/seed). The rate was increased to expand the range of insects adequately controlled, and/or to control higher insect populations. For example, 80% of the corn seed sold in 2007 by corn seed market leader Pioneer Hi-Breed Int. was treated with Poncho 250 or 1250 seed treatments containing clothianidin at 0.25 and 1.25 mg/seed respectively, plus two fungicides (the systemic azoxystrobin, and fludioxonil). Pioneer first sold seeds treated with the 5-X rate of clothianidin in 2004.

Moreover, simultaneous bee exposure to nicotinyls and fungicides (triflumizole and propiconazole) can increase the potency of nicotinyls up to 1,141-fold. Possible synergistic effects between nicotinyls and other fungicides have not been explored to date.

A growing body of evidence suggests that the most decisive and concrete action that can be taken worldwide to reduce the chances that honey bee CCD will persist, or grow worse, is to end seed treatments with any pesticide that is: (a) systemic, and (b) highly toxic to bees. The only class of contemporary seed treatments that meets both criteria is the nicotinyls.

Moreover, the impacts of nicotinyls on bees are likely just the first of many surprises in terms of the ecological impacts of systemic pesticides. Most regulatory programmes, and certainly those in the US, pay little attention to pesticide impacts on bees. In the face of clear evidence of substantial potential harm to bees, registrations are still granted, along with label language designed to limit bee exposures.

The US EPA has never denied an application for a new pesticide, nor banned a currently registered product because of adverse impacts on bees, nor is it likely to without new legislation and a push from the public and Congress.

Lessons learned

Residues of systemic pesticides cannot be washed off the surface of foods, because they are inside the food. This increases the frequency and potential risk associated with dietary residues. Organisms other than target pests that feed on plants treated with systemic pesticides are more likely to be exposed, since the residues of systemic pesticides, or their metabolic breakdown products, tend to be more persistent inside plant tissues than when lodged outside, on plant surfaces, where rainfall and sunshine washes them off and breaks them down.

By incorporating systemic toxins into plants, pesticide and seed companies bear a more complex scientific burden, since the impacts of the toxins on the physiology of the plant should be explored with a high degree of sophistication. Today’s cursory reviews and ‘substantial equivalence’ policies are grossly inadequate for this purpose and will not detect most subtle changes in gene expression and regulation brought about by the presence of systemic pesticidal toxins and, in the case of Bt-transgenic plants, the genes needed to produce Bt endotoxins within plant cells.

Moreover, the trend toward systemic pest management technologies is likely to alter how plants respond to unusual biotic or abiotic stresses. Such responses by plants trigger and control production of phytochemicals, and hence can lead to possibly significant nutritional and food safety consequences, some beneficial, others likely not.

The best way to minimize the chance that systemic pest management solutions trigger unforeseen problems is to rely on them sparingly and only when prevention-based biointensive IPM systems are overwhelmed. That is not the path we are now on. Our current path is leading inevitably to the need for more toxins, which will trigger more resistance, kill more beneficial organisms, narrow biodiversity and set the stage for higher costs and new and unanticipated problems.

If we travel too far down our current path, we could create conditions in our food system much like those that brought down the financial system. That is an outcome we should all work tirelessly to avoid.