Pesticidal (GM) crops and organic farming
 

E. Ann Clark, Plant Agriculture, University of Guelph, Guelph, ON (eaclark@uoguelph.ca)©2000 E. Ann Clark


Genetic engineering to produce pesticidal crops(1) has been portrayed as a blessing to environmentally conscious farmers and to organic farmers in particular. Many growers have responded to this premise with an intuitive or ethical aversion. However, the notion of replacing synthetic pesticides with "plant-produced" pesticides has achieved some resonance with society in general and perhaps with some organic growers as well. The human and environmental risks of synthetic pesticides are increasingly acknowledged by society at large, but the striking parallels between pesticides and pesticidal plants remain obscure to many.

Consider, for example, the scenario painted in the April 2000 issue of Canadian Gardening Magazine. In an article entitled Designer Genes, we are treated to an idyllic vision of a future most of us could live to see:
 
"The month is June, the year is 2030, and you're relaxing in your garden. The perennial border is looking good in the colours you chose from the colour chart. The roses, an intense periwinkle blue, match perfectly. You lift your head to catch their scent - not the overpowering sweetness of the old-fashioned roses, but the more bracing lemon smell you ordered from the catalogue." 

"Meanwhile, in the vegetable patch, the anti-cancer broccoli and tomatoes are nearly ripe. Naturally, you've never sprayed pesticides on them" (emphasis added).

This is not a spoof or satirical jest, but an article written in deadly earnest, to convince the gardening public of the consumer benefits of genetic engineering awaiting just around the corner - if they will only stop delaying progress by fussing over the imaginings of those meddlesome activists.


So, what is the beef? With eyes rolling heavenward, proponents express frustration and abject disbelief at the persistent objections of organic growers to even so environmentally friendly a GM product as Bt-crops. "First they complain about the pesticides, and now when we give them GMO's to reduce the pesticides, still they object! Like, what do these people want!?" "Who", they ask rhetorically, "could possibly argue with the ecological and health benefits of pesticidal plants?!" (or golden rice, or whatever)

Me. These arguments, whether for pesticidal crops or golden rice, are appealing precisely because they do not consider the whole story. They do not ask such troubling questions as:

Proponent arguments, whether for used cars or for pesticidal crops, are meant to be persuasive. As everyone can appreciate, however, persuasive arguments bear no necessary relationship to reality.

In this paper, we will discuss evidence to dispute the thesis that organic farmers - and indeed society as a whole - should embrace pesticidal crops are a guilt-free alternative to synthetic pesticides. We will consider challenges to the following arguments, namely, that:

1. Pesticidal plants are "natural" and therefore, implicitly, "safer"
2. Pesticidal plants will displace insecticides, and hence, avoid the human health risks associated with insecticides
3. Pesticidal plants are the best way to control pests
 
 

1. Pesticidal Plants are "Natural"

Proponents are quick to point out - and rightly so - that plant-produced anti-herbivory compounds did not originate with genetic engineering (Table 1).

Indeed, a truly staggering range of self-defence compounds evolved in many higher and lower order species, whether it be the ubiquitous tannins (Robbins et al. 1987), saponins, and alkaloids, or the less well known endocrine disruptors discussed by Colborn et al. (1996). It is fair to say that chemicals have been and continue to be prominent in mediating relationships among organisms in nature, irrespective of human intervention.

So prevalent is herbivore deterrence via naturally-produced chemicals that some have contended that eating fruits and vegetables - the same ones being actively promoted as essential to human health - poses more risk to human health than pesticide residues (Ames and Gold, 1989). However, contrary to the extensive and continually expanding body of knowledge on the diverse health risks of synthetic pesticides (see Benbrook, 1996; Colborn et al., 1996; Garry et al., 1996; Porter et al., 1999), "there is, at present, no firm evidence to demonstrate a link between long-term ingestion of natural toxicants...and any type of chronic human illness" (quoted in Culliney et al., 1992).

Table 1. Brief overview of some naturally occurring anti-herbivory compounds found in crop species and fungi (adapted from Harborne, 1988; Culliney et al. 1992 and Cummins, 1998)
 
Type of toxicant Mode of Action Found in:
Proteinase inhibitors  Inhibits digestive enzymes, as trypsin and chymotrypsin; may be inducible in response to herbivore attack (as Colorado potato beetle on potato) Many species, including cereals and tubers and particularly the Leguminosae, e.g. legumes must be germinated (sprouts), fermented (tofu) or cooked to inactivate natural inhibitors before consumption
Lectins (also called phytohaemagglutinins) Proteins found in plants, fungi, bacteria, and animals that bind to sugars or glycoproteins, including coagulating red blood cells; also bind to the cells of the intestinal tract, reducing nutrient absorption; when present in high concentrations, some are toxic - causing immune system dysfunction and growth stunting Some legumes (as black beans, but not cowpeas) and cereals, slightly in tomatoes and fresh vegetables; destroyed by heat
Cyanogenic glycosides Convert to poisonous hydrogen cyanide (HCN) or prussic acid upon ingestion; act on the cytochrome system to inhibit respiration Cassava, seed of "bitter" almonds and peaches, lima beans, some Acacia sp., and herbage species, as sorghum, clover, and birdsfoot trefoil; "bitter" cassava must be washed and processed, by cooking or fermenting, to inactivate the enzymes and volatilize the cyanide
Alkaloids, as solanine and chaconine Solanine is a cholinesterase inhibitor, depressing nervous system function; alkaloids also have teratogenic effects on offspring About 20% of all angiosperm species, including potatoes, comfrey leaves, reed canarygrass, lupines
Oxalates Only harmful in presence of Na or K; only very high doses are toxic (e.g. plants with 10% or more oxalate as dry weight exhibit mammalian toxicity); diminishes absorption of Ca Spinach, rhubarb leaves, beet leaves, tea, and cocoa
Mycotoxins (fungal origin, not plants) e.g. ergot - St. Anthony's Fire; aflatoxins - liver carcinogen for pigs and cattle (not sheep) Fungal growth on cereals and nuts in storage

Nonetheless, with commendable dexterity, the same argument on the naturalness of chemical deterrents has since been reformulated to rationalize the safety of transgenic insertion of plant pesticidal compounds such as Bt or lectin, into crop plants. Because chemical deterrence is natural, it is reasoned that engineered deterrence is just mimicking nature - and that is a good thing, right? At least superficially, this is a plausible argument. But are they really the same? What distinguishes natural vs. synthetic deterrents to herbivory?

Natural vs. Synthetic: an example from endocrine-disruptors. The answer is simple: time. Evolutionary time, to be specific. Biological life has evolved in a kind of intricate, long-term dance of many competing partners. Each newly evolving screen or defence mechanism - often involving chemical deterrents - engendered a corresponding new resistance or response strategy, which in turn stimulated yet another defence strategy. The partners "knew" each other, and recognized each other's co-evolving chemistry over evolutionary time. But not so the synthetic interlopers. There hasn't been time.

To illustrate, consider the example of endocrine(2) disruptors - chemicals which through a variety of means are able to affect hormone balance in the bloodstream. Both natural and synthetic chemicals have now been identified as acting in a wide range of animals, including humans(3)

. Hormonal imbalance before and during pregnancy has been associated with a wide range of reproductive, immune system, and growth abnormalities in offspring (Colborn et al., 1996)(4).

Natural estrogens operate at extremely low concentrations - as in parts per trillion in the blood. However, synthetic estrogen mimics can occur in parts per billion or million, because they are not recognized and removed by the natural regulatory processes. Synthetic mimics cannot be dealt with properly because, in the words of Claude Hughes, a specialist in reproductive endocrinology at Wake Forest University, humans lack evolutionary history with them (cited in Colborn et al., 1996).

As a result, while natural estrogens are regularly broken down and excreted to maintain very low and physiologically appropriate concentrations, synthetic estrogens can accumulate, leading to chronic, low-level exposures. Chronic human exposure to blood estrogen levels thousands or millions of times higher than normal is without precedent in human evolution. The tragic implications of such exposure may be manifested intergenerationally, as discussed by Colborn et al. (1996), Garry et al., (1996), Repetto and Baliga (1996), and the USEPA (1997).

Thus, the premise that engineering synthetic pesticides into plants is "natural", because chemical deterrents to herbivory evolved naturally, is overly-simplistic.

But Bt is natural - not synthetic, right? Isn't a Bt-crop more environmentally friendly than chemical insecticides?

Wrong. It is fair to say that growing a Bt crop - particularly for crops which are highly dependent on deadly pesticides to control Bt-target pests - may reduce insecticide dependence (but see next section) - and hence, human health risk. But the ecological advantage of Bt crops, if any, remains to be seen.

Why? Because the "Bt" in genetically engineered crops is different from naturally occurring Bt. In effect, genetic engineering has transformed

Background. The endotoxin in Bt crops consists of a crystal protein toxin ("Cry" toxin) coded for by genes which have been isolated from Bacillus thuringiensis, a soil organism. According to Andow and Hutchison (1998), over 100 Bt Cry toxin genes may have been patented, but those active against lepidopterans such as corn borer, for example, appear to be limited to Cry1Ab, Cry1Ac and a few others. Other Bt Cry genes are active against colepterans (beetles) such as Colorado potato beetle, and dipterans such as mosquitos. Thus, it was believed that one could insert the gene(s) coding for specific toxins into crop plants, and act selectively against the target group.

However, the selectivity of foliar-applied Bt arises from at least two critical steps which are bypassed entirely in Bt-crops. The Bt in soil microbes exists as a protoxin, a precursor which is not insecticidal. It becomes activated (and insecticidal) only when a) ingested by an insect with the proper, alkaline intestinal pH, and b) specific enzymes are present to cleave the precursor into the active form, which then c) binds with receptor sites in the gut, leading to the death of the insect. In GMO applications, it is active endotoxin - not the precursor molecule - which is synthesized in the plant cells. Thus, the first two screening steps are absent, and the potential for non-target effects is increased.

Selectivity/Ecological Ramifications. Hilbeck et al. (1999) at the Swiss Federal Research Station for Agroecology and Agriculture demonstrated that the Bt in GMO crops behaves entirely differently from what would be expected from foliar Bt. A non-lepidopteran "prey" species - Spodoptera littoralis (Egyptian cotton leafworm) - was fed on either Cry1Ab protoxin or activated Cry1Ab toxin (as Bt-corn). Neither mortality nor weight of the non lepidopteran prey individuals were affected at any level of protoxin, as would be expected of a product selective for lepidopterans. However mortality rate doubled and weight of surviving individuals was reduced at the highest level of active endotoxin - which should not have happened in a non-lepidopteran species.

The active Bt-fed and protoxin-fed prey larvae were in turn fed to a non-target, non-lepidopteran predator species, Chrysoperla carnea, which is an important biocontrol agent in many agricultural systems. Neither mortality nor development were adversely affected when the C. carnea predator was fed protoxin-fed prey larvae. However, mortality was increased and the percent success in developing through each life stage was reduced when the diet consisted of Bt-corn fed prey larvae.

The tri-trophic study of Hilbeck et al. (1999) challenges the claim that Bt crops retain the selectivity of foliar Bt. In essence, if validated over a wider range of organisms and conditions, these findings suggest a loss of selectivity in transgenic vs. natural Bt applications. The study further suggests the potential for adverse ramification out into the wider ecosystem - analogous to what happens with bioaccumulative pesticides.

Persistence. One reason why decades of foliar Bt applications on organic and IPM operations has generated so little resistance in target organisms is because the Bt organisms are short-lived in the aerial environment. Foliar applications are vulnerable to UV radiation, essentially eliminating their efficacy in as little as a week. Usage can thus be timed and targeted to specific pests, without risk of harm to non-target species at other times in the season. Again, GE-Bt is an entirely different proposition, because it must remain active - in every cell of every plant - throughout the season.

Stotzky and colleagues (Crecchio and Stotzky, 1998; Tapp and Stotzky, 1998; Saxena et al., 1999) have demonstrated that the Bt endotoxin, whether coming from crop residues or from root exudates can persist for at least 234 days bound to clay particles in the soil. Further compounding the exposure issue, Bt crops also exude the insecticidally active endotoxin from the root system during the growing season. Thus, the time duration of exposure of target and non-target organisms to the insecticidal properties of Bt is vastly prolonged in Bt-crops as compared to foliar Bt sprays. Risk/likelihood of development of resistance in target organisms is concomitantly greater.

In essence, the process of engineering insecticidal traits into crop plants has taken a product that was short-lived and selective in its native state and turned it into a product that mirrors the persistent, bioaccumulative, ramifying harms associated with chemical insecticides. Thus, justification that genetically engineered Bt is environmentally benign and safe because Bt is a natural product is unsound.
 
 

2. Insecticide Use Reduction

The evidence presented above challenges the premise that pesticidal plants are more natural, and implicitly less harmful to the environment than are synthetic pesticides. In fact, evidence of nontarget pest responses to genetically engineered Bt (see also Birch et al. 1999 for parallel findings with lectins) and persistence profiles in the soil suggest striking parallels between synthetic and plant pesticides.

But even discounting the naturalness premise, there could still be merit in the argument that pesticidal plants displace insecticide use and hence reduce risks to human health. At least on the face of it, this is a plausible and compelling argument. But how well does it stand up to scrutiny? Is insecticide use, in fact, reduced by growing Bt crops?

The ERS-USDA (1999) published a 3-year study of yield and insecticide use data comparing GM and non-GM crops in various growing regions in the US. Results (5% level of significance) must have been unsettling to GMO proponents.

Reduced insecticide use for Bt target pests would be expected given that Bt is intended to replace chemical insecticides. However, the trend was different for the "other" pests of cotton. Table 2. Insecticide use patterns for Bt- and non-Bt-cotton in three regions in 1997.
 
 
Insecticide Acre-Treatments for Bt-Cotton in 19971

                            For Bt Target Pests          For All Other Pests            % Diff.
                            Bt   NonBiotech                   Bt    NonBiotech
Mississippi Portal           0.54*  1.27                   8.19*  4.43                    + 85
Southern Seaboard            0.31*  1.95                   2.19   1.37                    + 60
Fruitful Rim                0.63   0.60                  3.19   4.14                    - 23
MEAN                         0.49   1.27                   4.52   3.31

SUM: For Bt cotton:  5.01 acre-treatments vs. For Non-Bt cotton:  4.58 acre-treatments

1An "acre-treatment" is the number of different active ingredients applied per acre times the number of repeat applications. A single treatment containing two ingredients is counted as two acre-treatments, as is two treatments each containing a single ingredient.

This pattern is quite consistent with insecticide-induced secondary pest outbreak, as non-target species multiply to occupy the niche vacated by elimination of the target organisms. This is an entirely predictable outcome - as has been amply demonstrated with chemical pesticides (see Benbrook, 1996). This is just one illustration of the kinds of adverse ecological and agronomic impacts GM-insecticidal crops are expected to have.

It should also be noted that while insecticide use was significantly reduced for Bt corn, the reduction was from 0.07 to 0.00 acre-treatments. Control of European cornborer (ECB) - the target pest of Bt-corn -l accounts for only 1-2% of all the insecticide applied to corn (Table 3).

Indeed, insecticide is rarely applied to corn to control ECB, in part because ECB outbreak is sporadic and unpredictable, making insecticide use impractical and uneconomic. Almost all of the insecticide used on corn is for corn rootworm and other soil pest control. Thus, whatever savings in insecticide use accrue to growing Bt-corn will have a negligible effect on overall insecticide use - and hence, risk to human health - from insecticide use on corn.

The evidence provided by the ERS-USDA (1999) for insecticide usage patterns is suggestive, but not conclusive. Data are reported in acre-treatments rather than in active ingredient, and are presented only for 1997. Nonetheless, these findings are consistent with those of independent (not industry-funded) sources (e.g. Duffy and Miller, 1999), and do not support the premise that growing pesticidal crops meaningfully reduces risks to human health from insecticides.

Indeed, it could not be otherwise, given the choice of target pests (e.g. ECB, which is a virtual non-issue in terms of pesticide usage) and the multiplicity of pests attacking conventionally grown crops, of which only 1 or 2 are targeted by the engineered genes. This conclusion may change in the future, as other crop types come on the market (e.g. Bt corn targeting corn rootworm), but for now, the promise of reduced insecticide use has yet to be realized.

Table 3. Insecticide uses for corn in the US - 1998 (adapted from USDA National Agricultural Statistics Service (http://www.usda.gov/nass/pubs/rptscal.htm, courtesy Chuck Benbrook, personal communication)
 
Insecticide % of 71.4 million ac treated in the US Target Pest
bifenthrin 2 rootworms, soil insects
carbofuran 1 ditto
chlorethoxyfos 1 ditto
cyfluthrin 3 ditto
dimethoate 1 possibly European cornborer (ECB)
fipronil 1 rootworms, soil insects
fonofos 1 ditto
lamba-cyhalothrin 2 some for ECB; mostly soil insects
methyl parathion  1 rootworms, soil insects
permethrin  2 possibly partly for ECB
tebupirimiphos 3 rootworms, soil insects
tefluthrin 5 ditto
terbufos 6 ditto

 

3. Pesticidal Plants are the "Best" Way

Evidence has now been presented to challenge the first two premises, namely, that the ubiquitous presence of naturally evolved chemical defences somehow confers safety and naturalness to engineered pesticidal plants, and secondly, that relying on pesticidal plants will necessarily reduce dependence on hazardous insecticides. But is there really any other option? The argument has been framed as "chemicals vs. biotech", which is certainly a win-win argument for the companies that produce and market both options. What about, for example, neither?

What is organic farming? Defining "organic farming" as "farming without chemicals" has led some to presume that pesticidal plants are "different", and should be "allowed" in organic farming, because the pesticide is not synthesized in a lab. This kind of definition really misses the point of organic farming. To an organic farmer, avoidance of agri-chemicals reflects not simply a distaste for the hazards of chemicals but more centrally, a rejection of the linear thinking which underlies the use of the chemicals. And as shown above, there is nothing that personifies linear thinking better than genetic engineering.

Controlling pests with an insecticide is dealing with symptoms rather than causes, rather like putting a band-aid on skin cancer. The insecticide is no more effective than the band-aid, because the weeds or bugs come back, as does the cancer. In addition to being ineffective, insecticidal band-aids have not one (the linear assumption) but many effects (holistic reality), including shifting pest populations to favor resistant species and biotypes; non-target effects on other organisms; and in the case of GM pesticidal plants, an increase in the level of active endotoxin (pesticide) in the harvested grain.

The single most defining element in organic farming is that it is designed to avoid problems rather than to solve them after the fact. To illustrate, consider how a pair of conventional and organic farmers might view a weed outbreak. Whereas the conventional farmer it likely to take a linear view - a patch of weeds is the "problem" and eradication is the "solution" - the organic farmer would likely view the same weeds not as a problem, per se, but as an indicator of a larger system dysfunction. Where the conventional farmer would act to control the weed using one of the few tools left on a specialized farm - an herbicide - the organic farmer would investigate what s/he has done to open up the niche which has allowed the weed to proliferate in the first place. The solution then is not just a short-term kill of the weeds, but system design to deny the niche to achieve longer term benefit. Denying the niche may involve alleviating soil compaction or including an aggressive winter cereal in the rotation, or withholding compost application - all serving to disadvantage the weeds.

Likewise, an organic farmer would not be inclined to grow the simple corn-soybean rotations which are common in southern Ontario. Why? Not because of adherence to some philosophical dogma but because corn and soybean are warm season, wide row crops. Growing these crops repeatedly opens up a niche for spring-vigorous weeds, and the niche is wide in both space and time, because a) planting of both crops has to be delayed until the soil warms up, and b) it is many weeks before either crop attains full cover, making it an effective deterrent to weed growth. Perhaps this is why corn and soybean, while occupying just 36% of the cropped land in Ontario accounted for 84% of the herbicide active ingredient applied to field crops (Clark and Poincelot, 1996).

Alternatives to Bt-corn? An issue which seems to have been lost in the flurry of Bt-crop offerings is consideration of how crop management practices have created the niche which has allowed European cornborer to become pestiferous in the first place. Just as growing simple corn-soybean rotations has created a wide niche for spring-vigorous weeds - and hence, the demand for herbicide-tolerant corn and soybeans - so too with European cornborer (ECB). An alternative approach would seek to deny or close the niche which has created favorable conditions for ECB proliferation. Both nutrient and residue management are critical niche determinants:

Naturally occurring chemical deterrence may also be an option. Miller (1999) described work by Bradley Binder, a chemical ecologist with the USDA. Binder has identified a line, B-96, which carries chemical traits such as HMBOA, which deters egg-laying, and DIMBOA which deters feeding by cornborer larvae. Other approaches, as with pheromone traps, also offer promise.

So, let us disabuse ourselves of the notion that the only solutions are chemicals or biotechnology. Other options - system options - exist. Indeed, the reality of "other options" poses an enormous threat to the purveyors of biotechnology, because it provides producers with a way out of their current dependent state. This, more than anything else, accounts for the upswing in anti-organic press, news reports, and TV programs in recent months. Organic farming has now achieved sufficient success and prominence to be a "threat". Congratulations!
 
 

Conclusions

Pesticidal crops, such as Bt-corn, have been presented to the public, and to farmers in particular, as an environmentally benign alternative to chemical sprays. It is noteworthy that those making the most of this argument are the same companies that have defended for decades the safety of chemical sprays for pest control. The writing is clearly on the wall, for all to see:

Evidence has been presented to dispute the central planks of this confident platform. The arguments are flawed, because they fail to encompass the whole of the story. Plant-produced pesticides are not inherently benign to humans, livestock, or wildlife, because we have not shared a common evolutionary history. A diet where every bite of sweet corn or mashed potatoes contains active Bt endotoxin is without precedent in human evolution. Does it matter that every kilo of gain or liter of milk from fed cattle is derived from grain with the same raw endotoxins? And what of the soil, to which their manure is applied, year after year? Have we even begun to ask these really critical questions?

Pesticidal crops show every likelihood of expressing the same ecologically ramifying risks as synthetic sprays - but arguably worse, because they are alive and can transfer traits to other organisms. Pest communities are dynamic and maleable, and have proven time and again their remarkable capacity to adjust and re-occupy niches vacated by the use of specific insecticides. Crops engineered to produce their own insecticides appear to pose the same, negligible obstacles for pest communities to surmount. Indeed, pesticidal crops appear to be adding to, rather than subtracting from, the reliance on pesticides.

Replacing a chemical spray with an purchased biocontrol agent does not an organic farm - or an organic research program - make. The key to organic farming is not substituting biological for chemical controls, but adopting an holistic system design which captures ecological synergies within a strategically chosen mix of enterprises. Specialized organic farms are just as vulnerable to the environmental hazards of linear system design as any specialized conventional farm. To a remarkable extent, the problems addressed by current GMO offerings are self-induced, by the way we grow the crops. Attention to the issue of pest niche creation, rather than pest control, is the only way to commercially produce wholesome foodstuffs, free of the taint of pesticidal products.
 
 



References
 

Ames, B.N. and L.S. Gold. 1989. Pesticides, risks and applesauce. Science 244:755-757.

Andow, D.A. and W.D. Hutchison. 1998. Ch. 3 B-Corn Resistance Management. In: M. Mellon and J. Rissler (eds) Now or Never. Union of Concerned Scientists. 150 pp.

Benbrook, C.M. 1996. Pest Management at the Crossroads. Consumers Union, Yonkers, NY.

Birch, A.N.E., I.E. Geoghegan, M.E.N. Majerus et al. 1999. Tri-trophic interactions involving pest aphids, predatory 2-spot ladybirds and transgenic potatoes expressing snowdrop lectin for aphid resistance. Molecular Breeding 5:75-83.

Clark, E. Ann and R.P. Poincelot (ed) 1996. The Contribution of Managed Grasslands to Sustainable Agriculture in the Great Lakes Basin. Haworth Press, N.Y.

Colborn, Theo, Diane Dumanoski, and John Peterson Myers. 1996. Our Stolen Future. Plume/Penguin Books, New York.

Crecchio, C. and G. Stotzky. 1998. Insecticidal activity and biodegradation of the toxin from Bacillus thuringiensis... Soil Biol. & Biochem. 30:463-470.

Culliney, T.W., D. Pimentel, and M.H. Pimentel. 1992. Pesticides and natural toxicants in foods. Agriculture, Ecosystems and Environment 41:297-320.

Cummins, J. 1998. Questions and Answers on Lectins (internet communication; jcummins@julian.uwo.ca)

Duffy, M.and L. Miller. 1999. 1998 Crop survey shows equal returns for GMO, non-GMO crops. http://www.leopold.iastate.edu/9-22-99gmorel.html

ERS-USDA. 1999. Genetically Engineered Crops for Pest Management(www.econ.ag.gov/new-at-ers)

Garry, V.F., D. Schreinemachers, M.E. Harkins, and J. Griffith. 1996. Pesticide appliers, biocides, and birth defects in rural Minnesota. Environmental Health Perspectives 104(4).

Harborne, J.B. 1988. Introduction to Ecological Biochemistry. 3rd Ed. Academic Press, London, 356 pp.

Hilbeck. A., W.J. Moar, M. Pusztai-Carey, A. Filippini and F. Bigler. 1999. Prey-mediated effects of Cry1Ab toxin and protoxin and Cry2A protoxin on the predator Chrysoperla carnea. Entomologia Experimentalis et Applicata 91:305-316.

Johnson, G. 1998. Arizona Department of Agriculture, IPM Cotton/Organic Specialist. Personal communication.

Martin et al. 1989. J. Econ. Entomol. 82:1455-1459.

Miller, D. 1999. A trait for the future. Progressive Farmer (Jan 1999) (http://progressivefarmer.com/commodities/0199/corn/index.html)

Phelan, P.L., K.H. Norris, and J.F. Mason. 1996. Soil-management history and host preference by Ostrinia nubilalis: evidence for plant mineral balance mediating insect-plant interactions. Environmental Entomology 25(6):1329-1336.

Porter, W.P., J.W. Jaeger, and I.H. Carlson. 1999. Endocrine, immune, and behavioral effects of aldicarb (carbamate), atrazine (triazine) and nitrate (fertilizer) mixtures at groundwater concentrations. Toxicology and Industrial Health 15:133-150.

Repetto, R. and S.S. Baliga. 1996. Pesticides and the Immune System: the Public Health Risks. World Resources Institute, Washington, D.C

Robbins, C.T., T.A. Hanley, A.E. Hagerman et al. 1987. Role of tannins in defending plants against ruminants: reduction in protein availability. Ecology 68:98-107.

Saxena, D., S. Flores, and G. Stotzky. 1999. Insecticidal toxin in root exudates from Bt corn. Nature 402:480.

Tapp, H. and G. Stotzky. 1998. Persistence of the insecticidal toxin from Bt subspecies kurstaki in soil. Soil Biol. & Biochem. 30:471-476.

USEPA. 1997. Special Report on Environmental Endocrine Disruption: An Effects Assessment and Analysis. EPA/630/R-96-012. Risk Assessment Forum, USEPA, Washington D.C.

USGS. 1996. Pesticides in the Nation's Water Resources: Initial NAWQA Results.
 


Footnotes

1. Plants which synthesize their own "pesticide" include Bt-crops (e.g. Bt-corn targets European cornborer; Bt-potato targets Colorado potato beetle; and Bt-cotton targets pink bollworm) and others, such as the snowdrop lectin engineered into the famous Pusztai potatoes.

2. Endocrine glands include the reproductive organs, pancreas, adrenals, pituitary gland, thyroid, parathyroid, and thymus, each of which produces hormones to regulate such processes as reproductive development, energy metabolism, and the immune system

3. At least 51 chemicals have been identified as having endocrine-disruptor properties. Included in the list are DES (diethylstilbesterol), DDT, PCBs (209 compounds), dioxins (75), and furans (135) (Colborn et al., 1996), as well as 5 herbicides (including 2,4-D), 11 insecticides , and 6 fungicides (Benbrook, 1996). However, many naturally occurring hormone mimics also exist - such as the phytoestrogens in soybean and red clover. Natural hormones in giant fennel, wild carrot, and pomegranate have been used since historic times for control of human reproduction (Colborn et al., 1996).

4. In a 4 year study involving close to 211,000 births in Minnesota, incidence of birth defects was related to both region of crop production/intensity of biocide use, and parental background (pesticide applicator > general population) (Garry et al., 1996). A significant increase in defects was found for children conceived in the spring in the region with highest biocide use intensity. In an unrelated study, the USGS (1996) found that highest levels of biocides occurred in seasonal pulses in the spring lasting from a few weeks to a few months following field application of biocides. Peak levels during pulse intervals frequently exceeded USEPA drinking water standards in some agricultural zones. The coincidence of above-threshold pulses of biocides in water in the spring and the propensity for birth defects in children conceived in the spring is consistent with the action of some pesticides as endocrine disruptors

5. HT = herbicide tolerant, as Roundup Ready (RR) or Liberty Link (LL)

6. As recently as 1995, the joint federal-state Boll Weevil Eradication Program (BWEP) applied up to 15 applications of insecticide to control boll weevil on cotton in an 81,000 ha region of Texas (Benbrook, 1996). The project was a success, in that boll weevils were controlled. But as a result of this farmer-driven, governmentally sanctioned process, populations of cotton aphids, beet armyworm, and sweet potato white flies exploded, reducing cotton yield within the spray zone by 80%. A team of ARS-USDA (Agricultural Research Service-United States Department of Agriculture) scientists was charged with determining what went wrong in the sprayed BWEP zone - as compared with the normal yields experienced in surrounding areas. They concluded "the (data) overwhelmingly implicate heavy pesticide usage as the primary causal factor for dramatic differences observed in pest and beneficial insect complexes. Furthermore, these differences were primarily responsible for the catastrophic crop losses experienced" (USDA, 1995, cited in Benbrook, 1996). The ongoing BWEP is still in operation in various southeastern states.

©2000 E. Ann Clark. This text is the property of the author, E. Ann Clark. It may be downloaded or reproduced in whole or in part by any member of the academic community for the purposes of discussion, debate and quotation and may be placed on web sites or on chat lines so long as this copyright notice is included. It may be reproduced on the Internet so long as no charges are levied for its use. It may not be reproduced for sale in any form anywhere without the express written permission of the owner.