We all want to eat foods that are free from, or at least low in, allergens, carcinogens, genetic toxicants, birthdefect-causing chemicals (teratogens), endocrine disruptors and the like. Yet we are living in odd times with regard to minimising human exposure to potential toxicants in crop foods. Governments are far more effective at implementing politically correct programmes on toxicants than implementing scientifically strong programmes. This inattention to science has led to a remarkable double standard in the testing and regulation of potential toxicants in foods. An unintended consequence of the double standard is an increase in the risk of exposure to some potentially toxic chemicals—but not the ones you thought. Potential toxicants in crop foods come from three main sources: (1) plant-made self-protection chemicals (“natural pesticides”); (2) fungal contamination and fungal toxins; (3) synthetic-pesticide residues. Plant self-defence is accurately described in the popular novel Prey, by Michael Crichton (p. ix, 2002): “And we do not ordinarily imagine the green world around us as a scene of constant, sophisticated chemical warfare, with plants producing pesticides in response to attack, and insects developing resistance.” Another statement explains why so many natural toxicants are quite potent: “Some people talked of evolution as an arms race, by which they meant an ever-escalating interaction. A plant attacked by a pest evolves a pesticide in its leaves. The pest evolves to tolerate the pesticide, so the plant evolves a stronger pesticide. And so on.” (p. 250). Sodium monofluoroacetate, commonly known as 1080, is an example of a toxin that some Australian and South African plants produce to deter herbivores. It is also reportedly found in low concentration in tea leaves. Animals native to Western Australia are highly resistant to the toxin, but it is a used as a poison there effective against introduced pest animals. The risk of harm from chemicals in foods, although generally low in developed countries, is posed predominantly by natural pesticides and fungal toxins rather than by residues of synthetic pesticides. This is because of the much larger quantities of natural pesticides in foods than of synthetic pesticides, and the fact that natural pesticides and fungal toxins are not designed by nature to be safe for human consumption. A single commonly occurring natural pesticide can be present in foods at levels ranging from just a few ppm to hundreds of ppm (1 ppm = 1 mg pesticide/kg food). Because a plant must be prepared for many kinds of attack, it is usually equipped with many natural pesticides. In contrast to natural pesticides, residues of synthetic pesticides in foods (including imports) in the United States in 2003 were below the limit of detection in about 50 per cent of foods sampled. When synthetic-pesticide residues were detectable, levels were typically a small fraction of 1 ppm. Furthermore, only 24 per cent of foods contained residue of more than one pesticide. Similar analytical results have been obtained in New Zealand, residue levels, when detected, being typically very low, and about 40 per cent of samples tested having no detectable levels of pesticides (Cressey et. al., 2000). Good crop protection through the proper use of synthetic pesticides and biotechnology-derived pesticides can significantly reduce our exposure to food toxicants. Adding a tiny amount of synthetic pesticide can reduce our exposure to larger amounts of natural allergens, carcinogens, genetic toxicants and the like. The explanation for the safety benefits of good crop protection is conceptually simple. Plants cannot evade attackers. When plants are attacked by insects and fungi, they respond by making large amounts of self-defence chemicals, and the fungi produce fungal toxins. The technical details of how plants respond to attack are well-explained by Karban and Baldwin (1997). Small amounts of synthetic pesticide protect crops, saving them from making greater amounts of natural toxins. The magnitude of chemical self-defence can be considerable. Consider a couple of examples. Furocoumarins are a class of natural pesticides found in carrots, celery, dill, parsley, parsnips, grapefruits, lemons, limes, oranges and potatoes. Excessive exposure to plant-made furocoumarins is associated with light-induced skin irritation and blisters. Furocoumarins are also toxic to genes, and are thought to cause skin cancer in some people. In a landmark study on crop stress, furocoumarin levels were 3.3 ppm of dried root in uninfected greenhouse-grown parsnips and 20 ppm in fungicide-treated farm-grown parsnips. In contrast, fungal infected greenhouse-grown parsnips had furocoumarin levels of up to 394 ppm of dried root. Thus, fungal infection resulted in furocoumarin levels over 100 times greater than in uninfected greenhouse parsnips and nearly 20 times greater than in fungicide-treated farm-grown parsnips. These are truly major increases in a natural toxicant due to fungal infection, although in practice it is likely that the most severely damaged roots would be culled. As an aside, most natural toxicants are located in a plant’s skin, and particularly at the site of insect and fungal attack. When fungal-damaged areas of parsnips were cut out, along with a 1cm buffer zone of healthy root, furocoumarin levels were reduced by about 50 per cent. This little bit of information has modified my behaviour. Before, if I didn’t throw out damaged fruit and vegetables, I excised the damaged portions with surgical precision. Now I cut out a major swath of healthy-looking tissue along with the damaged portion. Wide excision is another way to reduce exposure to natural toxicants. Glycoalkaloids are another good example of damage-induced plant self-defence chemicals, found in potatoes, green tomatoes, eggplants and green peppers. Potato glycoalkaloids are perhaps the most thoroughly studied of the natural toxicants in foods. Excessive exposure can cause vomiting and diarrhoea, while especially high doses can induce neurological effects. Average background levels of potato glycoalkaloids are readily increased five- to twentyfold by a variety of stressors such as tuber blight, while levels of several hundred ppm have been recorded in some individual potatoes. It is surprising how few people realise that greening of potatoes is not a good sign, being associated with elevated, possibly worrisome, levels of glycoalkaloids (see http://www. foodscience.afisc.csiro.au/spuds. htm). Green potatoes should be avoided. A plant’s self-defence chemicals clearly have to be potent enough to deter or kill its attackers or it won’t survive. This isn’t benign chemistry. When natural toxicants are tested in laboratory cell systems (in vitro) or in laboratory animals (in vivo), they cause a range of toxic effects, such as cancer, birth defects, endocrine effects, genetic toxicity and liver toxicity. Unfortunately for many people, when a plant is under stress, levels of some allergenic proteins are increased. These stress-induced allergens belong to a group of proteins called pathogenesis-response proteins. Physicians have expressed concern that selection of plants for natural insect resistance may inadvertently also select for higher levels of these allergenic proteins. Similarly, selection of food plants for disease resistance may inadvertently raise natural toxicants to worrisome levels. Fungi add another layer of complexity. When a plant is damaged by insects, fungi can more easily invade it. And many fungi make potent toxins (mycotoxins) that can cause mild to severe disease in humans and animals. The range of potential toxic effects from natural toxicants and allergenic proteins, coupled with high levels of exposure, should cause regulators to reconsider the role of crop protection in food safety. Unfortunately, a holistic approach to the regulation of toxicants in foods hasn’t even begun. Almost always, the arguments in favour of the use of synthetic pesticides and biotechnology-derived pesticides are agronomic and environmental. Good crop protection increases yield per hectare, which allows production of high quality and less expensive fruits and vegetables, while more food per hectare means less destruction of habitat. These are important and valid arguments, but they do not address the health and safety concerns of the public. The unheard argument is that concerning the food-safety benefits of synthetic pesticides and biotechnology-derived pesticides. Synthetic pesticides are used to augment the self-defence chemistries of a crop in order to minimise insect and fungal damage. When injury to plants is minimised, the plants reduce their manufacture of self-defence toxicants. And less fungal invasion means reduced exposure to fungal toxins. When natural toxicants in foods are mentioned, many people seek refuge in the idea that the body somehow differentiates between natural and synthetic chemicals and is somehow more tolerant of natural chemicals. Studies have shown this is simply not true. High doses of either natural or synthetic chemicals can make rats (and people) sick. All chemicals exhibit biological activity, and have toxic properties, based solely on their structure. The body doesn’t “care” about the origin of chemicals. Fortunately, the human body has substantial detoxification systems, presumably to allow us to eat plant foods high in natural toxins. These detoxification systems also handle synthetic chemicals. While evolution has acted to make natural pesticides more potent, synthetic pesticides are vigorously tested to ensure they are readily detoxified by the body. As a result, synthetic pesticides are commonly much less toxic than many natural pesticides and fungal toxins in food. The toxicity of both natural and synthetic chemicals depends on two factors: their potency, and how much of them gets into the body. In the case of natural toxicants, safety margins are often narrow. The importance of minimising exposure to natural toxicants can be appreciated by considering the large quantities to be found in foods. Beier and Nigg (2001, p. 132) wrote: “What is a large dose anyway?... synthetic pesticides and herbicides might be consumed at 60 µg (millionths-gram)/day and many natural compounds are consumed at 4.8–6 million µg/day. These numbers result in a natural pesticide potential of 80,000–100,000 times that of synthetic chemicals in the diet.” Herein lies the problem with the double standard on evaluation and regulation of the different toxicants in foods. A severe regulatory approach to modern crop-protection chemicals and biotechnology traits, coupled with a spotty and poorly coordinated approach to management of natural toxicants, inevitably leads to a bias against synthetic pesticides and biotechnology-derived pesticides. Data and publicity concerning synthetic pesticides are abundant, while data and public knowledge concerning natural toxicants are minimal. The immediate consequence of this bias is, on the one hand, a continuously escalating regulatory threshold for the development and use of potentially effective man-made pesticides, and, on the other, very low or non-existent regulatory requirements for the development of “naturally resistant” food plants and for agricultural practices that minimise the use of modern pesticides. The bias against synthetic pesticides has also stunted public understanding of the safety benefits of good crop protection and of the reality of natural food toxicants and fungal toxins. This is unfortunate because the amounts of natural toxicants and allergens in our food could be largely controlled, but control cannot be optimised in the absence of good science and open dialogue. As early as 1966, then again in 1973, the National Academy of Sciences of the United States produced a book on natural toxicants in foods, stating: “Several considerations have prompted the writing of this report. Perhaps the main one is the hope that it may contribute to a more informed, realistic, and sensible attitude on the part of the public toward the food supply.” (p. 2); and: “On a worldwide basis various substances in categories 1 [natural components] and 2a [natural contaminants and toxins] have produced greater known injury to man than have those in the other categories...groups 3 to 6 [agricultural chemicals, food additives and packaging] are not known to have been responsible for adverse effects on human health when such materials have been used in accordance with good agricultural and manufacturing practices.” (p. 573). In 1995, Speijers wrote in a scientific paper: “Although the awareness that natural compounds in foodstuffs can have implications for human health is growing, there is a lack of data on the toxicology and occurrence...Of most inherent plant toxins at best only limited toxicological data are available, which makes it impossible to perform accurate safety evaluation. This limited knowledge of inherent plant toxins permits the mystical claim of safety on the basis of history of food use, and thus the development of specific food safety regulation has been postponed...As long as nobody is held responsible to study safety aspects of inherent plant toxins, the lack of data will persist.” One of the most useful sources of information on natural toxicants in foods is the article by Beier and Nigg (2001) with 1015 references. The authors’ concerns and conclusion: “There are no guidelines or regulations regarding naturally occurring toxicants in food...Do we know what we have placed in the marketplace? We do not. New food varieties traditionally are placed on the market with no toxicological testing. We have always experimented with foods on ourselves.” (p. 136). “In our opinion, we need to identify human health hazards due to naturally occurring chemicals in food. Scientific progress in this new frontier will require hard thinking and new facts.” (p. 137). The goal for society should be to maximise food production from the limited arable land available and to minimise human exposure to all toxicants, natural and synthetic. An impediment to this goal is that while passionate arguments are made about public safety, and the need for further research and more regulation, where manmade pesticides in foods are concerned, regulatory bodies virtually ignore the presence, sometimes tens of thousands of times greater, of natural toxicants in foods. This dichotomy cannot be scientifically justified. It is my opinion that: Although in general our food supplies are quite safe, natural toxicants in foods occur in concentrations, and have toxicity profiles, that should be carefully considered with regard to food safety. Safety margins are often narrow. To be scientifically rational, the risk assessment on which pesticide safety regulations are based should cover natural toxicants. Neglecting natural toxicants can lead to unintended decreases in food safety. We should assess the risk posed by natural and by synthetic chemicals in foods in identical fashion. We should be aware that “natural resistance” to pests means some components of a plant exhibit significant bioactivity against living organisms. It is not prudent to develop food crops or to select cultivars for natural resistance without serious evaluation of the potential health consequences. We should consider that plants respond to attack, and that crops that are not well protected by pesticides are at risk of developing elevated levels of self-defence toxicants, allergenic proteins and fungal toxins. The goal of a safer food supply cannot be realised as long as the regulation of pesticides ignores the presence of naturally occurring toxins in food plants.
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