Herbicide Toxicity to Humans and Animals

Herbicides are generally not very toxic to humans or to animals, including mammals, birds, amphibians, and invertebrates, as well as to microbial organisms. There are some exceptions, however, notably paraquat, which is very toxic to humans. It is still used extensively in the United States1301 and many developing countries. A large epidemiological study suggested that the herbicides pendimethalin and EPTC may be linked with human pancreatic cancer.11311 Sulfonyl ureas, which comprise a large number of low-dose herbicides widely used in agriculture, are known to affect humans as they are used in medicine to treat Type 2 diabetes and other illnesses.1321 They act by increasing insulin release from the beta cells in the pancreas, and side effects such as incidence of hypoglycemia have been reported.

As early as 1976, the herbicide diquat was shown to have an adverse effect on body size and pigmentation of Xenopus laevis, the South African clawed frog (family: Pipidae; subfamily: Xenopinae). Moreover, when treated with diquat and the fungicide nabam, the deleterious effect was more pronounced.1331 More recently, the herbicide atrazine has been implicated in a number of reports demonstrating effects on animals as an endocrine disruptorJ341 Similarly, the formulated product containing glyphosate is widely known to affect amphibians.1341 Glyphosate formulation has been implicated in a synergistic effect with a trematode species on fish.I35) Survival of juvenile fish was unaffected by exposure to glyphosate alone or by an infectious trematode parasite alone. However, simultaneous exposure to infection and glyphosate significantly reduced fish survival. Spinal malformations of juvenile fish were also enhanced when both stressors were present. A species of snail acts as the vector between the fish and the trematode. Glyphosate at high concentration killed all the snails, but at moderate concentrations, the snail produced more trematodes than in control and low-concentration groups.1351 This elegant experiment demonstrated the intricate interactions between different components of ecosystems.

Herbicides are categorized for their effect on unwanted plants, yet a number of them demonstrate toxicity to microbial organisms. A recent study revealed the control activities of glyphosate against rust diseases (Puccinia striiformis and Puccinia triticina) on glyphosate-resistant wheat and soybeans.1361 Control was equivalent to that of registered fungicides. Similarly, diquat was investigated for its potential to control the bacterial infection Columnaris disease (Flavobacterium columnare) affecting several fish species and was found to reduce Columnaris infection.1371

These findings demonstrate that herbicides can be directly toxic not only to plants but also to different types of life form at various trophic levels, including humans.

Toxicity to Plants and Effects to Terrestrial Habitats

Herbicides are especially designed to control weeds and therefore are of particular concern for unwanted effects on desirable plants. However, several types of pesticides can injure plants since pesticides are mostly classified by target organisms. For example, the widely used insecticides chlorpyrifos, diazinon, carbaryl, malathion and others can cause injury to several crops and ornamental species.1381 Several fungicides belonging to the benzimidazole chemical class were shown to be toxic to several plants.1391 Nevertheless, this entry will concentrate on herbicides.

Effects of herbicides on crops and weeds are well documented for obvious agronomic and economic reasons. Unwanted effects on native species is usually assessed through regulatory processes using crops as surrogate species (see below) and via studies performed sporadically by research scientists. By and large, herbicides affect native species at different levels. Herbicides can alter biochemical and developmental processes in plants as well as plant morphology. Habitats within agroecosystems can experience modifications in their species abundance, composition, and diversity when subjected to herbicides. Plants as terrestrial primary producers constitute the basis of terrestrial ecosystems. Herbicide effects on them can have cascading effects at other trophic levels, on overall biodiversity, and on ecosystem functions. These will be addressed in turn.

Effects at the Species Level

Herbicides can modify biochemical processes in plants and as a result can increase plant susceptibility to pests and diseases. Most of the work demonstrating these effects has been performed with crop plants, but there is no reason to believe that native plants would not be affected in the same manner. The incidence of mildew on spring wheat was enhanced by three different herbicides as a result of stress induced by metabolic interference.1401 Wheat treated with 2,4-D was higher in protein content resulting in a proliferation of aphids.1411 The concentration of nitrogenous compounds in crops was enhanced by sublethal doses of several phenoxy, triazine, and uracil herbicides,1421 sometimes leading to an increase in pathogens and pests on corn1431 and rice.1441

Symbiotic processes with plants such as nodulation and mycorrhizae, which are vital for the biochemical activities of most terrestrial plants, can be greatly modified by herbicides. Nodulation and nitrogen fixation was disrupted by herbicides resulting in deleterious effects on growth and reproduction in crops such as dry bean (Phaseolus vulgaris), soybean (Glycine max), broad bean (Vicia faba), and peanut (Arachis hypogea) (Schnelle and Hensley1451 and references therein). Mycorrhizal activities were affected by MCPA sprayed on (Pisum sativum) with ensuing decreases in growth observed.1461

Herbicides can exert anomalous effects on plant developmental processes. They have been shown to affect seed production and seed germination. It was demonstrated as early as 1948 that applications of 2,4-D caused a delay in seed germination and growth of wheat plants sufficient to favor an increase of wireworm damage.1471 It has been known for some time that when some of these herbicides are applied to cereal crops late in their growth stage, just before seed formation, the plants produced far fewer seeds. Greenhouse experiments recently revealed that at typically used rates, dicamba and picloram reduced all or nearly all seed production while 2,4-D was much less effective.1481 Further field test experiments supported these greenhouse results.1491

Research with glyphosate showed that depending upon the plant species, application rate, and the timing of application, effects on seed production, seed germination, and seedling development have been observed on a large number of plant species from various families.1501 Glyphosate produced an inhibitory effect on pollen germination and seed formation when applied at the flower bud stage of goldenrod (S. canadensis).1511 Germination, emergence, and plant establishment of native Australian plant species were impeded by the herbicide fluazifop-p-butyl.1521 Plants of Stellaria media treated with the herbicide glufosinate ammonium produced seeds with reduced germination and emergence.1531

Herbicides can instigate unexpected effects on plants that have not been studied as part of the registration package because they are not relevant from an agronomical viewpoint. Sulfonylurea herbicides are selective herbicides that act by inhibiting the enzyme acetolactate synthase, which catalyzes the synthesis of the three branched-chain amino acids valine, leucine, and isoleucine. They are very potent herbicides applied at exceedingly low doses, in the order of a few grams per hectare. When applied at the fraction of the recommended label rate at the onset of flower formation, however, they were found to reduce the reproductive outputs of several species with significant reproductive damage occurring with only scant visible symptoms on leaves. Cherry trees sprayed at doses as low as 0.2% of the field application rate of the sulfonylurea chlorsulfuron showed a significant reduction in the production of fruits, with almost no observable damage to vegetative parts.1541 Low doses of metsulfuron methyl produced important injury on the vegetative biomass when crop and native species were sprayed at the seedling stage, but plants sprayed at later stages showed considerable reduction in the reproduction.1551 Potato bulking was greatly affected by low rates of sulfometuron methyl whereas few visible symptoms were observed on the vegetative parts.1561 Under field situations, it was found that berry production in hawthorn (Crataegus monogyna Jacq.) was severely affected by average spray drift concentrations higher than 2.5% of the label rate of the sulfonyl urea metsulfuron methyl (0.1 g-ai/ha) and that the effect was still observed lyear after the spray event.157,581

Imidazolinones are another chemical family classified as low-dose herbicides. They also inhibit the enzyme acetolactase synthase and as such have been implicated in unforeseen effects. Potato (Solanum tuberosum L. from the Solanaceae family) tuber size and quality were most detrimentally affected by exposure to imidazolinone herbicides, as low as 0.1 times the recommended field rate, when exposure occurred during tuber bulking, as compared to exposure at seedling emergence or at tuber initiation.1591 While reductions in the weight and the overall yield of sensitive species were problematic, another major concern was the potential lowering of fruit quality, which could lead to significant economic losses in the case of crops.156,591 Effects on native species have not been investigated, but it is easy to stipulate that drift of imidazolinones to non-target habitats could elicit a reduction in weight of sensitive species, including effects on underground and reproductive parts. This may lead to species of the Solanaceae family and other families to produce fruits and storage organs that are less attractive to wildlife.

Damage to or modification of plant morphology, including epinasty, inhibition of leaf expansion, and stem and root distortion, has been reported in weeds and crops, particularly for phenoxy herbicides.1601 Herbicides can cause morphological deformation with unforeseen repercussions. For instance, it was possible to demonstrate that morphological deformations of the flowering parts in Arabidopsis thaliana (L.) Heynh. induced by some herbicides prevented pollination and seed production.1611 Bud and flower abortion has been reported for sulfonylureas (see above). Such effects, usually undetected, can have long term adverse impacts, particularly on monocarpic species.

Population/Community Level

Herbicide use in modern agriculture alters species abundance, composition, and diversity in non-target habitats. Effects of low doses of herbicides on plants (grown in pots and placed at different distances from the spray swath) have been reported.162,631 Marshall and Bernie1641 showed that several of the broadleaved species found in field margins were susceptible to the six different herbicides tested separately in pots. In the field, Marrs et al.1651 assessed effects of spray drift in relation to plant damage and yield for a range of plant species of conservation interest in Britain after applying each of six herbicides with a standard agricultural hydraulic ground sprayer. They observed lethal effects at 2-6 m from field edges and damage at greater distances, although damaged plants were able to recover within the growing season. Effects on seedlings were observed up to 20 m.1661 The long-term effect of such damage to plants remains unknown. In North America, work performed by Jobin et al.1671 showed that recurrent applications of herbicides had a long-term effect on plant populations inhabiting hedgerows and woodlot edges adjacent to crop fields. In Britain, several native arable weeds are considered endangered due to destruction of their habitats and extensive use of agrochemicals.1681

In the Netherlands, it was calculated that 9.5% of all pesticides applied was dispersed outside croplands.1181 Drift scenarios together with herbicide toxic effects investigated using bioassays and taking into account distances from spray events were used to estimate impact on biodiversity. In 2005, 41% of the linear landscape features near cropland were affected. This was an improvement since, in 1998, 59% of the area was affected. Natural areas located within farming regions were also affected by herbicide displacement in 31% and 11% of the area in 1998 and 2005, respectively. Measures in place such as unsprayed buffer zones and better equipment as well as reduced reliance on herbicides were largely responsible for this decline in unwanted effects on plant diversity. Also in the Netherlands, small plot experiments used to investigate the effects of the herbicide fluroxypyr on plants monitored for 3 years showed a decline in diversity and biomass.1691 Change in plant populations was also noticed.

Ecosystem/Trophic Level

Alterations by herbicides on primary producers through effects on morphology, physiology, phenology, species composition, diversity, and abundance can resonate considerably to other trophic levels. The best documented study implicating herbicide repercussions was conducted in Britain over several decades. The grey partridge (Perdix perdix) has been surveyed since 1933 in the margins of crop fields, and it was found that numbers declined by 80% between 1952 and the mid-1980s.1701 Studies conducted from the 1960s led to the conclusion that the use of herbicides and, to a lesser extent, insecticides precipitated the decline of grey partridge populations. Although partridges are largely herbivorous, newly hatched chicks feed largely on arthropods during the first 2-3 weeks of their lives. The falling number of grey partridges in agricultural land was attributed to declining chick survival early in the season due to weed removal by herbicides. A reduction in weed diversity and density on which insects feed and inhabit caused a food shortage at this very crucial period of the year.1711 Removal of field margins was also a contributing factor.

Many subsequent studies have shown that as a result of herbicidal effects, cover and diversity of flowering plant species are reduced in crop fields and field margins, thus subsequently reducing the resources available to flower- visiting insects and other arthropods.172-741 Likewise, abundant floral diversity was found to be the prevailing factor related to high Lepidopteran diversity in farmland habitats (Boutin et al.[751 and references therein).

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