Impact of Pesticide Use on Natural Enemies

Pesticides including insecticides and miticides are primarily used to regulate insect and mite populations in agricultural and horticultural crop production systems. However, continuous dependence on pesticides may eventually result in a number of potential ecological problems including resistance, secondary pest outbreaks, and/or target pest resurgence.11415! Therefore, implementation of alternative management strategies is justified in order to conserve existing pesticides and produce crops with minimal damage from insect pests. One option that has gained interest by producers is integrating pesticides with biological control agents or natural enemies including parasitoids and predators.1161 This is often referred to as “compatibility,” which is the ability to integrate or combine natural enemies with pesticides so as to regulate arthropod pest populations without directly or indirectly affecting the life history parameters or population. This may also refer to pesticides being effective against targeted insect pests but relatively non-harmful to natural enemies.117,181 Pesticides vary in their activity, which not only impacts how they kill arthropod pests but also how they may indirectly influence natural enemy populations. Pesticides may be classified as contact, stomach poison, systemic, and/or trans- laminar.119,201 In addition, the application method—foliar versus drench or granular—may determine the extent of any indirect effects on natural enemies1211 as well as the pesticide mode of action. The type of natural enemy-parasitoid or predator may be influenced differently based on the factors mentioned above. Furthermore, the type of pesticide may substantially contribute to any indirect effects on natural enemies. For example, broad-spectrum, nerve toxin pesticides such as most of the older pesticides in the chemical classes, organophosphate (acephate and chlorpyrifos), carbamate (carbaryl and methiocarb), and pyrethroid (bifenthrin and cyfluthrin) may be both directly and indirectly more harmful to natural enemies than non-nerve toxin-type pesticides (often referred to a “selective pesticides”) including insect growth regulators (kinoprene and pyriproxyfen), insecticidal soaps (potassium salts of fatty acids), horticultural oils (petroleum or neem-based), selective feeding blockers (flonicamid and pymetrozine), and microbials (entomopathogenic fungi and bacteria and other microorganisms).1221 The non-nerve toxin pesticides are generally more specific or selective in regards to arthropod pest activity with broader modes of action than nerve toxin pesticides.1161 The effects of pesticides on natural enemies are typically associated with determining direct effects such as mortality or survival over a given time period (24-96 hours).1231 While evaluations associated with the direct effects of pesticides on natural enemies are important, what are actually more relevant are the indirect or delayed effects of pesticides because this provides information on the long-term stability and overall success of a biological control program when attempting to integrate the use of pesticides with natural enemies.124-271 Any indirect effects, which are sometimes referred to as sublethal, latent, or cumulative adverse effects, may be associated with interfering with the physiology and behavior of natural enemies by inhibiting longevity, fecundity, reproduction (based on the number of progeny produced or eggs laid by females), development time, mobility, searching (foraging) and feeding behavior, predation and/or parasitism, prey consumption, emergence rates, and/or sex ratio.115,25,28,29-301

In apple ecosystems, many host species of phytophagous arthropods among which red spider mite and two-spotted spider mite are substantial worldwide. Predatory mites play an important role in checking the population of these mites. In India, the red spider mite Panonychus ulmi was a minor pest up to 1990, but the commercialization of apple led to excessive and repeated use of pesticides for quality apple production, as a result of which the natural mite predators were destroyed and it emerged as a serious pest of apples. Most of the spray schedules are now focused to this pest, further deteriorating the condition. Pyrethroids and carbamates, i.e., carbaryl (Sevin), are highly toxic to predatory mites, e.g., Typhlodromus occidentalis and use of Sevin for thinning causes mite flare-ups. Another well-known example is the resurgence of brown plant hopper (BPH) in rice ecosystem. If no pesticides are used, BPH is kept under control by its natural enemies (mirid bugs, ladybird beetles, spiders, and various pathogens). Since rice is a heavily sprayed crop, pesticides kill the natural enemies and create a situation where BPH can multiply rapidly. Thus, similar to P. ulmi, it has also become a serious man-made pest. Synthetic pyrethroids result in spider mite resurgence.1311 In a study conducted by Beers,1321 pyrethroids, carbamates, organophosphates, Assail, Calypso, and Actara are toxic to T. occidentalis and Zetzellia mali, which are mostly found associated with P. ulmi and other phytophagous mites. Organophosphates and carbamates are reported to cause high levels of mortality to coccinellids and lacewings.

Pesticide Use and Bt Transgenics

A common pest management technology used in agroecosystems is the use of Bacillus thuringiensis (Bt) transgenic. Bt crops, particularly cotton, are grown all over the world. Bt crops were mainly introduced with an aim to reduce pesticide use, but growing secondary pest populations and efforts to control them have further increased the use of pesticides The major cotton-growing countries, i.e., the United States, China, India, and Argentina have quickly adopted this technique for cotton seeds. For example, before the commercialization of Bt cotton, the Chinese farmers applied an average of 20 pesticide treatments in a season to control bollworm infestations. With the adoption of Bt, the average number of treatments has fallen to only 6.6 in the early stages of Bt adoption.1331 As a result, the pesticide use decreased by 43.3 kg/ha in 1999, i.e., a 71% decrease in pesticide use. For the years 2000 and 2001, Bt cotton was associated with an average reduction of 35.7 kg/ha of pesticide or a percentage deduction of 55%.|341 Similar results have been found in other major cotton-growing countries, and Indian farmers save 39% of expenditures by planting Bt crops.1351 Argentine farmers save 47% of expenditures,!361 Mexican farmers can save 77%,1371 and South African farmers can save 58% by planting Bt.|3S| Evidence shows that, though Bt seed costs 2 to 3 times more than a conventional seed, savings on pesticide expenditures guarantee a much higher net return for Bt adopters. Using a household survey from 2004,7 years after the initial commercialization of Bt cotton in China, we show that total pesticide expenditure for Bt cotton farmers in China is nearly equal to that of their conventional counterparts, about $101/ha. Bt farmers in 2004, on the average, have to spray pesticide 18.22 times, which are more than 3 times higher compared with 6 times the pesticide spray in 1999. Detailed information on pesticide expenditures reveals that, though Bt farmers saved 46% of bollworm pesticides relative to non-Bt farmers, they spend 40% more on pesticides targeted to kill an emerging secondary pest. These secondary pests, e.g., mirid bugs, were rarely found in the field prior to the adoption of Bt cotton, presumably kept in check by bollworm populations and regular pesticide spraying.

Cotton is attacked by more than 165 pests, and farmers repeatedly spray pesticides, which increase the chances of resurgence of secondary pests. In Andhra Pradesh, the number of attacks of aphids, thrips, and jassids has increased since the introduction of Bt cotton in 2002. Many diseases and pests such as tobacco leaf streak virus and tobacco caterpillars have newly emerged in Bt cotton ecosystems in this state.1111

Pesticide Use in Weeds

Herbicide should be applied at the time when their impact on weeds is highest. If preemergence weed control is optimized, the need for pest emergence measures may be reduced. The cultivation of genetically modified herbicide-tolerant crops has the potential to reduce herbicide inputs. The world sales of agrochemicals is dominated by herbicides (46%) followed by insecticides (26%), fungicides (23%), and others (5%).|M1 On the other hand, the Indian market trend indicates domination of insecticides (61.39%) followed by fungicides (19.06%), herbicides (16.75%), and others (2.80%).1401

The large-scale adoption of dwarf high-yielding varieties (HYV) and hybrids and the increased use of irrigation, fertilizers, and monocropping have increased weed problem in agro-horticultural ecosystems, simultaneously leading to increased herbicide use. Herbicides, such as isoproturon, atrazine, alachlor, buta- chlor, and oxyfluorfen, are applied on agro-horticultural ecosystems for control ofweeds. Globally, herbicides constitute 52% of the total pesticide sales, and in some countries such as the United States, Germany, and Australia, the figure is as high as 60%—70%.|4,l According to USDA-NASS (US Department of Agriculture- National Agricultural Statistics Service) report, the use of genetically modified crops is the main reason for the rise in herbicide use.1421 For example, widespread introduction of genetically modified soybeans, cotton, and corn by Monsanto resulted in a 15-fold increase in the use of glyphosate (Roundup) from 1994 to 2005 on these three crops in the United States. The excessive use of glyphosate has resulted in resistant weeds, as a result of which the application of glyphosate, atrazine, 2,4-D, and other leading weed-killing chemicals has further increased since 2002. 2,4-D, the second most heavily used herbicide on soybeans (after glyphosate) in the United States, is associated with a number of adverse health impacts on agricultural workers. These herbicides have increased the risk of cancer, have increased the rate of birth defects in children of men who apply the herbicide, and are also a suspected endocrine disruptor. Similarly, atrazine, the most heavily used herbicide on corn, has been linked to endocrine disruption, neuropathy, and cancer (particularly breast and prostate cancer). It is regularly detected in drinking water supplies in the United States and has been associated with low sperm counts in men. Exposure to extremely low levels of atrazine can cause sex change and/ or deformities in frogs, fish, and other organisms. Based on this evidence, and the widespread presence of atrazine in drinking water supplies, the European Union announced a ban on atrazine in 2006. However, the US EPA reregistered atrazine in 2003 despite objections from scientists and environmental groups.143! Cheaper formulations of herbicides containing 2,4-D and 2-methyl-4-chlorophenoxyacetic acid (MCPA) are still used in many countries, and weeds have developed resistance, e.g., in Bulgaria, 47% of wheat and barley crops were affected by 2,4-D-resistant weeds in 2000.1441

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