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REVIEW ARTICLE t Managing resistance is critical to future use of and

Frank G. Zalom Nick C. Toscano Frank J. Byrne t

Synthetic pyrethroids and neonicoti- noids are the most readily available alternatives to the and . Pyre- throids have become widely used in California, and problems with resistance and nontarget impacts have already been identi- fied. Neonicotinoids are a new class of insecticide with uses only now being realized. Managing insecticide resistance will be crucial to preserv- ing these new materials as organo- phosphate uses are lost.

nsecticides are often referred to as having a broad or narrow spectrum of activity,I depending on the diversity of pest species they kill. Narrow-spectrum insecticides are generally thought of as and insecticides have become important replacements for organo- being less disruptive to biological con- phosphates. UC Riverside staff research associate Greg Ballmer uses a micropipette to extract trol and more environmentally benign xylem from a grapevine in the Temecula Valley. because of their specificity to a few target pest species. In the presence of a complex unique and economically important In a recent report funded by the Cali- pest community, however, use of an in- components of California’s agricultural fornia Department of Food and Agricul- secticide with a high degree of specificity industry. California Department of Pes- ture (Metcalfe et al. 2002), pyrethroid and can require additional applications of ticide Regulation (DPR 2003) reports of neonicotinoid insecticides were identified products that target other taxa. OP usage for 2002 (the most recent data as the most likely alternatives to the OPs. The ability of organophosphate (OP), published) indicate that , Even before the OPs are withdrawn, organochlorine and methyl carbamate and are the most however, the number of applications of insecticides to control a broad range of widely used OPs, while and insects with a single application led to are the only two methyl carba- TABLE 1. Usage of organophosphate and methyl their widespread use for . mates used to any great extent (table 1). carbamate insecticides in California, 2002 With the cancellation of DDT by the The widespread use of these products U.S. Environmental Protection Agency has led to the development of pesticide Pounds a.i.* No. in 1973, followed by bans on the use of resistance in many insect populations Chemical (trade name) applied applications most other organochlorines, agricultural (Roush and Tabashnik 1990). Their use use of the OP and methyl carbamate has also raised concerns about surface- Chlorpyrifos (Lorsban) 1,446,547 36,802 Diazinon 689,603 31,757 insecticides became dominant, with water contamination, resulting in the list- Malathion 619,811 14,653 more than 200 OP insecticides available ing of some California rivers as impaired (Imidan) 405,088 7,533 worldwide at their peak. waterways under the U.S. Clean Water (Cygon) 332,543 24,355 OPs and methyl are still Act. The U.S. Food Quality Protection Methyl carbamates widely registered for use on Califor- Act (FQPA) of 1996 has focused particu- Methomyl (Lannate) 321,476 17,216 Carbaryl (Sevin) 256,030 3,354 nia crops and have been regarded as lar attention on the human risks of ex- * Active ingredient. especially important tools for growers posure to OPs and has already imposed Source: DPR 2003. of vegetable and fruit crops, which are restrictions on their use (see page 7).

http://CaliforniaAgriculture.ucop.edu • JANUARY-MARCH 2005 11 these alternative insecticides is fast ap- in extracts from Chrysanthemum flowers proaching that of the OPs in California (Tanacetum [Chrysanthemum] cinerariae- agriculture (table 2). This is alarming, folium). Research to develop synthetic because it suggests that application of pyrethroids began in the 1940s to en- these materials will continue to increase, hance their efficacy, facilitate large-scale raising immediate concerns about the po- production and improve stability. Al- tential development of resistance. lethrin (Pynemin) was the first synthetic Although non-OP alternatives are al- pyrethroid to be developed and was ready available for most crops, phasing registered in 1949 for public health and out the OPs will require some adjust- urban uses, primarily against mosquitoes ment to current management programs and houseflies. This was considered a as suitable replacements among the first-generation pyrethroid, because it remaining insecticide classes are sought. was chemically similar to a component Pyrethroids are fast-acting insecticides of the natural extract. that kill a broad spectrum of insect Second-generation pyrethroids were pests. They are most often applied as registered in the 1960s to control ur- foliar sprays, by air or ground. For a ban insects. was about 20 number of crop uses, they are serving times more effective than pyrethrum as a direct substitute for an OP. All cur- for controlling houseflies and had lon- - rently registered neonicotinoids in Cali ger residual activity, but like allethrin Top, UC Riverside extension entomologist fornia agriculture are available as foliar was photolabile (containing molecules Nick Toscano examines a Coachella Valley formulations and compare favorably that break down quickly in light) and grapevine trunk for adult and nymph popu- with the OPs in terms of efficacy against therefore unsuitable for outdoor use. lations of vine mealybug, part of a field trial of various treatments. Above, vine mealybug specific groups of insect pests, impacts was the first synthetic pyre- damages grapevines, causing them to lose on natural enemies, and worker and en- throid with sufficient photostability for vigor and diminishing grape quality. vironmental safety. agricultural applications. Permethrin and became Pyrethroids increasingly popular the most widely used of the third- cally 10% of the third-generation rates). Pyrethroid insecticides are more stable generation pyrethroids and were The fourth-generation pyrethroids are analogs of the natural insecticides found particularly significant for their broad photostable and relatively nonvolatile, TABLE 2. Usage of synthetic pyrethroid and spectrum of insecticidal so their residual activity is longer than neonicotinoid insecticides in California, 2002 activity at relatively low that of earlier pyrethroids. rates, as well as their Efficacy and cost. Pyrethroids have Pounds a.i.* No. Common improved photostability, become the favored insecticide alterna- Chemical name applied applications agricultural uses which resulted in residual tives to the OPs for growers because in Pyrethroids activity of up to 1 week many cases, they are a direct substitute 47,443 5,646 Cotton, corn, strawberry, alfalfa on foliage. Permethrin in terms of the range of insects killed, (Pounce or Ambush) is treatment timing and residual activity. 57,524 10,258 Alfalfa, cotton, orange, corn still the most widely used Perhaps the only arthropod groups for and 306,291 8,326 Lettuce, cole crops, pyrethroid in California, which they are not as effective are soil (s)-cypermethrin onion, cotton and is commonly applied insects and mites, and certain insects 13,001 956 Greenhouse, nursery to leafy vegetables and with piercing-sucking mouthparts. The some tree crops. availability of pyrethroids continues to 30,758 24,623 Almond, cotton, artichoke, stone fruit A number of fourth- increase as more products are registered 34,525 4,012 Cotton, grape, generation pyrethroids for additional California crops, includ- strawberry, orange have been registered ing fruits and vegetables. In general, Lambda- 58,381 22,642 Alfalfa, lettuce, rice, during the past 20 years, they are cost-competitive as a direct ` tomato the most commonly substitute for the OPs and in some cases Permethrin 385,403 46,267 Lettuce, celery, used being esfenvalerate are even less expensive. spinach, almond (Asana) and lambda- Toxicity. In addition to efficacy and Neonicotinoids cyhalothrin (Warrior or cost, pyrethroids present a lower risk to 6,632 3,519 Cotton, lettuce, celery, Karate). Because they are workers and applicators, as indicated by pear more effective against oral and dermal LD50 data (table 3). LD50 224,730 41,924 Lettuce, grape, cotton, insects at lower dosages is the dose that kills 50% of test animals cole crops than the third-generation to which a product is administered and 11,091 2,826 Cotton, tomato, pyrethroids, these con- is expressed as milligrams per kilogram melon, pepper temporary pyrethroids of body weight. Pyrethroid toxicity to * Active ingredient. Source: DPR 2003. are generally applied at amphibians, mammals and birds is much lower rates (typi- relatively low compared to the OPs;

12 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1 Perhaps the most immediate insect-control problem for California agriculture will not be finding a suitable replacement for the organophosphates, but rather to delay the onset of and manage pest resistance to the pyrethroids and neonicotinoids that are replacing them. however, most aquatic invertebrates and are generally not compatible with bio- ity, nithiazine was not made commer- fish are highly susceptible (Smith and logical control programs. They also tend cially available due to its photolability. Stratton 1986). Acute toxicity expressed to persist for longer periods in the envi- Efficacy and cost. The efficacy of as 96-hour LC50 values (the concentration ronment and can be especially disruptive the neonicotinoids both as persistent lethal to 50% of a group of organisms when used in perennial crops. Pyrethroid systemic treatments and as less- within 96 hours) for esfenvalerate to use has been associated with outbreaks persistent foliar sprays offers excep- juvenile fish was reported at 0.25 mi- of secondary pests such as spider mites tional flexibility that is similar to that of crograms per liter (µg/L)(Werner et al. in orchards both during the season in some OPs. For example, imidacloprid

2002), while the respective 96-hour LC50s which they are applied and possibly in is currently available for systemic, seed, of diazinon are as much as 1,000-fold subsequent seasons (Bentley et al. 1987). soil, chemigation (applied via the ir- higher (EXTOXNET 2003). Molluscs are This will lead to increased use of miti- rigation system) and foliar applications. relatively insensitive to both OPs and cides and other chemical pesticides in The systemic activity of neonicotinoids pyrethroids, but have been shown to order to control these outbreaks. enables their integration into California bioaccumulate these chemicals, thereby agriculture as a satisfactory alternative to Neonicotinoids more selective representing a potential hazard to higher the OPs for the control of sucking insects, trophic levels within the food chain. There are four neonicotinoid in- as well as some Coleoptera (beetles) Water quality. The off-site move- secticides (synthetic chemicals based and Diptera (flies). However, the neo- ment of pyrethroids, a concern with the on the structure of nicotine) cur- nicotinoids will not control some insect OPs in California surface waterways, is rently registered for agricultural use orders — such as the Lepidoptera — as generally believed to be minimal due to in California — acetamiprid (Assail), effectively as the OPs, preventing their their hydrophobic chemical properties imidacloprid (Admire or Provado), thia- direct substitution for OPs and pyre- and generally high soil-adsorption coef- cloprid (Calypso) and thiamethoxam throids in many cases. This charac- ficients, which indicate that they will (Platinum or Actara). is teristic of neonicotinoids is good for bind to surfaces they come into contact registered in California for flea control resistance management in that growers with rather than run off. However, data in cats and dogs. Others are under de- must utilize other available chemistries has recently been collected that found velopment. for some species rather than relying permethrin, esfenvalerate, bifenthrin and Imidacloprid was introduced in 1991 solely on one insecticide class for con- lambda-cyhalothrin in 75%, 32%, 25% as the first commercially available neo- trolling all insect pests. One limitation and 12%, respectively, of sediment sam- nicotinoid and is by far the most widely is their cost, which tends to be much ples taken from surface-water bodies in used (table 2). Like all neonicotinoids, higher than either OPs or pyrethroids. California’s Central Valley (Weston et al. it is a remarkably potent neurotoxic Toxicity. Neonicotinoids share with the 2004). With increases in pyrethroid use insecticide, which acts as a nicotinic acetyl- pyrethroids a relatively low risk of dermal likely, this may prove to be problematic choline receptor agonist. The target- toxicity to mammals (table 3), and their in the future (see page 5). site selectivity of imidacloprid and oral LD50s make them suitable for use on Secondary pests. Beneficial insects other neonicotinoids is a major factor in fruit and vegetable crops. As their regis- and mites are an important component their favorable toxicological properties tered crop uses expand on California’s of integrated pest management (IPM) because they act at much lower con- “minor use” or “specialty” crops (gener- since they can reduce the need for in- centrations in insects than in mammals. ally those grown on 300,000 acres or less), secticides when present at sufficient Imidacloprid was developed from nithi- they will likely replace many OPs. Where densities. Pyrethroids have been shown azine, a heterocyclic nitromethylene that they have already been registered, such as to seriously affect beneficial arthropods was first reported in 1978. Although it on lettuce and cole crops, their use is well present in agricultural crops, and they exhibited considerable insecticidal activ- established (table 2). Jack Kelly Clark Kelly Jack

Left, xylem is placed in a pressure bomb and will later be tested in the winged sharpshooter, center. The insect carries the pathogen that causes UC Riverside laboratory for neonicotinoid insecticides that kill the glassy- Pierce’s disease, which has killed vines in the Temecula Valley, right.

http://CaliforniaAgriculture.ucop.edu • JANUARY-MARCH 2005 13 Water quality. Neonicotinoids are more similar to OPs than pyrethroids in their potential to move through the soil and run off in surface water. The California Pollution Contamination Prevention Act of 1985 established a set of specific numerical values (SNV) for pesticides and required DPR to place ac- tive ingredients on a list of candidates as potential leachers if their water solubility value exceeds 3 parts per million (ppm) or if the soil adsorption coefficient is less than 1,900 cm3/g, and if one of three persistence parameters is exceeded. The three major neonicotinoids currently registered in California all exceed the SNVs and are on the list, suggesting that care is needed when using these products to protect water quality. Imidacloprid is soluble in water (5.14 g/l), has moderate binding affinity to Top: left, UC Riverside postgraduate researcher Jian Bi catalogues peppers for an efficacy study of various alternatives to organophosphate insecticides, including neonicotinoids, pyre- organic materials in soils (Koc = 262) and throids, insect growth regulators and organic products; right, Ballmer collects insects using a a relatively long half-life in soils (365 suction sampler. Bottom: left, an adult potato psyllid; right, psyllid damage to a red pepper. days). Acetamiprid is also water-soluble (2.95 g/l), has similar binding affinity and its intended target. The OPs bind to similarity in binding sites. However, to organic materials in soils (Koc = 260), and inhibit the activity of the synaptic cross-resistance between insecticide but is short-lived in soils (1 to 8 days). enzyme acetylcholinesterase (AChE), classes having different modes of action Thiamethoxam is water-soluble (3.26 resulting in the disruption of the normal is viewed as a more serious problem, g/l), but has low binding affinity to transmission of nerve impulses across because insecticides to which an insect organic materials in soil (Koc = 43 to 77) the synapse. In resistant insects, insensi- has previously been unexposed may be and is more persistent (385 to 408 days) tivity of the AChE to binding by the OP jeopardized through the selective forces than the others. Soil type and irrigation restores synaptic function even in the of an unrelated insecticide. This can have practices will therefore be important presence of the OP. a serious impact on the development of considerations for growers in order to Pyrethroids bind to sites on the so- pest management strategies, particularly optimize neonicotinoid efficacy while dium channel and in so doing disrupt when emergency registrations of new preventing possible unwanted environ- the transmission of impulses along the insecticides are under consideration as mental effects. nerve axon by holding the channels in potential control agents. Detoxification Nontarget organisms. The impacts an open position (Bradbury and Coats mechanisms are an extremely impor- of neonicotinoids on nontarget organ- 1989). Pyrethroid resistance occurs tant source of cross-resistance between isms remain unclear. For example, there when mutations in sodium channel insecticides that differ in their target is some controversy over the safety of genes reduce the capacity of the py- sites. There are three broad groups of systemic treatments to both natural rethroids to bind effectively, thereby detoxification enzymes — the carboxy- enemies and bees that may encounter neo- enabling the channels to function nor- TABLE 3. Oral and dermal toxicities of commonly nicotinoid residues in nectar and pollen mally. Currently, there is no evidence for applied insecticides on California crops* (Schmuck et al. 2001). This is a current area target-site resistance in neonicotinoids. of research to better define specific risks and This is important because target-site Oral LD50 Dermal LD50 evaluate mitigation measures if necessary. resistance can act as a foundation upon Chemical name rat; mg/kg rabbit; mg/kg which other resistance mechanisms Organophosphates Pest resistance is a major concern develop. These in turn can disrupt Chlorpyrifos 96­–270 2,000 Diazinon 1,250 2,020 The effective deployment of new management programs due to cross- Dimethoate 235 400 insecticides within pest management resistance to other insecticide classes. Pyrethroids programs should include strategies for Cross-resistance occurs in an insect Esfenvalerate 458 > 2,000 delaying the development of pest resis- when a resistance mechanism selected Lambda-cyhalothrin 1,593 > 2,000 tance. The two most common mecha- for in response to exposure to one Permethrin 430–4,000 > 2,000 nisms conferring resistance to the OP insecticide also confers resistance to Neonicotinoids and pyrethroid insecticides are target- a second insecticide to which the in- Acetamiprid 1,064 > 2,000 Imidacloprid > 4,870 > 2,000 site insensitivity and detoxification. sect has not been exposed. Target-site Thiamethoxam > 5,000 > 2,000 Target-site insensitivity arises from a cross-resistance is very common within * Higher LD50 values indicate lower oral or dermal toxicity. reduced binding between the insecticide individual insecticide classes due to the

14 CALIFORNIA AGRICULTURE, VOLUME 59, NUMBER 1 Photos: Jack Kelly Clark Kelly Jack Photos: References Armegaud C, Labin M, Gauthier M. 2002. Effects of imidacloprid on the neural pro- cesses of memory in honey bees. In: Devillers J, Pham-Delegue MH (eds.). Honey Bees: Esti- Left, pyrethroids can be disruptive of natural enemies, such a the western orchard predator mating the Environmental Impact of Chemi- mite. Right, whiteflies are often the target of neonicotinoid applications. cals. London: Taylor Francis. p 85–100. Bentley WJ, Zalom FG, Barnett WW, Sanderson JP. 1987. Population densities of lesterases, the cytochrome P450s and the ber of pesticide applications (Ellsworth Tetranychus spp. (Acari: Tetranychidae) after glutathione-S-transferases — and each 1998) and the restoration of susceptibility treatment with insecticides for Amyelois of these has been implicated in resis- to synergized pyrethroids and nonpyre- transitella (Lepidoptera: Pyralidae). J Econ tance to the OPs and pyrethroids. throids (Dennehy et al. 1997). Entomol 80:193–200. Bradbury SP, Coats JR. 1989. Comparative Unfortunately, resistance to pyre- Delaying the onset of resistance toxicology of pyrethroid insecticides. Rev En- throids has already been reported for a viron Contam Toxicol 108:133–77. number of insect species in California The ultimate impact to California Byrne FJ, Castle S, Prabhaker N, Toscano NC. 2003. Biochemical study of resistance and elsewhere. The neonicotinoids, agriculture of losing OP insecticides will to imidacloprid in B biotype Bemisia tabaci however, are relatively new to Califor- depend very much upon how alterna- from Guatemala. Pest Manag Sci 59:347–52. nia agriculture, and there has yet to be a tive insecticides are deployed. Perhaps Dennehy TJ, Williams L, Russell JS, et substantiated case of resistance arising the most immediate insect-control prob- al. 1997. Monitoring and management of whitefly resistance to insecticides in Arizona. from their application under field condi- lem for California agriculture will not In: Dugger P, Richter E (eds.). Proc Beltwide tions. Continuous laboratory selection be finding a suitable replacement for the Cotton Conference; Memphis, TN. Memphis: of a whitefly population collected from OPs as insecticides, but rather to delay National Cotton Council. p 65–8. melon crops in the Imperial Valley re- [DPR] California Department of Pesticide the onset of and manage pest resistance Regulation. 2003. Summary of Pesticide Use sulted in 80-fold resistance to imidaclo- to the pyrethroids and neonicotinoids Report Data 2002 Indexed by Chemical. Sac- prid, illustrating that resistance genes that are replacing them. ramento, CA. http://www.cdpr.ca.gov. 500 p. are present in California whiteflies. The pyrethroids have an established Ellsworth PC. 1998. Whitefly manage- ment in Arizona: Looking at whole systems. Resistance has been documented in field history of use in California and much In: Dugger P, Richter E (eds.). Proc Beltwide populations of the silverleaf whitefly is known about their efficacy as pest Cotton Conference; Memphis, TN. Memphis: (Bemisia) in Arizona and worldwide in control agents, as well as their negative National Cotton Council. p 743–8. Spain, Israel and Guatemala (Byrne et impacts on nontarget species and the [EXTOXNET] Extension Toxicology Net- work. 2003. Pesticide Information Profiles. al. 2003). In the northeastern United environment. They are prone to resis- Oregon State University, Corvallis, OR. http:// States, resistance to imidacloprid was tance, and a concern is that they may ace.orst.edu/info/extoxnet/ detected in the Colorado potato beetle face additional problems with resistance Metcalfe M, McWilliams B, Hueth B, et al. 2002. The Economic Impact of Organophos- (Leptinotarsa decemlineata) just 2 years af- without their OP synergists. By contrast, phates in California Agriculture. California ter its initial use (Zhao et al. 2000). the neonicotinoids are a new class of Department of Food and Agriculture Report. The OPs are occasionally used in insecticide and their influence in pest Sacramento, CA. 41 p + app. www.cdfa. mixtures with pyrethroids to synergize control is only now being realized as ca.gov/publications.htm Roush RT, Tabashnik BE. 1990. Pesticide their activity. The synergistic effect is new products are developed and new Resistance in Arthropods. New York: Chap- believed to occur when the OPs inhibit uses identified. There is no evidence of man Hall. 303 p. pyrethroid-hydrolyzing esterases, there- resistance to neonicotinoids at present Schmuck R, Schoning R, Stork A, Schramel by enabling toxic doses of the pyrethroid O. 2001. Risk posed to honeybees (Apis mel- in California agriculture, although resis- lifera L, Hymenoptera) by an imidacloprid to accumulate at the target site. Mixtures tance has been documented elsewhere. seed dressing of sunflowers. Pest Manag Sci of the OP (Orthene) and the It will be necessary for growers and 57:225–38. pyrethroid fenpropathrin (Danitol) were pest management specialists to use both Smith TM, Stratton GW. 1986. Effects of synthetic pyrethroid insecticides on nontar- used effectively for whitefly control on classes of materials judiciously and in get organisms. Residue Rev 97:93–120. cotton, although in recent years reliance combination with other alternatives as Werner IL, Deanovic A, Hinton DE, et al. on this strategy has suffered due to the feasible, to avoid resistance problems 2002. Toxicity of stormwater runoff after development of target-site resistance and maintain environmental quality. dormant spray application of diazinon and esfenvalerate (Asana) in a French prune to the pyrethroid, a mechanism that is orchard, Glenn County, California, USA. Bull not synergizable by the OP. In Arizona, Environ Contam Toxicol 68:29–36. a resistance management strategy was Weston DP, You JC, Lydy MJ. 2004. Distri- bution and toxicity of sediment-associated introduced in 1996 to combat whitefly F.G. Zalom is Entomologist, Agricultural Ex- pesticides in agriculture-dominated water resistance problems. A strategy of incor- periment Station, and Cooperative Extension bodies of California’s Central Valley. Environ porating insect growth regulators (IGRs), Entomologist, Department of Entomology, Sci Technol 38(10):2752–9. pyrethroids and nonpyrethroid conven- UC Davis; and N.C. Toscano is Cooperative Zhao JZ, Bishop BA, Grafius EJ. 2000. Inheritance and synergism of resistance to tional insecticides in a multistage pro- Extension Entomologist, and F.J. Byrne is imidacloprid in the Colorado potato beetle gram proved successful, as documented Assistant Research Entomologist, Depart- (Coleoptera: Chrysomelidae). J Econ Entomol by a dramatic reduction in the total num- ment of Entomology, UC Riverside. 93:1508–14.

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