Soil texture has a strong impact on termiticide performance, but effects differ with insecticide. In assays conducted with bifenthrin, chlorfenapyr, and fipronil, *C. formosanus* mortality was generally highest when clay content was low (Wiltz, 2010). Clay content of soil was significantly related to termite mortality across all termiticides, rates, and exposure times (Wiltz, 2010). Likewise, Osbrink and Lax (2002) found that *C. formosanus* workers experienced greater mortality in fipronil-treated sand than in treated potting soil or a mixture of soil and clay. Bobé et al. (1997) reported that for fipronil there was a significant decrease in adsorption coefficient as the soil clay content decreased, thereby increasing bioavailability. However, the opposite result occurs with some insecticides. Smith and Rust (1993) found that increased clay content increased the toxicity of certain pyrethroids, such as cypermethrin. The authors concluded that cypermethrin and clay apparently interacted creating a formulation similar to a wettable powder, which may have an increased affinity for the nonpolar termite integument. Gao et al. (1998) investigated the adsorption of seven pesticides and metabolites with different physiochemical properties, finding that adsorption was generally more effective on smaller and larger soil particles than on intermediate-sized particles.

#### **3.3 pH**

Effects of pH on adsorption and desorption vary with insecticide chemistry and interact with other soil properties. Low pH soils increase the adsorption of weakly acidic pesticides (Boivin et al., 2005; Carrizosa et al., 2000; Halfon et al., 1996,). Desorption of endosulfan was higher at both acidic and alkaline pH ranges compared to neutral pH (Kumar & Philip, 2006). The authors found that in clay soil, adsorption decreased drastically when the pH was reduced. In soil column experiments, deltamethrin was essentially immobile in three different soils. Kaufman et al. (1981) suggested that for nonacidic soils, the pH may be a primary factor affecting mobility of deltamethrin. In bioassays of treated soils against *C. formosanus*, there was an interaction between effects of soil pH and clay content on effectiveness of chlorfenapyr and fipronil (Wiltz, 2010).

#### **3.4 Organic carbon**

Partitioning of insecticides between soil organic matter and soil solution affects bioavailability (Felsot & Lew, 1989). Like clay, organic matter decreases adsorption of fipronil (Bobé et al., 1997). Mulrooney and Gerard (2007) applied fipronil to 3 soils and found that *R. flavipes* mortality decreased with increasing organic carbon. Although no soil effects were found when soils were treated at label rates, pyrethroids applied at low rates were less available in soils with high OC (Henderson et al., 1998). Soil OC has been shown to affect adsorption of several non-acidic pesticides, but have little or no effect on weakly acidic chemicals (Barriuso & Calvet, 1992; Boivin et al., 2005; Worrall et al., 2001).

#### **4. Application technique**

In addition to properties of the soil and chemicals, variations in application technique can influence availability, persistence, and impenetrability of toxins. Such variables include gaps in soil treatment, thickness of treated layer, and watering method. Within certain ranges of application rates, availability increases with rate; however, the opposite is true at other rates.

Soil texture has a strong impact on termiticide performance, but effects differ with insecticide. In assays conducted with bifenthrin, chlorfenapyr, and fipronil, *C. formosanus* mortality was generally highest when clay content was low (Wiltz, 2010). Clay content of soil was significantly related to termite mortality across all termiticides, rates, and exposure times (Wiltz, 2010). Likewise, Osbrink and Lax (2002) found that *C. formosanus* workers experienced greater mortality in fipronil-treated sand than in treated potting soil or a mixture of soil and clay. Bobé et al. (1997) reported that for fipronil there was a significant decrease in adsorption coefficient as the soil clay content decreased, thereby increasing bioavailability. However, the opposite result occurs with some insecticides. Smith and Rust (1993) found that increased clay content increased the toxicity of certain pyrethroids, such as cypermethrin. The authors concluded that cypermethrin and clay apparently interacted creating a formulation similar to a wettable powder, which may have an increased affinity for the nonpolar termite integument. Gao et al. (1998) investigated the adsorption of seven pesticides and metabolites with different physiochemical properties, finding that adsorption was generally more effective on smaller and larger soil particles than on intermediate-sized

Effects of pH on adsorption and desorption vary with insecticide chemistry and interact with other soil properties. Low pH soils increase the adsorption of weakly acidic pesticides (Boivin et al., 2005; Carrizosa et al., 2000; Halfon et al., 1996,). Desorption of endosulfan was higher at both acidic and alkaline pH ranges compared to neutral pH (Kumar & Philip, 2006). The authors found that in clay soil, adsorption decreased drastically when the pH was reduced. In soil column experiments, deltamethrin was essentially immobile in three different soils. Kaufman et al. (1981) suggested that for nonacidic soils, the pH may be a primary factor affecting mobility of deltamethrin. In bioassays of treated soils against *C. formosanus*, there was an interaction between effects of soil pH and clay content on

Partitioning of insecticides between soil organic matter and soil solution affects bioavailability (Felsot & Lew, 1989). Like clay, organic matter decreases adsorption of fipronil (Bobé et al., 1997). Mulrooney and Gerard (2007) applied fipronil to 3 soils and found that *R. flavipes* mortality decreased with increasing organic carbon. Although no soil effects were found when soils were treated at label rates, pyrethroids applied at low rates were less available in soils with high OC (Henderson et al., 1998). Soil OC has been shown to affect adsorption of several non-acidic pesticides, but have little or no effect on weakly

In addition to properties of the soil and chemicals, variations in application technique can influence availability, persistence, and impenetrability of toxins. Such variables include gaps in soil treatment, thickness of treated layer, and watering method. Within certain ranges of application rates, availability increases with rate; however, the opposite is true at other rates.

acidic chemicals (Barriuso & Calvet, 1992; Boivin et al., 2005; Worrall et al., 2001).

effectiveness of chlorfenapyr and fipronil (Wiltz, 2010).

**3.2 Clay**

particles.

**3.3 pH**

**3.4 Organic carbon**

**4. Application technique**

Initial concentration of termiticides in soil varies from several hundred to over one thousand micrograms per gram. Kard and McDaniel (1993) reported initial concentrations of 858± 990mg/g after application to a Mississippi soil, and Davis and Kamble (1992) reported initial concentrations of chlorpyrifos as high as 1500mg/g in a Nebraska loamy sand soil. Application rate affects both initial availability and degradation rate. Saran and Kamble (2008) reported an inverse relationship between the initial concentrations of bifenthrin, fipronil, and imidacloprid and their LT50 and LT90 values against *R. flavipes*. Greater bioavailability at higher concentrations may explain similar trends reported by Smith and Rust (1992), Forschler and Townsend (1996), and Ramakrishnan et al. (2000). At low rates, fipronil has low soil affinity, but adsorption increases with concentration (Bobé et al., 1997). Kamble and Saran (2005) found that at termiticide application rates of 0.06–0.125%, there is a reversal in the fipronil adsorption process, whereby there is a decrease in adsorption coefficient with an increase in concentration, resulting in an increase in bioavailability. Chlorpyrifos exhibited a lower degradation rate when applied at ≈1,000 μg/g soil than when applied at typical agricultural levels of 0.3–32 μg/g (Racke et al., 1994). When fipronil was applied at the labeled rate for locust control (8g AI per ha), 75% degraded within 3 d (Bobé et al., 1998). However, when applied at termiticidal rates (60-125 μg AI per g), fipronil did not show much degradation, and no metabolites were detected in residue analysis after 180 d (Saran and Kamble 2008). Gahlhoff and Koehler (2001) found that concentration and treatment thickness significantly affected both mortality and penetration by *R. flavipes* into imidacloprid-treated soil, with mortality remaining low after 7 d exposure to low concentrations, as well as affecting bioavailability, high termiticide concentrations may indirectly affect degradation by negatively impacting bacterial and fungal populations, resulting in prolonged inhibition of soil dehydrogenase and esterase activities (Felsot & Dzantor, 1995). Racke et al. (1996) examined hydrolysis of chlorpyrifos in 37 soils at agricultural application rates (10mg/g) and observed that in some alkaline soils hydrolysis constituted the major degradation pathway. However, they also noted that in several soils, with pH values in the range of 7.1 to 8.5, the hydrolytic reaction was inhibited at higher concentrations (1000mg/g).

Termites can circumvent soil treatments by using untreated gaps, building materials, or debris as bridges between the surrounding soil and structure (Forschler, 1994; Smith & Zungoli, 1995; Su & Scheffrahn, 1998). Subterranean termite foragers are able to detect and avoid repellant termiticides so areas treated with pyrethroids are rarely contacted. The subterranean termites' ability to detect chemical barriers allows termite foragers to follow the edge of the pyrethroid treated area until they find a gap in the treatment (Forschler, 1994; Rust & Smith, 1993; Su & Scheffrahn, 1990b; Su et al., 1982). Thus, gaps in pyrethroid applications may actually funnel foragers toward the structures they are intended to protect (Forschler, 1994; Kuriachan & Gold, 1998). The inevitability of gaps in soil termiticide barriers is a major limitation to the efficacy of repellant liquid termiticides (Forschler, 1994; Kuriachan & Gold, 1998). Gaps may exist in a soil termiticide treatment for a number of reasons. Pre-construction treatments often contain gaps due to imperfect initial application or physical disturbance of the soil after application (Koehler et al., 2000; Su & Scheffrahn, 1990a, 1998). When an existing structure becomes infested and requires a remedial termiticide application, it is difficult to create a continuous horizontal barrier of liquid termiticide beneath the structure (Su & Scheffrahn, 1990a, 1998; Koehler et al., 2000). Finally, all termiticides degrade over time. An ageing soil treatment, applied below the foundation

Factors Affecting Performance of Soil Termiticides 161

adsorption at higher temperatures. Dios-Cancela et al. (1990) found that sorption of the

Microbial degradation occurs when fungi, bacteria, and other soil microorganisms use pesticides as food or consume pesticides along with other substances. Activity of microbes is affected by soil organic matter and texture and is usually highest in warm, moist, wellaerated soils with a neutral pH. Because microbial degradation is mediated by enzymes, temperature is important in determining the rate degradation: the rate of most reactions catalyzed by enzymes tends to double for each 10C increase in temperature between 10

Naturally-occurring pesticide-degrading microorganisms may be relatively rare in pristine environments and non-exposed agricultural soils (Bartha, 1990). Some of the pesticidedegrading microbes that have been identified include *Arthrobacter, Brevibacterium, Clavibacter, Corynebacterium, Micromonospora, Mycobacterium, Nocardia, Nocardioides,*

A review of earlier work on organophosphate and carbamate insecticide degradation was prepared by Laveglia and Dahm (1977). Although organophosphates are no longer used in many parts of the world, there have been several recent studies on their degradation by microbes. Li et al. (2007) reported the isolation of a bacterium, *Sphingomonas* sp., that degrades chlorpyrifos, parathion, parathion-methyl, fenitrothion and profenofos. However, several other studies have found little microbial degradation of chlorpyrifos. Goda et al. (2010) showed that the intact cells of *Pseudomonas putida* IS168 were able to degrade fenitrothion, diazinon and profenofos when present as sole carbon sources, but failed to grow on chlorpyrifos. Trichloropyridinol (TCP), one of the main chlorpyrifos metabolites, has antimicrobial properties (Cáceres et al., 2007; Feng et al., 1997; Racke et al., 1990), possibly accounting for the scarcity of chlorpyrifos-degrading microorganisms. Degradation of pyrethroids in soil has also been extensively studied (Gan et al., 2005; Jorhan & Kaufman, 1986; Kaufman et al., 1981; Lee et al., 2004; Lord et al., 1982). Most of these studies show that microorganisms play an important role in the degradation of pyrethroid compounds in soils

In studies evaluating termite tunneling through chlordane, chlorpyrifos, or permethrin treated soil, large groups of termites were able to tunnel farther than small groups (Beal & Smith, 1971; Jones, 1990). At low population density, different colonies of *C. formosanus* either totally avoided permethrin-treated soil or tunneled slightly (Jones, 1989, 1990). Jones (1990) found that while large groups of termites tunneled more than small groups in soils treated with chlordane, chlorpyrifos, or permethrin, group size had different effects on mortality in different soil treatments. Several experiments have demonstrated correlations between termite survival rates and population density (Lenz et al., 1984; Lenz, 2009; Santos et al., 2004). At population densities below 0.1 g termites / ml, Lenz et al. (1984) found that, in the absence of termiticide treatment, survival of *Coptotermes lacteus* (Froggatt) and

Susceptibility differences occur among termite species and colonies. Most soil termiticide evaluations have included only one target species. However, in studies comparing

herbicide cyanazine to peats decreased with increasing temperature.

and 45C and is greatly reduced above and below these temperatures.

*Rhodococcus* and *Streptomyces* genera (De Schrijver and De Mot, 1999).

**5.3 Micromial degradation**

and sediments.

**6. Termite pressure and susceptibility**

*Nasutitermes exitiosus* (Hill) increased with population density.

before a structure was built, is inaccessible after construction and cannot be reapplied (Su & Scheffrahn, 1990a; Su, 1997; Koehler et al., 2000).

The total volume of pesticide suspension applied to soil affects penetration depth and concentration in the soil. In tests using imidacloprid and fipronil in five different soils, when equal amounts of pesticide were diluted in different volumes of water, the higher volume treatments penetrated further into the soil, but the more concentrated treatments deposited more pesticide in the top 1cm of soil (Peterson 2010). It is likely that the thicker barrier of lower active ingredient concentration would provide better protection, at least in the short term because it might be better able to withstand disturbances to the top 1 cm of soil. Additionally, termites are less able to tunnel through thicker barriers of lower active ingredient concentration than through thinner barriers of higher concentration (Smith et al. 2008). However, pesticide treatments with low initial concentrations degrade faster than those with higher initial concentrations (Bobé et al., 1998; Felsot & Dzantor, 1995; Saran & Kamble, 2008). In addition to total volume of liquid applied, initial thickness of the treated zone depends on soil and termiticide properties. Smith and Rust (1992) found that termiticidal amounts of chlordane and cypermethrin moved to soil depths of at least 7 cm, while chlorpyrifos moved to a depth of at least 30 cm.

#### **5. Environmental factors**

Both biotic and abiotic pathways have been found to be important for insecticide degradation and transformation in soils (Racke et al., 1996).

#### **5.1 Moisture**

Water can compete with pesticides for sorption sites on soil particles. Dry soils become more sorptive for both polar and non-polar chemicals (Chen et al., 2000). However, chemicals with low polarity are released when soil becomes wet (Harper et al., 1976). Repeated cycles of wetting and drying affect pesticide availability and degradation, but depend on properties of the chemical, soil, number of wetting and drying cycles, time since pesticide application, and time since wetting (Garcia-Valcarcel & Tadeo, 1999; Xia & Brandenburg 2000; Ying & Kookana, 2006; Peterson, 2007).

#### **5.2 Temperature**

Soil temperature affects termiticide bioavailability through its influence on solubility and adsorption. In addition to its effect on the physical and chemical properties of the pesticide, extreme temperatures affect the rate of microbial degradation, as described in the following section. Several studies have demonstrated that temperature affects adsorption of pesticides to soil, but that the nature of this effect varies among pesticides. Although most of the work on pesticide availability and degradation has been conducted in the temperate climates of North America and Europe, soil temperature is likely to play an important role in termiticide degradation in tropical regions. Khan et al. (1996) found that lindane adsorption to silty loam and silty clay loam soils increased with temperature. Likewise, Valverde-Garcia et al. (1988) found that higher temperatures increased the adsorption of the fungicide thiram and the organophosphate insecticide dimethoate to organic soils. Temperature may interact with pH, particularly in saturated soils. In aqueous solutions, fenamiphos, fipronil, and trifluralin degradation increased with temperature and pH (Ramesh & Balasubramanian, 1999). Other studies have demonstrated a reduction in pesticide adsorption at higher temperatures. Dios-Cancela et al. (1990) found that sorption of the herbicide cyanazine to peats decreased with increasing temperature.

#### **5.3 Micromial degradation**

160 Insecticides – Basic and Other Applications

before a structure was built, is inaccessible after construction and cannot be reapplied (Su &

The total volume of pesticide suspension applied to soil affects penetration depth and concentration in the soil. In tests using imidacloprid and fipronil in five different soils, when equal amounts of pesticide were diluted in different volumes of water, the higher volume treatments penetrated further into the soil, but the more concentrated treatments deposited more pesticide in the top 1cm of soil (Peterson 2010). It is likely that the thicker barrier of lower active ingredient concentration would provide better protection, at least in the short term because it might be better able to withstand disturbances to the top 1 cm of soil. Additionally, termites are less able to tunnel through thicker barriers of lower active ingredient concentration than through thinner barriers of higher concentration (Smith et al. 2008). However, pesticide treatments with low initial concentrations degrade faster than those with higher initial concentrations (Bobé et al., 1998; Felsot & Dzantor, 1995; Saran & Kamble, 2008). In addition to total volume of liquid applied, initial thickness of the treated zone depends on soil and termiticide properties. Smith and Rust (1992) found that termiticidal amounts of chlordane and cypermethrin moved to soil depths of at least 7 cm,

Both biotic and abiotic pathways have been found to be important for insecticide

Water can compete with pesticides for sorption sites on soil particles. Dry soils become more sorptive for both polar and non-polar chemicals (Chen et al., 2000). However, chemicals with low polarity are released when soil becomes wet (Harper et al., 1976). Repeated cycles of wetting and drying affect pesticide availability and degradation, but depend on properties of the chemical, soil, number of wetting and drying cycles, time since pesticide application, and time since wetting (Garcia-Valcarcel & Tadeo, 1999; Xia & Brandenburg

Soil temperature affects termiticide bioavailability through its influence on solubility and adsorption. In addition to its effect on the physical and chemical properties of the pesticide, extreme temperatures affect the rate of microbial degradation, as described in the following section. Several studies have demonstrated that temperature affects adsorption of pesticides to soil, but that the nature of this effect varies among pesticides. Although most of the work on pesticide availability and degradation has been conducted in the temperate climates of North America and Europe, soil temperature is likely to play an important role in termiticide degradation in tropical regions. Khan et al. (1996) found that lindane adsorption to silty loam and silty clay loam soils increased with temperature. Likewise, Valverde-Garcia et al. (1988) found that higher temperatures increased the adsorption of the fungicide thiram and the organophosphate insecticide dimethoate to organic soils. Temperature may interact with pH, particularly in saturated soils. In aqueous solutions, fenamiphos, fipronil, and trifluralin degradation increased with temperature and pH (Ramesh & Balasubramanian, 1999). Other studies have demonstrated a reduction in pesticide

Scheffrahn, 1990a; Su, 1997; Koehler et al., 2000).

while chlorpyrifos moved to a depth of at least 30 cm.

2000; Ying & Kookana, 2006; Peterson, 2007).

degradation and transformation in soils (Racke et al., 1996).

**5. Environmental factors**

**5.1 Moisture**

**5.2 Temperature**

Microbial degradation occurs when fungi, bacteria, and other soil microorganisms use pesticides as food or consume pesticides along with other substances. Activity of microbes is affected by soil organic matter and texture and is usually highest in warm, moist, wellaerated soils with a neutral pH. Because microbial degradation is mediated by enzymes, temperature is important in determining the rate degradation: the rate of most reactions catalyzed by enzymes tends to double for each 10C increase in temperature between 10 and 45C and is greatly reduced above and below these temperatures.

Naturally-occurring pesticide-degrading microorganisms may be relatively rare in pristine environments and non-exposed agricultural soils (Bartha, 1990). Some of the pesticidedegrading microbes that have been identified include *Arthrobacter, Brevibacterium, Clavibacter, Corynebacterium, Micromonospora, Mycobacterium, Nocardia, Nocardioides, Rhodococcus* and *Streptomyces* genera (De Schrijver and De Mot, 1999).

A review of earlier work on organophosphate and carbamate insecticide degradation was prepared by Laveglia and Dahm (1977). Although organophosphates are no longer used in many parts of the world, there have been several recent studies on their degradation by microbes. Li et al. (2007) reported the isolation of a bacterium, *Sphingomonas* sp., that degrades chlorpyrifos, parathion, parathion-methyl, fenitrothion and profenofos. However, several other studies have found little microbial degradation of chlorpyrifos. Goda et al. (2010) showed that the intact cells of *Pseudomonas putida* IS168 were able to degrade fenitrothion, diazinon and profenofos when present as sole carbon sources, but failed to grow on chlorpyrifos. Trichloropyridinol (TCP), one of the main chlorpyrifos metabolites, has antimicrobial properties (Cáceres et al., 2007; Feng et al., 1997; Racke et al., 1990), possibly accounting for the scarcity of chlorpyrifos-degrading microorganisms. Degradation of pyrethroids in soil has also been extensively studied (Gan et al., 2005; Jorhan & Kaufman, 1986; Kaufman et al., 1981; Lee et al., 2004; Lord et al., 1982). Most of these studies show that microorganisms play an important role in the degradation of pyrethroid compounds in soils and sediments.

#### **6. Termite pressure and susceptibility**

In studies evaluating termite tunneling through chlordane, chlorpyrifos, or permethrin treated soil, large groups of termites were able to tunnel farther than small groups (Beal & Smith, 1971; Jones, 1990). At low population density, different colonies of *C. formosanus* either totally avoided permethrin-treated soil or tunneled slightly (Jones, 1989, 1990). Jones (1990) found that while large groups of termites tunneled more than small groups in soils treated with chlordane, chlorpyrifos, or permethrin, group size had different effects on mortality in different soil treatments. Several experiments have demonstrated correlations between termite survival rates and population density (Lenz et al., 1984; Lenz, 2009; Santos et al., 2004). At population densities below 0.1 g termites / ml, Lenz et al. (1984) found that, in the absence of termiticide treatment, survival of *Coptotermes lacteus* (Froggatt) and *Nasutitermes exitiosus* (Hill) increased with population density.

Susceptibility differences occur among termite species and colonies. Most soil termiticide evaluations have included only one target species. However, in studies comparing

Factors Affecting Performance of Soil Termiticides 163

Anonymous. (2008). State of the industry. Termites: Kicked to the "B" list? PCT October 10,

Baker, P. B., and D. E. Bellamy. (2006). Field and laboratory evaluation of persistence and

(Isoptera: Rhinotermitidae). *Journal of Economic Entomology,* 99: 1345-1353. Barriuso, E. & Calvet, R. (1992). Soil type and herbicide adsorption. *International Journal of*

Bartha, R., (1990). Isolation of microorganisms that metabolize xenobiotic compounds. In:

Baskaran, S., Kookana, R. S. & Naidu, R. (1999). Degradation of bifenthrin, chlopyrifos, and

Beal, R. H., & Smith, V. K. (1971). Relative susceptibilities of *Coptotermes formosanus*,

Bedient, P.H., Rifai, H. S. & Newell C. J. (1994). Ground Water Contamination: Transport

Bobé, A., Coste, C. M. & Copper, J –F. (1997). Factors influencing the adsorption of fipronil

Bobé, A., Cooper, J. -F., Coste, C. M. & Muller, M. -A. (1998). Behaviour of fipronil in soil

Boivin, A., Cherrier, R. & Schiavon, M. (2005). A comparison of five pesticides adsorption

Cáceres T, He, W., Naidu, R. & Megharaj, M. (2007). Toxicity of chlorpyrifos and TCP alone

Carrizosa, M. J., Calderon, M. J, Hermosin, M. C. & Cornejo, J. (2000). Organosmectites as

Chen D., Rolston, D. E., and Yumaguchi, T. (2000). Calculating partition coefficients of organic vapors in unsaturated soils and clays. *Soil Science*, 165: 217-225. Cheung, M. W., Mingelgrin, V. & Biggar, J. W. (1979). Equilibrium and kinetics of

Connelly, P. (2001). Environmental fate of fipronil. Environmental Monitoring Branch. Department of Pesticide Regulation. California Environmental Protection Agency. Cox, L. Koskinen W. C., Celis, R., Yeen, P. Y., Hermosin, M. C. & Cornejo, J. (1998). Sorption

and desorption processes in thirteen contrasting field soils. *Chemosphere,* 61: 668-

and in combination to *Daphnia carinata*: the influence of microbial degradation in

sorbent and carrier of the herbicide bentazone. *Science of the Total Environment,* 247:

desorption of picloram and parathion in soils. *Journal of Agricultural and Food*

of imidacloprid on soil clay mineral and organic components. *Soil Science of America*

bioavailability of soil termiticides to desert subterranean termite *Heterotermes aureus*

*Isolation of Biotechnological Organisms from Nature*, Labeda, D. P. (Ed.), pp. 283-307,

imidacloprid in soil and bedding materials at termiticidal application rates.

*Reticulitermes flavipes*, and *R. virginicus* to soil insecticides. *Journal of Economic*

2008. http://www.pctonline.com/Article.aspx?article\_id=37550. Aventis Environmental Science. (2001). Termidor SC termiticide label. Montvale, NJ.

BASF Corporation. (2001). Phantom termiticide label. Triangle Park, NC.

*Environmental Analytical Chemistry,* 46: 117–128.

*Pesticide Science,* 55:1222–1228.

*Entomology*, 64: 472-475.

676.

285–293.

*Chemistry*, 27: 1201-1206.

*Journal,* 69: 911-915.

McGraw-Hill Publishing Company, New York, USA.

Bayer Corporation. (2000). Premise 75 WSP termiticide label. Kansas City, MO.

and Remediation, Prentice Hall, Englewood Cliffs, NJ, 1994.

natural water. *Water Research,* 41: 4497–4503

on soils. *Journal of Agricultural and Food Chemistry,* 45: 4861–4865.

under Sahelian plain field conditions. *Pesticide Science,* 52: 275–281.

responses of two or more species, there are frequently differences in susceptibility. *C. formosanus* penetrated soil treated with aldrin, chlordane, dieldrin, or heptachlor, while *R. virginicus* and *R. flavipes* failed to penetrate lower rates of the same chemicals and were killed more quickly than *C. formosanus* (Beal & Smith 1971). In a laboratory assay, chlorpyrifos, permethrin, cypermethrin, bifenthrin, isofenphos, lambda-cyhalothirn, and fenitrothion all provided equal barrier protection against *R. flavipes* (Su et al. 1993). However, in the same assay, *C. formosanus* generally tunneled deeper into sand treated with organophosphates than with pyrethroids. Penetration of sand treated with thiamethoxam or fipronil was similar for *C. formosanus* and *R. flavipes*, but thiamethoxam was more toxic to *C. formosanus* than to *R. flavipes* (Remmen & Su 2005). Osbrink and Lax (2002) evaluated seven insecticides against termites from colonies that had been previously been identified as either insecticide susceptible or tolerant, finding differences in substrate penetration and mortality among colonies and insecticides.

Termite traits other than population size or susceptibility to toxicants can increase the likelihood that soil treatments will fail to protect a structure. Aerial infestations account for a large percentage of structural infestations by *C. formosanus* (Su & Scheffrahn, 1990), making soil treatments ineffective. Additionally, *C. formosanus* colonies may seal off or avoid treated areas (Su et al. 1982) when repellent toxicants are used, but use gaps in the soil barrier to access the structure (Forschler, 1994).

#### **7. Conclusion**

Several long-term studies of termiticide persistence have been conducted. In USDA Forest Service trials, which have been conducted for the past 40 years, tests consist of treated soil plots covered by concrete slabs. Treatments are considered failures when termites penetrate >50% of field replicates to reach a wood block placed in a pipe running through the slab (Kard, 2003; Wagner, 2003). In these tests, longevity differed with geographic location and termiticide class (Mulrooney et al., 2007). Such studies have the advantage of being performed under natural soil weathering conditions for an extended period of time and provide a standard method of comparing termiticides. However, products are evaluated on a limited number of soils and it is impossible to tell if a lack of penetration into plots should be attributed to effectiveness of the termiticide or to the absence of termite pressure. To overcome this problem, other studies have included laboratory bioassays coupled with field termiticide persistence studies (Gold et al., 1996; Grace, 1991; Su et al., 1993). Unfortunately, most of these studies have evaluated relatively few soil types. Because performance is so dependent on a combination of temiticide and soil properties and weathering, more research is needed to evaluate new and existing products under a larger range of conditions. Soil termiticides have been extensively evaluated for toxicity, bioavailability, and degradation. However, reasons for termiticide failure are complex and often local in nature, indicating the need for more research and localized treatment recommendations regarding choice of toxicant, application technique, and treatment frequency.

#### **8. References**

Alley, W., (1993). *Regional Groundwater Quality*, Van Nostrand Reinhold, New York, New York, 1994.

responses of two or more species, there are frequently differences in susceptibility. *C. formosanus* penetrated soil treated with aldrin, chlordane, dieldrin, or heptachlor, while *R. virginicus* and *R. flavipes* failed to penetrate lower rates of the same chemicals and were killed more quickly than *C. formosanus* (Beal & Smith 1971). In a laboratory assay, chlorpyrifos, permethrin, cypermethrin, bifenthrin, isofenphos, lambda-cyhalothirn, and fenitrothion all provided equal barrier protection against *R. flavipes* (Su et al. 1993). However, in the same assay, *C. formosanus* generally tunneled deeper into sand treated with organophosphates than with pyrethroids. Penetration of sand treated with thiamethoxam or fipronil was similar for *C. formosanus* and *R. flavipes*, but thiamethoxam was more toxic to *C. formosanus* than to *R. flavipes* (Remmen & Su 2005). Osbrink and Lax (2002) evaluated seven insecticides against termites from colonies that had been previously been identified as either insecticide susceptible or tolerant, finding differences in substrate penetration and mortality

Termite traits other than population size or susceptibility to toxicants can increase the likelihood that soil treatments will fail to protect a structure. Aerial infestations account for a large percentage of structural infestations by *C. formosanus* (Su & Scheffrahn, 1990), making soil treatments ineffective. Additionally, *C. formosanus* colonies may seal off or avoid treated areas (Su et al. 1982) when repellent toxicants are used, but use gaps in the soil barrier to

Several long-term studies of termiticide persistence have been conducted. In USDA Forest Service trials, which have been conducted for the past 40 years, tests consist of treated soil plots covered by concrete slabs. Treatments are considered failures when termites penetrate >50% of field replicates to reach a wood block placed in a pipe running through the slab (Kard, 2003; Wagner, 2003). In these tests, longevity differed with geographic location and termiticide class (Mulrooney et al., 2007). Such studies have the advantage of being performed under natural soil weathering conditions for an extended period of time and provide a standard method of comparing termiticides. However, products are evaluated on a limited number of soils and it is impossible to tell if a lack of penetration into plots should be attributed to effectiveness of the termiticide or to the absence of termite pressure. To overcome this problem, other studies have included laboratory bioassays coupled with field termiticide persistence studies (Gold et al., 1996; Grace, 1991; Su et al., 1993). Unfortunately, most of these studies have evaluated relatively few soil types. Because performance is so dependent on a combination of temiticide and soil properties and weathering, more research is needed to evaluate new and existing products under a larger range of conditions. Soil termiticides have been extensively evaluated for toxicity, bioavailability, and degradation. However, reasons for termiticide failure are complex and often local in nature, indicating the need for more research and localized treatment recommendations regarding

Alley, W., (1993). *Regional Groundwater Quality*, Van Nostrand Reinhold, New York, New

choice of toxicant, application technique, and treatment frequency.

among colonies and insecticides.

access the structure (Forschler, 1994).

**7. Conclusion**

**8. References**

York, 1994.

BASF Corporation. (2001). Phantom termiticide label. Triangle Park, NC.

Factors Affecting Performance of Soil Termiticides 165

Gold, R. E., Howell, H. N., Pawson, B. M., Wright, M. S. & J. C. Lutz. (1996). Persistence and

Grace, J. K. (1991). Response of eastern and Formosan subterranean termites (Isoptera,

Grace, J. K., Yates, J. R., Tamishiro, M. & Yamamoto, R. T. (1993). Persistence of

Henderson, G., Walthall, P. M., Wiltz, B. A. Rivera-Monroy, V. H., Ganaway, D. R. & H. M.

Horwood, M. A. (2007). Rapid degradation of termiticides under field conditions. *Australian*

Itawa, H., Tanabe, S., Sakai, N., Tatsukawa, R., (1993). Distribution of persistent

Jones, S. C. (1990). Effects of population density on tunneling by Formosan subterranean

Jorhan, E. G. & Kaufman, D. D. (1986). Degradation of cis- and transpermethrin in flooded

Kamble, S. T. & Saran, R. K. (2005). Effect of concentration on the adsorption of three

Kard, B. M. (2003). Integrated pest management of subterranean termites (Isoptera*). Journal*

Kard B. M. & McDaniel, C. A. (1993). Field evaluation of the persistence and efficacy of

soil. *Journal of Agricultural and Food Chemistry,* 34: 880-884.

Kard, B. (1999). Termiticides: the Gulfport report. *Pest Control,* 67: 42-46.

from five soil types in Texas. *Sociobiology,* 28: 337-363.

84: 1753–1757.

*Quality*, 5: 236-242.

Diego, CA, April 26-28, 1998.

*Journal of Entomology,* 46: 75-78.

control. *Sociobiology,* 15: 33-41.

*of Entomological Science,* 38: 200–224.

Chemical Society: Washington DC. pp 42-62.

*Entomology*, 83: 875-878.

1085.

bioavailability of termiticides to subterranean termites (Isoptera: Rhinotermitidae)

Rhinotermitidae) to borate dust and soil treatments. *Journal of Economic Entomology,*

organochlorine insecticides for Formosan subterranean termite (Isoptera: Rhinotermitidae) control in Hawaii. *Journal of Economic Entomology*, 86: 761-766. Halfon, E., Galassi, S., Bruggemann, R. &. Provini, A. (1996). Selection of priority properties to assess environmental hazard of pesticides, *Chemosphere,* 33: 1543–1562. Harper, L. A., White, A. W. Jr., Bruce, R. R., Thomas, A. W., and Leonard, R, A. (1976) Soil

and microclimate effects on trifluralin volatilization. *Journal of Environmental*

Selim. (1998). Analysis of soil properties in relation to termiticide performance in Louisiana. In Proceedings of the National Conference on Urban Entomology, San

organochlorines in the oceanic air and surface seawater and the role of ocean on their global transport and fate. *Environmental Science & Technology,* 27: 1080-1098. Jones, D. (1999). Environmental fate of cypermethrin. Environmental Monitoring and Pest Management Branch. California Department of Pesticide Regulation. Jones S. C. (1989). Field evaluation of fenoxycarb as a bait toxicant for subterranean termite

termite (Isoptera: Rhinotermitidae) through treated soil. *Journal of Economic*

termiticides in soil. *Bulletin of Environmental Contamination and Toxicology,* 75: 1077-

pesticides used for termite control, in Pesticides in Urban Environments - Fate and Significance, ed by Racke KD and Leslie AR, ACS Symposium Series 522, American

http://www.epa.gov/pesticides/op/chlorpyrifos/agreement.pdf.

Davis, R. W. & Kamble, S. T. (1992). Distribution of sub-slab injected Dursban TC

De Schrijver, A. & De Mot, R., (1999). Degradation of pesticides by actinomycetes. *Critical*

Dios-Cancela, G., Romero, T. E. & Sanchez-Rasero, F. (1990). Adsorption of cyanazine on

Environmental Protection Agency. (2000). Chlorpyrifos revised risk assessment and

Fecko, A. (1999). Environmental fate of bifenthrin. Environmental Monitoring and Pest Management Branch. California Department of Pesticide Regulation. Felsot, A. S., & Lew, A. (1989). Factors affecting bioactivity of soil insecticides: relationships

Felsot, A. S., & Dzantor, E. K. (1995). Effect of alachlor concentration and an organic

Feng Y, Racke, K. D. & Bollag, J. M. (1997). Isolation and characterization of a chlorinatedpyridinol-degrading bacterium. *Applied Environmental Microbiology,* 63: 4096–4409 Forschler, B. T. (1994). Survivorship and tunneling activity of *Reticulitermes flavipes* (Kollar)

Forschler, B. T. & Townsend, M. L. (1996). Mortality of Eastern subterranean termites

Gahlhoff, J. E. & Koehler, P. G. (2001). Penetration of the eastern subterranean termite into

Gan, J., Lee, S. J., Liu, W. P., Haver, D. L., Kabashima, J. N. (2005). Distribution and

Gao, J. P., Maguhn, J., Spitzauer, P. & Kettrup, A. (1998). Sorption of pesticides in the

Garcia-Valcarcel, A. I. & Tadeo, J. L. (1999). Influence of soil moisture on sorption and

Goda, S. K., Elsayed, I. E., Khodair, T. A., El-Sayed, W. & Mohamed, M. E. (2010). Screening

carboxylestrase in soil bacteria. *Biodegradation,* 21: 903–913.

gaps of untreated soil. *Journal of Entomological Science,* 29: 43–54.

among uptake, desorption, and toxicity of carbofuran and terbufos. *Journal of*

amendment on soil dehydrogenase activity and pesticide degradation rate*.*

(Isoptera: Rhinotermitidae) in response to termiticide soil barriers with and without

(Isoptera: Rhinotermitidae) exposed to four soils treated with termiticides. *Journal*

soil treated at various thicknesses and concentrations of Dursban TC and Premise

persistence of pyrethroids in runoff sediment*. Journal of Environmental Quality*, 36:

sediment of the Teufelsweiher pond (Southern Germany). I: Equilibrium assessments, effect of organic carbon content and pH. *Water Research,* 32: 1662-1672.

degradation of hexazinone and simazine in soil. *Journal of Agricultural and Food*

for and isolation and identification of malathion-degrading bacteria: cloning and sequencing a gene that potentially encodes the malathion-degrading enzyme,

*Bulletin of Environmental Contamination and Toxicology,* 48: 585-591.

peat and montmorillonite clay surfaces. *Soil Science*, 150: 836-843

http://www.epa.gov/pesticides/op/chlorpyrifos/agreement.pdf.

*Environmental Toxicology and Chemistry,* 14: 23-28.

*Reviews in Microbiology*, 25: 85-119.

Dupont. (2010). Dupont Altriset MSDS.

agreement with registrants. -

*Economic Entomology,* 82: 389-395.

*of Economic Entomology,* 89: 678-681.

834-841.

*Chemistry,* 47: 3895–3900.

75. *Journal of Economic Entomology,* 94: 486-491.

(chlorpyrifos) in a loamy sand soil when used for subterranean termite control,

Factors Affecting Performance of Soil Termiticides 167

Osbrink, W. L A., Cornelius, M. L. & Lax, A. R. (2005). Effect of imidacloprid soil treatments

Peterson, C. J. (2007). Imidacloprid mobility and longevity in soil columns at a termiticidal

Peterson, C. J. (2010). Varying termiticide application rate and volume affect initial soil

Potter, M. H. & Hillery, A. E. (2001). Exterior-targeted liquid termiticides an alternative

Racke, K. D., Fontaine, D. D., Yoder, R. N. & Miller, J. R. (1994). Chlorpyrifos degradation in

Racke K. D., Laskowski D. A. & Schultz M. R. (1990). Resistance of chlorpyrifos to enhanced biodegradation in soil. *Journal of Agricultural and Food Chemistry,* 38: 1430–1436. Racke K. D., Steele, K. P., Yoder, R. N., Dick, W.A. & Avidov E. (1996). Factors affecting the

Ramakrishnan, R., Suiter, D. R., Nakatsu C. H. & Bennett, G. W. (2000). Feeding inhibition

Remmen, L. N. & Su, N.-Y. (2005). Tunneling and mortality of eastern and Formosan

Ramesh, A. & Balasubramanian, M. (1999). Kinetics and Hydrolysis of Fenamiphos,

Rust, M. K. & Saran, R. K. (2006). The toxicity, repellency, and transfer of chlorfenapyr

Rust, M. K. & Smith, J. L. (1993). Toxicity and repellency of components in formulated

imidacloprid-treated soils. *Journal of Economic Entomology,* 93: 422-428. Randall, M. and Doody, T. C. (1934). Wood preservatives and protective treatments, pp. 463-

thiamethoxam or fipronil. *Journal of Economic Entomology,* 98: 906–910. Rice, R. C., Jaynes, D. B. & Bowman, R. S. (1991). Preferential flow of solutes and herbicide

approach to managing subterranean termites (Isoptera: Rhinotermitidae) in

hydrolytic degradation of chlorpyrifos in soil, *Journal of Agricultural and Food*

and mortality in *Reticulitermes flavipes* (Isoptera: Rhinotermitidae) after exposure to

476. In C.A. Kofoid [ed.] Termites and Termite Control. University of California

subterranean termites (Isoptera: Rhinotermitidae) in sand treated with

under irrigated fields. *Transactions of the American Society of Agricultural Engineers,*

Fipronil, and Trifluralin in Aqueous Buffer Solutions. *Journal of Agricultural and*

against western subterranean termites (Isoptera: Rhinotermitidae). *Journal of*

termiticides against western subterranean termites (Isoptera: Rhinotermitidae).

independent monitors. *Journal of Economic Entomology,* 98: 2160–2168. Parman, V. & Vargo, E. L. (2010). Colony-Level Effects of Imidacloprid in Subterranean Termites (Isoptera: Rhinotermitidae). *Journal of Economic Entomology,* 103: 791-798. Pawson, B. M. & R. E. Gold. (1996). Evaluation of baits for termites (Isoptera:

Rhinotermitidae) in Texas. *Sociobiology,* 28: 485-491.

buildings. *Sociobiology* 39: 373–405.

*Chemistry,* 44: 1582-1592.

Press, Berkeley, CA.

*Food Chemistry*, 47: 3367-3371.

*Economic Entomology,* 99: 864–872.

*Journal of Economic Entomology,* 86: 1131-1135.

34: 914-918.

application rate. *Pest Management Science*, 63: 1124-1132.

penetration. *Journal of Economic Entomology*. 103: 433-436.

soil at termiticidal application rates. *Pesticide Science* 42: 43-51.

on occurrence of Formosan subterranean termites (Isoptera: Rhinotermitidae) in

Kaufman, D. D., B. A. Russell, C. S. Helling, and A. Kayser. (1981). Movement of

Koehler, P.G., Su, N. –Y., Scheffrahn, R. H. & Oi, F.M. (2000). Baits to control subterranean

Kumar, M., & Philip, L. (2006). Adsorption and desorption characteristics of hydrophobic pesticide endosulfan in four Indian soils. *Chemosphere,* 62: 1064-1077. Kuriachan, I. & Gold, R. E. (1998). Evaluation of the ability of *Reticulitermes flavipes* Kollar, a

Lenz, M. (2009). Laboratory bioassays with subterranean termites (Isoptera) – the

Lenz, M., Barrett, R. A. & Williams, E. R.. (1984). Implications for comparability of

Li, X., He, J., & Li, S. (2007). Isolation of a chlorpyrifos-degrading bacterium, *Sphingomonas*

Lord, K. A., Mckinley, M. & Walker, N. (1982). Degradation of permethrin in soils.

Masters, G. M., (1991). Introduction to Environmental Engineering and Science, Prentice

Means, J. C., Wood, S. G. Hassett, J. J., & Banwart W. L. (1982). Sorption of amino-and

Mulrooney, J. E., & Gerard, P. D. (2007). Toxicity of fipronil in Mississippi soil types against *Reticulitermes flavipes* (Isoptera: Rhinotermitidae). *Sociobiology* 50: 63-70. Mulrooney, J. E., Wagner, T. L., Shelton, T. G., Peterson, C. J. & Gerard, P. D. (2007).

Ntow, W. J. (2005). Pesticide residues in Volta Lake, Ghana, Lakes Reservoirs. *Research and*

Osbrink, W. L. A., & Lax, A. R. (2002). Effect of tolerance to insecticides on substrate

sp. strain Dsp-2, and cloning of the mpd gene. *Research in Microbiology* 158(2):14–

carboxy-substituted polynuclead aromatic hydrocarbons by sediments and soils.

Historical review of termite activity at Forest Service termiticide test sites from 1971

penetration by Formosan subterranean termites (Isoptera: Rhinotermitidae). *Journal*

*Journal of Agricultural and Food Chemistry,* 29: 239-345.

Institute of Food and Agricultural Services.

*Environmental Toxicology & Chemistry* ,23: 1-6.

Sociobiology. 5: 197-203.

Hall, Englewood Cliffs, NJ.

*Management,* 10: 243-248.

*of Economic Entomology,* 95: 989-1000.

*Environmental Pollution,* 29 (2): 81-90.

*Environmental Science Technology,* 16: 93-98.

to 2004. *Journal of Economic Entomology,* 100: 488-494.

143.

importance of termite biology. *Sociobiology*, 53: 573-595.

cypermethrin, decamethrin, permethrin and their degradation productions in soil.

termites: the Sentricon system, ENY 2000, Florida Cooperative Extension Service,

subterranean termite (Isoptera: Rhinotermitidae), to differentiate between termiticide treated and untreated soils in laboratory tests. *Sociobiology,* 32: 151-166. Lee, S, Gan, J. Y., Kim, J. S., Kabashima, J. N. & Crowley, D. E. (2004). Microbial

transformation of pyrethroid insecticides in aqueous and sediment phases.

laboratory experiments revealed in studies on the effects of population density on vigor in *Coptotermes lacteus* (Froggatt) and *Nasutitermes exitious* (Hill) (Isoptera: Rhinotermitidae & Termitidae). *Bulletin of Entomological Research*. 74: 477-485. Lenz, M, Watson, J.A L., Barrett, R.A. & Runko, S. (1990). The effectiveness of insecticidal soil barriers against subterranean termites in Australia*. Sociobiology*, 17: 9-35. Lewis, D. L. (1980). Environmental and health aspects of termite control chemicals.

Factors Affecting Performance of Soil Termiticides 169

Su, N. -Y., Tamashiro, M., Yates, J. R. & Haverty, M. I. (1982). Effect of behavior on the

Su, N. -Y., Wheeler, G. S. & Scheffrahn, R. H. (1995). Subterranean termite (Isoptera:

Sunti, L. R., Shiu, W. Y., Mackay, D., Sieber, J. N. & Glotfelty, D. (1988). Critical review of

Tamashiro, M., Yates, J. R. & Ebesu, R. H. (1987). The Formosan termite in Hawaii: problems

Thorne, B. L. & Breisch, N. L. (2001). Effects of sublethal exposure to imidacloprid on

USEPA. (1986). U.S. Environmental Protection Agency. Pesticide fact sheet: chlordane. U.S.

USEPA. (2001). U.S. Environmental Protection Agency. Pesticide fact sheet: chlorfenapyr.

USEPA. (2000). U.S. Environmental Protection Agency. Pesticide fact sheet. Indoxacarb. U.S.

USEPA. (2008). U.S. Environmental Protection Agency. (2008). Pesticide fact sheet: chlorantraniliprole. U.S. Environmental Protection Agency. Washington, DC.

Ware, G.W. (2000). The Pesticide Book 5th Ed. Thompson Publications. Fresno, CA. 386

Wauchope, R. D., Yeh, S., Linders, J., Kloskowski, R., Tanaka, K., Rubin, B., Katayama, A.,

Wiltz, B. A. (2010). Laboratory Evaluation of Effects of Soil Properties on Termiticide

Wing, K. D., Sacher, M., Kagaya, Y., Tsurubuchi, Y., Mulderig, L., Connair, M. & Schnee, M.

Wood, T. G. & Pierce, M. J. (1991). Termites in Africa: The environmental impact of control

Worrall, F., Fernandez-Perez, M., Johnson, A. C., Flores-Cesperedes, F. & Gonzalez-Pradas,

pesticide leaching, *Journal of Contaminant Hydrology,* 49: 241–262.

Kördel, W., Gerstl, Z., Lane, M. & Unsworth, J. B. (2002). Review: Pesticide soil sorption parameters: theory, measurement, uses, limitations, and reliability. *Pest*

Performance against Formosan Subterranean Termites (Isoptera: Rhinotermitidae*).*

(2000). Bioactivation and mode of action of the oxadiazine indoxacarb in insects.

measures and damage to crops, trees, rangeland and rural buildings. *Sociobiology,*

E. (2001). Limitations on the role of incorporated organic matter in reducing

Rhinotermitidae). *Journal of Economic Entomology*, 94: 492–498.

Environmental Protection Agency. Washington, DC.

Environmental Protection Agency. Washington, DC.

U.S. Environmental Protection Agency. Washington, DC.

Wagner, T. L. (2003). U.S. Forest Service termiticide tests. *Sociobiology,* 41: 131–141.

subterranean termite. *Journal of Economic Entomology,* 75: 188-193.

termiticides. *Journal of Economic Entomology*, 88: 1690–1694.

Toxicology. 103: 1−59.

Hawaii, Honolulu.

pages.

*Management Science,* 58: 419–445.

*Sociobiology,* 56 (3): 755-773.

*Crop Protection*, 19: 537-545.

19: 221-234.

evaluation of insecticides for prevention of or remedial control of the Formosan

Rhinotermitidae) penetration into sand treated at various thicknesses with

Henry's law constants for pesticides. Reviews of Environmental Contamination &

and control, pp. 15-22. In Biology and control of the Formosan subterranean termite: M. Tamashiro and N. –Y. Su, eds., 67th Meeting of the Pacific Branch of the Entomological Society of America, Research Extension Series 083, University of

subsequent behavior of subterranean termite *Reticulitermes virginicus* (Isoptera:

Santos, C. A., DeSouza, O. & Guedes, R. N. C. (2004). Social facilitation attenuating

Saran, R. K., & Kamble, S. T. (2008). Concentration-dependent degradation of three

Saran, R. K. & Rust, M. K. (2007). The toxicity, uptake, and transfer efficiency of fipronil in

Shelton, T. G. & Grace, J. K. (2003). Effects of exposure duration on transfer of nonrepellent

Smith, B. C. & Zungoli, P. A. (1995). Rigid board insulation in South Carolina: its impact on

Smith, J. L. & Rust, M. K. (1990). Tunneling response and mortality of the western

Smith, J. L., & Rust, M. K. (1992). Activity of water-induced movement of termiticides in soil.

Smith, J. L. & Rust, M. K. (1993). Cellulose and clay in sand affects termiticide treatments.

Spomer, N. A., Kamble, S. T. & Siegfried, B. D. (2009). Bioavailability of chlorantraniliprole

Su, N.-Y. (1997). Protecting Historic Buildings and structures from termites. Cultural

Su, N. -Y. (2005). Response of the Formosan subterranean termites (Isoptera:

Su, N.-Y. & Scheffrahn, R. H. (1990a). Economically important termites in the United States

Su, N.-Y. & Scheffrahn, R. H. (1990b). Comparison of eleven soil termiticides against the

Su, N.-Y. & Scheffrahn, R. H. (1998). A review of subterranean termite control practices and

Su, N.-Y., Scheffrahn, R. H. & Ban P. M. (1993). Barrier efficacy of pyrethroid and

Rhinotermitidae). *Journal of Economic Entomology,* 83: 1918-1924.

Rhinotermitidae). *Journal of Economic Entomology,* 86: 772-776.

Rhinotermitidae*). Journal of Economic Entomology,* 96: 456–460.

various soils. *Journal of Economic Entomology,* 102: 1922-1927.

*Journal of Economic Entomology,* 83: 1395–1401.

*Journal of Economic Entomology,* 85: 430-434.

*Journal of Economic Entomology,* 86: 53-60.

http://crm.cr.nps.gov/issueindex.cfm.

and their control. *Sociobiology*, 17: 77-92.

*Reviews,* 3: 1 -13.

*Journal of Economic Entomology,* 98: 2143–2152.

539-546.

101: 1373-1383.

*Entomology,* 100: 495–508.

*Entomologist,* 78: 507-515.

insecticide-driven stress in termites (Isoptera: Nasutitermitinae). *Sociobiology*, 44:

termiticides in soil under laboratory conditions and their bioavailability to eastern subterranean termites (Isoptera: Rhinotermitidae). *Journal of Economic Entomology,*

western subterranean termites (Isoptera: Rhinotermitidae). *Journal of Economic*

termiticides among workers of *Coptotermes formosanus* Shiraki (Isoptera:

damage, inspection and control of termites (Isoptera: Rhinotermitidae). *Florida*

subterranean termite (Isoptera: Rhinotermitidae) to soil treated with termiticides.

and indoxacarb to eastern subterranean termites (Isoptera: Rhinotermitidae) in

Resource Management 20(7). National Park Service.

Rhinotermitidae) to baits or nonrepellent termiticides in extended foraging arenas.

Formosan subterranean termite and the eastern subterranean termite (Isoptera:

prospects for integrated pest management programs*. Integrated Pest Management*

organophosphate formulations against subterranean termites (Isoptera:

**9**

Eric J. Rebek1, Steven D. Frank2,

*1Oklahoma State University 2North Carolina State University*

> *3Texas A&M University United States of America*

Tom A. Royer1 and Carlos E. Bográn3

**Alternatives to Chemical Control of Insect Pests**

In 2011, practitioners and advocates of Integrated Pest Management (IPM) find themselves addressing agricultural, societal, and political pressures worldwide resulting from human population growth. This growth brings simultaneous burdens of sustaining a steady food supply; these include preventing losses from pests, dealing with increased human global travel, which in turn intensifies opportunities for the establishment of non-endemic pests into new ecosystems, and addressing global climate change that potentially will shift pest distributions into new areas. Concurrently, societal concerns about pesticide presence in our food and environment have resulted in political and economic pressures to reduce chemical pesticide use, or at a minimum, emphasize the development and use of products that are less toxic and more environmentally safe. These concerns drive the discovery and development of alternatives to chemical control of plant pathogens, weeds, and insect pests. The term Integrated Pest Management has, more often than not, been identified with entomologists. Stern et al. (1959) first used the term "integrated control" to describe the potential for integration of chemical and biological control tactics. Yet from a historical view, the concept of integrating chemical control with other tactics was proposed much earlier (Hoskins et al., 1939). Furthermore, integrating multiple non-chemical tactics to control a pest has been a cornerstone of the discipline of plant pathology throughout much of its early history (Jacobsen, 1997). In fact, because plant pathologists did not have an array of corrective pesticides available to them, the development and integration of control methods that emphasized non-pesticide controls (e.g., genetic host resistance, crop rotations, tillage, and plant sanitation) for plant diseases was a necessity, not simply an option for plant disease management. In contrast, entomologists and weed scientists were more insulated from that necessity due to the availability of relatively inexpensive pesticides to correct a problem. Several events stimulated the necessity for developing IPM programs in entomology, including those that emphasized development of non-chemical methods of insect control (e.g., cultural, biological, and physical control described herein). The chlorinated hydrocarbon, DDT, had been used for control of various insects since the 1950's. Soon after its use began, some pests began to develop resistance to DDT, including house flies, mosquitos, bed bugs, and body lice (Metcalf, 1989). The publication of Rachel Carson's book, "Silent Spring", in 1962 also generated public concern. Carson highlighted the negative

**1. Introduction**

### **Alternatives to Chemical Control of Insect Pests**

Eric J. Rebek1, Steven D. Frank2,

Tom A. Royer1 and Carlos E. Bográn3 *1Oklahoma State University 2North Carolina State University 3Texas A&M University United States of America*

#### **1. Introduction**

170 Insecticides – Basic and Other Applications

Xia, Y. & Brandenburg, R. L. (2000). Effect of irrigation on the efficacy of insecticides for

Xue, N., Zhang, D. & Xu, X., (2006). Organochlorinated pesticide multiresidues in surface sediments from Beijing Guanting reservoir. *Water Research,* 40: 183-194. Ying, G. G. & Kookana, R. S. (2006). Persistence and movement of fipronil termiticide with

courses. *Journal of Economic Entomology,* 93: 852–857.

2045–2050.

controlling two species of mole crickets (Orthoptera: Gryllotalpidae) on golf

under slab and trenching treatments. *Environmental Toxicology and Chemistry,* 25:

In 2011, practitioners and advocates of Integrated Pest Management (IPM) find themselves addressing agricultural, societal, and political pressures worldwide resulting from human population growth. This growth brings simultaneous burdens of sustaining a steady food supply; these include preventing losses from pests, dealing with increased human global travel, which in turn intensifies opportunities for the establishment of non-endemic pests into new ecosystems, and addressing global climate change that potentially will shift pest distributions into new areas. Concurrently, societal concerns about pesticide presence in our food and environment have resulted in political and economic pressures to reduce chemical pesticide use, or at a minimum, emphasize the development and use of products that are less toxic and more environmentally safe. These concerns drive the discovery and development of alternatives to chemical control of plant pathogens, weeds, and insect pests. The term Integrated Pest Management has, more often than not, been identified with entomologists. Stern et al. (1959) first used the term "integrated control" to describe the potential for integration of chemical and biological control tactics. Yet from a historical view, the concept of integrating chemical control with other tactics was proposed much earlier (Hoskins et al., 1939). Furthermore, integrating multiple non-chemical tactics to control a pest has been a cornerstone of the discipline of plant pathology throughout much of its early history (Jacobsen, 1997). In fact, because plant pathologists did not have an array of corrective pesticides available to them, the development and integration of control methods that emphasized non-pesticide controls (e.g., genetic host resistance, crop rotations, tillage, and plant sanitation) for plant diseases was a necessity, not simply an option for plant disease management. In contrast, entomologists and weed scientists were more insulated from that necessity due to the availability of relatively inexpensive pesticides to correct a problem.

Several events stimulated the necessity for developing IPM programs in entomology, including those that emphasized development of non-chemical methods of insect control (e.g., cultural, biological, and physical control described herein). The chlorinated hydrocarbon, DDT, had been used for control of various insects since the 1950's. Soon after its use began, some pests began to develop resistance to DDT, including house flies, mosquitos, bed bugs, and body lice (Metcalf, 1989). The publication of Rachel Carson's book, "Silent Spring", in 1962 also generated public concern. Carson highlighted the negative

Alternatives to Chemical Control of Insect Pests 173

Plant resistance to herbivores is a cultural control strategy having the most direct influence on herbivore behavior, fitness, and damage. Plant resistance is achieved through three general mechanisms: antibiosis, antixenosis, and tolerance. Antibiosis is the adverse effect of plant physical or chemical traits on arthropod biology (Painter, 1951). This may include reduced size, survival, fecundity, or longevity and increased development time or mortality. Antixenosis is the effect of plant traits on herbivore behavior that reduces herbivore interactions with the plant (Painter, 1951). These effects can include reduced feeding, preference, residence time, or oviposition on plants having particular traits such as trichomes or defensive compounds. Tolerance is a plant trait that reduces the impact of herbivory on plant growth, allowing tolerant plants to sustain herbivore damage but

Physical plant traits such as leaf pubescence, trichomes, and epicuticular wax, and chemical traits such as alkaloids and terpenoids have antibiotic and antixenotic effects on herbivores (Kennedy & Barbour, 1992; Painter, 1951). In the well-studied tomato production system, effects of leaf trichomes as a plant resistance trait are well documented (Kennedy, 2003; Simmons & Gurr, 2005). Trichomes and associated chemicals confer resistance to some tomato varieties against mites, aphids, whiteflies, beetles, and caterpillars (Gentile & Stoner, 1968; Heinz & Zalom, 1995; Kennedy, 2003; Kennedy & Sorenson, 1985; Simmons & Gurr, 2005). Trichomes are stiff hairs that sometimes contain chemical glands. Glandular trichomes have chemical exudates that confer resistance through antibiosis and kill or reduce longevity of pests feeding on them and entrap pests that forage on the leaves (Simmons & Gurr, 2005). Trichomes also have antixenotic effects on herbivore pests. Increasing trichome density can reduce oviposition by many species of beetles, caterpillars, true bugs, and mites. Of particular relevance is the effect of trichome density on whitefly and mites pests (Simmons & Gurr, 2005). The antibiotic and antixenotic effects of leaf pubescence on whitefly behavior and fitness have been studied in depth in a number of systems such as tomato, tobacco, cucurbits, and ornamental plants (Hoddle et al., 1998;

The soybean aphid offers a current example of how identifying pest resistance in crop plants can benefit IPM. Soybean aphid arrived in the U.S. from Asia in 2000 (Ragsdale et al., 2011). Since that time plant resistance conferred through antibiosis and antixenosis mechanisms has played an important role in mediating the economic impact of this pest on soybean yield (Ragsdale et al., 2011). Aphid fitness is negatively affected in resistant lines because it takes twice as long for aphids to probe into the phloem and initiate feeding (Diaz-Montano et al., 2007). Further, feeding bouts are reduced by more than 90% from less than 7 minutes per bout in resistant lines compared to greater than 60 minutes in susceptible lines (Diaz-Montano et al., 2007). Likewise, production of nymphs was reduced by 50-90% in resistant versus susceptible varieties, confirming antibiosis in resistant lines (Diaz-Montano et al., 2006; Hill et al., 2004). Antixenosis was also demonstrated in resistant varieties wherein adult aphids preferred to colonize susceptible over some resistant lines (Diaz-Montano et

In contrast to conventional breeding programs, plants can now be genetically modified to include lethal traits from other organisms, such as the bacterium, *Bacillus thuringiensis* (Bt). Bt genes are now used in many crop species to confer antibiosis in otherwise susceptible crops. Although we do not focus on this mode of plant resistance here, transgenic traits have had a tremendous effect on modern crop production and yield. However, like any

**2.1 Cultural control via plant resistance**

Inbar & Gerling, 2008).

al., 2006; Hill et al., 2004).

maintain yields similar to undamaged plants (Painter, 1951).

impacts that widespread use of insecticides could have on the environment and ultimately, human health. What followed was a passionate global reaction that generated intense economic and political pressure to regulate pesticide use and monitor their relative impacts on biological systems. In the United States, the Environmental Protection Agency was created and charged with regulating the registration of all pesticides through the Federal Insecticide, Fungicide and Rodenticide Act (as amended in 1972). Concerns over pesticide use also stimulated the political thrust necessary for support of IPM programs. In the United States and worldwide, IPM flourished in the following three decades and was adopted as policy by various governments (Kogan, 1998).

Today, IPM has attained many successes but fallen short on some issues. Due to the awareness and biological understanding of how insecticide resistance develops, and because insecticides are so expensive to develop, in 1984 the manufacturers of insecticides created the Insecticide Resistance Action Committee (IRAC) to encourage the responsible use of their products in a manner that minimizes the risk of insecticide in target pest populations (IRAC, 2010). New calls have been made for changing the direction of IPM in response to waning political support for funding IPM programs. Frisbie & Smith (1989) coined the term "biologically intensive" IPM, which involves reliance on ecological methods of control based on knowledge of a pest's biology. Benbrook et al. (1996) promoted the idea of moving IPM along a continuum from simple to complex, or 'biointensive". The National Research Council officially introduced the term, "Ecologically Based Pest Management", calling for a new paradigm for IPM in the 21st Century (National Research Council, 1996); eight years earlier, however, Horn (1988) outlined how principles of insect ecology could be incorporated into insect pest management strategies. More recently, Koul & Cuperus (2007) published "Ecologically Based Integrated Pest Management", essentially capturing the breadth and depth of the evolution that IPM has undergone over the past 60 years. While the scope of the "New Solutions" aspect of the NRC's charge has been challenged (Kogan, 1998; Royer et al., 1999), the term "ecologically based" has become infused into the IPM lexicon.

#### **2. Cultural control methods to reduce insecticide applications**

Cultural controls are management tools and activities that make the crop habitat less favorable for pests to survive and cause damage (Horne & Page, 2008). Cultural management practices may make the crop or habitat inhospitable to pests directly, for example, by planting cultivars resistant to pest feeding or rotating crops to deny overwintering pests their preferred food source. Cultural management practices can also make the habitat less hospitable to pests in an indirect manner by encouraging natural enemies (predators and parasitoids) to enhance biological control (see Section 3).

Cultural control is a key pest management tool available to growers because the crop variety, habitat, and selected inputs set the stage for future pest fitness and abundance. Thus, implementing preventive cultural control tactics that slow pest population growth can delay or negate the need for insecticide applications and significant plant damage. In this section we outline the major types of cultural control tactics available to growers and other pest management personnel. Our objective is to demonstrate the breadth of tactics that are used, although we do not have the space to consider them in depth. We draw examples from a diversity of well-studied plant systems from field crops to ornamental landscapes to provide examples of how they affect plant-herbivore-natural enemy interactions to reduce pest abundance and damage.

impacts that widespread use of insecticides could have on the environment and ultimately, human health. What followed was a passionate global reaction that generated intense economic and political pressure to regulate pesticide use and monitor their relative impacts on biological systems. In the United States, the Environmental Protection Agency was created and charged with regulating the registration of all pesticides through the Federal Insecticide, Fungicide and Rodenticide Act (as amended in 1972). Concerns over pesticide use also stimulated the political thrust necessary for support of IPM programs. In the United States and worldwide, IPM flourished in the following three decades and was adopted as

Today, IPM has attained many successes but fallen short on some issues. Due to the awareness and biological understanding of how insecticide resistance develops, and because insecticides are so expensive to develop, in 1984 the manufacturers of insecticides created the Insecticide Resistance Action Committee (IRAC) to encourage the responsible use of their products in a manner that minimizes the risk of insecticide in target pest populations (IRAC, 2010). New calls have been made for changing the direction of IPM in response to waning political support for funding IPM programs. Frisbie & Smith (1989) coined the term "biologically intensive" IPM, which involves reliance on ecological methods of control based on knowledge of a pest's biology. Benbrook et al. (1996) promoted the idea of moving IPM along a continuum from simple to complex, or 'biointensive". The National Research Council officially introduced the term, "Ecologically Based Pest Management", calling for a new paradigm for IPM in the 21st Century (National Research Council, 1996); eight years earlier, however, Horn (1988) outlined how principles of insect ecology could be incorporated into insect pest management strategies. More recently, Koul & Cuperus (2007) published "Ecologically Based Integrated Pest Management", essentially capturing the breadth and depth of the evolution that IPM has undergone over the past 60 years. While the scope of the "New Solutions" aspect of the NRC's charge has been challenged (Kogan, 1998; Royer et al., 1999), the term "ecologically based" has become infused into the IPM

**2. Cultural control methods to reduce insecticide applications**

enemies (predators and parasitoids) to enhance biological control (see Section 3).

Cultural controls are management tools and activities that make the crop habitat less favorable for pests to survive and cause damage (Horne & Page, 2008). Cultural management practices may make the crop or habitat inhospitable to pests directly, for example, by planting cultivars resistant to pest feeding or rotating crops to deny overwintering pests their preferred food source. Cultural management practices can also make the habitat less hospitable to pests in an indirect manner by encouraging natural

Cultural control is a key pest management tool available to growers because the crop variety, habitat, and selected inputs set the stage for future pest fitness and abundance. Thus, implementing preventive cultural control tactics that slow pest population growth can delay or negate the need for insecticide applications and significant plant damage. In this section we outline the major types of cultural control tactics available to growers and other pest management personnel. Our objective is to demonstrate the breadth of tactics that are used, although we do not have the space to consider them in depth. We draw examples from a diversity of well-studied plant systems from field crops to ornamental landscapes to provide examples of how they affect plant-herbivore-natural enemy interactions to reduce

policy by various governments (Kogan, 1998).

lexicon.

pest abundance and damage.

#### **2.1 Cultural control via plant resistance**

Plant resistance to herbivores is a cultural control strategy having the most direct influence on herbivore behavior, fitness, and damage. Plant resistance is achieved through three general mechanisms: antibiosis, antixenosis, and tolerance. Antibiosis is the adverse effect of plant physical or chemical traits on arthropod biology (Painter, 1951). This may include reduced size, survival, fecundity, or longevity and increased development time or mortality. Antixenosis is the effect of plant traits on herbivore behavior that reduces herbivore interactions with the plant (Painter, 1951). These effects can include reduced feeding, preference, residence time, or oviposition on plants having particular traits such as trichomes or defensive compounds. Tolerance is a plant trait that reduces the impact of herbivory on plant growth, allowing tolerant plants to sustain herbivore damage but maintain yields similar to undamaged plants (Painter, 1951).

Physical plant traits such as leaf pubescence, trichomes, and epicuticular wax, and chemical traits such as alkaloids and terpenoids have antibiotic and antixenotic effects on herbivores (Kennedy & Barbour, 1992; Painter, 1951). In the well-studied tomato production system, effects of leaf trichomes as a plant resistance trait are well documented (Kennedy, 2003; Simmons & Gurr, 2005). Trichomes and associated chemicals confer resistance to some tomato varieties against mites, aphids, whiteflies, beetles, and caterpillars (Gentile & Stoner, 1968; Heinz & Zalom, 1995; Kennedy, 2003; Kennedy & Sorenson, 1985; Simmons & Gurr, 2005). Trichomes are stiff hairs that sometimes contain chemical glands. Glandular trichomes have chemical exudates that confer resistance through antibiosis and kill or reduce longevity of pests feeding on them and entrap pests that forage on the leaves (Simmons & Gurr, 2005). Trichomes also have antixenotic effects on herbivore pests. Increasing trichome density can reduce oviposition by many species of beetles, caterpillars, true bugs, and mites. Of particular relevance is the effect of trichome density on whitefly and mites pests (Simmons & Gurr, 2005). The antibiotic and antixenotic effects of leaf pubescence on whitefly behavior and fitness have been studied in depth in a number of systems such as tomato, tobacco, cucurbits, and ornamental plants (Hoddle et al., 1998; Inbar & Gerling, 2008).

The soybean aphid offers a current example of how identifying pest resistance in crop plants can benefit IPM. Soybean aphid arrived in the U.S. from Asia in 2000 (Ragsdale et al., 2011). Since that time plant resistance conferred through antibiosis and antixenosis mechanisms has played an important role in mediating the economic impact of this pest on soybean yield (Ragsdale et al., 2011). Aphid fitness is negatively affected in resistant lines because it takes twice as long for aphids to probe into the phloem and initiate feeding (Diaz-Montano et al., 2007). Further, feeding bouts are reduced by more than 90% from less than 7 minutes per bout in resistant lines compared to greater than 60 minutes in susceptible lines (Diaz-Montano et al., 2007). Likewise, production of nymphs was reduced by 50-90% in resistant versus susceptible varieties, confirming antibiosis in resistant lines (Diaz-Montano et al., 2006; Hill et al., 2004). Antixenosis was also demonstrated in resistant varieties wherein adult aphids preferred to colonize susceptible over some resistant lines (Diaz-Montano et al., 2006; Hill et al., 2004).

In contrast to conventional breeding programs, plants can now be genetically modified to include lethal traits from other organisms, such as the bacterium, *Bacillus thuringiensis* (Bt). Bt genes are now used in many crop species to confer antibiosis in otherwise susceptible crops. Although we do not focus on this mode of plant resistance here, transgenic traits have had a tremendous effect on modern crop production and yield. However, like any

Alternatives to Chemical Control of Insect Pests 175

theoretical and empirical research suggests that multiple resistance traits or genes and a combination of different modes of action such as antibiosis and antixenosis should confer more stable resistance to crops. In addition, mixing resistant and susceptible varieties in the same field can reduce evolution of resistance by insect pest populations (Gould, 1986, 1998).

Plant fertility and water stress play a major role in plant susceptibility to herbivore feeding, tolerance to herbivore damage, and herbivore population growth. Nitrogen can be a limiting nutrient for herbivorous insects due to the nitrogen-poor quality of their host plants (Mattson, 1980). Therefore, increasing nitrogen concentration within plants by applying fertilizer has a tendency to increase plant quality for herbivores (Mattson, 1980). Increasing foliar nitrogen can reduce pest development time and increase survival and fecundity, leading to more rapid population growth (Mattson, 1980). Research in potato crops has found that increasing nitrogen fertilization increases leaf consumption, reduces development time, and increases abundance of Colorado potato beetles (Boiteau et al., 2008). Likewise, in greenhouse ornamental production, increasing fertilization increases the fecundity, body size, and development rate of citrus mealybug (Hogendorp et al., 2006), and through similar mechanisms increases population growth rates of whiteflies, thrips, aphids, and spider mites (Bentz et al., 1995; Chau et al., 2005; Chau & Heinz, 2006; Chow et al.,

In ornamental landscapes, fertilizer is often applied to improve the growth of trees and other plants and increase their resistance to abiotic and biotic stress, including herbivore feeding. However, nitrogen fertilization of trees has been shown to reduce plant resistance to many arthropod pests (Herms, 2002; Kytö et al., 1996). This reduced resistance occurs through a combination of fertilizer effects on plant nutrition for herbivores and defense against herbivores (Herms & Mattson, 1992). Herms & Mattson (1992) hypothesized that as nitrogen fertilization stimulates rapid plant growth, carbon available for production of defensive compounds is limited. Thus, over-fertilization of trees, shrubs, and other plants provides a dual benefit to many herbivores via increased nitrogen availability and decreased

Pesticide applications are often an essential aspect of plant culture. Managing the type and frequency of applications is a cultural control tactic with well-documented implications. Insecticides can disrupt natural enemy communities and biological control via several mechanisms. Direct toxicity of pyrethroids and organophosphates to natural enemies has been documented frequently (Desneux et al., 2004b; see Galvan et al., 2005). Direct toxicity of insecticides to natural enemies results in smaller natural enemy populations on crop and landscape plants (Frank & Sadof, *in press*; Raupp et al., 2001). Insecticides also cause sublethal effects in parasitoids and predators. For example, the pyrethroid, lambdacyhalothrin, disrupts the host location and oviposition behavior of *Aphidius ervi*, resulting in

Non-target impacts on natural enemy communities are not limited to contact insecticides. Systemic neonicotinoids such as imidacloprid and thiamethoxam have lethal and sublethal effects on natural enemy development, fitness, and efficacy (Cloyd & Bethke, 2009; Desneux et al., 2007). These compounds can reduce survival of developing parasitoids and intoxicate

**2.2 Cultural control via fertility management**

defensive compounds (Raupp et al., 2010).

**2.3 Cultural control via pesticide selection and management**

lower parasitism rates of aphids (Desneux et al., 2004a).

2009).

management tactic, Bt crops do not function in a vacuum and effects on natural enemies and other non-targets, secondary pest outbreaks, and evolution of pest resistance have been intensely studied (Gould, 1998; O'Callaghan et al., 2005; Shelton et al., 2002).

#### **2.1.1 Interaction of plant resistance traits and biological control**

Effects of plant resistance and biological control can be contradictory, complementary, or synergistic (Cai et al., 2009; Farid et al., 1998; Johnson & Gould, 1992). Plant resistance can work in conjunction with natural enemies to maintain low pest abundance and damage. In general, natural enemies have slower population growth rates than pests. Thus, by reducing pest population growth rates, plant resistance may help natural enemies better regulate pest populations. For example, research in wheat systems has shown that aphid-resistant wheat varieties do not have negative effects on parasitoid life history parameters such as size and development time (Farid et al., 1998). Parasitism rates may be equal or greater on resistant varieties, which when combined with reduced aphid population growth due to host plant resistance, can improve pest management dramatically (Cai et al., 2009).

Just as trichome exudates reduce herbivore survival they can also have negative effects on natural enemies. Survival and development of natural enemies may be reduced by poisoning or entrapping them, and natural enemy foraging efficiency, predation, or parasitism rate may be inhibited (Kaufman & Kennedy, 1989a, b; Obrycki & Tauber, 1984; Simmons & Gurr, 2005). For example, increasing trichome density and related changes in chemical composition of tomato leaves reduced the walking speed, parasitism rate, and survival of the egg parasitoid, *Trichogramma pretiosum* (Kashyap et al., 1991a, b). Tiny whitefly parasitoids in the genera, *Eretmocerus* and *Encarsia*, are highly affected by plant pubescence and trichome density (Hoddle et al., 1998; van Lenteren et al., 1995). Biological control may be disrupted because these parasitoids avoid highly pubescent plants. Once on the plants, pubescence reduces walking speed, foraging efficiency, oviposition, and parasitism rate (De Barro et al., 2000; Headrick et al., 1996; Hoddle et al., 1998; Inbar & Gerling, 2008).

Trichomes and other plant resistance traits also affect predator behavior and efficacy. Predatory mites used in biological control of spider mite, *Tetranychus urticae*, are readily trapped by trichomes and forage less efficiently due to reduced mobility (Nihoul, 1993a; van Haren et al., 1987). The consequence of mortality and reduced foraging efficiency is reduced biological control on cultivars with high trichome density, although the effect is also dependent on environmental factors such as temperature (Nihoul 1993a, b). Likewise, foraging efficiency of the spotted lady beetle, *Coleomegilla maculata*, and the bigeyed bug, *Geocoris punctipes*, was reduced by high trichome density, resulting in less predation of *Heliothis zea* eggs (Barbour et al., 1993, 1997). Increasing pubescence on poinsettia leaves by just 15% reduced oviposition and whitefly predation by *Delphastus catalinae* and other predators (Heinz & Parrella, 1994).

#### **2.1.2 Herbivore resistance to plant resistance traits**

Herbivores are in a constant evolutionary arms race with plants to overcome resistance traits (Ehrlich & Raven, 1964). It is not surprising then that pests have developed physiological resistance to genetically modified and conventional plant resistance traits (Gould, 1998). For example, certain soybean aphid biotypes are resistant to Rag1 or Rag2 genes that confer resistance to soybean plants (Hill et al., 2009, 2010). Evidence from

management tactic, Bt crops do not function in a vacuum and effects on natural enemies and other non-targets, secondary pest outbreaks, and evolution of pest resistance have been

Effects of plant resistance and biological control can be contradictory, complementary, or synergistic (Cai et al., 2009; Farid et al., 1998; Johnson & Gould, 1992). Plant resistance can work in conjunction with natural enemies to maintain low pest abundance and damage. In general, natural enemies have slower population growth rates than pests. Thus, by reducing pest population growth rates, plant resistance may help natural enemies better regulate pest populations. For example, research in wheat systems has shown that aphid-resistant wheat varieties do not have negative effects on parasitoid life history parameters such as size and development time (Farid et al., 1998). Parasitism rates may be equal or greater on resistant varieties, which when combined with reduced aphid population growth due to host plant

Just as trichome exudates reduce herbivore survival they can also have negative effects on natural enemies. Survival and development of natural enemies may be reduced by poisoning or entrapping them, and natural enemy foraging efficiency, predation, or parasitism rate may be inhibited (Kaufman & Kennedy, 1989a, b; Obrycki & Tauber, 1984; Simmons & Gurr, 2005). For example, increasing trichome density and related changes in chemical composition of tomato leaves reduced the walking speed, parasitism rate, and survival of the egg parasitoid, *Trichogramma pretiosum* (Kashyap et al., 1991a, b). Tiny whitefly parasitoids in the genera, *Eretmocerus* and *Encarsia*, are highly affected by plant pubescence and trichome density (Hoddle et al., 1998; van Lenteren et al., 1995). Biological control may be disrupted because these parasitoids avoid highly pubescent plants. Once on the plants, pubescence reduces walking speed, foraging efficiency, oviposition, and parasitism rate (De Barro et al., 2000; Headrick et al., 1996; Hoddle et al., 1998; Inbar &

Trichomes and other plant resistance traits also affect predator behavior and efficacy. Predatory mites used in biological control of spider mite, *Tetranychus urticae*, are readily trapped by trichomes and forage less efficiently due to reduced mobility (Nihoul, 1993a; van Haren et al., 1987). The consequence of mortality and reduced foraging efficiency is reduced biological control on cultivars with high trichome density, although the effect is also dependent on environmental factors such as temperature (Nihoul 1993a, b). Likewise, foraging efficiency of the spotted lady beetle, *Coleomegilla maculata*, and the bigeyed bug, *Geocoris punctipes*, was reduced by high trichome density, resulting in less predation of *Heliothis zea* eggs (Barbour et al., 1993, 1997). Increasing pubescence on poinsettia leaves by just 15% reduced oviposition and whitefly predation by *Delphastus catalinae* and other

Herbivores are in a constant evolutionary arms race with plants to overcome resistance traits (Ehrlich & Raven, 1964). It is not surprising then that pests have developed physiological resistance to genetically modified and conventional plant resistance traits (Gould, 1998). For example, certain soybean aphid biotypes are resistant to Rag1 or Rag2 genes that confer resistance to soybean plants (Hill et al., 2009, 2010). Evidence from

intensely studied (Gould, 1998; O'Callaghan et al., 2005; Shelton et al., 2002).

**2.1.1 Interaction of plant resistance traits and biological control**

resistance, can improve pest management dramatically (Cai et al., 2009).

Gerling, 2008).

predators (Heinz & Parrella, 1994).

**2.1.2 Herbivore resistance to plant resistance traits**

theoretical and empirical research suggests that multiple resistance traits or genes and a combination of different modes of action such as antibiosis and antixenosis should confer more stable resistance to crops. In addition, mixing resistant and susceptible varieties in the same field can reduce evolution of resistance by insect pest populations (Gould, 1986, 1998).

#### **2.2 Cultural control via fertility management**

Plant fertility and water stress play a major role in plant susceptibility to herbivore feeding, tolerance to herbivore damage, and herbivore population growth. Nitrogen can be a limiting nutrient for herbivorous insects due to the nitrogen-poor quality of their host plants (Mattson, 1980). Therefore, increasing nitrogen concentration within plants by applying fertilizer has a tendency to increase plant quality for herbivores (Mattson, 1980). Increasing foliar nitrogen can reduce pest development time and increase survival and fecundity, leading to more rapid population growth (Mattson, 1980). Research in potato crops has found that increasing nitrogen fertilization increases leaf consumption, reduces development time, and increases abundance of Colorado potato beetles (Boiteau et al., 2008). Likewise, in greenhouse ornamental production, increasing fertilization increases the fecundity, body size, and development rate of citrus mealybug (Hogendorp et al., 2006), and through similar mechanisms increases population growth rates of whiteflies, thrips, aphids, and spider mites (Bentz et al., 1995; Chau et al., 2005; Chau & Heinz, 2006; Chow et al., 2009).

In ornamental landscapes, fertilizer is often applied to improve the growth of trees and other plants and increase their resistance to abiotic and biotic stress, including herbivore feeding. However, nitrogen fertilization of trees has been shown to reduce plant resistance to many arthropod pests (Herms, 2002; Kytö et al., 1996). This reduced resistance occurs through a combination of fertilizer effects on plant nutrition for herbivores and defense against herbivores (Herms & Mattson, 1992). Herms & Mattson (1992) hypothesized that as nitrogen fertilization stimulates rapid plant growth, carbon available for production of defensive compounds is limited. Thus, over-fertilization of trees, shrubs, and other plants provides a dual benefit to many herbivores via increased nitrogen availability and decreased defensive compounds (Raupp et al., 2010).

#### **2.3 Cultural control via pesticide selection and management**

Pesticide applications are often an essential aspect of plant culture. Managing the type and frequency of applications is a cultural control tactic with well-documented implications. Insecticides can disrupt natural enemy communities and biological control via several mechanisms. Direct toxicity of pyrethroids and organophosphates to natural enemies has been documented frequently (Desneux et al., 2004b; see Galvan et al., 2005). Direct toxicity of insecticides to natural enemies results in smaller natural enemy populations on crop and landscape plants (Frank & Sadof, *in press*; Raupp et al., 2001). Insecticides also cause sublethal effects in parasitoids and predators. For example, the pyrethroid, lambdacyhalothrin, disrupts the host location and oviposition behavior of *Aphidius ervi*, resulting in lower parasitism rates of aphids (Desneux et al., 2004a).

Non-target impacts on natural enemy communities are not limited to contact insecticides. Systemic neonicotinoids such as imidacloprid and thiamethoxam have lethal and sublethal effects on natural enemy development, fitness, and efficacy (Cloyd & Bethke, 2009; Desneux et al., 2007). These compounds can reduce survival of developing parasitoids and intoxicate

Alternatives to Chemical Control of Insect Pests 177

and Northern corn rootworm *Diabrotica barberi*, damage in corn (Levine & Oloumi-Sadeghi, 1991; Spencer et al., 2009). Corn rootworm eggs overwinter in corn fields and larvae are present to feed on corn roots the following year (Spencer et al., 2009). Therefore, rotating to a different crop such as soybeans denies food to hatching rootworm larvae (Spencer et al., 2009). Likewise, corn planted after soybeans or other crops has less rootworm damage because the field is free of overwintering eggs and larvae. However, Western and Northern corn rootworm populations eventually developed resistance to this strategy (Gray et al., 2009; Levine et al., 2002; Spencer & Levine, 2008). Northern corn rootworms circumvent crop rotation by prolonging egg diapause for two winters instead of one (Chiang, 1965; Levine et al., 1992). Therefore, larvae hatch when fields are replanted in corn two years after the eggs were laid. Western corn rootworm has become resistant to crop rotation by a behavioral rather than physiological mechanism. Western corn rootworm adults move from corn fields to soybean and other crop fields, feeding on soybean leaves and ovipositing in soybean fields (Levine et al., 2002). Selection pressure imposed by rotation of two primary crops, corn and soybeans, strongly rewarded female beetles that strayed from corn for

Other planting practices such as delayed planting dates can also benefit pest control. Hessian fly is an introduced pest of winter wheat that has been in the U.S. since the 1700's. Prior to the development of resistant wheat varieties, growers exploited the fly's life cycle to reduce damage to winter wheat crops. Hessian fly adults become active in the fall when they oviposit in wheat and other grasses. By planting after a "fly free date" when fly activity subsides, winter wheat is protected from oviposition from the fall hessian fly generation (Buntin et al., 1991). This is a perfect example of how simple changes in plant culture can reduce the need for insecticide applications, increase yield, and provide economic benefit to

Many definitions of biological control have been published in the literature since the term was first used by H.S. Smith more than 90 years ago (Caltagirone & Huffaker, 1980; Cook, 1987; Coppel & Mertins, 1977; DeBach & Rosen, 1991; Garcia et al., 1988; see Huffaker & Messenger, 1976; Perkins & Garcia, 1999; Rabb, 1972; Smith, 1919). In its strictest sense, biological control is the use of beneficial organisms to reduce the relative abundance of, and damage caused by, noxious ones. This definition attributes economic rather than biological characters to organisms that fall into two categories, beneficial and noxious, based on their positive or negative impact on human-valued resources. It is also important to distinguish *biological* from *natural* control, which does not require human intervention, and from similar methods of pest control that do not involve whole (living) organisms (Huffaker et al., 1984). In fact, biological control involves interspecific, population-level processes by way of predation, parasitism, competition, or a combination of these mechanisms (van Driesche & Bellows, 1996). In practice, the effectiveness and appropriateness of biological control methods rely on real-time evolutionary forces that shape the beneficial organism's genotype, phenotype, and performance. This is not the case for similar, biologically based methods such as the application of insecticides formulated with pathogens, antagonists, or their byproducts. Furthermore, in its strictest definition, biological control does not include the deployment of pest-tolerant organisms, regardless of the source or origin of the resistance-

oviposition.

growers (Buntin et al., 1992).

**3. Biological control of insect pests**

conferring characters (e.g., Bt crops) (see Perkins & Garcia, 1999).

predators such as lady beetles and lacewing larvae exposed to the chemicals topically or by feeding on exposed prey (Moser & Obrycki, 2009; Papachristos & Milonas, 2008; Smith & Krischik, 1999; Szczepaniec et al., 2011). Parasitoids are also affected negatively via feeding on plant nectar or hosts exposed to the chemicals (Krischik et al., 2007; Rebek & Sadof, 2003). The consequence of disrupting natural enemy populations can be outbreaks of primary or secondary pests due to the loss of underlying biological control services (Raupp et al., 2010). Considerable work has documented this effect in field crops, orchards, vineyards, and landscape ornamentals (Penman & Chapman, 1988; Raupp et al., 2010). The effect is particularly prevalent among spider mites and scale insects that are not killed as easily as their natural enemies by insecticide applications. Pyrethroids and other broad-spectrum insecticides have direct and indirect effects on spider mites that can promote mite outbreaks. First, pyrethroids promote spider mite dispersal from treated to untreated areas of reduced competition (Iftner & Hall, 1983; Penman & Chapman, 1983). Spider mites have many predators including lady beetles, predatory bugs, lacewing larvae, and predatory mites. Pyrethroids can promote outbreaks of spider mites indirectly by killing the natural enemies that otherwise help suppress spider mite populations (Penman & Chapman, 1988).

Predatory mites in the family Phytoseiidae feed on spider mite eggs, juveniles, and adults and are effective at reducing spider mite abundance and damage on plants (McMurtry & Croft, 1997). In addition, phytoseiid mites often respond with a numerical increase to burgeoning spider mite populations via aggregation and increased reproduction. However, the abundance and efficacy of phytoseiid mites depends in large part on plant culture practices and plant characteristics. Phytoseiid mites are extremely susceptible to insecticides such as pyrethroids, organophosphates, and carbamates (Hardman et al., 1988). In many cases, phytoseiids have been found to be more vulnerable to these insecticides than spider mites (e.g., Sanford, 1967; Wong and Chapman, 1979). Therefore, by killing a disproportionate number of predatory mites compared to target pests, broad-spectrum insecticides frequently lead to spider mite outbreaks (Hardman et al., 1988). Similar dynamics have been demonstrated for scale insects, which are generally not killed by cover sprays of contact insecticides due to their protective cover. Moreover, by drastically reducing natural enemy abundance and efficacy, these insecticide applications create enemy-free space for scales, which can result in outbreak populations (McClure, 1977; Raupp et al., 2001).

Insecticide applications can directly benefit pest reproduction and survival through a process known as hormoligosis. Increased spider mite fecundity has been demonstrated after exposure to sublethal doses of pyrethroids (Iftner & Hall, 1984; Jones & Parrella, 1984). However, this is most evident in spider mites that frequently outbreak after applications of the neonicotinoid, imidacloprid (Gupta & Krischik, 2007; Raupp et al., 2004; Sclar et al., 1998; Szczepaniec et al., 2011). Outbreaks are triggered in part by negative effects on predators, but also by greater fecundity of spider mites that feed on imidacloprid-treated foliage (Szczepaniec et al., 2011). Although not commonly observed, this phenomenon points out another reason for proper insecticide management as a cultural control strategy.

#### **2.4 Cultural control via crop rotation and planting practices**

Exploiting the biological limitations of the pest to minimize insecticide applications is the essence of cultural control tactics such as crop rotation. This strategy has been used successfully to control corn rootworm for over 100 years (Forbes, 1883). Crop rotation has been highly effective as a tool to reduce Western corn rootworm, *Diabrotica virgifera virgifera,*

predators such as lady beetles and lacewing larvae exposed to the chemicals topically or by feeding on exposed prey (Moser & Obrycki, 2009; Papachristos & Milonas, 2008; Smith & Krischik, 1999; Szczepaniec et al., 2011). Parasitoids are also affected negatively via feeding on plant nectar or hosts exposed to the chemicals (Krischik et al., 2007; Rebek & Sadof, 2003). The consequence of disrupting natural enemy populations can be outbreaks of primary or secondary pests due to the loss of underlying biological control services (Raupp et al., 2010). Considerable work has documented this effect in field crops, orchards, vineyards, and landscape ornamentals (Penman & Chapman, 1988; Raupp et al., 2010). The effect is particularly prevalent among spider mites and scale insects that are not killed as easily as their natural enemies by insecticide applications. Pyrethroids and other broad-spectrum insecticides have direct and indirect effects on spider mites that can promote mite outbreaks. First, pyrethroids promote spider mite dispersal from treated to untreated areas of reduced competition (Iftner & Hall, 1983; Penman & Chapman, 1983). Spider mites have many predators including lady beetles, predatory bugs, lacewing larvae, and predatory mites. Pyrethroids can promote outbreaks of spider mites indirectly by killing the natural enemies

that otherwise help suppress spider mite populations (Penman & Chapman, 1988).

Raupp et al., 2001).

Predatory mites in the family Phytoseiidae feed on spider mite eggs, juveniles, and adults and are effective at reducing spider mite abundance and damage on plants (McMurtry & Croft, 1997). In addition, phytoseiid mites often respond with a numerical increase to burgeoning spider mite populations via aggregation and increased reproduction. However, the abundance and efficacy of phytoseiid mites depends in large part on plant culture practices and plant characteristics. Phytoseiid mites are extremely susceptible to insecticides such as pyrethroids, organophosphates, and carbamates (Hardman et al., 1988). In many cases, phytoseiids have been found to be more vulnerable to these insecticides than spider mites (e.g., Sanford, 1967; Wong and Chapman, 1979). Therefore, by killing a disproportionate number of predatory mites compared to target pests, broad-spectrum insecticides frequently lead to spider mite outbreaks (Hardman et al., 1988). Similar dynamics have been demonstrated for scale insects, which are generally not killed by cover sprays of contact insecticides due to their protective cover. Moreover, by drastically reducing natural enemy abundance and efficacy, these insecticide applications create enemy-free space for scales, which can result in outbreak populations (McClure, 1977;

Insecticide applications can directly benefit pest reproduction and survival through a process known as hormoligosis. Increased spider mite fecundity has been demonstrated after exposure to sublethal doses of pyrethroids (Iftner & Hall, 1984; Jones & Parrella, 1984). However, this is most evident in spider mites that frequently outbreak after applications of the neonicotinoid, imidacloprid (Gupta & Krischik, 2007; Raupp et al., 2004; Sclar et al., 1998; Szczepaniec et al., 2011). Outbreaks are triggered in part by negative effects on predators, but also by greater fecundity of spider mites that feed on imidacloprid-treated foliage (Szczepaniec et al., 2011). Although not commonly observed, this phenomenon points out

Exploiting the biological limitations of the pest to minimize insecticide applications is the essence of cultural control tactics such as crop rotation. This strategy has been used successfully to control corn rootworm for over 100 years (Forbes, 1883). Crop rotation has been highly effective as a tool to reduce Western corn rootworm, *Diabrotica virgifera virgifera,*

another reason for proper insecticide management as a cultural control strategy.

**2.4 Cultural control via crop rotation and planting practices**

and Northern corn rootworm *Diabrotica barberi*, damage in corn (Levine & Oloumi-Sadeghi, 1991; Spencer et al., 2009). Corn rootworm eggs overwinter in corn fields and larvae are present to feed on corn roots the following year (Spencer et al., 2009). Therefore, rotating to a different crop such as soybeans denies food to hatching rootworm larvae (Spencer et al., 2009). Likewise, corn planted after soybeans or other crops has less rootworm damage because the field is free of overwintering eggs and larvae. However, Western and Northern corn rootworm populations eventually developed resistance to this strategy (Gray et al., 2009; Levine et al., 2002; Spencer & Levine, 2008). Northern corn rootworms circumvent crop rotation by prolonging egg diapause for two winters instead of one (Chiang, 1965; Levine et al., 1992). Therefore, larvae hatch when fields are replanted in corn two years after the eggs were laid. Western corn rootworm has become resistant to crop rotation by a behavioral rather than physiological mechanism. Western corn rootworm adults move from corn fields to soybean and other crop fields, feeding on soybean leaves and ovipositing in soybean fields (Levine et al., 2002). Selection pressure imposed by rotation of two primary crops, corn and soybeans, strongly rewarded female beetles that strayed from corn for oviposition.

Other planting practices such as delayed planting dates can also benefit pest control. Hessian fly is an introduced pest of winter wheat that has been in the U.S. since the 1700's. Prior to the development of resistant wheat varieties, growers exploited the fly's life cycle to reduce damage to winter wheat crops. Hessian fly adults become active in the fall when they oviposit in wheat and other grasses. By planting after a "fly free date" when fly activity subsides, winter wheat is protected from oviposition from the fall hessian fly generation (Buntin et al., 1991). This is a perfect example of how simple changes in plant culture can reduce the need for insecticide applications, increase yield, and provide economic benefit to growers (Buntin et al., 1992).

#### **3. Biological control of insect pests**

Many definitions of biological control have been published in the literature since the term was first used by H.S. Smith more than 90 years ago (Caltagirone & Huffaker, 1980; Cook, 1987; Coppel & Mertins, 1977; DeBach & Rosen, 1991; Garcia et al., 1988; see Huffaker & Messenger, 1976; Perkins & Garcia, 1999; Rabb, 1972; Smith, 1919). In its strictest sense, biological control is the use of beneficial organisms to reduce the relative abundance of, and damage caused by, noxious ones. This definition attributes economic rather than biological characters to organisms that fall into two categories, beneficial and noxious, based on their positive or negative impact on human-valued resources. It is also important to distinguish *biological* from *natural* control, which does not require human intervention, and from similar methods of pest control that do not involve whole (living) organisms (Huffaker et al., 1984). In fact, biological control involves interspecific, population-level processes by way of predation, parasitism, competition, or a combination of these mechanisms (van Driesche & Bellows, 1996). In practice, the effectiveness and appropriateness of biological control methods rely on real-time evolutionary forces that shape the beneficial organism's genotype, phenotype, and performance. This is not the case for similar, biologically based methods such as the application of insecticides formulated with pathogens, antagonists, or their byproducts. Furthermore, in its strictest definition, biological control does not include the deployment of pest-tolerant organisms, regardless of the source or origin of the resistanceconferring characters (e.g., Bt crops) (see Perkins & Garcia, 1999).

Alternatives to Chemical Control of Insect Pests 179

typically mass reared in an insectary, either to inoculate or inundate the target area of impact (Obrycki et al., 1997; Parrella et al., 1992; Ridgway, 1998). Inoculative releases involve relatively low numbers of natural enemies, typically when pest populations are low or at the beginning of a growth cycle or season. Inundation involves relatively high numbers of natural enemies released repeatedly throughout the growth cycle or season. Thus, inundative release of natural enemies is similar to insecticide use in that releases are made when pests achieve high enough density to cause economic harm to the crop. In both types of release, the objective is to inflict high mortality by synchronizing the life cycles of the pest and natural enemy. Hence, an effective monitoring program of pest populations is essential

Augmentation biological control has been used successfully against key pests of field and greenhouse crops. A well-known example of augmentation biological control is the use of the parasitoid, *Encarsia formosa*, for control of greenhouse whitefly (Hoddle et al., 1998). Indeed, augmentation plays an important role in greenhouse production, especially in Europe, and many natural enemies are commercially available for control of perennial greenhouse pests such as spider mites, aphids, scales, and whiteflies (Grant, 1997; Pottorff & Panter, 2009). The success of augmentative releases in greenhouses, and elsewhere, depends on the compatibility of cultural practices such as insecticide use with natural enemies (see Section 2.3). Greenhouses are often ideal sites for augmentation biological control because of the relative stability of the enclosed environment. In contrast, a critical review of augmentation biological control in field crops revealed that augmentation was typically less effective and more expensive than conventional control with pesticides (Collier & van Steenwyk, 2004). The authors found that the low success rate of augmentation biological control in field crops is influenced by ecological limitations such as unfavorable environmental conditions, natural enemy dispersal, and refuge for herbivores from released

Conservation biological control involves any practice that increases colonization, establishment, reproduction, and survival of native or previously established natural enemies (Landis et al., 2000). Conservation biological control can be achieved in two ways: modifying pesticide use and manipulating the growing environment in favor of natural enemies. Conservation practices have proven effective in a wide variety of growing situations ranging from small garden plots to large fields, agricultural to urban environments, and commercial to private settings (Frank & Shrewsbury, 2004; Landis et al.,

Modifications to pesticide regimens include reducing or eliminating insecticide use, using pest-specific insecticides when needed, making applications when beneficial arthropods are not active, and making treatment decisions based on monitoring and the presence of vulnerable life stages. While total independence from chemical control is not feasible for most situations, reductions in insecticide use are possible through IPM programs based on rigorous pest monitoring, established treatment thresholds, and/or insect population models (see Horn, 1988; Pimental, 1997). Thus, insecticides are used only when needed to prevent crop damage that results in economic loss. When insecticide use is warranted,

2000; Rebek et al., 2005, 2006; Sadof et al., 2004; Tooker & Hanks, 2000).

**3.3.1 Conserving natural enemies via modified pesticide use**

to the success of augmentation biological control.

natural enemies.

**3.3 Conservation biological control**

The history and origins of biological control have been extensively covered in previous volumes (Caltagirone & Doutt, 1989; DeBach & Rosen, 1991; van Driesche & Bellows, 1996) and is not the subject of this review. However, it is significant to note that early theory and application of biological control principles pre-date the modern insecticide era (Smith, 1919). Therefore, it is modern insecticides that became an alternative to biological control and not the other way around. In this context, biological control should not be viewed as a novel tactic but as the foundation of a successful pest management strategy involving, at minimum, the conservation of ecosystem resources to facilitate the process of pest-natural enemy colonization, host/prey finding, and ultimately, damage reduction. Although what constitutes biological control (or not) continues to be a subject of discussion and will likely evolve with new technologies, the recognition of three principal biological control methods remains unchanged. These three approaches are importation (a.k.a., classical biological control), augmentation, and conservation biological control (Smith, 1919).

#### **3.1 Importation biological control**

Importation biological control is the oldest of the three approaches (hence its alternative name, 'classical'). The first successful case of importation biological control occurred over a century ago in the control of cottony cushion scale in California citrus following importation of the vedalia beetle (Horn, 1988). The classical approach involves re-establishing the interspecific interactions (and their impact on population regulation) between pests and their natural enemies (i.e., predators, parasitoids, or insect-killing pathogens) as they occur in the pest's endemic range (Howarth, 1983). The need to re-establish these interactions arises because pests are commonly introduced into areas outside their native range where they lack natural enemies, or those that are present do not significantly impact the pest's abundance and local distribution. Since its inception, importation biological control has been used with varying degrees of success against noxious pests like cassava mealybug in Africa, Rhodesgrass mealybug in Texas, walnut aphid in California, and southern green stink bug in Australia, New Zealand, and Hawaii (Hokkanen, 1997).

The technical expertise, time commitment, and considerable expense necessary to carry out importation biological control require the involvement of specially trained university and government scientists. Importation is highly regulated in many countries, largely due to growing concern over the introduction of exotic, invasive species into new environments. In the U.S., the Animal and Plant Health Inspection Service (APHIS) oversees and coordinates importation biological control programs. The agency's charge is to preserve the safety and effectiveness of biological control primarily through post-release monitoring of biological control agents (USDA APHIS, 2011). Although there are a few documented cases of introduced biological control agents causing economic or ecological harm, societal perceptions that importation biological control is too risky are often influenced by subjectivity and misinformation (Delfosse, 2005). To minimize risk, researchers must provide evidence that introduced natural enemies are unlikely to harm crops, humans, and ecosystems. This requires substantial analysis of host feeding preference and other biological traits of prospective biological control agents (see Briese, 2005).

#### **3.2 Augmentation biological control**

The aim of augmentation biological control is to improve the numerical ratio between pest and natural enemy to increase pest mortality. It involves the release of natural enemies,

The history and origins of biological control have been extensively covered in previous volumes (Caltagirone & Doutt, 1989; DeBach & Rosen, 1991; van Driesche & Bellows, 1996) and is not the subject of this review. However, it is significant to note that early theory and application of biological control principles pre-date the modern insecticide era (Smith, 1919). Therefore, it is modern insecticides that became an alternative to biological control and not the other way around. In this context, biological control should not be viewed as a novel tactic but as the foundation of a successful pest management strategy involving, at minimum, the conservation of ecosystem resources to facilitate the process of pest-natural enemy colonization, host/prey finding, and ultimately, damage reduction. Although what constitutes biological control (or not) continues to be a subject of discussion and will likely evolve with new technologies, the recognition of three principal biological control methods remains unchanged. These three approaches are importation (a.k.a., classical biological

Importation biological control is the oldest of the three approaches (hence its alternative name, 'classical'). The first successful case of importation biological control occurred over a century ago in the control of cottony cushion scale in California citrus following importation of the vedalia beetle (Horn, 1988). The classical approach involves re-establishing the interspecific interactions (and their impact on population regulation) between pests and their natural enemies (i.e., predators, parasitoids, or insect-killing pathogens) as they occur in the pest's endemic range (Howarth, 1983). The need to re-establish these interactions arises because pests are commonly introduced into areas outside their native range where they lack natural enemies, or those that are present do not significantly impact the pest's abundance and local distribution. Since its inception, importation biological control has been used with varying degrees of success against noxious pests like cassava mealybug in Africa, Rhodesgrass mealybug in Texas, walnut aphid in California, and southern green stink bug

The technical expertise, time commitment, and considerable expense necessary to carry out importation biological control require the involvement of specially trained university and government scientists. Importation is highly regulated in many countries, largely due to growing concern over the introduction of exotic, invasive species into new environments. In the U.S., the Animal and Plant Health Inspection Service (APHIS) oversees and coordinates importation biological control programs. The agency's charge is to preserve the safety and effectiveness of biological control primarily through post-release monitoring of biological control agents (USDA APHIS, 2011). Although there are a few documented cases of introduced biological control agents causing economic or ecological harm, societal perceptions that importation biological control is too risky are often influenced by subjectivity and misinformation (Delfosse, 2005). To minimize risk, researchers must provide evidence that introduced natural enemies are unlikely to harm crops, humans, and ecosystems. This requires substantial analysis of host feeding preference and other

The aim of augmentation biological control is to improve the numerical ratio between pest and natural enemy to increase pest mortality. It involves the release of natural enemies,

control), augmentation, and conservation biological control (Smith, 1919).

in Australia, New Zealand, and Hawaii (Hokkanen, 1997).

biological traits of prospective biological control agents (see Briese, 2005).

**3.1 Importation biological control**

**3.2 Augmentation biological control**

typically mass reared in an insectary, either to inoculate or inundate the target area of impact (Obrycki et al., 1997; Parrella et al., 1992; Ridgway, 1998). Inoculative releases involve relatively low numbers of natural enemies, typically when pest populations are low or at the beginning of a growth cycle or season. Inundation involves relatively high numbers of natural enemies released repeatedly throughout the growth cycle or season. Thus, inundative release of natural enemies is similar to insecticide use in that releases are made when pests achieve high enough density to cause economic harm to the crop. In both types of release, the objective is to inflict high mortality by synchronizing the life cycles of the pest and natural enemy. Hence, an effective monitoring program of pest populations is essential to the success of augmentation biological control.

Augmentation biological control has been used successfully against key pests of field and greenhouse crops. A well-known example of augmentation biological control is the use of the parasitoid, *Encarsia formosa*, for control of greenhouse whitefly (Hoddle et al., 1998). Indeed, augmentation plays an important role in greenhouse production, especially in Europe, and many natural enemies are commercially available for control of perennial greenhouse pests such as spider mites, aphids, scales, and whiteflies (Grant, 1997; Pottorff & Panter, 2009). The success of augmentative releases in greenhouses, and elsewhere, depends on the compatibility of cultural practices such as insecticide use with natural enemies (see Section 2.3). Greenhouses are often ideal sites for augmentation biological control because of the relative stability of the enclosed environment. In contrast, a critical review of augmentation biological control in field crops revealed that augmentation was typically less effective and more expensive than conventional control with pesticides (Collier & van Steenwyk, 2004). The authors found that the low success rate of augmentation biological control in field crops is influenced by ecological limitations such as unfavorable environmental conditions, natural enemy dispersal, and refuge for herbivores from released natural enemies.

#### **3.3 Conservation biological control**

Conservation biological control involves any practice that increases colonization, establishment, reproduction, and survival of native or previously established natural enemies (Landis et al., 2000). Conservation biological control can be achieved in two ways: modifying pesticide use and manipulating the growing environment in favor of natural enemies. Conservation practices have proven effective in a wide variety of growing situations ranging from small garden plots to large fields, agricultural to urban environments, and commercial to private settings (Frank & Shrewsbury, 2004; Landis et al., 2000; Rebek et al., 2005, 2006; Sadof et al., 2004; Tooker & Hanks, 2000).

#### **3.3.1 Conserving natural enemies via modified pesticide use**

Modifications to pesticide regimens include reducing or eliminating insecticide use, using pest-specific insecticides when needed, making applications when beneficial arthropods are not active, and making treatment decisions based on monitoring and the presence of vulnerable life stages. While total independence from chemical control is not feasible for most situations, reductions in insecticide use are possible through IPM programs based on rigorous pest monitoring, established treatment thresholds, and/or insect population models (see Horn, 1988; Pimental, 1997). Thus, insecticides are used only when needed to prevent crop damage that results in economic loss. When insecticide use is warranted,

Alternatives to Chemical Control of Insect Pests 181

Lenteren, 1980). In practice, the successful application of biological control usually requires a combination of at least two of the three approaches, importation, augmentation, and conservation of natural enemies (DeBach & Rosen, 1991; van Driesche & Bellows, 1996). What drives the success or failure of biological control programs in plant crops has been the subject of many analyses, either using historical records or theoretical approaches (Andow et al., 1997; Murdoch et al., 1985; Murdoch & Briggs, 1996; van Lenteren, 1980). In general terms, biological control programs are more likely to succeed under certain production systems and environmental conditions (Clausen, 1978; van Driesche & Heinz, 2004). Biological control has been more successful in crops that: 1) are perennial versus annual; 2) grow in areas with few pests versus many pests; 3) the harvested portion is not damaged by the target pest; 4) the target pest is not a disease vector; and 5) the aesthetic damage is

Failures in biological control programs, especially those recorded in the literature, also involve cases where the biology and ecology of the natural enemy or the pests are not well understood or altogether unknown. Historically, failures in importation biological control have occurred after errors in identification of a pest or natural enemy at the level of species, biotype, or even local strain; a mismatch in micro-environmental requirements for natural enemy growth and development; incorrectly timing natural enemy release when the production system is not conducive to establishment; or when socioeconomic or regulatory barrier have prevented adoption or implementation (Clausen, 1978; Greathead, 1976; Hall & Ehler, 1979; Knutson, 1981). Similarly, failures in augmentation and conservation biological control, although not commonly recorded in the literature, may be due to a lack of understanding of the basic biology and ecology of the species involved, the basic requirements of the production system, and any socioeconomic barriers including real or perceived costs and benefits (Murdoch et al., 1985; Perkins & Garcia, 1999; Collier & van Steenwyk, 2004). The success of biological control programs involves integrated efforts at many levels ranging from biology to economics, from research to implementation and

Plant health can benefit greatly from preventing or limiting injury from arthropod pests from the start. Indeed, the cornerstone of an effective IPM program is prevention, which can be achieved, in part, through physical control. Physical control strategies include methods for excluding pests or limiting their access to crops, disrupting pest behavior, or causing direct mortality (Vincent et al., 2009). Physical control methods can be categorized as active and passive (Vincent et al., 2009). Active methods involve the removal of individual pests by hand, pruning out infested plant tissues, and rogueing out heavily infested plants. Passive methods usually include the use of a device or tool for excluding or removing pests from a crop. Typically, these devices serve as barriers between plants and insect pests, thus protecting plants from injury and damage. Other passive tools include repellents and traps. While traps are often used for monitoring pest abundance and distribution, many are designed as "attract and kill" technologies, which attract insect pests through color, light,

The greatest disadvantage to physical control is that these methods can be laborious and time consuming, especially for crops grown in large areas. Also, a moderate degree of specialization or training is often required due to the highly technical nature of some

acceptable (e.g., some food and fiber crops versus ornamentals).

experience, and from the farm to the community and region.

shape, texture, and scent, or a combination of these factors.

**4. Physical control strategies to reduce pest incidence**