This Journal of Environmental Horticulture article is reproduced with the consent of the Horticultural Research Institute (HRI www.hriresearch.org), which was established in 1962 as the research and development affiliate of the American Nursery & Landscape Association (ANLA http://www.anla.org). HRI s Mission: To direct, fund, promote and communicate horticultural research, which increases the quality and value of ornamental plants, improves the productivity and profitability of the nursery and landscape industry, and protects and enhances the environment. The use of any trade name in this article does not imply an endorsement of the equipment, product or process named, nor any criticism of any similar products that are not mentioned. Copyright, All Rights Reserved
3. Dirr, M.A. 1990. Manual of Woody Landscape Plants: Their Identification, Ornamental Characteristics, Culture, Propagation and Uses. Fourth Ed. Stipes Publishing Co. Champaign, IL. 1007 p. 4. Fare, D.C., C.H. Gilliam, H.G. Ponder and W.A. Griffey. 1987. Evaluation of ornamental pears. In: Ornamental Research Report. Res. Rept. Series #5. Alabama AES, Auburn Univ., AL. 5. Johnson, E.W. 195 I. Ornamental shrubs for the southern Great Plains. USDA Farmer's Bull. 2025. 6. Johnson, E. W. 1966. Ornamental and windbreak trees for the southern Great Plains. USDA ARS Bull. 34-77. 7. Kozel, P.c. 1974. Shade trees for suburban and city arboriculture. HortScience 9:5 I5-5 18. 8. Krussmann, G. 1984. Manual of Cultivated Broad-Leaved Trees and Shrubs (translated by M.E. Epp) Volume I. Timber Press, Beaverton, OR. 9. Self, H. 1978. Environment and Man in Kansas. Regents Press of Kansas, Lawrence, KS. 228 p. 10. Stephens, H.A. 1973. Woody plants of the North Central Plains. Regents Press of Kansas, Lawrence, KS 530 p. II. Wandell, W.N. 1989. Handbook of Landscape Tree Cultivars. East Prairie Publishing Co., Gladstone, IL. 318 p. Kairomone Response, Pesticide Tolerance and Field Efficacy of the Predatory Mite, Neosieulus collegae (De Leon)1 Russell F. Mizell III and Daniel E. SchitThauer 2 University of FLorida AgriculturaL Research and Education Center Rt. 4, Box 4092 Monticello, FL 32344-9302,.----------------- Abstract --------------------, Neosieulus (Cydnodromus) collegae (De Leon) (Acari:Phytoseiidae) is a heretofore relatively unknown species of predatory mite. In an olfactometer, female predators were attracted to kairomones produced by Tetranychus urticae Koch, Oligonychus ilicis (McGregor), O. ununguis (Jacobi), Eotetranychus hicoriae (McGregor), and E. sexmaculatus (Riley). Predators were repelled by odors emanating from lima bean leaves treated with Mavrik (fluvalinate) and Ammo (cypermethrin), but unresponsive to those treated with Tame (fenpropathrin) and Talstar (bifenthrin). This predator species was tolerant of residues of Vendex (hexakis), Omite (propargite), Pentac (dienochlor) and Avid (abamectin) but not to residues of Tame (fenpropathrin) and Kelthane (dicofol). Eggs of T. urticae treated with Tame (fenpropathrin) were toxic to the predator when consumed. Female N. collegae would not consume eggs treated with Avid (abamectin); starvation reduced fecundity. Prey eggs treated with Vendex (hexakis) and Omite CR (propargite) were consumed without affecting predator fecundity or mortality. Eggs treated with Pentac (dienochlor) or Kethane (dicofol) were consumed, but significantly reduced predator fecundity. Predators released into plots in a commercial nursery during winter in north Florida reduced field populations of T. urticae within 20-30 days, if released in high numbers. Neosieulus collegae may have significant potential as a biological control agent in nursery crops for control of mite pests. Index words: Acari, Phytoseiidae, acaricide, kairomone, biological control Pesticides/Kairomones used in the study; Pentac AF (dienochlor), decachloro bis{2-4-cyclopentadiene-l-y); Tame 2.4 EC (fenpropathrin), alpha-cyano-3-phenoxybenzyl 2,2,3,3-tetramethyl-l-cyclopropane carbaroxylate; Vendex 4L (hexakis), hexakis (2-methyl-2-phenylpropyl) distannoxane; Avid 0.15EC (abamectin), avermectin B la; Omite CR (propargite), 2-(p-tert-butylphenoxy)cyclohexyl 2-propynyl sulfite; Ammo 2.5EC, (cypermethrin), (±) cyano (3-phenoxyphenyl)methyl (±) cis-trans 3-(2,2 dichloroethenyl)-2,2 dimethylcyclopropane-carboxylate; Kelthane 35WP (dicofol), I, I-bis(chlorophenyl)-2,2,2-trichloroethanol; Talstar IOWP (bifenthrin), (2 methyl[ I, l-biphenyl]-3-yl) methyl 3-(2-chloro-3,3,3,3-trifluoro- I-propenyl)-2,2dimethylcyclopropanecarboxylate; Mavrik AF (fluvalinate), N-[2-chloro-4-(trifluoromethyl) phenyl]-d-valine (± )-alpha-cyano-(3-phenoxyphenyl)methyl ester. Significance to the Nursery Industry tolerate several acaricides, is attracted to kairomones of a This research indicates that the predatory mite, N. colvariety of mite pest species, and appears capable of rapidly Legae, has excellent potential as a biological control agent for spider mites in landscape plants. The predator is able to I Received for publication February 27, 1991; revised form May 21. Acknowledgment: We thank John Sparman and Douglas Miller of Imperial Nursery. Quincy, Florida for providing the field study sites. Cheryl Manasa and J.L. Baggett provided technical assistance. We thank Jack DeAngelis, Ronald Oetting and an anonymous reviewer for helpful comments on an earlier draft. This work was partially supported by a grant from the Horticultural Research Institute to the senior author. Florida Agricultural Experiment Station Journal Series No. R-O 1260. 2Associate Professor of Entomology and Senior Biologist, resp. controlling spider mites in the field, when released in reasonably high numbers. Future research should determine the optimum predator-to-prey release ratio and the impact of nursery management practices on the predator's ability to regulate populations of various pest species. Introduction Landscape nursery crops are attacked by many pests. Aesthetic thresholds require control at low pest numbers to maintain quality plants. Spider mites are the most important pests of container-grown woody landscape plants in terms J. Environ. Hort. 9(3):155-159. September 1991 155
of damage and control costs. In the southeastern U. S. the twospotted spider mite, Tetranychus urticae Koch, is the predominant species, followed by the southern red mite, Oligonychus ilicis (McGregor), and the spruce spider mite, O. ununguis (Jacobi). Growers presently rely on chemical pesticides to manage mites and other pests. However, environmental, sociological, and economic pressure necessitate research to develop alternatives to conventional pesticides. Use of biological control agents to manage pests is a viable alternative, but requires extensive research efforts to implelnent. Furthermore, because of the broad spectrum of pests and the low aesthetic thresholds for pests, chemical pesticides cannot be totally eliminated. Therefore, biological controls may often have to function coincident with chemicals in an integrated progranl. Integration of chemical and biological controls is not new (1, 4, 19), however, selective pesticides that kill pest species, but not natural enenlies, are badly needed for IPM programs. Unfortunately, few registered pesticides are generally selective of natural enemies (4). Predatory mites have been touted for biological control of phytophagous mite pests for many years (10, 14) and have been evaluated on nlany crops (9, 18, 23, 15, 11, 7). Availability of effective chemical pesticides for mite managenlent has limited development and use of predatory mites as biological control agents in nursery crops. Containergrown nursery crops have many characteristics conducive to the study and implementation of predatory mites as biological controls: plots in a continuum of sizes are readily available and most if not all inputs (water, light, plant species, plant nutrition, plant density and size) can be controlled. Nurseries also have a large labor force to implement biological control programs. The objective of this paper is to present results of research designed to evaluate a predatory mite for release into landscape nurseries for spider mite control. Materials and Methods Kairomone response. A Y-tube olfactometer, modified after Sabelis and van de Baan (21) was constructed of glass tubing 3 cm (1.2 in) in diameter with the arms 15 cm (6 "in) long. A small Y-shaped wire was inserted into the middle of the tubes to direct mite movement. An air outlet was connected to the main arnl and to a Nalgene water vacuum pump (11.5 IImin capacity, No. 6140-0010) on a water spigot. Air flowed through a canister of activated charcoal into detachable jointed glass containers on the ends of both test arms and through the olfactometer. Air exchange was adjusted equally in both test arms to about 100 mllmin using adjustable flowmeters. Kairomone and acaricide treatments for each test were placed upwind in the jointed glass containers so as to insure that both sides of the air stream had equal volumes of leaves and air flow. Predators. Newly-eclosed adult female predators from a laboratory colony (collected originally at Monticello, Florida) reared on Tetranychus urticae Koch on lima bean, Phaseolus vulgarus L., 'Henderson', were starved (with access to water) for 24 h before the tests. Thirty to 75 predators (used only once) were tested individually to each treatment. Each predator was placed on the wire at the downwind end of the olfactometer. Each predator was observed a maximum of 10 min and was scored as either no 156 response, + or - depending on which side of the olfactometer was chosen. The olfactometer was cleaned with acetone and the position of the treatments in each arm were switched after each ten predators were tested. The bioassay was conducted from 0930-1500 EST in the laboratory under fluorescent lighting with ambient temperatures from 27 34 C. Treatments are listed in Table 1. The pesticides in the olfactometer were tested at the labeled rate on bean leaves, as described below for the residue tests. The rates tested on bean leaves in the olfactometer were: Tame (fenpropathrin) 167 mg ai/i; Ammo (cypermethrin) 96 mg ai/i; Mavrik (fluvalinate) 140 mg ai/i; Talstar (bifenthrin) 84 mg ai/i. Treatment differences were determined using a two-tailed Sign test with P == 0.5 (3). Toxicity of acaricide residues. Lima bean leaves were dipped in acaricide + water for 10 sec and allowed to dry under a hood. Leaves were placed upside down on watersaturated cotton. Ten to 20 female N. collegae from a laboratory colony reared on twospotted spider mites were placed on each leaf along with untreated twospotted spider mite eggs, a few strands ofcotton and a small piece of microscope coverslip over the cotton. Six to 10 leaf replicates were Table 1. Response of adult Neosieulus collegae (De Leon) (n = 30 75) females to odors produced in an olfactonleter by several acaricides and spider mite species that are potential prey. Statistical significance is scored with respect to preference for the first treatment in the couplets. Zero and n.s. equal no significant difference between the treatments, + + and - - are explained as comments. Treatment Outcome Probability Comment Blank vs Blank 0 n.s. f. Bioassay is valid Tetranychus urticae ++ 0.04 Attraction on lima bean leaves vs lima bean leaves Bean leaves with T. ++ <0.05 Stimulus remains urticae removed vs on leaves wlo BlankY TSSM Eotetranychus hicor ++ <0.05 Attraction iae on pecan leaves vs pecan leaves E. sexmaculatus on ++ <0.05 Attraction azalea leaves vs azalea leaves Oligonychus ilicis on ++ <0.05 Attraction azalea leaves vs azalea leaves O. ununguis on juni ++ <0.05 Attraction per leaves vs juniper leaves x Fluvalinate (Mavrik) <0.05 Repellency treated bean leaves Cypermethrin <0.05 Repellency (Ammo) treated bean leaves Fenpropathrin (Dani 0 n.s. No response tol) treated bean leaves Bifenthrin (Talstar) 0 n.s. No response treated bean leaves ZDetermined using Sign Test, P = 0.5. YInfested leaves vs uninfested leaves were also tested with similar results. xthis test was conducted several times using different juniper cultivars. Significant attraction was observed only to O. ununguis on Juniperus conferta "Blue pacifica'. J. Environ. Hort. 9(3):155-159. September 1991
tested for each acaricide concentration and compared to predators on untreated control leaves. The number of concentrations tested for each acaricide varied, as necessary, to develop an LCso, but was never less than 5. Predator mortality on the leaves was scored 24, 48, and 72 h after treatment. Predators were scored as dead if they failed to move when prodded with a fine probe. Response lines to each acaricide were developed using the POLO program (20). Response to acaricide-treated prey. Circular leaf disks (2.5 em) were cut from untreated lima bean leaves, ringed with Tangle Foot (The Tangle Foot Co., Grand Rapids, MI 49504) and placed on saturated cotton. Lima bean leaves infested with T. urticae eggs were dipped in acaricide + water solutions for 10 sec and allowed to dry. Eggs were then brushed from leaves for use in the bioassay. The concentrations tested were chosen based on the results from the residue tests and compared to similar female predators held with untreated eggs. Free feeding, newly edosed, mated adult females (one per disk, 20 disks per concentration) from the laboratory colony were starved for 24 h and then placed on the leaves with a large number of treated prey eggs. After 48 h the number of live, dead, and stuck (in Tangle Foot) females were recorded along with the number of predator eggs produced. We did not determine the number of prey eggs consumed by each predator during the test. We did observe predator response to treated eggs under the microscope. Field efficacy trials. Adult male and mostly female N. collegae were reared in the laboratory (after 16) on twospotted spider mites. Approximately 200 predators were drawn into 10 em pieces of drinking straws, using a vacuum device, sealed with parafilm, held in an ice chest and taken to the field within 24 h. The predators were then released into holly, flex crenata 'Bullata', plants by unsealing the straws and distributing them evenly in the plant canopy of the plots. Release plots were the center 100 plants in 400 plant blocks of # I holly about 15-30 em (6-12 in) in height which were heavily infested (5-l5I1eaf) with two spotted spider mites. Before and after release of the predators, mites were sampled by removing two 10 em (4 in) stems from each of 30 plants chosen at random to cover the entire release plot. Samples were placed in plastic bags on ice, returned to the laboratory and all stages of the spider mites and predators were counted under a microscope. Control plots without predators were monitored concurrently. Three plots were used for each density of predators released. The number of predators released per plot was 200, 800, 1,000, 5,000, or 8,000 per block. The experiment was conducted during November to February of 1989 and 1990. Results and Discussion Kairomone response. N. collegae responded significantly to kairomones produced by the 5 species of phytophagous mites tested (Table I). No response to O. ununguis was observed in several tests using Juniperus chinensis 'San Jose' as the host plant (data not shown). However, attraction to O. ununguis was observed when the host plant was 1. conferta' Blue Pacifica'. The effect of host plant volatiles on kairomone response by the predator warrants further investigation. Janssen et al. (13) suggested that determination of a predator's response to host volatiles in an olfactometer is a quick and accurate method to screen and select the most likely candidates for field release against specific mite pest species. Prior to this work, nothing was known of the host range of N. collegae, although, it has been collected from Florida to Canada on a variety of host plants (5). We also have collected it from 1. coi?ferta/o. ununguis in Valdosta, Georgia. N. collegae were repelled by 2 of 4 synthetic pyrethroid acaricide/insecticides tested (Table I). Repellency by pyrethroids to phytophagous mites is well documented (12, 17) and is a mechanism that may allow escape and survival from toxicant-treated surfaces. The pyrethroids were extremely toxic to N. collegae, the ability of predators to detect pyrethroid presence prior to contact may enhance their survival in the field. No response to Tame (fenpropathrin) or Talstar (bifenthrin) was observed. While the active ingredients of the 4 presticides are known, the inert ingredients are proprietary. This differential response to synthetic pyrethroids should be explored further to identify the specific components in the Mavrik (fluvalinate) and Ammo (cypermethrin) which stimulate the avoidance behavior. Toxicity of acaricide residues. Tests of the mortality to N. collegae demonstrated a wide range of susceptibility to acaricide residues (Table 2). Kelthane (dicofol) and Tame (fenpropathrin) were highly toxic, while Vendex (hexakis), amite (propargite) and Pentac (dienochlor) were not. The response to Avid (abamectin) was interesting in that the LCso for the predator was about half the recommended field rate for phytophagous mites. Thus, reduced rates of Avid (abamectin) could be used in the field to adjust prey density while conserving this predator. Toxicity of acaricide-treated prey. Exposure or feeding on prey eggs treated with Vendex (hexakis) or amite (pro- Table 2. Toxicity of acaricide residues to adult female Neosieulus collegae (De Leon) in a laboratory residue bioassay. Field rate LC so (mg ai/i) LC so (mg ai/i) Acaricide mg ai/i N N. collegae 95% CL T. urticae' Vendex (hexakis) 450 368 29,436 25.113-37,547 419-1.136 Omite (propargite) 360 370 16,933 11.918-20,713 10.7-128.0 Pentac (dienochlor) 600 686 2.321 1803-3027 -, Avid (abamectin) 5.8 463 2.3 1.35-3.85 <0.55 Kelthane (dicofol) 478 503 96.8 80.6-115.6 71-166 Tame (fenpropathrin) 167 447 0.13 0.082-0.190 _Y 'From Schiffhauer and Mizell (1988). YNot determined, but much less than recommended field rate. 1. Environ. Hort, 9(3): 155-159. September 1991 157
Table 3. Mortality, fecundity and behavior of Neosieulus collegae (De Leon) fed acaricide-treated twospotted spider mite eggs. Dose Percent Percent Mean eggs Acaricide (mg ai/i) mortality repelled per female Vendex (hexakis) 0 10.5 51. 4.6 :±: 1.6 45 0 15 4.0 :±: 1.1 45JY 0 0 4.8 :±: 0.9 4510 5 10 3.9 ± 2.0 Omite (propargite) 0 0 15 3.0± 1.4 36 0 25 3.5 ± 1.1 360Y 0 5 3.9 :±: 1.5 3600 0 20 I.9 ± 1.0 X Pentac (dienochlor) 0 300 0 15 6 15 4.4 :±: 0.7 1.9 :±: 0.8 X 600 Y 35 30 0.7 ± 0.8 x Avid (abamectin) 0 1.4 10 4.0 ± 1.5 575 0 15 2.5 :±: 1.1 2.9 5 20 1.5 ± I.P 5.75Y 0 15 0.8 ± 1.0 x Kelthane (dicofol) 0 0 13 4.5 :±: 1.6 4.8 0 5 3.8 :±: 0.5 48 0 45 478Y 5 15 1.0 :±: 0.8 X 0.4 :±: 0.5 x Tame (fenpropathrin) 0 1.4 10 4.0 ± 1.5.17 0 40 0.7 ± 0.9 x 16.7 50 50 O.Ox 167Y 100 0 O.Ox ZNumber found in the stickenl ring. Ylndicates the 1x labeled field dose for phytophagous mites. XSignificantly lower than the control as determined by t-test, P = 0.05. pargite) had no effect on the mortality of fecundity of N. collegae (Table 3). Female predators consumed eggs treated with Pentac (dienochlor), but had significantly reduced fecundity and higher mortality than the controls. Tame (Fenpropathrin) treated eggs were extrenlely toxic to N. collegae, as were the surface residues. Kelthane (dicofol)-treated eggs were not as toxic as the Pentac (dicofol) residues to N. collegae, but Pentac (dicofol) did significantly reduce fecundity. N. collegae were repelled by eggs treated with Avid (abamectin) and would not feed on them; therefore fecundity was greatly reduced, although mortality to the females was low. These results indicate that Pentac (dicofol) and Tame (fenpropathrin) are inappropriate, but that Vendex (hexakis) and amite (propargite) are suitable for integrated approaches to manage spider mites. A reduced rate of Avid (abamectin) could be applied in the field to conserve predators. However, the remaining, treated prey would probably not be available as food for N. collegae. If the rate used was low enough to conserve a residual population of adult prey, perhaps N. collegae could survive and reproduce by consuming newlyoviposited or untreated eggs. Similar results with Avid (abamectin) residues and treated prey were reported by Grafton Cardwell and Hoy (6) for Metaseiulus occidentalis (Nesbitt) and by Zhang and Sanderson (24) for Phytoseiulus persimilis Anthias-Henriot. Based on the observed tolerance to Avid (abamectin), Hoy and Ouyang (8) developed an Avid (abamectin)-resistant population (3.8 fold LC so ) of M. occidentalis. Figure 1 presents the change in N. collegae and T. urticae populations following release of N. collegae into infested plots of container-grown nursery plants. At 8,000 predators per 1000 plants (the highest rate released), T. urticae were reduced to very low populations in 20-30 days. Other plots 158 with fewer predators took longer or did not eliminate the spider mite populations. Populations of twospotted spider mites in control plots continued at high levels during and after the populations in the treatment plots decreased (data not shown). Although the test was conducted under typical late winter-early spring conditions (night temperatures <7 C) in north Florida, the predators did not appear to diapause, but continued to reproduce and disperse from test plots as prey were depleted. Clearly, larger field tests are necessary to fully evaluate the potential of N. collegae as a biological control agent for 3.5 ~ -0 N. ~ NYMPHS + ADULTS 120 ~ I. ~ NYMPHS 2 3.0a /1 G-El I. ~ w ADULTS l- I U1 U1 100 2.5 n::: n::: w w,,, 0... 0... 80,, r 2.0I 81, 60 ~I 1.si, ~I 40 / / \ 1.0 zl Z / \, <{ ~, Z \ <{ w 20 5 w 2 \ \", '2 \' Fig. 1. 0 ~ ~ ~ \, Jan 15 Feb 7 March 2 DATE Changes in populations of Tetranychus urticae Koch and Neosieulus collegae De Leon in field plots after inoculative release. Multiple releases (indicated by arrows) of N. colleage in each plot were made: 2,300 predators on January 20; 2,300 on January 25; 1,800 on February 5 and 2,500 on February 12. J. Environ. Hort. 9(3):155-159. September 1991 0.0
spider mites in nursery and perhaps other crops. The optimum predator to prey release ratio remains to be determined. The predator could be integrated into current chemicallybased pest management schemes, without harm, if Vendex (hexakis) or amite (propargite) were used. Further, it is capable of responding to kairomones produced by several important mite pests in nurseries. The predator also will feed and reproduce in the laboratory on many of these species (Mizell, unpublished data 1989) and appears amenable to mass culture. Previous investigations (Mizell unpublished, 1988) suggest that spider mite infestations are endemic to nursery stock rather than originating and spreading from other vegetation. Twospotted spider mite populations are lowest in the winter and spring and probably serve as foci for outbreaks that occur at other times. Detection of endemic populations would require intense, cost-prohibitive sampling efforts. We believe that N. collegae could be released into nurseries to reduce or eliminate endemic populations of spider mites. This may delay the build up of damaging mite populations during the growing season, thereby reducing or eliminating further mite control inputs. Other management applications are possible. For example, a similar scenario for control of O. ilicis (a cool weather pest) could occur at times when T. urticae was less active. In any case, N. collegae appears to have excellent potential for release into nursery crops for biological control of spider mites. This hypothesis warrants further research. Literature Cited I. Bartlett, B.R. 1964. Integration of chemical and biological control. pp. 489-511. In Debach, P. (ed.). Biological control of insect pests and weeds. Reinhold Publ. Co. N.Y. 2. Chant, D.A. and E. Yoshida-Shaul. 1982. On the identity of Amblyseius umbraticus (Chant) Acarina: Phytoseiidae). Can. J. Zoo. 60: 1998 2005. 3. Conover, W.J. 1971. 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Savin. 1977. POLO: a new computer program for probit analysis. Bull. Entomol. Soc. Am. 23:209 213. 21. Sabelis, M.W. and H.E. van de Baan. 1983. Location of distant spider mite colonies by phytoseiid predators: demonstration of specific kairomones emitted by Tetranychus urticae and Panonychus ulmi. Entomol. Exp. and Appl. 33:303-314. 22. Schiffhauer, D.E. and R.F. Mizell. 1988. Behavioral response and mortality of nursery populations of twospotted spider mite (Acari: Tetranychidae) to residues of six acaricides. J. Econ. Entomol. 81:1155-1162. 23. Waite, G.K. 1988. Control of Tetranychus urticae Koch by Phytoseiulus persimilis Athias-Henriot in low-chill stonefruit. Queensland J. Agric. & An. Sci. 45:185-188. 24. Zhang, Z. and J.P. Sanderson. 1990. Relative toxicity of abamectin. to the predatory mite, Phytoseiulus persimilis (Acari: Phytoseiidae) and two spotted spider mite (Acari: Tetranychidae). J. Econ. Entomol. 83: 1783 1790. J. Environ. Hort. 9(3):155-159. September 1991 159