A Laboratory Evaluation of the Astigmatid Mite Hemisarcoptes cooremani Thomas (Acari: Hemisarcoptidae) as a Potential Biological Control Agent for an Armored Scale, Aonidiella aurantii (Maskell) (Homoptera: Diaspididae)

Biological Control 15, 173–183 (1999) Article ID bcon.1999.0706, available online at http://www.idealibrary.com on

A Laboratory Evaluation of the Astigmatid Mite Hemisarcoptes cooremani Thomas (Acari: Hemisarcoptidae) as a Potential Biological Control Agent for an Armored Scale, Aonidiella aurantii (Maskell) (Homoptera: Diaspididae) Robert F. Luck,* G. Jiang,*,1 and M. A. Houck† *Department of Entomology, University of California, Riverside, California 92521; and †Biology Department, Texas Tech University, Lubbock, Texas 79409-3131 Received August 13, 1998; accepted January 21, 1999

INTRODUCTION The host stage and species utilized by a parasitic mite, Hemisarcoptes cooremani Thomas (Acari: Hemisarcoptidae), was studied to evaluate the mite’s potential as an augmentative biological control agent against California red scale, Aonidiella aurantii (Maskell) (Diaspididae: Homoptera). We compared how readily the mite established on five oleander scale, Aspidiotus nerii (Bouche´), stages and eight red scale stages using no-choice experiments in which mites were offered a single scale stage and species. We also offered the mite a choice between two stages of the same species, a choice between oleander and red scale in the same stage, and a choice between oleander and red scale in the same two stages. We found that few mites established on scales younger than second molt, but they readily established on the older oleander scale stages. They accepted gravid and parturient female red scale less readily than they did the same oleander scale stages. We suspect that the heavily scleratized body of California red scale attached to the cover in these stages prevented the mite from gaining access to the scale body on which to feed. Our results suggest that red scale is a poor-quality host for the mite. Consequently, this predator/parasitoid is unlikely to be an effective augmentative biological control agent against A. aurantii in California’s San Joaquin Valley. The younger stages provide insufficient resources for the mite to develop and reproduce and the older stages are too difficult to feed on. r 1999 Academic Press Key Words: augmentation; Hemisarcoptes coorermani; California red scale; Aonidiella aurantii; oleander scale; Aspidiotus nerii; host selection.

1 Present address: The Laboratory of Molecular Biology and Virology, The Salk Institute for Biological Research, 10010 North Torrey Pine Road, La Jolla, CA 92037-1099.

We are contemplating the use of a parasitic mite, Hemisarcoptes cooremani Thomas (Acari: Hemisarcoptidae), as an augmentative biological control agent to suppress California red scale, Aonidiella aurantii (Maskell) (Diaspididae: Homoptera) in California citrus, especially in the citrus growing region of central California’s San Joaquin Valley in which this insect remains a pest. Our interest stems from the successful use of several Hemisarcoptes species as classical biological control agents against armored scales and from the ability of several indigenous species to suppress resident armored scale populations (Gerson et al., 1990). The introduction of H. malus (Shimer) into British Columbia, Canada, in 1917 suppressed the oystershell scale, Lepidosaphes ulmi (L.) (Tothill, 1919) in the province’s apple orchards. Similarly, the introduction of H. coccophagus Meyer into New Zealand from Israel in 1987–1989 suppressed latania scale, Hemiberlesia lataniae Signoret (Hill et al., 1993). Moreover, a resident population of Hemisarcoptes species reportedly suppressed the date palm scale, Parlatoria blanchardi Targioni, in the Sahel region of Niger (Kaufmann, 1977). Similarly, H. malus is credited with suppressing oystershell scale in the apple orchards of Nova Scotia (Pickett and Patterson, 1953) and Quebec (Samagasinghe and Leroux, 1966) in eastern Canada. Two Hemisarcoptes introductions, however, have been unsuccessful. H. malus was introduced into Bermuda from Canada in 1946 against Lepidosaphes newsteadi (Sulc) infesting Bermuda cedar, Juniperus bermudiana L., and into New Zealand from Canada in 1967 against San Jose scale, Quadraspidiotus perniciosus (Comstock). Although the mite became established in Bermuda, it failed to suppress L. newsteadi (Rosen and DeBach, 1978). This same mite did not establish on San Jose scale in New Zealand (Hill, 1989; Hill et al., 1993).

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1049-9644/99 $30.00 Copyright r 1999 by Academic Press All rights of reproduction in any form reserved.

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In the studies reported herein, we evaluated the potential of H. cooremani as an augmentative or inoculative biological control agent for release against California red scale. Its potential use is part of an evolving pest management program for citrus in California’s San Joaquin Valley (Luck, 1983; Luck et al., 1997). H. cooremani is indigenous to California, where it parasitizes several armored scale species (Gerson et al., 1990). Field populations of H. cooremani have been found on California red scale (Houck, pers. obs.; Gerson, pers. com., 1992); Italian pear scale, Epidiaspis leperii (Signoret), infesting walnut in California (Houck, 1989; Houck and O’Conner, 1990); and (as H. malus) latania scales infesting avocado in California (Bartlett and DeBach, 1952; Houck, 1989; Houck and O’Conner, 1990). It has also been reported from purple scale, Lepidosaphes beckii (Newman), infesting citrus in Texas (Houck, 1989; Houck and O’Connor, 1990). Hemisarcoptes species are obligate parasites of armored scales (Diaspididae: Homoptera) (Gerson et al., 1990). Their eggs are laid on the scale and hatch into larvae that feed on the scale body beneath the scale cover. Typically, the parasitic mite passes through two additional immature stages, a protonymph and tritonymph, before becoming an adult. In some species when host resources become heavily exploited, immature individuals molt into a heteromorphic deutonymph, called a hypopus, and seek out a scalefeeding Chilocorous species (Coccinellidae: Coleoptera) on which to attach and disperse (Gerson et al., 1990). Searching mites gain access to the scale body by penetrating the margin of the scale cover and the mite’s feeding either reduces the scale’s fecundity or kills it (Gerson et al., 1990). When scales die, the mite leaves the scale and searches for a new host. California red scale, the target for this agent, is one of two key pests in California citrus and it infests all above-ground portions of the tree (Ebeling, 1950, 1959; Luck, 1983). At modest densities, the scale’s economic impact is cosmetic; it infests the fruits, which reduces the fruits’ grade or causes them to be culled in the packinghouse. At higher densities, this pest causes leaf and fruit drop and can kill twigs and branches. At extremely high densities, A. aurantii can kill portions of the tree (Ebeling, 1950). Although the scale is under excellent biological control in most coastal and inland coastal valleys of southern California, it occasionally becomes a pest when pesticides, ants, or dust disrupts its biological control (DeBach and Rosen, 1991). Also, established natural enemies are less effective against scale populations infesting young citrus trees (Ebeling, 1950) and against scale populations that infest the trunks or scaffolding branches of a tree (Luck and Podoler, 1985; Walde et al., 1989). This ineffectiveness is frequently associated with Argentine ant, Linipothema humile (Meyer), populations foraging in such

trees (DeBach and Rosen, 1991; Moreno et al., 1987). Augmentative releases of Aphytis melinus DeBach (Aphelinidae: Hymenoptera) in conjunction with Argentine ant control suppresses such disrupted populations (Moreno and Luck, 1992). In the San Joaquin Valley, red scale remains an economic problem (Flaherty et al., 1973). Although the same complex of natural enemies exist in the San Joaquin Valley as in the inland coastal valleys of southern California, the natural enemy complex is less effective in suppressing the scale in the Valley (Flaherty et al., 1973). Thus, scale control has traditionally relied on broad-spectrum, synthetic pesticides (Haney et al., 1992; Morse and Klonsky, 1994; Luck et al., 1997). The same is true for the suppression of most of the pest complex infesting citrus in the San Joaquin Valley. This continued reliance on broad-spectrum pesticides has selected for resistant populations of both California red scale and of yellow scale, Aonidiella citrina (Coq.) (Grafton-Cardwell, 1994). In the absence of replacement chemicals, and with a growing concern about worker safety, citrus growers in the San Joaquin Valley are seeking alternative approaches to pest management (Haney et al., 1992; Luck et al., 1997). We seek additional natural enemies for use as classical or augmentative agents in this system. H. cooremani is one such candidate. We propose to use it as a chronic mortality agent of red and yellow scale populations infesting young trees and the interior branches and trunks of older trees. To evaluate this natural enemy’s potential, we determine which stages of California red scale it uses and whether it reproduces on them. We compare how readily the mite established on California red scale with its establishment on oleander scale, Aspidiotus nerii (Bouche´). The gravid and parturient third-instar stages of California red scale have sclerotized bodies that are attached to a hardened scale cover (Fondi, 1990; Honda and Luck, 1995). These morphological features make these stages largely invulnerable to most natural enemies (Forster et al., 1995; Honda and Luck, 1995). In contrast, oleander scale has a soft scale cover and body throughout its development; thus, natural enemies readily breach this species’ older stages (DeBach and White, 1960; Honda and Luck, 1995). Host selection information will be useful in developing a mass rearing system for the mite and to synchronize its releases in the field with the appropriate red scale stages should we adopt it as an augmentative agent. Host selection information is also necessary to assess the impact of these mites in a grove following largescale releases (cf. Forster et al., 1995). METHODS

Scale and mite cultures. As host material for H. cooremani, laboratory cultures of a parthenogenetic

LABORATORY EVALUATION OF Hemisarcoptes cooremani

strain of oleander scale (DeBach and White, 1960) and of a bisexual strain of California red scale were maintained on lemon fruits using methods described by Tashiro (1966). The oleander scale culture was maintained at 23 ⫾ 1°C/50–60% RH and the red scale culture was maintained at 26 ⫾ 1°C/70% RH in the insectary at the University of California, Riverside (UCR). H. cooremani was originally collected from purple scale infesting citrus trees at Donna, TX. Since 1984, a mite culture has been maintained in the laboratory on potatoes infested with oleander scale (Houck, 1989). This culture was supplemented with additional fieldcollected individuals in December 1986 (Houck, 1989). Two experimental cultures were initiated at UCR from this original culture, one on lemon fruits infested with oleander scale and one on lemon fruits infested with California red scale. The mite was cultured on fresh lemon fruits infested with either third instar oleander scale or virgin (third instar) female California red scale. Fresh lemons with either red or oleander scales were added to the appropriate cultures every 2 to 4 weeks when the old lemon fruits in the culture began to deteriorate. About 20 third instar scales from each culture were dissected weekly to monitor whether sufficient live scale and mites were present and the number of dead scales present on the lemons. Experimental protocol. Four sets of experiments were conducted to determine on which host stage and species H. cooremani most readily established. We conducted three additional sets of experiments to test the assumptions we used in our initial set of experiments. We used the number of mites that established on the scale stage and species as an index of the mite’s successful utilization of that stage and species. These experiments consisted of (1) no-choice experiments in which mites were offered a single scale stage and species, (2) choice experiments in which mites were offered a mixture of two developmental stages of the same scale species, (3) choice experiments in which mites were offered a mixture of oleander and red scale in the same developmental stage, and (4) a choice experiment in which mites were offered a mixture of two scale species each in the same two developmental stages (i.e., four scale ‘‘types’’). We also determined if a mite’s rearing history influenced its probability of establishing on a host species. In these choice experiments we offered the mites a mixture of oleander and red scale in the same developmental stages. An experimental replicate consisted of placing a mixture of 20 nonphoretic H. cooremani stages (i.e., larva ⫹ protonymph ⫹ tritonymph ⫹ adult) within a covered, 5-cm-diameter ⫻ 2-cm-high, plastic arena affixed with Blu-Tack to a lemon fruit infested with the appropriate number of scale species and stage(s). Mites were introduced into the arena by transferring them

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with a single-bristled paintbrush from fruits taken from the mite cultures. After 24 h, we assessed mite establishment by removing the scale covers and counting the number of mites feeding on each scale body. We conducted our laboratory experiments at 25 ⫾ 1°C/50 ⫾ 1% RH and L:D ⫽ 24:0. We used the number of mites that established on a scale stage and/or species as an index of host acceptance. We reasoned that each individual mite in a particular treatment had an equal likelihood of encountering the scale stage that was offered; but the likelihood of encountering a scale stage was related to its size. To ensure that similar-sized hosts were present in the choice experiments in which two species of scale were offered, a lemon fruit was infested twice and incubated until the desired scale size/stage was attained. For example, lemons infested with second instar scales of both scale species were obtained by inoculating a lemon with scale crawlers on days 1 (oleander scale) and 6 (red scale) and incubating the lemon for 19 days (total). For third instar scales, lemons were inoculated with crawlers on days 1 (oleander scale) and 12 (red scale) and incubated for 33 days. Similar procedures were used to obtain the other mixtures of scale species and stages as required by our experiments. Scales in excess of those needed were removed with a dissecting needle prior to conducting the experiment. Scale-infested lemons were incubated at 23.9 ⫾ 1°C/55 ⫾ 5% RH and L:D ⫽ 24:0. To determine whether the differences in establishment on different scale stages of the same species depended on scale size, we conducted an experiment in which we increased the ratio of a smaller scale stage relative to the larger scale stage. The experiment is described below (see under Additional Experiments to Test Assumptions). Single species, single stage experiments. In these two no-choice experiments, we offered a mixture of 20 mite stages either 60 oleander scales (Exp. 1) or 60 California red scales (Exp. 2) in a single stage. In Experiment 1, we offered the mites one of six treatments. Each treatment consisted of a fruit infested with 60 oleander scales in the first instar, first molt, second instar, second molt, early third instar female, or parturient (crawler-producing) third instar female stage with five replications per treatment. In Experiment 2, we offered the mites one of eight treatments. Each treatment consisted of a fruit with 60 California red scales in the first instar, first molt, early second instar (before the male and female scales differentiated morphologically), second molt female, male pupa, third instar virgin female, gravid female, or parturient female (crawler producing) stage with five replications per treatment. To preclude confounding the results of the single species choice experiment with a mite’s rearing history, mites reared on oleander scale were

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exposed only to lemons with oleander scale, and mites reared on red scale were exposed only to lemons with red scale. We used a one-way ANOVA to analyze each of the two experiments after transforming the data (log[X ⫹ 1]). Mean differences were compared using a Ryan–Einot–Gabriel–Welsch (REGWQ) multiple-range test (SAS, 1988) as suggested by Day and Quinn (1989). Mixed stage, single species experiments. We designed these experiments to determine whether H. cooremani established more frequently on one of two scale stages when given a choice between two scale stages of the same species. The logistics of this experiment allowed us to compare only two stages of the same scale species at any one time (⫽ one experiment). We offered 20 mites a choice of 60 early third instar versus 60 gravid third instar (Exp. 1), 60 early third instar versus 60 parturient third instar (Exp. 2), or 60 gravid third instar versus 60 parturient third instar oleander scale (Exp. 3). Similarly, we offered 20 mites a choice of 60 second molt versus 60 male pupa (Exp. 1), 60 second instar versus 60 virgin females (Exp. 2), 60 virgin females versus 60 male prepupae (Exp. 3), 60 virgin females versus 60 gravid females (Exp. 4), 60 virgin females versus 60 parturient females (Exp. 5), and 60 gravid females versus 60 parturient females red scale (Exp. 6). (See Table 2 for the number of replicates per experiment and treatment.) Again, to preclude confounding the results of the single species choice experiment with a mite’s rearing history, mites reared on oleander scale were exposed only to lemons with two stages of oleander scale, and mites reared on red scale were exposed only to lemons with two stages of red scale. We transformed the number of mites establishing on a stage (log[X ⫹ 1]) and compared their mean number within each of the nine experiments using a two-tailed t test. We used an experimentwise error rate based on the Dunn–Sidak method (Sokal and Rohlf, 1995) in which k ⫽ 3 for the oleander scale experiments and k ⫽ 6 for the red scale experiments (see also Rohlf and Sokal, 1995, Table C). Rearing history, single stage, two species experiments. These experiments were designed to test whether the number of mites that established on a host species was influenced by the host species on which the mite had been reared. We exposed 20 mites to a lemon infested with a mixture of either 60 oleander or 60 red scales (n ⫽ 120). We compared establishment on one of three stages: (1) early third instar female oleander versus third instar virgin female red scales (Exp. 1), (2) gravid oleander versus gravid red scales (Exp. 2), and (3) parturient oleander versus parturient red scale (Exp. 3). These were the scale stages of each species on which the mites most readily established in the no-choice experiments. (See Table 3 for the number of replicates run per treatment in each experiment.) We used a

two-way factorial ANOVA to analyze the results from each of the three experiments after transforming the data (log[X ⫹ 1]). The means were compared using a Ryan–Einot–Gabriel–Welsch (REGWQ) multiple-range test (SAS, 1988). Between species choice experiments. This experiment was designed to determine on which scale species the mites were most likely to establish when they were offered a mixture of the two most preferred scale stages of both species. We offered the mites a mixture of 60 third instar oleander, 60 gravid oleander, 60 virgin red, and 60 gravid red scale (n ⫽ 240 scales) in a single arena on a single fruit. These mites had been reared on red scale. We used a two-way factorial ANOVA to analyze the results from this experiment after transforming the data (log[X ⫹ 1]) and compared the means using a REGWQ multiple-range test (SAS, 1988). Additional experiments to test assumptions. We conducted a second set of experiments to test the validity of the assumptions that we made in our initial set of experiments. These additional experiments were designed to determine: (1) whether the mite stages differed in their establishment rate on the same scale stage, (2) whether exposing mites to the scale stages for longer periods, i.e., 120 versus 48 h, produced a different establishment pattern, and (3) whether the mite’s apparent preference was affected by the greater probability of encountering a larger (⫽older) scale when equal numbers of two scale stages occurred together. Mite stage and exposure time. In our initial set of experiments, we used a mixture of mite stages in each of the experiments because the mites were difficult to manipulate in large numbers as a single stage. Also, we exposed the scale stages to the mites for 24 h. In this second set of experiments, we exposed 20 H. cooremani (1) larvae, (2) protonymphs, or (3) tritonymphs ⫹ adults, reared on red scale, to a mixture of 180 second instar and 60 virgin third instar red scales. We used only mite stages reared on California red scale. Each arena containing the scale mixture was divided into two sections and each section had an equal number of scales. The scales in one section were dissected 24 h after the mites were released into the arena and those in the second section were dissected 80 h after the mites were released. We recorded the number of scales with established mites, total number of mites per scale, and total number of parasitized scales under which reproducing mites were observed 24 and 80 h later. Five replicates were conducted per treatment. The number of mites established by scale stage, mite stage, and exposure time was transformed (log [X ⫹ 1]) and was subjected to a three-way factorial ANOVA. The means were compared using a REGWQ multiple-range test (SAS, 1988).

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LABORATORY EVALUATION OF Hemisarcoptes cooremani

Influence of exposure time on choice of host species. We designed this experiment to test whether mites exposed to hosts for 120 h differed in their pattern of establishment on a host species compared with the pattern observed after 24 h. We placed 20 H. cooremani tritonymphs and adults reared on red scale in an arena containing a mixture of 60 gravid oleander and 60 gravid red scale. We chose the gravid scale stage because our previous experiments had shown that the mite did not establish as readily on red scale as oleander scale in this stage. Perhaps the mite required a longer period to penetrate the red scale’s cover. We recorded the number of mite eggs and feeding mite stages on each parasitized scale, total number of mites established on each scale species, and the total number of parasitized scales of each species 120 h (5 days) after introduction. Five replicates were conducted per treatment. We compared the number of mite eggs and active mite stages found on third instar oleander with those found on red scale using a paired, two-tailed t test after transformation (log[X ⫹ 1]). Influence of scale density on choice of scale stage. In our initial set of experiments (above), we offered mites a choice of 60 second versus 60 third instar scale of the same species. However, third instar scales are larger than second instar scales. Thus, the greater number of mites we observed on third instar scales might have been due to a higher probability that a searching mite encountered the larger scale stages. To test this hypothesis, we varied the ratio of the second (smaller) versus third instar (larger) scales. Twenty mites of mixed stages, reared on oleander scale, were exposed to a mixture of second and third instar oleander scales in ratios ranging from 53:60 to 260:60 (second to third instar scales, see Fig. 1 for the specific ratios we used). Only one replicate was run per ratio. We recorded the number of mites that established on second and third instar scale 24 h after the mites were introduced into the arena. We used Spearman rank order correlation to determine whether the number of mites that established on second instar scale was related to the ratio of second to third instars scale present in the arena.

RESULTS

No choice experiments. The number of H. cooremani that established on oleander scale differed significantly among scale stages when a single scale stage was offered to a mixture of mite stages (F[5,24] ⫽ 57.52; P ⬍ 0.001) (Table 1). More mites established on early third and parturient third instar oleander scale than on any of the younger oleander scale stages. An intermediate number of mites established on second instar oleander scales. Very few mites established on the first

TABLE 1 The Number of Hemisarcoptes cooremani Thomas that Established on Different Stages of Oleander Scale, Aspidiotus nerii (Bouche´), Parthenogenetic Strain, and California Red Scale, Aonidiella aurantii (Maskell), Bisexual Strain, when Offered a Single Scale Stage and Species for 24 h (No Choice)

Scale species Oleander scale

California red scale

Scale stage

Replicates

No. of established mites per replicate (mean ⫾ SD) a

1st Instar 1st Molt 2nd Instar 2nd Molt 3rd Instar Parturient F 1st Instar 1st Molt 2nd Instar 2nd Molt Pupa 3rd Instar Gravid F Parturient F

5 5 5 5 5 5 5 5 5 5 5 5 5 5

0.00 ⫾ 0.00a 0.00 ⫾ 0.00a 2.20 ⫾ 1.34b 0.20 ⫾ 0.45a 8.00 ⫾ 3.74c 11.40 ⫾ 2.61c 0.40 ⫾ 0.89a 0.40 ⫾ 0.89a 0.40 ⫾ 0.55a 0.20 ⫾ 0.89a 5.20 ⫾ 2.39b 7.40 ⫾ 1.82b 3.60 ⫾ 2.30b 5.00 ⫾ 2.35b

Note. Sixty oleander scale were offered to 20 mites (mixed stages) reared on oleander scale and 60 California red scale were offered to 20 mites (mixed stages) reared on California red scale per replicate. a Mean ⫾ standard deviation was calculated prior to transformation. Mean ⫾ SD’s followed by the same letter within a species do not differ significantly at the 0.05 level of significance. REGWQ’S multiplerange tests were calculated on transformed data [log (x ⫹ 1)].

instar, first molt, or second molt stages. The few that established on these younger stages did so in similar numbers, but they established in significantly fewer numbers on these stages than on the second instar or older scale (Table 1). Similar results were obtained with red scale. The number of H. cooremani that established on this scale species differed among the scale stages when a single stage was offered to a mixture of mite stages (F[7,32] ⫽ 17.92; P ⬍ 0.001) (Table 1). More mites established on third instar virgin females (3I) and on male prepupae (PU) than on any other stage. Few mites established on the first instar, first molt, second instar, or second molt stages. The few that did establish on these younger stages were similar in number, but they established in significantly fewer numbers than they did on the male prepupae or on third instar or older scales (Table 1). Thus, we conclude from these no-choice experiments that the mite did not readily establish on the first instar, first molt, or second molt of either oleander or red scale or on the second instar of red scale. Therefore, in the remaining experiments, we limited the mite’s choices to the older, more readily accepted stages of both host species (Table 1). Choice experiments. When offered pair-wise choices between two oleander scale stages, significantly more

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TABLE 2 The Number of Hemisarcoptes cooremani Thomas that Established on One of Two Stages of Oleander Scale, Aspidiotus nerii (Bouche´) and California Red Scale, Aonidiella aurantii (Maskell), when Offered a Choice between Either Two Oleander Scale or Two California Red Scale Stages for 24 h No. of established mites per replicate b Scale species Oleander scale

California red scale

Stages offered a (A vs B)

No. replicates

No. scales per replicate

A

B

Probability a t test c

3I vs FM 3I vs FC FM vs FC 2M vs PU 2I vs 3I 3I vs PU 3I vs FM 3I vs FC FM vs FC

6 6 7 10 7 8 10 8 8

60 ⫹ 60 60 ⫹ 60 60 ⫹ 60 60 ⫹ 60 60 ⫹ 60 60 ⫹ 60 60 ⫹ 60 60 ⫹ 60 60 ⫹ 60

1.33 ⫾ 0.52 1.67 ⫾ 2.73 1.29 ⫾ 1.49 0.10 ⫾ 0.32 1.90 ⫾ 1.37 4.00 ⫾ 2.33 13.60 ⫾ 2.84 8.75 ⫾ 2.96 1.12 ⫾ 1.88

10.33 ⫾ 1.96 7.33 ⫾ 3.13 7.71 ⫾ 2.62 5.90 ⫾ 2.92 5.14 ⫾ 2.11 5.63 ⫾ 1.50 0.20 ⫾ 0.42 2.75 ⫾ 1.39 5.88 ⫾ 2.42

P ⬍ 0.01 P ⬍ 0.01 P ⬍ 0.01 P ⬍ 0.01 P ⬍ 0.05 P ⬎ 0.05 P ⬍ 0.01 P ⬍ 0.01 P ⬍ 0.01

Note. Sixty oleander scale in each of two stages were offered to 20 mites of mixed stages reared on oleander scale and 60 California red scale in each of two stages were offered to 20 mites of mixed stages reared on California red scale per replicate. a Oleander and California red scale stages: 2I, 2nd instar; 2M, 2nd molt; 3I, 3rd instar; PU, male prepupa; FM, mature or gravid female; FC, parturient or crawler-producing female. For California red scale: 3I, virgin female. b Mean ⫾ SD’s calculated on untransformed data. c Paired t test of stage A vs stage B using the experimentwise error rate using the Dunn–Sidak method on transformed data [log (1 ⫹ x)] (Sokal and Rohlf, 1995) where k ⫽ 3 for Oleander scale and k ⫽ 6 for California red scale. See Table C of Rohlf and Sokal (1995).

H. cooremani established on parturient third instars (FC) than on either the early third (3I) or the gravid third instar scales (FM) (Table 2). Also, significantly more H. cooremani established on gravid third instar (FM) than on early third instar oleander (3I) scales (Table 2). Similarly, when offered pair-wise choices between two red scale stages, significantly more mites established on virgin third instar (3I) than on second instar (2I), gravid (FM), or parturient red scale (FC). Similar numbers of mites established on male prepupae (PU) and virgin third instar red scales (3I), whereas more mites established on parturient (FC) than on gravid (FM) red scale. We interpret these results as suggesting that more mites established on virgin third instar red scale or on male prepupae than on the other red scale stages. Also, our results suggest that the mite prefers the crawler-producing parturient female to the gravid female red scale (Table 2). Rearing history. When the mites had a choice between two scale species in the same stage (Table 3), significantly more mites established on oleander scale in the gravid (FM) (F[1,20] ⫽ 163.55; P ⬍ 0.001) or parturient stages (F[1,36] ⫽ 42.22; P ⬍ 0.001) than on the comparable red scale stages, regardless of the host on which the mites had been reared. In the case of third instar scales, a similar number of mites established on this instar in both scale species (F[1,36] ⫽ 1.52; P ⫽ 0.23). Regardless of their rearing history, mites offered only a single species in the third instar (no choice) established more often on oleander than on red scale (F[1,35] ⫽ 24.25; P ⬍ 0.001) (Table 4), but the number of

mites that established on a third instar of a given scale species depended on the host on which they had been reared (Table 4) (interaction term: F[1,35] ⫽ 7.62; P ⬍ 0.01). Relatively more mites established on red scale if they had been reared on red scale and more mites established on oleander scale if they had been reared on oleander scale. TABLE 3 The Number of Hemisarcoptes cooremani Thomas that Established on Oleander Scale, Aspidiotus nerii (Bouche´) (OS), and California Red Scale, Aonidiella aurantii (Maskell) (CRS) Reared on Either Oleander or California Red Scale when Offered a Mixture of Two Species in the Same Stage

Scale stage and species offered a 3I OS vs 3I CRS 3I OS vs 3I CRS FM OS vs FM CRS FM OS vs FM CRS FC OS vs FC CRS FC OS vs FC CRS

Scale species on which No. of mite was replireared cates OS CRS OS CRS OS CRS

10 10 6 6 10 10

No. of established mites b OS stage

CRS stage

6.10 ⫾ 2.80 4.20 ⫾ 1.93 10.17 ⫾ 1.47 10.17 ⫾ 3.31 8.00 ⫾ 3.30 6.90 ⫾ 3.30

3.30 ⫾ 1.95 5.20 ⫾ 2.82 0.83 ⫾ 1.17 0.40 ⫾ 0.55 3.40 ⫾ 2.07 1.00 ⫾ 1.05

NS NS *** *** *** ***

a Oleander and California red scale stages: 3I, 3rd instar; FM, mature or gravid female; FC, parturient or crawler-producing female. For California red scale: 3I, virgin female. b Mean ⫾ SD’s were calculated on untransformed data. Analysis of variance conducted on transformed data [log (x ⫹ 1)]. *** 0.001 level of significance; NS, nonsignificant.

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LABORATORY EVALUATION OF Hemisarcoptes cooremani

TABLE 4 Comparison of the Number of Hemisarcoptes cooremani Thomas that Established on Oleander Scale, Aspidiotus nerii (Bouche´) and California Red Scale, Aonidiella aurantii (Maskell) when Reared on Either Oleander or Red Scale

Scale species offered

Scale species on which mite was reared

No. of replicates

No. of mites established per arena a

Oleander scale

9

10.56 ⫾ 3.32a

Calif. red scale

10

9.10 ⫾ 4.11ab

Oleander scale

10

3.50 ⫾ 2.51c

Calif. red scale

10

6.30 ⫾ 2.26b

Scale stage offered

Oleander scale Early 3rd instar Oleander scale Early 3rd instar Calif. red scale Virgin 3rd instar Calif. red scale Virgin 3rd instar

Note. The mites were offered a single stage and species of scale. a Mean ⫾ SD’s were calculated on untransformed data. Mean differences were compared using REGWQ’s (Day and Quinn, 1989) on transformed data [log (x ⫹ 1)]. Values with the same letter do not differ at the 5% level of significance.

When given a choice, a similar effect of rearing history was observed for the number of mites that established on the third instars of a given scale species (interaction term: F[1,36] ⫽ 4.84; P ⫽ 0.034) (Table 3). Also, when offered a choice, more mites established on parturient scale of either species if they had been reared on oleander versus red scale (main effect: F[1,36] ⫽ 6.48; P ⬍ 0.02) (Table 3). Mites reared on red scale established more often on oleander than on red scale when they were offered a choice between early third and gravid third instar oleander scales and between virgin and gravid third instar red scales (F[1,36] ⫽ 59.7; P ⬍ 0.001) (Table 5). Also, significantly more mites established on gravid

oleander scale than on any of the other scale stages and species (host species by host stage interaction: F[1,36] ⫽ 44.74; P ⬍ 0.001) (Table 5). We conclude from these experiments that H. cooremani establishes more readily on the older stages of oleander scale, equally readily on the third instar stages of both scale species, and less readily on younger stages. Test of assumptions. A single mite stage (larva, protonymph, or tritonymph ⫹ adult) offered a choice between 180 second (small) and 60 third instar red scale (large) established on the scale stages in a pattern similar to those obtained for mixed mite stages. Significantly fewer mites of each stage established on the smaller second instars than on the larger third instars of female red scale (F[1,48] ⫽ 143.13; P ⫽ 0.001) (Table 6). This difference was independent of mite stage (F[1,48] ⫽ 0.01; P ⫽ 0.99) or its exposure time to the scale stage, i.e., 24 versus 80 h (F[1,48] ⫽ 0.01; P ⬎ 0.93) (Table 6). Moreover, none of the interactions was significant. When offered a choice between gravid third instar red and oleander scale for 5 days (120 h), significantly more mite stages were present on gravid oleander than on red scale (oleander scale: X ⫽ 66.0 ⫾ 23.3 [SD] per replicate; red scale: X ⫽ 2.4 ⫾ 3.4; t ⫽ 12.3, P ⬍ 0.003, df ⫽ 4). Also, more mite eggs were associated with gravid oleander than red scale (oleander scale: X ⫽ 20.8 ⫾ 2.3 per replicate; red scale: X ⫽ 5.8 ⫾ 3.9; t ⫽ 6.0, P ⬍ 0.001, df ⫽ 4) (Table 7). Finally, increasing the ratio of second to third instar from 52:60 to 260:60 (Fig. 1) did not increase the likelihood that a mite established on a second versus third instar (rs ⫽ 0.48, n ⫽ 12, P ⬍ 0.05, one-tailed test). We conclude from these results that mite stage, mixtures of mite stages, or the length of time that mites were exposed to the two scale species did not significantly influence the pattern of their establishment on these host scales. We also conclude that the mites reproduce on virgin third instar red scale and on gravid

TABLE 5

TABLE 6

The Number of Established Hemisarcoptes cooremani Thomas on Different Stages of Oleander Scale, Aspidiotus nerii (Bouche´), and California Red Scale, Aonidiella aurantii (Maskell), when Offered a Choice of a Mixture of Two Oleander and Two California Red Scale Stages for 24 h

Number of an Established Hemisarcoptes cooremani Thomas Stage When Offered a Choice between Second and Third Instar California Red Scale Aonidiella aurantii (Maskell) for 24 Versus 80 h a 24 h

Oleander scale

80 h

California red scale 2nd Instars

3rd Instar (n)

Gravid 3rd instar (n)

3rd Instar (n)

Gravid 3rd instar (n)

1.9 ⫾ 1.6a (10)

8.9 ⫾ 1.3b (10)

1.4 ⫾ 1.1ac (10)

0.3 ⫾ 1.0c (10)

Note. The mites were reared on California red scale. Mean ⫾ SD were calculated on untransformed data. Means were compared using REGWQ’s (Day and Quinn, 1989) on transformed data [log (X ⫹ 1)]. Values with the same letter did not differ significantly at the 5% level of significance.

3rd Instars

2nd Instars

3rd Instars

Larva 0.2 ⫾ 0.4a (5) 10.2 ⫾ 4.3b (5) 0.4 ⫾ 0.9a (5) 0.4 ⫾ 4.9b (5) Protonymph 0.2 ⫾ 0.4a (5) 9.6 ⫾ 2.4b (5) 0.6 ⫾ 0.9a (5) 10.2 ⫾ 4.0b (5) Tritonymph ⫾ Adult 0.2 ⫾ 0.4a (5) 9.8 ⫾ 1.9b (5) 0.0 ⫾ 0.0a (5) 10.0 ⫾ 6.71b (5) a Mean ⫾ SD’s were calculated on untransformed data. ANOVA was conducted on transformed data (log [X ⫹ 1]).

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TABLE 7 The Number of Mites that Established and the Number of Hemisarcoptes cooremani Thomas Eggs Laid on Gravid Third Instar Oleander Scale, Aspidiotus nerii (Bouche´) and Virgin Third Instar California Red Scale, Aonidiella aurantii (Maskell), When Exposed to Both Scale Species and Stages Concurrently Gravid 3rd instar

Mite stage

Oleander scale

California red scale a

Probability t test

Eggs Mites

66.0 ⫾ 23.3 (5) 20.8 ⫾ 3.2 (5)

2.4 ⫾ 3.4 (5) 5.8 ⫾ 3.9 (5)

0.003** 0.016*

Note. Five replicates per treatment and the mites used in the experiment were reared on California red scale. Mean ⫾ SD’s were calculated on untransformed data. The mean number of eggs and the mean number of mites were each compared using a paired t test. a Gravid third instar California red scale produced crawlers by the end of the experiment.

third instar red and oleander scale. In the latter case, significantly more mites reproduced on gravid oleander than on gravid red scale (Table 7). DISCUSSION

If the information from our experiments is taken collectively, the number of H. cooremani that established on a given scale stage depended on scale stage and species and, to a lesser extent, on rearing history. Few mites established on the younger scale stages: i.e., ⱕ second molt scales (Table 1). However, they readily established on the older scale stages (Table 1). If the number of established mites per stage is used as an index with which to rank the scale stages within

species, then the stages of oleander scale can be ordered: parturient female ⬎ gravid female ⬎ third instar female ⬎ younger scale stages. This ordering ranks the oleander scale stages from oldest to youngest and from largest to smallest. Israylevich and Gerson (1993) show a similar ranking for H. coccophagus infesting oleander scale in laboratory cultures and in a field population. Ovipositing (⫽ parturient) oleander scale supported more H. coccophagus per scale than did the younger scale stages. The ordering of California red scale stages, using the same criterion, does not rank the scale stages from oldest to youngest or from largest to smallest. Instead, it orders them as follows: virgin third instar female ⫽ male pupa ⬎ parturient third instar female ⬎ gravid third instar female ⬎ younger scale stages. Fewer mites established on parturient and gravid third instar red scales probably because of the morphology of the scale’s cover and body in these stages, i.e., the body is heavily sclerotized and joined, dorsally, to a hardened scale cover and, ventrally, to a waxy sheath (the vellum) (Fondi, 1990; Honda and Luck, 1995). These features likely make the scale cover difficult to penetrate and the scale body difficult to pierce. Moreover, the mite produced fewer offspring on gravid female red scale than on either gravid oleander scale or third instar red scale. The gravid red scale has also proven to be less vulnerable to other natural enemies. For instance, the parasitoids, Aphytis melinus, A. lingnanensis Compere, and Encarsia perniciosi (Tower), and the coccinellid scale predator, Rhyzobius lophanthae (Blaisdahl), were unable to penetrate the scale cover or the sclerotized scale body; or, they were able to do so only with great difficulty (Rosen and DeBach, 1979; Yu et al., 1990; Honda and Luck, 1995; Forster et al., 1995). Unlike red

FIG. 1. The number of Hemisarcoptes cooremani Thomas that established on second and third instar oleander scale, Aspidiotus nerii (Bouche´), in mixtures of the two instars at differing ratios. The number of third instar scale was held constant at 60 per fruit, whereas the number of second instars in the mixture ranged from 53 to 260 per fruit. See text for further details.

LABORATORY EVALUATION OF Hemisarcoptes cooremani

scale, the body of oleander scale does not become sclerotized in the older age classes and its cover remains soft and unattached to the body (Honda and Luck, 1995). These features appear to explain the higher establishment rate of H. cooremani on the older oleander scales. A mite’s rearing history influenced this ranking only slightly and the effect was limited largely to one scale stage, the third instar. If a mite was reared on oleander scale, it was more likely to establish on a third instar oleander scale. If it was reared on red scale, it was more likely to establish on a third instar red scale. This influence appeared to be independent of whether or not the mites were offered a choice among the two scale species (Tables 3 and 4). Invulnerability of gravid and parturient red scale probably precluded any rearing effect from being manifested on a mite’s choice of these stages, although more of the mites reared on oleander scale established on parturient red scale than did mites reared on red scale. Finally, the mite’s propensity to establish on a specific host species or stage was independent of the mite’s stage or the length of time that it was exposed to a host species or stage. Moreover, an increasing ratio of second to third instar oleander scale did not increase the likelihood that a mite would establish on the smaller, second instar scale (Fig. 1). Thus, our results suggest that H. cooremani does not establish on oleander or red scale stages randomly. Rather, it establishes more readily on the larger, more easily penetrated scale stages. These stages support the largest number of mites and yield the most mite offspring. We suspect that the mite’s lower rate of establishment on the smaller scale stages, i.e., second molts and instars or younger, reflects the paucity of resources that these stages provide. Feeding on the younger, smaller scale stages kills them (Gerson and Schneider, 1981a; G. Jiang, pers. obs.), whereas feeding on the larger stages allows the mite to develop and reproduce before the scale dies. Also, a parturient oleander scale is substantially larger than a third instar red scale (DeBach and White, 1960). Studies with H. coccophagus (Gerson and Schneider, 1981a) show that these mites are negatively phototropic and remain on a scale for their entire life cycle unless they are forced to move by the scale’s deterioration or death. Thus, the results from our study, when coupled with those of Gerson and Schneider, (1981a,b), suggest that a large scale provides sufficient resources for a single female mite to develop and, perhaps, reproduce. The mite would not be required to move to other scales if she were the sole occupant feeding on a large scale. At higher mite densities, interspecific competition might force her to move to new scales because of the old scale’s deterioration or death. Similarly, feeding on small stages would also force a mite to move

181

before it matures because of the scale’s death. Forced moves likely subjects the mite to higher mortality rates. Thus, we are suggesting that the nonrandom settling pattern on hosts by Hemisarcoptes reflects the likely survival and reproductive prospects for a mite choosing that host type. In general, the mites appear to prefer the larger host stages as modified by morphological characteristics. Clearly, additional behavioral studies similar to those conducted by Gerson and Schneider (1981a,b) and by Israylevich and Gerson (1993) are required to determine the trade-off between resource size and host/prey species and a mite’s reproductive potential on that species and stage. An alternative explanation exists, however, for the pattern of mite establishment with scale size and age. The likelihood that a mite establishes on a scale may also be related to the scale’s size: the smaller the scale the less likely it will be encountered by the mite. While this may explain encounter rate, it seems unlikely to explain the establishment pattern. When we increased the ratio of small to large oleander scales in an arena, we substantially increased the likelihood that a mite would encounter the smaller scale stage. This did not lead to an increase in the number of mites that established on this smaller stage, however. Thus, we conclude that, even though the mites encountered the smaller scale more often, they rarely chose to establish on them. This is also suggested by the pattern of establishment on the larger, gravid female stages. It is unlikely that the mites encountered fewer gravid female red scales when they were offered a choice between gravid oleander and red scale. It seems more likely that the choice of rejecting or accepting these scale stages occurred after the mites encountered them. Scale morphology seems to be the most likely factor influencing a mite’s choice of the gravid scale stage, e.g., the hardened scale cover and sclerotized scale body of a gravid female red scale. Based on our experiments, H. cooremani can be mass produced on oleander scale using a production system similar to that developed by DeBach and White (1960) for the mass production of Aphytis species (Aphelinidae: Hymenoptera). Red scale appears to be a poor choice of an insectary host for mass production because the mite seems restricted to the use of one scale stage, the virgin female, if it is to reproduce. This scale stage represents only 17% of the scale’s life cycle (Yu and Luck, 1988) and the mite produces fewer offspring on this species than on third instar or gravid instar oleander scale. While the mite will establish on gravid and parturient female red scales, it appears reluctant to do so and, when it does, it produces few offspring. Thus, of the two species we tested, oleander scale appears to be the best suited species for mass producing the mite. However, studies by Izraylevich and Gerson (1993)

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suggest that oleander scale may not be as good a host as latania scale for mass production. These workers found that H. coccophagus evinced substantially better survival and was much more fecund on latania scale than on oleander scale when both species were grown on potatoes. In fact, of the four scale species they studied (latania scale, oleander scale, and the chaff scales, Parlatoria pergandii Comstock and P. cinerea Hadden), oleander scale was the poorest host for H. coccophagous. Thus, latania scale should be tested as a potential laboratory host for H. cooremani. In their laboratory and field study, Izraylevich and Gerson (1993) found that H. coccophagus occurred on latania scale in higher numbers than on either the chaff or the oleander scales. It did the poorest on oleander scale. This pattern was manifested in both mite survival and fecundity. Moreover, in the laboratory, the mite suffered substantially more mortality on oleander than on latania scale. Although H. coccophagus showed the same pattern of host-associated survival and reproduction in both the field and the laboratory on latania and oleander scale, it suffered substantially more mortality in the field. These investigators suggested that this difference was probably due to the increased mortality that H. coccophagus suffered when it searched for and penetrated new hosts following dispersal after their original hosts became overcrowded, deteriorated, or died. Our study of H. cooremani, that of H. coccophagus by Israylevich and Gerson (1993), and the field observations of H. malus by Gulmahamad and DeBach (1978) all suggest that Hemisarcoptes prefers larger scale stages with softer bodies, i.e., either the adult or reproducing female scale (⫽ parturient female). These stages are easily penetrated. Although care must be exercised when extrapolating laboratory results to the field situation, we conclude from our study and those of these workers that Hemisarcoptes does not hold much promise as an augmentative biological control agent for the suppression of California red scale. We base our conclusion on the scale’s invulnerability during the gravid and parturient stages, the virgin female scale’s small size, the stage’s intermittent availability ontogenetically, and the interspecific competition to which the mite would be subjected from other natural enemies. The scale’s small virgin female stage and its intermittent availability (17% of the scale’s life history; Yu and Luck, 1988) provides insufficient resources for the mite to reproduce at a rate that would permit it to suppress a red scale population. This effect would only be exacerbated by the scale’s smaller size when it grows on the trunk or scaffolding branches of a citrus tree. These scales are smaller than the virgin female scales growing on the fruits or leaves of the same tree (Luck and Podoler, 1985; Walde et al., 1989; Hare and Luck, 1991). Clearly, however, Hemisarcoptes spp. have potential as

a biological control agent of other diaspidid species (Tothill, 1919; Hill et al., 1993, Kaufmann, 1977; Gerson and Smiley, 1990). ACKNOWLEDGMENTS We thank Dr. U. Gerson, Department of Entomology, Hebrew University of Jerusalem, Rehovot, Israel for advice and discussion of Hemisarcoptes biology, experimental protocols, and their use in biological control. We also thank Dr. R. J. Beaver, Department of Statistics, University of California, Riverside for statistical advice and Drs. J. G. Morse and M. Hoddle, Department of Entomology, University of California, Riverside for critical review of the manuscript. The research was supported by BARD Grant US-2359-93C to R.F.L. and M.A.H. and by a Citrus Research Board grant to R.F.L.

REFERENCES Bartlett, B., and DeBach, P. 1952. New natural enemies of avocado pests. Citrus Leaves 32, 16–17. Day, R. W., and Quinn, G. P. 1989. Comparisons of treatments after an analysis of variance in ecology. Ecol. Mono. 59, 433–463. DeBach, P., and Rosen, D. 1991. ‘‘Biological Control by Natural Enemies.’’ Cambridge Univ. Press, New York. DeBach, P., and White, E. B. 1960. Commercial mass culture of the California red scale parasite, Aphytis lingnanensis. Calif. Agric. Exp. Stn. Bull. 770, 1–58. Ebeling, W. 1950. ‘‘Subtropical Entomology,’’ Lithotype Processing Co., San Francisco. Ebeling, W. 1959. ‘‘Subtropical Fruit Pests,’’ Univ. Calif. Div. Agric. Sci., Berkeley. Flaherty, D. L., Pehrson, J. E., and Kennett, E. E. 1973. Citrus pest management studies in Tulare County. Calif. Agric. (May), 3–7. Fondi, I. 1990. The scale cover. In ‘‘Armored Scale Insects’’ (D. Rosen, Ed.), Vol. A, pp. 43–57. Elsevier, New York. Forster, L. D., Luck, R. F., and Grafton-Cardwell, E. E. 1995. ‘‘Life Stages of California Red Scale and its Parasitoids.’’ Univ. Calif., Div. Agric. Nat. Resources Publ. no. 21529, 12 pp. Gerson, H., and Schneider, R. 1981a. Laboratory and field studies on the mite Hemisarcoptes coccophagus Meyer (Astigmata: Hemisarcoptidae), a natural enemy of armored scale insects. Acarologia 22, 199–208. Gerson, H., and Schneider, R. 1981b. The hypopus of Hemisarcoptes coccophagus Meyer (Acari: Astigmata: Hemisarcoptidae). Acarologia 23, 171–176. Gerson, U., and Smiley, R. L. 1990. ‘‘Acarine Biocontrol Agents.’’ Chapman & Hall, New York. Gerson, U., O’Connor, B. M., and Houck, M. A. 1990. Acari. In ‘‘Armored Scale Insects’’ (D. Rosen, Ed.), Vol. B, pp. 77–97. Elsevier, New York. Grafton Cardwell, E. E. 1994. Resistance of California red and yellow scale in the San Joaquin Valley of California. Resistance Pest Management 6, 7–9. Gulmahamad, H., and DeBach, P. 1978. Biological control of the San Jose scale Quadraspidiotus perniciosus (Comstock) (Homoptera: Diaspididae) in southern California. Hilgardia 46, 205–238. Haney, P. B., Morse, J. G., Luck, R. F., Griffiths, H., Grafton-Cardwell, E. E., and O’Connell, N. V. 1992. ‘‘Reducing Insecticide Use and Energy Costs in Citrus Pest Management.’’ UC IPM Publ. No. 15, 62 pp. Hare, J. D., and Luck, R. F. 1991. Indirect effects of citrus cultivars on life history parameters of a parasitic wasp. Ecology 72, 1576–1585.

LABORATORY EVALUATION OF Hemisarcoptes cooremani Hill, M. G. 1989. Diaspididae, armoured scales (Homoptera). In ‘‘A Review of Biological Control of Insect Pests and Weeds in New Zealand 1874 to 1987’’ (P. J. Cameron, R. L. Hill, J. Bain, and W. P. Thomas, Eds.), pp. 177–182. Tech. Comm. CAB International Institute of Biological Control 10. CAB International, Wallingford, UK. Hill, M. G., Allen, D. J., Henderson, R. C., and Charles, J. G. 1993. Introduction of armoured scale predators and establishment of the predatory mite Hemisarcoptes coccophagus (Acari: Hemisarcoptidae) on latania scale, Hemiberlesia lataniae (Homoptera: Diaspididae) in kiwifruit shelter trees in New Zealand. Bull. Entomol. Res. 83, 369–376. Honda, J. Y., and Luck, R. F. 1995. Scale morphology effects on feeding behavior and biological control potential of Rhyzobius lophanthae (Coleoptera: Coccinellidae). Ann. Entomol. Soc. Am. 88, 441–450. Houck, M. A. 1989. Isozyme analysis of the phoretic mite, Hemisarcoptes (Acari: Acariformes) and its beetle associate, Chilocorus (Coleoptera: Coccinellidae). Entomol. Exp. Appl. 52, 167–172. Houck, M. A., and O’Connor, B. M. 1990. Ontogeny and life history of Hemisarcoptes cooremani Thomas. Ann. Entomol. Soc. Am. 83, 161–205. Izraylevich, S., and Gerson, U. 1993. Mite parasitization on armored scale insects: Host suitability. Exp. Appl. Acarol. 17, 861–875. Kaufmann, T. 1977. Hemisarcoptes sp. and biological control of the date palm scale, Parlatoria blanchardi Targioni, in the Sahel region of Niger. Environ. Entomol. 6, 882–884. Luck, R. F. 1983. Integrated pest management in California citrus. Proc. Int. Soc. Citriculture, Nov. 9–14, 1981. Tokyo, Japan 2, 630–635. Luck, R. F., and Podoler, H. 1985. Competitive exclusion of Aphytis lingnanensis by A. melinus: Potential role of host size. Ecology 66, 904–913. Luck, R. F., Forster, L. D., and Morse, J. G. 1997. An ecologically based IPM program for citrus in California’s San Joaquin Valley using augmentative biological control. Proc. Int. Soc. Citriculture, May 12–17, 1996, Sun City, South Africa 1, 499–503. Morse, J. G., and Klonsky. 1994. Pesticide use on California citrus: A baseline to measure progress in adoption of IPM. Calif. Grower 18, 16, 19–26. Moreno, D. S., and Luck, R. F. 1992. Augmentative releases of Aphytis

183

melinus (Hymenoptera: Aphelinidae) to suppress California red scale (Homoptera: Diaspididae) in southern California lemon orchards. J. Econ. Entomol. 85, 1112–1119. Moreno, D. S., Haney, P. B., and Luck, R. F. 1987. Control of the Argentine ant, Iridomyrmex humilis (Hymenoptera: Formicidae), with chlorpyrifos and diazinon and subsequent effects on populations of several citrus pests. J. Econ. Entomol. 80, 208–214. Pickett, A. D., and Patterson, N. A. 1953. The influence of spray programs on the fauna of apple orchards in Nova Scotia. IV. A Review. Can. Entomol. 85, 472–478. Rohlf, F. J., and Sokal, R. R. 1995. ‘‘Statistical Tables.’’ Freeman, New York. Rosen, D., and DeBach, P. 1978. Diaspididae. In ‘‘Introduced Parasites and Predators of Insect Pests and Weeds: A World Review’’ (C. P. Clausen, Ed.), pp. 78–128. U.S. Dept. Agric. Agric. Handbk. 480 U.S. Gov. Printing Off. Washington, D.C. Rosen, D., and DeBach, P. 1979. Species of Aphytis of the World (Hymenoptera: Aphelinidae). Junk, The Hague. SAS Institute Inc. 1988. ‘‘SAS Language for Personal Computers, Release 6.03 Edition.’’ Cary, NC: SAS Institute Inc. Samarasinghe, S., and LeRoux, E. J. 1966. The biology and dynamics of the oystershell scale Lepidosaphes ulmi (L.) (Homoptera: Diaspidae), on apple in Canada. Ann. Entomol. Soc. Quebec 11, 206–292. Sokal, R. R., and Rohlf, F. J. 1995. ‘‘Biometry.’’ Freeman, New York. Tashiro, H. 1966. Improved laboratory technique for rearing California red scale on lemons. J. Econ. Entomol. 59, 604–608. Tothill, J. D. 1919. Some notes on the natural control of the oystershell scale. Bull. Entomol. Res. 9, 183–196. Walde, S. J., Luck, R. F., Yu, D. S., and Murdoch, W. W. 1989. A refuge for red scale: The role of size selectivity by a parasitoid wasp. Ecology 70, 1700–1707. Yu, D. S., and Luck, R. F. 1988. Temperature dependent size and development of California red scale (Homoptera: Diaspididae) and its effect on host availability for the ectoparasitoid, Aphytis melinus DeBach (Hymenoptera: Aphelinidae). Environ. Entomol. 17, 154– 161. Yu, D. S., Luck, R. F., and Murdoch, W. W. 1990. Competition, resource partitioning and coexistence of an endoparasitoid Encarsia perniciosi (Tower) and ectoparasitoid Aphytis melinus DeBach (Hymenoptera: Aphelinidae) of the California red scale (Homoptera: Diaspididae). Ecol. Entomol. 15, 496–480.