Sublethal Effects of Pesticides on the Parasitoid Aphytis melinus (Hymenoptera: Aphelinidae)
JAY A. ROSENHEIM ANDMARJORIE A. HOY Department of Entomological Sciences, University of California, Berkeley, California 94720
J. Econ.Entomo!.81(2): 476-483 (1988) ABSTRACT Sublethal effects of insecticides on the parasitoid Aphytis melinus DeBach were investigated. Longevity, daily rate of progeny production per female, and size and sex ratio of offspring were measured for parasitoids exposed to rates near the LC,;s of carbaryl, chlorpyrifos, dimethoate, malathion, and methidathion. Survivorsof the exposure to carbaryl exhibited no significantsublethal effects.Exposure to each of the organophosphorous materials reduced longevity by 73-85% and temporarily depressed progeny production. Chlorpyrifos also shifted the sex ratio of offspring toward more males. The strength and variability of sublethal effects found in this and other studies indicate that sublethal effects must be considered to evaluate accurately the selectivity of pesticides in favor of parasitoids.
KEY WORDS Insecta, Aphytis melinus, biological control, integrated pest management
THE IMPORTANCEof integrating chemical and bi- (Irving & Wyatt 1973, Croft & Brown 1975, O'Brien ological control has become increasingly apparent et al. 1985, Hassan et al. 1987). since the advent of synthetic organic pesticides. The facultatively gregarious ectoparasite Aphy- Use of pesticides incompatible with parasitoid and tis melinus DeBach is the major biological control predator activity has produced target pest resur- agent of California red scale, Aonidiella aurantii gences and secondary pest outbreaks throughout (Maskell) (Homoptera: Diaspididae), a key pest of the world's agroecosystems (Luck et al. 1977, Met- citrus in California and other areas of the world calf 1986). These ecological disruptions have re- (Rosen & De Bach 1979). Because biological control sulted in increased crop damage, increased need of A. aurantii and other key pests of citrus, in- for additional pesticide applications, accelerated cluding citrus thrips, Scirtothrips citri (Moulton), evolution of pesticide resistance, and increased citrus red mite, Panonychus citri (McGregor), and general contamination of the environment (Met- several lepidopteran species, is often incomplete in calf 1986). An important means of avoiding these California, application of pesticides is currently a problems is the use of pesticides whose action spares major element of citrus IPM (University of Cali- natural enemies through either physiological or fornia 1984, Luck et al. 1986). Pesticide impact on ecological selectivity. Identification of selective A. melinus in the field appears to be severe (Phillips compounds depends upon an understanding of pes- et al. 1983, Griffiths et al. 1985). Attempts have ticidal effects on both pest and natural enemy pop- been made to lessen this impact by identifying ulations in the field. Therefore, host-parasitoid- pesticides with low acute toxicity to A. melinus pesticide interactions have been investigated since (Bartlett 1966, Abdelrahman 1973, Davies & the acceptance of the integrated pest management McLaren 1977, Morse & Bellows 1986), short re- (IPM) approach (e.g., DeBach & Bartlett 1951, Stern sidual activity (Campbell 1975, Bellows et al. 1985), et al. 1959, Bartlett 1964, 1966, Hull & Beers 1985, or pesticides to which A. melinus has evolved in- Hassan et al. 1987). creased tolerance (Rosenheim & Hoy 1986). The The complexity of host-parasitoid-pesticide in- results of these laboratory studies have not always teractions is introduced by parasitoid behavior agreed with observations in the field. Chlorpyrifos, (Bartlett 1966, Croft 1977), pesticide residue chem- consistently the most acutely toxic scalicide in the istry, insect developmental physiology (Schoonees laboratory (Morse & Bellows 1986, Rosenheim & & Giliomee 1982, Flanders et al. 1984, Bellows et Hoy 1986), appears to be one of the least disruptive al. 1985, Bull & Coleman 1985), the variable ge- to A. melinus in the field (]. Gorden, Pest Man- netic composition of parasitoid populations (Schoo- agement Associates, Exeter, Calif.; H. J. Griffiths, nees & Giliomee 1982, Rosenheim & Hoy 1986), Entomological Services Inc., Corona, Calif., per- and the impact of pesticides upon the host popu- sonal communications), apparently at least in part lation (Waage et al. 1985). A pesticide's toxic effects due to a shorter residual toxicity (Luck et al. 1986; on the parasitoid are also complex. Pesticides may H. J. Griffiths, personal communication). An ad- cause both acute mortality and various sublethal ditional factor possibly contributing to these ap- effects that may alter the parasitoid's ability to parently conflicting results is the variable sublethal reproduce at the expense of the host population effects of different insecticides. This possibility was
0022-0493/88/0476-0483$02.00/0 © 1988 EntomologicalSocietyof America April 1988 ROSENHEIM & Hoy: SUBLETHAL EFFECTS ON PESTICIDES ON Aphytis 477 suggested by observations, made during artificial ed strip of electrician's tape (5 x 18 mm) affixed selection for increased pesticide tolerance in A. to the gauze cap. melinus, that parasitoids surviving exposures to in- Three materials widely used for California red secticides were not reproducing at normal rates scale control-carbaryl (Sevin 80S [sprayable]; (unpublished data). Union Carbide Chemical Co., Research Triangle Our study was conducted to determine if vari- Park, N.C.), malathion (Malathion 25S; American able sublethal effects explain the discrepancies be- Cyanamid Co., Wayne, N.J.), and methidathion tween laboratory and field studies of pesticide se- (Supracide 2EC [emulsifiable concentrate]; CIBA- lectivity towards A. melinus, and to use A. melinus Geigy Co., Basel, Switzerland)-one material used in citrus as a model system to evaluate the contri- for citrus thrips control (dimethoate [Cygon 400]; bution of sublethal effects to the overall impact of American Cyanamid Co., Wayne, N.J.), and one pesticides on parasitoids. material used for control of both California red scale and several lepidopteran pests (chlorpyrifos [Lorsban 4EC]; Dow Chemical Co., Midland, Mich.) Materials and Methods were tested, along with a water plus spreader con- Colony Collection and Maintenance. The A. trol. Time requirements precluded completely si- melinus colony was collected October 1984 in a multaneous treatments, but all treatments began commercial navel orange grove in Tulare County, within a 6-d period and were evaluated together Calif. The population's field history of pesticide during the following 4-6 wk. exposure has been described previously (colony no. Approximately 10 female A. melinus, distin- 1, Rosenheim & Hoy [1986]). The colony has a high guished from males under a stereomicroscope with- tolerance to insecticides relative to other field pop- out using anaesthesia, were added to each of 10 ulations tested (Rosenheim & Hoy 1986). The col- vials after carbon dioxide anaesthesia (10 s). The ony was maintained in the laboratory at 27 ± 2°C, vials were held for 24 h at 27 ± 0.5°C and 74% 70 ± 15% RH, and a photoperiod of 16:8 (L:D) on RH under constant light. On day 4, results of the a uniparental strain of oleander scale, Aspidiotus tests were recorded. Individuals were considered nerii Bouche, that was grown under constant dark- dead if they were unable to maintain a normal ness at 24 ± 1°Con russet potatoes, Solanum tuber- posture or walk normally at a rate of at least 1 osum L. Honey was provided in the colony cage. mm/s. Survivors from two exposure vials or a single Experimental Design, Our general approach was control vial (about 10 females total) were added to to expose young female A. melinus to pesticide a single glass jar (3.8 liter) covered with gauze and residues that would cause about 50% mortality provided with honey and a single potato bearing within 24 h, remove the survivors, provide them excess mature oleander scales (ca. 70 d old). These with excess numbers of hosts, and then assess their colony jars (n = 5 for each treatment) were held longevity, progeny production, and the size and for parasitoid oviposition at 27 ± 2·C, 70 ± 15% sex ratio of their progeny. Exposure to an LCso was RH, and a photoperiod of 16:8 for the remainder chosen as a means of comparing sublethal effects of the experiment. of pesticides with widely varying acute toxicities. On each successive day, mortality was assessed. In the field, parasitoids are exposed to a range of Jars were filled with carbon dioxide for 60 s to pesticide concentrations that is high at the time of anaesthetize the parasitoids, which were collected application and decreases as the residue degrades, by removing the potato and inverting the jar over so that some parasitoids are exposed to rates equiv- a glass funnel positioned over a small collecting alent to the LCso' vial. Parasitoids were scored as dead or alive using Our experimental protocol was as follows. On the same criterion described earlier. Dead parasit- day 1, adult parasitoids (0-24 h old) were collected oids were removed every day, a fresh potato with for testing by placing parasitized A. nerii in an scales was provided (on oviposition days 1-6 and emergence cage. The emergence cage was light- every third day thereafter), and fresh honey was proof except for 12 removable glass test tubes, each added every fifth day. Parasitoids found dead were provided with streaks of honey, in which the para- assigned a time of death 12 h before. Those para- sitoids congregated due to their positive phototro- sitoids that were still alive were returned to the pism. On day 2, the host material was removed colony jars following 10 s of additional carbon diox- and the parasitoids were left in the cage to ensure ide anaesthesia. This procedure was continued until mating. On day 3, disposable plastic cups (30 ml) all parasitoids had died. Parasitoids lost between and polyester gauze were treated by dipping them successive scorings (13/287 = 4.5% of all females) for 5 s into commercial grade insecticide solutions were assumed to have died (dead wasps became formulated in distilled water with a spreader dry and were difficult to collect). To avoid biasing (0.025% Triton AG-98; Rohm & Haas Co., Phila- the data, live parasitoids that escaped or were delphia, Pa.). The cups were drained onto paper crushed during handling (4/287 = 1.4% of total) toweling, the gauze was pressed to remove excess were assigned longevities equal to the average of solution, and both were air-dried in a hood. The the other parasitoids then alive. cups capped with the gauze were then used as Potatoes removed from the colony jars were held exposure vials. Honey was provided on an untreat- individually for parasitoid development and emer- 478 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 81, no. 2
gence in glass jars (950 ml) covered with gauze and peat ed-measures ANOVA. An orthogonal polyno- not provided with honey. (By withholding honey, mial decomposition of the within subjects terms the emerging parasitoids quickly starved, enabling (the main effect for time and the interaction of us to assess more accurately the duration of the time with insecticide) into linear, quadratic, and emergence period.) A preliminary experiment was cubic trend components was performed to provide conducted to determine the development rate of a detailed analysis of the progeny production curves A. melinus under our experimental conditions. (Sokal & Rohlf 1981; Dixon 1985, 367-379). Anal- Twenty female parasitoids were held for 24 h on yses were performed using the BMDP computer day 0 with excess A. nerii for oviposition (three statistical package, programs P7D and P2V (Dixon replicates). The parasitoids were then removed. The 1985). progeny were reared at 28 ± 0.5°C, 65 ± 10% RH, and a photoperiod of 16:8, and monitored daily for Results adult emergence. No emergence occurred before day 12; 1.00 ± 1.00 (f ± SD) parasitoids emerged Acute mortality and sublethal effects of insec- on day 12, 36.33 ± 12.66 on day 13, 16.33 ± 2.08 ticides on the longevity, progeny production, and on day 14, 0.33 ± 0.58 on day 15, 0.33 ± 0.58 on size and sex ratio of offspring of A. melinus are day 16, and none thereafter until the second gen- summarized in Table 1. The total number of prog- eration began emerging on day 24. Thus, potatoes eny produced per female surviving the exposure removed from the colony jars were held for 21 d varied significantly between treatments (F = 19.07; (or 19 d for potatoes left in colony jars for 3 d) df = 5, 11; P < 0.0001). Exposure to carbaryl, the under the same conditions used with the colony only carbamate tested, did not reduce progeny pro- jars. This holding period encompassed the entire duction, whereas the remaining four chemicals, all emergence of the first generation and excluded the organophosphates (OPs), caused reductions of about second generation. Although sublethal effects of 82-90%. Most of these reductions are attributable pesticide exposure on the developmental rate of to the impact of the OPs on longevity, which also progeny were not specifically investigated, 25 hold- varied significantly between treatments (F = 71.71; ing jars for each treatment were inspected daily to df = 5, 11; P < 0.0001). Carbaryl produced an determine the earliest day of emergence; in no case insignificant increase in mean longevity relative to did emergence occur before day 12. In addition, the control, whereas the OPs caused reductions of none of the emerged parasitoids was still alive at about 73-85%. Survivorship curves (Fig. 1) re- the end of the 19- or 21-d holding periods in any vealed substantial delayed mortality of the OP- of the jars (parasitoids die in one to several days exposed parasitoids during days 1-3 after exposure. when held without honey), indicating that the Parasitoids surviving this early period of high mor- emergence was complete in all cases. tality displayed longevities similar to those of the All emerged progeny were collected from the controls. This unimodal distribution of mortalities holding jars, counted, and their sex was deter- is not analogous to "latent toxicity" sensu Moriarty mined. Progeny from oviposition days 1 and 2 were (1969), which implies a polymodal distribution. cleared in glacial acetic acid and chloral phenol Progeny production figures were standardized for 24 h and mounted on slides using the procedure to include the effects of variable longevity by cal- of Rosen & De Bach (1979). Hind tibia length, an culating the average progeny production per fe- index of parasitoid size, was measured to the near- male per day lived (i.e., progeny per female-day) est 0.003 mm at 400 x magnification with an ocular (Table 1). Overall average numbers of progeny per micrometer. female-day were not significantly lower in the OP Statistical Analysis. Data on longevity, overall treatments than in the carbaryl or control treat- progeny production per female, average rate of ments (F = 1.31; df = 5,24; P = 0.29). These overall progeny production, and the sex ratio and size of average figures are, however, somewhat mislead- offspring were analyzed with one-way analyses of ing, because they are confounded by the consid- variance (ANOVA). Sex ratio data were analyzed erable variation in daily progeny production as- as the arcsine transformed proportion of female sociated with parasitoid age (Fig. 2). To include progeny. Families of pairwise contrasts, computed the effects of this variation, the data were analyzed for each one-way ANOV A, were done using the in two ways: first, simple one-way analyses of vari- Bonferroni inequality to maintain overall a ::;0.05 ance on each day's progeny production values were (Dixon 1985). The assumption of equal variance of made separately. These analyses revealed signifi- ANOV A was explicitly tested in all cases, and sep- cant treatment effects on days 1 and 2 after ex- arate variance tests (Welch model) were employed posure (F = 7.86; df = 5, 24; P = 0.0002 and F = when variances differed with P < 0.10 (Dixon 1985). 3.80; df = 5, 24; P = 0.0112, respectively), with Trends in arcsine transformed proportion of female the parasitoids in the OP treatments producing progeny produced (the dependent variable) over fewer progeny than the parasitoids in the carbaryl time (the independent variable) were examined or control treatments (Fig. 2). Differences in daily with simple linear regression (regression model I, progeny production between treatments decreased Sakal & Rohlf [1981]). Changes in progeny pro- rapidly, becoming statistically insignificant after duction rate per female were analyzed using re- day 2. (One exception-significantly greater prog- April 1988 ROSEN HElM & HOY: SUBLETHAL EFFECTS ON PESTICIDES ON Aphytis 479
100
~ Control .•. Carbaryl .•. Dlmothoale 80 .•. Malathion t-C":)CJ:lOl1:lO"> C'J.....•O_OO -+- Chlorpyrifos 000000 - Mathidathlon 000000 +1 +1 +1 +1 +1 +1 •....•\Xl_ •....•cnC':! OOClCJ)CJ:lCOCO 60 C'I •....••....••....•...... •...... • ~ 000000 'E il ~.2t):t~.5t..!t ~f6~~g}~ j 40 ----~~ COC'?lI)OO_ 8-,....;---00000 000000 +1 +1 +1 +1 +1 +1 20 ~OC(lr-c-100 l1:lll':lC':l~-ql"" c\lC'lC'lC'lC'JCl 000000
;... ",{J{J~ '" '" 10 20 30 40 50 c (;i'OOC;;-Oe.lOO [~ ~ ee~~;2OC'l
~ Cl3 Cl3 C'tI ctI C'!3 C\lt.ncnOOe\l eny production by methidathion-treated parasit- "'l:J'C":lC':lC\l (Fig. 2). Because our experimental design entailed ClSCl:lCU(f$~..!:J COC?C?C? .....•o.l the repeated measurement of progeny production, .....ici""';""';C"Se.:i an ANOVA with a repeated-measures design was +1 +1 +1 +1 +1 +1 lCr.ot-l1":ltOCO appropriate. One complication, however, was that -.;<-.; less intoxicated parasitoids that occurred when the most highly intoxicated individuals died. -0- Control All offspring sex ratios were strongly female- .•• Gillbaryl .•• DImeIhoaI8 biased, as is normal for A. melinus, except for that ••• Mal ••thion •• Chtorpyrif08 - M8thldatllion of females exposed to chlorpyrifos. In the chlor- pyrifos treatment, a significant increase in the pro- portion of males occurred (F = 5.80; df = 5, 11; P = 0.0073 [the result for chlorpyrifos is based upon 150 progeny produced over 21 d]) (Table 1). Results of linear regression analyses for each treatment indicated that the sex ratio was independent of parasitoid age for the control and all the experi- o mental treatments except for methidathion, which o 6 9 15 21 27 33 3D 45 showed an increasing proportion of female off- 2 Days post-exposure spring as wasps aged (control, r = 0.08, B (slope) = -0.79 ± 0.42 (f ± SD), P > 0.05; carbaryl, r2 = Fig. 2. Sublethal effects of five insecticides on the 0.02, B = -0.30 ± 0.37, P > 0.25; dimethoate, progeny production schedule of A. melinus. Mean num- ber of progeny produced per female-day isplotted versus T2 = 0.001, B = -0.09 ± 0.63, P > 0.10; malathion, time since the end of the exposure. r2 = 0.01, B = 0.37 ± 0.89, P > 0.25; chlorpyrifos, r2 = 0.02, B = -0.50 ± 0.95, P > 0.25; methida- thion, T2 = 0.50, B = 1.71 ± 0.44; P < 0.01). Thus, aging. The significant interaction of time and in- the divergent offspring sex ratio observed for the secticide (F = 4.03; df = 15, 57; P = 0.0001) in- parasitoids exposed to chlorpyrifos did not simply dicated that the shapes of the curves differed sig- reflect their reduced longevities. The mechanism nificantly. The significant interaction of the linear of chlorpyrifos action on offspring sex ratio is not component of time x insecticide (F = 2.98; df = clear but might include effects on the viability of 5,57; P = 0.0374) confirmed that the slopes of the stored sperm, maternal behavioral control of the linear components of the different progeny pro- primary sex ratio, or a sex-specific mortality during duction curves were not equal; the curves de- progeny development. creased more rapidly for the control and carbaryl The five insecticides did not change the size, as treatments than for the OP treatments. The qua- measured by hind tibia length, of male or female dratic trend component, which tests for a "hump- progeny produced on day 1 or 2 after exposure shaped" component in the curves, also interacted (F = 0.73; df = 5, 10; P = 0.6151 and F = 2.12; significantly with insecticide (F = 8.38; df = 5, 57; df = 5, 42; P = 0.0818, respectively). P = 0.0003), reflecting the increasing progeny pro- duction by "recovering" OP-exposed parasitoids Discussion after the initially depressed levels of days 1-2. It is difficult to distinguish between two possible ex- Our investigation has revealed significant sub- planations for this recovery-there may have been lethal effects of four OP insecticides (chlorpyrifos, a physiological recovery of intoxicated individuals dimethoate, malathion, and methidathion) on the within each replicate, or the recovery may have longevity and progeny production rates of A. mel- been caused simply by the increased relative inus. One insecticide, chlorpyrifos, also shifted the weighting of the progeny production levels of the offspring sex ratio away from the strong female Table 2. Repeated-measures ANOVA of progeny production per female-day, days 1-12, for A. melinas exposed to rcsidues of five insecticides and a water control Degrees of Source Sum of squares Mean square F P freedom Insecticide 28.79 5 5.76 4.81 0.0052 Error 22.73 19 1.20 Time 29.77 3 9.92 15.45 <0.0001 Time (l)a 29.39 29.39 28.43 <0.0001 Time (2) 0.09 0.09 0.22 NS Time (3) 0.28 0.28 0.59 NS Time x insecticide 38.87 15 2.59 4.03 0.0001 Time (1) x insecticide 15.42 5 3.08 2.98 0.0374 Time (2) x insecticide 17.30 5 3.46 8.38 0.0003 Time (3) x insecticide 6.14 5 1.23 2.56 NS Error 36.62 57 0.64 a Main effect sums of squares for time (days) and time x insecticide interaction are orthogonally decomposed into linear, quadratic, and cubic trend components. The number in parentheses following "Time" indicates the order of the orthogonal polynomial: (1) indicates the linear polynomial, (2) the quadratic polynomial, and (3) the cubic polynomial (Dixon 1985, 367-379). April 1988 ROSENHEIM & Hoy: SUBLETHAL EFFECTS ON PESTICIDES ON Aphytis 481 bias characteristic of the species (Hoffman & Ken- detected by Hsieh & Allen (1986) for Diaeretiella nett 1985). No effects on the size of progeny pro- rapae (M'Intosh) exposed as immatures within aphid duced during the first 2 d after exposure to any mummies to a LC7_16 of methomyl (a carbamate), insecticide were observed. The magnitude of the LC22_29 of acephate (an OP), or LC28-51 of permeth- combined sublethal effects of the OPs on longevity, rin. Hsieh (1984) found that D. rapae exposed to progeny production rate, and sex ratio was great. acephate residues as an adult suffered no sublethal Exposure to residues of a dimethoate solution (1.20 effects, but that exposure to a LC60 of methomyl mg/liter) caused 24-h mortality of 50.7% (a lethal resulted in a 50% reduction in longevity and a 93% effect) but actually reduced the production of fe- decrease in fecundity. Finally, O'Brien et al. (1985) male offspring by 93.4% compared with the con- found that chronic exposure of Bracon mellitor Say trols. (The figure of 93.4% was obtained from Table to an LC5 of azinphosmethyl (an OP) or chlordime- 1 by multiplying the proportional reduction in total form (a formamidine) caused moderate decreases progeny production by the proportional change in in fecundity and a significant shift of the sex ratio the percentage of females produced.) Analogous toward more females. figures (percent 24-h mortality and total percent From these examples we cannot discern any clear reduction in female progeny) for malathion, meth- patterns of the type or magnitude of sublethal ef- idathion, and chlorpyrifos are 56.7% and 91.3%, fects based upon the specific compound, class of 47.5% and 94.5%, and 48.6% and 95.8%, respec- insecticide, or parasitoid species in question. The tively (Table 1). In contrast to the OPs, carbaryl total number of studies performed to date is small, did not cause any detectable sublethal effects, a however, and it is possible that additional investi- 24-h mortality of 62.8% causing only a 58.4% re- gations will reveal patterns not yet apparent. Most duction in the number of female offspring pro- field studies and many laboratory studies combine duced. Variation among different insecticides, acute mortality and sublethal effects (e.g., Hassan combined with the magnitude of the effects of the et al. 1987) and therefore cannot be used to eval- OPs, indicates that sublethal effects must be con- uate the isolated impact of sublethal effects. sidered to evaluate accurately the selectivity of The unpredictability of potentially significant pesticides towards A. melinus. sublethal effects has prompted the 28-member Previous laboratory studies suggest that highly working group "Pesticides and beneficial organ- variable and potentially strong sublethal effects may isms" of the International Organization for Bio- be general features of the impact of synthetic or- logical Control of Noxious Animals and Plants to ganic pesticides on parasitoids. Flanders (1943) ob- adopt bioassays which are relatively long-term served that contact with sublethal sulfur residues (generally ;::.7 d), and evaluate the reduction in on citrus leaves caused Metaphycus he/vo/us (Com- "beneficial capacity" instead of simple mortality pere) to lose permanently its ability to recognize (Hassan et al. 1985, 1987). For parasitoids, the abil- hosts. Grosch (1970, 1975) found that topical ap- ity to parasitize hosts is the parameter measured. plications of the chlorinated hydrocarbon (CHC) However, this approach has not been adopted gen- heptachlor on Bracon hebetor Say at about the LD25 erally. produced a slight decrease in longevity and a small, In the case of A. melinus, our understanding of temporary depression of fecundity, but applica- acute lethality, sublethal effects, and residue dy- tions of carbaryl at the LD50 yielded a slight de- namics and toxicity of insecticides has not permit- crease in longevity and a large (> 50%), permanent ted the formulation of clear recommendations for decrease in fecundity. Irving & Wyatt (1973) found the use of the least disruptive materials for Cali- that nonlethal residues of two fungicides, benomyl fornia citrus IPM. All of the widely used materials and dichlofJuanid, and two eHC insecticides, tet- appear to be highly toxic in the laboratory (Bartlett radifon and lindane, reduced the host stabbing be- 1966, Abdelrahman 1973, Campbell 1975, Davies havior of Encarsia formosa Gahan, while the car- & McLaren 1977, Bellows et al. 1985, Morse & bamate pirimicarb had the reverse effect. Bellows 1986, Rosenheim & Hoy 1986), and we Abdelrahman (1973) found that Aphytis melinus are unable to predict the actual host-parasitoid- exposed for 24 h to residues of a LC50 of malathion pesticide interaction that may occur in the field. continued to suffer delayed mortality during 3 d The results of our study have not resolved the dis- after exposure, a result confirmed in our study. crepancy between the high acute toxicity of chi or- Plewka et al. (1975) and Krukierek et al. (1975) pyrifos in the laboratory (Morse & Bellows 1986, found progressively reduced longevities for Rosenheim & Hoy 1986) and the relatively low Trichogramma evanescens Westwood exposed to degree of disruption in the field (Luck et al. 1986; increasing doses of metasystox (an OP), DDT (a J. Gorden and H. J. Griffiths, personal communi- CHe), and methoxychlor (a CHC). Jacobs et al. cations). In fact, chlorpyrifos produced the most (1984) found no sublethal effects on the number of severe sublethal effects of any of the materials tested eggs deposited per host egg or the resulting off- in these laboratory trials. The differences between spring sex ratio for Trichogramma pretiosum (Ri- laboratory results and field experience may thus ley) exposed to up to an LC55 of endosulfan (a CHe) depend primarily upon the duration of residual or an LC90 of permethrin (a pyrethroid). Similarly, toxicity. Because the intensity of sublethal effects no sublethal effects on longevity or fecundity were may vary with the magnitude of the initial expo- 482 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 81, no. 2 sure (Krukierek et al. 1975, Plewka et al. 1975, Croft, B. A. 1977. Susceptibility surveillance to pes- Hsieh 1984), it may not be appropriate to extrap- ticides among arthropod natural enemies: modes of olate our results to sublethal effects caused by dos- uptake and basic responses. Z. P£lanzenkrank. p£lan- zenschutz. 84; 140-157. ages very different from the LC , 50 Croft, B. A. & A. W. A. Brown. 1975. Responses of To understand fully the impact of insecticides arthropod natural enemies to insecticides. Annu. Rev. on A. melinus, field studies may be necessary. Entomol. 20: 285-335. However, the design of appropriate field plots is Davies, R. A. H. & I. W. McLaren. 1977. Tolerance complex because movement of parasitoids is not of Aphytis melinus DeBach (Hymenoptera: Aphe- constrained. In general, plot size will be a critical Iinidae) to 20 orchard chemical treatments in relation consideration for field studies and will depend on to integrated control of red scale, Aonidiella aurantii knowledge of the parasitoid's dispersal ability. Re- (Maskell) (Homoptera: Diaspididae). Aust. J. Exp. covery of parasitoid populations following insec- Agric. Anim. Husb. 17: 323-328. De Bach, P. & B. Bartlett. 1951. Effects of insecticides ticide applications may depend in part upon im- on biological control of insect pests of citrus. J. Econ. migration from adjacent unaffected fields. Field Entomol. 44: 372-383. studies that measure host population levels and per- Dixon, W. J. [ed.]. 1985. BMDP statistical software. cent parasitism both before and after a pesticide University of California, Berkeley. application can reveal the combined impact of both Flanders, R. V., L. W. Bledsoe & C. R. Edwards. 1984. lethal and sublethal pesticide effects. Field studies Effects of insecticides on Pediobius foveolatus (Hy- should also reflect the outcome of the complex in- menoptera: Eulophidae), a parasitoid of the Mexican teractions generated by parasitoid behavior, de- bean beetle (Coleoptera: Coccinellidae). Environ. velopment, and population genetics, as well as pes- Entomo!. 13: 902-906. Flanders, S. E. 1943. The susceptibility of parasitic ticide residue dynamics and the ecological interplay Hymenoptera to sulfur. J. Econ. Entomol. 36: 469. of the parasitoid and host populations. Griffiths, H. J., R. Hoffman, R. Luck & D. Moreno. 1985. New attempt at managing red scale in the Acknowledgment central valley. Newsl. Assoc. Appl. Insect Ecol. 5(3): 1-6. We thank D. J. Sandri for assistance in the laboratory, Grosch, D. S. 1970. Reproductive performance of a J. Gorden (Pest Management Associates, Exeter, Calif.) braconid after heptachlor poisoning. J. Econ. Ento- and H. J. Griffiths (Entomological Services Inc., Corona, mol. 63: 1348-1349. Calif.) for discussing unpublished data, and L. E. Cal- 1975. Reproductive performance of Bracon hebe tor tagirone (University of California, Berkeley) and J. G. after sublethal doses of carbaryl. J. Econ. Entomol. Morse (University of California, Riverside) for critical 68: 659-662. review of the manuscript. We also thank the American Cyanamid, CIBA-Geigy, Dow Chemical, and Union Hassan, S. A., F. Bigler, P. Blaisinger, H. Bogenschutz, J. Brun, P. Chiverton, E. Dickler, M. A. Easter- Carbide Corporations for providing insecticides for test- brook, P. J. Edwards, W. D. Englert, S. I. Firth, P. ing. This material is based upon work supported in part Huang, C. Inglesfield, F. Klingauf, C. Kuhner, M. by USDA Competitive Grant #84-CRCR-I-1452, Re- S. Ledieu, E. Naton, P. A. Oomen, W. P. Over- gional Research Project W-84, and under a National J. meer, P. Plevoets, N. Reboulet, W. Rieckmann, Science Foundation Graduate Fellowship to J.A.R. J. L. Sam see-Petersen, S. W. Shires, A. Staiihli, J. Stevenson, J. J. Tuset, G. Vanwetswinkel & A. Q. References Cited Van Zon. 1985. Standard methods to test the side- effects of pesticides on natural enemies of insects and Abdelrahman, I. 1973. Toxicity of malathion to the mites developed by the IOBC/WPRS working group natural enemies of California red scale, Aonidiella "Pesticides and beneficial organisms." EPPO Bulletin aurantii (Mask.) (Hemiptera: Diaspididae). Aust. J. 15: 214-255. Agric. Res. 24: 119-133. Hassan, S. A., R. Albert, F. Bigler, P. Blaisinger, H. Bartlett, B. R. 1964. Integration of chemical and bi- Bogenschutz, E. Boller, J. Brun, P. Chiverton, P. ological control, pp. 489-514. In P. De Bach [ed.], Edwards, W. D. Englert, P. Huang, C. Inglesfield, Biological control of insect pests and weeds. Reinhold, E. Naton, P. A. Oomen, W. P. J. Overmeer, W. New York. Rieckmann, L. Samsille-Petersen, A. Stiiuhli, J. J. 1966. Toxicity and acceptance of some pesticides fed Tuset, G. Viggiani & G. Vanwetswinkel. 1987. Re- to parasitic Hymenoptera and predatory coccinellids. .suIts of the third joint pesticide testing programme Econ. Entomol. 59: 1142-1149. J. by the IOBC/WPRS-Working group "Pesticides and Bellows, T. S., Jr., J. G. Morse, D. G. Hadjidemetriou beneficial organisms." J. Appl. Entomol. 103: 92-107. & Y. Iwata. 1985. Residual toxicity of four insec- Hoffman, R. W. & C. E. Kennett. 1985. Effects of ticides used for control of citrus thrips (Thysanoptera: winter temperatures on the sex ratios of Aphytis mel- Thripidae) on three beneficial species in a citrus in us (Hym.: Aphelinidae) in the San Joaquin Valley agroecosystem. J. Econ. Entomol. 78: 681-686. of California. Entomophaga 30: 125-132. Bull, D. L. & R. J. Coleman. 1985. Effects of pesti- cides on Trichogramma spp. Southwest. Entomol. Hsieh, C.- Y. 1984. Effects of insecticides on Diae- Suppl. 8; 156-168. retiella rapae (M'lntosh) with emphasis of bioassay Campbell, M. M. 1975. Duration of toxicity of resi- techniques for aphid parasitoids. Ph.D. dissertation, dues of malathion and spray oil on citrus foliage in University of California, Berkeley. South Australia to adults of a California red scale Hsieh, c.-Y. & W. W. Allen. 1986. Effects of insec- parasite Aphytis melinus DeBach (Hymenoptera; ticides on emergence, survival, longevity, and fecun- Aphelinidae). J. Aust. Entomol. Soc. 14: 161-164. dity of the parasitoid Diaeretiella rapae (Hymenop- April 1988 ROSENHEIM & Hoy: SUBLETHAL EFFECTS ON PESTICIDES ON Aphytis 483 tera: Aphidiidae) from mummified Myzus persicae O'Brien, P. J., G. W. Elzen & S. B. Vinson. 1985. (Homoptera: Aphidiidae). J. Econ. Entomol. 79: 1599- Toxicity of azinphosmethyl and chlordimeform to the 1602. parasitoid Bracon mel/itor (Hymenoptera: Braconi- Hull, L. A. & E. H. Beers. 1985. Ecological selectivity: dae): lethal and reproductive effects. Environ. Ento- modifying chemical control practices to preserve nat- mol. 14: 891-894. ural enemies, pp. 103-121. In M. A. Hoy & D. C. Phillips, P., D. Machlitt & M. Mead. 1983. Impact Herzog [eds.], Biological control in agricultural IPM of two pesticides on beneficiaIs in IPM. Citrograph systems. Academic, Orlando, Fla. 68: 162-163, 168, 170. Irving, S. N. & I. J. Wyatt. 1973. Effects of sublethal Plcwka, T., J. Kot & T. Krukierek. 1975. Effect of doses of pesticides on the oviposition behaviour of insecticides on the longevity and fecundity of Tricho- Encarsia formosa. Ann. Appl. BioI. 75: 57-62. gramma evanescens Westw. (Hymenoptera, Tricho- Jacobs, R. J., C. A. Kouskolekas & H. R. Gross, Jr. grammatidae). Pol. Ecol. Stud. 1: 197-210. 1984. Responses of Trichogramma pretiosum (Hy- Rosen, D. & P. DeBach. 1979. Species of Aphytis of menoptera: Trichogrammatidae) to residues of per- the world (Hymenoptera: Aphelinidae). Ser. Ento- methrin and endosulfan. Environ. Entomol. 13: 355- mol. (The Hague) 17. 358. Rosenheim, J. A. & M. A. Hoy. 1986. Intraspecific Krukierek, T., T. Plewka & J. Kot. 1975. Suscepti- variation in levels of pesticide resistance in field pop- bility of parasitoids of the genus Trichogramma (Hy- ulations of a parasitoid, Aphytis melinus (Hymenop- menoptera, Trichogrammatidae) to metasystox in re- tera: Aphelinidae): the role of past selection pressures. lation to their species, host species, and ambient J. Econ. Entomol. 79: 1161-1173. temperature. Pol. Ecol. Stud. 1: 183-196. Schoonees, J. & J. H. Giliomee. 1982. The toxicity Luck, R. F., R. van den Bosch & R. Garcia. 1977. of methidathion to parasitoids of red scale, Aonidiel/a Chemical insect control-a troubled pest manage- aurantii (Hemiptera: Diaspididae). J. Entomol. Soc. ment strategy. Bioscience 27: 606-611. South. Afr. 45: 261-273. Luck, R. F., J. G. Morse & D. S. Moreno. 1986. Cur- Sokal, R. R. & F. J. Rohlf. 1981. Biometry, 2nd ed. rent status of integrated pest management in Cali- Freeman, San Francisco. fornia citrus-groves, pp. 533-543. In R. Cavalloro & Stern, V. M., R. F. Smith, R. van den Bosch & K. S. E. Di Martino [eds.], Integrated pest control in citrus- Hagen. 1959. The integrated control concept. Hil- groves, proceedings of the experts' meeting, Acireale, gardia 29: 81-101. 26-29 March 1985. Balkema, Boston. University of California. 1984. Integrated pest man- Metcalf, R. L. 1986. The ecology of insecticides and agement for citrus. Publ. 3303. Statewide Integrated the chemical control of insects. pp. 251-297. In M. Pest Management Project. Division of Agriculture Kogan [ed.], Ecological theory and integrated pest and Natural Resources, Berkeley, Calif. management practice. Wiley, New York. Waage, J. K., M. P. Hassell & H. C. J. Godfray. 1985. Moriarty, F. 1969. The sublethal effects of synthetic The dynamics of pest-parasitoid-insecticide interac- insecticides on insects. BioI. Rev. 44: 321-357. tions. J. Appl. Ecol. 22: 825-838. Morse, J. G. & T. S. Bellows, Jr. 1986. Toxicity of major citrus pesticides to Aphytis melinus (Hyme- Received for publication 26 May 1987; accepted 26 noptera: Aphelinidae) and Cryptolaemus montrouz- October 1987. ieri (Coleoptera: Coccinellidae). J. Econ. Entomol. 79: 311-314.