POPULATION ECOLOGY Peach Pest Management Programs Impact Beneficial Fauna Abundance and molesta (: ) Egg Parasitism and Predation

1 2 ATANAS ATANASSOV, PETER W. SHEARER, AND GEORGE C. HAMILTON

Department of Entomology, Rutgers, The State University of New Jersey, Rutgers Agricultural Research & Extension Center, 121 Northville Road, Bridgeton, NJ 08302Ð5919 Downloaded from https://academic.oup.com/ee/article/32/4/780/357650 by guest on 24 September 2021

Environ. Entomol. 32(4): 780Ð788 (2003) ABSTRACT We conducted timed visual observations of the peach canopy to monitor beneÞcial fauna diversity and abundance in orchards with reduced risk and conventional management programs. In addition, we placed sentinel Grapholita molesta (Busck) (Lepidoptera: Tortricidae) eggs in the peach canopy and determined egg parasitism, predation, and the total impact of natural enemies. Reduced risk orchards used minimal insecticide, G. molesta mating disruption, and managed sod ground cover to suppress Lygus lineolaris (Palisot de Beauvois) (Heteroptera: Miridae). Conventional orchards used organophosphorus and carbamate insecticides to control G. molesta, L. lineolaris, and other pests. Chrysoperla rufilabris (Burmeister) and C. plorabunda (Fitch) (Neuroptera: Chrysopi- dae), Coccinella septempunctata L. and Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), Orius insidiosus (Say) (Heteroptera: Anthocoridae), and Trichogramma minutum Riley (Hymenoptera: Trichogrammatidae) were the most frequently observed natural enemies in southern New Jersey peach orchards. Hippodamia convergens (Guerin-Meneville), Adalia bipunctata L., Coleomegilla macu- lata De Geer (Coleoptera: Coccinellidae), and T. exiguum Pinto et Platner (Hymenoptera: Tri- chogrammatidae) were observed less frequently. BeneÞcial fauna was more abundant in orchards with the reduced risk program compared with conventionally farmed orchards. The rate of G. molesta sentinel egg parasitism and predation was signiÞcantly higher in reduced risk orchards compared with conventional orchards. Overall, predators destroyed more sentinel eggs than did egg parasitoids.

KEY WORDS Oriental fruit , parasitoids, predators, sentinel eggs, peach orchards

THE ORIENTAL FRUIT MOTH, Grapholita molesta (Busck) Research regarding predator (Chrysopidae, is a key pest of Mid-Atlantic peach orchards and is Anthocoridae, and Coccinellidae) in fruit orchards controlled primarily with insecticide (Polk et al. refer mostly to their impact on aphids and mites 1995). Successful noninsecticidal control of G. molesta (Holdsworth 1970, Lord 1971, Carroll and Hoyt 1984, has been achieved with pheromone-mediated mating Wyss et al. 1999, Daane and Hagen 2001). Several disruption, resulting in fewer insecticide sprays ap- publications discuss the mass rearing and release of plied against this pest (Rice and Kirsch 1990, Vickers predators in fruit orchards. Hagley (1989) released 1990, Pree et al. 1994, Trimble et al. 2001, Atanassov et 335,000 Chrysoperla carnea Stephens (Neuroptera: al. 2002). Fewer broad-spectrum insecticide sprays Chrysopidae) eggs per hectare against Aphis pomi should conserve natural enemies in the orchard eco- DeGeer (Homoptera: Aphididae) and concluded that system. Thus, more studies are needed to determine if, predator:prey ratios and daily temperatures might in- and to what extent, natural enemies can contribute to ßuence predator efÞciency. Westigard and MofÞtt successful G. molesta mating disruption programs. (1984) reported enhanced control of Psylla pyricola Likewise, studies on the impacts of natural enemies Foerster (Homoptera: Psyllidae) by predators when present in orchards can help evaluate the effective- organophosphorus insecticide control of codling moth ness of beneÞcial for managing primary was substituted with mating disruption in southern and secondary pests. Finally, the impact of natural Oregon pear orchards. Kehrliand Wyss (2001) re- enemies on G. molesta eggs may play an essential role leased Adalia bipunctata L. (Coleoptera: Coccinelli- in developing pest life tables and short-term predic- dae) on Þve different dates in autumn and found tion models. signiÞcant reduction of Dysaphis spp. (Homoptera: Aphididae) overwintering eggs. 1 E-mail: [email protected]. Egg exploitation of Choristoneura fumiferana 2 Pest Management OfÞce, Rutgers, The State University of New (Clements) (Lepidoptera: Tortricidae) by Þeld pop- Jersey, Blake Hall 217, 93 Lipman Drive, New Brunswick, NJ 08901. ulations of Trichogramma minutum revealed that 35%

0046-225X/03/0780Ð0788$04.00/0 ᭧ 2003 Entomological Society of America August 2003 ATANASSOV ET AL.: NATURAL ENEMIES OF THE ORIENTAL FRUIT MOTH 781 Downloaded from https://academic.oup.com/ee/article/32/4/780/357650 by guest on 24 September 2021

Fig. 1. Dates and spray application number of organophosphorus and carbamate insecticides applied to reduced risk and conventional orchards during 1999 and 2000. of parasitized egg masses were completely parasitized described here. Each orchard was divided in half, and (Baiand Smith1994). Yu et al. (1984a) showed that T. each half was designated as either reduced risk or minutum reared from Þeld collected eggs of Cydia conventional. Reduced risk orchards used mating dis- pomonella L. (Lepidoptera: Tortricidae) could not be ruption to control G. molesta and managed sod drive used to indicate the efÞciency of resident parasitoids. rows (hard or tall fescue) to suppress Lygus lineolaris In previous studies, sentinel host eggs were used to populations. The conventional orchards used organ- monitor the activity of released egg parasitoids. For ophosphorus and carbamate insecticides to control G. instance, sentinel C. rosaceana (Harris) (Lepidoptera: molesta populations throughout the season and their Tortricidae) egg masses were used to monitor the naturalized weedy drive rows were maintained by efÞciency of artiÞcially reared T. minutum, T. pretio- mowing and/or disking. In 1999, reduced risk orchards sum Riley, and T. platneri Nagarkatti(Hymenoptera: received, on average, 2.5 organophosphorus and car- Trichogrammatidae) that were released in apple or- bamate “alternate-row middle” (Hull and Beers 1985) chards (Lawson et al. 1997). Bourchier and Smith sprays versus 6.0 alternate-row middle sprays in con- (1998) investigated the interaction between released ventional orchards (Fig. 1). In 2000, the average num- T. minutum and indigenous spruce budworm, C. fumif- ber of alternate-row middle sprays was 2.8 and 8.5 in erana parasitoids, using sentinel host eggs. However, reduced risk and conventional orchards, respectively in these studies, the impact of predators on sentinel (Fig. 1). In 1999, reduced risk orchards used, on av- egg masses was not evaluated. In addition, no research erage, 2.2 kg (AI) per ha organophosphates and car- has been done to evaluate the beneÞcial fauna abun- bamates versus 4.3 kg (AI) in conventional orchards. dance and the role of predators and parasitoids in In 2000, the average amount of organophosphate and reducing G. molesta egg populations in peach orchards carbamate insecticides was 1.3 and 5.4 kg (AI)/ha in using mating disruption and ground cover manage- reduced risk and conventional orchards, respectively. ment to suppress pest populations. Disease management was the same for both pest pro- The objectives of this study were to monitor pred- gram orchards. ators and parasitoids by timed visual examinations of Field Observation of Beneficial Arthropods. Timed peach canopies and to evaluate parasitism and preda- bi-weekly visual examinations were conducted in re- tion of laboratory reared G. molesta eggs placed on duced risk and conventional orchards. Instead of sam- peach trees. pling a certain proportion of trees per block, we col- lected data from 10 randomly chosen trees per block (80 trees per sample date) because sample trees were Materials and Methods far enough apart to be considered independent. In This study was conducted in four commercially 1999, monitoring started on 16 June and was repeated managed peach, Prunus persica L., orchards ranging in on Þve additional dates. In 2000, observations started size from 1.6 to 7.3 ha in southern New Jersey during on 20 April and were repeated on nine additional 1999 and 2000. These study sites and their respective dates. During each 3-min observation of individual pest management programs have previously been de- tree canopies, the number of beneÞcial arthropods scribed (Atanassov et al. 2002) but will brießy be (Chrysopidae adults, larvae, and eggs, Coccinellidae 782 ENVIRONMENTAL ENTOMOLOGY Vol. 32, no. 4

Table 1. Number of beneficial insects monitored in orchards with reduced risk and conventional ground cover management

Average Ϯ SE of seasonal totals Species 1999 2000 Reduced risk Conventional Reduced risk Conventional Chrysopidae adults 4.0 Ϯ 1.1a 1.8 Ϯ 0.6b 8.3 Ϯ 2.6a 3.0 Ϯ 1.1b Chrysopidae eggs 1377.0 Ϯ 352.0a 898.0 Ϯ 255.0b 912.0 Ϯ 113.0a 595.7 Ϯ 81.2b Chrysopidae larvae 2.3 Ϯ 0.9a 1.0 Ϯ 0.4a 0.5 Ϯ 0.3a 1.5 Ϯ 1.5a Coccinellidae adults 18.0 Ϯ 6.6a 9.5 Ϯ 5.9b 43.7 Ϯ 27.8a 14.5 Ϯ 7.2b Anthocoridae adults 31.3 Ϯ 7.8a 14.8 Ϯ 5.0b 8.5 Ϯ 1.2a 3.5 Ϯ 1.3b and nymphs Hymenoptera adults 29.0 Ϯ 5.1a 9.5 Ϯ 2.3b 10.0 Ϯ 1.8a 2.3 Ϯ 0.5b Spiders 17.5 Ϯ 3.0a 7.5 Ϯ 1.4b 20.0 Ϯ 5.0a 11.5 Ϯ 8.5b

For each year, means within rows followed by the same letter are not signiÞcantly different. Downloaded from https://academic.oup.com/ee/article/32/4/780/357650 by guest on 24 September 2021 adults, Anthocoridae adults and nymphs, parasitoid temperature and ambient light conditions until para- wasps, and spiders) observed was recorded. On each sitism could be assessed. On each sample date, a rep- sample date, a representative sample of natural ene- resentative sample of parasitoids that emerged from mies was collected and taken to the laboratory for eggs were kept for later identiÞcation. Rates of para- identiÞcation. Examples of insects collected during sitism were determined from the portion of eggs this study are maintained as voucher specimens at the brought back that were not destroyed by predators. Rutgers Agricultural Research and Extension Center, The total impact of natural enemies (parasitized and Bridgeton, NJ. consumed eggs) was based on the total number of Parasitism and Predation of Sentinel G. molesta sentinel eggs placed in each orchard. Eggs. Laboratory reared G. molesta eggs (Ϸ16 h old) Data Analysis. BeneÞcial fauna counts were log- laid on wax paper were used to monitor resident egg transformed to meet assumptions of normality and parasitoid and predator populations. We used G. mo- were then analyzed with PROC GLM (SAS Institute lesta sentinel eggs, age up to 16 h, because T. minutum 1991). The model analyzed the effect of pest manage- prefers to parasitize earlier stages of host egg devel- ment programs, site, year, tree, and variation between opment (Houseweart et al. 1982, Yu et al. 1984a). Wax sample dates and years within treatments using re- paper pieces (Ϸ1 by 2.5 cm) containing G. molesta peated measures. Sentinel egg data were arcsine trans- eggs were glued onto the bottom of randomly selected formed then analyzed using PROC GLM (SAS Insti- peach leaves at the tip of shoots using nontoxic glue tute 1991). The model analyzed the effect of pest (ElmerÕs Products, Columbus, OH). All eggs on each management programs, site, height of egg placement, piece of wax paper were counted before placement in height of egg placement within treatments, year, tree, the Þeld. Average Ϯ SE number of G. molesta eggs per and variation between sample dates and years within wax paper piece was 5.4 Ϯ 0.5 in 1999 (total 5,491 eggs) treatments using repeated measures. and 6.6 Ϯ 0.2 in 2000 (total 10,007 eggs). Three wax paper pieces per height were placed at three heights Results in the peach canopy (low: 74.6 Ϯ 1.5 cm; middle: 167.1 Ϯ 2.0 cm; and high level: 268.0 Ϯ 3.0 cm). This Field Observation of Beneficial Arthropods. The procedure was repeated on each sample date for a following beneÞcial insects were observed on peach total of nine wax paper pieces per tree on three trees trees in 1999 and 2000: Chrysopid adults, eggs, larvae, per orchard. Sample trees were at least 50 m apart and and pupae, Coccinellid adults, Anthocorid adults and were considered independent of each other. This was nymphs, various Hymenopteran parasitoids, and spi- replicated Þve times in 1999 and seven times in 2000. ders (Table 1). Species authenticity was conÞrmed by Direct observation (Luck et al. 1988) of the sentinel laboratory identiÞcations of sampled individuals as eggs for predation events was conducted 2 d later, at Chrysoperla rufilabris (Burmeister) and C. plorabunda the time of wax paper removal from leaves. All the (Fitch) (Neuroptera: Chrysopidae), Coccinella sep- predators found feeding on the sentinel eggs were tempunctata L., Harmonia axyridis (Pallas), Hippo- collected and identiÞed. damia convergens (Guerin-Meneville), Adalia bipunc- After the wax paper pieces were detached from tata L., Coleomegilla maculata De Geer (Coleoptera: leaves, they were placed singly into clear plastic petri Coccinellidae), and Orius insidiosus (Say) (Heterop- dishes (50 by 9 mm, Falcon; Becton Dickinson Lab- tera: Anthocoridae). The parasitoids observed most ware, Franklin Lakes, NJ). Once in the laboratory, all frequently belonged to the following families: Bra- eggs were checked using a stereomicroscope for pred- conidae, Ichneumonidae, and superfamily Chal- ators, and if found, predators were immediately re- cidoidea. In addition, a few Cynipoidea and Proc- moved and identiÞed. Eggs were then counted and totrupoidea species were observed. classiÞed as either partially or completely consumed We observed signiÞcantly more Chrysopidae adults by predators or intact. Rates of predation were cal- (F ϭ 14.6; df ϭ 1, 1226; P ϭ 0.0001) and eggs (F ϭ 53.2; culated as the portion of all sentinel eggs placed in the df ϭ 1, 1226; P Ͻ 0.0001) in reduced risk orchards orchards. All intact eggs were then incubated at room compared with conventional orchards, but no differ- August 2003 ATANASSOV ET AL.: NATURAL ENEMIES OF THE ORIENTAL FRUIT MOTH 783 Downloaded from https://academic.oup.com/ee/article/32/4/780/357650 by guest on 24 September 2021

Fig. 2. Mean number of Chrysopidae eggs (left) and Chrysopidae adults (right) observed per 3-min sample per tree in 1999 and 2000. Error bars are SEM. ence in abundance of larvae (F ϭ 0.04; df ϭ 1, 1226; (F ϭ 39.58; df ϭ 1, 1226; P Ͻ 0.0001) for both years (F ϭ P ϭ 0.837; Table 1). Abundance of Chrysopidae adults 19.4; df ϭ 1, 1226; P Ͻ 0.0001; Table 1). Temporal was higher in 2000 than in 1999 (F ϭ 3.89; df ϭ 1, 1226; changes in abundance were no different between pest P ϭ 0.049; Table 1), and abundance varied between management programs (F ϭ 1.48; df ϭ 18, 1226; P ϭ sample dates within the treatments (F ϭ 3.4; df ϭ 18, 0.089; Fig. 3). 1226; P Ͻ 0.0001; Fig. 2). We observed more Chry- Parasitic Hymenoptera were observed throughout sopidae eggs in reduced risk orchards both years (F ϭ the season and were more abundant in reduced risk 16.78; df ϭ 1, 1226; P Ͻ 0.0001; Table 1), and these orchards than in conventional orchards (F ϭ 56.1; df ϭ levels varied signiÞcantly between sample dates (F ϭ 1, 1226; P Ͻ 0.001) for both years (F ϭ 20.43; df ϭ 1, 105.59; df ϭ 18, 1226; P Ͻ 0.0001; Fig. 2). 1226; P Ͻ 0.001; Table 1; Fig. 4). The abundance of We observed more Coccinellid adults in reduced parasitoids varied between sample dates (F ϭ 3.49; risk orchards (F ϭ 9.66; df ϭ 1, 1226; P ϭ 0.0019; Table df ϭ 18, 1226; P Ͻ 0.001; Fig. 4). 1; Fig. 3). Coccinellid adults were more abundant in More spiders were observed in reduced risk or- 2000 than in 1999 (F ϭ 21.28; df ϭ 1, 1226; P Ͻ 0.0001; chards than in conventional orchards (F ϭ 17.88; Table 1). df ϭ 1, 1226; P Ͻ 0.001), and whereas levels varied Anthocorids were signiÞcantly more abundant in between sample dates within treatments (F ϭ 5.61; reduced risk orchards than in conventional orchards df ϭ 18, 1226; P Ͻ 0.001), abundance did not vary

Fig. 3. Mean number of Coccinellidae adults (left) and Anthocoridae adults and nymphs (right) observed per 3-min sample per tree in 1999 and 2000. Error bars are SEM. 784 ENVIRONMENTAL ENTOMOLOGY Vol. 32, no. 4 Downloaded from https://academic.oup.com/ee/article/32/4/780/357650 by guest on 24 September 2021

Fig. 4. Mean number of Hymenoptera adults (left) and spiders (right) observed per 3-min sample per tree in 1999 and 2000. Error bars are SEM. between years (F ϭ 0.03; df ϭ 1, 1226; P ϭ 0.87; Table orchards. Frequently, sentinel eggs were completely 1; Fig. 4). or partially eaten by chrysopid larvae. Rarely we ob- Parasitism and Predation of Sentinel G. molesta served partially eaten eggs that have been parasitized. Eggs. Parasitoids reared from G. molesta sentinel eggs The number of G. molesta sentinel eggs consumed by were identiÞed as T. minutum and T. exiguum. T. minu- predators was signiÞcantly higher in reduced risk or- tum was the major parasitoid recovered. Higher levels chards compared with amounts consumed in conven- of parasitism were observed in reduced risk orchards tional orchards (F ϭ 11.19; df ϭ 1, 819; P ϭ 0.0009) for compared with levels in conventional orchards (F ϭ both years (F ϭ 5.84; df ϭ 2, 819; P ϭ 0.003; Table 2). 9.16; df ϭ 1, 819; P ϭ 0.0026), and parasitism levels We also observed that predation varied between sam- were signiÞcantly higher in reduced risk orchards for ple dates within a treatment (F ϭ 2.26; df ϭ 12, 819; P Ͻ both years of the study (F ϭ 16.26; df ϭ 2, 819; P Ͻ 0.008; Fig. 6). The highest rate of predation in reduced 0.0001; Table 2). We also observed that parasitism risk orchards occurred in July of both years, whereas, varied between sample dates within a treatment (F ϭ in conventional orchards, predation was highest in 2.26; df ϭ 12, 819; P ϭ 0.0082; Fig. 5). In 1999, para- July 1999 and August 2000. sitized sentinel eggs were collected on all sample dates The total impact of natural enemies on G. molesta in both program orchards. In 2000, sentinel eggs were sentinel eggs followed the same pattern as the para- parasitized throughout the season in reduced risk or- sitoid and predator data above. SigniÞcantly more eggs chards, whereas parasitism only occurred during the were destroyed in reduced risk orchards compared second half of the season in conventional orchards. with conventional orchards (F ϭ 22.69; df ϭ 1, 819; P Ͻ For both years, reduced risk orchards had the highest 0.0001) for both years of the study (F ϭ 21.09; df ϭ 2, rate of parasitism during August, whereas, in conven- 819; P Ͻ 0.0001; Table 2). Total G. molesta egg de- tional orchards, the highest rates were not observed struction varied between sample dates within the until September. treatments (F ϭ 2.70; df ϭ 12, 819; P ϭ 0.0014; Fig. 7). Chrysopid larvae and O. insidiosus nymphs and Temporal changes in the total impact of natural ene- adults were identiÞed to prey on G. molesta sentinel mies on G. molesta sentinel eggs (Fig. 7) and those eggs in both reduced risk and conventional peach representing consumed G. molesta sentinel eggs (Fig. 6) appeared similar in the two arthropod management Table 2. G. molesta sentinel eggs destroyed by natural enemies programs for both years. However, these temporal in 1999-2000 changes were quite different from those showing the rate of parasitized G. molesta sentinel eggs through the Average percent Ϯ SE of sentinel G. sample periods (Fig. 5). Year Treatment molesta eggs affected by natural enemies Within treatments, peach canopy height had a sig- Parasitism Predation Total destroyed niÞcant impact on the parasitism rate (F ϭ 3.49; df ϭ 1999 Reduced risk 15.8 Ϯ 2.5a 33.3 Ϯ 2.7a 45.9 Ϯ 2.8a 2, 819; P ϭ 0.031) but no effect on G. molesta sentinel Conventional 11.1 Ϯ 2.3b 20.9 Ϯ 2.2b 30.1 Ϯ 2.9b eggs consumption (F ϭ 1. 3; df ϭ 2, 819; P ϭ 0.881) or Ϯ Ϯ Ϯ 2000 Reduced risk 8.6 1.6a 19.2 1.8a 25.9 2.1a total egg destruction (F ϭ 2.21; df ϭ 2, 819; P ϭ 0.11; Conventional 2.2 Ϯ 0.8b 15.5 Ϯ 1.5b 17.1 Ϯ 1.6b Table 3). Combining the G. molesta sentinel egg data Within each column for each year, different letters indicate sig- for both reduced risk and conventional orchards by niÞcant differences between means (P Ͻ 0.05). canopy height resulted in no signiÞcant differences in August 2003 ATANASSOV ET AL.: NATURAL ENEMIES OF THE ORIENTAL FRUIT MOTH 785 Downloaded from https://academic.oup.com/ee/article/32/4/780/357650 by guest on 24 September 2021

Fig. 5. Levels of parasitism of G. molesta sentinel eggs when placed in orchards on various dates during 1999 and 2000. Error bars are SEM. the rate of parasitism between any of the explored Discussion heights (F ϭ 1.1; df ϭ 2, 819; P ϭ 0.333; Table 3). However, we observed signiÞcant differences be- We demonstrated that our reduced risk peach ar- tween lowest and highest egg placement levels on thropod management program (Atanassov et al. 2002) both consumed (F ϭ 2.95; df ϭ 2, 819; P ϭ 0.05) and was conducive to arthropod natural enemies. Natural total destroyed eggs (F ϭ 3.58; df ϭ 2, 819; P ϭ 0.028; enemies in reduced risk orchards were more abundant Table 3). and had greater impact on G. molesta eggs compared

Fig. 6. Levels of predation of G. molesta sentinel eggs when placed in orchards on various dates during 1999 and 2000. Error bars are SEM. 786 ENVIRONMENTAL ENTOMOLOGY Vol. 32, no. 4 Downloaded from https://academic.oup.com/ee/article/32/4/780/357650 by guest on 24 September 2021

Fig. 7. Total impact of egg parasitoids and predators on G. molesta sentinel eggs placed in orchards on various dates during 1999 and 2000. Error bars are SEM. with levels of abundance and activity observed in phorus and carbamate insecticide applications have adjacent conventionally managed orchards. We at- ceased. tribute these observations to the decreased frequency Trichogramma minutum, the predominant egg para- of organophosphorus and carbamate insecticide ap- sitoid reared from our sentinel G. molesta eggs, is plications in reduced risk orchards. This conserved the considered an arboreal species (Pinto et al. 2002). Yu resident natural enemy populations in higher numbers et al. (1984b) reported uniform vertical dispersion of than what was observed in orchards sprayed on a T. minutum when released within apple trees yet par- season-long basis. Our Þndings support others who asitism was greater in the lower canopy of adjacent reported higher levels of beneÞcial arthropod abun- apple trees. However, Dolphin et al. (1972) observed dance in orchards with minimal or no insecticide ap- that Þeld released T. minutum parasitized up to 80% of plications when compared with orchards under full the C. pomonella sentinel eggs placed 174 cm above insecticide spray programs (Wisniewska and Prokopy ground in apple trees, whereas no parasitism occurred 1997, Kinkorova´ and Kocourek 2000, Miliczky et al. to eggs stapled to the ground. In our study, the dif- 2000). Fewer insecticide applications in reduced risk ferences in sentinel G. molesta egg parasitism that peach orchards also beneÞt mobile natural enemies occurred at different peach canopy heights within because insecticide use is limited to early season crop treatments could be a result of one or more factors. growth and pest infestation. BeneÞcial insects that Ground cover and other agronomic practices that in- disperse into reduced risk orchards are more likely to ßuence microclimate conditions like humidity and survive, especially after mid-May, when organophos- temperature can result in differences in parasitoid

Table 3. G. molesta sentinel eggs destroyed by natural enemies at three different heights of peach canopy

Average percent Ϯ SE of sentinel G. molesta eggs affected by natural Height above Program enemies ground level Parasitism Predation Total destroyed High (268.0 cm) Reduced risk 7.8 Ϯ 2.0 20.9 Ϯ 2.5 26.9 Ϯ 2.8 Conventional 8.7 Ϯ 2.4 15.0 Ϯ 2.2 21.9 Ϯ 2.8 Overall 6.5 Ϯ 3.8a 17.9 Ϯ 4.9b 24.4 Ϯ 5.9b Middle (161.1 cm) Reduced risk 10.9 Ϯ 2.3 25.7 Ϯ 2.6 34.5 Ϯ 2.9 Conventional 3.6 Ϯ 1.5 18.6 Ϯ 2.4 21.9 Ϯ 2.6 Overall 6.1 Ϯ 3.5a 22.2 Ϯ 5.3ab 28.2 Ϯ 5.9ab Low (74.6 cm) Reduced risk 15.7 Ϯ 2.7 28.1 Ϯ 2.9 40.6 Ϯ 3.2 Conventional 4.8 Ϯ 1.4 19.4 Ϯ 2.5 23.2 Ϯ 2.6 Overall 8.1 Ϯ 3.9a 23.8 Ϯ 5.7a 31.9 Ϯ 6.3a

Within each column different letters indicate signiÞcant differences between means (P Ͻ 0.05). August 2003 ATANASSOV ET AL.: NATURAL ENEMIES OF THE ORIENTAL FRUIT MOTH 787 habit selection and efÞciency (Orr et al. 1997). Like- tional studies are required to evaluate the overall im- wise, abiotic factors such as solar radiation, tempera- portance of natural enemy impact on fruit injury. ture, wind (Fournier and Boivin 2000), rain, and low temperature (Yu et al. 1984b) can signiÞcantly affect some species of Trichogramma but not others. For Acknowledgments instance, rain did not seem to trap T. minutum when We thank F. de Lame (Michigan State University), G. sheltered on the undersurface of leaves (Allen 1962), Wigman, A. Guinta, J. A. Davis, and K. Foster (Rutgers nor did wind reduce the overall rate of parasitism University), who provided substantial technical assistance. within apple canopies (Yu et al. 1984b). We also thank J. Pinto (University of California, Riverside), The difference in parasitism rates between pest who identiÞed T. minutum and T. exiguum, and J. Oswald control programs and canopy height in our study was (Texas A&M University) for C. rufilabris and C. plorabunda more likely caused by irregular pesticide spray distri- identiÞcation. The USDA Pest Management and Alternatives Program provided funding (Award 98-34381Ð6855) for this

butions within the peach canopy. In this instance, Downloaded from https://academic.oup.com/ee/article/32/4/780/357650 by guest on 24 September 2021 air-blast sprayers frequently deposit greater amounts study. This paper is publication number D08-08184-05-03 of the New Jersey Agricultural Experiment Station. of insecticide residues to the mid and low parts of the canopy. This most likely occurred in conventional orchards where the lowest rate of parasitism was de- References Cited tected. Similarly, Yu et al. (1984a) showed that insec- ticide residues on apple leaves signiÞcantly lowered Allen, H. W. 1962. Parasites of the oriental fruit moth in the rates of T. minutum parasitism on C. pomonella eggs. Eastern United States. Technical Bulletin No. 1265: 1Ð139, Contrary to the relatively low egg parasitism rates, ARS, U.S. Dep. Agric., Washington, DC. Al Rouechdi, K., and J. Voegele. 1981. Pre´dation des tri- fairly high egg predation rates occurred in reduced chogrammes par les chrysopides. Agronomie. 1: 187Ð189. risk and conventional orchards with respect to canopy Atanassov, A., P. W. Shearer, G. Hamilton, and D. Polk. 2002. height. We frequently observed Chrysopidae larvae Development and implementation of a reduced risk feeding on G. molesta eggs as did Briand (1931), and peach arthropod management program in New Jersey. J. we attribute the high levels of predation in our study Econ. Entomol. 95: 803Ð812. to insecticide tolerance of Chrysopidae larvae (Lin- Bai, B. B., and S. M. Smith. 1994. Patterns of host exploita- gren and Ridgway 1967, Shour and Crowder 1980, Pree tion by the parasitoid wasp Trichogramma minutum (Hy- et al. 1989). menoptera: Trichogrammatidae) when attacking eggs of We rarely observed partially consumed parasitized the spruce budworm (Lepidoptera: Tortricidae) in Ca- nadian forests. Ann. Entomol. Soc. Am. 87: 546Ð553. G. molesta eggs. 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