Control of by naturally occurring predators

M. A. Schmaedick1, A. M. Shelton1, and M. P. Hoffmann2 1Department of Entomology, New York State Agricultural Experiment Station, Cornell University, Geneva, NY 14456, U.S.A. 2Department of Entomology, Cornell University, Ithaca, NY 14853, U.S.A.

Abstract In recent years, pesticide resistance in some lepidopteran , along with a general desire to reduce dependence on chemical pesticides, have led to increased interest in evaluating and enhancing the effects of naturally occurring biological control agents on the crucifer Lepidoptera. Due to the relative ease of documenting the impact of parasitoids on pest populations, however, virtually all the research on natural enemies have focused on parasitoids, while the role of predators has remained largely unexplored. Our work evaluating the effects of predatory on rapae in cabbage shows that generalist predators are responsible for much of the mortality of this pest in our area. We describe predator exclusion experiments and laboratory predation assays that demonstrate the important role of these natural enemies in reducing populations of P. rapae. As generalist feeders, these predators undoubtedly affect populations of other crucifer Lepidoptera as well and have the potential to survive in the crop at low pest densities by feeding on alternative prey. These attributes, along with their propensity to destroy the early stages of pests, make these predators potential key players in efforts to increase reliance on non chemical methods for managing crucifer Lepidoptera.

Key words: Pieris rapae, predation, cabbage

Introduction Materials and Methods Occurrence of insecticide resistance in populations of Estimation of mortality from arthropod predation lepidopteran pests of cabbage, along with a desire to Mortality of P. rapae and larvae due to arthropod reduce use of broad spectrum insecticides, have led to predators in cabbage fields was estimated by increased interest in ecologically based management comparing survivorship on protected and exposed strategies. Improved understanding of the natural plants infested with known numbers of P. rapae eggs. mortality factors affecting populations of Lepidoptera The experiment was conducted in two 0.2 ha cabbage in cabbage is critical to development of such strategies. fields planted with “Vantage Point” seedlings on 2–5 While numerous studies have addressed the role of June 1995. An additional 120 seedlings were planted parasitoids in controlling crucifer Lepidoptera, into 30.5 cm diam. plastic pots and placed in an much less is known about the effects of predators outdoor screenhouse. The seedlings were entirely (Jones, 1981; Talekar and Shelton, 1993). Pieris rapae enclosed by no-see-um mesh bags (Balson-Hercules L.(Lepidoptera: ) is one of the most important Group, Ltd., Providence, RI, U.S.A.). The mesh bags pests of crucifer vegetables (e.g., cabbage, , lined the pots and were supported above the plant by cauliflower) in New York State and many other 46 cm high (2.5 cm mesh) wire net cylinders resting crucifer growing areas worldwide. We describe initial on the soil surface in the pots and anchored by two results of our efforts to estimate the overall mortality short bamboo stakes. The bags were tied at the top to of P. rapae eggs and larvae due to arthropod predation exclude arthropods yet allow access for sampling. and to determine the predator species causing the On 11 July the potted plants were placed in an mortality. Overall mortality was estimated by enclosed screenhouse, the bags opened, and adult P. comparing P. rapae survivorship on plants from which rapae from a laboratory culture released and allowed predators were excluded to that on plants to which to oviposit for 24 h. Sixty of the plants were then arthropod predators were allowed access. Species placed in each of the two cabbage fields, replacing preying on P. rapae were determined by use of sticky every fifteenth plant in every third row, forming a 30.5 traps to ascertain predator species that occur on x 24.7 m grid in the plot center. The pots were cabbage plants followed by laboratory predation assays embedded to just below the soil surface in the plots. to learn which of these species feed on P. rapae early On each plant the locations of five well-spaced eggs stages. on the leaf undersides were marked by drawing a circle on the leaf’s upper surface with a permanent marker. Any additional eggs were removed. Plants at alternate points of the grid were designated as sham cage plants. On 14 July the lower 15 cm of the above-ground

308 Proceedings: The Management of Diamondback and Other Crucifer Pests portion of the mesh bags on these plants was cut away cm length of dental wick. The arenas containing and the upper portion left in place and fastened to the predators were placed in an environmental chamber wire netting cylinder using straight pins. The pot rims at 22:17 (L:D) °C, 60% RH, and 15:9 (L:D) h and and soil inside the pots were then covered with field starved for 24 h before adding either 10 or 20 P. rapae soil to form a continuous surface with the surrounding eggs or five first instars. Eggs and first instars were soil. P. rapae on the plants were counted and any newly used because the exclusion cage experiments indicated oviposited eggs or colonizing aphids were removed that virtually all predation occurred during these stages. on 16, 22, and 26 July. By 26 July most larvae had The eggs were presented on pieces of parafilm cut from reached fifth instar. sheets used for oviposition in our P. rapae The plants and P. rapae were removed from the laboratory culture. The larvae were transferred shortly pots on 26 July and replaced later with new plants after hatching from egg sheets to 3.2 cm cabbage leaf (variety “Bravo”) in 10 cm diam. pots bearing five P. disks which were then placed with the predators. After rapae eggs per plant. The five eggs /plantwere obtained an additional 24 h in the environmental chamber, by placing the plants in our lab culture’s oviposition remaining eggs and larvae were counted. A minimum cage for a few minutes apiece until >5 eggs were laid of five control arenas identical to the test arenas except then removing the excess eggs. The smaller pots were without predators were included with each batch of embedded in the soil inside the larger pots that were predators tested. No eggs or larvae were damaged or already in the field such that the soil in the pots formed disappeared in any of the control arenas. a continuous surface. The second set of plants was placed in one of the fields on 2 Aug. and in the other Predation on cabbage plants in the laboratory on 8 Aug. P. rapae were counted and any new P. rapae Three of the four most abundant predator species eggs or aphids were removed from the plants every captured on sticky traps were further tested for 2Ð3 d until most of the larvae had reached the fifth predation ability on cabbage plants in the laboratory. instar. For each of the four experiments survivorship Predators were collected by hand or by dry pitfall traps curves for the two treatments were compared visually and starved for 24 h as in the small arena assays. to determine stages at which most mortality occurred. Groups of predators were then placed in plastic In addition, 95% confidence intervals for total cylinder cages with screen tops covering small (4Ð6 mortality due to treatment effect were constructed leaf) cabbage plants that had been transplanted into using Elston’s (1969) method as described by 25 cm diam. plastic pots and infested with ten first Rosenheim and Hoy (1989). instar P. rapae. A moist 2.5 cm length of dental wick was placed on the surface in each pot. Three control Monitoring predators on cabbage plants with P. rapae but no predators were included in Cabbage (variety ‘Cheers’) was transplanted into 0.2 each trial. After 24 h at 22 °C, 40% RH, and 16:8 (L:D) ha plots at three locations ≥1 km apart on 22Ð26 May h, remaining P. rapae larvae were counted. No larvae 1995. Sticky traps were placed on 36 plants in a 6 x 6 disappeared from any of the control plants in the three grid in the center of each plot on 10 July when most experiments. of the plants were in precupping stage (13Ð19 leaves). The outermost trap plants were ≥6.4 m from the plot Results edges. The traps consisted of two 8.6 cm rings of insect Estimation of mortality from arthropod predation trap coating (Tanglefoot Co., Grand Rapids, MI, The survivorship curves for the four experiments U.S.A.) pressed onto the upper and lower surfaces showed a reduction in survival of the larvae on plants respectively of two opposite frame leaves of each trap in the sham cages versus those in the predator plant. A plastic “deli container” (32T, Fabri-Kal Corp., exclusion cages. In all cases almost all of the difference Kalamazoo, MI, U.S.A.) with a hole cut out of the arose during the egg or first instar. The bulk of the bottom was used to apply the trap coating to the leaf mortality (52Ð84%) was common to both cage types, surfaces. The traps were checked every 3Ð4 d and all apparently arising from factors that acted equally on predaceous arthropods removed and preserved for P. rapae in both treatments. The 95% confidence identification. Each week the coated leaves were intervals for total mortality attributable to the treatment removed and new trap coating applied to leaves of the were 58 ± 22% and 51 ± 21% for the two fields in the same or nearby plants. Trapping continued until 14 July experiments and 79 ± 19% and 71 ± 20% for the August when the plants were close to maturity. same fields in the August experiments.

Predation in small arenas Monitoring predators on cabbage Species of arthropod predators that were most The most abundant predatory arthropods identified on abundant in the sticky traps were collected from the traps were Lygus sp. (Hemiptera: Miridae) (almost cabbage fields and surrounding weedy areas both all Lygus lineolaris Palisot de Beauvois) (305 manually and by use of dry pitfall traps. Predators were captured), Stenolophus comma F. (Coleoptera: placed individually into white plastic 7.6 cm high 11.8 Carabidae) (126), Coleomegilla maculata lengi cm diam. arenas with clear plastic lids (Fabri-Kal Timberlake (Coleoptera: Coccinellidae) (125), and Corp., Kalamazoo, MI, U.S.A.). The containers were Phalangium opilio (L.) (Opiliones: Phalangiidae) (56). lined with filter paper and provided with a moist 2.5 Predators that were caught less frequently included

Poster Papers 309 other Coccinellidae (44), Syrphidae (adults) (33), other were occasionally seen in the plots, they were excluded Carabidae (27), Anthicidae (21), Araneae (9), Vespidae from all the experimental plants by the wire netting (8), Sphecidae (4), Nabidae (3), Chrysopidae (2), and cloth covers, so could not have been responsible Pompilidae (2), and Cleridae (2). for the observed differences. Other studies that have evaluated the impact of Predation in small arenas predators explicitly have concluded that arthropod As shown in Tables 1 and 2, all the predator species predators caused the bulk of mortality in immature P. fed on P. rapae to some extent. Because number of rapae (Dempster, 1967; Parker, 1970; Ashby, 1974; prey per predator was limited in the experiment, it is Hasui, 1977; Jones, 1987). While predation was difficult to evaluate relative voracity of those species significant in our study, mortality attributable to that tended to consume most of the prey provided. predators excluded by our cages was much less than However, the proportion of individuals that fed on at mortality resulting from factors that were not excluded. least one prey can be used to compare the propensity These factors could not be identified, but may include of the different species to feed on P. rapae. weather effects or small predators such as thrips or mites that could penetrate the cage cloth. Predators Predation on cabbage plants in the laboratory that were excluded by the cages caused high levels of Both C. m. lengi and P. opilio fed on P. rapae first mortality to the remaining P. rapae in the sham cages. instars on cabbage plants (Table 3), however many Our sticky traps and laboratory predation larvae escaped predation in spite of the high number experiments identified two species that are probably of predators per plant. L. lineolaris did not prey on P. at least partly responsible for the mortality observed rapae larvae on the plants. in the exclusion experiments: C. m. lengi and P. opilio. L. lineolaris appears less likely to prey on P. rapae in Discussion the field, and although S. comma was relatively The confidence intervals for mortality of P. rapae in abundant in the sticky traps and fed readily on P. rapae the predator exclusion experiments, though large, eggs and first instars, its ability to forage on cabbage provide convincing evidence of a high level of plants must still be evaluated. Currently we are arthropod predation in the field. Because P. rapae attempting to quantify the contribution of each species larvae rarely leave suitable host plants (Harcourt, 1961; to prey mortality by estimating relative densities and Jones, 1977), the treatment effects are not likely a result predation frequencies in the field. of dispersal from the sham cage plants. Although birds

Table 1. Consumption of P. rapae eggs by individual predators in small arenas

Species No. prey Mean prey SD Percent No. provided consumed consuming tested ≥ 1 prey Coleomegilla maculata lengi 10 6.0 4.9 65 20 Stenolophus comma 20 17.0 7.3 85 20 Phalangium opilio adults 20 12.6 8.1 84 43 Phalangium opilio 10 5.6 4.4 80 20 immatures Lygus lineolaris 10 3.3 4.6 40 20

Table 2. Consumption of P. rapae first instars by individual predators in small arenas

Species No. prey Mean prey SD Percent No. provided consumed consuming tested ≥ 1 prey Coleomegilla maculata lengi 5 4.3 1.5 96 23 Stenolophus comma 5 4.1 1.7 88 25 Phalangium opilio adults 5 2.9 1.8 88 49 Phalangium opilio 5 4.1 1.6 95 21 immatures Lygus lineolaris 5 0.6 1.0 43 23

Table 3. Consumption of P. rapae first instars on potted cabbage plants by groups of predators (10 P. rapae placed on each plant initially)

Species Predators Mean prey SD N per plant consumed Coleomegilla maculata lengi 6 5.70 3.37 10 Phalangium opilio adults 4 2.00 2.00 6 Lygus lineolaris 60 010

310 Proceedings: The Management of Diamondback Moth and Other Crucifer Pests While the sticky traps indicate occurrence of References predatory arthropods on the cabbage leaves, a species’ Ashby, J. W. (1974). A study of arthropod predation of Pieris occurrence in trap catches does not necessarily imply rapae L. using serological and exclusion techniques. that it was foraging on the foliage. Many individuals Journal of Applied Ecology 11: 419Ð425. may become entrapped only after inadvertently Dempster, J. P. (1967). The control of Pieris rapae with DDT. I. The natural mortality of the young stages of Pieris. alighting on the sticky surface. Conversely, a species’ Journal of Applied Ecology 4: 485Ð500. absence in the trap catch does not necessarily imply Ehler, L .E. (1977). Natural enemies of cabbage looper on that it does not occur on cabbage foliage. Because cotton in the San Joaquin Valley. Hilgardia 45: 73Ð106. species differ in their susceptibility to sticky traps, their Harcourt, D.G. (1966). Major factors in survival of the relative abundances in trap catches may not correspond immature stages of Pieris rapae (L.). Canadian to their relative abundances on the foliage. Under our Entomologist 98: 653Ð662. laboratory conditions all species except L. lineolaris Hasui, H. (1977). On the seasonal variability of survivorship showed a high propensity to feed on eggs and first curves and life tables of Pieris rapae crucivora instars. Actual impact of a species in the field, however, Boisduval (Lepidoptera: Pieridae) Japanese Journal of Ecology 27: 75Ð82. will depend on many factors, including predator and Jones, R. E. (1977). Search behaviour: a study of three prey abundance, searching ability on plants, alternative caterpillar species. Behaviour 60: 237Ð259. prey, and numerical and functional responses to prey Jones, R. E. (1981). The cabbage , Pieris rapae (L.): density. Much additional work is necessary to evaluate ‘A just sense of how not to fly’. In The Ecology of Pests: the relative contribution of each of the predator species Some Australian Case Histories (ed. R. L. Kitching and to mortality of P. rapae in cabbage fields. R. E. Jones) pp. 217Ð228. Melbourne: CSIRO. Although more work is needed, our initial results Jones, R. E. (1987). Ants, parasitoids, and the cabbage suggest that arthropod predators can contribute a great butterfly Pieris rapae. Journal of Ecology 56: deal to reduction of P. rapae in the field. Because these 739Ð749. Murdoch, W. W. (1985). Biological control in theory and predators are often generalists, they most likely practice. The American Naturalist 125: 344Ð366. contribute to reduction of other crucifer Lepidoptera Parker, F. D. (1970). Seasonal mortality and survival of Pieris as well and have the potential to persist in the field at rapae (L.) (Lepidoptera: Pieridae) in Missouri and the low pest densities by subsisting on alternative prey effect of introducing an egg parasite, Trichogramma (Ehler, 1977; Reichert and Lockley, 1984; Murdoch evanescens Westwood. Annals of the Entomological et al., 1985). In addition, unlike many parasitoids, these Society of America 63: 985Ð999. predators act primarily on the early stages of the pest, Riechert, S. E. and Lockley, T. (1984). Spiders as biological killing it before it reaches the most damaging late larval control agents. Annual Review of Entomology 29: 299Ð instars. These desirable qualities, along with evidence 320. Talekar, N. S. and Shelton, A. M. (1993). Biology, ecology, of their importance from this and other studies, justify and management of the diamondback moth. Annual continued efforts to elucidate the effects of arthropod Review of Entomology 38: 275Ð301. predators on P. rapae and other cabbage Lepidoptera.

Acknowledgments The authors thank Rick Piccioni, Mary Balsley, Bill Wilsey, and Juliet Tang for technical assistance. This work was supported in part by the New York State Integrated Pest Management Program.

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