Submitted to: : Advances in Horticultural Science Send correspondence to Joseph M. Patt - Department of Entomology - Rutgers University - New Brunswick, NJ- 08903 - USA
Joseph M. Patt, George C. Hamilton and James H. Lashomb
Department of Entomology Rutgers University New Brunswick, NJ 08903, USA
Key words: conservation biological control, strip-insectary intercropping, anthophily, floral architecture, insect predators, dill, Anethum graveolens, coriander, Coriandrum sativa, Leptinotarsa decimlineata, Coleomegilla maculata, Coccinella septempunctata, Hippodamia variegata, Chrysoperla carnea
Predators of Colorado potato beetle (Leptinotarsa decimlineata (CPB)) are an important component of CPB suppression by biological control in New Jersey (USA) eggplant fields. Here we report the results of a preliminary study on the effects of strip-insectary intercropping with flowers on predator abundance and CPB suppression in experimental eggplant fields. Strip-insectary intercropping with flowers is known to increase beneficial insect survivorship, fecundity and retention and crop pest suppression in agroecosystems. However, little is known about the compatibility of predator foraging ability with floral architecture; i.e., the spatial relationship of the nectary with other floral parts. This a critical factor in the selection of 'proper' floral host plants; i.e., those having pollen and nectar that is accessible to predators. Laboratory evaluations and field observations of the foraging performance of Coleomegilla maculata and Chrysoperla carnea on flowers with disparate floral architectures indicated that dill (Anethum graveolens) and coriander (Coriandrum sativa) had floral architectures that were complimentary to the head morphology and foraging behavior of these representative CPB predators. To measure the effect of strip-insectary intercropping with "proper" flowers on CPB suppression, the fate of 100 eggmasses and resultant larvae placed on individual sentinel eggplant plants was followed during two 9-day periods in 100 m x 40 m eggplant fields intercropped with two rows of either dill or coriander and in a flowerless control field. In addition, coccinellid species richness and abundance was censused weekly in each test field from early July to mid-August. Throughout this study, the number of coccinellids observed during each census were significantly higher in the fields interplanted with dill and coriander than in the flowerless control field. Although there were no differences among treatments in the number of hatched CPB eggmasses, significantly more CPB eggmasses were consumed in the dill-intercropped fields than in the control field. Survivorship of CPB larvae at the end of each survey was highest in the control field and lowest in the dill field. These results suggest that strip-intercropping with "proper" flowers can greatly enhance CPB predator conservation and augmentation in vegetable cropping systems.
Flowers promote biological control--Nutritional provisioning may be required for biological control programs to succeed because critical nutrients needed by predators & parasitoids are often scarce in large monocultures (Wolcott 1942, Clausen 1956). Since many predators are also anthophilous ( = "flower visiting") (Hagen 1962, Hodek 1967, Proctor & Yeo 1972, Jervis & Kidd 1996), their establishment and performance is improved when flowering herbaceous plants are placed within cropping systems (Zandstra & Mootka 1978, Altieri & Whitcomb 1979, Andow 1983, Altieri & Letourneau 1982, Bugg & Wilson 1989, van Emden 1989, Kloen & Altieri 1990, Maingay et al. 1991, King & Olkowski 1991, Grossman & Quarles 1993, Cowgill, Wratten, & Sotherton 1993, White et al. 1995, Jervis & Kidd 1996). Flowers provide a concentrated reservoir of resources and can improve predator efficacy through the combined effects of increased survivorship, fecundity, retention and immigration (Altieri & Whitcomb 1979, Altieri & Letourneau 1982, Jervis & Kidd 1996). While providing nutrients (pollen and nectar) which support metabolism and gamete development, flowers also provide mating sites, alternate hosts and shelter (Altieri & Whitcomb 1979, Altieri & Letourneau 1982, Andow 1983, van Emden 1989, Jervis & Kidd 1996). Because these resources are available, predator emigration from cropping systems with flowers may be minimized, while floral color and scent may attract these insects from a distance and promote immigration from areas lacking floral resources (Haslett 1989). The placement of flowering herbaceous plants into vegetable cropping systems, a method that has been referred to as "strip-insectary intercropping" or "strip-nursery intercropping", can be an important tool for the enhancing predator conservation and augmentation. (Grossman and Quarles 1993). Because flowers provide a concentrated source of nutrients and other resources, intercropped floral host plants need only take up a small proportion of the total acreage in a field to be effective. For example, an intercropping program that utilizes alyssum (Lobularia maritima L.) to promote the survivorship and fecundity of Diaretiella raphae (McIntosh), a parasitoid of the green peach aphid (Myzus persicae Sulzer), in California lettuce fields required that only one in twenty rows is planted in alyssum to be effective (W. Chaney, California Department of Agriculture, personal communication; Grossman & Quarles 1993). The loss of land productivity at this proportion of lettuce to alyssum has been shown to be cost effective with traditional spray controls (W. Chaney, personal communication). Earlier approaches to the development of efficient biological control systems were attempts to determine the proper combination of plants necessary to provide resources such as pollen, nectar or alternate hosts in synchrony with the temporal progression of crop plants (Andow 1983). Andow (1983) points out, however, that "proper" was never clearly defined, and that the potential of these approaches has never been realized due to difficulties in predicting what types of plants were "proper" for given biological control agents. To provide nectar and pollen, "proper" floral host plants should have blooming phenologies that coincide with the seasonality of a given predator (Andow 1983, Cowgill, Wratten & Sotherton 1993). Just as important, these plants should have floral architectures (i.e., the spatial arrangement of floral parts in relation to the nectary) that are compatible with the predator's head and mouthparts morphology and floral foraging abilities because a particular predator species' behavioral and physical ability to manipulate floral parts to obtain nectar or pollen may limit its foraging range to only certain types of flowers (Proctor & Yeo 1972, Feagri & van der Pijl 1973, Gilbert 1981, Haslett 1989, Jervis & Kidd 1996). Unfortunately, the floral foraging behavior of few anthophilous predators have been studied in detail and frequently little or no information is available on either a predator species' floral foraging ecology or floral preferences in its natural range (Gilbert 1981, Haslett 1989, Jervis & Kidd 1996).
Therefore, information on a predator's floral foraging ability and morphological compatibility with certain kinds of floral architectures can be a critical requisite for selecting "proper" floral hosts for that particular predator. Due to the lack of detailed studies, however, there is no way to predict or know a priori if the morphology and foraging capabilities of many species of anthophilous predators are compatible with certain types of floral architectures. To remedy this situation, we are conducting ongoing studies aimed at comparing the morphology of anthophilous predators with floral architecture and evaluating their foraging performance on a variety of flowers with disparate floral architectures in the lab. Here we report on the results of preliminary field trials designed to evaluate the effects of the most promising candidate floral hosts on predator abundance and diversity in experimental eggplant fields. Study System--Under an biological control intensive pest management program, developed by the New Jersey Department of Agriculture (NJDA) and Rutgers University, inoculation of a solitary egg parasitoid Edovum puttleri Grissell (Hymenoptera: Eulophidae) reduces the density of Colorado potato beetle Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae) (CPB) below economically damaging levels in commercial eggplant (Solanum melongena L.) fields (Lashomb et al. 1987, Lashomb 1989, Hamilton 1995). Curtailment of insecticide application permits establishment of E. puttleri as well as large numbers of indigenous predators which feed on CPB eggmasses and larvae (Mark Mayer, NJDA, personal communication; Lashomb and Hamilton, unpublished). These predators include several lady beetles such as Coleomegilla maculata Muls. (Coleoptera:Coccinellidae), Hippodamia variegata Goeze (Coleoptera:Coccinellidae), predatory stink bugs, Perillus bioculatus (F.) (Hemiptera: Pentatomidae) and Podisus maculaventris Say (Hemiptera:Pentatomidae), and common green lacewing, Chrysoperla carnea L. (Neuroptera:Chrysopidae). Taken together, they comprise an important component of this pest management program (Mark Mayer, NJDA (personal communication), Lashomb and Hamilton, unpublished), and have been implicated as important biological control agents of CPB elsewhere (Groden et al. 1990, Hazzard & Ferro 1991, Hazzard et al. 1991, Nordlund et al. 1991, Biever & Chauvin 1992, Hough-Goldstein & Whalen 1993).
The combined action of E. puttleri and these predators keeps CPB and other pest species below the economic injury threshold for the length of the growing season (Lashomb 1989). Eggplant growers participating in the program have reduced their number of insecticide applications from 12-17 to 0-4 per growing season (Mayer & Hudson 1993, Hamilton 1995). The program and is also cost-competitive with traditional spray methods (Hamilton 1995). However, constraints in E. puttleri rearing may limit the total acreage the program may reach. By increasing predator efficacy, the number of E. puttleri needed to suppress CPB on a per acre basis could be reduced and would permit the program to protect more acreage at current E. puttleri production levels. Because many of the key CPB predators in eggplant are either anthophilous or prey on alternate hosts found in inflorescences (J. M. Patt, personal observation), strip insectary interplanting with "proper" flowers may be the most effective means of increasing their abundance and species diversity in this cropping system.
Experimental field set-up: During July and August 1995, we compared suppression of CPB eggmasses and larvae with predator abundance in eggplant fields interplanted with either dill or coriander, two "proper" floral host plants (See Below), and a control field containing only eggplant. We predicted that predation of CPB eggmasses would be higher in the fields planted with "proper" floral hosts than in the flowerless control field. The test fields were established at the Rutgers University Horticulture Research Farm in North Brunswick, NJ (USA) and CPB eggmasses for experimental use were obtained from the NJDA Philip Alampi Beneficial Insect Laboratory in West Trenton, New Jersey. Eggplant (cv. Harris) was planted in rectangular test plots, measuring 40 m wide by 100 m long. Test plots were divided into 18 rows, ca. 2 m apart from each other, and contained eggplant planted at 1 m intervals, the same planting density used in commercial eggplant fields in New Jersey. All test fields were spaced at least 300 m apart from each other. Eggplant, grown from seed in the greenhouse, were transplanted into the test fields in late May when the plants had five-six leaves. No insecticides were applied to any of the test fields during the course of the study. Each test field had one of three treatments: 1) Interplanted with dill, "proper" floral host #1: Dill (cv. Bouquet) (Anethum graveolens L.) was tested as a "proper" floral host plant CPB predators because: 1) Behavioral observations in the field and the laboratory demonstrated that the adults and larvae of anthophilous predators such as Colemegilla maculata and Chryoserla carnea readily foraged for pollen and nectar from the dill flower's exposed stamens and nectaries (Patt, unpublished); 2) It flowers in ca. 45 days and its blooming period extends throughout the summer (Fig. 1a); Figure 1. Blooming phenology of: A) Dill; and, B) Coriander during the 1995 field season at the Rutgers Vegetable Research Farm in East Brunswick, NJ, USA.3) It thrives in full sun and well-drained soils, the same cultural conditions required by eggplant; and, 4) The fresh foliage and dried seeds can be marketed, providing growers with added incentive to intercrop. Two 100 m long strips of dill were planted inside the field, dividing the field into three equal subsections. The strips were divided into two rows spaced 50 cm apart with each row contained dill planted at 10 cm intervals. The dill seed was planted in early May at two 14-day intervals to ensure continuous bloom during the study period. 2) Intercropped with coriander, "proper" floral host #2: Coriander (Coriandrum sativa L.), also known as cilantro, was tested as an "proper" floral host because behavioral observations showed that adult C. maculata and C. carnea also readily accessed its nectar glands and because coriander is very similar to dill in cultivation requirements, number of days to flowering and blooming duration (Fig. 1b). Because we observed adult C. maculata and C. carnea foraging on coriander flowers in the lab, we expected to observe higher rates of predation on CPB eggmasses and larvae within the field interplanted with coriander than in the flowerless control field. The coriander was grown and handled the same as dill. 3) Control: The test field contained only eggplant, with bare ground maintained in the areas that would have been occupied as floral strips. Influence of interplanting with "proper" flowers on coccinellid species diversity and abundance in test plots: Because we observed both adult and larval predators foraging from dill and coriander flowers (see above), we expected to see an increase in the predator species diversity and abundance in the eggplant fields interplanted with these flowers. For the purpose of this preliminary study we chose to focus on adult coccinellids because these insects are easy to locate on eggplant foliage and are important predators of CPB eggmasses and larvae (Groden et al. 1990, Hazzard et al 1991, Hazzard & Ferro 1991). Coccinellid species diversity and abundance were measured by conducting morning (9:00-11:00 hr) and afternoon (13:00-15:00) censuses within each field at weekly intervals. During each census, every eggplant and flower row was visually inspected twice and all lady beetles observed were collected and held in ventilated plastic bottles until the census was completed, at which time they were released back into the field. During each census, care was taken to inspect both the upper and lower sides of the eggplant foliage. In all, six weekly censuses were conducted in each field from July 14 to August 15. The number of C. maculata, H. variegata and C. septempunctata in each field were compared by Contigency Table Analysis (Zar 1974). Impact of interplanting with "proper" flowers on predation of CPB in test fields: To assess the influence of strip insectary interplanting with "proper" flowers on EP parasitism on CPB eggmasses and predation on CPB eggmasses and larvae, we conducted two surveys of the fate of CPB eggmasses placed on sentinel eggplant plants over a nine-day long period. We designated 120 sentinel eggplant plants distributed evenly throughout each test field and deployed individual CPB eggmasses onto each one. A single one-day old CPB eggmass was glued to a 3 cm x 3 cm piece of artist's reference paper which closely matched the color of the eggplant leaf underside. A single eggmass card was stapled to a leaf underside of each sentinel plant, with a corresponding piece of coded flagging tape stapled to the top of the leaf or identification. Deployment of eggmasses took place on August 9 and 16, 1995. On every third day following deployment, each eggmass was examined to determined if it had: 1) hatched; 2) been consumed by predators; or, 3) been mechanically damaged by wind-blown sand or adjacent leaves. In addition, the number and instar stage of surviving CPB larvae from each eggmass were also noted and records where made of predators observed on eggmasses. The numbers of hatched and attacked CPB eggmasses and the number of surviving CPB larvae in each field were compared by Contigency Table Analysis (Zar 1974).
Influence of interplanting with "proper" flowers on coccinellid species diversity and abundance in test plots: A total of six coccinellid species were observed over the course of the study: C. septempunctata, C. maculata, H. variegata, Harmonia axyridis (Pallas), Hippodamia parenthesis (Say), and Proplea quatuordecimpunctata (L.). All six species were observed in the fields interplanted with dill and coriander. The least-observed species, P. quatuordecimpunctata was never found the control field. In all fields, C. septempunctata, C. maculata, and C. variegata were much more abundant than the other three species. The overall numbers of all coccinellid species observed during each census were significantly higher in the fields interplanted with dill and coriander than in the flowerless control field (Fig. 2a). Figure 2. Mean (+ SE) number of coccinellids observed during each survey by field treatment. A) All coccinellid species combined; B) C. maculata; C) H. variegata; D) C. septempunctata. Bars with different letters are significantly different at the P < 0.05 level.and - fig2 part 2While equivalent numbers of C. maculata were found in each of the flower-interplanted field (Fig. 3b), higher numbers of H. variegata were observed in the dill field than in the coriander field (Fig. 3c). Coccinella septempuncta was more abundant in the dill field than in either the coriander field or control field (Fig. 3d). This indicates that some coccinellid species may have a distinct preference for certain flower species. Coccinellids foraged on both umbels and eggplant foliage and were observed to move from the flowers to the eggplant and visa versa. While on the umbels, the coccinellids fed on nectar and pollen and actively foraged within the umbels for hidden micro-arthropods (i.e., mites, thrips and small leafhopper nymphs) hidden within the inflorescences. Mating pairs of coccinellids were also frequently observed on both dill and coriander inflorescences. Numerous other predators, especially adults and immatures of C. carnea and P. maculiventris and a variety of sphecid wasps, were present within the dill- and coriander-interplanted fields. Impact of interplanting with "proper" flowers on predation of CPB in test fields: There were no differences among treatments in the number of hatched CPB eggmasses (Fig. 3a). However, significantly more CPB eggmasses were attacked and consumed in the dill-intercropped fields than in the control field (Fig. 3b). Figure 3. Mean (+ SE) numbers of CPB eggmasses (A) hatched and (B) consumed; and, (C) numbers of CPB larvae surviving at the end of each survey by field treatment. Bars with different letters are significantly different at the P < 0.05 level.Survivorship of CPB larvae at the end of each survey was highest in the control field and lowest in the dill field (Fig, 3c). Both immature and adult stages of C. maculata, C. carnea, and P. maculiventris were observed feeding on CPB eggmasses and larvae on the sentinel eggplant plants and large numbers of sphecid wasps were observed foraging not only on the flowers but also on the surface of eggplant leaves. The greater amount of predation of CPB eggmasses and larvae observed in the dill and coriander fields is most likely due to the larger number of coccinellids and other predators observed in those fields.
These results indicate that strip insectary interplanting with "proper" flowers can have a strong effect on anthophilous CPB predator abundance and species diversity in eggplant fields. The scent and color of the dill and coriander flowers may have attracted the predators to the flower-interplanted fields (Patt, personal observation). Once the coccinellids and other predators entered the flower-interplanted fields they encountered more resources, in terms of the flowers providing additional nutrients and mating sites, than in the flowerless control fields. The greater resource pool present within the flower-interplanted fields may have retained these insects for a longer amount of time (Wright & Laing 1980, Groden et al. 1990, Ives, Karieva & Perry 1993). Increased predator conservation consequently resulted in increased mortality of CPB eggmasses and larvae. Based on these preliminary results, we believe that we have developed a promising method for enhancing predator efficacy and conservation in vegetable fields. The results from this study can be used to establish a set of criteria that can be used for selecting "proper" floral host plants that will enhance the conservation and augmentation of specific groups of beneficial insects in specific vegetable cropping systems. In addition, strip-insectary interplanting with "proper" floral host plants is very compatible with pest control strategies that include the application of insecticides that are targeted for specific types of pest insects (i.e., Bt and imidacloprid) or that include the deployment of Bt-transgenic crop plants, since CPB predators are not adversely affected by these compounds (Mark Mayer, NJDA, unpublished data ). Because it is compatible with herbivore-specific sprays and provides predators with a concentrated source of resources on a relatively small proportion of crop land, strip-insectary interplanting with "proper" floral host plants has the potential to become a very important component of IPM programs aimed at suppressing not only CPB but other vegetable pest insects as well.
The authors wish to acknowledge the assistance of their undergraduate research assistants: William Merritt, Barbara Dove, Jamie Furneisen, Christine Makosky, Nicole Synder and Erol Sati; and extend thanks to Dan Palmer, Mark Mayer and Robert Chianese of the New Jersey Department of Agriculture's Philip Alampi Beneficial Insect Laboratory for providing CPB eggmasses, logistical support and insect identification. REFERENCES ALTIERI, M. A. and WHITCOMB W. H., 1979 - The potential use of weeds in manipulation of beneficial insects - Hort. Science, 14: 12-18. ALTIERI, M. A. and LEPTOURNEAU D. K., 1982 - Vegetation management and biological control in agroecosystems - Crop Protection, 1: 405-430. ANDOW, D. A., 1983 - Effect of agricultural diversity on insect populations, p. 91-115. In: LOCKERETZ, W., (ed.), Environmentally Sound Agriculture, Praeger, New York. BIEVER, K. D. and CHAUVIN R. L., 1992 - Suppression of the Colorado potato beetle (Coleoptera:Chrysomelidae) with augmentive releases of predaceous stink bugs (Hemiptera: Pentatomidae) - J. Econ. Entomol., 85: 720-726. BUGG, R. L. & WILSON T., 1989 - Ammi visnaga (L.) Lamark (Apiaceae): Associated beneficial insects and implications for biological control, with emphasis on the bell-pepper agroecosystem - Biological Agriculture and Horticulture, 6: 241-268. CLAUSEN, C. P., 1956 - Biological Control of Insect Pests in the Continental United States. United States Department of Agriculture Technical Bulletin No. 1139, U. S. Government Printing Office, Washington, D. C.. COWGILL, S.E., WRATTEN S. D., and SOTHERTON N. W., 1993 - The selective use of floral resources by the hoverfly Episyrphus balteatus (Diptera:Syrphidae) on farmland - Ann. Appl. Biol., 122: 223-231. FAEGRI, K. and VAN DER PIJL L., 1979. The Principles of Pollination Ecology, 3rd. Ed. Pergamon Press, New York. GILBERT, F. S., 1981 - Foraging ecology of hoverflies: morphology of mouthparts in relation to feeding on nectar and pollen in some common urban species - Ecological Entomology, 6: 245-262. GRODEN, E., DRUMMOND F. A., CASAGRANDE R. A., and HAYNES D. L., 1990 - Coleomegilla maculata (Coleoptera:Coccinellidae) and its incidence in potatoes and surrounding crops - J. of Economic Entomology, 83:1306-1315. GROSSMAN, J. and QUARLES W., 1993 - Strip intercropping for biological control - The IPM Practioner, 15: 1-11. HAGEN, K. S., 1962 - Biology and ecology of predaceous Coccinellidae - Ann. Rev. Entomol., 7: 289-326. HAMILTON, G. C., 1995 - A comparison of eggplant grown under conventional and biological control intensive pest management conditions in New Jersey - Rutgers Cooperative Extension Bulletin E196, Rutgers University, New Brunswick, NJ. HASLETT, J. R., 1989 - Interpreting patterns of resource utilization: randomness and selectivity in pollen feeding by adult hoverflies - Oecologia, 78: 433-442. HAZZARD, R. V. and FERRO D. N., 1991 - Feeding responses of adult Coleomegilla maculata (Coleoptera:Coccinellidae) to eggs of Colorado potato beetle (Coleoptera:Chrysomelidae) and green peach aphid (Homoptera:Aphidae) - Environmental Entomology, 20: 644-651. HAZZARD R. V., FERRO D. N., VAN DRIESCHE, R. G. and TUTTLE R. F., 1991 - Mortality of eggs of Colorado potato beetle (Coleoptera:Chrysomelidae) from predation by Coleomegilla maculata (Coleoptera:Coccinellidae) - Environmental Entomology, 20: 841-848. HODEK, I., 1967 - Bionomics and ecology of predaceous Coccinellidae - Ann. Rev. Entomol., 12: 76-104. HOUGH-GOLDSTEIN, J. and WHALEN, J., 1993. Innudative release of predatory stink bugs for control of Colorado potato beetle - Biological Control, 3: 343-347. IVES, A. R, KARIEVA P., and PERRY R., 1993 - Response of a predator to variation in prey density at three hierarchical scales: lady beetles feeding on aphids - Ecology, 74: 1929-1338. JERVIS, M. A. and KIDD N. A. C., 1996 - Insect Natural Enemies - Chapman and Hall, London. KING, S, and OLKOWSKI W., 1991 - Farmscaping and IPM - The IPM Practitioner, 13: 1-12. KLOEN, H. and ALTIERI M. A., 1990 - Effect of mustard (Brassica hirta) as non-crop plant on competition and insect pests in broccoli (Brassica oleracea) - Crop Protection, 9: 90-96. LASHOMB, J. H., 1989 - Use of biological control measures in the intensive management of insect pests in New Jersey - Amer. J. Alter. Ag., 3: 77-83. LASHOMB, J. H., KRAINACKER D., JANSSON R. K., NG Y. S., and CHIANESE R., 1987 - Parasitism of Leptinotarsa decemlineata (Say) eggs by Edovum puttleri Grissell (Hymenoptera: Eulophidae): effects of host age, parasitoid age, and temperature - Can. Ent., 119: 75-82. MAINGAY, H. M., BUGG R. L., CARSON R. W., and DAVIDSON N. A., 1991- Predatory and parasitic wasps (Hymenoptera) feeding at flowers of sweet fennel (Foeniculum vulgare Miller var. dulce Battandier (Trabut), Apiacea) and spearmint (Mentha spicata L. Lamiaceae) in Massachusetts - Biological Agriculture and Horticulture, 7: 363-383. MAYER, M. and HUDSON W., 1993 - Biological control and management of Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) in eggplant using Edovum puttleri (Hymentoptera: Eulophidae) - 1993 Cooperative Project Report, New Jersey Department of Agriculture. NORDLUND, D. A., VACEK D. C., and FERRO D. N., 1991 - Predation of Colorado potato beetle (Coleoptera:Chrysomelidae) eggs and larva by Chrysoperla rufilabris (Neuroptera: Chrysopidae) larvae in the laboratory and field cages - J. Entomol. Sci., 26: 443-449. PROCTOR, M. and YEO P., 1972 - The Pollination of Flowers - Taplinger Publishing Co., New York. VAN EMDEN, H. F., 1989 - Plant diversity and natural enemy efficiency in agroecosystems, p. 63-80 In: Critical Issues In Biological Control. Intercept, Andover, UK. WHITE, A. J., WRATTEN S. D., BERRY N. A., and WEIGMANN U., 1995 - Habitat manipulation to enhance biological control of Brassica pests by hover flies (Diptera:Syrphidae), J. Econ. Entomol., 88: 1171-1176. WRIGHT E. J. and LAING J. E., 1980 - Numerical response of coccinellids to aphids in corn in southern Ontario - Can. Entomologist, 112: 977-988. WOLCOTT, G. N., 1942 - The requirements of parasites for more than host - Science 96: 317-323. ZANDSTRA, B. H. and MOTOOKA P. S., 1978 - Beneficial effects of weeds in pest management-A review- PANS, 24: 333-338. ZAR, J. H., 1974 - Biostatistical Analysis - Prentice-Hall, Inc. Englewood Cliffs, NJ.