BIOLOGICAL CONTROL

SPIDERS FOR PEST CONTROL

Keith Sunderland from Horticulture Research International (Wellesbourne, UK), Matthew Greenstone of the Agricultural Research Service of US Department of Agriculture (Stillwater, Oklahoma) and Bill Symondson of Cardiff University, UK, discuss whether spiders could make a worthwhile contribution to pest control

Introduction • "do spiders make a worthwhile contribution to pest More than 54,000 species of spiders (Figure 1) have been controP described from a vast range of habitats and spiders are • "how can spiders, as generalist predators, ever control frequently the dominant insectivores in many natural pests ?" ecosystems and crops. The majority are generalist predators, • "how is it possible to quantify the predation rate of so are not dependent on one prey type. Ibis article explores spiders on pests ill the field" current knowledge and attempts to answer the questions: • "is it realistic to niodify farming methods to boost the abu nd nice and hioeoii t rol clii ci eney of spiders

Do spiders control pests? Ill years evidence liasaicuiniilated, from field experiments, that spiders do control pests ill Some situations. Ill field experiments spider numbers were manipulated wit hi n plots by various methods, including removal b y hand, use of short-persistence insecticides arid provision of artificial web sites. Pest numbers, crop damage and yield were then measured ill and control plots. These ietliodsn cleinoii - strated a significant impact of spiders oil ill •1r (Oraze and Grigarick, 1989) and oil in a range of crops, including cotton, taro and apple. Spiders also controlled scale in citrus and several pests iii old fields" (i.e. cultivated fields that have been abandoned). Ill( effect of spider predation oil populations was shown to be sufficient to significantly reduce crop damage levels in soybean (Carter and Rypstra, 199) and vegetables (Riechert and Bishop, 1990)

How do spiders control pests? lrnl iv dual spider species are unlikely to regulate pest populations because they lack the typical attributes of effective specialist natural enemies. such as short generation times arid aggregative and reproductive responses to pest 4 density. 1 low then call control pests? The trick is diversi- fication. There are relatively few specialist natural enemy species in our crops, but many generalists, including spiders. Recent surveys have identified 60 species of spider in apple orchards, 88 in barley and 112 ill It has been found that the different species in a crop tend to occupy cornplemen lary niches (LJetz et a/., 1999). The spider fauna of apple trees, Figure I. Tetra gnat ha laboriosa Hentz (Araneae: [Or example, segregate spatially and in terms of foraging mode Tetragnathidae). This long-jawed orb-weaver is ubiquitous and and diel activity pattern (Marc and Canard, 1997). This abundant in North American agroecosytems. The prey in the increases the chances that all life stages of a pest will come web is a greenbug, graminum (Rondani) (Insecta: under attack. Some species of spicier even eat the eggs of pests. ), an pest of cereals throughout Europe, Asia, So it is the assemblage of spider species, rather than a single Africa and the Americas. Photograph courtesy of Scott Bauer, species, that makes all on the pest population. These Agricultural Research Service, United States Department of spider assemblages can, ill forin one component of a Agriculture. larger natural eneniv roniplex. The relative inportann ol

82 Pesticide Outlook - April 1999 BIOLOGICAL CONTROL

Spiders \V it liiii these (iiipl(\es Varies hctwceii cl()pS iiiid countries, but spiders are a dominant component in Soiiie. such as in cotton iii China and the USA. The ver y lack at feeding specialism exhibited by generalist spiders can, iii itself, he advantageous For pest control since it allows spiders to be present in the crop, feeding on alternative prey, even before the pest arrives. V\ilien the pest does arrive, the spider. pest ratio is initially high, enabling the rate of increase of the pest to he heir] at a moderate level until specialist predators and parasitoids arrive to finish the job later in the season. Spiders and specialists can "cooperate" in other ways too. For example, it has been demonstrated in cereals that foraging aphid 1iarasi aids and lad ybirds dislodge niaitv from the plants. In this crop there are more than 60 species of spicier located on the ground, or at a inaximnuni of 10 cm above ground, and their webs can cover 50 0/o of the ground surface (Sunderland ct al., 1986). Iliiis the pest dislodgement activity of foraging specialists will empower ground-based spiders as predators of foliage pests. III her crops, such as apple (Niansour ct a/., 198 1) and taro ( akasuji t/ al.. 1973), it is tile spiders that do the dislodging. ]it crops there are spider species that, in the course of foraging on the plant, dislodge about a third of the caterpillars they encounter. This results in death of the caterpillars on the ground. A number of other aspects of spider biolog y suit them well for biological control. lucy are physiologically adapted for "feast or famiiitie", and can gorge themselves when prey are abundant and store food reser cs in extensive gut diverticula that extend even into thu legs. \\ lien prey iire scarce they can survive for very long periods by reducing their metabolic rate. Iliey also may kill far more prey than theyey eat. This (,art come about when a satiated spider remains in "killing mode" III presence of Figure 3. James Harwood in the Invertebrate Molecular Ecology superabundant prey, or when a naive spider kills a prey that Laboratory in Cardiff, biochemically analysing spiders to turns out to he distasteful. Pests may die in webs even if the determine their diets. Photo by Viv Williams, School of spider does not attack them, because the y are too small for tile Biosciences, Cardiff University spider, or it is satiated, has an aversion to them or has abandoned the web.

Can predation rates be quantified? Now that we are beginning to appreciate the potential value of spiders in pest control it becomes worthwhileorthhile to make detailed studies of exactly which I i. .. $ shmecics of spider are killing which species of pest and a what extent. Tins is riot a simple matter given that we want realistic figures that relate to the field uation rather than to the laborator y, and bearing in iund that spiders often operate cryptically at night 1ft: iff under vegetation, and often eat a much wider inge of prev species than just pests. How then can 11 determine the diet of spiders in the field and try a quantify how many pests each spider has eaten? Spider diet and rate of predation (,art hea determined bv direct observation. This works best or web spiders, where one can find prev carcasses. md for active and conspicuous hunting spiders, such ... some diurnal wolf spiders, that can be observed irrying prey in their jaws (Greenst one and l11yt "ilnderlaucl, 1999). Nevertheless, direct observation Figure 2. Keith Sunderland monitoring Ballooning spiders in the field. is time and labour intensive, and also may interfere Photo Nigel Cattlin. © Holt Studios wit 11 the population processes one wishes to sturd y. A

Pesticide Outlook - April 1999 83 BIOLOGICAL CONTROL more efficient approach is the biochemical analysis of the gut Conclusion contents of samples of spiders collected from the field (Figure There is now good evidence-that spiders are able to control 2). Currently, immunological assays employing antibodies to pests and reduce damage to crops. This is achieved by an prey proteins are the only methods in routine use. assemblage of spider species, impacting on all life stages of the Contemporary technologies, including monoclonal antibodies pest, and working in concert with a wide range of other and very sensitive ELJSA and immunodot assays, are natural enemies, including specialists. There are many aspects employed (Greenstone, 1996; Symondsori and Hemingway, of spider biology that render them highly suitable for 1997) (Figure 3). It will soon be possible to identify prey biological control, and the view that it is only specialist remains in spider guts by DNA fingerprinting and other natural enemies able to coordinate their reproduction with molecular techniques. changes in pest density that can contribute to pest control, is Spiders are liquid feeders and the remains of several meals now out-dated. Detailed quantitative studies of pest control by may be found concurrently. This presents technical problems spiders in the field are now justified, and a range of sophisti- in estimating rates of predation from the immunological assay cated and innovative biochemical techniques are under results (Stuart and (;reenstone, 1990). Early statistical development to meet this challenge. There seem to be good estimates were largely based on the proportion of assay prospects for managing agroecosystems in ways that boost the positives (Nakamura and Nakamura, 1977; (;reenstone 1979). biocontrol component of pest control. An important aspect of Later, equations were developed that incorporated digestive this management that still remains to be developed is to find rates (determined in the laboratory) and measurement of the ways of using more specific chemical or bio-pesticides that mass of prey ingested using quantitative assays (Sopp et at., work with, rather than against, spiders. 1992; Mills, 1997). However precise our measurements of consumption become, however, they will still provide conserv- ative estimates of predation. This is because many prey are, in fact, only partially consumed, and therefore biochemical tests Acknowledgements must be allied to studies of the feeding behaviour of the We thank the 151K Ministry of Agriculture, Fisheries and Food spiders concerned. for sponsoring this work, and Mark Tatchell, Kris Giles and Tom Phillips for helpful comments on the manuscript.

Can spider effectiveness be boosted by modifying farming techniques? At a recent International Symposium of spider agroecology References (Greenstone and Sunderland, 1999) there was much interest Carter, P C.: Rvpst ia. A. L. (1995) Top-down effects in so y bean agroecosvs- tenis: spider iliiisiiy affects herbivore damage. Oiko.s 72, 433-439. in the prospects for improving biological control of pests Greenstone, M. II.; Sunderland, K. I). (lids) (1999) Spiders in through ecosystem engineering. Practical measures that Agroecosysteins: Ecological Processes and Biological Control. Journal of increase the structural complexity of the habitat, such as .47-achnology, in press. intercropping, mulching and conservation tillage, are known (;reenstone, M. H. 1979. Spider feeding behaviour opiiniises dietary essential amino acid composition. Nature 181, 301-501 to enhance the density and diversity of spiders and other pre- Greenstone, M. II. 1996. Serological analysis of predation: past, dators. Conservation tillage (e.g. direct-drilling) and mulches present and future. In: The Ecology of .4gricultural Pests: Biochemical are examples of approaches that could simultaneously provide Appi-oaches N. 0. C. Syinondson and J. C. Liddell (Eds.), Chapnian & spiders with a more diversified habitat structure and a Hall, London, pp. 65-300. nutrient and energy boost from the detritivore food chain Mansour, C; Rosen, D.; Shulov, A. (1981) Disturbing effect of a spider on larval aggregations of Spodopteia Li Ito, a/is. lsntomologza Eiperuneotalis (Riechert, 1999; Wise et at., 1999) The latter principle et-lpplicata 29, 234-37. operates successfully in tropical paddy fields. Populations of Marc, P.; Caiiard, A. (1997) Maintaining spider biodiversity in agroecosys- spiders and other generalist predators build up early in the terns as a tool iii pest control. Agricu Loire, Ecosystems and Environment season by feeding on detritivores and plankton-feeders. Then, 62, 229-233. when this non-pest prey resource collapses naturally in the Mills, N. (1997). Techniques to evaluate the efficacy of natural enemies. In: Methods in Ecological and Agricultural Entomology. I). R. Dent and mid-season, the generalists switch to feeding on herbivores, M. P. Walton (Ms.), CAB International, Oxford, pp. 271-291. including hopper pests, and thereby prevent pest outbreaks Nakamura, M.; Nakamura, K. (1977) Population dynamics of the chestnut (Settle et at., 1996). This natural control of hopper pests is gall wasp, Dryocosmus kuriphillus Yasuinatsu (Hyinenoptera: disrupted if insecticides are applied to the crop. In general Cynipidae). Oecologia 27, 97-116. though, and for the forseeable future, biological control of Nakasuj i,E; Yamanaka, H.; Kiritani, K. (1973) The disturbing effect of pests by spiders will be part of integrated management micryphantid spiders on the larval aggregation of the tobacco cutworm, Spodoptera litora (Lepidoptera: Noctuidae). Kontyu 41, 220-227. systems that include the use of pesticides. Research is required Oraze, M .... Grigarick, A. A. (1989) Biological control of aster leafhopper into the selective use of pesticides that work with spiders, (Hoinopnera: Cicadellidae) and midges (Diptera: C}iironomidae) by rather than against them. This will need to be based on a Pa,dosa ramulosa (Araneae: I.ycosidae) in California rice fields. Journal sound understanding of the ecotoxicology of spiders, but ofEconomoic Entomology 82, 745- 749. unfortunately, at the moment, our knowledge of spider ecotox- Riechert, S. E. (1999) The bows and whys of successful pest suppression by spiders: insights from case studies. In: Spiders in Agroecosysterns: icology is lagging significantly behind that of other generalist Ecological Processes and Biological Control. M. H. Greenstone & predators, such as carabid beetles. K. D. Sunderland (Eds). JournalfArachnology, in press.

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Rice her t, S. F.; Bishop, I .. (1990) lre y control by an assemblage of generalist predators: spiders iii garden test systems. Ecology 71 , 1141- Keith Sunderland is a research scientist with Horticulture Research 1450. International at Wellesbourne. UK. He has worked on the ecology Settle, W. H.; Ariawan, A.; Astuii, F. T; Cah yana, W; Hakim, A. 1.0; of generalist predators and their role in pest control, for 25 years. Hindayana, 0.; Lestari, A. S.; Pajarningsih (1996) Managing tropical His current research interests include interactions between rice pests through conservation of generalist natural enemies and predators, parasitoids and pathogens, and the role of prey biodiver- alternative prey. Ecology 77, 1975-1988. Sopp, P I.; Sunderland K. Ii.; Fenlon, J. S.; Wratten, S. D. (1992) An sity in influencing biocontrol efficiency of generalist predators. improved method for estimating invertebrate predation iii the field Matthew H. Greenstone has been a Research Entomologist with the using an enzyme-linked immunosorbent assay (ELISA). Journal of United States Department of Agricultures Agricultural Research Applied Ecology 29, 295-302. Service for seventeen years. He is stationed in Stillwater, Oklahoma, Stuart, M. K; Greeristone, M. H. (1990) Beyond ELISA: a rapid, selisitis where he uses antibody and nucleic acid-based methods to specific immnunodot assay for identification of predator stomach contents. Annals n/the Entomological Society ofAnierica 83, 11(11 111)7. determine the impact of parasitic and predatory on Sunderland, K. I).; Fraser, A. M.; Dixon, A. F 0. (1986) Field and laboratory cereal aphid pests. He has a special interest in the ecology of studies on money spiders (Linyphndae) as predators of cereal aphids. spiders, and has studied their predatory behavior, metabolism, and Journal o/.ipplted Ecology 23, 433-447. aerial dispersal, and how the physical structure of the plant Symondson, W. 0. C; I Iemingway, J. (1997) Biochemical and molecular techniques. In: Methods in Ecological ant]. igricultural l.ntoiiiology. communities in which they live influences their diversity and D. R. Dent and M. P Walton (Eds.), CAB International, Oxford, pp. 295- abundance. 350. Bill Symondson is a crop ecologist and lecturer within the School of [etz, G. W.; I lalaj, J.; Cady, A. B. (1999) Guild structure of spiders in major Biosciences of Cardiff University. His main interest over the last 12 Spidem;c in Agroecosyaennc Ecological Processes and Biological crops. In: years has been in detecting and quantifying predation by ground Control. M. II. Greenstone and K. I). Sunderland (Eds) Journal of beetles and, more recently, spiders on pests within arable Arach,iology, in press. Wise, D. H.; Snyder, W. F.; Tuntibunpakul, P; Halaj, J. (1999) Spiders in ecosystems. He has developed a range of biochemical and decomposition food webs of agroecosystems: theory and evidence. In: molecular techniques for monitoring predator-prey interactions and Spiders iii .igtoecos-cstems Icological Processes and Biological Control. uses this information to improve our understanding of the long- \J. H. Greenstone and K. D. Sunderland (Eds). Journal ojArachnoloas. term effects of predation on pest populations. in press.

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