1999. The Journal of Arachnology 27:351±362

THE IMPLICATIONS OF INTRAGUILD PREDATION FOR THE ROLE OF IN BIOLOGICAL CONTROL

Margaret A. Hodge: Department of Biology, The College of Wooster, Wooster, OHIO 44491 USA

ABSTRACT. Evidence is growing that spiders can be effective biological control agents, particulary assemblages of several species. Other evidence ®nds that spiders prey on each other and other generalist predators, and as such are of limited value in biological control. Such predatory interactions between species which use similar resources have been dubbed intraguild predation (IGP) due to their potential to modify competition as well as cause direct mortality. IGP interactions can have unexpected effects at other trophic levels, and sometimes result in enhancement of a pest population. In this paper I review the evidence for intraguild predation interactions involving spiders in natural systems, and other generalist predators in agroecosystems. To date not much research has examined whether such interactions in¯uence biological control potential. Some suggestions as to how we might begin to address these issues are presented.

Given their generalist diet and that use similar resources (Root 1967; Polis et abundance in most terrestrial habitats, spiders al. 1989; Simberloff & Dayan 1991). Preda- likely in¯ict substantial mortality on insect tory interactions among members of the same populations. While the mechanisms by which guild are termed intraguild predation (IGP). spiders limit insect prey populations have This is distinguished from predation as tradi- been debated (Riechert & Lockley 1984; Wise tionally de®ned because, by eating a guild 1993), it is generally agreed that they are im- member, an individual not only directly gains portant in reducing insect numbers, and as energy and nutrients, but also reduces poten- such are of potential value in biological con- tial competition for food (Polis et al 1989; Po- trol (Riechert & Lockley 1984; Nyf¯er & lis & Holt 1992). Intraguild predation and Benz 1987; Young & Edwards 1990; Wise cannibalism (killing and eating a member of 1993). Several studies have shown that assem- the same species), may have profound effects blages of many predator species may be more on community structure (Polis 1981, 1988; effective at controlling agricultural pests than Polis et al. 1989; Polis & Holt 1992). Given single species augmentation (Chiverton 1986; their ubiquity in terrestrial ecosystems, spiders Riechert & Bishop 1990; Clark et al. 1994; are model organisms to investigate the occur- Provencher & Riechert 1994; Chang 1996; rence and consequences of IGP. Riechert & Lawrence 1997). On the other IGP: predation among potential compet- hand, different species of predators and/or itors.ÐIntraguild predation and cannibalism parasitoids may compete with or prey on each have been shown to directly limit predator other, potentially reducing their biological populations (Polis & McCormick 1986, 1987; control potential (Force 1974; Ehler & Hall Spiller & Schoener 1988; Wissinger 1989; 1982; Spiller 1986; Briggs 1993; Rosenheim Leonardsson 1991; Finke 1994; Wagner & et al. 1995; Chang 1996; Ferguson & Stiling Wise 1996; Wissenger et al. 1996). Since un- 1996; Kester & Jackson 1996; Cisneros & Ro- successful predation attempts represent ex- senheim 1997; Rosenheim 1998). treme forms of interference competition (Polis The nature of the diet of spiders suggests et al. 1989; Elgar & Crespi 1992), IGP can that they can prey on each other and other also lead to behavioral adaptations to reduce arthropod predators (Polis 1981; Jackson mortality and con¯ict, resulting in habitat and 1992; Wise 1993), as well as overlap in prey diet shifts by IG prey (Fox 1975; Turner & taxa consumed, thus potentially competing for Polis 1979; Doncaster 1992; Sih 1982; Eben- resources. Diet overlap is one distinguishing man & Persson 1988; Foster et al. 1988; Polis feature of a guild, a group of sympatric taxa et al. 1989; Polis 1993; Dong & Polis 1992;

351 352 THE JOURNAL OF ARACHNOLOGY

Holt & Polis 1997). These changes in foraging Two alternative hypotheses could explain and habitat distribution may in turn have ef- these results: removal of the scorpions could fects at other trophic levels (Polis 1984; Wil- have resulted in competitive release by the bur 1988). spiders in experimental plots, or IGP (by scor- The traditional view of feeding relation- pions) in the control plots may have reduced ships has been to assign species in a com- spider population size. There was no evidence munity to a ``trophic-level'', such as second- of competitive release in that there were no ary consumer (predator), primary consumer differences between the experimental and con- (herbivore), primary producer (plant), and so trol plots in insect prey abundance or spider forth, with each level feeding on the former reproduction. Release from scorpion predation (Krohne 1998). Thus, in classic biological was the most likely cause of the increased control, insect herbivore populations are re- numbers of spiders. duced by addition of predators, and this in Two independent studies on Anolis lizards turn reduces damage to crop plants (van den examined evidence for intraguild predation on Bosch et al. 1982). In reality, however, ani- spiders cascading to populations of shared in- mals may feed from a variety of trophic lev- sect prey. Pacala & Roughgarden (1984) ma- els, especially generalist predators, which take nipulated anole densities in a Carribean forest prey of whatever size they can handle (Polis and found a direct effect of lizards on forest 1988; Polis et al. 1989; Spence & Carcamo ¯oor , their primary prey, and an 1991; Dong & Polis 1992; Finke 1994). If indirect effect on ¯ying insects, the prey of these prey include younger conspeci®cs or orb-weaving spiders. Since anoles also prey other predators, then control of the herbivore on orb-weavers, the increase in ¯ying insects population is not guaranteed. Various studies on the high density lizard plots was thought suggest that direct effects of one predator on to be due to intraguild predation by the lizards another can indirectly affect a shared prey on the spiders. On Bahamian islands Spiller species by releasing it from intense predation & Schoener (1990) also found a direct effect or competition (Press et al. 1974; Pacala & of lizards on spiders, but no indirect effect on Roughgarden 1984; Hurd & Eisenburg 1990; ¯ying insects. They did, however, observe that Polis & Holt 1992; Rosenheim et al. 1993; more spiders were feeding on lizard removal Wissinger & McGrady 1993; Wootton 1993; plots than on plots where they co-existed with Cisneros & Rosenheim 1997; Fagan & Hurd lizards. The authors hypothesized that inter- 1994). If shared prey are herbivores then the ference competition or predation by lizards indirect effects could cascade to plants, in¯u- may displace spiders from prime web-sites, encing primary productivity, an issue of ag- resulting in a reduction in prey capture for the ricultural relevance. The purpose of this paper spiders. is to review the theory and empirical evidence Although the generalist diet of most spider relevant to the implications of IGP for the po- species suggests that exploitative competition tential role of spiders in biological control of for food should be important (Marshall & herbivorous pests in agriculture. Rypstra, this volume), experimental tests have IGP between spiders and other generalist found little evidence (Schaefer 1978; Wise predators.ÐSeveral studies of IGP in natural 1981; Horton & Wise 1983; Riechert & Cady communities have uncovered direct and indi- 1983; see Spiller 1984 a, b for an exception). rect interactions involving spiders. Polis & In spider removal experiments to test for ex- McCormick (1986, 1987) investigated a desert ploitative competition among four genera of community of including spiders, web-building spiders, Riechert & Cady (1983) solpugids and scorpions, all generalist preda- not only found no competitive release, but on tors that use similar prey and prey on each some of their removal plots they observed a other. Scorpions were continually removed negative effect of spider removals on the spe- from experimental plots, but not from control cies remaining. They hypothesized that this plots, and the relative abundances of the spi- may have been due to the fact that by remov- ders and solpugids were tracked over time. At ing the other species of spiders, they may have the end of the experiment (29 months), sig- been removing potential prey. ni®cantly more spiders occurred in the scor- Hodge & Marshall (1996) tested Riechert pion removal plots than in the control plots. & Cady's hypothesis that intraguild predation HODGEÐIGP, SPIDERS & BIOLOGICAL CONTROL 353 masked competitive release in their system of ground caused the crickets to move upward web-building spiders on rock outcrops in Ten- on vegetation (a direct effect of spiders on nessee. After 12 weeks of removing each of crickets); but when present with both mantids three species from experimental plots we and lycosids, crickets were captured by man- found that one of the species, Hypochilus tho- tids hunting in the vegetation. Finally, lyco- relli (Araneae, Hypochilidae) had lower body sids may have consumed other cricket preda- condition indices (indicating lower fecundity, tors (other spiders; an indirect effect of spiders Jakob et al. 1996) on spider removal plots as on crickets); this was supported by the ®nding compared to control plots. This species was that there were signi®cantly fewer heterospe- the major intraguild predator in the system, ci®c spiders in the lycosid enclosures. These with spiders comprising over 40% of its diet results should be of interest to biological con- (Riechert & Cady 1983; Hodge & Marshall trol because mantids are often augmented, at 1996). These results support Riechert & least in small scale crop systems. On the other Cady's interpretation of the lack of competi- hand one may question the reality of this ex- tive release in their study. Another species, periment since many predators were packed Achaearanea tepidariorum (Araneae, Theri- into small enclosures, whereas normally they diidae) exhibited greater spiderling popula- could ¯ee from one another. tions on rock outcrops from which the other Enclosure effects were not a factor in the two species had been removed as compared open-plot studies performed by Moran & to control plots, suggesting that the manipu- Hurd (1994) in the same system. They added lation removed predators (Hodge & Marshall ®rst instar mantids to 2 m ϫ 2 m plots sepa- 1996). The fact that this study found IGP-re- rated by 2 m wide barriers of black plastic lated effects was striking given that the re- sheeting which had a band of insect trapping movals occurred over a relatively short time compound painted down the middle to inter- frame. cept arthropods leaving the plots. By compar- Hurd & Eisenberg (1990) examined how ing arthropods captured around mantid addi- interactions between praying mantises (Ten- tion plots to those captured around control (no odera sinesis) and wolf spiders (Lycosa (Ra- mantids) plots, they discovered a behavioral bidosa) rabida) affected overall arthropod response by spiders to the presence of elevat- numbers in a temperate early successional ed mantid densities. Spiders dispersed from ®eld habitat. They established four treatments, plots in which mantids were augmented. each of which enclosed a cubic meter of old- Smaller spiders (Ͻ 8 mm) are prey of the ®eld vegetation in screen cages: mantids mantids whereas larger spiders (primarily alone, wolf spiders alone, mantids and wolf wolf spiders) prey on the mantid nymphs and spiders, and a control with neither predator smaller spiders. Larger wolf spiders may have added, and then sampled the number and bio- departed mantid addition plots because small- mass of other arthropods after 10 days. The er spiders had dispersed. In this case the threat `mantids alone' enclosures had lower arthro- of IGP caused smaller spiders to leave, and pod biomass than any of the other treatments. scarcity of this IG prey caused the larger spi- Examining the arthropods on a taxa-by-taxa ders to leave. Addition of supplemental food basis revealed that in the `wolf spiders alone' (Drosophila) reduced the tendency for spiders treatments there was a signi®cant increase in to emigrate from mantid augmented plots the density of crickets as compared to the oth- (Moran & Hurd 1997). This in turn increased er treatments. The explanation for this coun- IGP by spiders on mantids, as their numbers ter-intuitive result illustrates the complexity of tended to decline in the food supplemented direct and indirect effects that can result from plots. As the authors point out, alternative IGP interactions. The authors concluded that prey does not always bene®t generalist pred- interactions between wolf-spiders (as evi- ators if they can prey on one another. denced by some cannibalism) decreased their These authors extended their investigation effectiveness as predators on crickets, and that to include the possibility of trophic cascades in mantid/lycosid enclosures this effect was (Moran et al. 1996; Moran & Hurd 1998). Of ameliorated because of mantid impact on spi- interest was how a diverse plant community der numbers (an indirect effect of mantids on would respond in the context of an assem- crickets). The presence of lycosids on the blage of many predator and herbivore species. 354 THE JOURNAL OF ARACHNOLOGY

In these experiments, control plots had no in the presence of bugs. To isolate the in¯u- mantids, and experimental plots had natural ences of predation cotton plants were caged densities of mantids. Cursorial spiders emi- with a variety of combinations of predators: grated from mantid plots throughout the each hemipteran species alone or in combi- course of the study (2 months) (Moran et al. nation with lacewing larvae (with appropriate 1996). Early emigration was probably due to controls). Lacewing survival was signi®cantly the threat of IGP by mantids, whereas later lower in the Z. renardii and Nabis spp. treat- emigration may have been a result of com- ments. Comparing aphid population growth petition for prey, since mantid numbers at this among the single-predator species treatments, point in time were too low to cause predator only in those cages with lacewing larvae alone avoidance. Herbivore biomass was signi®- was there a signi®cant impact on aphids, sug- cantly lower and plant biomass was 30% high- gesting that of all of these predator species, er in the mantid addition plots by the end of lacewings are the most effective at aphid con- the experiment. Mantids therefore caused a trol. Given these results, it is not suprising that trophic cascade that extended to plants. cages with lacewing larvae and Z. renardii or These studies demonstrate that, contrary to Nabis spp. exhibited a non-additive effect on theoretical predictions that interactions be- aphid population control. Not only were the tween trophic levels in complex communities effects non-additive, but aphid populations ac- will be diffuse and buffer the intensity of re- tually increased in these treatments. There- sponses of any given species to another fore, predator interference generated a trophic (Strong 1992), a single predator in a speciose cascade, increasing the abundance of herbi- natural assemblage can indeed initiate a tro- vores. phic cascade. Perhaps this bodes well for po- They also examined the effect that nymphal tential predator in¯uences on primary produc- hemipterans can have on lacewing eggs. The tion in less speciose agroecosytems: that is, presence of hemipterans reduced the propor- despite the potential for IGP, strong interac- tion of lacewing eggs surviving to larval stag- tions can cascade through trophic levels in es. Cisneros & Rosenheim (1997) examined such a way as to bene®t crops. On the other the effect of predation by Z. renardii of dif- hand, these strong interactions could be such ferent age-size classes on control of cotton that IGP interactions disrupt rather than en- aphid populations by lacewing larvae. Surviv- hance the control of herbivore populations al of lacewing larvae was signi®cantly lower (Rosenheim et al. 1993; Rosenheim 1998). in the presence of larger, older Zelus, and this IGP in agroecosystems.ÐThe fact that the produced a signi®cant disruption of lacewing self-limiting nature of spiders (via interfer- control of aphid populations. Observations of ence, territoriality or araneophagy) can de- freely foraging bugs in the ®eld showed an crease their potential as biological control ontogenetic shift in foraging height and for- agents has been recognized (Reichert & Lock- aging behavior resulting in higher encounter ley 1984; Wise 1993), but rarely quanti®ed. rates between Zelus adults and other predators The bulk of my review will therefore cover (Cisneros & Rosenheim 1998). experimental studies involving IGP among ar- Another study of aphidophagous predators thropod generalist predators other than spi- examined interactions between generalists and ders, since they have as yet not been well specialists and evaluated predator mobility as studied. a potential factor in¯uencing vulnerability to Rosenheim et al. (1993) examined interac- IGP (Lucas et al. 1998). The predators were tions between three species of predatory hem- lacewings (Chrysoperla ru®labris), spotted iptera (Geocoris spp., Nabis spp., and Zelus lady beetles (Coleomegilla maculata), both renardii) and green lacewing larvae (Chryso- generalists, and larvae of the gall midge (Ap- perla carnea (Neuroptera)), all of which eat idoletes aphidimyza), a specialist on the aphid pests (Aphis gossypii) of cotton. To de- shared prey, potato aphids (Macrosiphum eu- termine whether hemipteran predators exert phorbiae). The lacewing and lady beetles are mortality on lacewings, they caged cotton very active foragers as larvae and adults, plants with aphids alone (control), and aphids whereas gall midge larvae are slow-moving with various combinations of the hemipterans. predators. Lacewing survival was signi®cantly reduced IGP interactions between all three predators HODGEÐIGP, SPIDERS & BIOLOGICAL CONTROL 355 were investigated in the absence of aphid uni®es all of these predictions, and all of the prey. Various combinations of predators at dif- experimental studies presented above, is that ferent developmental stages (egg-adult) yield- a detailed understanding of the ontogeny, be- ed 37 different test combinations. Symmetric havior and ecology of predators and prey is IGP occurred between lacewings and lady required to understand the role that IGP plays beetles; that is, larger developmental stages of in the dynamics of complex communities, in- one predator fed on smaller developmental cluding agroecosystems. stages of the other. A few exceptions were ex- IGP & spiders in agroecosystems.Ð plained by behavioral and morphological dif- Though some research has been conducted ferences between the predators. Third instar evaluating the effectiveness of spiders as bio- lacewings were able to prey on larger fourth control agents in agroecosystems (Riechert & instar lady beetles as well as adult beetles. It Bishop 1990; Clark et al. 1994; Provencher & may be that a more aggressive hunting style Riechert 1994; Carter & Rypstra 1995; Riech- and effective grasping mouthparts of lace- ert & Lawrence 1997), there has been scant wings allow them to defy the general trend research on their potential interactions with that the larger predator wins (Lucas et al. other predators. Fagan et al. (1998) discovered 1998). Interactions between both lacewings an unpredicted interaction between IGP, pes- and lady beetles with gall midges were asym- ticide application and biological control. They metric: gall midges were almost never IG set out to examine the compatibility of insec- predators. This con®rmed the authors' predic- ticide-based and natural enemy-based pest tion that more mobile predators have an ad- control methods in tropical rice. Using open- vantage over slow moving predators. top cages (to ameliorate enclosure effects) In the presence of shared or extraguild prey they established four treatments: insecticide (potato aphids) IGP was lower in several of added, wolf spiders added, both insecticide the predator/life-stage combinations. Some of and wolf spiders added, nothing added. As the IGP interactions persisted though, except would be predicted, rice pests were lower in when extraguild prey densities were very the insecticide and wolf spider treatments, and high. Based on the outcomes of IGP interac- each reduced pest densities to similar levels. tions between their different predators at var- The combination of insecticide and wolf spi- ious levels of extraguild prey, Lucas et al. der addition, however, resulted in an increase (1998) developed some general predictions as in pests such that these enclosures were indis- to the effect of extraguild prey and predator tinguishable from the controls. They attribute characteristics on the direction and outcome these results to the additive impact of spiders of IGP interactions. In cases where both pred- and insecticide on predatory hemipterans (me- ators forage randomly, IGP will decrease soveliids) which are also important biological steadily with increasing extraguild prey. Ran- control agents of rice pests. The combination dom search will, in this case, bring predators spider-insecticide treatment lowered the den- into contact with extraguild prey more often. sities of these alternative predators below the When IGP interactions are risky for both pred- threshold of effective biological control. This ators, IGP should decrease exponentially as study has important implications for integrat- extraguild prey increases in density. Abun- ed pest management, and further illustrates the dance of alternative prey has similarly been importance of a clear understanding of the observed to in¯uence the tendency towards role of IGP in agricultural systems. cannibalism in many (Elgar & Crespi Given the general lack of experimental 1992). In some cases IGP may remain con- studies, what evidence (beyond Fagan et al. stant despite increasing extraguild prey, es- 1998) do we have that IGP involving spiders pecially if IG prey are vulnerable, sessile and/ might be important in agroecosystems? Sev- or aggregated. Finally, IGP may remain high eral studies have documented that spiders do at low extraguild prey densities, and only de- engage in IGP interactions with other gener- cline at very high extraguild prey densities. alist predators, and many of these observa- When extraguild prey are at low density, IG tions come from crop systems (Table 1). predators may bene®t from removing potential These data were gleaned from tables in pri- competitors, whereas at high prey density this mary research papers and from several re- bene®t disappears. Overall, the theme that views of spider diets by Nyffeler and col- 356 THE JOURNAL OF ARACHNOLOGY

Table 1.ÐA survey of the literature containing ®eld observations of the spectrum of prey captured by a variety of spider species focusing on taxa that are potentially intraguild prey. The percent of the total observed diet for the majority of species in the list is obtained from a total number of observed prey exceeding 50.

%of IG predator IG prey taxon diet Habitat Source Araneidae: Argiope bruennichi Araneae 3.3 Grassland Nyffeler 1982 Linyphiidae: Oedothorax insecticeps Araneae 16.3 Rice Kiritani et al. 1972 Theridiidae: Latrodectus mactans Solenopsis in- 75.3 Cotton Nyffeler et al. 1988 victa Achaearanea tepidario- Araneae 22 Rock outcrop Hodge & Marshall 1996 rum Lycosidae: Paradosa spp. Araneae 6.8 Winter Wheat Nyffeler & Benz 1988 Paradosa ramulosa Araneae 19.6 Alfalfa Yeargan 1975 Lycosa pseudoannulata Araneae 8.9 Rice Kiritani et al. 1972 Lycosa antelucana Lycosidae 4 Cotton Hayes & Lockley 1990 Lycosa antelucana Staphylinidae 6.7 Cotton Hayes & Lockley 1990 Lycosa antelucana Carabidae 10.9 Cotton Hayes & Lockley 1990 unspeci®ed Araneae 19.2 Peanuts Agnew & Smith 1989 Pardosa lugubris Araneae 24 Forest Edgar 1969 Pardosa lugubris Araneae 34 Forest Hallander 1970 Pardosa amentata Araneae 11 ? Edgar 1970 Pardosa pullata Araneae 38 Meadow Hallander 1970 Pardosa purbeckensis Araneae 23 Salt Meadow Nyffeler & Benz 1988 Pardosa ramulosa Araneae 20 Alfalfa Yeargan 1975 Pardosa hokkaido Araneae 12 Forest Suwa 1986 Pirata piraticus Araneae 22 Salt Meadow Schaefer 1974 Pirata piraticus Araneae 28 River Bank Gettmann 1977, 1978 Pardosa agrestis Araneae 16 ? Nyffeler 1982 Lycosa osceola Araneae 27.5 Florida scrub Hodge, unpublished Lycosa pseudoceratiola Araneae 9 Florida scrub Hodge, unpublished Oxyopidae: Oxyopes salticus Araneae 15.9 Cotton Nyffeler et al. 1992 Oxyopes salticus Araneae 14.1 Cotton Nyffeler et al. 1987a Oxyopes salticus Araneae 9 Cotton Nyffeler & Sterling 1994 Peucetia viridans Araneae 40 Cotton Nyffeler et al. 1987b Peucetia viridans Hemiptera 8 Cotton Nyffeler et al. 1987b Peucetia viridans Neuroptera 8 Cotton Nyffeler et al. 1987b Peucetia viridans Araneae 16 Croton Nyffeler et al. 1987b Peucetia viridans Araneae 13.3 Peanuts Agnew & Smith 1989 Peucetia viridans Araneae 7 shrubs Turner 1979 various Araneae 15 ? Nentwig 1986 Thomisidae: Xysticus spp. Araneae 6.4 Meadow: Plants Nyffeler 1982 Xysticus spp. Araneae 26 Meadow: Soil Sur- Nyffeler 1982 face Misumenops spp. Araneae 16.7 Peanuts Agnew & Smith 1989 HODGEÐIGP, SPIDERS & BIOLOGICAL CONTROL 357

Table 1.ÐContinued

%of IG predator IG prey taxon diet Habitat Source Salticidae: Phidippus audax Araneae 22.2 Wild Plants & Dean et al. 1987; Nyffeler Cotton et al. 1994 Phidippus audax Araneae 15.5 ? Young 1989 Phidippus johnsoni 27 ? Jackson 1977 various Araneae 20 ? Nentwig 1986 Amaurobiidae Coras montanus Araneae 24 Rock outcrop Hodge & Marshall 1996 Hypochilidae Hypochilus thorelli Araneae 46 Rock outcrop Hodge & Marshall 1996 Pisauridae Pisaura mirabilis Araneae 18 ? Nitzsche 1981 Pholcidae Pholcus phalangiodes Araneae 6 Cellars Nentwig 1983 Scytodidae longipes Araneae 17.4 outside buildings Nentwig 1985 Unspeci®ed Araneae Hemiptera 14.5 Peanuts Agnew & Smith 1989 Araneae 17.3 Peanuts Agnew & Smith 1989

leagues. Higher levels of IGP might have been direct effects that might cascade to herbivores reported in some cases if more speci®c taxo- and crops. nomic categories were used, for example, breaking insect orders into families which of- CONCLUSIONS ten exhibit characteristic feeding habits (e.g., How can we determine the implications of Carabidae rather than Coleoptera). Even so, it IGP for the role of spiders in agroecosystems? is not uncommon to ®nd spider diets consist- How does one begin to identify which of a ing of almost one-®fth IG prey (mean for Ta- suite of predators present in a particular crop ble 1 ϭ 18.3% Ϯ 12.7%). have the potential for IGP interactions? Clas- It is hard to form any general conclusions si®cation systems exist for spider guilds (Uetz based on the data in Table 1 since the list is et al., this volume), predator and herbivore not comprehensive, and the methodology and guilds in crops (Breene et al. 1993) and struc- intensity of data collection vary among stud- tural zones in crop plants which may support ies. The most striking feature, however, is the distinct suites of predator and prey species number of studies involving lycosids and ox- (e.g., LeSar & Unzicker 1978). Using these as yopids in agricultural systems, and the some- a starting point, one can begin to de®ne po- times high percentage of IG prey reported tential predator-predator and predator-herbi- from these spiders (e.g., 40% Araneae in the vore interactions in which IGP may be of con- diet of Oxyopes salticus). It may be that cur- sequence. Quanti®cation of the potential for sorial spiders dominate as IG predators due to IGP and/or competition should be achieved by their active hunting style (Lucas et al.1998; careful study of the relative densities, habitat Cisneros & Rosenheim 1998). It would be use, activity period and space, and diet. From quite informative to have greater taxonomic these measures one can calculate indices of resolution to the IG prey reported, to see if the opportunity for predation (IOP) and the they are represented disproportionately by less opportunity for competition (IOC), as derived mobile predators. This type of resolution by Wissinger (1992) from pre-existing indices would also suggest the types of direct and in- of resource overlap (Hurlbert 1978). Wissin- 358 THE JOURNAL OF ARACHNOLOGY ger's indices allow for comparisons of the rel- classes, generating possibilities for both can- ative strengths of predation, cannibalism, and nibalism and intraguild predation between dif- resource competition between and within spe- ferent life stages of different predator species. cies by quantifying these interactions in the Given the variety of crop systems, manage- ®eld and laboratory (Wissinger 1992). In a ment practices (e.g., tillage versus no-tillage), sense, they simply involve collecting the rel- and diverse predator and prey assemblages, evant natural history information about each agricultural systems provide models for in- species, and quantifying this information to vestigating the role of IGP from both pure and make speci®c predictions of the relative im- applied perspectives. portance of cannibalism, IGP and intra- or in- ACKNOWLEDGMENTS terspeci®c competition. This allows the design of more rigorous and meaningful ®eld exper- I would like to thank Sam Marshall for help iments (Wissinger 1992). in ®nding references and for valuable discus- Future ®eld experiments should heed les- sions of early drafts; Gary Polis and the Spi- sons from the past regarding the use of enclo- der Lab of Miami University for editorial in- sures and the duration of experiments. Stock- put; Beth Jakob and Karen Cangialosi for ing closed cages with predators may not moral support; Matt Greenstone and Keith reveal information relevant to the real world; Sunderland for organizing the symposium. and responses in the short term may lead to LITERATURE CITED very different conclusions than might be Agnew, C.W. & J.W. Smith, Jr. 1989. Ecology of reached from experiments of duration more spiders (Araneae) in a peanut agroecosystem. En- similar to the actual seasonality of the partic- viron. Entomol., 18:30±42. ular system (Wise 1993; Moran & Hurd 1994, Breene, R.G., D.A. Dean, M. Nyffeler & G.B. Ed- 1998), and should be repeated across years to wards. 1993. Biology, predation ecology, and detect the effects of temporal variability (Polis signi®cance of spiders in Texas cotton ecosys- et al. 1998). tems with a key to the species. Report B-1711, Despite the recent revival of interest in food Texas Agric. Exp. Stn., College Station, Texas. web interactions, (``top-down'' versus ``bot- Briggs, C.J. 1993. Competition among parasitoid tom-up'' effects ) and the complex nature of species on a stage structured host and its effect on host suppression. American Nat.,141:372± feeding relationships (Strong 1992; Polis 397. 1994; Polis & Strong 1996; Polis & Wine- Carter, P.E. & A.L. Rypstra. 1995. Top-down ef- miller, 1996; Holt & Polis 1997), the scenario fects in soybean agroecosystems: Spider density still generally used for biocontrol is that of a affects herbivore damage. Oikos, 72:433±439. 3-tiered system in which herbivores eat plants, Chang, Gary C. 1996. Comparison of single versus and in turn are eaten by predators. As the multiple species of generalist predators for bio- studies reviewed in this paper demonstrate, logical control. Environ. Entomol., 25:207±212. animals do not recognize these arti®cial tro- Chiverton, P.A. 1986. Predator density manipula- phic boundaries, and often feed from several tion and its effects on populations of Rhopalo- trophic levels. This can generate a complex siphum padi (Hom.: Aphididae) in spring barley. Ann. Appl. Biol., 109:49±60. array of direct and indirect effects which can Cisneros, J.J. & J.A. Rosenheim. 1997. Ontoge- have important and unexpected consequences netic change of prey preference in the generalist for the effectiveness of generalist predators as predator Zelus renardii and its in¯uence on pred- biological control agents. The paucity of ex- ator-predator interactions. Ecol. Entomol., 22: perimental research on the potential web of 399±407. IGP interactions involving spiders is surpris- Cisneros, J.J. & J.A. Rosenheim. 1998. Changes in ing since they are widely recognized as model the foraging behavior, within-plant vertical dis- organisms for the types of manipulative ®eld tribution, and microhabtat selection of a gener- studies used to investigate these interactions alist insect predator: an age analysis. Environ. (Polis 1993; Wise 1993). Other generalist Entomol., 27:949±957. Clark, M.S., J.M. Luna, N.D. Stone, & R.R. Young- predators studied to date (hemiptera, lace- man. 1994. Generalist predator consumption of wings, beetles) are similar in nature to spiders armyworm (Lepidoptera: Noctuidae) and effect in that they include animals with a both sit of predator removal on damage in no-till corn. and wait and active foraging hunting styles, Environ. Entomol., 23:617±622. and also involve animals with distinct size Dean, D.A., W.L. Sterling, M. Nyffeler, & R.G. HODGEÐIGP, SPIDERS & BIOLOGICAL CONTROL 359

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