Ecology, 84(10), 2003, pp. 2538±2548 ᭧ 2003 by the Ecological Society of America

OMNIVORY AND THE INDETERMINACY OF PREDATOR FUNCTION: CAN A KNOWLEDGE OF FORAGING BEHAVIOR HELP?

JAY A. ROSENHEIM1 AND ANDREW CORBETT Department of Entomology, University of California, Davis, California 95616 USA

Abstract. In 1960, N. G. Hairston, F. E. Smith, and L. B. Slobodkin proposed that terrestrial ecosystems are composed of three trophic levels: predators, herbivores, and plants. Under this model, predators act in a predictable manner to suppress herbivore populations, freeing plant populations from the strong effects of herbivory. However, empirical work has recently demonstrated that many predators exhibit trophic-level omnivory, consuming both herbivores and other predators. This creates a problem for terrestrial ecologists: pred- ator function is indeterminate, because predators may operate from either the third trophic level (``intermediate predators'') or the fourth trophic level (``omnivorous top predators'') and have opposite effects on herbivore and plant populations. Here we attempt to use a basic understanding of the foraging behavior of predators and their prey to make predictions about predator function. A simulation model produces four predictions: (1) actively foraging predators may be effective regulators of sedentary herbivore populations; (2) sit-and-wait predators are unlikely to suppress populations of sedentary herbivores, but may act as omnivorous top predators, suppressing populations of widely foraging intermediate pred- ators and thereby increasing herbivore densities; (3) among widely foraging predators attacking a common herbivore prey, predators that are large relative to the body size of their prey will be more mobile, and therefore more vulnerable to predation by sit-and-wait omnivores, compared to predators that are similar in size to their prey; and (4) widely foraging omnivores, unlike sit-and-wait omnivores, are unlikely to disrupt herbivore pop- ulation suppression generated by intermediate predators, and may instead enhance herbivore suppression. These predictions appear to explain the results of several experimental studies of the function of predatory arthropods in terrestrial ecosystems. Key words: biological control; food webs; foraging behavior; generalist predator; herbivore population suppression; higher order predation; indirect effects; individual-based model; intraguild predation; omnivory; trophic cascades. Special Feature INTRODUCTION as workers have reported the prevalence and impor- tance of predators that consume not only herbivores, In a paper that has proven to be controversial and but also other predators (reviewed by Polis et al. 1989, yet highly in¯uential, Hairston et al. (1960; see also Polis 1991, Rosenheim et al. 1995, Rosenheim 1998; Slobodkin et al. 1967, Hairston and Hairston 1993, this phenomenon has been variously labeled ``trophic 1997) proposed that terrestrial ecosystems are com- level omnivory,'' ``intraguild predation,'' ``higher-or- posed of three functionally discrete trophic levels: der predation,'' or ``hyperpredation''). These obser- plants, herbivores, and predators. Under this model, vations have supported new proposals for the general predators suppress populations of herbivores to low structure and function of terrestrial ecosystems that in- levels, freeing plants from the strong effects of her- corporate the possibility that predators may function bivory, and producing a world that is predominantly primarily from the third trophic level, suppressing her- ``green.'' This model of terrestrial ecosystem function bivore populations, or primarily from the fourth trophic has been criticized on several grounds, with especial level, suppressing populations of intermediate preda- attention given to the complementary in¯uences of var- tors and thereby potentially releasing herbivore pop- iable plant quality and plant defenses on herbivore pop- ulations from ``top down'' control (Hurd and Eisenberg ulation dynamics (Murdoch 1966, Polis 1999). Less 1990, Polis 1991, 1999, Wise 1993, Polis and Strong questioned until recently was the thesis that terrestrial 1996, Janssen et al. 1998, Rosenheim 1998, Halaj and predators function in a relatively predictable manner to suppress herbivore populations. Wise 2001). An important shift in our view of terrestrial ecosys- The new models create a problem for ecologists: the tems has, however, occurred over the past two decades indeterminacy of predator function. To address this problem of uncertain predator function, we need to ask: what is it that makes a predator function as a consumer Manuscript received 31 July 2002; revised 16 October 2002; accepted 1 November 2002. Corresponding Editor: A. A. Agra- of herbivores vs. a consumer of other predators? This wal. For reprints of this Special Feature, see footnote 1, p. 2521. question may not have a simple answer. Predation rates 1 E-mail: [email protected] are shaped by many factors, including encounter prob- 2538 October 2003 WHY OMNIVORY? 2539 abilities, attack probabilities, capture success, and con- sumption probabilities, and each of these factors may in turn be in¯uenced by traits of the predator, the prey, and their shared environment (Sih 1993). Researchers exploring predator±predator interactions have indeed demonstrated important roles for habitat structure and physical refuges (MacRae and Croft 1996, Agrawal and Karban 1997, Roda et al. 2000, Norton et al. 2001, Finke and Denno 2002), active prey defenses (Lucas et al. 1998, Snyder and Ives 2001), and predator pref- erences (Colfer and Rosenheim 2001). Many omniv- orous predators are, however, also extreme generalists, consuming any prey that they can capture. For such predators, encounter frequencies with different prey FIG. 1. Trophic web of the arthropod community repre- species often become the overriding in¯uence on diet. sented in the simulation model. For this reason, we focus here on determinants of en- counter frequency between predators and prey. Encounter probabilities between predators and prey are heavily in¯uenced by their foraging behaviors. senting each individual in the population (DeAngelis Pianka (1966) introduced one of the most basic de- and Gross 1992, Judson 1994). The dynamics of the scriptors of predator foraging mode when he described simulated populations and community can then be de- the difference between widely foraging predators and rived as emergent properties from rules given to in- sit-and-wait predators. Although these two strategies dividuals governing their movement, feeding, repro- are probably best viewed as the ends of a continuum duction, and mortality. The individual-based modeling of foraging strategies (Perry 1999), both verbal models approach is intended to re¯ect more faithfully the phys- Feature Special (Turnbull 1973, Huey and Pianka 1981) and mathe- ical reality of the system, and the behavioral rules given matical treatments (Gerritsen and Strickler 1977) pre- to individuals are attempts to simulate actual behav- dict that predator foraging mode shapes the types of ioral traits and variability in those traits. prey that are encountered and potentially consumed. The model that we developed was designed to rep- Sedentary prey are consumed by widely foraging ``in- resent herbivorous and predatory arthropods foraging termediate'' predators, which may in turn be captured on a plant surface. We attempted to ground our model by sit-and-wait ``top'' predators; thus ``crossovers'' in in the real world by choosing parameter values that foraging mode occur as one ascends the food chain. re¯ected, at least loosely, the community of predators Mobile prey, in contrast, may be consumed by either associated with the herbivorous mite Tetranychus cin- widely foraging or sit-and-wait predators. These ideas nabarinus feeding on the foliage of papaya, Carica have found widespread acceptance among ecologists papayae (J. A. Rosenheim, D. D. Limburg, R. G. Col- studying diverse taxa (reviewed by Perry and Pianka fer, V. Fournier, T. Glik, R. Goeriz, C. L. Hsu, T. E. 1997), including predatory arthropods (e.g., Turnbull Leonardo, E. H. Nelson, and B. RaÈmert, unpublished 1973, Polis and McCormick 1987, Johansson 1993). manuscript). The arthropod community on papaya was In this study, we apply the theory of crossovers in useful as a case study because it presented natural con- foraging mode to understand the ecological roles of trasts in foraging style (widely foraging vs. sit-and- omnivorous predators, including their in¯uence on the wait predators) and strong variation in the relative body population dynamics of terrestrial herbivorous arthro- sizes of predator and prey. The model is general pods. Using a simulation model, we extend the theory enough, however, that it should allow us to explore to include the in¯uence of the relative body sizes of predator±prey systems more broadly. predators and prey. Our simulations produce simple, The model community.ÐWe simulated a community testable predictions for omnivore function that link for- (Fig. 1) comprising an herbivore; an intermediate pred- aging behavior with population dynamics and com- ator, which feeds only on the herbivore; and an om- munity structure. nivorous predator, which can feed on either the her- bivore or the intermediate predator. For the papaya case METHODS study, the herbivore was Tetranychus, a sedentary her- bivore that creates small, silk-lined colonies on papaya The simulation model leaves; two species were present as intermediate pred- We employed a stochastic individual-based model to ators, both of which are widely foraging specialist con- explore the link between the foraging behavior of om- sumers of spider mites, Stethorus siphonulus (Cole- nivorous predators and their trophic function. An in- optera: Coccinellidae) and Phytoseiulus macropilis dividual-based model is distinguished from a popula- (Acari: Phytoseiidae); and the omnivorous predator tion-state model by explicitly and separately repre- was the tangle-web spider Nesticodes ru®pes (Araneae: Special Feature ucin sasrc i-n-atpredator. sit-and-wait thus strict and a web as its functions with prey detects which Theridiidae), predator Omnivorous predator Intermediate Herbivore 2540 fteeg fteds secutrd hnteindi- the then encountered, is around. disk turns simply the prey. vidual of animal for edge forage the they If which on their surface at neu- ¯at a resources tral, as disk food the experience obtain Predators location. always surface, current leaf can a they as that papaya disk in a the a of experience size with Herbivores the leaf. approximately surface cm, circular 30 of two-dimensional, diameter a disk: ple .Gi,R orz .L s,T .Load,E H. E. Leonardo, E. T. Hsu, Ra L. B. and C. Nelson, Fournier, Goeriz, V. Colfer, R. G. Glik, R. T. Limburg, A. D. match J. h D. see to 280 experiments; Rosenheim, chose manipulative the our we than of (which duration longer the simulation much the cycle of life duration a has and ator ethrioefeigrt xlctylnsormodel our links explicitly rate density-depen- feeding This herbivore mean. dent the standard about a 10% randomly having of distribution was deviation normal individual a an from by sampled realized actual The rate zero. becomes feeding rate feeding the time which at tn nestesz ftepplto xed h car- ( the universe exceeds the for population capacity the rying of con- size is rate the feeding unless mean stant The are re- feed. they herbivores, can whenever they For substrate; stationary the birth. in of present moment are sources the at parent its ABLE hiewsaporaefrteppy aesuy be- this study, reproduce; case papaya spider or the the cause for move appropriate not was choice did om- the that predator assumed we nivorous simulations, of sets possible, the three for as ®rst First, simple assumptions. simplifying as several made model we our of interpretation the yeo individual of Type niiulsat iewt h ae( same the An with reproduction. by life of starts decreased cost individual given the is represents pool a that the exceeds amount and an pool occurs birth the a When threshold, feeding. by mented birth. of adults moment be to their considered from are individuals structure all age model; or the represent in immigration not did no we with Finally, community, uni- emigration. closed model a the mortality as treated of we verse Third, sources predation. excluded than we other community, members to all the predator for of Second, top reproduce. omnivorous and the widely forage allowed simulations, of we set which last in the for relaxed was assumption otlt,rpouto,adresources and reproduction, Mortality, universe model The T l niiul oss eorepo hti aug- is that pool resource a possess individuals All .Bsln e fprmtrvle sdi h iuainmodel. simulation the in used values parameter of set Baseline 1. Nesticodes Èmert, rsuc units) (resource Ðh oe nvrei sim- a is universe model .ÐThe reproduction nulse manuscript unpublished otof Cost 1000 sasrc i-n-atpred- sit-and-wait strict a is ´´´ 40 N A .RSNEMADADE CORBETT ANDREW AND ROSENHEIM A. JAY ϭ x,y 00individuals), 1000 Walking (cm/h) oriae as coordinates ) speed 10 0.5 0 Ðomake .ÐTo .This ). 0.5 0 5 xesv search Extensive en1 Mean iydpnec,i hc h edn aedcie by (1 declines of rate factor feeding a den- the which herbivore in of also dependence, form we sity complicated results, more our a skew evaluated not herbivore for did function step dependence simple density a en- of To use our dynamics. that population sure or performance predictions make plant to for model we our however, extend to level; attempt trophic not did producer primary the with 0.125 1.25 0 oelnt (cm) length Move oeeti admycoe rmauiomdistri- of uniform angle a (0±360 from The bution chosen sequence. be- randomly the is movement at movement each chosen randomly of the are ginning and pause of displacement, the angle the of the duration of pause; distance a the by of movement, followed series displacement straight- a a line of of consisting consists each an sequences,'' lifetime of ``movement its trajectory The during pauses. individual by punctuated ran- walk a dom executing by move individuals search''), tensive e sdpneto h niiulssed hc is which speed, type. individual's its the by on determined cho- distance dependent the is traverse sen to required intervals time of number The 1). (Table intermediate predator herbivore, omnivorous e.g., or deviation predator, individual, standard of type and the mean for normal a constant from of chosen randomly distribution are pause the of ration eaieyhg pe.Tedrcino oeetfor movement of direction The speed. high relatively ilcnuetecoetidvda,rgrls of predator.predators: intermediate regardless an or individual, herbivore an closest is and it discovery the whether of area consume its will within herbivores and ators pred- intermediate-level om- both An detects area. will predator the it nivorous within discovery; herbivore of closest area the its consume in are that An herbivores location. prey only potential current as their detect will on predator intermediate-level centered radius circle a ®xed as de®ned of discovery'' of ``area an possess ators yacntn ersnigtefo au fteprey. the of value food the augmented representing is constant predator a the by of con- pool is resource prey the a sumed, When individuals. other consume and ter function step the here. using reported the are results with function; generated those step to simpler similar very pro- results function duced complicated more this using Simulations rdtrfrgn ue n encounters and rules foraging Predator Movement eipeetdtrefrgn oe o mobile 1) for modes foraging three implemented We rdtr cur eore nywe hyencoun- they when only resources acquire Predators SD xesv search Extensive Ðihoeecpinntdblw(``In- below noted exception one .ÐWith 0.2 ´´´ ´´´ nesv search Intensive en1 Mean Њ Ϫ .Tedsac ftemv n h du- the and move the of distance The ). pplto iecryn capacity] size/carrying [population 0.05 ´´´ ´´´ h rdtri akn ta at walking is predator The . SD clg,Vl 4 o 10 No. 84, Vol. Ecology, 10 ´´´ 0 as uain(h) duration Pause en1 Mean Ðl pred- .ÐAll 2.5 0 ´´´ SD 2 ). October 2003 WHY OMNIVORY? 2541

TABLE 1. Extended. orous predator population, the intermediate-level pred- ator population, then the herbivore population. Next, all predatory interactions are resolved, with omnivo- Feeding rate Area of Value as food (resource discovery (resource Handling rous predators feeding before intermediate predators. units/h) radius (cm) units) time (h) Since there is only one direction of predation in any 5 ´´´ 10 ´´´ one interaction, no unintended advantage is afforded ´´´ 0.5 50 0.1 the omnivorous predator by virtue of its ``going ®rst.'' ´´´ 2 ´´´ 0.25 Time intervals between updates are short relative to the walking speed and area-of-discovery of predators; thus, predators are, in effect, continuously checking a new movement sequence is chosen from a 360Њ range, their area of discovery for potential prey as they forage. i.e., the predator executes a pure random walk. A pred- The simulation is initialized at time 0 with 10 her- ator shifts from extensive search into handling mode bivores. After allowing the herbivores 25 h to feed and upon encountering a prey. initiate small ``colonies'' on the leaf surface, predators 2) Handling. The predator is handling (e.g., ingesting (N ϭ 4, with a single exception noted in the Results or digesting) a prey item. The predator remains sta- section) are added to the system. These predators are tionary and does not consume other prey within its area initialized by assigning (x,y) coordinates randomly of discovery. A predator shifts from handling into in- throughout the universe. Predators are initialized with tensive search mode upon completion of a ®xed han- a single unit of resources in their resource pool. In- dling time. dividuals immediately initiate a movement sequence; 3) Intensive search. The predator is walking at a thus angle of movement, movement distance, and pause relatively low speed and engages in a correlated ran- duration are randomized at initialization. dom walk (Kareiva and Shigesada 1983), where the The model was compiled with Microsoft Visual angle of movement is chosen from a normal distribu-

Cϩϩ (Microsoft, Redmond, Washington, USA). Pseu- Feature Special tion with mean equal to the current angle of movement do-random numbers were generated using the ``RAN0'' and standard deviation of 28.6Њ (0.5 radians). This for- routine and normal deviates were generated using the aging mode is designed to represent the local search ``GASDEV'' routine in Press et al. (1988). A copy of that widely foraging predators often express once with- the programming code is available upon request from in a patch of prey (Bell 1991). A predator shifts from JAR. intensive search mode into extensive search mode once Simulations.ÐWe report here four sets of simula- 0.1 h of search time has passed without encountering tions, which examined (1) the in¯uence of intermediate a prey. predator mobility in the presence of a sedentary her- Intermediate predator body size.ÐTo represent pred- bivore population and a sit-and-wait omnivore, (2) the ators of varying body sizes attacking a common prey, in¯uence of herbivore mobility in the presence of a we varied the prey handing time and the cost of re- production. Handling time re¯ects body size because mobile intermediate predator and a sit-and-wait om- larger predators can consume and digest more individ- nivore, (3) the in¯uence of the body size of a widely uals of a given prey per unit time than can smaller foraging intermediate predator in the presence of a sed- predators, largely because their larger gut contents entary herbivore and a sit-and-wait omnivore, and (4) mean that many prey can be digested simultaneously. the in¯uence of the body size of a widely foraging The cost of reproduction re¯ects body size, because intermediate predator in the presence of a widely for- larger predators must consume more prey to produce aging omnivore and either a sedentary or a mobile her- a copy of themselves than do smaller predators. Han- bivore. For each set of simulations, we applied four dling time and the cost of reproduction were varied in ``treatments'': (1) herbivores alone, (2) herbivores plus concert so that the reproductive rate of a food-satiated the intermediate predator, (3) herbivores plus the om- intermediate predator was held constant. Although nivorous predator, and (4) herbivores plus both the in- body size may also be associated with other trait dif- termediate and omnivorous predators. All simulations ferences (e.g., walking speed, or the area of discovery were run for 280 h, with 75 iterations per hour, and radius), we held all other parameters constant for pred- were replicated 10 times for each parameter set (see ators of different sizes to isolate what we consider to Table 1). We report the mean herbivore density over be the most essential features of larger predators, name- the 280-h simulation as our primary index of herbivore ly that they must eat more prey to reproduce, and they population dynamics. Thus, our focus is on short-term process individual prey more quickly. population suppression, rather than equilibrium den- Implementing the model.ÐA simulation update oc- sities or the stability properties of the community. Al- curs in two phases. First, each individual engages in though it is useful to understand equilibrium dynamics all activities other than predation; these include, in or- (e.g., Holt and Polis 1997), transient dynamics are also der, reproduction, feeding by herbivores, and move- important (Hastings 2001), and are particularly relevant ment. Populations are updated as a group; the omniv- to predator±predator interactions in arthropod com- Special Feature eg,Sye n vs2003). Ives disturbed and or Snyder seasonal (e.g., highly often are which munities, 2542 iy opiigtehrioe h nemdaepred- intermediate commu- the herbivore, three-species the a comprising simulate population. nity, prey we as sedentary if function a Furthermore, of to regulator unlikely effective is result an predator the sit-and-wait reiterates population a simply that This minimal 2). the obtain (Fig. of suppression predator we only herbivore, the as sedentary present omnivore community a the dy- simulate with we the When on system? have this of mode namics foraging sit-and-wait a ploying 1996). Bellows and Driesche (Van predators her- arthropods targeting bivorous for programs control trait biological appreciated in employed universally ability a searching the been Indeed, therefore has negligible. and is other, rate prob- each predation high encountering a have of not im- do ability They two space. essentially in are objects herbivore mobile pred- sedentary sit-and-wait a a and result; effectively, intuitive (Fig. ator highly cannot a population is predator This ambush 2). prey sit-and-wait a sedentary whereas a can predator suppress intermediate foraging in- widely predator±prey a of teractions: model verbal (1981) Pianka's (1977) and Huey Strickler's and frequencies and encounter of model Gerritsen most mathematical of the predictions supported simulations basic Our have foraging predators pauses). (widely sit-and-wait lengthy pauses; bouts no of have duration movement predators varied the and between adjusting 1, by pauses Table mode in foraging shown parameters predator of the used set We base densities. of herbivore ability suppress the to for predators mode foraging con- predator the of explored sequences and population, herbivore sedentary sedentary. highly case be our in still mites may spider study, the Many like bearers). feeders, external case for the of and opportunity feeders signi®cant (external any movement with groups leaving two feeders), root only borers, gallers, soil, miners, leaf or bers, plant (rollers/web- high movement host for involve opportunities the minimal ®ve with within which concealment of of herbivores, degrees by styles rela- feed- ing be seven a identi®ed can (1994) of Hawkins sedentary. herbivores demands tively many nutritional pool arthropod, the large to developing a relative represents resources often because of plant style that host is life individual observation key an parasite-like ®rst Our a host 1980). (Price one adopting on individual, development immature plant re- entire com- food often their key herbivores plete Indeed, their plant. host on their right source: live her- arthropods Many herbivore. bivorous focal the considering of behavior by foraging begin the we associ- predators, their of community and ated arthropods terrestrial herbivorous to hti¯ec osa mioospeao em- predator omnivorous an does in¯uence What a on focused therefore simulations of set ®rst Our mode foraging in crossovers of notion the apply To R SLSAND ESULTS D ISCUSSION A .RSNEMADADE CORBETT ANDREW AND ROSENHEIM A. JAY nay o2 m(ihymbl) ieyforaging of widely suppression A strong (sed- produced mobile). cm predator (highly 0.5 intermediate cm from hour 20 distance the to the of entary) varied course the and be- over bouts, period moved movement feeding 0.5-h 1-h a tween herbivore set the parameter assigning base by the modi®ed We pred- our system. of ator±prey in¯u- dynamics the the on mobility We explore herbivore of sites. to ence oviposition simulations when suitable performed stage, out therefore adult seek winged must mobile, females more much may stages a immature have their during sedentary highly that Singer herbivores are 2001, even Furthermore, Suttle 2001). and Stireman Schmitz and species 1994, plant al. many et of in- (Howard diets plant mixing different even from and meals dividuals small feed taking grasshoppers grazers, and as caterpillars mobile. some quite it are instance, animals, herbivores For some of that class true certainly sedentary is generally a as thropods releasing control. level, top-down trophic strong from fourth population omni- herbivore the the the from foraging case, acting this widely is In vore the 2). by (Fig. predator generated intermediate is herbivore that the of population om- suppression the strong that the see disrupts we nivore predator, omnivorous the and ator, muhpeao) ausaemean t are Values foraging) predator). (widely ambush 0 was which from predator, intermediate varied the of duration of pause except points the used for were as 1) (Table shown parameters baseline are The reference. only'') pred- (``No omnivorous predator the predators (``Omnivorous only of of ator presence absence population. the in the herbivore and in predators'') sedentary densities a herbivore of Mean regulator a as ef®cacy lhuhi a eueu ove ebvru ar- herbivorous view to useful be may it Although ie20h nsm ae,errbr ( to bars 0 error time cases, some from in runs h; simulation 280 replicate time 10 across bivores ob shown. be to F IG .I¯ec fitreit rdtrmblt nits on mobility predator intermediate of In¯uence 2. . hgl sedentary (highly h 2 o clg,Vl 4 o 10 No. 84, Vol. Ecology, Ϯ Ϯ 1 1 SE SE est fher- of density r o small too are ) October 2003 WHY OMNIVORY? 2543

like the beetle Stethorus, which are large relative to the size of their prey (spider mites), must consume many prey to develop and reproduce successfully, and thus must move large distances through their foraging en- vironment to harvest many prey. In contrast, a predator like the mite Phytoseiulus, which is similar in size to its prey, may be satiated for lengthy periods after con- suming just one or a few prey individuals. We may expect, then, that movement requirements will be more modest. This does not mean that a small predator like Phytoseiulus cannot be highly mobile; instead, our sug- gestion is that small predators may not need to use their mobility very often, because their prey needs are smaller. We used our simulation model to explore the role of body size of the intermediate predator. We represented larger predators by giving them shorter handling times (e.g., Stethorus has a handling time of ϳ0.13 h), where- as smaller predators were given longer handling times FIG. 3. In¯uence of herbivore mobility on herbivore pop- ulation suppression by predators. Curves are shown for the (e.g., Phytoseiulus has a handling time of ϳ4h;J.A. individual and combined abilities of a widely foraging inter- Rosenheim, D. D. Limburg, R. G. Colfer, V. Fournier, mediate predator and a sit-and-wait omnivorous top predator T. Glik, R. Goeriz, C. L. Hsu, T. E. Leonardo, E. H. to suppress the herbivore's population density. The baseline Nelson, and B. RaÈmert, unpublished manuscript). We parameters (Table 1) were used for the predators; herbivore varied the cost of reproduction in concert with the prey

parameters were baseline, with the following modi®cations: Feature Special walking speed, 0.5±20 cm/h; move length, 0.5±20 cm (1 SD, handling time to hold the reproductive rate of a food- 0.125±5 cm); pause duration, 0.5 h (1 SD ϭ 0.125 h). Values satiated intermediate predator constant (all food-sati- are mean Ϯ 1 SE density of herbivores across 10 replicate ated intermediate predators could produce one off- simulation runs from time 0 to time 280 h; in some cases, spring after 10 h). We emphasize that we did not vary error bars (Ϯ1 SE) are too small to be shown. any of the parameters that directly control movement (e.g., walking speed, move lengths, pause durations, the herbivore population for all values of herbivore etc.); rather, we used the simulation model to explore mobility (Fig. 3). The sit-and-wait omnivore, on the the possibility that mobility would vary as an emergent other hand, was only effective as a regulator of highly property of predator body size through prey handling mobile herbivores, a result again consistent with the times. model of crossovers in foraging mode between predator The simulations showed that predator body size has and prey. Although the combined effects of the inter- a major in¯uence on community dynamics. Larger mediate predator and the omnivore produced strong predators, which have shorter prey handling times, did suppression of highly mobile herbivores, relatively indeed move more than smaller predators (Fig. 4A). sedentary herbivore populations were poorly regulated, This movement translated into an enhanced risk of pre- reaching densities close to those seen in the absence dation by the sit-and-wait omnivorous predator: the of any predators (Fig. 3). intermediate predators were very strongly over-repre- Is there, then, no way in which a sedentary herbivore sented in the diet of the omnivore relative to herbivore population can be regulated by intermediate predators prey (Fig. 4B). In the absence of the omnivore, the in the face of a potentially disruptive sit-and-wait om- widely foraging intermediate predator was highly ef- nivore? The papaya case study suggests a possible an- fective as a suppressor of the herbivore population swer to this question. For widely foraging intermediate across the full range of handling times (Fig. 4C). Thus, predators, and indeed for virtually all foraging animals, large and small widely foraging predators have similar a key determinant of exposure to predation risk is the basic potentials to suppress sedentary herbivore pop- amount of movement (Werner and Anholt 1993, Anholt ulations. However, herbivore suppression by the larger, and Werner 1995, Lima 1998). Movement produces more mobile intermediate predators was strongly dis- opportunities for encounters with sedentary predators, rupted by the omnivorous predator, whereas the small- and also enhances the likelihood of detection by con- er, less mobile intermediate predator continued to pro- sumers that use visual, vibratory, or auditory cues pro- duce substantial levels of herbivore suppression even duced by movement to detect prey (Foelix 1982, Skelly when the omnivore was present. Thus, the predictions 1994, MeyhoÈfer and Casas 1999, Eubanks and Denno of the crossovers model can be signi®cantly altered by 2000). A primary determinant of the movement re- body size effects. quirements of widely foraging predators is their body Small-bodied intermediate predators may generate size relative to the body size of their prey. Predators control of herbivore populations that is robust to the Special Feature t 2544 tri h ito h mioospeao dt hw are shown (data predator omnivorous the from of means diet the pred- in intermediate the ator of Over-representation (B) decline). to rdtr rdtr ihbd ie uhlre hntheir than larger much top sizes omnivorous (e.g., body prey sit-and-wait with an a herbivore, Predators an predator. and of predator, community a intermediate in interactions on predator fol h mioospeao `Onvru predator (``Omnivorous predator presence omnivorous the the in and only predators'') the (``No of dif- in predators of densities of presence Herbivore absence the predators. pred- in of intermediate combinations densities were ferent herbivore that Mean leaf (C) the ators). on prey made present potential diet all arthropods omnivore's of predators)/(proportion of intermediate (proportion of up as calculated was This ryadonvru rdtr;dt hw r en from means are shown data predators; with leaves omnivorous on and foraging prey predators intermediate (A) for per alive reproduction. displacement (mean hour of predator repro- intermediate rate of the main- possible of cost to Mobility maximum the 2000 constant and to a h, 25 from 4 tain varied to simultaneously 0.05 was from duction varied hand- prey was the time that except ing used were 1) (Table parameters line rdtr hs oyszsaesmlrt hto hi prey their of that to similar are (e.g., sizes body whose predators ϭ F IG ni h ebvr ouaindniypae n began and peaked density population herbivore the until 0 Phytoseiulus .I¯ec fpe adigtm fteintermediate the of time handling prey of In¯uence 4. . Stethorus t ϭ ni h ebvr ouainpeaked). population herbivore the until 0 aeln ryhnln ie.Tebase- The times. handling prey long have ) aesotpe adigtms whereas times, handling prey short have ) A .RSNEMADADE CORBETT ANDREW AND ROSENHEIM A. JAY Ϯ 4.04 only ate time example, handling For 4-h Ϯ prey. a of with predators number small small relatively a eating only population the of member large each up with building populations, by predators omnivorous of presence ny' r hw spit frfrne ausaemeans SE are Values reference. of points as Ϯ shown are only'') ← iayo mioospeao ucin u model Our function. predator omnivorous of minacy trigpplto ffu niiul n averaged and individuals 1.4 four only of population starting mioei de otesystem. the to foraging added widely is to a omnivore when populations control herbivore top-down intermediate expect from vs. escape not (herbivore do type we prefer- prey predator), no either expresses when for omnivore population ence the herbivore and singly the similar present suppress have to omnivore the the abilities which and in predator here, explored intermediate wide scenario simple a least the across at under Thus, sizes. observed body mobile predator is intermediate and of and range 5A) This 5B), (Fig. 5). (Fig. sedentary herbivores (Fig. both for predator combi- holds intermediate in result present the when with intermediate suppression nation somewhat of the a level or similar greater by a produces instead popu- generated but herbivore predator, the suppression disrupts longer lation no simulations: omnivore earlier the the in explored sit- omnivore the from and-wait differently very functions omnivore aging f00 ,ec rdtrcnue naeaeo 194 of average an time consumed handling predator prey each we a h, when 0.05 with of example, predator they large For that a reproduce. predators simulated to omnivorous survive of so hands rarely predation ®nd intense the to such at to required risks them is per expose may prey that prey more movement many many the consume but larger- to capita, able is be that may predator bodied intermediate An simulation). usfo ie0t ie20h nsm ae,errbr ( bars error cases, some in h; 280 time to 0 time from runs in h ouaino hs agrbde predators larger-bodied suppress these to unable of was population consump- the prey capita tion, per large the Despite simulation. fteohrseils pdrmt predator, mite spider specialist other the of eeoe ag ouain ma ouainsz of size population 614 (mean populations large developed inbcueoeo h `pcait'sie iepred- mite spider ``specialist'' the ators, ques- of this one of because consideration tion a The motivates foraging? system widely papaya are and predator predator top intermediate omnivorous the the both if expect we do sion predator. omnivorous an of presence lus r o ml ob shown. be to small too are ) u td sa tep ogapewt h indeter- the with grapple to attempt an is study Our 1 0pe,btpeao ouain elndfo the from declined populations predator but prey, 10 .3(mean 0.03 h iuainmdlsget htawdl for- widely a that suggests model simulation The . ial,wa ee fhrioepplto suppres- population herbivore of level what Finally, SE Ϯ Stethorus est fhrioe cos1 elct simulation replicate 10 across herbivores of density 1idvdasoe h oreo h 280-h the of course the over individuals 11 Ϯ .6idvdasoe h oreo the of course the over individuals 0.16 Ϯ G loet h gsadmtl stages motile and eggs the eats also , 1 ENERAL SE ryprcpt naeae but average, on capita per prey ) Tetranychus D ISCUSSION clg,Vl 4 o 10 No. 84, Vol. Ecology, ouain nthe in populations Phytoseiu- Ϯ 1 October 2003 WHY OMNIVORY? 2545

predators. Sit-and-wait predators, in contrast, are un- likely to act in this way. Instead, sit-and-wait predators are predicted to consume a diet that includes not only herbivores but also a heavy over-representation of widely foraging intermediate predators. Sit-and-wait predators are therefore predicted to function as omniv- orous top predators, acting from the fourth trophic lev- el. All of these results are straightforward applications of the long-established model of crossovers in foraging mode to arthropod predator±prey dynamics; it is per- haps surprising that similar predictions have not, to our knowledge, been discussed previously in the literature. Our results also suggest that the relative body sizes of predator and prey can modify the predictions of the crossover model. Smaller predators, even if they are widely foraging, have reduced prey consumption ca- pacities, and therefore have less need to travel to har- vest prey. Thus, they may incur a smaller risk of en- countering a sit-and-wait predator or being detected by a motion-sensitive predator. As a result, our model pre- dicts that the omnivore's impact will be ameliorated, and the system as a whole will be more likely to exhibit three-trophic-level dynamics. Finally, our model suggests that a consideration of encounter frequencies alone will probably be inade- Feature Special quate for predicting predator function in communities dominated by mobile herbivores (e.g., Moran and Hurd 1998, Schmitz and Suttle 2001). For these communities we will need to understand more about predator pref- FIG. 5. In¯uence of prey handling time of the intermediate predator on interactions in a community of a widely foraging erences and prey defenses to address the question of intermediate predator, a widely foraging omnivorous top predator function. predator, and either (A) a sedentary herbivore or (B) a mobile herbivore. Intermediate predators with body sizes much larger Experimental evidence than their prey have short prey handling times, whereas pred- The crossovers in foraging mode across four trophic ators whose body sizes are similar to that of their prey have long prey handling times. The baseline parameters (Table 1) levels predicted by our model have been observed in were used with the following modi®cations: for both (A) and several terrestrial arthropod communities (Jaffee et al. (B), the intermediate predator's handling time was varied 1996, Strong et al. 1996, Gastreich 1999, Snyder and from 0.05 to 4 h, and the cost of reproduction simultaneously Wise 2001, Finke and Denno 2002). Indeed, part of varied from 25 to 2000 to maintain a constant maximum possible rate of reproduction; the widely foraging omnivore our motivation for building a model linking predator was given the same parameters as the baseline widely for- foraging behavior with predator±prey dynamics was to aging intermediate predator (Table 1), but it could prey upon create a tool to help us understand the results of our either the herbivore or the intermediate predator. For (B) the earlier work on the aphid, Aphis gossypii (Rosenheim herbivore had a walking speed of 10 cm/h, a mean move et al. 1993, 1999, Cisneros and Rosenheim 1997, Ro- length of 5 cm (1 SD ϭ 1.25 cm), a pause duration of1h(1 SD ϭ 0.25 h), and simulations were initiated with only a single senheim 2001). Field experimentation showed that this intermediate predator and a single omnivorous predator. Mean highly sedentary aphid could be suppressed to very low herbivore densities in the absence of predators (``No preda- densities by a guild of widely foraging predatory lace- tors'') and in the presence of only the omnivorous predator wings (family Chrysopidae), but that this control was (``Omnivorous predator only'') are shown as points of ref- not observed in nature because lacewings were sup- erence. Values are means Ϯ 1 SE density of herbivores across 10 replicate simulation runs from time 0 to time 280 h; in pressed by another guild of omnivorous top predators some cases, error bars (Ϯ1 SE) are too small to be shown. (Order Hemiptera), several of which use visual cues associated with movement to identify prey. The empirical literature also supports the prediction suggests that in terrestrial ecosystems dominated by that widely foraging omnivorous predators are unlikely sedentary herbivores, predator foraging mode can pro- to disrupt herbivore population suppression generated vide useful insights into predator function. Widely for- by a widely foraging intermediate predator, and may aging predators are predicted to have the potential to instead enhance herbivore suppression. Excluding act as effective regulators of herbivore populations, those widely foraging omnivores that use cues asso- even when they also act as omnivores, consuming other ciated with prey movement to detect prey (e.g., praying Special Feature CotadMca 92 byk ta.19,Lucas al., 1998, et al. Colfer 2002; et Alomar Obrycki and 1992, MacRae system and predator±prey existing (Croft foraging an to widely added a is when omnivore enhanced or unchanged most often is suppression dem- population have herbivore that studies onstrated experimental spiders), and mantids 2546 rdtrbcuei a 1 lmnt oeta com- another potential be a consume eliminate may (1) to may it it predator that because predator suggested one (1989) for al. advantageous et Polis in- For func- explanation stance, omnivory. with, trophic-level Our for compete explanations foraging than species. tional the rather interacting of complement, outcome the should of direct type of a this modes be that may suggested have omnivory We an- predator. consumes a predator other trophic- a proposed when of namely have expression omnivory, we level one study, for this explanation In proximate expression. consequences its functional of or be- ``ultimate'' the the for and basis havior mechanistic considering or by ``proximate'' obtained the be both can trait behavioral a of ing rsinof pression clgclrlso mioospredators. the omnivorous resolving of on work roles additional ecological for point starting a be n-atpredator and-wait bet h irpieefcsof effects disruptive the to able belvl fsie iesuppression. mite spider of levels able .Gi,R orz .L s,T .Load,E H. E. Leonardo, E. T. Hsu, Ra L. B. and C. Nelson, Fournier, Goeriz, V. Colfer, R. G. Glik, A. R. T. Limburg, (J. D. community D. arthropod Rosenheim, papaya the in imentation ayprleswt h aaacmuiy(ofret (Colfer has community otherwise papaya al., the that with system parallels deci- another many was in insensitive predators relatively top rejected omnivorous be sively of will impacts prey the their to to size systems. sim- are in many that predators ilar of that dynamics prediction the the example, For explain to cer- fail almost tainly will defenses active prey ignores and preferences ex- and predator that frequencies model encounter a only that model. amines however, our emphasize, for to support initial wish We some is there Thus, tem. rsineetdb h mle-oidpredator, smaller-bodied the by exerted sup- mite pression spider whereas dynamics, four-trophic-level is,tewdl oaigpredators supported. foraging was widely model the the First, from predictions main the of os hr,sie iesprsineetdb h larg- the predator, by er-bodied exerted preda- suppression foraging mite spider widely Third, the tors. of both consume however, n ieyfrgn omnivore, foraging add- widely by a enhanced slightly ing was rather but disrupted, not rxmt n liaeepaain o omnivory for explanations ultimate and Proximate pdrmt upeso rdcdby produced suppression Finally, mite spider dynamics. three-trophic-level robust yielding toseiulus toseiulus ibre 16)sgetdta ihrunderstand- richer a that suggested (1963) Tinbergen etse u oe' rdcin ih®l exper- ®eld with predictions model's our tested We npress in a eaieyisniieto insensitive relatively was , eebt aal fgnrtn togsup- strong generating of capable both were .W oe oee,ta u oe will model our that however, hope, We ). Tetranychus Èmert, Nesticodes Stethorus nulse manuscript unpublished ouain.Scn,tesit- the Second, populations. a on ob vulner- be to found was , ee rdcddetect- produced never A .RSNEMADADE CORBETT ANDREW AND ROSENHEIM A. JAY Nesticodes npress in Stethorus Stethorus Phytoseiulus Nesticodes ). otesys- the to , producing , Nesticodes and .Each ). Phy- Phy- did, was , hl lmntn oeta opttr rpredators. or nitrogen, competitors in potential enriched was eliminating prey part that while diet in with a to favored associated led selectively they cues because been of have may use movement the foraging and sit-and-wait that strategies possible exclusive. is it mutually contrary, her- not the typical On are typical a hypotheses a is These that than chain, meal bivore. higher-quality food a the is up predator moves in- one be- tissues as arthropod and crease in limited, concentrations nitrogen nitrogen often cause are growth reproduction arthropod because and that argued Fa- have and (2003) Denno gan Similarly, [2003]). Bernays also and their (see Singer or predation'') them intraguild (``reciprocal attack progeny subsequently could in- that an eliminate dividual (2) or predation'') (``intraguild petitor inrs .J,adJ .Rsnem 97 Ontogenetic 1997. Rosenheim. A. J. and J., Hall, J. and Chapman Cisneros, behaviour. Searching 1991. J. W. Bell, between Interaction 1995. Werner. mediate E. Domatia E. and 1997. R., B. Karban. Anholt, R. and A., A. Agrawal, rga/SA(rns9-50-86ad2001-35302- Grants Competitive and NRI 96-35302-3816 the 10955). by manuscript. (grants supported the Program/USDA was on work suggestions This constructive for reviewers ofr .G,J .Rsnem .D ofe,adC L. C. and Godfrey, D. L. Rosenheim, A. J. G., R. Colfer, im- on Predation 2001. Rosenheim. A. J. and G., R. Colfer, rf,B . n .V aRe 92 essec of Persistence 1992. MacRae. V. I. and A., B. Croft, en,R . n .F aa.20.Mgtntoe limi- nitrogen Might 2003. Fagan. F. W. and F., R. Denno, Individual- 1992. Gross,editors. J. L. and L., D. DeAngelis, atec,K .19.Tatmdae nietefcso a of effects indirect Trait-mediated 1999. R. University Harvard K. spiders. Gastreich, of Biology 1982. F. predation R. Intraguild Foelix, 2002. Denno. F. R. and L., D. Finke, fast vs. food Health 2000. Denno. F. R. and D., M. Eubanks, hneo rypeeec nagnrls predator, generalist a in preference prey of change UK. London, Ecology behavior. adap- by tive mediated mortality predation and availability food Nature mutualism. plant±arthropod etakE .Mno,A .Zn,adtoanonymous two and Zink, G. A. Mondor, B. E. thank We rdtritrcin.Eooia Entomology Ecological interactions. predator Hsu. population aphid of in¯uence Oecologia its suppression. and parasitoids mature rdtr.EvrnetlEntomology. Environmental generalist predators. naturally-occurring and mites predaceous leased a Entomology tal ainpooeonvr mn anvru arthropods? carnivorous among Ecology omnivory promote tation New Hall, populations, USA. and York, ecology: Chapman New York, in ecosystems. approaches and and communities, models based hrdi pdro natpatmtaim Ecology mutualism. ant±plant an 1066±1070. on spider theridiid USA. Massachusetts, Cambridge, Press, Ecology suppression. prey implications for vegetation: complex-structured in diminished interactions indirect Entomology se- and Ecological prey species. predator on prey generalist mobility among and a quality by prey lection of effects the food: oeia)o pl fe ncltv ees n competi- and release inoculative with tion after apple on toseiidae) renardii hormspyri phlodromus npress. In n t nuneo h nest fpredator± of intensity the on in¯uence its and , ezli mali Zetzellia 84 :2522±2531. 21 neatosbtenagettvl re- augmentatively between Interactions and A L :1168±1177. CKNOWLEDGMENTS ITERATURE eaeuu occidentalis Metaseiulus 76 126 Aai tgaia) Environmen- Stigmaeidae). (Acari: :2230±2234. :292±304. 83 C :643±652. ITED clg,Vl 4 o 10 No. 84, Vol. Ecology, 387 :562±563. 22 25 Aai Phy- (Acari: :399±407. :140±146. Zelus 80 Ty- : October 2003 WHY OMNIVORY? 2547

Gerritsen, J., and J. R. Strickler. 1977. Encounter probabil- Norton, A. P., G. English-Loeb, and E. Belden. 2001. Host ities and community structure in zooplankton: a mathe- plant manipulation of natural enemies: leaf domatia protect matical model. Journal of the Fisheries Research Board of bene®cial mites from insect predators. Oecologia 126:535± Canada 34:73±82. 542. Hairston, N. G., F. E. Smith, and L. B. Slobodkin. 1960. Obrycki, J. J., K. L. Giles, and A. M. Ormord. 1998. Ex- Community structure, population control, and competition. perimental assessment of interactions between larval Co- American Naturalist 94:421±425. leomegilla maculata and Coccinella septempunctata (Co- Hairston, N. G., Jr., and N. G. Hairston, Sr. 1993. Cause± leoptera: Coccinellidae) in ®eld cages. Environmental En- effect relationships in energy ¯ow, trophic structure and tomology 27:1280±1288. interspeci®c interactions. American Naturalist 142:379± Perry, G. 1999. The evolution of search modes: ecological 411. vs. phylogenetic perspectives. American Naturalist 153: Hairston, N. G., Jr., and N. G. Hairston, Sr. 1997. Does food 98±109. web complexity eliminate trophic-level dynamics? Amer- Perry, G., and E. R. Pianka. 1997. Animal foraging: past, ican Naturalist 149:1001±1007. present and future. Trends in Ecology and Evolution 12: Halaj, J., and D. H. Wise. 2001. Terrestrial trophic cascades: 360±364. how much do they trickle? American Naturalist 157:262± Pianka, E. R. 1966. Convexity, desert lizards, and spatial 281. heterogeneity. Ecology 47:1055±1059. Hastings, A. 2001. Transient dynamics and persistence of Polis, G. A. 1991. Complex trophic interactions in deserts: ecological systems. Ecology Letters 4:215±220. an empirical critique of food-web theory. American Nat- Hawkins, B. A. 1994. Pattern and process in host±parasitoid uralist 138:123±155. interactions. Cambridge University Press, Cambridge, UK. Polis, G. A. 1999. Why are parts of the world green? Multiple Holt, R. D., and G. A. Polis. 1997. A theoretical framework factors control productivity and the distribution of biomass. for intraguild predation. American Naturalist 149:745±764. Oikos 86:3±15. Howard, J. J., D. Raubenheimer, and E. A. Bernays. 1994. Polis, G. A., and S. J. McCormick. 1987. Intraguild predation Population and individual polyphagy in the grasshopper and competition among desert scorpions. Ecology 68:332± Taeniopoda eques during natural foraging. Entomologia 343. Experimentalis et Applicata 71:167±176. Polis, G. A., C. A. Myers, and R. D. Holt. 1989. The ecology Huey, R. B., and E. R. Pianka. 1981. Ecological consequenc- and evolution of intraguild predation: potential competitors es of foraging mode. Ecology 62:991±999. that eat each other. Annual Review of Ecology and Sys- Hurd, L. E., and R. M. Eisenberg. 1990. Arthropod com- tematics 20:297±330 Feature Special munity responses to manipulation of a bitrophic predator Polis, G. A., and D. R. Strong. 1996. Food web complexity guild. Ecology 71:2107±2114. and community dynamics. American Naturalist 147:813± Jaffee, B. A., D. R. Strong, and A. E. Muldoon. 1996. Nem- 846. atode-trapping fungi of a natural shrubland: tests for food Press, W. H., B. P. Flannery, S. A. Teukolsky, and W. T. chain involvement. Mycologia 88:554±64. Vetterling. 1988. Numerical recipes in C. Cambridge Uni- Janssen, A., A. Pallini, M. Venzon, and M. W. Sabelis. 1998. versity Press, Cambridge, UK. Behaviour and indirect interactions in food webs of plant- Price, P. W. 1980. Evolutionary biology of parasites. Prince- inhabiting arthropods. Experimental and Applied Acarol- ton University Press, Princeton, New Jersey, USA. ogy 22:497±521. Roda, A., J. Nyrop, M. Dicke, and G. English-Loeb. 2000. Johansson, F. 1993. Intraguild predation and cannibalism in Trichomes and spider-mite webbing protect predatory mite odonate larvae: effects of foraging behaviour and zooplank- eggs from intraguild predation. Oecologia 125:428±435. ton availability. Oikos 66:80±87. Rosenheim, J. A. 1998. Higher-order predators and the reg- Judson, O. P. 1994. The rise of the individual-based model ulation of insect herbivore populations. Annual Review of in ecology. Trends in Ecology and Evolution 9:9±14. Entomology 43:421±447. Kareiva, P. M., and N. Shigesada. 1983. Analyzing insect Rosenheim, J. A. 2001. Source±sink dynamics for a gener- movement as a correlated random walk. Oecologia 56:234± alist insect predator in a habitat with strong higher-order 238. predation. Ecological Monographs 71:93±116. Lima, S. L. 1998. Nonlethal effects in the ecology of pred- Rosenheim, J. A., H. K. Kaya, L. E. Ehler, J. J. Marois, and ator±prey interactions. BioScience 48:25±34. B. A. Jaffee. 1995. Intraguild predation among biological Lucas, EÂ ., and O. Alomar. 2002. Impact of the presence of control agents: theory and evidence. Biological Control 5: Dicyphus tamaninii Wagner (Heteroptera: Miridae) on white¯y (Homoptera: Aleyrodidae) predation by Macro- 303±335. lophus caliginosus (Wagner) (Heteroptera: Miridae). Bio- Rosenheim, J. A., D. D. Limburg, and R. G. Colfer. 1999. logical Control 25:123±128. Impact of generalist predators on a biological control agent, Lucas, EÂ ., D. Coderre, and J. Brodeur. 1998. Intraguild pre- Chrysoperla carnea: direct observations. Ecological Ap- dation among aphid predators: characterization and in¯u- plications 9:409±417. ence of extraguild prey density. Ecology 79:1084±1092. Rosenheim, J. A., L. R. Wilhoit, and C. A. Armer. 1993. MacRae, I. V., and B. A. Croft. 1996. Differential impact of In¯uence of intraguild predation among generalist insect egg predation by Zetzellia mali (Acari: Stigmaeidae) on predators on the suppression of an herbivore population. Metaseiulus occidentalis and Typhlodromus pyri (Acari: Oecologia 96:439±449. Phytoseiidae). Experimental & Applied Acarology 20:143± Schmitz, O. J., and K. B. Suttle. 2001. Effects of top predator 154. species on direct and indirect interactions in a food web. MeyhoÈfer, R., and J. Casas. 1999. Vibratory stimuli in host Ecology 82:2072±2081. location by parasitic wasps. Journal of Insect Physiology Sih, A. 1993. Effects of ecological interactions on forager 45:967±971. diets: competition, predation risk, parasitism and prey be- Moran, M. D., and L. E. Hurd. 1998. A trophic cascade in haviour. Pages 182±211 in R. N. Hughes, editor. Diet se- a diverse arthropod community caused by a generalist ar- lection: an interdisciplinary approach to foraging behav- thropod predator. Oecologia 113:126±132. iour. Blackwell, Oxford, UK. Murdoch, W. W. 1966. ``Community structure, population Singer, M. S., and E. A. Bernays. 2003. Understanding om- control, and competition''Ða critique. American Naturalist nivory needs a behavioral perspective. Ecology 84:2532± 100:219±226. 2537. Special Feature 2548 kly .K 94 ciiylvladtessetblt of susceptibility the and level Activity 1994. K. foraging D. How Skelly, 2001. III. Stireman O. J. and S., M. Singer, ndr .E,adA .Ie.20.Itrcin between Interactions 2003. Ives. R. A. and E., predators W. Generalist Snyder, 2001. Ives. R. A. and E., W. Snyder, Regulation 1967. Hairston. N. and Smith, F. L., Slobodkin, ndr .E,adD .Ws.20.Cnrsigtrophic Contrasting 2001. Wise. H. D. and E., W. Snyder, nrnlra opeain nmlBehaviour Animal predation. to larvae anuran cater- polyphagous a by Oecologia use pillar. host-plant determine tactics tr,adpaahdbooto.Ecology biocontrol. aphid pea and pred- parasitoids, ators, enemies: natural generalist and specialist Ecol- parasitoid. specialist a ogy by control biological disrupt nature. of Naturalist balance American implied the and ecosystems, terrestrial in acdsgnrtdb omnt fgnrls predators. generalist Ecology of community a by generated cascades 82 :705±716. 82 :1571±1583. 129 101 :98±105. :109±124. A .RSNEMADADE CORBETT ANDREW AND ROSENHEIM A. JAY 84 :91±107. 47 :465±468. ie .H 93 pdr neooia es Cambridge webs. ecological in Spiders 1993. H. D. Wise, conse- Ecological 1993. Anholt. R. B. and E., Biological E. 1996. Werner, Jr. Bellows, S. T. and (Araneo- G., spiders R. true Driesche, the Van of Ecology 1973. L. A. Zeit- ethology. Turnbull, of methods and aims On 1963. N. Tinbergen, tog .R,H .Ky,A .Wipe .L hl,S. Child, L. A. Whipple, V. A. Kaya, K. H. R., D. Strong, nvriyPes abig,UK. Cambridge, Press, University Naturalist American activity. 242±272. foraging by mortality-rates mediated and growth between trade-off the USA. of quences York, New York, New Hall, & Chapman control. Entomology of Review Annual morphae). fu schrift 173. edn aeplaso uhlpn.Oecologia 1996. lupine. Maron. bush L. root- on of J. caterpillars enemies and feeding natural Dyer, nematodes: K. Entomophathogenic Bondonno, M. Kraig, rTierpsychologie Èr 20 :410±433. clg,Vl 4 o 10 No. 84, Vol. Ecology, 18 :305±348. 108 :167± 142 :