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SPECIAL FEATURE

Why Omnivory?1

Omnivory, broadly de®ned as feeding on more than one , is an ecological habit that ought to be widespread. At the most basic level, the omnivorous , as a generalist, should have higher performance in variable environments than some more specialized feeder. Yet the problem of which, why, and how organisms are omnivorous was somehow supplanted by the apparent observation that omnivory is rare in nature and destabilizing in webs. From an historical perspective, Joel E. Cohen and Stuart L. Pimm independently began to advocate the ``rare and destabilizing'' position in the late 1970s. Unfortunately, naturalists who knew better failed to displace this notion. Not until the late Gary Polis published his now classic study (G. A. Polis 1991. Complex trophic interactions in deserts: an empirical critique of theory. American Naturalist 138:123±155) was there a resurgence of interest in understanding the and ecological importance of . The ubiquity of omnivory is now widely recognized, and theory has demonstrated conditions under which omnivores can stabilize food webs. As theoreticians con- tinue to work out the in¯uence of omnivory on the stability and lengths of food chains, empiricists have gotten busy in identifying and studying the causes and consequences of omnivory in nature. The question about why omnivores have such diversi®ed feeding strategies remains a critical question that is ripe for diverse hypotheses. Ironically, although arthropods are probably not omnivory-dominated as a (vertebrates probably are), a large portion of omnivory research is focused on omnivorous arthropods. As such, this Special Feature focuses mostly on the causes of omnivory in arthropods and touches on the consequences across taxa. The authors of this Special Feature each take a different creative approach to understanding omnivory. There are clear differences in the paradigms (stoichiometry of the essential elements, costs and bene®ts of mixing, behaviorally motivated decisions, and dynamic constraints) and approaches (literature review, models, and phylogenetic analyses) that the authors employ. The result is a stimulating set of papers that should be evaluated, challenged, and tested.

ÐANURAG A. AGRAWAL Special Features Editor

Key words: dynamic constraints models; food selection; host range ; intraguild ; omnivory; optimal diet theory; ±animal interactions.

᭧ 2003 by the Ecological Society of America

1 Reprints of this 47-page Special Feature are available for $7.00 each, either as pdf ®les or as hard copy. Prepayment is required. Order reprints from the Ecological Society of America, Attention: Reprint Department, 1707 H Street, N.W., Suite 400, Washington, D.C. 20006.

2521 , 84(10), 2003, pp. 2522±2531 ᭧ 2003 by the Ecological Society of America

MIGHT NITROGEN LIMITATION PROMOTE OMNIVORY AMONG CARNIVOROUS ARTHROPODS?

ROBERT F. D ENNO1 AND WILLIAM F. F AGAN2 1Department of Entomology, University of Maryland, College Park, Maryland 20742 USA 2Department of Biology, University of Maryland, College Park, Maryland 20742 USA

Abstract. Omnivory is a frequent feeding strategy in terrestrial arthropods, occurring across a diversity of taxa occupying a wide array of . Because omnivory has im- portant consequences for broad areas of theoretical and , it is essential to understand those factors that favor its occurrence. Here we address the limiting role of nitrogen in promoting omnivory, not so much from the historical perspective of supplementing their -poor plant diet, but by extending the argument to higher trophic levels where predators feed on each other as well as herbivores. Drawing on the historically documented mismatch in nitrogen stoichiometry between herbivores and their host

(C:Nplants k C:Nherbivores), and a recently documented, though smaller, difference in nitrogen content between predators and their prey (C:Nherbivores Ͼ C:Npredators), we discuss the existence of a trade-off between nutrient quality and quantity that occurs across trophic levels. The existence of this trade-off suggests that arthropod predators, which we show to be frequently nitrogen-limited in nature, can enhance their nitrogen intake by broadening their diet to include nitrogen-rich predators. We conclude by outlining the consequences of this trade-off for the relative balance between dietary specialization and supplementation among consumers, emphasizing the divergent roles that large vs. small stoichiometric mis- matches may have had for the evolution of omnivory. Key words: arthropods; ; ; nitrogen limitation; nutrient stoichi- ometry; omnivory.

INTRODUCTION spectrum of ecology. In this paper, we explicitly ad- dress the limiting role of N in promoting omnivory, For our consideration of omnivory, we focus on the not so much in the historical context of herbivores sup- contribution of nitrogen (N) limitation to feeding strat- plementing their nutrient-poor plant diets (Mattson egies in terrestrial arthropods. We adopt a broad view Special Feature 1980, White 1993), but instead extending the - in which omnivory is de®ned as feeding on two or more sion to include species feeding at higher trophic levels. trophic levels (Menge and Sutherland 1987, Polis and Recently, important connections between omnivory Strong 1996), a de®nition that includes ``herbivores'' that extract from nonplant sources (e.g., en- and nutrient ¯ow in have emerged (e.g., gage in ), ``predators'' that feed on both Ostrom et al. 1997). One such linkage has been iden- herbivores and selected plant tissues (e.g., seeds, pol- ti®ed using the framework of , len), as well as predators that feed on herbivores and the study of the relative balance of nutrients and energy other predators (e.g., intraguild predators, facultative in organisms from different trophic levels (Elser et al. hyperparasitoids) (Coll 1998, Rosenheim 1998, Sulli- 1996, 2000; Sterner and Elser 2002). This emerging van and VoÈlkl 1999, Coll and Guershon 2002). Om- framework provides opportunities for connecting om- nivory is widespread in terrestrial arthropods, occur- nivory with larger-scale processes such as food web ring across a diversity of taxa that occupy a wide va- and dynamics through its focus on the func- riety of habitats (Coll and Guershon 2002). The pro- tional consequences of nutrient and energy ¯ow be- found consequences of omnivory for population and tween trophic levels. One of the most profound con- food web dynamics (Menge and Sutherland 1987, Fa- sequences of a stoichiometric perspective is that gross gan 1997, McCann et al. 1998, Rosenheim 1998, Eu- growth ef®ciencies of consumers are in¯uenced by banks and Denno 2000a), (Polis et their demands for limiting resources (Sterner and Elser al. 1997), and biological control (Rosenheim et al. 2002). A classic example is the mismatch in C:N con- 1995, Hodge 1999) are just beginning to be realized. tent between herbivores and their host plants that has Thus, understanding the factors that promote and main- led to a diversity of behavioral, physiological, and eco- tain omnivory in ecosystems is critical across a broad logical in herbivores that help offset this inherent discrepancy (McNeill and Southwood 1978, Mattson 1980, White 1993). Because of stoichiometric Manuscript received 19 June 2002; accepted 14 August 2002. Corresponding Editor: A. A. Agrawal. For reprints of this Special mismatches, an herbivore with a speci®c body com- Feature, see footnote 1, p. 2521. position (e.g., C:N ratio) cannot take full advantage of 2522 October 2003 WHY OMNIVORY? 2523

FIG. 1. Predators regularly incorporate oth- er predators in their diets. Plotted data (Hodge 1999) summarize the frequency of intraguild predation (percentage of diet) for spiders. Ad- ditional examples show that there are predators specializing at both ends of the diet spectrum such as aphidophagous syrphids feeding exclu- sively on herbivores (Rotheray and Gilbert 1989) and pompilid wasps and aranaeophagic spiders specializing on predators (Li and Jack- son 1997).

with insuf®ciently low nutrient con- conocephaline katydids, extensive plant feeding oc- tent. In a sense, available C in excess of the 's curs, but individuals cannot complete development body requirement for N is ``wasted'' (Sterner and Elser without consuming prey (R. Denno, unpublished data). 2002), because it cannot be utilized for growth. How- For omnivorous ¯ower thrips, reductions in plant qual- ever, this excess C may be available for other uses such ity cause shifts from herbivory to predation (Agrawal as or dispersal. Stoichiometric limitations are et al. 1999). Similarly, many ``predators'' either oc- especially critical to herbivore growth processes (Elser casionally or frequently feed on N-rich plant parts (e.g., et al. 2000), but dietary mismatches can also limit the and seeds) in addition to animal prey (Coll 1998, processes of reproduction and self-maintenance. Based Coll and Guershon 2002), and in so doing, can persist on accumulating evidence concerning the stoichio- through periods of prey scarcity (Polis and Strong metric structure of foodwebs (Fagan et al. 2002, Sterner 1996, Eubanks and Denno 1999). Numerous omnivores Feature Special and Elser 2002), we will argue here that stoichiometric perform best on mixed diets of plants and prey when mismatches, similar but less severe than the well- compared to restricted feeding on either diet (Coll known herbivore±plant mismatch, also exist at higher 1998). Nonetheless, across a diversity of omnivorous trophic levels, and that these disparities appear func- arthropods, a spectrum of dietary mixing exists with tionally connected to the preponderance of omnivory the fraction of plant material and prey varying greatly, among terrestrial arthropods. and with both obligate and facultative mixing strategies Here, we explore how stoichiometric imbalances represented (Coll 1998, Thompson 1999). across trophic levels, particularly those involving N, Omnivory is also prevalent at higher trophic levels, may generate trophic complexity via omnivory in ter- where predators or parasitoids not only attack herbi- restrial arthropod food webs. We ®rst detail the back- vores but also prey extensively on other predators (Ro- ground for our thinking, outlining the regularity of prey senheim 1998, Sullivan and VoÈlkl 1999). For example, limitation for terrestrial arthropod predators and its intraguild prey comprised 3% to 75% (mean ϳ20%) manifold consequences, including extensive omnivory. of prey taken for 45 spider species in 12 families (Hodge We next discuss the evidence for N-limitation in pred- 1999; Fig. 1). Facultative hyperparastioids and pred- ators, and outline the consequences of such N-limita- ators that feed on parasitized herbivores are omnivo- tion for predator ®tness and prey selection. To synthe- rous by virtue of intraguild or multitrophic-level pre- size our views we describe the conditions favoring om- dation (Rosenheim 1998, Hodge 1999, Sullivan and nivory and intraguild predation over strict predation on VoÈlkl 1999). The behavior underlying these diverse herbivores. We conclude by discussing some of the examples of omnivory can be categorized as either co- ecological consequences of omnivory, emphasizing incidental or directed in nature (reviewed in Polis et how mismatches in nutrient stoichiometry across tro- al. 1989). phic levels may in¯uence patterns of diet breadth, lin- eage diversi®cation, and food web structure. PREY LIMITATION AND ITS CONSEQUENCES FOR PREDATORS THE WIDESPREAD OCCURRENCE OF OMNIVORY Spiders (Riechert and Harp 1987, Tanaka 1991, Wise An extensive literature documents instances of ``her- 1993, Hodge 1999), mites (McRae and Croft 1997), bivorous'' arthropods occasionally or frequently feed- scorpions (Polis and McCormick 1986), mantids (Hurd ing at higher trophic levels (McNeil and Southwood and Eisenberg 1984), heteropterans (Spence and Car- 1978, Coll and Guershon, 2002). These include in- camo 1991), (Lenski 1984, Bommarco 1999), stances of cannibalism and interspeci®c predation that caddis¯ies (Wissinger et al. 1996), neuropterans (Ro- are often viewed as mechanisms for obtaining supple- senheim et al. 1993), and wasps (Mead et al. 1994, mental N from sources other than host plants (McNeill Stamp 2001) are among the many predatory arthropod and Southwood 1978). In some cases, such as some taxa that routinely face prey limitation. Evidence for Special Feature nefc Mtsn18,Wie19) a locon- also performance. may predator 1993), strain White 1980, (Mattson plant±herbivore interface the lim- at N historically Thus, documented 1999). Toft itation, 1999, ar- al. an Thompson et 1986, of Pennacchio 1999, Bonnot constituents (e.g., limiting diet the predator's fact thropod in are ami- acids essential or bio- no fundamental gross more that such a level, sug- at chemical strongly occurs studies limitation other pred- that but limit gest 1993), may Wise scarcity (see prey ators predator cases, limits some speci®cally In what success. of un- issue leaves the generally resolved limitation prey of documentation extensive host this by However, affected 1999). is (Thompson size availability population or parasitoids and for ®tness shown whose 1979, been (Wise have effects fecundity al. Similar or et 1993). survival Denno enhanced 1993, or (Wise 2002), (Do growth population density creased areas prey in aggregation high as local of such to density, responses prey of in variety increases a includes limitation this 2524 tttn o- aeil o ihNmtrasi con- sub- in by materials food high-N low-N for to materials adapt low-N to stituting able her- be example, might For N. bivores dietary to of response scarcity in differential both) the di- or for predators, herbivores, selected (in Second, be rectly content. may conse- N composition higher a body with differential as food simply herbivores of have than quence may predators content First, N here. higher only these We over (2002). on predators al. touch et of brie¯y Fagan ratio, in detailed C:N are lower herbivores thus and content, factors. confounding potentially and other dilution, gut difference , This for accounting demand. after persists dietary thus increase and relative N-content 27% in to than 5% a biomass representing unit differences percentage-point per these with N 0.5 relatives, more from herbivorous their points have percentage to absolute 3 found an to were on Indeed, predatory phylogenetically 2B). basis, do (Fig. than herbivores ratio al. C:N related et lower (Fagan a content and N 2002) higher consistently have pred- ators arthropod terrestrial particular, has In N also observed. herbivores the been and predators between arthropod difference of interface. content a plant±herbivore however, the recently, major across More the quality in- with in starting quality jump position, resource trophic and with contrast, Pauly creases In 1984, Price 1995). (e.g., Christensen documented to 4 being of ef®ciencies in- 33% transfer with with decreases level, trophic biomass creasing that ecologists example, recognized For long 2A). have (Fig. and webs trophic quantity food across exist in the to levels appears between that resources trade-off of quality a consider ques- this answering tion, begin To context? web food larger eea oeta xlntosfrteeeae N elevated the for explanations potential Several a within ®t predators of limitation prey does How : R C:N TO OF ATIOS H OF ERBIVORES P REDATORS bladDno19) in- 1994), Denno and Èbel OETF EN N ILA .FAGAN F. WILLIAM AND DENNO F. ROBERT E XCEED T HOSE lntos oee,acerdfeec nNcontent N arthropods. in predaceous and difference herbivorous between ex- clear exists underlying a the however, of have Regardless planations, conducted. operate be would to they yet which the clarify under or circumstances mechanisms these of the importance identify expla- to relative experiments potential analysis knowledge, these our and To among nations. dissection distinguish tissue help (herbi- would prey with N-poor coupled or (predators) needs. vores), are N-rich their of omnivores exceeds diets where that fed experiments supply planned N dietary Carefully cre- a problems by to ated responses maladaptive) other (or or sequestration adaptive re¯ect may Fourth, predators allo- in structures. N lower-N different higher other for vs. muscle select to might cations predation and her- example, bivory of For consequence habits. trophic indirect different an to dif- be Third, may cuticle. content as N such ferential parts, body some structing mtcly ipevrino h E a eex- be can TER the of as version pressed simple Math- a C-limited. or ``energy-'' ematically, vs. nutritional prey the their by of limited quality are ``threshold consumers the which the identi®es at which level of TER), concept (hereafter ratio'' the elemental developed perspec- They quantitative a tive. from quality-limitation issue to prey the explored of contributors (1992) Watanabe other and Urabe and ®tness? reproduction, growth, pred- ator on constraints stoichiometric impose to suf®cient ie,tefato figse httepredator the that N ingested biomass), of new into fraction converts the (i.e., N foeecue h .%o h ln±ebvr com- plant±herbivore the of 2.5% the excludes even one example, For if distributions. consumer-resource these can from of gleaned observations be Several kinds occur. the can that of combinations estimate provide rough they Nevertheless, a distri- database. the regional in among in species behavior the and differences speci®city, host of size, body virtue bution, Ad- by occur not 2C). nature would (Fig. in combinations issue these of TER some the mittedly, into provides 2002) insight al. et additional Fagan compiled 2000; al. from et (Elser pairs databases predator±predator and predator, rwhe®inyfrC n C:N and C, for ef®ciency growth eg,ahdldbg ol aesrn limitation N 2002). al. strong et face (Fagan pairs could herbivore±predator aphid±ladybug) speci®c and (e.g., that N-limitation, suggested for data evidence also arthropod ho- consistent our strong showed under of set and Analysis speci®c regulation. species meostatic are be which biomass, to predator and assumed prey of ratios C:N the where C:N steeeetlmsac nbd otn (C:N) content body in mismatch elemental the Is osdrto fptnildsrbtoso C:N of distributions potential of Consideration consumer E ␣ N IEC FOR VIDENCE stemxmmgosgot fcec for ef®ciency growth gross maximum the is o l osbepathrioe herbivore± plant±herbivore, possible all for CN/: ) /C:N (C:N rypeao C N predator prey IN P N REDATORS ITROGEN ␣ C Ͼ␣ stemxmmgross maximum the is clg,Vl 4 o 10 No. 84, Vol. Ecology, prey L IMITATION n C:N and / ␣ predator resource are (1) / October 2003 WHY OMNIVORY? 2525 pca Feature Special

FIG. 2. Ratio of carbon to nitrogen (C:N) content across trophic levels, among taxa, and between potential resource± consumer pairs. Panel (A) outlines a trade-off between decreasing resource availability (standing crop biomass, on a loga- rithmic axis) and increasing resource quality (i.e., decreasing C:N ratio) across four trophic levels. Resource quantity curves represent hypothetical scenarios assuming trophic transfer ef®ciencies of 4% and 33% between adjacent trophic levels and are scaled relative to plant biomass. Resource quality data are averaged across phylogenetic, allometric, and other sources of intratrophic-level variation. Panel (B) gives the mean (ϩ1 SE) C:N ratio for herbivorous and predaceous arthropods, grouped phylogenetically according to lineage. The groupings lower Neoptera and Panorpida facilitate comparisons of herbivorous Orthoptera with predaceous Mantodea, and herbivorous Lepidoptera with predaceous Diptera, respectively. Panel (C) gives frequencies of relative C:N ratios of resources and consumers in terrestrial arthropod food webs determined by calculating all pairwise combinations of resource versus consumer C:N ratios. Resource quality data are from Elser et al. (2000) and Fagan et al. (2002), the latter of which provides statistical analyses documenting consistent and signi®cant differences in N content between predaceous and herbivorous arthropods. binations that are most nutrient rich, 22% of the her- ample, one way for a growing predator to avoid nutrient bivore±predator combinations are as N limited as are limitation is to increase its expenditure or excretion of better matched plant±herbivore combinations (C:N ra- C, thus lowering ␣C (Sterner and Elser 2002). This leads tios ranging from 1.4 to 3.1). In comparison, 48% of to the expectation that predators with high N require- predator±predator combinations have ratios Յ1, sug- ments will more likely be active hunters rather than gesting substantial opportunities for predators to obtain sit-and-wait predators. relatively N-rich diets via intraguild predation. Sterner (1997) extended the TER concept to explore These ®ndings also have interesting implications for explicitly the interaction between the quality and quan- understanding predator foraging strategies. For ex- tity of prey. He suggested that the TER is a decreasing Special Feature oelkl ob iie yeeg C hnb N. by as than are (C) such ef®cient energy availability nutrients by limited lack prey be to and/or increase likely more prey to mechanisms of routinely search that shortages predators severe Thus, energy. face consumer for a if starving consideration prey major is that a in be not sense becomes will intuitive quality food makes as result for This threshold higher scarcer. the becomes that limitation such nutrient quantity, prey of function 2526 ete Sye ta.20) n oemts(Schaus- mites some and 2000), al. et (Snyder beetles coccinellid 1991), Carcamo and spe- (Spence meet Heteropterans to circumstances. way certain under one requirements represent nutrient ci®c may thus predator and diet, between and match for stoichiometric opportunity near-perfect an a mal- present potentially does cannibalism Although that adaptive, cannibalism. species from from lim- comes is bene®t predators N arthropod that for evidence iting Other nitrogen 2000). to (Mira attributed been limitation has that behavior a molting, 2000). Williams and Duval variation (e.g., temporal di- quality as be resource such can in factors, or other universal, by not N minished is par- that predators and suggesting of predators limitation occur, many limit Counterexamples can asitoids. N that suggest stud- these ies Collectively, 1986). (Bonnot ami- levels and no-acid protein dietary time with development correlated negatively parasitoid, was 1995). tachinid (LeRalec a eggs for of Likewise, content Thompson protein 1986, the Kidd and sur- and 1999) (Jervis improved fecundity parasitoids and pre- vival hymenopterous intraguild (including in feeding dation) 1999). host (Thompson example, diets For high-protein on survival and widespread especially insects, spiders. limitation predatory among N most make for may that that and more than be meet may spiders to for demand dif®cult et N (Fagan the (10.8%) Thus, 2002). general than al. in higher insects is predatory also that for but that exceeds (9.5%), statistically insects only herbivorous for not content N (11.7%) the spiders average on of that suggesting data light limi- recent in N of interesting particularly indicate are also results These pro- may tation. their 1998), (Opell recycle silk spiders tein-rich 1997). which Jackson in and reclamation, (Li Web insects herbivorous mix a N-poor with of than prey spider intraguild with provisioned when and survivorship enhanced 2001), exhibited Toft their spiders and enhanced jumping (Mayntz spiders survivorship of and diet growth the of to addition experimental acids the amino example, (Strohmeyer For bugs 1998). stink al. et predaceous as such other and predators 1999) Toft 1992, spi- al. for et occur (Uetz ®tness ders of components on balance dietary rdtr n mioe fe a hi xva upon exuviae their eat often omnivores and Predators growth optimal achieve typically also Parasitoids and limitation N of impacts front, empirical the On C NEUNE OF ONSEQUENCES P REDATOR F TESAND ITNESS N ITROGEN P OETF EN N ILA .FAGAN F. WILLIAM AND DENNO F. ROBERT REY L MTTO FOR IMITATION S ELECTION uvvlwe e oseic,bttervrei true 1999 is Wise and reverse (Toft spiders the some but for conspeci®cs, fed or when performance increased survival show 2000) Croft and berger n no19,Srhee ta.19,Tf n Wise and Toft 1998, Endo al. 1999 et 1993, Strohmeyer al. 1994, et Endo and size, (Rosenheim behavior, prey or in , differences by prey confounded in are differences potential however, ators, oe 95 icetadMui 98,ntteleast the not 1998), Maupin and 1987, con- Riechert (Sih 1995, explanations partial Cohen multiple the has prey Also, of ther- sumption 1998). adaptive and (Oxford serve aposematism, also moregulation crypsis, may including but products functions waste just are pigments not exoskeletal guanine-rich spiders' stance, in- potential For interpretations. these evidence alternative of has as counterexamples each However, stand limitation. 1998) (Sih N Maupin against consumption and prey Riechert partial 1987, and in engaging killing and 1998), excessive (Oxford exoskeleton their in N prey. nutritious most the pred- arthropod attack equal, selectively being ators else avail- all are that, data verify to limited able only Overall, 2002). Denno and yk 96 ot19,Tf n ie1999 Wise and Toft Ob- 1999, and Toft (Strand and 1996, prey'' (Endo quality rycki prey ``higher larger 1994), pred- preferred Endo studies, parasitoids other al. In or et 2002). ators Denno Rosenheim and 1979, Finke 1993, (Greenstone nutritious most available the prey on feed selectively Indeed, predators 1996). some Obrycki and Strand 1991, Friedman and (Waldbauer optimization optimal- dynamic by and predicted models as foraging (other and (1981) prey as Polis (herbivores), N-rich by suggested options on nutritious less feed over to predators) prefer pred- generally if ask ators can one predators, arthropod in limitation N 2000). al. tissues et plant Elser N-rich 1980, these (Mattson N) even higher (4±6% is of average, prey that herbivorous than On of (6±10%) 1980). content (NcNeill N contents Mattson the N however, 1980, high Southwood with parts and plant Denno all and Eubanks 1999), 1998, (Coll or feed fruits, to which ¯owers, on seeds, pollen select beetles (Eu- coccinellid heteropterans tissues and predatory plant Many 1999). of Denno choice and banks dietary their from comes 2000). Croft and (Schausberger hoels urtospe EbnsadDenno and (Eubanks prey nutritious 2000 less they contents instances other N choose in and differing 2000), Williams of and prey (Duval among do predators discriminate cases, not some In 1999). (Toft avail- spectrum the from how- able item predators, prey N nutritious arthropod most the all the select Not to ever, prey. linked the but explicitly of 2001), not content (Stamp were prey'' preferences palatable such ``more or 2001), oi ry'(ot19,Tf n ie1999 Wise and Toft 1999, (Toft prey'' toxic tcudas eage htpeaossequestering predators that argued be also could It ie h usata oueo vdnesupporting evidence of volume substantial the Given predators for limiting is N that evidence Further a b uak n en 2000 Denno and Eubanks , pred- by selection prey of studies all almost In ). clg,Vl 4 o 10 No. 84, Vol. Ecology, b tm 01 Finke 2001, Stamp , a n oemites some and ) b b Stamp , ,``less ), October 2003 WHY OMNIVORY? 2527 of which might be the rapid and selective extraction of (hereafter EOD), a mechanism by which an estimated N before leaving the remainder behind (Cohen 1995). 79% of predatory insects and arachnids feed (Cohen Because predatory arthropods contain more N per 1995). For example, both heteropterans and carabid unit biomass on average than do herbivores (Fagan et beetles are highly ef®cient at extracting nutrients from al. 2002; Fig. 2B), predators could reduce this inherent prey, reaching ef®ciencies of 94% and 84%, respec- stoichiometric mismatch by concentrating their feeding tively (Cohen 1995). Some parasitoid larvae selectively on other predators. Several arthropod predators, in- ingest particulate materials within their host and em- cluding numerous araneophagic spiders (e.g., Li and ploy EOD, a behavior that concentrates nutrients and Jackson 1997), some ®re¯ies (Eisner et al. 1997), and promotes rapid growth (Wu et al. 2000). The advan- many obligate hyperparasitoids (Sullivan and VoÈlkl tages of EOD are reduced handling time, increased ex- 1999) in fact specialize on other predators or primary traction rate of nutrients, and an increase in the ef®- parasitoids. More commonly, however, predators with ciency of nutrient extraction and concentration, allow- specialized diets feed exclusively on herbivorous prey ing small predators to obtain nutrients from relatively (Rotheray and Gilbert 1989, Strand and Obrycki 1996, large prey (Cohen 1995). Thompson 1999). In the case of many coccinellid and EOD also allows for the differential extraction of syrphid predators that specialize on aphids and scale nutrients from prey, whereby are ingested ear- insects (Rotheray and Gilbert 1989), their prey are N lier in the feeding process than are lipids (Cohen 1995). de®cient compared to many other herbivores (Fa- In a stoichiometric context, such differential extraction gan et al. 2002). In these instances, the apparent nu- would be advantageous by reducing the intake of C tritional disadvantage of feeding on such N-de®cient relative to more limiting nutrients. For example, by prey is offset in part by specializing on prey that are consuming internal tissues of their prey, the predators often extremely abundant, aggregated, sessile, and easy avoid consumption of the high C:N exoskeleton and to catch (e.g., Dixon 1998; Fig. 2A). thus avoid dilution of prey tissue N with excess car-

PREDATORS COPING WITH THE STOICHIOMETRIC bohydrate. The rapid and selective of N from Feature Special CONSTRAINTS OF LOW-NITROGEN PREY prey may also explain why predators occasionally con- sume only part of the utilizable portion of their catch Faced with prey of lower than optimal nutritive val- (see Johnson et al. 1975, Sih 1987, Riechert and Mau- ue, predators employ a diversity of mechanisms to pin 1998). Thus, when faced with low-quality prey, an makeup shortfalls in key nutrients. One of the most alternative to feeding compensation is selective feeding obvious methods available to a consumer faced with via enhanced discrimination among prey (Greenstone poor-quality resources is feeding compensation, the 1979) and differential extraction of high-value nutri- process of increasing feeding rate (Simpson and Simp- ents from prey (Cohen 1995, Furrer and Ward 1995, son 1990, Slansky 1993). Though extensively em- Wu et al. 2000). ployed by herbivores, the extent to which predators employ feeding compensation is not clear. Further- THE NUTRITIONAL ADVANTAGE OF AN more, even when used, feeding compensation is not a OMNIVOROUS DIET universally successful solution to problems of nutrient acquisition because physiological constraints such as Having established a difference between the N con- maximal gut capacity and throughput time limit the tent of predators and prey, a key issue that emerges is degree to which eating more can compensate for eating whether the difference is large enough to promote om- nutrient-poor food (Johnson et al. 1975, Sih 1987). In nivory? In other words, under what conditions does a addition, compensatory feeding on low-quality food predator that feeds on other predators enhance its rate can lead to increased levels of dietary toxins, and these of N uptake over one that feeds only on herbivores? toxins can negatively affect growth, survival, and other Speci®cally, might a predator face increases in han- contributors to herbivore ®tness (Slansky and Wheeler dling time or dif®culties in assimilating N from pred- 1992). Predators also accumulate prey-derived toxins ator tissues that outweigh the potential gain from feed- with adverse effects (Toft and Wise 1999a, Francis et ing on prey with lower C:N content? As a preliminary al. 2001), but the two-way relationship between feeding exploration of this issue, we examined the relative gain rate and toxin accumulation has not been investigated in N uptake that a predator would enjoy as a function extensively in predators. In a stoichiometric context, a of three factors: (1) the proportion of diet made up of possible disadvantage to feeding compensation is that other predators, (2) the average nutritional advantage in the process of satisfying an absolute need for nu- from feeding on predators with low C:N tissues, and trients, such feeding increases the absolute amount of (3) the cumulative (dis)advantages resulting from dif- extra C that must be used or eliminated. ferences in handling times or assimilation ef®ciencies. Predators can also cope with low-quality prey by To calculate a dimensionless measure of nutritional ad- ef®ciently extracting nutrients and by increasing ex- vantage, we used the following equation: traction rates (Cohen 1995, Furrer and Ward 1995).

These processes are enhanced by extra-oral digestion z ϭ (1 Ϫ pdietppp/hp/h ) ϩ pdiet *⌬N *⌬e (2) Special Feature hr pdiet where 2528 n ies®ain o xml,oecmn h se- the breadth overcoming diet example, of For patterns diversi®cation. to and contribute also may levels well be mobile would predators. against techniques same prey the employ herbivore to equipped chem- mobile or subdue mechanically ically that exoskele- predators arthropod Likewise, physi- tons. penetrate same to the could, adaptations employ seeds ological changes, nutrient-rich few and but relatively tough, mouthparts with on sucking feed ex- use to For EOD that . herbivores to consumer ample, transi- specialist such scarcer from facilitate but tions may quality Preadaptations higher or resources. resources qual- abundant low spe- ity, on either from feeding break with associated evolutionary cializations an feeding require a may such strategy omnivory, promoting factor an be important may ``predators'' and ``herbivores'' between tent 2B). of Fig. content 2002; al. N et average (Fagan of higher predators because discovered herbivores, recently on on the than feeding by rather demands predators N other their can predators meet that effectively recognition more the 1999). is Thompson here 1999, nu- novel (Toft is view prey What new on a decisions not is foraging trition their preda- base That should prev- interactions. tors the predator±predator explain of help alence may ar- and terrestrial one assemblages, in is thropod omnivory levels extensive trophic across promoting organisms factor of mismatch of content prevalence the N the that on in suggest we that Speci®cally, factors of omnivory. mix the includ- in be ed should stoichiometry ecological have that we argued Here, the- ecology. of the application for and practice, consequences ory, important has and thropods po rdtr seFg 1), Fig. (see predators of up nonesaohrpeao,i tavnaeu oin- to individual? advantageous that it clude predator is a predator, if rather another but encounters prey, as predators not other out should do predators seek whether we is because question pertinent here the time think search predators. include nutrient-rich don't more We eating or by predators diet more nu- all-herbivore either an their to increase relative can uptake trient preda- predators from herbivores, extract than to are tors dif®cult nutrients more that substantially Provided not nu- ef®ciencies. and uptake factors three trient the on on depending the predation vary how strict herbivores shows over 3 omnivory Fig. favoring factors). conditions han- related ef®ciency, and time, assimilation dling in differences of effects potential cumulative the for her- (accounting vs. tissues predator bivore from nutrients uptake can predator the seFg C,and 2C), tissues herbivore Fig. vs. (see tissue predator of content N) (e.g., imthsi uretsocimtyars trophic across stoichiometry nutrient in Mismatches con- nutrient in mismatches stoichiometric Although ar- terrestrial among ubiquitously occurs Omnivory p S stepooto fapeao' itmade diet predator's a of proportion the is NHSSAND YNTHESIS ⌬ e p/h sterltv aewt which with rate relative the is ⌬ N P ROSPECTUS p/h OETF EN N ILA .FAGAN F. WILLIAM AND DENNO F. ROBERT sterltv nutrient relative the is mn osmrseis(i.2) vle solutions Evolved 2A). discrepancies (Fig. species smaller consumer the among for challenges compensating does ecological/evolutionary than greater likely availability presents N in mismatch plant±herbivore vere oepeaoso oentin-ihpredators. nutrient-rich either more eating their or by diet predators increase all-herbivore more can an to predators extract relative to uptake herbivores, nutrient dif®cult than more not predators are from (see nutrients from rates herbivores that from uptake Provided than 2). ef®cient (C), Eq. less predators in or from slower whereas are rates equal, predators from uptake are nutrients nutrient herbivores up (B), and take In which ef®ciently predators. in or other case quickly the depicts more (A) predators Panel predators. and herbivores F IG .Ntin paefronvrswt ie it of diets mixed with omnivores for uptake Nutrient 3. . clg,Vl 4 o 10 No. 84, Vol. Ecology, October 2003 WHY OMNIVORY? 2529 to the plant±herbivore N mismatch (e.g., McNeill and consequences of stoichiometric disparities across tro- Southwood 1978) may involve physiological, morpho- phic levels will help link population and logical, or behavioral modi®cations that constrain her- ecology on the one hand, with ecosystem science on bivores from employing alternative strategies for ac- the other. quiring N such as feeding on a diversity of plant parts or taxa. Such constraints have promoted monophagy, ACKNOWLEDGMENTS dietary specialization, and diversi®cation in such taxa This paper is a contribution from the Ecological Stoichi- (Bernays and Graham 1988). In contrast, stoichiometric ometry working group at the National Center for Ecological Analysis and Synthesis, a center funded by the National Sci- differences between predators and herbivores are not ence Foundation, the University of California, and the State as extreme, and overcoming these smaller disparities of California. We thank the staff of NCEAS for their logistical may not constrain predators in the same way that N support and the working group participants, especially J. El- limitation affects herbivores. In other words, ``preda- ser, C. Mitter, and E. Siemann, for their inspiration and op- tors'' can make up the difference by dietary supple- portunities to explore the bene®ts of mixed diets. A. Agrawal, S. Diehl, J. Elser, M. Eubanks, F. Slansky, D. Wise, and six mentation and opportunistic, generalized feeding habits anonymous referees provided comments on an earlier draft rather than by specialization, thus providing the mo- of this article, and we hope to have incorporated their many tivation and prospect for feeding across trophic levels. insightful suggestions. This research was supported as well Thus, as the disparity in C:N stoichiometry between by National Science Foundation Grants to R. F. Denno (DEB- 9527846 and DEB-9903601) and to W. F. Fagan (IBN- consumers and their resources decreases from lower to 9977047). higher trophic levels, we expect there to be a general dietary trend from specialization to supplementation LITERATURE CITED and omnivory. We suspect one reason why lineages of Agrawal, A. A., C. Kobayashi, and J. S. Thaler. 1999. 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UNDERSTANDING OMNIVORY NEEDS A BEHAVIORAL PERSPECTIVE

MICHAEL S. SINGER1 AND ELIZABETH A. BERNAYS Department of Entomology and Center for Insect Science, University of Arizona, Tucson, Arizona 85721 USA

Abstract. While the importance of omnivory in community and food web ecology has received recent recognition, the behavioral basis of omnivory has not been thoroughly explored. Here we argue that understanding the basis of food mixing (i.e., eating different food types) and food selection behavior is central to understanding the causes and con- sequences of omnivory. Despite the existence of several alternative hypotheses, constraints imposed by nutrients are often assumed to explain the function of food mixing by omnivores and herbivores. However, few studies have actually addressed this issue through rigorous tests of multiple hypotheses. To illustrate the importance of non-nutritive factors, we marshal evidence for the roles of toxin dilution, parasite avoidance and resistance, and predation risk in food mixing and food selection by omnivores and polyphagous herbivores. Whether food mixing stabilizes population, community, and food web dynamics is likely to depend on the details of food selection and the spatial and temporal scales of food mixing. Key words: deterrents; diet; food selection; foraging; ; omnivory; polyphagy; predation risk; toxins; tritrophic interactions.

INTRODUCTION ically. We then discuss why the function of food mixing and food selection might determine the ecological con- In the last few decades, omnivory has assumed an sequences of omnivory. Finally, we suggest that the important position in the study of population, com- spatial and temporal scale of food mixing might de- munity, and food web ecology (e.g., Pimm and Lawton termine its ecological consequences. 1978, Polis and Strong 1996). Here we argue that study- ing the causes and consequences of omnivory could WHY EAT A MIXED DIET? also bene®t from the perspective of . Namely, we need to understand how and why omni- Here we consider several hypotheses (summarized vores make particular foraging decisions. Central in Hailey et al. 1998) proposed to explain ``varied among these is the habit of eating different food types, diets,'' ``diet mixing,'' or ``food mixing'' in our ter- i.e., food mixing. We de®ne food mixing as the inges- minology. As applied to omnivores (e.g., mixing plant Special Feature tion of multiple food types over an animal's lifetime and animal ), these hypotheses are: (1) a quali- or stage of a complex life cycle; we consider food types tatively superior food type exists but is limited in sup- as different species that differ qualitatively to the con- ply (e.g., prey), necessitating the inclusion of subop- sumer. Food mixing is a fundamental type of foraging timal (e.g., plant) food in the diet; (2) no single food strategy that includes omnivory, as well as polyphagy type is qualitatively superior, so food mixing allows by individual herbivores and carnivores. Because our the intake of nutritionally complementary foods (e.g., focus is on food mixing and our expertise is herbivores, animal and plant material), enhancing digestion or the we will draw examples from both omnivores and food postdigestive utilization of nutrients; (3) foods contain mixing herbivores from terrestrial and marine ecosys- toxins (e.g., plants and noxious prey), so food mixing tems. limits the ingestion of particular compounds from par- We think that understanding the behavioral causes ticular food types; (4) the relative quality of food types of omnivory will inform its ecological consequences. changes over time, so food mixing allows the animal It is too often assumed, for example, that nutritional to periodically sample different food types and switch constraints (including food availability) uniquely de- to a currently superior food type; (5) food mixing may termine the function of food mixing behavior under- minimize exposure to other environmental risks (e.g., lying omnivory. Here we consider some alternative, natural enemies, abiotic factors). functional explanations for food mixing. One of our A potentially separate but related issue is the func- main points is that food mixing per se and selecting tional basis for selecting particular food types in the particular foods are actually different issues and may mixture. Indeed, there may be functional differences need separate consideration, conceptually and empir- between the basis for mixing and the basis for selecting particular foods. While both contribute to an individ- ual's pattern of foraging and diet, they are separate Manuscript received 5 July 2002; revised 11 October 2002; accepted 17 October 2002. Corresponding Editor: A. A. Agrawal. issues and addressing them may require separate ex- For reprints of this Special Feature, see footnote 1, p. 2521. periments. For example, a food mixing animal that en- 1 E-mail: [email protected] counters hypothetical food types A, B, and C may select 2532 October 2003 WHY OMNIVORY? 2533 all three, or only two of them. Food selection patterns other animals. However, the critical decisions to eat a may differ for a given mixture of food types: this an- particular food in the ®rst place, and to continue eating imal may eat a large amount of A relative to B and C, it rather than the available alternatives are likely to or feed in some other pattern. Although food mixing depend proximately and ultimately on other aspects of per se and speci®c food selection go hand in hand, they food quality (e.g., secondary metabolites, physical bar- may have different functional explanations. To contin- riers to feeding), ecological risks (e.g., natural enemies) ue the above example, the function of mixing foods A, and competing needs (e.g., thermoregulation) that may B, and C may be to obtain a balanced intake of nutri- modify or take precedence over responses to food's ents, or to minimize the intake of particular toxins as- nutritive value. Further, foraging decisions of this sort sociated with each food. However, food A may be eaten that accumulate into patterns of mixing and selecting in the largest amount because it is the most abundant foods (i.e., diet) may vary according to the consumer's food type or it provides a physical or chemical defense experience and the prevailing environmental conditions against natural enemies. It is also possible that a food (e.g., availability and quality of alternative foods). We of seemingly less importance, like food B or C, pro- expect the relative importance of these factors, and vides a critical micronutrient or chemical used in re- precisely how they interact, to vary depending on the production, making it essential for survival and repro- natural history of the omnivore. However, we will em- duction. The numerous possible reasons for selecting phasize the complex roles of noxious chemicals and particular foods have been reviewed elsewhere (e.g., natural enemies because their importance has been rel- Stephens and Krebs 1986), and we will not attempt this atively neglected. here as it is not an issue unique to food mixers. Despite the abundance of nonexclusive hypotheses EVIDENCE FOR ALTERNATIVE DETERMINANTS OF for both mixing and selecting foods, studies of food FOOD MIXING AND FOOD SELECTION mixing by omnivores have often focused on how nu- We believe the importance of mixing and selecting tritional constraints may drive food mixing (hypotheses foods to avoid overingestion of particular secondary 1, 2, and 4 above) and food selection, with scant em- metabolites (toxin dilution: Freeland and Janzen 1974) Feature Special pirical attention given to the rest. We do not think any is vastly underappreciated. Freeland et al. (1985) of the above hypotheses (for food mixing or food se- showed that food mixing by mice can counteract neg- lection) is generally tested at present because few stud- ative effects of individually harmful secondary metab- ies have employed critical experiments to distinguish olites. This laboratory study demonstrated reduced among them. Nevertheless, several current notions in growth rates for mice given foods with tannins or sa- community, food web, and assume ponins, and for those given a food containing set con- that constraints imposed by nutrients primarily, if not centrations of both toxins (no-choice trials). However, exclusively, determine patterns of mixing and selecting when mice were allowed to choose between foods con- food by omnivores and herbivores. This assumption, taining either tannins or saponins, growth rates were for example, apparently underlies the recent approach no different from those of control mice given food of reducing such trophic interactions to the ratios of without toxins. Similar studies with other species and essential atomic elements across trophic levels (``eco- their natural foods are needed. Agrawal et al. (1999) logical stoichiometry'') to understand food web dy- showed that the induction of elevated secondary me- namics and nutrient cycling (e.g., Elser et al. 2000, tabolites in cotton plants promoted switching from her- Sterner and Elser 2002, Denno and Fagan 2003). Ex- bivory to predation of mite eggs by the omnivorous trapolating trophic interactions to food web dynamics thrips, Frankliniella occidentalis. Thrips performance strictly on the basis of nutritive elements ignores much was reduced on induced plants without mite eggs, sug- empirically documented, meaningful complexity in ter- gesting that the deterrence or toxicity of secondary restrial (e.g., Stamp and Casey 1993, Abrahamson and metabolites in cotton was driving switching behavior. Weis 1997, Dicke 2000, Schmitz and Suttle 2001) and Various studies have shown that secondary metabolites marine (reviewed in Paul et al. 2001) trophic interac- deter food-mixing insects. For example, secondary me- tions. For example, it is often assumed that animal food tabolites produced by plants (Dyer et al. 2001) and is more nutritious than plant food. Several recent stud- various compounds sequestered by caterpillars from ies show that this is not necessarily the case (e.g., Eu- their host plants (Dyer 1995, Dyer and Bowers 1996) banks and Denno 1999, Cruz-Rivera and Hay 2000). deter omnivorous ants, suggesting that toxin avoidance While it may be true that nutrient ratios of prey tissues in¯uences food selection by this ecologically important are usually more similar to an animal consumer than group of omnivores (Tobin 1994). To our knowledge, those of plant tissues, a consumer's growth, survival, no studies have yet tested the in¯uence of secondary and reproductive responses depend on its particular metabolites on food mixing per se by omnivorous ants. feeding behavior (i.e., tissue selection) and physiology Many secondary metabolites evoke a ``bitter'' taste as well as other aspects of food quality (e.g., toxins). response in , yet behavioral responses by food There is no doubt that nutritive needs are important mixing mammals to ecologically relevant mixtures of determinants of foraging choices by omnivores and food types containing them are rarely measured. In a Special Feature hc r elkont eetfo ntebssof caterpillar found bear basis geneura woolly have forb-feeding the Grammia the we by on mixing example, herbivores, food food For reject generalist metabolites. to by secondary known an well than are to extent which omnivores by greater selection even food in¯uence neg- may toxins atively and deterrents that browsers. implies then pattern This grazers, of omnivores, by likelihood sen- followed most expected were sitive, response carnivores the food: rejection in to toxins related encountering bitter be the to threshold found (1994) dinning Glen- browsers), grazers, omnivores, strat- foraging (carnivores, differing egies with species 30 of test 2534 rnei epnet aaieatc.Tefo mixing food caterpillar, The bear attack. woolly parasite to response in erence Field 2001). omnivorous needed. with al. are issue et this addressing (Vitazkova studies to their increasing resistance thereby ingested chloroquine, routinely of amounts mice one small study, In resistance. laboratory parasite interesting with for foods metabolites select food-mixers secondary that (e.g., suggest studies 1997) Various a Hart like- parasites. for its transmitting evidence and of value is lihood nutritive (Pfennig there food's cases, a tadpoles between these trade-off of omnivorous both and In et 2000). 2002) (Hutchings grazers 1999, vertebrate al. by selection food patterns of gen- explains of example, quite for use be avoidance, may Parasite the latter eral. and the for resistance, metabolites and secondary basis avoidance the on parasite partly of food select animals food-mixing of is species. pre- effect host-plant from ferred tritrophic acquired metabolites this secondary suspect by mediated we cost; at parasitoids nutritional species to a plant resistance ``toxic'' caterpillar's certain a increase on may feeding case, 2003). Stireman this and par-In of (Singer likely value species defensive host-plant is and ticular nutritive preference) the (i.e., both al. on selection et based (Singer food Yet dilution toxin 2002). me- with secondary consistent plant tabolites to response behavioral negative, gn eg,Lm n il19,HumnadDill and Houtman 1990, Dill and Lima for- (e.g., on aging constraints ecological and evolutionary portant Wolfe and (Clayton suspected is than 1993). or widespread more known far currently be may careful and through revealed This observation, been only 2001). has (Huffman behavior of species infections type plant parasite particular reduce of that parts by ingesting nature selectively in ) sur- termed frequently pharmacophagy (speci®cally exhibit host commonly the particular and Sick this vive. parasitoid In the survival both 1997). case, its English-Loeb and increasing to (Karban thereby response in infection, preference parasitoid host-plant its changes idae) oefo-iigaiascag hi odpref- food their change animals food-mixing Some range wide a that suggests evidence Accumulating aysuisageta rdto ikpae im- places risk predation that argue studies Many Acide ob rdmnnl a predominantly be to (Arctiidae) ltpei virginalis Platyprepia IHE .SNE N LZBT .BERNAYS A. ELIZABETH AND SINGER S. MICHAEL (Arcti- nsc ok o xml,teonvru ant omnivorous the example, For work. McCarthy such prominently and in ®gured have Sih animals 1999, Food-mixing Bednekoff 2002). and Lima 1998, o osmr,arltvl ml oeo medicinal a of dose small relatively population. a a the in consumers, increase plants For individual greatly killing may of shoots) likelihood young from extract- pith (e.g., ing tissue the medicinal example, critical for some resources, of removal of case the consumer In and populations. have resource both may on consumption impact great their relatively rel- types, a small food be other may to ingested ative foods medicinal the of zoophar- Although amount of 2001). example (Huffman primates the in to macognosy point we consequences. this, se- ecological illustrate food To their and determine mixing may food in lection variation fac- govern precise that the tors think we Tardiff Furthermore, residents, 1978). vs. Gray immigrants and 2001; al. et differenc- Hailey sexual es, (e.g., population conspeci®c a and envi- within 1999), or individuals Bradtke populations Dilks and 1998), (Wilson and al. ronments et O'Donnell varies Ellis (, rodents, nature 1994; species in omnivores related by among consumed of quantities types relative food and range omnivore The another. one food by by to mixing equivalent mixing ecologically be food to assumed that be pres- clear cannot at is question it this Yet, address ent. to data limited scales? ecological are larger There at matter selection food of and orssipsdb e rdtr n aaiod,re- parasitoids, and predators response key in at spectively. 1998) by only Seike imposed forage abundance and risks (Orr may to food day ants of lower and times 2002) certain and al. 1996) (e.g., et cover (Abramsky al. vegetative et with patches Abramsky exclu- feed in food may sively available rodents of polyphagous range Highly the species. changing times particular thus to places, feeding and limit and and Sih 2002), 1999, McCarthy Bednekoff and (Lima foraging in¯uence Suttle and (Schmitz ®elds old 2001). in herbivory of different causing patterns turn in , responses polyphagous feeding by of different cause species from a depend within risk spiders not predation may of dif- example, types or another ferent may In reward. that nutritional food's way a on a of of in levels quantity risk different and to predation response range in the taken foods vary col- particular ant would that nature suggest in studies onies These 1999). (Folgarait Gilbert quantity food and of regardless in manner ants) same the the to predators (effectively parasitoids phorid tde hwta h mioos®eant ®re omnivorous the that Field 1990). show Dill and studies (Nonacs risk species predation ant with another from quality food balancing by ronment richteri pallitarsis o uhde aito ntebsso odmixing food of bases the in variation does much How eprlvraini h heto rdto may predation of threat the in variation Temporal E COLOGICAL eue oaigatvt ntepeec of presence the in activity foraging reduced eetdfo ace nalbrtr envi- laboratory a in patches food selected C NEUNE OF ONSEQUENCES clg,Vl 4 o 10 No. 84, Vol. Ecology, F OOD M Solenopsis IXING Lasius October 2003 WHY OMNIVORY? 2535 plant may determine the life or death of infected in- scales, for example, omnivorous birds may forage by dividuals, with important consequences for the popu- migrating between patches with different food types. lation's demography. Some species may feed primarily on plant or fungal The ¯exibility of food selection exhibited by indi- material or arthropod prey in each one (O'Donnell and vidual omnivores has pivotal but complex consequenc- Dilks 1994). At large temporal scales, a related strategy es for population, community, and food web dynamics. is switching between food types over the season. Several authors have recently made this general point O'Donnell and Dilks (1994) show that omnivorous (Agrawal et al. 1999, Agrawal and Klein 2000, Coll birds in a temperate New Zealand forest switched be- and Guershon 2002). Here we elaborate a bit further. tween speci®c foods during the year. Seasonal food While it is currently argued that omnivory stabilizes switching by omnivores typically involves relatively of both consumers and their re- increased carnivory during the breeding season and rel- sources (e.g., prey and plants), this putative stabilizing atively increased herbivory (including granivory) dur- effect depends on food-mixing behavior. The stabili- ing the rest of the year (Polis and Strong 1996). A third zation of omnivore populations follows from the ability related food-mixing strategy at relatively large tem- to switch from one food type to another (i.e., food poral scales involves ontogenetic shifts in food selec- mixing) when the ®rst food is depleted or absent (e.g., tion. Such omnivores may typically feed primarily on Naranjo and Gibson 1996, Fagan 1997, Eubanks and prey during periods of rapid growth (e.g., early de- Denno 1999). Populations of prey or plants may be velopment; McCauley and Bjorndal 1999, Choat and stabilized by the refuge created when their omnivorous Clements 1998) and during reproductive periods, while consumers switch to alternative food rather than con- feeding primarily on plant material during other parts tinuing to reduce populations at low levels (e.g., Cot- of the life cycle. trell and Yeargan 1998, Lalonde et al. 1999) or when Small-scale food mixing may result in weak and dis- the trophic interaction between omnivores and their persed trophic interactions in food webs, however its food is dampened by intraguild predation (Rosenheim impact is relatively unstudied. This type of food mixing 2001). However, the existence of this refuge over the occurs within small-scale patches of variable food Feature Special long term is not clear. High quality alternative food types and a temporal scale of days, hours, or minutes. may maintain large omnivore populations that continue Highly omnivorous rodents (Ellis et al. 1998) and ar- to suppress populations of prey (Eubanks and Denno thropods (e.g., ants; Stradling 1987) exemplify such 2000) and perhaps those of competing carnivores (M. extreme food mixers, and undoubtedly have important E. Hay, personal communication). roles in food webs. In most cases studied to date, the How do these population level effects extrapolate community and food web consequences of mixing and into food web dynamics and community structure? food selection have yet to be tested. A few recent stud- There is presently no clear answer. The stabilizing ef- ies have been done with food mixing grasshoppers fect of food mixing by omnivores is associated with (e.g., Beckerman et al. 1997, Schmitz et al. 1997, weak trophic links in the web. Recent theory (e.g., Polis Schmitz and Suttle 2001), showing that predator-in- and Strong 1996, McCann et al. 1998) and empirical duced changes in small-scale food mixing by grass- evidence from simple food webs (Fagan 1997, Holyoak hoppers can have a large impact on the plant com- and Sachdev 1998) support the idea that omnivory sta- munity. bilizes food webs via weak trophic interactions. In ``weak'' interactions, however, indirect effects of al- CONCLUSION ternative foods can magnify the variance in interaction The causes and consequences of omnivory depend strength between consumers and prey, with seemingly on foraging behavior. We have focused on some func- important, unstudied consequences for community tional reasons for mixing foods and selecting particular structure (Berlow 1999). Furthermore, evidence from foods that have received less attention than constraints complex ecosystems shows that it is the pattern of weak imposed by nutrients. Nutritive factors alone cannot be trophic interactions that accounts for food web stability assumed to explain the ecologically important variation rather than interaction strength per se (de Ruiter et al. in food mixing and food selection in terrestrial and 1995). marine ecosystems. We think an understanding of om- nivory will be advanced by the use of critical experi- SPATIAL AND TEMPORAL SCALE OF FOOD MIXING ments that consider multiple, ecologically relevant, We think the ecological impact of food mixing re- functional hypotheses for mixing and selecting food. sults from its spatial and temporal scale, in addition to Some key questions include: What factors in¯uence the functional bases of food mixing and food selection. decisions to leave one food and accept others? What Murdoch (1969) made a similar point, but few studies choices are made when food-mixing species face mul- have followed this line of work. Large-scale food mix- tiple food types with different bene®ts and costs? Di- ing may typically involve dietary speci®city at partic- rect observations in nature will be valuable in design- ular times and places with consequences similar to the ing appropriate experiments because the central issue impact of feeding by dietary specialists. At large spatial is how factors such as nutrient balancing, toxin dilu- Special Feature basy . .Srus .Sbc,adB .Kte.1996. Kotler. P. B. and Subach, A. Strauss, E. Z., The Abramsky, 2002. Subach. A. and Rosenzweig, L. M. Z., Abramsky, Evolutionary 1997. Weis. E. A. and G., W. Abrahamson, ecosystem and web, dynamics. food community, consequences to population, scales) for temporal and spatial causes, different different ®rmly (e.g., mixing investigators Only food in can several? variation connect questions or such another answering versus by cause is one that mixing by food driven of consequences such ecological one the what are does And behavior? food-mixing circumstances drive several out what or factor play Under risk nature. of in avoidance and pharmacophagy, tion, 2536 n naoyosrvee o epu icsinadcri- Weeks, and J. discussion manuscript. Perlman, helpful the S. for of Hunter, reviewer tiques S. anonymous M. an Holland, and N. J. Hay, E. ha,J . n .D lmns 98 etbaeherbivores Vertebrate 1998. in Clements. D. interactions K. weak and H., of J. Choat, effects Strong 1999. L. E. Berlow, Ex- 1997. Schmitz. J. O. and Uriarte, M. P., A. Beckerman, otel .E,adK .Yagn 98 feto olnon pollen of Effect 1998. Yeargan. V. 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October 2003 WHY OMNIVORY? 2537

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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 . 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 . 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, , 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 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 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 ), 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. 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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. 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Kraig, rTierpsychologie Èr 20 :410±433. clg,Vl 4 o 10 No. 84, Vol. Ecology, 18 :305±348. 108 :167± 142 : Ecology, 84(10), 2003, pp. 2549±2556 ᭧ 2003 by the Ecological Society of America

THE EVOLUTION OF OMNIVORY IN HETEROPTERAN INSECTS

MICKY D. EUBANKS,1,3 JOHN D. STYRSKY,1 AND ROBERT F. D ENNO2 1Department of Entomology and Plant Pathology, Auburn University, Auburn, Alabama 36849 USA 2Department of Entomology, University of Maryland, College Park, Maryland 20742 USA

Abstract. Although omnivory is common and widespread across many animal taxa, the evolutionary origin of omnivory, the selective forces that promote or constrain omni- vory, and the morphological, physiological, and behavioral hurdles that animals have to overcome to become omnivores have not been studied. The goal of this paper is to stimulate the development of ideas concerning the evolution of omnivory. We focus on the terrestrial lineages of the insect order Heteroptera and use published life history data and recent phylogenies to test two hypotheses concerning the evolutionary origin of feeding on both plants and prey: (1) that the propensity to feed on seeds and pollen is correlated with the evolution of omnivory, and (2) that broad host range (polyphagy) is correlated with the evolution of omnivory. In order to test these hypotheses, we mapped the plant part consumed and host plant range of insect species in two heteropteran suborders onto their respective phylogenies and used phylogenetically independent contrasts to test for correlations of these traits with omnivory. We found evidence that seed and pollen feeding and broad host ranges are correlated with the evolution of omnivory within both ancestrally herbivorous and ancestrally predaceous lineages of terrestrial heteropterans. Key words: feeding habits; herbivory; Heteroptera; omnivory; predation; seed and pollen feeding; sister-group comparisons. pca Feature Special

INTRODUCTION holding prey) (Faucheux 1975, Cobben 1979, Cohen 1996). Feeding on both prey and plant food is a widespread The ecological signi®cance of omnivory has histor- feeding habit in insects (Whitman et al. 1994, Alomar ically received little attention. Recent studies, however, and Wiedenmann 1996, Coll and Guershon 2002). suggest that omnivory can deny prey density-related Thousands of omnivorous insect species occur through- refugia from predation, dictate the strength of top-down out a broad range of insect taxa, including grasshop- control and resulting trophic cascades, alter the stabil- pers, earwigs, thrips, true bugs, beetles, and ants. These insects represent a unique blend of morphological, ity of food webs, and profoundly in¯uence the move- physiological, and behavioral adaptations found in ment of energy and nutrients through ecosystems (Polis their predaceous and herbivorous relatives. Omnivo- et al. 1989, Polis 1991, Polis and Strong 1996, Fagan rous insects in the order Heteroptera (true bugs), for 1997, Holt and Polis 1997, Ostrum et al. 1997, Holyoak example, possess digestive tracts and accessory sali- and Sachdev 1998, McCann et al. 1998, Rosenheim vary glands that are intermediate in length, size, and 1998, Eubanks and Denno 1999, 2000). placement of those found in their herbivorous and pre- Studies of the evolution of omnivory, in contrast, are daceous relatives (Slater and Carayon 1963, Goodchild almost nonexistent in the literature (but see Cooper 1966). In addition, many species of omnivorous het- 2002, Denno and Fagan 2003, Diehl 2003). We know eropterans produce protein-digesting enzymes (pro- relatively little about the adaptive advantages of om- teinases and phospholipases) and plant-digesting en- nivory and the selective forces that favor or constrain zymes (amylases and pectinases) whereas their strictly the evolution of omnivory. The evolution of the mor- herbivorous and predaceous cousins produce only a phological, physiological, and behavioral traits asso- subset (Baptist 1941, Goodchild 1966, Kahn and Ford ciated with omnivory have not been studied and we do 1967, Miles 1972, Varis et al. 1983, Cohen 1990, 1996, not know if these traits evolve as a suite of correlated Schaefer and Panizzi 2000, Wheeler 2001). Omnivo- characters. Further, we know very little about the evo- rous heteropterans also have piercing-sucking mouth- lutionary consequences of evolving the ability to feed parts (stylets) with characteristics of both herbivorous on both plants and prey. For example, the evolution of heteropterans (smooth stylets to penetrate plants) and omnivory might in¯uence the diversi®cation rate of predaceous heteropterans (toothed or curved stylets for omnivorous taxa, but questions such as this have not been raised in the literature. The goal of this paper is to stimulate the devel- Manuscript received 5 July 2002; revised and accepted 28 opment of ideas concerning the evolution of omni- October 2002. Corresponding Editor: A. A. Agrawal. For reprints of this Special Feature, see footnote 1, p. 2521. vory. Insight into the evolutionary origin of omnivory 3 E-mail: [email protected] will help us understand the adaptive signi®cance of 2549 Special Feature loafc hi rpniyt vleteadaptations 1979). Cobben the 1979, (Sweet evolve feeding prey to for necessary propensity their affect also both from omnivory of predation. evolution and transi- herbivory a the be in to state seeds hypothesized tional on therefore, Feeding is, to 1979). pollen similar and Cobben parts more 1979, plant nutritionally (Sweet nitrogen are prey pollen) high and because (seeds foliage feed that plant omnivores than on pollen omnivores and to seeds rise on hy- give feed to that are likely more insects be to of be- pothesized lineages match nutritional predaceous a Conversely, prey. nitrogen-rich of and parts basis plant nitrogen-rich the tween on This predicted 1979). Cobben is foliage- 1979, to (Sweet of rise herbivores lineages feeding give than frequently will more herbivores of omnivores pollen-feeding lineages or that consequently, seed and, ni- prey consume to trogen-rich preadapted 2001). be may pollen- Wheeler herbivores and feeding seed 2000, that hypothesized Cohen have Panizzi authors 1985, Some and Kirk Schaefer 1984, al. 1996, pollen-feeding et and en- (Houseman seed these their relatives but by pollen, produced and are seeds zymes in found digest to proteins them the allow would produce that enzymes not digestive do the species 1985). Kirk foliage-feeding 1979, example, (Janzen plants For or part plant particular a host on their feed of al. to herbivorous adapted result, et usually a are Strong As insects 1988). 1979, me- al. et al. antiherbivore Thomison et of 1984, (Tamas degree defenses and type chanical the of and concentrations allelochem- icals, the defensive , in nutrients, vary Weaver other also and Douglas parts 1984, Plant Cordova-Ed- al. 1989). and et Strong Murray 1984, 1982, wards Evans 1935, (An- respectively) drews 0.0002%, nitrogen and less (0.005% even leaves contain nitrogen than tissues 10% xylem and nitrogen. to 0.7% Phloem as little up as contain Seeds often contain leaves 1984). whereas frequently al. et pollen (Strong and insects most limiting important for an is nutrient concentra- nitrogen the and in nitrogen tremendously of of vary tions parts can species plant Different the host 1979). by same Cobben consumed part 1979, plant (Sweet the may to prey consume related and be capture to ability the species evolve herbivorous to an of propensity the herbivory, of with omnivory. associated of is evolution (polyphagy) (2) the range and host omnivory, of broad evolution that pollen the and seeds with on correlated feed is to and tendency plants the both that on (1) feeding prey: of origin and concerning evolutionary hypotheses data the two order test history insect to life phylogenies the published recent of use We lineages and food. terrestrial Heteroptera plant must the and on animals prey focus both that consume hurdles to overcome behavioral physio- morphological, and the logical, elucidate and omnivory 2550 h otrneo ebvru netseismay species insect herbivorous of range host The state ancestral an from omnivory of evolution the In IK .EBNSE AL. ET EUBANKS D. MICKY ots o orltosbtenteetat n omni- and traits these between vory. correlations contrasts for independent test to phylogenetically used phyloge- two and respective in nies their insects onto of range suborders plant heteropteran host plant and the consumed mapped parts we omnivory, of origin evolutionary om- of evolution the nivory. regarding historical ideas and test biological to rich framework Heteropter- a 1998). provide Coll therefore, Schuh 1995, ans, 1979, Slater Sweet and Schuh 1979, 1986, (Cobben herbivores giving to lineages rise predaceous and predators lineages to herbivorous rise with giving order, mul- this evolved within have times habits tiple feeding three the addition, relationships. In evolutionary well- and relatively taxonomic have established and biologies, di- well-known have have species, omnivorous they many because contain habits, studying habits feeding verse for feeding group of Ter- evolution ideal the Heteroptera. an order are ter- insect heteropterans several restrial the of of history lineages evolutionary restrial and histories life they plants host the about speci®c consume. are very omnivores be these to taxa, unlikely plant spe- for speci®c selection on to undergo cialization likely they Until also recently polyphagous. are be have lineages predaceous that within evolved species omnivorous om- relatives. evolve monophagous Conversely, their to are likely than her- species more nivorous polyphagous be may of consume therefore, Lineages and bivores, attack 2001). to (Wheeler predisposition prey their as well requirements monophagous nutrient as their their affect may than this often and relatives move more oli- far herbivores or plants Polyphagous among monophagous their relatives. than gophagous omnivorous they that be likely more will it make that (Sweet traits behavioral also species have may herbivores monophagous Polyphagous 1979). than Cobben 1979, prey consume likely more to species polyphagous detox- make as enzymes such ifying adaptations that Some suggested have 1997). authors Minkenberg and (Bernays allelochemical-based defenses have of plant and variety a species detoxify plant to of ability enzymes the variety a the digest produce to For necessary lifestyle. insects omnivorous polyphagous an families) example, to plant themselves more lend or may two representing di- plants on (feeding verse polyphagy with taxa associated adaptations behavioral plant and of physiological, morphological, spe- diversity The insect cies. omnivorous the or herbivorous by an by de®ned consumed is range Host 2fmle,adtosbresfo 4 published 146 terrestrial the from on focused suborders We Appendices). two (see sources genera, and 232 families, in 22 distributed heteropterans terrestrial of nodrt etortohptee ocrigthe concerning hypotheses two our test to order In the on focusing by hypotheses these evaluated We eetatdlf itr nomto o 9 species 398 for information history life extracted We M ETHODS clg,Vl 4 o 10 No. 84, Vol. Ecology, October 2003 WHY OMNIVORY? 2551 heteropterans in the suborders Cimicomomorpha and TABLE 1. Numbers of omnivores and herbivores used in eight independent contrasts to test for correlations of feed- Pentatomomorpha because they include large numbers ing habit with plant part consumed (foliage vs. reproductive of herbivores, omnivores, and predators, and because parts) and with host range (monophagy or oligophagy vs. strict herbivory, omnivory, and strict predation have polyphagy). evolved independently multiple times within these groups (Cobben 1979, Sweet 1979, Schuh 1986, Schuh No. No. omnivores herbivores and Slater 1995, Alomar and Wiedenmann 1996). We Taxa in contrast in contrast used the most recent phylogenies for each suborder, Miridae 54 66 Schuh and Stys (1991) for the Cimicomomorpha (Ap- Pentatomoidea² 28 64 pendix A) and Henry (1997) for the Pentatomomorpha Alydidae ϩ Coreidae 1 14 (Appendix B), for our analyses. Both of these phylog- Rhopalidae 1 3 Pyrrhocoridae 2 7 enies are based on morphological characters. These two Berytidae 7 4 lineages are particularly useful for this study because Ishnorhynchinae ϩ Orsillinae 1 8 the Cimicomomorpha is ancestrally predaceous and the Lygaeinae 3 7 Pentatomomorpha is ancestrally herbivorous (Sweet ² Includes families Acanthosomatidae, Cydnidae, Penta- 1979, Cobben 1979, Schuh 1986, Schuh and Stys 1991, tomidae, Scutelleridae, and Thyreocoridae. Henry 1997). The correlation of seed and pollen feed- ing and broad host range with the evolution of omni- vory in both lineages would suggest that these traits orous; Table 1). This procedure reduced our data to play a pivotal role in the evolutionary transition from eight family-level groups (Table 1). We then conducted herbivory to omnivory and from predation to omni- a logistic regression analysis with family group, plant vory. part consumed (foliage or reproductive), and host range For each heteropteran species surveyed, we scored (restricted or polyphagous) as predictor variables and the family and subfamily classi®cation, the plant part

feeding habit (herbivory or omnivory) as the dependent Feature Special consumed by the species, and whether or not the spe- variable (SAS version 8.2, Proc Logistic with class cies consumed prey. From this information, we char- statement; Stokes et al. 2000). acterized the species' feeding habit as strictly herbiv- This analysis corrects for phylogenetic noninde- orous (consumes only plants), omnivorous (consumes pendence among family-level groups, but treats spe- plants and prey), or strictly predaceous (consumes only cies within these groups as independent and does not prey). We also characterized the species host range as control for phylogenetic non-independence at levels monophagous (consumes plants belonging to one ge- above family. The second analysis controls for phy- nus), oligophagous (consumes plants in two or more logenetic nonindependence at all levels and is con- genera within the same plant family), or polyphagous sidered a conservative test of correction for similarity (consumes plants in two or more families). due to common ancestry. In this analysis, we reduced We used two analyses to control for possible phy- logenetic nonindependence among heteropteran spe- the data set further to include only phylogenetically cies. Our approach follows that of Fagan et al. (2002) independent contrasts among sister taxa (Ridley 1983, and all methods are based on the principal of phylo- Felsenstein 1985, Harvey and Pagel 1991). This re- genetically independent contrasts (Felsenstein 1985). quired that we assign a feeding habit to each family- The two tests represent each end of the continuum be- level group. If all species within a group were her- tween strictness of correction for similarity due to com- bivorous, then we scored that group as herbivorous. mon ancestry and potential statistical power (Mazer If some or all species within the group were omniv- 1998, Ackerly and Reich 1999). We used both liberal orous, then we scored that group as omnivorous. We and conservative techniques to control for phylogenetic identi®ed four meaningful phylogenetically indepen- constraints because omnivory has evolved multiple dent contrasts using the phylogenies of Schuh and times within multiple heteropteran lineages and is un- Stys (1991) and Henry (1997): Miridae (omnivorous) likely to be highly conserved (i.e., is phylogenetically vs. Tingidae (herbivorous), Coreidae (herbivorous) labile). vs. Alydidae (omnivorous), Berytidae (omnivorous) The ®rst analysis partitioned species into a set of vs. Colobathristidae (herbivorous), and Ischnorhyn- family-level groups each containing at least one phy- chinae (omnivorous) vs. Orsillinae (herbivorous). We logenetically independent contrast between herbivores used two 2 ϫ 2 contingency table analyses to test the and omnivores (sensu Fagan et al. 2002). These group- hypotheses that evolutionary changes in feeding habit ings corresponded to single, monophyletic taxa in the were independent of plant part consumed and host case of the superfamily Pentatomoidea, the families range. A signi®cant G is evidence that pairs of char- Berytidae, Miridae, Pyrrhocoridae, and Rhopalidae, acter states are not independent, but that some com- and the subfamily Lygaeinae. In other cases, these fam- binations of characters are more or less common than ily-level groups consisted of pairs of sister taxa with expected by chance (Ridley 1983, Harvey and Pagel different feeding life histories (omnivorous vs. herbiv- 1991). Special Feature ␹ ϭ 2552 nflaewr mioos(i.1.Teefc of (Wald effect signi®cant The not was 1). analysis this (Fig. in group omnivorous fed family that were species pollen the foliage and of seeds on 25% Bery- on only the fed and that in omnivorous species were striking the more of even 85% (Fig. tidae: was omnivorous were pattern foliage This on 1). fed of that 37% only species reproduc- whereas on the omnivorous fed were that parts species Miridae, plant the tive the of In omnivorous 53% 1). be example, for (Fig. to species likely foliage-feeding more than were pollen and seeds nivory fteegtfml-ee rusue norlgsi ersinaayi.Msigbr niae`zr' values. ``zero'' indicate bars Missing analysis. regression logistic our in used groups family-level eight the of h ee ffml ru (Wald group at family nonindependence of level phylogenetic the for analysis the controlled in signif- habit feeding that a on part was the plant There of with effect pollen. icant correlated and is seeds of omnivory consumption of evolution the that in®atymr ieyt eonvru hntheir than omnivorous ( taxa be were sister pollen foliage-feeding to and likely seeds on more fed signi®cantly that taxa analysis, levels. this all In at nonindependence phylogenetic for trolled 2 pce fet t rpniyt eonvru.There heteropteran omnivorous. a be to of propensity range its host affects species the that evidence found aooopa eg,Brtdei i.1). Fig. in (Pen- Berytidae lineage (e.g., herbivorous ancestrally tatomomorpha) the ancestrally and 1) the Miridae Fig. in both (e.g., (Cimicomomorpha) to in lineage appeared omnivory predaceous pollen with and correlated seeds be on feeding addition, In F oyhg screae ihomnivory with correlated is Polyphagy om- with correlated is pollen and seeds on Feeding .4) vrl,htrpea pce htconsumed that species heteropteran Overall, 0.045). ϭ efudtesm atr nteaayi htcon- that analysis the in pattern same the found We IG .Pretgso pce htaeonvru mn pce htfe nflaeo nsesadple,i each in pollen, and seeds on or foliage on feed that species among omnivorous are that species of Percentages 1. . 11,df 11.10, Ðefudsrn upr o h hypothesis the for support strong found .ÐWe ϭ 7, P R ϭ ESULTS 0.134). G ϭ .,df 6.1, ␹ 2 ϭ ϭ .1 df 4.01, 1, IK .EBNSE AL. ET EUBANKS D. MICKY P Ðealso .ÐWe Ͻ 0.025). ϭ 1, P edn ai nteaayi htcnrle o phy- for (Wald level controlled family-group on that the range analysis at logeny host the of in affect habit signi®cant feeding statistically a was anonvru pce hntermnpaosor monophagous ( their taxa sister than oligophagous species omnivorous con- to tain likely more signi®cantly levels: were taxa all polyphagous at nonindependence phylogenetic for trolled omnivores. of distribution phylogeny of the effect on an was there that indicating 0.038), ϭ ihteeouino mioyi ersra heterop- terrestrial in correlated omnivory are of range evolution plant the host with broad and feeding len ettmie,teAlydidae the Pentatomoidea, sssaitcly hr a ttsial signi®cant (Wald group statistically family a of hypoth- was effect this There neither test was statistically. to set enough esis data balanced more nor our are enough but large species omnivorous, be monophagous to groups likely other omnivorous in be to and likely more groups are some in effect species that polyphagous such interactive range an host and be group family may These of there 2). that (Fig. in suggest Pyrrhocoridae evident results the was and pattern Rhopalidae opposite the The 2). (Fig. gaeinae a,teIschnorhynchinae the dae, a nFg 2). ancestrally Fig. the in Beryti- dae and (e.g., 2) (Pentatomomorpha) Fig. lineage herbivorous in (Cimicomo- Miridae lineage (e.g., predaceous in morpha) ancestrally correlated be the to appeared both omnivory and range Host eswtesm atr nteaayi htcon- that analysis the in pattern same the saw We u eut upr h yohssta edadpol- and seed that hypotheses the support results Our 1, P Ͻ .0) hswseieti h iia,the Miridae, the in evident was This 0.001). D ISCUSSION G ϩ ϭ ␹ ϩ .,df 6.0, rilne n h Ly- the and Orsillinae, 2 clg,Vl 4 o 10 No. 84, Vol. Ecology, ϭ oede h Beryti- the Coreidae, 48,df 14.83, ϭ ␹ 1, 2 P ϭ Ͻ ϭ 65,df 26.52, 0.025). 7, P ϭ October 2003 WHY OMNIVORY? 2553

FIG. 2. Percentage of species that are omnivorous among species with restricted host ranges (monophagous ϩ oligoph- agous) or broad host ranges (polyphagous) in each of the eight family-level groups used in our logistic regression analysis. Missing bars indicate ``zero'' values. pca Feature Special

terans. Heteropteran species that fed on seeds and pol- be addressed by comparative studies of closely related len were signi®cantly more likely to be omnivorous herbivores, omnivores, and predators. than their foliage-feeding relatives (Fig. 1). Likewise, polyphagous species were signi®cantly more likely to Ecological consequences be omnivorous than their relatives with restricted host ranges (monophagous or oligophagous), although this The consumption of seeds and pollen as well as po- effect may vary to some extent among family-level lyphagy could dramatically affect the spatial and tem- groups (Fig. 2). These patterns were apparent when we poral abundance of omnivorous insects. Omnivores used both liberal and conservative methods to control that consume seeds and pollen may be forced to track for the effects of phylogeny on the evolution of om- changes in the abundance of these plant resources in nivory and were apparent in both ancestrally preda- space and time (Eubanks and Denno 1999, 2000). Om- ceous (Cimicomomorpha) and ancestrally herbivorous nivorous insects are noted for their attraction to pollen (Pentatomomorpha) lineages. and seeds (Kiman and Yeargan 1985, Read and Lamp- We suggest that seed and pollen-feeding insects are man 1989, Coll and Bottrell 1991, 1992) and some preadapted to consume prey and that predaceous insects studies even suggest that omnivorous ``predators'' ac- are similarly predisposed to consume nitrogen-rich tually track variation in the production of seeds and plant parts. Preadapation may be associated with phys- pollen more than they track variation in the population iological traits. For example, the digestive enzymes size of prey (Cottrell and Yeargan 1998, Eubanks and produced by seed and pollen-feeding herbivores may Denno 2000). The impact of these omnivores on prey be able to digest prey. Similarly, the digestive enzymes is largely dictated by variation in the abundance of produced by predators may be able to digest seeds and seeds and pollen because the presence of high quality pollen. Further, some morphologies or behaviors of plant food not only affects omnivore abundance, but seed and pollen-feeding herbivores and predators may also alters the per capita consumption of prey by om- be functionally interchangeable. For example, how nivores (Cottrell and Yeargan 1998, Eubanks and Den- similar do the mouthparts of omnivores have to be to no 2000). Likewise, the abundance of polyphagous their herbivorous and predaceous relatives to function plant feeders is affected by spatial and temporal vari- adequately in both prey and plant consumption? Do ation in host plants, and polyphagous herbivores are host-plant identi®cation behaviors and mobility asso- frequently more widespread and abundant than mo- ciated with polyphagous heteropterans allow them to nophagous relatives, especially if the monophagous in- track prey? To our knowledge, these hypotheses have sects specialize on relatively rare plants (Ehrlich and never been tested; however, questions like these could Raven 1964). Special Feature lmr . n .N idnan dtr.19.Zooph- 1996. editors. Wiedenmann, N. R. and O., Alomar, and Convergence 1999. Reich. B. P. and D., D. Ackerly, 2554 930 oR .Dno n E-434 oR .Denno F. R. to Eubanks. DEB- DEB-9423543 D. grant and M. Denno, Foundation and F. Science R. to National 9903601 to Eubanks, Agriculture of D. Department in M. States supported United was the and from research DEB-0074556 funding grant This Foundation Science project. National by this part of var- stages at encouragement Al ious and and discussion Raupp, thoughtful Mike for Singer, Wheeler Mike Mitter, Charlie Lamp, Bill im- this of habit. consequences feeding portant and origin evolutionary concerning the ideas as- of heteropteran our development in the hope stimulates omnivory We insects pre- of range. evolution be host the may of broad and sessment a pollen have and to seeds pre- adapted on be or feed may single to predators a adapted Conversely, on species. specialize plant that few relatives their in their prey include than to diet ability are the evolve species to likely polyphagous more Likewise, foliage- relatives. their than feeding diet their adaptations in the prey include evolve to to necessary likely more far are parts reproductive herbivorous plant nitrogen-rich, heter- that these consume within suggest that range results species of host Our consumption broad insects. the and opteran with pollen and correlated seeds is omnivory of . of generation the for consequenc- es profound have may omnivory the of that evolution suggests Co- result vs. interesting Berytidae This and lobathristidae). Tingidae vs. herbivorous (Miridae taxa taxa their omnivorous sister than the diverse contrasts, more three dramatically the were of out (herbivorous). two Colobathristidae In vs. Beryti- (omnivorous) and Coreidae dae (omnivorous), (herbivorous), Alydidae vs. Miridae Tingidae (herbivorous) species: extant vs. of number (omnivorous) the of and/ species estimates described we or of number which the for ®nd of readily taxa could contrasts sister herbivorous independent hy- and are three omnivorous this results found test preliminary We to our intriguing. data but enough statistically, have pothesis not rel- predaceous did We or herbivorous atives. ``success- strictly more their be than to ful'' plant species and omnivorous prey both allows consume food to ¯exibility ability the ecological by the provided if diversi®cation taxonomic ayad USA. Maryland, in Landham, America, Publications of Society Say Entomological Entomology, Thomas and management. history pest life integrated for implications Heteroptera: ytophagous American contrasts. Botany independent of a plants: Journal using seed in test function and comparative size leaf among correlations etakMseCl,EtleRse-oe,CagGuyer, Craig Russek-Cohen, Estelle Coll, Moshe thank We ncnlso,w on vdneta h evolution the that evidence found we conclusion, In to leads that innovation key a be may Omnivory vltoayconsequences Evolutionary A L 86 CKNOWLEDGMENTS ITERATURE :1272±1281. C ITED IK .EBNSE AL. ET EUBANKS D. MICKY eny,E . n .P .Mnebr.19.Isc her- Insect 1997. Minkenberg. J. P. O. and A., E. Bernays, oe,A .19.Feigaattoso oepredaceous some of adaptations Feeding 1990. the C. A. of Cohen, habits feeding original the On 1979. H. R. Cobben, oe,A .19.Patfeigb rdtr Heteroptera: predatory by feeding Plant 1996. C. A. 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Lan- America, USA. of Maryland, Society ham, Entomological Entomology, Publications Say in Thomas management. pest integrated and history life for implications Heteroptera: Zoophytophagous aindniy rdto,adcniaimi we corn. sweet in cannibalism Entomology and Environmental predation, density, lation ainpooeonvr mn anvru arthropods? carnivorous among Ecology omnivory promote tation yai osrit n h oeo odqaiy Ecology quality. food of role 84 the and constraints dynamic uini hcpa( chickpea in bution sup- prey Ecology in¯uence pression. and interactions omnivore±herbivore omnivorous an Ecology for prey insect. and plants in variation of sequences Evolution coevolution. in study a devel- pod during Soil cowpea Plant in opment. nitrogen ®xed biologically onbrrlra yeeisi ifrn onmicrohab- corn different in Control enemies Biological itats. by larvae borer corn En- corn. ®eld Maryland in Entomology enemies Pyral- vironmental natural (Lepidoptera: its borer and corn idae) European the of selection Mary- Lanham, America, USA. of land, Entomol- in Society in use Entomological Publications Say ogy, and Thomas ecology control. their biological Heteroptera: Predatory editors. a iad.Junlo Zoology of Journal sceroglos- lizards. herbivorous san and omnivorous by discrimination of Review Annual diets. Entomology prey and plant mixing arthropods: 83 culture rlcmuiis mrcnNaturalist American communities. ural ry .A od,adJ .Esr 02 irgni insects: in Nitrogen 2002. Elser. J. J. and Woods, A. H. erty, :2557±2567. :1215±1223. 18 84 :339±351. :2522±2531. in 47 .Aoa n .N idnan editors. Wiedenmann, N. R. and Alomar O. :267±297. 80 81 :1253±1266. 116 ie arietinum Cicer :936±947. :129±131. Clotr:Ccielde popu- Coccinellidae) (Coleoptera: 83 2 20 :95±103. :91±139. in :526±533. 27 .Cl n .R Ruberson, R. J. and Coll M. :1402±1410. 257 clg,Vl 4 o 10 No. 84, Vol. Ecology, 18 33 72 :53±66. .Eprmna Agri- Experimental ). :586±608. :473±476. :711±715. 150 :554±568. October 2003 WHY OMNIVORY? 2555

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APPENDIX A The phylogeny of family relationships in the heteropteran suborder Cimicimomorpha is available in ESA's Electronic Data Archive: Ecological Archives E084-063-A1. Special Feature E084-063-A3. 2556 nsbresCmcmmrh n ettmmrh saalbei S' lcrncDt Archive: Data Electronic ESA's in available is Pentatomomorpha and Cimicimomorpha suborders in aooi lcmn,hs ag,patpr edn rfrne n edn ai f38tretilhtrpea insects heteropteran terrestrial 398 of habit feeding and preference, feeding part plant range, host placement, Taxonomic Archive: h hlgn ffml eainhp ntehtrpea uodrPnaooopai vial nEAsEetoi Data ESA's Electronic in available is Pentatomomorpha suborder heteropteran the in relationships family of phylogeny The clgclArchives Ecological E084-063-A2. IK .EBNSE AL. ET EUBANKS D. MICKY PEDXC APPENDIX PEDXB APPENDIX clg,Vl 4 o 10 No. 84, Vol. Ecology, clgclArchives Ecological Ecology, 84(10), 2003, pp. 2557±2567 ᭧ 2003 by the Ecological Society of America

THE EVOLUTION AND MAINTENANCE OF OMNIVORY: DYNAMIC CONSTRAINTS AND THE ROLE OF FOOD QUALITY

SEBASTIAN DIEHL1 Department Biologie II, Ludwig-Maximilians-UniversitaÈt, Karlstrasse 23-25, 80333 MuÈnchen, Germany

Abstract. In several taxa, the ability to feed omnivorously from more than one trophic level has evolved from more specialized feeding habits. A prerequisite for this evolutionary scenario is initial coexistence (on the same or different trophic levels) of the consumers subsequently involved in omnivory. Evolution of omnivory should also be favored by prior asymmetries in consumer interactions. I use a dynamic model to explore conditions for coexistence of two consumers depending on a single biotic resource in simple food webs of increasing asymmetry between consumers: (1) pure resource competition, (2) resource competition with unidirectional interference, (3) omnivory, and (4) pure predation. If con- sumers are energy limited, omnivory is unlikely to evolve from a competitive system, because stable coexistence of two consumers on a single resource is impossible, even if there is a trade-off between resource exploitation and interference abilities. Initial coex- istence of two consumers is easier to achieve, if the species are arranged in a food chain. If costs of diet generalization are low, selection should then favor the inclusion of the resource in the top consumer's diet. In systems with high resource , the intermediate consumer will then, however, be frequently driven to extinctionÐin which case omnivory is not maintained. Low nutritional quality of the resource can stabilize the omnivory system and allow three-species coexistence at high resource carrying capacities. Low nutritional quality of the resource may also create conditions for the evolution of Feature Special omnivory from a competitive system. If the content of an essential nutrient in resource biomass is dynamic, stable coexistence of two competitors becomes possible if both are limited by the nutrient content of the resource. In this case, selection may favor the evolution of omnivory, because competitor biomass is usually of higher nutritional quality than resource biomass. An explicit treatment of ¯exible resource stoichiometry thus broadens the possibilities for the evolution of omnivory. Key words: coexistence; conversion ef®ciency; food web; interference competition; intraguild predation; invasibility; nutritional quality; omnivory; ; predation; resource com- petition; stoichiometry.

INTRODUCTION able to ®nd, catch, ingest, and digest food types span- It is now widely accepted that omnivory, the con- ning a potentially vast range of behaviors, morpholo- sumption of resources from more than one trophic lev- gies, and biochemical compositions. Coping with a el, is very common in natural communities (Polis et wide variety of food types may have to involve speci®c al. 1989, Diehl 1993, Coll and Guershon 2002). From adaptations. For example, omnivores that feed on both the perspective of an individual consumer, being an animals and plants must possess a morphology allow- omnivore seems advantageous, because food abun- ing them to physically harm and subdue animal prey dance is usually highest at lower trophic levels, where- while at the same time carrying a digestive tract capable as food quality (e.g., content in proteins) normally in- of processing both plant and animal material (Coll and creases with position in the food chain (Hastings and Guershon 2002, Eubanks et al. 2003). Morphological Conrad 1979, Hairston and Hairston 1993, Whitman et and phylogenetic evidence suggests that, for many om- al. 1994, Elser et al. 2000, Denno and Fagan 2003). nivorous taxa, the ability to feed on resources from An omnivorous feeding mode may thus enable the har- more than one trophic level is a derived trait that has vesting of both more abundant but less nutritious and evolved from more specialized, ancestral states (Whit- of less abundant but more nutritious food sources in man et al. 1994, Cohen 1996, Eubanks et al. 2003). variable proportions (Coll and Guershon 2002). This begs the question: which ecological circumstances Omnivory should, however, also involve trade-offs. would favor the evolution of omnivory from more spe- Omnivores are, by de®nition, generalists that must be cialized feeding habits? A related question is: under which ecological cir- Manuscript received 8 July 2002; revised 2 October 2002; cumstances is omnivory maintained in a community? accepted 17 October 2002; ®nal version received 12 November From a population dynamical perspective, the com- 2002. Corresponding Editor: A. A. Agrawal. For reprints of this Special Feature, see footnote 1, p. 2521. monness of omnivory poses a puzzle, because omni- 1 E-mail: [email protected] vory frequently causes extinctions in simple model 2557 Special Feature mioyi ipetreseisfo webs. of food maintenance three-species may simple the processes) in and feedback omnivory expression of the result both the it facilitate (be or resource trait basal ®xed the show a of stoichi- will quality I nutrient nutritional consumers. low the to that and latter resource quality the the of nutritional In ometry ¯exible. relate or I ®xed case, either is the of resource quality nutritional basal the which therefore in I 1974, 2000). systems (Droop al. consider et itself Elser trait 1999, Denno dynamic and a Eubanks be can of and composition elemental tissues stoichiometric frequently the is coexistence to quality related on Nutritional consumers. resource two basal the the of I nu- of levels, and quality capacity trophic carrying tritional various of at in¯uences types the emphasize food of abundance relative quality the in and differences to related are diet of case possible food simplest to the omnivory. precursors represents potential which as 3, viewed 1, web be webs can Food 4 predation. and pure 2, intra- (4) and (3) predation, interference, competition guild unidirectional resource of with (2) webs (1) combined competition, food interactions: resource simple consumer pure in in resource asymmetry biotic increasing single a on depending consumers explore two to of model coexistence for dynamical conditions a use on I Based assumptions, resources. these in- shared both and with consumers omnivore termediate requires the feeding of omnivorous coexistence continuous enabling traits mainte- of the nance sub- Third, the consumer. the to intermediate superior if subsequent physically facilitated, already is be omnivore evo- should sequent the omnivory Second, of it. lution in involved subsequently the of species coexistence prior Still, requires omnivory First, complex. of made. be evolution be more can to assumptions on likely plausible feed simple, are three level to trophic consumers one enabling than traits of nance resources. con- shared specialist formerly the a of into the sumer and evolve community should the omnivore from circumstances, lost former such facto de Under is prey. omnivory intermediate competitor the omnivore resource a the of and omnivore, consumer direct an go a both of to being presence In prone the 2001). are in al. extinct species et prey Mylius intermediate 2000, particular, Feiûel Polis and and Diehl Holt 1978, 1997, Lawton and (Pimm communities 2558 eac fonvr,Iuetefloiggnrlmodel general following the use main- I and omnivory, evolution of tenance the investi- To on constraints quality. dynamical competi- resource gate a ¯exible is with precursor system the with tive ®xed (3) chain food quality; with a resource system is ®xed precursor competitive the (2) a quality; is resource precursor systems: the one-resource±two-consumer (1) in omnivory of T eas h oeta datgso nomnivorous an of advantages potential the Because mainte- and evolution the in involved factors The osdrtreptnilseaisfrteevolution the for scenarios potential three consider I HE G ENERAL A POC N THE AND PPROACH B ASIC M EATA DIEHL SEBASTIAN ODEL oeta rcro ytm r pca cases: special the are which systems of precursor omnivory, potential with system three-species a of ␳ resource biotic a of consists system This dN dP dR esrdi nt fboas h eorehsamax- rate a growth has speci®c resource The imum biomass. of units in measured w ims ihef®ciency with biomass own truhmtbls n otlt)a rate a at mortality) and metabolism (through dt dt dt ue yconsumers by sumed resource/consumer hs susaeadesdb ayn h eorecar- resource the capacity varying on rying Law by quality addressed and and are issues abundance (Hutson these resource system of Effects omnivory 1985)]. the per- the of for of conditions sistence evolution suf®cient the are [which after omnivory possible remains then equilibria I bound- omnivory. ary stable locally of of invasibility evolution mutual whether the ask to missing prior the possible by is coexistence three-species consumer) stable whether one and only consumer with (i.e., system systems investigate full the of ®rst of sets I boundary of scenarios. invasibility approach the evolutionary following three the all apply locally to thus cases have I to must equilibria. simplicity systems stable for precursor analysis potential the where limit I question, resource? basal the of capacity quality productive the and sys- by three-species affected a omnivory of with tem persistence the has is omnivory how prior once evolved, coexist Second, omnivory? fundamental must of species the evolution to three ful®ll the scenarios that the requirement do ques- basic First, more much tions. two dynamically ask a I Rather, be feed trait. would evolving level to trophic one capacity than the more on which in approach, evolutionary sections later in detail in 2). Table explained also be (see will Ta- and in listed 1 are ble scenarios evolutionary different three pc® om ftefunctions the of forms speci®c 97 oie l 02.Teapiaiiyo h results the of applicability The 2002). al. equilibria et stable Kooi Hastings and 1997, locally McCann 1980, of McGehee and existence (Armstrong the require however, does, not systems both omnivory the of and precursor Persistence the biomass. omnivore into resources sraie taygvntm.Consumer time. given any at realized is eas h ou fti ae so h second the on is paper this of focus the Because truly a with scenarios three the investigate not do I ϭ ϭ ϭ ϩ e Ϫ e Ϫ r ␳ NR NP RP RN RP RN ( e mN a ,K ,N P N, B, K, R, ( ( ,R ,P N, R, B, PNPN P NP P N NP ,R ,P N, R, B, RP N ( ( q ,N R, K , q n h ovrinef®ciency conversion the and ) P i ) a ihrate with ) ) N a a ) ( R and ,N R, ( ( ,N R, ,P R, Ϫ r, P, a ) fwihol fraction a only which of a P RN ) ) N ij P e hs este r all are densities whose , ( clg,Vl 4 o 10 No. 84, Vol. Ecology, Ϫ ij ,P R, ␳ ovrsisfo into food its converts , Ϫ , mP n oe biomass loses and a a ij ) , N (1c) . ( and ,N R, R hti con- is that j e ) ij ed on feeds P m o the for j e . RP (1b) (1a) The of October 2003 WHY OMNIVORY? 2559

TABLE 1. Speci®c forms of the functions describing resource renewal, functional responses, and conversion ef®ciences used in the examples to illustrate the cases of (1) a competitive system with (c Ͼ 0) or without (c ϭ 0) unidirectional interference and with ®xed resource quality (Model I), (2) a food chain with (aRP Ͼ 0) or without (aRP ϭ 0) omnivory and with ®xed resource quality (Model II), and (3) a competitive system with (aNP Ͼ 0) or without (aNP ϭ 0) omnivory and with ¯exible resource quality (Model III).

Speci®c function Description General function Model I Model II Model III R R R Resource renewal ␳(R, K, B, N, P) 1 Ϫ 1 Ϫ 1 Ϫ K K (B Ϫ qNϪ qP) min K, NP []qRmin

aRRN aRRN Functional response of N aRN(R, P) aRRN feeding on R 1 ϩ cP 1 ϩ ahRRN RN

aRRP Functional response of P aRP(R, N) aRRP aRRP feeding on R 1 ϩ ahRRP RPϩ ahN NP NP

aNNP Functional response of P aNP(R, N) 0 aNNP feeding on N 1 ϩ ahRRP RPϩ ahN NP NP

(B Ϫ qNNPϪ qP) Conversion of R into NeRN(B, R, N, P) eRN eRN eRN min 1, Ά·[]qRN

(B Ϫ qNNPϪ qP) Conversion of R into PeRP(B, R, N, P) eRP eRP eRP min 1, Ά·[]qRP pca Feature Special qN Conversion of N into PeNP(q N, q P) 0 eNP eNP min 1, Ά·[]qP Note: For de®nitions of parameters see Table 2. to nonequilibrium systems will be brie¯y addressed in quality. These assumptions can be included in the gen- the Discussion. eral model by setting the attack rate of consumer P on consumer N to zero and the conversion ef®ciencies of SCENARIO 1: RESOURCE COMPETITION WITH AND consumed resources R into consumer biomass to con- WITHOUT INTERFERENCE COMPETITION IN A SYSTEM stant values (Model I in Table 1). Because an omnivore WITH FIXED RESOURCE QUALITY must be able to harm its prey, I also investigate the Scenario 1 assumes that the precursor to an omnivory situation in which one of the consumers is already system is a competitive system with ®xed resource physically superior to the other consumer. Such phys-

TABLE 2. De®nitions of model parameters.

Parameter De®nition Units

aRN search and attack rate of N on R area per biomass of N per time aRP search and attack rate of P on R area per biomass of P per time aNP search and attack rate of P on N area per biomass of P per time B total nutrient content in system mass of nutrient per area c per capita interference effect of P on N per biomass of P eRN conversion of R into N dimensionless number between 0 and 1 eRP conversion of R into P dimensionless number between 0 and 1 eNP conversion of N into P dimensionless number between 0 and 1 hRN handling time of N feeding on R time ϫ biomass of N per biomass of R hRP handling time of P feeding on R time ϫ biomass of R per biomass of P hNP handling time of P feeding on N time ϫ biomass of P per biomass of N K carrying capacity of R biomass of R per area mN biomass loss rate of N per time mP biomass loss rate of P per time qRmin minimal nutrient quota per biomass of R mass of nutrient per biomass of R qN nutrient quota per biomass of N mass of nutrient per biomass of N qP nutrient quota per biomass of P mass of nutrient per biomass of P r maximum speci®c growth rate of R per time ␳ fraction of r attained by R dimensionless number Note: The de®nitions assume that the densities of R, N, and P are expressed in biomass per unit area. Special Feature aiyo h eorei ih nefrnefo high a from interference of high, ca- density is carrying resource the the possible of If pacity only systems. is productive suf®ciently scenario in This equilibrium. at system RN- competitor in resource possible as inferior much the as of as- balance favor the by tilt model To the consumers. in between interference included behavioral unidirectional, be suming can asymmetry ical 2560 ytmi ierfo hi ih®e eorequal- resource ®xed with chain food linear a is system B.Oc established, Once 1B). opttr(sue obe to (assumed competitor wt h nefrneconstant interference illus- the Model be (with of isoclines I can zero-net-growth of This plots with 1980). exploitative trated McGehee purely and is (Armstrong competition the if exclude consumer, competitively will other low- resource the the at of level population the est a that maintain and can homogeneous impossible which single, is consumer quality a constant by of limited resource consumers two of 1). Table in I (Model aigpplto of population vading nefrnede o ovyaydrc eetto bene®t direct any convey not does interference olvl hr h ouaingot aeof rate growth population the where levels to uto 1/(1 duction fitreec (consumer interference of e nwihteifro xliaiecmeio (as- competitor exploitative be to inferior sumed the which in tem n h ytmstlsete oan to B) either settles 1A, system (Fig. the impossible and is consumer the other by respective equilibrium a at of system invasion consumer-resource single systems, productive suf®ciently in Thus, te.I h neirepottv competitor exploitative inferior the abil- is If interference there and ities. if exploitation and between trade-off interference a in engage also consumers 1A). (Fig. resource the with rmlwdniisi an in densities low from fitreec (consumer ``donor'' interference the of to cost no incurs behavior interference that eiri nefrnecmeiin h ueirex- superior the competition, competitor ploitative interference in perior hr nefrnebtencnuesi mutual is situations consumers to between 2002). extend (Amarasekare interference and the A) where of (Appendix responses functional consumers nonlinear in- of inclusion unidirectional against the of robust are case results These the is competition. resource terference in single also a impossible sharing thus consumers coex- two Stable of conditions. istence initial on depending librium, oe eaieand negative comes nbet naeasse nwhich in system a invade to unable osnt oee,ehneteaiiyof ability the enhance however, not, does cnro2asmsta h rcro oa omnivory an to precursor the that assumes 2 Scenario ti eletbihdrsl htsal coexistence stable that result well-established a is It h ucm fcmeiinmycag,i h two the if change, may competition of outcome The CENARIO S and O NVR NA IN MNIVORY RP- P P ϩ tthe at sa qiiru ihtersuc (Fig. resource the with equilibrium at is ) :F 2: usses h ueirexploitative superior The subsystems. cP R OOD ESOURCE nisatc aeo h resource the on rate attack its in ) RP P N N N C osetnt Conversely, extinct. goes a eual oivd an invade to unable be may qiiru ilcuea in- an cause will equilibrium odcie(i.1) Because 1B). (Fig. decline to ilqikydieteresource the drive quickly will ANWT N WITHOUT AND WITH HAIN S N SE WITH YSTEM N P RN ufr rprinlre- proportional a suffers ) Q ,weeste``receiver'' the whereas ), a lasivd sys- a invade always can ) UALITY ytma equilibrium. at system c RN N e ozr)i the in zero) to set sa equilibrium at is ran or F IXED P P, oincrease to assume I RP EATA DIEHL SEBASTIAN P ssu- is P equi- P, P be- RP is it oe ystigteatc aeo consumer of rate general attack the the in setting included by be model can assumptions These ity. atclri aiaswt ihrsuc arigca- carrying resource high pacity in with diet, habitats consumer's diet top in the of particular in costs resource the the favor If of then inclusion should omnivory. selection of low, are evolution generalization coexist the to able to be must prior species three the that condition chain. food equi- stable the globally of a librium of existence the guarantees also scnb eni h ln fthe of plane the in seen be can extinction, as to driven frequently be however, will, sumer rdcieatraiefo source food alternative productive iis(i.1) ntecs flna ucinlre- functional linear an of of case invasibility 1C), the (Fig. In sponses 1C). (Fig. sities ec spsil loa nntl high in®nitely at also possible is tence B.As 2B). o eoreqaiy(o ovrinef®ciency by conversion (low neutralized quality completely resource be low however, can, capacity of consumer specialist resource. top a the former into the evolve and should expressed goes consumer not consumer is intermediate omnivory the extinct, which carrying resource for At capacities omnivory. constraint of dynamical maintenance a 2001, the poses on 2000, This 2001). Feiûel al. and carrying et resource Mylius Diehl of 2A±C; range (Fig. narrow capacities lim- relatively often a therefore to is consumers ited two the of co- on and existence consumer invasibility Mutual top consumer. intermediate the the from pressure predation creased naigtpconsumers top invading (an eorei ih u®in est fintermediate of the density of suf®cient capacity a consumers carrying high, the is If resource resource). the on feed xsec sipsil.Wt eraigrsuc qual- resource decreasing With impossible. is existence ioostpcnue eed nteblneo re- of balance ( the capacity carrying on source depends om- consumer an stable top with how nivorous consumer illustrates intermediate 3 the Fig. ef®- of B9. conversion coexistence Eq. threshold in given shown the is is where ciency This B, 3). 2D±F, Appendix (Figs. in value threshold a than eilsrtdwt nioln lti the in plot isocline capacity again an can with carrying This illustrated 1992). be high DeAngelis the 1981, suf®ciently of al. et base a a (Oksanen the has at in resource chain arranged the are food if and species chain the single food if linear a possible, on is depending resource consumers two of coexistence 1). Table values constant in to II biomass (Model consumer con- into of food ef®ciencies sumed conversion the and zero to resource nonvr ytma some at system omnivory of persistence an the stable allows Whenever parameters biomass). of combination consumer top into resources hnrsuc ult shg (here, high is quality resource When ierfo hi hsceryfllstebasic the ful®lls clearly thus chain food linear A h etblzn feto ihrsuc carrying resource high a of effect destabilizing The ncnrs oaprl opttv ytm stable system, competitive purely a to contrast In RP K. usse osnteit because exist, not does subsystem K ntelte iuto,teitreit con- intermediate the situation, latter the In N nrae,teicesnl bnatand abundant increasingly the increases, smitie nan in maintained is P K a nraefo o den- low from increase can n eoreqaiy( quality resource and ) K, clg,Vl 4 o 10 No. 84, Vol. Ecology, he-pce persis- three-species RP RN R RN usse (Fig. subsystem K utisa in- an sustains e ytms that so system RN RP if ytmby system e Ͼ P subsystem RP osnot does P .)co- 0.3) slower is nthe on e RP e RP of P ). October 2003 WHY OMNIVORY? 2561

FIG. 1. Invasibility of boundary equilibria in a competitive system with and without interference and in a food chain. Panel A shows zero-net-growth isoclines in the RN plane (i.e., P ϭ 0) of a system where N and P are exploitative competitors (Model I). Panel B shows zero-net-growth isoclines in the RP plane (i.e., N ϭ 0) of a system where N and P are exploitative competitors and P may additionally interfere with N (Model I). Panel C shows zero-net-growth isoclines in the RN plane (i.e., P ϭ 0) of a system where P feeds on N but not on R (Model II). In panels A and C, the gray areas mark conditions under which P can increase (i.e., PЈϾ0) from low densities in an RN-system. If the intersection of the R and N isoclines is in the gray area, then P can invade an RN system at equilibrium. Likewise, the gray areas in panel B mark the conditions under which N can increase (i.e., NЈϾ0) from low densities in an RP system. The dark gray area applies to a system with unidirectional interference of P against N. In the absence of interference, NЈϾ0 in the entire gray area. In the example, N Feature Special can invade an RP system at equilibrium only in the absence of interference (panel B). Invasibility of boundary equilibria: ®lled circle ϭ noninvasible; open circle ϭ invasible; open circle in a ®lled square ϭ noninvasible with interference, invasible without interference. Default parameter values are aRN ϭ 0.1, aRP ϭ 0.1, aNP ϭ 0.14, mN ϭ 0.15, mP ϭ 0.5, eRN ϭ 0.12, eRP ϭ 0.1, eNP ϭ 0.9, K ϭ 160, r ϭ 0.5. In panels A and B, aNP ϭ 0 and eNP ϭ 0; in panel C, aRP ϭ 0 and eRP ϭ 0. ity, coexistence becomes ®rst possible over a narrow The model is an extension of the one-resource±two- range of relatively low resource carrying capacities. consumer model of Loladze et al. (in press; see also With further decreases in resource quality, the coex- Loladze et al. 2000), to which I have added the pos- istence region extends to ever increasing resource car- sibility of predation by consumer P on consumer N rying capacities. Below the threshold conversion ef®- (Model III in Table 1). At any given time, plant pro- ciency (here eRP Ͻ 0.0706), stable persistence of the duction is assumed to be limited either by a mineral omnivory system is possible at in®nite K. nutrient or by some other resource (e.g., light, space). The total amount of nutrient in the system is given by SCENARIO 3: RESOURCE COMPETITION AND B, whereas the supply of other limiting plant resources OMNIVORY IN A SYSTEM WITH DYNAMICALLY is implicitly modeled as a carrying capacity K. The FLEXIBLE RESOURCE QUALITY limiting nutrient occurs in the system only in organic Scenario 3 assumes that the precursor to an omnivory form, i.e., incorporated in plant and consumer biomass. system is a competitive system with ¯exible resource This corresponds to the assumption that there is no stor- quality. In scenarios 1 and 2, food quality was modeled age pool of the limiting nutrient, as is approximately phenomenologically as constant conversion ef®cien- true for, e.g., pelagic aquatic systems. Any nutrient ex- cies of consumed food into consumer biomass. The creted by consumers or lost in dead consumer bodies is nutritional quality of many plants (and some animals) assumed to be instantly mineralized and incorporated can, however, be a dynamic trait related to ¯exible into plant biomass. Thus, the speci®c nutrient content tissue contents of essential components (e.g., mineral nutrients, , fatty acids) or toxic compounds. qR of plant biomass is dynamic and given by Here, I focus on mineral nutrient to biomass stoichi- B Ϫ qNϪ qP q ϭ NP (2) ometry as a broadly relevant, mechanistic representa- R R tion of food quality (Elser et al. 2000). I consider a system consisting of a plant species R with ¯exible where qN and qP are the speci®c nutrient contents per nutrient stoichiometry and two herbivorous consumers biomass of consumer N and P. I assume qN and qP to N and P with ®xed stoichiometry and explore the pos- be constant, although these ratios may vary somewhat sibilities for three-species coexistence with and without in practice (DeMott et al. 1998, Sterner and George an additional omnivorous feeding link between the con- 2000). The nutrient content of plants has a physiolog- sumers. ically set lower bound qRmin. Plant growth is limited by Special Feature Ͼ limitation ( plant of the in forms bend two a by as the limited shows between is resources. transition growth limiting The other plant for reversed, competition is intraspeci®c 3 Eq. When expres- the renewal into resource 2 Eq. for ful®lled of sion substitution is from inequality follows following (as the when nutrient the an invade to able be will consumer intermediate the and E), (panel 2562 capacities uretcneto odseisi agrta the than (i.e., larger biomass is consumer of species content food nutrient a speci®c of speci®c content the nutrient When ef®ciencies. conversion these culate ue ims r olne osat olwn Lo- ( Following al. constant. et longer ladze no con- are into biomass biomass plant sumer of conversion the for ®ciencies e-rwhiolnsi the in isoclines net-growth aesAadD n h mioecno naean invade cannot omnivore the and D, and A panels circle F q akcniin ne hc h mioecnices (i.e., increase can omnivore the which under conditions mark ihrsuc ult (high quality resource high osmr eas h nescino the of intersection the because consumer, pnlB.Cneunl,sal essec fa mioysse srsrce oanro ag fcryn aaiis(gray capacities carrying (low of range quality narrow resource a low to restricted At is C). system panel omnivory an in of area persistence stable Consequently, B). (panel ryaesi aesBadEmr h odtosudrwihteitreit osmrcnices (i.e., increase can consumer intermediate the which under conditions the mark E and B panels in areas gray ihntiinlqaiyo lnsbigdnmc ef- dynamic, being plants of quality nutritional With IG ) tsfcetylwcryn aaiis the capacities, carrying low suf®ciently At F). n hwtecrepnigzr-e-rwhiolnsi the in isoclines zero-net-growth corresponding the show E and o este nan in densities low npnl D±F, panels in j , .Ivsblt fbudr qiiraadsqec feulbimboassaogagain frsuc carrying resource of gradient a along biomasses equilibrium of sequence and equilibria boundary of Invasibility 2. . ϭ where oivsbe pncircle open noninvasible; K o ifrn ovrinef®ciencies conversion different for i npress in e stefo and food the is RP ϭ RP 0.06. ,asml uei dpe ocal- to adopted is rule simple a ), ytm nteeape h mioecnawy naean invade always can omnivore the example, the In system. qR qK R min R e RN RP ␳ Ͼ ,a nraein increase an ), nMdlII[al 1]): [Table III Model in ln (i.e., plane j R ϭ stecnue) con- consumer), the is . scie(i.4). (Fig. isocline ) nail.Prmtrvle r si i.1(eal aus.I aesA±C, panels In values). (default 1 Fig. in as are values Parameter invasible. N P ϭ and K e )frtodfeetcryn aaiis( capacities carrying different two for 0) R uteetal edt oivsblt fthe of noninvasibility to lead eventually must RP e P and EATA DIEHL SEBASTIAN ,teitreto fthe of intersection the ), RP scie sblwteitreto fthe of intersection the below is isoclines frsucsit mioe nMdlI.Pnl n hwzero- show D and A Panels II. Model in omnivores into resources of RN N (3) scie a nesc ntelwrlf onr wieaes of areas) (white corners left lower the in intersect may isoclines q ytma qiiru.Ivsblt fbudr qiira ®lled equilibria: boundary of Invasibility equilibrium. at system i eso fcec sstt t aiu value maximum its to set is ef®ciency version P etcllnsa nsseswt osatrsuc qual- resource constant with systems in as lines vertical spsil,i ln ult sdnmc hscnbe can the This in dynamic. plots is isocline plant quality with single plant illustrated a if by possible, limited is consumers two of existence RP ЈϾ ln n osmrdniisfrwhich for The densities 2). (Eq. consumer densities and consumer plant and plant of function ae oiscnue,ol fraction a only consumer, com- its de®cient to nutrient is pared species food a when versely, tagtln ihngtv lp.T h eto that content of carbon ( the plants left by of the limited To is slope. growth consumer negative line, with line straight a ytm Fg A ) ln quality Plant B). 4A, (Fig. systems t od niprat®a supini htcon- that is responses. assumption functional saturating ®nal of have important content sumers carbon An by the food. limited than its is rather content growth nutrient consumer the case, this In realized. oaz ta.( al. et Loladze RP ln (i.e., plane )fo o este nan in densities low from 0) ytmas ti®ieyhigh in®nitely at also system q R N Ͼ and N q j ϭ n osmriolnsaestraight are isoclines consumer and ) npress in P RN ) npnl n ,tega areas gray the D, and A panels In 0). scie cusa ihrvle of values higher at occurs isoclines ytm(aesA ) ncnrs,at contrast, In D). A, (panels system K ϭ aesonta tbeco- stable that shown have ) RP 0 and 100 R ytmb h intermediate the by system sciewt h ordinate the with isocline RN clg,Vl 4 o 10 No. 84, Vol. Ecology, ytm ieie the Likewise, system. K K q ga rai panel in area (gray RN R ϭ sadecreasing a is 0) aesB Panels 600). q q and N i R /q ЈϾ ϭ j e RP e RP of q ij )from 0) . j ϭ Con- form e sub- ij 0.1; is P October 2003 WHY OMNIVORY? 2563

when feeding on plants. Nevertheless, because P has a lower mortality rate than N, the former is actually the superior competitor in situations where plant qual- ity is high. This can be seen by comparison of the vertical parts of the consumer isoclines in the purely

competitive system. At high plant quality (qR Ͼ qj), P requires a lower plant density than does N to achieve zero net population growth (Fig. 4A, B). Thus, when plant quality is dynamic, competitive ranking may change with changing plant quality and stable coex- istence of a three-species omnivory system may be possible, even if the omnivore is the superior compet- itor under some environmental conditions. In the ex- ample, P can invade the system at a lower plant car- rying capacity than can N (Fig. 5A). This is in stark contrast to a fundamental coexistence requirement in more traditional models (e.g., Model II). When the FIG. 3. Combinations of resource carrying capacities K quality of the basal resource is ®xed, stable coexistence and conversion ef®ciencies eRP of resources into omnivores of a three-species omnivory system is only possible if for which omnivores P and intermediate consumers N coexist the intermediate consumer is the superior resource stably in Model II. Coexistence is possible in the gray area bounded by e and e . Parameter values are as in Fig. 2; competitor under all environmental conditions, which RP1 RP2 implies that it can invade the system at a lower resource eRP1 asymptotes at 0.0706. A three-species equilibrium with omnivory is feasible whenever eRP is high enough to allow carrying capacity than can the omnivore (Fig. 2; Polis P to invade an RP system at equilibrium (i.e., eRP Ͼ eRP2) but and Holt 1992, Holt and Polis 1997). low enough to not drive N extinct (i.e., e e ) (see Ap- Feature Special RP1 Ͼ RP Fig. 5A also illustrates how plant quality and quan- pendix B). tity interact in determining coexistence of the omnivore with the intermediate consumer. As plant carrying ca- ity. To the right of the qR ϭ qj line, consumer growth pacity K increases, plant quality at equilibrium qR(R*) is limited by the nutrient content of plants (qR Ͻ qj). decreases. Because the intermediate consumer is the Here, any increase in plant density R is more than com- superior resource competitor at low resource quality, pensated for by a concomitant decrease in food quality it may eventually invade the system. At even higher qR; i.e., the consumers' nutrient intake rates and, con- K, all species may be so strongly nutrient limited that sequently, their growth rates decrease with increasing their densities become independent of further increases R and consumer isoclines have negative slopes in the in K. In this case, three-species coexistence is possible region where qR Ͻ qj (Fig. 4A, B). If the equilibria of also at in®nitely high K. This result seems to recover both the RN and the RP subsystems lie in this region the similar result from the model with ®xed quality of of low plant quality, mutual invasibility is possible and the basal resource (Fig. 3). Still, the in¯uence of plant a globally stable equilibrium with both competitors quality and quantity on consumer coexistence is more may exist (Fig. 4A, B). At the resulting three-species complex when plant quality is dynamic, because the equilibrium, both consumers are limited by plant qual- productive capacity of plants now depends on two lim- ity qR rather than plant quantity R (Loladze et al., in iting resources (modeled as K and B). For example, if press). the productive capacity of plants is varied through var- A competitive system with ¯exible plant quality thus iation in the total amount of nutrient in the system B, also ful®lls the condition that the three species must three-species coexistence is, again, possible only at rel- be able to coexist prior to the evolution of omnivory. atively low plant quality (Fig. 5B). At still lower levels If costs of diet generalization are low, selection should of plant quality (at levels of B, where plant biomass is then favor the inclusion of the competitor in the sub- kept below the carrying capacity set by other limiting sequent top consumer's diet. This evolutionary scenario resources), however, none of the consumers can exist may indeed lead to a stable omnivory system. After at all (Fig. 5B). the inclusion of a feeding link from consumer P on Fig. 5B indicates that dynamic ¯exibility in resource consumer N in the competitive system depicted in Fig. quality may lead to complex patterns of species co- 4A, B, mutual invasibility and stable three-species co- existence and abundance along environmental gradi- existence are still possible (Figs. 4C, D, 5). ents. These patterns include multiple stable states (e.g., In the numerical example, I have assumed a tradeoff at B Ͼ 0.31, there is an with between the omnivore's capacities to feed on plants vs. only R and P) and unstable dynamics (e.g., at B Ͼ 0.38, intermediate consumers. Compared to the intermediate the R-P system starts to oscillate). A detailed analysis consumer N, the omnivore P has a lower maximum of Model III is, however, beyond the scope of this conversion ef®ciency eRj and a longer handling time hRj paper. The main point of the limited numerical analysis Special Feature ϭ e N 2564 capacity nMdlII aesAadCso eontgot scie nthe in isoclines zero-net-growth show C and A Panels III. Model in slmtdb h uretdniyrte hntecro est ftepat.Ti cust h ih fteti otdline dotted thin the of right the to occurs This plant). the of density carbon the than rather density nutrient where the by limited is RN ЈϾ F F ) rniinfo uretlmtto fpatgot olmtto yohrrsucs(hc eemn h ln carrying plant the determine (which resources other by limitation to growth plant of limitation nutrient from transition a 0), opttv ytmada mioysse.Prmtrvle are values Parameter system. omnivory an and system competitive orsodn eontgot scie nthe in isoclines zero-net-growth corresponding oe I.Sal essec fa mioysse spsil ntega ra.Prmtrvle r si i.4C D. C, 4 Fig. in as are values Parameter areas. gray the in possible is system omnivory B, an panel of In persistence Stable III. Model IG IG ϭ n B, and A ooscillate. to rdeto eorecryn capacities carrying resource of gradient a .Sqec feulbimboassado h uretqoaprboaso eorea equilibrium at resource of biomass per quota nutrient the of and biomasses equilibrium of Sequence 5. . omnivory D) (C, with and B) (A, without system competitive a in circles) (open equilibria boundary of Invasibility 4. . )fo o este.I h xml,mta naiiiy(n stable (and invasibility mutual example, the In densities. low from 0) 0.8, q R K ϭ a cusa h ed osmriolnshv eaiesoe hr ln ult slw(.. osmrgrowth consumer (i.e., low is quality plant where slopes negative have isoclines Consumer bend. the at occurs ) e NP RP K q N ϭ ϭ ϭ ϭ .I aesCadD, and C panels In 0. 0.66, 0 nta odtoswere conditions Initial 70. q P . ryaesmr odtosudrwihtersetv isn osmrcnices (i.e., increase can consumer missing respective the which under conditions mark areas Gray e NP ϭ 0.9, h RN ϭ a NP 0.16, K ϭ R pnlA n rdeto oa uretcontent nutrient total of gradient a and A) (panel .5 and 0.05, h ϭ RP RP 58.5, ϭ EATA DIEHL SEBASTIAN ln (i.e., plane 0.4, N h NP K ϭ ϭ ϭ 1.07, 0.5. N 70, ϭ q P a ( isocline plant the along right to left from Moving 0). R min RN ϭ ϭ ϭ ..I ae ,for B, panel In 1.6. RN 0.085, 0.003, ln (i.e., plane NP a q RP oxsec)i osbei ohapurely a both in possible is coexistence) N ϭ ϭ 0.08, 0.03, P ϭ B B q ) aesBadDso the show D and B Panels 0). P Ͼ ϭ B ϭ 0.3, .8 the 0.38, ntesse pnlB in B) (panel system the in 0.03, clg,Vl 4 o 10 No. 84, Vol. Ecology, m N r ϭ ϭ RP 0.25, .8 npanels In 0.58. ytmstarts system q R ( m R* P P ЈϾ ϭ along ) 0.15 0or R Ј October 2003 WHY OMNIVORY? 2565 of Model III was to demonstrate, that the evolution of petitive system with dynamic plant quality. Stable co- omnivory from a purely competitive system is theo- existence of competing herbivores requires furthermore retically possible and that the interplay of resource that their competitive ranking depends on plant quality; quality and quantity may, again, play a key role in the i.e., the species that is superior at high plant quality evolution and maintenance of omnivory. must be inferior at low plant quality and vice versa. Building on the model of Loladze et al., I have shown DISCUSSION that evolution of omnivory from a competitive system Intuitively, interference among resource competitors is indeed feasible, if the quality of the shared plant is seems to be a plausible avenue for the evolution of affected by plant and consumer densities (Model III). omnivory. A hypothetical progression has been pro- The competitive ranking of consumers may also in this posed starting from exploitation competition, followed case vary with plant quality, creating the intriguing by aggression to monopolize local resources, eventu- possibility of stable persistence of a herbivore with an ally leading to intraguild predation (Polis 1988). The omnivore, in spite of the latter being superior in ex- analysis of Model I suggests, however, that omnivory ploitative competition under some environmental con- is unlikely to evolve from a competitive system with ditions. Low plant quality may be important also for a single, homogeneous resource of constant quality, the maintenance of omnivory in such a system, as in- because stable persistence of two competitors is then dicated by strongly negative correlations between re- impossible even if consumers exhibit a trade-off be- source quality q(R*) and equilibrium density of the tween resource exploitation and interference abilities intermediate consumer N in presence of the omnivore (see also Case and Gilpin 1974, Briggs 1993, Amar- P (Fig. 5A and B). It seems that N can only coexist asekare 2002). Clearly, such an evolutionary scenario with P at low plant quality, i.e., under conditions where requires an additional stabilizing mechanism. N was assumed to be superior in exploitative compe- The analysis of Model II shows that omnivory can tition. Given the limited analysis of Model III, it is not evolve from a food chain, but that persistence of an possible to generalize these observations. The numer- omnivory system and, thus, the maintenance of om- ical examples do, however, clearly indicate that an ex- Feature Special nivory, is dynamically constrained. Stable persistence plicit treatment of ¯exible resource stoichiometry is impossible or limited to a narrow range of resource broadens the possibilities for the evolution of omni- carrying capacities, if resource quality is high (Fig. 3), vory, at least at the plant±herbivore interface. but may occur over much broader ranges of resource Model III makes the simplifying assumption that carrying capacities, if resource quality is low. The latter consumers metabolize carbon and nutrients in the same situation is encountered by many omnivores feeding proportions as found in their body tissues. Under the on both plant and animal material. Compared to animal more realistic assumption that carbon is disproportion- prey, plant abundance is usually much higher, but the ally metabolized to meet maintenance needs (Sterner quality of most plant tissues is rather low (Mattson 1997, Kooijman 2000) the boundary between carbon 1980, DeVries and Stein 1992, White 1993, Whitman and nutrient limitation of consumer growth (thin dotted et al. 1994, Elser et al. 2000). It is, for example, not lines in Fig. 4) would be moved towards lower nutrient uncommon that exclusive plant feeding only delays quota per plant biomass (i.e., to the right). This would starvation but does not allow reproduction of zooph- limit the conditions for coexistence of the herbivores ytophagous insects (Naranjo and Gibson 1996). In this to a smaller area in parameter space. Possibly more case, the omnivore cannot persist on the plant alone, restrictive is the assumption that a suf®ciently large and exclusion of the intermediate consumer (which is amount of nutrients can be bound in herbivore biomass needed to transform low quality plant tissue into high to affect the nutrient stoichiometry of plants. This may quality animal tissue) by the omnivore becomes im- be realistic in, e.g., pelagic aquatic systems (to which possible even in the most productive environments (J. the model of Loladze et al. was originally applied), but van de Koppel and P. M. J. Herman, unpublished man- is less likely in terrestrial arthropod systems, where uscript). plants are big compared to herbivores and the nutrient Loladze et al. (in press) have shown that low re- content of plant tissues is usually scarcely affected by source quality may also enable stable coexistence of the amount of nutrients stored in herbivores. Terrestrial two herbivores competing for a single plant with ¯ex- plant quality may, however, vary in response to her- ible nutrient content (see Fig. 4A, B). In their model, bivore densities because of inducible plant defenses nutrients bound up in herbivore biomass are not avail- (Agrawal and Karban 1999). It is quite conceivable that able to plants, and herbivores may, in turn, be limited the effects of density-dependent variation in defensive by the nutrient content of their food. This creates com- plant chemicals are similar to the effects of variation petition for limiting nutrients among herbivores and in plant nutrient content, because increases in herbivore plants and stable coexistence of the two herbivores is densities should, in both cases, negatively affect the only possible, if all three species are nutrient limited. growth rates of both plants and herbivores. Thus, low nutrient content in plant biomass is a pre- For simplicity, I have limited the analysis of the roles requisite for the evolution of omnivory from a com- of resource quality and abundance to stable precursor Special Feature bas .A,adR .Hl.20 h mato consumer± of impact The 2002 Holt. D. R. and A., P. Abrams, bene®ts specialization. and vs. costs generalization to diet ef®ciencies) of response conversion in more (e.g., dynamically on level evolve feed trophic to capacity one the than affecting traits which models, in with are investigated be pathways should likely these evolutionary Whether omnivory. towards path- the ways evolutionary of for the feasibility conditions Still, dynamical delineates population type. mainly food specialist analysis pro®table a present more into the evolve of should consumer omnivore oth- the because, the erwise, omnivory, for of requirement maintenance important and an evolution con- is intermediate This higher the alone. or a sumer resource the has when either than on types always food feeding both omnivore on feeding when the rate growth I±III Models of highly systems. therefore nonequilibrium is to quality extend resource to likely low stabiliz- of The effect extinction. ing to suf®- consumer drive a to intermediate that sustained the is risk population the omnivore large reduce ciently omnivore the the from ¯ows to weak resource Essentially, 1998). al. 1997, and et Hastings equilibrium McCann and both (McCann omnivore in systems the nonequilibrium omnivory to maintain resource help en- the of can from ¯ows consistent nutrients weaker that and case, notion ergy any general more in sta- the is, quality with systems resource omnivory low not is that bilizes population omnivory result case The such which in maintained. extinct, during go and mortality troughs with- to additional able be not the stand may however, the predation hand, intraguild of of other troughs victim the during On high population. com- especially resource the be on may feeding petitor one towards the pressure On tendencies. selection opposing hand, two of depend will balance scenario the likely omni- a on of is system evolution a such Whether from vory 2002). 1980, Holt McGehee ¯uc- and and populations Abrams (Armstrong consumer synchrony two in the tuating resource with single a possible, on is consumers two of a Unsta- coexistence quality. from ble resource evolves ®xed with omnivory however, system that competitive may, possibility the scenario up open nonequilibrium A systems. 2566 uddb S Gat#E-020) h nvriyof University Barbara. the Santa #DEB-0072909), UC and (Grant California, NSF Center a by Na- Synthesis, and the funded Analysis by Ecological for supported Center the unpublished tional of Group, part Working sharing as conducted Theory for was Competition work Koppel This de me. with van manuscripts Amar- Johan Priyanga thank and especially asekare I manuscript. earlier the and an of on Loladze, version comments Irakli and/or discussions Krivan, for Vlastimil McCann Kevin Koppel, de van Johan eorecce nteceitneo optn species. competing of Biology coexistence Population the Theoretical on cycles resource hn ee bas rynaAaaeae ilFagan, Bill Amarasekare, Priyanga Abrams, Peter thank I tms epitdotta nalnmrclexamples numerical all in that out pointed be must It A L CKNOWLEDGMENTS ITERATURE 62 C ITED :281±295. 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M. and S., Diehl, of strengths the and sizes consumer Relative 1993. S. Diehl, interactions Complex 1992. Stein. A. R. and R., D. DeVries, ro,M .17.Tentin ttso la el ncon- in cells algal of status nutrient The 1974. R. M. Droop, artn .G r,adN .Hiso,S.19.Cause± 1993. Sr. Hairston, G. N. and Jr., G. N. The Hairston, 2003. Denno. F. R. and Styrsky, D. J. D., M. Eubanks, con- ecological The 1999. Denno. F. R. and D., M. Eubanks, A. Dobberfuhl, R. D. Denno, F. R. Fagan, F. W. J., J. Elser, ot .D,adG .Pls 97 hoeia framework theoretical A 1997. Polis. A. evolu- G. and and D., Length R. Holt, 1979. Conrad. M. and M., H. Hastings, tg-tutrdhs n t feto otsuppression. host on effect Naturalist its American and host stage-structured a ae 1±17 switching. trophic Pages of aspects adaptational and evolutionary of Academy National (USA) the Sciences of Proceedings theory. niche and lso.Aeia Naturalist American clusion. London of Society Royal B the of Proceedings coexistence. USA. 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APPENDIX A The derivations of the stability of the three-species equilibrium of a two-consumer±one-resource system with unidirectional consumer interference and of the criteria for mutual invasion of the two consumers are available in ESA's Electronic Data Archive: Ecological Archives E084-064-A1.

APPENDIX B

The derivation of the coexistence region in eRP-K space for model II with omnivory is available in ESA's Electronic Data Archive: Ecological Archives E084-064-A2.