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

MIGHT NITROGEN LIMITATION PROMOTE OMNIVORY AMONG CARNIVOROUS ?

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 habitats. Because omnivory has im- portant consequences for broad areas of theoretical and applied ecology, 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 herbivores supplementing their nutrient-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 plants

(C:Nplants k C:Nherbivores), and a recently documented, though smaller, difference in nitrogen content between predators and their herbivore 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 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; carnivores; intraguild predation; 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 discus- 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 nutrients from nonplant sources (e.g., en- and nutrient ¯ow in ecosystems have emerged (e.g., gage in cannibalism), ``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 ecological stoichiometry, 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 ecosystem 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), landscape ecology (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 adaptations 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).

resource biomass with insuf®ciently low nutrient con- conocephaline katydids, extensive plant feeding oc- tent. In a sense, available C in excess of the consumer'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 foraging 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 pollen and seeds) in addition to 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), beetles (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 protein 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 eating 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 allometry, 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- adaptation 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 mineral 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 wolf survivorship of and diet growth the of to addition experimental acids the amino example, (Strohmeyer For bugs 1998). stink al. et predaceous as invertebrate 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, abundance prey or in toxicity, differences nutrition 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 proteins 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 ingestion 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 omnivore. 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 bear 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 community 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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