Concepts & Synthesis

CONCEPTS & SYNTHESIS EMPHASIZING NEW IDEAS TO STIMULATE RESEARCH IN ECOLOGY

Ecology, 86(10), 2005, pp. 2568±2577 ᭧ 2005 by the Ecological Society of America

PARADOXICAL AVOIDANCE OF ENRICHED HABITATS: HAVE WE FAILED TO APPRECIATE OMNIVORES?

DOUGLAS W. M ORRIS1 Department of Biology and Faculty of Forestry and the Forest Environment, Lakehead University, Thunder Bay, Ontario P7B 5E1 Canada

Abstract. Omnivores have not ®gured prominently in our understanding of food webs and prey dynamics even though they can have substantial direct and indirect effects on the structure of ecological communities and on the dynamics of interacting species. The important role of omnivores is implicated by the paradoxical results of a food-supplementation experiment. The experiment was designed to test theories that predict how habitat change affects the distribution of habitat-selecting species. According to theories of habitat selection, a quantitative change in habitat (as caused by supplemental food) should increase consumer population size and alter habitat selectivity. Related theories of patch use predict that consumers should increase their use of enriched patches. A two-year experiment on two species of small mammals in Canada's boreal forest failed to alter population densities of red-backed voles, but did cause a dramatic shift in vole habitat use. Rather than increasing their use of feeding stations as predicted by classical theory, voles avoided them. Deer mice did not respond to the experimental treatments. The paradoxical results occurred because omnivorous black bears altered prey behavior by increasing predation risk at feeding stations. Revised theory con®rms the indirect omnivore effect, and demonstrates that the behavioral paradox is far more likely for omnivores than for other types of predators. The behavioral paradox of enrichment highlights not only important new, and potentially sta- bilizing, roles for omnivores, but also the pervasive in¯uences of behavior and habitat selection on population dynamics and regulation. Key words: boreal forest; competition; deer mice, ecology of fear; food web; habitat selection; ideal-free distribution; omnivore; paradox of enrichment; population regulation; predation risk; red- backed voles.

INTRODUCTION zero. The result was anathema to those ecologists who believed that competition could be estimated from On occasion, great ecological insights emerge from niche (and habitat) overlap. Rosenzweig (1979) had a ``failed'' experiments. Perhaps the most famous ex- better idea. The species are in fact strong competitors; ample is Schroder and Rosenzweig's (1975) reciprocal so strong that the persistent threat of competition cre- removal experiment on two competing kangaroo rats. ates the very habitat preferences that eliminate our abil- When Schroder and Rosenweig removed Dipodomys ity to measure their competitive interaction. Rosen- ordii from its preferred desert grassland, they expected invasion by the closely related D. merriami. Instead, zweig's invention of isoleg theory proved the point, the grids were quickly repopulated by Ord's kangaroo and his clever metaphor to the ghost of competition rats. When they removed D. merriami from its favored cemented the concept ®rmly in the minds of community desert scrub, the area was reinvaded by Merriam's kan- ecologists. garoo rats. Even though the two seed-eating rodent I report on a similar ``failed'' experiment in Canada's species are similar, the experiment revealed stereotyped boreal forest that also reveals an extremely interesting habitat preferences that reduced competition to near and potentially widespread effect. My assistants and I enriched habitats exploited by red-backed voles (Cleth- rionomys gapperi). Study plots contained an equal mix- Manuscript received 31 May 2004; revised 8 December 2004; ture of ``shrub'' and ``moss'' habitat. We added sun- accepted 7 February 2005; ®nal version received 24 March 2005. Corresponding Editor: B. J. Danielson. ¯ower seed and rodent chow on different plots at sta- 1 E-mail: [email protected] tions representing either shrub, moss, or a mixture of 2568 October 2005 ON THE IMPORTANCE OF OMNIVORES 2569 the two. In the second year of the experiment we re- dix C). We used pretreatment vole data to measure versed the treatments. Voles avoided the enriched habitat preference along the habitat gradient so that we patches. When we reversed the treatments, voles re- could de®ne, for each plot, two equal groups of stations versed their preferences. We think we know why. Om- representing preferred (shrub), and less preferred nivorous black bears foraged extensively on the en- (moss) habitat. riched patches and increased the risk of predation to We estimated habitat use by trapping small mammals small mammals. with ``Longworth'' live traps for several trapping pe- I begin by describing the context and design of the riods (each station trapped over three consecutive ®eld experiment. I demonstrate how the experiment's nights) in 1991 through 1994 (Appendix B). We com- paradoxical results can be interpreted in the light of plemented our habitat-use data from live-trapping with increased predation risk from omnivorous predators. I counts of rodent tracks (an estimate of ``activity den- develop a simple theory that links the behavioral par- sity''; Kotler 1985; Appendix B). adox of enrichment to theories of habitat selection. I We collected control data on small-mammal abun- then use the theory to evaluate the relative roles of dance during three trapping periods in 1991. We col- predators vs. omnivores on prey habitat use and pop- lected experimental data in 1992 and 1993 (nine trap- ulation regulation, as well as their respective in¯uences ping periods each year) followed by a second control on the structure of food webs. year in 1994 (eight trapping periods). Each ®eld season began in mid-May and ended in early September. I CONTEXT OF THE EXPERIMENT estimated population densities and recruitment for each Theories of habitat selection predict that the spatial plot during each trapping period (Appendix B). distribution of individuals should re¯ect the ®tness that Beginning in 1992, I randomly assigned the eight they can expect to achieve in different habitats (Fre- ®eld plots to four treatment groups for supplemental twell and Lucas 1969, Rosenzweig 1981, Morris 1988, feeding in the 1992 and 1993 ®eld seasons. Two plots Synthesis & Concepts 2003; Appendix A). Fitness will depend on resource (1 and 6) served as natural controls. The controls re- levels (e.g., Sutherland 1983, Pulliam and Caraco 1984, ceived no supplement in either year. Plots 4 and 7 Fagen 1987, Morris 1994), on the ef®ciency of har- served as ``quantitative'' controls. I selected nine sta- vesting those resources (Morris 1988), and on the risks tions at random from each of the shrub and moss hab- associated with their harvest (Brown 1988). I attempted itats. The 18 stations received supplemental food in to test the theory with a multi-year experiment using 1992. The other 18 stations on plots 4 and 7 received red-backed voles as the primary model organism. The food in 1993. The remaining plots received ``qualita- experiment was centered on food-supplementation tive'' treatments. Plots 2 and 5 received supplemental treatments (increased resource), that allocated those food in the ``shrub'' habitat. All 18 shrub stations on supplements differentially to preferred (shrub), less each plot received supplemental food in 1992. Plots 3 preferred (moss), or a shrub±moss mixture of habitats. and 8 received supplemental food in the ``moss'' hab- According to current theory and intuition, vole densities should have increased in treated plots relative to itat. I reversed the treatments in 1993 (plots 2 and 5 controls, and the increase should have been greater in received food in the moss habitat, plots 3 and 8 received preferred habitat (with its associated high foraging ef- food in the shrub habitat). We trapped all plots again ®ciency and low risk of mortality) than in secondary in 1994 for comparison with the pretreatment data col- or mixed treatments. lected in 1991 (temporal control). The six treatment plots received the twice-weekly METHODS food supplements. We calculated the expected ener- Several assistants and I manipulated habitat richness getic needs of voles when at maximum density (30 in a large homogeneous fragment of boreal forest in voles per plot from the 1991 data; mean August density northwestern Ontario, Canada (48Њ55Ј N, 89Њ55Ј W; ϭ 29.125 voles), then doubled that value (Appendix Appendix B). In 1991 we established eight 1-ha rep- D). We broadcast two forms of resources, sun¯ower licate study plots, arranged with two columns and four seeds and rodent chow (to ensure access to both energy rows. We separated each 100 ϫ 100 m plot from its and essential nutrients), at the calculated rate (totaling neighbors by an intervening equal-sized, 1-ha area that four times the energetic requirements of voles). we avoided during the entire study. The outside margin I compared vole population numbers, habitat selec- of the ``checkerboard'' was at least 200 m from the tivity, and recruitment on treatment plots with the nat- edge of disturbed habitat (roads and small cutblocks). ural controls to assess the in¯uence of supplemental Each study plot was composed of a 6 ϫ 6 sampling food (Table 1). I compared ``shrub and moss treat- grid with 20-m spacing between the 36 sample points. ments'' with the quantitative controls to evaluate pos- We began by measuring habitat and vegetation at all sible differences in foraging ef®ciency or risk associ- sampling stations, and then summarized the data with ated with food located in alternative habitats. I repeated principal-components analysis to create a single com- the tests with deer mice, the second most abundant posite variable representing habitat variation (Appen- rodent species. Concepts & Synthesis est pe s otramn) pre posttreatment)² vs. (pre- Density 2570 (eigenvalue signi®cant A year food. supplemental doc- of in¯uence would the within-subjects effect ument treatment a signi®cant as A effect). analyzed ®xed period ran- trap between-subjects effect; a dom as design analyzed split-plot group balanced a (treatment (GLM in 2001) variance SPSS of procedure, analysis three- repeated-measures shrub full a on factor with recruitment based and categories), here moss (electivity; and choice habitat sizes, seeds). partially sun¯ower and included seeds digested which of consume (many to piles fecal ¯oor and forest chow) the open bears ripped fort- where had sites and two (feeding omnivores digs for as for activity plot bear weekly recorded each twice searched as we food stations Then same added nights. the We in at adding 1992. resources So, by in of activity. experiment amount their the same repeated the quantify we not on 2004, presence did August their we of plots, notes the casual made and periment aia h odi de o sdacmaal sim- comparable a used I (paired to. analysis added pli®ed which is on food depend food the of habitat addition the to related effects apigaeuc [KMO] adequacy sampling h la atr fba ciiyddntrqiesta- require not did activity analysis. bear tistical of pattern clear The in rmsalsrb ( shrubs gra- small a from comprised var- axis dient habitat habitat screened The seven E). (Appendix of iables set ®nal the in variation nams-oee oet¯o toeed(positive end one (e.g., shrubs at large ¯oor to forest values), moss-covered a on itdde itro evsadwoydbi tthe at debris woody and values). leaves (negative of other litter deep ciated ABLE uniaietetet eevdfo tbt rfre n espeerdhabitats. experiment). preferred the less after and and preferred (before both 4 at year not. food and did ࿣ received controls 1 treatments food; year Quantitative supplemental in § received collected plots were Treatment data ³ posttreatment and Pre- ² eevdfo nls rfre aia nya n npeerdhbtti er3. year in habitat preferred in and 2 year in habitat preferred less in food Received ¶ oe npeerdadls rfre aiasi oelfrs oae nnrhr nai,Canada. Ontario, northern in located forest boreal in habitats preferred less and preferred in voles igepicplcmoetacutdfr44% for accounted component principal single A population mouse and vole on data the analyzed I ex- main the during bears encountered we Though T eevdfo npeerdsrbhbtti er2adi espeerdms aia nya 3. year in habitat moss preferred less in and 2 year in habitat shrub preferred in food Received lciiy(er2v.ya ;cnrl)y 2 yr treatments treatments controls) 3; year vs. 2 (year Electivity controls)³ vs. (treatments Recruits controls) vs. (treatments Density lciiy(er2v.ya ;ls rfre) r2 yr pre 2 yr pre preferred)¶ less 3; preferred) year vs. 3; 2 year (year Electivity vs. quantitative)§ 2 3; (year year Electivity vs. 2 (year Electivity posttreatment) vs. (pre- Electivity posttreatment) vs. (pre- Recruits eris(er2v.ya )y 2 yr 2 yr 3) year vs. 2 (year Recruits 3) year vs. 2 (year Density ϫ .Abifsmayo e rdcin n eut rma®l xeietta upeetdfo o red-backed for food supplemented that experiment ®eld a from results and predictions key of summary brief A 1. ramn neato ol eosrt that demonstrate would interaction treatment ϭ .8 asrMyrOknmaueof measure Kaiser-Meyer-Olkin 3.08, otatPeito Result Prediction Contrast ttsia design Statistical R t ESULTS et)t sestetakdata. track the assess to tests) Vaccinium ϭ Alnus .0 ftecommon the of 0.80) ࿣ n es herbs dense and ) ihterasso- their with ) OGA .MORRIS W. DOUGLAS r2 yr tv ausidct rfrnefrmoss). for preference a neg- indicate habitat, values shrub ative for preference indicate were values (pos- categories itive values clas- habitat two electivity were these re¯ect subsequent value to recalculated All high moss. a as with si®ed stations clas- shrub, were PC1 as for si®ed value score. PC (negative) median low the a at with two Stations Consequent- in 1). habitats (Fig. partitioned gradient I the sta- ly, of extreme ends avoid both at to tions tended somewhat Mice were preferences complicated. mouse more Deer 1). Fig. 0.89; Ͼ lndmr-rls ieryfo `hu' o``moss'' to ``shrub'' de- (electivity from electivities linearly Habitat more-or-less gradient. clined the along habitat for oetaudneaddistribution. in that roles and suggests key abundance habitats, play rodent shrub risk both for habitat-dependent in and species cover predation both for of in and than preference habitat, cover The under open). tracks in with the than tubes shrub more in and tubes of moss, tracked that less more to were similar (marginally was voles tracks preference mouse habitat the deer abundant, Though G). (Appendix pce Apni ) oohrseiscomprised species other No F). (Appendix additional 12 species among divided re- were The proportions [18%]). maining captures 1225 [17%], individuals (285 n nec aia oetbscontained tubes moss, more in than habitat shrub each in in greater and was con- tracks tubes vole tracking for of taining voles number mean red-backed The habitat. of mirrored shrub live- data preference the track trap-revealed The in F). that the Appendix to (68%; similar data proportion trap a in and tracks, n 1 falcpue 49 f6750). of (4798 captures all of 1718) of 71% (1123 and individuals the of 65% with community oet[C scores, [PC] ponent maniculatus mys %o h community. the of 5% e-akdvlshdaceradovospreference obvious and clear a had voles Red-backed Clethrionomys ഡ ഡ ഡ Clethrionomys Ͻ Ͼ ഡ ഡ ഡ ഡ rcswe lcdudrcvrta nteopen the in than cover under placed when tracks otpre pre pre post post post r3y 2 yr 2 yr 2 yr 2 yr 2 yr 2 yr 3 yr 3 yr 3 yr 3 yr 3 yr 3 yr Ͼ Ͼ ϭ otostreatments treatments controls controls a h eodms bnatspecies abundant most second the was . to 0.7 lodmntdordt nmammal on data our dominated also oiae h niesmall-mammal entire the dominated oe n mice and Voles Ϫ F .6wt akdprincipal-com- ranked with 0.06 1,23 ϭ 203.5, clg,Vl 6 o 10 No. 86, Vol. Ecology, P ഡ Ͼ Ͼ Ͻ Ͼ Ͻ Ͻ ഡ ഡ ഡ post post post r3 yr 3 yr 3 yr 3 yr 3 yr 3 yr 0.001, Peromyscus Clethriono- ഡ ഡ controls controls R 2 ϭ October 2005 ON THE IMPORTANCE OF OMNIVORES 2571

FIG. 2. Vole density and recruitment were greater in 1991 than in 1994, but habitat preference (electivity) was similar. Values are mean Ϯ SE; N ϭ 8 plots.

shrubs. And, when we reversed treatments in 1993, the voles also reversed their preference! The response by deer mice was also a paradox. Deer mice were indifferent to the experiment (Appendix H).

Habitat electivity and densities were similar between Synthesis & Concepts the two control years (P Ͼ 0.3 for each). Densities

tended to be higher in period 9 than in period 8 (F1,4 ϭ 5.63, P ϭ 0.08), and there was a suggestion that FIG. 1. Red-backed vole habitat preference (estimated by ϫ Ivlev's index of electivity using all vole captures from 1991; electivity also varied through time (year period in- ϭ ϭ see Appendix C) declined linearly along a principal-com- teraction in electivity [F1,4 5.73, P 0.075]). But ponent gradient from ``shrub'' to ``moss'' habitat. Deer mice the theory's predicted year ϫ treatment interaction in avoided extreme sites. ϭ habitat electivity was ``highly nonsigni®cant'' (F3,4 0.39, P ϭ 0.77). No other effect or interaction was signi®cant for ei- Adequate numbers of voles necessary for reasonable ther species (there was a hint of a year ϫ trap period ϭ ϭ estimates of habitat choice (set, arbitrarily, at 10 cap- interaction for vole recruitment [F1,4 5.54, P tures per plot per period) were available only in the 0.08]). The number of vole recruits was virtually iden- late summer of each year. Preference for shrub habitat tical in both periods in 1992, but was much greater in (electivity) during this time was similar among treat- period 9 than 8 in 1993 (mean recruits ϭ 10.88 and ments and in the two control years (1991 and 1994, 6.00, respectively). The detection of recruits depends ϭ ϭ F1,4 0.21, P 0.67) despite much higher densities critically on the timing of live trapping and a pulse of ϭ ϭ and recruitment in 1991 (F1,4 24.31, P 0.008 and recruits from synchronized reproduction could easily ϭ ϭ F1,4 46.81, P 0.002, respectively; Table 1, Fig. 2). be restricted to a single trapping period. Such an effect No interaction was close to statistical signi®cance (set could produce the apparent year ϫ trap period inter- at P ϭ 0.05). Densities in the two treatment years were not different, but did increase during the summer (period main ϭ ϭ effect, F1,4 14.63, P 0.019, analyses restricted to periods 8 and 9; Fig. 3). Most importantly, voles altered their selection of habitat depending on which treatment was applied in each year (year ϫ treatment interaction, ϭ ϭ F1,4 31.38, P 0.003; Table 1, Fig. 4). Habitat selection in the two types of control plots was similar in both years, and re¯ected Clethrionomys' clear preference for shrub habitat. But the paradoxical pattern of habitat choice in the other treatments was opposite ex- pectation. Voles ``avoided'' supplemental feeding stations in both years. When treatments received food in FIG. 3. Vole density in eight 1-ha study plots was greater shrub habitat, voles increased their use of moss. When in trap period (TP) 9 than in trap period 8 during both 1992 treatments received food in moss, voles preferred the and 1993. Concepts & Synthesis o nunetedaai aao nhbttselection. habitat does in exists, paradox truly dramatic it the if in¯uence even not interaction, the But action. N 2572 h nihetsts lc er ( exploited bears Black mammals, sites. small enrichment to the addition two But in stations. omnivores, food-supplemented at abundant than more control were at voles, red-backed small- prey, dominant at The mammal true. than was captured) opposite The easily sites. more other (or prey abundant if more only but were Perhaps, sites? enriched the to attracted lt nbt years. of both set in different control represents a plots Control/Control at and years, represents (but both habitats Both/Both in both 1993, stations) in in in food habitat habitat receiving shrub moss plots the the Moss/ in 1993, in and in food habitat 1992 receiving moss plots the represents in and Shrub 1992 in habitat shrub a opeeec o n ramn.Vle r mean are years. Values treatment. different any two for preference in mice no Deer plots treatment. had in study reversals with reversed to choice Habitat applied treat- which were on depended ments habitat) shrub for preference dicate oaiu aswt naptt o ml rodents. small for appetite an and with bears jays ravening voracious from threats serious potentially the edxI.Ee huhteewr bnatsesfor seeds bears, abundant and were voles, there jays, though (Ap- Even stations I). feeding of pendix distribution the about learned Jays quickly robbers. seed sun¯ower persistent became h atm,adGa as( Jays during Gray as well and as daytime, night at the seeds sun¯ower for foraged F ol h aao ecue eas rdtr were predators because caused be paradox the Could ϭ IG .SrbMs ersnsposrciigfo nthe in food receiving plots represents Shrub/Moss 4. .Vl aia hie(lciiy oiievle in- values positive (electivity; choice habitat Vole 4. . Omnivores Clethrionomys eioescanadensis Perisoreus ru americanus Ursus uthv feared have must OGA .MORRIS W. DOUGLAS Ϯ SE ) ) ; n te oeta mioe eeconspicuously were omnivores potential sparse. squirrels, Jays, other J). sta- (Appendix feeding plots and treated of they all proportion and on night, large tions and equally day an both disturbed active were con- all the Bears from on absent trols. active virtually were were yet bears plots, treatment Black bears. toward directly eal r nApnie ,L n M. and L, Full K, bears). Appendices by of in activity paradox are increased details the habitat-selection for not the (but voles for account could pn oteeprmn tall. re- at to experiment failed the species, to abundant spond most Deer second pattern. the the mice, explain to for insuf®cient or was reversed traps resources, for voles whether the Competition, treatments, preference. their the reversed shrubs. we choosing by When responded they habitat, moss food the added to we When responded moss. of voles exploitation habitat, increased consumers. shrub by to by food patches added we enriched When of theo- use and increased intuitive predict theory both patch-use and to Intuition opposite expectations. retical was habitat the voles treatment And, by recruitment. detectable use or no density supple- vole were in to there effects response But in food. selection mental and habitat sites their shrub-covered for altered preference strong a sessed hs ae a ototnopst oexpectation. to opposite in often use most habitat of was pattern cases in the used these because years) pos- and 2 32 periods, analyses, the 2 my of plots, ®ve (8 only comparisons in re- sible problem competition potential trap the a rejected of vealed I estimates animals). because contained traps hypothesis all than of more half when lost one was single experiment a the occupy during to habitat opportunity the (the by captures constrained of number are measures electivity the because ybas hr a lasa bnac fsupple- mice. of and voles abundance for an available always food was mental there bears, disturbances by the despite because, failed hypothesis competitors. re- The different supplemented many by because consumed were quality sources habitat increase to treatments. with predictably foraging vary age the not and did voles distribution, of body-size distribution hypothesis class ratio, this sex rejected I the sites. because foraging rich the be- food. from different without controls not the was and voles plots of feeding tween rate be- capture failed hypothesis the This cause traps. to attracted been have h 04eprmn one niciiaig®nger incriminating an pointed experiment 2004 The H that hypotheses additional four least at are There e-akdvlsaehbttslcos oe pos- Voles selectors. habitat are voles Red-backed H H H 1 4 3 2 h aia-eeto aao ol cu simply occur could paradox habitat-selection The . h odadto xeiet a aefailed have may experiments food-addition The . subordinates excluded have may voles Dominant . not may stations feeding of vicinity the in Voles . D ISCUSSION Caveats clg,Vl 6 o 10 No. 86, Vol. Ecology, October 2005 ON THE IMPORTANCE OF OMNIVORES 2573

Meanwhile, at a smaller scale of habitat use revealed only if the intercept of Eq. 4 is Յ 0, and if the slope by their tracks, voles preferred the protective cover of is less than unity (diverging isodars). Since, in our shrubs over open areas. The preference was clear in all example, the two types of sites are otherwise identical, years and in both shrub and moss habitat. The pattern the slopes of the ®tness curves can be assumed equal ϭ ϭ of microhabitat use is consistent with numerous studies (b2A b2 b1, e.g., Morris 1988; the slopes could on small mammals that have demonstrated higher pre- differ if foraging behavior changes with resource den- dation risk in the open than under protective cover (e.g., sity). Thus, for the paradox to occur, the risk of pre- Ͼ Brown et al. 1988, Kotler et al. 1991, 1992, Brown et dation must be greater in the manipulated set (p2A al. 1992, 1994, Kotler and Blaustein 1995, Morris p1), and 1997, Morris and Davidson 2000). The pattern in microhabitat use is also consistent with the larger-scale Ͻ p1 W2A W1 (5) preference of voles for shrub habitat in our control data. p2A Vole habitat use suggests a major role of predators, and (the prediction of unequal predation risk could be ver- the risk of predation, in their habitat choice. Indeed, i®ed by careful foraging experiments in the two types predators may play a crucial role in maintaining sep- of sites, e.g., Brown 1988, Brown and Kotler 2004). arate habitat preferences for voles and deer mice (Mor- Are omnivores or ``obligate'' predators most likely ris 1996). But why should that risk be related to sup- to cause the paradox? Consider, ®rst, the case for om- plemental feeding? nivores. Assume, as in the case of adult black bears, A theory that the omnivore is not at risk from other predators. Assume, as well, that consumption of prey is incidental Imagine that prey individuals have a choice of for- and forms a negligible component of the omnivore's aging at two sets of identical sites, that they use the diet. Following similar logic as above, the omnivore's sites in a way that maximizes an individual's ®tness, Synthesis & Concepts isodar is given by and that an individual's expected ®tness is equal in both sets at equilibrium (an ideal-free distribution; Fretwell Ϫ ϭϩWO2AOWb1 O1 and Lucas 1969). Following Brown and Kotler (2004), O2A O1 (6) bbO2AO2A ϭ pF11(N 1) pF 22(N 2) (1) where O is the number of omnivores and subscripts where p is the probability of surviving predation, F is identify the omnivore and the two types of sites. Thus, the ®tness of survivors, and N is the number of indi- omnivores will be attracted to the augmented sites dividuals using the two types of sites (subject to the rectly by the additional food (the omnivore isodar in- constraint that the total number of individuals is a con- tercept with supplemental food is greater than zero) Ͼ ϭ ϩ and O2A O2. For omnivores, there is no paradox. But stant N N1 N2). For simplicity, assume that ®tness is a linear and negative function of the number of in- the increased presence of omnivores at supplemented dividuals using a particular type of site: sites can create a paradox for their prey. Even if consumption of prey by omnivores is only incidental, more ϭ Ϫ Fii(N ) W ibN ii (2) omnivores are present at augmented sites and predation Ͼ where W is the maximum ®tness achieved at low den- risk will increase (p2A p1). Meanwhile, the omnivore sity. When the sites are identical, each set should have is consuming the added resource, and the augmenta- an equal number of individuals: tion's incremental ®tness to prey will be less than if the omnivores were absent. And if omnivores are the ϭ N21N . (3) ®rst to arrive at manipulated sites, or if they are more Now, imagine that we add supplemental food (A) to ef®cient at consuming the added food than are prey, all sites in one of the sets (2). Then, the supplement may fail to increase the ``total'' ®tness of prey individuals at augmented sites (W Ͻ W ). p (W Ϫ bN) ϭ p (W Ϫ bN) 2A 1 2A 2A 2A 2A 11 11 Each effect will reinforce inequality (Eq. 5). Ͼ such that W2A W1. Following rearrangement, So a behavioral paradox (Eq. 5) will depend on the omnivore's ability to consume the added resource (and ϭϪWpWpb2A 11 ϩ 1 1 N2A ΂΃N1. (4) the paltry prey in this example) as well as how large bpbpb2A 2A 2a 2A 2A of a threat it poses to prey. But even if the intercept Eqs. 3 and 4 represent the linear habitat isodars (Morris of Eq. 4 is positive, the slope will be Ͻ1, and the 1987, 1988) where ®tness is identical in ``control'' and manipulated isodar (Eq. 4) will cross over the control manipulated sites, respectively. In the absence of pre- isodar (Eq. 3). It is thereby possible that a prey species dation, the intercept of Eq. 4 will be positive, and more living at low density (such as the deer mouse) could individuals will occupy sites (Eq. 2) following food respond positively to the manipulation, or not at all addition than before (when densities were equal; Eq. (where the two isodars cross one another). A prey spe- 3). But with predation, a behavioral paradox of prey cies living at high density (vole) would always exhibit Ͼ distribution (N2 N2A) will occur (for all values of N) the behavioral paradox of enrichment. Concepts & Synthesis saddta hni sasn ( food absent when is it captured when easily than par- added more is behavioral are no prey be unless can the adox There by predators. unaffected of is number occupying sites prey control of vs. number food-augmented the that demonstrates 8 Eq. equi- the prey: yields of isodar, distribution the librium to converted when which, ®t- Predator in rate. ness death instantaneous predator's the is where i 2574 97 hr hrdpeaossbiieterde of diet their subsidize predators shared Kotler where and Holt 1987) 1977, (Holt competition apparent with habitat in determined is abundance prey that ®rst, ine, nbt ye fstsi hseulwhen equal thus is sites of comparing types both example ®tness in predator's our the sites, In food-augmented and predators. control of number the niiulsrie rdto ( predation survives individual ee padt h ettohclvl(omnivores). level trophic next the to het- upward spatially neled chan- are of resources prey and advantage patches, high, take productive erogeneous to alter is unable and risk are risk trophic predation species predation same When increase the distribution. prey, at prey sites their rich as in level Om- feeding ago. by years 30 nivores, over (1971) Rosenzweig de- paradox by numerical scribed the to comparable paradox ioral unlikely. impossible, nevertheless not be- is while predator-induced enrichment, of a and paradox that risk havioral share conclude prey prey We with when vigilance). decline especially should individual (and under prey abundance densities, a But prey to predators. most risk across the of and number circumstances, those the many at would increase as would re- predation functional sites, of occur III Type risk may a the (as in sponse), added densities is prey food moderate when at catch to prey easier If are responses. functional and numerical predator's ihwihte ovr ryit e predators, new into prey convert they which with rysol epeettee(rdtr aen direct no have (predators on there effect present be more should because prey indirectly only sites enriched to attracted sites. food-supplemented in larger is mortality oeyb rdtr LtaVler dynamics): (Lotka-Volterra predators by solely h e aiaatc aeo rdtr npe,and prey, on predators of rate attack capita per the h hr-emercmn aao irr htseen that mirrors paradox enrichment short-term The Imag- predators. obligate for case the consider Now, hs ohter n aahv eeldabehav- a revealed have data and theory both Thus, titpeaos ncnrs ihonvrs ilbe will omnivores, with contrast in predators, Strict P i stenme fpredators, of number the is sgvnb iiigbt ie fE.7by 7 Eq. of sides both dividing by given is W 2A N eaN 2 .Mawie h rbblt htaprey a that probability the Meanwhile, ). 2 A A 2 ϭ dP A dt 2 aea ea i A ad ea 2 ϭ A 112 1 11 Implications Ϫ 2 eaNP A iiiii i i i ii d 2 N A 1 ϭ Ϫ 111 1 11 eaN ΂΃ a Ϫ p 2A ildpn nthe on depend will ) 2 A dP Ϫ Ͼ 2 e A d a Ϫ A steef®ciency the is 2 ,o fpredator if or ), d (8) . OGA .MORRIS W. DOUGLAS a (7) is d oe.Pe a eeteescnrgt tenriched at omni- congregate attracts nevertheless to may resource response Prey their in vores. because behavior their but alter predators, prey al. because et special, not is Polis enrichment of paradox (e.g., behavioral The predation 1989). intra-guild with dynamics. sociated population vole on bene®t net the no and has habitat, The food by ``compartmentalized'' sites. pro®table is less web and food risky less shift to voles activity and food their to supplemental appears of In risk bene®t be. the predation exceed would voles, red-backed otherwise of they case than the less pop- reduces are and ®tness size response Prey ulation ef®ciency. prey foraging prey each overall prey's the Regardless, than rather resources. prey the consuming on and placed ef®ciency, value digestive depend the renewal, and would and foraging omnivore abundance omnivore's resource the as to things The site such omnivore. on each the of to reduce value sites may net those sites of rich attractiveness of of the avoidance are prey prey of size, and use omnivores similar omnivore's when the But on sites. will augmented effect patches insigni®cant rich of an avoidance have prey prey voles), small and and asymmetric (bears omnivores of case large the between In relationships patches. om- rich the best-of-all- of by use repelled nivore's are otherwise prey Adaptive omnivore's strategy. worlds the that apprehension compromise and vigilance increased and patches, competi- apparent long-term tion. and short- both har-through and to mortality, predator-induced ability through resources, their vest in the interference different with through four competition omnivore, resource least through at lose that in Prey prey ways. lose But omnivores sites. enriched with the coexist lower poten- to through a attraction again at prey and tial prey, resources win their rich than can on level trophic Omnivores foraging by rates. once capture twice, prey associated any in and increases abundance only prey far win increased Predators of predators. through be strict by to caused com- likely apparent petition and is mortality the prey than to magnitude on attractiveness greater their effect by The depreciated valu- omnivores. are patch prey a of make to risk that able species' resources very prey of The the predation. resources increase shared prey, the intermediate on keying Omnivores, ilarly. Ko- and (Holt 1987). size population tler thereby and and ®tness distribution, both prey. and modify potential behavior other their for alter predation Prey species of prey risk one the in rich increase ac- patches term, in foraging ef®ciency their short and increase the tivity or in aggregate But that resources. predators not shared do otherwise for they compete if interaction even negative, net is the prey ones. between and abundant increase, on populations concentrating Predator by species prey rare oehtsmlrhbttsit aeotnbe as- been often have shifts habitat similar Somewhat rich of avoidance include responses prey Adaptive sim- functions enrichment of paradox behavioral The clg,Vl 6 o 10 No. 86, Vol. Ecology, October 2005 ON THE IMPORTANCE OF OMNIVORES 2575 patches when either the patches are exceptionally rich, ACKNOWLEDGMENTS or when competing omnivores represent small risks. This research would have been impossible without the ded- As they do so, additional predators may alter their patch icated hard work and friendship of numerous assistants in- selection to mirror that of the prey (or other more abun- cluding R. Christie, D. Davidson, D. Duckert, L. Heidinga, S. Hoffstrom, M. Kelly, S. Kingston, T. Knight, R. Madell, dant prey, including omnivorous members of the pred- K. Morris, M. Norton, M. Oatway, G. Pardalis, and T. Sa- ator guild). Prey distribution will then depend on the lavich. Many others have helped to maintain the northern- frequency, duration, and relative value of resource Ontario project since 1994. I thank you all. I am especially patches, as well as the risks of direct and indirect pre- thankful to Brent Danielson, Joel Brown, Burt Kotler, and John Orrock for many candid and helpful suggestions that dation. improved this contribution, as did those by Kate Lessells and Omnivores visiting rich patches will have a dispro- Kelly Morris. I also thank W. Smith, J. Westbroek, and Ab- portionate effect on the trade-offs between food and itibi-Consolidated, Incorporated, for access to research sites, safety of their prey. Unlike predators, whose risk to use of the Sorrel-Lake camp, and for their patient, cheerful encouragement of our long-term research in a valuable com- prey may decline with the amount of time the predator mercial forest. I gratefully acknowledge Ontario's Environ- lingers in a patch (e.g., a detected predator is not nearly mental Youth Corps, which helped to fund ®eld personnel, as dangerous as a stealthy one), the opposite is likely and Canada's Natural Sciences and Engineering Research to apply to omnivores. True, the risk of predation from Council for its continuing support of my research in evolutionary and community ecology. omnivores may also decline with time, but so, too, does the food value of the patch. Prey that could otherwise LITERATURE CITED tolerate a declining level of predation risk in a rich Brown, J. S. 1988. Patch use as an indicator of habitat pref- patch exploited only by other equally brave conspe- erence, predation risk, and competition. Behavioral Ecol- ci®cs may not be able to balance the risk against the ogy and Sociobiology 22:37±47. depleting value of a patch harboring a hungry omni- Brown, J. S., and B. P. Kotler. 2004. Hazardous duty pay and

the foraging cost of predation. Ecology Letters 7:999± Synthesis & Concepts vore. The resulting paradox could even produce an in- 1014. verse relationship between resource abundance and the Brown, J. S., B. P. Kotler, R. J. Smith, and W. O. Wirtz, II. local population density of consumers if omnivores 1988. The effects of owl predation on the foraging behavior concentrate only on the richest patches. Exciting new of heteromyid rodents. Oecologia 83:512±518. Brown, J. S., B. P. Kotler, and T. J. Valone. 1994. Foraging predictions will emerge when the prey also possess under predation risk: a comparison of energetic and pre- omnivorous diets. Food web models that fail to account dation costs in rodent communities of the Negev and Son- for such coadaptive behaviors are very likely to mis- oran deserts. Australian Journal of Zoology 42:435±48. represent the ¯ows of energy and nutrients, and pos- Brown, J. S., M. W. LaundreÂ, and M. Gurung. 1999. The ecology of fear: optimal foraging, game theory and trophic sibly misinterpret the dynamics and stability of the interactions. Journal of Mammalogy 80:385±399. community. Brown, J. S., R. A. Morgan, and B. D. Dow. 1992. Patch It is unclear how frequently predation risk from om- use under predation risk. II. A test with fox squirrels, Sciu- nivores may have caused food supplementation, food rus niger. Annales Zoologici Fennici 29:311±318. Fagen, R. 1987. A generalized habitat matching rule. Evo- web, habitat-selection, and predator manipulation stud- lutionary Ecology 1:5±10. ies (e.g., Sih et al. 1985) to ``fail.'' It is even possible, Fretwell, S. D., and H. L. Lucas, Jr. 1969. On territorial despite the ``smoking gun'' of our 2004 ``bear exper- behavior and other factors in¯uencing habitat distribution iment,'' that omnivores were not responsible for the in birds. Acta Biotheoretica 14:16±36. Holt, R. D. 1977. Predation, apparent competition, and the paradoxical use of enriched habitats by red-backed structure of prey communities. Theoretical Population Bi- voles. Even so, the concept deserves our attention. ology 12:197±229. Competitive omnivory is potentially widespread and Holt, R. D., and B. P. Kotler. 1985. Microhabitat utilization adds substantially to the panoply of behaviorally me- in desert rodents: a comparison of two methods of mea- surement. Journal of Mammalogy 66:374±378. diated ``third-party'' trophic effects that in¯uence the Holt, R. D., and B. P. Kotler. 1987. Short-term apparent com- distribution and abundance of species, and that may petition. American Naturalist 130:412±430. act to stabilize communities. It may even be time to Kotler, B. P.,and L. Blaustein. 1995. Titrating food and safety discard cherished ecological notions about top-down in a heterogeneous environment: when are the risky and safe patches of equal value? Oikos 74:251±258. vs. bottom-up processes (control by omnivores, if we Kotler, B. P., L. Blaustein, and J. S. Brown. 1992. Predator can call it that, is not only top-down and bottom-up, facilitation: the combined effects of snakes and owls on but also horizontal and diagonal). As we do so, we the foraging behavior of gerbils. Annales Zoologici Fennici need to pay more attention to how the dynamics of 29:199±206. Kotler, B. P., J. S. Brown, and O. Hasson. 1991. Factors populations, the interactions among species, the struc- affecting gerbil foraging behavior and rates of owl pre- ture of communities, the resulting implications to food dation. Ecology 72:2249±2260. webs, and the ``ecology of fear'' (Brown et al. 1999), Morris, D. W. 1987. Tests of density-dependent habitat se- are played out through adaptive habitat selection. Ig- lection in a patchy environment. Ecological Monographs nore habitat, or ignore behavior, and you risk misin- 57:269±281. Morris, D. W. 1988. Habitat-dependent population regulation terpreting both the processes, and their emergent pat- and community structure. Evolutionary Ecology 2:253± terns, in populations and communities. 269. Concepts & Synthesis 2576 oe saalbei S' lcrncDt Archive: Data Electronic ESA's in available is voles vial nEAsEetoi aaArchive: Data Electronic ESA's in available -asuyposi otenOtro aaa saalbei S' lcrncDt Archive: Data Electronic ESA's in available is Canada, Ontario, northern in plots study 1-ha vial nEAsEetoi aaArchive: Data Electronic ESA's in available Archive: Data Electronic ESA's in available is voles ula,H . n .Crc.18.Lvn ngop:is groups: in Living 1984. Caraco. T. and R., H. Pulliam, ecology The 1989. Holt. D. R. and Myers, A. C. A., G. Polis, 1981. Niemala. P. and Arruda, J. Fretwell, D. S. L., Oksanen, foraging Optimally 2000. Davidson. L. D. and W., habitat D. of Morris, theories apply we can How 2003. W. D. Morris, prairie in mice deer foraging Optimally 1997. W. D. generalist Morris, and specialist of Coexistence 1996. W. D. Morris, im- and alternatives matching: Habitat 1994. W. D. Morris, ecito f®l ie swl stapn n rcigmtosue oass est n aia s yred-backed by use habitat and density assess to used methods tracking and trapping as well as sites ®eld of description A S' lcrncDt Archive: Data Electronic ESA's A6. lcrncDt Archive: Data Electronic al umrzn h eut fapicplcmoet nlsso h omnvraino ee aia aibe is variables habitat seven of variation common the on analysis principal-components a of results the summarizing table A al ouetn h uuaienme fsalmma niiul,ttlcpue,adtak eoddo eight on recorded tracks and captures, total individuals, small-mammal of number cumulative the documenting table A ecito ftemtost eemn o uhsplmna eoresol eaddt xeietlposis plots experimental to added be should resource supplemental much how determine to methods the of description A red-backed on change habitat of effects the assess to analysis and measurements habitat and vegetation of description A hr notmlgopsz?Pgs122±147 Pages size? group optimal an Sys- there and Ecology of Review Annual other. tematics each eat competitors that potential predation: intraguild of evolution and produc- primary Naturalist of American gradients tivity. in ecosystems Exploitation ®tness. in differences habitat with use Ecology patch match mice Wild- management? Research and life conservation wildlife to selection landscape of absence and theory Oikos habitat effects. of test a mosaics: Ecology selection. habitat via rodents Evolutionary communities. and Ecology populations to plications al ouetn aia rfrne frdbce oe n ermc sidctdb hi rcsi vial in available is tracks their by indicated as mice deer and voles red-backed of preferences habitat documenting table A eiwo h neligter rdcighwhbttuesol epn ohbttcag saalbei ESA's in available is change habitat to respond should use habitat how predicting theory underlying the of review A 81 8 20 :387±406. :2061±2066. :297±330. 30 80 :303±319. :31±42. clgclArchives Ecological 118 clgclArchives Ecological :240±261. 77 clgclArchives Ecological clgclArchives Ecological :2352±2364. E086-138-A1. in OGA .MORRIS W. DOUGLAS .R Krebs R. J. E086-138-A7. clgclArchives Ecological Archives Ecological PEDXB APPENDIX PEDXE APPENDIX PEDXF APPENDIX PEDXD APPENDIX C APPENDIX PEDXG APPENDIX PEDXA APPENDIX oezeg .L 91 aao fercmn:tedesta- the enrichment: of Paradox 1971. L. M. Rosenzweig, oezeg .L 99 pia aia eeto ntwo- in selection habitat Optimal 1979. L. M. Rosenzweig, iiaino xliaineoyesi clgcltm.Sci- time. ence ecological in ecosytems exploitation of bilization Second UK. ecology. Oxford, Behavioural Publications, editors. Scienti®c Blackwell Davies, edition. B. N. and pce opttv ytm.Pgs283±293 Pages systems. competitive species oezeg .L 91 hoyo aia eeto.Ecol- selection. habitat of theory A 1981. L. M. Rosenzweig, crdr .D,adM .Rsnwi.17.Perturbation 1975. Rosenzweig. L. M. and D., G. Schroder, E086-138-A5. E086-138-A4. uhrad .J 93 grgto n h ielfe'dis- free' `ideal the Illinois, and Aggregation Chicago, 1983. SPSS, J. W. 11. Sutherland, Version SPSS. 2001. SPSS. Stroh- K. and Petranka, J. McPeek, M. Crowley, P. A., Sih, ogy Fischer Gustav Germany. ecology. Stuttgart, Population Verlag, editors. Jacobs, J. and nlsso optto n vra nhbttutilization habitat in overlap and between competition of analysis ologia rbto.Junlo nmlEcology Animal of Journal tribution. USA. Ecol- of Systematics Review and Annual communi- experiments. ogy ®eld prey of and review a competition, ties: Predation, 1985. meier. 171 62 :385±387. E086-138-A3. E086-138-A2. :327±335. 19 iooy ordii Dipodomys :9±28. 16 :269±311. and clgclArchives Ecological iooy merriami Dipodomys clg,Vl 6 o 10 No. 86, Vol. Ecology, 52 :821±828. in .Halbach U. E086-138- Oec- . October 2005 ON THE IMPORTANCE OF OMNIVORES 2577

APPENDIX H A table documenting the indifferent response of deer mice to food supplements is available in ESA's Electronic Data Archive: Ecological Archives E086-138-A8.

APPENDIX I Evidence demonstrating increased presence of omnivores at feeding stations avoided by red-backed voles is available in ESA's Electronic Data Archive: Ecological Archives E086-138-A9.

APPENDIX J An illustration of the results from a 2004 replicate of the original experiment is available in ESA's Electronic Data Archive: Ecological Archives E086-138-A10.

APPENDIX K A description of the tests of four alternative hypotheses that could possibly account for the behavioral paradox of enrichment observed in red-backed voles is available in ESA's Electronic Data Archive: Ecological Archives E086-138-A11.

APPENDIX L An illustration of how vole habitat choice (electivity) varied among plots and between the two years of the supplemental feeding experiment is available in ESA's Electronic Data Archive: Ecological Archives E086-138-A12. ocps&Synthesis & Concepts

APPENDIX M A table documenting abundances of sun¯ower seeds and mouse-chow pellets at feeding stations used to augment resources consumed by red-backed voles is available in ESA's Electronic Data Archive: Ecological Archives E086-138-A13.