Oecologia (2006) 149:256264 DOI 10.1007/s00442-006-0439-7COMMUNITY ECOLOGY
Habitat context influences predator interference interactions and the strength of resource partitioning
A. Randall Hughes Jonathan H. Grabowski
Received: 6 September 2005 / Accepted: 10 April 2006 / Published online: 17 May 2006 Springer-Verlag 2006
Abstract Despite increasing evidence that habitatstructure can shape predatorprey interactions, fewstudies have examined the impact of habitat context oninteractions among multiple predators and the conse-quences for combined foraging rates. We investigatedthe individual and combined eVects of stone crabs(Menippe mercenaria) and knobbed whelks (Busyconcarica) when foraging on two common bivalves, thehard clam (Mercenaria mercenaria) and the ribbedmussel (Geukensia demissa) in oyster reef and sand Xathabitats. Because these species co-occur across theseand other estuarine habitats of varying physical com-plexity, this system is ideal for examining how habitatcontext inXuences foraging rates and the generality ofpredator interactions. Consistent with results from pre-vious studies, consumption rates of each predator inisolation from the other were higher in the sand Xatthan in the more structurally complex oyster reef habi-tat. However, consumption by the two predators whencombined surprisingly did not diVer between the twohabitats. This counterintuitive result probably stemsfrom the inXuence of habitat structure on predatorpredator interactions. In the sand-Xat habitat, whelkssigniWcantly reduced their consumption of their less
preferred prey when crabs were present. However, thestructurally more complex oyster reef habitat appearedto reduce interference interactions among predators,such that consumption rates when the predators co-occurred did not diVer from predation rates whenalone. In addition, both habitat context and predatorpredator interactions increased resource partitioningby strengthening predator dietary selectivity. Thus, anunderstanding of how habitat characteristics such asphysical complexity inXuence interactions among pre-dators may be critical to predicting the eVects of modi-fying predator populations on their shared prey.
Keywords Context dependency Habitat structure Oyster reef Predator dietary selectivity Predator interference
Ecologists are increasingly realizing the importance ofmulti-species interactions and their consequences forcommunity structure and ecosystem function (Chapinet al. 2000; Shurin et al. 2002; DuVy et al. 2005; Iveset al. 2005). Recently, several lines of research haveconverged on examining the role of species interactionsin a food web context (Shurin et al. 2002; DuVy et al.2005; Ives et al. 2005). Of primary interest is whetherinteractions in a multi-species assemblage can be pre-dicted by combining the pair-wise interactions of thecomponent species, or whether emergent eVects arise(Strong 1992). For example, there is a rapidly growingliterature on emergent multiple predator eVects on preysuch as risk enhancement (i.e., more prey are consumedthan expected based on the single predator eVects) as
Communicated by Pete Peterson
A. R. Hughes (&)Bodega Marine Laboratory and Section of Evolution and Ecology, University of California-Davis, P.O. Box 247, Bodega Bay, CA 94923, USAe-mail: email@example.com
J. H. GrabowskiGulf of Maine Research Institute, 350 Commercial St., Portland, ME 04101, USA123
Oecologia (2006) 149:256264 257well as risk reduction (i.e., fewer prey are consumedthan expected based on the single predator eVects;Soluk and Collins 1988; Sih et al. 1998).
In addition to a growing understanding of how inter-actions among multiple predator species impact preyconsumption, there is a long history of research on theeVects of habitat context on predatorprey interac-tions. Predator foraging eYciency generally variesinversely with habitat heterogeneity (Diehl 1992; Beckand Watts 1997; Beukers and Jones 1997; Cowlishaw1997), and predatorprey interactions can change dra-matically in response to habitat complexity (Crowderand Cooper 1982; Werner et al. 1983; Schriver et al.1995; Grabowski and Powers 2004). In general, individ-ual predators consume fewer prey in more structurallycomplex habitats (Peterson 1982; Blundon and Ken-nedy 1982; Irlandi and Peterson 1991; Finke andDenno 2002; Grabowski 2004; Warfe and Barmuta2004). The fact that structurally complex habitats (e.g.,submerged macrophytes, oyster reefs, coral reefs)often support greater abundances and diversity thanunstructured habitats is often attributed to reducedpredation in these habitats (Heck and Wetstone 1977;Summerson and Peterson 1984; Beck 2000; Lenihanet al. 2001; Grabowski et al. 2005), although these pat-terns could also be due to greater propagule retentionor enhanced food concentration in complex habitats(Tegner and Dayton 1981; Summerson and Peterson1984).
The negative eVects of structural complexity on pre-dation success probably depend on a combination ofseveral factors. Refuge availability for prey is oftenpositively associated with habitat structure (HuVaker1958) and can stabilize predatorprey interactions byproviding habitat patches where predators are nolonger capable of accessing prey resources. For exam-ple, whelk predation on clams is lower in seagrass habi-tats than in unvegetated areas; this reduction inpredation is greater for clams living in and among thedense seagrass roots than those living above the sea-grass root mat, suggesting that the belowground struc-ture physically prevents whelks from readily locatingand extracting subsurface clams (Peterson 1982). Evenwhen habitat complexity does not completely removethe risk of predation, the very elements of habitats thatcreate structure can decrease the foraging eYciency ofpredators by interfering with a predators ability tolocate and handle prey (Crowder and Cooper 1982;Summerson and Peterson 1984). For instance, crabsspend more time handling non-prey shell fragments instructurally complex shell/sand mixtures, reducingtheir overall foraging eYciency on clams (Sponaugleand Lawton 1990).
Despite a growing emphasis on multiple predatoreVects and the well-documented impact of habitat com-plexity on predator foraging eYciency in individualpredatorprey interactions, understanding of the eVectsof habitat context on predatorpredator interactions islimited (but see Siddon and Witman 2004). Habitatstructure can reduce intraspeciWc interference competi-tion among predators, and thereby counteract negativeeVects of habitat complexity on individual foragingeVectiveness (Grabowski and Powers 2004). Thus, insome cases when multiple predators are present,increased structural complexity may result in greateroverall prey consumption than in less complex habitats(Finke and Denno 2002; Siddon and Witman 2004;GriVen and Byers 2006). Determining how habitat con-text generally aVects interactions among predators willrequire sorting out the relative strength of these coun-teracting mechanisms. Given that variation in habitatcomplexity is a feature of most if not all ecological sys-tems, understanding how such variability inXuencesinteractions among predators and the resulting conse-quences for prey survivorship is critical to our ability tomodel trophic interactions and food web dynamics.
In estuarine systems, species often co-occur acrosshabitats of varying complexity, making them ideal sys-tems in which to examine the impact of habitat varia-tion on species interactions. In estuaries of thesoutheastern US, stone crabs (Menippe mercenaria)and knobbed whelks (Busycon carica) utilize seagrassmeadows, sand Xats, and oyster reefs to forage forcommon bivalve prey such as hard clams (Mercenariamercenaria) and ribbed mussels (Geukensia demissa)(Irlandi and Peterson 1991; Nakaoka 2000). PreviousWeld and laboratory studies indicate that crabs (Summ-erson and Peterson 1984; Sponaugle and Lawton 1990)and whelks (Irlandi and Peterson 1991) have higherconsumption rates in unvegetated sand Xats than struc-turally complex habitats such as seagrass meadows oroyster reefs. Yet despite a long history of researchexamining the impact of predation on bivalve survivor-ship and growth rates (e.g., Peterson 1982; Sponaugleand Lawton 1990; Irlandi and Peterson 1991; Micheliand Peterson 1999; Nakaoka 2000), little is known ofhow habitat characteristics inXuence the potentialinteractions between the multiple species of predatorsthat consume bivalve prey in this system.
We investigated the interactions between stone crabsand knobbed whelks when foraging on two commonbivalves, hard clams and ribbed mussels. Althoughwhelks are incapable of consuming stone crabs, thesecrabs do occasionally consume whelks (Williams 1984),suggesting the potential for predator interference whencrab and whelk encounters are common. At the sizes123
258 Oecologia (2006) 149:256264 used in our experiment (see below) actual intraguildpredation is unlikely, although behavioral interferencebetween predators possibly still occurs. We assessed theimpact of habitat context on predator interactions byconducting the experiment in habitats of diVering struc-tural complexity and refuge availability: sand Xat (sim-ple) versus oyster reef (more complex) habitat.Characteristics other than habitat complexity also diVerbetween these habitats, such as the presence of shell as apotential physical barrier to predators in the oyster reef.
We included multiple bivalve prey species to mimicthe presence of alternative prey items in nature andallow for potential resource partitioning (Ives et al.2005). In addition, prey switching by crabs (Siddon andWitman 2004; GriVen and Byers 2006) and whelks(Walker 1988; Nakaoka 2000) has been documented inprevious studies, highlighting the potential importanceof including alternative prey. Although both predatorsconsume epifaunal and infaunal prey species, the com-mon intertidal bivalve species used in this experimentprobably diVer in their susceptibility to predominantlysurface-feeding crabs and burrowing whelks. In sandXat habitats, hard clams live in the sediment, whereasmussels reside on the sediment surface; in oyster reefs,mussels attach themselves on the surface of the shelllayer, while clams are found just beneath the oystershell layer. Thus, variation in the susceptibility of theprey to particular predators is potentially magniWed inthe oyster reef, where the shell functions as an addi-tional barrier between surface and burrowing organ-isms. Determining how predator interactions andhabitat context inXuence predator selection of preyand subsequent prey survivorship will increase ourunderstanding of how these factors contribute to thedistribution, abundance, and diversity of prey speciesin coastal estuaries.
One of the strengths of this system for examiningmulti-species trophic interactions is that each predatorleaves behind characteristic predation marks: crabschip or crush bivalve shells, while whelks Wle the edgeof the shell (Peterson 1982; Irlandi and Peterson 1991;Nakaoka 2000). Thus, assuming that predators do notcrush or Wle prey that were previously consumed byanother predator species or died from natural causes,the shell fragments remaining after a bivalve is con-sumed can be used to distinguish among predators andto evaluate species-speciWc relative rates of predation.Although the shell markings used to infer predatorconsumption patterns could overestimate crab con-sumption if some of the crushed bivalve shells wereWrst Wled open and consumed by whelks, we did notWnd any evidence of crushed shells with Wle markings.We hypothesized that:
1. Predation rates by each predator are reduced inthe habitat providing a structural refuge for prey(i.e., oyster reef).
2. Overall predation rates are lower than expectedwhen both predators are present due to a negativeinteraction between the predators.
3. Habitat complexity reduces this negative interac-tion between predators, which could counteractreductions in per capita foraging rates.
4. Habitat complexity and multiple predators eachinXuence predator selectivity of prey.
Materials and methods
This study was conducted in a randomized completeblock design with two replicates per treatment perblock and four blocks through time, beginning inAugust 2000. Treatments were randomly assigned toeach of 16 mesocosms (see below) in a balanced222 factorial design, with habitat (sand Xat or oys-ter reef), stone crab (presence or absence), andknobbed whelk (presence or absence) as Wxed factors.Predator and prey densities were based on ourobservations and a previous Weld survey (Nakaoka2000). We used an additive design: stone crab treat-ments received one Menippe [mean carapace width(SE)=104.7 (2.6) mm]; whelk treatments received twoBusycon [mean length (SE)=142.4 (2.5) mm; 193.1(2.4) mm]; and multiple predator treatments receivedone Menippe and two Busycon. Because crabs gener-ally consume prey at higher rates than whelks (J. Gra-bowski, personal observation), we included multiplewhelks per treatment to achieve similar rates of preda-tion across treatments.
The experiment took place in 16 large, Xow-throughmesocosms encasing experimental habitat plots in aconcrete tank (6 m9 m1.2 m) at the University ofNorth CarolinaInstitute of Marine Sciences (UNCIMS). Each mesocosm consisted of a plastic cylindricalpool (1.7 m diameter=2 m2) enclosed on the sideswith 6-mm plastic fence that extended 1.2 m from thebottom of the pool. The mesocosms were covered with10-mm-mesh bird netting on top to prevent escape ofenclosed organisms and deter bird predation.
Before each run of the experiment (treated as blocksin time), we collected predators and mussels from theWeld. Predators were starved for at least 3 days beforethe start of the experiment. Stone crabs were collectedusing baited crab pots, while whelks and mussels werecollected by hand. Hard clams were obtained from123
Oecologia (2006) 149:256264 259Mark Hooper, Hooper Family Seafood, Smyrna, NorthCarolina. The experimental pools were assembled byWrst stocking each mesocosm with 95 l of sieved (10-mmmesh) sand. Twenty-Wve adult clams of known size[mean shell length (SE)=50.1 (0.1) mm] were thenadded to each mesocosm to allow them enough time(approximately 2 h) to burrow naturally in the sand.Following the addition of clams, the oyster reef treat-ments received 19 l of dead oyster shell scattered care-fully on top of the mud to avoid clam mortality. Inaddition, 57 l of vertically oriented shells of dead oys-ters was added to these treatments to mimic the verticalstructure of natural oyster reefs. Once the reefs wereconstructed, 25 mussels [mean length (SE)=76.8(0.3) mm] were spread across the surface of each habi-tat. These prey densities are within the range of whatwe have observed in Back Sound, North Carolina (J.Grabowski, unpublished data). The holding pond wasthen Wlled with Xowing (0.270.29 l/s; Grabowski 2004),unWltered seawater from Bogue Sound, North Caroli...