OPENQ ACCESS Freely available online e pLOSl- Preference Alters Consumptive Effects of Predators: Top- Down Effects of a Native Crab on a System of Native and Introduced Prey EmilyW. Grason"'', BenjaminG. Miner"' 1 WesternWashington University, Biology Department, Bellingham, Washington, United States of America,zshannon Point MarineCenter, Anacortes, Washington, UnitedStates of America

Abstract Top-down effects of predators in systems depend on the rate at which predators consume prey, and on predator preferences among available prey. In invaded communities, these parameters might be difficult to predict because ecological relationships are typically evolutionarily novel. We examined feeding rates and preferences of a crab native to the Pacific Northwest, Cancer productus, among four prey items: two invasive of drill the marine whelks Urosaipinx cinerea and inornata! and two species of oyster Crassostrea gigas and Ostrea iurida! that are also consumed by U. cinerea and O. inornata. This system is also characterized by intraguild predation because crabs are predators of drills and compete with them for prey !. When only the oysters were offered, crabs did not express a preferenceand consumedapproximately 9 juvenileoysters crab " day ". Wethen testedwhether crabs preferred adult drills of either U. cinerea or O. inornata, or juvenile oysters C. gigas!. While crabs consumed drills and oysters at approximately the same rate when only one type of prey was offered, they expressed a strong preference for juvenile oysters over drills when they were allowed to choose among the three prey items. This preference for oysters might negate the positive indirect effects that crabs have on oysters by crabs consuming drills trophic cascade! because crabs have a large negative direct effect on oysters when crabs, oysters, and drills co-occur.

Citation:Grason EW, Miner BG 012! PreferenceAlters Consumptive Effects of Predators:Top-Down Effects of a NativeCrab on a Systemof Nativeand IntroducedPrey. PLos ONE 72!: e51322.doi:10.1371/journal. pone.0051322 Editor:Louis-Felix Bersier, University of Fribourg,Switzerland ReceivedJuly 17,2012; Accepted October 31, 2012; Published December 6, 2012 Copyright:! 2012Grason, Miner. This is an open-accessarticle distributed under the termsof the CreativeCommons Attribution License, which permits unrestricteduse, distribution, and reproductionin any medium,provided the originalauthor and sourceare credited. Funding:This work wasalso funded in part by NSFaward OCE-0741372, and a grantfrom the WashingtonSea Grant Program, University of Washington, pursuantto NationalOceanic and Atmospheric Administration Award No. NA07OAR4170007. Theviews expressed in the manuscriptare those of the authorsand do not necessarilyreflect the viewsof NOAAor anyof its sub-agencies.Additional financial support was received from the WesternWashington University Office of SponsoredPrograms and BiologyDepartments. The funders provided financials support only, and hadno role in studydesign, data collection and analysis, decisionto publish,or preparationof the manuscript. CompetingInterests: The authors have declared that no competinginterests exist. ' E-mail:[email protected]

Introduction chain might not function in the same way as a comparable chain comprised only of co-evolved natives [12]. Prey preference in the Predation is a major force structuring un-invaded [1,2] and European green crab, Garcinusmaenas, destabilized competitive invaded P,4] communities. Directly, predators can limit [5,6], interactions between native and non-native clams, allowing the regulate [7], or extirpate [8] prey populations through consump- established non-native gem clam, Gemma gemma, to become tion. These effects can, in turn, be propagated indirectly through invasive [13]. Appropriate management of invasions therefore the community in many ways, including trophic cascades,indirect requires investigation of the pathways by which predators impact facilitation, and apparent competition [9]. Direct and indirect the community. effects of predation can engender quantitative, as well as We investigated a commercially and ecologically important food qualitative, shifts in community composition. For instance, web with a native predator, mediated by invasive intermediate predators can enhance community diversity by consuming prey Figure 1!. In Washington State, two invasive speciesof oyster competitively dominant prey, thereby reducing interspecific drill, the marine whelks Ocenebrainornata and Urosalpinxcinerea, are competition and facilitating the persistence of competitively common predators of oysters. Because drills threaten the recovery inferior prey [10]. The population and community effects of efforts of a rare native oyster Ostrealuridu! and yield of commercial predators depend on the number of prey they consume, and their oyster harvest, the effects of drills as predators of oysters have been preference. well studied [14 16]. Drills ofboth speciesgenerally prefer to prey The trophic dynamics of an invaded food web are not always on small oysters, and can consume juveniles at a rate of 0.3 oysters predictable because predator-prey interactions are typically per day [16] potentially limiting oyster populations at this life evolutionarily novel. Predators might not be able to recognize history stage. However, relatively little is known about predatory an invasive prey as potential food, or overcome defenses of control that native crabs, which are common predators of marine invasive prey [11]. Even where predators are generalists and snails, exert on this system but see [12]!. As predators ofboth drills invasive prey are ecologically similar to natives, an invaded trophic and oysters, crabs could impact oysters directly by preying on

PLOSONE ~ www.plosone.org December2012 ~ Volume 7 ~ Issue 12 ~ e51322 PreferenceAlters Consumptive Effectsof Predators them, and indirectly by consuming drills and releasing oysters and preference of crabs differed for the two oyster species. We from drill predation Figure I!. Where all three species coincide, then investigated crab feeding on both speciesof invasive drill and the relative importance of direct and indirect effects of crabs on non-native C. gigas. oysters will be determined by which prey, drills or oysters, the crabs prefer. The drills' habitat overlaps with that of several native System decapod crabs, including the red rock crab, Cancerproductus [17]. A Both Atlantic U. cinerea!and Japanese oyster drills . inornata, large-clawed generalist predator, C. productuspreys on native synonyms include Ceratostomainornatum, and Ocinebrellusinornatus! whelks and can strongly influence the community structure of were unintentionally introduced to the Pacific Northwest by the intertidal habitats [18]. early 1920's [24]. Both drills arrived as hitchhikers on cultch This system is also characterized by asymmetric intraguild newly settled larvae on shell material! of non-native oysters predation IGP!: crabs are both predators of, and competitors imported to buoy the oyster-growing industry U. cinereafrom the with, drills, but drills do not prey on crabs [19]. Similar systemsare east coast of the United States on Crassostreavirginica Eastern common in native intertidal communities where generalist crabs oyster!, and 0. inornatafrom the Asian Pacific Ocean on Crassostrea and seastars feed on both predatory snails and bivalve prey of gigas !. Because they lack a larval planktonic stage, snails e.g., [20,21]!. Additionally, models predict unintuitive drills are dispersed primarily through human-mediated transport. dynamics caused by IGP in systemswhere the intraguild predator Notably, native whelks are not considered a pest in oyster beds is a non-native species [22], and demonstrate that IGP by non- [24], so we did not include them in our study. natives can accelerate the speed of invasion [23]. Less is known While at least five species of oyster are currently grown and about IGP in systems where the intraguild prey is a non-native. harvested in Washington, we were particularly interested in the Therefore, to estimate the potential for both direct and indirect effects of crabs on non-native C. gigas and native 0. lurida. The effects of crabs on oysters, and the dynamics of IGP, we Pacific oyster, C. gigas, is the most widely introduced, and investigated crab feeding rates and preferences for invasive drills, commercially valuable oyster species worldwide, and has also and two species of oyster. This information will be critical to established naturally recruiting, wild populations in bays and predicting the trajectory of this system, and will help enhance our inland waters of Puget Sound and coastal Washington [25]. In understanding of the role of IGP in invaded communities. contrast, populations of 0. lurida, the only native oyster species in Washington, collapsed in the late 1000's due to overharvesting and Materials and Methods pollution, and have not sustained a harvestable wild population In two experiments conducted at Shannon Point Marine since [26]. Drills are pests to the oyster industry, costing shellfish Center, in Anacortes, WA, we estimated feeding rates and growers money in control and eradication efforts, as well as in preferences of the native red rock crab, Cancerproductus, for two decreased revenues. Additionally, drills could be inhibiting re- species of juvenile oysters Crassostreagigas, and Ostrealurida! and covery efforts aimed at restoring wild populations of the rare and their invasive drill predators Urosalpinx cinerea, and Ocenebra ecologically important native 0. lurida [16,27]. inornata!. We initially tested whether the rates of consumption

Figure 1. Diagram of trophic interactions in our study system. Diagramof trophic interactionsamong native red rock crabs,Cancer productus, two speciesof invasiveoyster drill, Urasalpinxcinerea and Ocenebrainarnata, and two oyster species,native Ostrealurida and non-native Crassostrea gigas. Solid lines represent direct interactions, dashed lines indirect interactions with all arrows pointing in the direction of the trophic effect. doi:10.1371/journal.pone.0051322.g001

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Due to their relatively thin shells,juveniles ofboth oyster species Two experiments were conducted to estimate preference and are most vulnerable to drill predation [16]. Both drills consume feeding rates among the prey items. We first estimated C. pradurtus small individuals of C. gigasand 0. lurida at similar rates of about feeding rates on and preferences among juvenile oysters, Pacific IC. 0.25 0.30 oysters per drill per day [16]. Preference for the two gt'gas!and Olympia IO. lurida' oysters ISeptember, 2009l. Then, we species of drills between these two species of oyster has already estimated C. pradurtusfeeding rates on and preferences for juvenile been established and so was not tested here. Despite divergent oysters, IC. gigas!and both speciesof drill IU. rinereaand 0. inornata! evolutionary histories with these oyster prey, both drills prefer C. IOctober, 2009l. Conducting these experiments separately, rather gigasto 0. lurida oysters of similar size [16]. Population growth of than as a single experiment with all four prey types, allowed for oysters depends on at least some recruits reaching reproductive greater replication. In this way we improved resolution in size without being consumed. Survival of oyster populations, determining crab preference between the two species of oyster therefore, could be strongly affected by predation on juvenile because we thought that a general preference for oysters over drills oysters by adult drills IE. Grason, unpublished data!. Buhle and might obscure any difference between the two oyster species. Ruesink [16] hypothesized that crab predation might limit Comparing preference among adult drills and juvenile oysters was distribution of drills, and therefore their effects on oysters, but ecologically relevant to oyster restoration efforts as well as there is, as yet, no experimental support for this hypothesis. aquaculture scenarios. Oysters in both experiments were marked with enamel to facilitate correct species identification. Different Collection and Husbandry individual crabs were used in each of the experiments. In the first Both male and female red rock crabs, C.pradurtus, were collected experiment, crabs Imean carapace width ~ SE: 106.7~2.1 mml by hand and trap from beaches and docks around Anacortes, WA. were randomly assigned to one of three treatments In = 12l: Ill 25 We assumed crabs had no experience with either speciesof drill or C. gigasonly, I2l 25 0. lurida only, or I3l 25 C. gigasand 25 0. lurida. oyster because those organisms or their remains were not found in In the second experiment, crabs Imean carapace width ~ SE: the areas where crabs were collected. Neither oysters nor invasive 107.2 ~2.2 mml were randomly assigned to one of four treatments drills were present at these sites, likely because oysters have not In = 14l: Ill 25 C. gigasonly, I2l 25 0. inarnataonly, I3l 25 U. rinerea historically been cultured at these sites. This reduces the only, or I4l 25 C. gigas, 25 0. inarnata, and 25 U. rinerea.We used probability that crabs had prior experience with any of the species only C. gigasin this experiment because there was no preference of prey used in our experiments and allows us to infer that between oyster species in our first experiment and this species is preferences are innate. While in the lab, crabs were maintained in more readily available and not of conservation concern. Obser- flow-through aquaria, on a diet of mussels IMytilus sp.l and frozen vation confirmed that there was no predation by drills on oysters fish fillet IZilapia sp.l. Crabs were not starved prior to the feeding during this experiment, and all oyster mortality was due to crab experiments. predation. Atlantic drills, U. rinerea,were collected from naturally recruiting One day prior to each experiment, individual crabs were placed C. gigas reefs in the southeastern corner of Willapa Bay, WA. in separate flow-through bins with 10 individuals of their assigned Japanese drills, 0. inarnata,were collected from commercial C. gigas prey types to allow feeding behavior to stabilize PI]. At the start beds owned by Taylor Shellfish Farms in West Samish Bay, WA. of the experiment, we removed all waste, uneaten food, and shell Drill species were maintained in separate, closed 140 L aquaria, material from the bins, and added individuals of each prey type and allowed to feed ad libitum on mussels and C. gigasjuveniles. appropriate for the treatment of each bin. The number of Juvenile oysters of both species were obtained as seed Isinglesl surviving prey of each type was recorded at 24 hours without from Taylor Shellfish Farm hatcheries. At the time of experiments, replacement. In one replicate, a crab consumed all available prey oysters were of a size at which they could typically be out-planted of one type Iall individuals of C. gigas consumed by one crab in by commercial or recreational growers IC. gigas= 2.7~0.4 cm, 0. choice treatment of oyster preference experiment!. lurida = 2.5~0.2 cml. Oysters were held in sea-tables and had access to a limited amount of plankton that came in with the Analysis natural seawater. We supplemented this diet with commercial To determine whether crabs preferred one type of prey, we shellfish diet IShellfish Diet 1800-Reed Mariculturel at least once developed a new method, which is described below. Currently a week. there is debate about how best to statistically test for preference, and the proposed methods all have benefits and drawbacks Preference Experiments [20,32 35]. With all available methods, it is diflicult to test for For the purpose of this study, preference was defined as preference with more than two species.Because we wanted to test a deviation of feeding behavior proportion of prey consumed of for preference for more than two prey species, we developed an one type! in the presence of choice compared to feeding behavior alternative method carefully considering the concerns raised in without choice [28]. Therefore each experiment included treat- previous studies [26,30 33]. ments in which crabs were offered one prey type only, and one To test for preference, we used the interaction term of a two- treatment where all prey types were offered simultaneously in factor ANOVA with prey type and choice both modeled as fixed equal abundance. This design has the advantage of providing factors. Prey type had two levels in the first experiment Itwo researchers with several relevant estimates of feeding rate and species of oyster! and three levels in the second experiment Itwo clearly differentiates between preference and electivity Ifor speciesof drill and one speciesof oyster!, and choice had two levels a discussion of "preference" versus "electivity" see [29]l. Electivity in both experiments Iwhether crabs had a choice of prey or notl. can cause diet changes in a predator via "prey switching", which The response variable, the proportion of prey consumed, was occurs when predators attack different prey depending on relative calculated as follows. In the no-choice bins, we randomly grouped prey abundance PO]. Such "switching" behavior can be one replicate from each prey type together and calculated the ecologically relevant, but was not tested in this experiment, as proportion of prey consumed for each prey type out of the total we chose to focus on preference as a trait of crabs, rather than how prey consumed for the group. In the choice treatment, we contexts affect the interaction between crabs and the two types of calculated the proportion of prey consumed for each prey type out prey. of the total prey consumed in a single replicate bin. If the

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proportion of each prey type consumed was different when crabs were offered a choice, versus when crabs were only offered a single type, the interaction term of a two-factor ANOVA with prey type and choice as fixed factors would be significant. However, because of our calculations of the response variable, the data were not independent the proportions of each prey type consumed in each replicate where crabs were allowed a choice were, by definition, constrained to total to 1.0. Therefore, use of the F-statistic distribution would calculate an incorrect probability of type 1 error. We therefore generated a null distribution of F-ratios for the interaction between choice and prey type by randomly assigning prey types to bins in both the no choice and choice treatments for each experiment 0,000 iterations!. We used the generated null distribution to calculate the probability of a type I error for the observed F-ratio for the interaction between choice and prey type. To ensure that the results were not particular to a random pairing of bins in the no choice treatment, we randomly re-paired bins in the no choice treatment and re-ran the analysis 1,000 times. Distributions of P values of the interaction between choice and prey type were generated and compared to an alpha value of 0.05 to determine whether crabs preferentially fed on the prey species.All analyses were conducted in R P6]. O. gigas only O /uric,'aonly Qholee

Results

Oyster Preference Experiment Figure 2. Crab feeding rates and preference on native and non- There was no evidence that crabs preferred one species of native oysters. Number mean +. 5E! of oysters consumed by crabs juvenile oyster to the other Figure 2!. Crabs consumed a similar over 24 hours in the oyster preference experiment. Gray bars are number of C. gigasas juvenile 0. lurida when they were offered only Crassostreagigas, Pacific oysters, and white bars are , one species and denied a choice, but consumed slightly more C. Olympia oysters. Crabs were randomly assigned to one of three treatments n = 12!: ! 25 C. gigas only, ! 25 O. lurida only, or ! the gigas than 0. lurida when offered a choice. However, all of the P treatment labeled "Choice", 25 C. gigas and 25 O. lurida. values of the interaction between prey type and choice generated do :10.1371/journal.pone.0051322.g002 in the random pairing of bins were greater than 0.05, suggesting that the interaction term is not significant. Crabs, therefore, do not results from a relatively greater energy yield per unit effort consume a different proportion of juvenile C. gigasand 0. lurida in required to obtain the food from oysters as opposed to well- the presence and absence of choice. armored drills. At sites where crabs, drills, and oysters co-occur, crab Pacific Oysters and Drills Preference Experiment preference could cause a direct negative effect on juvenile oysters There was evidence that crabs preferred non-native oysters to that negates the positive indirect effect of crabs eating drills. In our drills Figure 3!. When offered only one type of prey, crabs did not treatment that allowed crabs to choose, crabs consumed an consume prey types at different rates. An average of 7 juvenile C. average of about 6 oysters and 2 drills one of each species! per gigas,7 0. inornata,or 9 U. rinereawere consumed per crab per day day. Individual drills consume at most approximately 0.3 juvenile in the absence of choice. However, in treatments in which crabs oysters per day [16]. In the presence of choice, therefore, the direct were allowed to choose from among the three prey types, oysters negative effect of an individual crab on oysters is approximately -6 were disproportionately preyed on compared to drills crabs oysters per day, while the positive indirect effect is +0.6 oysters per consumed nearly 6 times as many oysters as either species of day. The net effect of crabs in the system is still strongly negative: drill. Approximately 99.9% of the P values of the interaction 5.4 oysters removed per crab per day. Therefore, despite the fact between factors prey species and choice generated by randomly that they can be highly efficient and motivated predators on drills, pairing bins were less than 0.05, indicating that crabs consumed C. pradurtusis likely to exert stronger direct consumptive effects on a significantly different proportion of oysters in the presence and oysters. Long-term dynamics in this system will depend on absence of choice. population responses of oysters to predation by both crabs and drills. For instance, predation on oysters could facilitate a popu- Discussion lation increase in crabs that could then impact drills negatively via Whether or not crabs demonstrated a preference among prey apparent competition, or deplete oysters to the extent that crabs choices depended on the types of prey offered. In the first switch their search image to prey primarily on drills. experiment, when both prey were oysters, the predator expressed As an intraguild predator, therefore, C. pradurtusinteracts more no preference for either the native or the invasive oyster. In the strongly with drills as a competitor for oysters than as a predator. It second experiment, when both species of drill were offered along is notable that this crab-drill-oyster system does not have the with one speciesof oyster, crabs strongly preferred C. gigas,oysters, characteristics of systemsin which IGP is believed to be stabilizing. to either species of drill. This difference is likely not a product of In asymmetric IGP systems, a condition for stability is that the different handling times for each prey species, as all prey types intraguild predator is the stronger competitor for the extraguild were consumed at relatively similar rates when offered in single resource P7]. In this study, not only is crab-drill predation species treatments. It is probable that the preference for C. gigas unidirectional, but it also seemslikely, based on differences in per

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mesocosmsto prevent drills from using refugia to avoid predation, because both drill species reduce feeding and increase use of refugia when they detect chemicals released by C. produrtns consuming conspecific drills P9]. This design enabled us to better isolate consumptive predation! from non-consumptive intimida- tion! effects of crabs in this system. However, in the field, we would expect that structural complexity could further reduce the rate at which crabs are able to prey on drills, and would also reduce the rate at which feeding drills consume oysters. Therefore, our estimates are likely conservative, as such non-consumptive effects would only increase the relative importance of the direct effects of crab predation on oysters. Notwithstanding the evidence presented here that crabs are unlikely to reduce drill densities in oyster beds, other researchers have noticed that in Willapa Bay, WA, there is an overall negative correlation between abundance of crabs and oyster drills [17]. This might be explained by the fact that crabs do still prey on drills at low levels, even when oysters are present. Additionally, along with emigration and predation, inducible defenses of drills in response to crabs likely carry fitness costs that explain lower drill densities where C. produrtusis present. gigas jQ, /rior;78te U otnerea Our study suggests the interesting possibility that oysters Cho!ce only only only facilitated the invasion of both speciesof drill, not only as a vector Treatment non-native oysters! and food source both native and non-native oysters!, but also by reducing the potential for biotic resistance by Figure 3. Crab feeding rates and preference on oyster drills native crabs. Both drills were originally introduced simultaneously and Crassostreagigas. Number mean +. SE! of prey consumed by with oysters, and, notably, are almost entirely restricted to oyster crabs over 24 hours in the drill/oyster preferenceexperiment. Blackbars beds in Washington State. This granted drills a degree of enemy are Crassostreagigas, Pacificoysters, gray bars are Ocenebrainornata, release, at least in the short term, because crabs preferentially prey Japanesedrills, and white bars are Urosalpinxcinerea, Atlantic drills. Crabswere randomly assignedto one of four treatments n = 14!: ! 25 on oysters when they have a choice. The corollary to this idea is C. gigas only, ! 25 Ocenebrainornata only, ! 25 Urosalpinxcinerea that while C. produrtusmight not strongly affect drill populations in only, or ! the treatment labeled "Choice", 25 C. gigas, 25 O. inornata, oyster beds, crabs could help limit the range of invasive drills to and 25 U. cinerea. oyster beds. Where oysters are rare, it is possible that crabs will doi:10.1371/journal.pone.0051322.g003 switch to consuming relatively more drills, and crabs could thereby provide greater biotic resistance against drill incursion into these capita feeding rates, that crabs are better at exploiting oysters than habitats. This provides one way that context-dependent species drills. Other researchers have pointed out that models of IGP interactions, such as those mediated by preference, could be stability have required systems of closed populations, a condition particularly important in invaded systems. which is clearly not met in many marine habitats where species often have widely-dispersing pelagic larvae [21]. Thus the Acknowledgments population growth rate of oysters in our system might be decoupled from local community and population dynamics. We are very gratefulfor logisticalsupport for this researchcontributed by Alternatively, theory predicts that the three speciesmight be able Taylor Shellfish Farms and the Pacific Northwest Shell Club. Helpful to co-exist exist in habitats where alternative food sources not feedbackon manuscriptswas provided by B. Bingham and M. Peterson. important in the crab's diet e.g., barnacles! could sustain drill populations PB]. Author Contributions Our laboratory experiments did not account for spatial and Conceived and designed i he experiments: EG BM. Performed the temporal heterogeneity that will affect the strength of these experiments: EG. Analyzed the data: BM. Contributed reagents/ interactions in the field. We purposely eliminated structure in our materials/analysistools: EG. Wrote the paper: EG.

References 1. PaineRT 974! Intertidalcommunity structure experimentalstudies on 6. GurevitchJ, MorrisonJA, HedgesLV 000! The interactionbetween relationshipbetween a dominant competitorand its principal predator. competitionand predation:A meta-analysisof field experiments.American Oecologia15: 95 120. Naturalist155: 455 455. 2. HixonMA, BeetsJP 995! Predation,prey refuges, and the structure of coral- 7. KorpimakiE, Krebs CJ 996! Predationand populationcycles of small reeffish assemblages. Ecological Monographs 65: 77 101. mammals A reassessmentof the predation hypothesis. Bioscience 46: 754 764. 5. SaloP, KorpimakiE, BanksPB, NordstromM, DickmanCR 007! Alien R KavanaghRP 988! Theimpact of predationby thePowerful owl, JVittox-rtrettua, predatorsare more dangerousthan nativepredators to prey populations. on a populationof the Greaterglider, Petauroafei-uolaai. Australian Journal of Proceedingsof the Royal Society B-Biologial Sciences 274: 1257 1245. Ecology15: 445 450. 4. GherardiF, AcquistapaceP 007! Invasivecrayfish in Europe:the impactof 9. WoottonJT 994! Thenature and consequences of indirect effects in ecological Proramfiarusclarku on the littoral community of a Mediterraneanlake. Freshwater communities.Annual Review of Ecologyand Systematics 25: 445 466. Biology52: 1249 1259. 10. PaineRT 966! Foodweb complexity and speciesdiversity. The American 5. FitznerRE, Eberhardt LE, RickardWH, GrayRH 994! GreatBasin Canada Naturalist100: 65 75. goosenesting on the mid-ColumbiaRiver, Washington:An historical 11. CarlssonNOL, Sarnelle0, StrayerDL 009! Nativepredators and exotic prey perspectiveand update, 1981 1990. Northwest Science 68: 57 42. an acquiredtasteg Frontiers in Ecologyand the Environment7: 525 552.

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12. Kimbro DL, GrosholzED, BaukusAJ, NesbittNJ, TravisNM, et al. 009i 26. WhiteJ, RuesinkJL, TrimbleAC 009i Thenearly forgotten oyster: Oitrea lunda Invasivespecies cause large-scale loss of nativeCalifornia oyster habitat by Carpenter1864 OlympiaOyster! history and managementin Washington disruptingtrophic cascades. Oecologia 160: 568 575. State.Journal of ShellfishResearch 28: 48W9. 18. GrosholzED 005i Recentbiological invasion may hasten invasional meltdown 27. CookAE, ShafferJA, DumbauldBR, Kauffman BE 000i A planfor rebuilding by acceleratinghistorical introductions. PNAS 102: 1088 1091. stocksof Olympiaoysters I Oitreola conchaphda, Carpenter 1857i in Washington 14. HanksJE 957i Therate of feedingof thecommon oyster driff, Urasalptnxmnerea State.Journal of ShellfishResearch 19: 409 412. Sayi,at controffedwater temperatures. Biological Bulletin 112: 880 885. 28. UnderwoodAJ, Chapman MG, CroweTP 004i Identifyingand understand- 15. ChewKK 960i Studyof food preferenceand rate of feedingof Japanese ing ecologicalpreferences for habitator prey.Journal of ExperimentalMarine OysterDrill, Octneltrajaponica Dunkeri. Washington, D.Cs UnitedStates Fish Biologyand Ecology 800: 161 187. andWildlife Service. 29. SingerMC 000i Reducingambiguity in describingplant-insect interactions: 16. BuhleER, Ruesink JL 009i Impactsof invasiveoyster drills on Olympia oyster "preference","acceptability" and "electivity." Ecology Letters 8: 159 162. IOitrealunda Carpenter 1864i recovery in WillapaBay, Washington, United 80. MurdochW 969i Switchingin GeneralPredators. Experiments on Predator States.Journal of ShellfishResearch 28: 87 96. Specificityand Stabilityof PreyPopulations. Ecological Monographs 89: 885 17. HolsmanKK, McDonaldPS, Armstrong DA 006i Intertidalmigration and 854. habitatuse by subadultDungeness crab Cancer magteter in a NEPacific estuary. MarineEcology Progress Series 808: 188 195. 81. JacksonAC, UnderwoodAJ 007i Applicationof new techniquesfor the 18. YamadaSB, Boulding EG 996i Therole of highlymobile crab predators in the accurateanalysis of choiceof prey.Journal of ExperimentalMarine Biology and intertidalzonation of their gastropodprey. Journal of ExperimentalMarine Ecology841: 1 9. Biologyand Ecology 204: 59 88. 82. ManlyBFJ 998i Commentson designand analysis of multiple-choicefeeding- 19. PolisG, MyersC, Holt R 989i The Ecologyand Evolutionof Intraguild preferenceexperiments. Oecologia 98: 149 152. Predation PotentialCompetitors That Eat EachOther. Annual Review of 88. UnderwoodAJ, Clarke KR 005i Solvingsome statistical problems in analyses Ecolotyand Systematics 20: 297 880. of experimentson choicesof foodand on associationswith habitat.Journal of 20. MengeB, LubchencoJ, GainesS, AshkenasL 986i A Test of the Menge- ExperimentalMarine Biology and Ecology 818: 227 287. SutherlandModel of CommunityOrganization in a TropicalRocky Intertidal 84. Taplin RH 007i Experimentaldesign and analysisto investigatepredator FoodWeb. Oecologia 71: 75 89. preferencesfor prey.Journal of ExperimentalMarine Biology and Ecology 844: 21. NavarreteSA, MengeBA, DaleyBA 000i Speciesinteractions in intertidal 116 122. foodwebs: Prey or predationregulation of intermediatepredatorsg Ecology 81: 85. UnderwoodAJ, ClarkeKR 007i More responseon a proposedmethod for 2264-2277. analysingexperiments on foodchoice. Journal of ExperimentalMarine Biology 22. CourchampF, LanglaisM, SugiharaG 999i Catsprotecting birds: modeffing andEcology 844: 118 115. themesopredator release effect. Journal of AnimalEcology 68: 282 292. 86. R DevelopmentCore Team 009i R: A Languageand Environmentfor 28. Hall RJ 011i Eatingthe competitionspeeds up invasions.Biology Letters 7: StatisticalComputing. Vienna, Austria: R Foundationfor StatisticalComputing. 807 811. Available:http://www.R-project.org. 24. ChapmanWM, BannerAH 949i Contributionsto the life historyof the 87. Holt RD, PolisGA 997i A theoreticalframework for intraguildpredation. Am Japaneseoyster drill, Tntanaliajaponica = Ceratastamatnamatum!, with noteson Nat 149:745 764. otherenemies of the Olympiaoyster, Oitrea lunda. Washington Department of 88. Holt RD, Huxel GR 007i Alternativeprey and the dynamicsof intraguild Fisheries. predation:Theoretical perspectives. Ecology 88: 2706 2712. 25. RuesinkJL, LenihanHS, TrimbleAC, HeimanKW, MicheliF, et al. 005i 89. GrasonEW, Miner BG 012i Behavioralplasticity in an invadedsystem: non- Introductionof non-nativeoysters: Ecosystem effects and restorationimplica- nativewhelks recognize risk from nativecrabs. Oecologia 169: 105 115. tions.Annual Review of EcologyEvolution and Systematics 86: 648 689.

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