Ecology, 86(2), 2005, pp. 487–500 ᭧ 2005 by the Ecological Society of America

MARINE RESERVES ENHANCE ABUNDANCE BUT NOT COMPETITIVE IMPACTS OF A HARVESTED NONINDIGENOUS

JAMES E. BYERS1 Friday Harbor Laboratories, University of , 620 University Road, Friday Harbor, Washington 98250 USA

Abstract. Marine reserves are being increasingly used to protect exploited marine species. However, blanket protection of species within a reserve may shelter nonindigenous species that are normally affected by harvesting, intensifying their impacts on native species. I studied a system of marine reserves in the San Juan Islands, Washington, USA, to examine the extent to which marine reserves are invaded by nonindigenous species and the con- sequences of these invasions on native species. I surveyed three reserves and eight non- reserves to quantify the abundance of intertidal suspension-feeding species, three of which are regionally widespread nonindigenous species ( obscurata, Mya arenaria, and philippinarum). Neither total nonindigenous nor native species’ abundance was significantly greater on reserves. However, the most heavily harvested species, V. philippinarum, was significantly more abundant on reserves, with the three reserves ranking highest in Venerupis biomass of all 11 sites. In contrast, a similar, harvested native species (Protothaca staminea) did not differ between reserves and non-reserves. I followed these surveys with a year-long field experiment replicated at six sites (the three reserves and three of the surveyed non-reserve sites). The experiment examined the effects of high Venerupis densities on mortality, growth, and fecundity of the confamilial Protothaca, and whether differences in predator abundance mitigate density-dependent effects. Even at densities 50% higher than measured in the field survey, Venerupis had no direct effect on itself or Protothaca; only site, predator exposure, and their interaction had significant effects. Analyses incorporating environmental variables tracked at each site indicated that crab biomass most heavily influenced clam responses, causing lower growth of both species and higher mortality of Venerupis, whose annualized loss rate was 50% when exposed to predators. A laboratory prey choice experiment indicated that ,aninfluential intertidal crab predator, favored small adult Venerupis at least 1.7 times over Protothaca. Venerupis’ high susceptibility to excavating crab and human pred- ators, as well as its faster growth compared to Protothaca can be explained by its shallower burial depth. By growing quickly and residing near the surface, Venerupis apparently ab- sorbs the brunt of harvest pressure while Protothaca maintains high biomass even outside of reserves. Key words: apparent competition; ; exotic species; fisheries; marine protected areas; mixed effects models; ; Protothaca staminea; San Juan Islands, Washington (USA); spa- tially replicated experiments; Tapes japonica; .

INTRODUCTION vention of harvesting by humans affects nontarget spe- cies as well (Edgar and Barrett 1999). Effects on non- Marine reserves, or marine protected areas, have target species could be both direct, through reduction emerged as a prominent conservation tool to protect of mortality due to bycatch or destructive harvesting exploited marine species (Ballantine 1991, Lauck et al. techniques (e.g., bottom trawling), and indirect, 1998, Murray et al. 1999, Wilder et al. 1999). These through alterations of ecological interactions due to reserves are intended to provide a refuge that both pro- recovery of target (often predatory) species (Babcock tects a minimum number of individuals of a species, et al. 1999, Eisenhardt 2001). and also maximizes the potential that the species’ prop- One seldom explored, yet potentially important agules can disperse and replenish other unprotected change in nontarget species is the proliferation of non- areas. While marine reserves are often established with indigenous species and their subsequent impact on na- a principal goal of protecting or restoring one or a tive species within marine reserves. In combination handful of target fishery species, comprehensive pre- with habitat loss, interactions with nonindigenous spe- cies have been identified as the primary cause of en- Manuscript received 2 September 2003; revised and accepted dangerment of native species (Czech and Krausman 9 July 2004. Corresponding Editor: J. R. Bence. 1997, Wilcove et al. 1998), and the number of marine 1 Present address: Department of Zoology, University of New Hampshire, 46 College Road, Durham, New Hampshire invasions continues to increase each year (Carlton and 03824 USA. E-mail: [email protected] Geller 1993, Lodge 1993, Cohen and Carlton 1998). 487 488 JAMES E. BYERS Ecology, Vol. 86, No. 2

reserve may increase nonindigenous species and their subsequent impacts on natives.

Study system Since 1990 the University of Washington and the Washington Department of Fish and Wildlife have jointly overseen a small system of intertidal and shal- low subtidal marine reserves in the San Juan Islands of northern Puget Sound (Tuya et al. 2000). Within the reserves fishing and collections of marine organisms are prohibited, except for herring and salmon and ex- cept for scientific purposes as permitted by the director of the Friday Harbor Laboratories, University of Wash- PLATE 1. Four of the numerically dominant clams sur- veyed in this study. Clockwise from bottom: Nuttallia ob- ington. Also in the San Juan Islands, the National Park scurata, Mya arenaria, Venerupis philippinarum, and Pro- Service oversees British Camp Historical Site that in- tothaca staminea. Protothaca is the only clam of these that cludes an area (BCC) that has been closed to shell- is native to the study region. For scale, mesh size is 1.25 cm. fishing since ϳ1977. Photo credit: J. Byers. Three nonindigenous suspension-feeding clam spe- cies, Nuttallia obscurata, Mya arenaria, and Venerupis philippinarum, have become abundant and widespread While almost nothing is known about the extent of throughout large regions of the western coast of Canada nonindigenous species in marine reserves, in terrestrial and the United States, including the San Juan Islands systems nonindigenous species are readily and increas- (Carlton 1979, Haderlie and Abbott 1980, Kozloff ingly found within reserve boundaries (Brockie et al. 1996, Byers 2002; see Plate 1). All three prefer partly 1988, Loope et al. 1988, Macdonald and Frame 1988, sandy, low wave energy environments. Nuttallia ob- Usher 1988, Smallwood 1994, Lonsdale 1999). To date, scurata, the purple varnish clam, is native to northern the focus of marine reserves has emphasized their de- Asia ( and Korea) and was first recorded in the sign, placement, and enforcement (e.g., Francour et al. northeastern Pacific in 1991 (Forsyth 1993; C. E. Mills, 2001, Shanks et al. 2003). However, if marine reserves unpublished), most likely introduced via shipping bal- N. obscurata protect nonindigenous species that are normally af- last water (Coan et al. 2000). is commonly found buried 8–10 cm deep (and up to 20–25 cm deep) fected by harvesting, nonindigenous species could di- and usually inhabits sandy sediments in the high in- minish benefits to native species that would otherwise tertidal (Byers 2002). Mya arenaria, native to the At- accrue within reserves (Simberloff 2000). Particularly lantic coast of , was introduced acci- if nonindigenous species strongly affect natives, mere- dentally in imported seed in the late 1800s to ly setting aside protected areas may be an insufficient the Pacific coast of North America, and was subse- strategy to bolster populations of native marine species. quently spread intentionally for human consumption Rather, to safeguard native biota within reserves non- (Carlton 1979, 1992). Venerupis philippinarum (ϭPa- indigenous species may need to be controlled. phia philippinarum, ϭProtothaca philippinarum ϭVe- In this study I use a system of intertidal reserves in nerupis japonica, ϭVenerupis semidecussata, ϭRudi- northern Puget Sound, Washington, USA to address the tapes philippinarum, ϭTapes japonica, ϭTapes semi- issue of nonindigenous species in marine reserves. Spe- decussata), the Japanese littleneck clam, was acciden- cifically I focus on nonindigenous clam species and the tally introduced to the eastern Pacific in the 1930s with resultant impact of these species on native clams within imported seed from Japan and is now found from and outside of reserves throughout the archipelago. I to southern (Quayle 1941, first explore the pattern of invasion through field sur- Haderlie and Abbott 1980). It is the most prolific of veys to address whether the abundance and biomass of these introduced clam species in the San Juan Islands nonindigenous clam species varies as a function of re- and accounts for 50% of the annual commercial land- serve/non-reserve status. Second, through field and lab- ings of hard-shell clams in Washington (available on- oratory experiments I explore potential mechanisms of line).2 The species is also cultivated within intertidal impact of one of the heavily harvested nonindigenous beds at several facilities throughout the clams, Venerupis philippinarum. Specifically, I address state. (1) whether protecting clams or clam predators from Several native clam species inhabit this region and removal on reserves differentially benefits the nonin- most of the Pacific coast of North America and were digenous clam species, and (2) whether a reduction in common in my surveys. nasuta and M. in- predation intensifies competitive impacts of the non- indigenous clam on natives. In sum, this investigation 2 ͗http://wdfw.wa.gov/fish/shelfish/beachreg/1clam. informs whether blanket protection of species within a htm#manila͘ February 2005 NONINDIGENOUS SPECIES IN MARINE RESERVES 489 quinata are capable of both suspension and deposit general physical variables (e.g., chlorophyll, salinity, feeding and often associated with sheltered bays and a temperature) were similar. Based on the area of each variety of sediment types. Clinocardium nuttallii, Sax- site, I sampled 7–11 replicate cores (0.125-m2 metal idomis giganteus, capax, and T. nuttalli are larg- cylinders 18 cm deep) spaced at haphazard intervals at er, deeper dwelling bivalves associated with sand or 0.5 and 1.0 m above mean lower low water tidal ele- mud sediments. Finally, Protothaca staminea is a com- vation (MLLW; U.S. datum MLLW ϭ 0 m). This rep- mon, harvested clam that was particularly prominent lication was sufficient to characterize clam density at in this study (Appendix A). a site because after only 4–6 replicates, the mean den- The clams’ longevity (5–10 years) provides a de- sity and its variance had always leveled off to within mographic buffer to temporal fluctuations in abundance a few percent of their final values. All clams were and helps isolate the effect of reserves using even a sieved from cores through a 5-mm mesh, identified to single sample in time. Not only are these clams com- species, and measured for length (maximum from an- mon, tractable species, but bivalves in general can com- terior to posterior edge of shell) and height (from the pete strongly (Peterson 1982, Weinberg 1998, Talman umbo to the ventral margin). and Keough 2001). In particular, the nonindigenous I determined empirical relationships between shell Venerupis shares a number of life history and ecolog- measures (length and height) and dry masses of tissue ical attributes with the native confamilial species, Pro- and shell. The strongest relationships were used to es- tothaca staminea (Family: ), and thus may timate biomass (r2 values all Ͼ0.95) from at least 25 be especially likely to compete with it for resources. total individuals of each common species collected Both are suspension-feeding species that occupy sim- from several surveyed sites. I then used these rela- ilar sediment types and intertidal height. Importantly, tionships to calculate the biomass of the field-surveyed Venerupis is popular with human clammers, potentially clams. The biomass of rare species (Ͻ1% of clams indicating that its abundance and resultant impact on surveyed) was approximated using relationships de- native species may differ substantially inside and out- rived for morphologically similar common clam spe- side protected areas. Also, other clam predators [e.g., cies. (Cancer magister); red rock crabs I evaluated variation in average core biomass be- (Cancer productus); starry flounder (Platichthys stel- tween reserves and non-reserves for both native and latus); rock, sand, and English sole (Lepidopsetta bil- nonindigenous clams using t tests. Using biomass as a ineata, Psettichthys melanostictus, Parophrys vetulus); response variable more heavily weights older (and thus and pile perch (Rhacochilus vacca)], which may prey larger) individuals compared to density measurements. differentially on the clam species, likely vary in abun- Thus, biomass naturally integrates reserve effects over dance between protected and non-protected areas. I ex- longer time periods. Data were log-transformed [xЈϭ amine in detail whether reserve attributes (increased ln(x)orxЈϭln(x ϩ 1)] as needed to meet t test as- clam and clam predator abundance resulting from har- sumptions. For all t tests reported in this paper (biomass vest restrictions) affect the competitive influence of and other variables as well), equality of variances was nonindigenous Venerupis on the native Protothaca. tested using PROC TTEST (SAS Institute 1999). If variances between treatments were not equal, t tests METHODS with Welch-Satterthwaite approximations for unequal variance were used (Stewart-Oaten et al. 1992). If Field survey equal, then regular t tests on pooled variances were In June 2000, I surveyed 11 soft-sediment intertidal reported. sites (three reserves, eight non-reserves) that were se- Because of particularly high nonindigenous biomass lected on the basis of suitable sediment characteristics, at one reserve site, the effect of reserves on nonindig- limited wave exposure, and a minimum combined Pro- enous biomass was also analyzed with a nonparametric tothaca and Venerupis density of 16 individuals/m2 Mann-Whitney test. Additionally, I analyzed separately (Fig. 1). This latter biological criterion directly ensured the density and biomass of the native Protothaca and the selected reserve and non-reserve sites were suitable the nonindigenous Venerupis (both species are the most habitat for these focal species. The San Juan archipel- commonly harvested species in their category) as a ago is dominated by rocky shores, so I was able to function of reserve status. As further evidence of the initially spot check essentially all intertidal soft-sedi- degree to which nonindigenous clam patterns were ment areas. The formally surveyed sites represent all driven by Venerupis,Iperformed a t test on the com- that met the selection criteria. With the exception of bined biomass of the two nonindigenous clams besides harvest restrictions, reserve and non-reserve sites were Venerupis (i.e., Nuttallia and Mya)asafunction of otherwise similar. Measurements of environmental var- reserve status. Finally, to calculate whether reserves iables at many of the sites (see Methods: Quantifying differentially affected the demography of Venerupis site-level physical and biological covariates) confirmed and Protothaca,Iexamined with a t test the average that while harvest-influenced variables (e.g., crab abun- difference in the size (length) of the clam species be- dance) differed between reserves and non-reserves, tween reserve and non-reserve sites that had at least 490 JAMES E. BYERS Ecology, Vol. 86, No. 2

FIG.1. Map of survey and experimental sites in the San Juan Islands, Washington, USA. Non-reserve (solid circles) and reserve sites (solid squares) were used in both the survey and the field experiment. Two of the reserve sites (Argyle and Shaw) are under University of Washington jurisdiction; the third (British Camp Closed) is overseen by the National Park Service. Additional non-reserve sites used in the field survey are depicted as solid triangles. Abbreviations for the sites are: Arg, Argyle Creek; BCC, British Camp Closed; BCO, British Camp Open; Bell, Bell Point; ES, Eastsound; Guth, Guthrie Cove; MB, Mud Bay; Shaw, Shaw Island Preserve; SS, Spenser Spit; Squaw, Squaw Bay; Stuart, Stuart Island State Park.

10 clams of each species (three reserves and four non- quantify their effects on the mortality, growth, and fe- reserve sites). cundity of Protothaca.Iused the three intertidal re- serves (Argyle, BCC, Shaw) and three non-reserve con- Experimental investigation of nonindigenous trol sites (ES, Bell, Guth). The three non-reserve sites clam impacts were selected haphazardly from the original eight sur- Experimental setup.—Marine reserves may influ- veyed areas, with emphasis placed on sites where I ence the abundance and size of potential competitors, could best safeguard the experiment over its duration. particularly the often-harvested, nonindigenous Vene- The site at Bell provided the added benefit of being rupis philippinarum,aswell as clam predators. There- adjacent to a reserve site. I collected all clams used in fore, to simulate reserve and non-reserve attributes at this experiment from the same site (Bell) to reduce the each experimental site, I manipulated Venerupis den- effects of potential genetic variability on outcomes. sity and predator exposure in an orthogonal design to Both species have similar allometric relationships, so February 2005 NONINDIGENOUS SPECIES IN MARINE RESERVES 491

I selected small adult clams from a size range of 36– ulation expansions where they are unchecked by either 40 mm in length (Protothaca, 38.2 Ϯ 3.7 mm; Vene- human or aquatic predators. Venerupis density was rupis, 37.4 Ϯ 2.2 mm, mean Ϯ 1 SD). treated as a ‘‘pulse’’ manipulation (sensu Bender et al. In late July 2000 at the six sites I inserted hardware 1984) to test if predation reduces and thus mitigates cloth enclosures (0.3 ϫ 0.3 m ϭ 0.09 m2, 1.25-cm mesh density-dependent competitive effects. Enclosures size) 17 cm into the substrate so that they extended 1 were cleaned every 2 wk for 10.5 mo (312 d) to keep cm above the sediment surface in a single line along the mesh free of fouling organisms, and I scoured the a tidal height contour of ϳ0.8 m above MLLW. The surrounding area for dead clams from the experiment. depth of these enclosures extended well beyond typical No substantive effects of enclosures on clam responses maximum burial depths (ϳ8 cm) for these species were observed (Appendix B). (Haderlie and Abbott 1980), thus serving to prevent Quantifying growth, fecundity, and burial depth.— lateral migration of the clams out of the experimental I measured burial depths of each clam species at the plot (Peterson and Andre 1980). Enclosure bottoms end of the experiment. To complement these field mea- were composed of naturally occurring hard clay and surements, more precise burial depths were measured lined with a few centimeters of cobble to further pre- with a ruler on 150 individuals (42–60 mm length) of vent clams from burrowing deeper (and potentially out both Venerupis and Protothaca, held in the laboratory of) the enclosed area. Prior to initiating the experiment for 10 d in running seawater tanks lined with 15 cm I excavated and sieved the sediment within each en- of sediment, and compared with a t test. In the field, Ͼ closure to remove all clams 5 mm. The excavated clams were sieved from the enclosures, counted, mea- sediment was filled back into the enclosure to within sured, and frozen for later dissection. I measured the 5cmofthe surface, at which point 10 Protothaca and marked clams’ final shell dimensions and dissected a specified number of Venerupis were added. I mea- them to extract their somatic and gonadal tissue, which sured and marked all 10 Protothaca and 10 Venerupis I dried for 9 h at 75ЊCtoobtain a dry tissue mass (for nonzero Venerupis density treatments) before add- following the methods of Peterson (1982). ing them. I then added and lightly packed the remaining At the beginning of the experiments, I had estimated sediment into the enclosure until it was flush with the initial dry tissue mass and dry gonad mass of each surrounding ambient sediment. Clam predators (e.g., marked clam using empirically determined relation- fish, crabs, and birds) were excluded from half the en- ships between external shell measurements and dry tis- closures by completely covering them with hardware sue mass. These relationships were calculated by hap- cloth tops (1.25-cm mesh). hazardly selecting clams of both species over a range Three densities of Venerupis (0, 10, 20 individuals of sizes from the source collection (Bell), measuring per enclosure) were crossed with exposure to predators their external shell dimensions, removing the tissue (presence or absence of enclosure tops) for a total of from the shells, drying the tissue for 9 h at 75ЊC, and six treatments. These six treatments were replicated in weighing it. For Protothaca I regressed dry tissue mass three contiguous blocks within each of the six sites (18 2 ϭ 2 enclosures per site). Blocks were used solely to ensure against shell length (total tissue, R 0.93; gonad, R ϭ adequate interspersion of treatments. Enclosures were 0.87); for Venerupis I regressed dry tissue mass 2 ϭ 2 spaced 6–8 cm apart to enhance the homogeneity of against shell height (total tissue, R 0.82; gonad, R ϭ environmental conditions between them. To reduce po- 0.67). I calculated the change in total dry tissue mass tential biases from predators foraging in open-topped (somatic and gonad) and change in gonadal dry tissue Ϫ enclosures and spilling over onto an adjacent open- mass of each clam as: final dry tissue mass estimated topped enclosure, I systematically interspersed topped initial dry tissue mass. The change in gonad dry mass and topless treatments. Assignment of density treat- served as a proxy for a clam’s investment in repro- ments was randomized within each predator treatment duction. Although change in dry tissue mass is a highly within each block. sensitive measure of growth, I also examined changes The density of 10 Protothaca/0.09 m2 was chosen in other growth metrics (shell length, height, thickness, because, for the size of the clams used in the experi- wet tissue mass, relative dry tissue mass [(final mass ment, the biomass matched closely the average Pro- Ϫ initial mass)/initial], and total shell plus tissue dry tothaca biomass found in the field surveys in areas mass) to ensure that species-specific differences in where it predominated. Also, having a minimum of 10 growth form or allocation between shell and tissue did Protothaca per enclosure provided acceptable resolu- not lead to any discrepancies in results that could alter tion for quantifying its mortality response. The levels conclusions drawn from dry tissue growth rates (Ap- of Venerupis density were chosen to bracket (and aug- pendix C). ment by 50%) the range of its biomass quantified in Growth of gonad and somatic dry tissue were highly the field survey. Treatments containing no Venerupis correlated for each species (Protothaca, R ϭ 0.84; Ve- simulated the maximum effect of clam reductions that nerupis, R ϭ 0.96). These strong correlations are con- can occur in harvested, non-reserve areas. Higher den- sistent with the tight coupling of size and fecundity in sity treatments simulated the effect of potential pop- venerid clams in general (Ansell 1967, Yap 1977, Pe- 492 JAMES E. BYERS Ecology, Vol. 86, No. 2 terson 1986). Thus, statistical analyses of fecundity site, and their interaction (Appendix E). Consequently, produced similar results to those I present for growth. I analyzed the effect of density and predator exposure Quantifying mortality.—Mortality of clams was tal- on the mortality and growth of each clam species while lied periodically during the year when cracked shells incorporating the physical and biological covariates were found during enclosure maintenance and thor- measured at each site, using a mixed-effects linear oughly at the end of the experiment when enclosures model (SAS proc mixed, Kenward-Rogers degrees of were excavated. For experimental clams that were re- freedom method). The mixed-effects model is useful covered with my identification markings I could typ- to examine spatially replicated experiments by fitting ically discern the source of mortality, i.e., cracked a covariance structure to account for the correlation of shells ϭ crab predation; empty valves intact and black- data from a common cluster, i.e., site (SAS Institute ened ϭ anoxia, disease, or starvation (although star- 1999). Because experimental enclosures at each site vation is unlikely due to flexible physiology and de- experience the same environmental conditions, each velopment [Peterson 1982]). Clams that were unable replicate at a site should be treated as a repeated mea- to be recovered (mostly Venerupis from topless enclo- sure relative to the site-level covariates. Thus, a random sures) were assumed dead. Biologically this is the most intercept is fitted for each site, which causes obser- realistic assumption since the most likely explanation vations within a site, even after adjusting for fixed ef- for a missing clam is that it was excavated and carried fects, to be correlated (a variance components model). off by a predator. Since Ͻ1% of clams were missing I treat these effects as random because I am not inter- from topped enclosures, the surface was the only fea- ested in the specific effect of site, but rather treat site sible direction of escape, and clams that expose them- as being randomly selected from all possible sites with- selves by coming to the surface are highly vulnerable in the region. This process can thereby identify specific to predators (e.g., Smith et al. 1999, Seitz et al. 2001, attributes of a site (environmental variables) that might Byers 2002). Mortality proportions for each species underlie the significant effect of site on clam responses, within each enclosure were Anscombe transformed to while still allowing sites to differ due to other intrinsic normalize their distributions for statistical analyses variables. (Zar 1996). To explore differential effects of predator The fixed factors predator exposure and density com- exposure on the two species, I regressed Venerupis’ prised the baseline model, and I first added the inter- mortality against Protothaca’s mortality at each site action of the two main factors into the baseline model. for both topped and topless enclosures. If the interaction was not significant, I proceeded to Quantifying site-level physical and biological co- add each covariate (including interactions with main variates.—I quantified several environmental variables factors) one at a time into the baseline model. Because at each site throughout the experiment to use as site- there were far more covariance parameters than sites level covariates in analyses. These physical and bio- (i.e., degrees of freedom), I used a combination of for- logical properties associated with each experimental ward and backward stepwise selection processes (Coo- site may influence clam responses directly, or through per et al. 2002). I report all variables that were sig- interactions with the predator and density treatments. nificant when entered alone into the original baseline These properties were measured approximately every model, but I emphasize the largest model where all two weeks during daytime low tides and conducted at included covariates and covariate interactions were sig- all sites as concurrently as possible (typically within nificant. If no covariate or covariate interaction was 48 hours). For use in analyses, averages and standard significant, I retained the variable that resulted in the deviations (to reflect seasonal variability) were com- smaller P values of the fixed factors. puted for each covariate at each site for the entire sam- Finally, for a more detailed analysis of the effects pling period. I measured temperature and salinity using of crab predators, the most influential covariate, I com- a thermometer and handheld refractometer. Potential pared the average growth of each clam species as a bird predators (i.e., crows [Corvus caurinus], gulls [La- function of crab biomass density at each site. Specif- rus sp.], and oystercatchers [Haematopus bachmani]) ically, to examine how tactile cues or other sublethal were quantified at each site along a transect band cen- effects of crabs (e.g., nipping or withdrawal) tered over the enclosures. I also quantified additional might have influenced clam growth, for each clam spe- predator abundance (crabs), competitor biomass (ambient cies I regressed the difference in dry tissue growth in clams), and food availability (chlorophyll, sediment or- the topped and topless enclosures at each site against ganic matter) at each site. Details on collection methods crab biomass. of these variables are presented in Appendix D. Statistical analysis of field experiment.—As a pre- Prey choice/susceptibility experiments liminary step, mixed-effects ANOVAs were used to To examine in detail the extent to which differential analyze clam growth and mortality responses due to predation by a major intertidal clam predator, the red the effects of Venerupis density and predator exposure rock crab (Cancer productus), contributes to observed (fixed factors) and site (random factor). These analyses patterns of native and nonindigenous species biomass demonstrated evidence for effects of predator exposure, observed in the field, I conducted a prey choice ex- February 2005 NONINDIGENOUS SPECIES IN MARINE RESERVES 493

FIG.2. The biomass (mean Ϯ 1 SE)ofnative and nonindigenous clams by site in the field survey. Biomass is the combined dry shell and dry tissue mass. The three reserve sites are grouped together on the left. Abbreviations for sites are the same as in Fig. 1. Dagger symbols indicate survey sites used in the subsequent field experiment.

periment using Protothaca and Venerupis. During late I performed individual ␹2 tests on each replicate crab summer and fall 2000 I filled four indoor seawater tray to compare the preference of each crab for Venerupis tables (60 ϫ 50 cm) with 6 cm of natural sand, mud, and Protothaca.Todetermine whether crab preference and gravel substrate, which I sieved to remove ma- was homogeneous among replicates I conducted a het- croorganisms (e.g., worms and clams). Running sea- erogeneity ␹2 analysis of data for all 10 crabs. This test water was added to each tank and kept at a depth of revealed that replicates were homogeneous (hetero- 17 cm. Tanks were covered on the outside with black geneity ␹2 ϭ 4.22; df ϭ 9; P Ͼ 0.75) and could thus plastic and a wooden lid was placed over the top to be pooled to test the null hypothesis of no preference darken each tank. Large crabs were collected by divers by Cancer productus for either species of clam. Pooled and traps in the immediate vicinity of Friday Harbor frequencies for each prey species were compared with Laboratories and held in tanks without food for several a ␹2 goodness-of-fit test using Yates’ correction for ␹2 days before their use in choice trials. continuity (C ) (Zar 1996). To eliminate clam size as a confounding variable in prey selection, I used clams between 29 to 32 mm in RESULTS length. The burrowing depth of these small adult clams Field survey rarely exceeds 4 cm (personal observation); however Protothaca may have been slightly constrained by the Similar numbers of clam species were present at each sediment depth provided. If full burial of Protothaca surveyed site (7.4 Ϯ 1.75 species, mean Ϯ 1 SD). Non- was restricted, results of this experiment may conser- indigenous clam species were present at all sites, and vatively underestimate differences in prey selection by Venerupis specifically was found at all but one site crabs in natural settings. Four marked clams of each (Figs. 2 and 3). The reserve at Argyle was the most species were alternately placed ϳ6cmapart in a 4 ϫ heavily invaded site, where 75% of the clam species 2 array in the center of the tank, and pushed down (three out of four) were nonindigenous, representing several millimeters below the sediment surface. Clams 94% of clam biomass. Of the 11 sites, the three reserves were allowed to acclimate and burrow to desired depths had the first, third, and fifth highest biomass of non- for one hour before a single crab was added. Each crab indigenous species (Fig. 2). For Venerupis, the reserves usually spent several days acclimating to its enclosure ranked 1, 2, and 4 in highest Venerupis density and 1, during which time it did not forage. 2, and 3 in Venerupis biomass (Fig. 3). Enclosures were examined twice a day, roughly 12 Although the average density of nonindigenous bio- hours apart in the early morning and evening. When I mass was more than three times higher inside reserves discovered a clam was eaten (i.e., broken shell frag- than outside, this difference was not significant (Welch- ments noted on surface), I removed the crab, recovered Satterthwaite t test: t ϭϪ1.55, df ϭ 2.17, P ϭ 0.25; the broken shell, and replanted another clam of the Mann-Whitney U ϭ 21, P ϭ 0.066; Fig. 2). While there same species several millimeters deep in the center of may have been a substantial real difference in biomass the tank. After one hour the crab was reintroduced. density within and outside of reserves, high among site Each crab was used until it had eaten a minimum of variability led to low statistical power. The large dif- 12 clams. At the end of the trial series for each crab, ference in average biomass density was substantially the tank was drained and the sediment sieved carefully influenced by a high value at Argyle, but this was in- to verify that the proper number of clams remained. terpreted by the t test procedure as potentially due to Over the course of the experiment 10 crabs were active naturally high variability at the reserve sites, and was consumers. One crab died before it ate any clams. Three given less weight by the U test based on ranks. Native crabs had not eaten any clams after two weeks and species biomass did not vary significantly as a function were subsequently replaced. of reserve status (t ϭ 0.31, df ϭ 2.13, P ϭ 0.78). 494 JAMES E. BYERS Ecology, Vol. 86, No. 2

TABLE 1. Status of shells of experimental clams and the mortality source suggested by each.

Status of shells (mortality source) Missing Undamaged Cracked clams shells (e.g., shells (probably Species, predator anoxia or (definitively predator- exposure treatment starvation) crab-killed) killed) Protothaca, topped 96 0 1 Protothaca,notop 86 9 26 Venerupis, topped 96 5 7 Venerupis,notop 22 45 203 Notes: Each predator treatment for each species (i.e., each row) began with a total of 540 clams. Mortality from anoxia, disease, , or starvation is indicated by empty, intact, and often blackened valves. Designation of definitively crab- killed clams was based on recovery of crab-cracked shell pieces with my identification markings. See Methods: Ex- perimental investigation...for fuller explanation.

The native clam, Protothaca, did not differ signifi- cantly between reserves and non-reserves in either den- sity (t ϭϪ0.38, df ϭ 2.24, P ϭ 0.74) or biomass (t ϭ Ϫ0.04, df ϭ 2.26, P ϭ 0.97; Fig. 3). In contrast, non- indigenous Venerupis was significantly higher inside reserves in both density (t ϭϪ3.35, df ϭ 9, P ϭ 0.0085) and biomass (t ϭϪ3.43, df ϭ 9, P ϭ 0.0075; Fig. 3). (Argyle was not a statistical outlier in these

FIG.3. The (A) density and (B) biomass of Prothothaca analyses.) Finally, the biomass of nonindigenous spe- staminea (native) and Venerupis philippinarum (nonindige- cies excluding Venerupis (i.e., the biomass of Mya and nous) by site in the field survey. Because of their commercial Nuttallia) was high, but was highly variable (reserves, and recreational value, these two species were a primary focus CV ϭ 1.03; non-reserves, CV ϭ 0.69) and did not differ of this study. As in Fig. 2, biomass is the combined shell and significantly with reserve status (t ϭϪ0.79, df ϭ 2.19, dry tissue mass. Error bars indicate Ϯ1 SE. Abbreviations for sites are the same as in Fig. 1. P ϭ 0.51). Reserve status differentially affected the demograph- ics of each clam species. Venerupis was on average 9 mm smaller than Protothaca at non-reserve sites, but was only 1 mm smaller on reserves. This size differ- ential as a function of reserve status was significant (one-tailed t test, t ϭ 2.19, df ϭ 5, P ϭ 0.04).

Experimental investigation of nonindigenous clam impacts Mortality.—Predator exposure affected Protothaca and Venerupis differently (Fig. 4). Protecting Proto- thaca from predators with enclosure tops decreased its mortality rate by only a few percentage points (Fig. 4). However, Venerupis’ mortality dropped significantly, from 50% to 21%, from the exposed to the protected enclosures (Fig. 4). In topped enclosures very few clams were missing or cracked by crabs, and approx- imately the same number of Protothaca and Venerupis died from causes other than crab predation (e.g., an- FIG.4. Mortality rate of Protothaca and Venerupis in the oxia, disease, senescence) (Table 1). However, in top- main field experiment (spanning 312 days) as a function of less enclosures 92% of Venerupis mortality was attrib- exposure to predators. Enclosure tops prohibited access by macropredators. Data are averages, and error bars are 95% utable to crab and other macropredators, compared to confidence intervals computed with Anscombe transforma- only 29% for Protothaca (Table 1). When clams were tion and back-transformed. protected from predators, overall mortality rates at each February 2005 NONINDIGENOUS SPECIES IN MARINE RESERVES 495

creased relative to predator-protected clams (Prototha- ca, R2 ϭ 0.88, P ϭ 0.0055; Venerupis, R2 ϭ 0.63, P ϭ 0.059; Appendix H). For Protothaca, although no other covariate (or covariate interaction) was signifi- cant when predator exposure ϫ crab biomass was in- cluded in the model, many interactions of predator ex- posure with other covariates (except birds, temperature, and salinity) were significant in initial exploratory models (Appendix G). In alternate, exploratory models for Venerupis, only covariates relating to ambient clam biomass and crab metrics (and their interactions with predator exposure and density) were significant when

FIG.5. Mortality (mean Ϯ 1 SE) for both clam species in added to the baseline model (Appendix G). topless enclosures as function of crab biomass at the six ex- In the laboratory tanks Protothaca buried nearly 3 perimental sites. cm deeper than Venerupis on average (3.8 vs. 1.0 cm; t test, t ϭ 18.3, df ϭ 248, P Ͻ 1 ϫ 10Ϫ15). Although both clams overall buried more deeply in the field, site were uncorrelated between the clam species (R2 ϭ Protothaca in both laboratory and field was consis- 1.8 ϫ 10Ϫ6; P ϭ 0.998). However, when exposed to tently 2–4 cm deeper than Venerupis on average—a macropredators, mortality was highly and significantly finding further corroborated by other studies (Haderlie correlated (R2 ϭ 0.84; P ϭ 0.010; Appendix F). and Abbott 1980, Richardson 1985, Lee 1996, Sakurai Not only did Venerupis experience higher mortality et al. 1996). than Protothaca in enclosures exposed to predators, but this difference increased as crab biomass density in- Prey choice/susceptibility experiments creased (Fig. 5). Cancer productus was the most abun- In the laboratory, Cancer productus given same- dant crab throughout the sites, while C. gracilis was sized, small adult clams significantly chose Venerupis sampled in moderate abundance at two sites, and C. over Protothaca by a factor of 1.7. Not one of the 10 magister only rarely. For Venerupis,inthe final model crabs used in the trials selected Protothaca more than the interactions of predator exposure with crab biomass Venerupis, and four crabs chose Venerupis at rates of and with temperature both significantly affected mor- 2to1orgreater (Appendix I). The heterogeneity ␹2 tality (Table 2). For Protothaca, although crabs in par- analysis indicated that the data were consistent with a ticular were not implicated, predator exposure inter- homogeneity assumption (heterogeneity ␹2 ϭ 4.22, df acted with organic content to significantly influence mortality (Table 2). The recurrence of predator expo- sure as an interaction term in nearly all of the signif- TABLE 2. Effects of predator exposure, density, and site- icant covariates emphasizes its influential role in driv- level covariates on the mortality and dry-tissue growth of Protothaca staminea and Venerupis philippinarum in ing clam mortality (Appendix G). In contrast, Vene- mixed-model analyses. rupis density had almost no effect on either clam’s mortality (Table 2; Appendix G). Likewise, the covar- Source df FP iates salinity, temperature, and chlorophyll had no sig- Protothaca staminea nificant effect on mortality (Appendix G). Mortality (transformed) Growth, fecundity, and burial depth.—Dry tissue Predation 1, 98 6.23 0.014 and gonad growth rates of both species were highly Density 2, 98 0.89 0.42 Predation ϫ organic content 2, 9.56 3.97 0.056 site specific and Venerupis grew significantly more than Protothaca at all sites except one (Fig. 6; Appendix Dry tissue growth E). Faster growth by Venerupis was consistent across Predation 1, 98 5.59 0.020 Density 2, 98 0.93 0.40 all growth metrics (Appendix C). In the final models, Predation ϫ crab biomass 2, 9.56 5.50 0.026 Venerupis density had no effect on the growth of either Venerupis philippinarum clam (Table 2). Mortality (transformed) The growth of both species of clam was negatively Predation 1, 62 9.01 0.0040 affected by exposure to predators, particularly when Density 1, 62 0.32 0.58 Predation ϫ crab biomass 2, 6.94 29.10 0.0004 crab biomass was high. Specifically, tissue growth of Predation ϫ temperature 2, 6.94 10.75 0.0075 both clams was significantly affected by predator ex- Dry tissue growth posure ϫ crab biomass (Table 2). For Venerupis, the ϫ Predation 1, 59.2 4.25 0.044 interaction of predator exposure number of crabs Density 1, 59.3 0.16 0.69 also significantly affected growth (Table 2). As further Predation ϫ crab biomass 2, 6.9 88.6 Ͻ0.0001 evidence of the large effect of crabs, as crab biomass Predation ϫ crab numbers 2, 6.9 72.9 Ͻ0.0001 increased, the growth of predator-exposed clams de- Note: A random site effect was specified for the intercept. 496 JAMES E. BYERS Ecology, Vol. 86, No. 2

quantified by Yap (1977), the larger size of Venerupis on reserves translates into an approximate 75% in- crease in per capita fecundity. Coupled with the higher densities of Venerupis found on reserves, these areas may contribute disproportionately to the regional pro- duction of Venerupis’ broadcast larvae. Because Ve- nerupis is a heavily harvested species, its increase in abundance and size inside reserves is intuitive; how- ever, the fact that the only species consistently bene- fiting from protection was nonindigenous highlights a potential, unintended consequence of marine reserves. Venerupis’ shallow burial depth, and not its nonin- digenous status per se, best explains why it so heavily benefited from reserve status compared to Protothaca. Because Venerupis burrows several centimeters shal- lower than Protothaca,itcan be excavated more easily FIG.6.Dry tissue growth (mean Ϯ 1 SE)ofProtothaca by human predators (in addition to possibly being sim- and Venerupis over the course of the experiment (312 days) ply preferred [Chew 1987]). In all areas crabs also mit- at each experimental site calculated from enclosure averages. igate high Venerupis density, preying on them differ- Abbreviations for sites are the same as in Fig. 1. entially more than Protothaca, presumably because crabs excavate the shallowly burrowing Venerupis more easily. While Protothaca and Venerupis’ shells ϭ 9, P ϭ 0.89), thus pooling of the data across crabs exhibit similar resistance to cracking (unpublished was justified. Overall, Cancer productus demonstrated data), search and handling times of crabs are decreased a highly significant preference for Venerupis (pooled for a shallower clam (Smith et al. 1999, Seitz et al. ␹2 ϭ 8.20, df ϭ 1, P Ͻ 0.005). C 2001). In general, annualized crab predation rates DISCUSSION Ͼ50% are characteristic of Venerupis in its native and introduced regions (Yap 1977, Lee 1996). Marine reserves substantially augmented the density, Not surprisingly, Venerupis was most abundant on biomass, and size structure of Venerupis philippina- reserves where protected from humans, especially rum,aheavily harvested nonindigenous species. In when these areas were also low in crab biomass density, contrast, the two nonindigenous clams with little to no e.g., BCC, Argyle. While not a formal part of the anal- harvest pressure (Mya arenaria and Nuttallia obscur- yses, crab biomass was lower at reserve sites than the ata) (see footnote 2), although abundant, demonstrated experimental non-reserve sites (reserves, 2.00 Ϯ 0.61 no consistent pattern in abundance with reserve status. Ϯ Ϯ Native clams in general also exhibited no significant kg; non-reserves, 3.62 1.37 kg, mean 1 SD). This pattern between reserves and non-reserves, including trend could stem from the fact that the two most com- a harvested native species (Protothaca staminea) that mon crabs sampled (C. productus and C. gracilis) ex- is morphologically and ecologically similar to Vene- perience limited harvest pressure themselves and ben- rupis. The moderate to high densities of Protothaca in efit from removal of other more heavily harvested pred- most sampled areas underscore that these areas pro- ator and competitor species from non-reserve areas. In vided suitable habitat for the similar confamilial clam, particular, the Dungeness crab, Cancer magister, which Venerupis. Hence, the observed differences between does not generally forage for intertidal clams, is heavily reserve and non-reserve sites for Venerupis are most harvested in the region and is known for its highly likely not driven by natural habitat differences, but agonistic interactions (Fernandez et al. 1993). instead by factors related to reserve status, such as Although high densities of Venerupis may rarely oc- harvest pressure. While occasional poaching within re- cur naturally because of its vulnerability to predation, serves is possible, a strong reserve effect still emerged even relatively higher densities, such as in reserves and for Venerupis. in experimentally augmented treatments, did not di- In addition to density, reserves also differentially rectly affect the ecologically similar, confamilial clam, affected the average sizes of Protothaca and Venerupis, Protothaca. Even within predator exclosures that ex- emphasizing the disparate effect of reserve status and perienced no density mitigation by predators, Proto- subsequent harvest pressure on the two species. Both thaca showed little discernable response to high Ve- species exhibit similar allometries and have the same nerupis density. Although Venerupis densities in the legal harvest size (38 mm length). Despite Venerupis’ experiment bracketed and even enhanced ambient den- faster growth rate, it averaged 9 mm smaller than Pro- sities, these apparently still did not extend high enough tothaca at non-reserve sites, but differed negligibly on to result in substantial interspecific or intraspecific reserves. Based on the size–fecundity relationship competition. February 2005 NONINDIGENOUS SPECIES IN MARINE RESERVES 497

While deeper burial depths do increase Protothaca’s with burial depth (Zaklan and Ydenberg 1997), at least protection from human and crab predators, deeper partially explaining why the more deeply burrowing depths also expose clams to a more reducing, i.e., an- Protothaca does not grow as fast as Venerupis.With oxic, environment. In fact, Protothaca exhibited great- a shallower burial depth, Venerupis can filter food par- er mortality indicative of anoxia (i.e., undamaged, ticles more quickly (Zaklan and Ydenberg 1997) and blackened shells) than Venerupis. Sites where Proto- can invest less in the development of its siphon com- thaca experienced a higher incidence of such mortality pared to a deeper clam with a longer siphon. in the field experiment (Argyle, ES) also had lower Although Venerupis is productive and attains rela- natural densities of Protothaca in surveys. Venerupis tively higher biomass in reserves, its absolute biomass died from anoxia at a rate equal to Protothaca when in all areas is still typically much lower than Proto- crab predation was prevented by the topped enclosures. thaca. Thus, Venerupis’ high mortality–high growth When exposed to predators, crab predation on Vene- trade-off, stemming in part from shallow burial, is rupis increased, but its effect on overall mortality was seemingly not as conducive for maintaining large pop- partially offset by a decrease in mortality by anoxia, ulations as the low mortality–low growth trade-off suggesting these mortality sources for Venerupis were manifested by Protothaca. Venerupis’ trade-off helps compensatory (Table 1). explain why it is overwhelmingly favored over Pro- Although predators caused little mortality of Pro- tothaca by aquaculturists who can benefit from Vene- tothaca (Table 1), the interaction between predator ex- rupis’ high growth rate while artificially protecting it posure and organic content was marginally significant from predators with nets and other exclusion devices (Table 2). Protothaca’s overall mortality increased with (e.g., Spencer et al. 1992). In natural settings, Vene- decreasing organic content in the topless enclosures, rupis’ trade-off explains why areas with low natural but was nearly constant in topped enclosures (Appen- and anthropogenic sources of mortality (e.g., reserves) dix J). However, Protothaca mortality attributable sole- are prone to enhanced aggregations of larger, more fe- ly to non-predation deaths (undamaged shells) was not cund clams that consequently contribute dispropor- different between topped and untopped enclosures (Ta- tionately to Venerupis populations within the region. ble 1). So tops were not simply trapping organic matter Even when human harvest pressure and crab biomass and helping Protothaca avoid starvation where organic are both high, as they are on non-reserves, Protothaca content was naturally lower. Rather, the significance of biomass is still on par with reserves where both factors predator exposure ϫ organic content on Protothaca are low. The absence of a reserve effect on Protothaca mortality is likely due either to an increase in crabs’ implies that in non-reserve areas Venerupis may be dependence on clams as a prey source when the en- largely satiating the demand of human harvesters and vironment is oligotrophic, or more likely, clams ex- intertidally foraging crabs. Given the clam species’ hibiting riskier behavior when organic content is low similar shell strength and caloric value, Venerupis’ (such as slow withdrawal of siphons), that renders them shallower burial depth translates into a higher energy more susceptible to discovery by predators. The inter- gain per unit handling time for an excavating predator. action between predator exposure and organic content Thus, the more profitable and vulnerable Venerupis was enhanced by a negative correlation of crab biomass may play a sacrificial role that at least partially protects with organic content, such that crabs were also more Protothaca from predator mortality. With Venerupis abundant at sites where organic content was low. apparently taking the brunt of predator pressure, even While crab biomass did not directly influence Pro- at open harvest sites Protothaca’s abundance is no dif- tothaca’s mortality, it did decrease the growth rates of ferent than reserves. both clams (Table 2; Appendix H). At high crab sites, However, a larger, negative effect of Venerupis on clams in topped enclosures not only survived better, Protothaca, and especially other prey species eaten by but also grew better. Presumably, enclosure tops re- crabs, may occur at larger temporal and spatial scales. duced the amount of physical contact between clams In the field experiment Venerupis was seven times more and crabs that would cause siphons to withdraw and likely to be taken than Protothaca when exposed to reduce feeding time. A limited laboratory trial corrob- predators (Table 1). Even in conservative laboratory orated that in the absence of crabs, Protothaca and prey choice trials, Venerupis was favored 1.7 times Venerupis grew up to two times faster compared to over Protothaca.Bygrowing quickly and by serving clams that were exposed (nonlethally) to crabs (un- as an easy prey source for crabs, this nonindigenous published data). Studies of sublethal effects of pred- prey species may be boosting regional crab abundance ators on clams have generally confirmed that predator and productivity. Given how widespread Venerupis is presence significantly decreases clam growth (Irlandi throughout the west coast of North America, this crab and Peterson 1991, Nakaoka 2000). food subsidy could be substantial. In addition, the thin Regardless of crab abundance, Venerupis is a highly shelled, nonindigenous Nuttallia obscurata is also an productive clam with a tissue growth rate up to six easy, novel prey item for crabs when it occurs in areas times faster than that of Protothaca (Fig. 5). The en- without appropriate physical refuges (Byers 2002). Be- ergetic efficiency of feeding with a siphon decreases cause Cancer crabs are omnivorous predators, their in- 498 JAMES E. BYERS Ecology, Vol. 86, No. 2 crease (particularly non-harvested sizes, sexes, and Bender, E. A., T. J. Case, and M. E. Gilpin. 1984. Perturbation species [Cancer gracilis and C. productus]) potentially experiments in community ecology: theory and practice. Ecology 65:1–13. affects many other native species that serve as crab Brockie, R. E., L. L. Loope, M. B. Usher, and O. Hamann. prey, including other bivalves, worms, fish, and crus- 1988. Biological invasions of island nature reserves. Bi- taceans (Butler 1954, Gotshall 1977, Stevens et al. ological Conservation 44:9–36. 1982). Subsidies of native predators may in fact be a Butler, T. H. 1954. Food of the commercial crab in the Queen largely disregarded means by which nonindigenous Charlotte Islands region. Fisheries Research Board of Can- ada, Progress Reports of the Pacific Coast Stations, report species that are consumed heavily by native predators number 99:3–5. enhance apparent competition, and thus escalate the Byers, J. E. 2002. Physical habitat attribute mediates biotic impact of predators on native species (Courchamp et resistance to non-indigenous species invasion. Oecologia al. 2000, Byers 2002). Furthermore, if Venerupis boosts 130:146–156. populations of a mobile, omnivorous predator, pro- Carlton, J. T. 1979. History, biogeography, and ecology of the introduced marine and estuarine invertebrates of the tecting broadcast spawning clams like Venerupis from Pacific coast of North America. Dissertation. University of substantial harvest reductions within reserves may fuel California, Davis, California, USA. an impact that transports well beyond the boundaries Carlton, J. T. 1992. Introduced marine and estuarine mollusks of the reserves themselves (Lenihan et al. 2001). of North America: an end-of-the-20th-century perspective. 11 In summary, although marine reserves strongly en- Journal of Shellfish Research :489–505. Carlton, J. T., and J. B. Geller. 1993. Ecological roulette: the hance the nonindigenous clam, Venerupis philippina- global transport of nonindigenous marine organisms. Sci- rum, its increase did not affect native populations of ence 261:78–82. one of its most likely competitor species, Protothaca Chew, K. 1987. Littleneck clam aquaculture in the Pacific staminea. Negative impacts on Protothaca resulting Northwest. Pages 99–102 in Fourth Aquaculture Conference. Sitka, Alaska, USA. from the productivity and increase of Venerupis are Coan, E. V., P. V. Scott, and F. R. Bernard. 2000. Bivalve small and indirect, with crabs that track Venerupis seashells of western North America; Marine bivalve mol- abundance slightly affecting Protothaca’s growth and lusks from Arctic Alaska to Baja California. Santa Barbara size-dependent fecundity. A potential positive effect of Museum Natural History, Santa Barbara, California, USA. Venerupis may stem from it being more readily con- Cohen, A. N., and J. T. Carlton. 1998. Accelerating invasion rate in a highly invaded . Science 279:555–558. sumed (by both humans and crabs) and thus decreasing Cooper, A. B., J. C. Pinheiro, J. W. Unsworth, and R. Hilborn. predation on Protothaca. However, by serving as a 2002. Predicting hunter success rates from elk and hunter more accessible food resource, Venerupis may boost abundance, season structure, and habitat. Wildlife Society regional crab abundance and productivity, thereby in- Bulletin 30:1068–1077. Courchamp, F., M. Langlais, and G. Sugihara. 2000. Rabbits fluencing nearshore community structure and killing birds: modelling the hyperpredation process. Journal dynamics. Terrestrial reserve managers routinely apply of Ecology 69:154–164. control measures for nonindigenous species; the find- Czech, B., and P. R. Krausman. 1997. Distribution and cau- ings presented here suggest a similar proactive ap- sation of species endangerment in the United States. Sci- proach for marine reserves as well. ence 277:1116–1117. Edgar, G. J., and N. S. Barrett. 1999. Effects of the decla- ACKNOWLEDGMENTS ration of marine reserves on Tasmanian reef fishes, inver- tebrates and plants. Journal of Experimental Marine Bi- I thank D. Byers, T. Byers, and J. Meyer for help in the ology and Ecology 242:107–144. field. Taylor Shellfish and M. Billington at Westcott Oyster Eisenhardt, E. P. 2001. Effect of the San Juan Islands Marine Farms allowed access to their operations and clams. 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APPENDIX A A plate showing four of the numerically dominant clams surveyed in this study: Nuttallia obscurata, Mya arenaria, Venerupis philippinarum, and Protothaca staminea is available in ESA’s Electronic Data Archive: Ecological Archives E086-025-A1. 500 JAMES E. BYERS Ecology, Vol. 86, No. 2

APPENDIX B A description of the test for potential effects of enclosures on clam responses is available in ESA’s Electronic Data Archive: Ecological Archives E086-025-A2.

APPENDIX C A table of exploratory analysis of numerous growth metrics of Venerupis and Protothaca is available in ESA’s Electronic Data Archive: Ecological Archives E086-025-A3.

APPENDIX D Additional details on measurements of environmental covariates at each experimental site are available in ESA’s Electronic Data Archive: Ecological Archives E086-025-A4.

APPENDIX E A table showing two separate mixed-effects ANOVAs for each clam species to examine the effects of site, predator exposure, and density on mortality and day tissue growth is available in ESA’s Electronic Data Archive: Ecological Archives E086-025-A5.

APPENDIX F A figure showing the relationship of Protothaca mortality and Venerupis mortality at each experimental site for topped and untopped enclosures is available in ESA’s Electronic Data Archive: Ecological Archives E086-025-A6.

APPENDIX G A table of significant site-level covariates that were significant in exploratory analyses when added individually to the baseline mixed model examining mortality and dry tissue growth responses of each species is available in ESA’s Electronic Data Archive: Ecological Archives E086-025-A7.

APPENDIX H A figure showing the effect of crab biomass on the average growth at each site in topped minus untopped enclosures for Protothaca and Venerupis is available in ESA’s Electronic Data Archive: Ecological Archives E086-025-A8.

APPENDIX I A table showing the number of clams (Venerupis philippinarum and Protothaca staminea) eaten by each replicate adult red rock crab, Cancer productus,inprey choice trials is available in ESA’s Electronic Data Archive: Ecological Archives E086-025-A9.

APPENDIX J A figure showing mortality of Protothaca in topped and topless enclosures as a function of sediment organic content is available in ESA’s Electronic Data Archive: Ecological Archives E086-025-A10.