Vol. 378: 47–54, 2009 MARINE ECOLOGY PROGRESS SERIES Published March 12 doi: 10.3354/meps07870 Mar Ecol Prog Ser

OPEN ACCESS Invasion resistance on rocky shores: direct and indirect effects of three native predators on an exotic and a native prey

J. S. Shinen1,*, S. G. Morgan2, A. L. Chan2

1Estación Costera de Investigaciones Marinas, Departamento de Ecología, Pontificia Universidad Católica de Chile, Alameda 340, Santiago, Chile 2Bodega Marine Laboratory, Department of Environmental Science and Policy, University of California Davis, PO Box 247, Bodega Bay, California 94923, USA

ABSTRACT: Trophic relationships among native and exotic species produce novel direct and indirect interactions that can have wide-ranging community level effects and perhaps confer invasion resis- tance. We investigated whether native predators have the potential to directly limit the spread of the exotic Mytilus galloprovincialis or mediate interactions among native and invasive at a rocky intertidal invasion front in northern California. Lower survival of M. galloprovincialis in transplanted cultures exposed to predators indicated that the invader was more vulnerable to preda- tors than the numerically dominant native M. californianus. Survival and per capita mortality rate in monocultures and polycultures did not vary for either M. galloprovincialis or M. californianus, sug- gesting that predator-mediated apparent competition and associational defense did not occur. Com- plementary laboratory feeding trials determined which among 3 intertidal predators preferred the exotic to 2 native species of mussel. The whelk ostrina was most selective, consuming the thinner shelled mussels (M. galloprovincialis and the native M. trossulus) rather than the thicker- shelled native species M. californianus. The crab Cancer antennarius and the sea star showed no preferences among mussel species. N. ostrina were commonly observed among field-transplanted mussels; thus whelk predation may be especially important in limiting the estab- lishment of the invasive mussel. However, 15% of M. galloprovincialis remained intact in the field after 1 yr, suggesting that predation alone may not inhibit establishment of the invader. A tenuous balance between larval settlement and early post-settlement predation likely characterizes the invasion front.

KEY WORDS: Invasion · Resistance · Predation · Indirect effects · Rocky intertidal · Mussel · Mytilus

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INTRODUCTION iting invasive species (Reusch 1998, Byers 2002, Ruesink 2007). Demographically, endemic predators Invasions of non-native species are a worldwide epi- can prevent the establishment of non-native species by demic, contributing to the biotic globalization of com- consuming the invader at a rate greater than or equal munities (Davis 2003). However, despite concerns over to its rate of arrival. If predators are incapable of limit- increased rates of introduction, as few as only 10% of ing establishment, they may still restrict the geo- exotic species become well established in endemic graphic extent of the spread of invaders (deRivera et communities (Williamson 1994). Much research on al. 2005). Predation can also act in concert with other invasive species has focused on the biotic resistance community level processes, such as immigration and mounted by native competitors and their emergent resource availability, to limit invasions through den- effects on species diversity (Levine 2000, Stachowicz et sity-mediated effects (Miller et al. 2002). al. 2002). More recently, investigators have targeted The indirect effects that native predators can have the important role that local predators can play in lim- on a community during an invasion by an exotic spe-

*Email: [email protected] © Inter-Research 2009 · www.int-res.com 48 Mar Ecol Prog Ser 378: 47–54, 2009

cies are not usually examined. For instance, local ferred by certain intertidal predators. In addition to predators can facilitate invasion of the non-native spe- invasion resistance, selective predation on a competi- cies via consumption of native competitors if they fail tively robust invasive like M. galloprovincialis can also to recognize a novel species as potential prey (Simon- lead to indirect effects that may promote coexistence cini & Miller 2007). Alternatively, invasive species can among native and invasive prey (Griswold & Lounibos release native species from natural enemies, if they are 2005). Moreover, the presence of the invader among preferred by native predators (reviewed by Rodriguez native congeners may change the native predator– 2006). If an invasive species is strongly preferred, then prey dynamics via apparent competition or associa- apparent competition may occur provided that preda- tional defense (Menge 1995) and may even cause tor density and predation rate on native prey increase declines in native species via hyperpredation (Smith & with the growing prevalence of the invader (Noonburg Quin 1996). & Byers 2005). Strong preferences for exotic prey also To evaluate the importance of predation in limiting may produce novel responses, such as associational the establishment of Mytilus galloprovincialis in a defenses that can occur when invasive prey are indi- rocky intertidal community within the invasion front, rectly facilitated by living near or among non- we experimentally determined both the direct impact preferred or unpalatable native species (reviewed by of multiple native predators on the invader and indi- Wahl & Hay 1995). rect effects on native competitors. The relative vulner- Predation may be contributing to post-settlement ability of native and invasive mussels to predators was mortality limiting the northward expansion of the Me- determined in a caging study the field, and the prey diterranean mussel Mytilus galloprovincialis along the preferences of 3 common intertidal predators were Pacific coast of the USA. An invasion front spanning determined in the laboratory. The differential survival approximately 560 km is located between Point Con- of native and invasive mussels outplanted in monocul- ception and Cape Mendocino, California, USA (San- ture in the field indicated their relative vulnerability to juan et al. 1997). This cryptic invader has become well predation. Differential survival among mussels out- established in protected bays and harbors, but has had planted in polyculture compared to monoculture limited success in becoming established in wave- would indicate the existence of predator-mediated exposed rocky intertidal communities along the open apparent competition (greater per capita mortality rate coast in this region (Geller 1999, Rawson et al. 1999). of M. californianus) or associational defense (lower per M. galloprovincialis co-occurs with 2 native congeners, capita mortality rate of M. galloprovincialis). The M. trossulus and M. californianus, within the invasion selectivity of different intertidal predators for native front. Larvae of all 3 species settle in open coast com- and invasive prey in the laboratory would suggest munities, but adult M. californianus are numerically which among 3 key predators play an important role in dominant while M. galloprovincialis and M. trossulus invasion resistance and the dynamics among native are rare (Johnson & Geller 2006). Physiological limita- and invasive mussels. Together, these results would tions and competitive interactions among native and reveal the effect of native predators on the invasion by invasive mussels are not likely to restrict further inva- M. galloprovincialis and indirect effects involving sion of M. galloprovincialis. Transplants of the invader native mussels within an invasion front on the Pacific experience high growth and survival rates in the Northwest coast. absence of predators and are competitively robust among 2 native species of mussels on the open coast (Shinen & Morgan 2009). Moreover, M. gallo- MATERIALS AND METHODS provincialis reduces growth and survival of M. trossu- lus (Shinen & Morgan 2009) and may be contributing Study site and species. All experiments were con- to the decline of M. trossulus in the southern extent of ducted at the Bodega Marine Reserve (BMR), approxi- its range (Geller 1999). mately 100 km north of San Francisco, California, USA Native predators may be limiting the invasion suc- (38° 18’ 18’’ N, 123° 3’ 8’’ W). The region is character- cess of Mytilus galloprovincialis via selective preda- ized by mixed semidiurnal tides and strong oceano- tion. Despite paradigmatic evidence of strong top- graphic upwelling. All 3 species of mussels occur in the down control in rocky intertidal communities (Robles & on the exposed rocky shores of BMR Desharnais 2002), the role of predators in limiting the (Rawson et al. 1999). invasion success of M. galloprovincialis in the Pacific All mussels used in this study were collected by hand Northwest has not been examined. The shell of the from naturally occurring mid-intertidal mussel beds in invader is generally thinner than that of the more April 2005. Small, newly settled ‘bay mussels,’ Mytilus abundant native M. californianus (Landenberger trossulus and M. galloprovincialis, can be difficult to 1968), making it potentially more vulnerable and pre- distinguish morphologically (Martel et al. 2000), and Shinen et al.: Invasion resistance on rocky shores 49

therefore, larger juvenile mussels that are readily dis- Predation rates on native and invasive mussels in tinguishable (length 2 to 4 cm) were used in all exper- the field. Predation rates on Mytilus californianus and iments. To be further assured of mussel species iden- M. galloprovincialis were determined by monitoring tity, M. trossulus were collected from Strawberry Hill, the survival of outplanted mussels on a rocky intertidal Oregon (44° 15’ 385’’ N, 124° 07’ 594’’ W), north of the bench. The native species M. trossulus was not in- zone of sympatry of the 3 species of mussels. M. gallo- cluded. This species is in decline and is uncommon provincialis were collected from Shell Beach in Toma- along the open coast in our study region. It is competi- les Bay, California (38° 06’ 59.75’’ N, 122° 52’ 23.93’’ W), tively inferior to M. californianus and M. galloprovin- where the population has historically comprised almost cialis and suffers high mortality in culture with het- entirely M. galloprovincialis (Sarver & Foltz 1993, erospecifics (Shinen & Morgan 2009). In May 2005, Suchanek et al. 1997). M. californianus were collected mussels were haphazardly assigned to 7 replicates of 3 from BMR. Each mussel was individually inspected for experimental treatment types: M. californianus mono- diagnostic morphological features to further reduce culture (n = 40), M. galloprovincialis monoculture (n = the inadvertent inclusion of non-target species or 40), and polyculture (n = 40; 20 M. californianus and hybrids (McDonald et al. 1991). Mussels that did not 20 M. galloprovincialis). Mussels were transplanted to resemble the target population were eliminated from a 5 × 10 m2 area of the middle intertidal zone at the the experiment. All mussels were transported to BMR, within the foraging range of all 3 target preda- Bodega Marine Laboratory and cleaned of epibionts. tors. They were held close to the rock surface for 4 wk The 3 species of mussels were acclimated separately using flexible plastic mesh (7 × 7 mm) to facilitate reat- in sand-filtered, flow-through seawater containers for tachment of byssal threads. In June, the mesh was 1mo. removed from half of the treatments to form spatially Three common intertidal predators with different paired caged (approximately 20 × 20 cm) and uncaged feeding modes were used in prey preference trials in cultures. Although the remaining mesh may have the laboratory. The ochre sea star Pisaster ochraceus is caused experimental artifacts that may affect mussel widely regarded to be a keystone predator in rocky survival such as changes in flow or sedimentation, the intertidal communities of the Pacific coast, where it experimental cultures were in an exposed, high flow preys heavily on the dominant space holders and frees area of the BMR, and we found no evidence of space for a greater diversity of invertebrates and algae increased sedimentation inside caged cultures. After (Paine 1974). P. ochraceus uses tube feet to remove 2 d, waves dislodged less than 5% of the mussels mussels from the substrate and pry open the shells of across all treatments, and thereafter missing mussels mussels. The stomach is then inserted to digest the soft were assumed to be removed by predation. Mussel tissue. survival was monitored periodically (approximately The second predator was the rock crab Cancer biweekly) in caged and uncaged cultures for 5 mo, and antennarius, which forages on invertebrate prey in a final observation was made after 1 yr. The presence submerged intertidal and shallow subtidal habitats. of predators and evidence of predation (drill holes, Mussels are eaten by breaking the shells of the bivalve broken shells, and empty shells) were noted at each prey with their claws. The effects of rock crab preda- low-tide sampling period. Predator abundance was not tion can be extremely variable in space and time, directly assessed since both Pisaster ochraceus and because they are highly mobile and often gregarious Cancer antennarius are likely to be more abundant (Yamada & Boulding 1996). Nevertheless, they can when the experimental plots were submerged. Fur- limit distributions of a wide variety of marine species thermore, often forage in the inter- (Byers 2002, Siddon & Witman 2004). stices of mussels and cannot be assessed without Lastly, the dog whelk Nucella ostrina is small, incon- destruction of the mussel bed. The abundance of spicuous, and abundant in the middle intertidal zone of predators within cultures was determined only at the rocky shores. Prey is consumed through a small hole end of the experiment when cultures were removed. created by a rasp-like . N. ostrina is a generalist Cumulative, proportional survival and per capita predator, but individuals can have highly specialized mortality rates were calculated for each species for the diets, preferring a narrow range of available prey first 5 mo. Predation was estimated by the difference in (West 1986). Direct and indirect effects of N. ostrina mortality observed in the paired predator-exclusion and other related Nucella spp. include changes to local control (caged) cultures and predator-exposed cultures species composition and diversity (Navarrete & Menge (see Menge et al. 2004 for general approach). Survival 1996), modification of the recovery rate of the commu- after 1 yr was estimated using only mussel counts in nity following a perturbation (Carroll & Highsmith uncaged plots, because the cage controls no longer ex- 1996), and alteration of predicted succession patterns cluded small Nucella ostrina after 1 yr of exposure. All (Wootton 2002). data were examined for deviations of statistical test as- 50 Mar Ecol Prog Ser 378: 47–54, 2009

sumptions using Levene’s test for variance homogene- mussel was eaten. Predators that did not eat or ate ity and visual inspection of the distribution of the resid- multiple prey before a primary choice was determined uals. The proportional survival of mussels after both were excluded from analyses. Frequency of predation 5 mo and 1 yr were compared using an analysis of vari- on each species of mussel was analyzed using Pear- ance (ANOVA) on arcsine square-root transformed son’s chi-squared test. data, with species and treatment type (monoculture versus polyculture) as factors. Species-specific per capita daily mortality rates in polycultures were aver- RESULTS aged over each sampling interval. The number of mus- sels missing from plots for each species of mussel was Predation rates on native and invasive mussels divided by the total number of mussels in the plot at the in the field previous time interval and the days between sampling intervals. To test for apparent competition or associa- After 5 mo of exposure to predators, overall survival tional defense between the 2 species in polyculture, of Mytilus galloprovincialis was less than for the native mortality rates were compared using an analysis of co- mussel M. californianus, indicating that the invasive variance (ANCOVA) with species as a factor and rela- mussel was more vulnerable to predators (Fig. 1). Nei- tive density of each species as a covariate (Schmidt & ther apparent competition nor associational defenses Whelan 1998). The abundance of N. ostrina was com- occurred, as indicated by the steady density-depen- pared among cultures using a single-factor ANOVA dent mortality rates of M. californianus and M. gallo- followed by Tukey’s HSD multiple comparison test. provincialis in polyculture (Table 1). After 1 yr, propor- Predator preferences for native and invasive mus- tional survival remained lower for M. galloprovincialis sels in the laboratory. Simultaneous feeding trials than M. californianus and was similar in monocultures were conducted to determine the preferences of and polycultures (Fig. 2). Predatory whelks Nucella predators for native and invasive mussels. In May of ostrina were observed within the experimental cul- 2006, Mytilus californianus, M. galloprovincialis, and tures at every sampling period and were often seen M. trossulus were collected and marked with a small positioned over mussels, presumably engaged in drop of nail polish on 1 valve to help distinguish spe- predatory efforts. Other predators were observed near cies during feeding trials. Average-sized adult preda- the experimental area, although none was noted tors, Pisaster ochraceus (11.5 ± 1.4 cm radial arm within the cultures during low tide. Similarly, only length, n = 35), Cancer antennarius (6.1 ± 1.7 cm claw shells that exhibited whelk drill holes were found. length, n = 35), and Nucella ostrina (1.9 ± 0.1 cm shell However, predation by non-whelk predators cannot be length, n = 20), were all hand-collected at BMR. The discounted, as any shells that may have been crushed predators were held in flow-through seawater at ambi- ent ocean temperature without food for 5 to 7 d to stan- dardize hunger level for each species. In each feeding 100 trial, a single predator was placed at 1 end of an aquar- ium (42 × 26 × 17 cm), and the 3 species of mussels were randomly and equidistantly arrayed at the oppo- 80 site end. Aquaria were constantly inundated and sup- plied with sand-filtered, flow-through seawater at ambient ocean temperature (9.4 to 14.8°C). Predators

Percent survival Percent 60 were observed 2 to 3 times daily for up to 3 wk until a Treatment p = 0.924 Species p = 0.007 T x S p = 0.518 Table 1. Mytilus galloprovincialis and M. californianus. AN- 40 COVA of mean daily per capita mortality rate in polycultures 0 20 40 60 80 100 120 140 160 over 5 mo of exposure to predators. Species-specific mortality Day rates were averaged over sampling intervals and were cor- Fig. 1. Mytilus californianus and M. galloprovincialis. Mean rected for mussel mortality in paired predator-exclusion plots. ± SE proportional survival of M. californianus (circles) and The relative density of the 2 species of mussels was included M. galloprovincialis (triangles) that were exposed to preda- as a covariate tors in experimental monocultures (shaded) and polycultures (unshaded) over 5 mo on the exposed rocky shores of the Source df SS F p Bodega Marine Reserve, California, USA. Data were adjusted for mortality observed in paired predator-exclusion plots. Species 1 <0.001 0.096 0.757 Results include a 2-way ANOVA of survival (arcsine square- Relative density 1 <0.001 0.051 0.821 root transformed) of mussel species (species) and culture type (treatment) Shinen et al.: Invasion resistance on rocky shores 51

70 12 P. ochraceus Treatment p = 0.500 10 60 Species p < 0.001 χ2 = 3.00 T x S p = 0.606 8 p = 0.22 50 n = 24 6

40 4

30 2 0 Percent survival Percent 20 16 14 C. antennarius 10 12 χ2 = 4.67 10 p = 0.10 0 n = 27 8 M. californianus M. galloprovincialis 6 Fig. 2. Mytilus californianus and M. galloprovincialis. Mean 4 ± SE survival in experimental monocultures (shaded) and

No. mussels eaten 2 polycultures (unshaded) that were exposed to predators after 1 yr on the exposed rocky shores of the Bodega Marine Re- 0 serve, California, USA. Results include a 2-way ANOVA of 14 survival (arcsine square-root transformed) of mussel species N. ostrina (species) and culture type (treatment) 12 10 χ2 = 14.00 p < 0.01 8 or pried open were likely dislodged and removed by n = 16 wave action. When the experiment was dismantled 6 after 1 yr, N. ostrina were found in similar proportions 4 in monocultures and polycultures of M. galloprovin- 2 (0) cialis and M. californianus (F2,14 = 1.69, p = 0.22). 0 Removal of the experiment also revealed hundreds of M. californianus M. trossulus M. galloprovincialis ‘bay’ mussel recruits, either M. galloprovincialis or M. Fig. 3. Frequency of predation by Pisaster ochraceus, Cancer trossulus, among the byssal threads of mussels. antennarius, and Nucella ostrina on native Mytilus californi- anus and M. trossulus and invasive M. galloprovincialis in the laboratory. Pearson’s chi-squared statistics and probability Predator preferences for native and invasive mussels values are shown in the laboratory each mussel species were also consistent throughout Of the 3 species of predators examined in the labora- the experiment, indicating that predator preference for tory, the whelk Nucella ostrina was most selective in the invader did not waiver even as mussel density laboratory feeding trials (Fig. 3). N. ostrina preferen- declined. Furthermore, the 2 species of mussels were tially consumed over the other 2 mus- not likely interacting indirectly via apparent competi- sel species (χ2 = 14.00, p < 0.01, n = 16). The crab Can- tion rather than through indirect facilitation or associa- cer antennarius and the sea star Pisaster ochraceus tional defense. The presence of novel prey could have showed a similar tendency to reject M. californianus, attracted predators and may have led to switching but did not demonstrate significant preferences among among prey, but per capita mortality rates of the mus- the 3 species of mussels (χ2 = 4.67, p = 0.10, n = 27 and sels did not decline with the decreasing proportions of χ2 = 3.00, p = 0.22, n = 24, respectively). the 2 species of mussels. Nucella ostrina may be a key species limiting the es- tablishment of Mytilus galloprovincialis. This mid-inter- DISCUSSION tidal predator always occurred within our plots, where it preferred M. galloprovincialis to M. californianus and The combined evidence from laboratory and field was often seen feeding on the invader. The preference experiments suggests that predation may be contribut- for M. galloprovincialis is likely due to its thinner shell ing to the limited establishment of Mytilus galloprovin- (Landenberger 1968), which would require less handling cialis. In the field cultures exposed to predators, sur- time for a drilling predator (Hart & Palmer 1987). The vival rates on the invader were consistently lower than whelk also preferred M. galloprovincialis to M. californi- those of M. californianus. Per capita mortality rates of anus in the laboratory, but it preferred M. trossulus to 52 Mar Ecol Prog Ser 378: 47–54, 2009

both of them. Like M. galloprovincialis, M. trossulus has ability of native predators to limit the distribution of a thin shell (Suchanek 1981), which explains why it was Mytilus galloprovincialis. Many predators, such as preferred to M. californianus. However, it cannot be Pisaster ochraceus and Cancer antennarius, produce ruled out that M. trossulus provides the greatest nutri- planktonic larvae that potentially disperse hundreds of tional reward among the mussel species. kilometers, connecting populations throughout a spe- Strong prey preferences of Nucella ostrina may also cies range (Kinlan & Gaines 2003). Wide diet breadth influence competitive hierarchies among native and may be favored for predators with long larval dispersal invasive mussels (Carroll & Highsmith 1996, Navarrete due to the range of available prey at potential settle- & Menge 1996) and may affect the decline of Mytilus ment sites (Beck & Kitching 2007). C. antennarius and trossulus and the invasion by M. galloprovincialis. P. ochraceus did not strongly prefer 1 species of mussel M. galloprovincialis is competitively dominant over over another, especially between the thin-shelled M. trossulus and is the fastest growing of the 3 species M. galloprovincialis and M. trossulus. In contrast, of mussels within the invasion front (Shinen & Morgan highly selective Nucella ostrina develop directly into 2009). Because whelks prefer M. trossulus to M. gallo- competent juveniles inside sessile eggs. Although the provincialis, predation by N. ostrina might have exac- N. ostrina used in our study were all collected from a erbated the negative competitive effects of M. gallo- single site, our results were consistent with prey pref- provincialis on native mussels and contributed to the erences of N. ostrina throughout the invasion front decline of the native species. Additionally, whelks (Danner 1999, J. Shinen et al. unpubl. data). The abil- strongly prefer M. galloprovincialis to M. californi- ity of N. ostrina to limit the distribution of M. gallo- anus; thus predation on settlers likely promotes coexis- provincialis may also be reflected by the inverse rela- tence between the 2 species of mussels by slowing the tionship between the predator and the prey along the advance of the invader. However, the direct and indi- invasion front. The invasive mussel is abundant only in rect effects of whelk predation on competition among protected bays and harbors (Braby & Somero 2006), the 3 mussels may vary over the range of the M. gallo- where N. ostrina usually does not occur. Thus, on a provincialis invasion, because both prey preferences regional scale crabs and seastars may be less likely to and predation rates of Nucella spp. can vary with prey limit the establishment or spread of M. galloprovin- availability (Wieters & Navarrete 1998) and across geo- cialis than N. ostrina and may be more likely to pro- graphic regions (Dahlhoff et al. 2001, Hunt & Scheib- mote coexistence among mussels (Shurin & Allen ling 2001, Sanford et al. 2003). 2001). Crabs and seastars may play a lesser role in limiting Despite evidence from our field and laboratory stud- the spread of Mytilus galloprovincialis than whelks. ies demonstrating that N. ostrina may be limiting the During low tide, we saw little conclusive evidence of invasion of Mytilus galloprovincialis in northern Cali- predation (cracked, broken, or empty shells) by these fornia, approximately 15% of the original M. gallo- predators in our experimental plots, but crabs and provincialis remained in the experimental plots after seastars generally forage in mussel beds during high 1 yr (monocultures and polycultures combined). Al- tide, making them very difficult to observe. As a crush- though selective predation on M. galloprovincialis ing predator, Cancer antennarius tended to avoid the occurred, predators could not remove all of the estab- thicker-shelled M. californianus in the laboratory, but lished mussels in our plots. Furthermore, patches of significant preferences were not evident. Least selec- M. galloprovincialis facilitated recruitment of ‘bay’ tive, Pisaster ochraceus is a prying predator, needing mussels, which previously have been shown to consist only a 0.5 mm gap between mussel valves to insert its of far more M. galloprovincialis than M. trossulus stomach and consume prey (Feder 1955). The lack of within the invasion front (Braby & Somero 2006). The strong feeding preferences of C. antennarius and recruitment rates of M. galloprovincialis will likely P. ochraceus suggests that any varying shell thickness increase, in part due to growing mariculture develop- or strength of the adductor muscles among experi- ment in bays that likely serve as larval sources for open mental mussels was not sufficient to deter predation. coast communities (FAO 2007). Although rapid preda- Nevertheless, C. antennarius and P. ochraceus have tory responses to stochastic high recruitment events the potential to help limit the expansion of M. gallo- have been documented for all 3 species of predators provincialis. Previous studies have shown that these (Robles et al. 1995, Hunt & Scheibling 2001, Bomkamp mobile predators can limit the distribution of prey et al. 2004), a large settlement event of M. gallopro- throughout the intertidal zone during high tide (Paine vincialis could swamp any biotic resistance (Hollebone 1974, Robles 1987) and can quickly converge on abun- & Hay 2007). For instance, along the west coast of dant prey (Bomkamp et al. 2004). South Africa where recruitment rates of M. gallo- In addition to feeding mode, differences in biogeo- provincialis are extremely high, the invader has been graphy and life history may play critical roles in the an important trophic subsidy for many native preda- Shinen et al.: Invasion resistance on rocky shores 53

tors, but their combined effect has not limited the Acknowledgements. We thank M. A. Holyoak and J. J. Sta- establishment and spread of M. galloprovincialis chowicz for commenting on the experimental design and an (Griffiths et al. 1992). early draft of the manuscript. We also thank B. G. Miner, J. Fisher, S. H. Miller, I. R. McCaslin, and E. J. Kolbeck for their Rocky shore predators create bare space on rocky assistance. This work was supported by the National Science shores that can be colonized by both native and intro- Foundation (OCE-0521023, OCE-0325028, OCE-0326110). duced species. For the time being, predation appears to be contributing to the limitation of a northward LITERATURE CITED expansion of Mytilus galloprovincialis on the exposed rocky coasts of northern California, but predicting its Beck J, Kitching IJ (2007) Correlates of range size and dis- long-term effectiveness at slowing the invasion of persal ability: a comparative analysis of sphingid moths M. galloprovincialis is complicated. N. ostrina, a key from the Indo-Australian tropics. Glob Ecol Biogeogr 16: 341–349 predator of M. galloprovincialis, is an intermediate Bomkamp RE, Page HM, Dugan JE (2004) Role of food subsi- predator in a complex interaction web that is subject to dies and habitat structure in influencing benthic commu- other biological and physical forces (Navarrete & nities of shell mounds at sites of existing and former off- Menge 1996, Dahlhoff et al. 2001). A recruitment fail- shore oil platforms. Mar Biol 146:201–211 Braby CE, Somero GN (2006) Ecological gradients and rela- ure or substantial post-settlement mortality event of tive abundance of native (Mytilus trossulus) and invasive 1 or several key predators within the invasion front (Mytilus galloprovincialis) blue mussels in the California may result in a substantial increase in cover of M. gal- hybrid zone. Mar Biol 148:1249–1262 loprovincialis. Additionally, further invasion success Byers JE (2002) Physical habitat attribute mediates biotic will likely have wide-ranging effects on intertidal com- resistance to non-indigenous species invasion. Oecologia 130:146–156 munity structure. Since M. galloprovincialis is compet- Carroll ML, Highsmith RC (1996) Role of catastrophic distur- itively robust among native mussels (Shinen & Morgan bance in mediating Nucella –Mytilus interactions in the 2009), the mussel bed community structure will Alaskan rocky intertidal. Mar Ecol Prog Ser 138:125–133 change if native mussels decline. 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Editorial responsibility: Richard Osman, Submitted: June 16, 2008; Accepted: November 26, 2008 Edgewater, Maryland, USA Proofs received from author(s): February 19, 2009