Vol. 483: 221–229, 2013 MARINE ECOLOGY PROGRESS SERIES Published May 30 doi: 10.3354/meps10276 Mar Ecol Prog Ser Ability of invasive green crabs to handle prey in a recently colonized region Gesa Schaefer1,2, Martin Zimmer1,3,4,* 1Zoologisches Institut, Christian-Albrechts-Universität zu Kiel, 24118 Kiel, Germany 2Bamfield Marine Sciences Centre, 100 Pachena Road, Bamfield, British Columbia V0R 1B0, Canada 3FB3: Benthic Ecology, IFM-GEOMAR, Leibniz-Institut für Meereswissenschaften, 24105 Kiel, Germany 4Present address: FB Organismische Biologie, AG Ökologie, Biodiversität & Evolution der Tiere, Paris-Lodron- Universität Salzburg, 5020 Salzburg, Austria ABSTRACT: During the past few decades, the green crab Carcinus maenas, a native to Europe, has invaded the North American Pacific coast. In this new habitat, C. maenas encounters North American periwinkles of the genus Littorina that differ from European Littorina spp. in size, shape and shell strength. We hypothesize that the ability to handle prey never encountered previously is a prerequisite for successful invasion of novel habitats. In a first approach to testing our hypothe- sis, we compared European (native) to Canadian (invaded) C. maenas in feeding trials with Litto- rina spp. from Europe as well as Canada. Canadian crabs had significantly larger crusher claws than European crabs of the same size. Prey handling by Baltic crabs, but not by North Sea crabs, significantly depended on shell morphometry and strength of European periwinkles. By contrast, neither European nor Canadian crabs were affected by shell characteristics of the relatively soft- shelled Canadian periwinkles. Baltic and Canadian crabs did not differ in terms of handling time for, and handling success of, different periwinkle species, but North Sea crabs needed more time for, and were less successful in, crushing periwinkles. We conclude that C. maenas exhibits plas- ticity in both claw morphometry and feeding behaviour that enables this predator to handle novel prey organisms, and contributes to its success as an invader. KEY WORDS: Predator–prey interaction · Invasive species · Carcinus maenas · Littorina spp · Prey morphometry · Predator morphometry Resale or republication not permitted without written consent of the publisher INTRODUCTION Predation is an important evolutionary and ecolog- ical factor that affects the composition and structure For understanding invasion processes, it is essen- of communities, the demographic characteristics of tial to gain insight into the basic mechanisms of inva- populations, and the activity and life style of individ- sion success that underlie biotic interactions of uals (Lima & Dill 1990). Upon establishment of an invaders in their novel habitat (cf. Lockwood et al. invader in a novel habitat, some species will change 2007). To this end, being released from enemies that phenotypically more readily than others because of exert pressure on a species in its native range may differences in the strength and persistence of newly facilitate its establishment in a novel habitat (‘enemy developed interactions (Edgell & Rochette 2008). For release’: Elton 1958). On the other hand, every estab- instance, Smith & Palmer (1994) demonstrated plasti- lishing individual will have to face thus far unknown city in morphology and claw strength of predaceous competitors, and predators will have to acclimate to crabs: crabs eating mussels without shells grew novel prey with unknown characteristics and defense smaller and weaker claws than crabs eating intact mechanisms. mussels with shells. Similarly, crusher-claw size of *Corresponding author. Email: [email protected] © Inter-Research 2013 · www.int-res.com 222 Mar Ecol Prog Ser 483: 221–229, 2013 invasive crabs increased significantly (relative to their shells may pose an obstacle to their predators’ carapace width) for crabs raised on thick-shelled predation success. However, phenotypic plasticity in rather than thin-shelled diet (Baldridge & Smith feeding structures may allow invasive predators, 2008), and the treatment of snail prey by crabs, i.e. such as C. maenas (Baldridge & Smith 2008), to shell-breaking versus flesh-winkling, depended on adjust to variation in prey defenses. snail shell thickness (Edgell & Rochette 2009). Con- Periwinkles of the genus Littorina are commonly versely, mussels and snails can respond with plastic found in intertidal and subtidal habitats around the traits that confer resistance to predators, such as world (Reid 1996). Primarily grazing on microalgae increasing shell thickness in response to water-borne and macroalgae, periwinkles may influence algal cues from shell-crushing predators or damaged prey distribution in areas where they are abundant. Some (Dalziel & Boulding 2005). Differential predation species of Littorina (e.g. the Palearctic L. littorea and pressure and/or different pre-invasion histories of the Northern Pacific L. scutulata) have long-lived prey species (cf. Vermeij 1982) result in species- pelagic larvae and sites of distinct habitats are thus specific responses to neobiotic predators (Edgell & recruited from a common gene pool. This largely pre- Rochette 2008). Morphological plasticity of prey vents local adaptation, but minor adjustments to the organisms in response to predation pressure has conditions of their prospective habitats are possible recently become a focal issue in ecological studies on through individual phenotypic plasticity. Other spe- trophic interactions (for review, see Kishida et al. cies of the genus (e.g. the Palearctic L. fabalis and the 2010), but rarely has predator plasticity been taken Northern Pacific L. sitkana) develop directly without into account (cf. Edgell & Rochette 2009). larval dispersal, and among these there is evidence The European green crab Carcinus maenas, the for strong local adaptation forming distinct ecotypes most common crab species in the North Sea and the in contrasting habitats (Behrens Yamada et al. 1998, Baltic Sea, is a strong competitor and a dominant Johannesson 2003). Differences in shell shape or benthic predator. Its native range stretches from strength among contrasting habitats have often been Mauritania in north-western Africa through Atlantic explained as adaptive to predators or wave action Europe to northern Norway and Iceland (Behrens (Reid 1996, Edgell & Rochette 2008). Yamada & Gillespie 2008). Carcinus maenas success- On the other hand, crabs should preferentially prey fully invaded both the Atlantic coast and, more upon those species and individuals that provide the recently, the Pacific coast of North America (Cohen best benefit:cost ratio (cf. Enderlein et al. 2003). For et al. 1995, Breen & Metaxas 2003) and other coasts C. maenas in their northern native range, this seem throughout the world (cf. Behrens Yamada et al. to be medium-sized Littorina littorea and L. fabalis, 2010). Populations on North American Pacific coasts the most common periwinkle species in the Baltic probably derived secondarily from earlier multiple and North Sea, and Mytilus edulis, regardless of their invasions of the North American Atlantic coast dur- hard shell. On the invaded northern Pacific coasts, 4 ing the 19th century (Darling et al. 2008). Following periwinkle species are common, namely L. scutulata, the strong El Niño event of 1997-1998, coastal cur- L. sitkana, L. subrotundata and L. plena (Boulding & rents transported crab larvae from source popula- Harper 1998), in addition to a number of clams and tions in California northwards to the Pacific North- mussels (cf. Behrens Yamada & Boulding 1998). Inva- west coast of North America, where local recruitment sive green crabs compete for these potential prey ensured the establishment of stable populations items with at least 3 native Pacific crab species, (Behrens Yamada & Gillespie 2008). Only in some namely Cancer productus, Cancer magister and places along the North American Pacific coast where Hemigrapsus nudus (Rochette & Dill 2000, Keppel & the native Red rock crab Cancer productus acts as Scrosati 2004, but see Lewis et al. 2007). Adaptation predator on C. maenas could the invasive crab not and/or acclimation with respect to morphometry and become established (Hunt & Behrens Yamada 2003). behavior that renders an invasive predator able to Its success as a global invader is based on its toler- handle novel prey is a prerequisite to success in the ance to a wide range of temperature and salinity as invaded habitat. well as its ability to thrive on a diversity of prey Considering the recent success of Carcinus maenas organisms (Cohen et al. 1995, Behrens Yamada et al. in establishing stable populations along the North 2010). Hard-shelled prey organisms, such as mussels American Pacific coast (Behrens Yamada & Gillespie (e.g. Mytilus edulis) and snails (e.g. Littorina spp.) 2008), we hypothesized that (1) geographically dis- may strongly affect the crab’s invasion success in a tinct populations of C. maenas in native and invaded particular habitat, because shape and strength of habitats differ in claw morphometry in response to Schaefer & Zimmer: Plastic prey-handling by invasive crabs 223 conditions in the biotic environment, and (2) C. mae- take into account the crabs’ diurnal activity (Naylor nas is able to successfully handle previously un - 1960, Crothers 1968). Water temperature in the known prey. Hence, we predicted that Baltic and aquaria was maintained at about 12°C. North Sea green crabs would be no better at han- Carapace width and propodus height