Deeply hidden inside introduced biogenic structures – Pacific oyster reefs reduce detrimental barnacle overgrowth on native blue mussels
Graphical abstract
Introduction
Introduced non-native species can considerably affect native ecosystems and their communities by e.g. altering biodiversity, species interactions, energy flow and evolutionary adaptations (e.g. Vitousek et al., 1997, Grosholz, 2002, Katsanevakis et al., 2014). In the beginning of invasion biology research, direct detrimental impacts of alien organisms on resident species were the most commonly considered consequences of human induced translocation of species across natural barriers (Elton, 1958, Carlton, 1989, Mack et al., 2000, Crooks, 2002). However, influences of non-native species are often more complex and can also include a variety of facilitative effects (Thieltges et al., 2006). It is likely that these are as common as inhibiting effects and therefore, should also be taken appropriately into account when assessing the overall consequences of an alien organism after establishing in a native habitat (Rodriguez, 2006). Especially, non-native habitat-forming species such as epibenthic bivalves and macroalgae can provide additional structures used by native organisms (Crooks, 2002, Gribben et al., 2013). These ecosystem-engineering effects (sensu Jones et al., 1994) are of particular importance in coastal ecosystems where epibenthic biotic structures are generally rare such as in the European Wadden Sea (south-eastern North Sea), which is mainly dominated by unconsolidated sediments. For this region, Buschbaum et al. (2006) and Polte and Buschbaum (2008) showed, for instance, that beds of the introduced Japanese seaweed Sargassum muticum (Yendo) Fensholt harbour a much more diverse species assemblage than native macroalgae and provide a suitable habitat for endangered resident fish species. Generally, S. muticum is considered a very aggressive invader and a lot of detrimental impacts on native species are reported from many coastal systems, which could not be confirmed for the Wadden Sea (Staehr et al., 2000, Britton-Simmons, 2004, Harries et al., 2007, Lang and Buschbaum, 2010, Engelen et al., 2015, Davidson et al., 2015).
A further ecologically important, habitat forming, non-native species in the south-eastern North Sea is the Pacific oyster Crassostrea gigas (Thunberg) with its origin at the Japanese coast (Nehring, 2011). It has been introduced for aquaculture purposes in many countries and today, the oyster is almost worldwide distributed including the Wadden Sea (Ruesink et al., 2005, Diederich, 2005, Diederich, 2006, Cardoso et al., 2007, Padilla, 2010, Troost, 2010, Van der Zee et al., 2012). Here, first free-living Pacific oysters were detected on beds of blue mussels (Mytilus edulis L.) in the 1980s (Reise, 1998, Troost, 2010). Since the late 1990s, Pacific oysters naturally occur in the entire region outside the aquacultures (Wehrmann et al., 2000, Troost, 2010) and transformed most intertidal mussel beds into mixed aggregations of mussels and oysters (Diederich, 2006, Troost, 2010). This shift was accompanied by an increase in habitat heterogeneity due to newly constructed biogenic reef structures, formed by the large-sized oysters. However, the associated species communities of former pure mussel beds and oyster reefs are largely the same, including a high number of sessile organisms, which live directly attached to the shells of the bivalves (Kochmann et al., 2008, Markert et al., 2009).
One of the most conspicuous epibionts on mussels and oysters are balanids such as the acorn barnacle Semibalanus balanoides (L.). They may completely cover shells of M. edulis and hereby cause a reduction in mussel growth and presumably also other life history traits such as reproduction (Buschbaum and Saier, 2001). Kochmann et al. (2008) and Markert et al. (2009) showed that number and biomass of barnacle epigrowth per area are not very different between mussel beds and oyster reefs. Additionally, Retuschat (2009) found no conspicuous differences in barnacle percent coverage on individual mussel and oyster shells. However, these studies did neither investigate the small-scale distribution of barnacles within oyster reefs, although it has been reported that barnacle cyprid larvae may execute a distinct substrate choice (e.g. Crisp et al., 1985, Le Tourneux and Bourget, 1988, Thompsen et al., 1998, Buschbaum, 2001), nor the spatial occurrence of mussels and oysters within an oyster reef.
The latter was done by Eschweiler and Christensen (2011), who revealed that blue mussels actively migrate from the top to the bottom of an oyster reef in an attempt to escape from crab predation. The resulting mussel distribution is a recurrent pattern (Fig. 1), and we now ask how barnacles respond to this stratification of mussels within oyster reefs. If barnacles follow the same pattern, than the advantage for mussels to keep away from crabs could be foiled. If barnacles show a reversed pattern than the advantage of a predation refuge would be reinforced by diminished overgrowth for the mussels.
To quantify the density of mussels and their barnacle epibionts, we conducted field investigations in different height layers of an oyster reef. We hypothesized that due to the known defence strategy against predation, most M. edulis occur near the bottom where, as a positive side effect, mussels become less overgrown and are, therefore, better protected from detrimental impacts caused by barnacles. This was tested by performing field experiments on barnacle recruitment on mussels at two spatially distinct oyster reefs in the Wadden Sea.
Section snippets
Study area and experimental sites
Field surveys on mussel abundance and its barnacle epibionts were carried out in a mixed bed of native M. edulis and introduced C. gigas located on tidal flats in the north-east of the island of Sylt in the northern Wadden Sea (Germany, North Sea, 55°02′N, 008°26′E; Fig. 2). Since the introduction of C. gigas into the area for aquaculture purposes in the mid of the 1980s, all former naturally pure blue mussel beds have been overgrown by Pacific oysters and both mussels and oysters are now
Mussel density near the top and the bottom of an oyster reef
The field surveys revealed that density of mussels with a shell size of > 40 mm differed between the top and bottom layer of an oyster reef in the northern Wadden Sea (Fig. 3). Mean mussel density was 387 ± 60 ind. m− 2 at the top and significantly reduced in comparison to the bottom layer with a mean density of 875 ± 440 ind. m− 2 (Mann-Whitney U test, p < 0.001).
Extent of barnacle overgrowth on M. edulis
Dry weight of recently recruited S. balanoides was significantly higher on mussels near the top of the oyster reef (1.44 ± 0.51 g mussel− 1) than on M.
Discussion
Our field surveys in the northern Wadden Sea revealed that blue mussels Mytilus edulis and their barnacle epibionts are not equally distributed in mixed aggregations of native mussels and introduced oysters C. gigas. Mussel density was significantly higher near the bottom than near the top of the oyster reef whereas coverage and biomass of barnacle epibionts per mussel was much higher on mussels sampled from the top layer. This barnacle distribution pattern can be caused by an increased
Acknowledgements
We are grateful to Karsten Reise, Tobias Dolch and two anonymous reviewers for valuable comments on earlier versions of this manuscript. Romy Cartiere and David Thieltges assisted in the field. We also thank the Netherlands Organization for Scientific Research (NWO) and the German Bundesministerium für Bildung und Forschung (BMBF) for funding (NWO-ZKO project 839.11.002).
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