Matthias Strasser

Wadden Sea mussel beds invaded by oysters and slipper limpets: competition or climate control?

Introduced species are often considered to be a threat to residents, but not all reciprocal trends may reflect species interaction. In the northern German Wadden Sea, native mussel Mytilus edulis beds are declining and overgrown by introduced Pacific oysters Crassostrea gigas and slipper limpets Crepidula fornicata. We review the population development of the three species and analyse whether the invading species may be responsible for the decline of native mussels. The Pacific oyster predominately settles on mussel beds in the intertidal and the slipper limpet dominates around low water line. We compare the development of mussels and invaders in two subregions: mussel beds near the islands of Sylt and Amrum decreased both in the presence (Sylt) and absence (Amrum) of the two invading species and more detailed investigations could not confirm a causal relationship between the increasing invaders and decreasing mussel beds. There is evidence that the decline of mussel beds is mainly caused by failing spatfall possibly due to mild winters, whereas the increase in slipper limpets and oysters is facilitated by mild winters and warm summers, respectively. We conclude that changing species composition is a result of the climatic conditions in the last decade and that there is no evidence yet that the exotic species caused the decline of the natives. It remains an open question whether the species shift will continue and what the consequences for the native ecosystem will be.

Mya arenaria - an ancient invader of the North Sea coast

Mya arenaria currently occupies a wide geographical range in the northern hemisphere, on both coasts of the Atlantic as well as on the Pacific east coast. Some authors claim it also occurs on the Pacific west coast. The species originated in the Pacific during the Miocene and was already present on both Atlantic coasts in the Pliocene. However, it died out on the east coasts of the Pacific and the Atlantic during glaciation of the Pleistocene. With the aid of man it was reintroduced to the North Sea some 400–700 years ago and to the East Pacific last century. In the 1960s it was also introduced to the Black Sea.M. arenaria invaded new habitats by different modes: (1) natural range expansion (2) intentional as plantings, (3) unintentional as a ballast species and (4) unintentional as a byproduct of oyster transplants. Properties that may favor its wide range of distribution and invading success are: high fecundity; planktonic dispersal stages and life stages that lend itself to unintentional transport by humans; a broad spectrum of habitat and food preference; tolerance of a wide range of environmental conditions such as salinity and temperature; longevity, and perhaps relatively large size.

Larval supply of predator and prey: temporal mismatch between crabs and bivalves after a severe winter in the Wadden Sea

Enhanced bivalve recruitment after severe winters is a well-known phenomenon in the coastal North Sea. By comparing the bivalve larval abundances in the northern Wadden Sea after a severe (1995/96), a moderate (1996/97) and a mild (1997/98) winter we found no evidence for the hypothesis that high bivalve recruitment after severe winters is caused by enhanced larval supply. Total and peak abundances of all bivalve larvae as well as of each of four separate species Ensis americanus, Mytilus edulis, Cerastoderma edule and Mya arenaria were three to six times lower after the severe than after the mild winter. In Macoma balthica total and peak abundances after the severe winter were only slightly higher than after the moderate winter. The larvae of the epibenthic predator Carcinus maenas appeared in lower numbers and six to eight weeks later after the severe winter than after the moderate and the mild winter. Since the bivalve larvae appeared without, or with less, delay after the severe winter, there was a temporal mismatch between Carcinus and the bivalves, supporting the hypothesis that reduced epibenthic predation is an important factor in high bivalve recruitment after severe winters.

Mytilid mussels: global habitat engineers in coastal sediments

Dense beds of mussels of the family Mytilidae occur worldwide on soft-bottoms in cold and warm temperate coastal waters and have usually been considered hot spots of biodiversity. We examined intertidal mussel beds at four distant locations around the globe with the same sampling method, to find out whether this “hot spot” designation holds universally. We studied species assemblages within the matrices of byssally interconnected mussels engineered by Mytilus edulis in the North Sea, by mixed Perumytilus purpuratus and Mytilus chilensis at the southern Chilean coast, by Musculista senhousia in the Yellow Sea and by Xenostrobusinconstans at the coast of southern Australia. In all cases, species assemblages inside mussel beds were significantly different from those outside with many species being restricted to one habitat type. However, species richness and diversity were not generally higher in mussel beds than in ambient sediments without mussels. In the North Sea (M. edulis) and at the Chilean coast (P. purpuratus, M. chilensis), mussel beds have markedly higher species numbers and diversities than surrounding sediments, but this was not the case for mussel beds in Australia (X. inconstans) and the Yellow Sea (M. senhousia) where numbers of associated species were only slightly higher and somewhat lower than in adjacent sediments, respectively. In conclusion, although soft bottom mytilid mussels generally enhance habitat heterogeneity and species diversity at the ecosystem level, mussel beds themselves are not universal centres of biodiversity, but the effects on associated species are site specific.

How predictable is high bivalve recruitment in the Wadden Sea after a severe winter

Higher than average recruitment among bivalves on the intertidal flats of the Wadden Sea was observed many times after severe winters in the period 1940 - 1995. The occurrence of another severe winter in 1995/96 prompted us to test the hypothesis of severe winters leading to universally high bivalve recruitment on a large geographic scale (500 km coastline) in temperate shallow waters. We analysed data sets on bivalve abundance from seven areas in the Dutch, German and Danish Wadden Sea. The longer data sets showed generally higher bivalve recruitment in the 1970Žs and 1980Žs than in the 1990Žs which may be related to the near absence of severe winters since 1987. Considering the period 1988 onwards (the longest possible period in which 1995/96 was the only severe winter), recruitment of Cerastoderma edule was in 1996 - in agreement with our hypothesis - above average at all seven investigated areas. In contrast, recruitment of Macoma balthica and Mya arenaria was for the same period above average only in the southern Wadden Sea (south-west of Jade Bay) but not in the northern Wadden Sea (north of Eiderstedt peninsula). These regional differences may be related to (i) the different topography of the northern Wadden Sea (with barrier islands westwards to the mainland) compared to the southern Wadden Sea (with barrier islands northwards to the mainland) and subsequent differential effects of wind induced currents on bivalve recruitment, (ii) differences in biotic factors such as standing stocks, larval supply or epibenthic predation or (iii) changes in environmental conditions. Our results demonstrate that large-scale comparisons along coasts are an indispensable addition to insights derived from local studies alone.

Differential effects of the severe winter of 1995/96 on the intertidal bivalves Mytilus edulis, Cerastoderma edule and Mya arenaria in the northern Wadden Sea

Abstract. Intertidal mussel beds were severely damaged by scouring ice floes during the winter of 1995/96. Aerial surveys before and after the winter showed that more clusters of mussel beds vanished in a region with a higher areal share of tidal flats and a lower salinity, suggesting that the amount of ice present determined the magnitude of the disturbance on beds of Mytilus edulis. Nehls and Thiel [(1993) Neth J Sea Res 31:181–187] observed a strikingly similar spatial pattern of disturbances caused by severe storms in the Wadden Sea. Areas on mussel beds mechanically undisturbed by ice showed no reduced abundance and biomass of mussels, indicating that temperature alone was of little importance as a lethal factor. Conversely, Cerastoderma edule was strongly affected by low temperature. On average 80% died during the winter with extinctions up to 100% in the high tidal zone. At the lowest tidal level, surviving cockles were larger than those killed by the frost. A reinvestigation of sampled sites in autumn revealed that substantial further mortality had occurred during spring and summer which may constitute a time-lag effect of the preceding winter. There was no increased mortality in juvenile and adult Mya arenaria during the winter of 1995/96, confirming that this clam is a hard-winter species like Macoma balthica.

How bad are invaders in coastal waters? The case of the American slipper limpet Crepidula fornicata in western Europe

Introduced species are assumed to exert a variety of negative ecological effects in their new environments. However, rigid studies on such effects are still rare. Using a case study we exemplify pitfalls and obstacles for research on ecological effects of invaders and highlight the need for a concise framework. The suspension feeding gastropod Crepidula fornicata was accidentally introduced with American oysters to Europe and was soon after defamed as an ‘oyster pest’ although no evidence was provided in justification. Recently, small-scale experiments with C. fornicata and the Pacific oyster Crassostrea gigas failed to prove competition. As an epizootic, however, C. fornicata is impeding native mussels Mytilus edulis but at the same time provides protection against starfish predation. It also may serve as a sink for infectious trematode parasites and hence be beneficial for bivalve basibionts. Another positive effect of C. fornicata, especially at the coast of France where it is superabundant, may be that it causes a shift of phytoplankton blooms from toxic flagellates to diatoms. The multiple interactions with recipient coastal ecosystems result in a complex interplay of negative as well as positive effects of the invader on native biota. Positive effects of invaders might occur with the same frequency as negative ones, and the general prejudice that introduced species exert per se a negative effect may dictate the outcome of research. We argue that considering both, negative as well as positive effects of an introduced species is needed to eventually enable us to evaluate the overall effect of an invasion on recipient ecosystems. Besides pointing to the importance of positive effects, this case study also shows that research on effects of introduced species should (1) be species specific, (2) consider different spatial scales, (3) clarify which stage of an invasive process is under observation and (4) clearly distinguish between ecological effects, human-relevant impacts and the ethical judgment of both. A concise framework for research on ecological effects of introduced species – which still has to be developed – should incorporate these aspects.

Juvenile-adult distribution of the bivalve Mya arenaria on intertidal flats in the Wadden Sea: why are there so few year classes?

Abstract Patchy distribution is frequently observed in benthic marine invertebrates. In order to indentify factors causing spatial patterns in the bivalve Mya arenaria, abundances of juveniles and adults, as well as death assemblages, were recorded on a 20-km scale in the intertidal zone of the Sylt-Rømø Bight. Both adults and juveniles exhibited pronounced patchiness. Shell length of juveniles rarely exceeded 2 mm in 1995, which was most likely a consequence of epibenthic predators truncating the size spectrum. Only a few yearclasses dominated the adult population. While the northern part of the Bight was colonized mainly by a 1993-cohort, most M. arenaria in the southern part were from the mid-1980s. It is hypothesized that epibenthic predation is a major cause of the lack of dense M. arenaria beds from other years. However, examination of the length–frequency distribution of death assemblages revealed that other unidentified causes of mortality exist. High abundances of adults were found in the mid and lower intertidal zone but not in the high intertidal zone. There was no indication that dispersal of M. arenaria spat in a landward or seaward direction contributed significantly to the observed distribution pattern, since spat occurred abundantly at all tidal levels except in the high intertidal zone. There was no evidence of negative adult-juvenile interaction. M. arenaria was not attracted by seagrass or projecting shell beds – the latter indicating erosion of the sediment – as abundances of adults and juveniles were generally low in these habitats. The effects of sediment type and of the bioturbating lugworm Arenicola marina were inconsistent. While adults were more abundant on muddy sand than on sand, recruitment was independent of sediment type. At all high density sites of adults (>50 ind m–2), lugworm densities were below 5 ind m–2, which may indicate a negative interaction. However, lugworm densities >30 ind m–2 did not prevent relatively high M. arenaria recruitment of >500 ind m–2.

Differential recruitment of bivalve species in the northern Wadden Sea after the severe winter of 1995/96 and of subsequent milder winters

Abstract. High recruitment of the bivalves Cerastoderma edule, Mytilus edulis, Macoma balthica and Mya arenaria in summer after severe winters is an often reported phenomenon in the Wadden Sea. After the severe winter of 1995/96 however, only Cerastoderma and Mytilus followed this pattern in the Sylt-Rømø Bight. Repeated sampling of Cerastoderma, Macoma and Mya following a severe (1995/96), a moderate (1996/97), and a mild winter (1997/98) revealed that early recruitment was highest after the mild winter. In Cerastoderma the eventual high recruitment at the end of summer 1996 was caused by reduced benthic mortality. Low recruitment of Macoma and Mya after the severe winter may have been caused by a higher susceptibility to epibenthic predation and/or a higher susceptibility to passive re-suspension than in Cerastoderma and Mytilus. In all cases, post-settlement processes were decisive for reproductive success.