Predation on 0-group and older year classes of the bivalve Macoma balthica: interaction of size selection and intertidal distribution of epibenthic predators
Introduction
Many intertidal benthic species in the Wadden Sea, a shallow coastal sea in The Netherlands, Germany and Denmark, use nurseries in the high intertidal Beukema, 1993a, Flach and Beukema, 1994. This holds, for example, for the lugworm Arenicola marina (Farke et al., 1979), the shore crab Carcinus maenas Klein Breteler, 1976, Beukema, 1991, the shrimp Crangon crangon (Kuipers and Dapper, 1984) and the bivalve Macoma balthica (Beukema, 1993a). It is assumed that in these nurseries juveniles of these benthic species are protected against predation by marine organisms such as shrimps, crabs and fish (Beukema, 1993a), that physical disturbance is less (Flach, 1992) and that growth is faster (Armonies and Hellwig-Armonies, 1992). We studied the relation between predation and nursery use of M. balthica.
M. balthica is a small bivalve found in coastal areas in temperate regions (Beukema and Meehan, 1985). In the Wadden Sea, juveniles of this species are mainly found on the high intertidal flats. Adults are more widespread and are found in both the low and high intertidal and the subtidal of the Wadden Sea and the adjacent North Sea (Beukema, 1993a). Since the locations where adults and juveniles live are partly spatially separated, M. balthica has to undertake migrations between these locations. Juvenile Macoma settles in May at a size of 300 μm in the low intertidal. Subsequently, these animals migrate to the high intertidal in June, where they stay until winter. In winter, juvenile Macoma migrates again, this time back to the low intertidal and the North Sea Beukema and De Vlas, 1989, Hiddink and Wolff, in press.
There are three groups of predators on M. balthica. Waders and ducks are numerous on tidal flats and exert a high predation pressure on the macrobenthos (Zwarts et al., 1992). Most birds can only forage on the tidal flats when the flats are emerged and therefore their predation pressure is higher on the high tidal flats (Sanchez-Salazar et al., 1987). Shorebirds generally select for relatively large prey. Oystercatchers and Knots for example do not eat Macoma smaller that 10 mm Hulscher, 1982, Zwarts and Blomert, 1992. Densities of shorebirds are usually in the range of 1–5 birds 10,000 m−2 (Van de Kam et al., 1999).
Another important group of predators on Macoma are epibenthic crustaceans and fish Van der Veer et al., 1998, Beukema et al., 1998. Being aquatic animals, most epibenthic species are only active when the tidal flats are submerged. Most abundant are the shrimp C. crangon, the crab C. maenas, gobies Pomatoschistus minutus and P. microps and juvenile flatfish Pleuronectes platessa, Platichthys flesus and Solea solea. In contrast to the bird predators, the epibenthic species probably select for the smallest individuals. Especially the shrimp C. crangon is known to eat large numbers of bivalve spat Keus, 1986, Van der Veer et al., 1998. C. maenas can cause large density reductions of Macoma in enclosure experiments (Fernandez et al., 1999) and Macoma is found is their stomach Scherer and Reise, 1981, Van der Veer et al., 1998, Richards et al., 1999. Stomach content studies showed that bivalves are no important part of the diet of gobies (Fonds, 1973) and no effect of Pomatoschistus enclosure on bivalve abundance has been found in enclosure experiments Berge and Hesthagen, 1981, Jaquet and Raffaelli, 1989, del Norte-Campus and Temming, 1994. We know only one study in which the effect of tidal level on mortality of Macoma-spat was examined; Reise (1978) exclosed epibenthic predators at four tidal levels tidal levels: the Corophium-zone, seagrass-beds, Arenicola-flats and low lying mud flats and found that mortality was only strongly reduced in the low intertidal. The set-up of that study, however, does not allow a conclusion on the effect of tidal level on predation on small bivalves. The third group of predators, which will be considered in a later paper, are infaunal polychaetes and gastropods.
This study tests the hypothesis the migrations of M. balthica are an adaptive strategy to avoid epibenthic predation on the juveniles and bird predation on the adults. This hypothesis was formulated by Beukema (1993a), based on descriptive studies in the western Wadden Sea. We looked at the effect of epibenthic and bird predation on density and growth of juvenile and adult M. balthica. Because high tidal flats are exposed for a long period, we expect a high predation pressure of birds on Macoma on the high flats. On the low tidal flats, we expect a high predation pressure by aquatic epibenthos, as these need water for activity.
This study tests the hypotheses that:
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predation pressure on juvenile Macoma is higher on the low than on high tidal flats due to predation by epibenthos, which select for relatively small prey;
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predation pressure on adult Macoma is higher on the high tidal flats due to predation by birds, which select for relatively large prey.
Together, these two groups of predators may force Macoma to live in the high intertidal as a juvenile and in the low intertidal as an adult.
Section snippets
Methods
This study was carried out between March and November in the years 1998, 1999 and 2000. What we call 0-group Macoma in this paper are the animals that settled between April and May and were 0–8 months old during the experiments. These animals measure 0.3–5 mm. 1+group Macoma are older animals and were at least 11 months old at the start of the earliest experiments in March.
These animals measure 6–20 mm and can reach an age of 4+ years in the study area.
Predator density and distribution
The fraction of predators caught by the pushnet, of those entering the net and caught or passing through the mesh, can be described as a function of predator length: P=1/(1+(exp (−A×L+B), where P is the proportion caught and L the predators size and A and B are constants (King, 1995). No shrimp smaller than 10 mm were caught, while no shrimps longer than 22 mm passed through the mesh (A=0.68, B=11, R2=0.89, p=0.000). No crabs smaller than 2 mm were caught, while no crabs wider than 6 mm passed
Stomach contents of epibenthic predators
The number of animals of which the stomach content was examined per month and the number of Macoma fragments per species is shown in Table 3. Fish are not presented in this table because the number of examined fish was low and no Macoma-remains were found in fish stomachs. In total, 38 fragments of Macoma shells were found in 338 examined stomachs. In 0-group Carcinus on average 0.20 Macoma was found. Both Crangon and adult Carcinus stomachs contained on average 0.10 Macoma per stomach.
Discussion
This study evaluates the effect of interaction between predation and tidal level on the abundance of M. balthica. The epibenthic predators C. crangon, adult C. maenas and juvenile flatfish were most abundant and largest on low tidal flats, as was already shown by Beukema (1993a). Only 0-group Carcinus was most abundant, but also smaller, on the high tidal flats. Crangon and 0-group Carcinus were the most abundant predators and their stomachs contained many Macoma remains. All epibenthic
Acknowledgements
All volunteers who helped with the fieldwork are thanked; without their help, it would have been impossible to do the exclosure experiments. Comments of two anonymous reviewers improved an earlier version of the manuscript. [RW]
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