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Predation on intertidal mussels: Influence of biotic factors on the survival of epibenthic bivalve beds
Waser, A.M. (2018). Predation on intertidal mussels: Influence of biotic factors on the survival of epibenthic bivalve beds. PhD Thesis. NIOZ Royal Institute for Sea Research: Texel. ISBN 978-94-6332-327-7. 240 pp. https://hdl.handle.net/1871/55620

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Documenttype: Doctoraat/Thesis/Eindwerk

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Abstract
    Coastal areas are amongst the most productive ecosystems in the world. Important components of these coastal areas are reef-forming bivalves such as mussels and oysters, as they have important facilitating effects on many associated organisms through the provision of substratum, shelter or food. In the pristine Wadden Sea, intertidal beds of blue mussels (Mytilus edulis)and subtidal reefs of European flat oysters (Ostrea edulis) were common throughout the area and diversified the seascape. Extensive exploitation in the 19thcentury, however, led to thedisappearance of the flat oyster from the Wadden Sea. As a consequence, mussels gainedin importance as human food source, ultimately resulting in the introduction of commercialmussel cultures in the 1950s. Mussel beds were intensively harvested, and juvenile musselswere fished from intertidal beds for relaying to subtidal culture plots. In the early 1990s, severalsuccessive years with low recruitment and ongoing fisheries resulted in the loss of nearly allintertidal mussel beds in the Dutch Wadden Sea. Fishing restrictions subsequently allowedfor the recovery of the intertidal beds. However, recovery was lower than hoped and a newpotential threat emerged from the invasion of the Pacific oyster (Crassostrea gigas). Since theearly 2000s, the alien oyster settled to an increasing degree on mussel beds, which often resultedin transformations into oyster dominated reefs, raising conservation concerns over competitionwith the native mussels. In order to further promote the recovery of intertidal mussel beds,restoration measures were considered. Earlier experiences indicated the difficulty of the musselbed restoration, as most man-made beds disappeared shortly after they had been created.In order to increase the success of mussel bed restoration measures, detailed insights inthe various environmental and ecological processes affecting the survival of mussel beds wereneeded. The work presented in this thesis formed part of the ’Mosselwad’ project, which waslaunched in 2010 to increase knowledge on several factors that play important roles in thesurvival and the stability of mussel beds. This thesis aims to investigate crucial biotic factorsthat act upon the survival of intertidal mussel beds. In particular, this thesis is concerned withthe predation by shore crabs and mussel-feeding birds on the intertidal mussels and the impactof the recent introduction of the Pacific oyster into the Wadden Sea.As a measure of predation pressure on mussels as well as other macrobenthic organismsamong different Wadden Sea regions, waterbird distributions in relation to the extent of potentialforaging habitats were explored (Chapter 2). Specifically, numbers of 21 waterbird species for theperiod 1999–2013 were investigated in relation to the surface area of six different habitats amongthe tidal basins of the Dutch and German Wadden Sea. The habitat areas were characterizedby data on abiotic characteristics (tidal exposure and sediment structure) and on distributionsof epibenthic bivalve beds. Linear regressions were used to explore bird-habitat associations,where the regression coefficients reflect bird densities in the various habitats. Most species werepositively correlated with bivalve beds and intertidal areas with low tidal exposure (below 28%)and rather coarse sandy sediment (median grain size > 138.5μm). By inspecting the regressionresiduals, we identified higher bird abundances of all investigated feeding guilds in the westernDutch Wadden Sea and in the south of Schleswig-Holstein, while lower abundances were foundin the eastern Dutch Wadden Sea, in Lower Saxony and the north of Schleswig-Holstein. Theobserved regional differences in bird abundance may be related to the abundance of PeregrineFalcons, human disturbance and properties of the landscape. However, alternative explanationscannot be ruled out and further research is needed to identify the involved drivers.224SummaryChapter 3describes the fate of bivalve beds within the Dutch Wadden Sea for the period1999–2013. Bed survival is analysed in relation to several covariates such orbital speed,inundationtime, bed size, and bed type with respect to the bivalve composition (musseldominated, dominated by Pacific oysters, or mixtures of both bivalve species). In general,beds were found to have a high survival when large, lying shallow, and experiencing low orbitalspeed. The highest effect on bed survival, however, was due to composition of bivalve species.Mixed beds had a much lower hazard rate than pure oyster or mussel beds.InChapter 4, the impact of Pacific oysters on the condition of mussels and on the spatialdistribution of birds on 18 bivalve beds with different grades of oyster occurrence throughout theDutch Wadden Sea was explored. Moreover, in comparing bird densities on bivalve beds withdensities expected on the total intertidal area, species exhibiting a preference for the structuredhabitat could be detected. Overall, 50 different bird species were observed on the beds, of whichabout half regularly frequent intertidal flats. Most of these species showed a preference forbivalve beds. The condition of mussels decreased with oyster dominance, whereas the majorityof bird species was not affected by oyster occurrence. Four species were found to be negativelyaffected by oyster occurrence. Three of these species (Oystercatcher, Red Knot, and CommonGull) depend on intertidal mussels as food source, while the Dunlin primarily uses other foodsources.Estimating shore crab (Carcinus maenas) abundance on bivalve beds is challenging, sincemost methods common for quantifying animal abundance in marine habitats cannot be used.As abundance estimates are needed for the quantification of crab predation on mussels, thepotential of two methods to quantify crab abundance on 14 epibenthic bivalve beds across theDutch Wadden Sea was explored inChapter 5. The use of the number of crabs migrating fromsubtidal towards intertidal areas as a proxy of abundance on bivalve beds yielded unreliableresults. In contrast, crabs caught with traps on the beds were correlated with the abundanceassessed on the surrounding bare flats by beam trawl and therefore provided usable results. Theestimates, however, were only reliable for crabs exceeding 35 mm in carapace width (CW ). Theapplication of these estimates indicated that crab abundances on bivalve beds were influencedby the biogenic structure. Beds dominated by oysters attracted many large crabs (> 50 mm CW ),whereas abundances of medium-sized crabs (35–50 mm CW ) showed no relationship to theoyster occurrence.InChapter 6, the impact of Pacific oysters on the survival of different sized mussels, whilebeing exposed to shore crab predation, was experimentally explored. Mussel survival wasdocumented in laboratory short-term experiments. A split-plot design was followed, withdifferences in the three among-plot factors (acclimatization type: control and induced clumping;crab size: small (45–50 mm CW ) and big crabs (60–65 mm CW ); and oyster presence: presenceand absence of oysters) and within-plot differences in the survival of four different mussel sizeclasses (6, 12, 18, and 24 mm shell length). The presence of Pacific oysters reduced the mortalityof unconditioned mussels as well as mussels that were acclimatized in presence of predatorycues, while being exposed to predation by crabs of two different size classes. The reductionin mortality was size-dependent both in terms of the predators and the prey. The presence ofoysters notably reduced mussel mortality in presence of small crabs, while the mortality ratein presence of big crabs was less affected. Mussels that benefited the most by the presence ofoysters were those of recruitment stages, smaller than 20 mm in shell length.InChapter 7andChapter 8, the potential importance of parasitism in relation topredationon mussels is explored. These two chapters focus on parasite infections in brachyuran crabsin the Dutch Wadden Sea.Chapter 7describes an extensive field survey throughout theDutchWaddenSea for the rhizocephalan parasiteSacculina carciniinfecting shore crabs. Thedistributionof shore crabs infected with the rhizocephalan parasite was investigated at 12locationsand in 3 adjacent habitats (intertidal mussel beds, intertidal bare sand flats andsubtidalgullies) along a tidal elevation gradient. The sampling revealed that of the 27629225

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