J. J. Beukema

Expected changes in the wadden sea benthos in a warmer world: Lessons from periods with mild winters

Changes observed in the macrozoobenthos at tidal flats in the westernmost part of the Wadden Sea during the 1969–1991 period were used to evaluate effects of mild winters. At least one third of the macrobenthic species in this area is sensitive to low winter temperatures. This has resulted in higher species richness and higher abundance of these species following mild as opposed to normal or cold winters. Negative effects of mild winters include greater weight loss in all bivalves during the winter and low reproductive success in the subsequent summer for various important (bivalve) species. A recent series of three mild winters in close succession (1988–1990, including the two mildest of the century) had profound effects: repeated recruitment failure in the bivalves Mya arenaria and the heavily fished Mytilus edulis and Cerastoderma edule resulted in low standing stocks of these species in the course of 1990. Effects were noted on algal stocks (elevation), other bivalves (higher weights) and predators (food shortage); problems arose particularly in the mussel and cockle fisheries as well as among the eiders (Somateria mollissima).

Impacts of Nutrient Reduction on Coastal Communities

Eutrophication due to high anthropogenic nutrient loading has greatly impacted ecological processes in marine coastal waters and, therefore, much effort has been put into reducing nitrogen and phosphorus discharges into European and North-American waters. Nutrient enrichment usually resulted in increase of biomass and production of phytoplankton and microphytobenthos, often coinciding with shifts in species composition within the primary producer community. Consequences of increasing eutrophication for higher trophic levels are still being disputed, and even less is known about the consequences of nutrient reduction on coastal food webs. Here, we present 30-year concurrent field observations on phytoplankton, macrozoobenthos and estuarine birds in the Dutch Wadden Sea, which has been subject to decades of nutrient enrichment and subsequent nutrient reduction. We demonstrate that long-term variations in limiting nutrients (phosphate and silicon) were weakly correlated with biomass and more strongly with community structures of phytoplankton, macrozoobenthos and estuarine birds. Although we cannot conclusively determine if, and if so to what extent, nutrient enrichment and subsequent nutrient reduction actually contributed to the concurrent trends in these communities, it appears likely that part of the variance in the studied coastal communities is related to changes in nutrient loads. Our results imply that nutrient reduction measures should not ignore the potential consequences for policies aimed at bird conservation and exploitation of marine living resources.

Biomass and species richness of the macrobenthic animals living on a tidal flat area in the Dutch Wadden Sea: Effects of a severe winter

Abstract The winter of 1979 was relatively severe in the Wadden Sea area. About 90% of the winters during the last century were milder. The mean temperature during the first 3 months of 1979 was 3°C below the long-term average. The effects of the low temperatures on the macro-zoobenthos living on the tidal flats in the western part of the Wadden Sea were studied by comparing abundance and biomass estimates found in spring 1979 and survival rates during the 1979 winter with comparable values observed at the same places during the 10 preceding years. Both total biomass and species richness were reduced after the 1979 winter, but the decline was only slight. Greatest reductions were observed in areas low in the intertidal. Most of the seriously affected species show their highest densities low in the intertidal or even subtidally. The following species suffered high losses that could be related to low temperatures: the bivalves Abra tenuis, Angulus tennis, Cerastoderma edule and Mysella bidentata and the worms Lanice conchilega and Nephtys hombergii . The reduced numbers of the shrimp Crangon crangon will have been caused by enhanced emigration to deeper water. The reduced numbers of the scale-worm Harmothoe lunulata could be explained by the absence of its host Lanice conchilega . Among these species, only Cerastoderma edule contributed substantially to the total biomass in the preceding years.

Year-to-year variability in the biomass of macrobenthic animals on tidal flats of the Wadden Sea: how predictable is this food source for birds?

Abstract The Wadden Sea is important as a stop-over and wintering area for several species of waders, foraging for shorter or longer times on its tidal flats. The size of the food stocks these birds encounter varies from place to place and from year to year. We studied characteristics of the variability in time of such prey stocks, using long-term data series of annual estimates of biomass of macrobenthic animals collected on tidal flats in various parts of the Dutch and German Wadden Sea. Year-to-year fluctuations were stronger in nearly all individual benhos species than in total macrozoobenthic biomass. The various species differed significantly in their year-to-year variability. Everywhere the tellinid bivalve Macoma balthica was relatively stable, whereas species such as the cockle Cerastoderma edule and the polychaetes Lanice conchilega, Nephtys hombergii and Anaitides mucosa fluctuated heavily and rapidly in all parts of the Wadden Sea where they were found. Within species, fluctuations in biomass of individual age or size classes were stronger than those in total biomass of the species. Several species showed minimal biomass values in the same years over vast areas. This synchronization of scarcity was caused particularly by similar responses to winter character, which was each year similar over the entire Wadden Sea. Such similar responses included low over-winter survival during severe winters and recruitment failure after exceptionally mild winters. Immediately after severe winters, such cold-sensitivee species as C. edule, L. conchilega and N. hombegii were scarce all over the Waden Sea, thus liimiting the possibilities for birds to switch to other parts of the Wadden Sea to find their preferred prey in sufficient quantitu. Simultaneous recruitment failure in several important bivalve species ( C. edule, Mytilus edulis , and Mya arenaria limited the possibility for specialized bivalve consumers to switch to alternative prey types in certain years.

Long-term changes in macrozoobenthic abundance on the tidal flats of the western part of the Dutch Wadden Sea

For 20 years (1969–1988), larger bottom animals have been sampled quantitatively once or twice annually at 15 stations scattered over Balgzand (a 50 km2 tidal flat area in the westernmost part of the Dutch Wadden Sea). In 29 species, numbers were sufficiently high to allow a statistical evaluation of the fluctuation patterns of their annual densities. The results revealed two main trends: (1) a sensitivity to low winter temperatures in 12 species, causing low densities in these species immediately after a severe winter (1979, 1985, 1986 and 1987) and relatively high densities during a period with some mild winters in succession (1973–1975); (2) an upward long-term trend in 11 (other) species, causing upward trends (viz. roughly a doubling) of total macrozoobenthic biomass and production over the 20-year period of observation, probably as a consequence of increasing eutrophication. By far the major part of the species thus exhibited either of these two patterns, causing total biomass and species number to be governed largely by the above two trends. Results of less frequent sampling (once per 5 or 10 years) of 26 transects scattered over the ≈500 km2 of tidal flats of the whole western half of the Dutch Wadden Sea showed that the two trends also represent the changes occurring in a much larger area. Some local departures from the general patterns are discussed and related to specific causes.

Zoobenthic biomass limited by phytoplankton abundance: evidence from parallel changes in two long-term data series in the Wadden Sea

Abstract We address the question of whether year-to-year variability in pelagic algal food supply can explain long-term variability in macrozoobenthic biomass in an estuarine area. Starting in the early 1970s, quantitative data were frequently collected in standardized ways in the western part of the Dutch Wadden Sea on (1) concentrations of phytoplankton species and chlorophyll (and rates of primary production) in the main tidal inlet (Marsdiep) and (2) numerical densities and biomass of macrozoobenthic animals (and growth rates in a few species) in a nearby extensive tidal-flat area (Balgzand). In both data series, the most distinctive feature was a sudden change that took place around 1980, viz. a rather sudden and persisting doubling of concentrations of chlorophyll and algal cells and of primary production rates, as well as of numerical densities and biomass of zoobenthos. From these parallel changes we hypothesise that algal food largely determines the abundance of zoobenthos in the Wadden Sea. The following observations substantiate this hypothesis: (1) the significant correlation between annual mean values of chlorophyll concentration and overall mean numerical density and biomass of zoobenthos (as estimated after an appropriate time lag), (2) the observed limitation of zoobenthic biomass doubling (after the doubling of food supply) to areas with already high biomass values (where food demand was high and food could therefore be in short supply), (3) the limitation of a strong response to changes in food supply to functional groups that are directly dependent on algal food, i.e. suspension and deposit feeders, as opposed to carnivores, (4) the significant correlation between annual growth rates in Macoma balthica and food supply in the growing season, particularly in areas close to the tidal inlet where food concentrations were monitored. Some other factors were identified that could decisively influence zoobenthic abundance locally and/or temporarily. Harsh environmental conditions will have limited zoobenthic biomass in extreme areas such as the upper part of the intertidal and areas exposed to strong currents and wave action. Severe winters temporarily reduced the abundance of several sensitive (southern) species, including most of the infaunal and epifaunal predators. Even stronger temporary and local reductions of zoobenthic biomass occurred as a consequence of fishery activities for such benthic species as cockles, mussels and lugworms. Recovery after temporary biomass reductions was generally rapid, but late-winter values of total-Balgzand zoobenthos biomass never exceeded an upper level of 45 g AFDW per m 2 probably set by maximal annual rates of primary production of between 400 and 500 g C per m 2 .

Expected Effects of Changes in Winter Temperatures on Benthic Animals Living in Soft Sediments in Coastal North Sea Areas

Dynamics of macrobenthic animals were studied quantitatively during a 20-year period on tidal flats in the Wadden Sea. During this period, 4 winters were very cold (mean temperature more than 2°C below the long-term average), whereas also a period with 8 too mild winters in succession occurred. No less than 10 out of the total of 28 species studied in detail were found to be sensitive to cold winters. Their overwinter survival and numbers found after a severe winter were lower than after normal or mild winters. The 4 polychaete and 4 bivalve species among these 10 sensitive species probably died from low temperatures, whereas the 2 crustaceans moved to deeper off-shore waters.

Reproductive investment in the intertidal bivalve Macoma balthica

Abstract Bivalve eggs generally contain large amounts of lipids which, in comparison with proteins and carbohydrates, have high energy contents and are thus costly in energetic terms. As lipid contents vary between species, comparisons of reproductive investments should not only include numbers and sizes of eggs, but also their energy content. We estimated the investment in egg material of mature females of the Baltic tellin Macoma balthica (L.) in terms of both mass and energy content. All mass below a minimum body mass (below which no eggs are produced) was defined as structural mass. This threshold amounts to a body mass index (BMI) of 5.6 (ash-free dry mass per cubic shell length in mg cm−3). More than half (55%) of the mass above the structural mass was invested in egg material and 45% in extra somatic tissue and tissue for production and storage of gametes. This means that the amount of eggs spawned ranged from 0 (at BMI = 5.6 mg cm−3) to 33% of the total ash-free dry mass (at a high BMI value of 14 mg cm−3). Eggs contained a relatively large amount of lipids, about 30% of their ash-free dry mass, whereas non-egg material contained only about 7% lipids. Eggs of two other bivalves in the Wadden Sea, the cockle Cerastoderma edule and the mussel Mytilus edulis, were smaller and contained only about 11% and 20% lipids, respectively. Energy content of M. balthica eggs amounted to ∼0.006 J, in the other two species to ∼0.002 J. The function of the more expensive eggs in M. balthica may be related to its early spawning in spring, causing slower larval development until first feeding.

Expected changes in the benthic fauna of Wadden Sea tidal flats as a result of sea-level rise or bottom subsidence

Abstract In different parts of the Dutch Wadden Sea, relationships between intertidal level and abundance of marine macrozoobenthos were similar. Numerical densities, biomass and species richness increased from values close to 0 at the high-water level to maximum values around mean-tide level (numbers) or halfway between this level and low-tide level (biomass). Species richness hardly declined below mean-tide level, whereas mean weight per individual continued to increase from high- to low-water level. Biomass was about 45 g ash-free dry weight per m2 at its maximum and declined in an approximately linear way to values close to 0 at the high-water level and to about 7 g per m2 at the low-water level. These two linear relationships were used to predict biomass changes on intertidal flats of the Wadden Sea at various scenarios of sea-level rise and bottom subsidence. Net sea-level rise is expected to result in increased amounts of intertidal zoobenthos in areas with predominantly high tidal flats, but in declines in lower areas. However, such changes will occur only if sea-level rise proceeds too fast to be compensated by extra sedimentation. Bottom subsidence as a consequence of gas extraction is expected to be too small to cause any measurable change in the benthic fauna.

Long-term development of biomass of intertidal macrozoobenthos in different parts of the Wadden Sea. Governed by nutrient loads?

Long-term data sets on intertidal macrozoobenthos from Danish, German and Dutch parts of the international Wadden Sea were analysed for trends in biomass of molluscs, polychaetes and crustaceans. Patterns in long-term development were compared with data on nutrient loads from freshwater sources and with regional data on chlorophyll a and nutrient concentrations in the water column. Fluctuation patterns of total biomass were strongly determined by fluctuations of bivalve biomass. Especially in bivalves these fluctuation patterns show synchronisation due to the different impact of severe winters (1979, 1985–87) and mild winters (1988–90). Indications were found for a consistent increasing trend in polychaetes. Most of the data sets do not allow a proper analysis of a possible causal relationship between nutrient input and biomass development of macrozoobenthos. Moreover, for such an analysis better information on nutrient load related food supply for macrozoobenthos is necessary.