Eutrophication -- 14.2 Benthic-pelagic coupling and eutrophication

14.3 The case of the silicate pump in the Bay of Brest

14.2 Benthic-pelagic coupling and eutrophication

14.2 Benthic-pelagic coupling and eutrophication

14.2.1 Pelagic production as food for benthic fauna

Oxygen deficiency in temperate coastal waters has led to an increased awareness of vertical particle flux to bottom waters. In recent years, particular attention has been paid to coupling and energy transfer between the benthos and plankton. It has been postulated that suspension-feeding communities can self-organize to enhance the efficiency of food capture and thus establish boundary systems capable of successfully exploiting the less structured planktonic system [172]. Others studies demonstrated that in temperate coastal waters the most prominent event in the annual flux of organic material to the benthos is usually the spring diatom bloom [433][213][488][352].

In coastal (and also temperate and polar) seas this rapidly sinking phytoplankton is often dominated by diatoms that reach the sea floor relatively intact without being ingested by zooplankton (see [433] for a review; [4]). Seasonally sedimented phytoplankton blooms are a major source of nutrients that are processed rapidly through the benthic system in open coastal areas [172][183]. Information from field studies supports the hypothesis that suspension feeders ingest a wide spectrum of particle sizes [389][98][372]. Many suspension feeders are capable of utilizing any type of food, and are limited only by morphological constraints [394].

For the case of suspension-feeding bivalves, food quality and quantity have been shown by Willdish and Kristmanson [496] and Rosenberg and Loo [399] to be a limiting factor. For example, infaunal bivalve growth was shown to be positively correlated with both the chlorophyll input to the sediment and the diatom availability in the near-bottom waters [466][297][496]. It has been widely recognized that benthic suspension feeders, which are among the main contributors to the biomass of benthic communities of coastal and estuarine ecosystems world-wide, benefit directly from pelagic primary production in the overlying water column [183][88]. Thus, suspension feeders are responsible for a considerable share of the energy flow from the pelagic to the benthic system, in addition to secondary production in benthic environments [370][172].

14.2.2 Regulation of benthic production by the benthic fauna

ragFig1

Figure: Graphical comparison of water mass residence time and clearance time in suspension feeder-dominated ecosystems. Ecosystems situated in the shaded area are potentially regulated by suspension feeders where clearance time is shorter than clearance time. AS: Ask� Bay. SSF: South San Francisco Bay. OS: Oosterschelde. CBO: Chesapeake Bay, past. BB: Bay of Brest. MO: Marennes-Ol�ron Bay. RA: Ria de Arosa. WW: Western Wadden Zee. NI: North Inlet. NB: Naragansett Bay. SY: Sylt, Eastern Wadden Zee. DB: Delaware Bay. CBP: Chesapeake Bay, Present. In Dame [115]. From Grall and Chauvaud [185].

Direct control of phytoplankton biomass.

There are strong indications that phytoplankton biomass may be severely reduced or regulated by active suspension feeders in shallow ecosystems [93][426][232][84]. From these studies, it can be concluded that the secondary trophic level is dominated by the benthic ecosystem where active suspension feeders can even regulate pelagic primary production when the water body is shallow, the residence time is long, and the suspension-feeding biomass is high [94]. Figure 1 illustrates the fact that suspension feeders are able to consume potentially high amounts of suspended food where the clearance time is shorter than the residence time of the water in the bay. Rates of suspension-feeding are a function of food supply for a variety of taxa, but since the process of filter-feeding uses a variety of different particle-trapping mechanisms and ranges from passive to active filter feeding, the relation between suspension feeders abundance and distribution is highly complex. Hydrodynamic factors may be critical in determining the food supply. The availability of food depends on the three-dimensional nature of the fluid and particulate fluxes to the benthic ecosystem [160]. Herman and Scholten [228] proposed three reasons why benthic suspension feeders may have a stabilising influence in benthic ecosystems. First, benthic suspension feeders are a stable component of the ecosystem. Secondly, the filtration rate of suspension feeders does not stabilise as food availability increases. Finally, the biomass of suspension feeders has a slow turnover rate. Together these three observations suggest that suspension feeders may limit the intensity and duration of phytoplankton blooms. In contrast, the zooplankton biomass increases in response to phytoplankton blooms and thus do not reach such an effective filtration level during the bloom period.

Suspension feeders and nutrient cycling.

Mussel or clam beds and oyster reefs may also supply nutrients in high amounts to the overlying water column and promote phytoplankton production. Thus suspension feeders are not only important in terms of direct control, but also affect nutrient recycling and sedimentation or resuspension of organic particulate matter (Figure 2). When the amount of food filtered by bivalves exceeds the needs of the individual, pseudofaeces are produced that incorporate the excess particulate organic matter. The formation of these pseudofaeces facilitates the sedimentation of POM and thus increases the overall sedimentation rate. Biodeposits are also a source of food for benthic organisms such as bacteria, meiofauna and macrofauna [182]. Faeces and pseudofaeces contribute to enhance bacterial activity on a day scale basis, while meiofauna and macrofauna populations rather respond on a week and month scale basis respectively [199][425]. Fauna may either feed directly on the organic matter of the biodeposits or on bacteria, which contributes to secondary production in the benthos but also to increase the turnover of nutrients ([182]; see below). Kautsky and Evans [263] argued that the role of suspension feeders in energy transfer may be minimal compared with the role they have in carbon and nutrient cycling in coastal ecosystems. In areas controlled and stabilized by suspension feeders and subject to increasing nutrient loads, the ecosystem is then highly vulnerable to changes in the suspension feeder community [84, see also].

ragFig2

Figure: Schematic representation of the nutrient fluxes and pelagic primary production dynamics in a suspension feeder-dominated ecosystem. PP = Primary Production. RPP = Regenerated Primary production. From Grall and Chauvaud [185].

Nutrient absorption/regeneration and zoobenthic communities.

Several studies have shown experimentally that degradation of organic matter was faster and more efficient in sediments with macrofauna populations. It has been suggested by various authors that the proportion of nutrient export from the benthic ecosystem to the water column due to macrofaunal activity supplies a significant proportion of the phytoplankton requirements [26][425]. However, there is no clear agreement on the amount published estimates range from 0 to 100%, with a mean of 28 - 30% [134]. A recent study by Grenz et al. [198] showed that during a phytoplankton bloom, nutrient fluxes from the sediment represented 20% (Si), 16%, (P) and 9% (N) of the primary production demand. Experimental studies in mesocosms with an intact benthos have showed that measured annual apparent primary production increased by 23% relative to mesocosms lacking benthos. Furthermore, in another experimental study, Christensen et al. [87] showed that nutrient release to the water column depends on the species function (both behavior and biology) in the system; NH₍4 and NO₃ release were 3 times higher in sediments which had the polychaete Nereis diversicolor as suspension feeder, and were just 1.5 times higher in sediments which included N. virens as a deposit feeder. The presence of Nereis in the sediment increased both NO₂ and silicate fluxes by two orders of magnitude. Magni et al. [303] showed that macrofauna rapidly and efficiently recycle the inorganic forms of nitrogen and phosphorus, thus playing a role in the process of nutrient regeneration. Using an open flow-through system, Asmus and Asmus [23] have shown that the potential for primary production induced by the nutrient release of an intertidal mussel bed was higher than the uptake of phytoplankton by the mussel bed itself. Thus, if benthic communities are able to reduce significantly the phytoplankton biomass, then they also have the potential to maintain eutrophication [119].

Oviatt et al. [358] note that as primary production increases, respiration and thus recycling of nutrients in the water column also increases. The pelagic production fuelled by nutrients derived from the benthos could then result in higher pelagic recycling rates. De Casabianca et al. [119] argued that the concentration of dissolved inorganic nitrogen did not vary much as a function of the presence or absence of a benthos, but rather in recycling of nutrients either in bottom sediments or in the water column. Thus, the effects of the benthos on pelagic production are two fold: supplying nutrients directly, and indirectly increasing regeneration rates in the overlying water column.

In the following section, we will explore the influence of benthic suspension-feeders on phytoplankton dynamics, in an ecosystem (the Bay of Brest, France) experiencing both excessive N inputs from the watersheds (leading to silicic acid limitation) and the proliferation of an invasive suspension-feeder, Crepidula fornicata (leading to enhanced biodeposition). Short-term ecological and long-term biogeochemical consequences of such an interaction will be explored in Section 14.4 of this chapter.

14.2 Benthic-pelagic coupling and eutrophication