Food Web of Intertidal Mussel and Oyster Beds

6.13

Food Web of Intertidal Mussel and Oyster Beds

H Asmus and R Asmus, Alfred Wegener Institute for Polar and Marine Research, List, Germany © 2011 Elsevier Inc. All rights reserved.

6.13.1 6.13.1.1 6.13.1.2 6.13.1.3 6.13.1.4 6.13.1.4.1 6.13.1.4.2 6.13.1.4.3 6.13.2 6.13.2.1 6.13.2.2 6.13.2.3 6.13.2.4 6.13.2.5 6.13.2.6 6.13.2.7 6.13.2.8 6.13.2.9 6.13.3 6.13.3.1 6.13.3.1.1 6.13.3.1.2 6.13.3.1.3 6.13.3.1.4 6.13.3.1.5 6.13.3.1.6 6.13.3.1.7 6.13.3.1.8 6.13.3.2 6.13.3.2.1 6.13.3.2.2 6.13.3.2.3 6.13.3.2.4 6.13.3.2.5 6.13.3.2.6 6.13.3.3 6.13.3.3.1 6.13.3.3.2 6.13.3.3.3 6.13.3.4 6.13.3.4.1 6.13.3.4.2 6.13.3.4.3 6.13.3.4.4 6.13.3.4.5 6.13.3.4.6 6.13.4 6.13.5 6.13.6 References

Introduction General Aspects of Suspension-Feeder Communities Types of Suspension-Feeding Communities Soft-Bottom versus Hard-Bottom Suspension-Feeding Communities A Biogeographical Overview of Suspension-Feeder Food Webs Tropics Temperate regions Polar regions Food-Web Components of Suspension-Feeder Assemblages Primary Producers Bacteria Herbivores Detritivores Invertebrate Predators Fishes Reptiles Birds Mammals Food-Web Case Studies of Mussel Beds in the North Sea and the Wadden Sea Ecological Carbon Transfer of Wadden Sea Mussel Beds Biomass of the dominant compartments Primary production: Gross primary production Net primary production Consumption Heterotrophic production Production to biomass ratio Respiration Excretion Trophic Analysis of Mussel Beds Diversity and biomass of trophic groups Total system throughput (TST) Average path length (APL) Average residence time (ART) Lindeman spine Mean trophic efficiency Structure and Magnitude of Cycling Number of cycles Cycle distribution Finn cycling index System Level Properties and System Organization Development capacity (DC) Redundancy Ascendancy Average mutual information (AMI) Flow diversity Connectance indices Food-Web Case Studies of Oyster Beds at the French Atlantic Coast Food-Web Case Studies of Oyster Beds at the American Atlantic Coast Role of Suspension-Feeder Assemblages in Coastal Food Web

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Food Web of Intertidal Mussel and Oyster Beds

Abstract Food webs of suspension-feeder communities in intertidal and sub-tidal areas are described, and a general portrait of the dominant components of these communities is given. A detailed case study of an intertidal mussel bed of the Sylt-Rømø Bight is performed by using the results of network analysis. Comparisons are made between North Sea mussel beds and oyster and mussel beds at the Atlantic Coast of France and the East coast of North America. The roles of suspension-feeder communities in the food webs of coastal areas are discussed.

6.13.1 Introduction 6.13.1.1 General Aspects of Suspension-Feeder Communities Trophic interactions between suspension-feeder communities and their ambient environment are among the most important ecological processes in shallow waters and may dominate benthic pelagic coupling particularly in coastal areas (Prins and Smaal, 1990; Dame et al., 1991a, 1991b; Smaal and Nienhuis, 1992, 1999; Smaal and Haas, 1997; Smaal and Zurburg, 1997; Prins et al., 1998; Asmus and Asmus, 2005). Although this is an important function, there have only been few attempts to quantify the trophic web of suspension-feeder communities integrating the different pathways from grazing phytoplankton to predation by birds (Baird et al., 2007). In the intertidal area, the effect of suspension-feeding com­ munities is most pronounced, because the water column is shallow and mixing of tidal water is intense; thus, suspension feeders may be able to use the total water column for feeding (Asmus et al., 1992, 2000). Where suspension feeders such as mussels occur on soft bottoms, intense filtering, feeding, and digestive processes lead to a high production of feces accumulat­ ing among and beyond the mussels and creating organic-rich sediments, which are suitable places for bacterial decomposition and detritivorous infauna (Commito and Boncavage, 1989, Commito et al., 2008). Shell-bearing suspension feeders, such as mussels and oysters, are also suitable substrates for other hard-bottom flora, and fauna characterizing suspension-feeder communities can be considered as oases of hard-bottom dwell­ ers in a sandy or muddy surrounding. The large aggregation of biomass of the suspension feeders in these communities attracts many invertebrate and vertebrate predators.

6.13.1.2

Types of Suspension-Feeding Communities

Suspension feeders include a wide spectrum of animal groups ranging from invertebrates, such as sponges, corals, bivalves, crustaceans, and ascidians (Gili and Coma, 1998), to verte­ brates, such as some fishes and whales (Bushek and Allan, 2005). Every group or species of suspension-feeding animals feeds on a slightly different size spectrum of living and dead particles and differ in the efficiency of filtering and the water volume processed (Defossez and Hawkins, 1997; Gili and Coma, 1998). The percentage of suspension feeding on the total food uptake may also vary. Obligate suspension feeders (such as blue mussels (Mytilus edulis) and oysters) use only suspended particles and plankton, whereas facultative suspen­ sion feeders (such as the bivalve Macoma balthica) and omnivores (such as the polychaete Hediste diversicolor) may switch to other food sources (such as microphytobenthos or sediment detritus) and other feeding modes (such as pipetting

the surface film or even predating) (Riisgård et al., 1992; Riisgård, 1994). Suspension feeders can be mobile or sessile and can live in pelagic as well as in benthic environments. Especially, sessile suspension feeders often show a tendency for aggregation and can, in this way, form communities offering space and nour­ ishment for associated fauna and flora. Benthic suspension-feeder communities occur in a wide range of habitats from the supratidal zone down to abyssal depths, occupying both hard and soft bottoms. Especially on soft bottoms, bivalve suspension feeders create special biotopes which reveal an increased biodiversity of species using the shells as settling substrate or as a shelter. These communities are distinctly different from their surrounding not only in their structural components but also in their function and the inter­ actions between the different animal and plant components. Therefore, they develop their own food web which may show some degrees of independence from the surrounding sandy or muddy bottoms but represent active sites of benthic pelagic coupling.

6.13.1.3 Soft-Bottom versus Hard-Bottom SuspensionFeeding Communities Although shell-bearing suspension-feeder communities on soft bottoms and hard bottoms consist of similar or even the same species, some fundamental differences occur in the species interactions. Only a limited number of epibenthic bivalves are able to cover soft bottoms and form dense aggre­ gations. These species play a key role for the total community particularly enabling the associated fauna and flora to find suitable conditions for settling. In hard-bottom communities, facilitating settlement for hard-bottom dwellers by a key species is of minor importance because the rocky substrate is not limited. In the latter situation, competition for space between different sessile organisms and the adaptation to strong water movements may become more important. This may also have consequences to the food web of both community types. In hard-bottom suspension-feeder communities, several species may occupy a certain area creat­ ing similar parallel trophic pathways resulting in a higher stability of the total community, whereas in epibenthic soft-bottom suspension-feeder communities the total community is dependent on the dominating key species and may vary with the population fluctuations of the key species and thus may represent a less-stable environment or habitat. In this chapter, we focus on soft-bottom bivalve-dominated suspension-feeder communities of the intertidal areas such as oyster beds and mussel beds where most of the few food-web studies have been compiled.

Food Web of Intertidal Mussel and Oyster Beds

6.13.1.4 A Biogeographical Overview of Suspension-Feeder Food Webs Dense aggregations of suspension feeders can be found on soft bottoms from the Arctic and Antarctic regions to the tropics; however, their ecological significance depends largely on the availability of their pelagic food sources. In general, phyto­ plankton availability is high in higher latitudes (e.g., Springer and McRoy, 1993; Sakshaug et al., 2004; Hill and Cota, 2005; Westwood et al., 2006; Platt et al., 2008) whereas it can be limited in oligotrophic equatorial regions (e.g., Yoo et al., 2008) where the suspension-feeder communities have devel­ oped special adaptations to overcome periods of lack of food.

6.13.1.4.1

Tropics

Reef-building bivalves are not documented from tropical coasts where most of the reefs in the intertidal and shallow sub-tidal zone are formed by corals. Coral reefs may show similar func­ tions as temperate bivalve beds; however, the process of filtration of particles by corals does not process large water masses; it is rather directed on larger particles and may be thus less efficient compared to temperate bivalve beds. Coral reefs are, however, rich communities that include other more efficient suspension feeders such as sponges, mollusks, crusta­ ceans, and ascidians. Additionally, a large part of energy for nutrition of coral reefs is derived from symbiotic autotrophic algae (Muscatine, 1967; Muscatine and Cernichiari, 1969; Porter, 1976; Patton et al., 1977; Davies, 1984, 1991). The latter process can also be found in tropical coastal bivalves, especially the giant clams of the genus Tridacna (Yonge, 1936; Klumpp et al., 1992; Hawkins and Klumpp, 1995; Atkinson and Falter, 2003). This symbiosis can be explained as an adap­ tation mechanism to overcome long periods of lack of plankton and detrital particles that occur often in tropical regions especially during the dry season. Other mechanisms to overcome the lack of food are the use of dissolved organic matter as an additional energy source, which has been proved for tropical bivalve species. Because of the close connectivity of species within food webs of tropical communities, a high degree of specialization and a large dependence on mechan­ isms such as mutualism and symbiosis are found. This may lead to a higher degree of clustering a community into subunits and smaller subsystems. In seagrass beds of the Indo-West Pacific, the thallassinid shrimp Neaxius acanthus creates large burrows of several dm³ of volume reaching up to 1 m into the ground. This species catches fresh drifting seagrass leaves which are shredded, mixed with loose sediment, and stored in large chambers of the burrow (Kneer et al., 2008; Vonk et al., 2008b). Besides the shrimps living in these burrows, an asso­ ciated community of different polychaetes, amphipods, fish, and even bivalves is present and depends on the food intake by the shrimp. Among this association, the bivalve Barrimysia cummingii lives attached to the burrow walls. This species is only found in these burrows where planktonic food is scarce. Stable isotope analysis of the tissue of this species suggests that this species is using chemoautotrophic bacteria to meet its energy requirements (Kneer et al., 2008). Although bivalve reefs comparable to temperate regions are not reported from tropical areas, bivalves can be found in rela­ tively high abundances. In the tropics, mangrove oysters such as Crassostrea rhizophorae in tropical America and Crassostrea

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cucullata and Saccoglossa glomerata in the Indo-Pacific region are frequently found as epizoa growing on stems and stilt roots of mangroves in high densities (Carranza et al., 2009a, 2009b; Summerhayes et al., 2009). There are few natural densities reported for mangrove oysters; however, for S. glomerata densi­ ties of about 500 individuals m−2 have been reported in South-East Australian mangrove areas (Summerhayes et al., 2009). Together with sponges and ascidians, mangrove oysters form rich faunal assemblages which may have similar ecological functions than temperate mussels or oyster beds. The food web of this assemblage or the contribution of this assemblage to the food web of a mangrove forest has not been investigated yet. A number of bivalves with chemo-symbiotic associations have also been reported from mangroves (e.g., Lebata and Primavera, 2001). Wood-boring bivalves are also common in the mangrove forest, and Singh and Sasekumar (1994), for example, reported 10 species of teredinids and one pholadid in several mangroves along the west coast of Peninsular Malaysia. These wood-boring bivalves are ecologically signifi­ cant as they stimulate the decomposition of wood and live in symbiosis with nitrogen-fixing bacteria (Waterbury et al., 1983). It has been suggested that the latter process may repre­ sent a very significant yet overlooked source of nitrogen fixation in mangrove ecosystems in view of the abundance of dead wood and Teredinidae (Boto and Robertson, 1990). Although mangrove-associated bivalves have only been rarely studied, their diversity can be surprisingly high. Alvarez-Leon (1983) reported 29 species of bivalves from the mangrove root systems on the Atlantic coast of Colombia, and Jiang and Li (1995) mentioned 24 bivalve species from a mangrove system in Hong Kong. A comprehensive overview on the diversity and function of macrobenthos and fishes in mangroves is given by Nagelkerken et al. (2008). The frequently cultivated pearl oyster Pinctada margaritifera is found in tropical coastal areas mainly attached to other mollusks or coral blocks, however, in lower densities of up to 10 individuals m−2 in the intertidal region of Kenya and in decreasing numbers at sub-tidal sites (Kimani and Mavuti, 2002). The genus Perna represents the temperate genus Mytilus in tropical areas. Perna perna is distributed along the tropical and subtropical coasts of the Atlantic and the African coast of the Indian Ocean including the Red Sea, whereas Perna viridis occurs at the Asian coasts of the tropical Indo-West Pacific. A further representative of the genus Perna canaliculus is restricted to temperate and subtropical waters of New Zealand. These mussels are found in littoral and sublittoral waters on rocky shores and also on mangrove mudflats (Macintosh, 1982) and even on compact mud and sand (Yap et al., 1979). These mussels are restricted to nutrient- and plankton-rich environ­ ments, and, thus, cultivation in lagoons with oligotrophic oceanic waters has failed (Glude, 1984). The contribution of dense aggregations of these mussels to the food web of tropical coasts did not attract much interest in the past, where the scientific focus has mostly been directed toward the culture of these mussels. Suspension feeders in tropical seagrass beds and mangrove forests can also reach high densities, especially sponges and infaunal bivalves. Vonk et al. (2008) reported on an Indonesian seagrass meadow that had faunal densities of 942 individuals m−2. Polychaetes (35%), bivalves (27%), and sipunculids (25%) accounted for the largest part of the total

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Food Web of Intertidal Mussel and Oyster Beds

fauna density. Including Nynantheae (4.7%), most of these species were small and lived inside the sediment. Crustaceans (5.1%), echinoderms (2.5%), and large bivalves (Atrina vexil­ lum, Pinna muricata, Pinna bicolor, Malleus albus, Isognomonpernum sp., and Modiolus micropterus) were the main groups of invertebrate species living (partly) on top of the sediment. The horse mussel (M. micropterus) lives in Indonesian seagrass beds attached to rhizomes of the large seagrasses Enhalus acoroides and Thalassia hemprichii (Asmus, personal observation). The mussel is hardly visible at the sedi­ ment surface, because it is buried into the sediment. In closed canopy meadows, this species reaches densities up to 284 individuals m−2 (Vonk et al., 2010). Its abundance is exceeded by the mussels of the family Lucinidae that appear with more than 1000 specimen m−2 in this environment. The latter group does not feed as a suspension feeder but has a reduced stomach and lives in symbiosis with sulfur-oxidizing bacteria (Taylor and Glover, 2006). Vonk et al., (2010) measured C and N stable isotope deple­ tion in these seagrass beds. The abundant filter feeders, such as A. vexillum and M. micropterus, have δ13C values indicating the use of both planktonic and benthic food sources (cf. Tewfik et al., 2005). The signature of planktonic sources, however, may vary largely over time and the signatures of fauna species result from their food sources of the last days to months (Bouillon et al., 2000). This indicates that planktonic sources may be more important than estimated in this study. However, the role these large aggregations of bivalves play for and within the food web of a tropical seagrass bed is poorly understood and still needs considerable research effort.

6.13.1.4.2

Temperate regions

Despite the bulk of literature on oyster and mussel beds from temperate regions, only few of these studies focus on food webs within these communities. In the North Sea, the blue mussel M. edulis forms large aggregations of up to several thousands of individuals in the intertidal region close to the low-tide level. The occurrence of mussel beds on soft bottoms can be explained by the ability of mussels to intertwine each other with their byssus threats forming aggregations of different sizes from mussel clumps to large beds of several square meters. These large aggregations of mussels are settling grounds for a large number of invertebrate species which live either firmly attached to the mussels or crawl among the mussel shells. Up to 120 species were recorded in intertidal mussel beds of the SyltRømø Bight in the Northern Wadden Sea (Asmus, 1987). These species show a variety of trophic interactions and form a com­ plex trophic net that has been explored by Baird et al. (2007, 2011) and will be described in this chapter in more detail. One special feature of the intertidal mussel beds is the appearance of a carpet of macroalgae covering this community to a large extent. This coexistence of mussels and brown algae (Fucus vesiculosus) has been interpreted as a symbiosis between both organisms (Nienburg, 1927). The alga has also been described as a separate species (Fucus mytili). When growing on a mussel bed, the bladder wrack (F. vesiculosus) does not develop gas chambers as drifting buoys, adhesive disks, or reproductive organs. Only the swimming branches of the plants are fixed by the byssus threads of mussels and this suggests that the algae has advantages in growing on a fixed position, whereas the mussels have the advantage that sinking into the soft sediment

is prevented by the buoyancy of the plants (Nienburg, 1927). Neither the existence of a separate Fucus species nor the sym­ biosis between mussel and algae can be confirmed at present, because algae develop into the normal plant while coming in contact with firm substrate. In the mussel beds, the algae, however, play an important role as a nutrient filter. Because of the high remineralization potential of the heterotrophic part of a mussel bed community, nutrients are produced and released by the animals and bacteria of a mussel bed and taken up by the algae carpet before it can reach the water column. In this way, the nutrients can be stored within the mussel bed system over longer time periods. For the food web of a mussel bed, the large biomass and productivity of macroalgae play an ancillary role, because only few animals such as the amphipod Gammarus locusta use macroalgae as food. The high macrophyte production is exported from the system when, during storms in autumn, most of this plant material breaks off and drifts to the beach. The large concentration of mussels in a mussel bed also attracts invertebrate and vertebrate predators. The shore crab Carcinus maenas is predating on a wide range of invertebrates. Especially the young-of-the-year recruits of shore crabs are able to feed upon post-larval mussels of the same year class. Because crabs settle only few weeks later than the mussel recruits, the latter still have a suitable size as prey. In the Sylt-Rømø Bay settlement, juvenile crabs occur in such large numbers that these animals are able to destroy most of the mussels’ recruit­ ment. In years with a cold winter, the crab recruitment is delayed in summer by which time the earlier-settling mussels have already grown up to a size that exceeds that of a suitable prey for the young crabs. This match/mismatch effect contri­ butes significantly to the fact that the recruitment success of M. edulis is larger after cold compared to mild winters. Adult mussels are also an important food source. In certain years, starfishes Asterias rubens may occur in high abundance and eat most mussels of the sub-tidal parts of the mussel beds. The predation pressure of starfishes often limits an expansion of a mussel bed into the sub-tidal area (Saier, 2001), whereas in the intertidal area mussels are protected from starfish predation because star fish do not survive longer periods of emersion. Birds are important predators on both intertidal and sub-tidal mussel beds. In the Sylt-Rømø Bight, eider ducks (Somateria mollissima) visit the mussel beds from late summer to spring and eat almost the total summer production of mus­ sels (Nehls et al., 1998). They forage for mussels by diving and swallow the total mussels (Nehls et al., 1998). It has been estimated that eider ducks spend much of their energy in winter for the swallowing process for warming up the cold mussel food to body temperature (Nehls et al., 1998). Eiders have special feeding territories on mussel beds and those specimens which are not able to occupy a territory have to switch to other feeding sources such as cockles in sand flats or in sub-tidal sandy areas. While eider ducks mainly feed on mussel beds during the immersion period, oystercatchers (Haemantopus ostralegus) and herring gulls (Larus argentatus) are dependent on the emersion period to reach their food resources. Among oystercatchers, several techniques have been developed for opening mussels. Some families of oystercatchers have culti­ vated the hammering techniques in that they peck a larger hole into the shell for getting the mussel flesh, whereas others insert the bill into the small valve opening of a mussel and try to

Food Web of Intertidal Mussel and Oyster Beds

dissect the constrictor muscle which leads to a wider opening of the shell and an easy removal of the flesh. Herring gulls have larger problems to open mussels. They fly with the total animal to a certain height and drop them down on the next hard substrate such as a rock or even a street in dune or marshy areas. Most other bird species are unable to open adult mussels and they have to predate upon younger mussels or associated snails, polychaetes, and crustaceans. This is also valid for most of the fish species that are abun­ dant in mussel beds. The majority of fish species in a mussel bed are residents that are attracted by this habitat because of shelter by the mussel shells and the algal carpet, as well as by the higher food availability. During ebb tide, they retreat only over a small distance from the intertidal mussel beds into tidal ponds and the sub-tidal parts of this community. Most of the fish species use the crustaceans of a mussel bed such as the abundant amphipods, isopods, and juvenile decapods as food source. In the Sylt-Rømø Bight, gunnel (Pholis gunellus) and five-bearded rockling (Ciliata mustela) seem to be restricted to mussel and oyster beds, whereas other species such as sea sculpin (Myoxocephalus scorpius) and eelpout (Zoarces viviparous) are distinctly more abundant in mussel beds than on bare sandflats and mudflats. Juvenile cod (Gadus morhua) and whit­ ing (Merlangius merlangus) are also often more abundant over mussel beds feeding to a large extent on amphipods, shrimps, and juvenile crabs. The productivity of the associated fauna of a mussel bed together with the young-of-the-year mussels thus plays an important role in the energy flow of a mussel bed as a through-flow compartment, whereas larger-sized mussels can be regarded as a storage compartment for the energy of the system and are only a food source for a limited number of predators (Asmus, 1987). Other bivalve feeders also play an important role in the food web of the Wadden Sea; especially, cockles (Cerastoderma sp.) may reach high abundances in sandy areas and muddy sands, where they feed on phytoplankton and partly also on resuspended microphytobenthos. Although the filtration potential of a cockle bed is far less per meter square compared to a mussel bed, its significance on the ecosystem level is much higher. While mussel beds only occupy small areas of about 1% of the intertidal part, cockles can settle in sandflats and mudflats that form about 70–80% of the inter­ tidal region (Asmus and Asmus, 2005). Their part in pelagic–benthic interactions for the total Sylt-Rømø Bight is thus much higher compared to mussel beds, but their role as a key species and as a settling substrate is lower because they live buried into the sediment. However, cockles play an important role as food for birds and fishes. The knot Calidris canutus is largely dependent on cockles as a food source during its migra­ tion between the arctic breeding grounds and the overwintering area at the West African coast. Flatfishes such as plaice (Pleuronectes platessa) and flounder (Plathichthys flesus) feed largely upon juvenile cockles. Suspension-feeder communities in the North Sea region have recently shown significant changes, especially due to the invasion of foreign species and their dispersal promoted by climate change. In the Sylt-Rømø Bight, the Pacific oyster (Crassostrea gigas) was introduced probably for oyster culture and has dispersed due to good spawning and settling success during the warm summers of the early 2000s. They first

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occupied established mussel beds building up mixed beds, where oysters settled on large-sized mussels as a substrate. Once established, they settled also on living oysters and oyster shells and occupied in this way larger areas by forming distinct reefs. Several field and laboratory experiments have shown that Pacific oysters are not a suitable prey for most of the mussel-eating predators such as shore crabs, starfish, eiders, oystercatchers, and gulls (Markert et al., 2010). However, they show a comparable role as eco-engineers and show a similar function as substrate for the associated faunal community (Markert et al., 2010) as mussel beds. Because of the lack of byssus threads, oysters do not fix drifting macroalgae such as F. vesiculosus. However, they are a suitable substrate for red and brown algae. Even M. edulis can use oysters as substrate, espe­ cially after the winter 2009/10 mussel recruits could be observed when settling on adult oysters and between them in pure oyster reefs. The role of a pacific oyster bed for the food web of the Wadden Sea still needs a great deal of research to be understood. Although this oyster is not eaten by predators, their beds can support a rich epibenthic community which is also of nutritional value for predatory invertebrates, fishes, and birds. During the turn of the nineteenth to the twentieth century, another suspension feeder, the North American slipper limpet (Crepidula fornicata), first became introduced into the North Sea region. For most of the time, this species was found on mussel beds but without showing high abundances. This situa­ tion has changed in the last decade. Probably due to higher environmental temperatures, both in winter and in summer, the slipper limpets have increased in numbers and formed large aggregations especially in the sub-tidal region of the inner parts of the Wadden Sea. Other European countries, such as France, have also reported a dispersal of slipper limpets. In the Bay of Brest, mass occurrence of slipper limpets has led to concerns for the commercial oyster and mussel fishery (Decottignies et al., 2007), because this species can compete with the commercial oysters for food. Differences in the isotopic deviations of C. fornicata and C. gigas in the Oosterschelde, the Netherlands, suggested that these two suspension feeders may not be compe­ titors in the absence of food limitation (Riera et al., 2002). In the Wadden Sea, there have been no reports so far on the trophody­ namic significance of slipper limpets at ecosystem level. Another suspension feeder, the razor clam Ensis americanus, has been introduced from North America into the North Sea in the 1980s. This endobenthic species settles as juvenile in large areas at the lower tidal sand flats and the shallow sub-tidal area. Adult specimens are found in high densities at each side of the tidal gullies in 2–3 m depth below mean spring tide level, forming a belt visible through a large number of holes within the sediment. It has been estimated that the biomass of Ensis in such high-density spots can reach that of an epibenthic mussel bed (Armonies and Reise, 1999) and thus this assemblage may also have a high impact on benthic pelagic coupling and nutri­ ent remineralization. It could be shown that Ensis is also included in the food web. The common scoter (Melanitta nigra) was observed to shift its diet from the decreasing popula­ tion of the sub-tidal bivalve Spisula solida to the increasing populations of Ensis directus (Leopold et al., 2007). In most of the coastal bays and intertidal areas in Europe, shellfish are exploited by man and thus most of the areas where natural mussel and oyster beds occur are now occupied by culture lots of these animals. In the German Wadden Sea,

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Food Web of Intertidal Mussel and Oyster Beds

such culture plots are restricted to a certain maximum area. However, shellfishery and mussel culture is a dominant feature in the Dutch Wadden Sea and the adjacent Delta region. Natural mussel beds in these areas are of the same type described for the Sylt-Rømø Bight, but at the ecosystem level the mussel and oyster culture are dominant. Also, the fishery on cockles is still allowed and thus the food web of the Western Wadden Sea is largely impacted by men. Shellfish farming and cultivation is also a predominant feature of the Atlantic coast of France. These systems are the major European area for oyster cultivation and the only ones that have been known to show an overstocking, especially, of oysters in the past (Héral et al., 1988; Bacher, 1989; Héral, 1993). The consequence is that only few natural oyster beds and mussel beds can still be found, whereas the cultivated shellfish stocks influence the system dynamics and their food webs distinctly. The ecosystem analysis of the Marénnes-Oleron Bay, particularly the Brouage Mudflat and the Aiguillon Bay, has shown the food web as well as the stress that is exerted to these systems due to the oyster cultivation (Leguerrier, 2006). In the cold and warm temperate areas of North America, oyster beds predominantly formed by the species Crassostrea virginica frequently occur on the intertidal mudflat areas along creeks of the East coast. The energy and carbon flow of the oyster beds of the North Inlet, South Carolina, have been described in great detail already during the 1980s by Dame and Patten (1981). Compared to mussel beds, oyster beds are home for many different plants and animals. Dame (1979) found about 37 species in oyster beds. Additionally, Bahr and Lanier (1981) found 42 species whereas 303 species could be found by Wells (1961) in intertidal and sub-tidal oyster beds along a salinity gradient. In an intertidal oyster reef of the North Inlet, South Carolina, C. virginica showed the highest abundance among the suspension-feeder guild followed by the mytilid bivalve Brachydontes exustus living among the oysters. Also, deposit feeders such as the polychaete Heteromastus fili­ formis reach high abundance in the sediment below and among the oysters. Other abundant polychaetes such as Nereis succinea also have a more omnivorous mode of life. The barnacle Balanus eburneus is a frequent sessile organism settling in oyster beds using mainly zooplankton and large phytoplankton as food resource. Many predators are attracted by oyster beds. Most abundant is the Atlantic mud crab Panopeus herbstii. Individuals prey on a variety of organisms, including oysters and clams; crustaceans; annelid worms; fishes; and the marsh periwinkle, Littorina irror­ ata (McDermott, 1960; Castagna and Kraeuter, 1977; Whetstone and Eversole, 1981; Silliman and Bertness, 2002; Silliman et al., 2004). In C. virginica reefs, this species often co-occurs with another crab Eurypanopeus depressus. Adult E. depressus are omnivores feeding primarily on algae, amphi­ pods, oyster spat, sponges, polychaetes, other crustaceans, and detritus (McDonald, 1982; Williams, 1984). The flatworm Stylochus ellipticus is an important predator on oysters in North American oyster beds (Loosanoff, 1956; Webster and Medford, 1959). These worms prefer to feed on barnacles but shift to oyster spat when they are abundant. Even fishes prey upon oyster beds but only few species are known to use oysters or even bivalves directly as food. Along the Atlantic coast of North America, the cow-nosed ray

Rhinoptera bonasus is reported to prey not only on clams and other bivalves in soft sediments but also on adult oysters (Smith and Merriner, 1978). In addition, a bony fish, the black drum Pogionias cromis, is known to feed on post-settlement oysters. In oyster beds, birds do not play an important role as predators of bivalves comparable to mussel beds. The asso­ ciated fauna of snails, crabs, and fishes, however, play an important role for predatory birds such as herons. The Atlantic mud crab is preyed upon by a variety of birds, fishes, and larger crustaceans. In North Carolina, the dominant pre­ dator of P. herbstii populations was the oyster toadfish, Opsanus tau (Grabowski et al., 2005). Even mammals, especially otters and racoons, visit oyster beds feeding on oysters as well as the associated fauna.

6.13.1.4.3

Polar regions

Although there exist a number of food-web studies from Polar regions, these studies focus mainly on larger areas at the scales of bays and sea regions and thus there is no food-web study to our knowledge that considered the community level at the scale of a single mussel bed. Due to the extreme winter condi­ tions in the Polar regions, especially the intertidal and shallow sub-tidal areas do not show a high biomass and abundance of macrobenthic animals. Most of the soft-bottom areas of the Arctic Ocean are additionally influenced by the large Siberian Rivers that drain large areas of the Asian continent and turn the marine environment of the ocean into a brackish environment especially during summer. In the Antarctic region, ice score (or scrape) is the dominant physical force that prevents settlement of larger macrofauna in shallow water regions. Deeper at the shelf region, rich communities in both diversity and biomass can, however, be found that may be comparable to tropical reefs, although their growth and turnover is much less. The Antarctic suspension-feeder communities show a variety of animal phyla that are comprised of sponges, hydrozoans, and echinoderms, but only few bivalve suspension feeders occur (Orejas et al., 2000). Epibenthic bivalve communities have hardly been reported from Arctic regions. However, some endobenthic communities such as the Hiatella arctica community around 5 m depth and the Portlandia arctica community occur in depths more than 15 m. They use phytoplankton as well as suspended detritus as food source, and also show significant filtration rates around 0 °C but already a decrease in filtration rate when temperature increase is more than 10 °C (Petersen et al., 2003). The large biomass of H. arctica is an important food source for the arctic subspecies of eider ducks (S. mollissima borealis in the North Atlantic; S. mollissima v-nigra in the North Pacific region). In contrast to eiders, the arctic king eider (Somateria spectabilis) is mainly omnivorous and forages in deeper waters off the coast or even uses freshwater ponds and upstream river regions for feeding and thus the diet is composed mainly of polychaetes, crustaceans and aquatic insect larvae. In the Arctic region, mammals use mussels as food. Especially, the Walrus (Odobenus rosmarus) can blow out endo­ benthic clams from the sediments and thus clams of the genus Hiatella and Mya are the main food source of this species. Mussels also play an important part in the diet of the bearded seal (Erignathus barbatus). Most studies of the diet of bearded seals have been conducted in the shallow Bering and Chukchi

Food Web of Intertidal Mussel and Oyster Beds

seas which provide the largest continuous area of favorable bearded seal habitat in the world (Burns and Frost, 1979). In a comprehensive study and review of the diet of the bearded seal in the Bering and Chukchi seas, Lowry et al. (1980) found that it consisted mainly of crabs, shrimps, and clams. Fish, they concluded, were of minor importance in the diet. Specimens of the Canadian area revealed that the species there is mainly eating fishes such as the polar cod (Finley and Evans, 1983).

6.13.2 Food-Web Components of Suspension-Feeder Assemblages In this section, the different compartments of the food web of soft-bottom oyster and mussel beds are portrayed.

6.13.2.1

Primary Producers

Phytoplankton is the main food resource for suspensionfeeding communities such as oysters and mussels. Because of the dense aggregation, the grazing pressure that is exerted from the bivalve bed to the phytoplankton is immense. A compre­ hensive overview of bivalve grazing in different parts of the world is given by Dame (1996). Bivalve filtration ranges from 4.9 mg-C m−2 yr−1 in large estuaries such as the Chesapeake Bay (Ulanowicz and Tuttle, 1992) to 263.7 mg-C m−2 yr−1 in sys­ tems characterized by an intensive culture of oysters such as the Marénnes-Oleron Bay in France. In many cases, the autochtho­ nous primary productivity of the phytoplankton is not sufficient to support the suspension-feeder compartment of the community. Therefore, most bivalve beds are dependent on a continuous transport of phytoplankton from the sea. This is the reason why in the Wadden Sea the occurrence of bivalve beds is restricted to the margins of the tidal inlets where the water currents are high and the mixing is intense. The filtration pressure that means the ratio between bivalve grazing and primary productivity in mg C m−2 yr−1 is thus ranging from 0.02 in Chesapeake Bay (Ulanowicz and Tuttle, 1992) to 3.3 in Marénnes-Oleron Bay (Zurburg et al., 1994). In more natural systems, the ratio is ranging between about 0.15 for the oyster beds in North inlet (Dame et al., 1991a, 1991b) and 1.8 in the Königshafen area of the Sylt-Rømø Bight (Asmus et al., 1990). Values above 1 indicate that a support of phytoplankton from outside is necessary to support the bivalve aggregations. The need for an auxiliary food import of phytoplankton could also be shown for mussel beds and the total Sylt-Rømø Bight by Baird et al. (2004, 2007, 2008, 2011). Microphytobenthos occurs in mussel and oyster reefs on the sediments between the mussels or as epiphytes on mussel shells and associated macrophytes. The primary production of this compartment is rarely measured in bivalve systems, but in mussel beds of the Sylt-Rømø Bight this component has a gross primary productivity (GPP) of 99 mg-C m−2 d−1 and a net primary productivity (NPP) of 64 mg-C m−2 d−1 (Baird et al., 2007, 2011). This is far less than the productivity of microphytobenthos in adjacent sand or mud flats. In muddy areas, microphytobenthos can be resuspended by currents and waves and, in this way, it can contribute to the dietary budget of suspension feeders. Macroalgae reach high biomasses over mussel beds but no reports are given by oyster beds or comparable bivalve-

293

dominated systems. Up to a GPP of 5300 mg-C m−2 d−1 are measured for macroalgae of mussel beds and NPP amounts at 3300 mg-C m−2 d−1 (Baird et al., 2007). Macroalgae are impor­ tant components for the nutrient and carbon cycling and exchange, but they play a minor role for the food web of the bivalve bed (see Chapter 6.01).

6.13.2.2

Bacteria

Bacteria can be found above mussel beds as free-living bacteria in the water column in concentrations of about 9.8 mg-C m−2. Because of the capability of mussels to filter particles down to a size of about 3 μm, free-living bacteria may contribute to the diet of mussels. Oysters (C. virginica) are less efficient to filter particles at the lower end of the size spectrum compared to marsh mussels (Geukensia demissa) and thus the efficiency of filtering bacteria ranges from 5% to 15.8%, respectively (Kreeger et al., 1988). Using higher efficiencies for bacteria filtration of 57% (Crosby, 1987), Langdon and Newell (1990) estimated that free-living bacteria could contribute 3.4–25.8% to the metabolic carbon requirements of oysters and marsh mussels, respectively. Because of the low C:N ratio of bacteria of about 3.7, they are of particular importance for the nitrogen budget of bivalves. Sediment bacteria also contribute to a food web of a mussel bed. It depends, however, on resuspension processes whether this food source that can live attached to the detrital particles is used by suspension feeders. In mussel beds, bacteria are settling in the sediment below the mussels or oysters. This sediment layer is enriched by organic matter due to the feces and pseudo feces production of the animal community. Bacteria are thus not only an important contribution to the diet of protozoans but also for macrofauna (such as oligochaetes and polychaetes) living in this sediment in higher densities compared to the adjacent areas (Commito et al., 2008).

6.13.2.3

Herbivores

The dietary budgets of suspension-feeding bivalves are domi­ nated by the uptake of phytoplankton. Thus, the uptake of primary producers from the pelagic domain by the benthic community is the dominant feature of mussel and oyster beds. In a mussel bed of the North Sea, mussels are the main herbivorous organisms of the system. They are accompanied by sponges (Halichondria panicea) in sub-tidal places and some other suspension feeders have been introduced to mussel beds such as the bivalve C. gigas, the gastropod C. fornicata, and some ascidians such as Styela clava and Molgula manhattan­ sis. Endobenthic suspension feeders such as Mya arenaria, Cerastoderma edule, and M. balthica also occur in mussel beds of the Wadden Sea but not in large numbers. In the recently established oyster beds, the associated herbivorous suspension feeders consist of the same species as observed in mussel beds. Among oyster reefs of the introduced species C. gigas, mussels M. edulis may also occur in high abundances as epibionts, whereas in the sediment below the oyster, the pullet carpet shell Tapes sp. occurs in higher abundances. In the native oyster reefs of the species C. virginica at the eastern North American coasts, the associated suspension fee­ der B. exustus may play a similar role as epibiont and possible food competitor like M. edulis in the oyster beds of the Wadden

294

Food Web of Intertidal Mussel and Oyster Beds

Sea. Infaunal suspension feeders of C. virginica beds are G. demissa and Mercenaria mercenaria. In addition to these suspension-feeding bivalves, some planktivorous polychaetes can be found such as Cirratulus grandis and Polycirrus eximius. Due to the occurrence of hard substrate in the form of mussel and oyster shells that can be settled by benthic microalgae, herbivorous benthic grazers are also present in mussel beds and oyster beds. In mussel beds of the North Sea, this group is dominated by the periwinkle Littorina littorea which reach high biomasses in this community. Food-web budgets have shown (Baird et al., 2007) that this species may be food limited when feeding exclusively on microphytobenthos because biomass and production of microphytobenthos is comparably low. During ebb tide, these snails thus migrate to adjacent sand flats where this food source is higher. It is also known that L. littorea can switch to epizootic organisms as food such as juvenile barnacles (Buschbaum, 2002). Other herbivor­ ous benthic grazers are less abundant in mussel beds. The Chiton Lepidochitona cinerea scrapes microalgae and crustac­ eous algae from the mussel shells. Another periwinkle, the Littorina mariae, is grazing epiphytes from the F. vesiculosus plants growing on mussel beds. Macroalgae are hardly used as food although their production is high in mussel beds and mussel beds offer the only suitable settling substrate on soft bottoms. The amphipod G. locusta is the most abundant grazer on macroalgae in mussel beds.

6.13.2.4

Detritivores

Because of the fecal and pseudo-fecal production of the suspen­ sion feeders, mussel beds and oyster beds accumulate high amounts of organic material in the sediment. While the avail­ ability of organic matter enhances bacterial decomposition processes, it also promotes macrobenthic animals that are feed­ ing upon both bacteria and dead organic material. Among the faunal detritivores are polychaetes such as H. filiformis and Capitella capitata and oligochaetes such as Tubificoides benedenii. The latter one was dominant in New England mussel beds where this oligochaete distinctly decreased in numbers when mussels were removed from the sediments (Commito and Boncavage, 1989). In addition to the positive effect of food enrichment below the mussels, this was explained by the pro­ tective effect of mussels from predators that could feed upon oligochaetes and by the fact that a number of polychaetes competing with the oligochaete for food are lowered under these mussel beds. Compared to the biomass of the suspension feeders, biomass of endobenthic deposit feeders is low but reaches similar values as known of other sediment types. In addition to the above-mentioned worms, some endobenthic species (e.g., M. balthica) use detritus to a large extent, although they are able to use other food sources. Suspension feeders use suspended detritus as food. In the Wadden Sea, the major compound of seston is dead organic matter, whereas phytoplankton contributes with less percen­ tage. Because most suspension feeders are able to select particles, they assimilate phytoplankton in favor of detritus.

6.13.2.5

Invertebrate Predators

Gastropods are well-known invertebrate predators in mussel beds. The dog whelk Nucella lapillus is widely distributed in

Northern Europe and at the Atlantic coast of North America. Dog whelks prefer to feed upon mussels and barnacles, but the percentage of mussels in their diet increases with the age of the animals (Hughes and Burrows, 1993; Seed, 1993). They are mostly found on hard substrates and occur only occasionally at soft-bottom mussel beds. In oyster beds of the American Atlantic coast, the Atlantic oyster drill Urosalpinx cinerea is one of the main predators on C. virginica. Newly settled spat and juveniles of oysters are subject to intense mortality due to predation, especially by the oyster drills (U. cinerea and Ocenebra erinacea) and starfish. This species has also been introduced into Europe in the nineteenth to the twentieth century and it also became a typical species of the British oyster beds; however it remains, in the first years after the introduction, restricted to the beds in Kent and Essex (Reise et al., 1998). It has also been found in the Oosterschelde and the presence there has been recently confirmed (Faasse and Ligthart, 2007). For example, in the Oosterschelde, Korringa (1952) reported 90% mortality in oyster spat by their first winter, with up to 75% being taken by U. cinerea, whereas Hancock (1995) noted that 73% of spat settling in summer 1953 died by December, 55–58% being taken by U. cinerea. On the European coast, the native European oyster Drill O. erinacea feeds on oysters and other epibenthic bivalves. Until now, this species has been one of the main intertidal predators able to inflict real damage on cultivated oysters (Deltreil and Marteil, 1976). This species occurs in oyster beds of the French Atlantic coast and the British Isles. At the British North Sea coast, this species has been wiped out in cold winters but has reappeared in recent days. This muricid gastro­ pod has been introduced with oysters to the Limfjord/Denmark a couple of times, but has not been established (Jensen and Knudsen, 2005). It was found again in 2006 with egg capsules, and thus it seems to be established, though this time it has probably extended its natural distribution due to higher tem­ peratures and presence of food (Jensen and Hoffmann, 2007). At the Marennes-Oléron Bay also the Japanese oyster drill Ocenebrella inornata has been introduced in 1995. This species is an additional strong predator on young oysters. Rapana venosa is a predatory gastropod that originally occurs at the East Asian Coast from Korea to China at the Bohai Sea and has been introduced into many parts of Europe. This gastropod is a very voracious predator and it is blamed in the Black Sea for the decline of the native, edible bivalve fauna (Zolotarev, 1996, in Harding, 2003). It has caused significant changes in the ecology of bottom-dwelling organisms and has resulted in the near extinction of the oyster Ostrea edulis in the area of Gudauta, Georgia (Chukhchin, 1984, in Harding, 2003). Although scientists are still studying the impacts of R. venosa, they are very concerned about its potential damage to native species. This species prefers sandy bottoms where it lives buried into the ground. In the North Sea and the Wadden Sea as well as the European Atlantic coasts, the main invertebrate predators on intertidal bivalve beds are crabs, especially the shore crab C. maenas (see Chapter 7.03). In oyster beds of North America, the Atlantic mud crab E. depressus is the dominant invertebrate pre­ dator. Starfishes are important predators on mussel beds of rocky shores at most of the temperate coasts, but they are restricted to sub-tidal regions. The above-mentioned gastropod and crustacean species prey on the bivalve stock directly.

Food Web of Intertidal Mussel and Oyster Beds

The number of predator species on associated fauna is even higher. Bivalve beds often are overgrown by sessile epizoans such as hydrozoans and anthozoans. Most of them use zoo­ plankton as food. These animals have again specialized predators preying on them such as the nudibranch Aeolidia pappilosa feeding on different anthozoans particularly Metridium senile. Also, barnacles use zooplankton as food and are in this way carnivorous. This is also true for the large polychaete Nereis virens. As juveniles these worms are detriti­ vorous, but as adults they shift to a carnivorous diet living as predators. Even different nemerteans, such as Lineus ruber which lives in mussel beds can feed on associated polychaetes.

6.13.2.6

Fishes

Only few fishes occurring in bivalve beds are known to feed upon bivalves directly. Most of them use the higher amount and diversity of small crustaceans such as amphipods, isopods, and juvenile decapods in bivalve beds as described in Section 6.13.1.4.2. In addition to the above-mentioned species, the gobiid species Neogobius maculatus has been invaded into the Baltic Sea especially in Poland, where it also feeds upon Mytilus trossulus. This species has already entered the Rhine area in Germany and occurs also in the Kiel Canal. However, due to its preference for brackish water, it is still absent from polyha­ line waters of the Wadden Sea.

6.13.2.7

Reptiles

There are only few references of the importance of reptiles as predators of marine mussels. Sea turtles prey upon tridacnid clams in the South Pacific (Copland and Lucas, 1988) and the Diamondback terrapins are thought to prey on Mytilus at the North American coast (Hurd et al., 1979).

6.13.2.8

Birds

Most birds have a large impact on the structure of bivalve associations. Especially, eider ducks, herring gulls, and oyster catchers are important predators on mussel beds (see above), whereas black-headed gulls, common gulls, herons, and waders visiting this community are predating on the associated poly­ chaete and crustacean fauna.

6.13.2.9

Mammals

Mammals do not play a large role in the food web of the bivalve beds of the North Sea. In the oyster beds of the Atlantic North America, racoons have been observed to forage on oyster beds and to feed upon these bivalves during low water. At the Pacific coast of North America, bivalves are also eaten by Sea otters, although these mammals feed mainly on mussels on hard substrates. Except sea urchins, the preferred prey is mollusks of the genus Haliotis. Walruses O. rosmarus are the largest animals which consume bivalves. They inhabit the Arctic and subarctic coasts of the Northern Hemisphere and feed upon different bivalve commu­ nities (Oliver et al., 1983). Walruses excavate mussels from soft sediment by sucking and expelling water and by movements of their snout (Oliver et al., 1985; Dame, 1996). They compete with bearded seals in some parts of their range. Especially, the

295

pacific species of the bearded seal E. barbatus nauticus feeds mainly on mollusks and only predates on fish when it cannot reach the bottoms. A study on the summer diet of the Canadian subspecies E. barabatus barbatus showed that most of the diet consists of fish such as polar cods, sculpins, and eelpouts.

6.13.3 Food-Web Case Studies of Mussel Beds in the North Sea and the Wadden Sea 6.13.3.1 Ecological Carbon Transfer of Wadden Sea Mussel Beds Among the benthic communities in the Wadden Sea, mussel beds are characterized by high consumption activity and sec­ ondary production per unit of area. The food requirement by the community exceeds autochthonous primary production due to the high density of suspension feeders and grazers. This imbalance is adjusted by the tidal plankton import from outside, by foraging migrations and probably by shifting to other food resources (i.e., microphytobenthos to juvenile bala­ nids by L. littorea (Buschbaum, 2002), or from phytoplankton to suspended detritus by suspension feeders (Smaal et al., 1986)). High consumption rates of extended mussel beds may lead to diminishing resources within the community. The high accumulation of macrobenthic biomass attracts an array of predators and results in an increased predation pres­ sure particularly on juvenile mussels and the associated fauna of mussel beds. The high predation by birds skims the main part of secondary production of this group.

6.13.3.1.1

Biomass of the dominant compartments

Mussel beds reveal the highest total biomass among the inter­ tidal communities of the Sylt-Rømø Bight with 954.8 g-C m−2. A dense settlement of mussels as well as an extensive cover of macroalgae on top of the mussel aggregations results in the highest heterotrophic and autotrophic biomass within this community and within boreal intertidal areas (Table 1). The heterotrophic biomass is dominated by the biomass of M. edulis which occupy 79.8% of the total biomass and 94% of the heterotrophic biomass. The share of F. vesiculosus in total and autotrophic biomass is 15% and 99%, respectively.

6.13.3.1.2

Primary production: Gross primary production

About 5378 mg-C m−2 d−1 is produced by the plants of a mussel bed (Table 1). The main part of this production (98%) is contributed by F. vesiculosus, and microphytobenthos has the balance of 2%.

6.13.3.1.3

Net primary production

Approximately 3998 mg-C m−2d−1 is converted into plant bio­ mass by primary production, which is about 74% of the gross primary production (Table 1). Grazing on macroalgae is low; only 5% of the available production is directly consumed mainly by crustaceans and most of plant production is stored in the system until winter when storms rupture the Fucus thalli and export the largest part of the plant production from the system to the beach. In contrast to grazing on macroalgae, grazing on microphytobenthos is immense due to the high biomass of L. littorea in mussel beds. This leads to a shortage of microphytobenthos production in mussel beds in the order of about 300 mg-C m−2d−1. To balance this carbon debt,

296

Food Web of Intertidal Mussel and Oyster Beds

Table 1

Biomass and energetic of all compartments in flow networks of the mussel bed subsystem of the Sylt-Rømø Bight

Mussel bed

Biomass (mg-C m−2)

GPP (mg-C m−2 d−1)

NPP (mg-C m−2 d−1)

Respiration

Autotrophic compartments Microphytobenthos Macroalgae (Fucus spp.) Total autotrophs

130.00 146236.00 146366.00

98.63 5279.10 5377.73

64.41 3933.70 3998.11

34.22 1345.40 1379.62

Production (mg-C m−2 d−1)

Respiration (mg-C m−2 d−1)

Egestion (mg-C m−2 d−1)

Consumption (mg-C m−2 d−1)

25.40 16.89 1.81 4.42 4.68 751.30 2.20 5.62 7.32 11.13 32.27 0.10 0.02 0.005 0.0002 0.00 0.04 0.04 24.45 7.00 0.01 0.01 7.50 0.01 121.53 10.96 1034.71

139.86 43.49 17.65 8.41 22.16 4132.30 24.40 18.48 24.00 20.00 55.40 0.35 0.04 0.01 0.0003 0.01 0.12 0.12 953.51 273.15 0.25 0.24 225.00 0.50 192.60 41.70 6193.74

239.22 106.87 8.95 56.29 7.50 690.00 21.70 3.50 4.44 6.32 88.60 0.10 0.34 0.16 0.0009 0.01 0.07 0.07 244.49 70.04 0.06 0.06 60.00 0.14 67.41 19.01 1695.36

404.48 167.25 28.41 69.11 34.40 5573.60 48.30 27.60 35.76 37.43 176.27 0.55 0.40 0.175 0.0014 0.03 0.23 0.23 1222.45 350.19 0.32 0.31 292.50 0.65 381.54 71.67 8923.85

Heterotrophic compartments Littorina littorea Capitellidae Oligochaeta Heteromastus filiformis Gammarus species Mytilus edulis Macoma balthica Balanus crenatus Semibalanus balanoides Small crustaceans Carcinus maenas Crangon crangon Pomatoschistus microps Pomatoschistus minutus Pleuronectes platessa Merlanguis merlangus Gadus morhua Myoxouphalus scorpius Somateria mollissima Haematopus ostralegus Larus ridibundus Larus canus Larus argentatus Other birds Sediment bacteria Meiobenthos Total heterotrophs Total

19337.20 1885.00 661.20 806.00 840.00 761770.00 498.80 1856.40 2496.00 1170.00 6370.00 9.20 1.79 0.47 0.03 0.56 7.5 7.5 9000.00 2043.75 2.29 2.40 2887.50 6.75 625.00 500.00 812785.34 959151.34

Biomass and standing stocks in mg-C m−2, GPP, NPP, P, R, E, and C in mg-C m−2 d−1.

Littorina uses other sources such as juvenile barnacles (Buschbaum, 2002) or migrates from the entire mussel beds to adjacent sand flats during low tide to graze on microphyto­ benthos that is more abundant there (personal observation).

6.13.3.1.4

Consumption

Approximately 8860 mg-C m−2 d−1 is consumed per day by the intertidal mussel bed. Pelagic suspension feeders consume about 5597.8 mg-C m−2 d−1 (Table 1). This is 63% of the total consumption of the community and shows the high depen­ dency of mussel bed on the overlying water. The consumption also exceeds the production of the phytoplankton over a mus­ sel bed by 4511 mg-C m−2 d−1 and demonstrates that mussel beds in the intertidal area are only supported with enough food when the tidal water imports rich phytoplankton biomass produced in the contiguous Wadden Sea or from the adjacent North Sea. The relation between consumption of imported pelagic material to total consumption of pelagic sources of 0.81 shows a high dependency of pelagic imports. The relation of total allochthonous food sources to total autochthonous

food sources of 1.36 strengthens the importance of imported food for the mussel bed community. The autochthonous food consumption must be seen in relation to trophic levels and production of the heterotrophic organisms. However, the above-mentioned ratios for consumption give us a quantitative parameter for the openness or closeness of an ecosystem.

6.13.3.1.5

Heterotrophic production

Heterotrophic production of a mussel bed community amounts to 1022 mg-C m−2 d−1. Most of the heterotrophic production is due to the second trophic level because of the prevalence of M. edulis and L. littorea in this system, which depends mainly on phytoplankton and detritus or microphytobenthos, respectively. However, secondary production is high and reveals the highest values among all investigated intertidal communities. Predation pressure on M. edulis, M. Balthica, and C. maenas is very high so that the production rates of these species were exceeded by 910, 93, and 55 mg-C m−2 d−1, respectively (Baird et al., 2007). This could be a consequence of the relatively low areal extent of mussel beds which probably leads to an overexploitation by their predators.

297

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P/B ratio day–1 of subsystem

Food Web of Intertidal Mussel and Oyster Beds

Community Figure 1 P/B ratio per day of the dominant intertidal communities of the Sylt-Rømø Bight.

Community respiration of mussel beds amounts to about 7530.88 mg-C m−2 d−1 and is exported from the system. This process is considered within the budgets of exchange processes.

species including eider ducks, oystercatchers, and herring gulls. The tertiary consumers are mainly represented by preda­ tory fishes such as whiting (M. merlangus) and sea sculpin (M. scorpius). Three species were included in the model at this trophic level. The consumers of the fourth level are mainly represented by the above-mentioned predatory fish species feeding to a small degree on smaller specimen at the tertiary consumer level, even on their own species. In general, seals, harbor porpoises, and cormorants, as well as terns, should also appear partly in this trophic level but were not included because of the lack of empirical data and thus in the model. It is also unknown whether these predate on the mussel-bed community.

6.13.3.1.8

6.13.3.2.2

6.13.3.1.6

Production to biomass ratio

Mussel beds show a very low production to biomass ratio of only 0.005 (on a daily basis) which is the lowest P/B ratio found among the intertidal communities in the Sylt-Rømø Bight (Figure 1). This is mainly because the main biomass is due to animals of older age groups showing low individual P/B ratios compared to juvenile specimens which have larger individual P/B ratios (Baird et al., 2007)

6.13.3.1.7

Respiration

Excretion

Whether community excretion is an exchange process depends on the system and on the element the ecological transfer is based upon. In mussel beds, C-excretion products like feces are mainly accumulated between the mussels and lead to elevation of the community in relation to the adjacent sediment. Thus, the excretion is accumulated within the detritus pool of the community. In total and including plant detritus production, 1763 mg-C m−2 d−1 is produced by a mussel bed (Baird et al., 2007). Most of the excreted C (86%) is recycled especially on the second trophic level.

6.13.3.2 6.13.3.2.1

Trophic Analysis of Mussel Beds Diversity and biomass of trophic groups

In mussel beds, up to five trophic levels including the primary production level can be identified. The biomass of secondary producers consists mainly of M. edulis followed by L. littorea. The food-web model constructed here includes eight species that con­ tribute mainly to this trophic group with biomasses larger than 0.1 g-C m−2 species. Species other than M. edulis, L. littorea, Capitella, Oligochaeta, Macoma, and Jaera (included in small crus­ taceans) are using primary producers or detritus only partly as food but feed mainly at higher trophic levels. Bacteria and meio­ fauna species also contribute to the secondary producer level, but their diversity in mussel beds is unknown. Within the secondary consumers, species diversity is higher and includes crustaceans, fishes, and birds. In the food-web model, 15 species were included with G. locusta and C. maenas representing crustaceans, seven fish species, and five bird

Total system throughput (TST)

The total system throughput is a measure of system size and represents the sum of all internal and exogenous inputs to the system compartments. Mussel beds contribute 41.5% to the daily production on a m2 basis of all investigated intertidal communities (Baird et al., 2007). They are thus areas of high activity indicated by the highest amount of C transported along the food web in a given time compared to the other commu­ nities. The total system throughput is estimated to be 33 571 mg-C m−2 d−1 (Table 2). The high rates of productivity of F. vesiculosus and the high activity of invertebrate and verte­ brate predators are largely responsible for the high total system throughput (TST) in mussel beds (Baird et al., 2007).

6.13.3.2.3

Average path length (APL)

The average path length of a food web of a community is a system descriptor that measures the average number of com­ partments that a unit of C passes through from its entry into the system before it leaves it. The APL is expected to be longer in systems with high degree of flow diversity and cycling (Christensen, 1995; Thomas and Christian, 2001). On average, a unit of C passes 1.94 compartments before it leaves a mussel bed. This means that short cycles prevail in a mussel bed in spite of the high flow diversity and the large number of cycles in this system.

6.13.3.2.4

Average residence time (ART)

Although APL is short, the material and energy appear to reside for a much longer time (ART = 84 days) in a mussel bed com­ pared to other systems. The organic material deposited onto the

298

Food Web of Intertidal Mussel and Oyster Beds

Table 2 Global system attributes derived from network analysis for the mussel bed subsystem of the Sylt-Rømø Bight System attributes

Mussel beds

Trophic efficiency (logarithmic mean, %, Sed POC retained) Detrivory (detritus pool to TL2, mg-C m−² d−1, Sed POC retained) Detrivory:herbivory ratio (D:) Number of cycles (Sed POC retained) Finn cycling index (%) Average path length (APL = TST-Z/Z) Ave residence time (ART; days)(Sum Biomass/sum exports, Resp) Total system throughput (mg-C m−² d−1) Total system throughput (tonnes-C area−1 d−1) Development capacity (mg-C m−² d−1 bits) Ascendency (mg-C m−² d−1 bits) Relative ascendancy (A/DC, %) Average mutual information (A/TST) (normalized A) Average internal mutual information (Ai/TST) Overheads on imports (mg-C m−² d−1 bits) Overheads on exports (mg-C m−² d−1 bits) Dissipative overheads (mg-C m−² d−1 bits) Redundancy (mg-C m−² d−1 bits) Relative redundancy (R/DC, %) Normalized redundancy (R/TST) Internal development capacity (mg-C m−² d−1 bits) Internal ascendency (mg-C m−² d−1 bits) Relative internal ascendency (Ai/DCi, %) Internal redundancy (mg-C m−² d−1 bits) Relative internal redundancy (Ri/DCi, %) Flow diversity DC (DC/TST, %) (normalized DC) ΦSum of overheads/TST (+#58) Overall connectance Intercompartmental connectance Food-web connectance (living compartments only) GPP/TST

14.92 1523 0.3:1 173 2.53 1.94 83.73 33571 12.1 135620 67521 49.8 2.01 0.91 17781 2690 23590 24034 17.7 0.72 54659 30624 56.0 24034 44.0 4.04 2.23 1.55 1.78 1.29 0.16

Values reflect results from network analysis where excess production and sediment POC were not exported from the subsystems. In compartments where predation exceeds production, no artificial imports were made to balance the compartment. Modified from Baird, et al. 2007. Trophic dynamics of eight intertidal communities of the Sylt-Rømø¸ Bight ecosystem, northern Wadden Sea. Marine Ecology Progress Series 351, 25–41.

mussel bed contributes to the long ART calculated for this system. This material is only removed during strong storms especially those from easterly directions.

6.13.3.2.5

Lindeman spine

The relation of production efficiencies between the trophic levels is shown in Table 2. The energy transfer can be computed by the Lindeman spine, which gives the food web as a conca­ tenated flux through all trophic levels and allows determination of the actual number of trophic levels within the community as well as to estimate the energy transfer, loss, and import from outside (Figure 2). The highest efficiency of energy transfer among the heterotrophic compartments is in the second level. In the third trophic level, energy transfer is very low with only 3.4%, but at the fourth trophic level it increases again to 10%. This is due to better efficiencies of higher-level predators such as birds and fishes, compared with predators on a lower level such as shore crabs, which may cause a bottleneck for the energy flow in this community.

6.13.3.2.6

Mean trophic efficiency

The logarithmic mean of the trophic efficiencies of the mussel bed is the highest (15%) among all intertidal communities investigated (Baird et al., 2007). Mussels are the main second­ ary producers and also the main food for predators in this system. Thus, the short food cycle from primary production of phytoplankton to mussels to birds is a dominating pathway within the food web and is responsible for the high trophic efficiency of the system.

6.13.3.3

Structure and Magnitude of Cycling

The cycling of energy and material is an inherent and universal process in all natural ecosystems that contribute to their auton­ omous behavior. Cycling occurs through a number of cycles of different path lengths.

6.13.3.3.1

Number of cycles

The number of cycles in the mussel beds is 173. Because of the dependency of mussel beds on phytoplankton input from

Food Web of Intertidal Mussel and Oyster Beds

299

Mussel beds 20.4

3740

10548

I 52.6%

79

5350

2471

II 30.0%

3613 1523

852

1180

2060

37.8

64.7

III 3.4%

1472

485

1.1

IV 10.0% 40.5

6.47

17

0.14

V 10.0% 4.33

0 VI

2

1684

Figure 2 Lindeman spine of an intertidal mussel bed of the Sylt-Rømø Bight. The box indicated D refers to the detrital pool, and the Roman numbers in the boxes of the Spine to discrete trophic levels. Percentage values in Spine boxes refer to the efficiency of energy transfer between the integer trophic levels.

outside, the number of cycles is lower compared to commu­ nities where most of the community is based on detritus or microphytobenthos.

6.13.3.3.2

Cycle distribution

In mussel beds, 11% of cycling takes place over longer path­ ways involving 4–6 compartments. Especially, the important role of top predators (birds and cod, whiting and sea sculpin) is reflected in these comparatively long cycles.

6.13.3.3.3

Finn cycling index

The amount of material cycled in each system is expressed as a fraction of the total system throughput in the Finn cycling index. The Finn cycling index is lowest in mussel beds. Little material is recycled in the mussel beds because of the high TST, which can be ascribed to the high F. vesiculosus production, little utilization of it, and its subsequent export from this system.

6.13.3.4 6.13.3.4.1

System Level Properties and System Organization Development capacity (DC)

The development capacity is a measure for the maximum number of potential fluxes and interactions which can be rea­ lized within a system. In the mussel bed, DC is highest compared to other intertidal communities of the Sylt-Rømø Bight (Table 2) (135 620 mg-C m−2 d−1 bits). The DC splits up into ascendancy which gives the realized structure of a system and the system overhead, which is the sum of the overheads of import, export, respiration, and redundancy. The system over­ head reflects the reserve strength of a system to counter perturbations. The higher the overhead of export and import, the more dependent is a system from external sources. In mussel beds, about 13% of the system overhead is due to imports from outside, which shows a high dependency from external sources compared to other communities of the SyltRømø Bight (range 3–9.6%).

6.13.3.4.2

energy and material transfers on the other hand can act as a buffer or reserve, should external perturbations occur and in changes in biodiversity. It is postulated that a sustainable sys­ tem requires a balance between ascendancy and redundancy. In mussel beds, the redundancy to ascendancy relation is 1.8:5, which shows that redundancy is too low for a sustainable and stable system probably because of the lack of parallel pathways. If both properties are balanced, then the system can draw activity from the overhead to keep it in operation, but at a less organized state.

Redundancy

Eighteen percent of system overhead is due to redundancy. A system with low redundancy is considered to be susceptible to external perturbations which may affect the trophic interac­ tions between system components. Parallel pathways of

6.13.3.4.3

Ascendancy

Ascendancy measures the efficiency and definitiveness by which energy transfers are made, whereas the overhead quan­ tifies how inefficient and ambiguous the system performs on average. Higher indices of ascendancy reflect increased ecologi­ cal succession characterized by, for example, species richness, decreased costs of overheads to the system, greater internaliza­ tion of resources, and finer trophic specialization. Fifty percent of the DC is realized as ascendancy in intertidal mussel beds which, thus, can be interpreted as having well-organized func­ tions of energy transfers. The internal relative ascendency is a function of internal exchanges only. If this ratio decreases compared with the relative ascendancy, then the system becomes more dependent from external than internal sources. Although we have seen that mussel beds are largely dependent on external phytoplankton as food, the internal relative ascen­ dancy increases compared with the relative ascendancy by 6.2%. The high in situ production of F. vesiculosus which uses internally produced nutrients for growth could explain this increase.

6.13.3.4.4

Average mutual information (AMI)

AMI or normalized ascendancy is highest in the mussel bed subsystem at 2.01 compared to other communities of the SyltRømø Bight. This index is indicative of the level of inherent organization and the degree of specialization. The high TST of mussel beds is mainly due to F. vesiculosus, which does not contribute much to the flow structure since only few species feed on it. However, the high AMI as well as the high A/DC or Ai/DCi can be ascribed to an inflated ascendancy, which is enhanced by high system activity due to the size of flows

300

Food Web of Intertidal Mussel and Oyster Beds

associated with F. vesiculosus. The low value of the GPP to TST ratio in mussel beds of 0.16 demonstrates the influence of F. vesiculosus to the system, once its high system throughput is removed.

6.13.3.4.5

Flow diversity

Flow diversity or relative ascendancy measures both the num­ ber of interactions and the evenness of flows in the food web, and is thus a much more dynamic concept than species diver­ sity. Comparatively higher values of this index indicate an increase in interactions and a lower degree of unevenness and variability in the flow structure. In intertidal mussel beds, flow diversity is 4.04 below the mean of all intertidal communities (4.33). This shows that most material is transported via path­ ways that are due to organisms, such as Fucus and Mytilus, which dominate the biomass of the system and create, in this way, an unevenness in flows.

6.13.3.4.6

northern part (1.5:1000 vs. 1.8:1000 and 3.5 vs. 3 km, respec­ tively). Current speeds average 0.2–0.6 m s−1 (SHOM, 2001). The mudflat was considered as composed of 97% of ‘free’ mudflat, 2% of mussel cultures, and 1% of oyster racks. The aim was to highlight emergent properties of food-web functioning in these two ecosystems and to compare these properties with other coastal ecosystems. Both ecosystems imported detritus in parallel to a high benthic primary produc­ tion. They were characterized by a high diversity of resources. Both also exported living material, leading to a high quality production. This export was mainly composed of cultivated bivalves during the cold season for Brouage Mudflat, and of the migration of grazing fish in Aiguillon Cove during the warm season. Their internal organization was characterized by short pathways, high recycling, high redundancy, and low net ecosystem production, compared to the other systems selected. These characteristics, encountered in many estuaries, presented less extreme values.

Connectance indices

The effective number of connections between compartments is given by three connectance indices and is derived from the logaveraged number of links calculated from the system overhead. The overall connectance includes the effect of external transfers. The internal connectance index characterizes only internal exchanges, whereas the food-web connectance index refers only to transfers among living compartments in the system. In mussel bed, all three connectance indices are lowest com­ pared with the other benthic communities. Connectance is higher when external sources as well as abiotic material are included in the considered web. The low food-web connec­ tance may be explained by the dominance of old mussels (storage compartment for C) linked only to the phytoplankton compartment and by a comparatively small through-flow com­ partment consisting of younger mussels as well as associated fauna, which is of less biomass and linked closely to birds and fishes, that exert a high predation and export of C from the system.

6.13.4 Food-Web Case Studies of Oyster Beds at the French Atlantic Coast Network analysis has been used to analyze steady-state models of the food webs of two intertidal mudflat ecosystems on the South-Western Atlantic Coast of France: Aiguillon Cove and Brouage Mudflat (Leguerrier et al., 2007). These food-web analyses have not been directed to the community level, such as to a certain oyster or mussel bed, but are considering large geographical units that includes oyster beds and mussel beds. The Brouage Mudflat is located on the eastern part of the Marennes-Oléron Bay. It covers 40 km2 (Gouleau et al., 2000), with a flat-bottom slope (1:1000) and a very wide (4.5 km) tidal area. The current speed varies from 0.2 to 0.6 m s−1 (Bassoullet et al., 2000; Le Hir et al., 2000). Oyster culture on racks covers 16% of the intertidal area, located on the lower part. The Aiguillon Cove is a large intertidal area (Verger, 1968), constituted mainly of large mudflats (33 km2) and surrounded by salt marshes (11 km2). This cove is a semicircular sedimen­ tation basin for silts and clays (Verger, 1968). It has a gentler bottom slope and a larger mudflat on the southern than on the

6.13.5 Food-Web Case Studies of Oyster Beds at the American Atlantic Coast The food web of an intertidal oyster bed of the species C. virginica has been analyzed by Dame and Patten (1981) by using input–output flow analysis, a technique that is included in the modern Ecological Network Analysis routine. They described the oyster bed as a strongly heterotrophic system utilizing tidal energy to bring food in and carry away waste material. The energy or material deposited by the filter feeders is processed by the sediment subsystem, including different organisms such as bacteria, meiofauna, and endobenthic deposit feeders. The sediment system increases the efficiency of the material or energy utilization by the reef as a whole. The detailed internal structure of the system shows the separation of the filter-feeder component from the rest of the system because no feedback energy flows to the filter feeders occurred from other components of the system. Approximately 11% of the energy moving through the reef system is cycled, and this happens predominantly in the sediment system, especially in the detritus compartment of the oyster bed. The recycling effi­ ciency of each compartment is highest in the deposited detritus and the meiofauna component, but was significant in the deposit feeders and microbiota. These components are also deeply embedded in the food web. It appears the majority of the energy and material is flowing through the oyster compo­ nent of the oyster reef, but these flows are only surficial and not deeply embedded in the food-web networks. This confirms the low APL of the oyster reef food web of only 2.02. Predators have a dominant function in controlling the whole system. Especially, the Atlantic mud crabs act as the major predator of the oysters and thus are able to reduce the amount of energy/ matter entering the deposited detritus component. Via energy flow this crab may control over the microbiota and meiofauna, and this may also control the deposit feeders. Because preda­ tors are resource limited, they are controlled by filter feeders and deposit feeders. In general, this food-web analysis shows that flow analysis may allow a much more detailed picture of energy/matter flow in an intertidal oyster reef. Important components and flows are more clearly recognized through this approach and the

Food Web of Intertidal Mussel and Oyster Beds

structural and functional reasons for their importance are sug­ gested. This may lead to a better understanding of ecological systems.

6.13.6 Role of Suspension-Feeder Assemblages in Coastal Food Web To show the role suspension feeders play on a system level, we have to extrapolate their functional role from the community level to the level of total ecosystems. At the level of the ecosys­ tem, the energy flow of the intertidal part of the Sylt-Rømø Bight has been described as a system of high ecological pro­ ductivity and activity (Asmus and Asmus, 1990, 1998, 2000, 2005). The Sylt-Rømø Bight not only shows comparable char­ acteristics and functionality with other estuarine and coastal ecosystems (Baird et al., 2004), but also exhibits unique com­ munity properties and rates of productivity. Primary productivity in the Bight is high and is approxi­ mately equal to pelagic and benthic production at the total system level (Asmus et al., 1998). Focusing on the intertidal region only, benthic primary production surpasses pelagic pri­ mary production. The autochthonous pelagic primary production is not sufficient to meet the energy requirements of the suspension feeders; thus, an additional import of North Sea phytoplankton is necessary. This supporting import has been described for the Wadden Sea and similar coastal systems (Baird et al., 2004, 2007). The magnitude of this import is, however, not precisely quantified even not for other estuaries and coastal systems (Nixon, 1980; Alongi, 1998; Ridd et al., 1988; Odum, 2002; Wolanski, 2007). However, to meet the requirements of the suspension feeders of the system, an import of at least 140 mg-C m−2 d−1 is required (Baird et al., 2004, 2007). In addition to phytoplankton, detritus is produced in the coastal zone of the North Sea and is transported into the Wadden Sea supporting its food web (Straaten and Kuenen, 1957; Groen, 1967; Postma, 1967, 1981; Austen et al., 1998). To what extent the Wadden Sea food web depends on the imported phytoplankton and detritus is indicated by the dom­ inance of suspension feeders in most benthic assemblages of the system (Asmus and Asmus, 2005). Mussel beds reveal a low areal coverage but control the seston input into those assem­ blages situated further landward (Asmus et al., 1990). As in most other ecosystems, secondary producers are the dominant consumer group in the energy flow of the SyltRømø Bight. Here, this group includes a broad range of organ­ isms from bacteria, meiobenthos, zooplankton, macro-invertebrates to herbivorous fishes and herbivorous birds. Regarding biomass, most benthic invertebrates are sus­ pension feeders followed by benthic detritus feeders and benthic grazers. Including the detritus-feeding consumers among the suspension feeders, the detritus feeder to grazer ratio is 1.44:1 (Baird et al., 2004). The energy transfer between primary and secondary consumers is characterized by a low trophic efficiency (Baird et al., 2004, 2007). This is deter­ mined by a low use of the rich microphytobenthos production by consumers and by an overexploited autochtho­ nous primary production of phytoplankton which requires allochthonous auxiliary import.

301

Higher trophic levels include macro-invertebrates, fishes, and birds. There is a remarkable bottleneck between the sec­ ondary producers and the higher trophic levels, indicated by a minimum trophic transfer within tertiary producers compared to higher trophic levels. This can be ascribed to the relatively high returns to the detrital pool at this group (Baird et al., 2004, 2007). There is only little energy transported within trophic levels higher than level 3.

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