The Use of Benthic Suspension Feeders to Mitigate Eutrophication in Coastal Ecosystems



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The Use of Benthic Suspension Feeders to Mitigate Eutrophication in Coastal Ecosystems

Lynn Ficarra

Introduction

According to Nixon (1995), eutrophication is “an increase in the rate of supply of organic matter to an ecosystem.” Nutrient enrichment is a major component of eutrophication in coastal systems. Nitrogen and phosphorus are especially important nutrients that have anthropogenic sources including land clearing, fertilizer, human waste, animal production, and fossil fuel combustion (Nixon 1995). Nutrient enrichment in coastal waters can cause phytoplankton blooms that block sunlight and reduce benthic primary production (Paerl 1988). Phytoplankton cells that die sink to the bottom to fuel microbial respiration (Diaz and Rosenberg 2008). The decreased benthic primary production coupled with increased microbial respiration leads to declining dissolved oxygen levels and thus, hypoxia or anoxia (Paerl 1988). Reduced benthic vegetation and hypoxia are two consequences of eutrophication that can negatively impact community structure in coastal aquatic ecosystems (Rice 2001).

Urban estuaries such as the Neponset River Estuary in Boston, Massachusetts are susceptible to eutrophication via industrial wastes, sewage outflow, and runoff from adjacent developed land (Gardner, Chen, and Berry 2005, Tucker et al. 1999). A potential method for managing nutrient levels in enriched estuaries is to establish populations of suspension feeders to filter the water. Many suspension feeders are benthic and largely sedentary (Levinton 1972). They include bivalves, tunicates, cnidarians, sponges, and some polychaete worms. These organisms strain plankton, dissolved organic matter, organic aggregates, and bacteria either actively or passively from their flowing water medium (Ruesink et al. 2005, Gili and Coma 1998, Levinton 1972). The amount of food consumed by these organisms is based on their filtration rate and efficiency of particle retention (Riisgard 1988). Filtration rate in suspension feeders varies depending on the species, the size of the individual, the velocity of the water, the water temperature, and other factors (Comeau et al. 2008, Rice 2001, Eastern Oyster Biological Review Team 2007).

In this paper, I will evaluate the filtration rate and particle retention efficiency of various bivalves and assess if there is an optimal species for water quality control. Then, I will outline important biological and environmental requirements of the superior filter feeding species. Next, I will discuss studies that support the usefulness of benthic filter feeders to combat eutrophication. Finally, I will explore possible negative impacts of introducing bivalves to coastal ecosystems.


Bivalves

Suspension feeding bivalves play an important role in benthic-pelagic coupling by filtering the water column and transporting materials to the benthos (Doall et al. 2008). These organisms use gills composed of parallel filaments with specialized ciliary tracts to pump water and to capture particles (Riisgard 1988). Collected particles are sorted and eventually expelled either as feces (digested particles) or pseudofeces (rejected particles) which are released to the sediment surface as mucus-coated aggregates (Newell 2004). Filtration rates in suspension feeders vary based on many factors including the species, the size of the individual, the velocity of the water, and the water temperatures (Comeau et al. 2008, Rice 2001, Eastern Oyster Biological Review Team 2007). This makes it difficult to accurately compare the filtering efficiencies of different bivalves.

To determine which bivalves have the highest filtering capacity, Riisgard (1988) measured the filtration rate and particle retention efficiency of Geukensia demissa (Ribbed mussel), Spisula solidissima (Atlantic surfclam), Brachiodontes exustus (Scorched mussel), Mercenaria mercenaria (Northern Quahog), Crassostrea virginica (Eastern oyster), and Argopecten irradians (Bay scallop). Riisgard (1988) found that C. virginica had the highest filtration rate, A. irradians and G. demissa had rates that were close to C. virginica, B. exustus and S. solidissima had intermediate rates, and M. mercenaria had the lowest filtration rate (Table 1). All six organisms were able to retain 100% of the particles that were 4-5 µm or larger in size. G. demissa, S. solidissima, B. exustus, and M. mercenaria retained about 35-75% of particles that were approximately 2 µm in size. C. virginica retained about 50% and A. irradians retained only 15%. From these results, the oyster C. virginica and the mussel G. demissa appear to perform slightly better than the rest of the bivalves in this study.

Gili and Coma (1998) compiled particle capture rate data (expressed in organic carbon units) for organisms within several phyla (Table 2). Among the bivalves in this study, the mussel Aulacomya ater, the Iceland scallop Chlamys islandica and the eastern oyster Crassostrea virginica have the highest particle capture rates. From the two bivalve studies discussed here, oysters and mussels appear to be good candidates for filtering coastal estuaries. Because they are both native to the Neponset Estuary region, I will use the oyster Crassostrea virginica and the mussel Mytilus edulis to continue this discussion (Ruesink 2005, Zagata et al. 2008).


Eastern Oyster

The eastern oyster Crassostrea virginica is a sedentary, reef-building, epifaunal, bivalve mollusk that is naturally distributed along the Atlantic coast of the United States (Ruesink 2005). In the coastal waters of the Mid-Atlantic States, C. virginica generally inhabits depths between 0.6 and 5 m (MacKenzie 1996). The optimal water temperature for the species ranges 20-30°C (Stanley and Sellars 1986). They can survive freezing and warm (>45°C) temperatures, but their feeding rate will be affected (Galtsoff 1964, Shumway 1996). Larvae must experience a minimum water temperature of 17.5°C to survive and develop, but 20-32.5°C is optimal (Hofstetter 1977, Calabrese and Davis 1970). Adults can survive at salinities from 5-40 ppt and larvae can survive at 10-27.5 ppt (Eastern Oyster Biological Review Team 2007, Shumway 1996). The eastern oyster required a dissolved oxygen level from 20-100% saturation and larvae need a pH of 6.75-8.75 (Eastern Oyster Biological Review Team 2007, Calabrese and Davis 1966). Larvae tend to need hard substrate on which to settle while adults can survive in muddy environments (Eastern Oyster Biological Review Team 2007).

Estimates of the filtration rate and particle retention efficiency of Crassostrea virginica vary widely. According to Nelson (1938), a C. virginica individual can filter up to 26 L h-1 under ideal conditions. The Eastern Oyster Biological Review Team (2007) reported that rates vary from 1.5-10 L h-1g-1 dry tissue and they can capture particles ranging in size from 1-30 µm. According to Brusca and Brusca (2003), C. virginica can process up to 37 L h-1 at 24°C and can capture particles as small as 1 µm in size. At 24°C, Pechenik (2005) reported that an individual moves 30-40 L of water past its gills each hour. In an experiment involving 200 oysters (about 35 mm valve height) within mesocosm tanks, Pietros and Rice (2003) estimated a filtration rate of 55 L/individual/day. The authors reported their estimate to be high relative to literature values and adjusted their estimate to 15 L/individual/day based on Powell et al. (1992). These rate estimates demonstrate the difficulty of establishing standard rates of filtration for suspension feeders.

Blue Mussel

The blue mussel Mytilus edulis is a sedentary, epifaunal bivalve that is widely distributed and can be found from southern Canada to North Carolina (Zagata et al. 2008). This species is well acclimated to temperatures between 5 and 20°C, but can survive for extended periods in freezing water and up to 29°C (Goulletquer 2012). They can also survive low salinities from 4-18 ppt, but growth rates decrease below 18 ppt (Goulletquer 2012). M. edulis exists in depth ranges of 1-10 m and typically requires hard substrate such as the rocky intertidal, though they can form mussel beds by growing on top of each other in loose substrate (Zagata et al. 2008). Bayne and Widdows (1978) determined the filtration rate of M. edulis to be 1.34-2.59 L h-1. Winter (1973) found that filtration rate in mussels increases with body size. On average, mussels with shell lengths of 8.5 mm filtered algal cells out of water at a rate of approximately 20 ml h-1 whereas mussels with shell lengths of 56.5 mm filtered at a rate of about 1300 ml h-1. Winter (1973) also found that halving the algal concentration approximately doubled the filtration rates. These data show how filtration rates can be influenced by many factors.
Oyster versus Mussel

Comeau et al. (2008) compared the filtration rates of the blue mussel Mytilus edulis and the eastern oyster Crassostrea virginica at low temperatures. At 9°C, M. edulis obtained significantly higher filtration rates than C. virginica. The average rate for M. edulis at 9°C was 1.82-2.90 L h-1 while a rate of 0.05-1.21 L h-1 was measured in C. virginica. There were similar results at 4°C, but sample sizes were too small for statistical comparisons. In optimal conditions, C. virginica filtration rates are generally faster than M. edulis. In cold temperatures, howerver, it may be more valuable to have populations of M. edulis in estuaries where eutrophication is a concern. These results in conjunction with the discussions above suggest that it would be beneficial to use both species in estuary restoration projects.


Other Suspension Feeders

Mytilus edulis and Crassostrea virginica are both native to the Boston Harbor and are capable (though it is not ideal) of settling and establishing populations in the soft-bottom benthos of an estuary. Placing hard structures throughout the estuary would help provide a more optimal settling substratum. Oyster reefs and mussel beds both provide solid biogenic structures necessary for many organisms to settle. As a result, these bivalve assemblages promote high biodiversity (Ruesink 2005). Oyster reefs provide especially large and complex structures to which other suspension feeders (including mussels) recruit. Organisms that recruit to oyster reefs include sponges, hydroids, corals, anemones, tunicates, polychaetes, etc. (Ruesink 2005). According to Gili and Coma (1998), sponges, tunicates, and cnidarians are not insignificant in their filtering capacities (Table 2). In fact, sponges retain up to 80% of suspended particles (Milanese et al. 2003). Despite a relatively low pumping rate, sponges are also capable of capturing miniscule particles, such as bacteria, that other filter feeders may miss (Milanese et al. 2003). According to Pomeroy, D’Elia, and Schaffner (2006) the mean filtering rate of suspension feeders per gram of dry weight at optimal conditions for 44 species (from sponges to ascidians) is 7.8 L g-1h-1.
Case Studies

There have been several studies to determine the effectiveness of using filter feeders to mitigate eutrophication, but there have been few actual experiments involving real introductions and ecosystem responses. Dame and Dankers (1991) measured the uptake and release of materials by mussel beds in the Western Wadden Sea in Holland and the Eastern Scheldt estuary in the Netherlands. They found that chlorophyll a, seston (suspended particulates), and particulate organic carbon were taken up by the mussel bed and ammonium, orthophosphate, and silicate were released from the mussel bed. This study confirms that mussel beds remove materials from the water and release materials as feces or pseudofeces to the benthos.

Gren, Lindahl, and Lindqvist (2009) measured the nutrient contents of farmed M. edulis in the Baltic Sea in Scandinavia and found that 1 kg of live mussels contains about 8.5-12 g of nitrogen, 0.6-0.8 g of phosphorus and 40-50 g of carbon. This study demonstrates the uptake by mussels of nitrogen, carbon, and small amounts of phosphorus from the water. In Liverpool, mussels were introduced to a series of docks in permanently eutrophic waters that occasionally experienced harmful algal blooms. Allen and Hawkins (1993) found that two years after the mussels were introduced, the water quality and oxygen content of the water column and sediment improved.

Dame and Prins (1998) calculated the clearance time (time it takes for all bivalves in a system to filter particles from a volume of water equal to that of the system) of bivalves and the turnover rates of water and phytoplankton primary production in 11 coastal and estuarine ecosystems (Table 3). They found that Carlingford Lough, Chesapeake Bay, and Delaware Bay have very long bivalve clearance times (480.2, 325, and 1278 days respectively) due to small filter feeding bivalve populations. According to Newell (1988), the pre-1870 oyster population in the Chesapeake Bay could filter the entire water column during the summer in 3-6 days. Since 1870, oysters have been heavily exploited and populations have declined. Around 1988 when Newell wrote this paper, he estimated that the present oyster stocks could filter the bay in 325 days. These studies show how drastically oyster populations can affect their ecosystem. Transplant studies should be done in order to measure actual effects of bivalves on eutrophic systems.


Negative Impacts

In addition to the positive effects that increased water filtration can have on coastal ecosystems, factors that may have negative impacts must be evaluated. Oysters (and other filter feeders) change the physical and chemical environment of the ecosystem that can lead to altered food webs, species interactions, faunal assemblages, sedimentation patterns, and water flow dynamics (Ruesink 2005). While oyster reefs benefit many organisms, they may also exclude others through competition (Ruesink 2005). Suspension feeding organisms introduced from other areas may also be important vectors for invasive species and disease pathogens (Ruesink 2005). There are many factors to take into account when planning a management strategy to counter coastal eutrophication.

Shellfish populations in eutrophic waters may be toxic if consumed by humans. When harmful algal blooms, heavy metals, and other toxins exist in the water column, bivalves will filter them out and incorporate them into their tissue (MacKenzie et al. 2004). Marine algal toxins incorporated into shellfish account for at least four toxic syndromes in humans: paralytic shellfish poisoning, neurotoxic shellfish poisoning, diarrhetic shellfish poisoning, and amnesic shellfish poisoning (Dolah 2000). In coastal ecosystems, poachers may remove and consume contaminated shellfish. To reduce the likelihood of this, ecosystems known to contain toxins should be posted with warnings not to consume shellfish.

Another concern about introducing non-native shellfish species is that they may carry disease pathogens that are foreign to native organisms. An Asian oyster Crassostrea ariakensis has been considered for introduction to Virginia and Maryland for aquaculture purposes (Moss et al. 2007). Moss et al. (2007) conducted a pathogen survey on C. ariakensis using DNA analyses and histopathology tests. They found several protistan parasites, two of which are not found in U.S. waters, several viruses, and cestodes. This study exposes the risks associated with non-native introductions.

Non-native bivalves introduced to a new area may result in species invasion. The bivalve itself may become invasive, or species hitchhiking on the bivalves may be released into the new region and become invasive (Ruesink 2005). The two species that I suggest for oyster restoration are both native to the east coast. The use of natives prevents any issues that could arise from invasives. Unfortunately, non-native oysters are being considered for the Chesapeake Bay because Crassostrea virginica populations have been dwindling since the late 1800s (Moss et al. 2007., Newell 1988) To avoid problems with introducing invasive species, C. virginica populations should be revived, or other effective native filter feeders such as M. edulis should be seeded into the bay.

Finally, Dame and Prins (1998) suggest that restoration of oysters to the Chesapeake Bay may not improve water quality because oysters have been functionally replaced by other bivalves and deep portions of the bay are not available to the bivalves due to anaerobic conditions. If this is true and oyster restoration will not improve water quality, then attempts to establish more bivalve populations will be a waste of money and management effort.

Conclusions

Bivalves are filter feeders that remove particles and nutrients from the water, which can help combat eutrophication and promote water clarity. Mytilus edulis and Crassostrea virginica are especially effective filter feeders as determined by their high filtration rates and particle retention efficiencies. Both bivalves produce biogenic structures that promote recruitment and high biodiversity. Other filter feeders such as sponges, tunicates, and cnidarians recruit to biogenic structures provided by the bivalves and contribute to the filtration of the water.



Dame and Dankers (1991) and Gren, Lindahl, and Lindqvist (2009) showed that mussels uptake nutrients and carbon from the water and release materials to the benthos. Hawkins (1993) suggested that introduced mussels cleared eutrophic water near docks in Liverpool. Dame and Prins (1998) studied the time it takes for bivalves to filter all the water in 11 different coastal systems. Newell’s calculation of past and present filtering capabilities of Chesapeake Bay oysters emphasizes the importance of benthic filter feeding on water quality. Possible negative consequences of combating eutrophication with bivalves include human illness due to consuming toxic shellfish, introduction of invasive species, vectoring pathogens, and wasting time and money. There is much more to be learned about bivalves as filter feeders, but there is promising evidence for an important role in clearing up nutrient enriched waters.






Filtration Rate (Rank)

Retention of Particles >4-5µm

Retention of 2µm Particles

Crassostrea virginica (Eastern oyster)

1

100%

50%

Geukensia demissa (Ribbed mussel)

2

100%

35-75%

Argopecten irradians (Bay scallop)

2

100%

15%

Brachiodontes exustus (Scorched mussel)

3

100%

35-75%

Spisula solidissima (Atlantic surfclam)

3

100%

35-75%

Mercenaria mercenaria (Northern Quahog)

4

100%

35-75%

Table 1. Data from Riisgard 1988. Relative filtration rate and particle retention efficiency of

six bivalves.





Table 2. From Gili and Coma 1998. Diets and particle capture rates in carbon units of various suspension feeders.


Table 3. From Dame and Prins 1998.Water residence time, phytoplankton primary production turnover, and bivalve clearance time for 11 coastal ecosystems.

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