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Hydrobiologia

, Volume 810, Issue 1, pp 15–27 | Cite as

Ecosystem services provided by freshwater mussels

  • Caryn C. VaughnEmail author
FRESHWATER BIVALVES Review Paper

Abstract

Ecosystem services are the benefits that humans derive from ecosystems. Freshwater mussels perform many important functions in aquatic ecosystems, which can in turn be framed as the ecosystem services that they contribute to or provide. These include supporting services such as nutrient recycling and storage, structural habitat, substrate and food web modification, and use as environmental monitors; regulating services such as water purification (biofiltration); and provisioning and cultural services including use as a food source, as tools and jewelry, and for spiritual enhancement. Mussel-provided ecosystem services are declining because of large declines in mussel abundance. Mussel propagation could be used to restore populations of common mussel species and their ecosystem services. We need much more quantification of the economic, social, and ecological value and magnitude of ecosystem services provided by mussels, across species, habitats, and environmental conditions, and scaled up to whole watersheds. In addition, we need tools that will allow us to value mussel ecosystem services in a way that is understandable to both the public and to policy makers.

Keywords

Biofiltration Biomonitor Habitat modification Hotspot Nutrient cycling and storage 

Humans derive many benefits from ecosystems. These benefits, known as ecosystem services, include provisioning services obtained directly from the ecosystem such as water, food, and timber; regulating services such as water purification, climate control, carbon storage, and pollination; supporting services such as nutrient recycling and storage; and cultural services, which are the benefits that people obtain through tourism and recreation, aesthetic experiences, or spiritual enrichment (Daily et al., 1997). Freshwater systems contribute to many important ecosystem services such as provisioning of clean water, recreation, and ecotourism (Brauman et al., 2007; Dodds et al., 2013). While ecosystem services can be categorized in different ways, this review follows the designations of the United Nations Millennium Ecosystem Assessment (http://www.millenniumassessment.org/en/index.html).

Freshwater mussels (hereafter mussels) perform many important functions in aquatic ecosystems, which have been well described (Vaughn & Hakenkamp, 2001; Strayer, 2008; Vaughn et al., 2008; Haag, 2012). Mussel functions in ecosystems can in turn be framed as the ecosystem services that they provide or contribute towards (Fig. 1; Table 1). Ecosystem services to which mussels contribute include the regulating service of water purification (biofiltration); supporting services such as nutrient recycling and storage, structural habitat, and substrate and food web modification; and provisioning and cultural services including use as a food source, as tools, jewelry and art, and for spiritual enhancement (Table 1). This review deals mainly with mussels in the order Unionoida, although I include some references to the invasive Asian clam, Corbicula fluminea, which in many ways functions similarly to unionids (Vaughn & Hakenkamp, 2001). This review concentrates on North American mussels, because most of the literature is for this region, but I have included information from other regions where it is available.
Fig. 1

Mussel tissue and activities that mussels perform can be translated into ecosystem services that are beneficial to humans

Table 1

Ecosystem service classes, mussel-provided ecosystem services, and the benefits that they provide for humans

Ecosystem service class

Mussel-provided ecosystem service

Benefits for humans

Regulating

Biofiltration

Water quality

Supporting

Nutrient cycling and storage

Water quality

Habitat/habitat modification

Fish habitat

Environmental monitoring

Water quality

Food webs

Biodiversity

Provisioning

Food for other species

Biodiversity

Food for humans

Food provisioning

Products from mussel shells

Pottery, jewelry, art

Cultural

Cultural value

Spiritual benefits

Existence value

Conservation value

Regulating services: mussels as biofilters that purify water

Mussels are powerful filter feeders that remove particles from both the water column and interstitial sediments (Fig. 1) (Vaughn et al., 2008). While it was long thought that mussels fed principally on phytoplankton, recent advances for tracking nutrient assimilation, such as stable isotopes and fatty acids, have shown them to be omnivores whose diet varies with habitat and food availability (Christian et al., 2004; Vaughn et al., 2008; Newton et al., 2013). For example, mussels in small temperate streams feed on a mixture of bacteria and suspended/re-suspended algae (Raikow & Hamilton, 2001), while mussels in large productive rivers feed primarily on phytoplankton (Thorp et al., 1998).

Biofiltration by mussels can remove significant quantities of particles from the water column. In a classic example, Welker & Walz (1998) found that high densities of unionids could remove enough phytoplankton to cause “biological oligotrophication” in the River Spree, Germany. Recently, Pigneur et al. (2014) estimated a 70% loss of phytoplankton biomass and a 61% decline in annual primary production in areas where invasive Corbicula have reached high densities in the River Meuse. Chowdhury et al. (2016) found that mussels in a Bangladesh Lake filtered the lake margins in 21 h, supporting high water clarity despite high nutrient levels. While this is an area of active research, most studies are lab-based, and simply applying laboratory filtration estimates to real mussel assemblages in heterogeneous habitats can be inaccurate. For example, Vanden Byllaardt & Ackerman (2014) found that unionid clearance rates could vary over an order of magnitude in the field depending on hydrodynamic conditions and algal flux. More work assessing filtration rates of natural mussel assemblages under varying conditions is needed.

Biofiltration capacities of mussel assemblages can vary substantially with mussel abundance, species composition, and with environmental conditions such as discharge, temperature, and productivity (Spooner & Vaughn, 2008; Vaughn, 2010). Individual mussel filtering rates are governed by mussel physiology and food availability, among other factors. Mussel species have different, temperature-dependent filtration rates (Spooner & Vaughn, 2008). Thus, the biofiltration capacity of a mussel assemblage can vary substantially with assemblage composition and seasonally with temperature. In addition, mussels adjust their feeding rates based on food concentrations (Bril et al., 2014). Disturbance can also influence biofiltration capacity: Lorenz et al. (2013) found that shear stress from boats can reduce daily filtration rates by up to 7%. Finally, biofiltration capacity is heavily dependent on mussel biomass and the volume and residence time of the overlying water (Strayer et al., 1999). For example, mussel assemblages in a small U.S. river (Kiamichi River, Oklahoma) can process the overlying water multiple times before it flows over them during periods of low summer discharge, but can process only a fraction of the water column during high spring and winter flows (Vaughn et al., 2004; Vaughn, 2010).

Human-engineered systems often lack “natural” ecosystem services. A solution is to reintegrate natural ecosystem services into engineered systems. There is a growing interest in using the natural filtering capacity of mussels to pretreat water for human use. For example, Newton et al. (2011) estimated that mussels in a 480-km reach of the Mississippi River filter approximately 53 million m−3 day−1, while a Minneapolis-St. Paul wastewater treatment plant produces wastewater flows for 0.7 million m−3 day−1. This interest extends to using mussels and other freshwater bivalves to selectively remove disease organisms and contaminants from water supplies, and this is a rapidly growing area of inquiry (Li et al., 2010; Izumi et al., 2012). For example, Faust et al. (2009) found that Corbicula fluminea can remove avian influenza viruses from the water, and reduce infectivity. Ismail et al. (2014) found that Anodonta californiensis and Corbicula fluminea can remove pharmaceuticals, personal care products, herbicides, and flame retardants from the water and either biodeposit or store them in their tissue. This research group also discovered that mussels can actually remove hydrophobic trace organic compounds that cannot be fully removed by conventional wastewater treatment such as ibuprofen and beta blockers. Anodonta californiensis also can remove significant amounts of E. coli from lake water (Ismail et al., 2015). There is also increasing interest in using mussel biofiltration to augment aquaculture. The mussel Diplodon chilensis was used to reduce nutrient loads from salmon farming (Soto & Mena, 1999). Othman et al. (2015) found that filtering mussels reduced bacterial populations by greater than 85% and led to higher growth and lower mortality of farmed Nile tilapia. Of course, while mussels remove contaminants and store them in their tissues or biodeposit them, we know relatively little about the effects of these contaminant burdens on the mussels themselves.

Supporting services: nutrient cycling and storage

Mussels feed on particulate nutrients and convert these nutrients into soft tissue and shell, biodeposits (feces and pseudofeces), and dissolved nutrients (Fig. 1) (Strayer, 2014). Thus, where mussel biomass is high, mussels play an important role in nutrient recycling, translocation and storage, can alter water quality, and potentially can play a role in nutrient abatement.

Mussels excrete soluble nutrients to the water column (Vaughn & Hakenkamp, 2001). These nutrients are readily taken up by algae and heterotrophic bacteria (Fig. 2) (Vaughn et al., 2008; Bril et al., 2014), and cascade up aquatic food webs (see discussion of food webs below). Mussels have been shown to alleviate nutrient limitation and alter algae communities in streams, impacting water quality (Atkinson et al., 2013a). For example, in three rivers in the southern U.S., sites without mussels were nitrogen-limited with approximately 26% higher relative abundance of N-fixing bluegreen algae, while sites with high mussel densities were co-limited (N and P) and dominated by diatoms (Atkinson et al., 2013b). Mussel roles in water column nutrient dynamics are described more thoroughly in Atkinson & Vaughn (2015), Vaughn & Hakenkamp (2001), and Vaughn et al. (2008).
Fig. 2

A Schematic showing that mussel beds are patchily distributed in rivers, separated by areas with no mussels or low mussel abundance. In many rivers, mussel beds will be further apart than shown here. B Potential fluxes in and out of mussel beds (hotspots of biological activity) and other river areas (coldspots)

We understand mussel roles in water column nutrient dynamics much better than we understand their role in sediment nutrient dynamics. Mussels couple the water column and sediment compartments by removing particulate materials from the water column and depositing them to the sediment as feces and pseudofeces (Figs. 1, 2). Mussel biodeposition rates can be quite high. Strayer (2014) has estimated that rates of unionid biodeposition, averaged over an entire lake or river, may be as high as 1–300 mg C m−2 day−1, 0.1–30 mg N m−2 day−1, and 0.03–100 mg P m−2 day−1. However, amounts are likely to be quite variable and we know little about the overall chemical composition of biodeposits. Most biodeposits are likely to be initially concentrated around mussel aggregations (Fig. 2), but then are dispersed downstream depending on sediment and hydrologic conditions. Thus, biodeposits likely represent an important nutrient translocation flux from mussel beds to other stream areas (Strayer, 2014). However, we have a poor understanding of the role and importance of these biodeposits in nutrient dynamics and food web support, and much more research is needed in this area.

Mussel effects on nutrient dynamics are highly context-dependent. First, as with biofiltration, mussels have species-specific, temperature-dependent excretion rates. These differences mean that species composition of mussel assemblages can have large effects on nutrient recycling and storage rates at the scale of river reaches and even entire rivers (Vaughn, 2010; Atkinson et al., 2013b; Atkinson & Vaughn, 2015). Secondly, also like biofiltration, mussel effects are much stronger at baseflow than under high discharge conditions (Atkinson & Vaughn, 2015). Finally, Strayer (2014) suggested that mussels should have much stronger effects in more “pristine” systems, where nutrients are limiting, and this does indeed seem to be the case. In the relatively undeveloped, nitrogen-limited rivers of southeastern Oklahoma, U.S., mussels alleviate nitrogen limitation, shorten nutrient spirals, and mussel-derived nutrients can account for up to 40% of nutrient demand (Atkinson et al., 2013b, 2014c). Spooner et al. (2013) examined how nutrients from mussels affected algae and macroinvertebrates across 14 streams in Ontario that varied in background nutrient loads. In more pristine areas, mussels had strong effects, increasing algal and macroinvertebrate biodiversity. In areas with high nutrient loads, these effects were diminished or lost. In an experiment with Corbicula, Turek & Hoellein (2015) found that these bivalves increased ammonium flux more than N2 production under low nutrient conditions. Under high nutrient loads, bivalves significantly increase both ammonium and N2 flux out of the sediments, either through increased nitrification–denitrification or enhanced exchange of nutrients between the water column and sediments via bioturbation.

Mussels accumulate nutrients in both their soft tissue and shell as they grow. These nutrients are then released as reproductive products (sperm, larvae, and structures that support larvae), via excretion as the result of protein breakdown (catabolism) under stress, via soft tissue decomposition at death, and through long-term shell dissolution (Strayer, 2014). As described above, mussels have different temperature tolerances that affect physiological rates. Thermally sensitive species will catabolize their tissue under high temperatures, leading to higher excretion rates and increased nutrient cycling (Spooner & Vaughn, 2008). Nutrients stored in mussel soft tissue are released at death through decomposition. If mussel deaths occur at a regular interval throughout the year, nutrient release from tissue breakdown may be offset by nutrient uptake by growing animals (“capacitance,” Strayer, 2014). However, mussels are long-lived, and in many cases deaths are synchronous and catastrophic (Haag, 2012). In these cases, mussel death can result in very large nutrient pulses into the ecosystem (Sousa et al., 2012; Bódis et al., 2014; McDowell et al., 2016). Mussels also store significant amounts of nutrients in their shells (Atkinson et al., 2014b; Vaughn et al., 2015), which are released slowly into the ecosystem as shells dissolve (Strayer & Malcom, 2007). These stored nutrients can have important and long-term effects on both aquatic and terrestrial systems. For example, recent work has shown that marine shell middens created by Canadian First Native groups in British Columbia act like a “slow release” fertilizer, increasing calcium and phosphorus in the soil, decreasing soil acidity, and leading to increased forest growth (Trant et al., 2016), and there is no reason to expect that this might not also occur in freshwater mussels. However, whether mussels serve as a short-term nutrient capacitors or longer-term nutrient sinks, these nutrients are retained in the ecosystem and incorporated into food webs rather than being transported downstream (Fig. 2) (Atkinson et al., 2014c). Although nutrients retained in this manner in one river may seem insignificant, summed across multiple watersheds this biological nutrient retention could help mitigate the effects of nutrient pollution (FMCS, 2016).

Mussels should have strong effects on coupled nitrification–denitrification by biodepositing organic material, thus increasing rates of both processes and by bioturbating sediments as they move. Denitrification is a particularly important ecosystem service, because it converts organic nitrogen to molecular nitrogen, moving it back into the atmosphere in an inorganic form. Marine bivalves, freshwater zebra mussels, and Corbicula have all been shown to increase denitrification, depending on the environmental conditions (Bruesewitz et al., 2009; Hoellein & Zarnoch, 2014; Turek & Hoellein, 2015). The effects of dense mussel assemblages on denitrification are an overlooked and potentially significant component of nitrogen removal from aquatic systems (Turek & Hoellein, 2015).

Supporting services: mussels as habitat and habitat modifiers

On a global basis, mollusks add physical structure to the environment via their shells, resulting in biogenic habitat such as oyster reefs (Gutierrez et al., 2003). Freshwater mussel shells provide habitat for other organisms as well as play a role in biogeochemical cycling (Strayer & Malcom, 2007). Rates of shell production and decay depend on the amount of accumulated spent shell material, but can exceed (>10 kg dry mass m−2) (Strayer & Malcom, 2007; Ilarri et al., 2015a, b).

Aggregations of mussels can support more abundant and diverse macroinvertebrate communities than similar habitat without mussels (Beckett et al., 1996; Howard & Cuffey, 2006; Vaughn & Spooner, 2006; Aldridge et al., 2007). Shells themselves provide habitat in otherwise soft sediments, and crevices on shells provide protection from flow and predation. Live mussels support different communities on their shells than dead mussels or stones (Spooner & Vaughn, 2006; Vaughn et al., 2008; Bódis et al., 2014; Ilarri et al., 2015a, b). Algae grow on mussel shells, which attract grazing invertebrates (Francoeur et al., 2002; Allen et al., 2012; Spooner et al., 2012) and cascade up the food web. This phenomenon is described more thoroughly in the section below on mussels’ roles in food webs.

Mussels tend to occur in areas that are more stable under high flows (Strayer, 1999; Gangloff & Feminella, 2007; Zigler et al., 2008; Allen & Vaughn, 2010). Strayer (1999) characterized river reaches with abundant mussels as areas that are protected from severe disturbance by floods with return periods of three to 30 years, and suggested that the patchiness of flow refugia in space therefore causes the patchiness of mussel beds in rivers. Do mussels simply proliferate in these areas or do mussels function as ecological engineers that actively modify sediments to make them more stable, such as been found for other animals such as salmon and caddisflies (Moore, 2006)? It has long been suggested that freshwater mussels stabilize sediment, decreasing downstream transport of labile sediments, and making sediments more favorable for other organisms. Yet, there are not good quantitative data demonstrating this phenomenon. In a mesocosm study, Zimmerman and de Szalay (2007) found that sessile mussels increased sediment cohesion and thus sediment stability, but burrowing activities increased erosion and destabilized sediments. However, Allen & Vaughn (2011), in a flume study, found that increasing mussel species richness increased sediment erosion at both low and high mussel densities. It is possible that observations of mussel–sediment interactions in small mesocosm and flume studies may not scale up well to large, dense mussel beds. We need much more research on this topic, particularly at the scale of whole mussel beds and river reaches (Allen et al., 2014).

Supporting services: mussels support food webs

Mussels play important roles in food webs through the bottom-up provisioning of nutrients and energy. In rivers, mussels often occur as aggregations called mussel beds that can be very dense (up to 100 ind m−2) and speciose (10–20 sp.) (Atkinson & Vaughn, 2015). Mussel beds are patchily distributed in streams because they are constrained to stable sediments with low shear stresses (as described above), and mussels recover very slowly from disturbance (Haag, 2012). Thus, mussel beds in streams are usually separated by long reaches where mussels either do not occur or occur in low abundance (Atkinson & Vaughn, 2015; Newton et al., 2011; Fig. 2A). These beds can be hotspots of biological activity that support the rest of the food web by providing habitat, as described above, and through the bottom-up provisioning of nutrients (Fig. 2B). Nutrients excreted and biodeposited by mussels lead to increases in benthic algae (Spooner & Vaughn, 2006, 2012; Vaughn et al., 2007) and subsequently macroinvertebrates (Vaughn & Spooner, 2006; Spooner et al., 2012). In separate laboratory (Allen et al., 2012; Sansom, 2013) and field (Atkinson et al., 2014c) experiments, seston was labeled with a heavy nitrogen isotope (15N), fed to mussels, and then nitrogen derived from mussel excreta was tracked throughout the food web. Mussel-derived nitrogen was found in most food web compartments including benthic algae, benthic macroinvertebrates, macrophytes, and primary consumer fish. Atkinson et al. (2014c) found that mussel excretion could account for 40% of the nitrogen in a nutrient-limited river reach and that mussels supplied up to 19% of the nitrogen in specific food web compartments. Allen et al. (2012) found that once the grazing insect larvae metamorphose into winged adults, this nitrogen moves into the riparian, terrestrial food web as the insects are consumed by spiders. In a different study, Novais et al. (2015) found that die offs of Corbicula provided carrion to adjacent terrestrial systems and entered the detrital food web. Thus, mussels are subsidizing both aquatic and terrestrial food webs and linking aquatic and terrestrial ecosystems

Supporting services: mussels as environmental monitors

Freshwater mussels have the potential to serve as important sentinels or biomonitors of environmental change, revealing past conditions and monitoring future change. Because they are sessile filter feeders, they bioaccumulate particles, allowing measurement of stressor levels in their soft tissues. They are widespread, often occur at high densities and are relatively long-lived, allowing repeated sampling over time (Green et al., 1985; Rocha et al., 2015). Finally, geochemistry of shells can reveal past physical and chemical conditions, over both large spatial and temporal scales (Brown et al., 2005).

Shells incorporate and retain patterns of the chemical and physical environment long after the animal’s death, and thus can act as historical archives to reveal long-term environmental change. First, simple patterns of aragonite deposition, revealed as growth lines in the shell similar to tree rings, can reflect past temperature, flow, and other conditions under which mussels grew (Schone et al., 2004; Dunca et al., 2005; Geist et al., 2005; Rypel et al., 2009; Black et al., 2010; Fritts et al., 2017). Trace metals incorporated into shell tissue can be used to uncover past pollution events (Jamil et al., 1999; Brown et al., 2005) and upwelling periods (Langlet et al., 2007). Isotopic signatures of O18 and C13 in mussels have been used to reveal climatic conditions as far back as the Miocene (Blazejowski et al., 2013).

Mussel soft tissue can be used to assess environmental conditions over shorter time scales. Chemical content in mussel hemolymph, mantle, and/or foot tissue can be used as sublethal biomarkers to monitor water quality, by stress or immune responses (Newton & Cope, 2007; Fritts et al., 2015; Goodchild et al., 2015; Jasinska et al., 2015; Kolarevic et al., 2016). Pharmaceuticals bioaccumulate in mussels at higher levels than many other aquatic organisms including fish (Du et al., 2014). Nitrogen signatures in mussel soft tissue reflect background nutrient conditions (Wen et al., 2010), in particular residential and agricultural land use (McKinney et al., 2002), and net nitrogen loading could be used as a bioassessment tool for tracking agricultural nitrogen sources (Atkinson et al., 2014a). Finally, the stable isotope composition of the periostracum on the outside of the shell can also be used to track environmental change and understand historical food web conditions (Delong & Thorp, 2009; Fritts et al., 2017).

Mussels have become an important indicator organism in ecotoxicology studies (Cope et al., 2008). Juvenile mussels are particularly useful because they are endobenthic and important for examining groundwater toxicity, and a great deal of recent work has gone into establishing water quality criteria using juveniles (Augspurger et al., 2007; Wang et al., 2007). Juvenile mussels are more sensitive to ammonium than any other freshwater organism studied to date (Newton & Bartsch, 2007), and this sensitivity resulted in the U.S. Environmental Protection Agency revising the water quality criteria for ammonia (FMCS, 2016). Finally, mussels are becoming a viable option to detect “real time” changes in water quality by monitoring physiological responses such as gape (shell opening and closing), variations in heart rate, and changes in filtration and behavior (Hauser, 2015; Goodchild et al., 2016; Hartmann et al., 2016).

Provisioning and cultural services

Mussels are prey for other organisms such as muskrats (Tyrell & Hornbach, 1998) and turtles (Atkinson, 2013). Prehistoric humans ate mussels and used their shells as ornaments, tools, and utensils. In the U.S., archeological data indicate that Native Americans harvested mussels for food as long as 10,000 years ago (Haag, 2012). Most present-day western cultures do not utilize mussels as food, although they are considered a Native American traditional (“first food”) by tribes in the Pacific Northwest (Brubaker et al., 2009) and mussel harvest is a reserved treaty harvest right for some Native American tribes (Brim Box et al., 2006). Mussels and Corbicula are commonly eaten in many southeast Asian regions (Bolotov et al., 2014), and recent work documents their overexploitation there (Ziertitz et al., 2016, 2017).

Native Americans in the southeastern U.S. used mussel shells for wood working, as digging tools, and ground them to powder to temper pottery (Rafferty & Peacock, 2008). Extensive harvest of mussels for freshwater pearls and for the pearl button industry began in the 1850s (Humphries & Winemiller, 2009). During the peak button harvest year of 1912, 50,000 tons of mussels were removed from North American rivers (Haag, 2012). A second wave of mussel harvest occurred following World War II and up until the mid 1990s. In this case, beads made of heavy pieces of shell were used as seeds for the Japanese cultured pearl industry (Haag, 2012). Freshwater pearl farming is still a large industry in China (Jiale & Yingsen, 2009).

Mussels played an important role in early Native American and white culture. Beads and other ornaments made from shells played a significant role in Native American rituals and ceremonies (Claassen, 2008). Some tribes, such as the Choctaw Nation in Oklahoma, have active programs to revive these cultural traditions (Choctaw Nation, 2016). In areas where mussels were historically very abundant, they invoked as “sense of place” that was translated into names of creeks and even as ornaments on graves (Haag, 2012). Historic and current human exploitation and cultural use of North American mussels are thoroughly reviewed by Haag (2012).

Losses, restoration and valuation

Freshwater mussels are one of the most imperiled groups of organisms globally (Lydeard et al., 2004; Lopes-Lima et al., 2014). Approximately 30 North American taxa have become extinct over the past century, and 65% of the remaining 300 North American species are considered vulnerable to extinction (Haag & Williams, 2014). Ricciardi & Rasmussen (1999) predict that we will lose as many of 50% of the remaining species in the next century. In addition, mussel declines include not only species losses but also large declines in the abundance and biomass of once common species (Haag & Williams, 2014). These losses of common species are undoubtedly leading to large losses in mussel-provided ecosystem services.

The Kiamichi River in southeastern Oklahoma, U.S., provides a case study of the link between mussel losses and declines in ecosystem services. My students and I sampled mussel communities in this river over a 20-year period where drought-induced changes in flows and poor water management from a tributary reservoir led to large declines in mussel biomass (Galbraith et al., 2010; Allen et al., 2013; Atkinson et al., 2014b). We used laboratory derived physiological rates and river-wide estimates of species-specific mussel biomass to estimate ecosystem services provided by mussels. We found that biofiltration, nitrogen and phosphorus cycling, and nitrogen, phosphorus and carbon storage provided by mussels declined almost 60% over this time period (Vaughn et al., 2015).

Although the importance of mussel-provided ecosystem services is increasingly recognized, there have been few attempts to determine how the loss of these services may affect freshwater ecosystems, and the subsequent social, cultural, and economic benefits for humans FMCS, 2016; Castro et al., 2016b). The value of most mussel-provided ecosystem services cannot be assessed with a traditional marketplace framework, rather we need to encompass non-market and modeling methods (Southwick & Loftus, 2003; Ruffo & Kareiva, 2009; Castro et al., 2016a). Valuation studies of oysters and other marine bivalves can guide these efforts. For example, while oysters are a fishery commodity, they also provide a host of non-market ecosystem services such as biogenic habitat, biofiltration, and nutrient removal (Grabowski et al., 2012). The value of these non-market services can be assessed using the value of engineered structures for water filtration, wastewater treatment costs, replacement costs for sewage treatment plants, and nutrient credit programs (Beck et al., 2011; Grabowski et al., 2012). Along these lines, the American Fisheries Society has produced guidelines for assessing monetary damage from mussel kills that include ecological, use and non-use values, plus restoration costs (Southwick & Loftus, 2003). Because information to accurately estimate non-economic value is rarely available, they recommend using replacement costs as a conservative method for determining restitution for killed mussels.

Valuation of ecosystem services must also consider the social demand for ecosystem services, which can be assessed with metrics such as social perceptions or willingness to pay for services such as biofiltration producing clean water. For example, Castro et al. (2016a, b) used face-to-face surveys to assess multiple stakeholders’ social perceptions and willingness to pay for ecosystem services in the Kiamichi watershed. These surveys included showing stakeholders photographs of mussel and fish species and the ecosystem services that they provide. This study found that most stakeholders identified habitat for species and water quality as the most important and economically valuable ecosystem services. Regulating services received the highest willingness to pay value. The study also identified potential conflicts between water user groups depending on whether they lived in the watershed or were distant water users (Castro et al., 2016a, b).

Technology for propagating freshwater mussels has improved greatly over the past 20 years. In the U.S., there are now over a dozen federal and state facilities dedicated mussel to propagation, usually related to restoring listed species (FMCS, 2016). Such facilities could also be used for the large-scale production of common mussel species, which could then be restored to rivers to re-establish lost ecosystem services such as biofiltration and nutrient abatement.

Haag & Williams (2014) suggest that a conservation goal should be to protect mussels for the benefit of stream ecosystems, rather than vice versa. To accomplish this, we need much more quantification of the value and magnitude of ecosystem services provided by mussels, across species, habitats, and environmental conditions, and scaled up to whole watersheds. We need tools that will allow us to value mussel ecosystem services in a way that is understandable to both the public and to policy makers. Achieving this will require collaboration with social scientists, economists, and stakeholders. Sustaining and restoring mussel ecosystem services represent a transdisciplinary challenge, but the benefits will likely far exceed the capital invested in this effort.

Notes

Acknowledgements

This article stems from a presentation at the Second International Conference on the Biology and Conservation of Freshwater Bivalves. I thank the conference organizers and participants, and Antonio Castro, Carla Atkinson, Daniel Spooner, Kiza Gates, Daniel Allen, Heather Galbraith, Brandon Sansom, Thomas Parr, Traci Popejoy, and Brent Tweedy for thoughtful conversations and comments. Antonio Castro assisted with Table 1 and Andy Vaughn drew the figures. Comments from Ronaldo Sousa and an anonymous reviewer improved the manuscript.

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© Springer International Publishing Switzerland 2017

Authors and Affiliations

  1. 1.Oklahoma Biological Survey, Ecology and Evolutionary Biology Graduate Program, Department of BiologyUniversity of OklahomaNormanUSA

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