Provisioning Services

Humans have used mollusks for food and as tools for millennia. Evidence of freshwater mollusks serving as a human food source dates to ∼6000 years BP in northern Europe and to greater than 2800 years BP in North America (Haag 2012; Meadows et al. 2014; CTUIR 2020). The presence of large shell middens at human habitation sites shows that freshwater mussels were used as food extensively in prehistory by people in North America, Australia, Europe, and likely elsewhere (Parmalee and Klippel 1974; Nicodemus 2011; Haag 2012; Garvey 2017). Columbia Plateau tribes in northwestern North America, such as the Confederated Tribes of the Umatilla Indian Reservation (CTUIR), historically harvested mussels in association with harvest of other food resources (e.g., salmon and plants; Quaempts et al. 2018; CTUIR 2020). The Umatilla named a site on the Columbia River Išáaxuyi, which means “covered with mussel shells,” due to the high abundance of mussels (Hunn et al. 2015). Freshwater mussels are still considered a first food, a food of significant cultural and ecological importance, by the CTUIR and are actively managed and protected (Quaempts et al. 2018; CTUIR 2020). Freshwater mollusks remain an important food resource in other parts of the world, especially Southeast Asia (Zieritz et al. 2018), where both freshwater mussels and gastropods are a common commodity in markets (Bolotov et al. 2014; Dee et al. 2019). Mollusks are also used for medicinal purposes, mainly in eastern Asia. For example, in its native range, Corbicula fluminea has long been a part of traditional Chinese medicine used to treat liver disease and the effects of alcoholism (Bai et al. 2020).

Table 1.

Examples of ecosystem services provided by freshwater mollusks. C = carbon, N = nitrogen, P = phosphorus.

continued.

Historically, mollusk shells were important for tools, jewelry, and other uses. Native American tribes used mussel shells for tools and ground them to powder to temper pottery (Rafferty and Peacock 2008). In the Pacific Northwest, tribes collected mussels seasonally, stored shells in large piles, and later worked them into hooks, spoons, and adornment (Brim Box et al. 2006; CTUIR 2020; Peacock et al. 2020). Beginning in the mid-1800s and lasting through the mid-1900s, the mollusk shell button industry was a lucrative business in North America (Coker et al. 1919; Haag 2012). During the peak harvest in 1912, 50,000 tons of mussels were removed from North American rivers, and between 1897 and 1963, the total value of buttons was approximately $6 billion U.S. dollars (Haag 2012; Strayer 2017). Subsequently, the Japanese pearl industry used beads made from freshwater mussel shells as nuclei to produce cultured pearls in marine bivalves (Haag 2012). Cultured pearls are also produced in freshwater mussels, and this is a large industry in Asia (Jiale and Yingsen 2009). Additionally, many freshwater bivalves and gastropods have been harvested in Thailand for jewelry and artwork (Nagachinta et al. 2005; Allen et al. 2012a).

Regulating Services

Water filtration.—Through their filter feeding and grazing, mollusks provide important regulating services such as water purification and regulation of algal communities. Freshwater mussels are filter feeders that remove particles and associated nutrients from the water column and interstitial sediments, which can in turn decrease water treatment costs and improve water quality (Vaughn et al. 2008; Newton et al. 2011; Kreeger et al. 2018). Where mussel biomass is high in comparison to water volume, or where hydrologic residence times are long, mussels can filter a substantial amount of water (Vaughn et al. 2004). For example, mussels were able to clear the entire volume of a 440,000 m³ lake in less than a day, resulting in enhanced water clarity (Chowdhury et al. 2016). Efforts are underway to restore freshwater mussel filtration capacity to U.S. mid-Atlantic watersheds with the goal of improving water clarity and quality (Kreeger et al. 2018). Some groups of gastropods (e.g., Viviparidea and Bithynidae) also function as filter feeders in aquatic ecosystems (Brown and Lydeard 2010), thus likely providing similar benefits to water clarity (see Olden et al. 2013) and particulate nutrient removal. Future research on snail filtration capacity and their effects on water quality could broaden our understanding of the ecosystem services gastropods provide. Freshwater mussels also improve drinking water quality by filtering pathogens or contaminants such as coliform bacteria, pharmaceuticals, personal care products, and algal toxins (Mersch and Johansson 1993; Downing et al. 2014; Ismail et al. 2014, 2015; Hwang et al. 2021) and sequestering these contaminants in their soft tissue and shell (Giari et al. 2017; Archambault 2020). Less is known about filter-feeding gastropods, but based on work on bivalves (Roditi et al. 2000; Baines et al. 2005), we hypothesize that gastropods may be able to remove dissolved organic matter as well as materials such as heavy metals. Further work is needed to understand what mollusks can filter from the environment, what they sequester, the ultimate fate of sequestered materials, and how these aspects of filtration vary among species and environmental contexts.

Biofilm grazing.—Snails are important grazers that can substantially reduce algal and biofilm biomass (Lamberti et al. 1987; Hill et al. 1992; Rosemond et al. 1993). Nuisance and toxic algal blooms negatively affect wildlife and human health (Wurtsbaugh et al. 2019). Some work has shown that freshwater snails can help control algal blooms including nuisance cyanobacteria and toxic algae (Zhang et al. 2012; Groendahl and Fink 2017). More research is needed to better understand snails' ability to control algal blooms and their other functional roles in freshwater systems, particularly for detritivorous and filter-feeding snails.

Supporting Habitat Services

Nutrient storage and cycling.—Mollusks provide important supporting services such as nutrient recycling, translocation, and storage, and they may influence nutrient abatement (i.e., nutrient removal). As mollusks filter feed or graze, they convert energy and associated nutrients in their food into soft tissue, shell, and biodeposits (feces and pseudofeces), and they release bioavailable dissolved nutrients that support primary producers (Spooner and Vaughn 2006; Strayer 2014; Atkinson and Vaughn 2015) and detritus-based food webs (Atkinson et al. 2021; Hopper et al. 2021a).

Nutrient storage by mollusks is an overlooked, but potentially valuable, ecosystem service for nutrient abatement. For example, nitrogen (N)-trading programs in estuarine settings estimate the value of nitrogen assimilated by oysters at $50 to $181/kg N /year (Rose et al. 2021). Currently, similar programs to mitigate nutrient loading in freshwater environments do not exist, but they are being considered (Strayer et al. 2019; Wood et al. 2021). Freshwater mollusks assimilate nutrients into both their soft tissues and shells and can store kilograms of carbon (C), N, and phosphorus (P), as well as micronutrients, at a river reach (Atkinson and Vaughn 2015; Hopper et al. 2021b). Additionally, many species are relatively long-lived, and their shells can persist for decades (Strayer and Malcolm 2007; Atkinson et al. 2018), possibly providing long-term storage of nutrients such as calcium. Thus, long-term storage and sequestration via burial could be an important, but often overlooked, ecosystem service provided by freshwater mollusks.

Nutrients that are not assimilated into soft tissue and shell are egested as biodeposits or excreted as bioavailable dissolved nutrients (Strayer 2014; Atkinson and Vaughn 2015; Hopper et al. 2021a). Soluble nutrients excreted into the water column by mollusks are readily taken up by algae and heterotrophic bacteria (Evans-White and Lamberti 2005; Liess and Haglund 2007; Vaughn et al. 2008; Bril et al. 2014). Snails (Elimia spp.) were an important source of recycled nitrogen in a U.S. stream, excreting 12 times more nitrogen than they accumulated in biomass during spring growth, and assimilating and excreting up to 50% of the nitrogen initially taken up by autotrophs and leaf microbes (Hill and Griffiths 2017). Thus, where mollusk biomass is locally high, mollusks can create “biogeochemical hotspots” where nutrient recycling and material flux are increased, leading to concentrations of nutrients that can exceed background ambient concentrations of bioavailable nutrients (Hall et al. 2003; Strayer 2014; Atkinson and Vaughn 2015; Hopper et al. 2021a). Mollusks also can affect nutrient cycling of entire ecosystems. In a small North American stream, nonnative New Zealand mud snails (Potamopyrgus antipodarum) dominated carbon sequestration and nitrogen excretion because of their high biomass and ubiquitous distribution (Hall et al. 2003). If bioavailable nutrients are limiting, fertilization by mollusk excreta can lead to spatial variation in algal community assemblages (Atkinson et al. 2013) and increases in biomass of benthic algae, macroinvertebrates, fishes, and riparian invertebrates and vertebrates (Allen et al. 2012b; Atkinson et al. 2014; Lopez et al. 2020; Simeone et al. 2021). Grazing by snails also can reduce macrophyte biomass. Most work on this topic focused on impacts of invasive snails on native aquatic plants (Yang et al. 2018; Bissattini et al. 2021), but native snails also can control invasive plants (Baker et al. 2010). Mollusks also have bottom-up food web effects as prey for other organisms such as crayfishes (Crowl and Covich 1990; Alexander and Covich 1991), fishes (Brown and Lydeard 2010), muskrats (Tyrrell and Hornbach 1998; Haag 2012), and turtles (Atkinson 2013).

Mollusks also have indirect effects on nutrient cycles by modifying biogeochemical reactivity, microbial communities, and redox gradients. Their interactions with the sediments alter oxygen profiles and fluxes of nutrients from the sediment and water column (Matisoff et al. 1985; Boeker et al. 2016). Due to their interactions with the benthic sediments and their high ammonia excretion and biodeposition rates, freshwater mussels enhance denitrification and anaerobic ammonium oxidation (anammox) rates in benthic sediments (Hoellein et al. 2017; Trentman et al. 2018; Nickerson et al. 2019; Atkinson and Forshay 2022). This is beneficial for water quality because denitrification results in the removal of nitrogen from the ecosystem; this service has received considerable attention in marine settings with oysters and other marine mollusks (Newell et al. 2005; Kellogg et al. 2018; Rose et al. 2021). Additional work examining how freshwater mollusks influence microbially mediated processes could increase our understanding of the breadth of ecosystem services mollusks provide. Such effects could be substantial given the high biomass of mollusks in some ecosystems and their important roles in nutrient cycling.

Habitat engineering.—Stream-dwelling organisms must cope with high flows (Lopez and Vaughn 2021). Mollusks physically engineer ecosystems through their shell production and movements across and within the benthic substrate, provisioning habitat for other organisms. Mollusk shells generate complexity in benthic habitats that influence processes across trophic levels (Gutiérrez et al. 2003). Both living shells and spent shells enhance habitat complexity and provide a hard substrate for the settlement and establishment of organisms, including microscopic and macroscopic algae (Francoeur et al. 2002; Abbott and Bergey 2007; Lukens et al. 2017), macrophytes (Vaughn et al. 2002), macroinvertebrates (Spooner and Vaughn 2006; Vaughn and Spooner 2006; Simeone et al. 2021), and fishes (Hopper et al. 2019). Freshwater mussel aggregations can modulate near-bed velocities and turbulence in rivers over decadal time scales, which may enhance bed stability and create habitat for other stream-dwelling organisms by decreasing flow force and velocity (Sansom et al. 2018a, 2018b, 2020). As water flows past mussels, low-velocity refugia form behind them (Kumar et al. 2019), decreasing the hydrodynamic forces on the streambed downstream. Moreover, horseshoe vortices or complex wake structures are created around partially exposed mussels (Constantinescu et al. 2013; Sansom et al. 2018a; Wu et al. 2020), and such features are further modified when mussels are filtering (Wu et al. 2020). These hydraulic modifications can have important implications for other stream-dwelling organisms with specific microhabitat hydraulic preferences (e.g., Davis 1986; Bouckaert and Davis 1998). Overall, mussel aggregations have a reciprocal influence on near-bed flow because they both influence, and are constrained by, hydrodynamic forces at the streambed (Lopez and Vaughn 2021). In addition, shells provide spawning sites and serve as refugia for some fishes (Etnier and Starnes 1993; Aldridge 1999; Wisniewski et al. 2013). Locally high densities of shells, such as at mussel beds, increase the potential for strong hydraulic effects over extended spatial (tens to hundreds of meters) and temporal (decadal) scales (Strayer 2020). Much less is known about whether snails provide hydrodynamic refugia and/or stabilize sediments, but small stream invertebrates, such as caddisflies, can alter stream sediment dynamics and hydraulics when densities are high (Albertson and Allen 2015; Maguire et al. 2020; Mason and Sanders 2021; Mason et al. 2022). Thus, it is reasonable to expect that gastropods, with their sturdy shell, gripping foot, and mucus trails, also might stabilize sediment.

Beyond the obvious direct habitat provisioning of the shell, mollusks can increase habitat availability through their grazing and bioturbation activities. Filter-feeding bivalves increase the photic zone in lakes and rivers and enhance benthic substrate organic matter, allowing colonization by benthic macrophytes and aquatic insects (Strayer 2020). Grazing by invasive snails (Pomacea canaliculata) can have strong top-down effects by reducing biomass of aquatic plants, especially in shallow lakes with high nutrient loads (Gao et al. 2021; Liu et al. 2021), possibly leading to shifts from clear to turbid stable states. State shifts such as this can reduce light penetration in littoral zones and visibility for sight-feeding predators, with cascading effects on food webs. Overall, mollusks appear to have varied and sometimes strong effects on stream and lake habitats, which likely influence many other aquatic organisms.

Cultural Services

Freshwater mollusks provide many cultural services to humans. Large, durable freshwater mussel shells are particularly important for these services. Archaeological studies have shown that in Neolithic northern Europe, large mussel shell middens were used seasonally by pottery-using hunter-gatherer communities to temper pottery (Bērziņš et al. 2014). In North America, beads and other ornaments made from shells were used in rituals and ceremonies (Claassen 2008; CTUIR 2020). For example, the Winnebago tribe in Wisconsin, USA, used shell beads in rituals, produced utensils and fishing hooks from shells, and used powdered shell to temper pottery (Kuhm 2007). Currently, mollusk shells are sometimes used to ornament graves in the southern USA (Haag 2012). In the USA, the abundance of mussels in some areas invoked a sense of place that was translated into names of river reaches (e.g., Muscle Shoals and Išáaxuyi; Haag 2012; Hunn et al. 2015; Vaughn 2018). Living mollusks also bring humans enjoyment and are commonly sold internationally in the aquarium and ornamental pet trade (Ng et al. 2016; Patoka et al. 2017). In some cases, this practice has resulted in accidental introductions of mollusks into new ecosystems (Karatayev et al. 2009). Additionally, mollusks' regulating services (e.g., filtration, grazing) improve human perceptions of freshwater ecosystems by enhancing water clarity and other characteristics. For example, grazing by snails (Haitia acuta) reduces the occurrence of large algal mats (Parr et al. 2020), which can be unsightly to humans. Mollusks are also used in education and research to improve understanding of ecosystem health, and they are used as biomonitors for contaminants and pathogens (Mersch and Johansson 1993; Giari et al. 2017). Extensive toxicology research has evaluated mollusks' sensitivities to various contaminants, which have been used to evaluate water quality criteria (Augspurger 2003; Wang et al. 2007). Last, the bequest or existence value of mollusks is an important cultural service because people derive satisfaction from preserving the natural environment for future generations (Turner and Schaafsma 2015; Strayer 2017).

The Conundrum of Services and Disservices by Invasive Mollusks

The role of invasive mollusk species in providing ecosystem services has received attention primarily in terms of their negative effects or “disservices,” but they can also enhance services (Charles and Dukes 2008; Limburg et al. 2010; Walsh et al. 2016; Zieritz et al. 2022). Invasive species often do not provide provisioning or cultural services in their introduced range because they have not been used traditionally for those purposes in the new area. However, some species may be introduced because of provisioning or cultural services they provide in their native range or elsewhere. For example, the bivalve Corbicula fluminea is thought to have been introduced into the USA in the 1930s by Chinese immigrants who used the species as a food item in its native range (Counts 1986). Thiarid snails have invaded freshwaters globally, and they frequently are introduced through the aquarium trade, where their grazing services are used to keep aquaria clean (Padilla and Williams 2004; Preston et al. 2022). However, despite their use in the aquarium trade, invasive snails often provide disservices, as many are intermediate hosts for trematodes and other parasites that negatively affect the health of fishes, birds, and humans (e.g., Pinto and de Melo 2011; Lv et al. 2018; Valente et al. 2020).

Filtering and nutrient recycling by invasive mussels can provide important regulating and supporting services. Nutrient fluxes from high densities of Corbicula exceeded or equaled those from native mussels in two North American rivers (Hopper et al. 2022). Invasive dreissenid mussels can drastically change energy and nutrient fluxes in a system (Li et al. 2021; Zieritz et al. 2022). At high densities, their filtering activity reduces phytoplankton and redirects nutrients and energy from the water column to the benthos, causing a decrease in pelagic production and an increase in benthic production (Higgins and Vander Zanden 2010; Karatayev et al. 2015). This includes an increase in benthic algae and macrophytes, which are often perceived as nuisances that inhibit boating, swimming, and other recreational uses in lakes and reservoirs. Fouling of native mussels by dreissenid mussels causes high native mussel mortality through resource competition (Haag et al. 1993; Karatayev et al. 2015; Beason and Schwalb 2022), and Corbicula clams also are suspected to negatively affect native mussels (Ferreira-Rodríguez et al. 2018, 2022; Modesto et al. 2019). Both invasive species diminish ecosystem services provided by native mussels, but they also provide important benefits, especially in areas where the native mollusk filter-feeding community has been lost or severely degraded. For example, Dreissena can be used as biofilters to clear bioavailable contaminants from effluents before discharge (Binelli et al. 2015), and invasive Corbicula in Portugal assist in the remediation of acid mine drainage and other contaminants (Ismail et al. 2014; Rosa et al. 2014). Understanding how invasive mollusks provide and alter ecosystem services can give additional insight about services provided by native mollusks and how replacement of native species by invasive species ultimately affects ecosystem structure and long-term function.