Mass mortality of a dominant invasive species in response to an extreme climate event: Implications for ecosystem function

Impacts of invasive species on ecosystems are often context dependent, making empirical assessments difficult when climatic baselines are shifting and extreme events are becoming more common. We documented a mass mortality event of the Asian clam, Corbicula fluminea, an abundant invasive clam, which has replaced native mussels as the dominant filter-feeding bivalve in the southeastern United States. During an extremely hot and dry period in the summer of 2012, over 99% of Corbicula died in our 10-km study reach of the Broad River, Georgia. Because Corbicula were the only filter-feeding organism in the ecosystem with substantial biomass, their death led to the nearly complete cessation of ecosystem services provided by filter-feeding bivalves. We estimate that following the mass mortality event, turnover time within the sampling reach (reach volume/total filtration) rose from approximately 5 h to over 1200 h. In addition to the loss of filtering capacity, concentrations of total dissolved phosphorus (TDP) and soluble reactive phosphorus (SRP) were also higher in areas where die-off was occurring than in an upstream area without mortality. Mass balance calculations and a manipulative mesocosm experiment predicted TDP and SRP concentrations much higher than our observed values, suggesting that rapid biotic or abiotic uptake of phosphorus may have occurred. Our study demonstrates that climate change can increase the temporal variability of populations of aquatic organisms that provide key ecosystem functions, and highlights that even pulsed, short-lived events can markedly affect systems of reduced diversity. Extreme events are becoming more common with climate change, and have the potential to interact with other stressors on ecosystems. Invasive species are one of the most pervasive stressors of ecosystems worldwide (Vitousek et al. 1997; Millennium Ecosystem Assessment 2005). Their effects on native species and community structure are widely known, but the effects of invasive species on nutrient cycling and other ecosystem functions are not as well documented (Strayer et al. 1999; Hecky et al. 2004). The impacts of invasive species are a function of their range, abundance, and per capita effects (Parker et al. 1999), which are often determined by the relationships among their species traits, the traits of other species in the ecosystem, and the abiotic conditions in their novel range. For example, the zebra mussel (Dreissena polymorpha) has reshaped nutrient dynamics in the Great Lakes, shifting phosphorus availability from open water areas to nearshore ecosystems thanks to its high densities and per capita filtration rates (Hecky et al. 2004). Because non-native invasive species have not evolved in the ecosystems where they are becoming established, they may not have the same tolerances to extreme episodic events in their new range as native species (Byers 2002; Cox 2004). Therefore, to fully understand the impact of an invasive species, one must consider how the invasive species responds to extreme events and how these responses differ from native species. In aquatic communities, invasive species often represent a large proportion of the community diversity, and some have been shown to have large-scale ecosystem effects. Many of those with the largest impacts are mollusks, because freshwater mollusks play a critical role in aquatic ecosystems by providing ecosystem services such as filtration, nutrient uptake, and sedimentation, all of which affect overall water quality (Strayer et al. 1999, 2006; Vaughn and Hakenkamp 2001; Vaughn 2010; Sousa et al. 2013). In North America, the native mussels in the Unionidae family are in significant decline (Bogan 1993; Neves et al. 1997; Haag 2012). In many systems these species are no longer present due to human impacts and have been replaced by invasive filter-feeding bivalves such as the zebra mussel D. polymorpha *Correspondence: [email protected] 177 LIMNOLOGY and OCEANOGRAPHY Limnol. Oceanogr. 62, 2017, 177–188 VC 2016 Association for the Sciences of Limnology and Oceanography doi: 10.1002/lno.10384 and the Asian clam Corbicula sp. (McMahon and Bogan 2001). Globally, nutrient cycles in aquatic ecosystems have been dramatically reshaped by invasive bivalves, such as the golden mussel (Limnoperna fortunei) in South America (Cataldo et al. 2012; Boltovskoy and Correa 2015), the zebra mussel in the Hudson River (Caraco et al. 1997; Strayer et al. 2004) and the Great Lakes (Arnott and Vanni 1996; Hecky et al. 2004), and Corbicula sp. in both Europe (Pigneur et al. 2012) and the United States (Phelps 1994). These introduced bivalves are classic r-selected species—they are short lived, reproduce early, and are sensitive to extreme environmental conditions (McMahon 2002). In many rivers in the southeastern United States, the native unionids are no longer abundant and instead Corbicula sp. are found in high densities (McMahon and Bogan 2001). Most likely Corbicula fluminea is the predominant species representing this genus in the southeastern United States, including in our study, because it is widespread (Leff et al. 1990; Atkinson et al. 2010 among others). However, because Corbicula represents a cryptic species complex and there is considerable taxonomic debate surrounding the number and identification of species within the genus (Sousa et al. 2008), we inclusively refer to it (and our study organism) as Corbicula. Corbicula is sensitive to both high temperatures (> 358C) and low dissolved oxygen levels (< 0.5 mg L) (McMahon and Bogan 2001). Within the family Unionidae a wide range of tolerances and life history strategies is seen, but with few exceptions they are longer-lived and more tolerant of abiotic stressors such as high temperature and desiccation than are Corbicula (McMahon and Bogan 2001; Haag 2012). Although unionids are not immune to the effects of these stressors (see Haag and Warren 2008; Atkinson et al. 2014; Vaughn et al. 2015), in several cases during extreme events Corbicula mortality was nearly complete while some native mussels survived (Haag and Warren 2008), or Corbicula mortality occurred before impacts on native mussels were observed (Golladay et al. 2004), indicating Corbicula’s lower tolerance to these stressors. Typically, mass mortality events affecting unionids occur when rivers and streams cease to be free flowing, and form disconnected pools with extremely high temperatures (Golladay et al. 2004; Haag and Warren 2008; Atkinson et al. 2014; Vaughn et al. 2015). Systems dominated by Corbicula may be particularly sensitive to mass mortality events, potentially even when systems maintain flow, and the impact of these events are both via the release of nutrients, and via the loss of ecosystem functions provided by the Corbicula (e.g., filter feeding and associated water column processing). The effects of these die-offs have not previously been described on a large spatial scale, or with direct measurements of water quality impacts. To examine the direct and indirect effects of a Corbicula mass mortality event, we used a combined observational and experimental approach. Specifically, we used field observations to quantify the extent of a naturally occurring mass mortality event and its water quality impacts, and scaled up the clam’s known per capita effects to quantify the loss of ecosystem function associated with Corbicula mortality. A mesocosm experiment provided a controlled examination of water quality impacts, including the timing, amount, and form of nutrients released during a simulated mass mortality event.