Assessment of uncontained Zequanox applications for zebra mussel control in a Midwestern lake

Abstract

Zebra mussels (Dreissena polymorpha) are invasive bivalves that have perturbed aquatic ecosystems within North America since their introduction in the mid-1980s. Control of zebra mussels has largely been restricted to raw water conveyance systems and associated infrastructures because few control products are registered for application in surface waters. The biopesticide Zequanox was registered in 2014 by the U.S. Environmental Protection Agency for controlling dreissenid mussels (zebra and quagga mussels (Dreissena rostriformis bugensis) in surface waters. Previous Zequanox applications in surface waters have used vertical impermeablemembrane barriers to contain treated water. Studies have indicated that uncontained applications may be successful if Zequanox suspensions of the correct viscosity are applied to facilitate the creation of stratified benthic treatment layer. In this study, Zequanox was applied to replicate 0.30-hectare plots within a small inland lake using a custom-engineered, boat-mounted application system to determine if uncontained Zequanox applications could be used to manage zebra mussel populations and to protect native unionid mussels within zebra mussel infested waters. To determine success, the following specific objectives were investigated during, 30 days after, and/or 1 year after Zequanox exposure: (1) evaluate Zequanox concentrations during exposure; (2) monitor water quality during and after exposure; (3) evaluate the mortality of zebra mussels that were caged within treatment zones during the exposures; (4) evaluate the densities of naturally occurring zebra mussels with treatment zones before and after Zequanox exposure; and (5) evaluate the survival, condition, and dreissenid infestation of native mussels in the treatment zones before and after Zequanox exposure. Zequanox rapidly dissipated from the treated plots, resulting in no appreciable treatmentrelated mortality of zebra mussels and insignificant impacts to water quality. Zequanox exposure-related impacts to native mussels were not observed. Introduction Zebra mussels (Dreissena polymorpha) are highly invasive, ecosystem-altering bivalves that have adversely impacted invaded waterways (Lewandowski and Stańczykowska, 2014; Orlova, 2014; Sousa and others, 2014; Benson and others, 2019). Because of their high fecundity, zebra mussels can quickly reach extremely high densities, and a microscopic, free-swimming early life stage allows for anthropogenic transport and rapid dispersal (Mackie and Claudi, 2010; Birnbaum, 2011). Zebra mussels can cause extensive ecological effects; such as, biogeochemical cycle alterations, energy flow disruptions, habitat alterations, shifts in population structures of invertebrate and fish communities, and promotion of harmful algal blooms through selective filtering (Vanderploeg and others, 2001; Orlova and others, 2004; Strayer and others, 2004; Bruesewitz, 2008; Hoyle and others, 2008; Knoll and others, 2008; Vanderploeg and others, 2010; Adlerstein and others, 2013; Colvin and others, 2015). Zebra mussels have also negatively impacted native unionid populations through competition for food resources and other effects related to biofouling (Ricciardi and others, 1998; Strayer and Malcom, 2007). Zebra mussels readily colonize hard surfaces, causing biofouling and corrosion of structures and equipment such as trash screens, dams, docks, boats, engines, and navigational aids (Mackie and Claudi, 2010; Chakraborti and others, 2013). The cost to mitigate the impacts of zebra mussels to infrastructure has been estimated at $100 million per year (De Leon, 2008). Remediation costs in the United States will likely increase as dreissenid mussels—zebra and quagga mussels (Dreissena rostriformis bugensis)—become established in waters west of the Continental Divide. Chlorination quickly became the primary means to combat zebra mussel fouling in industrial water systems (Mackie and Claudi, 2010; Chakraborti and others, 2013) and although effective, the use of chlorine has environmental consequences. Chlorine reacts with organic matter and can result in the 2 Assessment of Uncontained Zequanox Applications for Zebra Mussel Control in a Midwestern Lake production of carcinogenic disinfection by-products such as trihalomethanes and haloacetic acids (Dojlido and others, 1999; Nokes and others, 1999; Richardson and others, 2007). The hazards associated with increased chlorine use and the concomitant increase of disinfection by-products increases environmental concerns (Molloy, 1998; Molloy and others, 2013b). In the 1990s, efforts were made to discover an environmentally compatible chlorine replacement for use in dreissenid mussel biofouling treatments. Hundreds of microorganisms were screened for dreissenid mussel toxicity, and a single bacterial strain, Pseudomonas fluorescens strain CL145A (Pf-CL145A), was determined to have potential for development into an environmentally compatible and selective control tool (Molloy, 1998; Mayer, 2011; Molloy and others, 2013a,b). Zequanox, a biopesticide containing 50 percent dead Pf-CL145A cells as the active ingredient, was developed by Marrone Bio Innovations (Davis, California) and is registered with the U.S. Environmental Protection Agency (registration number 84059–15) for defined discharge system and surfacewater applications (Weber, 2015; Marrone Bio Innovations, 2019). As of 2019, Zequanox is approved for application in 41 states, with ongoing research and label expansions in the United States, Canada, Europe, and South America (Carrie Link, Marrone Bio Innovations, written commun., 2019). Various experimental Zequanox applications have been completed in surface waters that used barriers to contain treated waters (Luoma and others, 2015b; Weber, 2015; Whitledge and others, 2015; Luoma and Severson, 2016). Zequanox also was applied within a containment barrier during a rapid-response action to eradicate zebra mussels from a newly infested lake (Christmas Lake, Hennepin County, Minnesota [not shown]; Lund and others, 2018). Several studies evaluated subsurface applications that were designed to target the benthic environment to maximize exposure to zebra mussels while reducing the amount of Zequanox required for treatment. No difference in mortality was detected among zebra mussels exposed to either wholewater column or subsurface Zequanox applications in 350-liter (L) tanks (Luoma and others, 2015a). Whole-water column versus subsurface Zequanox applications were further evaluated using 27-square meter (m2) in-lake enclosures (Luoma and Severson, 2016). Results indicated a reduction in zebra mussel mortality ranging from about 13 to 17 percent with subsurface applications; however, the loss in efficacy with the subsurface applications was offset by the need to apply more Zequanox in the whole water column applications (Luoma and Severson, 2016). Two independent experiments that used subsurface Zequanox applications within enclosures were completed during 2 subsequent years in a small quarry lake. In the first experiment, Zequanox was observed to mix into the upper, untreated portion of the water column within 24-m2 enclosures; however, treatment-related mortality of zebra mussels still exceeded 91 percent for zebra mussels attached to benthic substrates and macrophytes and 97 percent for zebra mussels contained within test chambers (Whitledge and others, 2015). In the second experiment, Zequanox was applied to a 324m2 enclosure using subsurface spot treatments, and mortality exceeded 90 percent for zebra mussels within 5 meters (m) of injection points (Whitledge and others, 2015). Subsurface Zequanox applications also were evaluated in laboratory experiments and replicated 9-m2 pond enclosures at temperatures ranging from approximately 9 to 20 degrees Celsius (°C) (Severson and Luoma, 2016). In these experiments, an obvious effect of water temperature on the viscosity of Zequanox suspensions was observed, and a formula was developed for determining temperature-specific Zequanox concentrations that would produce a suspension with the desirable viscosity for subsurface applications in waters with temperatures ranging from 7 to 22 °C (Severson and Luoma, 2016). The use of barriers to contain Zequanox-treated water creates logistical difficulties and increases costs associated with barrier acquisition and placement. Previous studies demonstrated the potential use of subsurface applications to reduce the amount of Zequanox required to achieve adequate control, but additional field-scale studies were needed to determine the efficacy and feasibility of uncontained Zequanox applications in surface waters. The purpose of this study was to determine if uncontained Zequanox applications could be used to manage zebra mussel populations and to protect native unionid mussels within zebra mussel infested waters. Specific objectives were investigated during, 30 days after, and/or 1 year after Zequanox exposure and included the following: (1) evaluate the Zequanox concentrations during exposures; (2) monitor the water quality during and after exposures; (3) evaluate of the mortality of zebra mussels that were caged within treatment zones during the exposures; (4) evaluate of the densities of naturally occurring zebra mussels in the treatment zones before and after Zequanox exposure; and (5) evaluate the survival, condition, and dreissenid infestation of native mussels before and after Zequanox exposure.