Spatial and temporal distributions of Dreissena spp. veligers in Lake Huron: Does calcium limit settling success?

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Abstract

The larval stage of invasive Dreissena spp. mussels (i.e., veligers) are understudied despite their seasonal numerical dominance among plankton. We report the spring and summer veliger densities and size structure across the main basin, North Channel, and Georgian Bay of Lake Huron, and seek to explain spatiotemporal variation. Monthly sampling was conducted at 9 transects and up to 3 sites per transect from spring through summer 2017. Veliger densities peaked in June and July, and we found comparable densities and biomasses of veligers between basins, despite differences in density of juvenile and adult mussels across these regions. Using a generalized additive model to explain variations in veliger density, we found that temperature, chlorophyll a, and nitrates/nitrites were most important. We generated an index of veliger attrition based on size distributions that revealed a higher rate of attrition in the North Channel than the rest of the lake. A logistic model indicated a threshold calcium concentration of around 22 mg/L was necessary for veligers to survive to larger sizes and recruit to their juvenile and benthic adult life stages. Improved understanding of factors that regulate the production and survival of Dreissena veligers could improve the ability of managers to assess future invasion threats as well as explore potential control options.

Introduction

Zebra (Dreissena polymorpha) and quagga mussels (Dreissena rostriformis bugensis, collectively referred to as dreissenid mussels) are commonly considered to be one of the most aggressive freshwater invaders in the northern hemisphere (Karatayev et al., 2015). Originally from the Black and Caspian seas and their tributaries in southern Russia and Ukraine, zebra mussels were first documented in North America in Lake Erie in 1986 (Carlton, 2008), and the first suspected quagga mussel sighting was in September 1989 near Port Colborne, Lake Erie (Mills et al., 1993). Since then, Dreissena have been spreading throughout waterways in the United States and Canada (Benson et al., 2020a, Benson et al., 2020b).

Both zebra and quagga mussels are characterized as ecosystem engineers (Karatayev et al., 2002) in the Laurentian Great Lakes and have had severe and wide-reaching ecological impacts (Hebert et al., 1991, Karatayev et al., 2002, Vanderploeg et al., 2002). One important example is their ability to shift nutrients from the pelagic to benthic habitat, both through filtration of phytoplankton and microzooplankton in the water column, as well as the direct ingestion of nutrients (Holland et al., 1995, Pothoven and Elgin, 2019, Whitten et al., 2018). For example, phytoplankton abundance in Saginaw Bay decreased by at least 60% by 1992, six years after zebra mussels were established (Holland, 1993). Likewise, Dreissena are hypothesized to have contributed to the oligotrophication of the pelagic offshore region of Lakes Huron and Michigan (Evans et al., 2011), including a significant reduction in the spring diatom bloom (Reavie et al., 2014, Barbiero et al., 2018). In more productive lakes, such as Lake Erie, Dreissena can enhance the frequency of harmful algal blooms due to selective filtration and rejection of toxic phytoplankton species (Vanderploeg et al., 2014, Vanderploeg et al., 2001). Finally, Dreissena can influence other components of the food web including reducing zooplankton abundance and changing community composition both through the direct ingestion of small-bodied zooplankton (MacIsaac et al., 1991) as well as by the sequestration of phosphorus and other nutrients (Hecky et al., 2004).

To date, the vast majority of Dreissena research has focused on understanding the distribution and impacts of juvenile and adult mussels that occupy the lake bottom and are sampled by benthic gear such as ponar grabs. In contrast, very few studies have examined the dynamics and ecological impacts of the planktonic larval veliger stage of Dreissena even though they can be an important (and sometimes dominant) part of the zooplankton (Bowen et al. 2018). Veligers are filter feeders, like the benthic life stages, and laboratory experiments indicate that peak densities of veligers in western Lake Erie (roughly 628,000 individuals/m3) may filter up to 20% of the entire water column each day (Klerks et al., 1996, MacIsaac et al., 1992). While adult filtering impacts can be more significant volumetrically during periods of lake mixing, adults commonly have limited access to phytoplankton and nutrients in the epilimnion during periods of thermal stratification. By contrast, veligers commonly occur in the epilimnion (Bowen et al., 2018, MacIsaac et al., 1992). Further research on veligers is vital in understanding the invasive ecology of Dreissena, given that veliger dispersal and survival likely plays a key role underlying the spread of these ecosystem engineers.

Although zebra and quagga mussels are closely related, they do have several important differences in their benthic stage that should be considered when studying the distribution and impacts of either species. Zebra mussels require a hard substrate for attachment and are better adapted to life in the littoral zone (Karatayev et al., 2015). Quagga mussels have a greater energetic efficiency, can reproduce in colder temperatures, have greater filtration rates during warmer months, and are able to colonize softer sediments (Karatayev et al., 2015). Because softer sediments are often found in the profundal zone (Karatayev et al., 2015, Nalepa et al., 2010) this is an important distinction in larger bodies of water, such as the Great Lakes, that allows for a much greater area for colonization. Consequently, quagga mussels can access a greater volume of water to filter, as well as the nutrients in the deep chlorophyll layer, than zebra mussels during periods of thermal stratification. Perhaps as a result of these differences, quagga mussels have largely replaced zebra mussels throughout the Great Lakes (Karatayev et al., 2015, Nalepa et al., 2010).

Given the limited basic data on the distribution and dynamics of veligers in the Laurentian Great Lakes, our study capitalized on veliger data from the monthly sampling of zooplankton during spring and summer throughout three basins of Lake Huron during the 2017 year of the Cooperative Science and Monitoring Initiative (CSMI, see https://www.epa.gov/great-lakes-monitoring/cooperative-science-and-monitoring-initiative-csmi) to answer some of those questions. This effort involved multiple federal agencies conducting spatially and temporally coordinated sampling for a suite of physical and biological parameters. These basins differed by orders of magnitude with respect to the mean densities of benthic quagga mussels sampled by ponar during the 2017 CSMI: main basin- 1497.7/m2, Georgian Bay- 178.1/m2, North Channel- 7.4/m2 (Karatayev et al., 2020). Zebra mussels were collected only in the North Channel (0.5/m2, Karatayev et al., 2020). Our first objective was to describe the monthly distribution and size structure of veligers in each basin of Lake Huron. Given the low density of benthic mussels in the North Channel, we hypothesized it would have the lowest density of veligers. Our second objective was to develop a model to explain variation in the density of veligers using environmental variables that were measured at the same time as zooplankton sampling. We expected that calcium concentrations would play the largest role in explaining variations in veliger density. Our results will provide improved understanding of the linkages between benthic Dreissena densities and their larval reproduction as well as insights into what limits Dreissena survival at the larval life stage.

Section snippets

Field survey design

Sampling occurred four times (i.e., monthly) in 2017: April 19 – May 11 (herein referred to as May), June 10 – 17, July 6 – 26, and August 8–26. The U.S. Geological Survey (USGS) and Environmental Protection Agency (EPA) collaborated in the sampling. For each month, sampling was conducted along nine transects located near rivers with varying nutrient inputs throughout the main basin of Lake Huron, the North Channel, and Georgian Bay (Fig. 1). Sites sampled in the North Channel extended out from

Density and biomass of veligers

Veligers were identified in zooplankton samples spanning April 19, 2017 through August 26, 2017. Average densities in all basins were relatively low (<5,000 individuals/m3) until June when density more than doubled, with the lowest average (~13,000 individuals/m3) in Georgian Bay and higher values observed in all other basins. In August, densities dropped dramatically in all basins of the lake, returning to average densities below 8,500 individuals/m3. It is important to note that there was

Discussion

To our knowledge, we are the first to report on the spring and summer Dreissena veliger densities and size structure across Lake Huron. Densities and biomasses of veligers were comparable between basins despite differences in density of benthic mussels across these regions (Karatayev et al., 2020). We found some variation between basins when looking at veliger length distributions and their respective attrition rates that may be due to differences in calcium concentration or other

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

We acknowledge the efforts of multiple individuals that assisted in different aspects of this study. We appreciate the vessel crews of multiple federal research vessels: R/V Arcticus, R/V Sturgeon, R/V Lake Guardian, and R/V Lake Explorer II. Many scientists contributed to the field sampling efforts on these vessels, especially Amelia Runco, Matt Welc, and Dave Warner from USGS, Paris Collingsworth and Joel Hoffman from EPA. Ann Cotter deserves additional credit not only for field work but also

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