Changes in the cladoceran community of Lake Superior and the role of Bythotrephes longimanus

Abstract

Introductions of Bythotrephes longimanus have resulted in reduced cladoceran species richness and biomass in the Laurentian Great Lakes and many inland lakes. Bythotrephes was first observed in Lake Superior in 1987 but its effect on the cladoceran community has been unknown. We compared the composition of the offshore cladoceran community of Western Lake Superior during 2014 and 2015 to zooplankton surveys from 1971–2001 to determine whether changes in the cladoceran community have occurred. Monthly comparisons show that the contribution of Bosmina longirostris to offshore cladoceran numbers was generally twice as much in the 1970s than during 2014–2015 while the relative contribution of Daphnia mendotae increased after the 1970s. These community changes are consistent with changes due to Bythotrephes observed in other lakes. To evaluate evidence for the role of Bythotrephes in these community changes, we used data from 2014–2015 to analyze patterns in spatial and vertical overlap between Bythotrephes and its cladoceran prey species (Bosmina, Daphnia, and Holopedium) and compared estimates of consumption by Bythotrephes to production of these potential prey. Bosmina was the species whose vertical position and rate of production made it most vulnerable to suppression by Bythotrephes. Of the potential cladoceran prey species, Bosmina densities were also the most negatively correlated with Bythotrephes densities. These findings support a hypothesis of top-down effects on Bosmina by Bythotrephes in Lake Superior. This work informs future zooplankton research in Lake Superior and furthers our understanding of the effects of Bythotrephes on the Lake Superior food web.

Introduction

Species introductions in aquatic ecosystems can alter the abundance and community composition of zooplankton (Brooks and Dodson, 1965, Carpenter et al., 1987). In North America, introductions of Bythotrephes longimanus, a predatory cladoceran native to northern Europe and Asia (Lehman, 1987, Burkhardt and Lehman, 1994), have resulted in reduced zooplankton species richness (particularly in cladocerans) and abundance in small inland lakes and in the Great Lakes (Barbiero and Tuchman, 2004, Strecker et al., 2006, Azan et al., 2015). Bythotrephes selects slow-moving cladocerans such as Bosmina longirostris and Daphnia spp. (Vanderploeg et al., 1993, Grigorovich et al., 1998, Schulz and Yurista, 1999). Bosmina and Daphnia consistently become less abundant in lakes following Bythotrephes invasion and multiple studies suggest that this is a direct result of consumption by Bythotrephes (Yan and Pawson, 1997, Yan et al., 2002, Strecker et al., 2006, Kerfoot et al., 2016).

Rapid cladoceran community changes in the Great Lakes following Bythotrephes invasion occurred in Lake Michigan in the late 1980s, when two of three common Daphnia species nearly disappeared within a year of the first detection of Bythotrephes (Lehman, 1988, Lehman, 1991, Lehman and Cáceres, 1993). Daphnia mendotae has remained common in Lake Michigan since Bythotrephes establishment, but appears to have done so partly by reducing the extent of its vertical overlap with Bythotrephes (Pangle and Peacor, 2006, Pangle et al., 2007). Other small cladocerans such as Bosmina have also become less common in Lake Michigan since the establishment of Bythotrephes (Makarewicz et al., 1995, Schulz and Yurista, 1999). Similar changes have been described in the cladoceran communities of Lakes Huron and Erie (Barbiero and Tuchman, 2004, Bunnell et al., 2012). In Lake Ontario, Bosmina longirostris and Eubosmina spp. abundance has declined by more than half since 2003 (Barbiero et al., 2014, Rudstam et al., 2015). These changes coincided with an order of magnitude increase in Bythotrephes abundance after 2003 which suggests that Bythotrephes has exerted top-down control on bosminids in Lake Ontario.

Bythotrephes was first detected in Lake Superior, the largest lake on Earth by surface area, in 1987 (Cullis and Johnson, 1988), but its effect on the zooplankton community is largely unknown. The Lake Superior zooplankton community is calanoid-dominated in terms of density and biomass (Patalas, 1972, Barbiero et al., 2001). Historically, the cladoceran community in Lake Superior was dominated by three species including Bosmina longirostris, Daphnia mendotae, and Holopedium gibberum (hereafter referred to by genus, unless otherwise noted). Brown and Branstrator (2004) reported a lower abundance of Bosmina in August of 2001 compared to observations from the early 1970s. Though reductions in Bosmina abundance are consistent with planktivory by Bythotrephes, the authors could not clearly demonstrate such a relationship given the temporal limitations of their dataset. Zooplankton surveys spanning multiple sampling seasons are needed to determine whether these or other community changes have occurred in the decades since Bythotrephes establishment.

Previous studies in Lakes Michigan and Huron have suggested that consumption by Bythotrephes can exceed production of cladocerans (Lehman and Cáceres, 1993, Bunnell et al., 2011, Bunnell et al., 2012). Consumption by Bythotrephes has not yet been estimated in Lake Superior. Bythotrephes densities in Lake Superior are generally lower than in Lakes Michigan and Huron (Barbiero et al., 2001, Brown and Branstrator, 2004, Brown et al., 2012, Pothoven et al., 2012, Bunnell et al., 2014). However, Lake Superior is also colder and less productive than the other Great Lakes (Patalas, 1972) and the consumptive demands of Bythotrephes in Lake Superior may still approach the rate of production of their preferred prey species. Cladoceran production is subject to a variety of losses other than by invertebrate predation. Thus, increased mortality due to Bythotrephes predation might be enough to reduce cladoceran abundance even if consumption by Bythotrephes does not exceed cladoceran production.

The addition of Bythotrephes to the Lake Superior food web is not the only important change that has occurred in this ecosystem in recent decades. Since the 1970s, population densities of planktivorous fish have fluctuated in Lake Superior and average summer surface temperatures have increased (Austin and Colman, 2007, Gorman, 2012, Pratt et al., 2016). One key change in the planktivorous fish community since the 1970s has been an overall increase in lake herring (Coregonus artedi) densities. Increasing vertebrate planktivory would be expected to cause a downward shift in the average body size of zooplankton (Brooks and Dodson, 1965). Temperature is a key factor driving zooplankton production and spatial aggregation in Lake Superior and increases in surface temperature might increase zooplankton production and density (Watson and Wilson, 1978, Zhou et al., 2001). In addition, the increase in summer surface temperatures in Lake Superior since the 1970s has the potential to favor warm water taxa such as small cladocerans (Lehman, 2002). Though zooplankton abundance and production can also be influenced by changes in primary production, changes in food quality and quantity for herbivorous zooplankton are unknown over the period of Bythotrephes invasion. However, changes in food availability would be expected to have similar effects on the densities of all herbivorous zooplankton rather than effects on specific taxa. Therefore, while changes in temperature, vertebrate planktivory, and primary production all can cause changes in zooplankton community structure, the effects of these ecosystem changes on the cladoceran community should be distinguishable from top-down effects by Bythotrephes.

The purpose of this study is to determine whether long-term changes in the cladoceran community of Lake Superior have occurred since the introduction of Bythotrephes. Based on changes observed in the cladoceran communities of the other Great Lakes and smaller, inland lakes following Bythotrephes invasion, we hypothesized that small cladocerans such as Bosmina would be less common in offshore areas of Lake Superior than before Bythotrephes invasion. To test this, we compared the offshore cladoceran community observed during the 2014 and 2015 growing seasons to past zooplankton surveys. Further, we used the data from 2014 and 2015 to evaluate three lines of evidence that Bosmina, Daphnia, and Holopedium populations are currently negatively impacted by the presence of Bythotrephes. These lines of evidence were: 1) the extent of synchronous spatial overlap among the prey taxa and Bythotrephes, 2) patterns in vertical position of the prey taxa relative to Bythotrephes, and 3) the difference in temperature-driven production of the prey taxa versus temperature-driven consumptive demands of Bythotrephes.