Zebra or quagga mussel dominance depends on trade-offs between growth and defense—Field support from Onondaga Lake, NY

Abstract

Two invasive mussels (zebra mussel, Dreissena polymorpha and quagga mussel D. rostriformis bugensis) have restructured the benthic habitat of many water bodies in both Europe and North America. Quagga mussels dominate in most lakes where they co-occur even though zebra mussels typically invade lakes first. A reversal to zebra mussel over time has rarely been observed. Laboratory experiments have shown that quagga mussels grow faster than zebra mussels when predator kairomones are present and this faster growth is associated with lower investment in anti-predator response in quagga mussels than zebra mussels. This led to the hypothesis that the dominance of quagga mussels is due to faster growth that is not offset by higher vulnerability to predators when predation rates are low, as may be expected in newly colonized lakes. It follows that in lakes with high predation pressure, the anti-predatory investments of zebra mussels should be more advantageous and zebra mussels should be the more abundant of the two species. In Onondaga Lake, NY, a meso-eutrophic lake with annual mussel surveys from 2005 to 2018, quagga mussels increased from less than 6% of the combined mussel biomass in 2007 to 82% in 2009 (from 3 to 69% by number), rates typical of this displacement process elsewhere, but then declined again to 11-20% of the mussel biomass in 2016-2018. Average total mussel biomass also declined from 344-524 g shell-on dry weight (SODW)/m 2 in 2009-2011 to 34-73 g SODW/m 2 in 2016-2018, mainly due to fewer quagga mussels. This decline in total mussel biomass and a return to zebra mussel as the most abundant species occurred as the round goby (Neogobius melanostomus) increased in abundance. Both the increase to dominance of quagga mussels and the subsequent decline following the increase in this molluscivorous fish are consistent with the differences in the trade-off between investment in growth and investment in defenses of the two species. We predict that similar changes in dreissenid mussel populations will occur in other lakes following round goby invasions, at least on the habitats colonized by both species.

Factors determining selective predation of the common carp on quagga versus zebra mussels

“…Zebra mussels were found to develop thicker shells under higher predation pressure as a result of phenotypic plasticity (induced response) (Naddafi & Rudstam, 2014b; Natesan & Strayer, 2016) or evolutionary changes (Czarnołęski et al., 2006). The more efficient anti‐predation defence could explain the reinstated dominance of the zebra mussel in a North American Lake Onondoga (reversing its earlier displacement by the quagga mussel) following the appearance of the molluscivorous round goby in the lake (Rudstam & Gandino, 2020). Although both mussel species responded to risk cues by decreasing their growth rates, and increasing attachment and shell strength, these changes were more pronounced in zebra than quagga mussels (Naddafi & Rudstam, 2014a, 2014b).…”

“…However, the observed ongoing reduction in the zebra mussel population, and parallel expansion of the quagga mussel in Lake Balaton (Balogh et al., 2018), must be linked to other reasons than consumptive predation effects, as this phenomenon occurs in contrast to the observed fish preferences. However, higher energy partitioning into anti‐predator defence may promote zebra mussels in environments experiencing high levels of predatory pressure (Natesan & Strayer, 2016; Rudstam & Gandino, 2020). This factor may contribute to explaining these exceptional cases, when the competitive advantage of zebra over quagga mussels was detected in the field (Rudstam & Gandino, 2020; Strayer & Malcolm, 2013; Zhulidov et al., 2010).…”

“…However, higher energy partitioning into anti‐predator defence may promote zebra mussels in environments experiencing high levels of predatory pressure (Natesan & Strayer, 2016; Rudstam & Gandino, 2020). This factor may contribute to explaining these exceptional cases, when the competitive advantage of zebra over quagga mussels was detected in the field (Rudstam & Gandino, 2020; Strayer & Malcolm, 2013; Zhulidov et al., 2010). Conversely, when predatory pressure is low, this difference could contribute to the invasion success of the quagga mussel, partitioning more energetic resources into growth and reproduction.…”

“…In fact, weaker anti‐predator responses and constitutive defence mechanisms of the quagga mussel compared to zebra mussel were observed and postulated as a potential source of the advantage of the former over the latter in novel areas, as enabling it to save energetic resources and partition them to growth and reproduction (Naddafi & Rudstam, 2014a, 2014b). However, in the presence of natural enemies with high predation pressure, the more efficient anti‐predator defence is likely to be beneficial (Natesan & Strayer, 2016; Rudstam & Gandino, 2020).…”

Serial invasions can disrupt the time course of ecosystem recovery

“…While quagga mussels quickly became dominant in all lakes they invade 25,64 , detailed mussel data were available only in Oneida Lake. However, the time dynamics of quagga mussels replacing zebra mussels is similar across lakes 64,65 and we therefore assumed that relative dreissenid species abundance followed a similar pattern in the two Dutch lakes. More intermittent data on zebra and quagga mussel densities in the two Dutch lakes that suggest similar fast replacement of zebra mussels by quagga mussels 52 .…”