Benthification of Freshwater Lakes

................................................................................................................................................................................575 Introduction ...........................................................................................................................................................................575 Benthification ........................................................................................................................................................................576 Epidemic of Benthic Stable States ........................................................................................................................................578 Long-Term Data ....................................................................................................................................................................578 Separating the Relative Importance of Declines in Total Phosphorus and Dreissena .........................................................578 Review from Other Systems ................................................................................................................................................ 580 Upside-Down Ecosystems Past and Future ..........................................................................................................................581 Physical versus Trophic Change .......................................................................................................................................... 582 Macrophytes versus Benthic Algae ......................................................................................................................................583 Conclusions ...........................................................................................................................................................................583 Acknowledgments .................................................................................................................................................................583 References .............................................................................................................................................................................583 576 Quagga and Zebra Mussels: biology, iMpacts, and control 1993, Ludsin et al. 2001); and (3) an accelerated rate of nonindigenous species introductions (e.g., Mills et al. 1994). Two of these anthropogenically-driven factors, planned reductions in phosphorus inputs and the unplanned introduction and spread of two efficient, invasive filter-feeders, zebra and quagga mussels (Dreissena polymorpha and Dreissena rostriformis bugensis), are frequently independently cited as the cause of recent increased clarity in north-temperate lakes. Increased water clarity is a potentially important alteration of physical structure that may have implications for a variety of ecosystem-level processes. However, defining the relative importance of Dreissena filter feeding and decreased nutrient inputs in promoting water clarity in lakes is complicated by the historical and temporal overlap in these two ecosystem drivers. Nonetheless, understanding which of these two factors, one planned and the other unplanned, is most responsible for returning lakes to a clearer state is crucial to lake and land management practices and to our understanding of ecological processes in aquatic ecosystems. Indeed, many north-temperate lakes currently have greater water clarity now than during the peak period of eutrophication. Negative consequences of eutrophication have spurred international policies to curb nutrient inputs and thereby ameliorate problems such as nuisance algal blooms. For example, in North America, reductions of nutrient loads in the Great Lakes began after the United States and Canada passed legislation during the early 1970s (e.g., the 1972 Clean Water Act and the Great Lakes Water Quality Agreement) that set target levels for phosphorus inputs. Further, research into the mechanisms underlying eutrophication and possible solutions contributed to the development of important concepts about ecosystem structure and function (Vollenweider 1968, Likens 1972, Shapiro and Wright 1984, Carpenter et al. 1985, McQueen et al. 1986). Phosphorus frequently limits phytoplankton growth in freshwater (Schindler 1977) and is usually implicated as the cause of eutrophication in lakes and rivers. Positive relationships between total phosphorus (TP) and standing crops of phytoplankton have been well documented (e.g., Dillon and Rigler 1974). Therefore, reductions in phosphorus loads via abatement programs likely resulted in lower standing stocks of phytoplankton. However, load reductions and declines in phosphorus levels occurred during the same time period as the introduction of a large number of nonindigenous species (Mills et al. 1994, Holeck et al. 2004), which also affected food web structure and hence productivity (Carpenter et al. 1985, McQueen et al. 1986). Consequently, defining the relative importance of these two potential factors in driving ecosystem-level change is a real challenge. Dreissenid mussels were introduced into the Great Lakes in 1986 (Carlton 2008) and have since spread to large areas across North America. Dreissenids are also widespread in Europe outside of their native Pontocaspian region. These mussels have been associated with reduced phytoplankton standing stocks and increased water clarity (e.g., Fahnenstiel et al. 1995a,b, Binelli et al. 1997, Higgins 2013). However, their spread coincided with the time period when nutrient loads were decreasing and similar changes in phytoplankton and water clarity were expected. Further, there is likely an interaction between TP and Dreissena effects because in addition to reducing phytoplankton standing stocks as measured by chlorophyll a, dreissenids modify the relationship between chlorophyll and TP so that chlorophyll levels are lower than would be expected for a given level of phosphorus (Higgins et al. 2011). It is unlikely that there will be an experimental answer to the question of the relative importance of these two anthropogenic drivers of ecosystem change as no intentional, whole-lake-scale studies on Dreissena introduction have been conducted. Consequently, the question remains: which of these two anthropogenic drivers of ecosystem change (reductions in phosphorus vs. dreissenid filter feeding) have had a greater impact on water clarity in north-temperate lakes? In this chapter, we present evidence that supports the theory that Dreissena, and not phosphorus reductions, is the more important driver of the observed improvements in water clarity. Further, we argue that changes in water clarity have triggered a suite of connected changes that increase the importance of benthic processes. We term this process “benthification” and propose that it is occurring over a broad geographic range and is having a strong influence on the structure and function of lake ecosystems.