Symposium 7 Ecological Processes across the Salinity Divide. Contrasts and Comparisons in Marine and Great Lakes Ecosystems

In Milwaukee, Wisconsin, bordering Lake Michigan, this special ESA symposium in August 2008 was a forum for comparison and discussion of marine and Laurentian Great Lakes ecology. The Great Lakes are, in many ways, neither limnology nor oceanography, and both limnology and oceanography. Most limnology texts deal little with the Great Lakes. For example, Wetzel's (2001) index directs the reader to only one page, which covers the glacial aspect of their formation. While not indexed under “Great Lakes,” aspects of their hydrodynamics are covered in Wetzel's fine book, but how these meso-oceanic dynamics relate to Great Lakes biota is not discussed. Great Lakes hydrodynamics have much in common with oceanography, particularly with regard to the importance of earth spin in producing large-scale water mass movements, such as upwellings and downwellings (Mortimer 2005). The marine scale and fetch of the Great Lakes' produces waves dangerous enough to sink ships 200+ m long, such as the Edmund Fitzgerald (Lightfoot 1976, Hultquist et al. 2006). The waves increasingly attract board surfers, as featured in recent movies, “Step Into Liquid” (Brown 2003) and “Surf's Up” (Rhymer et al. 2007). But, in common with limnology, the Great Lakes' native flora and fauna are primarily freshwater. A few species are considered relics of former marine connections during Pleistocene glaciation. Consequently, Great Lakes ecologists are challenged by the need to think about limnological biota in the context of meso-oceanographic physics. Training and reading in both limnology and oceanography are required. This symposium in Milwaukee, Wisconsin was based on the proposition that the Great Lakes provide a fertile interface between limnology and oceanography. We propose that comparative study of ecosystem function of both marine and Great Lakes systems will foster a more profound understanding of both. Jim Kitchell initiated the symposium with an historical overview of key ecological concepts and how they migrated and/or were altered across the salinity divide. The first concept was the size-selective predation and size efficiency hypothesis developed by Brooks and Dodson (1965) to explain changes in zooplankton size and species composition in response to introduction of the alewife (Alosa pseudoharengus), a marine planktivorous herring, into some Connecticut lakes. The hypothesis posits that larger zooplankter species are competitively superior to smaller species at suspension feeding, but more vulnerable to size-selective predation by fishes. The application of the concept to the Great Lakes was rapid because of the dramatic invasion of Lake Michigan and the population explosion of the alewife with consequences similar to the Connecticut lakes (Wells 1970). The hypothesis stimulated an explosion of zooplankton grazing studies especially focused on Cladocera. The migration of this idea to marine research was limited in part because suspension-feeding Cladocera are nearly absent from marine systems (except in estuaries), and the demonstration by Strickler and co-workers that the dominant marine crustacean suspension feeders, calanoid copepods, do not filter algal prey, but accept and reject individual particles by modifying feeding currents, based on aspects of prey quality (Koehl and Strickler 1981, Strickler 1982). The second concept, that of a keystone predator species that alters community structure was first presented by Paine (1966, 1980). Paine's concept was illustrated by the impact of a predaceous starfish on the abundance and distribution of intertidal invertebrates, especially mytilid mussels and barnacles. The potential common features of Brooks and Dodson's and Paine's work was noted by Hall et al. (1970) in an experimental pond study, and these diverse research ideas were consolidated by Carpenter et al. (1985) as the trophic cascade concept. Arguably the trophic cascade concept was first proposed more poetically by Aldo Leopold (1949) in the Sand County Almanac: “I have watched the face of many a new wolfless mountain and seen the south-facing slopes wrinkle with a maze of new deer trails. I have seen every edible bush and seedling browsed, first to anemic desuetude, and then to death.” Leopold's seemingly causal observations precede documentation of dramatic resurgence of certain flora of Yellowstone National Park as a consequence of the reestablishent of wolves (Canis lupis) (Ripple et al. 2001). The trophic cascade concept stimulated contrary arguments from other ecologists that ecosystem function is driven “bottom-up” by lower trophic levels, especially primary production. Perhaps a sign of maturity and generality of the concept of the trophic cascade is its practical application via biomanipulation (Shapiro and Wright 1984). This application arose from study of freshwater resources with the idea that ecosystem function (and health) can be manipulated by human intervention of adjusting the top predators, i.e., that fish can change water quality. This has had a strong influence on lake management, especially in Europe in freshwater and to a lesser extent marine (Baltic Sea) ecosystems, as a top predator may even influence biogeochemistry and determine whether nitrogen or phosphorus limits primary production (Elser et al. 1988). Freshwater research also derived the concept of a trade-off between predation risk and growth (Werner et al. 1983), a trade-off that the presentation by Rudstam et al. applied to vertical migration of mysid “shrimps” in Lake Ontario. Marine research contributed the Match/Mismatch hypothesis that recruitment of higher trophic level species, particularly fishes, was dependent upon a synchrony including a spring bloom, grazing zooplankton, and larval fishes (Cushing 1969). Migration of this concept across the salinity barrier inspired the study by Rice et al. (1987) of a Lake Michigan fish, the bloater (Coregonus hoyi), which is one of the most widely cited supporting papers. The presentation by Dettmers et al. (2005) applies the concept to yellow perch (Perca flavescens) in Lake Michigan (see presentation by Dettmers below). The introduction of invasive species into freshwater and marine ecosystems has caused radical changes in the ecology of some aquatic ecosystems (see presentation by Hecky et al., below), and is a chief cause of changes in biodiversity and trophic structure in the Great Lakes and marine coastal waters. Understanding the ecological changes associated with invasive species spans marine and freshwater research and illustrates many of the key ecological processes outlined by Kitchell by disrupting previous ecosystem balances. In the Laurentian Great Lakes, successive waves of invasive species, chiefly introduced and spread via ballast water from ocean-going vessels, can be viewed as an ongoing, unplanned biomanipulation experiment. Hugh MacIsaac presented an examination of modern invasive species research, starting with the publication of Charles Elton's (1958) seminal book The Ecology of Invasions by Animals And Plants, which continues to have a important influence on invasive species research. (In 2006 the book was cited as 186 in ISI-listed publications.) Interest in invasion ecology increased dramatically during the early 1990s as a wave of freshwater (e.g., Dreissena polymorpha, D. bugensis, Bythotrephes longimanus), and marine (e.g., Carcinus maenas, Caulerpa taxifolia, Mnemiopsis leidyi, Mytilus galloprovincialis, Spartina spp.) invasive species were documented. The escalating rate of publication on aquatic and terrestrial invasive species (Ricciardi and McIsaac 2008) has recently been coupled with concerns about ecosystem vulnerability to climate change. With the enormous ecological impact of invasive species, research focus in invasive species is likely to continue. After Kitchell's Introduction and MacIsaac's overview of invasive species, the subsequent symposium speakers presented ideas from Great Lakes and/or marine environments, many of which explored aspects of these key ecological concepts. Four presentations explored biogeochemical ecology of marine and freshwater ecosystems, and the concluding three presentations were focused primarily on the upper trophic levels. Between these clusters of talks was presentation on undergraduate research. Consecutive presentations by Bob Hecky, Sairah Malkin, Tedy Ozersky, David Depew, Adam Houben, and Stephanie Guildford (presented by Sairah Malkin) and Cathy Pfister demonstrated important effects of mussel beds in providing inorganic nutrients to attached macrophytic algae. Pfister's example came from intertidal pools in the Pacific Northwest, with the mussel Mytilus californianus (Pfister 2007, Pfister et al. 2007). The Great Lakes “parallel” was a consequence of the invasion by dreissenid mussels (Dreissena polymorpha and D. bugensis) (Hecky et al. 2004), which now occupy a niche similar to marine mytilid mussels and attach to hard substrata via byssal threads. Thus, despite the paradigm that large-scale physical processes in oceans (e.g., upwelling) and the Great Lakes (e.g., currents) supply inorganic nutrients, both studies showed pronounced local enrichment of the limiting macronutrient effect arising from mussel excretion as phosphorus for the Great Lakes and nitrogen for the marine intertidal system. While the Great Lakes invasion by dreissenids can be viewed as an unplanned “biomanipulation” experiment, Pfister (2007) carried out manipulative experiments in replicate tidepools to reveal the impact of M. californianus ammonium excretion in stimulating primary production and growth of the macroalga Prionitis lanceolata (Fig. 1). Hecky and co-workers have been using in situ benthic chambers to quantify P excretion by dreissenid mussels and compare these rates with P loading from the catchment (T. Ozersky et al., unpublished manuscript) and stimulation of benthic algal growth (Malkin et al. 2008). In terms of “trophic cascades,” these presentations demonstrated that bottom-up and top-down approaches are both important and not mutually exclusive approaches for understanding aquatic ecology. Because bivalves are suspension feeders on phytoplankton, both mytilid and dreissenid mussels provide avenues for benthic–pelagic coupling in marine, estuarine, and freshwater ecosystems (Newell 2004, Wall et al. 2008). In Pfister's marine system, epilithic algae and seaweeds close to M. californianus benefit from the coupling through the release of inorganic N (Fig. 1), presumably an ancient interaction. Hecky et al. argued that such benthic–pelagic coupling in the Great Lakes arose recently, with dreissenid invasions over the last ~20 years. Efficient grazing by dreissenids has resulted in increased water clarity, along with increased sedimentation of particulate P from the water column, concentrating scarce P resources in the nearshore benthos (Fig. 2). Estimates of allochthonous P inputs and P excretion rates suggest that the benthic growth of the nuisance alga Cladophora may depend on P excreted from mussels (Bootsma et al. 2005, T. Ozersky et al., unpublished manuscript). Concentration of P in the benthos has stimulated nearshore benthic production (Hecky et al. 2004) and could also be changing phytoplankton diversity in the open lake (Barbiero et al. 2006). In the marine example, the stimulation of algal production due to mussel excretion was also related to significantly higher δ15N values in tidepool seagrasses exposed to mussel-excreted N. Pfister also presented evidence for tidepool transformations of inorganic N from mussel excretion mediated by a dynamic but as yet poorly understood microbial community. (Top) The mean ammonium concentrations during low tide in tide pools with their natural complement of mussels, tide pools where mussels were experimentally removed (arrow), and open. Points are means of five replicates (±SE). At the six dates, ammonium was significantly higher where mussels were present (repeated measures ANOVA, P < 0.040). (Bottom) The effect of the ammonium on stimulating growth of the red alga Prionitis lanceolata. Points are means of 1–3 individuals (±SE) for each tide pool. Algal area was significantly larger in July and August when exposed to mussels (RM ANOVA P < 0.034). Figures modified from Pfister (2007). The Nearshore Shunt Hypothesis as proposed by Hecky et al. (2004), describing the change in near-shore–offshore and benthic–pelagic nutrient exchange in the Laurentian Great Lakes since the establishment of dreissenid mussels. Pfister compared quantitative estimates of regenerated N from mussels in intertidal marine vs. Great Lakes ecosystems using published estimates of density and excretion rates (Bayne 1977, Suchanek 1979, Gardner et al. 1995). In the marine intertidal, mussels can excrete grams of ammonium m−2·d−1 whereas in the Great Lakes, this estimate was < 0.3 g N·m−2·d−1. However, although regenerated N is important in marine systems limited by upwelling for NO3− supply (Dugdale 1967), microbial transformation, tidal flushing, and wave action may dilute the local effects of mussel N excretion on intertidal ecosystems. In the Great Lakes, although mussel excretion will provide inorganic N to benthic photoautotrophs, nitrate availability is consistently high enough to expect little effect of additional inorganic N (see Sterner and Seegers' presentation below). However, dreissenid mussel excretion will have a much stronger effect via supply of chronically limiting P. Despite the difference in focus on N vs. P, the influence of mussels on nutrient cycling and pelagic–benthic coupling have strong similarities across the salinity divide, and suggest that alterations to the benthic animal assemblage can have “ripple effects” throughout the ecosystem. Steven Wilhelm provided an overview of the viral nanoscale contribution to global-scale aquatic ecological processes through biogeochemical cycling and as agents of genetic change. A core development in aquatic science was the recognition of the microbial contribution to pelagic food webs and nutrient regeneration (Pomeroy 1974, Azam et al. 1983), and the role of viruses in nutrient regeneration has more recently been recognized (Fig. 3). In common with other aspects of aquatic ecology, we know much more about viruses in marine than in freshwater ecosystems; over 1000 publications on marine viruses contrast with only 11 on viruses in all the Laurentian Great Lakes. Schematic showing the role of viral lysis in the aquatic microbial food web, in context with a more traditional food chain model. Modified from De Bryn et al. (2004). To understand the biogeochemical role of viruses, their abundance needs to be comprehended: ~1030 viruses in the oceans (Brussaard et al. 2008) and ~1011 viruses/L in Lake Erie (Wilhelm and Matteson 2008). Viral cell lysis releases nutrients (108–109 t C, globally) and drives nutrient transfer from the particulate (biological) to the dissolved phase. The key role of viruses in the aquatic microbial food web is conceptualized in Fig. 3. Hutchinson's (1961) “Paradox of the Plankton” expresses the apparent support of a wider range of planktonic organisms in aquatic ecosystems than the law of competitive exclusion might allow (Hardin 1960). Hutchinson (1961) and later, others, proposed a range of environmental factors to explain the paradox, but viral lysis of cells and the associated nutrient release could provide additional resolution to the paradox (Wilhelm and Matteson 2008). In marine and freshwater ecosystems, viral cell lysis can release significant bioavailable quantities of limiting nutrients to maintain nutrient cycling and cell production (Gobler et al. 1997, DeBruyn et al. 2004, Poorvin et al. 2004). In the Great Lakes, where P is often chronically limiting, viral lysis of phytoplankton could release 122–1080 nM P daily, a similar magnitude to anthropogenic P loadings (Dean et al. 2008). This biogeochemical role of viruses is likely to be similar in marine and freshwater ecosystems, but the key difference is that the nutrients are iron in open oceans and phosphorus in freshwater ecosystems. Moreover, these nutrients are released to the system as organic complexes, which may provide a selective advantage for organisms capable of assimilating these nutrients relative to those equipped to assimilate only inorganic forms. Viruses are also known to be agents of genetic change by facilitating gene transfer between hosts (Hendrix et al. 1999, Lindell et al. 2004). Some viruses carry genes that code for functional host proteins (e.g., psbA and psbD genes encoding the D1 and D2 proteins in photosynthetic electron transport [Mann et al. 2003, Sullivan et al. 2005]). Viruses can possibly regulate these genes to control host metabolic pathways to maintain host function. Host psbA genes are widespread in aquatic virioplankton, and sequences reveal distinct phylogenies for marine and freshwater viruses (Bench et al. 2008, Wilhelm and Matteson 2008). Emerging and future developments in exploring this role of viruses may employ recent metagenomics approaches to viruses and their host communities (Angly et al. 2006). Wilhelm concluded that the factors controlling viral infections in ecosystems are still largely a mystery, and also challenged the audience to explore marine and Great Lakes ecological processes during less comfortable seasons of autumn, winter, and early spring! Bob Sterner and Bridget Seegers concluded the biogeochemical talks with a perspective on ecological stoichiometry across marine and freshwater ecosystems. Ecological stoichiometry examines how the elemental content of an organism shapes its ecology. Stoichiometric formulae (the ratios of the elements composing an individual) vary among species and the ratios change in response to an imbalance in food quality and with differences in nutrient cycling processes, within and between ecosystems. In ecological stoichiometry the ratio of C:N:P at the base of the food web is a crucial parameter in consumer growth, nutrient cycling, and other ecological dynamics. Study of nutrient stoichiometry was founded in the work of Alfred C. Redfield (1890–1983) who found a conserved ratio of 106:16:1 for C:N:P in marine seston (live algae, other cells, and dead suspended material) in oceanic surface water. This implies that, for the broad spectrum of sestonic organisms, the optimal ratio of N:P for growth approximates 16:1, and Redfield found that the deep-sea water had a similar ratio. He suggested that the biota modified of nutrients to its stoichiometry Sterner and Seegers found that open seston ratios are less than in and ratios are higher in lakes than in the oceans (Fig. structure can the et al. found that the introduction of into an lake caused a cascade of including the of the increased zooplankton and a in zooplankton N:P and seston Freshwater and marine seston C:N:P ratios are known to from Sterner et al. seston ratios from aquatic ecosystems from lakes to the open are on a or N:P ratios showed slopes of a ratio between of et al. 2008). However, Sterner and Seegers noted an within of water with slopes for and when the were as and (Fig. in Sterner et al. 2008). The for this is not yet but may that the efficiency of N or P with The coupling between seston and P were explored in Lake a in which production is limited by P availability et al. 2007). In Lake the is at m during For m the macronutrient stoichiometry was However, seston and P with and showing ratios for surface or water This needs to be considered when for and C:N:P at seston P than C, to lower ratios with In surface a high nutrient ratio content relative to P. The ratios for the three were more N:P ratios reveal that seston P is the most supporting a nutrient efficiency model. P is the most limiting in the system, and N are more in response to that vary with is still how ratio to and such ratios may only be for in both marine and freshwater systems on recruitment and of new of as presented by and This “bottom-up” which aquatic research is by the National by the of research, in aquatic research at more than including one Great Lakes The of the on from and the host and research At the of for Great Lakes for from the in research over a to the is and an and research are including research on the and from to on the Laurentian and and experimental and hypothesis and and and with and research in a where they are exposed to and the the was or to their have to within marine and freshwater research, including one who is on in and argued that the early of some Great Lakes fishes that of marine fishes, more than the of most freshwater fishes in lakes. of freshwater fishes is considered to be during the and is a pelagic for a species, is et al. the for marine fishes is that they have pelagic and a in which and is during this pelagic phase. This has been the for the of marine fish at the larval is the of and such as primary and production of zooplankton and of larval may also depend on of physical and can carry to In the Great Lakes, recruitment of some fishes more the marine one of the primary cited by marine ecologists as evidence for the from work on a Great Lakes the bloater et al. and are pelagic from larval through although the has aspects to its are challenged by the need to to coastal Dettmers et al. presented a more example of yellow perch (Perca flavescens) in Lake A yellow perch recruitment to zooplankton the of a (Fig. perch only in nearshore of lakes and also along of Lake with in a on the The are and hydrodynamics but the are and water is not much of a for yellow perch in lakes with from of to a few and but may be a in a lake the size of Lake Michigan, where the is might expect that, to to the scale of Lake Michigan, the larval yellow perch may have that the based both on larval et al. and et al. is that the do in the of by may be by in (Fig. Lake Michigan may have that this marine of early The most similar Great Lakes, lakes and have yellow perch to Lake is Lake Erie hosts a population of yellow but is by the of the Great Lakes. between zooplankton density and yellow perch recruitment for Lake Modified from and Dettmers in of larval yellow perch in Lake Michigan from an along the Lake Modified from et al. and presented the example of Great Lakes and marine the of the Great Lakes and and marine nor are are marine and are primarily marine, the few freshwater species considered glacial for both phytoplankton and In the Great Lakes the of is about an of phytoplankton and zooplankton in the and primarily zooplankton in the and and are important as to higher trophic levels. is the of the Great Lakes' and the first or second most important prey for the most native and fishes, the alewife and and a dramatic vertical to For vertical distribution is dependent on the of the as as the of the system, with to during new vs. the may in the water their are than (Fig. Rudstam et al. that the extent of the vertical migration of both and has to predation risk than where prey are most with the need to Thus, many of the between and and their prey and at the upper of their vertical (Fig. of and fish vertical distribution in Lake during the and The water is about the is a of at about are both within the and the base of the At the has to the base of the distribution of their fish predators, and their zooplankton prey August in Lake between their prey, and at the upper of the mysid that is based on a trade-off between the need to and the risk of Rudstam et al. concluded with a discussion of Lake an with a has vertical similar to both and and has within the system. The marine Great and are all important between phytoplankton and zooplankton to higher trophic levels, and an for across ecosystem To the the open and open Great Lakes to compared to terrestrial of of water that

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