Pelagic Phytoplankton Community Change‐Points Across
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Freshwater Biology (2017) 62, 366–381 doi:10.1111/fwb.12873 Pelagic phytoplankton community change-points across nutrient gradients and in response to invasive mussels † † , ‡ KATYA E. KOVALENKO*, EUAN D. REAVIE*, J. DAVID ALLAN , MEIJUN CAI*, SIGRID D. P. SMITH AND LUCINDA B. JOHNSON* *Natural Resources Research Institute, University of Minnesota Duluth, Duluth, MN, U.S.A. † School of Natural Resources and Environment, University of Michigan, Ann Arbor, MI, U.S.A. SUMMARY 1. Phytoplankton communities can experience nonlinear responses to changing nutrient concentrations, but the nature of species shifts within phytoplankton is not well understood and few studies have explored responses of pelagic assemblages in large lakes. 2. Using pelagic phytoplankton data from the Great Lakes, we assessed phytoplankton assemblage change-point responses to nutrients and invasive Dreissena, characterising community responses in a multi-stressor environment and determine whether species responses to in situ nutrients can be approximated from nutrient loading. 3. We demonstrate assemblage shifts in phytoplankton communities along major stressor gradients, particularly prominent in spring assemblages, providing insight into community thresholds at the lower end of the phosphorus gradient and species-stressor responses in a multi-stressor environment. We show that responses to water nutrient concentrations could not be estimated from large-scale nutrient loading data likely due to lake-specific retention time and long-term accumulation of nutrients. 4. These findings highlight the potential for significant accumulation of nitrates in ultra-oligotrophic systems, nonlinear responses of phytoplankton at nutrient concentrations relevant to current water quality standards and system-specific (e.g. lake or ecozone) differences in phytoplankton responses likely due to differences in nutrient co-limitation and effects of dreissenids. Keywords: algae, community thresholds, Dreissena, eutrophication, water quality phytoplankton directly respond to many stressors associ- Introduction ated with human development such as excess nutrients, Cycling of nitrogen and phosphorus, the two most limit- and can therefore be one of the early-warning signals for ing nutrients for primary production, has been greatly ecosystem change in response to stress (McCormick & altered by human activities (Falkowski, Fenchel & Delong, Cairns, 1994). 2008; Galloway et al., 2008; Canfield, Glazer & Falkowski, There is evidence that algal communities can experi- 2010; Bouwman et al., 2013). Primary producers are ence nonlinear changes in response to increasing nutri- strongly affected by nutrient limitation (e.g. Tilman, 1982; ent concentrations (Smucker et al., 2013a). The abrupt Wetzel, 2001), and changes in their assemblages in transition from macrophyte-dominated to an algal-domi- response to nutrients propagate up the food web through nated state is one of the classic examples of alternative a multitude of pathways including decreased diver- stable states (Scheffer & Jeppesen, 1998); however, the sity, increased biomass turn-over and overwhelming nature of species shifts within the phytoplankton assem- contribution of bloom taxa to the overall energy flow blage is not as well documented. In addition to nutrient (McCann & Rooney, 2009). In the pelagic zones of lakes, loading, proliferation of invasive filter feeders has been Correspondence: Katya E. Kovalenko, Natural Resources Research Institute, University of Minnesota Duluth, 5013 Miller Trunk Highway, Duluth, MN 55811-1442, U.S.A. E-mail: [email protected] ‡ Present address: College of Agriculture and Related Sciences, Delaware State University, Dover, DE, U.S.A. 366 © 2016 John Wiley & Sons Ltd Phytoplankton change-points 367 linked to major shifts in primary producer community well as in situ water nitrate and total phosphorus con- composition due to grazing and the resulting broader centrations, known to be relevant in water predictors for changes in food-web structure and nutrient cycling phytoplankton assemblages based on previous studies across aquatic ecosystems such as the shift from mostly (Reavie et al., 2014a). Some of the predictors examined pelagic to benthic–littoral energy pathways (Higgins & in our study are not necessarily stressors from the per- Vander Zanden, 2010; Karatayev, Burlakova & Padilla, spective of phytoplankton; however, these predictors are 2015a; Gallardo et al., 2016). Understanding the degree often referred to as stressors for consistency with other of nonlinearity in phytoplankton assemblage shifts and studies and to reflect the general perception of nutrient identifying key species responding to these anthro- loading. Our major goals were to (i) test whether there pogenic stressors is necessary to relate changes in water is a relationship between nitrogen loading and water quality, nutrient cycling and precipitation patterns to the nitrate concentrations, (ii) determine whether there is rest of the food web. This approach can contribute evidence of nonlinear changes in phytoplankton assem- strong ecology-based evidence for developing nutrient blage composition in response to in situ nutrient concen- criteria (Smucker et al., 2013a) and is particularly impor- trations and estimates of offshore environmental stress tant since there are few biotic indicators available for the (nitrogen loading and Dreissena abundance) and (iii) pelagic zones of large lakes, making it difficult to moni- examine key species responses along the stressor gradi- tor assemblage responses to such large-scale stressors as ents, characterise assemblage responses in a multi-stres- invasive species and nutrient loading. sor environment and test whether large-scale estimates The Laurentian Great Lakes have a long history of of nutrient loading can be related to similar assemblage anthropogenic stress affecting phytoplankton, often responses as in situ water nutrient concentrations. resulting in undesirable effects such as cultural eutrophi- cation (Stoermer, 1978). Excess phosphorus loading has most commonly been cited as the major causal agent in Methods water quality and algal problems (Conley et al., 2009). Data collection and processing Nitrogen concentrations in the Great Lakes region have also increased greatly over the past century (Han & The pelagic zones of the Laurentian Great Lakes, which Allan, 2012) and are likely implicated in changes encompass lakes Erie, Ontario, Huron, Michigan and throughout the ecosystem (e.g. Elser et al., 2010). Effects Superior, range from ultra-oligotrophic in the northern of nitrogen loading on pelagic phytoplankton dynamics GL to eutrophic-mesotrophic in the south. The standard received less attention than effects of phosphorus (but operating procedure for phytoplankton collection and see Reavie, Heathcote & Shaw Chra€ıbi, 2014a); but, there analysis is described in detail in the published proce- is evidence of nitrogen limitation and co-limitation of dures (USEPA, 2010) and a comprehensive summary is coastal algal biofilms (Cooper et al., 2016). More recently, provided by Reavie et al. (2014a). Briefly, water samples the extensive invasion of zebra and quagga mussels were collected during biannual synoptic sampling (Dreissena polymorpha and D. bugensis: Dreissenidae) (‘spring’ – April, ‘summer’ – August) from 72 standard throughout most of the basin has greatly impacted pri- pelagic stations throughout the Great Lakes (Fig. 1), mary production in the lakes by shunting energy flow with each station sampled each year in April and from the pelagic to the benthic food web (Hecky et al., August for a total of eight samples per station (2007–10). 2004; Bunnell et al., 2014). This has further altered phyto- Integrated water samples were collected from the rosette plankton communities, particularly in Lake Michigan sampler onboard the R/V Lake Guardian. In the labora- and Lake Huron (Reavie et al., 2014b), but the mechanis- tory, water samples were digested by acid persulfate tic processes that drive these phytoplankton changes are and measured by a Lachat QuikChem AE autoanalyzer still under discussion (e.g. Kerfoot et al., 2010). This (Hach Company, Loveland) for total phosphorus (Bar- + dreissenid invasion was ranked as the top environmen- biero et al., 2006). Nitrate nitrite (NOx) concentrations, tal threat out of the comprehensive list of 50 stressor hereafter referred to as nitrate due to much lower nitrite variables in the Great Lakes, according to a recent expert concentrations in open water, were determined by dia- survey (Smith et al., 2015), and is probably the most zotising with sulfanilamide dihydrochloride after nitrate important stressor relevant to pelagic autotrophs along was reduced by copper-coated cadmium (GLNPO, with atmospheric nutrient deposition. 2010). We used NOx because organic N and ammonia We examined responses of phytoplankton communi- were a very minor component of the TN budget (<0.2%) ties to Dreissena abundance and nitrogen (N) loading as and were no longer being measured at the pelagic © 2016 John Wiley & Sons Ltd, Freshwater Biology, 62, 366–381 368 K. E. Kovalenko et al. Fig. 1 Map of pelagic sampling stations in the Great Lakes superimposed on estimates of nitrate loading (percentile/quintiles) across the basin. See main text and Allan et al. (2013) for more details on nitrogen deposition and USEPA (2010) and Reavie et al. (2014a) for more details on the sampling stations. stations during the years of this study. We used total immersion [10009 or higher;