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2016 Trophic Dynamics of Shrinking Subarctic Lakes

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2016 Trophic Dynamics of Shrinking Subarctic Lakes Oecologia DOI 10.1007/s00442-016-3572-y ECOSYSTEM ECOLOGY – ORIGINAL RESEARCH Trophic dynamics of shrinking Subarctic lakes: naturally eutrophic waters impart resilience to rising nutrient and major ion concentrations Tyler L. Lewis1,3 · Patricia J. Heglund2 · Mark S. Lindberg1 · Joel A. Schmutz3 · Joshua H. Schmidt4 · Adam J. Dubour1 · Jennifer Rover5 · Mark R. Bertram6 Received: 15 May 2015 / Accepted: 24 January 2016 © Springer-Verlag Berlin Heidelberg 2016 Abstract Shrinking lakes were recently observed for chlorophyll concentrations, remained unchanged in both several Arctic and Subarctic regions due to increased shrinking and stable lakes from the 1980s to 2010s. Mov- evaporation and permafrost degradation. Along with lake ing up the trophic ladder, we found significant changes in drawdown, these processes often boost aquatic chemical invertebrate abundance across decades, including decreased concentrations, potentially impacting trophic dynamics. abundance of five of six groups examined. However, these In particular, elevated chemical levels may impact pri- decadal losses in invertebrate abundance were not limited mary productivity, which may in turn influence popula- to shrinking lakes, occurring in lakes with stable surface tions of primary and secondary consumers. We examined areas as well. At the top of the food web, we observed that trophic dynamics of 18 shrinking lakes of the Yukon Flats, probabilities of lake occupancy for ten waterbird species, Alaska, that had experienced pronounced increases in including adults and chicks, remained unchanged from the nutrient (>200 % total nitrogen, >100 % total phosphorus) period 1985–1989 to 2010–2012. Overall, our study lakes and ion concentrations (>100 % for four major ions com- displayed a high degree of resilience to multi-trophic cas- bined) from 1985–1989 to 2010–2012, versus 37 stable cades caused by rising chemical concentrations. This resil- lakes with relatively little chemical change over the same ience was likely due to their naturally high fertility, such period. We found that phytoplankton stocks, as indexed by that further nutrient inputs had little impact on waters already near peak production. Communicated by Ulrich Sommer. Keywords Alaska · Aquatic invertebrates · Eutrophication · Waterbirds · Resilience * Tyler L. Lewis [email protected] 1 Department of Biology and Wildlife and Institute of Arctic Introduction Biology, University of Alaska Fairbanks, Fairbanks, AK 99775, USA The highest global concentration of lakes occurs at Arctic 2 US Fish and Wildlife Service, 2630 Fanta Reed Road, and Subarctic latitudes (Verpoorter et al. 2014), providing La Crosse, WI 54603, USA important habitat for a diversity of wildlife species. The 3 US Geological Survey, Alaska Science Center, regions’ abundant lakes are largely a byproduct of its cold 4210 University Drive, Anchorage, AK 99508, USA climate, in which short ice-free seasons limit evapotran- 4 US National Park Service, Central Alaska Network, spiration and widespread permafrost inhibits soil perme- 4175 Geist Road, Fairbanks, AK 99709, USA ability (Ford and Bedford 1987). In recent decades, how- 5 US Geological Survey, Earth Resources Observation ever, Arctic and Subarctic areas have experienced a period and Science (EROS) Center, 47914 252nd Street, Sioux Falls, SD 57198, USA of unprecedented warming (New et al. 2011), potentially stressing the region’s long-term water balance. In particu- 6 US Fish and Wildlife Service, Yukon Flats National Wildlife Refuge, 101 12th Avenue, Room 264, Fairbanks, AK 99701, lar, warmer temperatures may lead to longer ice-free sea- USA sons and increased evaporative water loss (Magnuson et al. 1 3 Oecologia 2000; Smol and Douglas 2007a, b), while simultaneously energy flow (Pinder et al. 2005). As ions concentrate in increasing drainage of lake water via degradation of extant shrinking lakes (Lewis et al. 2015a), raising salinity levels, permafrost (Jorgenson et al. 2001; Jepsen et al. 2013a, b). invertebrates with low salt tolerances may become osmoti- To date, net losses in lake surface area have been docu- cally stressed, causing reduced growth or death (James et al. mented for certain Arctic and Subarctic regions of Alaska 2003). Hence, simultaneous increases of nutrients and ions (Riordan et al. 2006; Rover et al. 2012), Canada (Smol and in shrinking lakes may have varying effects on invertebrate Douglas 2007a, b; Carroll et al. 2011), and Siberia (Smith abundance, favoring some taxa while harming others. et al. 2005). Aquatic invertebrates constitute the primary prey base Two of the major processes causing losses in lake sur- for a variety of predators in Arctic and Subarctic lakes, face area—increased evaporation and permafrost thaw— including fish and waterbirds (Lewis et al. 2015b). Accord- may simultaneously generate pronounced changes in water ingly, changes in invertebrate abundance may transfer chemistry (Lewis et al. 2015a). Increased evaporation, if upward to the highest trophic levels, thereby influencing not balanced by concurrent increases to water inputs, con- distributions and abundance of several animals that hold centrates solutes into smaller water volumes. Lakes that significant anthropogenic and economic value. In this man- lose water in this manner tend to exhibit greater increases ner, rising nutrient concentrations in shrinking lakes may in nutrient and ion concentrations than those that lose water ultimately cascade across multiple trophic levels, from pri- via surface outflow or subsurface infiltration (Fritz 1996). mary producers to aquatic invertebrates to predators (Car- At the same time, thawing permafrost, by exposing previ- penter et al. 1985). Such multi-trophic cascades have been ously frozen organic matter to decomposition and flush- experimentally demonstrated in freshwater systems through ing, may increase nutrient and ion concentrations in nearby the use of artificial fertilization; long-term additions of lakes (Petrone et al. 2006; Wrona et al. 2006). Overall, phosphorus to an Arctic stream caused a positive response recent research has indicated that shrinking lakes, relative at all trophic levels, including increases in algal stocks, to their stable counterparts, have higher specific conductivi- grazing invertebrate densities, and fish growth rates (Slavik ties (Roach et al. 2011), indicative of higher ion loads, and et al. 2004). In addition to multi-trophic impacts caused by higher nitrogen and phosphorus concentrations (Corcoran nutrient additions, pronounced changes in salinity may also et al. 2009; Lewis et al. 2015a). impact top-level predators by causing osmotic stress, espe- Despite these compelling trends for shrinking lakes, lit- cially for fishes, while having little impact on waterbirds tle is known about how such chemical changes may impact and other semi-aquatic species (James et al. 2003). ecosystem processes. In general, nitrogen and phosphorus, Our study was situated on lakes of the Yukon Flats, Alaska, rather than light or carbon, limit productivity in shallow which are characterized by their shallow depth, colored water, Arctic and Subarctic lakes (Ogbebo et al. 2009). Accord- and high fertility, with over 70 % classified as eutrophic or ingly, as nitrogen and phosphorus levels increase, shrinking hypereutrophic on the basis of their nutrient loads (Heglund and lakes may experience elevated productivity, in which the Jones 2003). In recent decades, high evaporation rates (Ander- added nutrients stimulate primary production and thereby son et al. 2013), decreased snowfall (Jepsen et al. 2013b), and add more overall energy to the lake ecosystem (Dodson thawing permafrost (Jepsen et al. 2013a) have contributed et al. 2000). Increased primary productivity at the base of to net losses in lake surface area across this Subarctic region. the food web may then transfer upward to primary con- These losses in lake area caused substantial chemical changes; sumers, thereby driving increases in their abundance and of 55 lakes originally sampled for water chemistry during biomass (Peterson et al. 1993; Slavik et al. 2004). In north- the period 1985–1989, eighteen shrank over the intervening ern lakes, primary consumer communities are typically 25 years, leading to mean solute concentrations that had, by dominated by aquatic invertebrates, whose populations 2010–2012, increased by 237 % for total nitrogen, 131 % for may quickly track changes in primary productivity because total phosphorus, 49 % for calcium, 510 % for chloride, 66 % of their low generation times and high fecundity (Greig for magnesium, and 118 % for sodium (Lewis et al. 2015a). et al. 2012). For example, artificial fertilization of a shal- In particular, the more than doubling of nitrogen and phospho- low Arctic lake caused increased benthic and planktonic rus concentrations occurred despite many of these lakes being primary production, which in turn supported a three- to eutrophic since the 1980s. Conversely, of the remaining 37 fivefold increase in snail densities (Hershey 1992; Hobbie lakes with stable surface areas, mean chemical concentrations et al. 1999). However, chironomid densities in this same changed much less over the same time period: 76 % for total + Arctic lake were unaffected by nutrient additions, demon- nitrogen, 50 % for total phosphorus, 10 % for calcium, − + strating that the response of invertebrates to fertilization 118 % for chloride, 49 % for magnesium, and 2 % for + + − varies widely by taxa. In addition to nutrients, abundance sodium
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