Differential stimulation and suppression of phytoplankton growth by ammonium enrichment in eutrophic hardwater lakes over 16 years

Abstract

Previous research suggests that fertilization of surface waters with chemically reduced nitrogen (N), including ammonium (NH4 ), may either enhance or suppress phytoplankton growth. To identify the factors influencing the net effect of NH4 , we fertilized natural phytoplankton assemblages from two eutrophic hardwater lakes with growthsaturating concentrations of NH4Cl in 241 incubation experiments conducted biweekly May–August during 1996– 2011. Phytoplankton biomass (as chlorophyll a) was significantly (p < 0.05) altered in fertilized trials relative to controls after 72 h in 44.8% of experiments, with a marked rise in both spring suppression and summer stimulation of assemblages over 16 yr, as revealed by generalized additive models (GAMs). Binomial GAMs were used to compare contemporaneous changes in physico-chemical (temperature, Secchi depth, pH, nutrients; 19.5% deviance explained) and biological parameters (phytoplankton community composition; 40.0% deviance explained) to results from fertilization experiments. Models revealed that that the likelihood of growth suppression by NH4 + increased with abundance of diatoms, cryptophytes, and unicellular cyanobacteria, particularly when water temperatures and soluble reactive phosphorus (SRP) concentrations were low. In contrast, phytoplankton was often stimulated by NH4 + when chlorophytes and non-N2-fixing cyanobacteria were abundant, and temperatures and SRP concentrations were high. Progressive intensification of NH4 + effects over 16 yr reflects changes in both spring (cooler water, increased diatoms and cryptophytes) and summer lake conditions (more chlorophytes, earlier cyanobacteria blooms), suggesting that the seasonal effects of NH4 + will vary with future climate change andmodes of N enrichment. Since the commercialization of the Haber-Bosch process in the 1940s, the global pool of manufactured nitrogen (N) has increased nearly 20-fold (Glibert et al. 2006, 2014a), resulting in large increases in runoff and atmospheric deposition of reactive N (Nr) to both freshwaters and coastal marine ecosystems (Galloway et al. 2008; Howarth 2008; Beusen et al. 2016). The combined effects of near-exponential increases in use of N-based agricultural fertilizers and growth of stormand waste-water effluent discharge (Bernhardt et al. 2008) have resulted in a more than twofold increase in total N-loads entering downstream river basins in many parts of the world (Green et al. 2004; Howarth 2008). In turn, not only have increases in total N fluxes intensified eutrophication of many coastal (Rabalais et al. 2002; Howarth and Marino 2006) and freshwater systems (Leavitt et al. 2006; Bunting et al. 2007; Glibert et al. 2014a; Paerl et al. 2015), but there has been an increase in the proportion of chemically reduced forms N, including ammonium (NH4 ) and urea, relative to nitrate, NO3 − (Glibert et al. 2006, 2014a, 2016, Glibert 2017). With a growing global population and anticipated doubling of fertilizer N application (Glibert et al. 2006, 2014a), the global pool of Nr should double by 2050 (Galloway et al. 2008) resulting in increased pollution of surface waters with reduced N. While an extensive body of literature has shown that increasing loads of Nmay promote eutrophication and the development of harmful algal blooms in marine systems (Glibert et al. 2006, 2014a; Howarth and Marino 2006; Zehr and Kudela 2011), the role of N in eutrophication of freshwater systems is less certain (Paerl et al. 2016; Schindler et al. 2016). In part, different *Correspondence: [email protected] Present address: Alberta Environment and Parks, Edmonton, Alberta, Canada This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Additional Supporting Information may be found in the online version of this article. Special Issue: Long-term Perspectives in Aquatic Research. Edited by: Stephanie Hampton, Matthew Church, John Melack and Mark Scheuerell.