The influence of nutrients limitation on phytoplankton growth and microcystins production in Spring Lake, USA

Highlights

• Nitrogen or phosphorus addition alone was not sufficient to induce algal blooms.

• N + P treatment resulted in high concentrations of chlorophyll-a and microcystins.

• Past management strategy solely on reducing P loads is insufficient in Spring Lake.

• Reduction of both N and P are necessary to control algal blooms and MC production.

Abstract

Due to excessive loadings of nitrogen (N) and phosphorus (P), frequent blooms of harmful cyanobacteria and their associated cyanotoxins pose serious threats to recreational usage and human health. However, whether cyanobacteria growth and toxin production are limited by N, P, or both N + P is still not clear. Thus, we conducted a nutrient enrichment bioassay in situ in Spring Lake, a eutrophic lake in west Michigan, USA, to examine the influence of nutrient limitation on the proliferation of algal blooms and the production of microcystins (MC). N or P addition alone resulted in a slight increase in the concentration of chlorophyll-a (Chl-a), suggesting a positive effect on phytoplankton growth, but alone, neither were sufficient to induce algal blooms. In contrast, the combination of N and P had a significant and positive influence on phytoplankton growth and MC production. Compared to controls, the N + P treatment resulted in high concentrations of Chl-a and MC, as well as high pH and dissolved oxygen. In addition, significant increases were observed in different MC analogues for each treatment; the highest concentrations of intracellular MC-LR, -RR, -YR, and TMC (total MC) were found in the N + P treatment with values of 9.16, 6.10, 2.57, and 17.82 μg/L, respectively. This study suggests that at least in this temperate coastal lake, cyanobacterial blooms and associated MC are influenced more by combined N and P enrichment than by N or P alone, indicating that managing both nutrients is important for effectively reducing algal blooms and MC production.

Introduction

Excess enrichment of nutrients from both internal and external loading accelerates water eutrophication and promotes the growth of phytoplankton, leading to frequent cyanobacterial blooms and subsequent decline in water quality in freshwater ecosystems (Paerl et al., 2015; Smith et al., 2016; Xu et al., 2017). The role of nutrients, mainly nitrogen (N) and phosphorus (P), in controlling phytoplankton growth has received considerable attention but the results have been inconsistent (Conley et al., 2009; Paerl et al., 2016; Steinman et al., 2016). Some researchers consider P to be the primary nutrient limiting the occurrence of cyanobacterial blooms, and therefore they promote methods to reduce P input or inactivate P already in the lake, as the most effective method to restore freshwater ecosystems (Bormans et al., 2016; Lürling et al., 2016). However, according to the results of the nutrient enrichment bioassay by Xu et al. (2010) conducted in Lake Taihu, the third largest freshwater lake in China, it is more likely that bioavailable N is the key factor controlling the proliferation of cyanobacterial blooms, especially toxic Microcystis spp. blooms. Recently, Steinman et al. (2016) suggested that phytoplankton were P-limited and benthic algae were co-limited by N and P in hypereutrophic Lake Macatawa, USA. Therefore, limitation by N and/or P appears to vary depending on habitat (benthic vs. planktonic), local environmental conditions (e.g., ambient nutrient concentrations and light conditions), and the taxonomic composition of the algae (N₂-fixing and non-N₂-fixing cyanobacteria). Furthermore, the nutrients limiting phytoplankton growth can vary seasonally, likely due to temperature and meteorological conditions, with P limitation often occurring in spring and winter, and N limitation being observed in summer and fall when the environmental conditions are more conducive to phytoplankton growth (Xu et al., 2010; Paerl et al., 2016).

It is widely accepted that there is no N limitation or P limitation if hypereutrophic lakes are nutrient replete (Xie et al., 2003; Xu et al., 2010). For example, when N and P water column concentrations were greater than 0.8 mg/L and 0.2 mg/L, respectively, the growth of the dominant bloom-forming cyanobacterium Microcystis spp. was not nutrient-limited in Lake Taihu (Xu et al., 2010). Therefore, reducing cyanobacterial blooms by controlling both N and P simultaneously rather than N alone or P alone may be the most effective management strategy in seriously eutrophic freshwater ecosystems (Conley et al., 2009; Paerl et al., 2016).

The production of microcystins (MC), the dominant cyanotoxin produced by freshwater cyanobacteria, is mainly regulated by environmental parameters, including water temperature, light intensity, pH, N, and P (Graham et al., 2004; Boopathi and Ki, 2014; Lee et al., 2015). Traditional approaches to manage cyanobacterial blooms and decrease MC production have focused on controlling P levels in water (Levy, 2017). However, recent studies suggest that increased N loadings are contributing to Microcystis blooms and MC release (Horst et al., 2014). Nitrogen was the primary factor limiting MC production (Yan et al., 2015) and different N forms likely influenced the concentration and composition of MC via changes in the cyanobacterial community structure (Monchamp et al., 2014). Therefore, it is important to understand which nutrient controls cyanobacterial blooms and impacts MC production in order to reduce the potential environmental risks posed by MC in aquatic ecosystems. In addition, extensive studies have shown that in situ nutrient enrichment bioassays are useful methods to investigate the influence of nutrients on phytoplankton growth (Elser et al., 1990; Xu et al., 2010, 2013, 2015; Deng et al., 2014; Steinman et al., 2016). However, their utility to examine the effect of nutrients on toxin production has received less attention, even though the global distribution of harmful cyanobacterial blooms and associated hepatotoxins have been well documented in many countries and territories (Harke et al., 2016).

Spring Lake is a eutrophic lake located in west Michigan and has been characterized by very high total P (TP) concentrations. An alum (aluminum sulfate) treatment with a concentration of 10–20 mg Al/L was applied in the surface water of Spring Lake in autumn 2005 to reduce internal P loading from the sediments (Steinman and Ogdahl, 2008). The alum treatment remained extremely effective both 8 months and 5 years after the application, based on the reduction of both TP concentrations in the surface water and measured P release rates from the sediment (Steinman and Ogdahl, 2012). However, TP concentrations near the bottom of the water column showed an unexpected increase and reached as high as 1.005 mg/L in 2016 (Steinman et al., 2018), suggesting that internal loading may be increasing and alum treatment is possibly losing its efficacy, some 11 years following application. Thus, it is necessary to keep track of Spring Lake nutrient dynamics, especially in summer from June to August, when planktonic algae are abundant and dominant in the surface water.

Given the concerns over frequent cyanobacterial blooms and possible toxin production in this heavily used lake, an in situ nutrient addition bioassay was conducted in Spring Lake to evaluate the influence of N and P, both separately and in concert, on phytoplankton growth and MC production. In addition, a survey of Spring Lake was performed after the bioassay to examine the distribution and variation in nutrients and MC at two different sites during the summer. We hypothesized the following: (1) N is now the primary factor controlling phytoplankton growth in Spring Lake given the recent high P concentrations, and (2) the production of MC is mainly regulated by N, via its influence on the MC-producing cyanobactera.