Winter nitrification in ice-covered lakes

Abstract

With changes in ice cover duration, nutrient loading, and anoxia risk, it is important to understand the mechanisms that control nitrogen cycling and oxygen depletion in lakes through winter. Current understanding is largely limited to description of changes in chemistry, with few measurements of the processes driving winter changes, how they differ across lakes, and how they are impacted by under-ice conditions. Nitrification is a process which consumes oxygen and ammonium (NH4+), and supplies nitrate (NO3-). To date, nitrification has been measured under ice cover in only two lakes globally. Here, we used 15NH4+ enrichment to measure rates of pelagic nitrification in thirteen water bodies in two ecozones. Our work demonstrates ecologically important rates of nitrification can occur despite low water temperatures, impacting NH4+, NO3- and, most importantly, oxygen concentrations. However, high rates are not the norm. When, where and why is nitrification important in winter? We found that nitrification rates were highest in a eutrophic lake chain downstream of a wastewater treatment effluent (mean: 226.5 μg N L-1 d-1), and in a semi-saline prairie lake (110.0 μg N L-1 d-1). In the boreal shield, a eutrophic lake had nitrification rates exceeding those of an oligotrophic lake by 6-fold. Supplementing our results with literature data we found NH4+ concentrations were the strongest predictor of nitrification rates across lentic ecosystems in winter. Higher nitrification rates were associated with higher concentrations of NH4+, NO3- and nitrous oxide (N2O). While more work is required to understand the switch between high and low nitrification rates and strengthen our understanding of winter nitrogen cycling, this work demonstrates that high nitrification rates can occur in winter.

Fig 1. Schematic of the nitrogen cycle, featuring the microbial processes of nitrification (NH₄⁺ to NO₂^– and then to NO₃^–) and denitrification (NO₃^– to NO₂^–, nitric oxide, N₂O then to nitrogen gas).

For every mole of NH₄⁺ nitrified to NO₃^–, two moles of oxygen are consumed (Stoichiometric relationships collectively found in [,,–13]). Note that the proportion of N₂O released from nitrification and denitrification is highly variable as indicated by the dashed arrows [14]. Nitrogen assimilation, dissimilatory NO₃^– reduction to NH₄⁺ (DNRA) and anaerobic NH₄⁺ oxidation (anammox) are excluded from the figure but may be important components of the nitrogen cycle [15].

Fig 2. Map of Canada with overlays of Saskatchewan and Ontario study sites (map courtesy of Rosa Brannen).

All Saskatchewan sites are in the prairie ecozone, while the Experimental Lakes area sites are in the boreal shield ecozone [42].

Fig 3. Relationship between nitrification rates and NH₄⁺ concentrations for water bodies from this study (ELA and Saskatchewan) and other cold water measurements from Lake Superior (no ice-cover; [40]), Lake St. George (ice-covered; [21]) and Lake Croche (ice-covered; [38]).

Note logged y-axis. The line plotted is the linear model (permutations) for all data from Tables 1 and 2. The linear model and statistics are presented in Table 3. Nitrification rates less than their sample specific LOQ are replaced by their LOQ.

Fig 4. Concentrations of NH₄⁺ and NO₃^–, and N₂O percent saturation partitioned according to nitrification rates that are above or below 0.11 μg N L^-1 d^-1.

There are significant differences between the two rate groups for all analyses (NH₄⁺, NO₃^–, and N₂O; Wilcox-Mann-Whitney test, P <0.05). The boxplot and whiskers encompass 95% of the data observed, data points outside of the box and whiskers are outliers. The box itself represents the first and third quartiles, and the center line is the median [65].

Fig 5. Principal component analysis showing the relationship between measured variables and nitrification rates.

PC1 and PC2 account for 61% of the variance exhibited by the relationship among these variables. Within a PCA, the closer the component vectors are (angle and length) the more closely they are related. Note the association of nitrification rates with NO₃^–, N₂O and NH₄⁺, and of CH₄ with chlorophyll and temperature.