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Seasonal and spatial patterns in nitrogen cycling and food web interactions in Lake Taupō New Zealand

Lakes with high water quality and low productivity, commonly referred to as ‘oligotrophic’, are often viewed as relatively pristine and highly aesthetic ecosystems, but may still require management of nutrient inputs and fisheries. The ecosystem processes that determine functions in oligotrophic lakes are often distinct from those in eutrophic lakes, which are traditionally more actively managed. This is particularly true for nitrogen cycling which, in oligotrophic lakes, is closely coupled with food web dynamics. Strong nitrogen cycling-food web coupling in oligotrophic systems is partly related to greater significance of consumer nutrient recycling. Given that processes affecting nutrient cycles and food web dynamics can be actively managed (e.g., through catchment nutrient load regulation and fisheries management, respectively), understanding the interactions between these two processes is key to management of oligotrophic lakes globally. This thesis examines interactions between nitrogen cycling and food web dynamics in oligotrophic Lake Taupō. Lake Taupō is a large (616 km² in area), deep (92 m mean depth), warm monomictic lake in the North Island of New Zealand. It shares many of the characteristics typical of large, deep oligotrophic lakes globally and can be viewed as a model system to examine nutrient cycling-food web interactions. Since 2008, nitrogen loads to the lake have been restricted by local government regulation with the objective to maintain high standards of water quality. Lake Taupō is the only example globally of exclusively N management for water quality purposes. Abundance of rainbow trout (Oncorhynchus mykiss: Salmonidae), the top predator in the Taupō system, is managed through a regulated recreational fishery. Coincident with a period of declining water quality between 1995 and 2005, the trout in Lake Taupō underwent a drastic decline in abundance and individual size. However, connection between the changes in water quality and trout abundance has never been examined. Globally, there have been few empirical studies, and little research generally, to examine interactions of food web dynamics and nutrient availability, despite growing awareness of the impact of these interactions on primary production. One component of this study synthesises literature and case studies of lakes to present a contemporary understanding of food web ecology and N-cycling processes. The synthesis indicates that consumer nutrient recycling effects on lake productivity are likely to be seasonally specific and act to supplement demand by primary producers, especially during periods when other nutrient supply processes (e.g., hypolimnetic upwelling) are suppressed. Consumer nutrient recycling itself is regulated by food web structure, with smaller organisms contributing disproportionately to recycling locally and large mobile organisms acting as nutrient dispersal vectors across boundaries (e.g., the thermocline). Tightly coupled nutrient cycling-food web interactions have the potential to provide ecosystem resilience to global environmental change drivers such as climate change. In this thesis I build on findings from the literature synthesis and use three methods to investigate nitrogen cycling food web interactions in Lake Taupō. First, δ¹⁵N and δ¹³C stable isotope analyses are used to quantify intra-annual patterns in, and drivers of, food web dynamics. The focus is on littoral-pelagic diet coupling by mobile consumers in response to variation in pelagic resource availability. Second, spatially resolved samples (littoral and pelagic surface waters, metalimnetic and hypolimnetic waters) taken at seasonal intervals over one year are used to contribute information towards consumer nutrient recycling. Stable isotope analyses of δ¹⁵N-POM (particulate organic matter), δ¹⁵N-NH₄⁺, δ¹⁵N-NO₃⁻ and δ¹⁸O-NO₃⁻; ¹⁵N are used to indicate how consumer nutrient recycling contributes to nitrogen availability. Third, food web dynamics and consumer nutrient recycling are used as inputs to a nitrogen mass-balance model for pelagic surface waters. This model explicitly considers littoral-pelagic exchange using a coupled three-dimensional hydrodynamic model to resolve advection and mixing. Littoral-derived nitrogen fluxes to the pelagic surface waters and nitrogen fluxes from hypolimnetic to pelagic surface waters were estimated from the three-dimensional hydrodynamic model and nitrogen concentrations of the respective layers. Output from the hydrodynamic model was used in combination with other nitrogen influxes to the pelagic surface waters (e.g., hypolimnetic upwelling, littoral exchange, catchment loading, atmospheric deposition and N-fixation) in a mass balance model quantifying the role of recycling fluxes in sustaining phytoplankton nitrogen uptake. Collectively, these research chapters demonstrated that there is close coupling of nitrogen cycling and the food web in Lake Taupō and that this coupling is strongly seasonally forced. Pelagic nutrient availability was strongly influenced by phytoplankton biomass. Highest nutrient availability was associated with winter mixing and the period of highest phytoplankton biomass. These conditions resulted in an increased reliance on pelagic trophic resources across all trophic levels with little evidence from stable isotope analyses for substantial nutrient recycling during this period. During summer stratification, however, surface water nutrient concentrations and pelagic phytoplankton abundance reached an annual minimum. Correspondingly, zooplankton abundance decreased while trout and smelt consumed more littoral resources. Strong littoral-pelagic dietary coupling was demonstrated by smelt and trout. This finding is contrary to previous assumptions that the Lake Taupō food web is predominantly supported by pelagic production but aligns with current theories that postulate that food web interactions are dynamic and adaptive to environmental conditions. Surface water POM, NH₄⁺ and NO₃⁻ all became increasingly δ¹⁵N-depleted over the period of summer stratification, indicated increased reliance on consumer nutrient recycling. Depleted δ¹⁵N-NO₃⁻ was associated with enriched δ¹⁸O-NO₃⁻, indicative of high heterotrophic biomass relative to primary producers. Strong correlations between δ¹⁵N-NH₄⁺ excreted by zooplankton and δ¹⁵N-NH₄⁺ in water taken from the deep chlorophyll maximum suggest particularly strong coupling of primary production and consumer nutrient recycling at this depth. Collectively, these findings demonstrate that seasonal alternation of bottom-up and top-down processes control nitrogen cycling and food web interactions in Lake Taupō. The pelagic surface water nitrogen mass balance model, inclusive of physical transport using the three-dimensional hydrodynamic model, quantified the seasonal contributions of consumer nitrogen recycling to pelagic primary production. Nitrogen fluxes from littoral to pelagic waters originating from consumer transport were greater than those arising from physical transport during early and mid-summer stratified periods. Physical transport of littoral-derived-N into pelagic surface waters was greatest during autumn, prior to destratification and were minimum during mid-stratification. In situ recycling accounted for between 75 and 95% of phytoplankton nitrogen demand throughout the year. Nitrogen recycling rates were found to be greatest during winter mixing when phytoplankton biomass was highest. A positive linear relationship between surface water δ¹⁵N-NO₃⁻ and modelled recycling rates suggests that phytoplankton nitrogen excretion, which is not ¹⁵N-depleted, drives much of the seasonal variation in nitrogen recycling and that consumer nutrient recycling provides a relatively constant nitrogen supply throughout the year. Given that nitrogen recycling rates were positively related to phytoplankton biomass, nitrogen recycling may act as a positive feedback, amplifying the growth response of phytoplankton to external nutrient supplies. The base level of consumer nutrient recycling, on the other hand, may provide resilience to strong seasonal fluctuations in nitrogen supply associated with other sources. This study demonstrates strong bi-directional interactions between nitrogen cycling and food web dynamics in Lake Taupō. These findings can be used to understand the reciprocating effects of observed long-term changes in nutrient concentrations and trout abundance in Lake Taupō. The observed inter-decadal variations observed in top-predator abundance could have substantial impacts on nitrogen availability for phytoplankton in the pelagic zone through changes in food web structure and consumer nutrient recycling. In oligotrophic lakes such as Taupō, management should be adopted to consider the interactions between food web dynamics and nutrient cycling. One potential action includes adapting trout harvest based on winter pelagic primary productivity data as a measure of resource availability. A second potential action is adapting trout harvest to regulate smelt populations, thus altering the degree of littoral-derived nutrient translocation during the stratified period. This thesis supports the growing recognition that ecosystem-level management of lakes will increasingly be required to counter multiple interacting ecosystem stressors (e.g., climate change, invasive species, fishery exploitation and cultural eutrophication). Informed management using these approaches will be critical for maintaining resilient oligotrophic lakes.
Type of thesis
Stewart, S. D. (2018). Seasonal and spatial patterns in nitrogen cycling and food web interactions in Lake Taupō New Zealand (Thesis, Doctor of Philosophy (PhD)). The University of Waikato, Hamilton, New Zealand. Retrieved from https://hdl.handle.net/10289/11865
The University of Waikato
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