Abstract
Globally rising concentrations of atmospheric carbon dioxide (CO2), fuelled by anthropogenic activities, such as the burning of fossil fuelsandchanges in land-useoften havedetrimental effects on freshwater ecosystems. The growth of freshwater phytoplankton, intimately linked with the availability of nutrients in lakes, can act as a buffer of global warming by sequestering atmospheric carbon, but the factors controlling the growth of freshwater phytoplankton are not yet entirely resolved.High levels of nutrients in lake systems are generally associated with lake eutrophication. This can lead to the formation of cyanobacterialblooms, which are harmful to the environment, often mitigating the positive effect of carbon sequestration. Conversely, lakes of lower trophic state and with lower nutrient concentrations often host blooms of other types of phytoplankton. Of particular importance are diatoms, which are known to play a crucial role in regulating the global CO2budget. Over the last several decades, the biological significance of the macronutrients nitrogen and phosphorusin the formation of phytoplankton blooms has been well constrained, while the exact roles trace metal micronutrients play in freshwater phytoplankton growth remain poorly understood. This is despite the fact that all phytoplankton have an indispensable demand for a number of bioessential trace elements, with iron (Fe) deemed to be the most important metal for algal growth. Consequently, it is now well-established that Fe plays a major role in limiting phytoplankton growth in vast areas of the world’s oceans, and it is equally plausible that Fe limits phytoplankton growth in freshwater systems, especially in oligotrophic lakes with lower nutrient contents. Other trace metals, such as manganese (Mn), cobalt (Co) and zinc (Zn), are also important for phytoplankton growth, as established through laboratory-manipulated culture experiments. However, comparatively little is known about the distributions, biogeochemical cycling, and influence of these trace metals on algal growth in natural freshwater systems.The lakes of the Taupō Volcanic Zone (TVZ) in the North Island of New Zealand are unique becausetheir surrounding geology is dominated by rhyolithic tephra emitted during the last eruption of the Taupō super volcano ca. 2,500 years ago. The concentrations of trace metals in the soils of the TVZ are up to three orders of magnitude lower than recorded in many other soil types worldwide. Consequently, lakes of the TVZ, which receive input via surface, riverine
iiiand groundwater inflowsthat drains the soils of the TVZ, are also expected to have low trace metal contents by global standards. This makes the TVZ lakes anideal case study for investigating the distributions and concentrationsof trace metals, their biogeochemical cycling, and in turn, the role of trace metal micronutrients in regulatingphytoplankton growth in freshwater lake systems. In this study, the interactions between trace metal micronutrients and phytoplankton productivity were investigated both under controlled conditions during culture-basedexperiments and in the natural lake environments of the TVZ to provide new insight into these processes. The phytoplankton growth experiments were designed to investigate the potential of trace metals to limit or promote phytoplankton growth by carefully manipulating the concentrations of a biologically important suite of trace metals. The growth responses of the cyanobacteria species Dolichospermum lemmermanniiand the diatom species Fragilaria crotonensiswere monitored in growth media inoculated with the trace metals Fe, manganese (Mn), copper (Cu), cobalt (Co), nickel (Ni) and zinc (Zn) at levels representative of annually-averaged ambient, two-times ambient and ten-times ambient concentrations of Lake Taupō. The effect on phytoplankton growth was assessed both independently for each trace metal and for all metals combined. The results demonstrate that the growth of D. lemmermanniiis limited when annually-averaged concentrations of Fe or a mixture of all trace metals (including Fe) are present in ambient Lake Taupō concentrations, while elevated concentrations of Fe and all trace metals lead to increased growth. In contrast, no growth response occurs when any other trace metal besides Fe is present in elevated concentrations. The growth of F. crotonensiswasnot limited by any of the trace metals investigated. This investigation further showed the importance of monitoring the concentrations of trace metals in the growth media via ICP-MS throughout media preparation and regularly during the growth experiments if picomolar to nanomolar trace metal concentrations are being manipulated, as these low concentrationsare prone to contamination from environmental sources. In parallel with the phytoplankton growth experiments, a year-long study was conducted to investigate the interaction of phytoplankton with trace metal micro-nutrients in three lakes of contrasting trophic status within the TVZ, namely oligotrophic Lake Taupō, oligotrophic-mesotrophic Lake Ōkataina and eutrophic Lake Rotorua. The trace metal distributions were investigated using a combination of highly specialised clean room techniques, pre-concentration methods, ICP-MS analysis, and trace metal speciation modelling. The sampling of surface waters of study lakes was performed on a monthly basis and the full water column
ivwas sampled twice annually, during summer and winter when the lakes were stratified and well mixed, respectively. The concentrations of a suite of 30 trace metals were obtained for the acid soluble, dissolved, bioavailable and particulate phases of the water column, supported by datasets for macronutrient concentrations, lake pH and temperature, phytoplankton species composition, and chlorophyll aas an indicator of productivity levels. This investigation of phytoplankton-micronutrient dynamics demonstrated that the trace metal Fe is very importantfor the growth of bulk phytoplankton in all studylakes. The results show, for the first time, that the growth of diatoms becomes limited when bioavailable Fe concentrations are <800 pmol·L-1, while the growth of cyanobacteria is limited when these concentrations are <4 nmol·L-1. These new constraints may allow freshwater management strategies to be devised based on bioavailable Fe concentrations by promoting growth of carbon sequestering phytoplankton species, such as diatoms, while simultaneously suppressing the growth of cyanobacteria.Iron concentrations aside, the interactions between phytoplankton and other biologically important trace metals, specifically Mn, Co, Cu, Ni and Zn, were also investigated in the year-long study of Lakes Taupo. Okataina and Rotorua. Trace metal concentrations and distributions were characterised in the surface waters and across the entire water column in the acid soluble, dissolved, bioavailable and particulate phases. The results show that the demand by phytoplankton for these trace metals investigated is largely met by the picomolar to nanomolar dissolved and bioavailable concentrations at which they are present in the waters of the study lakes. However, Ni and Zn, may act to co-limit phytoplankton growth in the sub-surface, and at the location of the ‘deep chlorophyll maximum’ that forms during summer in Lakes Taupō and Ōkataina. Additionally, the uptake of Co and Zn by phytoplankton increased as bulk phytoplankton growth intensified, but no indication of growth limitation was observed. The complexation of Cu by fulvic acids is important in all study lakes, acting to lower its bioavailable concentration and potential toxicity. The biogeochemical cycling of these additional trace metals differed greatly between the study lakes, each of different trophic state, depth and level of anthropogenic influence in the watershed. This demonstrates that while the cycling of trace metals in the world’s oceans follows established distribution types, many different factors control the cycling of trace metals in freshwater lakes, and stark differences in their cycling and distribution can be found, even when lakes are in close spatial proximity.