The role of zooplankton in cyanobacteria bloom development in Australian reservoirs

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Cyanobacteria occupy diverse aquatic habitats and their ecological success is expected to increase under predicted future climate scenarios. Managing cyanobacteria abundance in freshwaters is therefore critical for reducing risks to human and animal health. One species that is currently undergoing range expansion from subtropical to temperate habitats is Cylindrospermopsis raciborskii. C. raciborskii is ecologically successful because of its (1) competitive nutrient acquisition and storage mechanisms (e.g. high affinity for phosphorus (P) and ammonium, high P-storage capacity); (2) wide thermal tolerance, superior shade tolerance and buoyancy regulation; (Briand et al. 2002) and (3) resistance to grazing. To date, research to understand the formation of C. raciborskii blooms and toxicity have mostly focused on environmental factors, but the importance of food web interactions in regulating blooms has been little investigated. In particular, there is a need to examine these foodweb interactions in subtropical systems in the Southern Hemisphere because much of the current understanding about zooplankton-cyanobacteria interactions comes from temperate systems dominated by large-bodied cladocerans. Given that warmer subtropical systems are dominated by copepods and smaller-bodied individuals, it is likely that interactions between zooplankton and phytoplankton have different outcomes for cyanobacterial bloom formation. To understand the mechanisms of toxic cyanobacterium C. raciborskii bloom formation in subtropical oligotrophic Australian lakes, a series of investigations were undertaken across multiple spatial and temporal scales to test the hypothesis that C. raciborskii growth is facilitated by meso-zooplankton. Specifically, small-scale laboratory experiments (~100 ml) examined zooplankton grazing and tested whether copepods avoid consumption of C. raciborskii under food saturating conditions (Chapter 2). Both the direct (grazing) and indirect (nutrient regeneration) effects of zooplankton on C. raciborskii were further examined in laboratory experiments (Chapter 3). These laboratory experiments were then scaled up to mesocosms (~500 litres), where in situ C. raciborskii growth was examined under different treatments (control, 1x and 5x ambient zooplankton abundance, 5x ambient zooplankton abundance + inorganic P) (Chapter 4). Comparisons between zooplankton populations were also made at the reservoir scale, testing to see whether lakes experiencing C. raciborskii blooms had different zooplankton biomass, size structure and functional group composition compared to lakes that do not experience blooms (Chapter 5). In Chapter 2, the hypothesis that copepod consumers discriminate against C. raciborskii was tested. Experiments were designed based on observed seasonal variation in food quantity and quality for zooplankton in subtropical Australian lakes and reservoirs, and tested whether clearance rates were dependent on the P-content of prey, the proportion of C. raciborskii present and the previous feeding history of zooplankton. The results indicated that the clearance rates of copepods on C. raciborskii were 2-4 times lower than that of a cladoceran Ceriodaphnia sp. when both grazers had prey choice. The copepod Boeckella sp. was found to select against C. raciborskii when alternative food was abundant, but selectivity declined when animals had been kept in low food conditions for 2-12 hours before experimentation. The clearance rates of Boeckella sp. on two toxic C. raciborskii strains were significantly lower than on a nontoxic strain. Clearance rates were also significantly lower on C. raciborskii with low cellular P content and when present at >5% relative abundance amongst natural phytoplankton assemblages. Together these results suggest that copepods largely avoid consumption of C. raciborskii. In Chapter 3, the impact of zooplankton nutrient regeneration on C. raciborskii growth was evaluated. Indirect effects of zooplankton interactions may be relatively important seasonally when dissolved nutrient concentrations are low. Dialysis experiments were designed to simultaneously test the direct (grazing) and indirect effects (nutrient regeneration) of zooplankton-algal interactions, enabling zooplankton to access food outside the dialysis tubing, and for zooplankton-derived nutrients to be accessible to algae inside the tubing. Controls with no zooplankton were also set up to account for nutrient contributions from algal prey. Zooplankton-derived nutrients alleviated P-limitation of C. raciborskii inside the dialysis tubes and stimulated growth. Furthermore, C. raciborskii growth was favoured above a green algal competitor when both algae were in dialysis tubes, indicating C. raciborskii is more efficient at taking up P recycled by zooplankton. Outside the dialysis bags, zooplankton grazed a green alga in preference to C. raciborskii and selectively consumed P-replete cells. C. raciborskii growth was therefore affected both directly and indirectly by zooplankton, suggesting that foodweb interactions can facilitate blooms of this cyanobacterium. In Chapter 4, zooplankton regulation of C. raciborskii dominance in a natural phytoplankton community was tested at a larger scale using mesocosms deployed in a subtropical reservoir. Laboratory studies often cannot account for diversity of natural assemblages, so treatments were set up to examine C. raciborskii growth under different zooplankton densities and P loading. To the best of our knowledge, this is the first field experiment to promote C. raciborskii through zooplankton manipulation. Zooplankton enrichment resulted in an increase in C. raciborskii relative abundance from 15% to 37% after four days. Simultaneously, elevated zooplankton lowered the C:P ratio of phytoplankton, supporting the notion that copepods tend to alleviate P limitation in the environment. The generality of zooplankton-cyanobacteria interactions were examined in Chapter 5, which describes a survey of 15 subtropical reservoirs. Reservoirs were split into two groups (those experiencing C. raciborskii blooms and those that don’t), and their zooplankton biomass, size structure and functional group composition were examined. The survey was carried out in both the wet and dry season to capture seasonal variations of phytoplankton and zooplankton communities and associated environmental variables. It was expected that C. raciborskii presence would be positively correlated to copepod abundance and negatively correlated to particulate N:P ratios. Ecological stoichiometry predicts that zooplankton with different body N:P content will differ in their relative rate of recycling of N and P. Copepods have low P content thus recycle nutrients with low N:P ratio into the environment. The survey demonstrated that reservoirs experiencing C. raciborskii blooms had a greater abundance of copepods compared to cladocerans, and a smaller proportion of juveniles. The correlation between environmental factors and C. raciborskii presence/absence was not statistically significant, but copepod abundance was negatively correlated to particulate N:P. Together, these results suggest that C. raciborskii is most likely facilitated through a planktonic foodweb subsidy in copepod-dominated subtropical oligotrophic lakes, whereby copepods consume other algae in preference to C. raciborskii when alternative algae are abundant, then regenerate nutrients that are then rapidly taken up by low P-adapted C. raciborskii. In terms of management implications, this thesis has demonstrated that biomanipulation by increasing zooplankton abundance in reservoirs of subtropical Queensland where calanoid copepods are dominant would not be very effective. Based on the data collected and the major findings, recommendations are made for sustainable management of Australian subtropical reservoirs.
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