title: Phosphorus sources contributing to phytoplankton blooms in a subtropical reservoir
Creators: name: Prentice, Matthew J
Publisher: name: Griffith University
Year: 2021
Subjects: subject: Lakes
subject: Freshwater
subject: Anthropogenic
subject: Nutrient inputs
subject: Cyanobacteria blooms
subject: Drivers

description: Lakes comprise 87% of surface freshwater existing in liquid form on Earth. In recent years, however, lake condition has deteriorated at an alarming rate primarily attributed to an increase in anthropogenic-related nutrient inputs. These inputs present the greatest challenge to lake ecosystem stability as they cause eutrophication, which is often characterised by deoxygenation of bottom waters and phytoplankton blooms. Blooms of cyanobacteria are of particular concern as some species or strains produce toxins that affect biodiversity and organisms that are part of the foodweb, as well as causing sickness and death of livestock, wildlife, and humans reliant on lakes for water consumption. In addition, cyanobacteria may also produce taste and odour-causing compounds, increasing water treatment costs. It is therefore imperative to develop an understanding of the drivers contributing to cyanobacteria blooms so that blooms may be better understood and predicted, as well as their effects mitigated. Phosphorus (P) is an essential element for all organisms—including phytoplankton—and in lakes is widely considered to be the key nutrient limiting or co-limiting (with nitrogen [N]) phytoplankton productivity. Excess P can alter phytoplankton communities and lead to phytoplankton blooms. The forms of P are usually determined operationally as: 1) particulate organic P (POP), including P in living and dead organisms; 2) particulate inorganic P (PIP), including inorganic complexes of P sorbed to mineral phases of rock and soil; 3) dissolved organic P (DOP), including low molecular-weight esters and organic colloids; and 4) dissolved inorganic P (DIP; or soluble reactive P [SRP]; or dissolved reactive P [DRP]), including orthophosphate (PO43-) and polyphosphates. Despite the DIP fraction composing the only forms able to be directly assimilated by the phytoplankton community, each fraction is in a constant state of flux and thus—on account of the action of various biogeochemical processes occurring across space and time—carries the potential to affect phytoplankton productivity. The influence of P on phytoplankton productivity is therefore highly dynamic, as a result of the transformations and transportation of P within the system. Phytoplankton are known to upregulate high-affinity transporters that increase P uptake under DIP-depauperate conditions. Therefore—Chapter 2 (i.e., the first data chapter)—examines the relationships between 1) physicochemical drivers and phytoplankton community P uptake rates, and 2) phytoplankton community P uptake and species composition, in the surface waters of the seasonally DIP-depauperate subtropical lake; Lake Wivenhoe, Queensland, Australia. P starvation was also examined in the dominant cyanobacterium Raphidiopsis raciborskii (Wołoszyńska 1912) Aguilera et al. 2018 (previously Cylindrospermopsis raciborskii) under controlled laboratory conditions. Phytoplankton P uptake was quantified using the radioisotope phosphorus-33, with field study measurements complemented by a suite of physicochemical parameters measured in the lake at monthly intervals over a 12-month period. Surface DIP concentrations and P uptake rates were demonstrated to be inversely related, with substantially higher uptake rates occurring under thermally stratified, DIP-depauperate conditions during summer. Surface DIP concentration and temperature explained 50.3% of the variation in P uptake rate, per classification and regression tree (CART). A primary split in the CART at 4.75 μg L−1 P indicated a transition between low- and high-affinity uptake, with high-affinity P uptake rates (i.e., P uptake &lt; 4.75 μg L−1 P) associated with a phytoplankton assemblage dominated by cyanobacteria, including the dominant cyanobacterium R. raciborskii. Field results were corroborated by the in vitro P-starvation study of the R. raciborskii strain, with uptake rates increasing as the culture became progressively starved of P. These results indicate that P scavenging via high-affinity uptake is advantageous under DIP-depauperate conditions, and the ability to scavenge P via high-affinity uptake may be a key factor in the dominance of bloom-forming cyanobacteria under DIP-depauperate stratified conditions. As demonstrated in Chapter 2, during stratified periods when DIP is low, the phytoplankton assemblage had elevated P uptake rates. Further, under these conditions, DOP became the dominant source of dissolved P (DP; i.e., DIP + DOP) available to phytoplankton. Therefore—Chapter 3 (i.e., the second data chapter)—examines how DOP mineralisation by alkaline phosphatase (AP) activity (APA), relative to regeneration processes in the SML, could meet phytoplankton P uptake and how it is associated with phytoplankton community composition changes under thermally stratified DIP-depauperate conditions in Lake Wivenhoe. APA was quantified fluorometrically using 4-methylumbelliferyl phosphate, and phytoplankton P uptake and regeneration determined radiometrically using the isotope phosphorus-33 at monthly intervals during a summer-stratified period. APA was demonstrated to increase when phytoplankton cell P quotas were low (&lt;0.65 μg P μg−1 Chl-a), with potential DOP mineralisation rates increasing to 88 μg L−1 h−1 P. Such rates are at the upper end of rates in the literature. APA represented up to 89% of the total phytoplankton P uptake and was much higher than the P regeneration rate in the SML. The highest APA coincided with peak phytoplankton biovolume and dominance of the phytoplankton assemblage by cyanobacteria. Further, APA was strongly positively related to the majority of the 10 most dominant cyanobacteria, including the toxin-producing species R. raciborskii. This indicates that under DIP-depauperate conditions, DOP mineralised by APA is a substantial source of P for phytoplankton, and the ability to produce AP may be a key factor in the occurrence of bloom-forming cyanobacteria. As demonstrated in Chapter 2 and Chapter 3, P fluxes strongly impact phytoplankton biomass in Lake Wivenhoe. Therefore—Chapter 4 (i.e., the third data chapter)—examines the key physical and biogeochemical fluxes of P available affecting the time-distance continuum of phytoplankton in Lake Wivenhoe. Physical transport and biogeochemical transformation was determined in the context of a horizontally-resolved mass balance, comprising four zones down the drowned river channel that forms the lake. The mass balance was informed by integrating field and laboratory measurements of selected biogeochemical P fluxes with transport fields from a hydrodynamic model (AEM3D). P regeneration within the surface waters was demonstrated as being more important than the physical processes introducing ‘new P’ into the surface waters. Vertical transport of DOP to the SML was comparable to regeneration at times during the stratified period, and advective fluxes of P were comparable to regeneration during a storm event in May of which remained elevated above pre-storm levels for several weeks. On an annual basis, the flux of P was also demonstrated to transition from one of physical to biogeochemical dominance, and the physical-component from one of horizontal to vertical dominance, longitudinally down-reservoir. Changes in phytoplankton biomass following the storm event were positively related to the down-reservoir DIP flux. In contrast, changes in phytoplankton biomass during stratification were negatively related to phytoplankton cell P quota and positively related to vertical transport of DOP, likely attributed to dominance by R. raciborskii and its capacity to metabolise luxury P storages and use organic P. In using a novel combination of in situ, in vitro, and in silico techniques to derive phosphorus fluxes, alongside phytoplankton community data, this study has demonstrated that vertical fluxes of DIP and DOP into the surface waters of a subtropical lake are critical for promoting the dominance of bloom-forming cyanobacteria, including toxic R. raciborskii. Cyanobacteria and R. raciborskii in particular possess the ability to effectively utilise DIP and DOP from regeneration and transient fluxes from the hypolimnion through mechanisms such as high affinity P uptake and mineralization of DOP. These findings provide new insights into the P-related strategies used by cyanobacteria, and how they interact with physical and chemical processes to drive phytoplankton dominance in lakes. It has important implications for our scientific understanding of P processes in lakes and management of P-depauperate lakes, and raises important questions with respect to potential directions for future research.