Environmental regulation of dissolved organic carbon release by seaweeds

Dissolved organic carbon (DOC) release by seaweeds (marine macroalgae) is a critical component of the ocean’s biogeochemical carbon cycle but is a relatively unstudied aspect of seaweed carbon physiology. To address this, the aim of this PhD research project was to explore how environmental factors ‒ seasonal fluctuations in nitrogen and temperature, ocean acidification (OA) and essential micronutrient limitation (iron, dFe) ‒ would influence and drive the DOC release rates of seaweeds with varied dissolved inorganic carbon (C_i, defined as CO₂ + HCO₃^-) uptake strategies.

To determine knowledge gaps in the research regarding seaweed DOC release, Chapter Two reviewed and synthesised the current scientific literature. DOC release rates from different studies were converted to a standard unit (μmol C gDW^-1 h^-1) which allowed comparisons between functional groups, phyla, and environmental influences to determine dominating factors regulating DOC release. We found that DOC release rates were increased under environmental factors such as desiccation (~90 times greater release than under ambient conditions), non-optimal temperatures, altered salinity, high irradiance, and elevated C_i concentrations. The fate of seaweed derived DOC was discussed in the context of ecological food webs and potential use of seaweeds for atmospheric carbon dioxide (CO₂) mitigation.

Chapter Three focussed in on the seasonal cycles of DOC produced by a temperate seaweed reef at Coal Point, Tasmania, Australia, to discern whether fluctuations in reef scale DOC production were associated with seasonal changes of DOC release, or with altered biomass of the seaweed assemblage. The reef was seasonally surveyed for biomass and dominant species were sampled for laboratory DOC release experiments over a one-year period. For each season, we calculated a reef-scale net DOC release for the Coal Point reef (27 500 m^-2) of 1116 ‒ 1820 Gg C d^-1 in spring and summer which was ~1600% greater than autumn and winter (36 ‒ 138 Gg C d^-1). The substantial difference in seasonal DOC release was likely a response to changes in nitrogen physiology of the seaweeds, indicated by variations in the percent carbon, nitrogen, and C:N ratios, rather than changes in seaweed biomass over season.

Chapter Four studied DOC release by three seaweed species with various C_i uptake strategies under OA ‒ two species which use carbon concentrating mechanisms (CCMs) to convert bicarbonate to CO₂ (Ecklonia radiata and Lenormandia marginata) and a non-CCM which only takes up CO₂ through diffusion (Plocamium cirrhosum). Results from this chapter showed that OA had no effect on the DOC release nor growth, C_ii uptake, photosynthesis, respiration, pigments, percent tissue carbon, nitrogen, and C:N ratios of all three species regardless of C_i uptake strategy. This indicates that the photosynthetic CO₂ fixation rate of these seaweeds will not increase in the future ocean.

Chapter Five studied the potential for seaweeds to be used as a method of CO₂ removal in the open ocean, referred to as ocean macroalgal afforestation (OMA). A key missing component of these OMA discussions has been the limitation of open ocean primary productivity by dissolved iron (dFe), with phytoplankton populations releasing more DOC under conditions of dFe limitation compared to dFe sufficiency. Both the limiting dFe concentrations for seaweed growth, and the role of dFe in seaweed DOC release, were unknown. This chapter focussed on the giant kelp, Macrocystis pyrifera to determine limiting dFe concentrations for functional physiologies, and importantly DOC production. The results of this chapter indicated that dFe additions of < 20.15 nM Fe′ (the sum of dissolved inorganic Fe(III) species available for biological uptake) resulted in impaired physiological functions, mortality and substantial DOC release by M. pyrifera. These results suggest that kelp growth cannot be sustained at oceanic dFe concentrations, which are 1000-fold lower than required by M. pyrifera, suggesting OMA may be restricted by dFe concentrations in the open ocean.

Overall, the findings from this thesis suggest that DOC release by seaweeds is regulated by environmental drivers ‒ specifically those which restrict the assimilation of organic carbon into new tissue growth, such as nutrient limitation (NO₃^- and dFe). Increasing the availability of CO2 drove no increase in DOC release, suggesting factors which influence downstream seaweed growth are more important in regulating DOC release from seaweed. This finding supports the overflow hypothesis whereby photosynthate is released as DOC when photosynthesis is occurring faster than required for growth. The results of this doctoral thesis highlight the significant contribution of seaweed DOC to the coastal ocean biogeochemical carbon cycle and the importance of seaweeds in supporting crucial food web linkages through DOC release.