Interactive effects of ocean acidification and declining water quality on tropical seagrass physiology

Ow, Yan Xiang (2016) Interactive effects of ocean acidification and declining water quality on tropical seagrass physiology. PhD thesis, James Cook University.

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Primary productivity is the conversion of inorganic carbon into structural and nonstructural carbon (growth and storage) and is thereby the basis of the ecosystem services provided by seagrass meadows. These services include provision of habitat, carbon sequestration, stabilisation and trapping of sediments as well as food for invertebrates, fish, and mega-herbivores. Increased carbon dioxide (CO₂) dissolved in seawater (ocean acidification, OA), can enable seagrass productivity to increase even though they also use HCO₃⁻ as an alternate form of dissolved inorganic carbon (DIC). However, productivity responses to increasing pCO₂ might be affected by other environmental factors that influence metabolic processes, such as water temperature and local water quality. The lack of empirical evidence for interactive effects of OA and localized impacts (e.g. light, nutrients) hampers our ability to factor these into predictive models and into coastal management decision-making processes. Therefore, in this thesis I aimed to investigate the physiological responses of tropical Great Barrier Reef (GBR) seagrass species to increasing pCO₂ (simulating OA), temperature, and key water quality parameters.

In an initial experiment (Chapter 2), productivity and growth responses of common tropical seagrass species, Cymodocea serrulata, Halodule uninervis and Thalassia hemprichii, to CO₂ enrichment were quantified. The seagrasses were exposed for two weeks to pCO₂ levels (442 – 1204 μatm) approximating the range of end-of-century emission scenarios. Net productivity and carbon budgets (PG:R) significantly increased with a rise in pCO₂ in all three species. The degree of productivity rise with pCO₂ was similar across species. While increased productivity in H. uninervis and T. hemprichii resulted in faster growth from CO₂ enrichment, this was not the case for C. serrulata. Varying carbon allocation strategies among species might have contributed to observed differences in growth responses and so internal carbon allocation was further explored in a later experiment (Chapter 5).

When light availability is reduced from declining water quality (e.g. land run-off), preference for utilisation of the DIC species (CO₂ vs HCO₃⁻), and therefore response to increasing pCO₂, might be affected. To test this, C. serrulata and H. uninervis were exposed to two DIC concentrations (447 and 1077 μatm pCO₂), and three light treatments (35, 100 and 380 μmol m-2 s-1) for two weeks (Chapter 3). DIC uptake mechanisms were separately examined by measuring net photosynthetic rates while subjecting C. serrulata and H. uninervis to changes in light and addition of bicarbonate (HCO₃⁻) use inhibitor (carbonic anhydrase inhibitor, acetazolamide) and TRIS buffer (pH 8.0). DIC enrichment stimulated maximum photosynthetic rates (Pmax) more in C. serrulata grown under lower light levels (36 – 60% increase) than for those in high light (4% increase) (DIC × light: P = 0.049). This was due to C. serrulata's greater dependence on CO₂ in low light. However, this increase due to DIC did not compensate for low light, as net productivity of DIC-enriched plants at low light was 85 – 208 % lower than non-DIC enriched plants growing under high light. In contrast, photosynthetic responses in H. uninervis increased with higher light and were independent of the concentrations of the DIC substrates available. H. uninervis has more flexible HCO₃⁻ uptake pathways. Light availability strongly affected productivity and also influenced productivity responses to DIC enrichment, via both carbon fixation and acquisition processes.

Nitrogen availability can limit productivity responses to OA, since nitrogenderived metabolites are required for carbon assimilation. In Chapter 4, the hypothesis that CO₂ and nitrate enrichment can have additive effects on seagrass productivity and biomass was tested. Nitrogen uptake and assimilation, photosynthesis, growth, and carbon allocation responses of H. uninervis and T. hemprichii to OA scenarios (428, 734 and 1213 μatm pCO₂) under two nutrient levels (0.3 and 1.9 μM NO3 -, approximating average GBR flood plume levels) were measured. Net productivity (53 – 78 %) and growth (18 – 52 %) in H. uninervis increased with CO₂ enrichment (P < 0.05), but were not affected by nitrate enrichment. T. hemprichii did not show significant changes with pCO₂ or nitrate by the end of the experiment (24 days) in net productivity and growth. There was no evidence that nitrogen demand increased with pCO₂ enrichment in either species. Overall, nutrient increases to levels approximating flood plumes levels in the GBR only had small effects on seagrass metabolism, and high tissue nutrient concentrations (2.53 – 2.75 %N) suggest that only small responses occurred because they were not nutrient limited.

Changes in ambient growth temperature can modulate seagrass response to OA by affecting assimilation and utilization of CO₂. Yet the combined effects of temperature and CO₂ enrichment on seagrass carbon metabolism are not known. In Chapter 5, C. serrulata and H. uninervis were exposed to three temperatures (20°C, 25°C and 30°C, spanning seasonal variation) and three target pCO₂ levels (present day 353 – 485 μatm; high 915 – 1102 μatm; extreme 1658 – 2297 μatm) for seven weeks. Net productivity, biomass allocation and enzyme activity as a proxy for carbon translocation (sucrosephosphate synthase SPS and sucrose synthase SS) were measured. Net productivity in C. serrulata and H. uninervis increased by 109 % and 197 % (P < 0.001) over the 10ºC rise (20 – 30ºC), respectively. In addition, temperature rise stimulated the increase of aboveground biomass in C. serrulata (26 – 35 %; P = 0.012) and H. uninervis (42 – 88 %; P = 0.006). Differences in the allocation of fixed carbon in response to temperature were evident. At warmer temperatures (where net productivity was highest), C. serrulata exported more carbohydrates to its rhizomes, while H. uninervis increased shoot density. In comparison, responses to CO₂ enrichment were limited to C. serrulata increasing above- to- below-ground ratio (P = 0.003) and H. uninervis increasing net productivity the least at 30ºC (pCO₂ × temperature: P = 0.047). This study highlights that temperature exerts a much stronger control over carbon metabolism than CO₂ enrichment in tropical seagrasses.

In summary, the effects of OA on seagrass physiology varied with light availability and water temperature. Ocean acidification cannot fully compensate for productivity losses caused by reduced light. Nitrate fertilization did not enhance seagrass productivity responses to CO₂ enrichment, but it might have indirect impacts encouraging the growth of algae, which can thrive in nutrient and CO₂ enriched conditions. An overall analysis (Chapter 6) of results from all chapters suggests that nutrient status (leaf N content) might be a strong determinant of CO₂ responses, as C. serrulata and H. uninervis increased productivity at high pCO₂ when their tissue nutrient concentrations were elevated, but not at low tissue nutrient concentrations. Species-specific responses to OA and environmental parameters were consistently demonstrated, warning against the generalisation of responses across seagrass species. Overall, seagrass productivity can increase under OA, which is likely to make them future "winners" (sensu. Fabricius et al 2011) among tropical marine habitats; however localised conditions will affect their response and many of these remain untested.

Item ID: 44650
Item Type: Thesis (PhD)
Keywords: carbon dioxide levels; carbon sequestration; carbon utilization; CO2 levels; light levels; ocean acidification; physiological responses; seagrass meadows; seagrass metabolism; seagrass physiology; seagrasses; water quality
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Appendix 2 (permissions) are not available through this repository.

Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 2: Ow, Y.X., Collier, C.J., and Uthicke, S. (2015) Responses of three tropical seagrass species to CO2 enrichment. Marine Biology, 162 (5). pp. 1005-1017.

Chapter 3: Ow, Yan X., Uthicke, Sven, and Collier, Catherine J. (2016) Light levels affect carbon utilisation in tropical seagrass under ocean acidification. PLoS ONE, 11 (3). pp. 1-18.

Chapter 4: Ow, Y.X., Vogel, N., Collier, C.J., Holtum, J.A.M., Flores, F., and Uthicke, S. (2016) Nitrate fertilisation does not enhance CO₂ responses in two tropical seagrass species. Scientific Reports, 6. pp. 1-10.

Date Deposited: 11 Aug 2016 04:59
FoR Codes: 06 BIOLOGICAL SCIENCES > 0607 Plant Biology > 060701 Phycology (incl Marine Grasses) @ 40%
06 BIOLOGICAL SCIENCES > 0607 Plant Biology > 060705 Plant Physiology @ 20%
06 BIOLOGICAL SCIENCES > 0699 Other Biological Sciences > 069902 Global Change Biology @ 40%
SEO Codes: 96 ENVIRONMENT > 9603 Climate and Climate Change > 960305 Ecosystem Adaptation to Climate Change @ 50%
96 ENVIRONMENT > 9603 Climate and Climate Change > 960307 Effects of Climate Change and Variability on Australia (excl. Social Impacts) @ 50%
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