Marguerite S. Koch

Climate change and ocean acidification effects on seagrasses and marine macroalgae

Although seagrasses and marine macroalgae (macro-autotrophs) play critical ecological roles in reef, lagoon, coastal and open-water ecosystems, their response to ocean acidification (OA) and climate change is not well understood. In this review, we examine marine macro-autotroph biochemistry and physiology relevant to their response to elevated dissolved inorganic carbon [DIC], carbon dioxide [CO2 ], and lower carbonate [CO3 (2-) ] and pH. We also explore the effects of increasing temperature under climate change and the interactions of elevated temperature and [CO2 ]. Finally, recommendations are made for future research based on this synthesis. A literature review of >100 species revealed that marine macro-autotroph photosynthesis is overwhelmingly C3 (≥ 85%) with most species capable of utilizing HCO3 (-) ; however, most are not saturated at current ocean [DIC]. These results, and the presence of CO2 -only users, lead us to conclude that photosynthetic and growth rates of marine macro-autotrophs are likely to increase under elevated [CO2 ] similar to terrestrial C3 species. In the tropics, many species live close to their thermal limits and will have to up-regulate stress-response systems to tolerate sublethal temperature exposures with climate change, whereas elevated [CO2 ] effects on thermal acclimation are unknown. Fundamental linkages between elevated [CO2 ] and temperature on photorespiration, enzyme systems, carbohydrate production, and calcification dictate the need to consider these two parameters simultaneously. Relevant to calcifiers, elevated [CO2 ] lowers net calcification and this effect is amplified by high temperature. Although the mechanisms are not clear, OA likely disrupts diffusion and transport systems of H(+) and DIC. These fluxes control micro-environments that promote calcification over dissolution and may be more important than CaCO3 mineralogy in predicting macroalgal responses to OA. Calcareous macroalgae are highly vulnerable to OA, and it is likely that fleshy macroalgae will dominate in a higher CO2 ocean; therefore, it is critical to elucidate the research gaps identified in this review.

Sulfide as a phytotoxin to the tropical seagrass Thalassia testudinum: interactions with light, salinity and temperature

Over the last several decades, sulfides have been identified as a potent phytotoxin. However, little is known about the effects of sulfide on Thalassia testudinum, a dominant tropical seagrass, or other seagrass species. It has been hypothesized that high sulfide exposure is a major contributor to T. testudinum “die-back” in the large subtropical lagoon of South Florida, Florida Bay. Three experiments were conducted to pursue the mechanism by which T. testudinum was resilient to sulfide exposure in our previous experiment and to investigate the levels of sulfide that cause T. testudinum mortality. Two low-light (∼150 μmol PAR m−2 s−1) experiments were conducted to evaluate the role of light and photosynthesis on sulfide toxicity. Secondly, we tested the effects of high salinity (HS) and high temperature (HT) on sulfide tolerance to determine if these interactions could synergistically create a “die-back” response. Leaf elongation rates were not significantly affected by below-ground sulfide exposure in the range of 1–10 mM when incubated at subsaturating light and ambient sediment pH (7.0). Leaf O2 production rates were also unaffected by sulfide exposure. In fact, all plants post-treatment possessed rhizome-extractable O2 concentrations greater than 30%. When sulfide treatments (6 mM) were combined with HS and HT treatments, however, we observed our first “die-back” response. Shoots exposed to 6.0 mM sulfide under HS and HT had 50% and 33% mortality rates, and those in the HT+HS treatment had 100% mortality. Interestingly, no mortality was seen in the HS or HT treatments without sulfides added. The first two experiments in this study and our previous experiment clearly suggest that T. testudinum may be tolerant to short-term (<28 days) below-ground tissue exposure to high sulfide concentrations. An important caveat appears to be, however, when sulfide exposure is combined with other stressors common in Florida Bay and other tropical/subtropical lagoons and estuaries. These results point to the importance of examining multiple interactive stressors when elucidating the factors causing “die-back” in seagrasses.

Phosphorus uptake kinetics of a dominant tropical seagrass Thalassia testudinum

Although nitrogen is primarily the dominant nutrient limiting seagrass production in temperate estuaries, phosphorus (P) limitation can be important in tropical carbonate-dominated seagrass systems. While nitrogen uptake kinetics of seagrasses are moderately well established, very limited data exist on the dynamics of P-uptake. In this study, we determined the kinetics of dissolved inorganic phosphorus (Pi) uptake for a dominant tropical seagrass Thalassia testudinumacross a range of Pi levels (0.5–25M). Under this broad range, leaf Pi-uptake (mol g −1 dw h −1 ) rates were similar under light (Vmax = 1.90) and dark (Vmax = 2.10) conditions, while root Pi-uptake rates declined 30% in the dark, and were significantly lower than leaves under both light ( Vmax = 0.57) and dark (Vmax = 0.38) conditions. At lower Pi concentrations (0.5–5.0M), leaf Vmax was 2–3-fold lower (0.50–0.77), while root Vmax was the same at high and low Pi ranges. Based on linear and non-linear models of Pi-uptake kinetics for T. testudinum, leaves can contribute a majority of the P sequestered by the plant when surface and porewater Pi levels are equally low (0.05–0.5M). Based on the calculated P-demand of T. testudinum in South Florida, solely root or leaf uptake can account for the P requirements of T. testudinum when porewater or surface water Pi levels are 0.5M. However, when surface and porewater Pi levels are extremely low (<0.10M), such as in Florida Bay and other carbonate seagrass systems where Pi sequestration by the sediment is highly efficient, even root + leaf Pi-uptake rates do not meet the P requirements for growth and P-limitation may occur.

Biotic Control of Surface pH and Evidence of Light-Induced H+ Pumping and Ca2+-H+ Exchange in a Tropical Crustose Coralline Alga

Presently, an incomplete mechanistic understanding of tropical reef macroalgae photosynthesis and calcification restricts predictions of how these important autotrophs will respond to global change. Therefore, we investigated the mechanistic link between inorganic carbon uptake pathways, photosynthesis and calcification in a tropical crustose coralline alga (CCA) using microsensors. We measured pH, oxygen (O2), and calcium (Ca2+) dynamics and fluxes at the thallus surface under ambient (8.1) and low (7.8) seawater pH (pHSW) and across a range of irradiances. Acetazolamide (AZ) was used to inhibit extracellular carbonic anhydrase (CAext), which mediates hydrolysis of HCO3-, and 4,4′ diisothiocyanatostilbene-2,2′-disulphonate (DIDS) that blocks direct HCO3- uptake by anion exchange transport. Both inhibited photosynthesis, suggesting both diffusive uptake of CO2 via HCO3- hydrolysis to CO2 and direct HCO3- ion transport are important in this CCA. Surface pH was raised approximately 0.3 units at saturating irradiance, but less when CAext was inhibited. Surface pH was lower at pHSW 7.8 than pHSW 8.1 in the dark, but not in the light. The Ca2+ fluxes were large, complex and temporally variable, but revealed net Ca2+ uptake under all conditions. The temporal variability in Ca2+ dynamics was potentially related to localized dissolution during epithallial cell sloughing, a strategy of CCA to remove epiphytes. Simultaneous Ca2+ and pH dynamics suggest the presence of Ca2+/H+ exchange. Rapid light-induced H+ surface dynamics that continued after inhibition of photosynthesis revealed the presence of a light-mediated, but photosynthesis-independent, proton pump. Thus, the study indicates metabolic control of surface pH can occur in CCA through photosynthesis and light-inducible H+ pumps. Our results suggest that complex light-induced ion pumps play an important role in biological processes related to inorganic carbon uptake and calcification in CCA.

Inorganic phosphorus uptake in a carbonate-dominated seagrass ecosystem

Seasonal phosphate (Pi) uptake kinetics were determined using chambers encompassing the water column, sediment and the entire system (water column + sediment + seagrass/epiphyte) in Florida Bay (FB) during 2003–2006 and on the Little Bahama Bank (LBB) during a cruise June, 2004. Pi uptake was a linear function of concentration at low Pi levels (< 2 μmo11-1). Applying the Pi system rate constant (Sp) from western (177 ±50 x 10-6 m s-1) and eastern (272 ±66 x 10-6 m s-1) bay sites, and using Pi measured during the study (0.02 to 0.177 μmol Pi 1-1), we calculated a Pi uptake rate of 0.30 to 2.62 mmol Pi m-2 d-1 for western and 0.47 to 4.16 mmol Pi m-2 d-1 for eastern bay sites which includes phytoplankton uptake (0.455 m height). During non-bloom conditions, phytoplankton dominated Pi uptake in the east (46%) and both phytoplankton and the seagrass-epiphyte consortium in the west (32 and 52%, respectively), with a smaller contribution by the sediment (15–20%). On LBB interior sites, the water column always dominated (≽94%) Pi uptake with a higher Sp (573-881 x 10-6 m s-1) than FB. During cyanobacterial blooms in FB (chla 17 μg 1-1), the water column dominated Pi uptake (100%) and Sp was the highest (>2,800 x 10-6 m s-1) measured. Phytoplankton accounted for 88% of this sequestered Pi with only 12% in the acid extractable fraction, likely as calcium bound and/or adsorbed P, and only 1% attributable to small heterotrophs. When chl α levels declined (2 μg I-1) Pi uptake was still dominated by phytoplankton (77%), the acid extractable pool increased (18%) and the heterotrophic community became more important (22%). In carbonate-dominated seagrass systems, Pi is primarily taken up by the water column biota and is subsequently remineralized/hydrolyzed in the water column or settles to the benthos where it becomes available to benthic primary producers.

The role of irradiance and C-use strategies in tropical macroalgae photosynthetic response to ocean acidification

Fleshy macroalgae may increase photosynthesis with greater CO2 availability under ocean acidification (OA) and outcompete calcifying macroalgae important for tropical reef accretion. Macroalgae use energy-dependent carbon concentrating mechanisms (CCMs) to take up HCO3−, the dominant inorganic carbon for marine photosynthesis, but carbon-use strategies may depend on the pCO2, pH and irradiance. We examined photosynthesis in eight tropical macroalgae across a range of irradiances (0–1200 μmol photon m−2 s−1), pH levels (7.5–8.5) and CO2 concentrations (3–43 μmol kg−1). Species-specific CCM strategies were assessed using inhibitors and δ13C isotope signatures. Our results indicate that the log of irradiance is a predictor of the photosynthetic response to elevated pCO2 (R2 > 0.95). All species utilized HCO3−, exhibited diverse C-use pathways and demonstrated facultative HCO3− use. All fleshy species had positive photosynthetic responses to OA, in contrast to a split amongst calcifiers. We suggest that shifts in photosynthetically-driven tropical macroalgal changes due to OA will most likely occur in moderate to high-irradiance environments when CCMs are ineffective at meeting the C-demands of photosynthesis. Further, facultative use of HCO3− allows greater access to CO2 for photosynthesis under OA conditions, particularly amongst fleshy macroalgae, which could contribute to enhance fleshy species dominance over calcifiers.

Primary Utricle Structure of Six Halimeda Species and Potential Relevance for Ocean Acidification Tolerance

Abstract Variations in utricle morphology may be responsible for different tolerances to ocean acidification (OA) within the macroalgal genus Halimeda, an important sediment producer on reefs. However, differences in species’ utricle morphology and their relationship to calcification and crystal formation have not been well articulated. In the present study, we characterized the utricle morphologies of six Halimeda species. Primary utricle ultrastructure was quantitatively and qualitatively compared to tissue inorganic content and crystal microstructure. Morphologies differed across species and several morphometric relationships were revealed. Primary utricle size (r2=0.70) and diffusion pathway length (r2=0.87) had inverse relationships with inorganic content based on regression analyses, and corresponded to crystal microstructure form. Species with large utricles and long diffusion pathways contained more narrow (~0.15 μm) aragonite needles and minimal micro-anhedral crystal formations. In contrast, species with small utricles and short diffusion pathways elucidated aggregates of micro-anhedral crystals and wider aragonite needles (~0.30 μm). Species’ utricle characteristics generally corresponded to specific evolutionary lineages. Thus, characteristics of Halimeda utricle morphology may control long-term adaptive responses to OA, an idea articulated in the broader literature.