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Impacts of ocean acidification on calcifying macroalgae: Padina sp. as a test case – a review

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Abstract

Since the Industrial Revolution, increasing atmospheric CO2 has been causing a rise in the concentration of carbon dioxide dissolved in seawater. This process results in seawater acidification, which has a major impact on the physical and chemical parameters of the oceans, consequently affecting the numerous calcifying organisms in the marine environment. Calcifying organisms secrete calcium carbonate in their inner or outer skeleton and include plankton (e.g. coccolithophores and foraminifera), corals, mussels and some of the macroalgae. Calcifying macroalgae make a critical contribution to the structure and function of marine ecosystems in several coastal biotas, providing food and shelter to diverse organisms. The present review summarizes the current information about the brown alga Padina sp. and its ecophysiology, focusing on the environmental control of the calcification process; suggests possible benefits that seaweeds may derive from their calcium carbonate cover, and discuss different future Intergovernmental Panel on Climate Change scenarios of ocean acidification and their likely impact on calcifying algae and on the ecosystems in which they are a key component.

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... In addition to altering pH, OA also reduces the availability of carbonate ions by decreasing the saturation state of calcium carbonate (CaCO 3 ) (Kleypas et al., 1999). Therefore, most studies investigating the physiological effects of OA have been conducted with calcifying organisms such as corals, echinoderms, and bivalve mollusks (Fine and Tchernov, 2007;Havenhand et al., 2008;Gazeau et al., 2010;Reuter et al., 2011;Hofmann and Bischof, 2014;Bhadury, 2015;Segman et al., 2016). However, the effects of OA on other marine species such as fishes remain poorly understood to date. ...
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Calcified macroalgae are distributed in marine habitats from polar to tropical latitudes and from intertidal shores to the deepest reaches of the euphotic zone. These algae play critical ecological roles including being key to a range of invertebrate recruitment processes, functioning as autogenic ecosystem engineers through provision of three-dimensional habitat structure, as well as contributing critical structural strength in coral reef ecosystems. Calcified macroalgae contribute significantly to the deposition of carbonates in coastal environments. These organisms are vulnerable to human-induced changes resulting from land and coastal development, such as altered patterns of sedimentation, nutrient enrichment through sewage and agricultural run-off, and are affected by coastal dredging and aquaculture. The consequences of increasing sea surface temperatures and fundamental changes in the carbon chemistry of seawater due to CO2 emissions from anthropogenic activities will have serious impacts on calcifying macroalgae. It is not yet understood how interactions between a range of variables acting at local and global scales will influence the viability of calcifying macroalgae and associated ecosystems. Research is urgently needed on all aspects of the taxonomy, biology and functional ecology of calcifying macroalgae. Without an understanding of the species present, measurement of change and understanding species-specific responses will not be possible.
Article
Anthropogenic CO2 is a major driver of present environmental change in most ecosystems1, and the related ocean acidification is threatening marine biota2. With increasing pCO2, calcification rates of several species decrease3, although cases of upregulation are observed4. Here, we show that biological control over mineralization relates to species abundance along a natural pH gradient. As pCO2 increased, the mineralogy of a scleractinian coral (Balanophyllia europaea) and a mollusc (Vermetus triqueter) did not change. In contrast, two calcifying algae (Padina pavonica and Acetabularia acetabulum) reduced and changed mineralization with increasing pCO2, from aragonite to the less soluble calcium sulphates and whewellite, respectively. As pCO2 increased, the coral and mollusc abundance was severely reduced, with both species disappearing at pH < 7.8. Conversely, the two calcifying and a non-calcifying algae (Lobophora variegata) showed less severe or no reductions with increasing pCO2, and were all found at the lowest pH site. The mineralization response to decreasing pH suggests a link with the degree of control over the biomineralization process by the organism, as only species with lower control managed to thrive in the lowest pH.
Article
The effects of elevated CO2 and temperature on photosynthesis and calcification in the calcifying algae Halimeda macroloba and Halimeda cylindracea and the symbiont-bearing benthic foraminifera Marginopora vertebralis were investigated through exposure to a combination of four temperatures (28 degrees C, 30 degrees C, 32 degrees C, and 34 degrees C) and four CO2 levels (39, 61, 101, and 203 Pa; pH 8.1, 7.9, 7.7, and 7.4, respectively). Elevated CO2 caused a profound decline in photosynthetic efficiency (F-V : F-M), calcification, and growth in all species. After five weeks at 34 degrees C under all CO2 levels, all species died. Chlorophyll (Chl) a and b concentration in Halimeda spp. significantly decreased in 203 Pa, 32 degrees C and 34 degrees C treatments, but Chl a and Chl c(2) concentration in M. vertebralis was not affected by temperature alone, with significant declines in the 61, 101, and 203 Pa treatments at 28 degrees C. Significant decreases in F-V : F-M in all species were found after 5 weeks of exposure to elevated CO2 (203 Pa in all temperature treatments) and temperature (32 degrees C and 34 degrees C in all pH treatments). The rate of oxygen production declined at 61, 101, and 203 Pa in all temperature treatments for all species. The elevated CO2 and temperature treatments greatly reduced calcification (growth and crystal size) in M. vertebralis and, to a lesser extent, in Halimeda spp. These findings indicate that 32 degrees C and 101 Pa CO2, are the upper limits for survival of these species on Heron Island reef, and we conclude that these species will be highly vulnerable to the predicted future climate change scenarios of elevated temperature and ocean acidification.
Article
Twenty-one studies on the effects of pH on marine phytoplankton were found and are herein reviewed. Under laboratory conditions, the optimum pH for growth is between pH 6.3 and 10. Some species can grow well at a wide range of pH, while others have growth rates that vary greatly over a 0.5 to 1 pH unit change. Different clones of the same species were found to have slightly to strikingly different relationships between pH and growth rate. The pH in typical coastal environments may vary by 1 or more pH units, with over 10% of observations being more than 0.5 units above or below equilibrium pH. This range is great enough, relative to the observed pH effect on growth rate for many species, for seawater pH to affect the growth rate, and hence the timing and abundance of coastal marine phytoplankton species. Effects of pH are not limited to extreme pH conditions. The growth rates of some species are influenced significantly by changes in pH near the equilibrium pH of coastal seawater. Care must be taken in growth experiments with phytoplankton to avoid effects due to pH of the culture media. Eutrophication of coastal waters may amplify the range of pH found in coastal environments.
Article
The influence of elevated CO2 concentrations on growth and photosynthesis ofGracilaria sp. andG. chilensis was investigated in order to procure information on the effective utilization of CO2. Growth of both was enhanced by CO2 enrichment (air + 650 ppm CO2, air + 1250 ppm CO2, the enhancement being greater inGracilaria sp. Both species increased uptake of NO3− with CO2 enrichment. Photosynthetic inorganic carbon uptake was depressed inG. chilensis by pre-culture (15 days) with CO2 enrichment, but little affected inGracilaria sp. Mass spectrometric analysis showed that O2 uptake was higher in the light than in the dark for both species and in both cases was higher inGracilaria sp. The higher growth enhancement inGracilaria sp. was attributed to greater depression of photorespiration by the enrichment of CO2 in culture.
Article
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.
Article
Bicarbonate-based photosynthesis requires equal numbers of proton equivalents. Aquatic plants and photosynthetic symbioses can scavenge protons from ambient solutions, or they can manufacture protons through calcification. Both mechanisms are widely employed. This review examines how aquatic photoautotrophs couple calcification to photosynthesis, and the advantages and limitations of this physiology.Key words: calcification, calcium, carbonate, bicarbonate, photosynthesis, aquatic.
Article
A crystallization pathway describes the movement of ions from their source to the final product. Cells are intimately involved in biological crystallization pathways. In many pathways the cells utilize a unique strategy: They temporarily concentrate ions in intracellular membrane-bound vesicles in the form of a highly disordered solid phase. This phase is then transported to the final mineralization site, where it is destabilized and crystallizes. We present four case studies, each of which demonstrates specific aspects of biological crystallization pathways: seawater uptake by foraminifera, calcite spicule formation by sea urchin larvae, goethite formation in the teeth of limpets, and guanine crystal formation in fish skin and spider cuticles. Three representative crystallization pathways are described, and aspects of the different stages of crystallization are discussed. An in-depth understanding of these complex processes can lead to new ideas for synthetic crystallization processes of interest to mate...
Article
ABSTRACT: Since pre-industrial times, uptake of anthropogenic CO2 by surface ocean waters has caused a documented change of 0.1 pH units. Calcifying organisms are sensitive to elevated CO2 concentrations due to their calcium carbonate skeletons. In temperate rocky intertidal environments, calcifying and noncalcifying macroalgae make up diverse benthic photoautotrophic communities. These communities may change as calcifiers and noncalcifiers respond differently to rising CO2 concentrations. In order to test this hypothesis, we conducted an 86 d mesocosm ex periment to investigate the physiological and competitive responses of calcifying and noncalcifying temperate marine macroalgae to 385, 665, and 1486 μatm CO2. We focused on comparing 2 abundant red algae in the Northeast Atlantic: Corallina officinalis (calcifying) and Chondrus crispus (noncalcifying). We found an interactive effect of CO2 concentration and exposure time on growth rates of C. officinalis, and total protein and carbohydrate concentrations in both species. Photosynthetic rates did not show a strong response. Calcification in C. officinalis showed a parabolic response, while skeletal inorganic carbon decreased with increasing CO2. Community structure changed, as Chondrus crispus cover increased in all treatments, while C. officinalis cover decreased in both elevated-CO2 treatments. Photochemical parameters of other species are also presented. Our results suggest that CO2 will alter the competitive strengths of calcifying and noncalcifying temperate benthic macroalgae, resulting in different community structures, unless these species are able to adapt at a rate similar to or faster than the current rate of increasing seasurface CO2 concentrations.
Article
Preferences of the sea urchin Diadema antillarum (Echinodermata: Echinoidea) feeding on five species of brown macroalgae (Padina pavonica, Dyctiota dychotoma, Cystoseira abies-marina, Lobophora variegata and Halopteris filicina) have been studied using caging field experiments on Gran Canaria Island during August to October 2000. Results of three assays of both single and multiple diet experiments rejected the null hypothesis that Diadema does not feed selectively on the five selected algal species. In the multiple diet assays, Diadema consumed an average of 68–98 mg algae urchin−1 h−1 and 4–120 mg algae urchin−1 h−1 in the single diet experiments. On the basis of consumption, the five species of algae eaten can be divided into three groups. Thus Halopteris, Lobophora and Dyctiota were considered preferred algae, while Padina was considered an intermediate alga. Finally Cystoseira was significantly the less preferred and consumed seaweed in all sets of assays.
Article
The various estimates of the amount of anthropogenic CO2 taken up by the ocean that have been published in recent years are evaluated. It is shown that the estimate of Tans et al. (1990) neglects several important processes, and it is concluded that available evidence to date supports an annual mean uptake of about 2 Gt C/yr. Having established a 'best guess' for the oceanic CO2 uptake, one can then show that the total accumulation of CO2 in the atmosphere and ocean from 1980 to 1989 is significantly less than current estimates of the total CO2 emitted during that period. This implies either that the CO2 release from tropical deforestation is much smaller than currently estimated or that there is indeed a 'missing sink' for the CO2, albeit smaller than the one proposed by Tans et al.
Article
Predicting the impacts of ocean acidification on coastal ecosystems requires an understanding of the effects on macro-algae and their grazers, as these underpin the ecology of rocky shores. Whilst calcified coralline algae (Rhodophyta) appear to be especially vulnerable to ocean acidification, there is a lack of information concerning calcified brown algae (Phaeophyta), which are not obligate calcifiers but are still important producers of calcium carbonate and organic matter in shallow coastal waters. Here, we compare ecological shifts in subtidal rocky shore systems along CO 2 gradients created by volcanic seeps in the Mediterranean and Papua New Guinea, focussing on abundant macro-algae and grazing sea urchins. In both the temperate and tropical systems the abundances of grazing sea urchins declined dramatically along CO 2 gradients. Temperate and tropical species of the calcifying macroalgal genus Padina (Dictyoaceae, Phaeophyta) showed reductions in CaCO 3 content with CO 2 enrichment. In contrast to other studies of calcified macroalgae, however, we observed an increase in the abundance of Padina spp. in acidified conditions. Reduced sea urchin grazing pressure and significant increases in photosynthetic rates may explain the unexpected success of decalcified Padina spp. at elevated levels of CO 2 . This is the first study to provide a comparison of ecologi-cal changes along CO 2 gradients between temperate and tropical rocky shores. The similarities we found in the responses of Padina spp. and sea urchin abundance at several vent systems increases confidence in predictions of the ecological impacts of ocean acidification over a large geographical range.
Article
Previous studies have shown that increasing atmospheric CO2 concentrations affect calcification in some planktonic and macroalgal calcifiers due to the changed carbonate chemistry of seawater. However, little is known regarding how calcifying algae respond to solar UV radiation (UVR, UVA+UVB, 280–400 nm). UVR may act synergistically, antagonistically or independently with ocean acidification (high CO2/low pH of seawater) to affect their calcification processes. We cultured the articulated coralline alga Corallina sessilis Yendo at 380 ppmv (low) and 1000 ppmv (high) CO2 levels while exposing the alga to solar radiation treatments with or without UVR. The presence of UVR inhibited the growth, photosynthetic O2 evolution and calcification rates by13%, 6% and 3% in the low and by 47%, 20% and 8% in the high CO2 concentrations, respectively, reflecting a synergistic effect of CO2 enrichment with UVR. UVR induced significant decline of pH in the CO2-enriched cultures. The contents of key photosynthetic pigments, chlorophyll a and phycobiliproteins decreased, while UV-absorptivity increased under the high pCO2/low pH condition. Nevertheless, UV-induced inhibition of photosynthesis increased when the ratio of particulate inorganic carbon/particulate organic carbon decreased under the influence of CO2-acidified seawater, suggesting that the calcified layer played a UV-protective role. Both UVA and UVB negatively impacted photosynthesis and calcification, but the inhibition caused by UVB was about 2.5–2.6 times that caused by UVA. The results imply that coralline algae suffer from more damage caused by UVB as they calcify less and less with progressing ocean acidification.
Article
Abstract The effects of elevated partial pressure of CO2 (pCO2) and temperature, alone and in combination, on survival, calcification and dissolution were investigated in the crustose coralline alga Lithophyllum cabiochae. Algae were maintained in aquaria during 1 year at near-ambient conditions of irradiance, at ambient or elevated temperature (+3 °C) and at ambient [ca. 400 parts per million (ppm)] or elevated pCO2 (ca. 700 ppm). Algal necroses appeared at the end of summer under elevated temperature first at 700 ppm (60% of the thallus surface) and then at 400 ppm (30%). The death of algae was observed only under elevated temperature and was two- to threefold higher under elevated pCO2. During the first month of the experiment, net calcification was significantly reduced under elevated pCO2. At the end of the summer period, net calcification decreased by 50% when both temperature and pCO2 were elevated while no effect was found under elevated temperature and elevated pCO2 alone. In autumn and winter, net calcification in healthy algae increased with increasing temperature, independently of the pCO2 level, while necroses and death in the algal population caused a net dissolution at elevated temperature and pCO2. The dissolution of dead algal thalli was affected by elevated pCO2, being two- to fourfold higher than under ambient pCO2. These results suggest that net dissolution is likely to exceed net calcification in L. cabiochae by the end of this century. This could have major consequences in terms of biodiversity and biogeochemistry in coralligenous communities dominated by these algae.
Article
Calcification in the marine environment is the basis for the accretion of carbonate in structures such as coral reefs, algal ridges and carbonate sands. Among the organisms responsible for such calcification are the Corallinaceae (Rhodophyta), recognised as major contributors to the process world-wide. Hydrolithon sp. is a coralline alga that often forms rhodoliths in the Western Indian Ocean. In Zanzibar, it is commonly found in shallow lagoons, where it often grows within seagrass beds and/or surrounded by green algae such as Ulva sp. Since seagrasses in Zanzibar have recently been shown to raise the pH of the surrounding seawater during the day, and since calcification rates are sensitive to pH, which changes the saturation state of calcium carbonate, we measured the effects of pH on photosynthetic and calcification rates of this alga. It was found that pH had significant effects on both calcification and photosynthesis. While increased pH enhanced calcification rates both in the light and in the dark at pH >8.6, photosynthetic rates decreased. On the other hand, an increase in dissolved CO2 concentration to ∼26 μmol kg−1 (by bubbling with air containing 0.9 mbar CO2) caused a decrease in seawater pH which resulted in 20% less calcification after 5 days of exposure, while enhancing photosynthetic rates by 13%. The ecological implications of these findings is that photosynthetically driven changes in water chemistry by surrounding plants can affect calcification rates of coralline algae, as may future ocean acidification resulting from elevated atmospheric CO2.
Article
Predictions of an evolutionary model were examined for 43 tropical macroalgae using a functional-form group approach. The ranking from high to low primary producers (Sheet- and Filamentous-Groups > Coarsely Branched- and Thick Leathery-Groups > Jointed Calcareous- and Crustose-Groups), and data from the literature, support the hypothesis that persistent forms which allocate resources for environmental resistance, interference competition or antiherbivory defenses do so at the cost of lower primary production rates. The results for percent thallus lost to fish grazing over a 24 h period support the hypothesis that members of the Thick Leathery-, Jointed Calcareous- and Crustose-Groups have evolved antipredator defenses, with a tendency for decreasing herbivore resistance toward the Sheet- and Filamentous-Groups. The most heavily-calcified species (e.g. crustose corallines) ranked among the most grazer resistant as did the thick rubbery or leathery species. The ranking of functional-form group means for resistance to predation was as follows: Filamentous-Group (62% lost-24 h−1), Sheet-Group (42%), Coarsely Branched-Group (33%), Jointed Calcareous-Group (10%), Thick Leathery-Group (7%) and Crustose-Group (0%), in accordance with the hypothesis. The algal groups generally showed an increase in mean penetration toughness from filaments (
Article
The biosphere's great carbonate deposits, from caliche soils to deep-sea carbonate oozes, precipitate largely as by-products of autotrophic nutrient acquisition physiologies. Protons constitute the critical link: Calcification generates protons, which plants and photosynthetic symbioses use to assimilate bicarbonate and nutrients.A calcium ATPase-based “trans” mechanism underlies most biological calcification. This permits high calcium carbonate supersaturations and rapid carbonate precipitation.The competitive advantages of calcification become especially apparent in light and nutrient-deficient alkaline environments. Calcareous plants often dominate the lower euphotic zone in both the benthos and the plankton. Geographically and seasonally, massive calcification concentrates in nutrient-deficient environments including alkaline soils, coral reefs, cyanobacterial mats and coccolithophorid blooms. Structural and defensive uses for calcareous skeletons are sometimes overrated.