Biogeographic variability in the physiological response of the cold‐water coral Lophelia pertusa to ocean acidification

Net calcification rates for coral reef and other calcifiers have been shown to decline as ocean acidification (OA) occurs. However, the role of calcium carbonate dissolution in lowering net calcification rates is unclear. The objective of this study was to distinguish OA effects on calcification and dissolution rates in dominant calcifying macroalgae of the Florida Reef Tract, including two rhodophytes (Neogoniolithon strictum, Jania adhaerens) and two chlorophytes (Halimeda scabra, Udotea luna). Two experiments were conducted: (1) to assess the difference in gross (45Ca uptake) versus net (total alkalinity anomaly) calcification rates in the light/dark and (2) to determine dark dissolution (45CaCO3), using pH levels predicted for the year 2100 and ambient pH. At low pH in the light, all species maintained gross calcification rates and most sustained net calcification rates relative to controls. Net calcification rates in the dark were ~84% lower than in the light. In contrast to the light, all species had lower net calcification rates in the dark at low pH with chlorophytes exhibiting net dissolution. These data are supported by the relationship (R2 = 0.82) between increasing total alkalinity and loss of 45Ca from pre-labelled 45CaCO3 thalli at low pH in the dark. Dark dissolution of 45CaCO3-labelled thalli was ~18% higher in chlorophytes than rhodophytes at ambient pH, and ~ twofold higher at low pH. Only Udotea, which exhibited dissolution in the light, also had lower daily calcification rates integrated over 24 h. Thus, if tropical macroalgae can maintain high calcification rates in the light, lower net calcification rates in the dark from dissolution may not compromise daily calcification rates. However, if organismal dissolution in the dark is additive to sedimentary carbonate losses, reef dissolution may be amplified under OA and contribute to erosion of the Florida Reef Tract and other reefs that exhibit net dissolution.

Irradiance, photosynthesis and elevated pCO2 effects on net calcification in tropical reef macroalgae

Ocean acidification, the decrease in seawater pH due to the absorption of atmospheric CO2, profoundly threatens the survival of a large number of marine species. Cold-water corals are considered to be among the most vulnerable organisms to ocean acidification because they are already exposed to relatively low pH and corresponding low calcium carbonate saturation states (?). Lophelia pertusa is a globally distributed cold-water scleractinian coral that provides critical three-dimensional habitat for many ecologically and economically significant species. In this study, four different genotypes of L. pertusa were exposed to three pH treatments (pH = 7.60, 7.75, and 7.90) over a short (2-week) experimental period, and six genotypes were exposed to two pH treatments (pH = 7.60 and 7.90) over a long (6-month) experimental period. Their physiological response was measured as net calcification rate and the activity of carbonic anhydrase, a key enzyme in the calcification pathway. In the short-term experiment, net calcification rates did not significantly change with pH, although they were highly variable in the low pH treatment, including some genotypes that maintained positive net calcification in undersaturated conditions. In the 6-month experiment, average net calcification was significantly reduced at low pH, with corals exhibiting net dissolution of skeleton. However, one of the same genotypes that maintained positive net calcification (+0.04% day?1) under the low pH treatment in the short-term experiment also maintained positive net calcification longer than the other genotypes in the long-term experiment, although none of the corals maintained positive calcification for the entire 6 months. Average carbonic anhydrase activity was not affected by pH, although some genotypes exhibited small, insignificant, increases in activity after the sixth month. Our results suggest that while net calcification in L. pertusa is adversely affected by ocean acidification in the long term, it is possible that some genotypes may prove to be more resilient than others, particularly to short perturbations of the carbonate system. These results provide evidence that populations of L. pertusa in the Gulf of Mexico may contain the genetic variability necessary to support an adaptive response to future ocean acidification.

Rates of net production, net calcification, and nutrient uptake were measured in a coral‐dominated reef flat community on Ningaloo Reef in northwestern Australia under seasonally minimum and maximum light levels. Daily integrated light decreased twofold while water temperatures remained relatively constant increasing by only 1°C on average from summer to winter. Rates of daily community gross primary production (GPP) were only 33% ± 9% higher in summer than in winter (1400 ± 70 versus 1050 ± 60 mmol C m−2 d−1), far less than the twofold seasonal changes reported for most shallow reef communities. Rates of daily community net calcification (Gnet) were not significantly different between seasons (190 ± 40 mmol CaCO3 m−2 d−1 in summer versus 200 ± 10 mmol CaCO3 m−2 d−1 in winter). The average rate of total nitrogen uptake (dissolved + particulate) was also not significantly different between summer and winter (8.3 ± 3.8 versus 6.6 ± 3.4 mmol N m−2 d−1, respectively), despite evidence of sporadically high nitrate uptake in both seasons. In summer, rates of hourly net calcification (gnet) were linearly correlated with diurnal changes in net production, pH, and aragonite saturation state (Ωar); and were mostly correlated with light except at mid‐day under heavy cloud cover. However, in winter,gnet was independent of diurnal changes in light, net production, pH, and Ωar indicating that the reef flat community had possibly reached a threshold above which rates of net calcification were insensitive to diurnal changes in their environment.

Ocean acidification is expected to intensify due to increasing levels in the partial pressure of atmospheric CO2 (pCO2). This could negatively affect major calcifying reef organisms. In this study, the effects of different levels of CO2-driven acidification of seawater (control: pH 8.1; moderate: pH 7.8; intermediate: pH 7.5; and severe: pH 7.2) on the net calcification rate and activity of enzymes related to the calcification process (Ca-ATPase and carbonic anhydrase) were evaluated in the calcareous hydrozoan Millepora alcicornis. The experiment was run for 30 d using a marine mesocosm system. Net calcification ratio was significantly reduced in hydrocorals exposed to intermediate seawater acidification for 16 d and to severe seawater acidification for 16 d or 30 d, compared to animals at control conditions. However, only hydrocorals exposed to severe seawater acidification showed lower net calcification rates than those exposed to control conditions for 30 d. In accordance, the activities of enzymes involved in the calcification process markedly increased in hydrocorals exposed to reduced pH. Ca-ATPase seemed to be more sensitive to seawater acidification than carbonic anhydrase as it increased in hydrocorals exposed to intermediate and severe seawater acidification for 30 d, while carbonic anhydrase activity was only stimulated under severe seawater acidification. Therefore, our findings clearly show that the hydrocoral M. alcicornis is able to cope, to some extent, with long-term CO2-driven acidification of seawater (pH ≥ 7.5). In addition, they show that Ca-ATPase plays a key role in the maintenance of calcification rate under scenarios of moderate and intermediate levels of seawater acidification. However, the observed increase in Ca-ATPase and carbonic anhydrase activity was not enough to compensate for the effects of CO2-driven reduction in seawater pH on the net calcification rate of the hydrocoral M. alcicornis under a scenario of severe ocean acidification (pH 7.2).

Ocean acidification is perceived to be a major threat for many calcifying organisms, including scleractinian corals. Here, we investigate (1) whether past exposure to low pH environments associated with CO2 vents could increase corals tolerance to low pH and (2) whether zooxanthellate corals are more tolerant to low pH than azooxanthellate corals. To test these hypotheses, two Mediterranean colonial corals Cladocora caespitosa (zooxanthellate) and Astroides calycularis (azooxanthellate) were collected from CO2 vents and reference sites and incubated in the laboratory under present day (pH on the total scale, pHT 8.07) and low pH conditions (pHT 7.70). Rates of net calcification, dark respiration, and photosynthesis were monitored during a 6‐month experiment. Monthly net calcification was assessed every 27–35 d using the buoyant weight technique, whereas light and dark net calcification was estimated using the alkalinity anomaly technique during 1‐h incubations. Neither species showed any change in net calcification rates, respiration, and photosynthesis regardless of their environmental history, pH treatment, and trophic strategy. Our results indicate that C. caespitosa and As. calycularis could tolerate future ocean acidification conditions for at least 6 months. These results will aid in predicting species' future responses to ocean acidification, and thus improve the management and conservation of Mediterranean corals.

Ocean acidification reduces net calcification and wound healing in the tropical crustose coralline alga, Porolithon onkodes (Corallinales, Rhodophyta)

Coral reefs are harboring a large part of the marine biodiversity and are important ecosystems for the equilibrium of the oceans. As a consequence of anthropogenic CO2 emission, a drop in pH and an increase in seawater temperature is observed in the Gulf coastal waters that potentially threaten coral assemblages. An experimental study was conducted on two species of corals to assess the effect of ocean warming and ocean acidification on the net calcification rate. Two pH conditions 8.2 and 7.5 and three temperatures, 22.5, 27.5 and 32.5 °C, were considered. Net calcification rates were measured using 45Ca radiotracer. Both temperature and pH had a significant effect on net calcification rates following a similar pattern for both species. The highest calcification rate was observed at low temperature and high pH. Increased temperature and decreased pH led to a decrease in net calcification rates. An interactive effect was observed as the effect of pH decreased with increasing temperature. However, the two species of coral were able to calcify in all the tested combination of temperature and pH suggesting that they are adapted to short term changes in temperature and pH. Ability to calcify even at a high temperature of 32.5 °C that is identical to the summertime Gulf seawater temperature under both the ambient and low pH condition with no mortalities, raises a question: are these corals adapted to high seawater temperatures and low pH? More in-depth assessments will be required to confirm if this is an adaptation to higher temperatures in Persian Gulf corals.

Abstract. The severity of the impact of elevated atmospheric pCO2 to coral reef ecosystems depends, in part, on how seawater pCO2 affects the balance between calcification and dissolution of carbonate sediments. Presently, there are insufficient published data that relate concentrations of pCO2 and CO32− to in situ rates of reef calcification in natural settings to accurately predict the impact of elevated atmospheric pCO2 on calcification and dissolution processes. Rates of net calcification and dissolution, CO32− concentrations, and pCO2 were measured, in situ, on patch reefs, bare sand, and coral rubble on the Molokai reef flat in Hawaii. Rates of calcification ranged from 0.03 to 2.30 mmol CaCO3 m−2 h−1 and dissolution ranged from –0.05 to –3.3 mmol CaCO3 m−2 h−1. Calcification and dissolution varied diurnally with net calcification primarily occurring during the day and net dissolution occurring at night. These data were used to calculate threshold values for pCO2 and CO32− at which rates of calcification and dissolution are equivalent. Results indicate that calcification and dissolution are linearly correlated with both CO32− and pCO2. Threshold pCO2 and CO32− values for individual substrate types showed considerable variation. The average pCO2 threshold value for all substrate types was 654±195 μatm and ranged from 467 to 1003 μatm. The average CO32− threshold value was 152±24 μmol kg−1, ranging from 113 to 184 μmol kg−1. Ambient seawater measurements of pCO2 and CO32− indicate that CO32− and pCO2 threshold values for all substrate types were both exceeded, simultaneously, 13% of the time at present day atmospheric pCO2 concentrations. It is predicted that atmospheric pCO2 will exceed the average pCO2 threshold value for calcification and dissolution on the Molokai reef flat by the year 2100.

To date, studies of ocean acidification (OA) on coral reefs have focused on organisms rather than communities, and the few community effects that have been addressed have focused on shallow back reef habitats. The effects of OA on outer barrier reefs, which are the most striking of coral reef habitats and are functionally and physically different from back reefs, are unknown. Using 5-m long outdoor flumes to create treatment conditions, we constructed coral reef communities comprised of calcified algae, corals, and reef pavement that were assembled to match the community structure at 17m depth on the outer barrier reef of Moorea, French Polynesia. Communities were maintained under ambient and 1200μatm pCO2 for 7weeks, and net calcification rates were measured at different flow speeds. Community net calcification was significantly affected by OA, especially at night when net calcification was depressed ~78% compared to ambient pCO2 . Flow speed (2-14cms(-1) ) enhanced net calcification only at night under elevated pCO2 . Reef pavement also was affected by OA, with dissolution ~86% higher under elevated pCO2 compared to ambient pCO2 . These results suggest that net accretion of outer barrier reef communities will decline under OA conditions predicted within the next 100years, largely because of increased dissolution of reef pavement. Such extensive dissolution poses a threat to the carbonate foundation of barrier reef communities.

Open–ocean observations have revealed gradual changes in seawater carbon dioxide (CO2) chemistry resulting from uptake of atmospheric CO2 and ocean acidification (OA), but, with few long–term records (>5 years) of the coastal ocean that can reveal the pace and direction of environmental change. In this paper, observations collected from 1996 to 2016 at Harrington Sound, Bermuda, constitute one of the longest time–series of coastal ocean inorganic carbon chemistry. Uniquely, such changes can be placed into the context of contemporaneous offshore changes observed at the nearby Bermuda Atlantic Time-series Study (BATS) site. Onshore, surface dissolved inorganic carbon (DIC) and partial pressure of CO2 (pCO2; >10% change per decade) have increased and OA indicators such as pH and calcium carbonate (CaCO3) saturation state (Ω) decreased from 1996 to 2016 at a rate of two to three times that observed offshore at BATS. Such changes, combined with reduction of total alkalinity over time, reveal a complex interplay of biogeochemical processes influencing Bermuda reef metabolism, including net ecosystem production (NEP = gross primary production–autotrophic and heterotrophic respiration) and net ecosystem calcification (NEC = gross calcification–gross CaCO3 dissolution). These long–term data show a seasonal shift between wintertime net heterotrophy and summertime net autotrophy for the entire Bermuda reef system. Over annual time-scales, the Bermuda reef system does not appear to be in trophic balance, but rather slightly net heterotrophic. In addition, the reef system is net accretive (i.e., gross calcification > gross CaCO3 dissolution), but there were occasional periods when the entire reef system appears to transiently shift to net dissolution. A previous 5–year study of the Bermuda reef suggested that net calcification and net heterotrophy have both increased. Over the past 20 years, rates of net calcification and net heterotrophy determined for the Bermuda reef system have increased by ~30%, most likely due to increased coral nutrition occurring in concert with increased offshore productivity in the surrounding subtropical North Atlantic Ocean. Importantly, this long–term study reveals that other environmental factors (such as coral feeding) can mitigate against the effects of ocean acidification on coral reef calcification, at least over the past couple of decades.

There are serious concerns that ocean acidification will combine with the effects of global warming to cause major shifts in marine ecosystems, but there is a lack of field data on the combined ecological effects of these changes due to the difficulty of creating large‐scale, long‐term exposures to elevated CO2 and temperature. Here we report the first coastal transplant experiment designed to investigate the effects of naturally acidified seawater on the rates of net calcification and dissolution of the branched calcitic bryozoan Myriapora truncata (Pallas, 1766). Colonies were transplanted to normal (pH 8.1), high (mean pH 7.66, minimum value 7.33) and extremely high CO2 conditions (mean pH 7.43, minimum value 6.83) at gas vents off Ischia Island (Tyrrhenian Sea, Italy). The net calcification rates of live colonies and the dissolution rates of dead colonies were estimated by weighing after 45 days (May–June 2008) and after 128 days (July–October) to examine the hypothesis that high CO2 levels affect bryozoan growth and survival differently during moderate and warm water conditions. In the first observation period, seawater temperatures ranged from 19 to 24 °C; dead M. truncata colonies dissolved at high CO2 levels (pH 7.66), whereas live specimens maintained the same net calcification rate as those growing at normal pH. In extremely high CO2 conditions (mean pH 7.43), the live bryozoans calcified significantly less than those at normal pH. Therefore, established colonies of M. truncata seem well able to withstand the levels of ocean acidification predicted in the next 200 years, possibly because the soft tissues protect the skeleton from an external decrease in pH. However, during the second period of observation a prolonged period of high seawater temperatures (25–28 °C) halted calcification both in controls and at high CO2, and all transplants died when high temperatures were combined with extremely high CO2 levels. Clearly, attempts to predict the future response of organisms to ocean acidification need to consider the effects of concurrent changes such as the Mediterranean trend for increased summer temperatures in surface waters. Although M. truncata was resilient to short‐term exposure to high levels of ocean acidification at normal temperatures, our field transplants showed that its ability to calcify at higher temperatures was compromised, adding it to the growing list of species now potentially threatened by global warming.

Ocean acidification caused by anthropogenic uptake of CO2 is perceived to be a major threat to calcifying organisms. Cold-water corals were thought to be strongly affected by a decrease in ocean pH due to their abundance in deep and cold waters which, in contrast to tropical coral reef waters, will soon become corrosive to calcium carbonate. Calcification rates of two Mediterranean cold-water coral species, Lophelia pertusa and Madrepora oculata, were measured under variable partial pressure of CO2 (pCO2) that ranged between 380 µatm for present-day conditions and 930 µatm for the end of the century. The present study addressed both short- and long-term responses by repeatedly determining calcification rates on the same specimens over a period of 9 months. Besides studying the direct, short-term response to elevated pCO2 levels, the study aimed to elucidate the potential for acclimation of calcification of cold-water corals to ocean acidification. Net calcification of both species was unaffected by the levels of pCO2 investigated and revealed no short-term shock and, therefore, no long-term acclimation in calcification to changes in the carbonate chemistry. There was an effect of time during repeated experiments with increasing net calcification rates for both species, however, as this pattern was found in all treatments, there is no indication that acclimation of calcification to ocean acidification occurred. The use of controls (initial and ambient net calcification rates) indicated that this increase was not caused by acclimation in calcification response to higher pCO2. An extrapolation of these data suggests that calcification of these two cold-water corals will not be affected by the pCO2 level projected at the end of the century.

Water quality and criculation in Florida Bay (a shallow, subtropical estuary in south Florida) are highly dependent upon the development and evolution of carbonate mud banks distributed throughout the Bay. Predicting the effect of natural and anthropogenic perturbations on carbonate sedimentation requires an understanding of annual, seasonal, and daily variations in the biogenic and inorganic processes affecting carbonate sediment precipitation and dissolution. In this study, net calcification rates were measured over diurnal cycles on 27 d during summer and winter from 1999 to 2003 on mud banks and four representative substrate types located within basins between mud banks. Substrate types that were measured in basins include seagrass beds of sparse and intermediate densityThalassia sp., mud bottom, and hard bottom communities. Changes in total alkalinity were used as a proxy for calcification and dissolution. On 22 d (81%), diurnal variation in rates of net calcification was observed. The highest rates of net carbonate sediment production (or lowest rates of net dissolution) generally occurred during daylight hours and ranged from 2.900 to −0.410 g CaCO3 m−2d−1. The lowest rates of carbonate sediment production (or net sediment dissolution) occurred at night and ranged from 0.210 to −1.900 g CaCO3 m−2 night−1. During typical diurnal cycles, dissolution during the night consumed an average of 29% of sediment produced during the day on banks and 68% of sediment produced during the day in basins. Net sediment dissolution also occurred during daylight, but only when there was total cloud cover, high turbidity, or hypersalinity. Diurnal variation in calcification and dissolution in surface waters and surface sediments of Florida Bay is linked to cycling of carbon dioxide through photosynthesis and respiration. Estimation of long-term sediment accumulation rates from diurnal rates of carbonate sediment production measured in this study indicates an overall average accumulation rate for Florida Bay of 8.7 cm 1000 yr−1 and suggests that sediment dissolution plays a more important role than sediment transport in loss of sediment from Florida Bay.

AB Aquatic Biology Contact the journal Twitter RSS Mailing List Subscribe to our mailing list via Mailchimp HomeLatest VolumeAbout the JournalEditorsTheme Sections AB 7:59-70 (2009) - DOI: https://doi.org/10.3354/ab00182 Effects of carbon dioxide on the coccolithophorid Pleurochrysis carterae in incubation experiments Beatriz E. Casareto1,2,*, Mohan P. Niraula2,4, Hiroyuki Fujimura3, Yoshimi Suzuki2 1Laboratory of Aquatic Science and Consultant Co., Ltd., Meishin Bldg. Kamiikedai 1-14-1, Ota-ku, Tokyo 145-0064, Japan 2Graduate School of Science and Technology, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka 422-8529, Japan 3Department of Chemistry, Biology and Marine Science, Faculty of Science, University of the Ryukyus, Senbaru 1, Nishihara, Okinawa 903-0213, Japan 4Institute of Science and Technology, Tribhuvan University Trichandra Campus, Kathmandu, Nepal *Email: casaretobe@aol.com ABSTRACT: Production (abundance and biomass) and net calcification rates of the coccolithophorid Pleurochrysis carterae under different partial pressures of CO2 (pCO2) were examined using short (15, 24 and 39 h), long (7 d) and dark (7 d) incubation experiments. Short incubations were conducted at ambient, 500 and 820 ppm pCO2 levels in natural seawater that was enriched with nutrients and inoculated with P. carterae. Long incubations were conducted at ambient and 1200 ppm pCO2 levels in natural seawater (0.2 µm filtered as well as unfiltered) that was enriched with nutrients and inoculated with P. carterae. Dark incubations were conducted at ambient and 1200 ppm pCO2 in unfiltered seawater that was inoculated with P. carterae. The abundance and biomass of coccolithophorids increased with pCO2 and time. The abundance and biomass of most noncalcifying phytoplankton also increased, and were hardly affected by CO2 inputs. Net calcification rates were negative in short incubations during the pre-bloom phase regardless of pCO2 levels, indicating dissolution of calcium carbonate. Further, the negative values of net calcification in short incubations became less negative with time. Net calcification rates were positive in long incubations during blooms regardless of pCO2 level, and the rate of calcification increased with pCO2. Our results show that P. carterae may adapt to increased (~1200 ppm) pCO2 level with time, and such increase has little effect on the ecology of noncalcifying groups and hence in ecosystem dynamics. In dark incubations, net calcification rates were negative, with the magnitude being dependent on pCO2 levels. KEY WORDS: pCO2 · Pleurochrysis carterae · Noncalcifying phytoplankton · Biomass · Net calcification rates · Adaptation Full text in pdf format PreviousNextCite this article as: Casareto BE, Niraula MP, Fujimura H, Suzuki Y (2009) Effects of carbon dioxide on the coccolithophorid Pleurochrysis carterae in incubation experiments. Aquat Biol 7:59-70. https://doi.org/10.3354/ab00182 Export citation RSS - Facebook - Tweet - linkedIn Cited by Published in AB Vol. 7, No. 1-2. Online publication date: September 24, 2009 Print ISSN: 1864-7782; Online ISSN: 1864-7790 Copyright © 2009 Inter-Research.