Effects of ocean acidification on population dynamics and community structure of crustose coralline algae

Calcification and growth of crustose coralline algae (CCA) are affected by elevated seawater pCO2 and associated changes in carbonate chemistry. However, the effects of ocean acidification (OA) on population and community-level responses of CCA have barely been investigated. We explored changes in community structure and population dynamics (size structure and reproduction) of CCA in response to OA. Recruited from an experimental flow-through system, CCA settled onto the walls of plastic aquaria and developed under exposure to one of three pCO2 treatments (control [present day, 389±6 ppm CO2], medium [753±11 ppm], and high [1267±19 ppm]). Elevated pCO2 reduced total CCA abundance and affected community structure, in particular the density of the dominant species Pneophyllum sp. and Porolithon onkodes. Meanwhile, the relative abundance of P. onkodes declined from 24% under control CO2 to 8.3% in high CO2 (65% change), while the relative abundance of Pneophyllum sp. remained constant. Population size structure of P. onkodes differed significantly across treatments, with fewer larger individuals under high CO2. In contrast, the population size structure and number of reproductive structures (conceptacles) per crust of Pneophyllum sp. was similar across treatments. The difference in the magnitude of the response of species abundance and population size structure between species may have the potential to induce species composition changes in the future. These results demonstrate that the impacts of OA on key coral reef builders go beyond declines in calcification and growth, and suggest important changes to aspects of population dynamics and community ecology.

Putting prey and predator into the CO2 equation-qualitative and quantitative effects of ocean acidification on predator-prey interactions

Little is known about the impact of ocean acidification on predator-prey dynamics. Herein, we examined the effect of carbon dioxide (CO(2)) on both prey and predator by letting one predatory reef fish interact for 24 h with eight small or large juvenile damselfishes from four congeneric species. Both prey and predator were exposed to control or elevated levels of CO(2). Mortality rate and predator selectivity were compared across CO(2) treatments, prey size and species. Small juveniles of all species sustained greater mortality at high CO(2) levels, while large recruits were not affected. For large prey, the pattern of prey selectivity by predators was reversed under elevated CO(2). Our results demonstrate both quantitative and qualitative consumptive effects of CO(2) on small and larger damselfish recruits respectively, resulting from CO(2)-induced behavioural changes likely mediated by impaired neurological function. This study highlights the complexity of predicting the effects of climate change on coral reef ecosystems.

Seawater carbonate chemistry and calcification rates of Porites rus and Hydrolithon onkodes in experiments of Moorea

Central to evaluating the effects of ocean acidification (OA) on coral reefs is understanding how calcification is affected by the dissolution of CO2 in sea water, which causes declines in carbonate ion concentration [CO3]2- and increases in bicarbonate ion concentration [HCO3]-. To address this topic, we manipulated [CO3]2- and [HCO3]- to test the effects on calcification of the coral Porites rus and the alga Hydrolithon onkodes, measured from the start to the end of a 15-day incubation, as well as in the day and night. [CO3]2- played a significant role in light and dark calcification of P. rus, whereas [HCO3]- mainly affected calcification in the light. Both [CO3]2- and [HCO3]- had a significant effect on the calcification of H. onkodes, but the strongest relationship was found with [CO3]2-. Our results show that the negative effect of declining [CO3]2- on the calcification of corals and algae can be partly mitigated by the use of [HCO3]- for calcification and perhaps photosynthesis. These results add empirical support to two conceptual models that can form a template for further research to account for the calcification response of corals and crustose coralline algae to OA.

Seawater carbonate chemistry, calcification rate, oxygen production, maximum quantum yield, symbiont density, chlorophyll concentration and crystal width of Halimeda macroloba, Halimeda cylindracea and Marginopora vertebralis during experiments, 2011

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°C, 30°C, 32°C, and 34°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 (FV : FM), calcification, and growth in all species. After five weeks at 34°C under all CO2 levels, all species died. Chlorophyll (Chl) a and b concentration in Halimeda spp. significantly decreased in 203 Pa, 32°C and 34°C treatments, but Chl a and Chl c2 concentration in M. vertebralis was not affected by temperature alone, with significant declines in the 61, 101, and 203 Pa treatments at 28°C. Significant decreases in FV : FM in all species were found after 5 weeks of exposure to elevated CO2 (203 Pa in all temperature treatments) and temperature (32°C and 34°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°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.

Seawater carbonate chemistry and calcification of the crustose coralline alga Hydrolithon onkodes in a laboratory experiment

Anthropogenic CO2 emissions have exacerbated two environmental stressors, global climate warming and ocean acidification (OA), that have serious implications for marine ecosystems. Coral reefs are vulnerable to climate change yet few studies have explored the potential for interactive effects of warming temperature and OA on an important coral reef calcifier, crustose coralline algae (CCA). Coralline algae serve many important ecosystem functions on coral reefs and are one of the most sensitive organisms to ocean acidification. We investigated the effects of elevated pCO2 and temperature on calcification of Hydrolithon onkodes, an important species of reef-building coralline algae, and the subsequent effects on susceptibility to grazing by sea urchins. H. onkodes was exposed to a fully factorial combination of pCO2 (420, 530, 830 µatm) and temperature (26, 29 °C) treatments, and calcification was measured by the change in buoyant weight after 21 days of treatment exposure. Temperature and pCO2 had a significant interactive effect on net calcification of H. onkodes that was driven by the increased calcification response to moderately elevated pCO2. We demonstrate that the CCA calcification response was variable and non-linear, and that there was a trend for highest calcification at ambient temperature. H. onkodes then was exposed to grazing by the sea urchin Echinothrix diadema, and grazing was quantified by the change in CCA buoyant weight from grazing trials. E. diadema removed 60% more CaCO3 from H. onkodes grown at high temperature and high pCO2 than at ambient temperature and low pCO2. The increased susceptibility to grazing in the high pCO2 treatment is among the first evidence indicating the potential for cascading effects of OA and temperature on coral reef organisms and their ecological interactions.

Carbon isotopic record of CO2 from the Holocene of the Dome C ice core

Reconstructions of atmospheric CO2 concentrations based on Antarctic ice cores reveal significant changes during the Holocene epoch, but the processes responsible for these changes in CO2 concentrations have not been unambiguously identified. Distinct characteristics in the carbon isotope signatures of the major carbon reservoirs (ocean, biosphere, sediments and atmosphere) constrain variations in the CO2 fluxes between those reservoirs. Here we present a highly resolved atmospheric d13C record for the past 11,000 years from measurements on atmospheric CO2 trapped in an Antarctic ice core. From mass-balance inverse model calculations performed with a simplified carbon cycle model, we show that the decrease in atmospheric CO2 of about 5 parts per million by volume (p.p.m.v.) and the increase in d13C of about 0.25% during the early Holocene is most probably the result of a combination of carbon uptake of about 290 gigatonnes of carbon by the land biosphere and carbon release from the ocean in response to carbonate compensation of the terrestrial uptake during the termination of the last ice age. The 20 p.p.m.v. increase of atmospheric CO2 and the small decrease in d13C of about 0.05% during the later Holocene can mostly be explained by contributions from carbonate compensation of earlier land-biosphere uptake and coral reef formation, with only a minor contribution from a small decrease of the land-biosphere carbon inventory.

Responses of the metabolism of the larvae of Pocillopora damicornis to ocean acidification and warming

Ocean acidification and warming are expected to threaten the persistence of tropical coral reef ecosystems. As coral reefs face multiple stressors, the distribution and abundance of corals will depend on the successful dispersal and settlement of coral larvae under changing environmental conditions. To explore this scenario, we used metabolic rate, at holobiont and molecular levels, as an index for assessing the physiological plasticity of Pocillopora damicornis larvae from this site to conditions of ocean acidity and warming. Larvae were incubated for 6 hours in seawater containing combinations of CO2 concentration (450 and 950 µatm) and temperature (28 and 30°C). Rates of larval oxygen consumption were higher at elevated temperatures. In contrast, high CO2 levels elicited depressed metabolic rates, especially for larvae released later in the spawning period. Rates of citrate synthase, a rate-limiting enzyme in aerobic metabolism, suggested a biochemical limit for increasing oxidative capacity in coral larvae in a warming, acidifying ocean. Biological responses were also compared between larvae released from adult colonies on the same day (cohorts). The metabolic physiology of Pocillopora damicornis larvae varied significantly by day of release. Additionally, we used environmental data collected on a reef in Moorea, French Polynesia to provide information about what adult corals and larvae may currently experience in the field. An autonomous pH sensor provided a continuous time series of pH on the natal fringing reef. In February/March, 2011, pH values averaged 8.075±0.023. Our results suggest that without adaptation or acclimatization, only a portion of naïve Pocillopora damicornis larvae may have suitable metabolic phenotypes for maintaining function and fitness in an end-of-the century ocean.

Seawater carbonate chemistry and Amphiprion melanopus activity during experiments, 2011

Two of the major threats to coral reefs are increasing sea surface temperature and ocean acidification, both of which result from rising concentrations of atmospheric carbon dioxide (CO2). Recent evidence suggests that both increased water temperature and elevated levels of dissolved CO2 can change the behaviors of fishes in ways that reduce individual fitness, however the interacting effects of these variables are unknown. We used a fully factorial experiment to test the independent and interactive effects of temperature (3 levels: 28.5, 30, and 31.5 °C) and pCO2 (3 levels: averaging 420, 530, and 960 µatm) on food consumption and activity level of juvenile anemonefish Amphiprion melanopus (Bleeker 1852). Experimental levels were consistent with current-day ocean conditions and predictions for mid-century and late-century based on atmospheric CO2 projections. Sibling fish were reared for 21 days from the end of their larval phase in each of the nine treatments, at which time behavioral observations were conducted. Food consumption and foraging activity decreased at the highest temperature. In isolation, CO2 level did not significantly affect behavior; however, there was an interaction with temperature. While rearing at high temperature (31.5 °C) and control (420 µatm) or moderate (530 µatm) CO2 resulted in a reduction of food consumption and foraging activity, rearing at high temperature and high CO2 (960 µatm) resulted in an elevation in these behaviors. Maintaining food consumption and foraging activity in high temperature and CO2 conditions may reduce energy efficiency if the thermal optimum for food assimilation and growth has been exceeded. Maintaining foraging effort might increase predation vulnerability. These results suggest that changes in foraging behaviors caused by the interactive effects of increased SST and CO2 could have significant effects on the growth and survival of juvenile reef fishes by late century.

Elevated CO2 affects embryonic development and larval phototaxis in a temperate marine fish

As an effect of anthropogenic CO2 emissions, the chemistry of the world's oceans is changing. Understanding how this will affect marine organisms and ecosystems are critical in predicting the impacts of this ongoing ocean acidification. Work on coral reef fishes has revealed dramatic effects of elevated oceanic CO2 on sensory responses and behavior. Such effects may be widespread but have almost exclusively been tested on tropical reef fishes. Here we test the effects elevated CO2 has on the reproduction and early life history stages of a temperate coastal goby with paternal care by allowing goby pairs to reproduce naturally in an aquarium with either elevated (ca 1400 µatm) CO2 or control seawater (ca 370 µatm CO2). Elevated CO2 did not affect the occurrence of spawning nor clutch size, but increased embryonic abnormalities and egg loss. Moreover, we found that elevated CO2 significantly affected the phototactic response of newly hatched larvae. Phototaxis is a vision-related fundamental behavior of many marine fishes, but has never before been tested in the context of ocean acidification. Our findings suggest that ocean acidification affects embryonic development and sensory responses in temperate fishes, with potentially important implications for fish recruitment.

Sponge bioerosion accelerated by ocean acidification across species and latitudes?

In many marine biogeographic realms, bioeroding sponges dominate the internal bioerosion of calcareous substrates such as mollusc beds and coral reef framework. They biochemically dissolve part of the carbonate and liberate so-called sponge chips, a process that is expected to be facilitated and accelerated in a more acidic environment inherent to the present global change. The bioerosion capacity of the demosponge Cliona celata Grant, 1826 in subfossil oyster shells was assessed via alkalinity anomaly technique based on 4 days of experimental exposure to three different levels of carbon dioxide partial pressure (pCO2) at ambient temperature in the cold-temperate waters of Helgoland Island, North Sea. The rate of chemical bioerosion at present-day pCO2 was quantified with 0.08-0.1 kg/m**2/year. Chemical bioerosion was positively correlated with increasing pCO2, with rates more than doubling at carbon dioxide levels predicted for the end of the twenty-first century, clearly confirming that C. celata bioerosion can be expected to be enhanced with progressing ocean acidification (OA). Together with previously published experimental evidence, the present results suggest that OA accelerates sponge bioerosion (1) across latitudes and biogeographic areas, (2) independent of sponge growth form, and (3) for species with or without photosymbionts alike. A general increase in sponge bioerosion with advancing OA can be expected to have a significant impact on global carbonate (re)cycling and may result in widespread negative effects, e.g. on the stability of wild and farmed shellfish populations, as well as calcareous framework builders in tropical and cold-water coral reef ecosystems.

Nongeniculate coralline algae from IODP Site 310-M0005D

Material cored during the Integrated Ocean Drilling Program (IODP) Expedition 310 'Tahiti Sea Level' revealed that the fossil reef systems around Tahiti are composed of two major stratigraphic sequences: (i) a last deglacial sequence; and (ii) an older Pleistocene sequence. The older Pleistocene carbonate sequence is composed of reef deposits associated with volcaniclastic sediments and was preserved in Hole 310-M0005D drilled off Maraa. Within an approximately 70-m-thick older Pleistocene sequence (33.22-101.93 m below seafloor; 92.85-161.56 m below present sealevel) in this hole, 11 depositional units are defined by lithological changes, sedimentological features, and paleontological characteristics and are numbered sequentially from the top of the hole downward (Subunits P1-P11). Paleowater depths inferred from nongeniculate coralline algae, combined with those determined by using corals and larger foraminifers, suggest two major sealevel rises during the deposition of the older Pleistocene sequence. Of these, the second sealevel rise is associated with an intervening sealevel drop. It is likely that the second sealevel rise corresponds to that during Termination II (TII, the penultimate deglaciation, from Marine Isotope Stages 6 to 5e). Therefore, the intervening sealevel drop can be correlated with that known as the 'sealevel reversal' during TII. Because there are limited data on the Pleistocene reef systems in the tropical South Pacific Ocean, this study provides important information about Pleistocene sealevel history, the evolution of coral reef ecosystems, and the responses of coral reefs to Quaternary climate changes.

Decline in growth of foraminifer Marginopora rossi under eutrophication and ocean acidification scenarios

The combination of global and local stressors is leading to a decline in coral reef health globally. In the case of eutrophication, increased concentrations of dissolved inorganic nitrogen (DIN) and phosphorus (DIP) are largely attributed to local land use changes. From the global perspective, increased atmospheric CO2 levels are not only contributing to global warming but also ocean acidification (OA). Both eutrophication and OA have serious implications for calcium carbonate production and dissolution among calcifying organisms. In particular, benthic foraminifera precipitate the most soluble form of mineral calcium carbonate (high-Mg calcite), potentially making them more sensitive to dissolution. In this study, a manipulative orthogonal two-factor experiment was conducted to test the effects of dissolved inorganic nutrients and OA on the growth, respiration and photophysiology of the large photosymbiont-bearing benthic foraminifer, Marginopora rossi. This study found the growth rate of M. rossi was inhibited by the interaction of eutrophication and acidification. The relationship between M. rossi and its photosymbionts became destabilized due to the photosymbiont's release from nutrient limitation in the nitrate-enriched treatment, as shown by an increase in zooxanthellae cells per host surface area. Foraminifers from the OA treatments had an increased amount of Chl a per cell, suggesting a greater potential to harvest light energy, however, there was no net benefit to the foraminifer growth. Overall, this study demonstrates that the impacts of OA and eutrophication are dose dependent and interactive. This research indicates an OA threshold at pH 7.6, alone or in combination with eutrophication, will lead to a decline in M. rossi calcification. The decline in foraminifera calcification associated with pollution and OA will have broad ecological implications across their ubiquitous range and suggests that without mitigation it could have serious implications for the future of coral reefs.

Contrasting effects of ocean acidification on tropical fleshy and calcareous algae

Despite the heightened awareness of ocean acidification (OA) effects on marine organisms, few studies empirically juxtapose biological responses to CO2 manipulations across functionally distinct primary producers, particularly benthic algae. Algal responses to OA may vary because increasing CO2 has the potential to fertilize photosynthesis but impair biomineralization. Using a series of repeated experiments on Palmyra Atoll, simulated OA effects were tested across a suite of ecologically important coral reef algae, including five fleshy and six calcareous species. Growth, calcification and photophysiology were measured for each species independently and metrics were combined from each experiment using a meta-analysis to examine overall trends across functional groups categorized as fleshy, upright calcareous, and crustose coralline algae (CCA). The magnitude of the effect of OA on algal growth response varied by species, but the direction was consistent within functional groups. Exposure to OA conditions generally enhanced growth in fleshy macroalgae, reduced net calcification in upright calcareous algae, and caused net dissolution in CCA. Additionally, three of the five fleshy seaweeds tested became reproductive upon exposure to OA conditions. There was no consistent effect of OA on algal photophysiology. Our study provides experimental evidence to support the hypothesis that OA will reduce the ability of calcareous algae to biomineralize. Further, we show that CO2 enrichment either will stimulate population or somatic growth in some species of fleshy macroalgae. Thus, our results suggest that projected OA conditions may favor non-calcifying algae and influence the relative dominance of fleshy macroalgae on reefs, perpetuating or exacerbating existing shifts in reef community structure.