Growth of cultured giant clams (Tridacna spp.) in low pH, high-nutrient seawater: species-specific effects of substrate and supplemental feeding under acidification

Four species of giant clams, Tridacna maxima, T. squamosa, T. derasa and T. crocea, were cultured in outdoor raceways for 364 days at the Waikīkī Aquarium and the Oceanic Institute on the island of O‘ahu, Hawai‘i, USA.  Growth of each species was compared among individuals grown with and without supplemental phytoplankton feeding, and directly on the substrate or mounted on concrete plugs in low pH, high nutrient seawater.  Among clams cultured with and without supplemental phytoplankton (Chaetoceros spp.), feeding resulted in significantly lower mortality in all species but T. deresa, whereas growth was significantly higher among fed clams for all species except T. squamosa. Tridacna derasa showed roughly a three-fold increase in growth when fed (88.5 g ± 4.4 SD) than when unfed (26.0 g ± 2.1 SD), whereas T. maxima growth was substantially lower, but nearly 10-fold greater in response to feeding (9.0 g ± 1.9 SD). The overall mortality rate of juvenile clams was significantly lower in the fed (44.4 ± 10.0%) than the unfed (71.8 ± 9.6%) trials, with the greatest effect observed in mortality of T. maxima (fed 15% versus unfed 80%) and T. squamosa (fed 65% versus unfed 95%). None of the T. squamosa remained on concrete plugs for the duration of the experiment. Among the remaining three species, there was no difference in either wet weight or shell length for T. maxima and for wet weight only in T. derasa on (186.5 g ± 16.1 SD) and off (147.0 g ± 6.0 SD) the concrete plugs.  In contrast, T. crocea had significantly greater shell growth off the plugs (14.3 mm ± 1.0 SD versus 8.5 mm ± 1.7 SD) but significantly greater gain in wet weight on the concrete plugs (26.3 g ± 1.5 SD versus 58.5 g ± 2.5 SD).  The seawater wells used for this study are well characterized with elevated levels of inorganic nutrients and higher pCO2 relative to tropical ocean waters, roughly approximating predictions for future oceanic conditions under IPCC IS92a emission scenarios. In comparison to previous studies in natural seawater, T. derasa had a significantly higher shell growth rate in the high-nutrient, low-pH well water.  In contrast, T. maxima and T. squamosa had significantly lower growth rates in low pH, whereas growth of T. crocea was not significantly different between low pH and ambient seawater.  These experiments demonstrate species-specific differences with each treatment, which cautions against making broad generalizations regarding the effects of substrate type, feeding effects, nutrient enrichment, and ocean acidification on tridacnid culture and survival.

Interactive effects of ocean acidification and temperature on two scleractinian corals from Moorea, French Polynesia

This study tested the hypothesis that the response of corals to temperature and pCO2 is consistent between taxa. Juvenile massive Porites spp. and branches of P. rus from the back reef of Moorea were incubated for 1 month under combinations of temperature (29.3 °C and 25.6 °C) and pCO2 (41.6 Pa and 81.5 Pa) at an irradiance of 599 μmol quanta m−2 s−1. Using microcosms and CO2 gas mixing technology, treatments were created in a partly nested design (tanks) with two between-plot factors (temperature and pCO2), and one within-plot factor (taxon); calcification was used as a dependent variable. pCO2 and temperature independently affected calcification, but the response differed between taxa. Massive Porites spp. was largely unaffected by the treatments, but P. rus grew 50% faster at 29.3 °C compared with 25.6 °C, and 28% slower at 81.5 Pa vs. 41.6 Pa CO2. A compilation of studies placed the present results in a broader context and tested the hypothesis that calcification for individual coral genera is independent of pH, [HCO3−], and [CO32−]. Unlike recent reviews, this analysis was restricted to studies reporting calcification in units that could be converted to nmol CaCO3 cm−2 h−1. The compilation revealed a high degree of variation in calcification as a function of pH, [HCO3−], and [CO32−], and supported three conclusions: (1) studies of the effects of ocean acidification on corals need to pay closer attention to reducing variance in experimental outcomes to achieve stronger synthetic capacity, (2) coral genera respond in dissimilar ways to pH, [HCO3−], and [CO32−], and (3) calcification of massive Porites spp. is relatively resistant to short exposures of increased pCO2, similar to that expected within 100 y.

Forecasted CO2 modifies the influence of light in shaping subtidal habitat

Some abiotic conditions are well known to play disproportionately large roles in shaping contemporary assemblages, yet their roles may not continue to have similar magnitudes of effect into the future. We tested whether forecasted levels of CO2 could alter the strength of influence of an abiotic factor (i.e., light intensity) well known for its strength of influence on the subtidal ecology of photosynthetic organisms. We investigated these dynamics in two subtidal algal species that form contrasting associations with kelp forests, one negatively associated with kelp canopies (turf-forming brown algae, Feldmannia spp.) and the other positively associated with kelp as understory (calcifying red crustose algae, Lithophyllum sp.). Using an experimental approach, we assessed the independent and combined effects of [CO2] (control and elevated) and light (shade, low ultraviolet B [UVB], full light) on growth, recruitment, and relative electron transport rate (rETR). Under control [CO2], the effects of light corresponded to the relative light environments of the two groups of algae. The influence of light on the percentage cover and biomass of understory crusts was substantially reduced under elevated [CO2], which caused crusts to grow less. While elevated [CO2] had the opposite effect of positively influencing turf cover and biomass, it had the same effect of reducing the structuring effects of light and UVB. Hence, if we are to predict the ecological consequences of future CO2 conditions, the role of contemporary processes cannot be assumed to produce similar effects relative to other processes, which will change with a changing climate.

Warmer more acidic conditions cause decreased productivity and calcification in subtropical coral reef sediment-dwelling calcifiers

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.

CO2 maximum in the oxygen minimum zone (OMZ)

Oxygen minimum zones (OMZs), known as suboxic layers which are mainly localized in the Eastern Boundary Upwelling Systems, have been expanding since the 20th “high CO2″ century, probably due to global warming. OMZs are also known to significantly contribute to the oceanic production of N2O, a greenhouse gas (GHG) more efficient than CO2. However, the contribution of the OMZs on the oceanic sources and sinks budget of CO2, the main GHG, still remains to be established.

We present here the dissolved inorganic carbon (DIC) structure, associated locally with the Chilean OMZ and globally with the main most intense OMZs (O2<20 μmol kg−1) in the open ocean. To achieve this, we examine simultaneous DIC and O2 data collected off Chile during 4 cruises (2000–2002) and a monthly monitoring (2000–2001) in one of the shallowest OMZs, along with international DIC and O2 databases and climatology for other OMZs.

High DIC concentrations (>2225 μmol kg−1, up to 2350 μmol kg−1) have been reported over the whole OMZ thickness, allowing the definition for all studied OMZs a Carbon Maximum Zone (CMZ). Locally off Chile, the shallow cores of the OMZ and CMZ are spatially and temporally collocated at 21° S, 30° S and 36° S despite different cross-shore, long-shore and seasonal configurations. Globally, the mean state of the main OMZs also corresponds to the largest carbon reserves of the ocean in subsurface waters. The CMZs-OMZs could then induce a positive feedback for the atmosphere during upwelling activity, as potential direct local sources of CO2. The CMZ paradoxically presents a slight “carbon deficit” in its core (~10%), meaning a DIC increase from the oxygenated ocean to the OMZ lower than the corresponding O2 decrease (assuming classical C/O molar ratios). This “carbon deficit” would be related to regional thermal mechanisms affecting faster O2 than DIC (due to the carbonate buffer effect) and occurring upstream in warm waters (e.g., in the Equatorial Divergence), where the CMZ-OMZ core originates. The “carbon deficit” in the CMZ core would be mainly compensated locally at the oxycline, by a “carbon excess” induced by a specific remineralization. Indeed, a possible co-existence of bacterial heterotrophic and autotrophic processes usually occurring at different depths could stimulate an intense aerobic-anaerobic remineralization, inducing the deviation of C/O molar ratios from the canonical Redfield ratios. Further studies to confirm these results for all OMZs are required to understand the OMZ effects on both climatic feedback mechanisms and marine ecosystem perturbations.

Unshelled abalone and corrupted urchins: development of marine calcifiers in a changing ocean

The most fragile skeletons produced by benthic marine calcifiers are those that larvae and juveniles make to support their bodies. Ocean warming, acidification, decreased carbonate saturation and their interactive effects are likely to impair skeletogenesis. Failure to produce skeleton in a changing ocean has negative implications for a diversity of marine species. We examined the interactive effects of warming and acidification on an abalone (Haliotis coccoradiata) and a sea urchin (Heliocidaris erythrogramma) reared from fertilization in temperature and pH/pCO2 treatments in a climatically and regionally relevant setting. Exposure of ectodermal (abalone) and mesodermal (echinoid) calcifying systems to warming (+2°C to 4°C) and acidification (pH 7.6–7.8) resulted in unshelled larvae and abnormal juveniles. Haliotis development was most sensitive with no interaction between stressors. For Heliocidaris, the percentage of normal juveniles decreased in response to both stressors, although a +2°C warming diminished the negative effect of low pH. The number of spines produced decreased with increasing acidification/pCO2, and the interactive effect between stressors indicated that a +2°C warming reduced the negative effects of low pH. At +4°C, the developmental thermal tolerance was breached. Our results show that projected near-future climate change will have deleterious effects on development with differences in vulnerability in the two species.

Deep-water carbonate concentrations in the southwest Pacific

We have compiled carbonate chemistry and sedimentary CaCO₃% data for the deep-waters (>1500 m water depth) of the southwest (SW) Pacific region. The complex topography in the SW Pacific influences the deep-water circulation and affects the carbonate ion concentration ([CO₃^2-]), and the associated calcite saturation horizon (CSH where Ωcalcite =1). The Tasman Basin and the southeast (SE) New Zealand region have the deepest CSH at ~3100 m, primarily influenced by middle and lower Circumpolar Deep Waters (m or lCPDW), while to the northeast of New Zealand the CSH is ~2800 m, due to the corrosive influence of the old North Pacific deep waters (NPDW) on the upper CPDW (uCPDW). The carbonate compensation depth (CCD; defined by a sedimentary CaCO₃ content of <20%), also varies between the basins in the SW Pacific. The CCD is ~4600 m to the SE New Zealand, but only ~4000 m to the NE New Zealand. The CaCO₃ content of the sediment, however, can be influenced by a number of different factors other than dissolution, therefore we suggest using the water chemistry to estimate the CCD. The depth difference between the CSH and CCD (ΔZ_CSH-CCD), however, varies considerably in this region and globally. The global ΔZ_CSH-CCD appears to expand with increasing age of the deep-water, resulting from a shoaling of the CSH. In contrast the depth of the chemical lysocline (Ωcalcite = 0.8) is less variable globally and is relatively similar, or close, to the CCD determined from the sedimentary CaCO₃%. Geochemical definitions of the CCD, however, cannot be used to determine changes in the paleo-CCD. Given the range of factors that influence the sedimentary CaCO₃%, an independent dissolution proxy, such as the foraminifera fragmentation % (>40% = foraminiferal lysocline) is required to define a depth where significant CaCO₃ dissolution has occurred back through time. The current foraminiferal lysocline for the SW Pacific region ranges from 3100-3500 m, which is predictably just slightly deeper than the CSH. This compilation of sediment and water chemistry data provide a CaCO₃ dataset for the present SW Pacific for comparison with glacial/interglacial CaCO₃ variations in deep-water sediment cores, and to monitor future changes in [CO₃^2-] and dissolution of sedimentary CaCO₃ resulting from increasing anthropogenic CO₂.

High CO2 enhances the competitive strength of seaweeds over corals

Space competition between corals and seaweeds is an important ecological process underlying coral-reef dynamics. Processes promoting seaweed growth and survival, such as herbivore overfishing and eutrophication, can lead to local reef degradation. Here, we present the case that increasing concentrations of atmospheric CO2 may be an additional process driving a shift from corals to seaweeds on reefs. Coral (Acropora intermedia) mortality in contact with a common coral-reef seaweed (Lobophora papenfussii) increased two- to threefold between background CO2 (400 ppm) and highest level projected for late 21st century (1140 ppm). The strong interaction between CO2 and seaweeds on coral mortality was most likely attributable to a chemical competitive mechanism, as control corals with algal mimics showed no mortality. Our results suggest that coral (Acropora) reefs may become increasingly susceptible to seaweed proliferation under ocean acidification, and processes regulating algal abundance (e.g. herbivory) will play an increasingly important role in maintaining coral abundance.

The basics of acidification: baseline variability of pH on Australian coral reefs

Ocean acidification is one of the key threats facing coral reef ecosystems, but there are few estimates of spatial and temporal variability in pH among reef habitats. The present study documents levels of spatial variability in pH among coral reef habitats (9 to 10), among locations separated by 100’s km of latitude and between east (Great Barrier Reef, GBR) and west (Ningaloo Reef) coasts of Australia. Differences were found in pH between inshore and offshore waters along Ningaloo Reef (means 8.45, 8.53, respectively). Replicate assessments here ranged from 8.22 to 8.64. On the GBR, the range of values over all habitats and replicates was 0.39 pH units (7.98 to 8.37). There were minor but significant differences of 0.05 pH units between 5 consecutive days for habitats on average. Highest pH was recorded in filamentous algal beds maintained by the damselfish Dischistodus perspicillatus. Lowest pH was found in water extracted from sand-dwelling goby holes. While there were marked changes in pH over a 48-h sampling period among 4 habitats at Lizard Island (GBR), there was little evidence of a diel trend. Understanding how pH varies at scales that are relevant to organisms that live on shallow coral reefs is crucial for the design and interpretation of experiments that test the effects on organisms of the changes in water chemistry predicted to affect oceans in the future.

Evidence for Ocean Acidification in the Great Barrier Reef of Australia

Geochemical records preserved in the long-lived carbonate skeleton of corals provide one of the few means to reconstruct changes in seawater pH since the commencement of the industrial era. This information is important in not only determining the response of the surface oceans to ocean acidification from enhanced uptake of CO2, but also to better understand the effects of ocean acidification on carbonate secreting organisms such as corals, whose ability to calcify is highly pH dependent. Here we report an ~200 year 11B isotopic record, extracted from a long-lived Porites coral from the central Great Barrier Reef of Australia. This record covering the period from 1800 to 2004 was sampled at yearly increments from 1940 to the present and 5-year increments prior to 1940. The 11B isotopic compositions reflect variations in seawater pH, and the 13C changes in the carbon composition of surface water due to fossil fuel burning over this period. In addition complementary Ba/Ca, 18O and Mg/Ca data was obtained providing proxies for terrestrial runoff, salinity and temperature changes over the past 200 years in this region. Positive thermal ionization mass spectrometry (PTIMS) method was utilized in order to enable the highest precision and most accurate measurements of 11B values. The internal precision and reproducibility for 11B of our measurements are better than ±0.2‰ (2), which translates to a precision of better than ±0.02 pH units. Our results indicate that the long-term pre-industrial variation of seawater pH in this region is partially related to the decadal-interdecadal variability of atmospheric and oceanic anomalies in the Pacific. In the periods around 1940 and 1998 there are also rapid oscillations in 11B compositions equivalent changes in pH of almost 0.5 units. The 1998 oscillation is co-incident with a major coral bleaching event indicating the sensitivity of skeletal 11 B compositions to loss of zooxanthellate symbionts. Importantly, from the 1940’s to the present-day, there is a general overall trend of ocean acidification with pH decreasing by about 0.2 to 0.3 units, the range being dependent on the value assumed for the fractionation factor α(B3-B4) of the boric acid and borate species in seawater. Correlations of 11B with 13C during this interval indicate that the increasing trend towards ocean acidification over the past 60 years in this region is the result of enhanced dissolution of CO2 in surface waters from the rapidly increasing levels of atmospheric CO2, mainly from fossil fuel burning. This suggests that the increased levels of anthropogenic CO2 in atmosphere has already caused a significant trend towards acidification in the oceans during the past decades. Observations of surprisingly large decreases in pH across important carbonate producing regions, such as the Great Barrier Reef of Australia, raise serious concerns about the impact of Greenhouse gas emissions on coral calcification.