Ocean acidification induces multi-generational decline in copepod naupliar production with possible conflict for reproductive resource allocation

Climate change, including ocean acidification (OA), presents fundamental challenges to marine biodiversity and sustained ecosystem health. We determined reproductive response (measured as naupliar production), cuticle composition and stage specific growth of the copepod Tisbe battagliai over three generations at four pH conditions (pH 7.67, 7.82, 7.95, and 8.06). Naupliar production increased significantly at pH 7.95 compared with pH 8.06 followed by a decline at pH 7.82. Naupliar production at pH 7.67 was higher than pH 7.82. We attribute the increase at pH 7.95 to an initial stress response which was succeeded by a hormesis-like response at pH 7.67. A multi-generational modelling approach predicted a gradual decline in naupliar production over the next 100 years (equivalent to approximately 2430 generations). There was a significant growth reduction (mean length integrated across developmental stage) relative to controls. There was a significant increase in the proportion of carbon relative to oxygen within the cuticle as seawater pH decreased. Changes in growth, cuticle composition and naupliar production strongly suggest that copepods subjected to OA-induced stress preferentially reallocate resources towards maintaining reproductive output at the expense of somatic growth and cuticle composition. These responses may drive shifts in life history strategies that favour smaller brood sizes, females and perhaps later maturing females, with the potential to profoundly destabilise marine trophodynamics.

Seawater carbonate chemistry and calcification rate of cold-water coral Lophelia pertusa during experiments, 2011

Ocean acidity has increased by 30% since preindustrial times due to the uptake of anthropogenic CO2 and is projected to rise by another 120% before 2100 if CO2 emissions continue at current rates. Ocean acidification is expected to have wide-ranging impacts on marine life, including reduced growth and net erosion of coral reefs. Our present understanding of the impacts of ocean acidification on marine life, however, relies heavily on results from short-term CO2 perturbation studies. Here we present results from the first long-term CO2 perturbation study on the dominant reef-building cold-water coral Lophelia pertusa and relate them to results from a short-term study to compare the effect of exposure time on the coral's responses. Short-term (one week) high CO2 exposure resulted in a decline of calcification by 26-29% for a pH decrease of 0.1 units and net dissolution of calcium carbonate. In contrast, L. pertusa was capable to acclimate to acidified conditions in long-term (six months) incubations, leading to even slightly enhanced rates of calcification. Net growth is sustained even in waters sub-saturated with respect to aragonite. Acclimation to seawater acidification did not cause a measurable increase in metabolic rates. This is the first evidence of successful acclimation in a coral species to ocean acidification, emphasizing the general need for long-term incubations in ocean acidification research. To conclude on the sensitivity of cold-water coral reefs to future ocean acidification further ecophysiological studies are necessary which should also encompass the role of food availability and rising temperatures.

Seawater carbonate chemistry and processes during experiments with amphipod Gammarus locusta, 2009

We report an investigation of the effects of increases in pCO2 on the survival, growth and molecular physiology of the neritic amphipod Gammarus locusta which has a cosmopolitan distribution in estuaries. Amphipods were reared from juvenile to mature adult in laboratory microcosms at three different levels of pH in nominal range 8.1-7.6. Growth rate was estimated from weekly measures of body length. At sexual maturity the amphipods were sacrificed and assayed for changes in the expression of genes coding for a heat shock protein (hsp70 gene) and the metabolic enzyme glyceraldehyde-3-phosphate dehydrogenase (gapdh gene). The data show that the growth and survival of this species is not significantly impacted by a decrease in sea water pH of up to 0.5 units. Quantitative real-time PCR analysis indicated that there was no significant effect of growth in acidified sea water on the sustained expression of the hsp70 gene. There was a consistent and significant increase in the expression of the gapdh gene at a pH of ~7.5 which, when combined with observations from other workers, suggests that metabolic changes may occur in response to acidification. It is concluded that sensitive assays of tissue physiology and molecular biology should be routinely employed in future studies of the impacts of sea water acidification as subtle effects on the physiology and metabolism of coastal marine species may be overlooked in conventional gross "end-point" studies of organism growth or mortality.

The responses of eight coral reef calcifiers to increasing partial pressure of CO2 do not exhibit a tipping point

The objective of this study was to investigate whether a tipping point exists in the calcification responses of coral reef calcifiers to CO2. We compared the effects of six partial pressures of CO2 (PCO2) from 28 Pa to 210 Pa on the net calcification of four corals (Acropora pulchra, Porites rus, Pocillopora damicornis, and Pavona cactus), and four calcified algae (Hydrolithon onkodes, Lithophyllum flavescens, Halimeda macroloba, and Halimeda minima). After 2 weeks of acclimation in a common environment, organisms were incubated in 12 aquaria for 2 weeks at the targeted PCO2 levels and net calcification was quantified. All eight species calcified at the highest PCO2 in which the calcium carbonate aragonite saturation state was ~1. Calcification decreased linearly as a function of increasing partial PCO2 in three corals and three algae. Overall, the decrease in net calcification as a function of decreasing pH was ~10% when ambient PCO2 (39 Pa) was doubled. The calcification responses of P. damicornis and H. macroloba were unaffected by increasing PCO2. These results are inconsistent with the notion that coral reefs will be affected by rising PCO2 in a response characterized by a tipping point. Instead, our findings combined among taxa suggest a gradual decline in calcification will occur, but this general response includes specific cases of complete resistance to rising PCO2. Together our results suggest that the overall response of coral reef communities to ocean acidification will be monotonic and inversely proportional to PCO2, with reef-wide responses dependent on the species composition of calcifying taxa.

Seawater carbonate chemistry and MgCO3 concentration in bryozoan Myriapora truncata branches during experiments, 2011

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.

Acclimatization of the crustose coralline alga Porolithon onkodes to variable pCO2

Ocean acidification (OA) has important implications for the persistence of coral reef ecosystems, due to potentially negative effects on biomineralization. Many coral reefs are dynamic with respect to carbonate chemistry, and experience fluctuations in pCO2 that exceed OA projections for the near future. To understand the influence of dynamic pCO2 on an important reef calcifier, we tested the response of the crustose coralline alga Porolithon onkodes to oscillating pCO2. Individuals were exposed to ambient (400 µatm), high (660 µatm), or variable pCO2 (oscillating between 400/660 µatm) treatments for 14 days. To explore the potential for coralline acclimatization, we collected individuals from low and high pCO2 variability sites (upstream and downstream respectively) on a back reef characterized by unidirectional water flow in Moorea, French Polynesia. We quantified the effects of treatment on algal calcification by measuring the change in buoyant weight, and on algal metabolism by conducting sealed incubations to measure rates of photosynthesis and respiration. Net photosynthesis was higher in the ambient treatment than the variable treatment, regardless of habitat origin, and there was no effect on respiration or gross photosynthesis. Exposure to high pCO2 decreased P. onkodes calcification by >70%, regardless of the original habitat. In the variable treatment, corallines from the high variability habitat calcified 42% more than corallines from the low variability habitat. The significance of the original habitat for the coralline calcification response to variable, high pCO2 indicates that individuals existing in dynamic pCO2 habitats may be acclimatized to OA within the scope of in situ variability. These results highlight the importance of accounting for natural pCO2 variability in OA manipulations, and provide insight into the potential for plasticity in habitat and species-specific responses to changing ocean chemistry.

Trace element profiles of the sea anemone Anemonia viridis living nearby a natural CO2 vent

Ocean acidification (OA) is not an isolated threat, but acts in concert with other impacts on ecosystems and species. Coastal marine invertebrates will have to face the synergistic interactions of OA with other global and local stressors. One local factor, common in coastal environments, is trace element contamination. CO2 vent sites are extensively studied in the context of OA and are often considered analogous to the oceans in the next few decades. The CO2 vent found at Levante Bay (Vulcano, NE Sicily, Italy) also releases high concentrations of trace elements to its surrounding seawater, and is therefore a unique site to examine the effects of long-term exposure of nearby organisms to high pCO2 and trace element enrichment in situ. The sea anemone Anemonia viridis is prevalent next to the Vulcano vent and does not show signs of trace element poisoning/stress. The aim of our study was to compare A. viridis trace element profiles and compartmentalization between high pCO2 and control environments. Rather than examining whole anemone tissue, we analyzed two different body compartments-the pedal disc and the tentacles, and also examined the distribution of trace elements in the tentacles between the animal and the symbiotic algae. We found dramatic changes in trace element tissue concentrations between the high pCO2/high trace element and control sites, with strong accumulation of iron, lead, copper and cobalt, but decreased concentrations of cadmium, zinc and arsenic proximate to the vent. The pedal disc contained substantially more trace elements than the anemone's tentacles, suggesting the pedal disc may serve as a detoxification/storage site for excess trace elements. Within the tentacles, the various trace elements displayed different partitioning patterns between animal tissue and algal symbionts. At both sites iron was found primarily in the algae, whereas cadmium, zinc and arsenic were primarily found in the animal tissue. Our data suggests that A. viridis regulates its internal trace element concentrations by compartmentalization and excretion and that these features contribute to its resilience and potential success at the trace element-rich high pCO2 vent.

Sensitivity to ocean acidification parallels natural pCO2 gradients experienced by Arctic copepods under winter sea ice

The Arctic Ocean is a bellwether for ocean acidification, yet few direct Arctic studies have been carried out and limited observations exist, especially in winter. We present unique under-ice physicochemical data showing the persistence of a mid water column area of high CO2 and low pH through late winter, Zooplankton data demonstrating that the dominant copepod species are distributed across these different physicochemical conditions, and empirical data demonstrating that these copepods show sensitivity to pCO2 that parallels the range of natural pCO2 they experience through their daily vertical migration behavior. Our data, collected as part of the Catlin Arctic Survey, provide unique insight into the link between environmental variability, behavior, and an organism's physiological tolerance to CO2 in key Arctic biota.

Hysteresis between coral reef calcification and the seawater aragonite saturation state

Some predictions of how ocean acidification (OA) will affect coral reefs assume a linear functional relationship between the ambient seawater aragonite saturation state (Omega a) and net ecosystem calcification (NEC). We quantified NEC in a healthy coral reef lagoon in the Great Barrier Reef during different times of the day. Our observations revealed a diel hysteresis pattern in the NEC versus Omega a relationship, with peak NEC rates occurring before the Omega a peak and relatively steady nighttime NEC in spite of variable Omega a. Net ecosystem production had stronger correlations with NEC than light, temperature, nutrients, pH, and Omega a. The observed hysteresis may represent an overlooked challenge for predicting the effects of OA on coral reefs. If widespread, the hysteresis could prevent the use of a linear extrapolation to determine critical Omega a threshold levels required to shift coral reefs from a net calcifying to a net dissolving state.

Seawater carbonate chemistry and coverage and dry weight of Ecklonia radiata during experiments, 2010

Predictions about the ecological consequences of oceanic uptake of CO2 have been preoccupied with the effects of ocean acidification on calcifying organisms, particularly those critical to the formation of habitats (e.g. coral reefs) or their maintenance (e.g. grazing echinoderms). This focus overlooks the direct effects of CO2 on non-calcareous taxa, particularly those that play critical roles in ecosystem shifts. We used two experiments to investigate whether increased CO2 could exacerbate kelp loss by facilitating non-calcareous algae that, we hypothesized, (i) inhibit the recovery of kelp forests on an urbanized coast, and (ii) form more extensive covers and greater biomass under moderate future CO2 and associated temperature increases. Our experimental removal of turfs from a phase-shifted system (i.e. kelp- to turf-dominated) revealed that the number of kelp recruits increased, thereby indicating that turfs can inhibit kelp recruitment. Future CO2 and temperature interacted synergistically to have a positive effect on the abundance of algal turfs, whereby they had twice the biomass and occupied over four times more available space than under current conditions. We suggest that the current preoccupation with the negative effects of ocean acidification on marine calcifiers overlooks potentially profound effects of increasing CO2 and temperature on non-calcifying organisms.

Seawater carbonate chemistry and length, weight, survival rate, metabolic rate of coral reef fish Amphiprion melanopus in a laboratory experiment

Carbon dioxide concentrations in the surface ocean are increasing owing to rising CO2 concentrations in the atmosphere. Higher CO2 levels are predicted to affect essential physiological processes of many aquatic organisms, leading to widespread impacts on marine diversity and ecosystem function, especially when combined with the effects of global warming. Yet the ability for marine species to adjust to increasing CO2 levels over many generations is an unresolved issue. Here we show that ocean conditions projected for the end of the century (approximately 1,000 µatm CO2 and a temperature rise of 1.5-3.0 °C) cause an increase in metabolic rate and decreases in length, weight, condition and survival of juvenile fish. However, these effects are absent or reversed when parents also experience high CO2 concentrations. Our results show that non-genetic parental effects can dramatically alter the response of marine organisms to increasing CO2 and demonstrate that some species have more capacity to acclimate to ocean acidification than previously thought.

Seawater carbonate chemistry and biological parameters during experiments with white sea bass Atractoscion nobilis, 2009

A large fraction of the carbon dioxide added to the atmosphere by human activity enters the sea, causing ocean acidification. We show that otoliths (aragonite ear bones) of young fish grown under high CO2 (low pH) conditions are larger than normal, contrary to expectation. We hypothesize that CO2 moves freely through the epithelium around the otoliths in young fish, accelerating otolith growth while the local pH is controlled. This is the converse of the effect commonly reported for structural biominerals.

Adverse effects of ocean acidification on early development of squid (Doryteuthis pealeii)

Anthropogenic carbon dioxide (CO2) is being absorbed into the ocean, altering seawater chemistry, with potentially negative impacts on a wide range of marine organisms. The early life stages of invertebrates with internal and external aragonite structures may be particularly vulnerable to this ocean acidification. Impacts to cephalopods, which form aragonite cuttlebones and statoliths, are of concern because of the central role they play in many ocean ecosystems and because of their importance to global fisheries. Atlantic longfin squid (Doryteuthis pealeii), an ecologically and economically valuable taxon, were reared from eggs to hatchlings (paralarvae) under ambient and elevated CO2 concentrations in replicated experimental trials. Animals raised under elevated pCO2 demonstrated significant developmental changes including increased time to hatching and shorter mantle lengths, although differences were small. Aragonite statoliths, critical for balance and detecting movement, had significantly reduced surface area and were abnormally shaped with increased porosity and altered crystal structure in elevated pCO2-reared paralarvae. These developmental and physiological effects could alter squid paralarvae behavior and survival in the wild, directly and indirectly impacting marine food webs and commercial fisheries.