Effects of sub-lethal CO2(aq) concentrations on the performance of intensively reared gilthead seabream (Sparus aurata) in brackish water: flow-through experiments and full-scale RAS results

The effects sub-lethal CO_2(aq) concentrations were tested for the first time on gilthead seabream (Sparus aurata) juveniles (4 to 25 g; 64 growth days) and adult (∼300-400 g; 71 days) fish, both in fully controlled pilot tests and the latter also as part of full-scale RAS (recirculating aquaculture system) operation. In the pilot experiments (concentration range 5.2 to 56.3 mgCO₂/L) the specific growth rate, mortality rate, and physical fish disorders were monitored. In the full scale experiment, two groups of fish, originally from the same batch, were exposed for 197 days to controlled (by NaOH dosage) and uncontrolled pH conditions, resulting in exposure of the fish to significantly different CO_2(aq) concentrations. The pilot results showed, as expected, that the seabream fish grew faster at the lower CO₂ concentrations and that the growth rate of both juveniles and adult fish was only minimally inhibited up to roughly 20 mg CO₂/L (compared to a previously published curve). Mortality rate was considerable only at the highest CO₂ concentration (∼56 mgCO₂/L). Physical irregularities were not observed, apart from abnormally-high absence of swim bladder at the highest CO_2(aq) treatment. The (statistically significant) results from the full-scale RAS operation showed that growing gilthead seabream for 197 days at roughly constant and relatively low (∼16 mg/L) CO_2(aq) concentration resulted in fish with ∼10% larger mean weight relative to the fish grown in ponds in which CO_2(aq) was not controlled and its concentration fluctuated daily between 19 and 37 mg/L.

High CO2 reduces the settlement of a spawning coral on three common species of crustose coralline algae

Concern about the impacts of ocean acidification (OA) on ecosystem function has prompted many studies to focus on larval recruitment, demonstrating declines in settlement and early growth at elevated CO₂ concentrations. Since larval settlement is often driven by particular cues governed by crustose coralline algae (CCA), it is important to determine whether OA reduces larval recruitment with specific CCA and the generality of any effects. We tested the effect of elevated CO₂ on the survival and settlement of larvae from the common spawning coral Acropora selago with 3 ecologically important species of CCA, Porolithon onkodes, Sporolithon sp., and Titanoderma sp. After 3 d in no-choice laboratory assays at 447, 705, and 1214 µatm pCO₂, the rates of coral settlement declined as pCO₂ increased with all CCA taxa. The magnitude of the effect was highest with Titanoderma sp., decreasing by 87% from the ambient to highest CO₂ treatment. In general, there were high rates of larval mortality, which were greater with the P. onkodes and Sporolithon sp. treatments (~80%) compared to the Titanoderma sp. treatment (65%). There was an increase in larval mortality as pCO₂ increased, but this was variable among the CCA species. It appears that OA reduces coral settlement by rapidly altering the chemical cues associated with the CCA thalli and microbial community, and potentially by directly affecting larval viability.

Complex responses of intertidal molluscan embryos to a warming and acidifying ocean in the presence of UV radiation

Climate change and ocean acidification will expose marine organisms to synchronous multiple stressors, with early life stages being potentially most vulnerable to changing environmental conditions. We simultaneously exposed encapsulated molluscan embryos to three abiotic stressors—acidified conditions, elevated temperate, and solar UV radiation in large outdoor water tables in a multifactorial design. Solar UV radiation was modified with plastic filters, while levels of the other factors reflected IPCC predictions for near-future change. We quantified mortality and the rate of embryonic development for a mid-shore littorinid, Bembicium nanum, and low-shore opisthobranch, Dolabrifera brazieri. Outcomes were consistent for these model species with embryos faring significantly better at 26°C than 22°C. Mortality sharply increased at the lowest temperature (22°C) and lowest pH (7.6) examined, producing a significant interaction. Under these conditions mortality approached 100% for each species, representing a 2- to 4-fold increase in mortality relative to warm (26°C) non-acidified conditions. Predictably, development was more rapid at the highest temperature but this again interacted with acidified conditions. Development was slowed under acidified conditions at the lowest temperature. The presence of UV radiation had minimal impact on the outcomes, only slowing development for the littorinid and not interacting with the other factors. Our findings suggest that a warming ocean, at least to a threshold, may compensate for the effects of decreasing pH for some species. It also appears that stressors will interact in complex and unpredictable ways in a changing climate.

CO2-induced ocean acidification impairs calcification in the tropical urchin Echinometra viridis

Atmospheric carbon dioxide (pCO₂) has risen from approximately 280 to 400 ppm since the Industrial Revolution, due mainly to the combustion of fossil fuels, deforestation, and cement production. It is predicted to reach as high as 900 ppm by the end of this century. Ocean acidification resulting from the release of anthropogenic CO₂ has been shown to impair the ability of some marine calcifiers to build their shells and skeletons. Here, we present the results of ocean acidification experiments designed to assess the effects of an increase in atmospheric pCO₂ from ca. 448 to 827 ppm on calcification rates of the tropical urchin Echinometra viridis. Experiments were conducted under the urchin’s winter (20 °C) and summer (30 °C) water temperatures in order to identify seasonal differences in the urchin’s response to ocean acidification. The experiments reveal that calcification rates decreased for urchins reared under elevated pCO₂, with the decline being more pronounced under wintertime temperatures than under summertime temperatures. These results indicate that the urchin E. viridis will be negatively impacted by CO₂-induced ocean acidification that is predicted to occur by the end of this century. These results also suggest that impact of CO₂-induced ocean acidification on urchin calcification will be more severe in the winter and in cooler waters.

Effects of ocean warming and acidification on embryos and non-calcifying larvae of the invasive sea star Patiriella regularis

Little is known about the effects of potential synergies between concurrent ocean warming and acidification on marine benthos. We investigated the effects of warming and acidification on development to the non-calcifying larval stage in the sea star Patiriella regularis, in embryos reared from fertilization in present and future (2100+) conditions. Fertilization using gametes from multiple parents, to represent populations of spawners, was resilient to both stressors, as were cleavage stage embryos. Warming increased developmental rate across all pH levels. For blastulae, there was a complex interaction between stressors, with +4°C/pH 7.6 lethal to many embryos. A 4°C warming increased mortality by the gastrulation stage by 13 to 25% across all pH levels. In conjunction with warming, pH 7.6 increased mortality by 25 to 27% across all temperatures. For embryos that reached the 3 d bipinnaria stage, warming reduced the percentage of normal larvae and larval size, with no effect of acidification. These results highlight the importance of considering both warming and acidification, and effects on early embryos, in assessing life history responses to ocean change. Bipinnaria reared to Day 28 to determine the effects of acidification on non-calcifying feeding larvae provided a comparison with results for calcifying echinoplutei. pH 7.6 resulted in smaller larvae and increased mortality by 30%. After 24 d, near-future ocean acidification levels (pH 7.8) also resulted in smaller larvae. The effects of acidification in reducing growth in larvae that do not calcify indicates that the stunting response of echinoderm feeding larvae to pH/pCO₂ is strongly influenced by hypercapnic changes in metabolism and teratogenic effects. The results have implications for P. regularis in its invasive range in Australia, where this species is likely to be deleteriously affected by ocean warming.

Tolerance of juvenile barnacles (Amphibalanus improvisus) to warming and elevated pCO2

We investigated the impacts of warming and elevated pCO₂ on newly settled Amphibalanus improvisus from Kiel Fjord, an estuarine ecosystem characterized by significant natural pCO₂ variability. In two experiments, juvenile barnacles were maintained at two temperature and three pCO₂ levels (20/24 °C, 700–2,140 μatm) for 8 weeks in a batch culture and at four pCO₂ levels (20 °C, 620–2,870 μatm) for 12 weeks in a water flow-through system. Warming as well as elevated pCO₂ hardly affected growth or the condition index of barnacles, although some factor combinations led to temporal significances in enhanced or reduced growth with an increase in pCO₂. While warming increased the shell strength of A. improvisus individuals, elevated pCO₂ had only weak effects. We demonstrate a strong tolerance of juvenile A. improvisus to mean acidification levels of about 1,000 μatm pCO₂ as is already naturally experienced by the investigated barnacle population.

Disturbance effects to coral recruitment dynamics on the Great Barrier Reef

Coral recruitment represents a critical phase in the development of coral populations, important to the recovery of coral reefs affected by anthropogenic and natural disturbances. Successful recruitment is significant to the resilience of coral reefs, and degraded reefs often exhibit declining rates of coral recruitment through a poorly understood combination of reduced adult fecundity, decreased settlement, increased competition for space, and high rates of early mortality. The stages of successful recruitment are complex and, whilst evidence indicates that climate change disturbances can adversely reduce coral recruitment, empirical investigations into ecological interactions are limited.

The first section of this thesis used experimental manipulations to investigate how anthropogenic ocean acidification (OA) affects both pre- and post-settlement processes associated with coral recruitment. The first data chapter (Chp. 2) focussed on how OA altered the encrusting benthic community and its subsequent effects on coral settlement. Strikingly, the only preferred settlement substrate in the experimental controls (Titanoderma) was avoided by coral larvae as pCO₂ increased, and other substrata were selected. Chapter 3 then used a series of laboratory settlement assays to isolate the effect of OA on the survival and settlement of coral larvae with three ecologically important species of crustose coralline algae (CCA). Here, with all CCA species, the rates of coral settlement declined as pCO2 increased, but the magnitude of this effect was highest with Titanoderma. The last experimental chapter (Chp. 4) tested whether the reduced growth of coral recruits caused by OA would increase their mortality by prolonging their vulnerability to an acute disturbance: fish herbivory on surrounding algal turf. Compared to ambient conditions, recruits needed to double their size at the highest pCO2 to escape incidental grazing mortality. This general trend was observed with three groups of predators (blenny, surgeonfish and parrotfish), and the magnitude of the effect was highest with parrotfish.

The final data chapter (Chp. 5) of this thesis used permanently marked benthic plots and settlement tiles in a disturbed reef flat and reef slope habitat to investigate how life-history and adult stock influenced early recovery dynamics over a three year period. The reef slope was characterised by higher amounts of available settlement substrata, more than twice the rates of coral recruitment, and significantly higher recruit survival compared to the reef flat. In both habitats, as adult coral populations increased, so too did the density of recruits, yielding a significant positive stock-recruitment relationship. This positive stock-recruitment relationship was confined to species that brood their larvae, while no relationship was found for spawning corals. However, the stock-recruitment function did not influence the early recovery in either habitat. Instead, it was the presence of particular fast-growing acroporids on the reef slope that drove the rapid increase in coral cover, demonstrating the importance of life-history traits in assessing coral assemblage recovery. Using population matrices, major recruitment bottlenecks were determined for coral taxa common to Indo-Pacific reefs.

This thesis has captured some of the effects of both natural and anthropogenic disturbances on processes intrinsic to coral recruitment ecology. Of particular importance are the documented interactions among different biological groups – i.e. corals, algae, and herbivores – influenced by different kinds of stressors – e.g. ocean acidification, competition, and herbivory. Benthic communities often respond to perturbations in complex and unpredictable ways, so increasing our understanding of how recruiting corals respond to acute and chronic disturbances assists in the predictive modelling of benthic communities to make better informed management decisions.

Structural and functional vulnerability to elevated pCO2 in marine benthic communities

The effect of elevated pCO₂/low pH on marine invertebrate benthic biodiversity, community structure and selected functional responses which underpin ecosystem services (such as community production and calcification) was tested in a medium-term (30 days) mesocosm experiment in June 2010. Standardised intertidal macrobenthic communities, collected (50.3567°N, 4.1277°W) using artificial substrate units (ASUs), were exposed to one of seven pH treatments (8.05, 7.8. 7.6, 7.4, 7.2, 6.8 and 6.0). Community net calcification/dissolution rates, as well as changes in biomass, community structure and diversity, were measured at the end of the experimental period. Communities showed significant changes in structure and reduced diversity in response to reduced pH: shifting from a community dominated by calcareous organisms to one dominated by non-calcareous organisms around either pH 7.2 (number of individuals and species) or pH 7.8 (biomass). These results were supported by a reduced total weight of CaCO₃ structures in all major taxa at lowered pH and a switch from net calcification to net dissolution around pH 7.4 (Ω_calc = 0.78, Ω_ara = 0.5). Overall community soft tissue biomass did not change with pH and high mortality was observed only at pH 6.0, although molluscs and arthropods showed significant decreases in soft tissue. This study supports and refines previous findings on how elevated pCO₂ can induce changes in marine biodiversity, underlined by differential vulnerability of different phyla. In addition, it shows significant elevated pCO₂-/low pH-dependent changes in fundamental community functional responses underpinning changes in ecosystem services.

Selective mortality associated with variation in CO2 tolerance in a marine fish

Predicted future CO₂ levels can affect reproduction, growth, and behaviour of many marine organisms. However, the capacity of species to adapt to predicted changes in ocean chemistry is largely unknown. We used a unique field-based experiment to test for differential survival associated with variation in CO₂ tolerance in a wild population of coral-reef fishes. Juvenile damselfish exhibited variation in their response to elevated (700 μatm) CO₂ when tested in the laboratory and this influenced their behaviour and risk of mortality in the wild. Individuals that were sensitive to elevated CO₂ were more active and move further from shelter in natural coral reef habitat and, as a result, mortality from predation was significantly higher compared with individuals from the same treatment that were tolerant of elevated CO₂. If individual variation in CO₂ tolerance is heritable, this selection of phenotypes tolerant to elevated CO₂ could potentially help mitigate the effects of ocean acidification.

Effects of exposure duration on the response of Pocillopora damicornis larvae to elevated temperature and high pCO2

Efforts to evaluate the response of coral larvae to global climate change (GCC) and ocean acidification (OA) typically employ short experiments of fixed length, yet it is unknown how the response is affected by exposure duration. In this study, we exposed larvae from the brooding coral Pocillopora damicornis to contrasts of temperature (24.00 °C [ambient] versus 30.49 °C) and pCO₂ (49.4 Pa versus 86.2 Pa) for varying periods (1–5 days) to test the hypothesis that exposure duration had no effect on larval response as assessed by protein content, respiration, Symbiodinium density, and survivorship; exposure times were ecologically relevant compared to representative pelagic larval durations (PLD) for corals. Larvae differed among days for all response variables, and the effects of the treatment were relatively consistent regardless of exposure duration for three of the four response variables. Protein content and Symbiodinium density were unaffected by temperature and pCO₂, but respiration increased with temperature (but not pCO₂) with the effect intensifying as incubations lengthened. Survival, however, differed significantly among treatments at the end of the study, and by the 5th day, 78% of the larvae were alive and swimming under ambient temperature and ambient pCO₂, but only 55–59% were alive in the other treatments. These results demonstrate that the physiological effects of temperature and pCO₂ on coral larvae can reliably be detected within days, but effects on survival require ≥ 5 days to detect. The detection of time-dependent effects on larval survivorship suggests that the influence of GCC and OA will be stronger for corals having long PLDs.