Direct and indirect effects of ocean acidification and warming on a marine plant–herbivore interaction

The impacts of climatic change on organisms depend on the interaction of multiple stressors and how these may affect the interactions among species. Consumer–prey relationships may be altered by changes to the abundance of either species, or by changes to the per capita interaction strength among species. To examine the effects of multiple stressors on a species interaction, we test the direct, interactive effects of ocean warming and lowered pH on an abundant marine herbivore (the amphipod Peramphithoe parmerong), and whether this herbivore is affected indirectly by these stressors altering the palatability of its algal food (Sargassum linearifolium). Both increased temperature and lowered pH independently reduced amphipod survival and growth, with the impacts of temperature outweighing those associated with reduced pH. Amphipods were further affected indirectly by changes to the palatability of their food source. The temperature and pH conditions in which algae were grown interacted to affect algal palatability, with acidified conditions only affecting feeding rates when algae were also grown at elevated temperatures. Feeding rates were largely unaffected by the conditions faced by the herbivore while feeding. These results indicate that, in addition to the direct effects on herbivore abundance, climatic stressors will affect the strength of plant–herbivore interactions by changes to the susceptibility of plant tissues to herbivory.

Multiple physiological responses to multiple environmental challenges: an individual approach

The injection of anthropogenically-produced CO₂ into the atmosphere will lead to an increase in temperature and a decrease in pH at the surface of the oceans by 2100. Marine intertidal organisms possess the ability to cope in the short term with environmental fluctuations exceeding predicted values. However, how they will cope with chronic exposure to elevated temperature and pCO₂ is virtually unknown. In addition, individuals from the same species/population often show remarkable levels of variation in their responses to complex climatic changes: in particular, variation in metabolic rates often is linked to differences in individuals’ performances and fitness. Despite its ecological and evolutionary importance, inter-individual variation has rarely been investigated within the context of climatic changes, and most investigations have typically employed orthogonal experimental designs paired to analyses of independent samples. Although this is undoubtedly a powerful and useful approach, it may not be the most appropriate for understanding all alterations of biological functions in response to environmental changes. An individual approach arguably should be favored when trying to describe organisms’ responses to climatic change. Consequently, to test which approach had the greater power to discriminate the intensity and direction of an organism’s response to complex climatic changes, we investigated the extracellular osmo/iono-regulatory abilities, upper thermal tolerances (UTTs), and metabolic rates of individual adults of an intertidal amphipod, Echinogammarus marinus, exposed for 15 days to combined elevated temperature and pCO₂. The individual approach led to stronger and different predictions on how ectotherms will likely respond to ongoing complex climatic change, compared with the independent approaches. Consequently, this may call into question the relevance, or even the validity, of some of the predictions made to date. Finally, we argue that treating individual differences as biologically meaningful can lead to a better understanding of the physiological responses themselves and the selective processes that will occur with complex climatic changes; selection will likely play a crucial role in defining species’ responses to future environmental changes. Individuals with higher metabolic rates were also characterized by greater extracellular osmo/iono-regulative abilities and higher UTTs, and thus there appeared to be no evolutionary trade-offs between these functions. However, as individuals with greater metabolic rates also have greater costs for maintenance and repair, and likely a lower fraction of energy available for growth and reproduction, trade-offs between life-history and physiological performance may still arise.

Chapter five – stress biology and immunology in Nephrops norvegicus

The Norway lobster Nephrops norvegicus lives at low-light depths, in muddy substrata of high organic content where water salinities are high and fluctuations in temperature are moderate. In this environment, the lobsters are naturally exposed to a number of potential stressors, many of them as a result of the surficial breakdown of organic material in the sediment. This process (early diagenesis) creates a heterogeneous environment with temporal and spatial fluctuations in a number of compounds such as oxygen, ammonia, metals, and hydrogen sulphide. In addition to this, there are anthropogenically generated stressors, such as human-induced climate change (resulting in elevated temperature and ocean acidification), pollution and fishing. The lobsters are thus exposed to several stressors, which are strongly linked to the habitat in which the animals live. Here, the capacity of Nephrops to deal with these stressors is summarised. Eutrophication-induced hypoxia and subsequent metal remobilisation from the sediment is a well-documented effect found in some wild Nephrops populations. Compared to many other crustacean species, Nephrops is well adapted to tolerate periods of hypoxia, but prolonged or severe hypoxia, beyond their tolerance level, is common in some areas. When the oxygen concentration in the environment decreases, the bioavailability of redox-sensitive metals such as manganese increases. Manganese is an essential metal, which, taken up in excess, has a toxic effect on several internal systems such as chemosensitivity, nerve transmission and immune defence. Since sediment contains high concentrations of metals in comparison to sea water, lobsters may accumulate both essential and non-essential metals. Different metals have different target tissues, though the hepatopancreas, in general, accumulates high concentrations of most metals. The future scenario of increasing anthropogenic influences on Nephrops habitats may have adverse effects on the fitness of the animals.

Deformities in larvae and juvenile European lobster (Homarus gammarus) exposed to lower pH at two different temperatures

Trends of increasing temperatures and ocean acidification are expected to influence benthic marine resources, especially calcifying organisms. The European lobster (Homarus gammarus) is among those species at risk. A project was initiated in 2011 aiming to investigate long-term synergistic effects of temperature and projected increases in ocean acidification on the life cycle of lobster. Larvae were exposed to pCO₂ levels of ambient water (water intake at 90 m depth, tentatively of 380 μatm pCO₂), 727 and 1217 μatm pCO₂, at temperatures 10 and 18 °C. Long-term exposure lasted until 5 months of age. Thereafter the surviving juveniles were transferred to ambient water at 14 °C. At 18 °C the development from Stage 1 to 4 lasted from 14 to 16 days, as predicted under normal pH values. Growth was very slow at 10 °C and resulted in only two larvae reaching Stage 4 in the ambient treatment. There were no significant differences in carapace length at the various larval stages between the different treatments, but there were differences in total length and dry weight at Stage 1 at 10 °C, Stage 2 at both temperatures, producing larvae slightly larger in size and lighter by dry weight in the exposed treatments. Stage 3 larvae raised in 18 °C and 1217 μatm pCO₂ were also larger in size and heavier by dry weight compared with 727 μatm. Unfortunate circumstances precluded a full comparison across stages and treatment. Deformities were however observed in both larvae and juveniles. At 10 °C, about 20% of the larvae exposed to elevated pCO₂were deformed, compared with 0% in larvae raised in pH above 8.0. At 18 °C and in high pCO₂ treatment, 31.5% of the larvae were deformed. Occurrence of deformities after 5 months of exposure was 33 and 44% in juveniles raised in ambient and low pCO₂, respectively, and 20% in juveniles exposed to high pCO₂. Some of the deformities will possibly affect the ability to find food, sexual partner (walking legs, claw and antenna), respiration (carapace), and ability to swim (tail-fan damages).

The role of preconditioning in ocean acidification experiments: a test with the intertidal isopod Paradella dianae

Environmental alterations are accelerating worldwide and the rate of change in ocean chemistry is predicted to happen so rapidly that it is unclear how marine ecosystems will respond. It is hypothesized that the phenotypic plasticity or acclimation capacity of an individual provides a buffer against environmental change; however, this plasticity depends on the speed at which the change occurs. Ocean acidification studies have found direct and acute responses from organisms exposed to elevated CO₂ levels. Now, the challenge lies in integrating acclimation into experimental design in short-term studies, requiring proper preconditioning setups. Here we experimentally show that different preconditioning approaches produce different physiological and behavioral responses in the intertidal isopod Paradella dianae. Isopods were impaired when immediately exposed to elevated CO₂ levels relative to individuals that were gradually acclimated to high CO₂ concentrations. Abruptly introducing organisms to severe changes in CO₂ conditions can produce confounding effects of short-term stress with acclimated responses to long-term shifts in ocean chemistry. By exposing organisms to sudden changes in CO₂ concentrations, we are forcing immediate physiological stress reactions that could be independent of exposure to specific CO₂ levels. We discuss how integrating acclimation in experimental design can help provide more accurate predictions about the impact of ocean acidification on marine ecosystems.

Biological impacts of enhanced alkalinity in Carcinus maenas

Further steps are needed to establish feasible alleviation strategies that are able to reduce the impacts of ocean acidification, whilst ensuring minimal biological side-effects in the process. Whilst there is a growing body of literature on the biological impacts of many other carbon dioxide reduction techniques, seemingly little is known about enhanced alkalinity. For this reason, we investigated the potential physiological impacts of using chemical sequestration as an alleviation strategy. In a controlled experiment, Carcinus maenas were acutely exposed to concentrations of Ca(OH)₂ that would be required to reverse the decline in ocean surface pH and return it to pre-industrial levels. Acute exposure significantly affected all individuals’ acid–base balance resulting in slight respiratory alkalosis and hyperkalemia, which was strongest in mature females. Although the trigger for both of these responses is currently unclear, this study has shown that alkalinity addition does alter acid–base balance in this comparatively robust crustacean species.

Effects of ocean acidification on juvenile red king crab (Paralithodes camtschaticus) and tanner crab (Chionoecetes bairdi) growth, condition, calcification, and survival

Ocean acidification, a decrease in the pH in marine waters associated with rising atmospheric CO₂ levels, is a serious threat to marine ecosystems. In this paper, we determine the effects of long-term exposure to near-future levels of ocean acidification on the growth, condition, calcification, and survival of juvenile red king crabs, Paralithodes camtschaticus, and Tanner crabs, Chionoecetes bairdi. Juveniles were reared in individual containers for nearly 200 days in flowing control (pH 8.0), pH 7.8, and pH 7.5 seawater at ambient temperatures (range 4.4–11.9 °C). In both species, survival decreased with pH, with 100% mortality of red king crabs occurring after 95 days in pH 7.5 water. Though the morphology of neither species was affected by acidification, both species grew slower in acidified water. At the end of the experiment, calcium concentration was measured in each crab and the dry mass and condition index of each crab were determined. Ocean acidification did not affect the calcium content of red king crab but did decrease the condition index, while it had the opposite effect on Tanner crabs, decreasing calcium content but leaving the condition index unchanged. This suggests that red king crab may be able to maintain calcification rates, but at a high energetic cost. The decrease in survival and growth of each species is likely to have a serious negative effect on their populations in the absence of evolutionary adaptation or acclimatization over the coming decades.

Impact of ocean acidification on metabolism and energetics during early life stages of the intertidal porcelain crab Petrolisthes cinctipes

Absorption of elevated atmospheric CO₂ is causing surface ocean pH to decline, a process known as ocean acidification (OA). To date, few studies have assessed the physiological impacts of OA on early life-history stages of intertidal organisms, which transition from habitats with fluctuating pH (intertidal zone) to relatively stable (pelagic zone) pH environments. We used the intertidal crab Petrolisthes cinctipes to determine whether metabolic responses to year 2300 predictions for OA vary among early developmental stages and to examine whether the effects were more pronounced in larval stages developing in the open ocean. Oxygen consumption rate, total protein, dry mass, total lipids and C/N were determined in late-stage embryos, zoea I larvae and newly settled juveniles reared in ambient pH (7.93±0.06) or low pH (7.58±0.06). After short-term exposure to low pH, embryos displayed 11% and 6% lower metabolism and dry mass, respectively, which may have an associated bioenergetic cost of delayed development to hatching. However, metabolic responses appeared to vary among broods, suggesting significant parental effects among the offspring of six females, possibly a consequence of maternal state during egg deposition and genetic differences among broods. Larval and juvenile metabolism were not affected by acute exposure to elevated CO₂. Larvae contained 7% less nitrogen and C/N was 6% higher in individuals reared at pH 7.58 for 6 days, representing a possible switch from lipid to protein metabolism under low pH; the metabolic switch appears to fully cover the energetic cost of responding to elevated CO₂. Juvenile dry mass was unaffected after 33 days exposure to low pH seawater. Increased tolerance to low pH in zoea I larvae and juvenile stages may be a consequence of enhanced acid–base regulatory mechanisms, allowing greater compensation of extracellular pH changes and thus preventing decreases in metabolism after exposure to elevated P_CO2. The observed variation in responses of P. cinctipes to decreased pH in the present study suggests the potential for this species to adapt to future declines in near-shore pH.

Effects of ocean acidification on early life-history stages of the intertidal porcelain crab Petrolisthes cinctipes

Intertidal zone organisms naturally experience daily fluctuations in pH, presently reaching values beyond what is predicted for open ocean surface waters from ocean acidification (OA) by the year 2100, and thus present an opportunity to study the pH sensitivity of organisms that are presumably adapted to an acidified environment. The intertidal zone porcelain crab, Petrolisthes cinctipes, was used to study physiological responses to low pH in embryonic, larval and newly recruited juvenile life-history stages. In these crabs, embryonic development occurs in the pH-variable intertidal zone (pH 6.9–9.5), larvae mature in the more stable pelagic environment (pH 7.9–8.2), and juvenile crabs settle back into the pH-variable intertidal zone. We examined survival, cardiac performance, energetics and morphology in embryonic, larval and juvenile crabs exposed to two pH conditions (pH 7.9 and 7.6). Embryos and larvae were split by brood between the pH treatments for 9 days to examine brood-specific responses to low pH. Hatching success did not differ between pH conditions, but ranged from 30% to 95% among broods. Larval survival was not affected by acidification, but juvenile survival was reduced by ~30% after longer (40 days) exposure to low pH. Embryonic and larval heart rates were 37% and 20% lower at low pH, and there was a brood-specific response in embryos. Embryos did not increase in volume under acidified conditions, compared with a 15% increase in ambient conditions. We conclude that sustained exposure to low pH could be detrimental to P. cinctipes embryos and larvae despite the fact that embryos are regularly exposed to naturally fluctuating hypercapnic water in the intertidal zone. Importantly, our results indicate that early life-history stage responses to OA may be brood specific through as yet undetermined mechanisms.

The response of abyssal organisms to low pH conditions during a series of CO2-release experiments simulating deep-sea carbon sequestration

The effects of low-pH, high-pCO₂ conditions on deep-sea organisms were examined during four deep-sea CO₂ release experiments simulating deep-ocean C sequestration by the direct injection of CO₂ into the deep sea. We examined the survival of common deep-sea, benthic organisms (microbes; macrofauna, dominated by Polychaeta, Nematoda, Crustacea, Mollusca; megafauna, Echinodermata, Mollusca, Pisces) exposed to low-pH waters emanating as a dissolution plume from pools of liquid carbon dioxide released on the seabed during four abyssal CO₂-release experiments. Microbial abundance in deep-sea sediments was unchanged in one experiment, but increased under environmental hypercapnia during another, where the microbial assemblage may have benefited indirectly from the negative impact of low-pH conditions on other taxa. Lower abyssal metazoans exhibited low survival rates near CO₂ pools. No urchins or holothurians survived during 30–42 days of exposure to episodic, but severe environmental hypercapnia during one experiment (E1; pH reduced by as much as ca. 1.4 units). These large pH reductions also caused 75% mortality for the deep-sea amphipod, Haploops lodo, near CO₂ pools. Survival under smaller pH reductions (ΔpH<0.4 units) in other experiments (E2, E3, E5) was higher for all taxa, including echinoderms. Cephalopods, gastropods, and fish were more tolerant than most other taxa. The gastropod Mohnia vernalis and octopus Benthoctopus sp. survived exposure to pH reductions that episodically reached −0.3 pH units. Ninety percent of abyssal zoarcids (Pachycara bulbiceps) survived exposure to pH changes reaching ca. −0.3 pH units during 30–42 day-long experiments.