Article

The Effects of Ocean Acidification on Feeding and Contest Behaviour by the Beadlet Anemone Actinia equina

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  • Marine Conservation Society
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Abstract

Increasing concentrations of atmospheric carbon dioxide are causing oceanic pH to decline worldwide, a phenomenon termed ocean acidification. Mounting experimental evidence indicates that near-future levels of CO2 will affect calcareous invertebrates such as corals, molluscs and gastropods, by reducing their scope for calcification. Despite extensive research into ocean acidification in recent years, the effects on non-calcifying anthozoans, such as sea anemones, remain little explored. In Western Europe, intertidal anemones such as Actinia equina are abundant, lower trophic-level organisms that function as important ecosystem engineers. Changes to behaviours of these simple predators could have implications for intertidal assemblages. This investigation identified the effects of reduced seawater pH on feeding and contest behaviour by A. equina. Video footage was recorded for A. equina feeding at current-day seawater (pH 8.1), and the least (pH 7.9) and most (pH 7.6) severe end-of-century predictions. Footage was also taken of contests over ownership of space between anemones exposed to reduced pH and those that were not. No statistically significant differences were identified in feeding duration or various aspects of contest behaviour including initiating, winning, inflating acrorhagi, inflicting acrorhagial peels and contest duration. Multivariate analyses showed no effect of pH on a combination of these variables. This provides contrast with other studies where anemones with symbiotic algae thrive in areas of natural increased acidity. Thus, novel experiments using intraspecific contests and resource-holding potential may prove an effective approach to understand sub-lethal consequences of ocean acidification for A. equina, other sea anemones and more broadly for marine ecosystems.

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... The foraging time was significantly longer due to the effects of OA in the sea urchin Strongylocentrotus fragilis (Barry et al., 2014). Some species such as the beadlet anemone Actinia equine have specific adaptability to OA; its feeding time and competition behavior under OA did not change significantly (Bamber et al., 2018). In a scavenging gastropod N. festivus, after short-term acidification treatment and returning back into the normal conditions, the foraging performance was able to return to a normal level (Leung et al., 2015). ...
Chapter
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Contest theory predicts the evolution of a stable mixture of different strategies for fighting. Here, we investigate the possibility that stable between-individual differences in startle-response durations influence fighting ability or 'resource-holding potential' (RHP) in the beadlet sea anemone, Actinia equina. Both winners and losers showed significant repeatability of pre-fight startle-response durations but mean pre-fight startle-response durations were greater for eventual losers than for eventual winners, indicating that RHP varies with boldness. In particular, individuals with short startle responses inflicted more attacks on their opponent. Both repeatability and mean-level responses were changed by the experience of fighting, and these changes varied with outcome. In losers, repeatability was disrupted to a greater extent and the mean startle-response durations were subject to a greater increase than in winners. Thus, following a fight, this behavioural correlate of RHP behaves in a way similar to post-fight changes in physiological status, which can also vary between winners and losers. Understanding the links between aggression and boldness therefore has the potential to enhance our understanding of both the evolution of animal personality and the 'winner and loser effects' of post-fight changes in RHP.
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Ocean acidification is predicted to affect marine ecosystems in many ways, including modification of fish behaviour. Previous studies have identified effects of CO(2)-enriched conditions on the sensory behaviour of fishes, including the loss of natural responses to odours resulting in ecologically deleterious decisions. Many fishes also rely on hearing for orientation, habitat selection, predator avoidance and communication. We used an auditory choice chamber to study the influence of CO(2)-enriched conditions on directional responses of juvenile clownfish (Amphiprion percula) to daytime reef noise. Rearing and test conditions were based on Intergovernmental Panel on Climate Change predictions for the twenty-first century: current-day ambient, 600, 700 and 900 µatm pCO(2). Juveniles from ambient CO(2)-conditions significantly avoided the reef noise, as expected, but this behaviour was absent in juveniles from CO(2)-enriched conditions. This study provides, to our knowledge, the first evidence that ocean acidification affects the auditory response of fishes, with potentially detrimental impacts on early survival.
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Ocean acidification (OA) refers to the ongoing decline in oceanic pH resulting from the uptake of atmospheric CO(2). Mounting experimental evidence suggests that OA will have negative consequences for a variety of marine organisms. Whereas the effect of OA on the calcification of adult reef corals is increasingly well documented, effects on early life history stages are largely unknown. Coral recruitment, which necessitates successful fertilization, larval settlement, and postsettlement growth and survivorship, is critical to the persistence and resilience of coral reefs. To determine whether OA threatens successful sexual recruitment of reef-building corals, we tested fertilization, settlement, and postsettlement growth of Acropora palmata at pCO(2) levels that represent average ambient conditions during coral spawning (∼400 μatm) and the range of pCO(2) increases that are expected to occur in this century [∼560 μatm (mid-CO(2)) and ∼800 μatm (high-CO(2))]. Fertilization, settlement, and growth were all negatively impacted by increasing pCO(2), and impairment of fertilization was exacerbated at lower sperm concentrations. The cumulative impact of OA on fertilization and settlement success is an estimated 52% and 73% reduction in the number of larval settlers on the reef under pCO(2) conditions projected for the middle and the end of this century, respectively. Additional declines of 39% (mid-CO(2)) and 50% (high-CO(2)) were observed in postsettlement linear extension rates relative to controls. These results suggest that OA has the potential to impact multiple, sequential early life history stages, thereby severely compromising sexual recruitment and the ability of coral reefs to recover from disturbance.
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Ecology Letters (2010) 13: 1419–1434 Abstract Ocean acidification is a pervasive stressor that could affect many marine organisms and cause profound ecological shifts. A variety of biological responses to ocean acidification have been measured across a range of taxa, but this information exists as case studies and has not been synthesized into meaningful comparisons amongst response variables and functional groups. We used meta‐analytic techniques to explore the biological responses to ocean acidification, and found negative effects on survival, calcification, growth and reproduction. However, there was significant variation in the sensitivity of marine organisms. Calcifying organisms generally exhibited larger negative responses than non‐calcifying organisms across numerous response variables, with the exception of crustaceans, which calcify but were not negatively affected. Calcification responses varied significantly amongst organisms using different mineral forms of calcium carbonate. Organisms using one of the more soluble forms of calcium carbonate (high‐magnesium calcite) can be more resilient to ocean acidification than less soluble forms (calcite and aragonite). Additionally, there was variation in the sensitivities of different developmental stages, but this variation was dependent on the taxonomic group. Our analyses suggest that the biological effects of ocean acidification are generally large and negative, but the variation in sensitivity amongst organisms has important implications for ecosystem responses.
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The biodiversity of coral reefs is dominated by invertebrates. Many of these invertebrates live in close association with scleractinian corals, relying on corals for food, habitat or settlement cues. Given their strong dependence on corals, it is of great concern that our knowledge of coralassociated invertebrates is so limited, especially in light of severe and ongoing degradation of coral reef habitats and the potential for species extinctions. This review examines the taxonomic extent of coral-associated invertebrates, the levels of dependence on coral hosts, the nature of associations between invertebrates and corals, and the factors that threaten coral-associated invertebrates now and in the future. There are at least 860 invertebrate species that have been described as coral associated, of which 310 are decapod crustaceans. Over half of coral-associated invertebrates appear to have an obligate dependence on live corals. Many exhibit a high degree of preference for one or two coral species, with species in the genera Pocillopora, Acropora and Stylophora commonly preferred. This level of habitat specialization may place coral-associated invertebrates at a great risk of extinction, particularly because preferred coral genera are those most susceptible to coral bleaching and mortality. In turn, many corals are also reliant on the services of particular invertebrates, leading to strong feedbacks between abundance of corals and their associated invertebrates. The loss of even a few preferred coral taxa could lead to a substantial decline in invertebrate biodiversity and have far-reaching effects on coral reef ecosystem function. A full appreciation of the consequences of further coral reef degradation for invertebrate biodiversity awaits a more complete description of the diversity of coral-associated invertebrates, the roles they play in coral reef ecosystems, their contribution to reef resilience and their conservation needs. © R. N. Gibson, R. J. A. Atkinson, J. D. M. Gordon, I. P. Smith and D. J. Hughes, Editors Taylor & Francis. All rights reserved.
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Pairwise contests occur when two individuals compete directly over ownership of an indivisible resource. Contests vary in the degree of escalation, some encounters being settled through non-injurious behaviour while others are only resolved after dangerous fighting. Here, we investigate the role of relatedness, assessed using AFLP analysis, on the occurrence of stinging during staged contests in the beadlet sea anemone Actinia equina. Contrary to our expectations, we found that the chance of stinging, and hence the chance of inflicting damage, increased with the degree of relatedness between the two opponents. This result may be explained by the negative relationship between asymmetry in fighting ability and escalation level predicted by theory. We suggest that in order to fully understand how relatedness influences aggression, predictions from kin selection theory should be incorporated with those from contest theory.
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The effects of oil pollution on the sea anemone Actinia equina were investigated. Chronic pollution with 2.5 ml.l−1 crude oil resulted, for about seven weeks, in ejection of increased numbers of the young which are normally brooded within the gastric cavity. Subsequently the numbers of surviving young being produced fell to zero, and the ovaries were found to be regressed and lacking ova. The anemones were also more frequently observed with tentacles expanded and mouth open, but the response to food offered to the tentacles was slow or absent. In separate tests it was found that crude oil presented on filter paper to the anemones could act as a feeding inducer, but that it interfered with or diluted the action of natural feeding inducers present in fish muscle extract. These effects are comparable with those which oil pollution has been found by other workers to have upon other anthozoans—the corals.
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The decisions that animals make are based on information gathered from their environment, and can have consequences for their fitness and survival. Such processes can be disrupted by environmental change. Hermit crabs find and select the gastropod shells they inhabit using chemical and visual cues, and tactile assessment. The choice of an optimal shell is important since it provides shelter against environmental extremes and protection against predators; inhabiting a suboptimal shell can also reduce fecundity. Hermit crabs are subject to cyclical reductions in the pH of the water in the intertidal rock pools that they inhabit, and such reductions may be further exacerbated by climate change. Reduced sea water pH, a consequence of ocean acidification and leaks from geological storage sites, has already been shown to disrupt the behaviour of marine animals. We investigated the effects of reduced sea water pH on the shell assessment and selection behaviour of the hermit crab Pagurus bernhardus. Under highly reduced pH conditions (pH 6.8) crabs were less likely to change from a suboptimal to an optimal shell than those in untreated sea water; those that did change shells took longer to do so. Crabs in the reduced pH treatment also showed significantly lower antennular flicking rates (the ‘sniffing’ response in decapods) and reduced movement. Thus, a reduction in sea water pH disrupts the resource assessment and decision-making processes of these crabs, indicating that the ability to acquire a vital resource may be influenced by both naturally occurring environmental cycles and anthropogenically induced environmental change.
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Increased seawater pCO 2 , and in turn 'ocean acidification' (OA), is predicted to profoundly impact marine ecosystem diversity and function this century. Much research has already focussed on calcifying reef-forming corals (Class: Anthozoa) that appear particularly susceptible to OA via reduced net calcification. However, here we show that OA-like conditions can simultaneously enhance the ecological success of non-calcifying anthozoans, which not only play key ecological and biogeochemical roles in present day benthic ecosystems but also represent a model organism should calcifying anthozoans exist as less calcified (soft-bodied) forms in future oceans. Increased growth (abundance and size) of the sea anemone (Anemonia viridis) population was observed along a natural CO 2 gradient at Vulcano, Italy. Both gross photosynthesis (P G) and respiration (R) increased with pCO 2 indicating that the increased growth was, at least in part, fuelled by bottom up (CO 2 stimulation) of metabolism. The increase of P G outweighed that of R and the genetic identity of the symbiotic microalgae (Symbiodinium spp.) remained unchanged (type A19) suggesting proximity to the vent site relieved CO 2 limitation of the anemones' symbiotic microalgal population. Our observa-tions of enhanced productivity with pCO 2 , which are consistent with previous reports for some calcifying corals, con-vey an increase in fitness that may enable non-calcifying anthozoans to thrive in future environments, i.e. higher seawater pCO 2 . Understanding how CO 2 -enhanced productivity of non-(and less-) calcifying anthozoans applies more widely to tropical ecosystems is a priority where such organisms can dominate benthic ecosystems, in particular following localized anthropogenic stress.
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Exposure to pollution and environmental change can alter the behaviour of aquatic animals and here we review recent evidence that exposure to elevated CO₂ and reduced sea water pH alters the behaviour of tropical reef fish and hermit crabs. Three main routes through which behaviour might be altered are discussed; elevated metabolic load, 'info-disruption' and avoidance behaviour away from polluted locations. There is clear experimental evidence that exposure to high CO₂ disrupts the ability to find settlement sites and shelters, the ability to detect predators and the ability to detect prey and food. In marine vertebrates and marine crustaceans behavioural change appears to occur via info-disruption. In hermit crabs and other crustaceans impairment of performance capacities might also play a role. We discuss the implications for such behavioural changes in terms of potential impacts at the levels of population health and ecosystem services, and consider future directions for research.
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Our planet is experiencing an increase in the concentration of atmospheric carbon dioxide (CO2) unprecedented in the past 800 000 years. About 30% of excess atmospheric CO2 is absorbed by the oceans, thus increasing the concentration of carbonic acid and reducing the ocean's pH. Species able to survive the physiological stress imposed by ocean acidification may still suffer strong indirect negative consequences. Comparing the tolerance of different species to dissolved CO2 is a necessary first step towards predicting the ecological impacts of rising CO2 levels on marine communities. While it is intuitive that not all aquatic species will be affected the same way by CO2, one could predict that closely related species, sharing similar life histories and ecology, may show similar tolerance levels to CO2. Our ability to create functional groups of species according to their CO2 tolerance may be crucial in our ability to predict community change in the future. Here, we tested the effects of CO2 exposure on the antipredator responses of four damselfish species (Pomacentrus chrysurus, Pomacentrus moluccensis, Pomacentrus amboinensis and Pomacentrus nagasakiensis). Although being sympatric and sharing the same ecology and life history, the four congeneric species showed striking and unexpected variation in CO2 tolerance, with CO2-induced loss of response to predation risk ranging from 30% to 95%. Using P. chrysurus as a model species, we further tested if these behavioural differences translated into differential ability to survive predators under natural conditions. Our results indicate that P. chrysurus larvae raised under CO2 levels predicted by 2070 and 2100 showed decreased antipredator responses to risk, leading to a five- to sevenfold increase in predation-related mortality in the first few hours of settlement. Examining ocean acidification, along with other environmental variables, will be a critical step in further evaluating ecological responses to predicted climatic change.
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The feeding habits of the Mediterranean sea anemonesCereus pedunculatus, Actinia equina andAnemonia viridis were examined mainly by analysing their coelenteron contents. The three species are opportunistic omnivorous suspension feeders. Main source of food forA. viridis andC. pedunculatus are crustaceans (mainly amphipods and decapods, respectively), while for the midlittoral speciesA. equina, it is organic detritus. Using the same method, the temporal and spatial changes in the diet ofA. viridis were examined. During the whole year, crustaceans seem to be the main source of food forA. viridis. The diet composition of this species, however, differs remarkably in space, possibly reflecting the different composition of the macrobenthic organismic assemblages in different areas. The data collected are compared with the limited bibliographical information.
Article
To function as an effective method to avoid build-up of anthropogenic carbon dioxide (CO2) in the atmosphere, storage of CO2 in geologic repositories must be designed and operated to minimize leakage. The design objectives include the obvious requirement to avoid large sudden releases and the more challenging task of keeping long-term leak rates to de minimis levels. Long-term retention requirements are a function of both the atmospheric stabilization target for greenhouse gases and the degree of reliance on CO2 capture and storage as a mitigation measure. A robust strategy will employ the CO2 capture and storage method as a component of a portfolio of programs that emphasize energy efficiency and use of renewable energy. To preserve options to stabilize greenhouse gases at prudent levels, it appears we will need to rely extensively on all three components of this portfolio. In developing criteria for management of leakage from geologic repositories, the policy and technical community will need to engage with environmental groups and the public at the earliest possible point in the process.
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Underground storage of industrial quantities of carbon dioxide in porous and permeable reservoir rocks has been taking place for the last 5 years at the Sleipner West gas field in the North Sea. Although there is still significant uncertainty in the actual figures, it appears that globally there is enough underground storage capacity for CO2 to make a significant impact on global emissions to the atmosphere. Some of the major issues that must be addressed if this technology is to spread to industrial plant such as power stations, and thus make an impact on global CO2 emissions, are cost of CO2 capture, demonstration of safety and security of storage and public acceptability.
Article
Fabry, V. J., Seibel, B. A., Feely, R. A., and Orr, J. C. 2008. Impacts of ocean acidification on marine fauna and ecosystem processes. – ICES Journal of Marine Science, 65: 414–432. Oceanic uptake of anthropogenic carbon dioxide (CO2) is altering the seawater chemistry of the world’s oceans with consequences for marine biota. Elevated partial pressure of CO2 (pCO2) is causing the calcium carbonate saturation horizon to shoal in many regions, particularly in high latitudes and regions that intersect with pronounced hypoxic zones. The ability of marine animals, most importantly pteropod molluscs, foraminifera, and some benthic invertebrates, to produce calcareous skeletal structures is directly affected by seawater CO2 chemistry. CO2 influences the physiology of marine organisms as well through acid-base imbalance and reduced oxygen transport capacity. The few studies at relevant pCO2 levels impede our ability to predict future impacts on foodweb dynamics and other ecosystem processes. Here we present new observations, review available data, and identify priorities for future research, based on regions, ecosystems, taxa, and physiological processes believed to be most vulnerable to ocean acidification. We conclude that ocean acidification and the synergistic impacts of other anthropogenic stressors provide great potential for widespread changes to marine ecosystems.
Article
While ocean acidification is predicted to threaten marine biodiversity, the processes that directly impact species persistence are not well understood. For marine species, early life history stages are inherently vulnerable to predators and an innate ability to detect predators can be critical for survival. However, whether or not acidification inhibits predator detection is unknown. Here, we show that newly hatched larvae of the marine fish Amphiprion percula innately detect predators using olfactory cues and this ability is retained through to settlement. Aquarium-reared larvae, not previously exposed to predators, were able to distinguish between the olfactory cues of predatory and non-predatory species. However, when eggs and larvae were exposed to seawater simulating ocean acidification (pH 7.8 and 1000 p.p.m. CO2) settlement-stage larvae became strongly attracted to the smell of predators and the ability to discriminate between predators and non-predators was lost. Newly hatched larvae were unaffected by CO2 exposure and were still able to distinguish between predatory and non-predatory fish. If this impairment of olfactory preferences in settlement-stage larvae translates to higher mortality as a result of increased predation risk, there could be direct consequences for the replenishment and the sustainability of marine populations. Ecology Letters (2010) 13: 68–75