ALBERT

Description: Ecosystem-based management on coral reefs has historically focused on biodiversity conservation through the establishment of marine reserves, but it is increasingly recognised that a subset of species can be key to the maintenance of ecosystem processes and functioning. Specific provisions for these key taxa are essential to biodiversity conservation and resilience-based adaptive management. While a wealth of literature addresses ecosystem functioning on coral reefs, available information covers only a subset of specific taxa, ecological processes and environmental stressors. What is lacking is a comparative assessment across the diverse range of coral reef species to synthesise available knowledge to inform science and management. Here we employed expert elicitation coupled with a literature review to generate the first comprehensive assessment of 70 taxonomically diverse and functionally distinct coral reef species from microbes to top predators to summarise reef functioning. Although our synthesis is largely through the lens of the Great Barrier Reef, Australia, a particularly data-rich system, it is relevant to coral reefs in general. We use this assessment to evaluate which taxa drive processes that maintain a healthy reef, and whether or not management of these taxa is considered a priority (i.e. are they vulnerable?) or is feasible (i.e. can they be managed?). Scientific certainty was scored to weight our recommendations, particularly when certainty was low. We use five case studies to highlight critical gaps in knowledge that limit our understanding of ecosystem functioning. To inform the development of novel management strategies and research objectives, we identify taxa that support positive interactions and enhance ecosystem performance, including those where these roles are currently underappreciated. We conclude that current initiatives effectively capture many priority taxa, but that there is significant room to increase opportunities for underappreciated taxa in both science and management to maximally safeguard coral reef functioning.

Description: Ocean acidification is one of the most pressing environmental concerns of our time, and not surprisingly, we have seen a recent explosion of research into the physiological impacts and ecological consequences of changes in ocean chemistry. We are gaining considerable insights from this work, but further advances require greater integration across disciplines. Here, we showed that projected near-future CO2 levels impaired the ability of damselfish to learn the identity of predators. These effects stem from impaired neurotransmitter function; impaired learning under elevated CO2 was reversed when fish were treated with gabazine, an antagonist of the GABA-A receptor - a major inhibitory neurotransmitter receptor in the brain of vertebrates. The effects of CO2 on learning and the link to neurotransmitter interference were manifested as major differences in survival for fish released into the wild. Lower survival under elevated CO2 , as a result of impaired learning, could have a major influence on population recruitment.

Description: Ocean acidification and warming, driven by anthropogenic CO2 emissions, are considered to be among the greatest threats facing marine organisms. While each stressor in isolation has been studied extensively, there has been less focus on their combined effects, which could impact key ecological processes. We tested the independent and combined effects of short-term exposure to elevated CO2 and temperature on the predator–prey interactions of a common pair of coral reef fishes (Pomacentrus wardi and its predator, Pseudochromis fuscus). We found that predator success increased following independent exposure to high temperature and elevated CO2. Overall, high temperature had an overwhelming effect on the escape behaviour of the prey compared with the combined exposure to elevated CO2 and high temperature or the independent effect of elevated CO2. Exposure to high temperatures led to an increase in attack and predation rates. By contrast, we observed little influence of elevated CO2 on the behaviour of the predator, suggesting that the attack behaviour of P. fuscus was robust to this environmental change. This is the first study to address how the kinematics and swimming performance at the basis of predator–prey interactions may change in response to concurrent exposure to elevated CO2 and high temperatures and represents an important step to forecasting the responses of interacting species to climate change.

Description: Bacteria associated with marine invertebrates are thought to have a range of important roles that benefit the host including production of compounds that may exclude pathogenic microorganisms and recycling of essential nutrients. This study characterised the microbiome of a gonochoric octocoral, Lobophytum pauciflorum, and investigated whether either sex or environmental stresses influenced the diversity of the associated microbiome through amplicon profiling of the bacterial 16S rRNA gene. Sequences affiliated to Spirochaetaceae and Endozoicimonaceae dominated the microbiome of L. pauciflorum, representing 43% and 21% of the community, respectively. Among the dominant class affiliations, no sex-specific differences were detected, though unassigned sequences were at a 2-fold higher relative abundance in samples from female individuals than from males. These potentially novel sequences contributed to observed differences between sexes as detected by a multivariate analysis at the OTU level. Exposing L. pauciflorum fragments to increased temperature (31°C), decreased pH (7.9) or both stressors simultaneously for 12 days did not significantly alter the microbial community, indicating that the soft coral microbiome is relatively resilient to short-term environmental stress.

Description: Anthropogenic carbon dioxide (CO2) emissions are being absorbed by the oceans, a process known as ocean acidification, and risks adversely affecting a variety of behaviours in a range of marine species, including inhibited learning in some fishes. However, the effects of elevated CO2 on learning in advanced invertebrates such as cephalopods are unknown. Any impacts to the learning abilities of cephalopods could have far-reaching consequences for their populations and the communities they inhabit. Cephalopods have some of the most advanced cognitive abilities among invertebrates and are one of the few invertebrate taxa in which conditional discrimination has been demonstrated, though the trait has not been demonstrated in any species of squid. Here, we tested for the first time the capacity for conditional discrimination in a squid species (Sepioteuthis lessoniana). Furthermore, we investigated the effects of projected future CO2 levels (1,084 µatm) on conditional discrimination and learning more generally. A three-task experiment within a two-choice arena was used to test learning and conditional discrimination. Learning was measured by improvements in task completion in repeated trials over time and the number of trials required to pass each task. Squid exhibited significant learning capabilities, with an increase in correct choices over successive trials and a decrease in the number of trials needed to complete the successive tasks. Six of the 12 squid tested successfully passed all three tasks indicating a capacity for conditional discrimination in the species. Elevated CO2 had no effect on learning or on the capacity for conditional discrimination in squid. This study highlights the remarkable cognitive abilities of S. lessoniana, demonstrated by their capacity for conditional discrimination, and suggests that ocean acidification will not compromise learning abilities. However, other behavioural traits in the species have been shown to be altered at comparable elevated CO2 conditions. It is not clear why some ecologically important behaviours are altered by elevated CO2 whereas others are unaffected. Future research should focus on the physiological mechanism responsible for altered behaviours in squid at elevated CO2.

Description: Recent research has shown that exposure to elevated carbon dioxide (CO2) affects how fishes perceive their environment, affecting behavioral and cognitive processes leading to increased prey mortality. However, it is unclear if increased mortality results from changes in the dynamics of predator-prey interactions or due to prey increasing activity levels. Here we demonstrate that ocean pCO2 projected to occur by 2100 significantly effects the interactions of a predator-prey pair of common reef fish: the planktivorous damselfish Pomacentrus amboinensis and the piscivorous dottyback Pseudochromis fuscus. Prey exposed to elevated CO2 (880 µatm) or a present-day control (440 µatm) interacted with similarly exposed predators in a cross-factored design. Predators had the lowest capture success when exposed to elevated CO2 and interacting with prey exposed to present-day CO2. Prey exposed to elevated CO2 had reduced escape distances and longer reaction distances compared to prey exposed to present-day CO2 conditions, but this was dependent on whether the prey was paired with a CO2 exposed predator or not. This suggests that the dynamics of predator-prey interactions under future CO2 environments will depend on the extent to which the interacting species are affected and can adapt to the adverse effects of elevated CO2.

Description: Ocean warming and acidification are serious threats to marine life. While each stressor alone has been studied in detail, their combined effects on the outcome of ecological interactions are poorly understood. We measured predation rates and predator selectivity of two closely related species of damselfish exposed to a predatory dottyback. We found temperature and CO2 interacted synergistically on overall predation rate, but antagonistically on predator selectivity. Notably, elevated CO2 or temperature alone reversed predator selectivity, but the interaction between the two stressors cancelled selectivity. Routine metabolic rates of the two prey showed strong species differences in tolerance to CO2 and not temperature, but these differences did not correlate with recorded mortality. This highlights the difficulty of linking species-level physiological tolerance to resulting ecological outcomes. This study is the first to document both synergistic and antagonistic effects of elevated CO2 and temperature on a crucial ecological process like predator-prey dynamics.

Description: There is increasing evidence that projected near‐future carbon dioxide (CO2) levels can alter predator avoidance behaviour in marine invertebrates, yet little is known about the possible effects on predatory behaviours. Here we tested the effects of elevated CO2 on the predatory behaviours of two ecologically distinct cephalopod species, the pygmy squid, Idiosepius pygmaeus, and the bigfin reef squid, Sepioteuthis lessoniana. Both species exhibited an increased latency to attack and altered body pattern choice during the attack sequence at elevated CO2. I. pygmaeus also exhibited a 20% decrease in predation rate, an increased striking distance, and reduced preference for attacking the posterior end of prey at elevated CO2. Elevated CO2 increased activity levels of S. lessoniana comparable to those previously shown in I. pygmaeus, which could adversely affect their energy budget and increase their potential to be preyed upon. The effects of elevated CO2 on predatory behaviours, predation strategies and activity levels of cephalopods reported here could have far‐reaching consequences in marine ecosystems due to the ecological importance of cephalopods in the marine food web.

Description: Squid and many other cephalopods live continuously on the threshold of their environmental oxygen limitations. If the abilities of squid to effectively take up oxygen are negatively affected by projected future carbon dioxide (CO2) levels in ways similar to those demonstrated in some fish and invertebrates, it could affect the success of squid in future oceans. While there is evidence that acute exposure to elevated CO2 has adverse effects on cephalopod respiratory performance, no studies have investigated this in an adult cephalopod after relatively prolonged exposure to elevated CO2 or determined any effects on aerobic scope. Here, we tested the effects of prolonged exposure (〉=20% of lifespan) to elevated CO2 levels (~1000 μatm) on the routine and maximal oxygen uptake rates, aerobic scope and recovery time of two tropical cephalopod species, the two-toned pygmy squid, Idiosepius pygmaeus and the bigfin reef squid, Sepioteuthis lessoniana. Neither species exhibited evidence of altered aerobic performance after exposure to elevated CO2 when compared to individuals held at control conditions. The recovery time of I. pygmaeus under both control and elevated CO2 conditions was less than 1 hour, whereas S. lessoniana required approximately 8 hours to recover fully following maximal aerobic performance. This difference in recovery time may be due to the more sedentary behaviours of I. pygmaeus. The ability of these two cephalopod species to cope with prolonged exposure to elevated CO2 without detriment to their aerobic performance suggests some resilience to an increasingly high CO2 world.