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 predicted to negatively impact the reproduction of many marine species, either by reducing fertilization success or diverting energy from reproductive effort. While recent studies have demonstrated how ocean acidification will affect larval and juvenile fishes, little is known about how increasing partial pressure of carbon dioxide (pCO2) and decreasing pH might affect reproduction in adult fishes. We investigated the effects of near-future levels of pCO2 on the reproductive performance of the cinnamon anemonefish, Amphiprion melanopus, from the Great Barrier Reef, Australia. Breeding pairs were held under three CO2 treatments [Current-day Control (430 µatm), Moderate (584 µatm) and High (1032 µatm)] for a 9-month period that included the summer breeding season. Unexpectedly, increased CO2 dramatically stimulated breeding activity in this species of fish. Over twice as many pairs bred in the Moderate (67% of pairs) and High (55%) compared to the Control (27%) CO2 treatment. Pairs in the High CO2 group produced double the number of clutches per pair and 67% more eggs per clutch compared to the Moderate and Control groups. As a result, reproductive output in the High group was 82% higher than that in the Control group and 50% higher than that in the Moderate group. Despite the increase in reproductive activity, there was no difference in adult body condition among the three treatment groups. There was no significant difference in hatchling length between the treatment groups, but larvae from the High CO2 group had smaller yolks than Controls. This study provides the first evidence of the potential effects of ocean acidification on key reproductive attributes of marine fishes and, contrary to expectations, demonstrates an initially stimulatory (hormetic) effect in response to increased pCO2. However, any long-term consequences of increased reproductive effort on individuals or populations remain to be determined.

Description: Behaviour and sensory performance of marine fishes are impaired at CO2 levels projected to occur in the ocean in the next 50-100 years, and there is limited potential for within-generation acclimation to elevated CO2. However, whether fish behaviour can acclimate or adapt to elevated CO2 over multiple generations remains unanswered. We tested for transgenerational acclimation of reef fish olfactory preferences and behavioural lateralization at moderate (656 µatm) and high (912 µatm) end-of-century CO2 projections. Juvenile spiny damselfish, Acanthochromis polyacanthus, from control parents (446 µatm) exhibited an innate avoidance to chemical alarm cue (CAC) when reared in control conditions. In contrast, juveniles lost their innate avoidance of CAC and even became strongly attracted to CAC when reared at elevated CO2 levels. Juveniles from parents maintained at mid-CO2 and high-CO2 levels also lost their innate avoidance of CAC when reared in elevated CO2, demonstrating no capacity for transgenerational acclimation of olfactory responses. Behavioural lateralization was also disrupted for juveniles reared under elevated CO2, regardless of parental conditioning. Our results show minimal potential for transgenerational acclimation in this fish, suggesting that genetic adaptation will be necessary to overcome the effects of ocean acidification on behaviour.

Description: An increasing number of studies have examined the effects of elevated carbon dioxide (CO2) and ocean acidification on marine fish, yet little is known about the effects on large pelagic fish. We tested the effects of elevated CO2 on the early life history development and behaviour of yellowtail kingfish, Seriola lalandi. Eggs and larvae were reared in current day control (450 µatm) and two elevated CO2 treatments for a total of 6 d, from 12 h post-fertilization until 3 d post-hatching (dph). Elevated CO2 treatments matched projections for the open ocean by the year 2100 under RCP 8.5 (880 µatm CO2) and a higher level (1700 µatm CO2) relevant to upwelling zones where pelagic fish often spawn. There was no effect of elevated CO2 on survival to hatching or 3 dph. Oil globule diameter decreased with an increasing CO2 level, indicating potential effects of elevated CO2 on energy utilization of newly hatched larvae, but other morphometric traits did not differ among treatments. Contrary to expectations, there were no effects of elevated CO2 on larval behaviour. Activity level, startle response, and phototaxis did not differ among treatments. Our results contrast with findings for reef fish, where a wide range of sensory and behavioural effects have been reported. We hypothesize that the absence of behavioural effects in 3 dph yellowtail kingfish is due to the early developmental state of newly hatched pelagic fish. Behavioural effects of high CO2 may not occur until larvae commence branchial acid-base regulation when the gills develop; however, further studies are required to test this hypothesis. Our results suggest that the early stages of kingfish development are tolerant to rising CO2 levels in the ocean.

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: 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.

Description: Elevated seawater CO2 can cause a range of behavioural impairments in marine fishes. However, most studies to date have been conducted on small benthic species and very little is known about how higher oceanic CO2 levels could affect the behaviour of large pelagic species. Here, we tested the effects of elevated CO2, and where possible the interacting effects of high temperature, on a range of ecologically important behaviours (anxiety, routine activity, behavioural lateralization and visual acuity) in juvenile yellowtail kingfish, Seriola lalandi. Kingfish were reared from the egg stage to 25 days post-hatch in a full factorial design of ambient and elevated CO2 (∼500 and ∼1000 μatm pCO2) and temperature (21 °C and 25 °C). The effects of elevated CO2 were trait-specific with anxiety the only behaviour significantly affected. Juvenile S. lalandi reared at elevated CO2 spent more time in the dark zone during a standard black-white test, which is indicative of increased anxiety. Exposure to high temperature had no significant effect on any of the behaviours tested. Overall, our results suggest that juvenile S. lalandi are largely behaviourally tolerant to future ocean acidification and warming. Given the ecological and economic importance of large pelagic fish species more studies investigating the effect of future climate change are urgently needed.

Description: The oceans are absorbing additional carbon dioxide (CO2) from the atmosphere and projected future CO2 levels and ocean acidification could have negative implications for many marine organisms, especially during early life stages. Cephalopods are ecologically important in marine ecosystems, yet the potential effects of increased partial pressure of CO2 (pCO2) in seawater on cephalopod reproduction and embryonic development are little studied. We allowed adult two-toned pygmy squid (Idiosepius pygmaeus) to breed in ambient control (∼445 μatm; ∼8.05 pH) or elevated pCO2 conditions (∼940 μatm; ∼7.78 pH) and compared reproductive traits in adults and developmental characteristics of their eggs, which remained in control or elevated pCO2 treatments until hatching. Breeding pairs at elevated pCO2 produced clutches with 40% fewer eggs, vitelli that were 14% smaller directly after spawning, embryos that were 5% smaller upon hatching, and eggs with an 8% increase in late-stage egg swelling compared with pairs at control conditions. Elevated pCO2 did not affect fertility, time to hatch, or hatching success. Eggs were laid 40% closer together in elevated pCO2 compared with control conditions, indicating a possible effect of elevated pCO2 on reproductive behaviour. These results show that elevated pCO2 can adversely affect reproduction and embryonic development of the two-toned pygmy squid. As the potential for adaptation is influenced by reproductive success, testing the capacity for squid to adapt to future ocean conditions should be a priority for future research.

Description: Ocean warming and acidification act concurrently on marine ectotherms with the potential for detrimental, synergistic effects; yet, effects of these stressors remain understudied in large predatory fishes, including sharks. We tested for behavioural and physiological responses of blacktip reef shark (Carcharhinus melanopterus) neonates to climate change relevant changes in temperature (28 and 31 °C) and carbon dioxide partial pressures (pCO2; 650 and 1050 µatm) using a fully factorial design. Behavioural assays (lateralisation, activity level) were conducted upon 7–13 days of acclimation, and physiological assays (hypoxia tolerance, oxygen uptake rates, acid–base and haematological status) were conducted upon 14–17 days of acclimation. Haematocrit was higher in sharks acclimated to 31 °C than to 28 °C. Significant treatment effects were also detected for blood lactate and minimum oxygen uptake rate; although, these observations were not supported by adequate statistical power. Inter-individual variability was considerable for all measured traits, except for haematocrit. Moving forward, studies on similarly 'hard-to-study' species may account for large inter-individual variability by increasing replication, testing larger, yet ecologically relevant, differences in temperature and pCO2, and reducing measurement error. Robust experimental studies on elasmobranchs are critical to meaningfully assess the threat of global change stressors in these data-deficient species.