Diversification of refugia types needed to secure the future of coral reefs subject to climate change.

Identifying locations of refugia from the thermal stresses of climate change for coral reefs and better managing them is one of the key recommendations for climate change adaptation. We review and summarize approximately 30 years of applied research focused on identifying climate refugia to prioritize the conservation actions for coral reefs under rapid climate change. We found that currently proposed climate refugia and the locations predicted to avoid future coral losses are highly reliant on  excess heat metrics, such as degree heating weeks. However, many existing alternative environmental, ecological, and life-history variables could be used to identify other types of refugia that lead to the desired diversified portfolio for coral reef conservation. To improve conservation priorities for coral reefs, there is a need to evaluate and validate the predictions of climate refugia with long-term field data on coral abundance, diversity, and functioning. There is also the need to identify and safeguard locations displaying resistance toprolonged exposure to heat waves and the ability to recover quickly after thermal exposure. We recommend using more metrics to identify a portfolio of potential refugia sites for coral reefs that can avoid, resist, and recover from exposure to high ocean temperatures and the consequences of climate change, thereby shifting past efforts focused on avoidance to a diversified risk-spreading portfolio that can be used to improve strategic coral reef conservation in a rapidly warming climate.

Diversificación de los tipos de refugio necesarios para asegurar el futuro de los arrecifes de coral sujetos al cambio climático Resumen Una de las principales recomendaciones para la adaptación al cambio climático es identificar los refugios de los arrecifes de coral frente al estrés térmico del cambio climático y mejorar su gestión. Revisamos y resumimos ∼30 años de investigación aplicada centrada en la identificación de refugios climáticos para priorizar las acciones de conservación de los arrecifes de coral bajo un rápido cambio climático. Descubrimos que los refugios climáticos propuestos actualmente y las ubicaciones que pueden evitarlos dependen en gran medida de métricas de exceso de calor, como las semanas de calentamiento en grados (SCG). Sin embargo, existen muchas variables alternativas de historia vital, ambientales y ecológicas que podrían utilizarse para identificar otros tipos de refugios que resulten en el acervo diversificado que se desea para la conservación de los arrecifes de coral. Para mejorar las prioridades de conservación de los arrecifes de coral, es necesario evaluar y validar las predicciones sobre refugios climáticos con datos de campo a largo plazo sobre abundancia, diversidad y funcionamiento de los corales. También es necesario identificar y salvaguardar lugares que muestren resistencia a la exposición climática prolongada a olas de calor y la capacidad de recuperarse rápidamente tras la exposición térmica. Recomendamos utilizar más métricas para identificar un acervo de posibles lugares de refugio para los arrecifes de coral que puedan evitar, resistir y recuperarse de la exposición a las altas temperaturas oceánicas y las consecuencias del cambio climático, para así desplazar los esfuerzos pasados centrados en la evitación hacia un acervo diversificado de riesgos que pueda utilizarse para mejorar la conservación estratégica de los arrecifes de coral en un clima que se calienta rápidamente.

A spatial framework for improved sanitation to support coral reef conservation.

Coral reefs are one of the most valuable yet threatened ecosystems in the world. Improving human wastewater treatment could reduce land-based impacts on coral reefs. However, information on the quantity and spatial distribution of human wastewater pollution is lacking. Here, we develop a spatial model linking residential human wastewater pollution (nitrogen and phosphorus/year) and conservation sectors [coral reefs] to better understand the relative differences in the distribution and efficacy of different sanitation services and their potential implications for conservation monitoring and management. We apply our model to Fiji, where ongoing initiatives and investments in wastewater treatment for human health could be leveraged to cost-effectively improve coral reef condition. We estimate that wastewater treatment plants account for nearly 80% of human wastewater nutrients released into surface waters. Wasterwater nutrient pollution is widespread, affecting 95% of reefs, but is concentrated across a few watersheds. Our spatially explicit approach can be used to better understand potential benefits and trade-offs between sanitation service improvements and coral reef health, helping to bridge the sanitation and conservation sectors as well as inform and prioritize on the ground action.

Coastal urbanization influences human pathogens and microdebris contamination in seafood.

Seafood is one of the leading imported products implicated in foodborne outbreaks worldwide. Coastal marine environments are being increasingly subjected to reduced water quality from urbanization and leading to contamination of important fishery species. Given the importance of seafood exchanged as a global protein source, it is imperative to maintain seafood safety worldwide. To illustrate the potential health risks associated with urbanization in a coastal environment, we use next-generation high-throughput amplicon sequencing of the 16S ribosomal RNA gene combined with infrared spectroscopy to characterize and quantify a vast range of potential human bacterial pathogens and microdebris contaminants in seawater, sediment and an important oyster fishery along the Mergui Archipelago in Myanmar. Through the quantification of >1.25 million high-quality bacterial operational taxonomic unit (OTU) reads, we detected 5459 potential human bacterial pathogens belonging to 87 species that are commonly associated with gut microbiota and an indication of terrestrial runoff of human and agricultural waste. Oyster tissues contained 51% of all sequenced bacterial pathogens that are considered to be both detrimental and of emerging concern to human health. Using infrared spectroscopy, we examined a total of 1225 individual microdebris particles, from which we detected 78 different types of contaminant materials. The predominant microdebris contaminants recovered from oyster tissues included polymers (48%), followed by non-native minerals (20%), oils (14%) and milk supplement powders (14%). Emerging technologies provide novel insights into the impacts of coastal development on food security and risks to human and environmental health.

Climate Velocity Can Inform Conservation in a Warming World.

Climate change is shifting the ranges of species. Simple predictive metrics of range shifts such as climate velocity, that do not require extensive knowledge or data on individual species, could help to guide conservation. We review research on climate velocity, describing the theory underpinning the concept and its assumptions. We highlight how climate velocity has already been applied in conservation-related research, including climate residence time, climate refugia, endemism, historic and projected range shifts, exposure to climate change, and climate connectivity. Finally, we discuss ways to enhance the use of climate velocity in conservation through tailoring it to be more biologically meaningful, informing design of protected areas, conserving ocean biodiversity in 3D, and informing conservation actions.

Species-specific impacts of suspended sediments on gill structure and function in coral reef fishes.

Reduced water quality, in particular increases in suspended sediments, has been linked to declines in fish abundance on coral reefs. Changes in gill structure induced by suspended sediments have been hypothesized to impair gill function and may provide a mechanistic basis for the observed declines; yet, evidence for this is lacking. We exposed juveniles of three reef fish species (Amphiprion melanopus, Amphiprion percula and Acanthochromis polyacanthus) to suspended sediments (0-180 mg l-1) for 7 days and examined changes in gill structure and metabolic performance (i.e. oxygen consumption). Exposure to suspended sediments led to shorter gill lamellae in A. melanopus and A. polyacanthus and reduced oxygen diffusion distances in all three species. While A. melanopus exhibited impaired oxygen uptake after suspended sediment exposure, i.e. decreased maximum and increased resting oxygen consumption rates resulting in decreased aerobic scope, the oxygen consumption rates of the other two species remained unaffected. These findings imply that species sensitive to changes in gill structure such as A. melanopus may decline in abundance as reefs become more turbid, whereas species that are able to maintain metabolic performance despite suspended sediment exposure, such as A. polyacanthus or A. percula, may be able to persist or gain a competitive advantage.

The impact of individual and combined abiotic factors on daily otolith growth in a coral reef fish.

Coral reefs are increasingly subjected to both local and global stressors, however, there is limited information on how reef organisms respond to their combined effects under natural conditions. This field study examined the growth response of the damselfish Neopomacentrus bankieri to the individual and combined effects of multiple abiotic factors. Turbidity, temperature, tidal movement, and wave action were recorded every 10 minutes for four months, after which the daily otolith growth of N. bankieri was aligned with corresponding abiotic conditions. Temperature was the only significant driver of daily otolith increment width, with increasing temperatures resulting in decreasing width. Although tidal movement was not a significant driver of increment width by itself, the combined effect of tidal movement and temperature had a greater negative effect on growth than temperature alone. Our results indicate that temperature can drive changes in growth even at very fine scales, and demonstrate that the cumulative impact of abiotic factors can be substantially greater than individual effects. As abiotic factors continue to change in intensity and duration, the combined impacts of them will become increasingly important drivers of physiological and ecological change.

Reserves as tools for alleviating impacts of marine disease.

Marine protected areas can prevent over-exploitation, but their effect on marine diseases is less clear. We examined how marine reserves can reduce diseases affecting reef-building corals following acute and chronic disturbances. One year after a severe tropical cyclone, corals inside reserves had sevenfold lower levels of disease than those in non-reserves. Similarly, disease prevalence was threefold lower on reserve reefs following chronic exposure to terrestrial run-off from a degraded river catchment, when exposure duration was below the long-term site average. Examination of 35 predictor variables indicated that lower levels of derelict fishing line and injured corals inside reserves were correlated with lower levels of coral disease in both case studies, signifying that successful disease mitigation occurs when activities that damage reefs are restricted. Conversely, reserves were ineffective in moderating disease when sites were exposed to higher than average levels of run-off, demonstrating that reductions in water quality undermine resilience afforded by reserve protection. In addition to implementing protected areas, we highlight that disease management efforts should also target improving water quality and limiting anthropogenic activities that cause injury.

Effects of reduced water quality on coral reefs in and out of no-take marine reserves.

Near-shore marine environments are increasingly subjected to reduced water quality, and their ability to withstand it is critical to their persistence. The potential role marine reserves may play in mitigating the effects of reduced water quality has received little attention. We investigated the spatial and temporal variability in live coral and macro-algal cover and water quality during moderate and major flooding events of the Fitzroy River within the Keppel Bay region of the Great Barrier Reef Marine Park from 2007 to 2013. We used 7 years of remote sensing data on water quality and data from long-term monitoring of coral reefs to quantify exposure of coral reefs to flood plumes. We used a distance linear model to partition the contribution of abiotic and biotic factors, including zoning, as drivers of the observed changes in coral and macro-algae cover. Moderate flood plumes from 2007 to 2009 did not affect coral cover on reefs in the Keppel Islands, suggesting the reef has intrinsic resistance against short-term exposure to reduced water quality. However, from 2009 to 2013, live coral cover declined by ∼ 50% following several weeks of exposure to turbid, low salinity water from major flood plume events in 2011 and subsequent moderate events in 2012 and 2013. Although the flooding events in 2012 and 2013 were smaller than the flooding events between 2007 to 2009, the ability of the reefs to withstand these moderate floods was lost, as evidenced by a ∼ 20% decline in coral cover between 2011 to 2013. Although zoning (no-take reserve or fished) was identified a significant driver of coral cover, we recorded consistently lower coral cover on reserve reefs than on fished reefs throughout the study period and significantly lower cover in 2011. Our findings suggest that even reefs with an inherent resistance to reduced water quality are not able to withstand repeated disturbance events. The limitations of reserves in mitigating the effects of reduced water quality on near-shore coral reefs underscores the importance of integrated management approaches that combine effective land-based management with networks of no-take reserves.

Exposure of clownfish larvae to suspended sediment levels found on the Great Barrier Reef: Impacts on gill structure and microbiome.

Worldwide, increasing coastal development has played a major role in shaping coral reef species assemblages, but the mechanisms underpinning distribution patterns remain poorly understood. Recent research demonstrated delayed development in larval fishes exposed to suspended sediment, highlighting the need to further understand the interaction between suspended sediment as a stressor and energetically costly activities such as growth and development that are essential to support biological fitness. We examined the gill morphology and the gill microbiome in clownfish larvae (Amphiprion percula) exposed to suspended sediment concentrations (using Australian bentonite) commonly found on the inshore Great Barrier Reef. The gills of larvae exposed to 45 mg L(-1) of suspended sediment had excessive mucous discharge and growth of protective cell layers, resulting in a 56% thicker gill epithelium compared to fish from the control group. Further, we found a shift from 'healthy' to pathogenic bacterial communities on the gills, which could increase the disease susceptibility of larvae. The impact of suspended sediments on larval gills may represent an underlying mechanism behind the distribution patterns of fish assemblages. Our findings underscore the necessity for future coastal development to consider adverse effects of suspended sediments on fish recruitment, and consequently fish populations and ecosystem health.

Using MODIS data for mapping of water types within river plumes in the Great Barrier Reef, Australia: towards the production of river plume risk maps for reef and seagrass ecosystems.

River plumes are the major transport mechanism for nutrients, sediments and other land-based pollutants into the Great Barrier Reef (GBR, Australia) and are a major threat to coastal and marine ecosystems such as coral reefs and seagrass beds. Understanding the spatial extent, frequency of occurrence, loads and ecological impacts of land-based pollutants discharged through river plumes is essential to drive catchment management actions. In this study, a framework to produce river plume risk maps for seagrass and coral ecosystems, using supervised classification of MODIS Level 2 (L2) satellite products, is presented. Based on relevant L2 thresholds, river plumes are classified into Primary, Secondary, and Tertiary water types, which represent distinct water quality (WQ) parameters concentrations and combinations. Annual water type maps are produced over three wet seasons (2010-2013) as a case of study. These maps provide a synoptic basis to assess the likelihood and magnitude of the risk of reduced coastal WQ associated with the river discharge (river plume risk) and in combination with sound knowledge of the regional ecosystems can serve as the basis to assess potential ecological impacts for coastal and marine GBR ecosystems. The methods described herein provide relevant and easily reproducible large-scale information for river plume risk assessment and management.

Suspended sediment prolongs larval development in a coral reef fish.

Increasing sediment input into coastal environments is having a profound influence on shallow marine habitats and associated species. Coral reef ecosystems appear to be particularly sensitive, with increased sediment deposition and re-suspension being associated with declines in the abundance and diversity of coral reef fishes. While recent research has demonstrated that suspended sediment can have negative impacts on post-settlement coral reef fishes, its effect on larval development has not been investigated. In this study, we tested the effects of different levels of suspended sediment on larval growth and development time in Amphiprion percula, a coral reef damselfish. Larvae were subjected to four experimental concentrations of suspended sediment spanning the range found around coastal coral reefs (0-45 mg l(-1)). Larval duration was significantly longer in all sediment treatments (12 days) compared with the average larval duration in the control treatment (11 days). Approximately 75% of the fish in the control had settled by day 11, compared with only 40-46% among the sediment treatments. In the highest sediment treatment, some individuals had a larval duration twice that of the median duration in the control treatment. Unexpectedly, in the low sediment treatment, fish at settlement were significantly longer and heavier compared with fish in the other treatments, suggesting delayed development was independent of individual condition. A sediment-induced extension of the pelagic larval stage could significantly reduce numbers of larvae competent to settle and, in turn, have major effects on adult population dynamics.

Otx2 expression and implications for olfactory imprinting in the anemonefish, Amphiprion percula.

The otx2 gene encodes a transcription factor (OTX2) essential in the formation of the brain and sensory systems. Specifically, OTX2-positive cells are associated with axons in the olfactory system of mice and otx2 is upregulated in odour-exposed zebrafish, indicating a possible role in olfactory imprinting. In this study, otx2 was used as a candidate gene to investigate the molecular mechanisms of olfactory imprinting to settlement cues in the coral reef anemonefish, Amphiprion percula. The A. percula otx2 (Ap-otx2) gene was elucidated, validated, and its expression tested in settlement-stage A. percula by exposing them to behaviourally relevant olfactory settlement cues in the first 24 hours post-hatching, or daily throughout the larval phase. In-situ hybridisation revealed expression of Ap-otx2 throughout the olfactory epithelium with increased transcript staining in odour-exposed settlement-stage larval fish compared to no-odour controls, in all scenarios. This suggests that Ap-otx2 may be involved in olfactory imprinting to behaviourally relevant settlement odours in A. percula.

A novel approach to model exposure of coastal-marine ecosystems to riverine flood plumes based on remote sensing techniques.

Increased loads of land-based pollutants are a major threat to coastal-marine ecosystems. Identifying the affected marine areas and the scale of influence on ecosystems is critical to assess the impacts of degraded water quality and to inform planning for catchment management and marine conservation. Studies using remotely-sensed data have contributed to our understanding of the occurrence and influence of river plumes, and to our ability to assess exposure of marine ecosystems to land-based pollutants. However, refinement of plume modeling techniques is required to improve risk assessments. We developed a novel, complementary, approach to model exposure of coastal-marine ecosystems to land-based pollutants. We used supervised classification of MODIS-Aqua true-color satellite imagery to map the extent of plumes and to qualitatively assess the dispersal of pollutants in plumes. We used the Great Barrier Reef (GBR), the world's largest coral reef system, to test our approach. We combined frequency of plume occurrence with spatially distributed loads (based on a cost-distance function) to create maps of exposure to suspended sediment and dissolved inorganic nitrogen. We then compared annual exposure maps (2007-2011) to assess inter-annual variability in the exposure of coral reefs and seagrass beds to these pollutants. We found this method useful to map plumes and qualitatively assess exposure to land-based pollutants. We observed inter-annual variation in exposure of ecosystems to pollutants in the GBR, stressing the need to incorporate a temporal component into plume exposure/risk models. Our study contributes to our understanding of plume spatial-temporal dynamics of the GBR and offers a method that can also be applied to monitor exposure of coastal-marine ecosystems to plumes and explore their ecological influences.

Determining trigger values of suspended sediment for behavioral changes in a coral reef fish.

Sediment from land use increases water turbidity and threatens the health of inshore coral reefs. This study performed experiments with a damselfish, Pomacentrus moluccensis, in four sediment treatments, control (0 mg l⁻¹), 10 mg l⁻¹ (∼1.7 NTU), 20 mg l⁻¹ (∼3.3 NTU) and 30 mg l⁻¹ (∼5 NTU), to determine when sediment triggers a change in habitat use and movement. We reviewed the literature to assess how frequently P. moluccensis would experience sub-optimal sediment conditions on the reef. Preference for live coral declined from 49.4% to 23.3% and movement between habitats declined from 2.1 to 0.4 times between 20 mg l⁻¹ and 30 mg l⁻¹, suggesting a sediment threshold for behavioral changes. Inshore areas of the Great Barrier Reef, P. moluccensis may encounter sub-optimal conditions between 8% and 53% of the time. Changes in these vital processes may have long-term effects on the persistence of populations, particularly as habitat loss on coral reefs increases.

Climate change and the performance of larval coral reef fishes: the interaction between temperature and food availability.

Climate-change models predict that tropical ocean temperatures will increase by 2-3°C this century and affect plankton communities that are food for marine fish larvae. Both temperature and food supply can influence development time, growth, and metabolism of marine fishes, particularly during larval stages. However, little is known of the relative importance and potential interacting effects of ocean warming and changes to food supply on the performance of larval fishes. We tested this for larvae of the coral reef anemonefish, Amphiprion percula, in an orthogonal experiment comprising three temperatures and three feeding schedules. Temperatures were chosen to represent present-day summer averages (29.2°C) and end-of-century climate change projections of +1.5°C (30.7°C) and +3°C (32.2°C). Feeding schedules were chosen to represent a reduction in access to food (fed daily, every 2 days, or every 3 days). Overall, larvae took longer to settle at higher temperatures and with less frequent feeding, and there was a significant interaction between these factors. Time to metamorphosis was fastest in the 30.7(o)C and high food availability treatment (10.5 ± 0.2 days) and slowest in the 32.2(o)C and low food availability treatment (15.6 ± 0.5 days; i.e. 50% faster). Fish from the lower feeding regimens had a lower body condition and decreased survivorship to metamorphosis. Routine oxygen consumption rates were highest for fish raised at 32.2°C and fed every third day (162 ± 107 mg O2  kg(-1) h(-1)) and lowest for fish raised at 29.2°C and fed daily (122 ± 101 mg O2 kg(-1) h(-1); i.e. 35% lower). The elevated routine oxygen consumption rate, and therefore greater energy use at higher temperatures, may leave less energy available for growth and development, resulting in the longer time to metamorphosis. Overall, these results suggest that larval fishes will be severely impacted by climate-change scenarios that predict both elevated temperatures and reduced food supply.