Carbon dioxide addition to coral reef waters suppresses net community calcification.

Coral reefs feed millions of people worldwide, provide coastal protection and generate billions of dollars annually in tourism revenue. The underlying architecture of a reef is a biogenic carbonate structure that accretes over many years of active biomineralization by calcifying organisms, including corals and algae. Ocean acidification poses a chronic threat to coral reefs by reducing the saturation state of the aragonite mineral of which coral skeletons are primarily composed, and lowering the concentration of carbonate ions required to maintain the carbonate reef. Reduced calcification, coupled with increased bioerosion and dissolution, may drive reefs into a state of net loss this century. Our ability to predict changes in ecosystem function and associated services ultimately hinges on our understanding of community- and ecosystem-scale responses. Past research has primarily focused on the responses of individual species rather than evaluating more complex, community-level responses. Here we use an in situ carbon dioxide enrichment experiment to quantify the net calcification response of a coral reef flat to acidification. We present an estimate of community-scale calcification sensitivity to ocean acidification that is, to our knowledge, the first to be based on a controlled experiment in the natural environment. This estimate provides evidence that near-future reductions in the aragonite saturation state will compromise the ecosystem function of coral reefs.

Functional and phylogenetic responses of motile cryptofauna to habitat degradation.

Biodiversity of terrestrial and marine ecosystems, including coral reefs, is dominated by small, often cryptic, invertebrate taxa that play important roles in ecosystem structure and functioning. While cryptofauna community structure is determined by strong small-scale microhabitat associations, the extent to which ecological and environmental factors shape these communities are largely unknown, as is the relative importance of particular microhabitats in supporting reef trophodynamics from the bottom up. The goal of this study was to address these knowledge gaps, provided coral reefs are increasingly exposed to multiple disturbances and environmental gradients that influence habitat complexity, condition and ecosystem functioning. We compared the density, biomass, size range, phylogenetic diversity and functional roles of motile cryptofauna in Palau, Western Micronesia, among four coral-derived microhabitats representing various states of degradation (live coral [Acropora and Pocillopora], dead coral and coral rubble) from reefs along a gradient of effluent exposure. In total, 122 families across ten phyla were identified, dominated by the Arthropoda (Crustacea) and Mollusca. Cryptofauna biomass was greatest in live Pocillopora, while coral rubble contained the greatest density and diversity. Size ranges were broader in live corals than both dead coral and rubble. From a bottom-up perspective, effluent exposure had mixed effects on cryptic communities including a decline in total biomass in rubble. From a top-down perspective, cryptofauna were generally unaffected by predator biomass. Our data show that, as coral reef ecosystems continue to decline in response to more frequent and severe disturbances, habitats other than live coral may become increasingly important in supporting coral reef biodiversity and food webs.

Reversal of ocean acidification enhances net coral reef calcification.

Approximately one-quarter of the anthropogenic carbon dioxide released into the atmosphere each year is absorbed by the global oceans, causing measurable declines in surface ocean pH, carbonate ion concentration ([CO3(2-)]), and saturation state of carbonate minerals (Ω). This process, referred to as ocean acidification, represents a major threat to marine ecosystems, in particular marine calcifiers such as oysters, crabs, and corals. Laboratory and field studies have shown that calcification rates of many organisms decrease with declining pH, [CO3(2-)], and Ω. Coral reefs are widely regarded as one of the most vulnerable marine ecosystems to ocean acidification, in part because the very architecture of the ecosystem is reliant on carbonate-secreting organisms. Acidification-induced reductions in calcification are projected to shift coral reefs from a state of net accretion to one of net dissolution this century. While retrospective studies show large-scale declines in coral, and community, calcification over recent decades, determining the contribution of ocean acidification to these changes is difficult, if not impossible, owing to the confounding effects of other environmental factors such as temperature. Here we quantify the net calcification response of a coral reef flat to alkalinity enrichment, and show that, when ocean chemistry is restored closer to pre-industrial conditions, net community calcification increases. In providing results from the first seawater chemistry manipulation experiment of a natural coral reef community, we provide evidence that net community calcification is depressed compared with values expected for pre-industrial conditions, indicating that ocean acidification may already be impairing coral reef growth.

Characterizing biogeochemical fluctuations in a world of extremes: A synthesis for temperate intertidal habitats in the face of global change.

Coastal and intertidal habitats are at the forefront of anthropogenic influence and environmental change. The species occupying these habitats are adapted to a world of extremes, which may render them robust to the changing climate or more vulnerable if they are at their physiological limits. We characterized the diurnal, seasonal and interannual patterns of flux in biogeochemistry across an intertidal gradient on a temperate sandstone platform in eastern Australia over 6 years (2009-2015) and present a synthesis of our current understanding of this habitat in context with global change. We used rock pools as natural mesocosms to determine biogeochemistry dynamics and patterns of eco-stress experienced by resident biota. In situ measurements and discrete water samples were collected night and day during neap low tide events to capture diurnal biogeochemistry cycles. Calculation of pHT using total alkalinity (TA) and dissolved inorganic carbon (DIC) revealed that the mid-intertidal habitat exhibited the greatest flux over the years (pHT 7.52-8.87), and over a single tidal cycle (1.11 pHT units), while the low-intertidal (pHT 7.82-8.30) and subtidal (pHT 7.87-8.30) were less variable. Temperature flux was also greatest in the mid-intertidal (8.0-34.5°C) and over a single tidal event (14°C range), as typical of temperate rocky shores. Mean TA and DIC increased at night and decreased during the day, with the most extreme conditions measured in the mid-intertidal owing to prolonged emersion periods. Temporal sampling revealed that net ecosystem calcification and production were highest during the day and lowest at night, particularly in the mid-intertidal. Characterization of biogeochemical fluctuations in a world of extremes demonstrates the variable conditions that intertidal biota routinely experience and highlight potential microhabitat-specific vulnerabilities and climate change refugia.

Altered sediment biota and lagoon habitat carbonate dynamics due to sea cucumber bioturbation in a high-pCO2 environment.

The effects of global change on biological systems and functioning are already measurable, but how ecological interactions are being altered is poorly understood. Ecosystem resilience is strengthened by ecological functionality, which depends on trophic interactions between key species and resilience generated through biogenic buffering. Climate-driven alterations to coral reef metabolism, structural complexity and biodiversity are well documented, but the feedbacks between ocean change and trophic interactions of non-coral invertebrates are understudied. Sea cucumbers, some of the largest benthic inhabitants of tropical lagoon systems, can influence diel changes in reef carbonate dynamics. Whether they have the potential to exacerbate or buffer ocean acidification over diel cycles depends on their relative production of total alkalinity (AT ) through the dissolution of ingested calcium carbonate (CaCO3 ) sediments and release of dissolved inorganic carbon (CT ) through respiration and trophic interactions. In this study, the potential for the sea cucumber, Stichopus herrmanni, a bêche-de-mer (fished) species listed as vulnerable to extinction, to buffer the impacts of ocean acidification on reef carbonate chemistry was investigated in lagoon sediment mesocosms across diel cycles. Stichopus herrmanni directly reduced the abundance of meiofauna and benthic primary producers through its deposit-feeding activity under present-day and near-future pCO2 . These changes in benthic community structure, as well as AT (sediment dissolution) and CT (respiration) production by S. herrmanni, played a significant role in modifying seawater carbonate dynamics night and day. This previously unappreciated role of tropical sea cucumbers, in support of ecosystem resilience in the face of global change, is an important consideration with respect to the bêche-de-mer trade to ensure sea cucumber populations are sustained in a future ocean.

From pole to pole: the potential for the Arctic seastar Asterias amurensis to invade a warming Southern Ocean.

Due to climatic warming, Asterias amurensis, a keystone boreal predatory seastar that has established extensive invasive populations in southern Australia, is a potential high-risk invader of the sub-Antarctic and Antarctic. To assess the potential range expansion of A. amurensis to the Southern Ocean as it warms, we investigated the bioclimatic envelope of the adult and larval life stages. We analysed the distribution of adult A. amurensis with respect to present-day and future climate scenarios using habitat temperature data to construct species distribution models (SDMs). To integrate the physiological response of the dispersive phase, we determined the thermal envelope of larval development to assess their performance in present-day and future thermal regimes and the potential for success of A. amurensis in poleward latitudes. The SDM indicated that the thermal 'niche' of the adult stage correlates with a 0-17 °C and 1-22.5 °C range, in winter and summer, respectively. As the ocean warms, the range of A. amurensis in Australia will contract, while more southern latitudes will have conditions favourable for range expansion. Successful fertilization occurred from 3 to 23.8 °C. By day 12, development to the early larval stage was successful from 5.5 to 18 °C. Although embryos were able to reach the blastula stage at 2 °C, they had arrested development and high mortality. The optimal thermal range for survival of pelagic stages was 3.5-19.2 °C with a lower and upper critical limit of 2.6 and 20.3 °C, respectively. Our data predict that A. amurensis faces demise in its current invasive range while more favourable conditions at higher latitudes would facilitate invasion of both larval and adult stages to the Southern Ocean. Our results show that vigilance is needed to reduce the risk that this ecologically important Arctic carnivore may invade the Southern Ocean and Antarctica.

Emigration patterns of motile cryptofauna and their implications for trophic functioning in coral reefs.

Patterns of movement of marine species can reflect strategies of reproduction and dispersal, species' interactions, trophodynamics, and susceptibility to change, and thus critically inform how we manage populations and ecosystems. On coral reefs, the density and diversity of metazoan taxa are greatest in dead coral and rubble, which are suggested to fuel food webs from the bottom up. Yet, biomass and secondary productivity in rubble is predominantly available in some of the smallest individuals, limiting how accessible this energy is to higher trophic levels. We address the bioavailability of motile coral reef cryptofauna based on small-scale patterns of emigration in rubble. We deployed modified RUbble Biodiversity Samplers (RUBS) and emergence traps in a shallow rubble patch at Heron Island, Great Barrier Reef, to detect community-level differences in the directional influx of motile cryptofauna under five habitat accessibility regimes. The mean density (0.13-4.5 ind cm-3) and biomass (0.14-5.2 mg cm-3) of cryptofauna were high and varied depending on microhabitat accessibility. Emergent zooplankton represented a distinct community (dominated by the Appendicularia and Calanoida) with the lowest density and biomass, indicating constraints on nocturnal resource availability. Mean cryptofauna density and biomass were greatest when interstitial access within rubble was blocked, driven by the rapid proliferation of small harpacticoid copepods from the rubble surface, leading to trophic simplification. Individuals with high biomass (e.g., decapods, gobies, and echinoderms) were greatest when interstitial access within rubble was unrestricted. Treatments with a closed rubble surface did not differ from those completely open, suggesting that top-down predation does not diminish rubble-derived resources. Our results show that conspecific cues and species' interactions (e.g., competition and predation) within rubble are most critical in shaping ecological outcomes within the cryptobiome. These findings have implications for prey accessibility through trophic and community size structuring in rubble, which may become increasingly relevant as benthic reef complexity shifts in the Anthropocene.

Knowledge Gaps in the Biology, Ecology, and Management of the Pacific Crown-of-Thorns Sea Star Acanthaster sp. on Australia's Great Barrier Reef.

AbstractCrown-of-thorns sea stars (Acanthaster sp.) are among the most studied coral reef organisms, owing to their propensity to undergo major population irruptions, which contribute to significant coral loss and reef degradation throughout the Indo-Pacific. However, there are still important knowledge gaps pertaining to the biology, ecology, and management of Acanthaster sp. Renewed efforts to advance understanding and management of Pacific crown-of-thorns sea stars (Acanthaster sp.) on Australia's Great Barrier Reef require explicit consideration of relevant and tractable knowledge gaps. Drawing on established horizon scanning methodologies, this study identified contemporary knowledge gaps by asking active and/or established crown-of-thorns sea star researchers to pose critical research questions that they believe should be addressed to improve the understanding and management of crown-of-thorns sea stars on the Great Barrier Reef. A total of 38 participants proposed 246 independent research questions, organized into 7 themes: feeding ecology, demography, distribution and abundance, predation, settlement, management, and environmental change. Questions were further assigned to 48 specific topics nested within the 7 themes. During this process, redundant questions were removed, which reduced the total number of distinct research questions to 172. Research questions posed were mostly related to themes of demography (46 questions) and management (48 questions). The dominant topics, meanwhile, were the incidence of population irruptions (16 questions), feeding ecology of larval sea stars (15 questions), effects of elevated water temperature on crown-of-thorns sea stars (13 questions), and predation on juveniles (12 questions). While the breadth of questions suggests that there is considerable research needed to improve understanding and management of crown-of-thorns sea stars on the Great Barrier Reef, the predominance of certain themes and topics suggests a major focus for new research while also providing a roadmap to guide future research efforts.

Resilience to the interactive effects of climate change and discard stress in the commercially important blue swimmer crab (Portunus armatus).

Globally, millions of people depend on nutritional benefits from seafood consumption, but few studies have tested for effects of near-future climate change on seafood health and quality. Quantitative assessments of the interactive effects of climate change and discarding of fisheries resources are also lacking, despite ~10% of global catches being discarded annually. Utilising the harvested blue swimmer crab (Portunus armatus), we experimentally tested the effects of near-future temperature and salinity treatments under simulated capture and discarding on a suite of health and nutritional quality parameters. We show that nutritional quality (protein, lipids, moisture content and fatty acid composition) was not significantly affected by near-future climate change. Further, stress biomarkers (catalase and glutathione S-transferases activity and glycogen content) did not differ significantly among treatments following simulated capture and discarding. These results support the inherent resilience of P. armatus to short-term environmental change, and indicate that negative physiological responses associated with discarding may not be exacerbated in a future ocean. We suggest that harvested estuarine species, and thus the industries and food security they underpin, may be resilient to the future effects of climate change due to their adaptation to naturally variable habitats.

Spatial patterns of microbial communities across surface waters of the Great Barrier Reef.

Microorganisms are fundamental drivers of biogeochemical cycling, though their contribution to coral reef ecosystem functioning is poorly understood. Here, we infer predictors of bacterioplankton community dynamics across surface-waters of the Great Barrier Reef (GBR) through a meta-analysis, combining microbial with environmental data from the eReefs platform. Nutrient dynamics and temperature explained 41.4% of inter-seasonal and cross-shelf variation in bacterial assemblages. Bacterial families OCS155, Cryomorphaceae, Flavobacteriaceae, Synechococcaceae and Rhodobacteraceae dominated inshore reefs and their relative abundances positively correlated with nutrient loads. In contrast, Prochlorococcaceae negatively correlated with nutrients and became increasingly dominant towards outershelf reefs. Cyanobacteria in Prochlorococcaceae and Synechococcaceae families occupy complementary cross-shelf biogeochemical niches; their abundance ratios representing a potential indicator of GBR nutrient levels. One Flavobacteriaceae-affiliated taxa was putatively identified as diagnostic for ecosystem degradation. Establishing microbial observatories along GBR environmental gradients will facilitate robust assessments of microbial contributions to reef health and inform tipping-points in reef condition.

Preferences and perceptions of the recreational spearfishery of the Great Barrier Reef.

Recreational fishing practices can have significant impacts on marine ecosystems but their catch dynamics are often difficult to quantify, particularly for spearfishing. On coral reefs, the impacts of recreational spearfishing are often considered to be negligible compared to other practices, but the highly selective method adopted by spearfishers can result in locally distinct ecological consequences. Here we investigated the spatial patterns and catch composition of recreational spearfishers on the Great Barrier Reef using an online survey (n = 141 participants) targeted at spearfishers active along the coastline of Queensland. Observations from within the Queensland spearfishing community were also used to explore perceived changes in catches of three functionally distinct spearing targets. Preferred reef regions (coastal, inshore, offshore) differed among spearfishers from Bundaberg (south) to Cooktown (north). The piscivorous coral trout, Plectropomus leopardus, was suggested to be the preferred target comprising 34% (±1.5 SE) of spearfishers' reported catch composition. Spearfishers also noted a variety of changes in their catch composition over time, particularly regarding parrotfishes (decreased landings) and tuskfishes (increased landings). How this relates to the relative abundance and population biology of these taxa on the Great Barrier Reef requires attention. Spearfishers can provide important information regarding the status of their fishery through direct observations, which can inform legislation when acknowledged.

Superstars: Assessing nutrient thresholds for enhanced larval success of Acanthaster planci, a review of the evidence.

Crown-of-thorns starfish, Acanthaster planci (COTS), predation is a major cause of coral reef decline, but the factors behind their population outbreaks remain unclear. Increased phytoplankton food resulting from eutrophication is suggested to enhance larval survival. We addressed the hypothesis that larval success is associated with particular chl-a levels in tightly controlled larval:algal conditions. We used chl-a conditions found on coral reefs (0.1-5.0µgchl-aL-1), including nominal threshold levels for disproportionate larval success (≥1.0µgchl-aL-1). High success to the juvenile occurred across an order of magnitude of chl-a concentrations (0.5-5.0µgchl-aL-1), suggesting there may not be a narrow value for optimal success. Oligotrophic conditions (0.1µgchl-aL-1) appeared to be a critical limit. With a review of the evidence, we suggest that opportunistic COTS larvae may be more resilient to low food levels than previously appreciated. Initiation of outbreak populations need not require eutrophic conditions.

Larval starvation to satiation: influence of nutrient regime on the success of Acanthaster planci.

High density populations of the crown-of-thorns seastar, Acanthaster planci, are a major contributor to the decline of coral reefs, however the causes behind periodic outbreaks of this species are not understood. The enhanced nutrients hypothesis posits that pulses of enhanced larval food in eutrophic waters facilitate metamorphic success with a flow-on effect for population growth. The larval resilience hypothesis suggests that A. planci larvae naturally thrive in tropical oligotrophic waters. Both hypotheses remain to be tested empirically. We raised A. planci larvae in a range of food regimes from starvation (no food) to satiation (excess food). Algal cell concentration and chlorophyll levels were used to reflect phytoplankton conditions in nature for oligotrophic waters (0-100 cells ml(-1); 0-0.01 µg chl a L(-1)), natural background levels of nutrients on the Great Barrier Reef (GBR) (1,000-10,000 cells ml(-1); 0.1-1.0 µg chl a L(-1)), and enhanced eutrophic conditions following runoff events (100,000 cells ml(-1); 10 µg chl a L(-1)). We determine how these food levels affected larval growth and survival, and the metamorphic link between larval experience and juvenile quality (size) in experiments where food ration per larvae was carefully controlled. Phytoplankton levels of 1 µg chl a L(-1), close to background levels for some reefs on the GBR and following flood events, were optimal for larval success. Development was less successful above and below this food treatment. Enhanced larval performance at 1 µg chl a L(-1) provides empirical support for the enhanced nutrients hypothesis, but up to a limit, and emphasizes the need for appropriate mitigation strategies to reduce eutrophication and the consequent risk of A. planci outbreaks.

Effects of ocean warming and acidification on survival, growth and skeletal development in the early benthic juvenile sea urchin (Heliocidaris erythrogramma).

Co-occurring ocean warming, acidification and reduced carbonate mineral saturation have significant impacts on marine biota, especially calcifying organisms. The effects of these stressors on development and calcification in newly metamorphosed juveniles (ca. 0.5 mm test diameter) of the intertidal sea urchin Heliocidaris erythrogramma, an ecologically important species in temperate Australia, were investigated in context with present and projected future conditions. Habitat temperature and pH/pCO2 were documented to place experiments in a biologically and ecologically relevant context. These parameters fluctuated diurnally up to 10 °C and 0.45 pH units. The juveniles were exposed to three temperature (21, 23 and 25 °C) and four pH (8.1, 7.8, 7.6 and 7.4) treatments in all combinations, representing ambient sea surface conditions (21 °C, pH 8.1; pCO2 397; ΩCa 4.7; ΩAr 3.1), near-future projected change (+2-4 °C, -0.3-0.5 pH units; pCO2 400-1820; ΩCa 5.0-1.6; ΩAr 3.3-1.1), and extreme conditions experienced at low tide (+4 °C, -0.3-0.7 pH units; pCO2 2850-2967; ΩCa 1.1-1.0; ΩAr 0.7-0.6). The lowest pH treatment (pH 7.4) was used to assess tolerance levels. Juvenile survival and test growth were resilient to current and near-future warming and acidification. Spine development, however, was negatively affected by near-future increased temperature (+2-4 °C) and extreme acidification (pH 7.4), with a complex interaction between stressors. Near-future warming was the more significant stressor. Spine tips were dissolved in the pH 7.4 treatments. Adaptation to fluctuating temperature-pH conditions in the intertidal may convey resilience to juvenile H. erythrogramma to changing ocean conditions, however, ocean warming and acidification may shift baseline intertidal temperature and pH/pCO2 to levels that exceed tolerance limits.

Vulnerability of the paper Nautilus (Argonauta nodosa) shell to a climate-change ocean: potential for extinction by dissolution.

Shell calcification in argonauts is unique. Only females of these cephalopods construct the paper nautilus shell, which is used as a brood chamber for developing embryos in the pelagic realm. As one of the thinnest (225 µm) known adult mollusc shells, and lacking an outer protective periostracum-like cover, this shell may be susceptible to dissolution as the ocean warms and decreases in pH. Vulnerability of the A. nodosa shell was investigated through immersion of shell fragments in multifactorial experiments of control (19 °C/pH 8.1; pCO(2) 419; Ω(Ca) = 4.23) and near-future conditions (24 °C/pH 7.8-7.6; pCO(2) 932-1525; Ω(Ca) = 2.72-1.55) for 14 days. More extreme pH treatments (pH 7.4-7.2; pCO(2) 2454-3882; Ω(Ca) = 1.20-0.67) were used to assess tipping points in shell dissolution. X-ray diffractometry revealed no change in mineralogy between untreated and treated shells. Reduced shell weight due to dissolution was evident in shells incubated at pH 7.8 (projected for 2070) after 14 days at control temperature, with increased dissolution in warmer and lower pH treatments. The greatest dissolution was recorded at 24 °C (projected for local waters by 2100) compared to control temperature across all low-pH treatments. Scanning electron microscopy revealed dissolution and etching of shell mineral in experimental treatments. In the absence of compensatory mineralization, the uncovered female brood chamber will be susceptible to dissolution as ocean pH decreases. Since the shell was a crucial adaptation for the evolution of the argonauts' holopelagic existence, persistence of A. nodosa may be compromised by shell dissolution in an ocean-change world.