Bleaching and mortality of a photosymbiotic bioeroding sponge under future carbon dioxide emission scenarios.

The bioeroding sponge Cliona orientalis is photosymbiotic with dinoflagellates of the genus Symbiodinium and is pervasive on the Great Barrier Reef. We investigated how C. orientalis responded to past and future ocean conditions in a simulated community setting. The experiment lasted over an Austral summer under four carbon dioxide emission scenarios: a pre-industrial scenario (PI), a present-day scenario (PD; control), and two future scenarios of combined ocean acidification and ocean warming, i.e., B1 (intermediate) and A1FI (extreme). The four scenarios also simulated natural variability of carbon dioxide partial pressure and temperature in seawater. Responses of C. orientalis generally remained similar between the PI and PD treatments. C. orientalis under B1 displayed a dramatic increase in lateral tissue extension, but bleached and displayed reduced rates of respiration and photosynthesis. Some B1 sponge replicates died by the end of the experiment. Under A1FI, strong bleaching and subsequent mortality of all C. orientalis replicates occurred at an early stage of the experiment. Mortality arrested bioerosion by C. orientalis under B1 and A1FI. Overall, the absolute amount of calcium carbonate eroded by C. orientalis under B1 or A1FI was similar to that under PI or PD at the end of the experiment. Although bioerosion rates were raised by short-term experimental acidification in previous studies, our findings from the photosymbiotic C. orientalis imply that the effects of bioerosion on reef carbonate budgets may only be temporary if the bioeroders cannot survive long-term in the future oceans.

Sponge bioerosion on changing reefs: ocean warming poses physiological constraints to the success of a photosymbiotic excavating sponge.

Excavating sponges are prominent bioeroders on coral reefs that in comparison to other benthic organisms may suffer less or may even benefit from warmer, more acidic and more eutrophic waters. Here, the photosymbiotic excavating sponge Cliona orientalis from the Great Barrier Reef was subjected to a prolonged simulation of both global and local environmental change: future seawater temperature, partial pressure of carbon dioxide (as for 2100 summer conditions under "business-as-usual" emissions), and diet supplementation with particulate organics. The individual and combined effects of the three factors on the bioerosion rates, metabolic oxygen and carbon flux, biomass change and survival of the sponge were monitored over the height of summer. Diet supplementation accelerated bioerosion rates. Acidification alone did not have a strong effect on total bioerosion or survival rates, yet it co-occurred with reduced heterotrophy. Warming above 30 °C (+2.7 °C above the local maximum monthly mean) caused extensive bleaching, lower bioerosion, and prevailing mortality, overriding the other factors and suggesting a strong metabolic dependence of the sponge on its resident symbionts. The growth, bioerosion capacity and likelihood of survival of C. orientalis and similar photosymbiotic excavating sponges could be substantially reduced rather than increased on end-of-the-century reefs under "business-as-usual" emission profiles.

Asymmetric competition prevents the outbreak of an opportunistic species after coral reef degradation.

Disturbance releases space and allows the growth of opportunistic species, excluded by the old stands, with a potential to alter community dynamics. In coral reefs, abundances of fast-growing, and disturbance-tolerant sponges are expected to increase and dominate as space becomes available following acute coral mortality events. Yet, an increase in abundance of these opportunistic species has been reported in only a few studies, suggesting certain mechanisms may be acting to regulate sponge populations. To gain insights into mechanisms of population control, we simulated the dynamics of the common reef-excavating sponge Cliona tenuis in the Caribbean using an individual-based model. An orthogonal hypothesis testing approach was used, where four candidate mechanisms-algal competition, stock-recruitment limitation, whole and partial mortality-were incorporated sequentially into the model and the results were tested against independent field observations taken over a decade in Belize, Central America. We found that releasing space after coral mortality can promote C. tenuis outbreaks, but such outbreaks can be curtailed by macroalgal competition. The asymmetrical competitive superiority of macroalgae, given by their capacity to pre-empt space and outcompete with the sponge in a size-dependant fashion, supports their capacity to steal the opportunity from other opportunists. While multiple system stages can be expected in coral reefs following intense perturbation macroalgae may prevent the growth of other space-occupiers, such as bioeroding sponges, under low grazing pressure.

A Standardised Vocabulary for Identifying Benthic Biota and Substrata from Underwater Imagery: The CATAMI Classification Scheme.

Imagery collected by still and video cameras is an increasingly important tool for minimal impact, repeatable observations in the marine environment. Data generated from imagery includes identification, annotation and quantification of biological subjects and environmental features within an image. To be long-lived and useful beyond their project-specific initial purpose, and to maximize their utility across studies and disciplines, marine imagery data should use a standardised vocabulary of defined terms. This would enable the compilation of regional, national and/or global data sets from multiple sources, contributing to broad-scale management studies and development of automated annotation algorithms. The classification scheme developed under the Collaborative and Automated Tools for Analysis of Marine Imagery (CATAMI) project provides such a vocabulary. The CATAMI classification scheme introduces Australian-wide acknowledged, standardised terminology for annotating benthic substrates and biota in marine imagery. It combines coarse-level taxonomy and morphology, and is a flexible, hierarchical classification that bridges the gap between habitat/biotope characterisation and taxonomy, acknowledging limitations when describing biological taxa through imagery. It is fully described, documented, and maintained through curated online databases, and can be applied across benthic image collection methods, annotation platforms and scoring methods. Following release in 2013, the CATAMI classification scheme was taken up by a wide variety of users, including government, academia and industry. This rapid acceptance highlights the scheme's utility and the potential to facilitate broad-scale multidisciplinary studies of marine ecosystems when applied globally. Here we present the CATAMI classification scheme, describe its conception and features, and discuss its utility and the opportunities as well as challenges arising from its use.

Effects of ocean warming and acidification on the energy budget of an excavating sponge.

Recent research efforts have demonstrated increased bioerosion rates under experimentally elevated partial pressures of seawater carbon dioxide (pCO2 ) with or without increased temperatures, which may lead to net erosion on coral reefs in the future. However, this conclusion clearly depends on the ability of the investigated bioeroding organisms to survive and grow in the warmer and more acidic future environments, which remains unexplored. The excavating sponge Cliona orientalis Thiele, is a widely distributed bioeroding organism and symbiotic with dinoflagellates of the genus Symbiodinium. Using C. orientalis, an energy budget model was developed to calculate amounts of carbon directed into metabolic maintenance and growth. This model was tested under a range of CO2 emission scenarios (temperature + pCO2 ) appropriate to an Austral early summer. Under a pre-industrial scenario, present day (control) scenario, or B1 future scenario (associated with reducing the rate of CO2 emissions over the next few decades), C. orientalis maintained a positive energy budget, where metabolic demand was likely satisfied by autotrophic carbon provided by Symbiodinium and heterotrophic carbon via filter-feeding, suggesting sustainability. Under B1, C. orientalis likely benefited by a greater supply of photosynthetic products from its symbionts, which increased by up to 56% per unit area, and displayed an improved condition with up to 52% increased surplus carbon available for growth. Under an A1FI future scenario (associated with 'business-as-usual' CO2 emissions) bleached C. orientalis experienced the highest metabolic demand, but carbon acquired was insufficient to maintain the sponge, as indicated by a negative energy budget. These metabolic considerations suggest that previous observations of increased bioerosion under A1FI by C. orientalis may not last through the height of future A1FI summers, and survival of individual sponges may be dependent on the energy reserves (biomass) they have accumulated through the rest of the year.

Sponge biomass and bioerosion rates increase under ocean warming and acidification.

The combination of ocean warming and acidification as a result of increasing atmospheric carbon dioxide (CO2 ) is considered to be a significant threat to calcifying organisms and their activities on coral reefs. How these global changes impact the important roles of decalcifying organisms (bioeroders) in the regulation of carbonate budgets, however, is less understood. To address this important question, the effects of a range of past, present and future CO2 emission scenarios (temperature + acidification) on the excavating sponge Cliona orientalis Thiele, 1900 were explored over 12 weeks in early summer on the southern Great Barrier Reef. C. orientalis is a widely distributed bioeroder on many reefs, and hosts symbiotic dinoflagellates of the genus Symbiodinium. Our results showed that biomass production and bioerosion rates of C. orientalis were similar under a pre-industrial scenario and a present day (control) scenario. Symbiodinium population density in the sponge tissue was the highest under the pre-industrial scenario, and decreased towards the two future scenarios with sponge replicates under the 'business-as-usual' CO2 emission scenario exhibiting strong bleaching. Despite these changes, biomass production and the ability of the sponge to erode coral carbonate materials both increased under the future scenarios. Our study suggests that C. orientalis will likely grow faster and have higher bioerosion rates in a high CO2 future than at present, even with significant bleaching. Assuming that our findings hold for excavating sponges in general, increased sponge biomass coupled with accelerated bioerosion may push coral reefs towards net erosion and negative carbonate budgets in the future.

Avoiding coral reef functional collapse requires local and global action.

Coral reefs face multiple anthropogenic threats, from pollution and overfishing to the dual effects of greenhouse gas emissions: rising sea temperature and ocean acidification. While the abundance of coral has declined in recent decades, the implications for humanity are difficult to quantify because they depend on ecosystem function rather than the corals themselves. Most reef functions and ecosystem services are founded on the ability of reefs to maintain their three-dimensional structure through net carbonate accumulation. Coral growth only constitutes part of a reef's carbonate budget; bioerosion processes are influential in determining the balance between net structural growth and disintegration. Here, we combine ecological models with carbonate budgets and drive the dynamics of Caribbean reefs with the latest generation of climate models. Budget reconstructions using documented ecological perturbations drive shallow (6-10 m) Caribbean forereefs toward an increasingly fragile carbonate balance. We then projected carbonate budgets toward 2080 and contrasted the benefits of local conservation and global action on climate change. Local management of fisheries (specifically, no-take marine reserves) and the watershed can delay reef loss by at least a decade under "business-as-usual" rises in greenhouse gas emissions. However, local action must be combined with a low-carbon economy to prevent degradation of reef structures and associated ecosystem services.

Ocean acidification accelerates reef bioerosion.

In the recent discussion how biotic systems may react to ocean acidification caused by the rapid rise in carbon dioxide partial pressure (pCO(2)) in the marine realm, substantial research is devoted to calcifiers such as stony corals. The antagonistic process - biologically induced carbonate dissolution via bioerosion - has largely been neglected. Unlike skeletal growth, we expect bioerosion by chemical means to be facilitated in a high-CO(2) world. This study focuses on one of the most detrimental bioeroders, the sponge Cliona orientalis, which attacks and kills live corals on Australia's Great Barrier Reef. Experimental exposure to lowered and elevated levels of pCO(2) confirms a significant enforcement of the sponges' bioerosion capacity with increasing pCO(2) under more acidic conditions. Considering the substantial contribution of sponges to carbonate bioerosion, this finding implies that tropical reef ecosystems are facing the combined effects of weakened coral calcification and accelerated bioerosion, resulting in critical pressure on the dynamic balance between biogenic carbonate build-up and degradation.