With rising anthropogenic carbon dioxide (CO2) emissions, ocean warming and acidification cooccur, and are predicted to impact calcifying organisms on coral reefs. However, decalcifying (i.e. bioeroding) organisms have largely been ignored in this context, despite their significant roles in regulating the carbonate budget of coral reefs. In particular, excavating sponges are often the most important internal macro-bioeroders on coral reefs, but they are understudied, partly due to their endolithic life style, and their complex composition of organic matter, siliceous spicules, salts and host calcareous substrate, and in some cases, microbial symbionts. Separation and quantification of these materials are required to answer key questions, but this is technically difficult. The first part of this study aimed to develop methodologies to quantify different components of the excavating sponge Cliona orientalis Thiele, 1900, which is widely distributed on many reefs and has symbiotic dinoflagellates of the genus Symbiodinium. Two distinct methodologies were derived: the loss after combustion (LAC) method and the acid decalcification (ADC) method. The LAC method showed low variability of data and was found to be simple and fast, and is therefore recommended. Due to the handling involved in the ADC method, more than half of the spicules were lost, suggesting that the ADC method requires careful data corrections. Moreover, the buoyant weight (BW) method, which assumes no weight contribution from organic components, was evaluated to be at least 97% effective to quantify actual substrate weight in the coral samples infested by C. orientalis, revealing that BW can potentially be used to quantify bioerosion by excavating sponges.
Using the methods developed in the first part, the second part of this study aimed to determine the combined effects of ocean warming and acidification on biomass and bioerosion rates of C. orientalis. The obtained results were supported by energy budgets calculated for the same sponge samples, and which are reported in the third part of this study. Experiments were performed in the ocean temperature and acidification simulation system on Heron Island, the southern Great Barrier Reef over twelve weeks in the Austral spring and early summer. Four CO2 emission scenarios were performed as offsets from ambient reef measurements of temperature and CO2 partial pressure (pCO2). Under a pre-industrial scenario (PI; lowered temperature and pCO2) and a present day scenario (PD; control), biomass and energy budgets were similar in C. orientalis, in which daily metabolic demands for carbon were likely to be satisfied by autotrophic carbon provided by Symbiodinium and heterotrophic carbon via filter-feeding. Under a B1 future scenario (future ocean temperature and pCO2 profiles associated with reduced CO2 emissions), C. orientalis apparently developed an improved condition among all tested scenarios. Lower mitotic rate and higher photosynthetic rate per cell were determined in B1 Symbiodinium that on average maintained a larger cell diameter. Although the cell number of Symbiodinium slightly decreased, overall autotrophic carbon supply to the B1 host sponge increased. After satisfying carbon demand for daily metabolism, surplus carbon increased by up to 77%, which was apparently used for growth, as evidenced by the highest biomass production rate in C. orientalis under the B1 scenario.
Under an A1FI future scenario (highly elevated temperature and pCO2 compatible with a ʻbusiness-as-usualʼ CO2 emission scenario), average population density of Symbiodinium was reduced by > 99% in C. orientalis, which was hence significantly bleached. Autotrophic carbon supply appeared to be terminated but net uptake of heterotrophic carbon did not increase to offset the energy loss, leading to a negative energy budget. However, greater biomass was still found in the bleached C. orientalis compared to PI and PD, probably due to the initial stimulation of growth in spring under A1FI, before bleaching. Moreover, the reduced biomass compared to B1 suggested that, after bleaching, the A1FI sponge might consume carbon from body reserves to maintain its metabolism and to survive, which is potentially unsustainable and the bleached C. orientalis may not survive through the height of the A1FI summers. Nevertheless, the clearly upward trend of bioerosion through chemical etching from PI to A1FI revealed that bioerosion by C. orientalis, even if bleached, could be facilitated by higher temperature and pCO2 in seawater. Assuming that our findings hold for other excavating sponges symbiotic with Symbiodinium spp., as long as they are not bleached, higher energy budgets, faster growth and accelerated bioerosion rates of the sponges under ocean warming and acidification may push coral reefs further towards net erosion.