• Energy Research

AbstractCoral reefs across the world have been seriously degraded and have a bleak future in response to predicted global warming and ocean acidification (OA). However, this is not the first time that biocalcifying organisms, including corals, have faced the threat of extinction. The end‐Triassic mass extinction (200 million years ago) was the most severe biotic crisis experienced by modern marine invertebrates, which selected against biocalcifiers; this was followed by the proliferation of another invertebrate group, sponges. The duration of this sponge‐dominated period far surpasses that of alternative stable‐ecosystem or phase‐shift states reported on modern day coral reefs and, as such, a shift to sponge‐dominated reefs warrants serious consideration as one future trajectory of coral reefs. We hypothesise that some coral reefs of today may become sponge reefs in the future, as sponges and corals respond differently to changing ocean chemistry and environmental conditions. To support this hypothesis, we discuss: (i) the presence of sponge reefs in the geological record; (ii) reported shifts from coral‐ to sponge‐dominated systems; and (iii) direct and indirect responses of the sponge holobiont and its constituent parts (host and symbionts) to changes in temperature andpH. Based on this evidence, we propose that sponges may be one group to benefit from projected climate change and ocean acidification scenarios, and that increased sponge abundance represents a possible future trajectory for some coral reefs, which would have important implications for overall reef functioning.

ABSTRACT Tropical lagoon-inhabiting organisms live in highly irradiated ecosystems and are particularly susceptible to thermal stress resulting from climate change. However, despite living close to their thermal maxima, stress response mechanisms found in these organisms are poorly understood. We used a novel physiological–proteomic approach for sponges to describe the stress response mechanisms of the lagoon-inhabiting sponge Amphimedon navalis, when exposed to elevated seawater temperatures of +2°C and +4°C relative to a 26°C ambient temperature for 4 weeks. After 4 weeks of thermal exposure, the buoyant weight of the sponge experienced a significant decline, while its pumping rates and oxygen consumption rates significantly increased. Proteome dynamics revealed 50 differentially abundant proteins in sponges exposed to elevated temperature, suggesting that shifts in the sponge proteome were potential drivers of physiological dysfunction. Thermal stress promoted an increase in detoxification proteins, such as catalase, suggesting that an excess of reactive oxygen species in sponge cells was responsible for the significant increase in oxygen consumption. Elevated temperature also disrupted cellular growth and cell proliferation, promoting the loss of sponge biomass, and the high abundance of multiple α-tubulin chain proteins also indicated an increase in cytoskeletal activities within sponge cells, which may have induced the increase in sponge pumping rate. Our results show that sustained thermal exposure in susceptible lagoonal sponges may induce significant disruption of cellular homeostasis, leading to physiological dysfunction, and that a combined physiological–proteomic approach may provide new insights into physiological functions and cellular processes occurring in sponges.

Marine heat waves (MHWs) are extended periods of excessively warm water1 that are increasing in frequency, duration, intensity, and impact, and they likely represent a greater threat to marine ecosystems than the more gradual increases in sea surface temperature.2,3,4 Sponges are major and important components of global benthic marine communities,5,6,7 with earlier studies identifying tropical sponges as potential climate change "winners."8,9,10,11 In contrast, cold-water sponges may be less tolerant to predicted ocean warming and concurrent MHWs. Here, we report how a series of unprecedented MHWs in New Zealand have impacted millions of sponges at a spatial scale far greater than previously reported anywhere in the world. We reported sponge tissue necrosis12 and bleaching (symbiont loss/dysfunction),13 which have been previously associated with temperature stress,6,12,14 for three common sponge species across multiple biogeographical regions, with the severity of impact being correlated with MHW intensity. Given the ecological importance of sponges,15 their loss from these rocky temperate reefs will likely have important ecosystem-level consequences.

AbstractSponges are major components of benthic communities across the world and have been identified as potential “winners” on coral reefs in the face of global climate change as result of their tolerance to ocean warming and acidification (OA). Previous studies have also hypothesised that photosymbiont‐containing sponges might have higher productivity under future OA conditions as a result of photosymbionts having increased access to CO2 and subsequently greater carbon production. Here we test this hypothesis for a widespread and abundant photosymbiont‐containing sponge species Lamellodysidea herbacea at a CO2 seep in Papua New Guinea simulating OA conditions. We found seep sponges had relatively higher cyanobacterial abundance, chlorophyll concentrations and symbiont photosynthetic efficiency than non‐seep sponges, and a three‐fold higher sponge abundance at the seep site. However, while gross oxygen production was the same for seep and non‐seep sponges, seep sponge dark respiration rates were higher and instantaneous photosynthesis: respiration (P:R) ratios were lower. We show that while photosymbiont containing sponges may not have increased productivity under OA, they are able to show flexibility in their relationships with microbes and offset increased metabolic costs associated with climate change associated stress.

AbstractOcean warming (OW) and ocean acidification (OA) are threatening coral reef ecosystems, with a bleak future forecast for reef‐building corals, which are already experiencing global declines in abundance. In contrast, many coral reef sponge species are able to tolerate climate change conditions projected for 2100. To increase our understanding of the mechanisms underpinning this tolerance, we explored the lipid and fatty acid (FA) composition of four sponge species with differing sensitivities to climate change, experimentally exposed to OW and OA levels predicted for 2100, under two CO2 Representative Concentration Pathways. Sponges with greater concentrations of storage lipid, phospholipids, sterols and elevated concentrations of n‐3 and n‐6 long‐chain polyunsaturated FA (LC PUFA), were more resistant to OW. Such biochemical constituents likely contribute to the ability of these sponges to maintain membrane function and cell homeostasis in the face of environmental change. Our results suggest that n‐3 and n‐6 LC PUFA are important components of the sponge stress response potentially via chain elongation and the eicosanoid stress‐signalling pathways. The capacity for sponges to compositionally alter their membrane lipids in response to stress was also explored using a number of specific homeoviscous adaptation (HVA) indicators. This revealed a potential mechanism via which additional CO2 could facilitate the resistance of phototrophic sponges to thermal stress through an increased synthesis of membrane‐stabilizing sterols. Finally, OW induced an increase in FA unsaturation in phototrophic sponges but a decrease in heterotrophic species, providing support for a difference in the thermal response pathway between the sponge host and the associated photosymbionts. Here we have shown that sponge lipids and FA are likely to be an important component of the sponge stress response and may play a role in facilitating sponge survival under future climate conditions.

AbstractAs atmospheric CO2 concentrations rise, associated ocean warming (OW) and ocean acidification (OA) are predicted to cause declines in reef‐building corals globally, shifting reefs from coral‐dominated systems to those dominated by less sensitive species. Sponges are important structural and functional components of coral reef ecosystems, but despite increasing field‐based evidence that sponges may be ‘winners’ in response to environmental degradation, our understanding of how they respond to the combined effects of OW and OA is limited. To determine the tolerance of adult sponges to climate change, four abundant Great Barrier Reef species were experimentally exposed to OW and OA levels predicted for 2100, under two CO2 Representative Concentration Pathways (RCPs). The impact of OW and OA on early life‐history stages was also assessed for one of these species to provide a more holistic view of species impacts. All species were generally unaffected by conditions predicted under RCP6.0, although environmental conditions projected under RCP8.5 caused significant adverse effects: with elevated temperature decreasing the survival of all species, increasing levels of tissue necrosis and bleaching, elevating respiration rates and decreasing photosynthetic rates. OA alone had little adverse effect, even under RCP8.5 concentrations. Importantly, the interactive effect of OW and OA varied between species with different nutritional modes, with elevated pCO2 exacerbating temperature stress in heterotrophic species but mitigating temperature stress in phototrophic species. This antagonistic interaction was reflected by reduced mortality, necrosis and bleaching of phototrophic species in the highest OW/OA treatment. Survival and settlement success of Carteriospongia foliascens larvae were unaffected by experimental treatments, and juvenile sponges exhibited greater tolerance to OW than their adult counterparts. With elevated pCO2 providing phototrophic species with protection from elevated temperature, across different life stages, climate change may ultimately drive a shift in the composition of sponge assemblages towards a dominance of phototrophic species.

AbstractOcean deoxygenation is one of the major consequences of climate change. In coastal waters, this process can be exacerbated by eutrophication, which is contributing to an alarming increase in the so‐called ‘dead zones’ globally. Despite its severity, the effect of reduced dissolved oxygen has only been studied for a very limited number of organisms, compared to other climate change impacts such as ocean acidification and warming. Here, we experimentally assessed the response of sponges to moderate and severe simulated hypoxic events. We ran three laboratory experiments on four species from two different temperate oceans (NE Atlantic and SW Pacific). Sponges were exposed to a total of five hypoxic treatments, with increasing severity (3.3, 1.6, 0.5, 0.4 and 0.13 mg O2 L−1, over 7–12‐days). We found that sponges are generally very tolerant of hypoxia. All the sponges survived in the experimental conditions, except Polymastia crocea, which showed significant mortality at the lowest oxygen concentration (0.13 mg O2 L−1, lethal median time: 286 h). In all species except Suberites carnosus, hypoxic conditions do not significantly affect respiration rate down to 0.4 mg O2 L−1, showing that sponges can uptake oxygen at very low concentrations in the surrounding environment. Importantly, sponges displayed species‐specific phenotypic modifications in response to the hypoxic treatments, including physiological, morphological and behavioural changes. This phenotypic plasticity likely represents an adaptive strategy to live in reduced or low oxygen water. Our results also show that a single sponge species (i.e., Suberites australiensis) can display different strategies at different oxygen concentrations. Compared to other sessile organisms, sponges generally showed higher tolerance to hypoxia, suggesting that sponges could be favoured and survive in future deoxygenated oceans.