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Location map of Queensland, with Orpheus Island (Palm Island Group) on the central Great Barrier Reef (top). The sample site in Little Pioneer Bay is just north of the Orpheus Island Research Station (OIRS)
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Coral reefs are under threat, exerted by a number of interacting effects inherent to the present climate change, including ocean acidification and global warming. Bioerosion drives reef degradation by recycling carbonate skeletal material and is an important but understudied factor in this context. Twelve different combinations of pCO(2) and temper...
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... sampling and experimental procedures were conducted at Orpheus Island Research Station (OIRS), located on Orpheus Island, central Great Barrier Reef, Australia (Fig. 1). The local community of bio- eroding sponges is diverse, comparatively well stud- ied (e.g. Schönberg 2000Schönberg , 2001, and has recently in - creased in abundance, possibly as a result of declin- ing reef health related to a heating event resulting in widespread coral death (Schönberg & Ortiz 2009). At the leeward fringing reef, C. ...
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... 2009). At the leeward fringing reef, C. orientalis was core- sampled in 1 to 3 m water depth from massive Porites sp. colonies with an air-drill and hole-saw (inner dia - meter: 30 mm), and later trimmed to 25 mm in length with an air-cutter, so that cores included sponge- penetrated material in the upper half and clean coral skeleton below (see Fig. 1D in Wisshak et al. ...
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... salinity, pH, mean and Δ total alkalinity [TA]) and computed carbonate system parameters (dissolved inorganic carbon [DIC] Tables 2, S1 & S2), no clear relationship with tem - perature could be demonstrated, also evidenced by only few and weakly significant differences found when testing temperature levels pairwise against each other (Fig. 4j, Tables 2, S1 & S2). The weaker and somewhat inconclusive temperature effect was confirmed by the multiple linear re gressions yielding a clear significance for the factor p CO 2 and a neg - ligible contribution of temperature (Table S2). At any given p CO 2 level, bioerosion rates were highest at 25°C (approx. ambient winter temperature), and slightly de ...
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... of the ammonium building up. The highest bioerosion rates were reached at the local ambient temperature of 25°C, decreasing towards colder as well as warmer tem peratures. Overall, the influence of temperature on the bioerosion capacity of C. orientalis appears to be very low to negligible despite other physiological responses caused by heat (Fig. 4, Tables 1, 2, S1 & S2), particularly with respect to ammonium, that can be interpreted as a sign of excretion and/or disintegrative processes (Wright 1995, Francis-Floyd et al. 2009). The ob served signif- icant positive correlation of ammonium with temper- ature (Table 2) likely suggests increasing heat stress, with resulting ammonium and/or ...
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... to correct A T change (Jacques & Pilson, 1980;Wisshak et al., 2013) as ammonium, nitrate and phosphate are naturally modified by the rubble inhabitants and affect A T . The mass of altered calcium carbonate (ΔM CaCO 3 , in μg) was calculated using the equation below (Zundelevich et al., 2007): ...
As the balance between erosional and constructive processes on coral reefs tilts in favor of framework loss under human‐induced local and global change, many reef habitats worldwide degrade and flatten. The resultant generation of coral rubble and the beds they form can have lasting effects on reef communities and structural complexity, threatening the continuity of reef ecological functions and the services they provide. To comprehensively capture changing framework processes and predict their evolution in the context of climate change, heavily colonized rubble fragments were exposed to ocean acidification (OA) conditions for 55 days. Controlled diurnal pH oscillations were incorporated in the treatments to account for the known impact of diel carbonate chemistry fluctuations on calcification and dissolution response to OA. Scenarios included contemporary pH (8.05 ± 0.025 diel fluctuation), elevated OA (7.90 ± 0.025), and high OA (7.70 ± 0.025). We used a multifaceted approach, combining chemical flux analyses, mass alteration measurements, and computed tomography scanning images to measure total and chemical bioerosion, as well as chemically driven secondary calcification. Rates of net carbonate loss measured in the contemporary conditions (1.36 kg m ⁻² year ⁻¹ ) were high compared to literature and increased in OA scenarios (elevated: 1.84 kg m ⁻² year ⁻¹ and high: 1.59 kg m ⁻² year ⁻¹ ). The acceleration of these rates was driven by enhanced chemical dissolution and reduced secondary calcification. Further analysis revealed that the extent of these changes was contingent on the density of the coral skeleton, in which the micro‐ and macroborer communities reside. Findings indicated that increased mechanical bioerosion rates occurred in rubble with lower skeletal density, which is of note considering that corals form lower‐density skeletons under OA. These direct and indirect effects of OA on chemical and mechanical framework‐altering processes will influence the permanence of this crucial habitat, carrying implications for biodiversity and reef ecosystem function.
... Under undisturbed, natural conditions, bioerosion is an important mechanism of CaCO 3 recycling, especially in the case of shallow-water habitats such as coral and mollusk reefs (Schönberg et al., 2017). Bioerosion equals there or remains lower than local calcification, but some studies indicated that it could strongly increase under more acidic conditions and warm climatic conditions (e.g., Tribollet et al., 2009;Wisshak et al., 2013;see Schönberg et al., 2017 for a review). Warm water temperatures could make the substratum more bioerosion-susceptible (Davidson et al., 2018). ...
Bioerosion is rare in large benthic foraminifera (LBF) in the Eocene of Ziarat Formation. Three bioerosion ichnotaxa have been identified, including more common Trypanites isp. and Entobia isp., and rare Meandropolydora sulcans. The rare bioerosional traces in LBF tests support the scenario of an oligotrophic nutrient regime at the studied interval. The sedimentation rate may have also been among the controls on the bioerosion of LBF in the Middle Eocene of Iran, but the oligotrophic nutrient regime likely had a stronger effect. The bioerosion of LBF tests during the Middle Eocene Climatic Optimum (MECO) was rather low or at maximum moderate, suggesting that an oligotrophic nutrient regime could compensate for the increase in bioerosion caused by ocean acidification and warming.
... There are shared aspects in the mechanisms of bioerosion that suggest similarities in the forces that drive bioerosion and its ecological outcomes. Recent research has shown that bioerosion intensity increases in response to modern climate change and human-induced impacts, e.g., increased temperature, alkalinity, eutrophication and sea level rise (e.g., Tribollet et al., 2009;Wisshak et al., 2013;Silbiger et al., 2016;Chazottes et al., 2017;Prouty et al., 2017). ...
... Such experimental work can isolate response values per taxon group, as well as by ecophysiological environment and requirement, and can thereby quantify rates under different conditions. This is an established method to predict bioerosion rates under climate change scenarios and into the future, e.g., [78][79][80]. Experimentally derived bioerosion rates are also used in comparison to calcification rates to assess local carbonate budgets and whether respective habitats are still positively calcifying or slipping into an erosional, deteriorating state, e.g., [81,82]. Such data are further vital in modelling coral reef health, e.g., [7,[83][84][85]. ...
Coral reefs are in decline globally, resulting in changed constructive and destructive processes. The South China Sea is a marginal sea that is of high biological importance, but also subjected to extreme local and global pressures. Yet, the regional calcium carbonate dynamics are not well understood, especially bioerosion. A literature search for research on bioerosion and bioeroders in the South China Sea found only 31 publications on bioerosion-related research and 22 biodiversity checklists that contained bioeroders, thus generating a paltry bibliography. Bioerosion research in the South China Sea is still undeveloped and reached only two publications per year over the last few years. Hong Kong is the hotspot of activities as measured in output and diversity of methods, but the research in Hong Kong and elsewhere was strongly favoring field surveys of sea urchins over other bioeroders. Overall, macroborers received almost equal attention as grazer-eroders, but interest in microborers was low. Almost 90% of the research was conducted by local workers, but 90% of the publications were still disseminated in English. Field surveys and laboratory analyses made up over 40% of the research, but experimental work was mostly missing and represents the largest, most important gap. A government initiative in Thailand generated much knowledge on the distribution of marine sponges; otherwise urchins were again prominent in diversity checklists. Comparatively, many checklists were produced for Vietnam from work by visiting scientists. Most studies investigated coastal habitats, but a fourth sampled at oceanic locations. About 36% of the checklist publications covered the entire South China Sea; the rest produced faunistic records for locations within single countries. Our efforts demonstrate that, while active bioerosion research and basic expertise exist in the South China Sea, research remained unrepresentative with respect to taxa, ecofunctional guilds, and especially to controlled experiments. The latter are urgently needed for prognoses, modelling and management in this populated and overused marine environment.
... Long-term exposure of experimental denuded dead coral CaCO 3 blocks and sponge-bearing cores to decreased seawater pH in a mesocosm exhibited a significant increase in bioerosion activity (Enochs et al., 2016;Schönberg et al., 2017;Tribollet et al., 2009;Wisshak et al., 2013). Measurements of coral bioeroder activity (species abundance) were carried out along naturally occurring pH gradients in coral reefs showing an increase in activity with decreasing pH . ...
... For a detailed description of seasonal nutrient and chlorophyll dynamics in the GOE, see, for example, Stambler (2006), Lazar et al. (2008), Silverman andGildor (2008), andMeeder et al. (2012). Higher net dissolution of CaCO 3 at lower bulk water Ω arag (e.g., Figure 5a), was also found in dark incubations of a single Acropora, without macro bioeroders (Schneider et al., 2006), in dead corals containing microbial endoliths (Tribollet et al., 2009(Tribollet et al., , 2019 and in the bioerosion activity of Clionaid sponge (Wisshak et al., 2013), which is an important bioeroder in coral reefs (Glynn & Manzello, 2015). Crook et al. (2013) showed that under naturally low pH conditions (Ω arag < 2), there is an increase of boring organism activity in Porites skeletons. ...
The current study (2015–2016) evaluated changes in the net community calcification (NCC) and maximum nighttime CaCO3 dissolution (Dmax) in the Nature Reserve Reef (NRR), northern Gulf of Eilat (GOE), and northern Red Sea, compared to measurements made at the same site during 2000–2002. The NCC and Dmax were calculated as a function of the reef‐water residence time, the difference between the open‐sea total alkalinity (TA) and its reef‐water daily average (for NCC), and its nighttime maximum (for Dmax). The average NCC was 50 ± 13 and 68 ± 22 mmol C m⁻² day⁻¹ in 2000–2002 and 2015–2016, respectively. This change is consistent with the live coral cover increase in the NRR during this period, following the final removal of fish cages from the northern GOE in 2008. In contrast, wintertime Dmax values in 2015–2016 were five times higher on average compared to 2000–2002. We hypothesize that these higher rates could be the result of increased boring organism activity and sedimentary organic content, which developed throughout the fish farming period and are maintained by the naturally occurring seasonal eutrophication in the northern GOE. Where, in general, Dmax was higher during the winters, when nighttime reef water aragonite saturation (Ωarag) was lower, while open water chlorophyll a and nitrate were higher, compared to summertime. Thus, it is possible that the combination of seasonal eutrophication and ocean acidification (OA) in the GOE and possibly other coral reef sites around the world, may shift coral reefs to net dissolution even sooner than previously predicted from OA alone.
... Numerous laboratory studies have also found elevated sponge bioerosion rates in response to OA conditions (Duckworth & Peterson, 2013;Enochs et al., 2015;Fang et al., 2013;Wisshak et al., 2013Wisshak et al., , 2014. While OA-stimulated bioerosion has been measured for both zooxanthellate and azooxanthellate species, the response is thought to be more pronounced among photosynthetic sponges due to an increase in the photosynthetic efficiency of sponge symbionts associated with OA (Achlatis et al., 2017). ...
... Significant differences across treatment conditions are denoted by *. Figure 2a,b). This response supports prior sponge studies investigating the influence of OA on sponge bioerosion under static conditions (Enochs et al., 2015;Wisshak et al., 2013Wisshak et al., , 2014, further underlining the positive impact of OA on sponge bioeroding capacity. The majority of these studies, however, measured biologically mediated chemical dissolution rather than buoyant weight derived bioerosion, and direct comparisons should be cautiously applied. ...
... Moreso, the CT variable treatment reached the most acidified conditions for a comparably shorter period of time each day (<8.0 pH for 6 hrs, CT variable; 7.80 pH for 24 h, OA static). Based on these discrepancies, results from prior literature would lead us to expect higher bioerosion rates for sponges exposed to the static OA treatment due to the stimulating effect of reduced pH conditions (Enochs et al., 2015;Wisshak et al., 2013Wisshak et al., , 2014. In our present study, however, the similar rates between the two treatments suggest that diel pH variability may modulate the sponge OA response in a way that requires an updated interpretation of the previously described relationship. ...
Ocean acidification (OA) is expected to modify the structure and function of coral reef ecosystems by reducing calcification, increasing bioerosion, and altering the physiology of many marine organisms. Much of our understanding of these relationships is based upon experiments with static OA treatments, though evidence suggests that the magnitude of diurnal fluctuations in carbonate chemistry may modulate the calcification response to OA. These light-mediated swings in seawater pH are projected to become more extreme with OA, yet their impact on bioerosion remains unknown. We evaluated the influence of diurnal carbonate chemistry variability on the bioerosion rates of two Caribbean sponges: the zooxanthellate Cliona varians and azooxanthellate Cliothosa delitrix. Replicate fragments from multiple colonies of each species were exposed to four precisely-controlled pH treatments: contemporary static (8.05 ± 0.00; mean pH ± diurnal pH oscillation), contemporary variable (8.05 ± 0.10), future OA static (7.80 ± 0.00), and future OA variable (7.80 ± 0.10). Significantly enhanced bioerosion rates, determined using buoyant weight measurements, were observed under more variable conditions in both the contemporary and future OA scenarios for C. varians, whereas the same effect was only apparent under contemporary pH conditions for C. delitrix. These results indicate that variable carbonate chemistry has a stimulating influence on sponge bioerosion, and we hypothesize that bioerosion rates evolve non-linearly as a function of pCO2 resulting in different magnitudes and directions of rate enhancement/reduction between day and night, even with an equal fluctuation around the mean. This response appeared to be intensified by photosymbionts, evident by the consistently higher percent increase in bioerosion rates for photosynthetic C. varians across all treatments. These findings further suggest that more variable natural ecosystems may presently experience elevated sponge bioerosion rates and that the heightened impact of OA enhanced bioerosion on reef habitat could occur sooner than prior predictions.
... Bioerosion is thought to contribute more to reef degradation globally than physical erosion or passive chemical dissolution (Schönberg et al. 2017) and, thus, plays an important role in carbonate (re)cycling. In warm-water coral reefs, chemical bioerosion by microphytes and excavating sponges was accelerated significantly under ocean acidification (Tribollet et al. 2006(Tribollet et al. , 2009Wisshak et al. 2012Wisshak et al. , 2013, highlighting the need to consider this process in assessments of ocean change impacts (see Schönberg et al. 2017 for a review). Bioerosion has been more extensively studied in shallow-water settings, but Beuck and Freiwald (2005) characterized bioerosion patterns of a L. pertusa coral mound in the northern Porcupine Seabight in the North Atlantic. ...
... To date, there is no experimental data on the influence of pCO 2 on bioerosion rates of microfungi, but bioerosion by phototrophic microborers in tropical coral reefs (chlorophytes and cyanobacteria) significantly increased under simulated ocean acidification (e.g., Tribollet et al. 2006Tribollet et al. , 2009 and as bioeroding microfungi apply a chemical mode of bioerosion as well, we suspect that fungal microbioerosion is similarly stimulated by elevated levels of pCO 2 as supported by our results. As far as bioeroding sponges are concerned, there is solid experimental evidence for several tropical to cold-temperate species that indicate that they accelerate their bioerosion activity (chemical biocorrosion and mechanical extraction of sediment chips in this case) at elevated pCO 2 levels (Wisshak et al. 2012(Wisshak et al. , 2013Stubler et al. 2015). This suggests that ecophysiological responses apply across species and latitudes (Wisshak et al. 2014). ...
... Since related species of the same sponge genera are abundant in cold-water coral reefs, they are likely affected in the same way. Experiments that have included temperature in separate and combined treatments (Wisshak et al. 2013;Stubler et al. 2015) suggest that temperature has comparatively little effect on the sponge's bioerosion rates until critically high temperature stress levels lead to adverse effects, which is supported by our results. ...
Physiological sensitivity of cold‐water corals to ocean change is far less understood than of tropical corals and very little is known about the impacts of ocean acidification and warming on degradative processes of dead coral framework. In a 13‐month laboratory experiment, we examined the interactive effects of gradually increasing temperature and pCO2 levels on survival, growth, and respiration of two prominent color morphotypes (colormorphs) of the framework‐forming cold‐water coral Lophelia pertusa, as well as bioerosion and dissolution of dead framework. Calcification rates tended to increase with warming, showing temperature optima at ~ 14°C (white colormorph) and 10–12°C (orange colormorph) and decreased with increasing pCO2. Net dissolution occurred at aragonite undersaturation (ΩAr < 1) at ~ 1000 μatm pCO2. Under combined warming and acidification, the negative effects of acidification on growth were initially mitigated, but at ~ 1600 μatm dissolution prevailed. Respiration rates increased with warming, more strongly in orange corals, while acidification slightly suppressed respiration. Calcification and respiration rates as well as polyp mortality were consistently higher in orange corals. Mortality increased considerably at 14–15°C in both colormorphs. Bioerosion/dissolution of dead framework was not affected by warming alone but was significantly enhanced by acidification. While live corals may cope with intermediate levels of elevated pCO2 and temperature, long‐term impacts beyond levels projected for the end of this century will likely lead to skeletal dissolution and increased mortality. Our findings further suggest that acidification causes accelerated degradation of dead framework even at aragonite saturated conditions, which will eventually compromise the structural integrity of cold‐water coral reefs.
... Sponges have widely been recognised as winners on coral reefs because of changing environmental conditions (see [6,7]) and particularly in response to the impacts of climate change [8]. Sponges are generally very tolerant to the impacts of ocean acidification [9,10] and show a high degree of tolerance to temperatures expected under the more moderate climate change scenarios [11,12]. For example, Bennett et al. [11] tested the thermal tolerance of four abundant Great Barrier Reef species and found all species were generally unaffected by conditions predicted under RCP6.0, ...
Despite the global focus on the occurrence of regime shifts on shallow-water tropical coral reefs over the last two decades, most of this research continues to focus on changes to algal-dominated states. Here, we review recent reports (in approximately the last decade) of regime shifts to states dominated by animal groups other than zooxanthellate Scleractinian corals. We found that while there have been new reports of regime shifts to reefs dominated by Ascidacea, Porifera, Octocorallia, Zoantharia, Actiniaria and azooxanthellate Scleractinian corals, some of these changes occurred many decades ago, but have only just been reported in the literature. In most cases, these reports are over small to medium spatial scales (<4 × 104 m2 and 4 × 104 to 2 × 106 m2, respectively). Importantly, from the few studies where we were able to collect information on the persistence of the regime shifts, we determined that these non-scleractinian states are generally unstable, with further changes since the original regime shift. However, these changes were not generally back to coral dominance. While there has been some research to understand how sponge- and octocoral-dominated systems may function, there is still limited information on what ecosystem services have been disrupted or lost as a result of these shifts. Given that many coral reefs across the world are on the edge of tipping points due to increasing anthropogenic stress, we urgently need to understand the consequences of non-algal coral reef regime shifts.
... Many experiments ranging from three days to twenty weeks suggest acidification may lead to increased sponge bioerosion rates [6,[75][76][77], consequently leading to decreased net calcification of living corals [78] and increased calcium carbonate (CaCO 3 ) dissolution of dead corals [76,[78][79][80]. Here, we also show that a non-photosynthetic encrusting/excavating sponge adjacent to S. radians does not impact net calcification of the coral. ...
Coral reef community composition, function, and resilience have been altered by natural and anthropogenic stressors. Future anthropogenic ocean and coastal acidification (together termed “acidification”) may exacerbate this reef degradation. Accurately predicting reef resilience requires an understanding of not only direct impacts of acidification on marine organisms but also indirect effects on species interactions that influence community composition and reef ecosystem functions. In this 28-day experiment, we assessed the effect of acidification on coral–algal, coral–sponge, and algal–sponge interactions. We quantified growth of corals (Siderastrea radians), fleshy macroalgae (Dictyota spp.), and sponges (Pione lampa) that were exposed to local summer ambient (603 μatm) or elevated (1105 μatm) pCO2 seawater. These species are common to hard-bottom communities, including shallow reefs, in the Florida Keys. Each individual was maintained in isolation or paired with another organism. Coral growth (net calcification) was similar across seawater pCO2 and interaction treatments. Fleshy macroalgae had increased biomass when paired with a sponge but lost biomass when growing in isolation or paired with coral. Sponges grew more volumetrically in the elevated seawater pCO2 treatment (i.e., under acidification conditions). Although these results are limited in temporal and spatial scales due to the experimental design, they do lend support to the hypothesis that acidification may facilitate a shift towards increased sponge and macroalgae abundance by directly benefiting sponge growth which in turn may provide more dissolved inorganic nitrogen to macroalgae in the Florida Keys.
... Without protective coral tissue, dead framework is directly exposed to the corrosive seawater and becomes increasingly unstable (Hennige et al. 2015(Hennige et al. , 2020. Further, acidification facilitates bioerosion by sponges, accelerating dead framework degradation (Wisshak et al. 2012(Wisshak et al. , 2013(Wisshak et al. , 2014. If reef erosion is no longer balanced by coral growth, the reef structure becomes flatter and eventually disappears (Perry et al. 2013, Büscher et al. 2019, Perry and Alvarez-Filip 2019, Hennige et al. 2020. ...
