Article

Temporal effects of ocean warming and acidification on coral–algal competition

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Abstract

While there is an ever-expanding list of impacts on coral reefs as a result of ocean warming and acidification, there is little information on how these global changes influence coral–algal competition. The present study assessed the impact of business-as-usual ocean warming and acidification conditions on the survivorship, calcification, photosynthesis and respiration of the coral–algal interaction between the macroalga Halimeda heteromorpha and the coral Acropora intermedia over 8 weeks in two seasons. The physiological responses of A. intermedia and H. heteromorpha were highly dependent on season, with both organisms demonstrating optimal rates of calcification and photosynthesis under present-day conditions in summer. Contact with H. heteromorpha did not influence A. intermedia survivorship, however did reduce long-term calcification rates. Photosynthetic rates of A. intermedia were influenced by algal contact temporally in opposing directions, with rates reduced in winter and increased in summer. Enhanced photosynthetic rates as a result of algal contact were not enough to offset the combined effects of ocean warming and acidification, which regardless of coral–algal contact, reduced survivorship, calcification and photosynthesis of A. intermedia and the calcification rates of H. heteromorpha. These findings provide experimental support for the idea that the effects of coral–algal competition are temporally variable, and help improve our understanding of how future ocean warming and acidification may alter the dynamics of coral–algal interactions.

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... two weeks intervals) via buoyant weight and photogrammetry using previously described methods [27][28][29] (electronic supplementary material, Methods, figures S4 and S5). At the end of the experiment, metabolic rates (net photosynthesis, dark respiration and light-enhanced dark respiration) were assessed via changes in oxygen evolution using oxygen optodes connected to an OXY-10 (PreSens) optical analyser [30] (electronic supplementary material, Methods). Upon completion of these living analyses, half of the coral fragments were flash frozen in liquid nitrogen and stored at −80°C. ...
... Host tissue was analysed for host-soluble protein concentration and mycosporine-like amino acids (MAAs) concentrations spectrophotometrically [31]. Endosymbiont densities were determined from cell counts of three aliquots using a haemocytometer [30]. Host protein concentration and endosymbiont cell densities were standardized to surface area (cm 2 ), which was determined using the single wax-dipping technique [32], whereas MAAs were normalized to host protein content. ...
... These observations suggest that autotrophic energy acquisition was not impeded by the daily, extreme, oscillations in pCO 2 to which these corals were acclimatized. This is in contrast to corals exposed to simulated seawater acidification and/or in situ thermal stress, which typically exhibit reductions in metabolic rates [30,35]. In addition, there were no significant differences in chlorophyll a concentrations (F = 0.21, p = 0.65) or photochemical efficiency (F v /F m ) between origin (F = 1.25, p = 0.26) or treatment (F = 0.01, p = 0.91) (electronic supplementary material, figure S8), suggesting that pCO 2 variability did not have an effect on these parameters. ...
Article
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Ocean acidification is a growing threat to coral growth and the accretion of coral reef ecosystems. Corals inhabiting environments that already endure extreme diel pCO2 fluctuations, however, may represent acidification-resilient populations capable of persisting on future reefs. Here, we examined the impact of pCO2 variability on the reef-building coral Pocillopora damicornis originating from reefs with contrasting environmental histories (variable reef flat versus stable reef slope) following reciprocal exposure to stable (218 ± 9) or variable (911 ± 31) diel pCO2 amplitude (μtam) in aquaria over eight weeks. Endosymbiont density, photosynthesis and net calcifica-tion rates differed between origins but not treatment, whereas primary calcification (extension) was affected by both origin and acclimatization to novel pCO2 conditions. At the cellular level, corals from the variable reef flat exhibited less intracellular pH (pHi) acidosis and faster pHi recovery rates in response to experimental acidification stress (pH 7.40) than corals originating from the stable reef slope, suggesting environmental memory gained from lifelong exposure to pCO2 variability led to an improved ability to regulate acid-base homeostasis. These results highlight the role of cellular processes in maintaining acidification resilience and suggest that prior exposure to pCO2 variability may promote more acidification-resilient coral populations in a changing climate.
... Investigations about coral-algal interactions have strongly increased during the last decade, monitoring interactions both in situ and in tank experiments (Bender et al., 2012;Birrell et al., 2008;Brown et al., 2019;Del Monaco et al., 2017;Diaz-Pulido et al., 2010;Diaz-Pulido and Barrón, 2020;Jompa and McCook, 2003;McCook, 2001;Rasher et al., 2011;Rasher and Hay, 2010;Vieira et al., 2016)However, information on the impacts of global and climate change on ecological interactions are still underrepresented in the literatura. ...
... A recent study by Brown et al. (2019) suggests that coral-algal interactions are temporally variable across seasons. Photosynthetic rates of the coral A. intermedia in contact with H. heteromorpha were reduced in winter and increased in summer, while calcification rates in summer reduced in contact with the algae. ...
... Even though photosynthetic activity was increased in contact with the algae, negative effects of a high-end ocean acidification and warming scenario (RCP8.5) reduced overall performance of corals (Brown et al., 2019), which is comparable to the results of our study. ...
Article
Competition between corals and macroalgae is frequently observed on reefs with the outcome of these interactions affecting the relative abundance of reef organisms and therefore reef health. Anthropogenic activities have resulted in increased atmospheric CO 2 levels and a subsequent rise in ocean temperatures. In addition to increasing water temperature, elevated CO 2 levels are leading to a decrease in oceanic pH (ocean acidification). These two changes have the potential to alter ecological processes within the oceans, including the outcome of competitive coral-macroalgal interactions. In our study, we explored the combined effect of temperature increase and ocean acidification on the competition between the coral Porites lobata and on the Great Barrier Reef abundant macroalga Chlorodesmis fastigiata. A temperature increase of +1 • C above present temperatures and CO 2 increase of +85 ppm were used to simulate a low end emission scenario for the mid-to late 21st century, according to the Representative Concentration Pathway 2.6 (RCP2.6). Our results revealed that the net photo-synthesis of P. lobata decreased when it was in contact with C. fastigiata under ambient conditions, and that dark respiration increased under RCP2.6 conditions. The Photosynthesis to Respiration (P:R) ratios of corals as they interacted with macroalgal competitors were not significantly different between scenarios. Dark calcification rates of corals under RCP2.6 conditions, however, were negative and significantly decreased compared to ambient conditions. Light calcification rates were negatively affected by the interaction of macroalgal contact in the RCP2.6 scenario, compared to algal mimics and to coral under ambient conditions. Chlorophyll a, and protein content increased in the RCP2.6 scenario, but were not influenced by contact with the macroalga. We conclude that the coral host was negatively affected by RCP2.6 conditions, whereas the productivity of its symbionts (zooxanthellae) was enhanced. While a negative effect of the macroalga (C. fastigiata) on the coral (P. lobata) was observed for the P:R ratio under control conditions, it was not enhanced under RCP2.6 conditions.
... Pigmentation loss at the interaction zone was clearly distinguishable from any other irregularities found on coral colonies (figure 1). Where macroalgae were covering coral, it was removed to determine the outcome in the area underneath, as not all contact by macroalgae results in discoloration to the competing coral [19,25,36]. Individual colonies were not tracked through time; therefore, the long-term fate (i.e. ...
... abrasion) are often found to result in no visible effects (e.g. coral bleaching) to competing coral [19,23,36]. ...
... Open Sci. 7: 201797 finding no temporal changes in the competitive ability of H. heteromorpha [36]. ACA was more damaging than Halimeda, with 33.5-43.9% of coral colonies losing interactions with ACA when compared with 3.2-14.5% for Halimeda (figure 1; electronic supplementary material, tables S3 and S4). ...
Article
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Understanding the effects of natural processes on coral–algal competition is an important step in identifying the role of macroalgae in perturbed coral reef ecosystems. However, studies investigating coral–algal interactions are often conducted in response to a disturbance, and rarely incorporate seasonal variability. Here, naturally occurring coral–algal interactions were assessed in situ four times a year over 2 years across eight sites spanning diverse benthic communities. In over 6500 recorded coral–algal interactions, cyanobacteria and turf algae were found to be the most damaging regardless of season, resulting in visible damage to coral in greater than 95% of interactions. Macroalgae that primarily compete using chemical mechanisms were found to be more damaging than those that compete using physical mechanisms (e.g. abrasion), with both groups demonstrating decreased competitive ability in summer. While crustose coralline algae were the least damaging to competing coral, during summer, it became three times more competitive. Our results demonstrate that the competitive ability of macroalgae and the outcomes of coral–algal competition can fluctuate in seasonal cycles that may be related to biomass, production of chemical defences and/or physical toughness. The results of this study have important implications for understanding the trajectory and resilience of coral reef ecosystems into the future.
... While the diverse responses in Halimeda spp. can potentially be the result of differences in species' susceptibilities, some evidence suggests that they may also be related to differences in the duration of the experiments [35] and/or thermal tolerance range of the organisms in relation to the temperatures increases used in the studies [21,72]. Regarding the latter, a key consideration that is often overlooked in temperature studies is the regional temperature acclimation (i.e., local maximum summer temperature) [73]. ...
... Regarding the latter, a key consideration that is often overlooked in temperature studies is the regional temperature acclimation (i.e., local maximum summer temperature) [73]. For example, in a seasonal study on the effects of OA and elevated temperature in H. heteromorpha, winter calcification rates were found to increase under the combined treatment (OA, +3.5 • C) [72]. In contrast, in the summer experiment the same treatment caused a decrease in calcification rates, which was most likely related to the fact that the elevated temperature scenario in summer represented a temperature above the local maximum summer value. ...
Article
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Ocean acidification (OA) has been identified as one of the major climate-change related threats, mainly due to its significant impacts on marine calcifiers. Among those are the calcareous green algae of the genus Halimeda that are known to be major carbonate producers in shallow tropical and subtropical seas. Hence, any negative OA impacts on these organisms may translate into significant declines in regional and global carbonate production. In this study, we compiled the available information regarding Halimeda spp. responses to OA (experimental, in situ), with special focus on the calcification responses, one of the most studied response parameters in this group. Furthermore, among the compiled studies (n = 31), we selected those reporting quantitative data of OA effects on algal net calcification in an attempt to identify potential general patterns of species- and/or regional-specific OA responses and hence, impacts on carbonate production. While obtaining general patterns was largely hampered by the often scarce number of studies on individual species and/or regions, the currently available information indicates species-specific susceptibility to OA, seemingly unrelated to evolutionary lineages (and associated differences in morphology), that is often accompanied by differences in a species’ response across different regions. Thus, for projections of future declines in Halimeda-associated carbonate production, we used available regional reports of species-specific carbonate production in conjunction with experimental OA responses for the respective species and regions. Based on the available information, declines can be expected worldwide, though some regions harbouring more sensitive species might be more impacted than others.
... Photosynthesis has been shown to increase calcification in marine macroalgae (Borowitzka and Larkum 1987;De Beer and Larkum 2001;Gao et al. 1993;Koch et al. 2013;Pentecost 1978;Semesi et al. 2009;Wizemann et al. 2014), but the influence of increasing pCO 2 and [H + ] on the coupling of these two processes is only recently being disentangled (Brown et al. 2019;Comeau et al. 2018;Hofmann et al. 2016;McNicholl et al. 2020McNicholl et al. , 2019. A majority of marine macroalgae use carbon concentrating mechanisms (CCMs) to saturate RuBisCO with CO 2 for photosynthesis (Raven and Hurd 2012). ...
... While the importance of photosynthesis in macroalgal calcification has long been appreciated (Borowitzka 1981;Koch et al. 2013;Pentecost 1978), how this relationship is sustained under low pH has not been resolved. Further, in some species, as was shown for H. heteromorpha, net photosynthetic rates do not always positively correspond to rates of calcification at low pH (Brown et al. 2019). Photosynthesis has been shown to elevate pH at the macroalgal thalli surface under low pH and elevated pCO 2 (Cornwall et al. 2015;Hofmann et al. 2016;McNicholl et al. 2019). ...
Article
Calcifying tropical macroalgae produce sediment, build three-dimensional habitats, and provide substrate for invertebrate larvae on reefs. Thus, lower calcification rates under declining pH and increasing ocean pCO2, or ocean acidification, is a concern. In the present study, calcification rates were examined experimentally under predicted end-of-the-century seawater pCO2 (1116 μatm) and pH (7.67) compared to ambient controls (pCO2 409 μatm; pH 8.04). Nine reef macroalgae with diverse calcification locations, calcium carbonate structure, photophysiology, and site-specific irradiance were examined under light and dark conditions. Species included five from a high light patch reef on the Florida Keys Reef Tract (FKRT) and four species from low light reef walls on Little Cayman Island (LCI). Experiments on FKRT and LCI species were conducted at 500 and 50 μmol photons m⁻² s⁻¹ in situ irradiance, respectively. Calcification rates independent of photosystem-II (PSII) were also investigated for FKRT species. The most consistent negative effect of elevated pCO2 on calcification rates in the tropical macroalgae examined occurred in the dark. Most species (89%) had net calcification rates of zero or net dissolution in the dark at low pH. Species from the FKRT that sustained positive net calcification rates in the light at low pH also maintained ~30% of their net calcification rates without PSII at ambient pH. However, calcification rates in the light independent of PSII were not sustained at low pH. Regardless of these low pH effects, most FKRT species daily net calcification rates, integrating light/dark rates over a 24h period, were not significantly different between low and ambient pH. This was due to a 10-fold lower dark, compared to light, calcification rate, and a strong correspondence between calcification and photosynthetic rates. Interestingly, low-light species sustained calcification rates on par with high-light species without high rates of photosynthesis. Low-light species' morphology and physiology that promote high calcification rates at ambient pH, may increase their vulnerability to low pH. Our data indicate that the negative effect of elevated pCO2 and low pH on tropical macroalgae at the organismal level is their impact on dark net calcification, probably enhanced dissolution. However, elevated pCO2 and low pH effects on macroalgae daily calcification rates are greatest in species with lower net calcification rates in the light. Thus, macroalgae able to maintain high calcification rates in the light (high and low irradiance) at low pH, and/or sustain strong biotic control with high [H⁺] in the bulk seawater, are expected to dominate under global change.
... Therefore, 50% of the algae were, along with the corals, growing at a mean summer maximum water temperature of approximately 2 o C below their lethal thermal limits, while the other algae species were more thermo-tolerant (lethal thermal thresholds >3 o C above the mean summer maximum water temperature). Nonetheless, to date, few studies assess the thermal performance of corals and algae from the same geographic location (Brown et al., 2019), and none have compared lethal thermal limits in combination with thermal performance curves between coral and algae, which may reveal differential vulnerability towards a warming ocean. ...
Article
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Marine heatwaves can lead to rapid changes in entire communities, including in the case of shallow coral reefs the potential overgrowth of algae. Here we tested experimentally the differential thermal tolerance between algae and coral species from the Red Sea through the measurement of thermal performance curves and the assessment of thermal limits. Differences across functional groups (algae vs corals) were apparent for two key thermal performance metrics. First, two reef‐associated algae species (Halimeda tuna and Turbinaria ornata,) had higher lethal thermal limits than two coral species (Pocillopora verrucosa and Stylophora pistillata) conferring those species of algae with a clear advantage during heatwaves by surpassing the thermal threshold of coral survival. Second, the coral species had generally greater deactivation energies for net and gross primary production rates compared to the algae species, indicating greater thermal sensitivity in corals once the optimum temperature is exceeded. Our field surveys in the Red Sea reefs before and after the marine heatwave of 2015 show a change in benthic cover mainly in the southern reefs, where there was a decrease in coral cover and a concomitant increase in algae abundance, mainly turf algae. Our laboratory and field observations indicate that a proliferation of algae might be expected on Red Sea coral reefs with future ocean warming.
... For example, the calcifying green alga Halimeda spp. forms habitat (Stoner and Lewis, 1985), shapes community structure through ecological interactions such as competition (Brown et al., 2019), and plays a role in carbon sequestration in tropical habitats (Payri, 1988;Rees et al., 2007;Krause-Jensen and Duarte, 2016). Non-geniculate coralline algae fill an additional suite of ecological roles in polar, temperate, and tropical systems by producing chemical cues that facilitate settlement of invertebrate larvae (Roberts et al., 2004), cementing coral reef ecosystems (Adey, 1998), and providing three-dimensional habitat for economically valuable and diverse species assemblages (Chisholm, 2000;Foster, 2001;Mc-Coy and Kamenos, 2015). ...
Article
Accurately predicting the effects of ocean and coastal acidification on marine ecosystems requires understanding how responses scale from laboratory experiments to the natural world. Using benthic calcifying macroalgae as a model system, we performed a semi-quantitative synthesis to compare directional responses between laboratory experiments and field studies. Variability in ecological, spatial, and temporal scales across studies, and the disparity in the number of responses documented in laboratory and field settings, make direct comparisons difficult. Despite these differences, some responses, including community-level measurements, were consistent across laboratory and field studies. However, there were also mismatches in the directionality of many responses with more negative acidification impacts reported in laboratory experiments. Recommendations to improve our ability to scale responses include: (i) developing novel approaches to allow measurements of the same responses in laboratory and field settings, and (ii) researching understudied calcifying benthic macroalgal species and responses. Incorporating these guidelines into research programs will yield data more suitable for robust meta-analyses and will facilitate the development of ecosystem models that incorporate proper scaling of organismal responses to in situ acidification. This, in turn, will allow for more accurate predictions of future changes in ecosystem health and function in a rapidly changing natural climate.
... While most studies continue to expose reef organisms to relatively sudden OA/OW 'shock', some experiments do consider a gradual change or ramp (from 72 h to four weeks) in OA and/or OW levels (e.g. Anderson et al., 2019;Brown et al., 2019;Kamenos et al., 2013;Scherner et al., 2018;Wright et al., 2019). For example, van der Zande et al. (2020) exposed coral colonies to OW and OA treatments by gradually increasing treatment levels for over four weeks. ...
Article
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Tropical marine habitat-builders such as calcifying green algae can be susceptible to climate change (warming and acidification). This study evaluated the cumulative effects of ocean warming (OW), ocean acidification (OA) and the herbicide diuron on the calcifying green algae Halimeda opuntia. We also assessed the influence of acclimation history to experimental climate change conditions on physiological responses. H. opuntia were exposed for 15 days to orthogonal combinations of three climate scenarios [ambient (28 °C, pCO2 = 378 ppm), 2050 (29 °C, pCO2 = 567 ppm) and 2100 (30 °C, pCO2 = 721 ppm)] and to six diuron concentrations (up to 29 μg L⁻¹). Half of the H. opuntia had been acclimated for eight months to the climate scenarios in a mesocosm approach, while the remaining half were not pre-acclimated, as is current practice in most experiments. Climate effects on quantum yield (ΔF/Fm′), photosynthesis and calcification in future climate scenarios were significantly stronger (by −24, −46 and +26%, respectively) in non-acclimated algae, suggesting experimental bias may exaggerate effects in organisms not appropriately acclimated to future-climate conditions. Thus, full analysis was done on acclimated plants only. Interactive effects of future climate scenarios and diuron were observed for ΔF/Fm′, while the detrimental effects of climate and diuron on net photosynthesis and total antioxidant capacity (TAC) were additive. Calcification-related enzymes were negatively affected only by diuron, with inhibition of Ca-ATPase and upregulation of carbonic anhydrase. The combined and consistent physiological and biochemical evidence of negative impacts (across six indicators) of both herbicide and future-climate conditions on the health of H. opuntia highlights the need to address both climate change and water quality. Guideline values for contaminants may also need to be lowered considering ‘climate adjusted thresholds’. Importantly, this study highlights the value of applying substantial future climate acclimation periods in experimental studies to avoid exaggerated organism responses to OW and OA.
... However, only Canistrocarpus (= Dictyota) cervicornis had increased allelopathy that led to decreased effective quantum yield of corals under high seawater pCO 2 (936 ppm) [12]. In contrast to these results, Brown et al. [74] reported no main or interactive effects of ocean acidification and direct contact with a calcifying macroalga Halimeda heteromorpha on coral survivorship or net calcification during eight-week experiments conducted in summer and winter months. Likewise, S. radians from the Florida Reef Tract appear to be resistant to coral-algal competition even under ocean acidification. ...
Article
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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.
... Despite this flexibility, as the frequency of coral bleaching increases, the shortened duration between events may be insufficient for complete recovery of many survivors Sale et al., 2019;Schoepf et al., 2015). These energetic or functional deficits during recovery from bleaching can increase coral susceptibility to subsequent stressors, including but not limited to temperature, disease, competition, and ocean acidification (Brown et al., 2019;Muller et al., 2018;Ward et al., 2000). Short intervals between heatwaves can also change the relative performance between coral species, as differential investments in resistance versus recovery strategies (e.g., Matsuda et al., 2020) may enable some species to withstand single but not repeat bleaching events . ...
Article
Ocean warming is causing global coral bleaching events to increase in frequency, resulting in widespread coral mortality and disrupting the function of coral reef ecosystems. However, even during mass bleaching events, many corals resist bleaching despite exposure to abnormally high temperatures. While the physiological effects of bleaching have been well documented, the consequences of heat stress for bleaching‐resistant individuals are not well understood. In addition, much remains to be learned about how heat stress affects cellular‐level processes that may be overlooked at the organismal level, yet are crucial for coral performance in the short term and ecological success over the long term. Here we compared the physiological and cellular responses of bleaching‐resistant and bleaching‐susceptible corals throughout the 2019 marine heatwave in Hawai‘i, a repeat bleaching event that occurred four years after the previous regional event. Relative bleaching susceptibility within species was consistent between the two bleaching events, yet corals of both resistant and susceptible phenotypes exhibited pronounced metabolic depression during the heatwave. At the cellular level, bleaching‐susceptible corals had lower intracellular pH than bleaching‐resistant corals at the peak of bleaching for both symbiont‐hosting and symbiont‐free cells, indicating greater disruption of acid‐base homeostasis in bleaching‐susceptible individuals. Notably, cells from both phenotypes were unable to compensate for experimentally induced cellular acidosis, indicating that acid‐base regulation was significantly impaired at the cellular level even in bleaching‐resistant corals and in cells containing symbionts. Thermal disturbances may thus have substantial ecological consequences, as even small reallocations in energy budgets to maintain homeostasis during stress can negatively affect fitness. These results suggest concern is warranted for corals coping with ocean acidification alongside ocean warming, as the feedback between temperature stress and acid‐base regulation may further exacerbate the physiological effects of climate change.
... Thirdly, other environmental factors such as temperature may play a role. For example, coral-algal interactions vary temporally due to seasonal changes in temperature (Brown et al. 2019). Finally, additional indirect effects, such as decreasing herbivory (see section below), can determine the likelihood of a phase shift (Enochs et al. 2015b). ...
Article
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Ocean acidification (OA) is a major threat to marine calcifying organisms. This manuscript gives an overview of the physiological effects of acidification on reef-building corals from a cellular to population scale. In addition, we present the first review of the indirect effects resulting from altered species interactions. We find that the direct effects of acidification are more consistently negative at larger spatial scales, suggesting an accumulation of sub-lethal physiological effects can result in notable changes at a population and an ecosystem level. We identify that the indirect effects of acidification also have the potential to contribute to declines in coral cover under future acidified conditions. Of particular concern for reef persistence are declines in the abundance of crustose coralline algae which can result in loss of stable substrate and settlement cues for corals, potentially compounding the direct negative effects on coral recruitment rates. In addition, an increase in the abundance of bioeroders and bioerosive capacity may compound declines in calcification and result in a shift towards net dissolution. There are significant knowledge gaps around many indirect effects, including changes in herbivory and associated coral–macroalgal interactions, and changes in habitat provision of corals to fish, invertebrates and plankton, and the impact of changes to these interactions for both individual corals and reef biodiversity as structural complexity declines. This research highlights the potential of indirect effects to contribute to alterations in reef ecosystem functions and processes. Such knowledge will be critical for scaling-up the impacts of OA from individual corals to reef ecosystems and for understanding the effects of OA on reef-dependent human societies.
... Increased temperature stress can cause corals to bleach and rises in pCO 2 may result in the microbioerosion of the calcium carbonate skeleton and induce bleaching (Brown 1997;Lesser 1997;Reyes-Nivia et al. 2013;Mason 2018). Generally, increased temperature and pCO 2 act in synergy, further lowering bleaching thresholds and reducing Symbiodiniaceae density, photosynthesis, energy reserves, calcification and survivorship of corals (Anthony et al. 2008;Godinot et al. 2011;Rodolfo-Metalpa et al. 2011;Schoepf et al. 2013;Horvath et al. 2016;Prada et al. 2017;Brown et al. 2019;Yuan et al. 2019). ...
Article
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Climate change is causing ocean temperature and partial pressure of carbon dioxide (pCO2) to increase. For sea anemones that have Symbiodiniaceae, high temperatures induce bleaching, whereas rises in pCO2 can enhance photosynthesis and increase host growth and abundance. It is, however, not clear how the interaction of these two stressors impacts sea anemones that provide habitat for anemonefishes. Here, we investigated the bleaching response of the sea anemone Entacmaea quadricolor, under four conditions: (i) current temperature and current pCO2 (control); (ii) future pCO2; (iii) future temperature; and (iv) future temperature and future pCO2. After 16 days of exposure, future temperature, but not pCO2 nor their interaction, significantly reduced the Symbiodiniaceae density and total chlorophyll Symbiodiniaceae cell⁻¹. Colour score was lower in the sea anemones exposed to future temperature than current temperature from day 4 onwards. In contrast, total chlorophyll symbiont cell⁻¹ increased in the future temperature treatments, and light-adapted effective quantum yield remained similar in all treatments. Although pCO2 had no impact within the time frame of our experiment, the predicted future temperature induced bleaching in E. quadricolor. As bleaching events increase in frequency and severity, this will likely impact the abundance of host sea anemones and their symbiotic anemonefishes.
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Ocean warming is causing global coral bleaching events to increase in frequency, resulting in widespread coral mortality and disrupting the function of coral reef ecosystems. However, even during mass bleaching events, many corals resist bleaching despite exposure to abnormally high temperatures. While the physiological effects of bleaching have been well documented, the consequences of heat stress for bleaching resistant individuals are not well understood. In addition, much remains to be learned about how heat stress affects cellular level processes that may be overlooked at the organismal level, yet are crucial for coral performance in the short term and ecological success over the long term. Here we compared the physiological and cellular responses of bleaching resistant and bleaching susceptible corals throughout the 2019 marine heatwave in Hawaii, a repeat bleaching event that occurred four years after the previous regional event. Relative bleaching susceptibility within species was consistent between the two bleaching events, yet corals of both resistant and susceptible phenotypes exhibited pronounced metabolic depression during the heatwave. At the cellular level, bleaching susceptible corals had lower intracellular pH than bleaching resistant corals at the peak of bleaching for both symbiont-hosting and symbiont-free cells, indicating greater disruption of acid-base homeostasis in bleaching susceptible individuals. Notably, cells from both phenotypes were unable to compensate for experimentally induced cellular acidosis, indicating that acid-base regulation was significantly impaired at the cellular level even in bleaching resistant corals and in cells containing symbionts. Thermal disturbances may thus have substantial ecological consequences, as even small reallocations in energy budgets to maintain homeostasis during stress can negatively affect fitness. These results suggest concern is warranted for corals coping with ocean acidification alongside ocean warming, as the feedback between temperature stress and acid-base regulation may further exacerbate the physiological effects of climate change.
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Global climate change and the impacts of ocean warming, ocean acidification and declining water quality are adversely affecting coral-reef ecosystems. This is of great concern, as coral reefs provide numerous ecosystem, economic and social services. Corals are also recognised as being amongst the strongest individual sources of natural atmospheric sulfur, through stress-induced emissions of dimethylsulfide (DMS). In the clean marine boundary layer, biogenic sulfates contribute to new aerosol formation and the growth of existing particles, with important implications for the radiative balance over the ocean. Evidence suggests that DMS is not only directly involved in the coral stress response, alleviating oxidative stress, but also may create an “ocean thermostat” which suppresses sea surface temperature through changes to aerosol and cloud properties. This review provides a summary of the current major threats facing coral reefs and describes the role of dimethylated sulfur compounds in coral ecophysiology and the potential influence on climate. The role of coral reefs as a source of climatically important compounds is an emerging topic of research; however the window of opportunity to understand the complex biogeophysical processes involved is closing with ongoing degradation of the world's coral reefs. The greatest uncertainty in our estimates of radiative forcing and climate change is derived from natural aerosol sources, such as marine DMS, which constitute the largest flux of oceanic reduced sulfur to the atmosphere. Given the increasing frequency of coral bleaching events, it is crucial that we gain a better understanding of the role of DMS in local climate of coral reefs.
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Calcification by calcified marine macroalgae is crucial to algal growth and the formation and maintenance of coral reefs. It involves complex processes, such as the uptake, transport and storage of Ca2+, HCO3– or CO32–, and the formation of crystals responsible for calcium deposition. Calcification is vulnerable to changes in global climate, including ocean acidification and warming. Studies investigating the mechanisms of macroalgal calcification are limited and restricted to physiological processes; however, the use of new approaches, such as genomics, provides avenues for new understandings. Here, we review the literature on macroalgal calcification from physiological to molecular levels and present a list of key issues that need to be resolved in order to understand the mechanism of calcification. This review offers insights into the potential effects of changing climate conditions on algal calcification to provide an accurate prediction of future changes in reef ecosystems.
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Extreme reef environments have become useful natural laboratories to investigate physiological specificities of species chronically exposed to future-like climatic conditions. The lagoon of Bouraké in New Caledonia (21°56′56.16′′ S; 125°59′36.82′′ E) is one of the only reef environments studied where the three main climatic stressors predicted to most severely impact corals occur. In this lagoon, temperatures, seawater pHT and dissolved oxygen chronically fluctuate between extreme and close-to-normal values (17.5–33.85 °C, 7.23–7.92 pHT units and 1.87–7.24 mg O2 L⁻¹, respectively). In March 2020, the endosymbiont functions (chl a, cell density and photosynthesis) and respiration rates were investigated in seven coral species from this lagoon and compared with those of corals from an adjacent reference site using hour-long incubations mimicking present-day and future conditions. Corals originating from Bouraké displayed significant differences in these variables compared to reference corals, but these differences were species-specific. Photosynthetic rates of Bouraké corals were all significantly lower than those of reference corals but were partially compensated by higher chlorophyll contents. Respiration rates of the Bouraké corals were either lower or comparable to those of reference corals. Conversely, photosynthesis and respiration rates of most studied species were similar regardless of the incubation conditions, which mimicked either present-day or future conditions. This study supports previous work indicating that no unique response can explain corals’ tolerance to sub-optimal conditions and that a variety of mechanisms will be at play for corals in a changing world.
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Coral reefs are being threatened by global climate change, with ocean warming and acidification, compounded by declining water quality in many coastal systems, adversely affecting coral health and cover. This is of great concern as coral reefs provide numerous ecosystem, economic and social services. Corals are also recognized as being amongst the strongest individual sources of natural atmospheric sulfur, through stress-induced emissions of dimethylsulfide (DMS). In the clean marine boundary layer, biogenic sulfates contribute to new aerosol formation and the growth of existing particles, with important implications for the radiative balance. Evidence suggests that DMS is not only directly involved in the coral stress response, alleviating oxidative stress, but may create an ocean thermostat which suppresses sea surface temperature (SST) through changes to aerosol and cloud properties. This review provides a summary of the current major threats facing coral reefs and describes the role of dimethylated sulfur compounds in coral physiology and climate. The role of coral reefs as a source of climatically important compounds is an emerging topic of research however, the window of opportunity to understand the complex biogeophysical processes involved is closing with ongoing degradation of the world's coral reefs. The greatest uncertainty in our estimates of radiative forcing and climate change are derived from natural aerosol sources, such as marine DMS, which constitutes the largest flux of oceanic reduced sulfur to the atmosphere. Gaining a better understanding of the role of coral reef DMS emissions is crucial to predicting the future climate of our planet.
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Globally, tropical coral reefs are being degraded by human activities, and as a result, reef-building corals have declined while macroalgae have increased. Recent work has focused on measuring macroalgal abundance in response to anthropogenic stressors. To accurately evaluate the effects of human impacts, however, it is necessary to understand the effects of natural processes on reef condition. To better understand how coral reef communities are influenced by natural processes, we investigated how spatial and seasonal changes in environmental conditions (temperature and PAR) influence benthic community structure, and the composition and frequency of coral-algal interactions across 8 distinct zones and over a 23-month period at Heron reef on the southern Great Barrier Reef. Hard coral cover and macroalgal density showed distinct spatio-temporal variations, both within and between zones. Broad hard coral cover was significantly higher at the reef slope sites compared to the lagoon and was not significantly influenced by season. The composition and biomass of macroalgae increased in spring and declined in summer, with maximum macroalgal abundance corresponding with average temperatures of between 22-24°C and average 24h PAR of 300-500 µmol qanta m-2 s-1. Changes in macroalgal biomass further influenced the composition and frequency of coral-algal interactions, however the incidence of coral-algal contact was best explained by coral cover. The results presented here emphasize that natural levels of macroalgae and coral-algal interactions are context -specific, and vary not only with-in zones, but in somewhat predictable seasonal cycles. Further, these results emphasize that the frequency of coral-algal interactions is dependent on hard coral, not just macroalgal cover, and an increase in coral-algal interactions does not necessarily translate to degradation of coral reefs.
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Carbon dioxide (CO2) emissions from fossil fuels and industry comprise ~90% of all CO2 emissions from human activities. For the last three years, such emissions were stable, despite continuing growth in the global economy. Many positive trends contributed to this unique hiatus, including reduced coal use in China and elsewhere, continuing gains in energy efficiency, and a boom in low-carbon renewables such as wind and solar. However, the temporary hiatus appears to have ended in 2017. For 2017, we project emissions growth of 2.0% (range: 0.8%−3.0%) from 2016 levels (leap-year adjusted), reaching a record 36.8 ± 2 Gt CO2. Economic projections suggest further emissions growth in 2018 is likely. Time is running out on our ability to keep global average temperature increases below 2 °C and, even more immediately, anything close to 1.5 °C.
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Shading substantially reduced the degree of bleaching in Acropora muricata, Pocillopora damicornis and Porites cylindrica in American Samoa. Experiments were conducted outdoors at two sites on Ofu and Tutuila Islands. An aquarium experiment was set up near some reef-flat pools in the National Park of American Samoa on Ofu Island, using different levels of shading (none, 50% and 75%) early in conditions of cumulative thermal stress corresponding to NOAA's Coral Reef Watch-Bleaching Alert System. We analyzed the effects of cumulative thermal stress regarding coral growth, as well as color changes (evaluated using a standardize reference card) as a proxy for decreases in symbiont density and chlorophyll a content (i.e. bleaching). Thermally stressed corals grew less than controls, but corals without shading experienced a more substantial decrease in growth compared to those under 50% or 75% shade. The analysis of coral color showed that both levels of shading were protective against bleaching in conditions of cumulative thermal stress for all species, but were particularly beneficial for the most sensitive ones: A. muricata and P. cylindrica. Heavier shading (75%) offered better protection than lighter shading (50%) in this experiment, possibly because of the intense light levels corals were subjected to. Although there were limits to the extent shading could mitigate the effects of cumulative heating, it was very effective to at least Degree Heating Week (DHW) 4 and continued to offer some protection until the end of the study (DHW 8). In Tutuila, a shaded/not-shaded platform experiment was carried out in a reef pool in which corals have shown repeated annual summer bleaching for several years. This experiment was designed to investigate if shading could attenuate bleaching in the field and also if there were negative consequences to shading removal. The only factor controlled was light intensity, and our main conclusion was that overall corals on the platform became darker than field colonies in response to shading, but adjusted back to the same color level as field colonies after shade removal. However, the latter results are preliminary and need to be confirmed by future studies under more controlled conditions. As bleaching becomes more frequent and regular due to global warming, we should consider proactively using shading to help mitigate the effects of thermal stress and prolong the survival of at least some coral communities, until solutions to address global climate change become effective.
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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.
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Coral reefs support immense biodiversity and provide important ecosystem services to many millions of people. Yet reefs are degrading rapidly in response to numerous anthropogenic drivers. In the coming centuries, reefs will run the gauntlet of climate change, and rising temperatures will transform them into new configurations, unlike anything observed previously by humans. Returning reefs to past configurations is no longer an option. Instead, the global challenge is to steer reefs through the Anthropocene era in a way that maintains their biological functions. Successful navigation of this transition will require radical changes in the science, management and governance of coral reefs.
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Many coral reefs have phase shifted from coral to macroalgal dominance. Ocean acidification (OA) due to elevated CO2 is hypothesised to advantage macroalgae over corals, contributing to these shifts, but the mechanisms affecting coral-macroalgal interactions under OA are unknown. Here, we show that (i) three common macroalgae are more damaging to a common coral when they compete under CO2 concentrations predicted to occur in 2050 and 2100 than under present-day conditions, (ii) that two macroalgae damage corals via allelopathy, and (iii) that one macroalga is allelopathic under conditions of elevated CO2, but not at ambient levels. Lipid-soluble, surface extracts from the macroalga Canistrocarpus (=Dictyota) cervicornis were significantly more damaging to the coral Acropora intermedia growing in the field if these extracts were from thalli grown under elevated vs ambient concentrations of CO2. Extracts from the macroalgae Chlorodesmis fastigiata and Amansia glomerata were not more potent when grown under elevated CO2. Our results demonstrate increasing OA advantages seaweeds over corals, that algal allelopathy can mediate coral-algal interactions, and that OA may enhance the allelopathy of some macroalgae. Other mechanisms also affect coral-macroalgal interactions under OA, and OA further suppresses the resilience of coral reefs suffering blooms of macroalgae.
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Herbivores greatly influence the productivity of algae but their impact can depend on the nuances of the timing, location, and intensity of herbivory. While plants can escape herbivory in spatial refugia, small-scale variations in habitat quality play a critical role in plant tolerance to herbivory and might generate complex trade-offs. On coral reefs, overstory branching corals provide a refuge from fish herbivory but also provide refugia for many small fish that excrete nutrients. Therefore, algae living in this habitat might also benefit from higher nutrient delivery. However, because coral branches occlude sunlight, algal growth rates might be impaired despite experiencing elevated nutrients and lower herbivory. In lab-based experiments, light, nutrients, and simulated herbivory were manipulated in summer and winter to investigate how these processes interact to influence the tolerance of herbivory in the calcifying green algae Halimeda, an important producer of reef carbonate sediments worldwide. Halimeda heteromorpha which is commonly found associated with branching corals tolerated tissue damage by increasing rates of segment production. Greater tolerance was observed at levels of light resembling those experienced under the coral’s canopy. Nutrient additions increased compensatory segment growth in winter but not summer. Levels of tolerance were seasonal and nutrient dependent. Results show that small-scale variations in habitat quality may influence tolerance to herbivory in Halimeda. This suggests that if coral habitats are degraded or lost and oceans continue to warm, a likely negative impact on Halimeda populations and its contribution to carbonate sediments could be expected if high levels of herbivory are maintained.
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Atmospheric pCO2 is predicted to rise from 400 to 900 ppm by year 2100, causing seawater temperature to increase by 1–4 °C and pH to decrease by 0.1–0.3. Sixty-day experiments were conducted to investigate the independent and combined impacts of acidification (pCO2 = 424–426, 888–940 ppm-v) and warming (T = 28, 32 °C) on calcification rate and skeletal morphology of the abundant and widespread Caribbean reef-building scleractinian coral Siderastrea siderea. Hierarchical linear mixed-effects modelling reveals that coral calcification rate was negatively impacted by both warming and acidification, with their combined effects yielding the most deleterious impact. Negative effects of warming (32 °C/424 ppm-v) and high-temperature acidification (32 °C/940 ppm-v) on calcification rate were apparent across both 30-day intervals of the experiment, while effects of low-temperature acidification (28 °C/888 ppm-v) were not apparent until the second 30-day interval—indicating delayed onset of acidification effects at lower temperatures. Notably, two measures of coral skeletal morphology–corallite height and corallite infilling–were negatively impacted by next-century acidification, but not by next-century warming. Therefore, while next-century ocean acidification and warming will reduce the rate at which corals build their skeletons, next-century acidification will also modify the morphology and, potentially, function of coral skeletons.
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The calcareous green alga Halimeda is a key contributor to carbonate sediment production on coral reefs. As herbivores have a direct negative effect on the abundance of Halimeda, protection from herbivory is critical for Halimeda growth. Branching corals such as Acropora are likely to provide refugia for Halimeda from grazers, yet studies are scarce. Here, we investigated the vulnerability of two Halimeda species to herbivory using fish exclusion cages and assessed the contribution of coral structural complexity to seasonal changes in Halimeda biomass and morphometrics. While up to 50 % Halimeda abundance was depleted outside cages due to herbivory and the exclusion of large herbivores resulted in an increase in net growth up to threefold, Halimeda recruitment was positively affected by herbivory, more than two times greater outside cages. However, these responses differed between species and seasons; only one species was affected in winter but not summer. Coral structural complexity facilitated an increase of total algal biomass particularly in summer. At the individual level, thalli growing inside the Acropora canopy were always significantly larger (thallus biomass, volume and height) than those growing in exposed areas. We estimated that the carbonate production of Halimeda was nearly three times greater inside refuges provided by Acropora. Because Halimeda species differ in growth rates and susceptibility to grazing, we predict that the ongoing degradation of the habitat complexity provided by branching corals will alter Halimeda community structure and its contribution to local sediment budgets.
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In the current global climate change scenario, stressors overlap in space and time, and knowledge on the effects of their interaction is highly needed to understand and predict the response and resilience of organisms. Corals, among many other benthic organisms, are affected by an increasing number of global change-related stressors including warming and invasive species. In this study, the cumulative effects between warming and invasive algae were experimentally assessed on the temperate reef-builder coral Cladocora caespitosa. We first investigated the potential local adaptation to thermal stress in two distant populations subjected to contrasting thermal and necrosis histories. No significant differences were found between populations. Colonies from both populations suffered no necrosis after long-term exposure to temperatures up to 29 °C. Second, we tested the effects of the interaction of both warming and the presence of invasive algae. The combined exposure triggered critical synergistic effects on photosynthetic efficiency and tissue necrosis. At the end of the experiment, over 90% of the colonies subjected to warming and invasive algae showed signs of necrosis. The results are of particular concern when considering the predicted increase of extreme climatic events and the spread of invasive species in the Mediterranean and other seas in the future.
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The physiological response to individual and combined stressors of elevated temperature and pCO2 were measured over a 24-day period in four Pacific corals and their respective symbionts (Acropora millepora/Symbiodinium C21a, Pocillopora damicornis/Symbiodinium C1c-d-t, Montipora monasteriata/Symbiodinium C15, and Turbinaria reniformis/Symbiodinium trenchii). Multivariate analyses indicated that elevated temperature played a greater role in altering physiological response, with the greatest degree of change occurring within M. monasteriata and T. reniformis. Algal cellular volume, protein, and lipid content all increased for M. monasteriata. Likewise, S. trenchii volume and protein content in T. reniformis also increased with temperature. Despite decreases in maximal photochemical efficiency, few changes in biochemical composition (i.e. lipids, proteins, and carbohydrates) or cellular volume occurred at high temperature in the two thermally sensitive symbionts C21a and C1c-d-t. Intracellular carbonic anhydrase transcript abundance increased with temperature in A. millepora but not in P. damicornis, possibly reflecting differences in host mitigated carbon supply during thermal stress. Importantly, our results show that the host and symbiont response to climate change differs considerably across species and that greater physiological plasticity in response to elevated temperature may be an important strategy distinguishing thermally tolerant vs. thermally sensitive species.
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The singular and interactive effects of ocean acidification and temperature on the physiology of calcified green algae (Halimeda incrassata, H. opuntia, and H. simulans) were investigated in a fully factorial, 4-week mesocosm experiment. Individual aquaria replicated treatment combinations of two pH levels (7.6 and 8.0) and two temperatures (28 and 31 °C). Rates of photosynthesis, respiration, and calcification were measured for all species both prior to and after treatment exposure. Pre-treatment measurements revealed that H. incrassata displayed higher biomass-normalized rates of photosynthesis and calcification (by 55 and 81 %, respectively) relative to H. simulans and H. opuntia. Furthermore, prior to treatment exposure, photosynthesis was positively correlated to calcification, suggesting that the latter process may be controlled by photosynthetic activity in this group. After treatment exposure, net photosynthesis was unaltered by pH, yet significantly increased with elevated temperature by 58, 38, and 37 % for H. incrassata, H. simulans, and H. opuntia, respectively. Both pH and temperature influenced calcification, but in opposing directions. On average, calcification declined by 41 % in response to pH reduction, but increased by 49 % in response to elevated temperature. Within each pH treatment, elevated temperature increased calcification by 23 % (at pH 8.0) and 74 % (at pH 7.6). Interactions between pH, temperature, and/or species were not observed. This work demonstrates that, in contrast to prior studies, increased temperature may serve to enhance the metabolic performance (photosynthesis and calcification) of some marine calcifiers, despite elevated carbon dioxide concentrations. Thus, in certain cases, ocean warming may mitigate the negative effects of acidification.
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Ocean acidification has been identified as a risk to marine ecosystems, and substantial scientific effort has been expended on investigating its effects, mostly in laboratory manipulation experiments. However, performing these manipulations correctly can be logistically difficult, and correctly designing experiments is complex, in part because of the rigorous requirements for manipulating and monitoring seawater carbonate chemistry. To assess the use of appropriate experimental design in ocean acidification research, 465 studies published between 1993 and 2014 were surveyed, focusing on the methods used to replicate experimental units. The proportion of studies that had interdependent or non-randomly interspersed treatment replicates, or did not report sufficient methodological details was 95%. Furthermore, 21% of studies did not provide any details of experimental design, 17% of studies otherwise segregated all the replicates for one treatment in one space, 15% of studies replicatedCO2 treatments in away that made replicates more interdependent within treatments than between treatments, and 13% of studies did not report if replicates of all treatments were randomly interspersed. As a consequence, the number of experimental units used per treatment in studies was low (mean ~ 2.0). In a comparable analysis, there was a significant decrease in the number of published studies that employed inappropriate chemical methods of manipulating seawater (i.e. acid–base only additions) from 21 to 3%, following the release of the “Guide to best practices for ocean acidification research and data reporting” in 2010; however, no such increase in the use of appropriate replication and experimental design was observed after 2010. We provide guidelines on how to design ocean acidification laboratory experiments that incorporate the rigorous requirements for monitoring and measuring carbonate chemistry with a level of replication that increases the chances of accurate detection of biological responses to ocean acidification.
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The historically unprecedented threats to the marine environment posed by increasing atmospheric carbon dioxide will probably require the use of unconventional, non-passive methods to conserve marine ecosystems. Soliciting such approaches and evaluating their cost, safety and effectiveness must be part of a robust ocean conservation and management plan going forward.
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Halimeda opuntia is a cosmopolitan marine calcifying green alga in shallow tropical marine environments. Besides Halimeda's contribution to a diverse habitat, the alga is an important sediment producer. Fallen calcareous segments of Halimeda spp. are a major component of carbonate sediments in many tropical settings and play an important role in reef framework development and carbonate platform buildup. Consequently the calcification of H. opuntia accounts for large portions of the carbonate budget in tropical shallow marine ecosystems. Earlier studies investigating the calcification processes of Halimeda spp. have tended to focus on the microstructure or the physiology of the alga, thus overlooking the interaction of physiological and abiotic processes behind the formation of the skeleton. By analyzing microstructural skeletal features of Halimeda segments with the aid of scanning electron microscopy and relating their occurrence to known physiological processes, we have been able to identify the initiation of calcification within an organic matrix and demonstrate that biologically induced cementation is an important process in calcification. For the first time, we propose a model for the calcification of Halimeda spp. that considers both the alga's physiology and the carbon chemistry of the seawater with respect to the development of different skeletal features. The presence of an organic matrix and earlier detected external carbonic anhydrase activity suggest that Halimeda spp. exhibit biotic precipitation of calcium carbonate, as many other species of marine organisms do. On the other hand, it is the formation of micro-anhedral carbonate through the alga's metabolism that leads to a cementation of living segments. Precisely, this process allows H. opuntia to contribute substantial amounts of carbonate sediments to tropical shallow seas.
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Anthropogenic increases in atmospheric CO2 over this century are predicted to cause global average surface ocean pH to decline by 0.1-0.3 pH units and sea surface temperature to increase by 1-4°C. We conducted controlled laboratory experiments to investigate the impacts of CO2-induced ocean acidification (pCO2 = 324, 477, 604, 2553 µatm) and warming (25, 28, 32°C) on the calcification rate of the zooxanthellate scleractinian coral Siderastrea siderea, a widespread, abundant and keystone reef-builder in the Caribbean Sea. We show that both acidification and warming cause a parabolic response in the calcification rate within this coral species. Moderate increases in pCO2 and warming, relative to near-present-day values, enhanced coral calcification, with calcification rates declining under the highest pCO2 and thermal conditions. Equivalent responses to acidification and warming were exhibited by colonies across reef zones and the parabolic nature of the corals' response to these stressors was evident across all three of the experiment's 30-day observational intervals. Furthermore, the warming projected by the Intergovernmental Panel on Climate Change for the end of the twenty-first century caused a fivefold decrease in the rate of coral calcification, while the acidification projected for the same interval had no statistically significant impact on the calcification rate-suggesting that ocean warming poses a more immediate threat than acidification for this important coral species.
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Seaweed–coral interactions are increasingly common on modern coral reefs, but the dynamics, processes, and mechanisms affecting these interactions are inadequately understood. We investigated the frequency and effect of seaweed–coral contacts for common seaweeds and corals in Belize. Effects on corals were evaluated by measuring the frequency and extent of bleaching when contacted by various seaweeds, and effects on a common seaweed were evaluated by assessing whether contact with coral made the seaweed more palatable to the sea urchin Diadema antillarum. Coral–seaweed contacts were particularly frequent between Agaricia corals and the seaweed Halimeda opuntia, with this interaction being associated with coral bleaching in 95 % of contacts. Pooling across all coral species, H. opuntia was the seaweed most commonly contacting corals and most frequently associated with localized bleaching at the point of contact. Articulated coralline algae, Halimeda tuna and Lobophora variegata also frequently contacted corals and were commonly associated with bleaching. The common corals Agaricia and Porites bleached with similar frequency when contacted by H. opuntia (95 and 90 %, respectively), but Agaricia experienced more damage than Porites when contacted by articulated coralline algae or H. tuna. When spatially paired individuals of H. opuntia that had been in contact with Agaricia and not in contact with any coral were collected from the reefs and offered to D. antillarum, urchins consumed about 150 % more of thalli that had been competing with Agaricia. Contact and non-contact thalli did not differ in nutritional traits (ash-free-dry-mass, C or N concentrations), suggesting that Halimeda chemical defenses may have been compromised by coral–algal contact. If competition with corals commonly enhances seaweed palatability, then the dynamics and nuances of small-scale seaweed–coral–herbivore interactions at coral edges are deserving of greater attention in that such interactions could scale-up to have important consequences for coral resilience and the persistence of reef structure and function.
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Despite the heightened awareness of ocean acidification (OA) effects on marine organisms, few studies empirically juxtapose biological responses to CO2 manipulations across functionally distinct primary producers, particularly benthic algae. Algal responses to OA may vary because increasing CO2 has the potential to fertilize photosynthesis but impair biomineralization. Using a series of repeated experiments on Palmyra Atoll, simulated OA effects were tested across a suite of ecologically important coral reef algae, including five fleshy and six calcareous species. Growth, calcification and photophysiology were measured for each species independently and metrics were combined from each experiment using a meta-analysis to examine overall trends across functional groups categorized as fleshy, upright calcareous, and crustose coralline algae (CCA). The magnitude of the effect of OA on algal growth response varied by species, but the direction was consistent within functional groups. Exposure to OA conditions generally enhanced growth in fleshy macroalgae, reduced net calcification in upright calcareous algae, and caused net dissolution in CCA. Additionally, three of the five fleshy seaweeds tested became reproductive upon exposure to OA conditions. There was no consistent effect of OA on algal photophysiology. Our study provides experimental evidence to support the hypothesis that OA will reduce the ability of calcareous algae to biomineralize. Further, we show that CO2 enrichment either will stimulate population or somatic growth in some species of fleshy macroalgae. Thus, our results suggest that projected OA conditions may favor non-calcifying algae and influence the relative dominance of fleshy macroalgae on reefs, perpetuating or exacerbating existing shifts in reef community structure.
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Tropical reefs are in global decline with seaweeds commonly replacing corals. Negative associations between macroalgae and corals are well documented, but the mechanisms involved, the dynamics of the interactions, and variance in effects of different macroalgal-coral pairings are poorly investigated. We assessed the frequency, magnitude, and dynamics of macroalgal-coral competition involving allelopathic and non-allelopathic macroalgae on three, spatially grouped pairs of no-take Marine Protected Areas (MPAs) and non-MPAs in Fiji. In non-MPAs, biomass of herbivorous fishes was 70-80% lower, macroalgal cover 4-9 fold higher, macroalgal-coral contacts 5-15 fold more frequent and 23-67 fold more extensive (measured as % of colony margin contacted by macroalgae), and coral cover 51-68% lower than in MPAs. Coral contacts with allelopathic macroalgae occurred less frequently than expected by chance across all sites, while contact with non-allelopathic macroalgae tended to occur more frequently than expected. Transplants of allelopathic macroalgae (Chlorodesmis fastigiata and Galaxaura filamentosa) against coral edges inflicted damage to Acropora aspera and Pocillopora damicornis more rapidly and extensively than to Porites cylindrica and Porites lobata, which appeared more resistant to these macroalgae. Montipora digitata experienced intermediate damage. Extent of damage from macroalgal contact was independent of coral colony size for each of the 10 macroalgal-coral pairings we established. When natural contacts with Galaxaura filamentosa were removed in the field, recovery was rapid for Porites lobata, but Pocillopora damicornis did not recover and damage continued to expand. As macroalgae increase on overfished tropical reefs, allelopathy could produce feedbacks that suppress coral resilience, prevent coral recovery, and promote the stability of algal beds in habitats previously available to corals.
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Rising atmospheric CO2 concentrations threaten coral reefs globally by causing ocean acidification (OA) and warming. Yet, the combined effects of elevated pCO2 and temperature on coral physiology and resilience remain poorly understood. While coral calcification and energy reserves are important health indicators, no studies to date have measured energy reserve pools (i.e., lipid, protein, and carbohydrate) together with calcification under OA conditions under different temperature scenarios. Four coral species, Acropora millepora, Montipora monasteriata, Pocillopora damicornis, Turbinaria reniformis, were reared under a total of six conditions for 3.5 weeks, representing three pCO2 levels (382, 607, 741 µatm), and two temperature regimes (26.5, 29.0°C) within each pCO2 level. After one month under experimental conditions, only A. millepora decreased calcification (-53%) in response to seawater pCO2 expected by the end of this century, whereas the other three species maintained calcification rates even when both pCO2 and temperature were elevated. Coral energy reserves showed mixed responses to elevated pCO2 and temperature, and were either unaffected or displayed nonlinear responses with both the lowest and highest concentrations often observed at the mid-pCO2 level of 607 µatm. Biweekly feeding may have helped corals maintain calcification rates and energy reserves under these conditions. Temperature often modulated the response of many aspects of coral physiology to OA, and both mitigated and worsened pCO2 effects. This demonstrates for the first time that coral energy reserves are generally not metabolized to sustain calcification under OA, which has important implications for coral health and bleaching resilience in a high-CO2 world. Overall, these findings suggest that some corals could be more resistant to simultaneously warming and acidifying oceans than previously expected.
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Significance The study explores the impact of anthropogenic ocean warming and acidification on intact coral reef assemblages using large-scale, replicated mesocosms that simulate future conditions under natural levels of seasonal variability.
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The effects of elevated CO2 and temperature on photosynthesis and calcification of two important calcifying reef algae (Halimeda macroloba and Halimeda cylindracea) were investigated with O2 microsensors and chlorophyll a fluorometry through a combination of two pCO2 (400 and 1,200 μatm) and two temperature treatments (28 and 32 °C) equivalent to the present and predicted conditions during the 2100 austral summer. Combined exposure to pCO2 and elevated temperature impaired calcification and photosynthesis in the two Halimeda species due to changes in the microenvironment around the algal segments and a reduction in physiological performance. There were no significant changes in controls over the 5-week experiment, but there was a 50–70 % decrease in photochemical efficiency (maximum quantum yield), a 70–80 % decrease in O2 production and a threefold reduction in calcification rate in the elevated CO2 and high temperature treatment. Calcification in these species is closely coupled with photosynthesis, such that a decrease in photosynthetic efficiency leads to a decrease in calcification. Although pH seems to be the main factor affecting Halimeda species, heat stress also has an impact on their photosystem II photochemical efficiency. There was a strong combined effect of elevated CO2 and temperature in both species, where exposure to elevated CO2 or temperature alone decreased photosynthesis and calcification, but exposure to both elevated CO2 and temperature caused a greater decline in photosynthesis and calcification than in each stress individually. Our study shows that ocean acidification and ocean warming are drivers of calcification and photosynthesis inhibition in Halimeda. Predicted climate change scenarios for 2100 would therefore severely affect the fitness of Halimeda, which can result in a strongly reduced production of carbonate sediments on coral reefs under such changed climate conditions.
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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 twelve 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 rates 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. This article is protected by copyright. All rights reserved.
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Competition between hard corals and macroalgae is a key ecological process on coral reefs, especially during reef degradation, which often involves a 'phase-shift' from coral- to alga-dominated reefs. However, there are relatively few published studies exploring the variability in this interaction. This paper expands the range of documented coral-algal interactions by comparing the mechanisms and outcomes of interactions involving 3 different algal species, as well as general, mixed algal turfs. Mixed filamentous turfs had relatively minor effects on corals. However, the turfing filamentous red alga Corallophila huysmansii provided a dramatic exception to this pattern, being able to settle on, overgrow and kill live coral tissue, perhaps due to allelochemical production by the alga, although this was not directly demonstrated. The larger filamentous alga Chlorodesmis fastigiata ('Turtle Weed'), which is conspicuous and abundant on Indo-Pacific reefs, caused polyp retraction but had little other noticeable effect on coral tissue. A corticated red alga Hypnea pannosa, frequently observed living within colonies of the branching coral Porites cylindrica, did not have a major impact on underlying coral tissue, even over a period of 1 yr, apparently because its relatively translucent and porous thallus structure does not strongly inhibit coral tissue functions. Together, the results demonstrate the considerable potential variability in both the process and outcome of coral-algal competition. This variability can be effectively interpreted in terms of the limited number of mechanisms by which algae can affect corals, with these mechanisms depending largely on the properties (physical, biological, chemical) of the algae. Given the central importance of coral-algal competition to the process of coral reef phase-shifts, understanding the variability and complexity in such competition will have important implications for the prediction and consequences of such phase-shifts.
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Ocean acidification represents a threat to marine species worldwide, and forecasting the ecological impacts of acidification is a high priority for science, management, and policy. As research on the topic expands at an exponential rate, a comprehensive understanding of the variability in organisms' responses and corresponding levels of certainty is necessary to forecast the ecological effects. Here, we perform the most comprehensive meta-analysis to date by synthesizing the results of 228 studies examining biological responses to ocean acidification. The results reveal decreased survival, calcification, growth, development and abundance in response to acidification when the broad range of marine organisms is pooled together. However, the magnitude of these responses varies among taxonomic groups, suggesting there is some predictable trait-based variation in sensitivity despite the investigation of approximately 100 new species in recent research. The results also reveal an enhanced sensitivity of mollusc larvae, but suggest that an enhanced sensitivity of early life history stages is not universal across all taxonomic groups. In addition, the variability in species' responses is enhanced when they are exposed to acidification in multi-species assemblages, suggesting it is important to consider indirect effects and exercise caution when forecasting abundance patterns from single species laboratory experiments. Furthermore, the results suggest that other factors, such as nutritional status or source population, could cause substantial variation in organisms' responses. Last, the results highlight a trend towards enhanced sensitivity to acidification when taxa are concurrently exposed to elevated seawater temperature. © 2013 Blackwell Publishing Ltd.
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The first decade of the new millennium saw a flurry of experiments to establish a mechanistic understanding of how climate change might transform the global biota, including marine organisms. However, the biophysical properties of the marine environment impose challenges to experiments, which can weaken their inference space. To facilitate strengthening the experimental evidence for possible ecological consequences of climate change, we reviewed the physical, biological and procedural scope of 110 marine climate change experiments published between 2000 and 2009. We found that 65% of these experiments only tested a single climate change factor (warming or acidification), 54% targeted temperate organisms, 58% were restricted to a single species and 73% to benthic invertebrates. In addition, 49% of the reviewed experiments had issues with the experimental design, principally related to replication of the main test‐factors (temperature or pH), and only 11% included field assessments of processes or associated patterns. Guiding future research by this inventory of current strengths and weaknesses will expand the overall inference space of marine climate change experiments. Specifically, increased effort is required in five areas: (i) the combined effects of concurrent climate and non‐climate stressors; (ii) responses of a broader range of species, particularly from tropical and polar regions as well as primary producers, pelagic invertebrates, and fish; (iii) species interactions and responses of species assemblages, (iv) reducing pseudo‐replication in controlled experiments; and (v) increasing realism in experiments through broad‐scale observations and field experiments. Attention in these areas will improve the generality and accuracy of our understanding of climate change as a driver of biological change in marine ecosystems.
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Ocean acidification represents a pervasive environmental change that is predicted to affect a wide range of species(1,2), yet our understanding of the emergent ecosystem impacts is very limited. Many studies report detrimental effects of acidification on single species in lab studies, especially those with calcareous shells or skeletons(3-5). Observational studies using naturally acidified ecosystems have shown profound shifts away from such calcareous species(6-8), and there has been an assumption that direct impacts of acidification on sensitive species drive most ecosystem responses. We tested an alternative hypothesis that species interactions attenuate or amplify the direct effects of acidification on individual species(9-12). Here, we show that altered competitive dynamics between calcareous species and fleshy seaweeds drive significant ecosystem shifts in acidified conditions. Although calcareous species recruited and grew at similar rates in ambient and low pH conditions during early successional stages, they were rapidly overgrown by fleshy seaweeds later in succession in low pH conditions. The altered competitive dynamics between calcareous species and fleshy seaweeds is probably the combined result of decreased growth rates of calcareous species, increased growth rates of fleshy seaweeds, and/or altered grazing rates(13). Phase shifts towards ecosystems dominated by fleshy seaweed are common in many marine ecosystems(14-16), and our results suggest that changes in the competitive balance between these groups represent a key leverage point through which the physiological responses of individual species to acidification could indirectly lead to profound ecosystem changes in an acidified ocean.
Article
Ocean acidification has been identified as a risk to marine ecosystems, and substantial scientific effort has been expended on investigating its effects, mostly in laboratory manipulation experiments. However, performing these manipulations correctly can be logistically difficult, and correctly designing experiments is complex, in part because of the rigorous requirements for manipulating and monitoring seawater carbonate chemistry. To assess the use of appropriate experimental design in ocean acidification research, 465 studies published between 1993 and 2014 were surveyed, focusing on the methods used to replicate experimental units. The proportion of studies that had interdependent or non-randomly interspersed treatment replicates, or did not report sufficient methodological details was 95%. Furthermore, 21% of studies did not provide any details of experimental design, 17% of studies otherwise segregated all the replicates for one treatment in one space, 15% of studies replicated CO2 treatments in a way that made replicates more interdependent within treatments than between treatments, and 13% of studies did not report if replicates of all treatments were randomly interspersed. As a consequence, the number of experimental units used per treatment in studies was low (mean ¼ 2.0). In a comparable analysis, there was a significant decrease in the number of published studies that employed inappropriate chemical methods of manipulating seawater (i.e. acid – base only additions) from 21 to 3%, following the release of the “Guide to best practices for ocean acidification research and data reporting” in 2010; however, no such increase in the use of appropriate replication and experimental design was observed after 2010. We provide guidelines on how to design ocean acidification laboratory experiments that incorporate the rigorous requirements for monitoring and measuring carbonate chemistry with a level of replication that increases the chances of accurate detection of biological responses to ocean acidification. © International Council for the Exploration of the Sea 2015. All rights reserved.
Article
Tropical reef systems are transitioning to a new era in which the interval between recurrent bouts of coral bleaching is too short for a full recovery of mature assemblages. We analyzed bleaching records at 100 globally distributed reef locations from 1980 to 2016. The median return time between pairs of severe bleaching events has diminished steadily since 1980 and is now only 6 years. As global warming has progressed, tropical sea surface temperatures are warmer now during current La Niña conditions than they were during El Niño events three decades ago. Consequently, as we transition to the Anthropocene, coral bleaching is occurring more frequently in all El Niño–Southern Oscillation phases, increasing the likelihood of annual bleaching in the coming decades.
Article
To evaluate the effects of ocean acidification (OA) and algal presence on the early life-history stages of corals, we conducted an aquarium study that examined the isolated and combined effects of reduced pH (pH 8.10 vs. 7.85) and contact with the alga Stypopodium zonale on the survival, settlement, and post-settlement growth of larvae from the brooding coral Porites astreoides. Two settlement substrates, biofilmed tiles and the crustose coralline alga (CCA) Hydrolithon boergesenii, were initially incubated for 12 d in separate tanks under a factorial combination of low pH and S. zonale contact, and then subjected to a series of settlement assays. Across both substrate types, S. zonale presence significantly reduced coral settlement. Low pH imposed relatively minor effects; however, there was a significant interaction between pH and S. zonale presence for settlement on the CCA substrate, such that low pH exacerbated the negative effects of S. zonale. Post-settlement growth for 2 wk was unaffected by either S. zonale or low pH on either substrate. While our results demonstrate that algal contact likely remains a dominant threat to larval survival and settlement, in certain cases, OA may amplify the negative effects of algal presence, highlighting the need to consider multiple factors in studies aimed at assessing the future health of coral reef ecosystems.
Book
This new edition to the classic book by ggplot2 creator Hadley Wickham highlights compatibility with knitr and RStudio. ggplot2 is a data visualization package for R that helps users create data graphics, including those that are multi-layered, with ease. With ggplot2, it's easy to: • produce handsome, publication-quality plots with automatic legends created from the plot specification • superimpose multiple layers (points, lines, maps, tiles, box plots) from different data sources with automatically adjusted common scales • add customizable smoothers that use powerful modeling capabilities of R, such as loess, linear models, generalized additive models, and robust regression • save any ggplot2 plot (or part thereof) for later modification or reuse • create custom themes that capture in-house or journal style requirements and that can easily be applied to multiple plots • approach a graph from a visual perspective, thinking about how each component of the data is represented on the final plot This book will be useful to everyone who has struggled with displaying data in an informative and attractive way. Some basic knowledge of R is necessary (e.g., importing data into R). ggplot2 is a mini-language specifically tailored for producing graphics, and you'll learn everything you need in the book. After reading this book you'll be able to produce graphics customized precisely for your problems, and you'll find it easy to get graphics out of your head and on to the screen or page. New to this edition:< • Brings the book up-to-date with ggplot2 1.0, including major updates to the theme system • New scales, stats and geoms added throughout • Additional practice exercises • A revised introduction that focuses on ggplot() instead of qplot() • Updated chapters on data and modeling using tidyr, dplyr and broom
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During 2015-2016, record temperatures triggered a pan-tropical episode of coral bleaching, the third global-scale event since mass bleaching was first documented in the 1980s. Here we examine how and why the severity of recurrent major bleaching events has varied at multiple scales, using aerial and underwater surveys of Australian reefs combined with satellite-derived sea surface temperatures. The distinctive geographic footprints of recurrent bleaching on the Great Barrier Reef in 1998, 2002 and 2016 were determined by the spatial pattern of sea temperatures in each year. Water quality and fishing pressure had minimal effect on the unprecedented bleaching in 2016, suggesting that local protection of reefs affords little or no resistance to extreme heat. Similarly, past exposure to bleaching in 1998 and 2002 did not lessen the severity of bleaching in 2016. Consequently, immediate global action to curb future warming is essential to secure a future for coral reefs.
Book
The first edition of this book has established itself as one of the leading references on generalized additive models (GAMs), and the only book on the topic to be introductory in nature with a wealth of practical examples and software implementation. It is self-contained, providing the necessary background in linear models, linear mixed models, and generalized linear models (GLMs), before presenting a balanced treatment of the theory and applications of GAMs and related models. The author bases his approach on a framework of penalized regression splines, and while firmly focused on the practical aspects of GAMs, discussions include fairly full explanations of the theory underlying the methods. Use of R software helps explain the theory and illustrates the practical application of the methodology. Each chapter contains an extensive set of exercises, with solutions in an appendix or in the book’s R data package gamair, to enable use as a course text or for self-study.
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The objective of this study was to investigate whether a tipping point exists in the calcification responses of coral reef calcifiers to CO2. We compared the effects of six partial pressures of CO2 (PCO2) from 28 Pa to 210 Pa on the net calcification of four corals (Acropora pulchra, Porites rus, Pocillopora damicornis, and Pavona cactus), and four calcified algae (Hydrolithon onkodes, Lithophyllum flavescens, Halimeda macroloba, and Halimeda minima). After 2 weeks of acclimation in a common environment, organisms were incubated in 12 aquaria for 2 weeks at the targeted PCO2 levels and net calcification was quantified. All eight species calcified at the highest PCO2 in which the calcium carbonate aragonite saturation state was ∼1. Calcification decreased linearly as a function of increasing partial PCO2 in three corals and three algae. Overall, the decrease in net calcification as a function of decreasing pH was ∼10% when ambient PCO2 (39 Pa) was doubled. The calcification responses of P. damicornis and H. macroloba were unaffected by increasing PCO2. These results are inconsistent with the notion that coral reefs will be affected by rising PCO2 in a response characterized by a tipping point. Instead, our findings combined among taxa suggest a gradual decline in calcification will occur, but this general response includes specific cases of complete resistance to rising PCO2. Together our results suggest that the overall response of coral reef communities to ocean acidification will be monotonic and inversely proportional to PCO2, with reef-wide responses dependent on the species composition of calcifying taxa.
Article
Many seaweeds and terrestrial plants induce chemical defences in response to herbivory, but whether they induce chemical defences against competitors (allelopathy) remains poorly understood. We evaluated whether two tropical seaweeds induce allelopathy in response to competition with a reef-building coral. We also assessed the effects of competition on seaweed growth and seaweed chemical defence against herbivores. Following 8 days of competition with the coral Porites cylindrica, the chemically rich seaweed Galaxaura filamentosa induced increased allelochemicals and became nearly twice as damaging to the coral. However, it also experienced significantly reduced growth and increased palatability to herbivores (because of reduced chemical defences). Under the same conditions, the seaweed Sargassum polycystum did not induce allelopathy and did not experience a change in growth or palatability. This is the first demonstration of induced allelopathy in a seaweed, or of competitors reducing seaweed chemical defences against herbivores. Our results suggest that the chemical ecology of coral-seaweed-herbivore interactions can be complex and nuanced, highlighting the need to incorporate greater ecological complexity into the study of chemical defence.
Article
Concern is growing about the potential effects of interacting multiple stressors, especially as the global climate changes. We provide a comprehensive review of multiple stressor interactions in coral reef ecosystems, which are widely considered to be one of the most sensitive ecosystems to global change. First, we synthesized coral reef studies that examined interactions of two or more stressors, highlighting stressor interactions (where one stressor directly influences another) and potentially synergistic effects on response variables (where two stressors interact to produce an effect that is greater than purely additive). For stressor-stressor interactions, we found studies that examined at least 2 of the 13 stressors of interest. Applying network analysis to analyze relationships between stressors, we found that pathogens were exacerbated by more co-stressors than any other stressor, with ~78% of studies reporting an enhancing effect by another stressor. Sedimentation, storms, and water temperature directly affected the largest number of other stressors. Pathogens, nutrients, and crown-of-thorns starfish were the most-influenced stressors. We found 187 studies that examined the effects of two or more stressors on a third dependent variable. The interaction of irradiance and temperature on corals has been the subject of more research (62 studies, 33% of the total) than any other combination of stressors, with many studies reporting a synergistic effect on coral symbiont photosynthetic performance (n=19). Second, we performed a quantitative meta-analysis of existing literature on this most-studied interaction (irradiance and temperature). We found that the mean effect size of combined treatments was statistically indistinguishable from a purely additive interaction, although it should be noted that the sample size was relatively small (n=26). Overall, although in aggregate a large body of literature examines stressor effects on coral reefs and coral organisms, considerable gaps remain for numerous stressor interactions and effects, and insufficient quantitative evidence exists to suggest that the prevailing type of stressor interaction is synergistic. This article is protected by copyright. All rights reserved.
Article
Halimeda opuntia and Diplosoma virens are common marine organisms in the Indo-Pacific. Halimeda grows to dense populations, and the ability of didemnids to overgrow coral has been well documented. In the light of their abundance in the Hikkaduwa Nature Park in Sri Lanka, this study investigated the effect of these two associates on the growth and survival of the commonly occurring staghorn coral, Acropora formosa. The results showed that both affected the growth rates of the host coral colonies significantly (P = 0.11 at 0.15 error level). The two associates also displayed a strong negative correlation between the spreading rate and the host growth rate (−0.71 for H. opuntia and −0.55 for D. virens). The results show that D. virens could have serious implications on coral survival with a population bloom.
Article
Tissue biomass (ash-free dry weight) and symbiotic dinoflagellates (density, chlorophyll a cell 21 or cm 22 of coral surface area) of five species of reef-building corals were monitored seasonally for up to 4 yr at three different depths in the Bahamas. The lowest values of all tissue biomass and algal symbiont parameters occurred during the late summer-fall sample periods. In contrast, the highest densities and pigment content of symbionts usually oc- curred during the winter, whereas tissue biomass peaked most often in the spring, the time lag implying a functional relationship between these variables. Corals living in shallow water often (but not always) had higher levels of all parameters measured compared to deeper corals, except chlorophyll a content, which usually displayed the opposite trend. The results show that corals from all depths exhibited bleaching (loss of symbiotic dinoflagellates and/or their pigments) every year, regardless of whether they appeared white, tan, or mottled to the human eye. We speculate that these patterns are driven by seasonal changes in light and temperature on algal and animal physiology. Furthermore, we hypothesize that all tropical reef-building corals, world-wide, exhibit similar predictable cycles in their tissue biomass and symbiotic algae.
Article
Coral reef recovery from major disturbance is hypothesized to depend on the arrival of propagules from nearby undisturbed reefs. Therefore, reefs isolated by distance or current patterns are thought to be highly vulnerable to catastrophic disturbance. We found that on an isolated reef system in north Western Australia, coral cover increased from 9% to 44% within 12 years of a coral bleaching event, despite a 94% reduction in larval supply for 6 years after the bleaching. The initial increase in coral cover was the result of high rates of growth and survival of remnant colonies, followed by a rapid increase in juvenile recruitment as colonies matured. We show that isolated reefs can recover from major disturbance, and that the benefits of their isolation from chronic anthropogenic pressures can outweigh the costs of limited connectivity.
Article
Studies on the distribution and photosynthetic chloroplast pigments of symbiotic zooxanthellae in the reef-building coral Montastrea annularis Ellis and Solander strongly suggest that photoadaptation to decreasing light intensity occurs within a population inhabiting the fore-reef of a West Indian (Jamaican) coral reef. It is suggested that the photoadaptation allows for the extension of the depth range of the species. The responses of M. annularis and its zooxanthellae to transplantation suggest that colonies have a certain capacity for modification when placed at different depths. The magnitude of these potential changes is small and colonies do not fare well in the transplant habitats. Such sub-optimal conditions are reflected in a decrease in algal density/cm2 living coral tissue, a decrease in zooxanthellar intracellular photosynthetic pigment concentration, and significant decreases in coral skeletal extension rates. Responses such as these are reasonably clear data in support of ecotypic variation and suggest that there are sun and shade populations of zooxanthellae in M. annularis.
Article
All reef-forming, or hermatypic, corals harbour photosynthetic endosymbiotic algae called zooxanthellae1–5, which are assumed to be predominantly a single dinoflagellate species, Gymnodinium microadriaticum Freudenthal6. The zooxan-thellae are essential for the well-being of their hosts7–9; nevertheless, little is known about how light affects the symbiotic association, especially regarding the numbers of zooxanthellae, their photosynthetic responses, and their overall productivity10–14. On the reefs of the Gulf of Eilat, Stylophora pistillata is an abundant hermatypic coral15; it is unique in that region in that it can adapt to a wide range of light intensities. In the high light intensities of lagoons or the upper areas of reefs, the corals are markedly lighter in colour than those living under ledges, in grottos, or near the reef floor (~ 15 m; Fig. 1). We report here on the biochemical and physiological adaptations of S. pistillata to variations in light intensity spanning more than two orders of magnitude.
Article
Experiments were conducted to establish the validity of the alkalinity anomaly technique for investigating rates of calcification and photosynthesis by coral reef-building organisms. Rates of CaCO sub(3) precipitation by whole colonies of the scleractinian coral Pocillopora damicornis) (L.) were estimated under light and dark conditions with two different methods: complexometric titration of Ca with EGTA and acid titration of total alkalinity, with and without correction for alterations in the concentrations of ions other than carbonate species. The two techniques provided equivalent estimates of light-enhanced and dark calcification, irrespective of whether corrections were applied to the total alkalinity data for changes in nutrient concentration. These results confirm that the assumptions of the alkalinity anomaly technique are fundamentally correct and that it is not necessary to correct total alkalinity data for changes in nutrient concentration because the corrections which apply are smaller than the variability observed in calcification data.
Article
Experiments are described in which tobacco (Nicotiana tabacum L.) transformed with antisense rbcS to decrease expression of ribulose-1,5-bisphosphate carboxylase-oxygenase (Rubisco) was used to evaluate the contribution of Rubisco to the control of photosynthetic rate, and the impact of a changed rate of photosynthesis on whole plant composition, allocation and growth. (1) The concept of flux control coefficients is introduced. It is discussed how, with adequate precautions, a set of wild-type and transgenic plants with varying expression of an enzyme can be used to obtain experimental values for its flux control coefficient. (2) The flux control coefficient of Rubisco for photosynthesis depends on the short-term conditions. It increases in high light, or low CO2. (3) When plants are grown under constant irradiance, the flux control coefficient in the growth conditions is low (<0.2) at irradiances of up to 1000μmol quanta m−2 s−1. In a natural irradiance regime exceeding 1500μmol quanta m−2 s−2 over several hours the flux coefficient rose to 0.8–0.9. It is concluded that plants are able to adjust the balance between Rubisco and the remainder of the photosynthetic machinery, and thereby avoid a one-sided limitation of photosynthesis by Rubisco over a wide range of ambient growth irradiance regimes. (4) When the plants were grown on limiting inorganic nitrogen, Rubisco had a higher flux control coefficient (0.5). It is proposed that, in many growth conditions, part of the investment in Rubisco may be viewed as a nitrogen store, albeit bringing additional marginal advantages with respect to photosynthetic rate and water use efficiency. (5) A change in the rate of photosynthesis did not automatically translate into a change in growth rate. Several factors are identified which contribute to this buffering of growth against a changed photosynthetic rate. (6) There is an alteration in whole plant allocation, resulting in an increase in the leaf area ratio. The increase is mainly due to a higher leaf water content, and not to changes in shoot/root allocation. This increased investment in whole plant leaf area partly counteracts the decreased efficiency of photosynthesis at the biochemical level. (7) Plants with decreased Rubisco have a lower intrinsic water use efficiency and contain high levels of inorganic cations and anions. It is proposed that these are a consequence of the increased rate of transpiration, and that the resulting osmotic potential might be a contributory factor to the increased water content and expansion of the leaves. (8) Starch accumulation in source leaves is decreased when unit leaf photosynthesis is reduced, allowing a more efficient use of the fixed carbon. (9) Decreased availability of carbohydrates leads to a down-regulation of nitrate assimilation, acting via a decrease in nitrate reductase activity.