Table 4.3: Summary of effects of treatment variables on response parameters forA. milleporaandH.
opuntia. Decreases > 100% are possible due to decalcification. ‘ns’ indicates no significant treatment effect, ‘measured additive effects’ represent differences of means between the control pCO2/high light and high pCO2/low light treatment
Response parameter Species pCO2 Light Predicted additive effect Measured additive effect
Growth A. millepora - 48% - 96% - 144% - 114%
H. opuntia ns ns ns ns
Net calcification A. millepora - 57% - 99% - 156% - 127%
H. opuntia ns ns ns ns
Light calcification A. millepora ns - 83% ns ns
H. opuntia ns ns ns ns
Dark calcification A. millepora - 155% - 155% - 310% - 204%
H. opuntia - 164% ns ns ns
Gross photosynthesis A. millepora ns - 56% ns ns
H. opuntia ns - 57% ns ns
Net photosynthesis A. millepora ns - 62% ns ns
H. opuntia ns - 60% ns ns
Respiration A. millepora ns - 43% ns ns
H. opuntia ns - 48% ns ns
Chlorophyll a content A. millepora ns ns ns ns
H. opuntia ns - 15% ns ns
of corals in a high pCO2 environment (Schneider and Erez 2006; Marubini et al. 2008). Due to a de-crease ofΩarin OA conditions, many organisms become impaired in building CaCO3skeletons (Raven et al. 2005; Kleypas and Langdon 2006; Hoegh-Guldberg et al. 2007). In contrast,H. opuntiashowed no significant trend on growth rates in relation toΩar/pCO2. Some previous studies suggest thatHalimeda spp. may be impacted in future OA conditions, showing reduced growth in elevated pCO2 (Ries et al.
2009; Price et al. 2011; Sinutok et al. 2011). However, similar to corals,Halimedaspp. exhibit different growth forms with associated morphological distinctions.Halimedaspp. occur as heavily calcified and less calcified species, sand-dwellers and rock-anchored species as well as species with different sizes and shapes of phylloids. Halimedaspp. with smaller phylloids have a higher surface to volume ratio than with larger phylloids and hence have a higher exposure to their physical environment. As shown by Comeau et al. (2013b),Halimeda macrolobashowed no impact of increased pCO2on calcification, butHalimeda minimashowed reduced calcification in elevated pCO2. However, different outcomes may also arise from different methodologies implemented such as flow conditions, nutrient availability, size of organisms, level of pCO2 condition implemented, or combinations of different stressors (e.g. OA and OW). The impact of elevated pCO2 on growth ofH. opuntia in Price et al. (2011) compared to the lack of response to elevated pCO2 in the present study is unclear. We propose that different results mainly arose due to different methodologies being implemented. The present study used flow-through conditions with constant supply of fresh filtered seawater and associated nutrients, while in Price et al.
(2011), 0.7 L tanks were utilized with water exchange every 48 h, not accounting for nutrient depletion.
Moreover, daily light sums of control light in the present study were considerably higher and closer to natural light conditions than reduced natural light regimes in Price et al. (2011), where light maxima at mid-day averaged 150 µmol photons m−2 s−1. In the present study we chose a pCO2 level which is likely to be reached by the year 2100 under projections between the RCP6.0 and RCP8.5 scenario (Moss et al. 2010), the experimental setup provided flow-through conditions with continuous supply of nutrients and light regimes naturally found on mid-shelf and inshore locations of the GBR, at 5 m below LAT. One potential explanation for whyH. opuntiais capable of growth in a high pCO2 environment whileA. milleporais not may be that calcification rates in Halimedaspp. are generally higher than in corals (when both standardized to either surface area or buoyant weight). ForH. opuntia, daytime calci-fication rates were approximately one order of magnitude higher than dissolution rates in the dark under elevated pCO2 conditions. Thus, even when some dissolution is taking place in the dark, higher light calcification rates sum up to positive net calcification rates. In contrast, forA. milleporadark dissolution and light calcification rate were in a similar range, indicating net dissolution if impacts of future OA and low light conditions become additive (Table 4.3).
Notably, light calcification rates of both organisms, determined using the alkalinity anomaly
tech-nique, were unaffected by increased pCO2. To our knowledge, this is the first study to show that calci-fication ofA. milleporaandH. opuntiain elevated pCO2 is not impacted during the light and supports the assumption that during the light, photosynthetic activity can counteract negative impacts of OA by increasing intracellular, surface and boundary-layer pH. By utilizing CO2, photosynthesis increases pH andΩar(de Beer et al. 2000; de Beer and Larkum 2001; Glas et al. 2012). As shown by Al-Horani et al.
(2003), pH increases under the calcioblastic layer of corals in light, which elevated the super saturation ofΩarfrom 3.2 up to 25, facilitating deposition of CaCO3(Goreau 1959; Al-Horani et al. 2003).
However, the present study also suggested that for dark calcification rates, the opposite effect is the case. During respiration in the dark, additional CO2 further reduces pH and Ωar (already lowered by OA) and impedes deposition of CaCO3. Hence, in the absence of light, both organisms were strongly negatively impacted by high pCO2conditions, leading to dissolution of their skeleton. In contrast, under present-day conditions both organisms can calcify in the dark (i.e. in the absence of photosynthesis).
This observation is in agreement with a previous study, showing decalcification ofAcropora eurystoma in high pCO2and darkness, while CaCO3 was still deposited under control conditions or in high pCO2 during light (Schneider and Erez 2006). Previous studies have also shown that reef communities can change the diurnal local seawater carbonate chemistry by photosynthesis, respiration, calcification and dissolution and that CaCO3dissolution is primarily taking place during the dark (Chisholm 2000; Lang-don and Atkinson 2005; Kleypas et al. 2011; Anthony et al. 2013). While respiration is taking place during the dark, additional CO2is added to the carbonate system and already lowered pH levels from OA are further reduced, leading to an additional reduction ofΩaras already provoked by OA. Consequently, A. millepora andH. opuntia were incapable of depositing CaCO3 in the dark and even experienced dissolution of their skeletons under these conditions.
Considering the negative impacts of OA in darkness, we demonstrated that low light conditions may likewise result in additional negative implications on organisms, once PAR is reduced below a level at which photosynthesis cannot buffer reduced pH by OA. Presumably, this threshold level is below 35 µmol photons m−2 s−1 as tested in the present study. As shown in the present study by measurements during the light, OA showed no impact on calcification rates of either organism. Thus, the availability of sufficient light, associated with photosynthetic activity and apparent buffer capacity, mitigated neg-ative effects of OA during light incubations. However, turbidity decreases PAR and therefore reduces the capability of the organisms’ photosynthesis to buffer the negative impacts of OA, even during the day. As shown by our O2flux measurements, low light regimes significantly decreased gross- and net photosynthesis in both organisms. This enhances negative impacts of OA during the day, especially at inshore reefs, where riverine runoff leads to reduced PAR (Devlin and Schaffelke 2009). Light data from mid-shelf and inshore GBR reefs at 5 m below LAT show that light availability can be extremely reduced
at inshore reefs, considerably impacting organisms’ photosynthetic capacities. Moreover, reduced pho-tosynthetic activity of organisms experiencing reduced light availability may also change DIC/carbonate chemistry on inshore reefs compared to mid-shelf locations. Under low light conditions, mean growth rates of both the coral and algae were reduced compared to higher light. Light enhanced photosynthesis and calcification of coral and algae is a well-documented phenomenon (Goreau 1959; Chalker and Tay-lor 1975; Chalker 1981; de Beer et al. 2000; de Beer and Larkum 2001). With increasing OA and the additive negative effects of low light on coral growth, as demonstrated in the present study, the mech-anism of light enhanced calcification may gain in importance. Moreover, under lower light conditions, when photosynthetic activity is reduced, organisms obtain less energy supply, thus reducing the scope for growth.
Photosynthesis of algae and coral can be limited by dissolved inorganic carbon (DIC) availabil-ity (Borowitzka and Larkum 1976; de Beer and Larkum 2001; Marubini et al. 2008; Crawley et al.
2010; Chauvin et al. 2011). Carbonic anhydrase can utilize elevated bicarbonate availability to in-crease the CO2 pool available for photosynthetic activity. Thus we assumed that photosynthesis could be enhanced under higher pCO2. However, photosynthesis of the organisms investigated here could not benefit from increased DIC concentrations. This may have two different reasons: (1) the organisms were not DIC-limited in experimental control conditions; (2) under present light conditions, photo-synthesis/calcification of organisms was not saturated and hence there was no detectable benefit from increased DIC availability. Studies indicating DIC limitation conducted by Marubini et al. (2008) and Crawley et al. (2010) both utilized higher light intensities than the present study (∼300 and∼1000 µmol photons m−2 s−1 respectively). This suggests that under present experimental conditions (i.e. present light intensities) calcification and photosynthesis were not DIC-limited.
Moreover, we showed that in decreased PAR,H. opuntiaincreased its tissue Chlacontent in order to compensate for less light availability, while the coral was not able to do so over the period of the experiment. By adjusting its Chla content the alga might acclimatize to reduced light availability in the short term, and increase its photosynthetic capacity in low light. Increased productivity changes the carbonate chemistry to the advantage of the algae, by facilitating deposition of CaCO3. In contrast,A.
milleporadid not have this advantage because it could not increase Chlaover the 16 days experimental period and thus may not be able to acclimate in the short term to decreased light availability. As shown by previous studies, corals alter their Chlacontent by having either, a higher number of zooxanthellae per unit area, or by an increase of Chlacontent in the zooxanthellae (Coles and Jokiel 1978; Chauvin et al. 2011). Field data suggest thatA. milleporashow increased pigmentation with decreasing water clarity from mid-shelf to inshore (Fabricius 2006). However, this might also be a response towards a more chronic exposure to low light conditions and other water quality parameters (i.e. increased
nutrient availability at inshore reefs). Therefore, the algae may show more immediate responses towards changing light regimes and thus have an advantage in acclimatization compared to the coral.
A. millepora andH. opuntia did not exhibit significant interactive effects on response parameters measured, which is an indication that effects were not synergistic (Dunne 2010). Similarly, Comeau et al. (2013a) and Comeau et al. (2014) found no interactive effects of OA and irradiance on calcification rates ofPorites rusandAcropora pulchra, respectively after three weeks exposure to experimental con-ditions. In contrast, a study onPocillopora damicornisrecruits presented interactive effects of OA and light after 5 days of experimentation (Dufault et al. 2013). However, the responses were non-linear and impacts of OA on calcification rates were only found at intermediate light intensities (70 µmol photons m−2s−1) and not at lower or higher light levels (31, 41, 122 and 226 µmol photons m−2s−1). Moreover, a study onAcropora horrida andPorites cylindricashowed impacts of OA on calcification that were greatest during light calcification of corals grown in lower light conditions (100 µmol photons m−2s−1) compared to corals grown in higher light (400 µmol photons m−2 s−1) after 5 weeks (Suggett et al.
2013). This is unexpected and in contrast to the present study, where the impact of OA on calcification was not significant in the light, but was strong in the dark. In the present studyA. millepora did not show interactive effects of OA and light; however, there were additive effects of both stressors. We detected reduced growth rates (−48%) when exposed to high pCO2conditions and also reduced growth rates when exposed to low light regimes (−96%), which resulted in a predicted additive growth rate of
−144% (which is similar to the measured−114% growth rate) (Table 4.3). This may have an ecological implication for corals inhabiting inshore reefs susceptible to land-runoff and thus decreased light avail-ability. Turbidity changes the attenuation of light penetrating the water column decreasing PAR with increasing depth more rapidly than in clear water conditions. This, in turn, may lead to a stronger depth limitation for corals and thus to potential habitat decline in future OA conditions, because they gain less light with lower water depth, compared to clear water habitats.
Conclusions
In the present experiment, we confirmed that the marine calcifiers investigated are negatively impacted by OA, withA. milleporashowing more negative impacts than H. opuntia. As long as sufficient light is available during the day, photosynthesis aids organisms to counteract negative impacts of OA. How-ever, if there is not sufficient light available (e.g. due to high turbidity), there may be impacts of OA on calcification also during the day. Thus, low light conditions inshore remove this advantage from pho-tosynthesizing organisms. As suggested by the dark incubations, respiration potentially aggravates the impacts of OA on the organisms, leading to dissolution of their skeleton. This highlights the importance of considering light-dependent impacts of OA on photosynthesizing calcifiers. Moreover, we showed
that decreased light availability is an additive stressor with OA, particularly for the coralA. millepora, because the coral exhibits reduced calcification in OA conditions as well as in low light conditions. H.
opuntia, on the other hand, grows marginally less in low light, but was not negatively impacted by OA in its overall growth. Consequently, the combination of OA and low light conditions may contribute to a changing coral reef ecosystem with even less hard corals as framework builders and more macroalgae on inshore reefs of the future. Potential acclimatization to environmental stressors in the long term could lead to different responses of organisms. Therefore, further investigations are needed to test the effects of OA in combination with light availability on coral reef organisms. Management of coastal runoff could also play an important role, as by improving water clarity on inshore reefs the additional stressor of low light availability for corals would be reduced.
Acknowledgments
The authors thank the SeaSim team at AIMS for providing the coral nubbins and their general assis-tance. We thank Michelle Liddy for her assistance in the field and laboratory. Many thanks for general assistance from Florita Flores. We acknowledge the National Environmental Research Program, which provided the stipend for Nikolas Vogel. This study was conducted with the support of funding from the Australian Government’s National Environmental Research Program and an Australian Research Council Discovery Grant.
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Effects of elevated dissolved inorganic carbon and nitrogen on the physiology of scleractinian corals and calcareous
macroalgae under ocean acidification and eutrophication conditions
Nikolas Vogel1,2,3, Yan Ow1,4, Florita Flores1, Catherine Collier4, Christian Wild2,3and Sven Uthicke
1
(1)Australian Institute of Marine Science, PMB 3, Townsville MC, Queensland 4810, Australia
(2)Leibniz Center for Tropical Marine Ecology, Fahrenheitstraße 6, 28359 Bremen, Germany
(3)Faculty of Biology and Chemistry (FB 2), University of Bremen, 28359 Bremen, Germany
(4)School of Marine and Tropical Biology, James Cook University, Townsville, Australia
Keywords: Nitrate, dissolved inorganic nutrients,Acropora tenuis,Seriatopora hystrix,Halimeda op-untia
This publication is in preparation
Abstract
Global (i.e. ocean acidification, OA) and local (i.e. eutrophication) stressors can have deleterious effects on coral reef organisms and their communities. On the other hand, calcifying and photosynthesizing organisms can be limited by dissolved inorganic carbon (DIC), or nutrient (DIN) concentrations in sea-water. Thus, increases of DIC under OA conditions and increases of DIN under eutrophication condi-tions may differentially affect the physiology of calcifying organisms. In a three week tank experiment, we investigated the individual and combined effects of DIC (∼400, 700, 1100 µatm pCO2) and DIN (0.4 and 1.9 µmol L−1 NO2 + NO3) on growth, calcification, photosynthesis, nutrient uptake, pigment content, protein content and carbon and nitrogen content of the scleractinian coralsAcropora tenuisand Seriatopora hystrixand the calcareous green algaHalimeda opuntia. Contrary to expectations, elevated DIC did not significantly affect any response parameter. We propose that the lack of responses to high DIC observed in corals, as opposed to some previous experiments, may be due to slower response times under close-to-natural experimental conditions as those used in the present experiment. Elevated DIN increased photosynthesis, nitrate uptake rates and pigment contents of the organisms investigated. More-over, forS. hystrixandH. opuntiawe observed an increased organic fraction, indicating an imbalanced growth between organic tissue and inorganic skeleton under elevated DIN. No significant interactions between elevated DIC and DIN were observed. Meanwhile, all experimental species showed strong physiological responses towards elevated DIN. Thus, organisms living in habitats affected by coastal runoff may rapidly respond to short-term pulses in DIN concentrations, accompanied by physiological alterations which may make some of them more susceptible to other environmental stressors.