0481216 400 µ
atm 700 µ
atm 1100 µ
atm 0.4 µ
mol 1.9 µ
mol
Treatment Chl a [µg cm-2]
A. tenius
0481216
400 µ atm
700 µ atm
1100 µ atm 0.4 µ
mol 1.9 µ
mol
Treatment S. hystrix
200300400500
400 µ atm 700 µ
atm 1100 µ
atm 0.4 µ
mol 1.9 µ
mol
Treatment Chl a [µg gFW-1]
H. opuntia
Figure 5.5: Chlorophyllacontent ofA. tenuis,S. hystrixandH. opuntiaafter three weeks experimental treatment. X-axes represent pCO2treatments in µatm and DIN treatments in µmol L−1NOx. Whiskers represent upper and lower extremes. Plots illustrate pooled data, due to non-significant interactions
calci-0.00.40.81.2 400 µ
atm 700 µ
atm 1100 µ
atm 0.4 µ
mol 1.9 µ
mol
Treatment Total protein content [mg cm-2]
A. tenius
0.00.40.81.2
400 µ atm
700 µ atm
1100 µ atm 0.4 µ
mol 1.9 µ
mol
Treatment S. hystrix
Figure 5.6: Total protein content ofA. tenuis andS. hystrix after three weeks experimental treatment.
X-axes represent pCO2treatments in µatm and DIN treatments in µmol L−1 NOx. Whiskers represent upper and lower extremes. Plots illustrate pooled data, due to non-significant interactions
fication ofA. tenuis,S. hystrix, orH. opuntia. While this observation agrees with previous studies on calcareous algaHalimedaspp., includingH. opuntia(Comeau et al. 2013; Hofmann et al. 2014; Vogel et al. 2015b; Vogel et al. 2015a), this result was somewhat unexpected for coralsA. tenuisandS. hystrix.
Previous literature indicated impacts of OA on calcification of several scleractinian corals, including the generaAcropora, after short-term (4 weeks) exposure to∼800 µatm pCO2(e.g. Renegar and Riegl 2005) andSeriatoporaafter life-long exposure to∼800 µatm pCO2(Strahl et al. pers. comm.). Why we did not see any impacts of OA on corals is unclear, but perhapsA. tenuisandS. hystrixdo not respond to OA in the short term. Several important differences exist between other studies and ours, such as artificial vs. natural light regimes, filtered vs. unfiltered seawater, or high vs. low nutrient background levels. For instance, temperatures in the present experiment were higher than in the study by Renegar and Riegl (2005). Calcification increases with temperatures andΩar(Silverman et al. 2007) which may have contributed to the observed differences between the two studies. In addition, experimental tanks in the present study were supplied with flow-through unfiltered reef seawater, while the other study uti-lized filtered seawater without continuous exchange (Renegar and Riegl 2005). Heterotrophic nutrition from unfiltered reef seawater used in the present experiment may have enhanced the nutritional status of corals. Higher energy levels may have enabled the corals to actively regulate internal pH levels to protect themselves against OA impacts, which is consistent with previous studies showing that energy levels can alleviate responses to other stressors such as warming (Fabricius et al. 2013). Moreover, the light intensity has been shown to affect responses coral reef organisms to OA (Vogel et al. 2015b). Natu-ral variable light regimes in the present study may have contributed to the high variability in growth/net calcification data, hence weakening the OA effects. Thus, other environmental factors, may affect the
481216 Corg
H. opuntia
0.40.81.21.6Total nitrogen 5.07.510.012.5
Cinorg 810121416
400 µ atm
700 µ atm
1100 µ atm
0.4 µ mol
1.9 µ mol
Treatment
C:N ratio
Figure 5.7: Organic carbon, nitrogen, inorganic carbon and C:N ratio ofH. opuntiaafter three weeks experimental treatment. X-axes represent pCO2 treatments in µatm and DIN treatments in µmol L−1 NOx. Whiskers represent upper and lower extremes. Plots illustrate pooled data, due to non-significant interactions
Table 5.3: Mixed Model ANOVA results of OA and elevated DIN on response parameters of organisms investigated. Asterisks indicate significant treatment effects
A. tenuis S. hystrix H. opuntia
Response variable
Source of variation
df F p df F p df F p
Growth pCO2 2 1.89 0.194 2 0.69 0.518 2 2.63 0.113 DIN 1 0.31 0.588 1 1.30 0.277 1 0.42 0.529 pCO2:DIN 2 0.23 0.798 2 2.12 0.163 2 0.24 0.793 Tank 12 3.03 0.004 12 1.08 0.401 12 0.75 0.696
Residuals 44 46 31
Light pCO2 2 0.14 0.875 2 0.14 0.873 2 3.11 0.082 calcification DIN 1 2.12 0.171 1 0.10 0.757 1 3.27 0.095 pCO2:DIN 2 0.42 0.663 2 0.08 0.921 2 0.65 0.538 Tank 12 0.88 0.580 12 2.37 0.047* 12 1.65 0.164
Residuals 18 18 18
Dark pCO2 2 0.67 0.531 2 0.81 0.469 2 2.75 0.104 calcification DIN 1 0.13 0.725 1 0.10 0.761 1 0.00 0.974 pCO2:DIN 2 0.27 0.772 2 0.05 0.949 2 0.94 0.419 Tank 11 2.13 0.078 12 8.45 < 0.001 12 3.01 0.020*
Residuals 17 17 17
Net pCO2 2 0.22 0.807 2 0.46 0.642 2 2.48 0.125 calcification DIN 1 1.39 0.264 1 0.00 0.999 1 2.05 0.178 pCO2:DIN 2 0.36 0.707 2 0.06 0.945 2 0.70 0.515 Tank 11 0.99 0.497 12 4.59 0.002* 12 1.69 0.161
Residuals 17 17 16
Net pCO2 2 2.19 0.154 2 0.20 0.818 2 2.61 0.114 photosynthesis DIN 1 3.21 0.098 1 18.11 0.001* 1 8.93 0.011*
pCO2:DIN 2 1.25 0.321 2 0.28 0.759 2 0.81 0.466 Tank 12 1.12 0.400 12 1.23 0.338 12 0.90 0.563
Residuals 18 18 16
Respiration pCO2 2 0.22 0.806 2 0.85 0.451 2 1.84 0.201 DIN 1 0.18 0.677 1 9.23 0.010* 1 2.90 0.114 pCO2:DIN 2 0.23 0.795 2 0.73 0.503 2 2.00 0.178 Tank 12 2.35 0.053 12 0.89 0.575 12 2.05 0.085
Residuals 17 17 17
Gross pCO2 2 1.72 0.223 2 0.11 0.899 2 2.35 0.141 photosynthesis DIN 1 2.31 0.157 1 17.57 0.002* 1 7.70 0.018*
pCO2:DIN 2 1.04 0.387 2 0.30 0.745 2 0.74 0.497 Tank 11 1.07 0.438 11 1.11 0.412 11 1.03 0.464
Residuals 17 17 15
responses of calcifying coral reef organisms to OA. But recent studies also reported resilience of several scleractinian coral species to OA, suggesting species-specific and regional scale variation in responses of organisms towards OA (Comeau et al. 2014).
Effects of DIN
As nitrate concentrations were elevated, the investigated organisms generally showed increased NOx uptake in darkness and in calculated net NOxuptake over 24 h. These results, accompanied with nitrate effects on other response parameters, suggest that the investigated organisms were nutrient limited in ambient concentrations and were able to utilize the additionally available nitrate in elevated
concen-Table 5.4: Continuation of Mixed Model ANOVA results of OA and elevated DIN on response parame-ters of organisms investigated. Asterisks indicate significant treatment effects
A. tenuis S. hystrix H. opuntia
Response variable
Source of variation
df F p df F p df F p
Light pCO2 2 2.37 0.135 2 4.95 0.027* 2 1.54 0.253 NOx flux DIN 1 1.55 0.238 1 2.23 0.161 1 4.14 0.065 pCO2:DIN 2 1.26 0.320 2 2.82 0.099 2 0.39 0.686 Tank 11 5.88 < 0.001* 12 3.53 0.010* 12 2.96 0.019*
Residuals 17 16 18
Dark pCO2 2 0.31 0.741 2 0.16 0.856 2 1.95 0.185 NOx flux DIN 1 16.05 0.002* 1 20.00 0.001* 1 6.22 0.028*
pCO2:DIN 2 0.24 0.790 2 1.11 0.362 2 0.14 0.873 Tank 12 1.19 0.362 12 1.12 0.411 12 5.06 0.002*
Residuals 17 16 16
Net pCO2 2 2.61 0.115 2 1.54 0.255 2 1.64 0.235 NOx flux DIN 1 6.56 0.025* 1 2.09 0.174 1 5.58 0.036*
pCO2:DIN 2 1.42 0.279 2 1.03 0.386 2 0.36 0.703 Tank 12 4.27 0.004* 12 3.52 0.010* 12 4.14 0.003*
Residuals 16 16 18
Chl a pCO2 2 0.48 0.628 2 0.76 0.491 2 1.48 0.266 DIN 1 50.61 < 0.001* 1 28.93 < 0.001* 1 10.36 0.007*
pCO2:DIN 2 1.21 0.331 2 9.24 0.004* 2 0.61 0.560 Tank 12 0.59 0.838 12 1.06 0.424 12 2.21 0.035*
Residuals 36 35 33
Protein pCO2 2 1.68 0.227 2 0.23 0.795 content DIN 1 0.27 0.613 1 4.92 0.047*
pCO2:DIN 2 2.00 0.178 2 1.58 0.247 Tank 12 0.50 0.899 12 1.04 0.440
Residuals 36 34
Corg pCO2 2 1.65 0.232
DIN 1 6.66 0.024*
pCO2:DIN 2 0.92 0.424
Tank 12 1.43 0.201
Residuals 33
Cinorg pCO2 2 0.28 0.763
DIN 1 4.45 0.057
pCO2:DIN 2 3.38 0.068
Tank 12 0.87 0.582
Residuals 33
N pCO2 2 1.12 0.358
DIN 1 17.71 0.001*
pCO2:DIN 2 1.51 0.261
Tank 12 1.62 0.135
Residuals 33
C:N pCO2 2 1.78 0.210
DIN 1 30.45 < 0.001*
pCO2:DIN 2 2.38 0.135
Tank 12 1.31 0.257
Residuals 33
trations. Coral nitrate uptake rates were in a similar range as determined in a previous study in-situ for Acropora palmataby Bythell (1990). The latter study also showed a linear trend between nitrate concentrations and uptake rates, suggesting corals/zooxanthellae are nitrate limited under naturally oc-curring concentrations (0.22-1.72 µmol L−1NO3–). Moreover, limited nutrient uptake rate ofH. opuntia in ambient conditions agrees with a study by Abel, Drew, et al. (1985), who showed nitrate uptake ofH.
opuntiasaturated around 13 µM NO3–.
An increase in photosynthesis under elevated nitrate, as observed forA. tenuisandH. opuntiain the present study, has also been reported for several other scleractinian corals (Tanaka et al. 2007; Chauvin et al. 2011) and calcareous algae includingH. opuntia(Littler et al. 1988; Delgado and Lapointe 1994).
These studies attributed increased zooxanthellae density and pigment content to increased light capture and photosynthetic rates. Contrary, results from Ferrier-Pagès et al. (2001) showed no nitrate effects (<1 µM and 2 µM) on zooxanthellae density or photosynthesis of the coral Stylophora pistillata, in-dicating concentration-specific or rather species-specific responses towards elevated nitrate, since NO3– concentrations were low in the present study (∼2 µmol L−1). Despite increased photosynthetic rates of organisms here, we did not see any elevation of calcification rates, indicating that additional available energy is primarily utilized in other ways. Most notably, we observed increasing organic carbon and host protein, results that are consistent with Tanaka et al. (2007), who observed an increase in organic tis-sue ofAcropora pulchraat elevated nitrate. Other potential sinks include proliferation of zooxanthellae density, zooxanthellae pigment concentration, and excess carbon may also lead to increased excretion of organic components into the water column (Haas et al. 2010; Naumann et al. 2010).
In the present study we did not see any significant effect of elevated nitrate on calcification rates of organisms. Previous studies have shown mixed effects including enhanced, neutral or negative effects of elevated DIN on growth rates of corals. A study by Atkinson et al. (1995) suggested no effects of increased nitrate on coral growth with concentrations of up to 5 µmol L−1. However, the majority of studies showed contradictory results with decreased coral calcification under elevated DIN, including nitrate (Stambler et al. 1991; Marubini and Davies 1996; Ferrier-Pages et al. 2000; Renegar and Riegl 2005). The latter studies presume competition between photosynthesis and calcification about the in-ternal DIC pool, and that enhanced photosynthesis under elevated nutrients may exhaust the inin-ternal DIC pool for calcification. In contrast, Tanaka et al. (2007) reported an increase of coral calcification under elevated nitrate, suggesting several possibilities for this nutrient enhanced calcification: (1) light enhanced calcification may have directly been raised by increased photosynthesis in elevated nutrient concentrations; (2) elevated nutrients may have promoted the synthesis of an organic matrix, which is a required step for calcification; (3) increased supply of metabolic CO2in the calicoblastic layer may have promoted calcification rates (Tanaka et al. 2007). In the present study, the effects of nutrients on
calcifi-cation were not significant, indicating neither light enhanced calcificalcifi-cation by increased photosynthesis, nor competition for the DIC pool between photosynthesis and calcification did take place under present experimental nitrate concentrations. Notably, in the present study nitrate concentrations were consider-ably lower, but at the same time more similar to naturally occurring concentrations at inshore reefs on the GBR compared to most other studies. In addition, non-significant effects of elevated nutrients on calcification ofH. opuntiaagrees with previous results by Delgado and Lapointe (1994).
Chlorophyllacontent of the investigated organisms increased under elevated nitrate concentrations.
Increased pigment content in corals can either derive from increased algal population density and/or in-creased pigment content per algal cell, which has been previously demonstrated for several corals under elevated nitrate (Marubini and Davies 1996; Chauvin et al. 2011) and other nutrient species (Tanaka et al. 2007). As demonstrated by Fabricius (2006) the warming of the coral surface is increased by up to 1.5 °C in darker coral colonies (i.e. corals with increased pigmentation) compared to the ambient seawater. Thus, even when higher pigment content does not seem to have a direct negative effect on corals, the indirect effects of darker coloration may make them more susceptible to other stressors such as warming accompanied by coral bleaching. Similarly, pigment content ofH. opuntiawas significantly increased under elevated nutrients. Thus, zooxanthellae in both corals and pigments inH. opuntiawere nitrate limited under ambient seawater conditions.
Nitrate addition led to an imbalance between organic and inorganic growth. While host protein content of coralA. tenuiswas unaffected by elevated nitrate, it was significantly increased for coralS.
hystrixmost likely due to an increase in nitrogen biomass of the host tissue, as presumed by Tanaka et al.
(2007). This increase in host protein content may lead to an imbalanced growth between organic tissue and the inorganic carbonate skeleton, as demonstrated by Tanaka et al. (2007). Interestingly, respiration ofS. hystrixsignificantly increased under elevated nitrate which most likely arose from the increased host-protein content and algae pigments.
In addition, organic carbon content ofH. opuntiawas significantly higher in nutrient treatments com-pared to controls. However, this elevation negatively correlated with inorganic carbon content, indicating organic components (e.g. pigments) increased at the expense of inorganic components. Additionally, total nitrogen content was increased with DIN, further contributing to the evidence thatH. opuntia is nitrate limited in ambient conditions. This result is also supported by accumulated nitrate ofHalimeda in nutrient up-welling locations on the GBR (Wolanski et al. 1988). Consequently, the calculated C:N ratio considerably decreased in high nutrient concentrations.
Interactive effects of pCO2and elevated nitrate
In the present study, we tested whether elevated DIN affects responses of organisms to elevated DIC, but we did not observe any significant interactive effects on the physiology of the organisms investigated.
Against our hypothesis, simultaneous increases in DIC and DIN did not show any synergistic effects on productivity or growth rates of coral or algae. The present study showed that the physiology of organ-isms investigated responded more strongly to increased DIN than DIC after three weeks under present experimental conditions. Elevated DIN reduces the thermal limit of corals due to an imbalanced supply of other nutrients. This leads to phosphate starvation of coral zooxanthellae, changes in the lipid com-position of the algal membranes and ultimately to the breakdown of the coral-zooxanthellae symbiosis (Wooldridge 2009; Wiedenmann et al. 2013). Organisms inhabiting reefs susceptible to coastal runoff may rapidly and strongly respond to DIN pulses in naturally occurring concentrations. These can lead to associated effects on organisms’ physiology and can increase their susceptibility to other stressors, which can ultimately lead to alterations in the community composition. It is unclear however, whether or how fast organisms’ physiology will return to the original state in low nutrient conditions, a question that should be addressed in future experimental approaches. Nevertheless, reducing fertilizer discharge by coastal runoff will increase the organisms’ chances to cope with global environmental changes.
Acknowledgments
We want to thank the staff of the Lizard Island Research Station, Anne Hoggett, Lyle Vail, Cassy Thomp-son and Bruce Stewart for their support in conducting this experiment and their hospitality on the island.
Thanks to Stephen Boyle, Cassie Payn and Jane Wu Won from AIMS analytical services, for their help with analyzing samples. Thanks to Jason Doyle for providing the protocol for pigment analyzes. This study was funded by the Australian Institute of Marine Science, the Great Barrier Reef Foundation and was conducted with the support of funding from the Australian Government’s National Environmental Research Program.
References
Abel, K. K. M., E. E. A. Drew, et al. (1985). “Response ofHalimedametabolism to various environ-mental parameters”. In: vol. 5. Proceedings of the 5th International Coral Reef Congress, Tahiti, 27 May-1 June, pp. 21–26 (cit. on p. 130).
Atkinson, M. J., B. Carlson, and G. L. Crow (1995). “Coral growth in high-nutrient, low-pH seawater:
a case study of corals cultured at the Waikiki Aquarium, Honolulu, Hawaii”. In:Coral Reefs14.4, pp. 215–223 (cit. on p. 130).
Bell, P. R. F. (1992). “Eutrophication and coral reefs - some examples in the Great Barrier Reef lagoon”.
In:Water Research26.5, pp. 553–568 (cit. on p. 115).
Bythell, J. C. (1990). “Nutrient uptake in the reef-building coralAcropora palmataat natural environ-mental concentrations”. In:Marine Ecology Progress Series68, pp. 65–69 (cit. on p. 130).
Chauvin, A., V. Denis, and P. Cuet (2011). “Is the response of coral calcification to seawater acidification related to nutrient loading?” In:Coral Reefs30.4, pp. 911–923 (cit. on pp. 130, 131).
Collins, M. et al. (2013). “Long-term climate change: projections, commitments and irreversibility”.
In: Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, pp. 1029–1136 (cit. on p. 114).
Comeau, S., R. C. Carpenter, Y. Nojiri, H. M. Putnam, K. Sakai, and P. J. Edmunds (2014). “Pacific-wide contrast highlights resistance of reef calcifiers to ocean acidification”. In:Proceedings of the Royal Society B: Biological Sciences281.1790, p. 20141339 (cit. on pp. 114, 128).
Comeau, S., P. J. Edmunds, N. B. Spindel, and R. C. Carpenter (2013). “The responses of eight coral reef calcifiers to increasing partial pressure of CO2 do not exhibit a tipping point”. In:Limnology and Oceanography58.1, pp. 388–398 (cit. on p. 126).
Crawley, A., D. I. Kline, S. Dunn, K. Anthony, and S. Dove (2010). “The effect of ocean acidification on symbiont photorespiration and productivity in Acropora formosa”. In:Global Change Biology 16.2, pp. 851–863 (cit. on p. 125).
De’ath, G. and K. E. Fabricius (2010). “Water quality as a regional driver of coral biodiversity and macroalgae on the Great Barrier Reef”. In: Ecological Applications 20.3, pp. 840–850 (cit. on p. 114).
Delgado, O. and B. E. Lapointe (1994). “Nutrient-limited productivity of calcareous versus fleshy macroal-gae in a eutrophic, carbonate-rich tropical marine environment”. In:Coral Reefs13.3, pp. 151–159 (cit. on pp. 130, 131).
Devlin, M. J. and J. Brodie (2005). “Terrestrial discharge into the Great Barrier Reef Lagoon: nutrient behavior in coastal waters”. In:Marine Pollution Bulletin51.1, pp. 9–22 (cit. on p. 114).
Devlin, M. and B. Schaffelke (2009). “Spatial extent of riverine flood plumes and exposure of marine ecosystems in the Tully coastal region, Great Barrier Reef”. In:Marine and Freshwater Research 60.11, pp. 1109–1122 (cit. on p. 115).
Devlin, M., J. Waterhouse, J. Taylor, and J. E. Brodie (2001).Flood plumes in the Great Barrier Reef:
spatial and temporal patterns in composition and distribution. Townsville, Australia: Great Barrier Reef Marine Park Authority (cit. on p. 125).
Dickson, A. G., C. L. Sabine, and J. R. Christian (2007).Guide to best practices for ocean CO2 mea-surements(cit. on p. 119).
Fabricius, K. E. (2005). “Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis”. In:Marine Pollution Bulletin50.2, pp. 125–146 (cit. on p. 114).
— (2006). “Effects of irradiance, flow, and colony pigmentation on the temperature microenvironment around corals: Implications for coral bleaching?” In:Limnology and Oceanography51.1, pp. 30–37 (cit. on p. 131).
— (2011). “Factors determining the resilience of coral reefs to eutrophication: a review and conceptual model”. In:Coral Reefs: An Ecosystem in Transition, pp. 493–505 (cit. on p. 114).
Fabricius, K. E., S. Cséke, C. Humphrey, and G. De’ath (2013). “Does trophic status enhance or reduce the thermal tolerance of scleractinian corals? A review, experiment and conceptual framework”. In:
PloS one8.1, e54399 (cit. on p. 126).
Fabricius, K. E., G. De’ath, L. McCook, E. Turak, and D. McB. Williams (2005). “Changes in algal, coral and fish assemblages along water quality gradients on the inshore Great Barrier Reef”. In:
Marine Pollution Bulletin51.1, pp. 384–398 (cit. on p. 114).
Fabricius, K. E., C. Langdon, S. Uthicke, C. Humphrey, S. Noonan, G. De’ath, R. Okazaki, N. Muehllehner, M. S. Glas, and J. M. Lough (2011). “Losers and winners in coral reefs acclimatized to elevated car-bon dioxide concentrations”. In:Nature Climate Change1.3, pp. 165–169 (cit. on p. 114).
Fabricius, K. E., M. Logan, S. Weeks, and J. Brodie (2014). “The effects of river run-off on water clarity across the central Great Barrier Reef”. In:Marine Pollution Bulletin84, pp. 191–200 (cit. on p. 114).
Ferrier-Pages, C., J.-P. Gattuso, S. Dallot, and J. Jaubert (2000). “Effect of nutrient enrichment on growth and photosynthesis of the zooxanthellate coralStylophora pistillata”. In:Coral Reefs19.2, pp. 103–
113 (cit. on pp. 114, 115, 130).
Ferrier-Pagès, C., V. Schoelzke, J. Jaubert, L. Muscatine, and O. Hoegh-Guldberg (2001). “Response of a scleractinian coral,Stylophora pistillata, to iron and nitrate enrichment”. In:Journal of Experimental Marine Biology and Ecology259.2, pp. 249–261 (cit. on p. 130).
Galloway, J. N., A. R. Townsend, J. W. Erisman, M. Bekunda, Z. Cai, J. R. Freney, L. A. Martinelli, S. P.
Seitzinger, and M. A. Sutton (2008). “Transformation of the nitrogen cycle: recent trends, questions, and potential solutions”. In:Science320.5878, pp. 889–892 (cit. on p. 114).
Haas, A. F., M. S. Naumann, U. Struck, C. Mayr, M. el-Zibdah, and C. Wild (2010). “Organic matter release by coral reef associated benthic algae in the Northern Red Sea”. In:Journal of Experimental Marine Biology and Ecology389.1, pp. 53–60 (cit. on p. 130).
Hintze, J. (2007).NCSS statistical software(cit. on p. 120).
Hoegh-Guldberg, O., P. J. Mumby, A. J. Hooten, R. S. Steneck, P. Greenfield, E. Gomez, C. D. Harvell, P. F. Sale, A. J. Edwards, and K. Caldeira (2007). “Coral reefs under rapid climate change and ocean acidification”. In:Science318.5857, pp. 1737–1742 (cit. on p. 114).
Hofmann, L. C., J. Heiden, K. Bischof, and M. Teichberg (2014). “Nutrient availability affects the re-sponse of the calcifying chlorophyte Halimeda opuntia(L.) JV Lamouroux to low pH”. In:Planta 239.1, pp. 231–242 (cit. on p. 126).
Humphrey, C., M. Weber, C. Lott, T. Cooper, and K. E. Fabricius (2008). “Effects of suspended sed-iments, dissolved inorganic nutrients and salinity on fertilisation and embryo development in the coralAcropora millepora(Ehrenberg, 1834)”. In:Coral Reefs27.4, pp. 837–850 (cit. on p. 115).
Hunte, W. and M. Wittenberg (1992). “Effects of eutrophication and sedimentation on juvenile corals”.
In:Marine Biology114.4, pp. 625–631 (cit. on p. 115).
IPCC (2013).Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. New York: Cambridge University Press (cit. on pp. 114, 120).
Kleypas, J. A., J. W. McManus, and L. A. B. Meñez (1999). “Environmental limits to coral reef devel-opment: where do we draw the line?” In:American Zoologist39.1, pp. 146–159 (cit. on p. 125).
Kleypas, J. A. and K. K. Yates (2009). “Coral Reefs and Ocean Acidification”. In:Oceanography22.4, pp. 108–117 (cit. on p. 114).
Koch, M., G. Bowes, C. Ross, and X. H. Zhang (2013). “Climate change and ocean acidification effects on seagrasses and marine macroalgae”. In:Global Change Biology19.1, pp. 103–132 (cit. on p. 114).
Langdon, C. and M. J. Atkinson (2005). “Effect of elevated pCO2 on photosynthesis and calcification of corals and interactions with seasonal change in temperature/ irradiance and nutrient enrichment”.
In:Journal of Geophysical Research110, pp. 1–16 (cit. on p. 125).
Leclercq, N., J.-P. Gattuso, and J. Jaubert (2002). “Primary production, respiration, and calcification of a coral reef mesocosm under increased CO2partial pressure”. In:Limnology and Oceanography47.2, pp. 558–564 (cit. on p. 125).
Leuzinger, S., K. R. N. Anthony, and B. L. Willis (2003). “Reproductive energy investment in corals:
scaling with module size”. In:Oecologia136.4, pp. 524–531 (cit. on p. 119).
Lichtenthaler, H. K. (1987). “Chlorophylls and carotenoids: pigments of photosynthetic biomembranes.”
In:Methods in Enzymology148, pp. 350–382 (cit. on p. 119).
Littler, M. M., D. S. Littler, and B. E. Lapointe (1988). “A comparison of nutrient-and light-limited photosynthesis in psammophytic versus epilithic forms of Halimeda(Caulerpales, Halimedaceae) from the Bahamas”. In:Coral Reefs6.3-4, pp. 219–225 (cit. on p. 130).
Lueker, T. J., A. G. Dickson, and C. D. Keeling (2000). “Ocean pCO2calculated from dissolved inor-ganic carbon, alkalinity, and equations for K1 and K2: validation based on laboratory measurements of CO2 in gas and seawater at equilibrium”. In: Marine Chemistry70.1-3, pp. 105–119 (cit. on p. 119).
Marubini, F. and P. S. Davies (1996). “Nitrate increases zooxanthellae population density and reduces skeletogenesis in corals”. In:Marine Biology127.2, pp. 319–328 (cit. on pp. 114, 115, 130, 131).
Naumann, M. S., A. Haas, U. Struck, C. Mayr, M. el-Zibdah, and C. Wild (2010). “Organic matter release by dominant hermatypic corals of the Northern Red Sea”. In:Coral Reefs29.3, pp. 649–659 (cit. on p. 130).
Orr, J. C., V. J. Fabry, O. Aumont, L. Bopp, S. C. Doney, R. A. Feely, A. Gnanadesikan, N. Gruber, A. Ishida, and F. Joos (2005). “Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms”. In:Nature437.7059, pp. 681–686 (cit. on p. 114).
R Development Core Team (2014). R: A language and environment for statistical computing(cit. on p. 120).
Renegar, D. A. and B. M. Riegl (2005). “Effect of nutrient enrichment and elevated CO2partial pressure on growth rate of Atlantic scleractinian coralAcropora cervicornis”. In:Marine Ecology Progress Series293, pp. 69–76 (cit. on pp. 126, 130).
Reynaud, S., N. Leclercq, S. Romaine-Lioud, C. Ferrier-Pages, J. Jaubert, and J. P. Gattuso (2003).
“Interacting effects of CO2partial pressure and temperature on photosynthesis and calcification in a scleractinian coral”. In:Global Change Biology9.11, pp. 1660–1668 (cit. on p. 125).
Ritchie, R. J. (2008). “Universal chlorophyll equations for estimating chlorophylls a, b, c, and d and total chlorophylls in natural assemblages of photosynthetic organisms using acetone, methanol, or ethanol solvents”. In:Photosynthetica46.1, pp. 115–126 (cit. on p. 119).
Robbins, L. L., M. E. Hansen, J. A. Kleypas, and S. C. Meylan (2010). “CO2calc-A user-friendly seawa-ter carbon calculator for Windows, Max OS X, and iOS (iPhone)”. In:Geological Survey2010-1280 (cit. on p. 119).
Silverman, J., B. Lazar, and J. Erez (2007). “Effect of aragonite saturation, temperature, and nutrients on the community calcification rate of a coral reef”. In:Journal of Geophysical Research: Oceans (1978–2012)112.C5, pp. 1–14 (cit. on p. 126).
Stambler, Noga, Nurit Popper, Zvy Dubinsky, and John Stimson (1991). “Effects of nutrient enrichment and water motion on the coralPocillopora damicornis”. In:Pacific Science45.3, pp. 299–307 (cit.
on p. 130).
Tanaka, Y., T. Miyajima, I. Koike, T. Hayashibara, and H. Ogawa (2007). “Imbalanced coral growth between organic tissue and carbonate skeleton caused by nutrient enrichment”. In: Limnology and Oceanography52.3, pp. 1139–1146 (cit. on pp. 130, 131).
Uthicke, S. and K. E. Fabricius (2012). “Productivity gains do not compensate for reduced calcification under near future ocean acidification in the photosynthetic benthic foraminifer speciesMarginopora vertebralis”. In:Global Change Biology18.9, pp. 2781–2791 (cit. on pp. 114, 118, 119).
Veal, C. J., M. Carmi, M. Fine, and O. Hoegh-Guldberg (2010). “Increasing the accuracy of surface area estimation using single wax dipping of coral fragments”. In:Coral Reefs29.4, pp. 893–897 (cit. on p. 118).
Vogel, N., K. E. Fabricius, J. Strahl, S. H. C. Noonan, C. Wild, and S. Uthicke (2015a). “Calcareous green alga Halimedatolerate ocean acidification conditions at tropical carbon dioxide seeps”. In:
Limnology and Oceanography60.1, pp. 263–275 (cit. on pp. 114, 118, 119, 126).
Vogel, N., F.W. Meyer, C. Wild, and S. Uthicke (2015b). “Decreased light availability can amplify negative impacts of ocean acidification on calcifying coral reef organisms”. In: Marine Ecology Progress Series.DOI:✶✵✳✸✸✺✹✴♠❡♣s✶✶✵✽✽(cit. on pp. 116, 118, 119, 126).
Vogel, N. and S. Uthicke (2012). “Calcification and photobiology in symbiont-bearing benthic foraminifera and responses to a high CO2environment”. In:Journal of Experimental Marine Biology and Ecology 424-425, pp. 15–24 (cit. on p. 116).
Wiedenmann, J., C. D’Angelo, E. G. Smith, A. N. Hunt, F.-E. Legiret, A. D. Postle, and E. P. Achterberg (2013). “Nutrient enrichment can increase the susceptibility of reef corals to bleaching”. In:Nature Climate Change3.2, pp. 160–164 (cit. on p. 132).
Wolanski, E., E. Drew, K. M. Abel, and J. O’Brien (1988). “Tidal jets, nutrient upwelling and their influence on the productivity of the alga Halimedain the Ribbon Reefs, Great Barrier Reef”. In:
Estuarine, Coastal and Shelf Science26.2, pp. 169–201 (cit. on p. 131).
Wooldridge, S. A. (2009). “Water quality and coral bleaching thresholds: Formalising the linkage for the inshore reefs of the Great Barrier Reef, Australia”. In:Marine Pollution Bulletin58.5, pp. 745–751 (cit. on p. 132).
Wooldridge, S., J. Brodie, and M. Furnas (2006). “Exposure of inner-shelf reefs to nutrient enriched runoff entering the Great Barrier Reef Lagoon: Post-European changes and the design of water quality targets”. In:Marine Pollution Bulletin52.11, pp. 1467–1479 (cit. on p. 114).
Interactive effects of ocean acidification and warming on coral reef associated epilithic algal communities under past, present and future ocean conditions
Nikolas Vogel1,2,3, Neal Cantin1, Julia Strahl1, Paulina Kaniewska1, Line Bay1, Christian Wild2,3 and Sven Uthicke1
(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
Keywords: Keywords: carbon dioxide, climate change, crustose coralline algae,Peyssonneliaspp.
This publication is in preparation
Abstract
Epilithic algal communities play critical ecological roles on coral reefs, but their response to individual and interactive effects of ocean warming (OW) and ocean acidification (OA) is still largely unknown. We investigated growth, photosynthesis and calcification of early epilithic community assemblages exposed to four temperature profiles (−1.1,±0,+0.9,+1.7) that were crossed with four carbon dioxide partial pressures (360, 440, 650, 940 µatm pCO2) under flow-through conditions and natural light regimes over a six month period. Additionally, we compared the cover of heavily calcified crustose coralline algae (CCA) and lightly calcified red algae of the genusPeyssonnelia. Increase in epilithic community cover was higher at moderately increased than at high temperature and it was higher at present-day (440 µatm) compared to reduced and elevated pCO2conditions. Community level light-, dark- and net calcification decreased with increasing pCO2. Interactive effects resulted in lowest net calcification at low temper-ature/high pCO2 and highest net calcification at high temperature/past pCO2. Final CCA cover was higher at moderately increased than at all other temperatures and higher at present-day compared to all other pCO2conditions.Peyssonneliacover was higher at high compared to ambient and moderate tem-perature, while it was lowered in past, but not affected by elevated pCO2. Interactive effects resulted in highestPeyssonneliacover at low temperature/present-day pCO2and lowest cover at moderate temper-ature/moderate pCO2. Thus, CCA experienced additive negative effects from high temperature and high pCO2, whilePeyssonneliashowed benefits in conditions where CCA were most affected, potentially due to a different calcification intensity or -mineral. The lower cover of CCA andPeyssonneliaunder past pCO2 conditions suggests that acclimatization occurred from past to present-day pCO2. If organisms have no potential to further acclimatize, interacting OW and OA may change epilithic communities in the future, leading to reduced reef stability and recovery.