exper-Table 2.3: Linear Model ANOVA results for oxygen production and respiration rates ofH. depressaand M. vertebralisafter long- and short-term exposition
Response variable Species Source of variation df F p Long-term exposition
Net photosynthesis H. depressa pCO2
run residual
3 7 21
1.73 2.99
0.248
<0.05*
M. vertebralis pCO2
run residual
3 8 23
0.93 1.61
0.469 0.177
Respiration H. dep. pCO2
run residual
3 7 21
0.98 2.22
0.454 0.075 M. vert. pCO2
run residual
3 8 24
2.23 0.68
0.162 0.704 Short-term exposition
Net photosynthesis H. dep. pCO2
run residual
3 4 16
2.05 1.33
0.250 0.302 M. vert. pCO2
run residual
3 12 28
1.11 4.2
0.384
<0.001*
Respiration H. dep. pCO2
run residual
3 4 16
1.67 0.53
0.310 0.720 M. vert. pCO2
run residual
3 12 32
0.97 1.69
0.440 0.115
imental treatments. The response curve model chosen (Fig. 2.4) explained 96 and 98% of the variation for ambient and elevated pCO2, respectively. Gross photosynthesis at light saturation (Pmax) was app.
400 µmol photons m−2s−1in both treatments. Mixed model ANOVA (Table 2.4) however, showed that production parameters (Pmax,α and Ek) did not vary significantly between the two pCO2treatments in the short term. Therefore, an acute increase in pCO2had no significant impact on the shape of the P-I curve inM. vertebralis. Thus, photosynthesis inM. vertebraliswas not impacted by increased pCO2 with increasing light intensities.
Light intensity [µmol photons m-2 s-1]
0 100 200 300 400 500
Gross photosynthesis [µg O2 L-1 h-1 mg(ww)-1]
0.0 0.1 0.2 0.3 0.4 0.5 0.6
Figure 2.4: Photosynthesis irradiance (P-I) curve forM. vertebralisin two different experimental treat-ments. Black symbols represent the control treatment (pCO2=496 µatm);n=9, R2=0.96,p<0.001.
White symbols represent the high CO2 treatment (pCO2 =1662 µatm); n=9, R2 =0.98, p<0.001.
Data are given as means±1 SE of 9 replicates in 3 experimental runs, each treatment. Data shown in graph are untransformed
conditions. Investigations on energy conversion efficiency (maximum quantum yield) and Chla con-tent showed no effect of increased CO2dosing after six weeks of experimentation in any species. After long-term (chronic) exposure, photosynthetic rates showed a trend towards decreased net photosynthesis and respiration forH. depressaand an increased net photosynthesis and respiration forM. vertebralisin elevated CO2conditions, however these trends were non-significant. Net photosynthesis and respiration rates after short-term exposures displayed no-significant changes in different pCO2treatments in either species.
Low mortality, a Chlacontent comparable to field conditions, photosynthetic rates and PAM
mea-Table 2.4: Regression parameters and Linear Model ANOVA results of light response experiments Regression Parameters
pCO2 Treatment R2 Pmax p α p Ek (Pmax/α) 518 µatm 0.96 0.5051 <0.001 3.3×10-3 <0.001 153.1 2130 µatm 0.98 0.5098 <0.001 3.8×10-3 <0.001 134.2 Mixed Model ANOVA
Response variable Source of variation df F p
Pmax pCO2
run residual
1 4 12
0.06 3.44
0.820
<0.05
α pCO2
run residual
1 4 12
3.97 0.36
0.117 0.832
Ek (P/α) pCO2
run residual
1 4 12
0.5 1.41
0.520 0.291
surements showed that LBF performed well in the aquarium system during the long-term experiment.
Effects on calcification rates
Despite an averageΩcaof 1.8 [µmol kgSW−1] in the highest pCO2treatments, the hyaline species A.
radiataandH. depressaas well as the miliolid species (de Nooijer et al. 2009)M. vertebralis experi-enced positive shell growth after six weeks of experimental treatment. Therefore, foraminiferal species investigated were able to deposit their calcite skeleton in pCO2 conditions (730-1020 µatm) predicted for the year 2100 and beyond.
Foraminifera in this study showed variable calcification rates within each species and within treat-ment replicates. This observation is in agreetreat-ment with a study by Fujita et al. (2011) and most likely resulted from different individual microenvironments, varying light gain in experimental cages and/or varying symbiont densities (i.e. Chlacontent) and therefore variable nutrition for individual LBF.
Experiments reducing pH by HCl addition (Kuroyanagi et al. 2009) showed the highest increase in shell diameter of the LBFAmphisorus kudakajimensisat pHNIST7.9 compared to control and pHNIST7.7 treatment, after 10 weeks of experimentation. However, shell weight decreased with decreasing pH in that study. In contrast, weight/surface ratios ofH. depressaandM. vertebralisin the present experiment displayed no trend in different pCO2conditions, suggesting LBF experienced no shell-thinning, due to decreasedΩca.
Similar to the present study, Fujita et al. (2011) conducted acidification experiments on several LBF by CO2bubbling, in static incubators. The authors determined the shellweight and shell diameter of two populations ofBaculogypsina sphaerulata,Calcarina gaudichaudiiandAmphisorus hemprichii. This study revealed variability between populations, and in almost all cultures, weight and diameter peaked at intermediate levels of pCO2 between 580 and 770 µatm (compared to 360 and 970 µatm pCO2).
Moreover, many treatment comparisons in Fujita et al. (2011) displayed no differences in calcification and differences between treatments were often small. Thus, the present study concurs with previous work that shows that short-term (up to 12 weeks) aquarium experiments indicate no major vulnerability in growth rates of LBF to OA.
A potential explanation for different results of the present study compared to results from Kuroyanagi et al. (2009) is the different experimental setups employed, namely that CO2bubbling was used in the present study instead of HCl addition. HCl addition does not alter the DIC concentration and only results in a small increase of [HCO3–], whereas CO2addition increases DIC, mainly in form of HCO3–(Hurd et al. 2009), which may be a limiting factor (ter Kuile et al. 1989a). Moreover, flow-through aquaria were used instead of static incubators (Kuroyanagi et al. 2009). The flow-through setup in the present study provided the host LBF with continuous nutrition. Additionally, static incubations result in artificially
large boundary layers between ambient seawater and foraminifera (Köhler-Rink and Kühl 2000) and carbonate parameters are subject to higher fluctuations between light and dark phase. Moreover, lower irradiance levels were chosen in the present study (app. 35 µmol compared to 60 and 190 µmol photons m−2s−1). As discussed below, high irradiance can cause lower tolerance towards an additional stressing agent, such as increased pCO2, and therefore can damage the photosystem. Other taxa have displayed variable responses in calcification to elevated pCO2 including the coccolithophore Emiliania huxleyi, where calcification has been seen to increase (Iglesias-Rodriguez et al. 2008) and decrease (Riebesell et al. 2000; Sciandra et al. 2003) under elevated pCO2regimes.
In a manipulative experimental study carried out with a large taxonomic range and a total of 18 ma-rine calcifying organisms, Ries et al. (2009) discovered increased calcification under intermediate CO2 regimes (606 and 903 µatm pCO2) in four experimental species. Interestingly, this group (Crepidula for-nicata(limpet),Arbacia punctulata(purple urchin),Neogoniolithonsp. (coralline red algae) and Hal-imeda incrassata(calcifying green algae) involved a variety of phototrophic and heterotrophic species with different types of calcium carbonate skeletons. Thus, a generalization of impacts on calcification on organisms is difficult to draw, referring to calcium carbonate type or trophic level. However, these factors may influence the response to acidification.
A potential explanation for the phenomenon of increased calcification in intermediate pCO2is that foraminiferal calcification and algal symbiont photosynthesis may be limited by DIC availability and therefore compete for this factor at present pCO2 conditions. Thus, increased pCO2 levels result in higher HCO3– concentrations available for photosynthesis and calcification. As shown in a previous study onAmphistegina lobifera(similar symbionts asH. depressaandA. radiata) calcification and pho-tosynthetic rates can be limited in lower DIC concentrations and calcification can profit from increased external DIC levels (ter Kuile et al. 1989a). Moreover, ter Kuile et al. (1989b) showed a linear increase in calcification rates of imperforate species A. hemprichii (similar symbionts as M. vertebralis) as a function of external DIC concentrations between 0 and 4000 µmol kgSW−1.
Although, here, LBF were exposed to more than two-fold decreased Ωcaconditions compared to controls, M. vertebralis was able to increase calcification in those conditions. Another potential ex-planation for this phenomenon arises from Köhler-Rink and Kühl (2000), who showed in microsensor studies onM. vertebralis,A. lobiferaandA. hemprichiithat the algal symbionts of foraminifera create a microenvironment in the boundary layer around the surface of the holobiont. During the light phase symbionts increased pH on the shells surface by up to 0.4 units and during the dark phase pH decreased to ambient seawater conditions. Increasing the pH of the surrounding seawater may therefore facili-tate carbonate deposition. Similarly, Rink et al. (1998) showed that algal symbionts from planktonic foraminiferaOrbulina universawere capable of creating a microenvironment surrounding the organism.
The pH level on the shell surface increased up to 0.5 units compared to ambient seawater. During the dark phase, however, the pH dropped to 7.9 units. This shows that foraminifera change the carbon-ate system parameters of seawcarbon-ater at a closer range and have to compenscarbon-ate for diurnal fluctuations of almost one pH unit (Rink et al. 1998).
Moreover, de Nooijer et al. (2009) revealed that foraminifera increase their intracellular pH at the site of calcification by up to one pH unit above ambient seawater conditions. This mechanism allows LBF to control and increaseΩcaat sites of calcification, which in turn facilitates the precipitation of calcium carbonate for the skeleton. This experiment also showed that both miliolid and hyaline species possess the ability to form intracellular high pH vesicles, which are used for calcification. The mechanism of increasing intracellular pH in decreased pH of ambient seawater however means that LBF have to provide more energy for active transport mechanisms to produce such cytoplasmic vesicles (de Nooijer et al. 2009).
Effects on photobiology
Responses of LBF in long-term exposure showed an increase in mean net photosynthesis ofM. verte-bralisin the two highest pCO2treatments. However, this increase was not statistically significant.
Experiments conducted on corals showed slightly decreased photosynthesis with increasing pCO2 and no effect on dark respiration (Reynaud et al. 2003). Anthony et al. (2008) observed productivity loss in high CO2conditions in coralline algae and corals up to levels of zero productivity. Contrary,A.
intermediashowed increased production at intermediate pCO2dosing. Similarly, Crawley et al. (2010) observed increased maximum photosynthetic capacity (Pmax) of corals in intermediate pCO2 regimes and no change in Pmaxwas found at highest CO2concentrations compared to controls. Experiments by Schneider and Erez (2006) revealed no significant impact of acidification on photosynthesis inAcropora eurystoma. Studies have also demonstrated thatE. huxleyishowed increased photosynthetic activity in elevated pCO2conditions (Fukuda et al. 2011; Iglesias-Rodriguez et al. 2008).
Moreover, CO2enrichment stimulated photosynthesis in seagrass as described by Jiang et al. (2010).
In addition, the authors conducted rapid light curves (RLC) with PAM fluorometry and observed an in-crease in relative maximum electron transport rate (rETRmax) and minimum saturating irradiance (Ek) with increasing CO2. P-I curves based on oxygen measurements, which were carried out onM. verte-bralisin the present short-term experiment, showed the expected shape of a saturation curve as in other primary producers. Experiments on free living diatoms showed positive effects of acidification in form of increased photosynthetic carbon fixation, yet other negative effects on carbon concentrating mechanisms were observed (Wu et al. 2010). Experimental studies on different phylotypes ofSymbiodinium(free liv-ing and symbiotic) showed mixed responses to OA, which vary from no effects to increased growth and
photosynthetic activity with increasing CO2 (Brading et al. 2011). Since photosynthesis experiments with diatom-bearingH. depressaand dinoflagellate-bearingM. vertebralisshowed no significant trend, symbionts in foraminifera might not have been affected differently in present experiments.
Experiments from ter Kuile et al. (1989b) indicate that photosynthetic DIC incorporation of LBF display optima around pH=8.2 and DIC incorporation in the skeleton show optima above 8.2 pH units.
However, the authors also found, that at constant pH, DIC levels can be limiting. Considering that algal symbionts of LBF are capable of increasing pH at the shells surface and foraminifera increase pH at sites of calcification, it is possible that increased pCO2, despite reducing pH of ambient seawater, provides higher DIC levels available for calcification and photosynthetic activity.
Carbon dioxide dosing showed no effect on maximum quantum yield, and thus on the energy con-version efficiency of PS II, after six weeks of experimental treatment. Previous studies revealed that maximum quantum yield can be a reliable indicator for health or stress of the photosystem in diatom-and dinoflagellate-bearing foraminifera (Schmidt et al. 2011; Uthicke et al. 2011, respectively).
Comparing initial Chlacontent with final values after six weeks of experiment showed that total Chl acontent of LBF was not negatively affected by decreased pH conditions. However, Chlacontent of M. vertebralisincreased two-fold when comparing initial with final measurements. SinceM. vertebralis was collected in shallow depths, this species was experiencing higher light gain in the field. Increasing Chlacontent in the experiment therefore might be a compensatory reaction towards lowered light levels.
Conclusions
The present study illustrated that species investigated were still able to build up their calcite skeleton in pCO2conditions predicted for the year 2100 and beyond. Calcification rates were not reduced compared to control treatments. Contrary to expectations, M. vertebralisshowed significantly increased growth rates in elevated CO2 dosing. Foraminifera possess the capability of changing intra- and extracellular carbonate chemistry to their advantage (de Nooijer et al. 2009; Köhler-Rink and Kühl 2000), however this is associated with energy costs. Expected DIC limitation in photosynthetic rates was not present in chosen experimental conditions. In field studies, Dias et al. (2010) showed a gradient of foraminifera diversities and assemblages in decreasing pH conditions at volcanic CO2vents in the Mediterranean Sea.
This indicates some high sensitivity of LBF to decreasing pH. Similarly, benthic foraminifera at coral reefs on volcanic CO2vents in Papua New Guinea also showed a clear reduction of foraminiferal densi-ties along pH gradients and total extinction at near future (pHtotal∼7.9) pH levels (Fabricius et al. 2011).
Thus field studies clearly indicate a negative impact of increased CO2on foraminiferal populations and diversity. Overall, this suggests that the pCO2threshold that foraminifera can tolerate in the long-term is not far from levels expected in the near future towards the end of the present century. However, this
also indicates that care needs to be taken when inferring on impacts of OA alone.
Considering that future foraminifera not only have to cope with one stressor, but also with increasing temperature and other factors such as land runoff, more research has to be conducted to assess the impacts of interacting components under the changing conditions predicted for upcoming decades.
Acknowledgments
We are grateful for the support of the crew of the research vessel Cape Fergusson. We thank Florita Flo-res for her assistance in the long-term experiment. Stephen Boyle contributed through processing water samples for carbonate system parameters. This research was supported by the Australian Government’s Marine and Tropical Sciences Research Facility, implemented in North Queensland by the Reef and Rainforest Research Centre Ltd. The International Office of Ludwig-Maximilians University Munich supported NV financially for his travel expenses, with the PROSA scholarship.
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Calcareous green alga Halimeda tolerates ocean acidification conditions at tropical carbon dioxide seeps
Nikolas Vogel1,2,3, Katharina Elisabeth Fabricius1, Julia Strahl1, Sam Hamilton Croft Noonan1, Chris-tian Wild2,3and 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: Carbon dioxide, vent, calcification, photosynthesis, carbon content, stable isotope signa-ture
This chapter has been published in Limnology and Oceanography (2015) 60.1: 263-275
Abstract
We investigated ecological, physiological and skeletal characteristics of the calcifying green alga Hal-imedagrown at CO2seeps (pHtotal∼7.8) and compared them to those at control reefs with ambient CO2 conditions (pHtotal∼8.1). Six species ofHalimedawere recorded at both the high CO2and control sites.
For the two most abundant speciesH. digitataandH. opuntiawe determined in-situ light and dark oxy-gen fluxes and calcification rates, carbon contents and stable isotope signatures. In both species, rates of calcification in the light increased at the high CO2 site compared to controls (131 and 41%, respec-tively). In the dark, calcification was not affected by elevated CO2inH. digitata, whereas it was reduced by 167% inH. opuntia, suggesting nocturnal decalcification. Calculated net calcification of both species was similar between seep and control sites, i.e. the observed increased calcification in light compen-sated for reduced dark calcification. However, inorganic carbon content increased (22%) inH. digitata and decreased (−8%) inH. opuntiaat the seep site compared to controls. Significantly lighter carbon isotope signatures ofH. digitataandH. opuntiaphylloids at high CO2 (1.01 and 1.94h, respectively) indicate increased photosynthetic uptake of CO2 over HCO3– potentially reducing dissolved inorganic carbon limitation at the seep site. Moreover,H. digitataandH. opuntiaspecimens transplanted for 14 days from the control to the seep site exhibited similarδ13C signatures as specimens grown there. These results suggest that theHalimedaspp. investigated can acclimatize and will likely still be capable to grow and calcify in pCO2conditions exceeding most pessimistic future CO2projections.