Sea anemones may thrive in a high CO 2 world

Global Change Biology (Impact Factor: 8.04). 04/2012; 18(10). DOI: 10.1111/j.1365-2486.2012.02767.x

ABSTRACT Increased seawater pCO 2 , and in turn 'ocean acidification' (OA), is predicted to profoundly impact marine ecosystem diversity and function this century. Much research has already focussed on calcifying reef-forming corals (Class: Anthozoa) that appear particularly susceptible to OA via reduced net calcification. However, here we show that OA-like conditions can simultaneously enhance the ecological success of non-calcifying anthozoans, which not only play key ecological and biogeochemical roles in present day benthic ecosystems but also represent a model organism should calcifying anthozoans exist as less calcified (soft-bodied) forms in future oceans. Increased growth (abundance and size) of the sea anemone (Anemonia viridis) population was observed along a natural CO 2 gradient at Vulcano, Italy. Both gross photosynthesis (P G) and respiration (R) increased with pCO 2 indicating that the increased growth was, at least in part, fuelled by bottom up (CO 2 stimulation) of metabolism. The increase of P G outweighed that of R and the genetic identity of the symbiotic microalgae (Symbiodinium spp.) remained unchanged (type A19) suggesting proximity to the vent site relieved CO 2 limitation of the anemones' symbiotic microalgal population. Our observa-tions of enhanced productivity with pCO 2 , which are consistent with previous reports for some calcifying corals, con-vey an increase in fitness that may enable non-calcifying anthozoans to thrive in future environments, i.e. higher seawater pCO 2 . Understanding how CO 2 -enhanced productivity of non-(and less-) calcifying anthozoans applies more widely to tropical ecosystems is a priority where such organisms can dominate benthic ecosystems, in particular following localized anthropogenic stress.

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Available from: Riccardo Rodolfo-Metalpa, Sep 28, 2015
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    • "An increase in trace element concentrations of anemones (whole body) exposed to elevated loads of dissolved trace elements in the water was frequently observed in laboratory studies (Harland & Nganro, 1990; Harland, Bryan & Brown, 1990; Mitchelmore et al., 2003; Mitchelmore, Ringwood & Weis, 2003; Main, Ross & Bielmyer, 2010; Brock & Bielmyer, 2013). Additionally, differences in the overall metabolic activity of the anemones under elevated pCO2 (Towanda & Thuesen, 2012; Suggett et al., 2012) may contribute to increased trace element bioaccumulation. This may be due to the higher rates of respiration in the more metabolically active anemone (Suggett et al., 2012), which directly affects feeding rate and thus the uptake of waterborne trace elements (Zamer, 1986). "
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    ABSTRACT: Ocean acidification (OA) is not an isolated threat, but acts in concert with other impacts on ecosystems and species. Coastal marine invertebrates will have to face the synergistic interactions of OA with other global and local stressors. One local factor, common in coastal environments, is trace element contamination. CO2 vent sites are extensively studied in the context of OA and are often considered analogous to the oceans in the next few decades. The CO2 vent found at Levante Bay (Vulcano, NE Sicily, Italy) also releases high concentrations of trace elements to its surrounding seawater, and is therefore a unique site to examine the effects of long-term exposure of nearby organisms to high pCO2 and trace element enrichment in situ. The sea anemone Anemonia viridis is prevalent next to the Vulcano vent and does not show signs of trace element poisoning/stress. The aim of our study was to compare A. viridis trace element profiles and compartmentalization between high pCO2 and control environments. Rather than examining whole anemone tissue, we analyzed two different body compartments-the pedal disc and the tentacles, and also examined the distribution of trace elements in the tentacles between the animal and the symbiotic algae. We found dramatic changes in trace element tissue concentrations between the high pCO2/high trace element and control sites, with strong accumulation of iron, lead, copper and cobalt, but decreased concentrations of cadmium, zinc and arsenic proximate to the vent. The pedal disc contained substantially more trace elements than the anemone's tentacles, suggesting the pedal disc may serve as a detoxification/storage site for excess trace elements. Within the tentacles, the various trace elements displayed different partitioning patterns between animal tissue and algal symbionts. At both sites iron was found primarily in the algae, whereas cadmium, zinc and arsenic were primarily found in the animal tissue. Our data suggests that A. viridis regulates its internal trace element concentrations by compartmentalization and excretion and that these features contribute to its resilience and potential success at the trace element-rich high pCO2 vent.
    PeerJ 09/2014; 2:e538. DOI:10.7717/peerj.538 · 2.11 Impact Factor
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    • "Indeed, there have been just two studies to focus on this, in which short-term experimental perfusions (b2 h) of isolated, symbiotic gastrodermal cells from the sea anemone Anemonia viridis in HCl-acidified seawater (Laurent et al., 2013b) and the coral Pocillopora damicornis in CO 2 -acidified seawater (Gibbin et al., 2014) revealed no detrimental effects on the pH i of the host cell, and host and symbiont cells, respectively. On the contrary, there is growing evidence that increased CO 2 availability associated with ocean acidification could enhance primary productivity in Symbiodinium cells (Brading et al., 2011; Jarrold et al., 2013; Marubini et al., 2008; Suggett et al., 2012; Towanda and Thuesen, 2012), and thus may limit the potential for host cell acidosis (Gibbin et al., 2014). This photosynthetically driven up-regulation of pH i under high CO 2 has been postulated as one potential mechanism for countering the negative impacts of acidification on coral calcification (Ries et al., 2009). "
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    ABSTRACT: We measured the relationship between CO2-induced seawater acidification, photo-physiological performance and intracellular pH (pHi) in a model cnidarian-dinoflagellate symbiosis - the sea anemone Aiptasia sp. - under ambient (289.94 ± 12.54 μatm), intermediate (687.40 ± 25.10 μatm) and high (1459.92 ± 65.51 μatm) CO2 conditions. These treatments represented current CO2 levels, in addition to CO2 stabilisation scenarios IV and VI provided by the Intergovernmental Panel on Climate Change (IPCC). Anemones were exposed to each treatment for two months and sampled at regular intervals. At each time-point we measured a series of physiological responses: maximum dark-adapted fluorescent yield of PSII (Fv/Fm), gross photosynthetic rate, respiration rate, symbiont population density, and light-adapted pHi of both the dinoflagellate symbiont and isolated host anemone cell. We observed increases in all but one photo-physiological parameter (Pgross: R ratio). At the cellular level, increases in light-adapted symbiont pHi were observed under both intermediate and high CO2 treatments, relative to control conditions (pHi 7.35 and 7.46 versus pHi 7.25, respectively). The response of light-adapted host pHi was more complex, however, with no change observed under the intermediate CO2 treatment, but a 0.3 pH-unit increase under the high CO2 treatment (pHi 7.19 and 7.48, respectively). This difference is likely a result of a disproportionate increase in photosynthesis relative to respiration at the higher CO2 concentration. Our results suggest that, rather than causing cellular acidosis, the addition of CO2 will enhance photosynthetic performance, enabling both the symbiont and host cell to withstand predicted ocean acidification scenarios.
    Journal of Experimental Marine Biology and Ecology 06/2014; 457. DOI:10.1016/j.jembe.2014.03.015 · 1.87 Impact Factor
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    • "This alkalinisation demonstrates the capacity of Symbiodinium cells to strongly buffer the external environmental pH signal, probably due to a fertilising effect on photosynthesis in these normally CO 2 -limited algae (Nimer et al., 1999). An increase in photosynthetic productivity after CO 2 addition has also been observed in other symbiotic associations, most notably in the temperate sea anemones Anemonia viridis (Suggett et al., 2012) and Anthopleura elegantissima (Towanda and Thuesen, 2012), and the benthic foraminiferan Marginopora vertebralis (Uthicke and Fabricius, 2012). The application of DCMU (a photosynthetic inhibitor) reversed the increase in pH i , confirming that the change was a direct consequence of photosynthesis, as the inhibited photosynthetic machinery of the symbionts is not able to ameliorate the increasing H + concentration (Fig.H3A). "
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    ABSTRACT: Regulating intracellular pH (pHi) is critical for optimising the metabolic activity of corals, yet mechanisms involved in pH regulation and the buffering capacity within coral cells are not well understood. Our study investigated how the presence of symbiotic dinoflagellates affects the response of pHi to pCO2-driven seawater acidification in cells isolated from Pocillopora damicornis. Using the fluorescent dye BCECF-AM, in conjunction with confocal microscopy, we simultaneously characterised the response of pHi in host coral cells and their dinoflagellate symbionts, in symbiotic and non-symbiotic states under saturating light, with and without the photosynthetic inhibitor DCMU. Each treatment was run under control (pH 7.8) and CO2 acidified seawater conditions (decreasing pH from 7.8 - 6.8). After two hours of CO2 addition, by which time the external pH (pHe) had declined to 6.8, the dinoflagellate symbionts had increased their pHi by 0.5 pH units above control levels. In contrast, in both symbiotic and non-symbiotic host coral cells, 15 min of CO2 addition (0.2 pH unit drop in pHe) led to cytoplasmic acidosis equivalent to 0.4 pH units. Despite further seawater acidification over the duration of the experiment, the pHi of non-symbiotic coral cells did not change, though in host cells containing a symbiont cell the pHi recovered to control levels. This recovery was negated when cells were incubated with DCMU. Our results reveal that photosynthetic activity of the endosymbiont is tightly coupled with the ability of the host cell to recover from cellular acidosis after exposure to high CO2 / low pH.
    Journal of Experimental Biology 03/2014; 217(11). DOI:10.1242/jeb.099549 · 2.90 Impact Factor
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