Article

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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    • "However, to date, all such studies on comparative growth and physiology have focused on chronic mean differences in pCO 2sw (e.g. Suggett et al., 2012; Calosi et al., 2013a, b), despite pCO 2sw at vent sites exhibiting considerable variation within the space of hours to days (Boatta et al., 2013). To date, we have little understanding of how short-term natural fluctuations in pCO 2sw affect animal acid–base regulation and so distribution at vent sites. "
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    ABSTRACT: Most studies assessing the impacts of ocean acidification (OA) on benthic marine invertebrates have used stable mean pH/pCO2 levels to highlight variation in the physiological sensitivities in a range of taxa. However, many marine environments experience natural fluctuations in carbonate chemistry, and to date little attempt has been made to understand the effect of naturally fluctuating seawater pCO2 (pCO2sw) on the physiological capacity of organisms to maintain acid–base homeostasis. Here, for the first time, we exposed two species of sea urchin with different acid–base tolerances, Paracentrotus lividus and Arbacia lixula, to naturally fluctuating pCO2sw conditions at shallow water CO2 seep systems (Vulcano, Italy) and assessed their acid–base responses. Both sea urchin species experienced fluctuations in extracellular coelomic fluid pH, pCO2, and [ HCO 3 − ] [HCO3−] (pHe, pCO2e, and [ HCO 3 − ] e [HCO3−]e, respectively) in line with fluctuations in pCO2sw. The less tolerant species, P. lividus, had the greatest capacity for [ HCO 3 − ] e [HCO3−]e buffering in response to acute pCO2sw fluctuations, but it also experienced greater extracellular hypercapnia and acidification and was thus unable to fully compensate for acid–base disturbances. Conversely, the more tolerant A. lixula relied on non-bicarbonate protein buffering and greater respiratory control. In the light of these findings, we discuss the possible energetic consequences of increased reliance on bicarbonate buffering activity in P. lividus compared with A. lixula and how these differing physiological responses to acute fluctuations in pCO2sw may be as important as chronic responses to mean changes in pCO2sw when considering how CO2 emissions will affect survival and success of marine organisms within naturally assembled systems.
    Full-text · Article · Dec 2015 · ICES Journal of Marine Science
    • "However, despite numerous investigations reporting negative impacts of thermal stress and OA on corals, some cnidarian symbioses occur near shallow volcanic seeps (Fabricius et al. 2011; Meron et al. 2012, 2013; Suggett et al. 2012) and in acidified nearshore waters (Shamberger et al. 2014) where pH conditions can fall well below pH values predicted for the upcoming century . Moreover, increased primary production, symbiont population density and growth were observed in anemones exposed to natural and simulated increases in pCO 2 (Suggett et al. 2012; Towanda & Thuesen 2012). Some corals have even survived incubations in low pH for over a year, increasing their soft tissue biomass and living as soft-bodied polyps after dissolution of their calcium carbonate skeleton (Fine & Tchernov 2007). "
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    ABSTRACT: Increasing sea-surface temperatures and ocean acidification (OA) are impacting physiologic processes in a variety of marine organisms. Many sea anemones, corals and jellies in the phylum Cnidaria form endosymbiotic relationships with Symbiodinium spp. (phylum Dinoflagellata) supply the hosts with fixed carbon from photosynthesis. Much work has focused on the generally negative effects of rising temperature and OA on calcification in Symbiodinium-coral symbioses, but has not directly measured symbiont photosynthesis in hospite or fixed carbon translocation from symbiont to host. Symbiodinium species or types vary in their environmental tolerance and photosynthetic capacity; therefore, primary production in symbiotic associations can vary with symbiont type. However, symbiont type has not been identified in a large portion of Symbiodinium-cnidarian studies. Future climate conditions and OA may favor non-calcifying, soft-bodied cnidarians, including zoanthids. Here we show that two zoanthid species, Palythoa sp. and Zoanthus sp., harboring different symbiont types (C1 and A4), had very different responses to increased temperature and increased partial pressure of CO2 (pCO2), or dissolved CO2, and low pH. Thermal stress did not affect carbon fixation or fixed carbon translocation in the Zoanthus sp./A4 association, and high pCO2/low pH increased carbon fixation. In contrast, both thermal stress and high pCO2/low pH greatly inhibited carbon fixation in the Palythoa sp./C1 association. However, the combined treatment of high temperature and high pCO2 increased carbon fixation relative to the treatment of high temperature alone. Our observations support the growing body of evidence that demonstrates that the response of symbiotic cnidarians to thermal stress and OA must be considered on a host-specific and symbiont-specific basis. In addition, we show that the effects of increased temperature and pCO2 on photosynthesis may change when these two stressors are combined. Understanding how carbon fixation and translocation varies among different host-symbiont combinations is critical to predicting which Symbiodinium associations may persist in warm, acidified oceans.
    No preview · Article · Dec 2015
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    • "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). It is commonly accepted that the excess trace elements are kept in a “chemically safe” form through binding by proteins or other organic molecules and/or formation of metal granules, and in some cases are stored in a specialized organ (i.e., hepatopancreas or digestive gland in crustaceans, Depledge & Rainbow, 1990; Rainbow, 1990; Rainbow, 1993). "
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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.
    Full-text · Article · Sep 2014 · PeerJ
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