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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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... Venom is an integral component to cnidarian biology as it is used for prey capture, defense, intraspecific aggression, and digestion [6][7][8]. Sea anemones are found in all marine habitats and have widespread ecological success, likely because of the diversity of their ecological and physiological strategies [9,10]. The diverse symbiotic, competitive, and predator-prey interactions of sea anemones certainly rely on venoms [11], although precise correspondence between venoms, ecology, and physiology has yet to be demonstrated (but see [12]). ...
... Kunitz-domain peptides block ion channels and inhibit protease, leading to blood coagulation and inflammation [69]. Transcripts matching the venom Kunitz-type family were found across all species, with Heteractina member M. doreensis recovering the greatest number of transcripts (9). Sea anemone type II potassium channel toxin (KTx2) is a neurotoxin that has Kunitz domain; transcripts belonging to this group were abundant in all species, being most abundant in C. adhaesivum (11) and E. quadricolor (9). ...
... Transcripts matching the venom Kunitz-type family were found across all species, with Heteractina member M. doreensis recovering the greatest number of transcripts (9). Sea anemone type II potassium channel toxin (KTx2) is a neurotoxin that has Kunitz domain; transcripts belonging to this group were abundant in all species, being most abundant in C. adhaesivum (11) and E. quadricolor (9). ...
Article
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Sea anemones are predatory marine invertebrates and have diverse venom arsenals. Venom is integral to their biology, and is used in competition, defense, and feeding. Three lineages of sea anemones are known to have independently evolved symbiotic relationships with clownfish, however the evolutionary impact of this relationship on the venom composition of the host is still unknown. Here, we investigate the potential of this symbiotic relationship to shape the venom profiles of the sea anemones that host clownfish. We use transcriptomic data to identify differences and similarities in venom profiles of six sea anemone species, representing the three known clades of clownfish-hosting sea anemones. We recovered 1121 transcripts matching verified toxins across all species, and show that hemolytic and hemorrhagic toxins are consistently the most dominant and diverse toxins across all species examined. These results are consistent with the known biology of sea anemones, provide foundational data on venom diversity of these species, and allow for a review of existing hierarchical structures in venomic studies.
... Symbiodiniaceae fuel their hosts with organic carbon by fixing inorganic carbon (Ci) through photosynthesis (Davy et al. 2012). While Ci uptake rates by the algal symbionts have rarely been measured, they appear strongly regulated by environmental factors, such as availability of CO 2 (pCO 2 ) (Suggett et al. 2012b;Brading et al. 2013) and temperature (Oakley et al. 2014). Recent work on cultured Symbiodiniaceae revealed that different environmental optima primarily drive variation in Ci uptake rates (Ros et al. 2020). ...
... Recent work on cultured Symbiodiniaceae revealed that different environmental optima primarily drive variation in Ci uptake rates (Ros et al. 2020). Within reef systems where Symbiodiniaceae are hosted within cnidarian tissues, symbiont cells are typically carbon-limited (Smith and Muscatine 1999;Doherty 2009;Towanda and Thuesen 2012); as such, cnidarians can exhibit a stimulated carbon metabolism under naturally higher pCO 2 (more acidic) environments (Suggett et al. 2012b). The efficiency of Symbiodiniaceae carbon metabolism across environments thus appears an important trait Topic editor Simon Davy ...
... The asterisk symbols denote statistically different shifts (P \ 0.05), the absence of asterisk symbol denotes trends, the equal signs denote no statistical differences (P [ 0.05), and NA denotes data not collected mangrove corals could come from a loss of P G . However, as the mangrove lagoon is more acidic (and has higher pCO2 availability), we expected to observe an increase in productivity (Brading et al. 2011;Suggett et al. 2012b;Hoadley et al. 2015), but in fact measured the opposite. This decrease in Ci uptake therefore might be driven by an upstream pathway independent of CO 2 availability. ...
Article
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Symbiosis between reef-building corals and unicellular algae (Symbiodiniaceae) fuels the growth and productivity of corals reefs. Capacity for Symbiodiniaceae to fix inorganic carbon (Ci) and translocate carbon compounds to the host is central to coral health, but how these processes change for corals thriving in environmental extremes remains largely unresolved. We investigate how a model coral—Pocillopora acuta—persists from a reef habitat into an adjacent extreme mangrove lagoon on the Great Barrier Reef. We combine respirometry and photophysiology measurements, Symbiodiniaceae genotyping, and 13C labelling to compare P. acuta metabolic performance across habitats, in relation to the Ci uptake and translocation capacity by symbionts’ autotrophy. We show that differences in P. acuta metabolic strategies across habitats align with a shift in dominant host-associated Symbiodiniaceae taxon, from Cladocopium in the reef to Durusdinium in the mangroves. This shift corresponded with a change in “photosynthetic strategy”, with P. acuta in the mangroves utilising absorbed light for photochemistry over non-photochemical quenching. Mangrove corals translocated similar proportions of carbon compared to the reefs, despite a lower Ci uptake. These trends indicate that coral survival in mangrove environments occurs through sustained translocation rate of organic compounds from coral symbionts to host.
... Reef-forming cnidarians are in global decline due to rapidly increasing levels of atmospheric CO 2 [1], yet non-calcified cnidarians appear to be more resilient [2][3][4][5][6]. Since Revolution, average surface ocean pH has decreased by 0.1 units and is projected to drop by further 0.2-0.4 units by the end of this century, depending on CO 2 emission scenarios [7]. ...
... Surveys in areas with naturally high levels of CO 2 have shown that non-calcified cnidarians (e.g. soft corals, sea anemones and jellyfish) are more resilient to the effects of ocean acidification [3,5]. However, the molecular mechanisms underlying this resilience are largely unknown. ...
... Physiological measurements of sea anemones exposed to high CO 2 conditions both in situ and during laboratory studies show that sea anemones with symbiotic algae increase their primary productivity at high CO 2 due to enhanced carbon availability [3,[16][17][18][19][20]. To better understand the physiological plasticity and adaptive potential of cnidarians to high CO 2 , several transcriptome-level studies have been performed, mostly using corals [21][22][23][24]. ...
Article
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Ocean acidification threatens to disrupt interactions between organisms throughout marine ecosystems. The diversity of reef-building organisms decreases as seawater CO2 increases along natural gradients, yet soft-bodied animals, such as sea anemones, are often resilient. We sequenced the polyA-enriched transcriptome of adult sea anemone Anemonia viridis and its dinoflagellate symbiont sampled along a natural CO2 gradient in Italy to assess stress levels in these organisms. We found that about 1.4% of the anemone transcripts, but only ~0.5% of the Symbiodinium sp. transcripts were differentially expressed. Processes enriched at high seawater CO2 were mainly linked to cellular stress, including significant up-regulation of protective cellular functions and deregulation of metabolic pathways. Transposable elements were differentially expressed at high seawater CO2, with an extreme up-regulation (> 100-fold) of the BEL-family of long terminal repeat retrotransposons. Seawater acidified by CO2 generated a significant stress reaction in A. viridis, but no bleaching was observed and Symbiodinium sp. appeared to be less affected. These observed changes indicate the mechanisms by which A. viridis acclimate to survive chronic exposure to ocean acidification conditions. We conclude that many organisms that are common in acidified conditions may nevertheless incur costs due to hypercapnia and/or lowered carbonate saturation states.
... Elevated pCO 2 of surrounding seawater may also stimulate the photosynthetic activity of Symbiodinium spp. where cells have become CO 2 limited (see Suggett et al., 2012Suggett et al., , 2013Ventura et al., 2016) and may act as a key condition needed to enhance oxygenation of the host tissues. Whilst this potential mitigating role of endosymbiotic algae is interesting, it may ultimately be restricted to certain Symbiodinium spp. ...
... Symbiodinium genetic type identity was further determined across all (symbiotic) treatments to confirm whether any changes associated with Symbiodinium reflected alterations in physiology of the same type vs. a switch in dominate type (e.g., Suggett et al., 2012). At the end of the experiment, ten polyps from each replicate aquarium containing Symbiodinium were sampled and stored in DMSO preservation buffer (Seutin, White, & Boag, 1991 | 5 end of the experiment, polyp numbers differed among pH treatments but their response depended on symbiont status, resulting in a significant pH 9 symbiont interaction (Table 1, Figure 1); specifically, greatest numbers were produced by symbiotic polyps under low pH conditions, with symbiotic polyps producing 58% more than aposymbiotic polyps. ...
... Maximum photochemical efficiency values of Symbiodinium were low relative to those previously observed for Symbiodinium in hospite of cnidarians (e.g., Enochs et al., 2014;Hoadley et al., 2015; including polyps of Cassiopea sp. Klein, Pitt, & Carroll, 2016) numbers and productivity, but natural population sizes were also substantially increased in proximity to a natural CO 2 vent (Suggett et al., 2012). As with this previous observation, ours similarly suggests that Symbiodinium of Cassiopea sp. ...
Article
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Anthropogenic nutrient inputs enhance microbial respiration within many coastal ecosystems, driving concurrent hypoxia and acidification. During photosynthesis, Symbiodinium spp., the microalgal endosymbionts of cnidarians and other marine phyla, produce O2 and assimilate CO2 and thus potentially mitigate the exposure of the host to these stresses. However, such a role for Symbiodinium remains untested for noncalcifying cnidarians. We therefore contrasted the fitness of symbiotic and aposymbiotic polyps of a model host jellyfish (Cassiopea sp.) under reduced O2 (~2.09 mg/L) and pH (~ 7.63) scenarios in a full-factorial experiment. Host fitness was characterized as asexual reproduction and their ability to regulate internal pH and Symbiodinium performance characterized by maximum photochemical efficiency, chla content and cell density. Acidification alone resulted in 58% more asexual reproduction of symbiotic polyps than aposymbiotic polyps (and enhanced Symbiodinium cell density) suggesting Cassiopea sp. fitness was enhanced by CO2-stimulated Symbiodinium photosynthetic activity. Indeed, greater CO2 drawdown (elevated pH) was observed within host tissues of symbiotic polyps under acidification regardless of O2 conditions. Hypoxia alone produced 22% fewer polyps than ambient conditions regardless of acidification and symbiont status, suggesting Symbiodinium photosynthetic activity did not mitigate its effects. Combined hypoxia and acidification, however, produced similar numbers of symbiotic polyps compared with aposymbiotic kept under ambient conditions, demonstrating that the presence of Symbiodinium was key for mitigating the combined effects of hypoxia and acidification on asexual reproduction. We hypothesize that this mitigation occurred because of reduced photorespiration under elevated CO2 conditions where increased net O2 production ameliorates oxygen debt. We show that Symbiodinium play an important role in facilitating enhanced fitness of Cassiopea sp. polyps, and perhaps also other noncalcifying cnidarian hosts, to the ubiquitous effects of ocean acidification. Importantly we highlight that symbiotic, noncalcifying cnidarians may be particularly advantaged in productive coastal waters that are subject to simultaneous hypoxia and acidification.
... Moreover, previous studies investigating the nature of A. viridis morphs did not systematically consider A. viridis as a holobiont. A. viridis' gastrodermal tissue harbours millions of dinoflagellate cells (Muscatine et al., 1998;Suggett et al., 2012;Zamoum and Furla, 2012; belonging to the family Symbiodiniaceae that live in a close trophic relationship and which are vertically transmitted presenting not only an intra-clade genetic diversity partially structured by host species but also an intrahost genetic diversity . Among A. viridis morphs, no study provided a clear view of the symbiont genetic diversity distribution which could however be a driver of the morphological differentiation of A. viridis morphs. ...
... Each sea anemone hosts up to one million Symbiodinium cells per cm² of tissue (Suggett et al., 2012), and therefore constitutes a pooled sample of symbionts. Because we could not estimate properly the number of symbionts per anemone in our samples, we considered the presence (1) or the absence (0) of each ITS2 variants rather than its number of reads in each individual. ...
... Located intracellularly, the Symbiodiniaceae translocate most of the organic compounds they produce by photosynthesis to their host cells and thus enabled the expansion of symbiotic cnidarians in oligotrophic waters. The Symbiodiniaceae family comprises different clades, seven of which were described as genera with clear different functional responses to acidification Suggett et al. 2012), to temperature , and light variation (Reynolds et al. 2008), or to pro-oxidant environment (Roberty et al. 2016). In addition, even within Symbiodiniaceae species, genetic differentiation between symbiont populations was correlated with different thermal sensitivities . ...
Thesis
Qu’est-ce qu’un individu ? Cette question est un prérequis pour toutes les études en génétique des populations et en biologie évolutive, mais elle est loin d’être naïve dès que l’on prend en compte les relations symbiotiques. Les interactions entre un hôte et ses micro-organismes symbiotiques peuvent conditionner le développement, la reproduction, les capacités adaptatives de l’holobiote qu’ils constituent et donc la trajectoire évolutive de l’espèce. Comprendre ces interactions, c’est appréhender la complexité des interactions symbiotiques et donc caractériser ces différents partenaires et élucider l’implication de chaque partenaire dans le fonctionnement de l’holobiote. Chez les Cnidaires, comme l’anémone de mer Anemonia viridis, les hôtes animaux peuvent établir une symbiose mutualiste avec des Dinoflagellés photosynthétiques de la famille des Symbiodiniacées (avec un seul clade de Symbiodiniacées pour A. viridis). Cette anémone de mer tempérée présente différents morphes caractérisés par la couleur des tentacules. Afin de comprendre la nature de cette diversité phénotypique et mesurer la diversité symbiotique associée chez A. viridis, nous avons génotypé des anémones de Manche et de Méditerranée à l’aide de séquençage RAD (pour l’hôte animal) et de marqueurs ciblés, ITS2 et microsatellites (pour les symbiotes). Nos études ont permis de mettre en évidence l’existence de plusieurs lignées génétiques différenciées en sympatrie chez l’hôte animal, mais qui ne sont pas congruentes avec la différenciation morphologique. La composition des populations de symbiotes in hospite quant à elle n’est pas corrélée avec ces lignées hôtes mais structurées par l’origine géographique des anémones. Ces résultats révèlent qu’A. viridis telle que décrite à l’heure actuelle correspond un complexe d’espèces qui, en plus d’hériter verticalement leurs symbiotes, semblent capables également de les acquérir horizontalement. Cette symbiose dynamique implique que la sélection puisse agir indépendamment aussi bien sur la composition symbiotique que sur l’hôte ; et fait d’A. viridis un excellent modèle pour comprendre les capacités adaptatives d’un holobiote.
... Such fluorometry approaches have proven extremely critical for retrieving highly resolved photophysiological parameterization of corals over space and time (e.g. Hennige et al., 2008;Suggett et al., 2012;Langlois and Hoogenboom, 2014;Warner et al., 2010), but tying these parameters to the underlying metabolic changes that regulate photoacclimation remains challenging and largely unresolved (see Nitschke et al., 2018;Warner and Suggett, 2016). ...
... Consistent with previous studies, corals were able to acclimate to both increases and decreases in light availability (Falkowski and Dubinsky, 1981;Cohen and Dubinsky, 2015) during the time frame of our experiment. Changes in photophysiological parameters, notably the light intensity for saturated photosynthesis (E k ) and maximum electron transport rate (rETR max ), but not maximum photochemical efficiency of PSII (F q ′/F m ′ (max) ), suggest photoacclimation in these shallow reef flat Acropora muricata occurred primarily through changes in capacity for maximum photosynthesis rather than light harvesting (Hennige et al., 2008;Suggett et al., 2012). Furthermore, metabolomic shifts were observed within 7 days of treatment, particularly following high light exposure, suggesting a link between metabolite profile and photoacclimation response. ...
... Furthermore, metabolomic shifts were observed within 7 days of treatment, particularly following high light exposure, suggesting a link between metabolite profile and photoacclimation response. The lack of change observed for F q ′/F m ′ (max) contrasts with results from a number of previous studies, which report concurrent shifts in F q ′/F m ′ (max) with shifts in light (Hennige et al., 2008;Warner et al., 2010;Suggett et al., 2012;Nitschke et al., 2018). This result is particularly intriguing, as other metrics (i.e. ...
Article
Corals continuously adjust to short-term variation in light availability on shallow reefs. Long-term light alterations can also occur as a result of natural and anthropogenic stressors, as well as management interventions such as coral transplantation. Although short-term photophysiological responses are relatively well understood in corals, little information is available regarding photoacclimation dynamics over weeks of altered light availability. We coupled photophysiology and metabolomic profiling to explore changes that accompany longer-term photoacclimation in a key Great Barrier Reef coral species, Acropora muricata High light (HL)- and low light (LL)-acclimated corals were collected from the reef and reciprocally exposed to high and low light ex situ Rapid light curves using pulse-amplitude modulation (PAM) fluorometry revealed photophysiological acclimation of LL corals to HL and HL corals to LL within 21 days. A subset of colonies sampled at 7 and 21 days for untargeted LC-MS and GC-MS metabolomic profiling revealed metabolic reorganization before acclimation was detected using PAM fluorometry. Metabolomic shifts were more pronounced for LL to HL corals than for their HL to LL counterparts. Compounds driving metabolomic separation between HL-exposed and LL control colonies included amino acids, organic acids, fatty acids and sterols. Reduced glycerol and campesterol suggest decreased translocation of photosynthetic products from symbiont to host in LL to HL corals, with concurrent increases in fatty acid abundance indicating reliance on stored lipids for energy. We discuss how these data provide novel insight into environmental regulation of metabolism and implications for management strategies that drive rapid changes in light availability.
... The vertical transmission guarantees the continuity of this important association, as the A. viridis holobiont has the potential to be completely autotrophic (Davy et al., 1996;Muller-Parker & Davy, 2005). Even if symbiont diversity has been studied in A. viridis (Casado-Amezúa et al., 2014;Porro et al., 2019;Savage et al., 2002;Suggett et al., 2012;Visram et al., 2006), no study of the dynamics of symbiont populations at the adult stage has been conducted so far, although it would fill an important gap in the understanding of the plastic and adaptive capacities of this species. Indeed, many studies have highlighted its strong capacity for resistance to extreme and disturbed environments (Richier et al., 2005;Suggett et al., 2012;Ventura et al., 2016). ...
... Even if symbiont diversity has been studied in A. viridis (Casado-Amezúa et al., 2014;Porro et al., 2019;Savage et al., 2002;Suggett et al., 2012;Visram et al., 2006), no study of the dynamics of symbiont populations at the adult stage has been conducted so far, although it would fill an important gap in the understanding of the plastic and adaptive capacities of this species. Indeed, many studies have highlighted its strong capacity for resistance to extreme and disturbed environments (Richier et al., 2005;Suggett et al., 2012;Ventura et al., 2016). In this context, the occasional occurrence of horizontal symbiont acquisition on top of the vertical transmission may provide a mechanism for adaptation, adding to the intergenerational stability of the association the capacity to acquire locally better adapted symbiont genotype (Parkinson & Baums, 2014). ...
... This result highlights the potential for a plastic response of A. viridis lineages to the environment by modifying their symbiont community composition. Previous studies stated that no genetic changes in the symbiont community composition occurred in A. viridis in response to environmental change between subtidal and intertidal habitats (Bythell et al., 1997) or different pH conditions (Borell et al., 2014;Suggett et al., 2012) the inherited symbiont diversity is then more plausible, as was also strongly suggested by Quigley et al. (2019) in another species of the same genus. However, these Montipora species harbour different genera (or species) of Symbiodiniaceae, known to have different ecophysiological profiles. ...
Article
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All metazoans are in fact holobionts, resulting from the association of several organisms, and organismal adaptation is then due to the composite response of this association to the environment. Deciphering the mechanisms of symbiont acquisition in a holobiont is therefore essential to understanding the extent of its adaptive capacities. In cnidarians, some species acquire their photosynthetic symbionts directly from their parents (vertical transmission) but may also acquire symbionts from the environment (horizontal acquisition) at the adult stage. The Mediterranean snakelocks sea anemone, Anemonia viridis (Forskål, 1775), passes down symbionts from one generation to the next by vertical transmission, but the capacity for such horizontal acquisition is still unexplored. To unravel the flexibility of the association between the different host lineages identified in A. viridis and its Symbiodiniaceae, we genotyped both the animal hosts and their symbiont communities in members of host clones in five different locations in the North Western Mediterranean Sea. The composition of within‐host–symbiont populations was more dependent on the geographical origin of the hosts than their membership to a given lineage or even to a given clone. Additionally, similarities in host–symbiont communities were greater among genets (i.e. among different clones) than among ramets (i.e. among members of the same given clonal genotype). Taken together, our results demonstrate that A. viridis may form associations with a range of symbiotic dinoflagellates and suggest a capacity for horizontal acquisition. A mixed‐mode transmission strategy in A. viridis, as we posit here, may help explain the large phenotypic plasticity that characterizes this anemone.
... Contrary to the mounting literature suggesting detrimental consequences for marine invertebrates, some studies suggest that symbiotic anemones could prosper in oceans enriched with CO 2 (Hall-Spencer et al. 2008;Towanda and Thuesen 2012;Suggett et al. 2012;Meron et al. 2013). The prospect that anemones with symbiotic algae may thrive in future oceans, whilst calcifying organisms will likely experience reduced growth and heightened mortality (Bibby et al. 2007;Ross et al. 2011), provides an intriguing basis for investigation. ...
... There is very little literature addressing the impact that ocean acidification may have upon non-calcifying invertebrates such as anemones, despite their ecological importance (Connell and Russell 2010;Suggett et al. 2012). The present study will help fill this gap. ...
... Neither were there significant effects on contest behaviour. This contrasts with non-calcifying anthozoa with symbiotic zooxanthellae which can thrive under the acidic conditions found at naturally occurring CO 2 vents (Hall-Spencer et al. 2008;Suggett et al. 2012;Meron et al. 2013). This may indicate such species will be 'winners' in more acidic oceans of the future. ...
Article
Increasing concentrations of atmospheric carbon dioxide are causing oceanic pH to decline worldwide, a phenomenon termed ocean acidification. Mounting experimental evidence indicates that near-future levels of CO2 will affect calcareous invertebrates such as corals, molluscs and gastropods, by reducing their scope for calcification. Despite extensive research into ocean acidification in recent years, the effects on non-calcifying anthozoans, such as sea anemones, remain little explored. In Western Europe, intertidal anemones such as Actinia equina are abundant, lower trophic-level organisms that function as important ecosystem engineers. Changes to behaviours of these simple predators could have implications for intertidal assemblages. This investigation identified the effects of reduced seawater pH on feeding and contest behaviour by A. equina. Video footage was recorded for A. equina feeding at current-day seawater (pH 8.1), and the least (pH 7.9) and most (pH 7.6) severe end-of-century predictions. Footage was also taken of contests over ownership of space between anemones exposed to reduced pH and those that were not. No statistically significant differences were identified in feeding duration or various aspects of contest behaviour including initiating, winning, inflating acrorhagi, inflicting acrorhagial peels and contest duration. Multivariate analyses showed no effect of pH on a combination of these variables. This provides contrast with other studies where anemones with symbiotic algae thrive in areas of natural increased acidity. Thus, novel experiments using intraspecific contests and resource-holding potential may prove an effective approach to understand sub-lethal consequences of ocean acidification for A. equina, other sea anemones and more broadly for marine ecosystems.
... For example, Ω declines may directly reduce calcification rates in numerous taxa [10], but if these taxa are then outcompeted by non-calcifers, community calcification rates may further decline. Similarly, OA can increase rates of community production by directly stimulating photosynthesis in some species [30,31], or indirectly by increasing the benthic cover of certain phototrophs [2]. To gain further insight into the community metabolic dynamics of coral reefs under OA, measurements must be made on communities that have developed in their entirety under altered seawater carbonate chemistries. ...
... While results are not universal [14], patterns in benthic communities at CO 2 seeps in the temperate Mediterranean [5,[49][50][51], as well as multiple tropical sites in the Indo-Pacific [11,12], concur with the present study. These studies similarly predict an increase in non-calcifying algae under OA, and there are suggestions that other non-calcifying phototrophs, such as seagrasses [11] and anemones [30], may also thrive. Interestingly, non-calcifying algae have increased abundances in the wider community at the seep sites in Milne Bay [11], however they do not dominate the benthos like on the settlement tiles of the present study, or at another tropical seep [12]. ...
... Here we documented a 10% increase in gross photosynthesis and a 20% increase in respiration at pH T 7.8 compared to control sites with a pH T 8.0, but no change in net community production. Gross photosynthesis may increase under OA by directly stimulating photosynthesis [30,31], and/or by increasing the benthic cover of phototrophs [2]. Studies that have investigated metabolic changes under OA at the reef community scale are few and from quite different communities, however they have not observed the increases in gross photosynthesis reported here [17,20,27,28]. ...
Article
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Ocean acidification is expected to alter community composition on coral reefs, but its effects on reef community metabolism are poorly understood. Here we document how early successional benthic coral reef communities change in situ along gradients of carbon dioxide (CO 2), and the consequences of these changes on rates of community photosynthesis, respiration, and light and dark calcification. Ninety standardised benthic communities were grown on PVC tiles deployed at two shallow-water volcanic CO 2 seeps and two adjacent control sites in Papua New Guinea. Along the CO 2 gradient, both the upward facing phototrophic and the downward facing cryptic communities changed in their composition. Under ambient CO 2 , both communities were dominated by calcifying algae, but with increasing CO 2 they were gradually replaced by non-calcifying algae (predominantly green filamentous algae, cyanobacteria and macroal-gae, which increased from ~30% to ~80% cover). Responses were weaker in the invertebrate communities, however ascidians and tube-forming polychaetes declined with increasing CO 2. Differences in the carbonate chemistry explained a far greater amount of change in communities than differences between the two reefs and successional changes from five to 13 months, suggesting community successions are established early and are under strong chemical control. As pH declined from 8.0 to 7.8, rates of gross photosynthesis and dark respiration of the 13-month old reef communities (upper and cryptic surfaces combined) significantly increased by 10% and 20%, respectively, in response to altered community composition. As a consequence , net production remained constant. Light and dark calcification rates both gradually declined by 20%, and low or negative daily net calcification rates were observed at an aragonite saturation state of <2.3. The study demonstrates that ocean acidification as predicted for the end of this century will strongly alter reef communities, and will significantly change rates of community metabolism.
... The effect of low pH on the density of symbionts in calcifying and non-calcifying organisms varies widely. When exposed to decreased pH levels, there is an increase in zooxanthellae density in Stylophora pistillata (Reynaud et al., 2003) and Anemonia viridis (Suggett et al., 2012); a decrease in density in Porites sp., S. pistillata (Krief et al., 2010) and Cliona orientalis (Fang et al., 2013); and no change in Anthopleura elegantissima (Towanda & Thuesen, 2012), ...
... Studies performed on non-calcifying hosts such as soft corals and anemones have also revealed varied results in regard to the relationship between zooxanthellae density and decreasing pH. Suggett et al. (2012) found an increase in zooxanthellae density in A. viridis. Towanda and Thuesen (2012) Sarcophyton sp. ...
... In conclusion, our results indicate that decreased pH levels do not have a negative effect on the health of individuals of Cassiopea sp. or their zooxanthellae. Because acidic conditions can be detrimental to other species, lower pH levels could provide the opportunity for this species to proliferate and disrupt ecological communities (Suggett et al., 2012). However, pH alone does not represent all of the factors associated with ocean acidification (Branch, DeJoseph, Ray, & Wagner, 2013;Feely et al., 2009 ...
Article
Ocean acidification is the decline in seawater pH that results from the absorption of atmospheric carbon dioxide (CO2). Decreased pH has negative effects on survivability, growth, and development in many marine calcifiers, potentially resulting in reduced coral species richness. This reduction in richness could open new niche space, allowing the spread of invasive species, such as the upside‐down jellyfish (Cassiopea spp.). Like corals, this jellyfish forms symbiotic relationships with zooxanthellae, photosynthetic dinoflagellates. This study focused on the effect of seawater acidification in Cassiopea spp. We monitored zooxanthellae density and two measures of health (bell diameter and volume) in individuals of Cassiopea sp. at three pH levels chosen to mimic different open‐ocean average conditions: 8.2, representing pre‐industrial revolution conditions; and 7.9 and 7.6, representing predicted declines in pH in the next century. Zooxanthellae density and health of the jellyfish were measured twice—prior to experimental manipulations and after four weeks of exposure to experimental pHs—in three consecutive trials. The effects of pH and Trial on proportional change in jellyfish attributes were analyzed using generalized linear mixed models. We found no significant effects of either factor. These results indicate that decreasing seawater pH has no apparent negative effect on zooxanthellae density or health in Cassiopea, which suggests that these jellyfish may be relatively insensitive to the impacts of ocean acidification, heightening its potential as an invasive species.
... Repercussions for the resident anemonefishes include reduced reproductive success, altered predator response and population declines (Jones et al. 2008;Lönnstedt and Frisch 2014;Beldade et al. 2017). In contrast, ocean acidification can improve sea anemone growth, asexual reproduction and abundance (Suggett et al. 2012;Hoadley et al. 2015). Symbiodiniaceae can also benefit through enhanced photosynthesis (Towanda and Thuesen 2012;Suggett et al. 2012;Gibbin and Davy 2014). ...
... In contrast, ocean acidification can improve sea anemone growth, asexual reproduction and abundance (Suggett et al. 2012;Hoadley et al. 2015). Symbiodiniaceae can also benefit through enhanced photosynthesis (Towanda and Thuesen 2012;Suggett et al. 2012;Gibbin and Davy 2014). ...
... However, Symbiodiniaceae density can vary when sea anemones are exposed to high pCO 2 , with an increase (Suggett et al. 2012), decrease (Towanda and Thuesen 2012) or no change (Ventura et al. 2016) being recorded. However, no studies have assessed the impact of pCO 2 on sea anemones that host anemonefish, and it is not known whether concurrent changes in ocean temperature and pCO 2 will have a combined effect, as they do with their coral counterparts. ...
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Climate change is causing ocean temperature and partial pressure of carbon dioxide (pCO2) to increase. For sea anemones that have Symbiodiniaceae, high temperatures induce bleaching, whereas rises in pCO2 can enhance photosynthesis and increase host growth and abundance. It is, however, not clear how the interaction of these two stressors impacts sea anemones that provide habitat for anemonefishes. Here, we investigated the bleaching response of the sea anemone Entacmaea quadricolor, under four conditions: (i) current temperature and current pCO2 (control); (ii) future pCO2; (iii) future temperature; and (iv) future temperature and future pCO2. After 16 days of exposure, future temperature, but not pCO2 nor their interaction, significantly reduced the Symbiodiniaceae density and total chlorophyll Symbiodiniaceae cell⁻¹. Colour score was lower in the sea anemones exposed to future temperature than current temperature from day 4 onwards. In contrast, total chlorophyll symbiont cell⁻¹ increased in the future temperature treatments, and light-adapted effective quantum yield remained similar in all treatments. Although pCO2 had no impact within the time frame of our experiment, the predicted future temperature induced bleaching in E. quadricolor. As bleaching events increase in frequency and severity, this will likely impact the abundance of host sea anemones and their symbiotic anemonefishes.
... Prolonged exposure to elevated CO 2 stimulates photosynthesis of growth of Symbiodiniaceae in the sea anemone Anthopleura elegantissima (Towanda and Thuesen 2012) in laboratory cultures. This is also the case for the sea anemone Anemonia viridis growing at different distances from a shallow water CO 2 vent near the island of Vulcano in the Mediterranean (Suggett et al. 2012) . For this long-term "natural experiment" there is the possibility that the inhabitant genotypes change as a function of distance from the vent; Suggett et al. (2012) showed that the same genotype dominated along the CO 2 and pH gradient from vent to the un-influenced benthic habitat. ...
... This is also the case for the sea anemone Anemonia viridis growing at different distances from a shallow water CO 2 vent near the island of Vulcano in the Mediterranean (Suggett et al. 2012) . For this long-term "natural experiment" there is the possibility that the inhabitant genotypes change as a function of distance from the vent; Suggett et al. (2012) showed that the same genotype dominated along the CO 2 and pH gradient from vent to the un-influenced benthic habitat. The response of the uncalcified sea anemones to ocean acidification differs from the calcified corals in not being constrained by inhibition of calcification. ...
Article
Photosynthetic dinoflagellates are ecologically and biogeochemically important in marine and freshwater environments. However surprisingly little is known of how this group acquires inorganic carbon or how these diverse processes evolved. Consequently, how CO2 availability ultimately influences the success of dinoflagellates over space and time remains poorly resolved compared to other microalgal groups. Here we review the evidence. Photosynthetic core dinoflagellates have a Form II RuBisCO (replaced by Form IB or Form ID in derived dinoflagellates). The in vitro kinetics of the Form II RuBisCO from dinoflagellates are largely unknown, but dinoflagellates with Form II (and other) RuBisCOs have inorganic carbon concentrating mechanisms (CCMs), as indicated by in vivo internal inorganic C accumulation and affinity for external inorganic C. However, the location of the membrane(s) at which the essential active transport component(s) of the CCM occur(s) is (are) unresolved; isolation and characterisation of functionally competent chloroplasts would help in this respect. Endosymbiotic Symbiodiniaceae (in Foraminifera, Acantharia, Radiolaria, Ciliata, Porifera, Acoela, Cnidaria and Mollusca) obtain inorganic C by transport from seawater through host tissue. In corals this transport apparently provides an inorganic C concentration around the photobiont that obviates the need for photobiont CCM. This is not the case for tridacnid bivalves, medusae, or, possibly, Foraminifera. Overcoming these long‐standing knowledge gaps relies on technical advances, e.g. the in vitro kinetics of Form II RuBisCO, that can functionally track the fate of inorganic C forms.
... Moreover, previous studies investigating the nature of A. viridis morphs did not systematically consider A. viridis as a holobiont. A. viridis' gastrodermal tissue harbours millions of dinoflagellate cells (Muscatine et al. 1998;Suggett et al. 2012;Zamoum and Furla 2012;Ventura et al. 2016) belonging to the family Symbiodiniaceae (LaJeunesse et al. 2018) that live in a close trophic relationship (Davy et al. 1996) and that are vertically transmitted (Schäfer 1984 Savage et al. 2002;Visram et al. 2006) presenting not only an intra-clade genetic diversity partially structured by host species but also an intra-host genetic diversity (Visram et al. 2006;Forcioli et al. 2011;Casado-Amezúa et al. 2014). Among A. viridis morphs, no study provided a clear view of the symbiont genetic diversity distribution that could however be a driver of the morphological differentiation of A. viridis morphs. ...
... Each sea anemone hosts up to 1 million Symbiodinium cells per cm 2 of tissue (Suggett et al. 2012), and therefore constitutes a pooled sample of symbionts. Because we could not estimate properly the number of symbionts per anemone in our samples, we considered the presence (1) or the absence (0) of each ITS2 variants rather than its number of reads in each individual. ...
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How can we explain morphological variations in a holobiont? The genetic determinism of phenotypes is not always obvious and could be circumstantial in complex organisms. In symbiotic cnidarians, it is known that morphology or colour can misrepresent a complex genetic and symbiotic diversity. Anemonia viridis is a symbiotic sea anemone from temperate seas. This species displays different colour morphs based on pigment content and lives in a wide geographical range. Here, we investigated whether colour morph differentiation correlated with host genetic diversity or associated symbiotic genetic diversity by using RAD sequencing and symbiotic dinoflagellate typing of 140 sea anemones from the English Channel and the Mediterranean Sea. We did not observe genetic differentiation among colour morphs of A. viridis at the animal host or symbiont level, rejecting the hypothesis that A. viridis colour morphs correspond to species level differences. Interestingly, we however identified at least four independent animal host genetic lineages in A. viridis that differed in their associated symbiont populations. In conclusion, although the functional role of the different morphotypes of A. viridis remains to be determined, our approach provides new insights on the existence of cryptic species within A. viridis.
... Carbon dioxide concentrations are greater and more variable in cold-water temperate environments. Observations from natural CO 2 vent sites in the Mediterranean demonstrated that Philozoon actiniarum (designated ITS2 type A19 in Suggett et al., 2012) in Anemonia viridis was unaffected by dynamic CO 2 environments, and even exhibited higher photosynthetic rates under raised CO 2 concentrations (Suggett et al., 2012). Future studies assessing the generality of enhanced photosynthesis under high CO 2 tensions among Philozoon spp. ...
... Carbon dioxide concentrations are greater and more variable in cold-water temperate environments. Observations from natural CO 2 vent sites in the Mediterranean demonstrated that Philozoon actiniarum (designated ITS2 type A19 in Suggett et al., 2012) in Anemonia viridis was unaffected by dynamic CO 2 environments, and even exhibited higher photosynthetic rates under raised CO 2 concentrations (Suggett et al., 2012). Future studies assessing the generality of enhanced photosynthesis under high CO 2 tensions among Philozoon spp. ...
Article
The dinoflagellate family Symbiodiniaceae comprises numerous genera and species with large differences in diversity, ecology and geographic distribution. An evolutionarily divergent lineage common in temperate symbiotic cnidarians and designated in the literature by several informal names including ‘temperate–A’, AI, Phylotype A´ (A-prime) and ‘Mediterranean A’, is here assigned to the genus Philozoon. This genus was proposed by Geddes (1882) in one of the earliest papers that recognized ‘yellow cells’ as distinct biological entities separate from their animal and protist hosts. Using phylogenetic data from nuclear (rDNA), chloroplast (cp23S) and mitochondrial genes (cob and cox1), as well as morphology (cell size), ecological traits (host affinity) and geographic distributions, we emend the genus Philozoon Geddes and two of its species, P. medusarum and P. actiniarum, and describe six new species. Each symbiont species exhibits high host fidelity for particular species of sea anemone, soft coral, stony coral and a rhizostome jellyfish. Philozoon is most closely related to Symbiodinium (formerly Clade A), but, unlike its tropical counterpart, occurs in hosts in shallow temperate marine habitats in northern and southern hemispheres including the Mediterranean Sea, north-eastern Atlantic Ocean, eastern Australia, New Zealand and Chile. The existence of a species-diverse lineage adapted to cnidarian hosts living in high latitude habitats with inherently wide fluctuations in temperature calls further attention to the ecological and biogeographic reach of the Symbiodiniaceae. HIGHLIGHTS • A dinoflagellate genus symbiotic with temperate invertebrates is characterized and named using a discarded taxonomic term revived from the golden age of Natural Historians. • The work highlights how animal–algal mutualisms are evolved to thrive under a broad range of environmental conditions.
... Whilst well-supported in tropical and subtropical scleractinian corals, it should be emphasised that a decrease in symbiont density under ocean acidification is not necessarily a universal pattern among all symbiotic Cnidaria. Symbiont densities (per mg of protein) increased with acidification in Aiptasia sp. in lab studies (Gibbin and Davy 2014) and in Anemonia viridis at marine volcanic vents (Suggett et al. 2012;Meron et al. 2013; but see Borell et al. 2014). Other anemones have demonstrated declines in symbiont densities under acidification (e.g. ...
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Ocean acidification changes the carbonate chemistry of seawater in a manner that reduces the biomineralisation rate of reef-building corals. Other effects of acidification on coral physiology are less well explored, and recent debate has focused on whether ocean acidification causes a change in Symbiodinium densities within tropical and subtropical reef-building corals. Within the framework of null-hypothesis significance testing, some aquaria experiments have provided evidence for a decrease in symbiont densities within coral tissue under ocean acidification (whilst others have suggested an increase). However, null effects have prevailed in the majority of such experiments, and so the question has remained unresolved. This study attempted to resolve this question using a meta-analytic framework, by establishing the effect sizes for symbiont density change under ocean acidification from a structured search of the literature. A regression of effect size (Hedge’s d) versus level of ocean acidification revealed a statistically significant negative relationship, with symbiont density per cm2 decreasing as the level of ocean acidification increased. The decline amounted to an additional 0.07 standard deviations of difference in symbiont density between corals in control (near present day) and acidified seawater with every 100 μatm of increase in partial pressure of CO2 in seawater (a relationship with an r2 of 0.24). A further unresolved question is whether ocean acidification will synergistically exacerbate (or diminish) symbiont density reductions caused by elevated temperature. An analysis of covariance did not reveal a greater decline in symbiont densities with increasing acidification at elevated temperature compared to non-stressful temperature, though this latter analysis should be viewed as exploratory due to a lower sample size. The well-supported evidence for a decline in symbiont densities in tropical and subtropical corals under ocean acidification now provides an impetus for sustained investigation of the consequences of such a change for holobiont functioning and the broader function of the coral reef ecosystem.
... These changes are expected to intensify in the future with potentially significant, but variable effects on marine organisms depending on their sensitivity (Hendrick et al., 2010;Kroeker et al., 2010). Calcifying organisms are more susceptible to ocean acidification than non-calcifying organisms (Suggett et al., 2012), even though their responses to ocean acidification are also dependent on the taxonomic group and their developmental stages (Hendrick et al., 2010;Kroeker et al., 2010). Realisation of the key role of seagrass in coastal ecosystems has fostered ever growing efforts to quantify their annual productivity and growth dynamics. ...
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Rising carbon dioxide (CO2) concentrations in the atmosphere will increase the average pCO2 level in the world oceans, which will have a knock-on effect on the marine ecosystem. Coastal seagrass communities are predicted to benefit from the increase in CO2 levels, but long term effects of elevated CO2 on seagrass communities are less understood. Population reconstruction techniques were used to investigate the population dynamics of Cymodocea nodosa meadows, exposed to long term elevated CO2 at volcanic seeps of Greece and Italy. Effect of elevated CO2 was noticed on the growth, morphometry, density, biomass and age structure at the stations close to the CO2 seeps than reference sites. Above to below ground biomass ratio of C. nodosa were higher close to the CO2 seeps. The plastochrome intervals were similar at all CO2 seeps. The shoot age and shoot longevity of plants were lower at seeps. The present recruitment (sampled year) of the seagrass were higher than long-term average recruitment of the communities near the seeps. Carbon to nitrogen ratios (%DW) of C. nodosa were higher in leaves at seeps. Annual leaf production was higher near the seeps. This study suggests increased production of C. nodosa under elevated CO2 levels, but other co-factors such as nutrients, trace metal toxicity must also be taken into consideration while predicting effects of future CO2 concentrations.
... (e.g. Borell et al., 2014;Januar et al., 2016;Suggett et al., 2012) (Table 4). Furthermore, among the most affected groups, such as molluscs, acidification-tolerant species are still being found, such as the bivalve Mytilus spp. in the Mediterranean and Baltic Seas (Ricevuto et al., 2012;Thomsen et al., 2010, the endemic Mediterranean species Pinna nobilis (Basso et al., 2015), the limpets Patella spp. ...
Chapter
Human activity is generating an excess of atmospheric CO2, resulting in what we know as ocean acidification, which produces changes in marine ecosystems. Until recently, most of the research in this area had been done under small-scale, laboratory conditions, using few variables, few species and few life cycle stages. These limitations raise questions about the reproducibility of the environment and about the importance of indirect effects and synergies in the final results of these experiments. One way to address these experimental problems is by conducting studies in situ, in natural areas where expected future pH conditions already occur, such as CO2 vent systems. In the present work, we compile and discuss the latest research carried out in these natural laboratories, with the objective to summarize their advantages and disadvantages for research to improve these investigations so they can better help us understand how the oceans of the future will change.
... Enhanced rates of photosynthesis and respiration have been observed in temperate sea anemones and corals exposed to elevated pCO 2 ( Crawley et al., 2010;Suggett et al., 2012;Towanda and Thuesen, 2012;Gibbin et al., 2014). In contrast, both R and NPP decreased significantly down to values near zero in specimens of E. crispata, subject to heat and/or hypercapnic conditions. ...
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The impact of temperature on photo-symbiotic relationships has been highly studied in the tropical reef-forming corals but overlooked in less charismatic groups such as solar-powered sacoglossan sea slugs. These organisms display one of the most puzzling symbiotic features observed in the animal kingdom, i.e., their mollusk-plastid association, which enables them to retain photosynthetic active chloroplasts (i.e., kleptoplasts) retrieved from their algae feed sources. Here we analyze the impact of thermal stress (+4 C) and high pCO 2 conditions (1pH = 0.4) in survival, photophysiology (i.e., bleaching, photosynthetic efficiency, and metabolism) and stress defense mechanisms (i.e., heat shock and antioxidant response) of solar-powered sacoglossan sea slugs, from tropical (Elysia crispata) and temperate (E. viridis) environments. High temperature was the main factor affecting the survival of both species, while pH only affected the survival of the temperate model. The photobiology of E. viridis remained stable under the combined scenario, while photoinhibition was observed for E. crispata under high temperature and high pCO 2. In fact, bleaching was observed within all tropical specimens exposed to warming (but not in the temperate ones), which constitutes the first report where the incidence of bleaching in tropical animals hosting photosynthetic symbionts, other than corals, occurs. Yet, the expulsion of kleptoplasts by the tropical sea slug, allied with metabolic depression, constituted a physiological response that did not imply signs of vulnerability (i.e., mortality) in the host itself. Although the temperate species revealed greater heat shock and antioxidant enzyme response to environmental stress, we argue that the tropical (stenotherm) sea slug species may display a greater scope for acclimatization than the temperate (eurytherm) sea slug. E. crispata may exhibit increased capacity for phenotypic plasticity by increasing fitness in a much narrower thermal niche (minimizing maintenance costs), which ultimately may allow to face severe environmental conditions more effectively than its temperate generalist counterpart (E. viridis).
... These on-going changes are expected to intensify in the future with potentially significant, but variable effects on marine organisms depending on their sensitivity ( Hendrick et al., 2010;Kroeker et al., 2010). Calcifying organisms are more susceptible to ocean acidification than non-calcifying organisms (Suggett et al., 2012), even though their responses to ocean acidification are dependent on the taxonomic group and their developmental stages (Hendrick et al., 2010;Kroeker et al., 2010). Realisation of the key role of seagrass in coastal ecosystems has fostered ever growing efforts to quantify their annual productivity and growth dynamics. ...
Preprint
Full-text available
Rising carbon dioxide (CO2) concentrations in the atmosphere will increase the average pCO2 level in the world oceans, which will have a knock-on effect on the marine ecosystem. Coastal seagrass communities are predicted to benefit from the increase in CO2 levels, but long-term effects of elevated CO2 on seagrass communities are less understood. Population reconstruction techniques were used to investigate the population dynamics of Cymodocea nodosa meadows, exposed to long term elevated CO2 at volcanic seeps off Greece and Italy. Effect of elevated CO2 was noticed on the growth, morphometry, density, biomass and age structure at CO2 seeps than reference sites. Above to below ground biomass ratio of C. nodosa were higher at CO2 seeps. The shoot age and shoot longevity of plants were lower at seeps. The present recruitment (sampled year) of the seagrass were higher than long-term average recruitment of the communities near the seeps. Carbon to nitrogen ratios (%DW) and annual leaf production of C. nodosa were higher in leaves at seeps. This study suggests under long-term CO2 enrichment C. nodosa production increases, but the plant survival rate decreases because of other co-factors such as nutrient availability and trace metal toxicity. Therefore, along with high CO2 other factors must be taken into consideration while predicting effects of future CO2 concentrations.
... There do appear to be defined physiological limits under which calcification can occur (McCulloch et al., 2012;Wall et al., 2016), and physiological plasticity appears important in supporting calcification at high pCO 2. For example, increased rates of calcification (Rodolfo-Metalpa et al., 2011), or the utilization of elevated external dissolved inorganic carbon (DIC) can fuel photosynthesis (Inoue et al., 2013;Strahl et al., 2015a) and offset the higher energetic cost of calcification under acidification. For soft corals (Inoue et al., 2013), sea anemones (Suggett et al., 2012a), and scleractinian corals (Strahl et al., 2015a), success at high pCO 2 seems to be driven by their capacity to enhance, or at least sustain, photosynthesis under elevated pCO 2 . Other physiological processes such as higher cell protective capacities, total lipid content, tissue biomass (Strahl et al., 2015b) and changes in fatty acid metabolism (Kenkel et al., 2017) may also promote resistance to environmental stress at low pH. ...
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Global climate change and localized anthropogenic stressors are driving rapid declines in coral reef health. In vitro experiments have been fundamental in providing insight into how reef organisms will potentially respond to future climates. However, such experiments are inevitably limited in their ability to reproduce the complex interactions that govern reef systems. Studies examining coral communities that already persist under naturally-occurring extreme and marginal physicochemical conditions have therefore become increasingly popular to advance ecosystem scale predictions of future reef form and function, although no single site provides a perfect analog to future reefs. Here we review the current state of knowledge that exists on the distribution of corals in marginal and extreme environments, and geographic sites at the latitudinal extremes of reef growth, as well as a variety of shallow reef systems and reef-neighboring environments (including upwelling and CO2 vent sites). We also conduct a synthesis of the abiotic data that have been collected at these systems, to provide the first collective assessment on the range of extreme conditions under which corals currently persist. We use the review and data synthesis to increase our understanding of the biological and ecological mechanisms that facilitate survival and success under sub-optimal physicochemical conditions. This comprehensive assessment can begin to: (i) highlight the extent of extreme abiotic scenarios under which corals can persist, (ii) explore whether there are commonalities in coral taxa able to persist in such extremes, (iii) provide evidence for key mechanisms required to support survival and/or persistence under sub-optimal environmental conditions, and (iv) evaluate the potential of current sub-optimal coral environments to act as potential refugia under changing environmental conditions. Such a collective approach is critical to better understand the future survival of corals in our changing environment. We finally outline priority areas for future research on extreme and marginal coral environments, and discuss the additional management options they may provide for corals through refuge or by providing genetic stocks of stress tolerant corals to support proactive management strategies.
... The sea anemone Anemonia viridis exposed to natural ocean acidification conditions appears to be physiologically acclimatized to low pH and optimizes its energy utilization under elevated pCO 2 through an increased autotrophic input (Suggett et al. 2012, Horwitz et al. 2015. Our recent transcriptome sequencing from the same sampling site indicates increased expression of stress-related transcripts, repression of global synthesis and boost in certain retrotransposon elements at low pH in A. viridis (Urbarova et al., unpublished results). ...
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Cnidarians harbour a variety of small regulatory RNAs that include microRNAs (miRNAs) and PIWI-interacting RNAs (piRNAs), but detailed information is limited. Here we report the identification and expression of novel miRNAs and putative piRNAs, as well as their genomic loci, in the symbiotic sea anemone Anemonia viridis. We generated a draft assembly of the A. viridis genome with putative size of 313 Mb that appeared to be composed of about 36% repeats, including known transposable elements. We detected approximately equal fractions of DNA transposons and retrotransposons. Deep sequencing of small RNA libraries constructed from A. viridis adults sampled at a natural CO2 gradient off Vulcano Island, Italy, identified 70 distinct miRNAs. Eight were homologous to previously reported miRNAs in cnidarians, while 62 appeared novel. Nine miRNAs were recognized as differentially expressed along the natural seawater pH gradient. We found a highly abundant and diverse population of piRNAs, with a substantial fraction showing ping-pong signatures. We identified nearly 22% putative piRNAs potentially targeting transposable elements within the A. viridis genome. The A. viridis genome appeared similar in size to that of other hexacorals with a very high divergence of transposable elements resembling that of the sea anemone genus Exaiptasia. The genome encodes and expresses a high number of small regulatory RNAs, which include novel miRNAs and piRNAs. Differentially expressed small RNAs along the seawater pH gradient indicated regulatory gene responses to environmental stressors.
... Size-frequency of the established coral communities of each habitat was binned into size categories; larger categories were pooled together to avoid the problems associated with low expected counts (Starnes et al., 2012). The maximum diameter for each colony was used for comparison to ensure standardization among colonies with different growth forms (per Suggett et al., 2012). Fits of exponential decay across the counts in each bin were performed for both 2012 and 2013 to assess the population size-classes (Santangelo et al., 2004). ...
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Coral communities are increasingly found to populate non-reef habitats prone to high environmental variability. Such sites include seagrass meadows, which are generally not considered optimal habitats for corals as a result of limited suitable substrate for settlement and substantial diel and seasonal fluctuations in physicochemical conditions relative to neighboring reefs. Interest in understanding the ability of corals to persist in non-reef habitats has grown, however little baseline data exists on community structure and recruitment of scleractinian corals in seagrass meadows. To determine how corals populate seagrass meadows, we surveyed the established and recruited coral community over 25 months within seagrass meadows at Little Cayman, Cayman Islands. Simultaneous surveys of established and recruited coral communities at neighboring back-reef sites were conducted for comparison. To fully understand the amount of environmental variability to which corals in each habitat were exposed, we conducted complementary surveys of physicochemical conditions in both seagrass meadows and back-reefs. Despite overall higher variability in physicochemical conditions, particularly pH, compared to the back-reef, 14 coral taxa were capable of inhabiting seagrass meadows, and multiple coral families were also found to recruit to these sites. However, coral cover and species diversity, richness, and evenness were lower at sites within seagrass meadows compared to back-reef sites. Although questions remain regarding the processes governing recruitment, these results provide evidence that seagrass beds can serve as functional habitats for corals despite high levels of environmental variability and suboptimal conditions compared to neighboring reefs.
... Photophysiology A diving-PAM underwater fluorometer (Waltz, Germany) was used to obtain maximal quantum yields (F v /F m ) of chlorophyll a fluorescence of colonies in situ (measurements taken early morning prior to direct sunlight exposure) and ex situ following 20 min of low light acclimation (settings: measuring light intensity = 8, saturation pulse intensity = 11, saturating width = 0.8, damp = 2, gain = 4) (e.g. Suggett et al. 2012). Triplicate measurements were made for each colony with a total of eight colonies measured at each timepoint. ...
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High-latitude coral communities are distinct from their tropical counterparts, and how they respond to recent heat wave events that have decimated tropical reefs remains unknown. In Australia, the 2016 El Niño resulted in the largest global mass coral bleaching event to date, reaching as far south as Sydney Harbour (~ 34°S). Coral bleaching was observed for the first time (affecting ca., 60% of all corals) as sea surface temperatures in Sydney Harbour remained > 2 °C above the long-term mean summer maxima, enabling us to examine whether high-latitude corals bleached in a manner described for tropical corals. Responses of the geographically cosmopolitan Plesiastrea versipora and southerly restricted Coscinaraea mcneilli were contrasted across two harbour sites, both in situ and among samples-maintained ex situ in aquaria continually supplied with Sydney Harbour seawater. While both coral taxa hosted the same species of microalgal endosymbiont (Breviolum spp; formerly clade B), only P. versipora bleached both in situ and ex situ via pronounced losses of endosymbiont cells. Both species displayed very different metabolic responses (growth, photosynthesis, respiration and calcification) and bleaching susceptibilities under elevated temperatures. Bacterial microbiome profiling, however, revealed a convergence of bacterial community composition across coral species throughout the bleaching. Corals species found in temperate regions, including the generalist P. versipora, will therefore likely be highly susceptible to future change as heat waves grow in frequency and severity unless their thermal thresholds increase. Our observations provide further evidence that high-latitude systems are susceptible to community reorganisation under climate change.
... Carbon dioxide seep studies show that acidification leads to greater dominance by non-calcified species; turf algae over coralline algae [19], soft corals and anemones over hard corals [41,42]. It also alters competitive interactions between organisms, favouring opportunistic organisms that can more easily adapt to the change in environmental conditions [43,44]. ...
Article
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The oceanic uptake of anthropogenic carbon dioxide emissions is changing seawater chemistry in a process known as ocean acidification. The chemistry of this rapid change in surface waters is well understood and readily detectable in oceanic observations, yet there is uncertainty about the effects of ocean acidification on society since it is difficult to scale-up from laboratory and mesocosm tests. Here, we provide a synthesis of the likely effects of ocean acidification on ecosystem properties, functions and services based on observations along natural gradients in pCO 2. Studies at CO 2 seeps worldwide show that biogenic habitats are particularly sensitive to ocean acidification and that their degradation results in less coastal protection and less habitat provisioning for fisheries. The risks to marine goods and services amplify with increasing acidification causing shifts to macroalgal dominance, habitat degradation and a loss of biodiversity at seep sites in the tropics, the sub-tropics and on temperate coasts. Based on this empirical evidence, we expect ocean acidification to have serious consequences for the millions of people who are dependent on coastal protection, fisheries and aquaculture. If humanity is able to make cuts in fossil fuel emissions, this will reduce costs to society and avoid the changes in coastal ecosystems seen in areas with projected pCO 2 levels. A binding international agreement for the oceans should build on the United Nations Sustainable Development Goal to 'minimise and address the impacts of ocean acidification'.
... Moreover,McClintock et al. (2014) reported similar results on the accumulation of trace elements(As, Cd, Co, Cr, Hg, Mo, Ni, Pb and V) in shells of four different species of gastropods, which were collected from three sites in Levante Bay with different pH values. On the other hand,Horwitz et al. (2014) found changes in trace elements accumulation in the sea anemone Anemonia viridis between impacted and control sites, although no apparent signs of stress were detected(Suggett et al. 2012). ...
Thesis
The “business-as-usual emission scenario” simulated by the IPCC (Intergovernmental Panel on Climate Change) suggests that atmospheric CO2 levels could approach 800 ppm by the end of the century. Corresponding biogeochemical models indicate that surface ocean water pH will drop from a pre-industrial value of about 8.2 to 7.8 within 2100 (Feely et al., 2010). This phenomenon known as "Ocean Acidification" (OA) is caused by the increasing CO2 emissions due to anthropic activities, with a current consequence decrease of about 0.1 unit of pH (Caldeira & Wickett 2003) that is having effects on seawater carbonate chemistry and on marine ecosystems. Many short-term laboratory experiments have shown the effects of OA on marine calcareous organisms (Doney et al., 2009), but also on not-calcifying ones. For instance, experiments on fish have revealed effects on physiological and behavioral aspects (Dixson et al., 2010; Munday et al., 2009), but many other aspects are still unknown (Ishimatsu et al., 2008). On the other hand, field experiments have been conducted in naturally acidified marine ecosystems, known as CO2 vents, which are currently investigated to study the long-term effects of OA on species, communities and ecological processes (Hall-Spencer et al. 2008). Shallow CO₂ vents are widespread in Mediterranean (Dando et al., 1999) and represent a sort of natural mesocosms, where marked pH gradients are present at small spatial scales. The aim of this PhD project is to assess the effect of high pCO2/low pH on the structural and functional organization of fish assemblages in a Mediterranean shallow CO₂ vent (Aeolian Archipelago, NE Sicily). In particular, we compare the responses of a chronic exposed fish assemblage living near the primary vent (mean pH = 7.8; hereafter “Low pH”) with other two fish assemblages living at normal pH (mean pH = 8.2; hereafter “Control 1” and “Control 2”) in Vulcano and Lipari Islands. We hypothesized that the organization of fish assemblage at the low pH site is different from that in controls. To test our hypothesis we use several descriptors and different methodologies. First, we compared fish community structure by using Underwater Visual Census technique to assess species richness and abundance (frequency of occurrence). Then we carried out samplings to evaluate trophic organization of fish assemblages (we used stable isotopes of carbon and nitrogen to analyze food web and trophic levels), bioaccumulation and biomagnification of trace elements (concentration and bio-availability of several trace elements, also toxic ones, may increase due to direct input from the vent and to peculiar pH and Eh conditions), and the characteristics of carbonate structures like otoliths (to assess the effect of acidification on these structures by morphological analysis). Otoliths are also used as natural tags to study fish “site fidelity” of this particular site through microchemistry analysis of trace elements and isotopic composition. This study provided a complete and exhaustive frame of fish assemblages structure and trophic organization at different pH levels. As scant data are available in the literature on this topic, the results of this research provide information about the ecological effects of long-term exposure to high CO2 levels on fish, a key biological component whose monitoring is relevant not only from the ecological side, but also for the economic one and for the implications on human health. Moreover, this study confirms the importance to use the naturally acidified environments to test ecological hypotheses on the effects of OA on communities and ecosystems.
... Carbon dioxide seep studies show that acidification leads to greater dominance by non-calcified species; turf algae over coralline algae [19], soft corals and anemones over hard corals [41,42]. It also alters competitive interactions between organisms, favouring opportunistic organisms that can more easily adapt to the change in environmental conditions [43,44]. ...
... Notably, these species often dramatically increase in abundance on coral reefs following disturbance events, e.g., blast fishing, Crown-of-Thorns starfish (Acanthaster planci) outbreaks, and eutrophication (Fabricius 1998), and thus can be considered 'opportunistic colonisers'. Evidence in fact suggests that under persistently disturbed habitats (CO 2 vents, coastal inlets), soft corals can become the dominant species within an alternate ecological state (Inoue et al. 2013), implying that reef communities may become increasingly dominated by soft corals in the future as anthropogenic pressures continue to accelerate (e.g., Suggett et al. 2012;Tsounis and Edmunds 2017). ...
Article
Corals synthesise large quantities of the sulphur metabolite dimethylsulphoniopropionate (DMSP), which contributes to key roles in coral reef ecology including the capacity of corals to withstand various stressors. While closely related to scleractinian corals and often occupying similar ecological niche space, it is currently poorly defined to what extent soft corals produce DMSP. We, therefore, examined DMSP content within four key species of soft coral in February and July–August of 2017, including two temperate species from Sydney Harbour (Erythropodium hicksoni, Capnella gaboensis) and two tropical species from the Great Barrier Reef (Sinularia sp., Sarcophyton sp.). We compared DMSP content of these soft coral species to that of commonly occurring temperate (Plesiastrea versipora) and tropical (Acropora aspera) scleractinian coral species. DMSP content was normalised to coral protein content, with soft coral DMSP content highly variable across species and locations [56–539 nmol (mg protein)−1], and lower than for the tropical [1242–4710 nmol (mg protein)−1], but not temperate [465–1984 nmol (mg protein)−1] scleractinian species. Further comparison with previously published values demonstrated that soft coral DMSP content falls within the “low–mid range” of scleractinian corals. Notably, DMSP content was also higher in summer samples than winter samples for the scleractinian corals, but did not differ between seasons for soft corals. Such contrasting dynamics of DMSP production by soft corals compared to scleractinian corals indicates that the regulation of DMSP content differs between these two important benthic cnidarian groups, potentially as a consequence of dissimilar ecophysiological roles for this compound.
... Experimental treatments: ambient temperature-ambient pCO 2 (ATAC), ambient temperature-high pCO 2 (ATHC), high temperatureambient pCO 2 (HTAC) and high temperature-high pCO 2 (HTHC) Coral Reefs (2020) 39:331-344 339 pCO 2 on the photosynthesis of in hospite symbionts (Reynaud et al. 2003;Anthony et al. 2008;Kaniewska et al. 2012;Wall et al. 2014;Comeau et al. 2017), with only a few exceptions where positive responses were reported (Strahl et al. 2015;Noonan and Fabricius 2016;Bahr et al. 2018). However, the fertilizing effect of high pCO 2 is quite common in soft-bodied symbiotic cnidarians, such as zoanthids (Graham and Sanders 2016), soft corals (Inoue et al. 2013), sea anemones (Suggett et al. 2012;Towanda and Thuesen 2012;Jarrold et al. 2013;Hoadley et al. 2015a) and jellyfish (Klein et al. 2014(Klein et al. , 2017b. Overall, these contrasting results pose a basic but intriguing conundrum for the diverse photosynthetic functionality of symbiotic cnidarians in response to OA. ...
Article
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In this study, we tested whether larvae brooded by the reef coral Pocillopora damicornis from a naturally extreme and highly variable environment are preadapted to cope with predicted increases in temperature and pCO2. We exposed larvae to two temperatures (29 vs. 30.8 °C) crossed with two pCO2 levels (~ 500 vs. ~ 1000 μatm) in a full-factorial experiment for 5 d. Larval performance was assessed as dark respiration (RD), net and gross photosynthesis (PN and PG, respectively), survival, settlement, and the activity of carbonic anhydrase (CA), the central enzyme involved in photosynthesis. The results showed that RD was unaffected by either elevated temperature or pCO2, while elevated temperature and/or pCO2 stimulated PN and PG and increased the ratios of PN to RD, indicating a relatively higher autotrophic capacity. Consequently, larval survivorship under elevated temperature and/or pCO2 was consistently 14% higher than that under the control treatment. Furthermore, elevated temperature and pCO2 did not affect host CA activity, but synergistically enhanced symbiont CA activity, contributing greatly to the stimulated photosynthetic capacity. These results suggest that brooded larvae of P. damicornis larvae from Luhuitou may be preadapted to cope with projected warming and ocean acidification. More generally, it appears that corals from highly variable environments may have increased resilience to the widespread climate change.
... Anthropogenic greenhouse gas emissions, and CO 2 specifically, are also widely recognized as one of the biggest long-term threats to functional oceans ( Rogers and Laffoley 2013 ), due to the suite of associated impacts. Ocean acidity is increasing, influencing large swathes of ocean ecosystems in a multitude of ways ( Suggett et al., 2012 ;Kroeker et al., 2013 ). The ocean has absorbed over 90% of the excess heat from global warming, with consequences for organisms that are adapted to specific temperature ranges both in terms of latitudinal range as well as depth ranges . ...
Preprint
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While much has been learnt about the impacts of specific stressors on individual marine organisms, considerable debate exists over the nature and impact of multiple simultaneous stressors on both individual species and marine ecosystems. We describe a modelling tool (OSIRIS) for integrating the effects of multiple simultaneous stressors. The model is relatively computationally light, and demonstrated using a coarse-grained, non-spatial and simplified representation of a temperate marine ecosystem. This version is capable of reproducing a wide range of dynamic responses.Results indicate the degree to which interactions are synergistic is crucial in determining sensitivity to forcing, particularly for the higher trophic levels, which can respond non-linearly to stronger forcing. Stronger synergistic interactions sensitize the system to variability in forcing, and combinations of stronger forcing, noise and synergies between effects are particularly potent. This work also underlines the significant potential risk incurred in treating stressors on ecosystems as individual and additive.
... Here we add on these observations, suggesting that the higher densities of G. incognitus under elevated CO 2 levels are related to the higher density of the sea anemone A. viridis, hence supporting one of the most uncontroversial responses of coastal fishes to OA: i.e. the changing habitat provisioning effect (Sunday et al., 2017;Cattano et al., 2020). In this regard, previous studies conducted along the Levante Bay gradient in Vulcano Island suggested that increased pCO 2 may boost abundance/size, photosynthesis of zooxanthellae algae, respiration (Suggett et al., 2012), trophic flexibility (e.g., a higher autotrophic/heterotrophic ratio) (Horwitz et al., 2015), and the mechanisms by which A. viridis acclimate to chronic exposure to OA conditions (Urbarova et al., 2019). ...
Article
An in situ reciprocal transplant experiment was carried around a volcanic CO2 vent to evaluate the anti-predator responses of an anemone goby species exposed to ambient (∼380 μatm) and high (∼850 μatm) CO2 sites. Overall, the anemone gobies displayed largely unaffected behaviors under high-CO2 conditions suggesting an adaptive potential of Gobius incognitus to ocean acidification (OA) conditions. This is also supported by its 3-fold higher density recorded in the field under high CO2. However, while fish exposed to ambient conditions showed an expected reduction in the swimming activity in the proximity of the predator between the pre- and post-exposure period, no such changes were detected in any of the other treatments where fish experienced acute and long-term high CO2. This may suggest an OA effect on the goby antipredator strategy. Our findings contribute to the ongoing debate over the need for realistic predictions of the impacts of expected increased CO2 concentration on fish, providing evidence from a natural high CO2 system.
... A 34% reduction in anemone size caused by a heatwave event coincided with lower levels of recruitment of the anemone fish Amphirion polymnus (Saenz-Agudelo et al. 2011). In contrast, elevated CO 2 has generally been observed to increase photosynthesis in anemones (Suggett et al. 2012;Hoadley et al. 2015) or have no effect in isolation (Pryor et al. 2021). Collection of anemonefish for the aquarium trade could exacerbate the direct effects of environmental stress on anemones. ...
... In situ records are even more scarce and, although there is type material for some of these species, the condition of their physiognomy prevents the determination of all the traits that are currently used for a complete characterization of a new taxon. This is especially pertinent in a global context of ocean acidification, where the distribution of species is deemed to change (Suggett et al., 2012;Quattrini et al., 2020), and studies on the physiological response of sea anemones are still mainly focused on intertidal taxa. ...
Article
New in situ records of the sublittoral sea anemone Oulactis coliumensis (Riemann-Zürneck & Gallardo, 1990) are provided from different localities of northern Chile and Peru. Specimens were generally observed buried in shallow soft bottoms (3–25 m depth), near port cities and in areas with a high organic load. This is the first report of the species outside its type locality (off the Bay of Coliumo, Chile; ~36°S), extending its range of distribution to lower latitudes.
... The diversity and abundance of shells available to hermit crabs and the abundance of these crabs were all significantly reduced at high CO2 (Tomatsuri and Kon, 2019). An increased abundance of anemones in acidified conditions ties in with similar observations in the Mediterranean and may relate to a decrease in competition with calcareous animals for living space (Suggett et al., 2012). ...
Article
Japan has many coastal carbon dioxide seeps as it is one of the most volcanically active parts of the world. These shallow seeps do not have the spectacular aggregations of specialist fauna seen in deep-sea vent systems but they do have gradients in seawater carbonate chemistry that are useful as natural analogues of the effects of ocean acidification on marine biodiversity, ecosystem function and fisheries. Here, we compare macroinvertebrate diversity and abundance on rocky habitats at ambient (mean ≤ 410 µatm) and high (mean 971-1484 µatm) levels of seawater pCO2 in the warm-temperate region of Japan, avoiding areas with toxic sulphur or warm-water conditions. We show that although 70% of intertidal taxa and 40% of shallow subtidal taxa were able to tolerate the high CO2 conditions, there was a marked reduction in the abundance of corals, bivalves and gastropods in acidified conditions. A narrower range of filter feeders, grazers, detritivores, scavengers and carnivores were present at high CO2 resulting in a simplified coastal system that was unable to retain the high standing stocks of marine carbon biomass found in ambient conditions. It is clear that cuts in CO2 emissions would reduce the risks of climate change and ocean acidification impacts on marine biodiversity, shellfish production and biomass in the rocky coastal shores of this region.
... Indeed, biosynthetic activities in M. senile are suppressed in higher temperatures, with a significant effect on mortality and a lethal temperature for 50% (LT50) over 40 days reported at 24°C (Walsh and Somero, 1981;Glon et al., 2019), corroborating the threefold increase in respiration rate of M. senile in this study's ocean warming treatment. However, an apparent insensitivity to lowered pH levels negated this effect in the combined climate change treatment, further substantiating the hypothesis that 'sea anemones may thrive in a high CO 2 world' (Suggett et al., 2012). Nevertheless, the increased clearance rates measured in the ocean acidification treatment suggest that a higher food intake is needed to support altered physiological needs and homeostasis under low pH conditions. ...
Article
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In the effort towards a decarbonised future, the local effects of a proliferating offshore wind farm (OWF) industry add to and interact with the global effects of marine climate change. This study aimed to quantify potential ecophysiological effects of ocean warming and acidification and to estimate and compare the cumulative clearance potential of suspended food items by OWF epifauna under current and future climate conditions. To this end, this study combined ecophysiological responses to ocean warming and acidification of three dominant colonising species on OWF artificial hard substrates (the blue mussel Mytilus edulis, the tube-building amphipod Jassa herdmani and the plumose anemone Metridium senile). In general, mortality, respiration rate and clearance rate increased during 3- to 6-week experimental exposures across all three species, except for M. senile, who exhibited a lower clearance rate in the warmed treatments (+3 °C) and an insensitivity to lowered pH (−0.3 pH units) in terms of survival and respiration rate. Ocean warming and acidification affected growth antagonistically, with elevated temperature being beneficial for M. edulis and lowered pH being beneficial for M. senile. The seawater volume potentially cleared from suspended food particles by this AHS colonising community increased significantly, extending the affected distance around an OWF foundation by 9.2% in a future climate scenario. By using an experimental multi-stressor approach, this study thus demonstrates how ecophysiology underpins functional responses to climate change in these environments, highlighting for the first time the integrated, cascading potential effects of OWFs and climate change on the marine ecosystem.
... Numerous studies have reported mixed findings on the effects of high pCO 2 on the photo-physiology of symbiotic cnidarians. For example, acidification stress has been shown to increase productivity, symbiont density and photochemical efficiency in non-calcifying anthozoans (Suggett et al., 2012;Towanda and Thuesen, 2012;Jarrold et al., 2013;Gibbin and Davy, 2014;Horwitz et al., 2015;Klein et al., 2017) but the opposite in corals (Anthony et al., 2008;Crawley et al., 2010;Edmunds, 2012;Kaniewska et al., 2012;Zhou et al., 2016), and in fewer cases, no significant effects have been observed FIGURE 4 | Differential transcriptomic response of in hospite Symbiodinium microadriaticum CCMP2467 to CO 2 acidification stress. (A) Heat map showing GO terms related to photosynthesis and carbon concentrating mechanisms. ...
Article
Ocean acidification (OA) has both detrimental as well as beneficial effects on marine life; it negatively affects calcifiers while enhancing the productivity of photosynthetic organisms. To date, many studies have focused on the impacts of OA on calcification in reef-building corals, a process particularly susceptible to acidification. However, little is known about the effects of OA on their photosynthetic algal partners, with some studies suggesting potential benefits for symbiont productivity. Here, we investigated the transcriptomic response of the endosymbiont Symbiodinium microadriaticum (CCMP2467) in the Red Sea coral Stylophora pistillata subjected to different long-term (2 years) OA treatments (pH 8.0, 7.8, 7.4, 7.2). Transcriptomic analyses revealed that symbionts from corals under lower pH treatments responded to acidification by increasing the expression of genes related to photosynthesis and carbon-concentrating mechanisms. These processes were mostly up-regulated and associated metabolic pathways were significantly enriched, suggesting an overall positive effect of OA on the expression of photosynthesis-related genes. To test this conclusion on a physiological level, we analyzed the symbiont’s photochemical performance across treatments. However, in contrast to the beneficial effects suggested by the observed gene expression changes, we found significant impairment of photosynthesis with increasing pCO2. Collectively, our data suggest that over-expression of photosynthesis-related genes is not a beneficial effect of OA but rather an acclimation response of the holobiont to different water chemistries. Our study highlights the complex effects of ocean acidification on these symbiotic organisms and the role of the host in determining symbiont productivity and performance.
... The number of gonads started decreasing from June; therefore, the spawning and fertilization likely occurred during this month. Sea anemones grow fast (Suggett et al., 2012), and quickly divide by fission (Horton, 2000;Shick, 1991); moreover, the increase of the temperature occurring in July-September could promote asexual reproduction (Louis, 1960). The peak in cover occurring in July-September is probably due to both asexual reproduction and planulae settling. ...
Article
Population dynamics in lower metazoans are strongly regulated by environmental factors. The running climate crisis could affect regularity of life strategies; therefore, studying life cycles and reproductive patterns of benthic species may provide key information on effects of environmental changes in temperate seas. The North Adriatic Sea is a peculiar basin due to high food availability and high fluctuations of physical parameters. Here, cnidarians are one of the most abundant taxa and sea anemones are the largest representatives. Aim of this study is to assess the life history and the reproductive biology of two potential species models: the sea anemones: Anemonia viridis and Exaiptasia diaphana. The present research is the first quantitative study on the variations in abundance and reproductive biology of the two species. We reported new insights about abundance fluctuations throughout the year and about the gametogenesis of the two sea anemones. In particular, data on spermatogenesis of A. viridis from the Mediterranean Sea were supplied for the first time.
... At the Ischia's vents (Thyrrenian sea, Italy), where a natural gradient of seawater acidification is observed, Donnarumma et al. (2014) found that calcareous epibionts of the seagrass Posidonia oceanica were progressively less recruited with increasing acidity. On the contrary, the sea anemones (Anemonia viridis; a soft-bodied anthozoan) at this site grew faster with increasing seawater acidification along the gradient, probably due to a boost in the photosynthesis of the symbionts due to the increase in CO 2 partial pressure (pCO 2 , Suggett et al., 2012). Still, among calcifiers, the impacts of OA are not experienced equally, e.g., the calcifying bryozoans Electra pilosa were found to be unaffected by a seawater acidification down to a pH T of 7.3 (Saderne and Wahl, 2013). ...
... If we do not act to change course, the ocean's key biophysical functions could collapse 1 . Wider global and regional pressures (what we refer to as 'landscape pressures'-see Glossary in Table 1) on the ocean include rising levels of greenhouse gas emissions 1,19 , changes in chemistry, which impact species and food webs throughout ocean ecosystems 2,8,20 , warming [21][22][23] , deoxygenation 24 , overfishing, and run-off of pollution from land and coastal sources 1,25 . The Earth system-and the ocean in particular-is at risk of "irreversible or unimaginable" change 26 . ...
Article
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An amendment to this paper has been published and can be accessed via a link at the top of the paper.
... In fact, coral reefs were most vulnerable to extinction under rapid increases in temperature and CO 2 combined with declines in aragonite saturation 8 . The loss of corals and other reef builders during these reef crises could have driven increases in the diversification rates of non-aragonitic or even non-calcifying anthozoans (for example, proteinaceous corals or sea anemones) as these more resilient 15 species invaded empty, shallow-water niches caused by the extinction of reef builders. For example, anemones and octocorals can overgrow coral reefs following a reduction in live coral cover 16,17 and can dominate areas with naturally high partial pressure of CO 2 ( p CO2 I ) conditions 18 . ...
Article
Full-text available
Identifying how past environmental conditions shaped the evolution of corals and their skeletal traits provides a framework for predicting their persistence and that of their non-calcifying relatives under impending global warming and ocean acidification. Here we show that ocean geochemistry, particularly aragonite–calcite seas, drives patterns of morphological evolution in anthozoans (corals, sea anemones) by examining skeletal traits in the context of a robust, time-calibrated phylogeny. The lability of skeletal composition among octocorals suggests a greater ability to adapt to changes in ocean chemistry compared with the homogeneity of the aragonitic skeleton of scleractinian corals. Pulses of diversification in anthozoans follow mass extinctions and reef crises, with sea anemones and proteinaceous corals filling empty niches as tropical reef builders went extinct. Changing environmental conditions will likely diminish aragonitic reef-building scleractinians, but the evolutionary history of the Anthozoa suggests other groups will persist and diversify in their wake.
... If we do not act to change course, the ocean's key biophysical functions could collapse 1 . Wider global and regional pressures (what we refer to as 'landscape pressures'-see Glossary in Table 1) on the ocean include rising levels of greenhouse gas emissions 1,19 , changes in chemistry, which impact species and food webs throughout ocean ecosystems 2,8,20 , warming [21][22][23] , deoxygenation 24 , overfishing, and run-off of pollution from land and coastal sources 1,25 . The Earth system-and the ocean in particular-is at risk of "irreversible or unimaginable" change 26 . ...
Article
Full-text available
Human wellbeing relies on the Biosphere, including natural resources provided by ocean ecosystems. As multiple demands and stressors threaten the ocean, transformative change in ocean governance is required to maintain the contributions of the ocean to people. Here we illustrate how transition theory can be applied to ocean governance. We demonstrate how current economic and social systems can adapt to existing pressures and shift towards ocean stewardship through incorporation of niche innovations within and across economic sectors and stakeholder communities. These novel approaches support an emergent but purposeful transition and suggest a clear path to a thriving and vibrant relationship between humans and the ocean. Oceans provide important natural resources, but the management and governance of the ocean is complex and the ecosystem is suffering as a result. The authors discuss current barriers to sustainable ocean governance and suggest pathways forward.
... (Avir) can tolerate a wide range (10-35°C) of temperatures and rapidly fluctuating temperatures, in comparison to other Symbiodiniaceae. This could relate to the species' association to a hosta sea anemone, Anemonia viridis, which inhabits intertidal and sublittoral zones of temperate latitudes (Suggett et al., 2012;Roberty et al., 2016) (i.e. areas characterized by relatively wide daily and seasonal changes of temperature conditions, Table 1). ...
Article
Disentangling the metabolic functioning of corals’ endosymbionts (Symbiodiniaceae) is relevant to understand the response of coral reefs to warming oceans. In this work, we first questioned if there is an energetic coupling between photosynthesis and respiration in Symbiodiniaceae (Symbiodinium, Durusdinium and Effrenium), and second, how different levels of energetic coupling will affect their adaptive responses to global warming. Coupling between photosynthesis and respiration was established by determining the variation of metabolic rates during thermal response curves, and how inhibition of respiration affects photosynthesis. Adaptive responses (not reversible) were studied exposing two Symbiodinium species, with different levels of photosynthesis‐respiration interaction, to high temperature (32°C) for one year. We found that some Symbiodiniaceae have a high level of energetic coupling, i.e. photosynthesis and respiration have the same temperature dependency, and photosynthesis is negatively affected when respiration is inhibited. Conversely, photosynthesis and respiration are not coupled in other species. In any case, prolonged exposure to high temperature caused adjustments of both photosynthesis and respiration but these changes were fully reversible. We conclude that energetic coupling between photosynthesis and respiration has wide variation amongst Symbiodiniaceae and does not determine the occurrence of adaptive responses in Symbiodiniaceae to temperature increase.
... Hard corals were absent along transects taken at elevated CO 2 conditions. In contrast to some other CO 2 seep systems (Suggett et al., 2012;Inoue et al., 2013), soft corals were rare and were absent in our elevated CO 2 transects. Instead, dense mats of Caulerpa chemnitzia var. ...
Article
Ocean acidification will likely change the structure and function of coastal marine ecosystems over coming decades. Volcanic carbon dioxide seeps generate dissolved CO2 and pH gradients that provide realistic insights into the direction and magnitude of these changes. Here, we used fish and benthic community surveys to assess the spatio-temporal dynamics of fish community properties off CO2 seeps in Japan. Adding to previous evidence from ocean acidification ecosystem studies conducted elsewhere, our findings documented shifts from calcified to non-calcified habitats with reduced benthic complexity. In addition, we found that such habitat transition led to decreased diversity of associated fish and to selection of those fish species better adapted to simplified ecosystems dominated by algae. Our data suggest that near-future projected ocean acidification levels will oppose the ongoing range expansion of coral reef-associated fish due to global warming.
... Acredita-se que diferentes linhagens colonizaram os recifes em diferentes épocas, com pelo menos dois períodos de intensa colonização, um no Cretáceo Superior (90-72 Ma) e outro imediatamente após a grande extinção do Cretáceo-Paleógeno (65-56 Ma)(BELLWOOD, 1998; PRICE; SCHMITZ, 2014). Os peixes recifais são principalmente compostos por Perciformes e contém uma elevada diversidade de espécies que representam linhagens evolutivas distintas ligadas às mudanças no nível do mar, temperatura dos mares e clima global ocorridas no Pleistoceno.A maioria das espécies de peixes recifais, em um momento inicial do ciclo de vida, apresenta uma fase larval planctônica com características morfológicas e ecológicas distintas das encontradas nos indivíduos adultos(LEIS, 1991;HALL; WAKE, 1999). Muitos desses animais, por apresentarem pouca capacidade de efetuar longas migrações quando adultos, se utilizam de sua fase planctônica para alcançar áreas distantes ainda não ocupadas(SALE, 1991). ...
Thesis
Este estudo apresentou dados novos e relevantes sobre a geomorfologia, geofísica e biota do ambiente recifal do Seixas/PB, sendo um dos pioneiros nesse ambiente recifal com esse nível de detalhamento. Os estudos geológicos, geofísicos e geoquímicos evidenciaram a existência de compartimentos (praia, plataforma interna e recife), áreas (abrigada, platô recifal e batida) e feições geomorfológicas (canal, planície recifal, crista, frente recifal, pós-recife), indicando que os processos deposicionais do fundo marinho sofreram influência oceanográfica. Não foi possível encontrar a rocha-base de sustentação para a edificação do recife através de três perfurações com profundidade máxima de 250 cm, os resultados das lâminas petrográficas, do difratograma de raios-X analisados e do material coletado nos mergulhos realizados na parede externa do recife demonstraram que o recife do Seixas é uma formação biogênica carbonática coral-algal recente - associada com a evolução da linha de costa, com a elevada sedimentação costeira e agindo em conjunto com a elevação do nível do mar (Período Quaternário Holocênico) -, apoiada no terraço marinho de abrasão sob a planície costeira moldada pela Bacia Sedimentar Paraíba, mais precisamente na Sub-bacia Alhandra e dista aproximadamente 30 km do talude continental nordestino. Atualmente, o recife possui 1,18 km2 de área consolidada com altura máxima de 6 m. A partir de uma base consolidada arenítica ocorreu o assentamento e povoamento de organismos bentônicos, passando por processos de sucessões continuamente. Perfazendo uma área amostral de 225 m², com esforço amostral de 120 h de pesquisas visuais subaquáticas (uso de transectos e fotoquadrados) foi possível mapear as comunidades macroalgais, coralíneas e íctica e verificar que as variáveis ambientais profundidade e granulometria exercem influência na estruturação das comunidades. Em uma cobertura dominada por macroalgas (68,99%), corais, hidrocorais e zoantídeos (7,62%), estruturas calcárias - rodolitos (9,73%), sedimento não-consolidado (11,89%) e sedimento consolidado (1,77%), foram identificados 1435 peixes recifais, representados pelas famílias Haemulidae (696 indivíduos), Labridae-Scarinae (272 indivíduos), Pomacentridae (248 indivíduos), Acanthuridae (108 indivíduos) e em menor número de indivíduos, as famílias Epinephelidae, Mullidae, Sciaenidae, Holocentridae e Gobiidae. Como análise geral, a relação entre as áreas Abrigada e Platô e entre as áreas Batida e Platô, aponta a área Platô como um ambiente de ecótono. A nível de endemismo, quatro famílias coralíneas da ordem Escleractinia e oito espécies da ictiofauna são endêmicas da Província Biogeográfica Atlântico Sul, corroborando com a caracterização geral desta província (baixa diversidade com alto grau de endemismo, sobrevivendo em águas turvas). Através de oficinas e mapas conceituais construídos pelos usuários locais, constatou-se que o grupo dos pescadores é o que mais conhece o ambiente, seja pela necessidade da navegação (formação rochosa) e da pesca (locais de maior oferta, maior número de indivíduos, sendo o hidrocoral “coral-de-fogo” o mais conhecido devido à fauna associada). A junção do conhecimento científico correlacionado com o contexto biogeográfico e saber local adquirido resultaram na aplicação de três práticas ambientais (desvendando as criaturas marinhas, trilha ecológica e rota subaquática) envolvendo a comunidade local conforme premissas da ciência cidadã. O contexto biogeográfico marinho atribuído às práticas para o microcosmo recifal do Seixas foi fundamentado pelos processos históricos e ecológicos de como surgiu este ambiente geológico e de onde vieram as comunidades biológicas, demonstrando as conectividades numa visão local até global dos dias atuais. Palavras-chave: ambiente recifal, geologia sedimentar, comunidade recifal, saber local, práticas ambientais.
... Anthropogenic greenhouse gas emissions, and CO 2 specifically, are also widely recognized as one of the biggest long-term threats to functional oceans ( Rogers and Laffoley 2013 ), due to the suite of associated impacts. Ocean acidity is increasing, influencing large swathes of ocean ecosystems in a multitude of ways ( Suggett et al., 2012 ;Kroeker et al., 2013 ). The ocean has absorbed over 90% of the excess heat from global warming, with consequences for organisms that are adapted to specific temperature ranges both in terms of latitudinal range as well as depth ranges . ...
Article
While much has been learnt about the impacts of specific stressors on individual marine organisms, considerable debate exists over the nature and impact of multiple simultaneous stressors on both individual species and marine ecosystems. We describe a modelling tool (OSIRIS) for integrating the effects of multiple simultaneous stressors. The model is relatively computationally light, and demonstrated using a coarse-grained, non-spatial and simplified representation of a temperate marine ecosystem. This version is capable of reproducing a wide range of dynamic responses. Results indicate the degree to which interactions are synergistic is crucial in determining sensitivity to forcing, particularly for the higher trophic levels, which can respond non-linearly to stronger forcing. Stronger synergistic interactions sensitize the system to variability in forcing, and combinations of stronger forcing, noise and synergies between effects are particularly potent. This work also underlines the significant potential risk incurred in treating stressors on ecosystems as individual and additive.
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Ocean acidification is one of the most dramatic effects of the massive atmospheric release of anthropogenic carbon dioxide (CO2) that has occurred since the Industrial Revolution, although its effects on marine ecosystems are not well understood. Submarine volcanic hydrothermal fields have geochemical conditions that provide opportunities to characterise the effects of elevated levels of seawater CO2 on marine life in the field. Here, we review the geochemical aspects of shallow marine CO2-rich seeps worldwide, focusing on both gas composition and water chemistry. We then describe the geochemical effects of volcanic CO2 seepage on the overlying seawater column. We also present new geochemical data and the first synthesis of marine biological community changes from one of the best-studied marine CO2 seep sites in the world (off Vulcano Island, Sicily). In areas of intense bubbling, extremely high levels of pCO2 (> 10,000 μatm) result in low seawater pH (< 6) and undersaturation of aragonite and calcite in an area devoid of calcified organisms such as shelled molluscs and hard corals. Around 100–400 m away from the Vulcano seeps the geochemistry of the seawater becomes analogous to future ocean acidification conditions with dissolved carbon dioxide levels falling from 900 to 420 μatm as seawater pH rises from 7.6 to 8.0. Calcified species such as coralline algae and sea urchins fare increasingly well as sessile communities shift from domination by a few resilient species (such as uncalcified algae and polychaetes) to a diverse and complex community (including abundant calcified algae and sea urchins) as the seawater returns to ambient levels of CO2. Laboratory advances in our understanding of species sensitivity to high CO2 and low pH seawater, reveal how marine organisms react to simulated ocean acidification conditions (e.g., using energetic trade-offs for calcification, reproduction, growth and survival). Research at volcanic marine seeps, such as those off Vulcano, highlight consistent ecosystem responses to rising levels of seawater CO2, with the simplification of food webs, losses in functional diversity and reduced provisioning of goods and services for humans.
Chapter
The role of abiotic parameters in determining the distribution of coral communities was assessed on the relatively pristine Maputaland reefs of South Africa from comprehensive reef survey data. The reefs, on which 42 communities could be defined, occur within three geographically separate complexes. Patterns in benthic distribution could be partially explained by latitude and depth, in particular, with slope, turbulence and reef aspect playing far less role in that order. A few species were associated exclusively or in high abundance with some of the communities; in most, it was the ratio of otherwise cosmopolitan species within all of the reef complexes that distinguished them. Complex biotic variables were also considered but not quantified and it is likely that low genetic connectivity and high levels of self-seeding result in a measure of isolation of the communities within a latitudinal gradient.
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This study investigates the effects of long-term exposure to OA on skeletal parameters of four tropical zooxanthellate corals naturally living at CO2 seeps and adjacent control sites from two locations (Dobu and Upa Upasina) in the Papua New Guinea underwater volcanic vent system. The seeps are characterized by seawater pH values ranging from 8.0 to about 7.7. The skeletal porosity of Galaxea fascicularis, Acropora millepora, massive Porites, and Pocillopora damicornis was higher (up to ~ 40%, depending on the species) at the seep sites compared to the control sites. Pocillopora damicornis also showed a decrease of micro-density (up to ~ 7%). Thus, further investigations conducted on this species showed an increase of the volume fraction of the larger pores (up to ~ 7%), a decrease of the intraskeletal organic matrix content (up to ~ 15%), and an increase of the intraskeletal water content (up to ~ 59%) at the seep sites. The organic matrix related strain and crystallite size did not vary between seep and control sites. This multi-species study showed a common phenotypic response among different zooxanthellate corals subjected to the same environmental pressures, leading to the development of a more porous skeletal phenotype under OA.
Chapter
This chapter focuses on a relatively small subset of literature relating health issues and remedies for sea anemones themselves. It provides only relatively basic information on natural history, taxonomy, anatomy, and physiology to allow a clinician's orientation. Sea anemones are members of the class Anthozoa, along with the corals. The Zoanthiniaria are a small group of polypoid anthozoans that differ from most sea anemones in details of internal anatomy. Good water quality is important for anemones held in captivity, but the variations in conditions that are tolerable can be extreme. Anemones need some water motion. The amount of motion varies with species. Actinarian sea anemones such as Actinia equina , the beadlet sea anemone, use vesicular organs called acrorhagi to deter conspecific territorial competitors. Anemones, as all coelenterates, are susceptible to trauma. The shotgun application of various drugs in the hopes that one drug or the other will result in a positive outcome may occasionally work.
Chapter
One of the important consequences of climate change is its effect on the global fish population. Though not very highly pronounced each year, the effect of climate change is of cumulative nature. Global aquaculture is being affected by temperature changes of both water and air. Fluctuations in the ocean surface temperatures, ocean current patterns, wind speeds, and wave directions, all have its impact on aquaculture. Each year we see more and more incidences of extreme weather conditions in different parts of the world, be it in the form of hurricanes, heavy floods, etc. Fishes are subjected to various stress factors which in turn take a toll on its growth and development. This can lead to lower weight gain and increased mortality due to higher susceptibility to diseases. This, coupled with direct unsustainable anthropogenic activities in the oceans and rivers may lead to collapse of the marine and freshwater ecosystem. Recent studies have identified specific regions where marine aquaculture production will be positively and negatively affected. One of the sustainable ways of developing aquaculture in the coming decades would be by developing region-wise strategies to maintain or increase fish population levels and thus meet the global seafood demands even in 2050. The current review is an attempt to assess the effects of ocean warming, ocean acidification, and ocean deoxygenation on the growth, survival, and diversity of marine lifeforms and suggest ways to stop a complete collapse of marine fish population by 2050, the year for which the complete collapse is predicted based on projections.
Chapter
Simultaneous with the increases in global sea surface temperature, increasing atmospheric carbon dioxide (CO2) is driving changes in the chemistry of the oceans—a process known as ocean acidification. Over the last two decades, reef-related ocean acidification research has focused primarily on the consequences of elevated CO2 on calcification. The impacts of ocean acidification on other critical processes such as coral-algal symbioses and bleaching thresholds are less well known. In this chapter, I review the available literature on the impacts of ocean acidification on coral bleaching. I begin by providing context for ocean acidification and its impacts on coral reefs. I focus primarily on primary literature investigating the effects of CO2 on photophysiology, coral–algal symbioses, and bleaching responses while shedding light on information needs and unresolved issues. I also briefly touch on environmental factors other than temperature and ocean acidification that have the potential to influence coral bleaching responses (e.g., nutrients).
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Atmospheric CO2 partial pressure (pCO2) is expected to increase to 700 ppm or more by the end of the present century. Anthropogenic CO2 is absorbed by the oceans leading to decreases in pH and the CaCO3 saturation state (Ω) of the seawater. While pCO2 was shown to drastically decrease calcification rates in tropical, fast growing corals, here we show, using the Mediterranean symbiotic coral Cladocora caespitosa, that the conventional belief that an increase in pCO2, in the range predicted to 2100, reduces calcification rates may not be widespread in temperate corals. We found that the seasonal change in temperature was the predominant factor controlling the physiology and growth of C. caespitosa, while an increase in pCO2, alone or in combination with global warming, had no significant effect on photosynthesis, photosynthetic efficiency and calcification. This result differs from that obtained on reef-building corals, which exhibit lower rates of calcification at elevated pCO2. The lack of sensitivity of temperate corals to high-pCO2 levels might be due to its slow growth rates, which seem to be more dependent on temperature than on the saturation state of calcium carbonate in the range predicted for the end of the century.
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The rise in atmospheric CO2 has caused significant decrease in sea surface pH and carbonate ion (CO32-) concentration. This decrease has a negative effect on calcification in hermatypic corals and other calcifying organisms. We report the results of three laboratory experiments designed specifically to separate the effects of the different carbonate chemistry parameters (pH, CO32-, CO2 [aq], total alkalinity [AT], and total inorganic carbon [C T]) on the calcification, photosynthesis, and respiration of the hermatypic coral Acropora eurystoma. The carbonate system was varied to change pH (7.9-8.5), without changing CT; CT was changed keeping the pH constant, and CT was changed keeping the pCO2 constant. In all of these experiments, calcification (both light and dark) was positively correlated with CO32- concentration, suggesting that the corals are not sensitive to pH or CT but to the CO 32- concentration. A decrease of ∼30% in the CO 32- concentration (which is equivalent to a decrease of about 0.2 pH units in seawater) caused a calcification decrease of about 50%. These results suggest that calcification in today's ocean (pCO2 = 370 ppm) is lower by ∼20% compared with preindustrial time (pCO2 = 280 ppm). An additional decrease of ∼35% is expected if atmospheric CO 2 concentration doubles (pCO2 = 560 ppm). In all of these experiments, photosynthesis and respiration did not show any significant response to changes in the carbonate chemistry of seawater. Based on this observation, we propose a mechanism by which the photosynthesis of symbionts is enhanced by coral calcification at high pH when CO2(aq) is low. Overall it seems that photosynthesis and calcification support each other mainly through internal pH regulation, which provides CO32- ions for calcification and CO2(aq) for photosynthesis. © 2006, by the American Society of Limnology and Oceanography, Inc.
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An investigation was conducted to determine the effects of elevated pCO2 on the net production and calcification of an assemblage of corals maintained under near-natural conditions of temperature, light, nutrient, and flow. Experiments were performed in summer and winter to explore possible interactions between seasonal change in temperature and irradiance and the effect of elevated pCO2. Particular attention was paid to interactions between net production and calcification because these two processes are thought to compete for the same internal supply of dissolved inorganic carbon (DIC). A nutrient enrichment experiment was performed because it has been shown to induce a competitive interaction between photosynthesis and calcification that may serve as an analog to the effect of elevated pCO2. Net carbon production, NPC, increased with increased pCO2 at the rate of 3 ± 2% (μmol CO2aq kg−1)−1. Seasonal change of the slope NPC-[CO2aq] relationship was not significant. Calcification (G) was strongly related to the aragonite saturation state Ωa. Seasonal change of the G-Ωa relationship was not significant. The first-order saturation state model gave a good fit to the pooled summer and winter data: G = (8 ± 1 mmol CaCO3 m−2 h−1)(Ωa − 1), r2 = 0.87, P = 0.0001. Both nutrient and CO2 enrichment resulted in an increase in NPC and a decrease in G, giving support to the hypothesis that the cellular mechanism underlying the decrease in calcification in response to increased pCO2 could be competition between photosynthesis and calcification for a limited supply of DIC.
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Massive coral species play a key role in coral reef ecosystems, adding significantly to physical integrity, long term stability and reef biodiversity. This study coupled the assessment of the distribution and abundance of 4 dominant massive coral species, Diploastrea heliopora, Favia speciosa, F matthaii and Porites lutea, with investigations into species-specific photoacclimatory responses within the Wakatobi Marine National Park of southeast Sulawesi, Indonesia, to determine the potential of photoacclimation to be a driver of biological success. For this, rapid light curves using pulse amplitude modulated (PAM) chlorophyll a fluorescence techniques were employed with additional manipulations to circumvent differences of light quality and absorption between species and across environmental gradients. P. lutea was examined over a range of depths and sites to determine patterns of photoacclimation, and all 4 species were assessed at a single depth between sites for which long-term data for coral community structure and growth existed. Light availability was more highly constrained with depth than between sites; consequently, photoacclimation patterns for P. lutea appeared greater with depth than across environmental gradients. All 4 species were found to differentially modify the extent of non-photochemical quenching to maintain a constant photochemical operating efficiency (qP). Therefore, our results suggest that these massive corals photoacclimate to ensure a constant light-dependent rate of reduction of the plastoquinone pool across growth environments.
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To investigate the molecular diversity of symbiotic algae at the latitudinal. limits of their distribution, the ribosomal RNA gene sequences (rDNA) of the dinoflagellate Symbiodinium in benthic Cnidaria (corals, sea anemones etc.) on Bermuda (32degreesN) and in the Mediterranean and NE Atlantic (35 to 53degreesN) were analysed. The algae in Bermudian Cnidaria were identified as Symbiodinium of Phylotypes A, B and C, as previously described for benthic Cnidaria in the Caribbean (12 to 27degreesN). The algae in every sample of sea anemones (Anemonia spp. and Cereus pedunculatus) in the NE Atlantic and Mediterranean were a previously undescribed group within Phylotype A, possibly endemic to this high latitude region.
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The consequences of ocean acidification to benthic organisms and ecosystems could be significant but are, overall, poorly known and quantified at this time. By integrating the current knowledge on the effects of ocean acidification on major benthic biogeochemical processes, individual benthic organisms, and observed characteristics of benthic environments as a function of seawater carbonate chemistry, it is possible to draw some general conclusions regarding the response of benthic organisms and ecosystems to a world of increasingly higher atmospheric CO2 levels. Large-scale geographical and spatial differences in seawater carbonate system chemistry, owing to both natural and anthropogenic processes, provide a powerful means to evaluate the effects of ocean acidification on marine benthic systems. Based on this approach, it is concluded that benthic biogeochemical processes such as calcification and CaCO3 dissolution as well as the community composition of benthic ecosystems will most likely be significantly altered by ocean acidification.
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Experiments have shown that ocean acidification due to rising atmospheric carbon dioxide concentrations has deleterious effects on the performance of many marine organisms. However, few empirical or modelling studies have addressed the long-term consequences of ocean acidification for marine ecosystems. Here we show that as pH declines from 8.1 to 7.8 (the change expected if atmospheric carbon dioxide concentrations increase from 390 to 750ppm, consistent with some scenarios for the end of this century) some organisms benefit, but many more lose out. We investigated coral reefs, seagrasses and sediments that are acclimatized to low pH at three cool and shallow volcanic carbon dioxide seeps in Papua New Guinea. At reduced pH, we observed reductions in coral diversity, recruitment and abundances of structurally complex framework builders, and shifts in competitive interactions between taxa. However, coral cover remained constant between pH 8.1 and ~7.8, because massive Porites corals established dominance over structural corals, despite low rates of calcification. Reef development ceased below pH 7.7. Our empirical data from this unique field setting confirm model predictions that ocean acidification, together with temperature stress, will probably lead to severely reduced diversity, structural complexity and resilience of Indo-Pacific coral reefs within this century.
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1] We present ocean chemistry calculations based on ocean general circulation model simulations of atmospheric CO 2 emission, stabilization of atmospheric CO 2 content, and stabilization of atmospheric CO 2 achieved in total or in part by injection of CO 2 to the deep ocean interior. Our goal is to provide first-order results from various CO 2 pathways, allowing correspondence with studies of marine biological effects of added CO 2 . Parts of the Southern Ocean become undersaturated with respect to aragonite under the Intergovernmental Panel on Climate Change Special Report on Emissions Scenarios (SRES) A1, A2, B1, and B2 emission pathways and the WRE pathways that stabilize CO 2 at 650 ppm or above. Cumulative atmospheric emission of 5000 Pg C produces aragonite undersaturation in most of the surface ocean; 10,000 Pg C also produces calcite undersaturation in most of the surface ocean. Stabilization of atmospheric CO 2 at 450 ppm produces both calcite and aragonite undersaturation in most of the deep ocean. The simulated SRES pathways produce global surface pH reductions of $0.3–0.5 units by year 2100. Approximately this same reduction is produced by WRE650 and WRE1000 stabilization scenarios and by the 1250 Pg C emission scenario by year 2300. Atmospheric emissions of 5000 Pg C and 20,000 Pg C produce global surface pH reductions of 0.8 and 1.4 units, respectively, by year 2300. Simulations of deep ocean CO 2 injection as an alternative to atmospheric release show greater chemical impact on the deep ocean as the price for having less impact on the surface ocean and climate. Changes in ocean chemistry of the magnitude shown are likely to be biologically significant.
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In this review, we seek to develop new insights about the nature of algal-sea anemone symbioses by comparing such associations in temperate and tropical seas. Temperate seas undergo pronounced seasonal cycles in irradiance, temperature, and nutrients, while high irradiance, high temperature, and low nutrients are seasonally far less variable in tropical seas. We compare the nature of symbiosis between sea anemones (= actinians) and zooxanthellae (Symbiodinium spp.) in both regions to test tropical paradigms against temperate examples and to identify directions for future research. Although fewer anemone species are symbiotic in temperate regions, they are locally dominant and ecologically important members of the benthic community compared to the tropics.
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Rising atmospheric CO2 and its equilibration with surface ocean seawater is lowering both the pH and carbonate saturation state (Ω) of the oceans. Numerous calcifying organisms, including reef-building corals, may be severely impacted by declining aragonite and calcite saturation, but the fate of coral reef ecosystems in response to ocean acidification remains largely unexplored. Naturally low saturation (Ω~0.5) low pH (6.70–7.30) groundwater has been discharging for millennia at localized submarine springs (called “ojos”) at Puerto Morelos, México near the Mesoamerican Reef. This ecosystem provides insights into potential long term responses of coral ecosystems to low saturation conditions. In-situ chemical and biological data indicate that both coral species richness and coral colony size decline with increasing proximity to low-saturation, low-pH waters at the ojo centers. Only three scleractinian coral species (Porites astreoides, Porites divaricata, and Siderastrea radians) occur in undersaturated waters at all ojos examined. Because these three species are rarely major contributors to Caribbean reef framework, these data may indicate that today’s more complex frame-building species may be replaced by smaller, possibly patchy, colonies of only a few species along the Mesoamerican Barrier Reef. The growth of these scleractinian coral species at undersaturated conditions illustrates that the response to ocean acidification is likely to vary across species and environments; thus, our data emphasize the need to better understand the mechanisms of calcification to more accurately predict future impacts of ocean acidification. KeywordsOcean acidification–Coral reefs–Calcification–Saturation state–Omega
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Nutrient sufficiency of zooxanthellae in the sea anemone Aiptasia pallida cultured in low nutrient seawater depends on the availability of particulate food to the host. Zooxanthellae in anemones unfed for 20 to 30 d exhibited the following characteristics of nutrient deficiency: cell division rates decreased; chlorophyll a content gradually decreased from 2 to –1; and C:N ratios increased from 7.5 to 16. Over a 3-mo period, algal populations in unfed anemones gradually decreased, indicating that zooxanthellae were lost faster than they were replaced by division. The mitotic index of zooxanthellae in unfed anemones was stimulated either by feeding the host or by the addition of inorganic N and P to the medium. Whether algae are nutrient-limited in hosts under field conditions has not been examined fully; however, C:N ratios in zooxanthellae from field-collected hosts are slightly higher (9.4 vs 7.5) than in hosts fed to repletion in laboratory cultures. This observation might indicate N limitation in the field.
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We present the first study of the effects of ocean acidification on settlement of benthic invertebrates and microfauna. Artificial collectors were placed for 1month along pH gradients at CO2 vents off Ischia (Tyrrhenian Sea, Italy). Seventy-nine taxa were identified from six main taxonomic groups (foraminiferans, nematodes, polychaetes, molluscs, crustaceans and chaetognaths). Calcareous foraminiferans, serpulid polychaetes, gastropods and bivalves showed highly significant reductions in recruitment to the collectors as pCO2 rose from normal (336–341ppm, pH 8.09–8.15) to high levels (886–5,148ppm) causing acidified conditions near the vents (pH 7.08–7.79). Only the syllid polychaete Syllis prolifera had higher abundances at the most acidified station, although a wide range of polychaetes and small crustaceans was able to settle and survive under these conditions. A few taxa (Amphiglena mediterranea, Leptochelia dubia, Caprella acanthifera) were particularly abundant at stations acidified by intermediate amounts of CO2 (pH 7.41–7.99). These results show that increased levels of CO2 can profoundly affect the settlement of a wide range of benthic organisms.
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Dynamics of a coral reef community at Tiao-Shi Reef, southern Taiwan were studied using permanent transects to examine coral recovery and successive cascades to collapse stage resulting from chronic anthropogenic impacts and typhoons. Three distinct zones were recognized within a relatively small study area (250m across) formerly dominated by large stands of branching Acropora corals. The first zone still retains the dominance of branching Acropora corals, although they show a significant decreasing tendency. The second zone exhibits recovery with a significant increase in branching Montipora stellata, which is recruited and grows faster than branching Acropora corals. The third zone is occupied by anemone, Condylactis sp., and demonstrates a stable phase of coral deterioration without recovery. Such differences in coral reef community dynamics within a small spatial scale illustrate mosaic dynamics which have resulted from degradation of the water quality, patchy mortality of large branching Acropora thickets caused by typhoons, the rapid asexual fragmentation and growth of M. stellata making it a successful colonizer, and occupation by anemone, Condylactis sp., together with unstable remnants of dead Acropora rubbles have not allowed coral recruits to survive.
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 Symbiotic dinoflagellates are abundant in the endoderm cells of tropical marine anthozoans, but the cell-specific density (CSD) of symbionts has not yet been investigated. In this study we used mechanical and enzymatic methods of maceration, and staining with substrate-specific fluorochromes, to observe a large number of individual host cells from 33 species of tropical anthozoans collected in Florida, Hawaii and Jamaica or cultured in Monaco. In the majority of species, most of the host cells contained a single algal cell (singlet). Host cells with two or more (up to six) algae were much less abundant. The average CSD for the 33 species was 1.54±0.30 (range 1.11 to 2.19). Singlets arranged in a monolayer can account for the areal density of algae observed in many anthozoans. The dinoflagellates occupy most of the interior of macerated host cells, leaving the host cytoplasm and cell membrane as a thin outer layer, often unresolvable by light microscopy. This spatial arrangement may favor diffusion and transport of CO2, bicarbonate ions, and nutrients from the environment to the algae. The effect of nutrient enrichment on CSD was determined by exposing eleven species to chronically elevated levels of ammonium-N. After four weeks all species exhibited a dramatic increase in algal mitotic index and CSD. The potential consequences of environmentally induced increases in CSD in tropical anthozoans are discussed in terms of the decreased cell-specific photosynthesis (CO2 limitation) and decreased rates of calcification observed in other studies.
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A community ecology approach to the study of the most common group of zooxanthellae, dinoflagellates in the genus Symbiodinium, was applied to symbiotic invertebrate assemblages on coral reefs in the western Caribbean, off the Yucatan peninsula (Puerto Morelos, Mexico) and over 1000 km away in the northeastern Caribbean, at Lee Stocking Island, Bahamas. Sequence differences and intragenomic variation, as determined by denaturing gradient gel electrophoresis and sequencing of the internal transcribed spacer 2 (ITS 2) region, were used to classify these symbionts. Twenty-eight genetically distinct Symbiodinium types were identified, eleven of which were found in hosts from both Caribbean locations. A single symbiont population was detected in 72% of hosts from the Yucatan and 92% of hosts from the Bahamas. The reef-wide community distribution of these symbionts is dominated by a few types found in many different host taxa, while numerous rare types appear to have high specificity for a particular host species or genus. Clade or lineage A Symbiodinium spp. was restricted to compatible hosts located within 3-4 m of the surface, while Symbiodinium spp. types from other lineages displayed differences in vertical zonation correlated with ITS type but were independent of clade designation. A comparison of the symbiont types found in field-collected hosts with types previously cultured from these hosts indicates the existence of low density or "background"-symbiont populations and cryptic, potentially non-mutualistic types in some hosts.
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