As the air's CO2 content rises in response to ever-increasing anthropogenic CO2 emissions, and as more and more carbon dioxide therefore dissolves in the surface waters of the world's oceans, theoretical reasoning suggests the pH values of the planet's oceanic waters should be gradually dropping. The IPCC and others postulate that this chain of events, commonly referred to as ocean acidification, will cause great harm -- and possibly death -- to marine life in the decades and centuries to come. However, as ever more pertinent evidence accumulates, a much more optimistic viewpoint is emerging. Such optimism is the focus of this summary examining the effects of ocean acidification on bivalves.
Sanders et al. (2013) "investigated the effects on oxygen consumption, clearance rates and cellular turnover in juvenile [king scallop] Pecten maximus following three months' laboratory exposure to four pCO2 treatments (290, 380, 750, and 1140 ppm)." In discussing their findings, the four researchers state "none of the exposure levels were found to have significant effects on the clearance rates, respiration rates, condition index or cellular turnover (RNA: DNA) of individuals." These findings are compatible with those of Anderson et al. (2013), who also studied the growth, development and survival of the initial larval stages of P. maximus and who found them to only be susceptible to the deleterious effects of ocean acidification at pCO2 levels of 1600 ppm and above. Sanders et al. conclude their results suggest that "where food is in abundance, bivalves like juvenile P. maximus may display a tolerance to limited changes in seawater chemistry."
Berge et al. (2006) collected blue mussels (Mytilus edulis L.) from the outer part of the Oslofjord outside the Marine Research Station Solbergstrand in Norway, and placed them in five 5-liter aquariums continuously supplied with low-food-supply sea water that was extracted from the top meter of the Oslofjord outside the Marine Research Station Solbergstrand in Norway, while CO2 was continuously added to the waters of the aquaria so as to maintain them at five different pH values (means of 8.1, 7.6, 7.4, 7.1 and 6.7) for a period of 44 days. Shell lengths at either the time of death or at the end of the study were determined and compared to lengths measured at the start of the study.
According to the authors, "the increased concentration of CO2 in the water and the correspondingly reduced pH had no acute effects on the mussels." With respect to growth, the Norwegian researchers report "mean increments of shell length were much lower for the two largest CO2 additions compared to the values in the controls, while for the two smallest doses the growth [was] about the same as in the control, or in one case even higher," such that there were "no significant differences between the three aquaria within the pH range 7.4-8.1."
Berge et al. conclude their results "indicate that future reductions in pH caused by increased concentrations of anthropogenic CO2 in the sea may have an impact on blue mussels," but "comparison of estimates of future pH reduction in the sea (Caldeira and Wickett, 2003) and the observed threshold for negative effects on growth of blue mussels [which they determined to lie somewhere between a pH of 7.4 and 7.1] do however indicate that this will probably not happen in this century." Indeed, Caldeira and Wickett's calculation of the maximum level to which the air's CO2 concentration might rise yields a value that approaches 2000 ppm around the year 2300, representing a surface oceanic pH reduction of 0.7 units, which only drops the pH to the upper limit of the "threshold for negative effects on growth of blue mussels" found by Berge et al., i.e., 7.4. Consequently, blue mussels will likely never be bothered, even in the least degree, by the tendency for atmospheric CO2 enrichment to lower oceanic pH values.
Noting "there is a particular need to study effects of OA [ocean acidification] on organisms living in cold-water environments due to the higher solubility of CO2 at lower temperatures," Bechmann et al. (2011) maintained mussel (Mytilus edulis) larvae in a laboratory setting under the OA scenario predicted for the year 2100 (pH 7.6) and compared them against batches of larvae held under the current oceanic pH of 8.1 (the control treatment), while water temperature was kept at a constant 10°C. Results indicated "there was no marked effect on fertilization success, development time, or abnormality to the D-shell stage, or on feeding of mussel larvae in the low-pH treatment," and the authors say the M. edulis larvae "were still able to develop a shell in seawater under-saturated with respect to aragonite (a mineral form of CaCO3)." On the negative side, they found after two months of exposure, the mussels were 28% smaller in the pH 7.6 treatment than in the control treatment. However, they say "if only the larger larvae settle and survive in the field, the effects of OA on the mussel population may not be dramatic."
According to Thomsen et al. (2010), "as most laboratory experiments cannot account for species genetic adaptation potential, they are limited in their predictive power." Thus studies investigating "naturally CO2-enriched habitats" have "recently gained attention, as they could more accurately serve as analogues for future, more acidic ecosystems." Taking this latter course, Thomsen et al. set out to study the macrobenthic community in Kiel Fjord-a naturally-CO2-enriched site in the Western Baltic Sea-that is dominated by calcifying marine invertebrates, where they determined in 34%, 23% and 9% of the 42 weeks they were there, the partial pressure (p) of CO2 in the water exceeded pre-industrial pCO2 (280 ppm) by a factor of three (>840 ppm), four (>1120 ppm) and five (>1400 ppm), respectively.
In describing their findings, the German scientists report juvenile blue mussel (Mytilus edulis) recruitment "peaks during the summer months, when high water pCO2 values of ~1000 ppm prevail." In addition, they say their short-term laboratory research indicates "blue mussels from Kiel Fjord can maintain control rates of somatic and shell growth at a pCO2 of 1400 ppm." At 4000 ppm pCO2, however, they say both shell mass and extension rates were significantly reduced; but they found "regardless of the decreased rates of shell growth at higher [1400] pCO2, all mussels increased their shell mass at least by 150% during the 8-week trial, even at Ωarg (Ωcalc) as low as 0.17 (0.28)," where Ω is the calcium carbonate saturate state of either aragonite (arg) or calcite (calc).
In concluding the report of their field and laboratory work, as well as their mini-review of the pertinent scientific literature, Thomsen et al. state it is likely "long-term acclimation to elevated pCO2 increases the ability to calcify in Mytilus spp.," citing the studies of Michaelidis et al. (2005) and Ries et al. (2009) in addition to their own. And they say they could find "no causal relationship between the acid-base status and metabolic depression in this species at levels of ocean acidification that can be expected in the next few hundred years (IPCC, 2007)," after discovering in the waters of Kiel Fjord (and demonstrating in the laboratory) "communities dominated by calcifying invertebrates can thrive in CO2-enriched coastal areas."
Working at the same location three years later with a different set of coauthors in a similarly coupled laboratory and field study, Thomsen et al. (2013) set out to examine "the annual pCO2 variability in [the Kiel Fjord] habitat and the combined effects of elevated pCO2 and food availability on juvenile M. edulis growth and calcification." In the laboratory experiment, "mussel growth and calcification were found to chiefly depend on food supply, with only minor impacts of pCO2 up to 3,350 µatm." In the field location (Kiel Fjord), where maximum pCO2 values experienced during the summer were about 2,500 µatm at the surface of the fjord and more than 3000 µatm at its bottom, they observed "seven times higher growth and calcification rates of M. edulis at a high pCO2 inner fjord field station (mean pCO2 ca. 1,000 µatm) in comparison to a low pCO2 outer fjord station (ca. 600 µatm)." And they note this high inner fjord productivity "was enabled by higher particulate organic carbon concentrations," as a result of the fjord's "being "highly impacted by eutrophication, which causes bottom water hypoxia and consequently high seawater pCO2." In light of such findings, in the concluding paragraph of their paper, Thomsen et al. state their study demonstrates "a high inherent resilience of calcifying benthic communities in an estuarine, eutrophic habitat to elevated seawater pCO2," where "food supply, and not pCO2, appears to be the primary factor driving biomass and biogenic CaCO3 production, as well as community structure."
In an experiment designed to test the effects of increased pCO2and reduced pH of seawater on the calcification, growth and mortality of juvenile Ruditapes decussatus clams, Range et al. (2011) conducted a 75-day controlled CO2 perturbation experiment, where the carbonate chemistry of seawater was manipulated by diffusing pure CO2 into natural seawater to attain two reduced pH levels (by -0.4 and -0.7 pH unit compared to un-manipulated seawater). Under such conditions, it was the hypothesis of the authors that the juvenile clams would exhibit reduced net calcification, reduced growth of the shell and soft tissue, and increased mortality. At the conclusion of their experiment, however, the eight researchers say they found "no differences among pH treatments in terms of net calcification, size or weight of the clams," disproving the first two of their three hypotheses. Their third hypothesis also proved to be wrong-doubly wrong, in fact-for not only was juvenile clam mortality not increased in the low pH seawater, they say mortality was significantly reduced in the acidified treatments, which was something they describe as a truly "unexpected result."
The Portuguese scientists conclude their paper by noting that life is intriguingly complex and "the generalized and intuitively attractive perception that calcification will be the critical process impacted by ocean acidification is being increasingly challenged," citing Widdicombe and Spicer (2008) and Findlay et al. (2009) in this regard. The results of their own study further contribute to this emerging perception.
In an effort to provide a better understanding of the potential for the Sydney rock oyster (Saccostrea glomerata) to adapt to the threat of ocean acidification, Parker et al. (2011) measured the within- and between-population variability in the species' growth response to elevated pCO2, working with oysters (denoted as wild) that they collected from intertidal and shallow subtidal habitats along the southeast coast of Australia, as well as two lines (QB and LKB) of the same species that had been selectively bred to support the country's oyster aquaculture industry. The authors report the wild oysters experienced a 64% reduction in growth after four days of living in an elevated pCO2 environment of 1000 ppm (with a water pH of 7.84) compared to wild oysters reared in the ambient pCO2 environment of 375 ppm (with a water pH of 8.20), whereas the growth reduction experienced by QB oysters growing in the same two environments was 45%, and that experienced by LKB oysters was 25%. What is more, they report the LKB oysters reared at elevated pCO2 actually "grew slightly better than the wild oysters reared at ambient pCO2." Such observations, in the words of Parker et al., provide "preliminary evidence that selective breeding may be a solution to 'climate-proof' important aquaculture industries from the impacts of ocean acidification." And it is indicative of the innate ability of the Sydney rock oyster to genetically adapt to ocean acidification-on its own-over an appropriate time scale.
Building upon their findings of the previous year, with three additional coauthors Parker et al. (2012) introduce their follow-up study by writing that analyses of the impact of ocean acidification on marine organisms that have been conducted to date "have only considered the impacts on 'adults' or 'larvae', ignoring the potential link between the two life-history stages and the possible carry-over effects that may be passed from adult to offspring," citing the work of Dupont et al. (2010), Hendriks et al. (2010) and Kroeker et al. (2010). To begin to fill this research void, Parker et al. placed adults of wild-collected and selectively-bred populations of the Sydney rock oyster (Saccostrea glomerata)-which they obtained at the beginning of reproductive conditioning-within seawater equilibrated with air of either 380 ppm CO2 or 856 ppm CO2 that produced seawater pH values of 8.2 and 7.9, respectively, after which they measured the development, growth and survival responses of the two sets of larvae.
Under such conditions, the six scientists found "larvae spawned from adults exposed to elevated pCO2 were larger and developed faster." In addition, they say "selectively bred larvae of S. glomerata were more resilient to elevated CO2 than wild larvae," noting "measurement of the standard metabolic rate (SMR) of adult S. glomerata showed that at ambient CO2, SMR is increased in selectively bred compared with wild oysters," and that it is further increased "during exposure to elevated CO2." Such findings suggest, in the words of the researchers, "previous studies that have investigated the effects of elevated CO2 on the larvae of molluscs and other marine organisms [whose predecessors had not been exposed to elevated CO2] may overestimate the severity of their responses," concluding that the results of their work suggest "marine organisms may have the capacity to acclimate or adapt to elevated CO2 over the next century."
Miller et al. (2009) grew larvae of two oyster species-the Eastern oyster (Crassostrea virginica) and the Suminoe oyster (Crassostrea ariakensis)-for up to 28 days in estuarine water in equilibrium with air of four different CO2 concentrations (280, 380, 560, and 800 ppm), which were chosen to represent atmospheric conditions in the pre-industrial era, the present day, and the years 2050 and 2100, respectively, as projected by the IS92a business-as-usual scenario of the IPCC, and which were maintained by periodically aerating the different aquaria employed in the study with air containing 1% CO2, while larval growth was assessed via image analysis and calcification was determined by means of chemical analyses of calcium in the shells of the oyster larvae.
Results indicated that when the larvae of both species were cultured continuously from 96 hours post fertilization for 26 to 28 days while exposed to elevated CO2 concentrations, they "appeared to grow, calcify and develop normally with no obvious morphological deformities, despite conditions of significant aragonite undersaturation," stating that these findings "run counter to expectations that aragonite shelled larvae should be especially prone to dissolution at high pCO2." More specifically, they state "both oyster species generated larval shells that were of similar mean thickness, regardless of pCO2, Ωarag [aragonite compensation point] or shell area," remarking that they "interpret the pattern of similar shell thickness as further evidence of normal larval shell development."
Working with another oyster species (Crassostrea gigas), Havenhand and Schlegel (2009) observed and measured the species' sperm swimming behavior and fertilization kinetics in response to ocean acidification. The oysters, which they collected from a mixed mussel/oyster bed on the coast of western Sweden, were kept within flow-through tanks of filtered sea water that they maintained at either the normal ambient pH level or a level reduced by about 0.35 units that was created by bubbling CO2 through the water. Results indicated that in water of pH 8.15, mean sperm swimming speeds were 92.1 &plsmns; 4.8µm/s, while in water of pH 7.8 they were actually slightly higher at 94.3 &plsmns; 5.5µm/s, although the difference was not statistically significant. Likewise, mean fertilization success in water of pH 8.15 was 63.4%, while in water of pH 7.8 it was also slightly higher at 64.1%; although this difference, too, was not statistically significant.
Based on these findings, the Swedish scientists state "the absence of significant overall effects of pH on sperm swimming behavior and fertilization success is remarkable," emphasizing that power analyses they conducted "showed clearly that these results were not due to inadequate statistical power," and adding "the absence of significant effect is likely a true reflection of the responses of Crassostrea gigas gametes and zygotes from the Swedish west coast to levels of CO2-induced acidification expected by the end of this century," which finding is very encouraging.
Also focusing on the same oyster species, Gazeau et al. (2011) set out to "assess the impact of several carbonate-system perturbations on the growth of Pacific oyster (Crassostrea gigas) larvae during the first three days of development (until shelled D-veliger larvae)." This was done using filtered seawater obtained from the Oosterschelde (a nearby tidal inlet) with five different chemistries obtained "by separately manipulating pH, total alkalinity and aragonite saturation state." Under such conditions, the seven scientists say their results showed "developmental success and growth rates were not directly affected by changes in pH or aragonite saturation state but were highly correlated with the availability of carbonate ions ... as long as carbonate ion concentrations were above aragonite saturation levels." But when carbonate ion concentrations dropped below aragonite saturation levels, they found growth and development "strongly decreased."
Gazeau et al. conclude according to their results, "the effects of ocean acidification on larvae of Crassostrea gigas from the Oosterschelde estuary during the first three days of development are not significant as long as CO32- concentrations remain above aragonite saturated conditions." And they add "due to relatively high levels of total alkalinity in this area, it is not expected that seawater will become corrosive for aragonite following a decrease of 0.3 to 0.4 pH unit," which is to be compared with the 0.1 decrease in pH that is believed to have occurred since before the beginning of the Industrial Revolution and the present point in time.
In further discussing the subject, the French, English and Dutch researchers write "most calcifying species, including mollusks, are able to concentrate Ca2+ and CO32- ions at the site of calcification (McConnaughey and Gillikin, 2008)," and they say the bivalves they studied "should therefore be able to regulate calcification rates under suboptimal concentrations of Ca2+ and CO32-." In fact, they note "Thomsen et al. (2010) have shown that blue mussels are actively growing in a bay of the Western Baltic Sea naturally enriched with high CO2 water," and "juvenile recruitment occurs in summer time coinciding with low pH levels and aragonite under-saturated conditions." Thus, it would appear that the ocean acidification threat is not something that will seriously affect mollusks.
In prefacing their work, Ginger et al. (2013) note "our knowledge of the effect of reduced pH on C. gigas larvae presently relies presumptively on four short-term (< 4 days) survival and growth studies." Against this backdrop, and based on multiple physiological measurements made during various life stages of the oysters, Ginger et al. studied "the effects of long-term (40 days) exposure to pH 8.1, 7.7 and 7.4 on larval shell growth, metamorphosis, respiration and filtration rates at the time of metamorphosis, as well as the juvenile shell growth and structure of C. gigas. In doing so the seven scientists discovered "mean survival and growth rates were not affected by pH," "the metabolic, feeding and metamorphosis rates of pediveliger larvae were similar, between pH 8.1 and 7.7," "the pediveligers at pH 7.4 showed reduced weight-specific metabolic and filtration rates, yet were able to sustain a more rapid post-settlement growth rate," and "no evidence suggested that low pH treatments resulted in alterations to the shell ultra-structures or elemental compositions (i.e., Mg/Ca and Sr/Ca ratios)." In light of these several positive findings, Ginger et al. conclude "larval and post-larval forms of the C. gigas in the Yellow Sea are probably resistant to elevated CO2 and decreased near-future pH scenarios." In fact, they opine "the pre-adapted ability to resist a wide range of decreased pH may provide C. gigas with the necessary tolerance to withstand rapid pH changes over the coming century."
Working with juvenile Mytilus galloprovincialis specimens obtained from a mussel raft in the Ria de Ares-Betanzos of Northwest Spain, and reared in an experimental bivalve hatchery in Tavira, Portugal, Fernandez-Reiriz et al. (2012) tested the effects of three levels of seawater acidification caused by increasing concentrations of atmospheric CO2: a natural control level plus two lesser levels of pH, one reduced by 0.3 pH unit and another reduced by 0.6 pH unit. The work was accomplished by measuring several responses of the mussels after 78 days of exposure to the three sets of pH conditions, focusing on clearance and ingestion rate, absorption efficiency, oxygen consumption, ammonia excretion, oxygen to nitrogen ratio, and scope for growth. In describing their findings, the five researchers report significant differences among treatments were not observed for clearance, ingestion and respiration rates. However, they say the absorption efficiency and ammonium excretion rate of the juvenile mussels were inversely related to the 0.6 pH reduction, while the maximal scope for growth and tissue dry weight were also observed in the mussels exposed to the pH reduction of 0.6 unit. Fernandez-Reiriz et al. conclude their report by stating that their results suggest Mytilus galloprovincialis "could be a tolerant ecophysiotype to CO2 acidification, at least in highly alkaline coastal waters," while noting "mytilids are also able to dominate habitats with low alkalinity and high pCO2," citing the work of Thomsen et al. (2010) in this regard.
Working with the same species of mussels obtained from the same location off the coast of Northwest Spain under an identical pH regime, Range et al. (2012) tested the effects of seawater acidification on six-month-old juveniles, focusing their attention on growth, calcification and mortality. According to the eight researchers, the growth of the mussels, measured as relative increases in shell size and body weight during the 84 days of the experiment, "did not differ among treatments." In fact, they say a tendency for faster shell growth under elevated CO2 was apparent, "at least during the first 60 days of exposure." In the case of calcification, however, they note this process was reduced, but by only up to 9%. Yet even here they state "given that growth was unaffected, the mussels clearly maintained the ability to lay down CaCO3, which suggests post-deposition dissolution as the main cause for the observed loss of shell mass." Last of all, with respect to mortality, Range et al. write "mortality of the juvenile mussels during the 84 days was small (less than 10%) and was unaffected by the experimental treatments." With respect to the implications of their findings, the Portuguese scientists say they further support the fact "there is no evidence of CO2-related mortalities of juvenile or adult bivalves in natural habitats, even under conditions that far exceed the worst-case scenarios for future ocean acidification (Tunnicliffe et al., 2009)."
One example of the incredible ability of a mussel species to adapt and survive in seawater conditions considered beyond extreme, is that of Bathymodiolus brevior. According to Tunnicliffe et al. (2009), Bathymodiolus brevior is "a vent-obligate species that relies partly on symbiotic sulphide-oxidizing bacteria for nutrition (von Cosel and Metivier, 1994)" that is found "at many sites in the western Pacific Ocean, where it occupies habitats of low hydrothermal fluid flux." Using remotely-operated vehicles to collect mussel specimens, water samples and imagery, Tunnicliffe et al. examined dense clusters of the vent mussel "in natural conditions of pH values between 5.36 and 7.29 on the northwest Eifuku volcano, Mariana arc, where liquid carbon dioxide and hydrogen sulfide emerge in a hydrothermal setting," which they studied along with mussels from "two sites in the southwestern Pacific: Hine Hina in the Lau backarc basin and Monowai volcano on the Kermadec arc," where "the same mussel species nestles in cracks and rubble where weak fluid flow emerges."
Based on the pH values they observed, the authors were able to calculate saturation ratios for calcite (Ωcalc), which ranged from 0.01 to 0.61, with an average value of only 0.18. Nevertheless, they discovered "a dense mussel population, along with many other associated species (Limen and Juniper, 2006), on NW Eifuku, where chemosynthetic symbiosis provides an energetic benefit to living in a corrosive, low-pH environment." In discussing these findings, Tunnicliffe et al. say they attest to "the extent to which long-term adaptation can develop tolerance to extreme conditions." In fact, they report discovering four-decade-old mussels living at the sites they visited, stating "the mussels' ability to precipitate shells in such low-pH conditions is remarkable."
In another study indicative of extreme environmental conditions, Hammer et al. (2011) exposed specimens of the deep-sea bivalve Acesta excavata that they collected from cold-water reefs to water maintained in equilibrium with an atmospheric CO2 concentration of approximately 33,000 ppm that resulted in a pH value of 6.35-corresponding to conditions reported for water in close proximity to natural CO2 seeps on the ocean floor-for periods of 0.5, 1, 4, 12, 24 or 96 hours, after which the bivalves were returned to normal CO2/pH conditions for 1, 4, 12, 24 or 96 hours, during which periods they measured a number of their physiological functions. The three researchers report their exposure of A. excavata to water in equilibrium with the super-high CO2 concentration they employed in their study "induced extra- and intra-cellular acidosis that remained uncompensated during exposure," and they say "oxygen consumption dropped significantly during the initial phase." However, they found it "approached control values at the end of exposure" and "no mortality was observed in exposed animals."
Such observations, in the words of the researchers who conducted the study, suggest "A. excavata displays higher tolerance to severe environmental hypercapnia [a condition where there is too much CO2 in the blood] than what may be expected for deep-sea animals." However, they note Tunnicliffe et al. (2009) "found evidence that permanent exposure to similar conditions causes reduced growth rates and shell thickness in mussels adapted to live at deep-sea vents," and they speculate "such long-term effects may also develop in A. excavata." On the other hand, they note previous studies on other species that mostly involved exposure to moderate hypercapnia (PCO2 = 10,000 ppm or less) found complete compensation of extracellular acidosis has frequently been observed in fish, citing Heisler (1984, 1986), and "marine invertebrates are often able to partially counteract acidosis through accumulation of bicarbonate ions," citing the work of Lindinger et al. (1984), Portner et al. (1988), Michaelidis et al. (2005), Miles et al. (2007), Pane and Barry (2007) and Gutowska et al. (2010). And, of course, such unusually high atmospheric CO2 concentrations are far more extreme than any expected to occur in the real world by even the most extreme estimates, which suggests the marine life investigated by this collection of scientists should not be unduly stressed by future anthropogenic CO2 emissions.
Simulating an intertidal environment, Ivanina and Sokolova (2013) examined the interactive effects of seawater pH and the presence of a pair of toxic trace metals, cadmium (Cd) and copper (Cu) at levels of 25 µM of each separately, on the mitochondrial functions of two common marine bivalves: hard clams (Mercenaria mercenaria) and eastern oysters (Crassostrea virginica). Their work revealed that "mitochondrial functions of the intertidal bivalves C. virginica and M. mercenaria are relatively insensitive to pH in a broad physiologically relevant range." But when they were impacted at more extreme values, they found that ocean acidification "modulates the response of their mitochondria," such that a decrease in pH was actually proven protective of the clams and oysters. Such findings led the two researchers to conclude that "moderate acidosis (such as occurs during exposure to air, extreme salinities or elevated CO2 levels in the intertidal zone) may have a beneficial side-effect of protecting mitochondria against toxicity of metals," in that "reduced intracellular pH caused by exposure to elevated CO2 levels abolished the metal-induced generation of reactive oxygen species in isolated clam cells (Ivanina et al., 2013) consistent with a mitochondrial mechanism of the cytoprotective effects of moderate acidification," while noting that a similar mechanism had been "experimentally demonstrated for the surface proteins of unicellular algae" in the studies of Niyogi and Wood (2004), Wilde et al. (2006) and Esbaugh et al. (2013).
In summation, based on the findings presented above there are ample reasons to reject the conclusion of acidification alarmists, who contend that future reductions in oceanic pH will most assuredly be negative and decimate bivalves. In contrast, a growing number of studies reveal ocean acidification to be much less of a problem, or no problem at all, for these marine species.
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Last updated 16 March 2015