Ocean acidification: comparative impacts on the photophysiology of a temperate symbiotic sea anemone and a tropical coral

Ocean acidification has the potential to drastically alter the coral reef ecosystem by reducing the calcification rate of corals and other reef-builders, and hence a considerable amount of research is now focused on this issue. It also is conceivable that acidification may affect other physiological processes of corals. In particular, acidification may alter photosynthetic physiology and hence the productivity of the coraldinoflagellate symbiosis that is pivotal to the reef’s survival and growth. However, very little is known about the impacts of acidification on the photophysiology of corals or, indeed, other invertebrate-algal symbioses. This gap in our knowledge was addressed here by measuring the impacts of acidification (pH 7.6 versus pH 8.1) on the photophysiology and health of the tropical coral Stylophora pistillata and its isolated dinoflagellate symbionts (‘zooxanthellae’), and the temperate sea anemone Anthopleura aureoradiata. The comparative nature of this study allowed for any differences between tropical and temperate symbioses, and zooxanthellae in a symbiotic or free-living state, to be assessed. Corals, anemones and cultured zooxanthellae were maintained in flowthrough seawater systems, and treated either with non-acidified (control) seawater at pH 8.1, or seawater acidified with CO2 or HCl to pH 7.6. A variety of parameters, including zooxanthellar density, chlorophyll content, photosynthetic health (Yi), and the ratio of gross photosynthetic production to respiration (P:R) were measured via cell counts, spectrophotometry, respirometry and PAM fluorometry, at a series of time-points up to a maximum of 42 days. Acidification generated by the addition of CO2 had no discernible effect on Yi of either the corals or anemones. However, in the coral, chlorophyll content per zooxanthella cell increased by 25%, which was countered by a near-significant decline (22%) in the rate of gross photosynthesis per unit chlorophyll; as zooxanthellar density remained unchanged, this led to a constant P:R ratio. When acidified via CO2, the isolated zooxanthellae exhibited no impacts in recorded Yi or chlorophyll levels. The response of the anemone to acidification via CO2 was different to that observed in the coral, as the density of zooxanthellae increased, rather than the chlorophyll content per cell, leading to an increased rate of gross photosynthesis. However P:R again remained constant as the increased photosynthesis was matched by an increased rate of respiration. In contrast to the impacts of CO2, HCl adversely impacted the chlorophyll content per cell in both the isolated zooxanthellae and sea anemone, and Yi, gross photosynthesis per cell, and overall gross photosynthesis in the sea anemone; however, despite the decline in gross photosynthesis, P:R remained constant due to the concurrent decline in respiration. Unfortunately, the corals in the HCl experiment died due to technical issues. There are two plausible reasons for this difference between CO2 and HCl. Firstly, HCl may have caused intracellular acidosis which damaged chloroplast structure and photosynthetic function. Secondly, the increased levels of aqueous CO2 stimulated photosynthetic function and hence mitigated for the effects of lowered pH. In addition, evidence is presented for a pH threshold for A. aureoradiata of between pH 6 and pH 6.75 (acidified with HCl), at which point photosynthesis ‘shuts-down’. This suggests that, even without the potentially beneficial effects from increased CO2 levels, it is likely that oceanic pH would need to decrease to less than pH 6.75 for any acidosis effects to compromise the productivity of this particular symbiosis. Since acidification will have the benefits of increased CO2 and will reach nowhere near such low pH levels as those extremes tested here, it is proposed that ocean acidification via increased dissolution of CO2 into our oceans will have no impact on the photosynthetic production of symbiotic cnidarians. Indeed, it is entirely likely that increased CO2 will add some benefit to the usually carbon-limited symbiotic zooxanthellae. Ocean acidification is not likely to benefit corals however, with compromised calcification rates likely to undermine the viability of the coral. Symbiotic sea anemones, which do not bio-mineralise CaCO3, are better placed to take advantage of the increased CO2 as we move toward more acidic oceans.

Effects of pH on asexual reproduction and statolith formation of the scyphozoan, Aurelia labiata

Although anthropogenic influences such as global warming, overfishing, and eutrophication may contribute to jellyfish blooms, little is known about the effects of ocean acidification on jellyfish. Most medusae form statoliths of calcium sulfate hemihydrate that are components of their balance organs (statocysts). This study was designed to test the effects of pH (7.9, within the average current range, 7.5, expected by 2100, and 7.2, expected by 2300) combined with two temperatures (9 and 15°C) on asexual reproduction and statolith formation of the moon jellyfish, Aurelia labiata. Polyp survival was 100% after 122 d in seawater in all six temperature and pH combinations. Because few polyps at 9°C strobilated, and temperature effects on budding were consistent with published results, we did not analyze data from those three treatments further. At 15°C, there were no significant effects of pH on the numbers of ephyrae or buds produced per polyp or on the numbers of statoliths per statocyst; however, statolith size was significantly smaller in ephyrae released from polyps reared at low pH. Our results indicate that A. labiata polyps are quite tolerant of low pH, surviving and reproducing asexually even at the lowest tested pH; however, the effects of small statoliths on ephyra fitness are unknown. Future research on the behavior of ephyrae with small statoliths would further our understanding of how ocean acidification may affect jellyfish survival in nature.

Reconsidering evidence for potential climate-related increases in jellyfish

Attrill et al. (2007) in their paper ‘‘Climate-related increases in jellyfish frequency suggest a more gelatinous future for the North Sea’’ present data showing the occurrence of nematocysts in continuous plankton recorder (CPR) samples collected over more than 40 yr. They suggest that, contrary to previous work examining a shorter period (Lynam et al. 2004), cnidarian nematocysts ‘‘most likely to be from scyphozoans’’ have increased, especially since the mid- 1980s. However, several problems with their analyses make it difficult to evaluate their conclusions.

Reply to Haddock, S.H.D. Reconsidering evidence for potential climate-related increases in jellyfish

Following the publication of our paper (Attrill et al. 2007), we became quickly aware of a couple of errors. We have subsequently been collaborating with Dr. Chris Lynam (Lynam et al. 2004, 2005) to bring together our two datasets, explore the common patterns within our data, and attempt to provide a consensus on how climate is affecting gelatinous plankton in the North Sea. During this reanalysis, two errors within the data were discovered, one involving a transcription error of a column of residuals during de-trended analysis, the other a major data entry error deep in the Continuous Plankton Recorder (CPR) database for sector B2.

Are jellyfish increasing in response to ocean acidification?

Ocean acidification may negatively affect calcifying plankton, opening ecological space for noncalcifying species. Recently, a study of climate-forcing of jellyfish reported the first analysis suggesting that there were more jellyfish (generally considered a noncalcifying group) when conditions were more acidic (lower pH) from one area within the North Sea. We examine this suggestion for a number of areas in the North Sea and beyond in the Northeast Atlantic using coelenterate records from the Continuous Plankton Recorder and pH data from the International Council for the Exploration of the Sea for the period 1946–2003. We could find no significant relationships between jellyfish abundance and acidic conditions in any of the regions investigated. We conclude that the role of pH in structuring zooplankton communities in the North Sea and further afield at present is tenuous.