Ocean Acidification and Photosynthetic Marine Organisms

Ocean acidification, often described as the “other CO₂ problem”, is of increasing concern for marine organisms as atmospheric carbon dioxide concentrations continue to rise.  Despite their large importance in the maintenance of marine ecosystems and their role as the base of the trophic food web, the effects of ocean acidification on photosynthesising marine organisms, has not received as much attention as other marine taxa, namely calcifying organisms. Consequently, this review shall assess the best current knowledge on the growth and photosynthesis responses of phytoplankton, seagrasses and macroalgae to ocean acidification. The review concludes that the effects on photosynthesising organisms can have a combination of positive, neutral and negative impacts depending on the species and the specific conditions (such as temperature and nutrients). This topic warrants greater attention and focus on the multiple stressors that are predicted for future oceans, due to the far-reaching implications of the potential loss of primary productivity on marine ecosystems.

Atmospheric carbon dioxide (CO₂) concentrations (pCO₂) are rising globally (Figure 1) from a pre-industrial pCO₂ of 280ppm to over 400ppm in the present day¹. Ocean acidification (OA) involves chemical changes to the carbonate system of seawater induced from the entry of anthropogenic CO₂ into the sea^2,3. Approximately 25% of anthropogenic emissions are absorbed in this way^2,3 and it is emerging as one of the significant environmental challenges of the 21^st century^2,4. The concentrations of hydrogen ions in seawater globally has risen by 30% since pre-industrial times, a rate unprecedented in the geologic record5, resulting in an approximate 26% increase in acidity³.

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Figure 1: Time series of increasing atmospheric CO₂, surface ocean pCO₂ and declining seawater pH between the years 1988 and 2008. Data collected atatmospheric Mauna Loa Observatory (MLO) on the island of Hawai‘I and Station ALOHA in the subtropical North Pacific north of Hawai‘i. Note that the current atmospheric CO₂ is currently over 410ppm as of February 2019. Figure from: Doney, 2010³.

Ocean acidification has been widely studied in respect to calcifying organisms⁶, consequently, many of the most cited ocean acidification publications have a focus on such organisms⁷. Therefore, this review will identify the interspecific differences of the effects of OA on photosynthesis and growth of photosynthetic marine organisms including phytoplankton, macroalgae and seagrasses. As research has developed OA is often no longer studied in isolation, therefore much of the literature used considers OA alongside other factors. The response to a decline in seawater pH on these key ecological species is poorly understood⁸, despite their pivotal role in the maintenance of marine ecosystems.

The Importance of Photosynthetic Organisms

Photosynthetic marine organisms play a crucial role in marine ecosystems. Firstly, phytoplankton alone are responsible for approximately 40% of oceanic primary production⁹. Similarly, seagrasses, which compose some of the richest coastal ecosystems, yet have a relatively low occurrence, covering only 0.2% of the ocean surface, contribute disproportionately to marine primary productivity, resulting in their great importance to carbon cycling10. Finally, macroalgae, as well as the other focus organisms provide many ecosystem services including habitat stability and primary productivity^6,11. Of overriding importance is the role of these photosynthesising organisms as carbon sinks, which becomes increasingly important as atmospheric CO₂ continues to rise⁶. The response of photosynthesising organisms to falling ocean pH has been considered one of the most significant consequences of OA.

Phytoplankton Responses to Ocean Acidification

The effects of OA depend upon species specific physiologies¹². Overall, phytoplankton are expected to experience neutral or increased growth in a reduced pH environment^13-15 (Figure 2A). Despite differing experimental strategies much of the research draws the same conclusions. This overall positive effect is a result of the species being growth limited by dissolved inorganic carbon under ambient conditions, and therefore OA unlocks the photochemical potential of organisms¹⁶. However, nutritional conditions, an additional stressor, could alter the response to OA. Nutrient limited conditions can result in negative effects on phytoplankton growth¹⁷ (Figure 2B).

As may be expected, the impact of OA on calcifying phytoplankton is somewhat different. Studies on the widely abundant phytoplankton Emiliania huxleyi and Gephyrocapsa oceanica have suggested that growth rates will be reduced under enhanced CO₂ treatments, yet greater light intensity has the potential to lessen this inhibition^2,18,19. Interestingly, E.huxleyi has many morphotypes with varying degrees of mineralization, from lightly to over calcified. Even individuals that are greatly over calcified due to living in acidified upwelling zones experienced growth inhibition under enhanced CO₂ conditions, suggesting that no morphotype is adapted to acidified conditions, contrary to some research (Figure 2C)^18,20.

Seagrasses Responses to Ocean acidification

Seagrasses have the potential to play an interesting role in OA. The photosynthesis by seagrasses can alter seawater chemistry to the benefit of calcified organisms²¹. Therefore, the response of seagrasses to OA could have a local but significant impact on the survival of other organisms²². Species specific responses of seagrasses have shown a spectrum of responses under varying experimental designs, most being either neutral or positive¹². The ability of several species of seagrasses to maintain or increase photosynthesis under elevated CO₂ has been proven^12,23 (Figure 3A).

Although, when elevated CO₂, temperatures, and reduced pH are studied in tandem the response of seagrasses, such as Zostera noltii, can vary¹⁶. Reduced pH and elevated temperature, the likely future of the world’s oceans, cause a decline in photosynthetic efficiency representing an increase in photosynthetic stress (Figure 3B-C). In contrast, net photosynthestic rate of Z.noltii is neutrally affected by elevated CO₂ and reduced pH when considering pH in isolation, suggesting that temperature induces a stress response in some seagrasses^24,25. Therefore, multiple stressors can greatly affect the physiological responses of organisms. Future studies should consider all the associated impacts of OA including increased temperatures to model the most realistic scenarios for the future oceans.

Figure 3: Growth and photosynthesis responses of seagrass species to different experimental conditions. (A)Net photosynthetic rates of nine seagrass species from south‐west Australia measured at different CO₂ scenarios.Pre‐industrial CO₂ (pH 8.2 and 9 μM CO_2aq), elevated CO₂ (potential 2100‐level, pH 7.8 and 24 μM) and a CO₂ level to maintain near‐maximum photosynthetic rates (P_N max; pH 6.7 and 274 μM). Error bars representmeans ± Standard error.  Letters indicate statistical differences among CO₂ levels within species (Figure from: Borum et al., 2016)²³. (B) maximum PSII quantum yield, F_v/F_m of Z.noltii  and (C) F_v/F_m variability of Z.noltii at a combination of ambient, warming (+4 °C) and acidified (ΔpH = 0.4) conditions. (showing mean ± Standard Deviation) (Figure from: Repolho et al., 2017).

Macroalgae Responses to Ocean Acidification

The photosynthetic strategy used by macroalgae vary significantly between species, for example the degree to which bicarbonate (HCO₃-) and/or CO₂ can be utilized for photosynthesis, resulting in different responses to OA by individual organisms²⁶. Many species have shown increased or maintained growth rates under elevated CO₂ compared with ambient conditions^1,6,26, while others have not²⁷. Differing experimental conditions may have been the cause of such disagreement. Rautenberger et al (2015²⁷), who focused on the impacts of OA alongside light levels, concluded that U.rigida is insensitive to OA,  resulting in an overall neutral effect on growth and photosynthesis. The reduced use of carbon concentrating mechanisms (CCMs) due to elevated pCO₂ results in greater use of CO₂ for carbon instead of HCO₃-, which is less energetically costly^6,28, allowing more energy to be allocated to growth⁸. Whereas at ambient pCO₂ concentrations macroalgae must rely on a combination of CO₂, HCO₃– and CCMs. The down-regulation of CCMs is not exclusive to macroalgae, both seagrasses and phytoplankton also possess the ability to do this. However, there is likely to be a differential success of this process among different species, resulting in the potential for the alteration of species composition in the future⁶.

In contrast, OA is mostly unfavourable for calcifying macroalgae ^28-30. Various species have shown decreased relative growth rates and inorganic content under elevated CO₂ compared to ambient CO₂ conditions (Figure 4a-c)^28-30. Although, OA has potentially inconsistent effects on photosynthetic parameters, with photosynthetic efficiency and maximum photosynthetic rate being negatively affected by decreasing pH for some species^29,30 while having no effect on others²⁸. Potential decreases in photosynthesis, which may appear an unexpected result, is likely due to decreased physiological health caused by reduced calcification³⁰.

Figure 4: Growth responses of three calcified macro algae to different ocean acidification scenarios. (A) The relative growth rates of C. officinalis under three pH treatments after 28 days (%FW day⁻¹). The corresponding pCO₂ to the pH values shown are 384, 1,313 and 1,939 µmol kg SW ^-1. Error bars show ±SE from the mean value (Data from: Hoffman et al., 2012²⁹). (B) Relative growth rates of A.corymbosa exposed to one of four pH treatments, two with static pH conditions and two with fluctuating pH for a period of 40 days (Figure from: Cornwall et al., 2012²⁸). (C) Change in average individual mass of Corallina sessilis over 30 days under two ambient CO₂ conditions (L-CO₂ – 380ppmv- pH 8.4) and two elevated CO₂ (H-CO₂– 1000ppmv, pH 7.9) (Figure from: Gao and Zheng, 2010³⁰).

The future for photosynthetic marine organisms

To conclude, there is a spectrum of responses, from stimulative through to inhibitory, displayed by photosynthetic organisms when tested under experimental conditions of OA. A variety of factors appear to be responsible for this, including the role of multiple stressors in modifying organisms’ responses. To improve our understanding of the potential consequences of OA, studies should be conducted over longer time scales to differentiate between shock responses and organisms that are capable of acclimatising to changing conditions. Chronic exposure to elevated pCO₂ could result in complex responses and potential adaptation not observed within these studies. 

Similarly, it seems of equal importance to test organisms under realistic future scenarios, such that all experimental conditions consider not only the reduced pH but also the inherent increase in temperatures, which has been seen in many of the reviewed publications. These factors must be considered to truly understand the potential synergistic effects of OA alongside other anthropogenic factors. Photosynthetic marine organisms play a crucial role in both primary productivity and ecosystem stability and therefore their survival has wider implications for marine life. For this reason, there should be more integrated research efforts focusing on the effects of OA on photosynthetic organisms and ecosystems as a unit.

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