0 John Beardall, Monash University, Clayton, Australia Living in a high CO 2 world: Biological responses to ocean acidification

We are living in a time that is seeing changes in the global environment that are occurring at a rate unsurpassed in geological history

Atmospheric CO 2 levels are increasing rapidly, causing a range of problems associated with global warming and, for the oceans, acidification

Despite the Montreal protocol starting to take effect, ozone depletion is still not showing signs of significant decline. Consequently organisms in the upper layers of the oceans will still be exposed to elevated UVB, especially in the Southern Ocean, but also at lower latitudes.

Global change will impact upon oceanic primary producers by: Elevated CO 2 and ocean acidification (1000 p.p.m., pH ~7.7 by 2100) Increased temperatures (average 4-5 o C increase by 2100) Continuing ozone depletion and elevated UVB

Our planet is dominated by water

Algae in marine systems are responsible for ~ 50% of the Pg /yr global primary productivity (modified from Behrenfeld et al. 2001; Falkowski &Raven 1997) EnvironmentAnnual Production Pg C yr –1 (% total) Biomass Pg (% total) Turnover Yr –1 Marine (mostly due to open ocean – coastal only ~25%) 54–59 (46–50 ) 1.0–2.0 (0.1–0.3) 27–59 Terrestrial57–58 (50–54)600–1000 (60–99.8) 0.06–0.10 The oceans have played a role as a major sink for ~50% of the anthropogenic CO 2 emissions since the Industrial Revolution (3.8 Pg/yr: 1.8 Pg/yr as photosynthesis, 2 Pg/yr as abiotic absorbtion)

Grazing and excretion Export production – organic carbon and carbonates as marine snow CO 2 respiration Recycling of C and other nutrients via the microbial foodweb Carbon assimilated by phytoplankton can suffer a number of fates. A high proportion is recycled via the microbial foodweb in surface waters but some is exported to deep water Phytoplankton play a key role in global C cycling

GLOBAL CHANGE IMPACTS ON PHYTOPLANKTON PRODUCTIVITY IN A NUMBER OF WAYS 1.Changes in photosynthesis and growth associated with elevated CO 2 per se 2.Elevated CO 2 may cause alterations of macromolecular composition, impacting on sinking, flow to higher trophic levels and nutrient cycling 3.Changes in calcification associated with acidification 4.Increased temperature driven stratification leading to enhanced nutrient limitation and alterations to export production 5.Effects of increased UVB radiation, especially in polar regions – enhanced by nutrient limitation

Changes in surface ocean chemistry as a result of increasing atmospheric CO 2 with surface ocean equilibrated with the atmosphere. Total alkalinity 2324 mmol kg -1, temperature 18 o C. Modified from Royal Society Policy Document 12/05 CO 2 (g)  CO 2 (aq)  HCO 3 -  CO 3 2- Pre-industrialPresent day3 ✕ pre- industrial 4 ✕ pre- industrial Atmospheric CO 2 (ppm) Dissolved CO 2 (mol/kg) HCO 3 - (mol/kg) CO 3 2– (mol/kg) Total dissolved inorganic carbon (mol/kg) Average surface pH Calcite saturation Aragonite saturation

Adapted from Feely (2008) in Levinson and Lawrimore (eds), Bull. Am. Meteorol. Soc, 89(7): S58. We can see these changes in our oceans

Direct impacts of increased CO 2 concentration on photosynthesis and metabolism

Photosynthesis of phytoplankton species differs with respect to CO 2 sensitivity: While most species (here Skeletonema costatum and Phaeocystis globosa) are at or close to CO 2 saturation at present day CO 2 levels (8– 20 μmol L –1 ), coccolithophores such as Emiliania huxleyi have comparatively low affinities for inorganic carbon and appear to be carbon-limited in today’s ocean. This raises the possibility that coccolithophores may benefit directly from the present increase in atmospheric CO 2. From Riebesell 2004 J. Oceanogr. 60: Most phytoplankton species are ~ C-saturated for photosynthesis under present day CO 2 levels

5 Other phytoplankton6 2 4 Winners? Seagrasses (though higher temperatures may inhibit growth) Coccolithophores – but calcification may be inhibited Some cyanobacteria (e.g.Trichodesmium) 1 Modified from Doney at al Annu. Rev. Mar. Sci :169–92

Species with highly efficient inorganic carbon use might show little stimulation of growth under elevated CO 2 but species lacking, or with lower, CO 2 acquisition activity could show enhanced growth Changes to composition of algal populations

The reverse was true at low CO 2 In phytoplankton of the Equatorial Pacific, exposure to high CO 2 (750 ppm) favoured diatoms at the expense of the haptophyte Phaeocystis sp. (Tortell et al MEPS 236: 37-42)

From Feng et al 2009 Increased CO 2 alone had little effect on productivity of North Atlantic phytoplankton in bottle experiments but some changes in phytoplankton composition were evident under different treatments Greenhouse conditions led to increased organic matter production but less particulate inorganic C formation

Increases in CO 2 bring about changes in cellular composition as well as in photosynthetic rate and growth rates

Elevated CO 2 will result in changes in uptake of other elements besides carbon Maximum Rate of uptake (fmol. cell -1. min -1 ) C. muelleri D. tertiolecta P N P N 0.03 % CO ± ± ± ± % CO ± ± ± ± 0.06 (Jenkins & Beardall, unpublished)

32 % 28 % Jenkins and Beardall (unpublished) This causes the elemental ratio of algae to alter

2 1 In Trichodesmium increased CO 2 stimulates N 2 fixation, but in Nodularia N 2 fixation rates decrease Modified from Doney at al Annu. Rev. Mar. Sci :169–92 Thus elevated CO 2 will lead to changes in C:N:P in phytoplankton

Redrawn from data in Riebesell et al (2000) Geochimica et Cosmochimica Acta, Vol. 64, No. 24, pp. 4179–4192. Growth of Emiliania huxleyi at elevated CO 2 leads to a decrease in polyunsaturated FA and an increase in shorter chain, more saturated, FAs

Changing composition of algae under elevated CO 2 has a ‘flow-on’ effect to higher trophic levels 0

From Urabe et al (2003) Global Change Biology 9: Elevated CO 2 for growth of feed algae (Scenedesmus) affects growth of Daphnia

Phytoplankton such as Emiliania huxleyi produce extracellular polysaccharide known as transparent exopolymer particles (TEP) TEP are known to promote cell aggregation and could thus promote sinking of cells as marine snow. Elevated CO 2 could also affect sinking and thus the export of carbon

From Arrigo (2007) Elevated CO 2 induces formation of more transparent exopolymer particles (TEP). These cause aggregation of cells and enhance sinking of organic matter

In addition to changes associated with elevated CO 2 per se, a “high CO 2 environment” will lead to a lower pH of seawater from 8.1 at present to ~pH 7.7 by 2100

From Doney 2006 Oceanic pH already varies slightly across the oceans – more acidic areas correspond mostly with zones of upwelling of deeper water

pH for maximum growth Phytoplankton can grow over a wide range of pH values, but some have clear preferences for pH values close to present day (dashed green line) and would not grow at pH values expected by 2100 (dashed red line). Others may cope well under lower pH conditions. Hinga 2002 MEPS 238:

Predicted pH and distribution of C i between its various forms in seawater under present-day CO 2 (350 ppm, 35 Pa) and at an atmospheric CO 2 level of 1000 ppm (100 Pa). Units for DIC components are  M pH HCO 3 - CO 2 CO 3 2- Total DIC Present day 35 Pa CO 2 15 o C Pa CO 2 15 o C i.e. elevated CO 2 leads to decreased [CO 3 2- ] and hence decreased calcification

Calcification is based on the formation of calcium carbonate in the form of the minerals aragonite or calcite The saturation of seawater with respect to aragonite is given by where K'sp is the stoichiometric solubility product of the aragonite form of CaCO 3 Since Ca 2+ is essentially constant in seawater, aragonite formation is determined by [CO 3 2- ] It is thus strongly affected by pH which in turn is dependent on the partial pressure of CO 2 in solution

Aragonite saturation of surface waters: note the dark blue regions in polar waters that are now only just above saturation but which will become under- saturated by the end of the century (purple) threatening species that build calcareous shells from aragonite. Under such conditions it is more difficult to make aragonite, and existing aragonite will dissolve. From Doney 2006 Bt the end of the century, many surface waters will be undersaturated for aragonite

Elevated CO 2 Decreased oceanic pH (ocean acidification) Decreased carbonate availability for calcification Diminished calcification and growth of calcifying organisms

Some microalgae e.g. coccolithophids show calcification - these are also likely to be affected by decreasing pH 0

0 Blooms of coccolithophores such as Emiliania huxleyi form huge blooms in oceans The calcium carbonate scales (coccoliths) can settle out and represent a major sink of carbon to the deep ocean

Calcification by Gephyrocapsa oceanica (  ) and Emiliania huxleyi (  ) was significantly decreased by elevated CO 2. From Riebesell et al (2000) Nature 407: 364–367.

Lost protection: making sea water more acidic (centre and right) dissolves the outer casings of coccolithophores (Source: Nature 442, August 2006) ( photo J. CUBILLOS )

Calcite content (pg per cell) pCO 2 (µatm) Coccolithus pelagicus BUT !

From Doney at al Annu. Rev. Mar. Sci :169–92 As for other processes, the effects of elevated CO 2 on calcification vary greatly

Courtesy Ove Hoegh-Guldberg © Centre for Marine Studies University of Queensland

Ocean acidification will impact on coral and coralline algal bleaching, productivity and calcification (Anthony et al, 2008)

Photo Credits: AWI (left); Ross Hopcroft, NOAA (right)] Limacina helicina, the dominant pteropod in polar waters The effects of ocean acidification will extend to grazers of Southern Ocean phytoplankton such as pteropods

Scanning electron microscope images of the shells of two pteropods. Left: a pteropod after swimming in present day seawater, which is not corrosive. Right: a pteropod after swimming for 48 hours in seawater made corrosive by the absorption of CO 2. © Victoria Fabry - California State University San Marcos

POC reaching the deep sea does so associated with mineral “ballast“. Decreasing pH may also affect the charge on POC, making the particles less likely to bind to minerals and reducing the sinking velocity of aggregates (Passow) Present day – high POC, high calcification → more ballast effect and export of POC and PIC Elevated CO 2 – high POC but with less calcification → less export of POC and PIC After a diagram of U. Riebesell CaCO 3 is the mineral most important to POC flux Decreased calcification leads to less drawdown of CO 2 into calcium carbonate but also decreases the ballast effect which could decrease the sinking of particulate organic carbon to deep waters ( Klaas and Archer 2002 )

Impacts of temperature on stratification of the oceans could lead to nutrient limitation and decreased productivity

Heating of surface water causes a density difference between upper and lower layers, preventing exchange of nutrients from deep water, so populations cannot fully develop In the absence of stratification, nutrient rich water can be supplied from the depths Phytoplankton activity in surface waters depletes the levels of nutrients needed to sustain growth N P Si N P N P N P N P N P NP N N N N N N N N P P P P N N N P P P P N N N P P N N P P N N P N N N N P N N N N P N N N

47 e.g. The data of Goffart et al (2002) show changes in the extent and composition of the winter-spring phytoplankton bloom in the Bay of Calvi in the NW Mediterranean Sea. The decrease in chl a was associated with increased stratification resulting from increased surface temperature. This decreases the supply of nutrients from the deeper waters, and hence limits phytoplankton growth. The decrease in phytoplankton was accompanied by a switch from diatom dominated populations to nanoflagellates, though in later years even these organisms were limited by N availability

From Goffart et al (2002) MEPS 236: Temporal changes in chl a concentration at 1 m in the Bay of Calvi from

Lower nutrient levels favour smaller celled organisms such as Prochlorococcus or, among the eukaryotes, coccolithophorids such as Emiliania huxleyi. In turn this may lead to lowered export production as smaller cells sink less readily than large cells

Mean area of the diatom frustule as a function of the tropical oceanic temperature gradient Finkel Z. V. et.al. PNAS 2005;102: Copyright © 2005, The National Academy of Sciences Temperature gradient between surface and deep water as a function of geological time (Falkowski & Oliver 2007 Nature Reviews Microbiology 5: 813-8)

These effects may be exacerbated by the combined effect of nutrient limitation on the UVB sensitivity of algae. increased stability of the surface mixed layer enhanced nutrient depletion Increased heating increased sensitivity to UVB damage

e.g. N-limitation increases sensitivity to UVB Data for D. tertiolecta from K. Shelly N sufficient N-limited No UV

The modelling data of Bopp et al (2005) suggest that enhanced stratification and nutrient limitation will lead to: decreased primary production by 15% decreased export ratio (export production divided by the primary production) by as much as 25% at 4xCO 2 (from 10 Pg C/yr to 7.5 Pg C/yr) Gregg et al. (2003) suggested, using satellite data, that global oceanic primary productivity had decreased by 6% between the and , though nearly 70% of this decline was in the high latitudes The big picture (see Boyd talk)

However : 1) In coastal areas the increased thermal contrast between marine and terrestrial environments will lead to enhanced upwelling of nutrient rich waters in coastal systems which will favour larger species such as diatoms 2) The effects of elevated CO 2 on TEP production has not been taken into account and this might mitigate to some extent the decrease in export production.

Summary However, there may be shifts in species composition and macromolecular composition of phytoplankton populations which may have flow-on effects to higher trophic levels Elevated CO 2 leads to decreased calcification in some (but not all) coccolithophorids and will inhibit growth and calcification in corals, coralline algae and some grazing animals Changes in CO 2 are unlikely to have major direct impacts on phytoplankton production Temperature rises will lead to dominance of smaller celled phytoplankton species and a major impact on export production and ocean productivity. UV impacts exacerbated by nutrient limitation

For phytoplankton at least the picture is hazy – we have only examined a few species, with differing results This is possibly due to different methodologies and /or strains Most studies have only been carried out for a relatively short time. Can cells/populations acclimate/adapt over time?

Work on algae and climate change in John Beardall’s laboratory is funded by the Australian Research Council