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John Beardall ,

Monash University, Clayton, Australia

Living in a high CO2 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 CO2 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 CO2 and ocean acidification (1000 p.p.m., pH ~7.7 by 2100)

•Increased temperatures (average 4-5 oC 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 111-117 Pg /yr global primary productivity

(modified from Behrenfeld et al. 2001; Falkowski &Raven 1997)

Environment Annual ProductionPg C yr–1 (% total)

BiomassPg (% total)

TurnoverYr –1

Marine (mostly due to open ocean – coastal only ~25%)

54–59 (46–50 )

1.0–2.0 (0.1–0.3)

27–59

Terrestrial 57–58 (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 CO2 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

CO2CO2

CO2 CO2CO2

respiration

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 CO2 per se

2. Elevated CO2 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 CO2 with surface ocean equilibrated with the atmosphere. Total alkalinity 2324 mmol kg-1, temperature 18oC.

Modified from Royal Society Policy Document 12/05

COCO22 (g) (g) CO CO22 (aq) (aq) HCO HCO33- - COCO33

2-2-

  Pre-industrial Present day 3✕pre-

industrial

4✕pre- industrial

Atmospheric CO2

(ppm)

280 380 840 1120

Dissolved CO2

(mol/kg)

9 13 28 38

HCO3- (mol/kg) 1768 1867 2070 2123

CO32– (mol/kg) 225 185 103 81

Total dissolved inorganic carbon (mol/kg)

2003 2065 2201 2242

Average surface pH 8.18 8.07 7.77 7.65

Calcite saturation 5.3 4.4 2.4 1.9

Aragonite saturation 3.4 2.8 1.6 1.2

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 CO2 concentration on photosynthesis

and metabolism

Photosynthesis of phytoplankton species differs with respect to CO2 sensitivity: While most species (here Skeletonema costatum and Phaeocystis globosa) are at or close to CO2 saturation at present day CO2 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 CO2. From Riebesell 2004 J. Oceanogr. 60: 719-729

Most phytoplankton species are ~ C-saturated for photosynthesis under present day CO2 levels

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Other phytoplankton 6 2 4

Winners?

Seagrasses (though higher temperatures may inhibit growth)

Coccolithophores – but calcification may be inhibited

Some cyanobacteria (e.g.Trichodesmium)

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Modified from Doney at al Annu. Rev. Mar. Sci. 2009. 1:169–92

Species with highly efficient inorganic carbon use might show little

stimulation of growth under elevated CO2 but species lacking , or with

lower, CO2 acquisition activity could show enhanced growth

Changes to composition of algal populations

The reverse was true at low CO2

In phytoplankton of the Equatorial Pacific, exposure to high CO2 (750 ppm) favoured diatoms at the expense of

the haptophyte Phaeocystis sp.

(Tortell et al. 2002 MEPS 236: 37-42)

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150 ppm 750 ppm

CO2

Na

no

fla

ge

llate

:dia

tom

ra

tio

From Feng et al 2009

Increased CO2 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 CO2 bring about changes in cellular composition as well as in

photosynthetic rate and growth rates

Elevated CO2 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 % CO2 1.24 ± 0.05 4.14 ± 0.04 1.20 ± 0.06 3.61 ± 0.09

0.1% CO2 2.25 ± 0.05 4.98 ± 0.08 2.04 ± 0.06 4.67 ± 0.06

(Jenkins & Beardall, unpublished)

0123456789

C:N Chaetoceros C:N Dunaliella

C:N

rat

io

0.03%

0.10% 32 %28 %

Jenkins and Beardall (unpublished)

This causes the elemental ratio of algae to alter

2 1

In Trichodesmium increased CO2 stimulates N2 fixation, but in Nodularia N2 fixation rates decrease

Modified from Doney at al Annu. Rev. Mar. Sci. 2009. 1:169–92

Thus elevated CO2 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.

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CO2 for growth (M)

% T

ota

l F

A

%14:0

%18:1

%22:6

Growth of Emiliania huxleyi at elevated CO2 leads to a decrease in polyunsaturated FA and an increase in shorter

chain, more saturated, FAs

Changing composition of algae under elevated CO2 has a ‘flow-on’ effect to higher

trophic levels

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From Urabe et al (2003) Global Change Biology 9: 818-825

Elevated CO2 for growth of feed algae

(Scenedesmus) affects growth of Daphnia

http://www.nostoc.pt/ensaios2.htm

http://www.nies.go.jp/biology/mcc/strainlist_s.htm

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 CO2 could also affect sinking and thus the export of carbon

From Arrigo (2007)

Elevated CO2 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 CO2 per se, a “high CO2

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 growth6 7 108 9

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: 281-300

Predicted pH and distribution of CPredicted pH and distribution of C ii between its various between its various

forms in seawater under present-day COforms in seawater under present-day CO22 (350 ppm, 35 (350 ppm, 35

Pa) and at an atmospheric COPa) and at an atmospheric CO22 level of 1000 ppm (100 level of 1000 ppm (100

Pa) . Units for DIC components are Pa) . Units for DIC components are MM

pHpH HCO HCO33-- CO CO22 CO CO33

2-2- Total DIC Total DIC

Present dayPresent day

35 Pa CO35 Pa CO2 2 1515ooCC

21002100

100 Pa CO100 Pa CO2 2 1515ooCC

8.11 1981 13.5 202 8.11 1981 13.5 202 2197 2197

7.71 2250 38.6 91 7.71 2250 38.6 91 2380 2380

i.e. elevated COi.e. elevated CO22 leads to decreased [CO leads to decreased [CO332-2-] and hence ] and hence

decreased calcificationdecreased 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

spK

COCaarag

]][[ 23

2

where K'sp is the stoichiometric solubility product of the aragonite form of CaCO3

Since Ca2+ is essentially constant in seawater, aragonite formation is determined by [CO3

2-]

It is thus strongly affected by pH which in turn is dependent on the partial pressure of CO2 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 CO2

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

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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 www.nhm.ac.uk

Calcification by Gephyrocapsa

oceanica () and Emiliania huxleyi

()

was significantly decreased by elevated CO2 .

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, 978-980 31 August 2006) (photo J. CUBILLOS)

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Calc

ite c

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nt

(pg p

er

cell)

pCO2 (µatm)

Coccolithus pelagicusCoccolithus pelagicus

BUT !BUT !

From Doney at al Annu. Rev. Mar. Sci. 2009. 1:169–92

As for other processes, the effects of elevated CO2 on calcification vary greatly

Courtesy Ove Hoegh-Guldberg ©Centre for Marine StudiesUniversity 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 CO2.

© 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 CO2 – high POC but with less calcification → less export of

POC and PIC

After a diagram of U. Riebesell

CaCO3 is the mineral most important to POC flux

Decreased calcification leads to less drawdown of CO2 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

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P

Si

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P

Si

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Si

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SiSi

N P

SiN

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NP

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SiN

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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: 45-60.

Temporal changes in chl a concentration at 1 m in theBay of Calvi from 1979 - 1998.

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• 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;102:8927-8932

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

Time (minutes)

0 20 40 60 80 100 120 140

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TO

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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 4xCO2

(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 1979-1986 and 1997-2002, 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 CO2 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 CO2 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 CO2 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