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LETTERS

Decreased abundance of crustos

e

coralline algae due to ocean acidification

ILSA B. KUFFNER1*, ANDREAS J. ANDERSSON2,3*, PAUL L. JOKIEL4, KU‘ULEI S. RODGERS

4

AND FRED T. MACKENZIE

2

1US Geological Survey, Florida Integrated Science Center, St Petersburg, Florida 33701, USA
2University of Hawaii, Department of Oceanography, 1000 Pope Road, Honolulu, Hawaii 96822, USA
3Bermuda Institute of Ocean Sciences, 17 Biological Lane, St George’s, GE01, Bermud

a

4Hawaii Institute of Marine Biology, PO Box 1346, Kaneohe, Hawaii 96744, USA
*e-mail: ikuffner@usgs.gov; andreas.andersson@bios.edu

Published online: 23 December 2007; doi:10.1038/ngeo10

0

Owing to anthropogenic emissions, atmospheric concentrations
of carbon dioxide could almost double between 2006 an

d

2100 according to business-as-usual carbon dioxide emission
scenarios1. Because the ocean absorbs carbon dioxide from
the atmosphere2–4, increasing atmospheric carbon dioxide
concentrations will lead to increasing dissolved inorgani

c

carbon and carbon dioxide in surface ocean waters, and hence
acidification and lower carbonate saturation states2,5. As a
consequence, it has been suggested that marine calcifyin

g

organisms, for example corals, coralline algae, molluscs and
foraminifera, will have difficulties producing their skeletons and
shells at current rates6,7, with potentially severe implications
for marine ecosystems, including coral reefs6,8–11. Here we
report a seven-week experiment exploring the effects of ocean
acidification on crustose coralline algae, a cosmopolitan group
of calcifying algae that is ecologically important in most shallow-
water habitats12–14. Six outdoor mesocosms were continuously
supplied with sea water from the adjacent reef and manipulated
to simulate conditions of either ambient or elevated seawater
carbon dioxide concentrations. The recruitment rate and growt

h

of crustose coralline algae were severely inhibited in the elevated
carbon dioxide mesocosms. Our findings suggest that ocean
acidification due to human activities could cause significant
change to benthic community structure in shallow-warm-water
carbonate ecosystems.

Crustose coralline algae (CCA) are a major calcifying
component of the marine benthos from tropical to polar oceans
at all depths within the photic zone in almost every habitat
type13–15. CCA carry out key ecological roles on coral reefs, such
as acting as framework organisms, cementing carbonate fragments
into massive reef structures16, providing chemical settlement cues
for reef-building coral larvae17,18 and as major producers o

f

carbonate sediments12. So far, the main focus of global climate
change research on coral reefs has been the impact of rising
temperatures on coral ‘bleaching’ and mortality, but lately the
effects of ocean acidification have received increased attention7,8.
Experimental work has demonstrated that corals calcify more
slowly under conditions of elevated partial pressure of carbon
dioxide (pCO2) and lower calcium carbonate saturation state

6,19,
and studies have shown similar results for select species of calcifying
macroalgae cultured in small incubation vessels20,21. The purpose of

our flow-through outdoor mesocosm experiment was to provide
empirical quantification of changes to benthic communities that
may result from the decrease in calcium carbonate saturation
state predicted for tropical and subtropical oceans over the next
centuries. Our approach was novel in that the experiment was
conducted in an outdoor flow-through system, enabling organisms
with pelagic larvae to settle in the mesocosms and develop
communities as natural recruitment occurred over several months.
The mesocosms were designed to experience natural diurnal cycles
in solar radiation, temperature and seawater chemistry typically
occurring on tropical reef flats. Although previous work examined
the effects of calcium carbonate saturation state on calcification
rates of corals and coral communities in realistic mesocosm
studies9,10,19,22, none has examined how community structure may
change under increasing degree of ocean acidification.

Our mesocosms showed marked diurnal cycles in seawater
chemistry (Fig. 1) similar to those observed on other tropical
reef flats (for example 1 0.6 pH units23). The encrusting algal
community that recruited to acrylic cylinders placed in the
treatment mesocosms was quite different from that found on
cylinders from control mesocosms (Fig. 2). The recruitment rate
and the percentage cover of CCA on cylinders in treatment
mesocosms at the end of the 51 d period were significantly
lower than those in controls (Fig. 2a–c, Table 1). Mean percentage
cover by non-calcifying algae (a mixed assemblage of macroalgal
germlings, diatoms and small filamentous algae) was statistically
higher on cylinders from treatment compared with control
mesocosms (Fig. 2d, Table 1). Under high pCO2 conditions, CCA
recruitment rate and percentage cover decreased by 78% and 92%,
respectively, whereas non-calcifying algae increased by 52% (Fig. 2

)

relative to controls. Decreased rates of space occupation by CCA
imply inhibition of growth and/or calcification, indicating that at
least one step in the calcification process is being directly affected;
however, the cellular and molecular mechanisms of calcification in
these organisms remain elusive6,24.

At tropical and subtropical seawater conditions, CCA and many
important reef calcifiers such as echinoderms, other calcifying algae
and benthic foraminifera deposit Mg calcite minerals that contain
significant mol% MgCO3. CCA in the present study contained
13.6 ± 0.4 mol% as determined from X-ray diffraction (XRD)
analysis (see the Supplementary Information), and there was no

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mailto:ikuffner@usgs.gov

mailto:andreas.andersson@bios.edu

http://www.nature.com/doifinder/10.1038/ngeo100

© 2008 Nature Publishing Group
LETTERS

Feb-01 Feb-15 Mar-0

1

Date

Date
Date

Time

Time
Time
Time

TA
(µ

m
ol

k
g

–1
)

Date

Mar-15

Feb-01 Feb-15 Mar-01 Mar-15

Feb-01 Feb-15 Mar-01 Mar-15
Feb-01 Feb-15 Mar-01 Mar-15
0
0
1
2

3

4

500

1,000

1,500

2,000

0
500
1,000
1,500
2,000

p
C

O
2

(µ
at

m
)

p
C
O
2
(µ
at
m
)

Sa
tu

ra
tio

n
st

at
e

13
.6

m
ol

%
M

g
ca

lc
ite

0
1
2
3
4
Sa
tu
ra
tio
n
st
at
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13
.6
m
ol
%
M
g
ca
lc
ite

7.6

7.8

8.0

8.2

pH
N

B
S

7.6
7.8
8.0
8.2
pH
N
B
S

1,900

2,000

2,100

2,200

TA
(µ
m
ol
k
g
–1
)
1,900
2,000
2,100
2,200

12:00 20:00 04:00 12:00

12:00 20:00 04:00 12:00
12:00 20:00 04:00 12:00
12:00 20:00 04:00 12:00
a

b

c
d
e
f
g
h

Figure 1 Seawater carbonate chemistry. Data observed at midday (a–d) and during a diurnal cycle (e–h) in control (circles) and treatment (squares) mesocosms.
a,e, Partial pressure of CO2 (pCO2); black dots are surface seawater values reported by the CRIMP/CO2-NOAA PMEL buoy. b,f, Saturation state (Ω) with respect to
13.6 mol% Mg calcite. c,g, pHNBS. d,h, Total alkalinity (TA). Data are means ±1 s.d. (n = 3 mesocosms). Dashed lines are values projected for the year 2100 (IPCC, IS92a).
See Supplementary Information for tabulated data.

significant difference between treatment and control samples. Our
results contrast with those of refs 20 and 25, which reported
that the Mg content of the calcifying alga Porolithon gardineri
varied positively with seawater calcite saturation state, temperature
and growth rate. The mechanisms controlling the concentration
of Mg ions in the mineral structure of biogenic calcites are
not well understood and probably exert different influences on
different organisms26. Large variability in the Mg content among
different taxa living in the same environment suggests that
there is strong taxonomic control12. Geographically, there is a
convincing correlation between Mg content within taxonomic
groups and environmental parameters such as temperature and
seawater carbonate saturation state. This correlation has been

attributed to growth rate, which is a function of temperature
and carbonate saturation state26. Control of Mg content in
marine calcifiers warrants further investigation, as the amount
of Mg incorporated in the mineral matrix directly affects its
solubility. Biogenic Mg calcite phases containing a significant
mol% MgCO3 (>8–12 mol%) are more soluble than aragonite,
the carbonate phase deposited by corals, and could initially be
more susceptible to rising pCO2 and decreasing seawater calcium
carbonate saturation state27,28. Nevertheless, the changes in seawater
chemistry anticipated during the 21st century under the business-
as-usual CO2 emission scenario are sufficiently large to affect
significantly both aragonite and Mg calcite precipitation rates and
the organisms depositing these minerals.

nature geoscience VOL 1 FEBRUARY 2008 www.nature.com/naturegeoscience 115

© 2008 Nature Publishing Group
LETTERS

C1 C2 C3 T1 T2 T3 C1 C2 C3 T1 T2 T3

C1 C2 C3
N

on
-c

al
ci

fy
in

g
al

ga
e

(%
c

ov
er

)
T1 T2 T3

0

40

80

1

20

1

60

0
0
20
40
60
80

10

20

30

40
C

C
A

(r
ec

ru
its

m
–2

d
–1

)

C
C

A
(%

c
ov

er
)

a b

dc

Figure 2 Encrusting algal communities on experimental cylinders. Recruitment rate (a) and percentage cover (b) of CCA on cylinder surfaces from control (white bars)
and treatment (black bars) mesocosms. c, Photograph of example cylinders from a control (left) and a treatment (right) mesocosm. d, Percentage cover of non-calcifying
algae on cylinder surfaces from control (white bars) and treatment (black bars) mesocosms. Data are means ±1 s.d. (n = 3 cylinders). C = control and T = treatment, and
the number refers to the replicate mesocosm. See Supplementary Information for tabulated data.

Table 1 Mean seawater carbonate chemistry near midday (n = 11 sample days), rate of CCA recruitment and percentage cover by CCA and non-calcifying algae found on
experimental cylinders in control and treatment mesocosms, and accompanying statistical tests.

Control Treatment One-way analysis of variance A priori contrast
n = 3 (ANOVA) by mesocosm between treatment

Mean (± 1 s.d.) and control mesocosms

F P t P

pCO2 (µatm)∗ 400 (47) 765 (39) 49.2 <0.0001 8.35 <0.0001 Saturation state 2.74 (0.21) 1.55 (0.06) 53.8 <0.0001 8.10 <0.0001

(13.6 mol% Mg calcite)∗
pHNBS∗ 8.17 (0.04) 7.91 (0.02) 53.7 <0.0001 8.52 <0.0001 Total alkalinity (µmol kg−1) 2,156 (2.1) 2,016 (9.2) 45.7 <0.0001 4.29 = 0.0001 CCA (recruits m−2 d−1)† 104 (26.1) 23.3 (3.5) 28.2 <0.0001 11.7 <0.0001 CCA (% cover)† 18.1 (7.5) 1.51 (0.8) 21.4 <0.0001 10.1 <0.0001 Non-calcifying algae (% cover) 27.7 (16.0) 57.5 (14.8) 10.9 = 0.0004 5.84 <0.0001 ∗Rank transformation applied to data to meet assumptions of ANOVA. †Square-root transformation applied to data to meet assumptions of ANOVA.

The lower percentage cover by CCA and higher mean
percentage cover by non-calcifying algae in the treatment
mesocosms compared with controls indicate that CCA may be less
competitive for space in a high-pCO2 world, possibly accelerating
the shift from dominance by calcifying organisms to fleshy
algae observed on many reefs today29. However, the effects of
ocean acidification on coverage by fleshy algae will depend on
complexities that we did not address in our experiment. Although
our study did show an increase in coverage by non-calcifying algae
on cylinders in the treatment mesocosms, we did not attempt to

replicate the natural compliment of herbivores found on Hawaiian
reef flats, and thus only microherbivores (for example sea hares
and amphipods) were in abundance. The variance in percentage
cover by non-calcifying algae found on our cylinders was high
within treatment (Fig. 2d), indicating that there were undoubtedly
factors other than carbonate saturation state and competition
with calcifying algae controlling this variable. Further, at the end
of our nine-month study, we did not see any patterns in total
(entire mesocosm) fleshy algal abundance or biomass related to
treatment, whereas we did see the same inhibition of CCA as on

116 nature geoscience VOL 1 FEBRUARY 2008 www.nature.com/naturegeoscience

© 2008 Nature Publishing Group
LETTERS

the cylinders (P.L.J. et al., manuscript in preparation). It will be
necessary to investigate the effects of ocean acidification on the
ecological process of herbivory and nutrient availability, two factors
important in controlling abundance of fleshy algae29, to understand
fully the consequences of decreased coverage by CCA for benthic
community structure. However, the projected decreased ability of
CCA to recruit and claim space in an ecosystem where competition
for hard substratum is keen implies that more substrata will be
available for colonization by other benthic organisms.

Under all proposed scenarios1, continuous anthropogenic
emissions of CO2 to the atmosphere will result in a continuous
decline in the pH and calcium carbonate saturation state of ocean
waters, with all the ecological implications of such a change in
a major Earth-surface-system carbon reservoir. The only way to
slow or prevent the continuing acidification of surface ocean waters
is to reduce the emissions of CO2 from human activities to the
atmosphere; however, because of the slow mixing rate of the
oceans, they will continue to be a major sink of anthropogenic
CO2 emissions well into the future, and ocean acidification will
continue to intensify. Our study demonstrates that changes in
benthic community structure on coral reefs may occur owing
to the impact of ocean acidification on ecological processes
such as recruitment and competition for space. Extrapolation of
experiments measuring decreases in calcification rates by various
organisms to predict future reef accretion rates may underestimate
the impacts of ocean acidification by failing to account for
the replacement of calcifying organisms by those that do not
produce calcium carbonate. Predicting changes in community
structure resulting from ocean acidification and other stressors
(for example high-temperature anomalies) will be important in
modelling future rates of carbonate production by coral reefs and
associated ecosystems.

METHODS

Six 1×1×0.5-m fibreglass mesocosm tanks were continuously supplied with
flowing sea water pumped from 2 m depth at the edge of the coral reef at
Moku O Loe (Coconut Island), Kaneohe Bay, Hawaii (21.4◦ N, 157.8◦ W), at
a rate of eight litres per min per mesocosm (complete turnover rate ≈ 1 h).
Three mesocosms were randomly chosen by role of dice to be maintained at an
ambient (control, mean midday±s.d. = 400±47µatm pCO2) chemical state,
and the remaining three were maintained at a daytime pCO2 level exceeding
control conditions by 365µatm on average. The latter level at midday is near
that expected by the end of the 21st century following the business-as-usual
IS92a CO2 emission scenario assuming equilibrium between the atmosphere
and surface sea water (765±39µatm, Fig. 1a). Note that the pCO2 of Kaneohe
Bay and many other coral reef environments, on average, is greater than
the overlying atmosphere30. Furthermore, on diurnal timescales, the surface
seawater pCO2 may fluctuate significantly owing to changes in reef metabolism
between day and night23. Carbonate chemistry was altered with hydrochloric
acid diluted with tap water to a 10% solution added at 1.3 ml min−1 by a
peristaltic pump to the inflow pipes of each treatment mesocosm (control
mesocosms received tap water at the same rate). The amount of tap water added
to the inflowing water represents a 0.016% addition and was not enough to
affect salinity in the mesocosms. Treatments were initiated in the mesocosms
on 31 October 2005. Temperature, salinity, dissolved oxygen and pH were
measured and water samples were taken in all six mesocosms at least once per
week around midday (10 a.m.–2 p.m. HST). Water samples were analysed for
dissolved inorganic carbon and total alkalinity following standard procedures
(see the Supplementary Information). Diurnal sampling (every 3 h for 24 h) was
conducted on several occasions in order to quantify the daily natural variability
in the mesocosms (for example Fig. 1e–h). Between 2 February and 24 March
2006, clear acrylic cylinders were added to the mesocosms (three replicates per
mesocosm) in order to provide symmetrical substrata that could be removed
and examined for encrusting community recruitment and development.
The resulting communities were quantified by taking six non-overlapping

still photographs of cylinder surfaces and tabulating the presence/absence of
crustose coralline and non-calcifying algae under randomly distributed points
on the image using PhotoGrid (C. Bird, University of Hawaii) software (n = 50
points per image).

Received 25 July 2007; accepted 19 November 2007; published 23 December 2007.

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Acknowledgements
Support for I.B.K.’s efforts on the project was provided by the USGS Terrestrial, Freshwater and
Marine Ecosystems program and the USGS Coastal and Marine Geology Program. A.J.A. and F.T.M.
were funded by NSF. The contributions of P.L.J. and K.S.R. were supported by the USGS, EPA
Star and the NOAA National Ocean Service. We thank R. Solomon, E. DeCarlo, C. Sabine and R.
Feely for permission to include the CRIMP/CO2-NOAA PMEL buoy pCO2 data in Fig. 1. Any use
of trade names herein was only for descriptive purposes and does not imply endorsement by the
US Government.
Correspondence and requests for materials should be addressed to I.B.K. or A.J.A.
Supplementary Information accompanies this paper on www.nature.com/naturegeoscience.

Author contributions
I.B.K., A.J.A., P.L.J. and F.T.M. contributed equally to the design and I.B.K., A.J.A. and K.S.R.
contributed equally to carrying out the experiments. All authors contributed to data synthesis and
writing of the manuscript.

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• Decreased abundance of crustose coralline algae due to ocean acidification

Main
Methods
Acknowledgements
References