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We thank M. Benbakkar, J. L. Devidal, A. Fabbrizio, G. Garbarino,
P. Parisiadis, V. Svitlyk, and F. van Wyk de Vries for their
help and three anonymous reviewers for fruitful comments.
The MORB starting material was kindly provided by P. Schiano.
This work is supported by Institut National des Sciences de
l’Univers, l’European Synchrotron Radiation Facility, and the project
Oxydeep of the Agence Nationale de la Recherche. This is
Laboratory of Excellence ClerVolc contribution no. 99. All
experimental data are presented in the supplementary materials.
Materials and Methods
Figs. S1 to S9
Tables S1 and S2
6 January 2014; accepted 3 April 2014
CORALS AND CLIMATE
Mechanisms of reef coral resistance
to future climate change
Stephen R. Palumbi,* Daniel J. Barshis,† Nikki Traylor-Knowles, Rachael A. Bay
Reef corals are highly sensitive to heat, yet populations resistant to climate change have
recently been identified. To determine the mechanisms of temperature tolerance, we
reciprocally transplanted corals between reef sites experiencing distinct temperature
regimes and tested subsequent physiological and gene expression profiles. Local
acclimatization and fixed effects, such as adaptation, contributed about equally to
heat tolerance and are reflected in patterns of gene expression. In less than 2 years,
acclimatization achieves the same heat tolerance that we would expect from strong natural
selection over many generations for these long-lived organisms. Our results show both
short-term acclimatory and longer-term adaptive acquisition of climate resistance. Adding
these adaptive abilities to ecosystem models is likely to slow predictions of demise for
coral reef ecosystems.
Reef-building corals have experienced global declines resulting from bleaching events parked by pulses of warm-water exposure (1–4). However, corals in naturally warm environments can have high resistance to
bleaching temperatures and can survive heat
exposure that would bleach conspecifics in cooler
microclimates (5, 6). Similarly, recent discovery of
populations of acidification-resistant corals show
that physiological or evolutionary mechanisms of
environmental accommodation exist (7, 8). Such
populations are ideal test sites for research into the
mechanisms of coral response to climate change.
Corals in adjacent backreef pools in the U.S.
National Park of American Samoa on Ofu Island
experience strong differences in temperature
(9, 10). In the highly variable (HV) pool, temperatures often exceed the local critical bleaching
temperature of 30°C, reaching 35°C during
strong noontime low tides (6). By contrast, the
moderately bariable (MV) pool rarely experiences
temperatures above 32°C. Corals in the HV Pool
have higher growth rates (9, 10), higher survivorship, and higher symbiont photosynthetic efficiency during experimental heat stress than
conspecifics from the MV pool (6). These pools
provide a powerful system to test the speed and
extent of coral acclimatization and adaptation to
warm-water conditions in the context of future
To test corals in their native habitats for phy-
siological resistance to heat stress, we collected
branches of the tabletop coral Acropora hyacinthus
[cryptic species E (11)] and exposed them to
experimental bleaching conditions. A. hyacinthus
is a cosmopolitan species that constitutes a large
percentage of hard coral cover on Pacific reefs and
shows high levels of bleaching and mortality
during large-scale bleaching events (4). We chose
A. hyacinthus for this study because it is a
dominant reef-builder and is especially sensitive
to environmental stress, making its relative ability
to acclimate or adapt extremely important to the
future of coral reef ecosystems as climate change
proceeds. We subjected branches of corals to a
prescribed ramp in water temperature of 29° to
34°C for 3 hours, followed by an incubation for
3 hours at 34°C. These conditions mimic the
natural increase in temperature observed in the
HV pool during a tidal cycle. Experiments on
fragments of tagged and monitored colonies
showed that individuals native to the HV pool
exhibit higher resistance to thermal stress, mea-
sured by retention of chlorophyll derived from
photosynthetic symbionts, than corals from the
MV pool (Fig. 1). The average retention of chlo-
rophyll a after experimental heat stress was 80%
in HV pool corals (Fig. 1C) but only 45% in MV
pool corals (Fig. 1A, t test, P < 0.00001) compared
To test for acclimatization, we transplanted
coral colonies of A. hyacinthus reciprocally from
their native locations in the HV and MV pools to
three transplant sites within each pool. We transplanted 6 colonies from the HV pool and 12 from
the MV pool. After 12, 19, and 27 months, we tested
transplanted colonies for thermal resistance. For
11 separate colonies, 22 of 23 paired bleaching
Department of Biology, Stanford University, Hopkins Marine
Station, Pacific Grove, CA 93950, USA.
*Corresponding author. E-mail: firstname.lastname@example.org †Present
address: Department of Biological Sciences, Old Dominion University,
Norfolk, VA 23529, USA.
Fig. 1. Chlorophyll retention in coral colonies exposed to experimental heat stress compared with
nonstressed controls. Upper panels show results from corals native to the moderately variable (MV)
pool (A) and from corals moved into the MV pool (B). The lower panels are from corals native to the
highly variable (HV) pool (C) and from corals moved into the HV pool (D). The smoothed curve reflects
the distribution in (A) and is included in other panels for reference.