Journal of Experimental Marine Biology and Ecology
302 (2004) 249 – 260
www.elsevier.com/locate/jembe
Sea surface temperature and the growth of the West
Atlantic reef-building coral Montastraea annularis
Juan P. Carricart-Ganivet
El Colegio de la Frontera Sur, Unidad Chetumal, Apdo Postal 424, Chetumal, Q. Roo 77000, Mexico
Received 1 April 2003; received in revised form 20 October 2003; accepted 22 October 2003
Abstract
Relationships were analyzed between sea surface temperature (SST) and annual growth
characteristics (density, extension rate and calcification rate) of the Caribbean reef-building coral
Montastraea annularis. Colonies were collected from 12 localities in the Gulf of Mexico and the
Caribbean Sea. Two well-separated relationships were found, one for the Gulf of Mexico and the
other for the Caribbean Sea. Calcification rate and skeletal density increased with increasing SST in
both regions, while extension rate tended to decrease. Calcification rate increased f 0.57 g cm 2
year 1 for each 1 jC increase in SST. Zero calcification was projected to occur at 23.7 jC in corals
from the Gulf of Mexico and at 25.5 jC in corals from the Caribbean Sea. The 24 jC annual average
SST isotherm marks the northern limit of distribution of M. annularis. Montastraea annularis
populations of the Gulf of Mexico are isolated from those of the Caribbean Sea, and results indicate
that corals from the Gulf of Mexico are adapted to growth at lower minimum and average annual
SST. Corals from both the Gulf of Mexico and the Caribbean Sea, growing at lower SSTs and having
lower calcification rates, extend their skeletons the same or more than those growing at higher SSTs.
They achieve this by putting more of their calcification resources into extension and less into
thickening, i.e., by sacrificing density.
D 2003 Elsevier B.V. All rights reserved.
Keywords: Density; Extension rate; Calcification rate; Stretching; Gulf of Mexico; Caribbean; proxy
environmental records
1. Introduction
Recovery of information about coral growth and coral growth histories, and reconstruction of proxy environmental records, was recognized as potential applications when
E-mail address: [email protected] (J.P. Carricart-Ganivet).
0022-0981/$ - see front matter D 2003 Elsevier B.V. All rights reserved.
doi:10.1016/j.jembe.2003.10.015
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annual density banding was first described in massive coral skeletons (Knutson et al.,
1972). Growth data that can be recovered from such bands are skeletal density, annual
extension rate and annual calcification rate. Annual calcification rate is the product of
annual average density and annual extension rate (g cm 3 cm year 1 = g cm 2
year 1). Dodge and Brass (1984) suggested that examination of all 3 variables is
necessary to have sufficient understanding to link coral growth with environmental
conditions. A considerable amount of research has been aimed at recovering environmental information from annual density banding patterns in skeletons of the massive coral
Porites. This has included worked aimed at understanding the way skeletons grow (e.g.,
Barnes and Lough, 1993; Taylor et al., 1993) and record information (e.g., Taylor et al.,
1995; Barnes et al., 1995; Barnes and Lough, 1996), and at which environmental variables
control growth processes (Lough and Barnes, 1997; Barnes and Lough, 1999; Lough and
Barnes, 2000).
Montastraea annularis is distributed throughout the Caribbean Sea and Gulf of Mexico
(Fig. 1) and belongs to a complex of three sibling species: M. annularis, M. faveolata and
M. franksi (Knowlton et al., 1992; Weil and Knowlton, 1994). The growth characteristics
of these three species have been used to assess local and global environmental change
(e.g., Druffel, 1982; Dodge and Lang, 1983), but no research has been carried out to
determine if Montastraea has the same growth strategy as massive Porites. Porites invests
Fig. 1. Distribution of M. annularis and location of study sites. The dashed line in the upper right corner is the 24
jC annual mean SST isotherm and marks the northern distribution limit of this species (see text for details).
J.P. Carricart-Ganivet / J. Exp. Mar. Biol. Ecol. 302 (2004) 249–260
251
increased calcification in extension, and that colonies with the least dense skeletons tend to
have the greatest calcification rate (Lough and Barnes, 1992; Scoffin et al., 1992). In most
reports of growth characteristics of M. annularis, M. faveolata and M. franksi, analyses of
relationships between annual extension, annual density and annual calcification have only
been done on the local scale. One study, Carricart-Ganivet and Merino (2001), considered
these relationships at the regional-scale. They analyzed density, extension rate and
calcification rate of M. annularis growing at reefs along a qualitative gradient of
continental influence in the southern Gulf of Mexico and found that corals inhabiting in
environments with high sedimentation rates, low light availability and anthropogenic
influence (see Cruz-Piñón et al., 2003) sacrifice skeletal density while maintaining or
increasing skeletal extension, despite having a lower calcification rate. This response was
named the ‘‘stretching modulation of skeletal growth’’ and was observed later by Cook et
al. (2002) for M. faveolata growing in the Florida Keys. Here, the data of CarricartGanivet and Merino (2001) are reanalyzed along with published growth data for M.
annularis from the Caribbean Sea. Calcification rate and the stretching response are
analyzed with respect to temperature gradients, which differ between the Gulf of Mexico
and the Caribbean Sea.
2. Materials
2.1. Growth variables
Average values of annual density, annual extension rate and annual calcification rate
for M. annularis were obtained from previously published reports for 12 localities in the
Gulf of Mexico and in the Caribbean Sea. These reports were Dodge and Brass (1984) for
St. Croix, US Virgin Islands, Carricart-Ganivet et al. (2000) for the Mexican Caribbean
and Carricart-Ganivet and Merino (2001) for the southwestern Gulf of Mexico. The
number of corals collected at each reef and the time period over which growth measurements were taken differ between localities. All corals were collected between 2 and 10 m
depth (Fig. 1, Table 1). Dodge and Brass (1984) collected Montastraea at eight reefs at St.
Croix, US Virgin Islands. At that time all corals of the Montastraea complex were
attributed to M. annularis and not separated into three sibling species. The description
they provided for their specimens shows that only specimens of M. annularis (sensu
Knowlton et al., 1992) were collected at Christiansted Harbor Fore-Reef, Airport BackReef and Hess Reef.
In all corals, skeletal extension rate was measured from X-radiographs as the width of
annual density bands (Knutson et al., 1972). Density measurements in corals from the Gulf
of Mexico were made using the freezing method (Carricart-Ganivet et al., 2000), who
reported a precision better than 1% for this method. This method takes advantage of coral
porosity and is based in weight change after water invasion and freezing of skeletal
fragments. In corals from the Caribbean Sea, density was measured in corals from the
Mexican Caribbean using the freezing method and by photodensitometry of X-radiographs
of corals collected in St. Croix, US Virgin Islands by Dodge and Brass (1984), who
estimated a possible systematic error for this technique of F 5%. In all corals, calcification
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Table 1
Average SST, maximum SST, minimum SST, number of specimens, period of time covered, density, extension
rate and calcification rate of M. annularis growing between 2 and 10 m depth in 12 localities of the Gulf of
Mexico and the Caribbean Sea (see Fig. 1 for geographical locations)
Locality
Gulf of Mexico
Cayo Arcas3
Triángulo
Oeste3
Alacrán3
Cayo Arenas3
Anegada de
Adentro3
Isla Verde3
Average
S.D.
Coefficient
of variation
Caribbean Sea
Mahahual4
Xahuayxol2
Puerto Morelos2
Christiansted
Harbor1
Airport BackReef1
Hess1
Average
S.D.
Coefficient
of variation
Average Maximum Minimum No. of Timeline
annual
SST (jC) SST (jC) corals
SST (jC)
Skeletal Skeletal
Calcification
density
extension rate
(g cm 3) rate
(g cm 2 yr 1)
1
(cm yr )
26.7
26.6
29.4
29.4
23.5
23.4
2
3
1968 – 1990
1982 – 1990
1.75
1.77
0.85
0.85
1.48
1.53
26.6
26.5
26.3
29.4
29.6
29.1
23.6
23.3
22.8
3
2
6
1977 – 1990
1980 – 1990
1972 – 1991
1.94
1.73
1.47
0.79
0.86
0.89
1.52
1.48
1.31
26.1
26.5
0.21
28.7
29.3
0.34
23.1
23.3
0.27
4
1977 – 1991
1.36
1.67
0.22
13%
0.92
0.86
0.04
5%
1.25
1.43
0.12
8%
28.2
28.1
27.9
27.6
29.7
29.5
29.4
29.0
26.5
26.6
25.8
26.1
11
7
5
7
1976 – 1997
1981 – 1995
1980 – 1994
1970 – 1979
2.09
1.69
1.79
1.26
0.78
0.91
0.82
0.99
1.63
1.53
1.46
1.24
27.6
29.0
26.1
8
1970 – 1979
1.28
1.00
1.29
27.6
27.8
0.29
29.0
29.3
0.44
26.1
26.2
0.28
8
1970 – 1979
1.30
1.60
0.32
20%
0.86
0.89
0.08
9%
1.12
1.40
0.19
13%
Reference for growth data: (1) Dodge and Brass (1984), (2) Carricart-Ganivet et al. (2000), (3) Carricart-Ganivet
and Merino (2001), (4) Carricart-Ganivet (unpublished data).
rate was calculated by multiplying de density value of each annual band by its
corresponding skeletal extension.
2.2. Sea surface temperature data
Annual mean sea surface temperatures (SST), mean annual maximum sea surface
temperatures (maximum SST) and mean annual minimum sea surface temperatures
(minimum SST) were obtained from the Comprehensive Ocean Atmosphere Data Set
(COADS) (http://iridl.ldeo.columbia.edu./SOURCES/.COADS/). Temperature data were
for 2j latitude-by-longitude squares associated with each reef and covered the 25-year
period from 1967 to 1992. No data were available from COADS for Isla Verde, Anegada
de Adentro and Mahahual Reefs (Fig. 1, Table 1). SSTs for Isla Verde Reef were obtained
J.P. Carricart-Ganivet / J. Exp. Mar. Biol. Ecol. 302 (2004) 249–260
253
from the Comisión Nacional del Agua (1998) data set, who make temperature measurements f 1.5 km from this reef, and SSTs for Anegada de Adentro and Mahahual Reefs
were obtained from the GOSTAPlus data set (Version GIST 2.2) produced by the United
Kingdom Meteorological Office in collaboration with the Massachusetts Institute of
Fig. 2. The three growth variables in M. annularis as a function of average annual SST in the Gulf of Mexico
(black circles) and in the Caribbean Sea (empty circles). IV = Isla Verde, AN = Anegada de Adentro, CR = Cayo
Arenas, CA = Cayo Arcas, AA = Alacrán, TO = Triángulo Oeste, CHF = Christiansted Harbor, A = Airport BackReef, H = Hess, PM = Puerto Morelos, XH = Xahuayxol, MH = Mahahual.
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J.P. Carricart-Ganivet / J. Exp. Mar. Biol. Ecol. 302 (2004) 249–260
Technology and the Physical Oceanography Distributed Archive Center (see Bottomley
et al., 1990).
3. Results
3.1. Growth variables and sea surface temperature
There were no significant differences in density, extension rate and calcification rate
between corals from the Gulf of Mexico and corals from the Caribbean Sea (t-test for
independent samples, p>0.05, in all cases; Table 1). Average and minimum SSTs were
significantly higher in the Caribbean Sea (t-test for independent samples, p < 0.0001, in
both cases), while maximum SST was not significantly different (t-test for independent
samples, p>0.05). The responses of the three growth variables to changes in SST were
similar between the Gulf of Mexico and the Caribbean Sea but occurred over lower
temperatures in the Gulf of Mexico (Fig. 2).
Calcification rate and density increased significantly with increasing SST in both the
Gulf of Mexico and the Caribbean Sea (Fig. 2). Extension rate tended to decrease but the
decrease was significant only amongst corals collected from the Gulf of Mexico (Fig. 2).
Calcification rate in the Gulf of Mexico increased 0.55 g cm 2 year 1 for each 1 jC
increase, while, in the Caribbean Sea, it increased 0.58 g cm 2 year 1 for each 1 jC
increase. The slopes were not significantly different ( F-test, p>0.05) although the
intercepts were significantly different ( F-test, p < 0.0005). The intercepts indicated
calcification would cease in corals from the Gulf of Mexico at 23.7 and at 25.5 jC in
corals from the Caribbean Sea.
3.2. Relationships between growth variables
Average annual calcification rate was inversely related to average annual extension
rate in both the Gulf of Mexico and the Caribbean Sea, although the relationship was
not significant amongst corals collected from the Caribbean Sea (Table 2, Fig. 3).
Average annual density was inversely related to average annual extension rate in corals
from both regions, although the relationship was not significant amongst corals collected
from the Caribbean Sea (Table 2, Fig. 3). Average annual calcification rate was
significantly related to average annual density in corals from both regions (Table 2,
Fig. 3). These relationships were maintained when data for corals from both regions
Table 2
Correlation coefficients between density, extension rate and calcification rate of M. annularis for the Gulf of
Mexico and the Caribbean Sea (asterisks indicate significant correlations, p < 0.05). N = 6 in both regions
Relationship
Density vs. extension rate
Density vs. calcification rate
Extension rate vs. calcification rate
Gulf of Mexico
0.97*
0.96*
0.85*
Caribbean Sea
0.78
0.91*
0.45
Combined data
0.83*
0.92*
0.57
J.P. Carricart-Ganivet / J. Exp. Mar. Biol. Ecol. 302 (2004) 249–260
255
Fig. 3. Relationships between the three growth variables in M. annularis. In the Gulf of Mexico (left) and in the
Caribbean Sea (right). Acronyms as in Fig. 2.
were pooled (Table 2). Thus, variations in calcification rate mostly resulted in variations
in skeletal density.
4. Discussion
Calcification rate in M. annularis increased with annual average SST in both the Gulf
of Mexico and the Caribbean Sea (Fig. 2). This is in accord with Lough and Barnes’
(2000) observations on massive Porites from the Indo-Pacific. Calcification rate in M.
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annularis was about twice as sensitive to temperature changes as calcification rate in
massive Porites (f 0.57 vs. f 0.3 g cm 2 year 1 for each 1 jC). Based upon regression
of calcification rate against SST, calcification in M. annularis is likely to cease as SST
declines towards 23.7 jC in the Gulf of Mexico and towards 25.5 jC in the Caribbean Sea.
I pooled the calcification rate data used here from the Caribbean Sea with those of
M. annularis and M. faveolata, growing up to 10 m depth in Carrie Bow Cay, Belize,
reported by Graus and Macintyre (1982), those of Dodge and Brass (1982) from all the
reefs they studied at St. Croix, US Virgin Islands, and those of M. faveolata, growing up to
10 m depth in Curacß ao, Netherlands Antilles, reported by Bosscher (1993), to obtain a
relationship of f 0.5 g cm 2 year 1 for each 1 jC (Fig. 4). More importantly,
calcification for the combined data was projected to cease at 24.3 jC. The 24.0 jC
annual average isotherm marks the northern boundary for M. annularis and M. faveolata
(Fig. 1). Thus, it seems probable that calcification rate limits the distribution of these
species to the north. In Bermuda (f 32jN), which has an annual average SST of 22.9 jC,
only Montastraea franksi, the third sibling species of the complex, is found (E. Weil,
personal communication). The southern distribution limit of M. annularis, M. faveolata
and M. franksi is at f 9jN (Fig. 1), whilst the 24.0 jC isotherm is at f 24jS. Hence,
there may be other environmental controls that are limiting their distribution to the south.
Milliman (1973) stated that reef development in the western south Atlantic is limited by
the high rates of sedimentation in the areas off the Orinoco and Amazon rivers.
The two well-separated relationships between calcification rate and SST (Fig. 2)
indicate that M. annularis populations in the Gulf of Mexico are adapted to grow in
lower average and minimum SST than populations in the Caribbean Sea (Table 1). These
populations are probably genetically isolated. Jordán-Dahlgren (2002), observed poor
larval connectivity between gorgonian communities of the Mexican Caribbean and the
Gulf of Mexico due, mainly, to oceanographic conditions and upwelling in the northern
zone of the Yucatán peninsula (see also Merino 1997).
The increase in density and decrease in extension rate with increasing SST observed
here (Fig. 2) contrast with the findings of Lough and Barnes (2000) for massive Porites in
Fig. 4. Calcification rate in M. annularis and M. faveolata as a function of average annual SST in the Caribbean Sea.
J.P. Carricart-Ganivet / J. Exp. Mar. Biol. Ecol. 302 (2004) 249–260
257
the Indo-Pacific. Porites invests increased calcification in extension (Lough and Barnes,
1992; Scoffin et al., 1992)—a strategy that allows Porites to occupy space as rapidly as it
can. Montastraea annularis uses its increased calcification resources to construct denser
skeletons. This response was called ‘‘stretching modulation of skeletal growth’’ by
Carricart-Ganivet and Merino (2001). They linked this response with a gradient in
continental influence. It now seems more likely that the stretching modulation mechanism
is related to SST. It may be that this mechanism allows M. annularis to be competitive for
space in colder waters, but further studies are needed to test this assumption.
Density was more variable than extension rate and calcification rate in corals from SST
gradients in both the Gulf of Mexico and Caribbean Sea (Table 1). In contrast, Lough and
Barnes (2000) reported that density was the least variable growth parameter along a SST
gradient in massive Porites. The negative relationship between calcification rate and
extension rate in M. annularis growing along SST gradients reported here (Fig. 3, Table 2)
apparently contrasts with published results for this species growing within a single reef
(Dodge and Brass, 1984; Carricart-Ganivet et al., 2000; Carricart-Ganivet and Merino,
2001). However, in results reported here, density in M. annularis is also the most
conservative growth variable within a single reef (e.g., Mahahual Reef; Table 3). It seems
possible that the effects of environmental variables, other than SST, become apparent
when variations in SST are small, as at a single site.
There was no significant relationship between the three growth variables studied here
and minimum SST ( p>0.05, in all cases), although all were altered by changes in
maximum SST (Fig. 5). Thus, M. annularis adapts its growth to maximum SST, in
contrast with massive Porites. In massive Porites, extension rate and calcification rate
were linked with minimum SST and not with maximum SST (Lough and Barnes, 2000).
The findings presented here indicate that the growth model for massive Porites (Lough
and Barnes, 1993; Taylor et al., 1993) may not be appropriate for M. annularis. Studies to
Table 3
Average density, extension rate and calcification rate of 11 colonies of M. annularis growing between 2 and 10 m
depth in Mahahual, Mexican Caribbean (see Fig. 1 for geographical location)
Coral
Skeletal
density
(g cm 3)
Skeletal
extension rate
(cm year 1)
Calcification rate
(g cm 2 year 1)
MH2
MH5
MH7
MH8
MH9
MH10
MH11
MH12
MH13
MH14
MH15
Average
S.D.
Coefficient of variation
2.07
2.09
2.11
2.14
2.16
2.23
2.11
2.13
1.94
1.95
2.05
2.09
0.09
4%
0.71
0.91
0.72
0.88
0.70
0.68
0.79
0.77
0.84
0.78
0.84
0.78
0.08
10%
1.48
1.91
1.51
1.88
1.51
1.52
1.65
1.63
1.63
1.51
1.72
1.63
0.15
9%
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J.P. Carricart-Ganivet / J. Exp. Mar. Biol. Ecol. 302 (2004) 249–260
Fig. 5. The three growth variables as a function of maximum SST in M. annularis growing in the Gulf of Mexico
and the Caribbean Sea.
understand how M. annularis grows and the environmental and biological controls on
growth are needed for better recovery and reconstruction of the records held within its
skeleton. Finally, Lough and Barnes (2000) concluded that calcification rate in massive
Porites would, at least initially, increase as a result of global warming. This suggestion was
based on evidence that the calcification rate of massive Porites, on the Great Barrier Reef,
J.P. Carricart-Ganivet / J. Exp. Mar. Biol. Ecol. 302 (2004) 249–260
259
has increased in association with the observed SST increase in the last century. The
evidence presented here indicates that M. annularis can adapt its growth responses to
different SST conditions. The important, unanswered question is whether corals can adapt
to increasing SSTs, or whether their response is genetically fixed. If the latter, then it seems
probable that corals will not have enough time to respond to global warming and
populations could collapse or migrate to higher latitudes.
5. Conclusions
Calcification rate of M. annularis is correlated to mean sea surface temperature.
Calcification rate of M. annularis increases by f 0.57 g cm 2 year 1 for each 1.0 jC
increase in SST.
Montastraea annularis populations in the Gulf of Mexico and the Caribbean Sea are
subject to different temperature regimes and have adapted accordingly.
The effect of lower temperatures upon calcification rate is one of the factors that limit
the distribution of M. annularis to the north.
Relationships amongst density, annual extension and annual calcification rate and the
stretching response in M. annularis are linked with lower maximum SST.
Studies to understand growth in M. annularis skeletons and the environmental and
biological controls on growth processes are needed to obtain better proxy environmental information from their skeletons.
Acknowledgements
This study was finished during my postdoctoral period with Dave Barnes at the
Australian Institute of Marine Science, with a scholarship of CONACyT (ref. 020156).
Special thanks to Dave Barnes, Janice Lough and Ray Taylor for arguing with me about
the stretching concept. The manuscript was notably improved by the comments of Dave
Barnes, Janice Lough and two anonymous reviewers. Glenn De’ath helped with some
statistical analysis. [RW]
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