Coral skeletal extension rate: An environmental signal or a subject to inaccuracies?

Author's personal copy Journal of Experimental Marine Biology and Ecology 405 (2011) 73–79

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Journal of Experimental Marine Biology and Ecology j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / j e m b e

Coral skeletal extension rate: An environmental signal or a subject to inaccuracies? Juan P. Carricart-Ganivet ⁎ Unidad Académica de Sistemas Arrecifales, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Apartado Postal 1152, Cancún, Q. Roo. 77500, México El Colegio de la Frontera Sur, Unidad Chetumal, Av. Centenario km 5.5, Apdo. Postal 424, Chetumal, Q. Roo. 77000, México

a r t i c l e

i n f o

a b s t r a c t

Article history: Received 28 April 2011 Accepted 19 May 2011 Available online 12 June 2011

Coral skeletal extension rate has been widely used to assess coral growth characteristics across environmental gradients and as an environmental proxy. Herein, the potential sources of errors when measuring skeletal extension rates are identified and discussed, and it is demonstrated that measurements of this growth parameter do not necessarily reflect an annual time scale and can result in substantial miscalculations. Instead, it is dissepiment spacing and number that best reflect the time scale. On the other hand, calcification rate is the growth parameter that appears to better reflect the environmental controls that regulate physiological processes in symbiotic corals. Nonetheless, any error associated with measuring extension rate would result in under- and overestimation of calcification rate values, which could lead to huge errors if this growth parameter is used as an environmental proxy. The aim is to promote further discussion, avoid future misuse of extension rate as an environmental proxy, and encourage future research about how to accurately measure extension rate and the use of calcification rate as an environmental proxy. © 2011 Elsevier B.V. All rights reserved.

Keywords: Coral bleaching Coral growth Density banding Environmental proxy Sclerochronology

1. Introduction An environmental proxy is any line of evidence that provides an indirect measure of climates or environments in space and time (Ingram et al., 1981; Lotter, 2003). The reconstruction of proxy environmental records was recognized as potential application when annual density banding was first described in the skeletons of massive reef-building corals (Knutson et al., 1972). These organisms contain a wealth of historical proxy climate and environmental information locked in their calcium carbonate skeletons (Lough, 2010), and such density banding provides historical information about mean annual skeletal density (bulk density; gCaCO3 cm− 3), annual extension rate (linear growth rate; cm year− 1) and annual calcification rate (calcium carbonate deposition rate; gCaCO3 cm− 2 year− 1). The annual calcification rate is the product of the annual extension rate and the average density of skeleton deposited in making that extension (Dodge and Brass, 1984): −2

gCaCO3 cm

−1

year

−1

= cm year

−3

× gCaCO3 cm

Coral skeletal growth and its variations are controlled by the available energy for the active deposition of the calcareous material (i.e., calcification rate) (Colombo-Pallotta et al., 2010; Fang et al.,

⁎ Corresponding author at: Unidad Académica de Sistemas Arrecifales, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Apartado Postal 1152, Cancún, Q. Roo. 77500, México. Tel.: + 52 998 8710219x184; fax: + 52 998 8710138. E-mail address: [email protected]. 0022-0981/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2011.05.020

1989) and by the way this material is used to construct the skeleton by the coral (Carricart-Ganivet and Merino, 2001). The latter process can lead to different growth strategies: investing calcification resources into either linear extension or into skeletal density (CarricartGanivet, 2004, 2007). Maximum calcification rates would be expected when environmental conditions are optimal for skeletal accretion of CaCO3; while, extension rate and density will vary depending on the skeletal architecture adopted by a particular coral species (CarricartGanivet, 2007). Estimates of calcification rate from coral density banding patterns require accurate measurements of skeletal density and extension rate. There are several ways to measure skeletal density: mercury displacement (Dustan, 1975), water displacement (Graus and Macintyre, 1982; Hughes, 1987), optical densitometry (Carricart-Ganivet and Barnes, 2007; Chalker et al., 1985; Dodge and Brass, 1984), gamma-densitometry (Chalker and Barnes, 1990), and computerized tomography (Bosscher, 1993). Annual extension rate, the most commonly reported parameter and the one most often used to assess coral growth characteristics across environmental gradients (e.g., Carilli et al., 2010; Hudson, 1981; Huston, 1985; Tomascik and Sander, 1985), is measured directly along the main axis of skeletal growth using the annual density-banding pattern seen in X-radiographs (e.g., Baker and Weber, 1975; Carricart-Ganivet and Merino, 2001; Hudson, 1981). This growth parameter can also be measured using a densitometry series (i.e., from successive density maxima or minima) generated by the densitometry techniques listed above, in conjunction with X-ray images (e.g., Carricart-Ganivet, et al. 2007; Dodge and Brass, 1984; Elizalde-Rendón, et al. 2010; Helmle et al., 2002). Annual extension rate has also been used as an environmental

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proxy (e.g., Dodge and Vaišnys, 1975). Recently, Saenger et al. (2009), using one specimen of Siderastrea siderea, presented an absolutely dated and annually resolved record of sea surface temperature from the Bahamas, based on a 440-year time series of coral growth rates, and Cantin et al. (2010), using one specimen of Diploastrea heliopora, predicted that if the ocean-warming trend continues, this coral could stop growing altogether by 2070. 2. Sea surface temperature, calcification rate, and density banding Fig. 1 shows monthly mean SSTs from January 1980 to December 2007 at Mahahual, in the Mexican Caribbean. The SST data were obtained from the Hadley Centre Sea Ice and SST (HadISST) data set produced by the United Kingdom Meteorological Office (see Rayner et al., 2003). This figure indicates that, during the 28-year time interval, the annual maximum monthly SSTs usually occurred in September but varied between June and October, and that the annual minimum monthly SSTs usually occurred in February but varied between December and March. Calcification is one of the most important processes occurring in coral reef systems. Reef-building corals produce large amounts of calcium carbonate substratum, which counters the physical erosion of the reef structure. Although there are several environmental variables that have effects on calcification rate, such as light (e.g., Barnes and Chalker, 1990) and reproduction (e.g., Mendes and Woodley, 2002), it is well known that temperature is a very important control of variations in coral calcification rate. Geographically, calcification rate increases as sea surface temperature (SST) increases (CarricartGanivet, 2004; Lough and Barnes, 2000), and short- and long-term experiments on corals adapted to a specific SST regime (i.e., living in a single reef) have shown that, as temperature increases, coral calcification increases until it reaches a maximum and thereafter declines (Clausen and Roth, 1975; Coles and Jokiel, 1978; Jokiel and Coles, 1977; Marshall and Clode, 2004). During the annual cycle, the calcification rate increases as temperature increases, until it reaches a maximum in midsummer, after which the calcification rate declines as SST decreases (see Carricart-Ganivet, 2007). However, since the month of the year in which the maximum monthly mean SST occurs could vary from year to year, maximum calcification rate could be reached on different months from year to year, assuming that the maximum calcification rate corresponds to the monthly mean SST maximum. In Montastraea, the major reef-building massive coral genus in the West Atlantic Ocean (Goreau, 1959; Knowlton et al., 1992), highdensity-band (HDB) formation is related to seasonally higher SSTs, while low-density-band (LDB) formation occurs during seasonally low SSTs (Carricart-Ganivet, 2007; Dodge and Brass, 1984). Dodge et al. (1992) and Dávalos-Dehullu et al. (2008) reported that annual

density variations during the annual cycle result from variations in the amount of thickening applied largely to the exothecal dissepiments (thin horizontal plates periodically laid down as the skeleton extends vertically), i.e., in the HDB exothecal dissepiments are thicker than in the LDB. Mendes and Woodley (2002) and Mendes (2004) found that extension rate in M. annularis was significantly lower in September than all months but October, these authors hypothesized that HDB formation is the result of resources being diverted from growth to reproduction. Dodge et al. (1992) and Dávalos-Dehullu et al. (2008) reported that the spacing between the exothecal dissepiments in Montastraea is invariant during the annual cycle and also between annual cycles. Dávalos-Dehullu et al. (2008) also reported that there is a rhythmical formation of dissepiments in M. annularis linked somehow to lunar cycles since this species forms ~3 exothecal dissepiments per year (i.e., a year has ~13 lunar cycles). The link between dissepiment formation and lunar cycles was also reported in M. faveolata by Winter and Sammarco (2010). The lack of variation in dissepiment spacing and the link between their formation and lunar cycles are evidence that the extension rate of this genus does not change over time as reported by Cruz-Piñón et al. (2003) for an annual cycle. Carricart-Ganivet (2004) reported that Montastraea uses its increased calcification resources to construct denser skeletons and Wórum et al. (2007) showed that SST influences on calcification rate are reflected as changes in the coral skeletal density-banding pattern in this genus. Therefore, density can be considered the primary control of calcification rate in Montastraea species (Carricart-Ganivet, 2007). Thus, a modeled density series against distance for M. annularis is illustrated for the period January 1980 to December 2007 in Fig. 2a. This density series was constructed using the monthly SST data set presented in Fig. 1, assuming that the highest SST values produce the highest density (i.e., as well as with calcification rate); density values were calculated for each month using the maximum density value for M. annularis reported for Mahahual (2.23 g cm − 3, Carricart-Ganivet, 2004), and the maximum SST value from January 1980 to December 2007 (30.59 °C): Density = ðSST × 2:23Þ = 30:59: The distance was calibrated using the mean exothecal dissepiment spacing (0.06 cm) reported by Dávalos-Dehullu et al. (2008) for M. annularis growing in Mahahual, and taking into account the number of full moons during each year. Measuring extension rate from successive density maxima in this density series, as usually done in this genus (e.g., Dodge and Brass 1984), can result in years containing less or more than 12 months (Fig. 2b). The idea that measurements of extension rate from successive density maxima (or minima) can result in years that are not of a true calendar duration is coincident with Buddemeier's “soft” year

Sea Surface Temperature (oC)

Month of the year that presented the maximum monthly mean SST:

31

Sep-80 Jun-82 Sep-84 Sep-86 Aug-88 Sep-90 Sep-92 Oct-94 Sep-96 Aug-98 Sep-00 Oct-02 Sep-04 Sep-06 Jul-81 Sep-83 Sep-85 Jul-87 Sep-89 Aug-91 Sep-93 Sep-95 Aug-97 Sep-99 Aug-01 Sep-03 Sep-05 Aug-07

29

27

25 Jan-80 Jan-82 Jan-84 Jan-86 Jan-88 Jan-90 Jan-92 Jan-94 Jan-96 Jan-98 Jan-00 Jan-02 Jan-04 Jan-06 Jan-08

Date Fig. 1. Monthly mean sea surface temperatures (SSTs) from January 1980 to December 2007 from Mahahual, Mexican Caribbean, and months of the year that present the maximum monthly mean SST for the same time period.

Author's personal copy J.P. Carricart-Ganivet / Journal of Experimental Marine Biology and Ecology 405 (2011) 73–79

Density (g cm-3)

term. Lough and Barnes (1990) wrote: “The density banding pattern in coral skeletons is unlikely to be a faithful record of time. R. W. Buddemeier, a pioneer in the field of coral density banding, describes the banding pattern as a record of “soft” years (pers. comm.). By this he means that equivalent points in different annual density patterns may not represent exactly the same time of year”. Carricart-Ganivet (2004) has reported a significantly positive correlation between density and calcification rate in M. annularis, and there are several reports that demonstrated that extension rate and calcification rate positively correlate in this genus (e.g., CarricartGanivet et al., 2000; Carricart-Ganivet and González-Diaz, 2009; Carricart-Ganivet and Merino, 2001; Dodge and Brass, 1984). CarricartGanivet's (2004) results are based on spatial gradients, where density was more variable than extension (see Table 1 on Carricart-Ganivet, 2004). Meanwhile, within a single reef, density is the most conservative variable in this genus (see Table 3 on Carricart-Ganivet, 2004). If when measuring extension rate from successive density maxima results in soft years (i.e., depending on the month of the year when density maxima is reached), then the resulted extension rate data have additional variability induced by the actual duration of the measurement. Hence, the positive correlations between extension rate and calcification rate observed in Montastraea within a single reef are caused by the soft years and arise from the way calcification rate is calculated (as the product of a high variable parameter and a conservative one). Since density resulted more variable than extension rate in the two environmental gradients studied by Carricart-Ganivet (2004) the error caused by the soft years was “filtered”, resulting in a positive correlation between density and calcification. In Fig. 3 a density series obtained using densitometry from digitized images of X-radiographs (Carricart-Ganivet and Barnes, 2007) of a 10 cm-high specimen of M. annularis collected in June 2004 at 1.5 m depth at the back reef of Mahahual is presented. Also shown are monthly mean SSTs from January 1994 to June 2004 from the

75

same locality (i.e., from the same data set presented in Fig. 1). The distance of the density series was contrasted with the distance calculated using the mean exothecal dissepiment spacing, taking into account the number of full moons each year, both distances resulted ~7.54 cm. There was a clear visual match between density maxima and SST maxima each year except for 1998, when a HDB was not formed (Fig. 3). At the beginning of 1998, the density tended to increase with increasing SST; however, it suddenly decreased reaching a minimum value that coincided with the SST maximum during August. Reef-building corals that experience thermal stress exhibit reduced calcification rates (Wórum et al., 2007). Also, during bleaching events, decrease and cessation in this growth parameter are reported for M. annularis (Goreau and MacFarlane, 1990; Mendes and Woodley, 2002; Porter et al. 1989). Moreover, Leder et al. (1991) demonstrated that a prolonged bleaching could result in the loss of an entire year's skeletal growth record (i.e., by suppression of dissepiment formation). Suppression of some dissepiments formation can also occur in years of cooler-than-average SST, as observed in M. faveolata by Winter and Sammarco (2010), who examined temperature data for their sampling location to determine whether there was any relationship between seawater temperature and number of dissepiments per year. During 1998 extensive bleaching events occurred along the Mesoamerican Reef System (Kramer and Kramer, 2000), and the lack of a HDB during 1998 can be explained assuming that this coral suffered thermal stress and bleaching during this year. If density maxima are formed at times of SST peaks, measuring extension rate from successive density maxima in the density series presented in Fig. 3 will result in a time duration that is not exactly a year, but rather the time duration between SST peaks. Consequently the extension rate calculated from the distance between such peaks needs to be adjusted to a true time value. An experienced analyst should note the growth hiatus for 1998 in the X-ray image (Fig. 3b), but the lack of a

a

Months with the theoretical highest density values at each year:

2.25

Sep-80 Jun-82 Sep-84 Sep-86 Aug-88 Sep-90 Sep-92 Oct-94 Sep-96 Aug-98 Sep-00 Oct-02 Sep-04 Sep-06 Jul-81 Sep-83 Sep-85 Jul-87 Sep-89 Aug-91 Sep-93 Sep-95 Aug-97 Sep-99 Aug-01 Sep-03 Sep-05 Aug-07

2.15

2.05

1.95 Number of full moons per year: 13

1.85

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Distance (cm)

b2

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Anomaly (months)

1

-1 -2 -3 -4

Year

Fig. 2. a) Modeled density series against distance from January 1980 to December 2007 and number of full moons per year from 1980 to 2007 (see text for details). b) Annual anomalies in months from 1980 to 2007 when the maximum density value occurs; note that this value occurs more frequently during September (17 times).

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Table 1 Mean extension rate, density and calcification rate from the modeled density-banding of Montastraea annularis presented in Fig. 2a, and percentage of under- and overestimations on calcification rate when comparing this growth parameter when extension rate is measured from density maxima with when measured from January to December each year (see text for details). Year

1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007

Measured extension rate from density maxima each year

Measured extension rate from January to December each year

Extension rate (cm year− 1)

Density (g cm− 3)

Calcification rate (g cm-2 year− 1)

Extension rate (cm year− 1)

Density (g cm− 3)

Calcification rate (g cm− 2 year− 1)

0.61 0.69 0.92 0.72 0.76 0.73 0.60 0.81 0.79 0.72 0.66 0.77 0.76 0.79 0.66 0.76 0.67 0.72 0.82 0.73 0.70 0.85 0.66 0.76 0.73 0.72 0.70

2.10 2.10 2.09 2.03 2.02 2.02 2.04 2.04 2.02 2.05 2.04 2.02 2.03 2.03 2.02 2.03 2.04 2.06 2.05 2.02 2.03 2.07 2.04 2.06 2.04 2.03 2.06

1.28 1.44 1.93 1.45 1.54 1.48 1.21 1.67 1.61 1.47 1.34 1.57 1.54 1.60 1.33 1.54 1.37 1.47 1.68 1.47 1.41 1.77 1.34 1.57 1.49 1.45 1.43

0.72 0.77 0.72 0.72 0.77 0.72 0.72 0.77 0.72 0.72 0.72 0.72 0.77 0.72 0.72 0.77 0.72 0.72 0.77 0.72 0.77 0.72 0.72 0.77 0.72 0.72 0.77

2.11 2.08 2.09 2.01 2.02 2.03 2.05 2.03 2.02 2.04 2.04 2.02 2.03 2.02 2.04 2.03 2.05 2.06 2.02 2.02 2.05 2.06 2.05 2.05 2.02 2.04 2.08

1.51 1.61 1.49 1.44 1.57 1.45 1.47 1.57 1.45 1.46 1.46 1.44 1.57 1.44 1.46 1.57 1.47 1.47 1.57 1.45 1.59 1.47 1.47 1.59 1.45 1.46 1.61

HDB in 1998 could result in erroneous or in loss of extension rate values for this and the next year in this specimen (i.e., a decision on how to measure – or not measure – 1998 and 1999 should be taken). This also highlights another factor that must be considered in developing growth histories: the use of multiple samples from the same reef environment. 3. Genera other than Montastraea Errors associated with skeletal extension measurements will depend on how density banding arises (i.e., in coral skeletal architecture and growth strategies, see Carricart-Ganivet, 2007). All species of Montastraea have plocoid corallites with individual dissepiments that seal the bottoms of the various, separate compartments formed between thecae and septa (Veron, 2000); in this genus HDB deposition is immediate (Carricart-Ganivet, 2007). In genera with a similar skeletal architecture such as Diploastrea and Diploria measurements of skeletal extension should present the same problems as illustrated using Montastraea. Meanwhile, in genera, such as Porites, with cerioid corallites and with sinapticulotheca that make the skeleton porous, and in which density banding arises from thickening of the skeleton through the depth of the tissue layer, (Barnes and Lough, 1993) the errors in the measurement of skeletal extension may arise in other ways. Massive Porites uses its increased calcification resources to grow faster during summer (Carricart-Ganivet, 2007) and the extension rate can be considered the primary control of calcification rate in this genus (Lough, 2008; Lough, 2011; Lough and Barnes, 2000). In Porites, density is more conservative than extension rate within a single reef (Scoffin et al., 1992) and in an environmental gradient (Lough and Barnes, 2000), and as observed in several works a positive correlation between extension rate and calcification rate would be expected in this genus (e.g., Carricart-Ganivet et al., 2007; Elizalde-Rendón et al., 2010; Lough and Barnes, 1992, 2000; Scoffin et al., 1992). Nonetheless, within massive Porites there are other causes of errors in measuring extension rate than those described above for

Under- and overestimation on calcification rate (%)

15 11 − 30 −1 2 −2 17 −6 − 11 −1 9 −9 2 − 11 9 2 7 0 −7 -2 11 − 20 9 1 −3 0 11

Montastraea. Although there are conflicting reports about the seasonal timing of HDB formation in massive Porites (see Barnes and Lough, 1996), HDBs have been mostly associated with summer in this genus growing in the Great Barrier Reef in Australia. However, the cerioid and porous structure of Porites skeletons allow coral tissue to penetrate and calcify above structures previously formed and, as a consequence, HDB deposition is not immediate. In this genus, there is an apparent timing of HDB formation that depends on the thickness of the tissue layer and extension rate, and errors in dating seasonal bands in Porites would be likely to average 3 months and could range from 1 to 8 months (Barnes and Lough, 1993). In addition, there is evidence that the thickness of the tissue layer varies from year to year in massive Porites (Barnes and Lough, 1992), thus the apparent timing of HDB formation may also vary from year to year (i.e., Buddemeier's “soft” year). Thus, the associated errors in dating seasonal bands in Porites and variations of tissue thickness from year to year should cause false annual extension rate values when measuring it from successive density minima, as usually done in this genus (e.g., Elizalde-Rendón et al., 2010; Lough and Barnes, 1992). Additionally, Lough (2008, 2011) suggested that assessing long-term trends in Porites skeletal growth requires caution, as there is evidence of an age effect, i.e., in earlier growth years corals will tend to extend less and form a higher density skeleton than in later years. Finally, it cannot be discarded that during bleaching or in years of cooler-than-average SST, suppression of dissepiment formation is also possible in Porites, causing errors when measuring extension rate. Lough (pers. comm.) has observed in massive Porites from the Great Barrier Reef in Australia that growth hiatus associated with coral bleaching years, e.g., 1998 and 2002, seem to be a higher density part of the skeleton, as if the coral has stopped extending but continued to calcify. 4. Calcification rate as an environmental proxy Coral calcification is a physiological process that requires energy to deliver calcium carbonate to the coral skeleton (Colombo-Pallotta et

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1.8 Aug-98

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00

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Fig. 3. a) Density series from a specimen of Montastraea annularis collected in Mahahual, Mexican Caribbean (continuous line), and monthly mean sea surface temperatures from January 1994 to June 2004 for the same locality (dashed line). The vertical thick-dashed line marks the minimum density value during 1998, which matches the maximum SST value of this year (see text for details). b) X-radiograph contact print of the same specimen, note the lack of high-density band during 1998.

al., 2010), and maximum calcification rates would be expected when environmental conditions are optimal for coral skeletal accretion (Carricart-Ganivet, 2007). Thus, calcification rate is the growth parameter that can give information about how the coral “senses” its environment, and it is this parameter then that should be used as an environmental proxy. Nonetheless, since calcification rate is

calculated as the product of annual extension rate and skeletal density, any errors associated with the measurement of the extension rate will be reflected in the calcification rate values. Depending on the number of months between successive density maxima (or minima), under- and overestimations of calcification rate values will result from year to year when annual extension rate is

Table 2 Mean extension rate, density and calcification rate from the specimen of Montastraea annularis used in Fig. 3, and percentage of under- and overestimations on calcification rate when comparing this growth parameter when extension rate is measured from density maxima with when measured from January to December each year (see text for details). Year

1995 1996 1997 1998 1999 2000 2001 2002 2003

Measured extension rate from density maxima each year

Measured extension rate from January to December each year

Extension rate (cm year− 1)

Density (g cm− 3)

Calcification rate (g cm− 2 year− 1)

Extension rate (cm year− 1)

Density (g cm− 3)

Calcification rate (g cm− 2 year− 1)

0.66 0.76 0.67 0.72 0.82 0.73 0.70 0.85 0.66

1.57 1.58 1.50 1.44 1.52 1.59 1.54 1.54 1.51

1.03 1.20 1.01 1.03 1.25 1.16 1.07 1.32 0.99

0.74 0.80 0.74 0.74 0.80 0.74 0.80 0.74 0.74

1.57 1.57 1.48 1.38 1.62 1.57 1.51 1.56 1.48

1.16 1.25 1.09 1.02 1.29 1.16 1.20 1.15 1.09

Under- and overestimation on calcification rate (%)

11 4 7 -2 4 0 11 -15 9

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measured directly from a density series. Measuring annual extension rate from successive density maxima in the modeled density series presented in Fig. 2a, resulted in calculated calcification rates underestimated between 1% and 30%, and overestimated between 1% and 15%, when comparing calcification rate values obtained when measuring extension rate from January to December each year (i.e., using the mean exothecal dissepiment spacing and taking into account the number of full moons) (Table 1). Similar errors, for the corresponding period of time in the modeled density series (underestimation between 2% and 15% and overestimation between 4% and 11%), resulted when this analysis was applied to the density series of the specimen of M. annularis presented in Fig. 3a (Table 2). The detected under- and overestimations on calcification rates could lead to huge errors if this growth parameter is used as an environmental proxy, for example to reconstruct or predict in a ocean-warming scenario mean annual SSTs. The use of the annual density banding in the skeletons of massive reef-building corals for the reconstruction of proxy environmental records can be enhanced when skeletal extension is accurately measured and the ideas presented herein highlight the necessity of develop a method to do it. Acknowledgements Special thanks to R. Iglesias-Prieto for arguing with me about the ideas translated here. The manuscript was notably improved by the comments of J.M. Lough, R.E. Dodge, and two anonymous reviewers. This work was supported by grants from CONACyT (project U48757-F). [SS] References Baker, P.A., Weber, J.N., 1975. Coral growth rate: variation with depth. Earth Planet Sci. Lett. 27, 57–61. Barnes, D.J., Chalker, B.E., 1990. Calcification and photosynthesis in reef-building corals and algae. In: Dubinsky, Z. (Ed.), Ecosystems of the world. : Coral Reefs, 25. Elsevier, New York, pp. 109–131. Barnes, D.J., Lough, J.M., 1992. Systematic variations in the depth of skeleton occupied by coral tissue in massive colonies of Porites from the Great Barrier Reef. J. Exp. Mar. Biol. Ecol. 159, 113–128. Barnes, D.J., Lough, J.M., 1993. On the nature and causes of density banding in massive coral skeletons. J. Exp. Mar. Biol. Ecol. 167, 91–108. Barnes, D.J., Lough, J.M., 1996. Coral skeletons: storage and recovery of environmental information. Global Change Biol. 2, 569–582. Bosscher, H., 1993. Computerized tomography and skeletal density of coral skeletons. Coral Reefs 12, 97–103. Cantin, N.E., Cohen, A.L., Karnauskas, K.B., Tarrant, A.M., McCorkle, D.C., 2010. Ocean warming slows coral growth in the central Red Sea. Science 329, 322–325. Carilli, J.E., Norris, R.D., Black, B., Walsh, S.M., McField, M., 2010. Century-scale records of coral growth rates indicate that local stressors reduce coral thermal tolerance threshold. Global Change Biol. 16, 1247–1257. Carricart-Ganivet, J.P., 2004. Sea surface temperature and the growth of the West Atlantic reef-building coral Montastraea annularis. J. Exp. Mar. Biol. Ecol. 302, 249–260. Carricart-Ganivet, J.P., 2007. Annual density banding in massive coral skeletons: result of growth strategies to inhabit reefs with high microborers' activity? Mar. Biol. 153, 1–5. Carricart-Ganivet, J.P., Barnes, D.J., 2007. Densitometry from digitized images of Xradiographs: methodology for measurement of coral skeletal density. J. Exp. Mar. Biol. Ecol. 344, 67–72. Carricart-Ganivet, J.P., Beltrán-Torres, A.U., Merino, M., Ruıíz-Zárate, M.A., 2000. Skeletal extension, density and calcification rate of the reef building coral Montastraea annularis (Ellis and Solander) in the Mexican Caribbean. Bull. Mar. Sci. 66, 215–224. Carricart-Ganivet, J.P., Merino, M., 2001. Growth responses of the reef-building coral Montastraea annularis along a gradient of continental influence in the southern Gulf of Mexico. Bull. Mar. Sci. 68, 133–146. Carricart-Ganivet, J.P., González-Diaz, P., 2009. Growth characteristics of skeletons of Montastraea annularis (Cnidaria: Scleractinia) from the northwest coast of Cuba. Cienc. Mar. 35, 237–243. Carricart-Ganivet, J.P., Lough, J.M., Barnes, D.J., 2007. Growth and luminescence characteristics in skeletons of massive Porites from a depth gradient in the central Great Barrier Reef. J. Exp. Mar. Biol. Ecol. 351, 27–36. Chalker, B.E., Barnes, D.J., 1990. Gamma densitometry for the measurement of skeletal density. Coral Reefs 9, 11–23. Chalker, B.E., Barnes, D.J., Isdale, P., 1985. Calibration of X-ray densitometry for the measurement of coral skeletal density. Coral Reefs 4, 95–100. Clausen, C.D., Roth, A.A., 1975. Effect of temperature and temperature adaptation on calcification rate in the hermatypic coral Pocillopora damicornis. Mar. Biol. 33, 93–100. Coles, S.L., Jokiel, P.L., 1978. Synergistic effects of temperature, salinity and light on the hermatypic coral Montipora verrucosa. Mar. Biol. 49, 187–195.

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