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Keywords:

  • coral;
  • lunar;
  • banding;
  • Montastraea;
  • sclerochronology

Abstract

  1. Top of page
  2. Abstract
  3. 1. Introduction
  4. 2. Materials and Methods
  5. 3. Results
  6. 4. Discussion
  7. Acknowledgments
  8. References
  9. Supporting Information

[1] Lunar cycles play an important role in controlling biological rhythms in many organisms, including hermatypic corals. Coral spawning is correlated with environmental factors, including surface seawater temperature (SST) and lunar phase. Calcium carbonate skeletons of corals possess minute structures that, when viewed via X-radiography, produce high-density (HD) annual banding patterns. Some corals possess dissepiments that serve as the microstructural base for upward corallite growth. Here we report the results of detailed structural analysis of the skeleton of Montastraea faveolata (Scleractinia) (Ellis and Solander, 1786) and quantify the number of dissepiments that occur between HD bands, including interannual and intercorallite variability. Using a 30 year database, spanning from 1961 to 1991, we confirm earlier speculation by several authors that the frequencies of these microbands within a year is tightly linked to the lunar cycle. We also demonstrate that the frequency distribution of the number of these dissepiments per year is skewed to lower numbers. Extensive statistical analyses of long-term daily SST records (University of Puerto Rico, Mayaguez) revealed that precipitation of dissepiments is suppressed in years of cooler-than-average seawater temperature. We propose that dissepiment deposition is driven primarily by lunar cycle and seawater temperature, particularly at lower temperatures, and banding is generally unaffected by normal or high temperatures. These fine-scale banding patterns are also strongly correlated with the number of lunar months between reproductive spawning events in average or warmer-than-average seawater temperature years. This microbanding may represent another proxy for high-resolution estimates of variance in marine palaeo-temperatures, particularly during cooler SST years.

1. Introduction

  1. Top of page
  2. Abstract
  3. 1. Introduction
  4. 2. Materials and Methods
  5. 3. Results
  6. 4. Discussion
  7. Acknowledgments
  8. References
  9. Supporting Information

[2] Biological rhythms in organisms are well studied in nature and are known to occur in response to different external cues. Daily and annual periodicities in animals are perhaps the best studied [Aschoff and Wever, 1976; Aschoff, 1981]. Circadian (24 h), ultradian (<24 h), and infradian (>24 h) rhythms are known to have major importance in biological systems [Kumar, 2002].

[3] Lunar cycles play an important role in controlling the biological rhythms in many different organisms [e.g., Korringa, 1957; Saunders, 1977; Bijma et al., 1990; Pineda, 1995; Daan and Beersma, 2002]. For example, direct variations in lunar light intensity, from illumination as low as 1.25 × 10−5μE m−2 s−1 (new moon or starlight) to 2.99 × 10−3μE m−2 s−1 (zenith of full moon), are postulated to cause shifts in lunar rhythms in the spawning of marine organisms on a global basis, including echinoids (Diadema spp. [Muthiga, 2003; Coppard and Campbell, 2005]), annelids (palolo worms [Caspers, 1984; Olive et al., 2005]), and fish [Austin et al., 1975; Gladstone, 2007; Pisingan and Takemura, 2007].

[4] Biological rhythms also occur in scleractinian zooxanthellate corals. This applies to corals that use either brooding/planulation as a mode of sexual reproduction [McGuire, 1998; Fan et al., 2002] or broadcast spawning [Vize, 2006; Zakai et al., 2006]. These rhythms can be either annual, lunar, or year-round and are species- and location-specific [Fadlallah, 1983; Harrison and Wallace, 1990]. They have been observed throughout the world in the tropics and subtropics [e.g., Vargas-Angel et al., 2006; Twan et al., 2007; Kruzic et al., 2008]. Montastraea is a genus that uses broadcast spawning [Harrison and Wallace, 1990]. Throughout the tropical western Atlantic, spawning has been observed to occur approximately 1 week after the full moon, primarily during August or September [Vanveghel, 1994; Steiner, 1995; Sanchez et al., 1999; Levitan et al., 2004; Bastidas et al., 2005; Severance and Karl, 2006; Vize, 2006; Woesik et al., 2006]. The precise timing of spawning varies species-specifically in Montastraea, partitioning the phase space of the lunar cycle, most likely to optimize success of fertilization within its own species. If the full moon occurs too early in August, spawning will often take place after the full moon in September.

[5] Spawning in corals is correlated with various environmental factors, including temperature, day length, lunar phase, and solar insolation [Vize, 2006]. It is known that tissue thickness in massive Porites in Papua New Guinea varies on a lunar cycle [Rotmann, 2004]. Gradual increases in SST may cue the onset of the coming spawning season [Vanveghel, 1994], along with photoperiod. The endosymbiotic zooxanthellae may also sense photoperiod [Babcock et al., 1994], although its specific link to spawning is equivocal [Holloran and Witteman, 1985; Beauchamp, 1993; Mendes and Woodley, 2002]. Corals are sensitive to extremely low light levels, down to 2 × 10−3μE m−2 s−1 [Gorbunov and Falkowski, 2002], just below full/zenith moonlight levels. It is not the photosynthetic system, however, that is sensing this stimulus and possibly responding to it as a cue for spawning. Cryptochromes (1 and 2) in the host tissue, not the zooxanthellae, are responsible for this response. These compounds are primitive, DNA photolyase-like blue-light photoreceptors [Levy et al., 2007], similar to those found in mammals (e.g., Mus) and insects (e.g., Drosophila [Stanewsky et al., 1998; Lin and Todo, 2005]). Related divergent proteins are also known to occur in plants and eubacteria [Falciatore and Bowler, 2005], but no reports exist to date regarding the presence of this specific set of compounds in the zooxanthellae.

[6] Coral banding may be broken down into three tiers, representing different levels of resolution in time. For the sake of simplicity, we shall refer to these as annual or high-density (HD) bands, monthly or lunar bands, and daily bands. High-density bands are deposited annually and can be indicative of a coral's age. They generally occur in genera such as Favia, Goniastrea, and Montastraea [Weber et al., 1975] that are pronounced annual spawning broadcasters [Willis et al., 1985; Babcock et al., 1986; Richmond and Hunter, 1990; Dai et al., 1992; Richmond, 1996; Mendes, 2004]. This character, however, can vary intraspecifically between regions [Highsmith, 1979; Lough and Barnes, 1990] and is often absent in brooding species of corals with multiple/lunar gametogenic cycles [see Mendes, 2004]. HD bands are routinely used to determine an age model for geochemical proxy records of the environment [Leder et al., 1996]. Two of the most important of these geochemical proxies for annual surface seawater temperatures (SSTs) are δ18O [e.g., Grottoli and Eakin, 2007] and trace element ratios (e.g., Mg/Ca) [Finch and Allison, 2008].

[7] HD banding is known to vary in response to seawater temperature. Goreau and Macfarlane [1990] reported that extraordinarily high temperatures occurring for up to 1 year in Jamaica, West Indies, resulted in extended bleaching in Montastraea annularis, and no HD band was being precipitated that year. They deduced that this would introduce potential variance into estimates of a coral's age (an underestimate). Leder et al. [1991] found similar results, where, in the same species, bleaching suppressed skeletal growth by as much as 63% and caused the loss of the following year's low-density band [Leder et al., 1991]. On the other hand, Wórum et al. [2007] predicted that HD bands are highly responsive to increased SSTs and that, if warmer than normal temperatures occurred, double high-density bands would be produced. In a modeling exercise, Wórum et al. [2007] predicted that at seawater temperatures <29°C, HD bands would be formed during the warmest months of the year, but as temperature rose, an annual doublet would occur as two narrow HD bands (HDBs). It was also predicted that if monthly mean temperatures were exceeded throughout the year, HDBs would form during the coldest versus the warmest months of the year, and calcification rates would decline. Evidence for this was presented in M. franksi and M. faveolata under high seawater temperatures, even in the absence of bleaching.

[8] Monthly or lunar banding is derived from one of the many different minute structures associated with coral skeletons. Some corals possess dissepiments that are part of that microstructure, along with theca and septa [Barnes and Devereux, 1988; Dodge et al., 1992]. Dissepiments are one of the basic horizontal building blocks, helping to form a “floor” for each corallite. Corallites produce new dissepiments as the polyps grow outward from the center of the coral colony. Dissepiments are similar in form to ladder rungs that are connected on either side to rails (i.e., the theca and columella [Barnes and Lough, 1993; Helmle et al., 2000, Figure 1]) and have been documented in a number of coral species (e.g., Porites, Pocillopora, Siderastrea [Nothdurft and Webb, 2007]). The first report of such bands derived from the skeletons of living corals was from Buddemeier [1974] who reported closely spaced density bands in the Indo-Pacific coral Porites lobata from Hawaii and the Line Islands. He also reported that the trabeculae of the coral's calex were responsible for the band and that lunar banding patterns disappeared during the winter months in Hawaiian colonies. This site occurs at the cooler, marginal limits of this coral's biogeographic range [Buddemeier and Kinzie, 1975]. Scrutton [1970] reported monthly banding in fossil corals and suggested a possible lunar link. Reuter et al. [2005] also documented these bands in Miocene Porites from Greece. Winter et al. [2000] confirmed the presence of dissepiments in the Atlantic species Montastraea faveolata and suggested that their deposition may be linked to the lunar cycle [also see Roark, 2006]. Dávalos-Dehullu et al. [2008] made similar observations on a number of the Atlantic species of Montastraea, including M. faveolata, from Mexico and also suggested that these microstructures were related to lunar cycles. Questions arise regarding whether the bands are regular and predictable features, confirmation of what microstructures are responsible for the observed patterns, whether banding patterns are associated with lunar cycle and spawning events, and whether they are associated with temperature.

[9] Higher-resolution banding patterns have also been reported to occur between dissepiments in corals. Daily growth bands have been detected in both fossil [Wells, 1963, 1970] and recent scleractinian corals, particularly the Caribbean hermatypic coral Montastraea faveolata [Gill et al., 2006]. Wells [1963] and Scrutton [1964] studied daily growth bands in ancient coral fossils. These structures have been used by geophysicists to determine day length and the number of days per year. These variables have changed through geological time as the moon has moved away from the Earth because of tidal dissipation [Runcorn, 1970; Barnes, 1972; Sorauf, 1972; Risk and Pearce, 1992; Lazier et al., 1999].

[10] Here we report the results of a detailed microstructural analysis of the skeleton of Montastraea faveolata [Ellis and Solander, 1786], a hermatypic scleractinian coral. We go beyond earlier studies and build upon their speculations that the deposition of these microstructural dissepiments may be linked to the lunar cycle. We do this by quantifying in detail number of dissepiments per annum and its annual variation over 30 years. We demonstrate that there is a strong relationship between dissepiment number per annum and lunar cycle, providing detailed supporting data over this time period. We also show that the frequency of this fine-scale banding pattern is consistent with the number of lunar months between reproductive spawning events. We also suggest, on the basis of preliminary data, that there may be a link between this annual variability and annual seawater temperatures, particularly with respect to cooler years. We propose that the deposition of dissepiments is related to and driven primarily by the lunar cycle and that it may be suppressed under conditions of cooler seawater temperatures. We suggest that, if this relationship can be confirmed in other corals, at least in the study region, it may represent a new proxy for reduced average annual seawater temperatures.

2. Materials and Methods

  1. Top of page
  2. Abstract
  3. 1. Introduction
  4. 2. Materials and Methods
  5. 3. Results
  6. 4. Discussion
  7. Acknowledgments
  8. References
  9. Supporting Information

[11] A colony of Montastraea faveolata, occurring approximately 3.2 km offshore from La Parguera, Puerto Rico, at a depth of 7 m (Figure 1), was drilled in situ in 1991. A 7 cm diameter core was extracted along the growth axis of the skeleton. A 3 mm slab was then cut along the length of the core, and an X-radiograph of the slab was taken and enlarged. We counted the number of dissepiments from an X-radiograph (positive; Figure 2) between high-density bands, both visually and using imaging software provided by the National Institutes of Health (Scion Image for Windows, Scion Corp, available at http://www.scioncorp.com/pages/scion_image_windows.htm). In this case we are fortunate in that the corallites revealed by the cross-sectioning of the colony were parallel to the growth axis, with little or no angular deviation. This provided us with an exceptionally low variance in our dissepiment counts. The same software was used to measure the distance from one dissepiment to the next. The program determined the number of dissepiments from the top of one HD band to the top of the next HD band. Bands were delineated by the beginning of a low-pixel density region along the exothecal portion of the calyx. Fifteen replicate coral corallites occurring adjacent to each other were scanned for number of dissepiments between HD bands for the years 1961–1991. This permitted the calculation of means, standard deviations, etc., for statistical analysis. The chronology of each HD band was determined by counting successive bands from the outer (1991) living layer inward. This assumes that the coral was growing continuously and produced an HD band every year.

image

Figure 1. Map of study area, located off La Parguera, southwestern Puerto Rico. Corals collected from the hard-bottom reef environment.

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image

Figure 2. Fine-scale positive print of an X-radiograph of the skeleton from Montastraea faveolata. Derived from a 3 mm slab cut through the coral along the length of a core, exposing the growth lines of multiple corallites. Dissepiments are the smaller dark bands between the larger annual high-density (HD) bands. Note striking linear growth habit of adjacent corallites. HD bands precipitated once a year at approximately the same time as spawning takes place. Montastraea spawn 6–8 days after full moon in August or September (also sometimes in July). LD, low-density band; DIS, examples of coral dissepiments that we propose are precipitated according to the lunar cycle.

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[12] In addition, temperature data from La Parguera were also examined to determine whether there was any relationship between seawater temperature and number of dissepiments per annum. Temperature data were derived from the long-term SST data set collected by the La Parguera Marine Laboratory of the University of Puerto Rico at Mayagüez [Winter et al., 1998; Sammarco et al., 2006]. Temperature data were collected by hand by laboratory personnel almost daily between 0700 h and 0900 h off Isla Magueyes at La Parguera, using a mercury-based thermometer, and logged. The temperatures measured at the laboratory were within ±0.4°C of temperatures measured at a nearby reef [see Winter et al., 1998]. Temperatures were considered on an annual basis, using the calendar year. Data were analyzed either using daily data or annual means. For the lunar cycle analysis, dissepiment counts were considered first on an annual basis and then from HD to HD band, which is associated with the spawning period.

[13] Using dates derived from well-known spawning behavior in this species [Knowlton et al., 1997; Sanchez et al., 1999; Levitan et al., 2004], we determined the number of full moons between spawning events. This facilitated a comparison between the number of dissepiments and the number of lunar phases. Data were analyzed by parametric statistical analyses and frequency analyses. The study followed a two-way, mixed model, replicated orthogonal design. Data were analyzed by two-way analysis of variance (ANOVA); a posteriori analyses, including T′ (Range STP Procedure, or Tukey's Honestly Significant Difference Method, second generation using Q′ as a critical value; Spjotvoll and Stoline [1973]), T-K (the Tukey–Kramer Procedure; Dunnett [1980]), and GT-2 (using the m distribution for comparison; Hochberg [1976]); correlation; autocorrelation; least squares regression; and row by column (R × C) frequency analysis using the G-statistic [Sokal and Rohlf, 1981]. BIOMStat, V. 3.2 and SIMSTAT were the software used. It was sometimes necessary to exclude some data from analysis because of software limitations (e.g., because of missing samples or exceeding the maximum limit for number of samples to be compared). In such cases, samples were removed randomly from the data set with the assistance of a random numbers table in order to meet the requirements of the test [Rohlf and Sokal, 1981]. Only significantly different results will be discussed in the text. Higher-order interactions will only be discussed if they are significant.

3. Results

  1. Top of page
  2. Abstract
  3. 1. Introduction
  4. 2. Materials and Methods
  5. 3. Results
  6. 4. Discussion
  7. Acknowledgments
  8. References
  9. Supporting Information

[14] In all, 442 dissepiments were counted. Of all corallites analyzed, across the 30 year period of records, the grand mean of the number of dissepiments per annum between HD bands was 11.8 with a standard deviation of 1.62 (Figure 3). There were no significant differences between the number of dissepiments between corallites (P > 0.05, two-way ANOVA, nadj = 12; Figure 3).

image

Figure 3. Mean number of dissepiments per corallite. Data taken from an enlarged X-radiograph and derived from number of high-density bands determined by Image software provided by the National Institutes of Health (Scion Image for Windows, Scion Corp, available at http://www.scioncorp.com/pages/scion_image_windows.htm). Mean (ni = 12) shown along with 95% confidence limits. Grand mean for number of dissepiments in all corallites also shown with confidence limits. No significant difference in dissepiment number between corallites (P > 0.05, two-way ANOVA).

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[15] Although the average number of dissepiments per corallite was relatively consistent, it varied significantly between years (P < 0.001, two-way ANOVA). The average number of dissepiments counted between HD bands for the years 1961–1991 ranged between 7 and 14 (Figure 4). The frequency distribution of the dissepiment numbers per annum was clearly skewed to the left; that is, the number of dissepiments more often fell below 12 than above it. The mode of the frequency distribution of dissepiment numbers was 12 (ni = 118; nt = 443), while the next highest frequencies were 13 (ni = 98) and 11 (ni = 84), respectively.

image

Figure 4. Frequency distribution of number of dissepiments per annum across all corallites, encompassing a record of 30 years. Note that the value of the mode is 12. This distribution indicates the amount of variability in the coral's response to number of lunar periods, influenced by a second factor, i.e., SST (see Figure 6). Note skewness toward left or the lower number of dissepiments, indicating a greater sensitivity to cooling than to warming in this character.

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[16] The number of dissepiments per year in the set of years encompassing 1965, 1972, 1973, 1974, 1976, 1977, and 1979 were significantly lower than in the remaining years (P < 0.05, T-K, and GT2 a posteriori tests, nadj = 20; Figure 5 and Table 1). The number of dissepiments per year was found to be significantly positively correlated with mean annual seawater temperature (P < 0.001, Pearson's product-moment correlation coefficient; P < 0.001, model II regression analysis; Figure 6), but the level of correlation was relatively low, −0.212. This low level of correlation is indicative of the amount of variance inherent in the relationship and of other confounding factors that might influence the number of dissepiments. The large sample size we used (n = 443) increased the power of the test [Sokal and Rohlf, 1981] sufficiently so that we were able to detect this correlative signal and was responsible for the high level of significance found in the relationship.

image

Figure 5. Mean number of dissepiments per year, calculated across corallites, shown with 95% confidence limits. Years listed in order of significant comparisons as determined by T-K and GT-2 a posteriori tests (P < 0.05). Years 1–7 are, in order, 1979, 1974, 1972, 1976, 1973, 1977, and 1965; years 8–20 are 1978, 1971, 1970, 1987, 1984, 1989, 1982, 1990, 1961, 1968, 1975, 1980, and 1962. Significantly different sets of years grouped together. Grand mean also shown, with 95% confidence limits.

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Figure 6. Number dissepiments per corallite versus mean annual SST in the study area. Number of dissepiments and mean SST positively correlated (P < 0.001, r = 0.21209, Pearson's product-moment correlation). Relationship described by a significant positive linear regression as well (P < 0.001, model II linear regression, y = 24.4556x + 0.0576).

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Table 1. Results of A Posteriori Tests for Differences in Number of Dissepiments Between Sample Yearsa
YearReference No.Year:Years, Ordered by Results of A Posteriori Tests
19791974197219761973197719651978197119701987198419891982199019611968197519801962
Reference No.1234567891011121314151617181920
  • a

    As determined by T-K and GT-2 techniques (P < 0.05). All pairwise comparisons are shown. Box indicates major break in groups, showing that first 7 years are all significantly different than remaining years. Asterisk denotes significant difference using the a posteriori tests T-K and GT-2 (P < 0.05). All years in left-hand group (1–7) have significantly lower mean SSTs than the right-hand group (8–20); see Table 2.

 
19791        *************
19742         ************
19723         ************
19764         ************
19735            *********
19776              *******
19657              *******
19788               ******
19719                   **
197010                    *
198711                    *
198412                    *
198913                     
198214                     
199015                     
196116                     
196817                     
197518                     
198019                     
196220                     

[17] Those years identified above to be significantly different than the remaining years also had below-average mean annual seawater temperatures. When only years that were normal or warm with respect to mean seawater temperatures were considered, the average number of dissepiments produced per year was 12.3 (Table 2). This value is exactly the same as the average number of full moons occurring per year for the same time period. On the other hand, when the number of dissepiments was considered only for the cooler seawater years, the number of dissepiments underestimated the number of full moons per annum by ∼2 (Table 3). The distance between dissepiments was nearly constant at 0.05 mm. This was the case irrespective of number of dissepiments per year.

Table 2. Mean Number of Dissepiments Per Annum Across All Corallites for Normal Or Warm Years Identified by A Posteriori Tests of Sea Surface Temperature Data Versus Number of Full Moons for That Yeara
YearNormal or Warm Years
Mean, All CorallitesRounded MeanFull Moons Per YearSDbnb
  • a

    Rounded mean number of dissepiments also shown. Standard deviation and ni pertaining to number of dissepiments shown, along with rounded and truncated means. Note precision and uniformity in estimation of number of full moons, whether by use of mean number of dissepiments per year or rounded mean.

  • b

    For Mean, all corallites.

196112.913130.9215
196213.814121.1515
196311.512120.9215
196412.713120.8815
196612.913131.0315
196711.011121.0015
196812.813120.9714
196911.812130.6815
197011.712121.2112
197111.912131.1915
197512.913120.8315
197811.912120.9215
198013.213131.0815
198111.812121.1515
198212.212131.2115
198311.211121.0815
198411.712120.8015
198512.513122.0315
198614.114121.1615
198712.212121.1515
198812.212120.8615
198912.012120.7615
199012.513130.9215
199113.113120.9215
nt    356
 
Mean12.3512.312.3  
Mean, rounded121212  
Mean, truncated121212  
SD0.7690.780.46  
n242424  
Table 3. Mean Number of Dissepiments Per Annum Versus Number of Full Moons for That Yeara
YearColder Years
Mean, All CorallitesRounded MeanFull Moons Per YearSDbnb
  • a

    Data shown for all corallites for the cooler years are identified to be significantly different from all remaining years by a posteriori tests. See Figure 2 for details. Note consistent underestimation of number of full moons under conditions of low SSTs.

  • b

    For Mean, all corallites.

196510.510121.1915
197210.010121.6015
197310.110120.8315
197410.110131.1915
19769.710120.7215
197710.310131.1815
19799.09120.5315
nt    105
 
Mean9.979.912.3  
Mean, rounded101012  
Mean, truncated10912  
SD0.5060.500.49  
n777  

[18] When the mean number of dissepiments per annum was regressed upon time, number of dissepiments was found to increase highly significantly with time in a linear fashion (P < 0.001, regression analysis; Figure 7). This increase, again, was detectable because of the high sample size used and its enhancing effect on the power and sensitivity of the test [Sokal and Rohlf, 1981].

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Figure 7. Mean number of dissepiments per corallite per year as a function of time, from 1965 through 1991. Mean plus 95% confidence limits shown. Significant positive relationship between the two variables (r = 0.250, P < 0.001; linear regression line with 95% confidence bands provided to emphasize nature of positive relationship; Y = 0.052X − 90.723, P < 0.001).

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[19] Mean annual seawater temperature for all years was not found to be correlated with time over the period of the study (P > 0.05, correlation analysis). However, when time-series data were plotted for both the number of dissepiments and mean annual seawater temperature in parallel, despite that fact that the two variables did not appear to be strongly related, correlation analyses revealed that they were indeed highly significantly correlated (P < 0.001, P = 5.492 × 10−5; Figure 8a). The overall level of correlation, however, was relatively low, r = 0.212, suggesting that confounding factors may be influencing number of dissepiments per annum. That confounding factor was identified as warmer mean temperatures. This was done by removing them from the plot and from the analysis (e.g., <26.2°C; Figure 8b). The two variates tracked each other much more closely, resulting in an increased correlation coefficient of 0.393 (P < 0.001).

image

Figure 8. Mean number of dissepiments per corallite (solid circle) in Montastraea faveolata and annual mean seawater temperature (open triangle) in La Parguera, Puerto Rico (study site), shown as a function of time from 1965 to 1991. (top) Data for all years and all annual seawater temperature conditions. Significant increase in number of dissepiments through time (see Figure 7) and significant increase in seawater temperature with time (r = 0.107, P < 0.001). Also, significant correlation between number of dissepiments and seawater temperature (r = 0.212, P < 0.001). Note decoupling of relationship at higher temperatures. (bottom) Data for years with annual mean seawater temperatures <26.2°C. Note increased coupling of these two variables in cooler years. Correlation coefficient is higher in cooler years versus when all years are considered; also increased significance of correlation (r = 0.393, P = 5.224 × 10−8 in the cooler years versus r = 0.212, P = 5.492 × 10−5 when all data are included).

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[20] In order to clarify the relationship between seawater temperature and dissepiment number, we conducted a series of correlation analyses in sequence. That is, all data were included in the first analysis. In the second analysis, the year with the highest annual mean seawater temperature was eliminated. In the third analysis, the year with the two highest mean seawater temperatures were eliminated, and so forth, for a total of 21 sequential analyses. The resulting correlation coefficients were then plotted against the maximum mean annual seawater temperature included in a given analysis. It was determined that the correlation coefficient was much higher in cooler years, reaching as high as 0.566 (Figure 9). The relationship between the number of dissepiments and maximum annual seawater temperature was negatively curvilinear and could be described by a second-degree exponential decay polynomial regression (Y = 136.556 − 10.174X + 0.190X2). A major drop in correlation between number of dissepiments and temperature occurred above a maximum seawater temperature of ∼25.8°C.

image

Figure 9. Relationship between mean annual seawater temperature and number of dissepiments per annum in Montastraea faveolata using sequential correlation analyses. Data from years with the highest mean annual seawater temperatures were removed from the analysis 1 year at a time, respectively. The relationship is described by a second-degree polynomial equation (Y = 136.556 − 10.174X + 0.190X2). Note that the correlation coefficients are higher (up to 0.566) when only the cooler years are considered, but they are not affected at higher mean temperatures, indicating that dissepiment count can be an indicator of years characterized by cooler seawater temperatures.

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[21] The spawning days and times for Montastraea faveolata are known for this region of Puerto Rico [Steiner, 1995; also see Sanchez et al., 1999; Levitan et al., 2004; Bastidas et al., 2005]. Therefore, it was possible to quantify the number of full moons between spawnings and the mean number of dissepiments deposited in that same time period. It was found that the number of full moons between spawnings and the mean number of dissepiments during the same period was very similar; there was no significant difference between the two (P < 0.05, P = 1.0, R × C goodness of fit test, G-test; Table 4).

Table 4. Mean Number of Dissepiments Per Annum (Rounded) as Determined Via Visual Inspection of Radiographs Versus Number of Full Moons Between Spawningsa
YearNo. of Full Moons Between Coral SpawningsMean No. of Dissepiments (Rounded)
  • a

    Data are derived from the coral Montastraea faveolata in the study area. Only data from second group of normal SST or warmer years are analyzed here. No significant difference between number of dissepiments and number of full moons (P > 0.05, P = 1.0, R × C goodness of fit frequency analysis, G-test). Note precision of estimates of number of full moons per annum using number of dissepiments per annum.

19611313
19621114
19631312
19641113
19661313
19671111
19681313
19691312
19701112
19711312
19751313
19771310
19781112
19801313
19811112
19821312
19831211
19841312
19851213
19861114
19871312
19881212
19891112
19901313
19911313
 
Mean12.212.3
SD0.920.87
n2525
   
No significant difference, P > 0.05 (P = 1.0), R × C goodness of fit test.

4. Discussion

  1. Top of page
  2. Abstract
  3. 1. Introduction
  4. 2. Materials and Methods
  5. 3. Results
  6. 4. Discussion
  7. Acknowledgments
  8. References
  9. Supporting Information

[22] The data indicate that there is a strong relationship between number of dissepiments per annum and number of full moons per year. In fact, it is known that corals exhibit strong biological responses to the lunar cycle. In addition, at present, there is no other known potential geophysical force that varies with the same frequency as the lunar cycle. It is possible that such might exist, but no data exist at present to support this concept. The data also indicate, however, that the variance in this relationship, and the distribution of that variance in dissepiment number, is skewed to the left or toward a lower number of dissepiments. If dissepiment number is driven solely by lunar phase, then the number of dissepiments between HD bands should be equal to the number of full moons between spawning. The number of full moons for any given calendar year can only be 12 or 13 (Table 2). The number of dissepiments per year in normal or warmer years varied generally from 11 to 14. This discrepancy may be partly due to the coral's near, but not perfect, linear upward growth. Although the corallites studied here appeared to be growing upward in a linear fashion, as evidenced by the almost parallel dissepiment structures (Figure 2), the coral may have had a slight curvature. In that case, a slice from the coral may have produced extraneous coral banding on the X-radiograph derived from a neighboring corallite.

[23] Another explanatory hypothesis is related to the spawning behavior of Montastraea spp. Spawning generally takes place 7 days after the full moon during a single month [Woesik et al., 2006]. That month can occur between August and October [Knowlton et al., 1997; Hagman et al., 1998; Sanchez et al., 1999; Mendes and Woodley, 2002; Levitan et al., 2004; Bastidas et al., 2005], when the HD band, used here as a benchmark, is deposited. Spawning is also dependent upon whether the full moon occurs early or late in a month and whether seasonal temperatures have reached a trigger threshold in alignment with the appropriate lunar phase [Vize, 2006]. If spawning occurred early in 1 year (e.g. July [Gittings et al., 1994]) and late the following year (e.g. September [Bastidas et al., 2005]), affecting the distance from one HD band to that of the following year, it might be possible for the coral to log 13 or 14 full moons between spawnings. Alternatively, if there were a late spawning 1 year (e.g., October) and an early spawning the next year (e.g., August), the coral could log the minimum number of 10 full moons. Another potential source of variance here is that bleached corals generally fail to spawn; the HD band is formed during spawning season, and under these conditions, the HD band is not formed [Szmant and Gassman, 1990].

[24] A comparison of the dissepiment counts versus the 30 year daily temperature records for La Parguera shows that the years with the lowest dissepiment counts (Table 1, italics) were the coldest summers in this set of records. That is, all years showing low dissepiment counts were years with colder-than-average summers. This suggests that the deposition of dissepiments is being suppressed during colder-than-average years. The overall frequency distribution of number of dissepiments per corallite supports this concept of the coral being more sensitive to cooler seawater temperatures than warmer ones. This first observation of this relationship raises the question as to whether dissepiment counts can act as a new indicator of lower-than-average seawater temperatures, both seasonally and annually. It is possible that bleaching may diminish the dissepiment count. This may have been the case especially in the well-known bleaching years at La Parguera of 1987 and 1990 [Sammarco et al., 2006]. However, our specimen appears to have been unaffected, indicating that it may have been genetically “unusual” or that bleaching did not affect carbonate deposition of dissepiments.

[25] Shimamura et al. [2005] reported that the optimal growth temperature for Porites spp. in the South China Sea is 22°C–26°C. They determined that corals in the Pacific do not grow above or below these temperature thresholds. Lower growth rates have been documented to occur at higher temperatures in, for example, Montastraea annularis in the Caribbean [Carricart-Ganivet, 2004, 2007] and Porites on the Great Barrier Reef [Lough and Barnes, 2000].

[26] Seasonal changes in growth rate are suspected to be correlated with the channeling of energy into planula production for brooding corals (e.g., Balanophyllia elegans [Vaughan, 2004]) or gamete production for broadcast spawning corals (e.g., Goniastrea aspera [Sakai, 1998]). Thus, changes in scleractinian coral calcification rates may be expected to be seasonal. Slowing or lack of calcification at temperatures lower than 22°C may be due to temperature influences on the symbiotic relationship between the coral and zooxanthellae, temperature effects on the physicochemical reactions involved in calcification, and/or the ability of the zooxanthellae to efficiently facilitate the deposition of calcium carbonate. Maximal growth rates in corals are often negatively [Buddemeier and Kinzie, 1975; Shi et al., 2003; Wagner and Slowey, 2006] and occasionally positively [Mitsuguchi et al., 2003] correlated with seawater temperatures in hermatypic corals. They can also vary in ahermayptic corals [Peirano et al., 2005; Dimond and Carrington, 2007]. Growth rates are also suspected to change with the age of the coral [Lough, 2008].

[27] In this study dissepiment count was highly significantly negatively associated with seawater temperature. The degree of the initial correlation calculated, however, was not overly strong, 0.219; but once the higher temperature years were eliminated sequentially from the analysis, it became apparent that the correlation was quite strong in the cooler years, up to almost 0.60. There may be several possible factors, which might help to explain the balance of the variance in the correlation. Dissepiment number is being influenced primarily by two factors that we can identify: lunar phase and temperature. Each of these factors will introduce their own variance into the data, and that variance may be additive. In addition, it is clear that the effect of seawater temperature on dissepiment count is operating at lower temperatures only, not at higher temperatures that have no enhancing effect on dissepiment number. Extraordinarily high temperatures cannot add additional dissepiments because such is capped by the number of lunar cycles per annum; there is only a maximum number of dissepiments that the coral can deposit within a given year: a ceiling. Dissepiment number can only be negatively affected by low temperatures.

[28] Other environmental factors may also be influencing the deposition frequency, such as turbidity [Carricart-Ganivet and Merino, 2001; Rotmann, 2004], surge, sedimentation, dissolved nutrients [Cruz-Piñón et al., 2003], or prolonged cloud cover. Unfortunately, we do not possess high-resolution data on these factors and can make no conclusions regarding their importance as influencing factors. Clearly, additional research would be of assistance here.

[29] The fact that the correlation between these two variables increased further when the analysis only included cooler years, where higher annual mean seawater temperatures were excluded from the analysis, indicates that changes in this micromorphological character are strongly linked to changes in temperature during cooler-than-average years, not warmer ones. It is likely that dissepiments are not being deposited during the winter, and growth is stunted or stops completely during cold winter months. This implies that corals are not precipitating as much calcium carbonate during cold years as they do in warm years. As atmospheric temperature increases, winter seawater temperatures may also be expected to rise. Under these conditions, coral growth may be expected to be maximal, except where temperatures exceed the temperature tolerances of corals, resulting in bleaching and a concomitant reduction in growth [Goreau and MacFarlane, 1990] and, in severe cases, mortality [Sammarco and Strychar, 2009].

[30] High-resolution stable isotopic analysis along the growth axis of Montastraea spp. in many islands within the Caribbean clearly shows that the lightest values of δ18O, indicative of the warmest SSTs, occur in September through October. These lightest values occur just prior to production of the HD bands [Watanabe et al., 2002]. The HD band occurs around spawning for this species and is thought to form as a result of decreased extension rates as the corals divert their energy from growth to gamete production, in preparation for mass spawning in August. Understanding potential causes for variance in the formation of HD bands is important because they are routinely used to establish effective chronologies.

[31] Predicted spawning windows based on timing of the full moon within the potential spawning period for corals in this region are shown in Table 3. The number of predicted full moons per year between one year's spawning event and that of the next year can only be 11,12, or 13. The number of full moons in the years considered here did not vary significantly from the average number of dissepiments associated with each of the years considered (Table 3). This relationship, in addition to the positive association between the average dissepiment counts in normal or warmer years and the average number of full moons, provides strong evidence that production of dissepiments by Montastraea faveolata is related to lunar cycle. The dissepiments that scleractinian corals produce, as in this species, may well act as a record of monthly calcification activities, based on lunar months. The sensing of lunar periodicity is necessary for reproductive success in these corals, since they participate in a mass synchronous spawning exercise. The number of lunar cycles changes from one spawning period to the next; thus, the corals must be able to respond to cues associated with the lunar cycle in combination with the seasonal solar cycle [Woesik et al., 2006] and changes in seawater temperature. It is unlikely that any one signal is sufficient to serve as a cue for a specific night and time for spawning. It is more likely that photoperiod and seasonal SSTs act as coarse cues for seasonal changes and that the lunar cycle acts as a finer resolution cue for spawning.

[32] The confirmation of lunar banding in corals here has several additional important implications. The first is that it confirms the observations of potential lunar cycles in dissepiment counts made by Dávalos-Dehullu et al. [2008] in several common congeners of Montastraea within the Montastraea species complex in the Caribbean. Second, Buddemeier [1974] and Buddemeier and Kinzie [1975] found similar lunar banding patterns in trabeculae of an Indo-Pacific coral, Porites lobata. Thus, this sclerochronological character may be a common character within the zooxanthellate Scleractinia, being distributed globally. Third, it implies that the physiological capacity of the coral to precipitate lunar bands evolved prior to the pre-Miocene and certainly before the Pleistocene. During the pre-Miocene (>25 Myr), corals had a pan-Tethyan distribution [Rosen, 1978; Stanley, 1979; Veron, 1986, 1995; Edinger and Risk, 1995]. During the early Miocene, 3.4 Myr, the Isthmus of Panama emerged separating the Atlantic and Pacific oceans and causing massive extinctions in the Caribbean [also see Stanley, 1984]. A second major extinction occurred in the Caribbean during the glaciation associated with the onset of the late Pliocene/early Pleistocene [also see Stanley, 1981, 1985, 1986]. Such extinctions did not occur in the Indo-Pacific, and this is why the recent Indo-Pacific coral fauna are so different and so much more species-diverse than their Caribbean counterparts [Kuhlmann, 1985; Sammarco and Coll, 1992]. Similar characters in these two sets of fauna most likely existed prior to the onset of the genetic bottlenecks that occurred in the Caribbean.

[33] It is clear that the lunar cycle has been a strong selective factor in the evolution of the Scleractinia. In the symbiotic relationship existing between the host coral and its zooxanthellae, it is likely that the host coral in this partnership is the one responding to changes in lunar light levels [Levy et al., 2007]. The holobiont will most likely respond to whatever the lunar cycle is at that time as an external stimulus. This should be testable, provided that the coral's microstructure has been well preserved. Further research is recommended in this area.

[34] The number of dissepiments between HD bands may be used to reconstruct fine-scale changes in environmental conditions. Although the exact timing of dissepiment deposition within the lunar month is not known, they must be precipitated within a period of about 28 days in a normal average temperature or cooler year. With further work, we may able to determine the environmental characteristics of the surface waters at higher (e.g., subseasonal) resolutions using dissepiment counts as a new indicator for lower-than-average temperatures. This might be applied to other recent and possibly fossil corals.

Acknowledgments

  1. Top of page
  2. Abstract
  3. 1. Introduction
  4. 2. Materials and Methods
  5. 3. Results
  6. 4. Discussion
  7. Acknowledgments
  8. References
  9. Supporting Information

[35] We thank André Paul, Wolfgang Berger, and Hans Thierstein for fruitful discussion. The crew of the R/V Pezmar and Milton Carlo were instrumental in coral coring. We also thank A. Lirette and Y. Tung for assistance with statistical analyses and graphics, and A. Kolker, S. Smith, and E. Weil for comments on the manuscript.

References

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  2. Abstract
  3. 1. Introduction
  4. 2. Materials and Methods
  5. 3. Results
  6. 4. Discussion
  7. Acknowledgments
  8. References
  9. Supporting Information
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Supporting Information

  1. Top of page
  2. Abstract
  3. 1. Introduction
  4. 2. Materials and Methods
  5. 3. Results
  6. 4. Discussion
  7. Acknowledgments
  8. References
  9. Supporting Information
FilenameFormatSizeDescription
jgrg663-sup-0001-t01.txtplain text document1KTab-delimited Table 1.
jgrg663-sup-0002-t02.txtplain text document1KTab-delimited Table 2.
jgrg663-sup-0003-t03.txtplain text document1KTab-delimited Table 3.
jgrg663-sup-0004-t04.txtplain text document1KTab-delimited Table 4.

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