Biol. Bull. 212: 20-28. (February 2007)
© 2007 Marine Biological Laboratory
Tissue Age Affects Calcification in the Scleractinian Coral Madracis mirabilis
Robin Elahi* and
Peter J. Edmunds
Department of Biology, California State University, Northridge, California 91330-8303
* To whom correspondence should be addressed, at Department of Biology, University of Washington, Seattle, Washington 98195-1800. E-mail: elahi{at}u.washington.edu
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Abstract
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In this study, two factorial experiments were used to investigate the role of tissue age in affecting the phenotypic expression of calcification in scleractinian corals. Both experiments tested whether calcification was altered by tissue age and whether corals of different ages exploit plasticity to differing degrees by altering calcification rates under new environmental conditions. To isolate age and size effects, branches of the Caribbean coral Madracis mirabilis were broken into a distal portion that was functionally young and a proximal portion that was functionally old. Fragments were transplanted from a deep (17 m) to a shallow (9 m) site in a Jamaican lagoon to test whether age affected the plasticity of calcification. Both experiments demonstrated that calcification scaled isometrically in the two age groups, and although scaling exponents were indistinguishable statistically among ages, young fragments calcified faster than old fragments. Thus, the effect of age on calcification rate was absolute and independent of size. However, the interactive effect of age and depth was not significant, demonstrating that ability to alter calcification rate (i.e., the extent of phenotypic plasticity for this trait) was unaffected by age. Together, these patterns are consistent with the hypothesis that the proximal modules (i.e., polyps) of M. mirabilis are subject to physiological senescence, as has been reported for other clonal organisms, including algae, fungi, plants, bryozoans, ascidians, and other cnidarians.
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Introduction
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The modular design of many benthic marine invertebrates, including cnidarians, bryozoans, and ascidians, has profound implications for their biology (Jackson et al., 1985). In particular, the ecological success of modular invertebrates on subtidal hard substrata is related directly to their ability to spread across the benthos by the rapid, asexual iteration of modules (e.g., polyps, zooids), which together compose individual colonies of physiologically integrated units. One direct consequence of this asexual iteration is a difference in age among modules of a colony, with the youngest tissue located at sites of active module proliferation, which typically occurs at peripheral margins (Boardman and Cheetham, 1973). Thus while a colony has an absolute age (defined by the time elapsed since larval settlement), it consists of a spatial mosaic of modules differing in age (as defined by the time elapsed since their asexual origin).
To date, the effects of age on the biology of modular invertebrates have largely been overlooked, partially because individual genotypes have the ability to persist indefinitely through asexual propagation and thus are regarded as "immortal" (Jackson and Coates, 1986). In addition, colony age is difficult to determine because colony fission, fusion, and fragmentation can uncouple the relationship between age and size (Hughes and Jackson, 1980), and therefore age can be reliably determined only by tracking sexual recruits through time. In spite of these issues, several studies have demonstrated significant physiological effects of age in modular organisms. For example, old zooids in the bryozoan Steginoporella exhibit decreased feeding and regenerative abilities relative to young zooids (Palumbi and Jackson, 1983), and in scleractinian corals, age has significant effects on reproduction (Kojis and Quinn, 1985) and the regeneration of tissue after lesion (Meesters and Bak, 1995). These studies suggest that the iterative units of modular invertebrates are subject to the nearly universal physiological constraints set by advancing age, as shown by other multicellular animals (Hughes and Reynolds, 2005).
Although the effects of age on modular invertebrates are unclear, the effects of the environment in driving phenotypic plasticity are well-documented (Anthony and Hoegh-Guldberg, 2003b, Kaandorp, 1999), and such plasticity is widespread among sessile organisms (Schlichting and Pigliucci, 1998). Much of the research attention accorded to phenotypic plasticity has focused on the interaction between genotypes and the environment, where a single genotype displays a gradient of phenotypes in response to an environmental gradient (i.e., a norm of reaction, sensu Schlichting and Pigliucci, 1998). Typically, reaction norms have been examined in adult stages (Schlichting, 1986), but recent studies highlight the potential importance of ontogenetic shifts in the type and extent of plasticity (Arnqvist and Johansson, 1998, Ostrowski et al., 2002, Pigliucci and Schlichting, 1995). In other words, the phenotypic response of organisms to their environment may vary with age.
The objective of the present study was to examine how age affects the phenotypic expression of calcification in scleractinian corals. Due to the difficulties associated with determining the age of coral colonies (Hughes and Jackson, 1980), we exploited the physiological age gradient created along the branches of a coral by apical growth to produce a relative age contrast between proximal (older) and distal (younger) portions of branches. Specifically, we tested whether (1) calcification is altered by tissue age, and (2) corals of various ages exploit plasticity to differing degrees by altering calcification rates under new environmental conditions. Calcification is the physiological basis of skeletal growth in scleractinian corals (Barnes, 1973, Gattuso et al., 1999), and it is an indirect measure of fitness due to strong inverse size-dependent mortality (Hughes and Jackson, 1985) and positive size-dependent fecundity (Soong, 1993). To achieve these objectives, we conducted two separate factorial transplant experiments. The first experiment was designed to test the effects of age, size, and genotype on the plasticity of calcification. The second experiment tested solely the effects of age and size on the plasticity of calcification, and also tested for intrinsic differences in tissue biomass and the population density of symbiotic unicellular algae (Symbiodinium) between young and old fragments. If such differences are present, they might provide important insight into the mechanistic basis for a physiological age contrast.
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Materials and Methods
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The Caribbean scleractinian coral Madracis mirabilis (Duchassaing and Michelotti, 1860) was selected as a model system because it is abundant in a variety of environments (Bruno and Edmunds, 1997) and has a branching morphology that facilitates an experimental analysis of age (described below). Branches were collected from aggregates (i.e., genets; defined as an aggregation of clonal branches connected by a common skeleton but not by tissue) separated by a distance of more than 15 m to increase the probability of sampling genetically distinct individuals (Bruno and Edmunds, 1997). Aggregates were sampled from 13- to 18-m depth at Columbus Park, Jamaica, where branches of M. mirabilis are long, slender, and widely spaced (Bruno and Edmunds, 1997, Sebens et al., 1997), and therefore well-suited to preparing experimental units (fragments) varying in age depending on the distance from the growing tip.
Because M. mirabilis grows primarily by apical extension (Bruno and Edmunds, 1997), the youngest tissue is located at the distal ends of branches, and the proximal portions of branches are covered by relatively older tissue. Thus, by breaking branches in two, physiologically young (i.e., distal) and old (i.e., proximal) fragments can be created. Using skeletal extension rates of 2.2 ± 0.5 cm yr–1 (mean ± SE; n = 12) for corals from 10-m depth at Columbus Park (calculated from fig. 6 in Bruno and Edmunds, 1997), we estimated that young fragments 2.5 cm in length ranged in age from several weeks at their tip to 1.3 years old at their base, and old fragments 2.5 cm in length ranged from 1.3 years at their tip to 2.6 years old at their base. These age estimates likely are conservative because coral growth rates decrease with depth (Huston, 1985) and the branches in this study were collected at depths greater than those used by Bruno and Edmunds (1997). The rounded tips of distal fragments were removed with a small chisel so that neither old nor young fragments possessed tissue-covered tips. Each fragment was epoxied (Z-spar Splash Zone A-788) upright to a plastic tile (4 x 4 cm), which then was transplanted to a platform made of cement blocks at one of two depths (described below) on the same reef from which it was collected. To consider fragments statistically independent, tiles were spaced so that fragments were 5 cm apart and exceeded the branch spacing found naturally in aggregations at 10-m depth at Columbus Park (
1 cm; Bruno and Edmunds, 1997) and at 20-m depth on the forereef at Discovery Bay (1.7–1.9 cm; Sebens et al., 1997).
To test the hypothesis that the plasticity of calcification rate varied with coral age (ontogenetic plasticity, sensu Pigliucci and Schlichting, 1995), the young and old fragments were transplanted to the Columbus Park reef and distributed randomly to one site at the collection depth (17 m), or to a second site in shallower water (9 m). First, we designed a 14-week experiment to be analyzed with a factorial three-way analysis of covariance (ANCOVA) testing the main effects of age (fixed), depth (fixed), and genet (random), using surface area as the covariate. Subsequently, we designed a second experiment that was similar to the first, but due to logistical constraints was shorter (3 weeks) and executed during a different season (summer rather than spring). Despite these differences, it was important to conduct a second experiment to determine whether distal and proximal fragments had any intrinsic variation in tissue content that could influence the effects of age and depth on calcification. Significant first-order interactions between either age and depth or genet and depth would represent ontogenetic and phenotypic plasticity, respectively, indicating that corals of different ages and genotypes exhibit dissimilar responses to changing environmental conditions (i.e., depth). Scaling relationships between calcification rate and coral surface area also were quantified for corals in each treatment to test the hypothesis that calcification scales isometrically, and that this relationship does not vary with the age of the coral. Because calcification may be mass-transfer limited (Dennison and Barnes, 1988) and is a surface area phenomenon (Gattuso et al., 1999), we expected it to scale isometrically with surface area. If, however, we observed a negative allometry in the scaling of calcification with surface area, this would indicate that small fragments calcify at disproportionately faster rates than larger fragments, regardless of age. The surface area of the skeleton covered by tissue was estimated geometrically from the surface area of a hollow cylinder having dimensions equal to the length and mean diameter of each branch fragment. Preliminary analyses demonstrated that geometric estimates of surface area were statistically indistinguishable (paired Student’s t-test, t = 0.551, df = 23, P > 0.5) from areas estimated using the foil-wrapping method (Marsh, 1970).
Calcification rate (in milligrams of skeleton per day) was quantified by using the buoyant weight method (Davies, 1989) to determine skeletal weight at the beginning and end of each transplant period. Each fragment was weighed (±1 mg) in seawater after epiphytes were removed, and the change in buoyant weight was converted to dry skeletal weight by using equations from Davies (1989), assuming the density of aragonite to be 2.93 mg cm–3.
The effects of age, depth, genet, and size on calcification were tested with the first experiment in the winter and spring of 2004. Branches of M. mirabilis were collected from each of three aggregates at 13- to 17-m depth, and 7–8 fragments of each aggregate and age group were weighed and transplanted to one shallow (9 m) and one deep (17 m) site on 5 March 2004. The collecting, weighing, and transplanting procedures were accomplished within 48 h; thereafter the corals were left undisturbed on the reef until they were retrieved on 13 June 2004, when they were again weighed by the buoyant method. The second experiment was conducted in the summer of 2004 to ensure that the outcome of the age contrast was not unique to the three aggregates originally sampled, and to test for intrinsic physiological differences between young and old fragments. For this shorter experiment, three young and three old fragments were generated from each of 12 aggregates of M. mirabilis collected from 15- to 18-m depth at Columbus Park reef. After buoyant-weighing, the fragments were pooled among collection genets, and 18 fragments of each age class were allocated haphazardly to shallow (9 m) and deep (17 m) transplant treatments on 13 June 2004; they were retrieved and reweighed on 3 July 2004.
To determine whether the age groups exhibited differences in tissue content and population densities of symbionts, 12 fragments of each age class were sacrificed prior to the start of the 3-week experiment. Coral tissue was removed from the skeletons using a Waterpik oral irrigator (Johannes and Wiebe, 1970) filled with 0.45-µm filtered seawater and used for the determination of Symbiodinium density and protein biomass. Symbiodinium densities were quantified for each age class (n = 12) using a hemacytometer (10 replicate counts/sample). Protein was solubilized from aliquots of coral slurry by incubating with 1 mol l–1 NaOH at 50°C for 5 h, followed by the addition of 1 mol l–1 HCl to neutralize the slurry. Duplicate subsamples then were assayed for protein content using the Coomassie brilliant blue procedure (Bradford, 1976) with standards prepared from bovine serum albumin in filtered seawater.
For the 14-week experiment, a three-factor ANCOVA was used to test for the effects of age, depth, and genet, using the log of the surface area as the covariate and the log of the calcification rate as the dependent variable. For the 3-week experiment, a two-factor ANCOVA tested the fixed effects of age and depth, using the log of the surface area as the covariate. After testing for heterogeneity of slopes (i.e., the significance of factor x covariate interactions), the mean square and degrees of freedom of statistical interactions between factors were pooled into the error term when not significant statistically (P > 0.05). To determine whether the initial size of fragments varied by treatment levels in both experiments, ANOVA tested the effects of age, depth, and genet (14-week experiment only) on mean initial surface area.
Logarithmic linear regressions using a measure of body size as the independent variable and a physiological trait as the dependent variable are commonly recognized as scaling relationships (Schmidt-Nielsen, 1984), which can be described as isometric or allometric depending on the slope of the linear regression (i.e., the scaling exponent). Reduced major axis (RMA) regression was used to calculate the scaling exponent (b) for each regression because surface area was a random variable potentially estimated with error (Quinn and Keough, 2002). The scaling exponent for each treatment was tested against the null hypothesis that b = 1 (isometry) using a two-tailed Student’s t-test (Sokal and Rohlf, 1981). Standard errors for the regression slopes were taken from ordinary least squares (OLS) analyses, because the variance of OLS and RMA estimators are identical to the third significant digit (McCardle, 1988). Because RMA ANCOVA techniques are not available, OLS ANCOVA was used to test for the main and interactive effects (Sokal and Rohlf, 1981). Assumptions for parametric testing were met by graphical inspection of residuals (Quinn and Keough, 2002). The hypothesis that young and old fragments regenerated new tissue-covered branch tips with equal frequency was tested using a 2 x 2 contingency table. A t-test was used to determine whether Symbiodinium densities (cells per square centimeter) and protein concentrations (micrograms per square centimeter) differed between the two age classes. All statistical analyses were completed using JMP 5.01 for Macintosh.
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Results
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Coral fragments from both experiments spanned a range of sizes as determined by the availability of suitable coral branches, and because fragments were assigned randomly to each depth, the mean size of fragments varied by treatment. Although the exact age of fragments varied due to this size variation, a relative two-fold difference in physiological age remained consistent between the tissue of young and old fragments. Corals used in the 14-week experiment ranged in initial mean size (surface area) from 7.0 to 8.8 cm2 (Table 1), but these differences in size among age x depth treatment combinations were not significant (F1,77 = 0.30, P > 0.5). During the experiment, two individuals died and the remainder calcified at a rate of 0.79–1.50 mg cm–2 day–1 (Table 1). After 14 weeks, 35 (79.5%) young fragments possessed tissue-covered branch tips, in contrast to 9 (20.5%) old fragments, which is a greater number than chance alone would predict (G = 31.11, df = 1, P < 0.001).
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Table 1 Surface area normalized calcification rates and sizes for fragments of Madracis mirabilis by age and depth treatments
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Calcification scaled isometrically with surface area (b = 1) for all treatments (Table 2), and the slopes of all regressions were homogenous (all factor by covariate terms P > 0.1); thus the main effects could be tested using ANCOVA. Young fragments calcified significantly faster (15%–30%) than old fragments, as shown by the difference in elevation of the regression lines (Fig. 1a, Tables 1 and 3). Therefore, it appears that the effect of age was absolute and independent of size. The effect of depth on calcification also was significant for both age classes (Table 3), with fragments at 9-m depth calcifying 46%–65% faster than fragments at 17-m depth (Table 1). However, the test for ontogenetic plasticity, the age x depth interaction, was not significant (Table 3), and therefore young and old corals expressed a similar response of calcification to depth treatments. The effect of genet and all associated interactions were not significant (Table 3), indicating that genotypes exhibited similar calcification responses to the experimental treatments.
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Table 2 Reduced major axis regression analyses used to estimate scaling relationships between log calcification (mg day–1) and log surface area (cm2) for fragments of Madracis mirabilis by age and depth treatments
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Figure 1. Log calcification rate (mg day–1) versus log surface area (cm2) of young and old fragments of Madracis mirabilis in shallow (9 m) and deep (17 m) environments at Columbus Park, Jamaica. Two experiments of differing durations and start times were completed: (A) the results of the first experiment lasting 14 weeks (6 March–13 June 2004), and (B) the results of the second experiment lasting 3 weeks (13 June–3 July 2004).
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Table 3 Results of a) a three-way analysis of covariance testing the effects of age (fixed), depth (fixed), and genet (random) on calcification rates (log mg day–1) in Madracis mirabilis during the first 14-week experiment, and b) a two-way analysis of covariance testing the fixed effects of age and depth on calcification rates in M. mirabilis during the second 3-week experiment
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Fragments used in the 3-week experiment ranged in initial mean surface area from 5.7 to 6.7 cm2 (Table 1), but this variation was not significant between age x depth treatment combinations (F1,68 = 0.71, P > 0.4). Over a period of 3 weeks, these corals calcified 1.81 to 2.47 mg cm–2 day–1 (Table 1). All fragments survived the transplant experiment, but none extended new tissue over the broken surface of the branch tips. Calcification again scaled isometrically for all treatments (Table 2). Relative to the 14-week experiment, the magnitude of the age effect (i.e., the difference between young and old normalized mean calcification rates) increased by 113% and 230% for corals at the shallow and deep depths, respectively (Table 1). However, the depth effect no longer was significant (Table 3), with corals calcifying at similar rates in shallow and deep environments (Fig. 1b, Table 1). The age x depth interaction for ontogenetic plasticity was not significant (Table 3).
Tissue characteristics did not vary with age in the fragments initially sacrificed from the 3-week experiment. Symbiodinium population densities were similar for both age classes (t = 0.22, df = 22, P = 0.83), with young and old fragments harboring 1.60 ± 0.14 and 1.61 ± 0.14 x 106 cells cm–2 (mean ± SE), respectively. Young fragments contained 153 ± 9 µg protein cm–2 (mean ± SE), which is indistinguishable statistically (t = 0.17, df = 22, P = 0.87) from the 156 ± 11 µg protein cm–2 (mean ± SE) contained by old fragments.
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Discussion
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This study demonstrates that the growth of fragments of the scleractinian coral Madracis mirabilis depends on their origin from within a branch, and suggests that an approximately two-fold difference in physiological age is responsible for the variation in calcification rates. To our knowledge, only two other experimental studies have suggested that polyp position, as a proxy for module age, has biological consequences for scleractinian corals, specifically with respect to reproduction (Kojis and Quinn, 1985) and tissue regeneration (Meesters and Bak, 1995). In addition, the calcification rates of Stylophora pistillata decrease prior to the appearance of tissue mortality, thus indirectly supporting senescence, or the deterioration of physiological function with age (Rinkevich and Loya, 1986). Notably, in Acropora palmata, the ability to regenerate tissue after a lesion decreased exponentially during the first 2–3 years of polyp life (Meesters and Bak, 1995), an age range equivalent to the relative difference in tissue age observed to affect calcification in the present study. Despite the cnidarian potential for cell renewal and exchange through gastrovascular connections between polyps, as demonstrated for hydrozoans (Crowell, 1953, Martínez, 1998, Müller et al., 2004), young polyps of branching scleractinian corals appear to be distinct physiologically from older polyps, exhibiting faster calcification and regeneration rates.
It is well known that calcification rates decline in a gradient from the apices of coral branches (Goreau and Goreau, 1959), with one of the best examples provided by the Caribbean coral Acropora cervicornis. In this acroporid, calcification rates are highest in the distal 10 mm of the branches—which are pale in color and harbor few symbiotic algae—and decline basally along at least 30 mm of the branch (Pearse and Muscatine, 1971). It is generally accepted that such gradients in calcification are driven by the apical translocation of organic compounds from the more distal regions of the branches where population densities of zooxanthellae are high (Fang et al., 1989, Pearse and Muscatine, 1971). Although the differences in growth rates we report here for proximal versus distal portions of branches from Madracis mirabilis appear superficially similar to those reported for other species (e.g., Pearse and Muscatine, 1971), important differences between these studies support our assertions regarding the effects of age on growth.
First, and of greatest importance, is that our study compared growth rates between proximal and distal portions of branches that had been grown independently in the same habitat for 3–14 weeks, and thus each fragment could acclimate individually to the conditions created by experimental manipulation. Thus, any initial gradient in Symbiodinium population density or chlorophyll content along the branches of M. mirabilis that might drive an "Acropora-like" growth gradient (sensu Pearse and Muscatine, 1971) would probably be counteracted by plastic responses to the new environmental conditions (Anthony and Hoegh-Guldberg, 2003a). Second, there is good reason to believe that any linear growth gradient along branches of M. mirabilis is less well developed than that in A. cervicornis, because Symbiodinium population densities statistically do not vary along the branches of M. mirabilis as they do in A. cervicornis (Pearse and Muscatine, 1971). Moreover, the similarity of protein biomass along branches of M. mirabilis (this study) and the likelihood that this species contains only one type of Symbiodinium (Diekmann et al., 2003) rule out these effects as factors confounding the contrast of age that the experiment was designed to establish.
Assuming that the effects of any putative pre-existing gradients along the branches of M. mirabilis were minimized in this study, the results support the assertion that the effect of age on calcification rates was absolute and independent of size, because calcification increased proportionately with surface area for all fragments in both experiments. The deposition of calcium carbonate is a surface area process in scleractinian corals, with calcium being taken up at the seawater-tissue interface and aragonite being deposited at the two-dimensional interface of the aboral ectoderm (Gattuso et al., 1999). Therefore it is not surprising that calcification scaled isometrically for M. mirabilis. Although modular organization theoretically alleviates the surface-to-volume constraints that limit the growth of unitary organisms (Hughes and Cancino, 1985), allometric limitations on resource capture can constrain isometric growth in modular organisms (Kim and Lasker, 1998). Such limitation probably was avoided in the present study by spacing the experimental fragments of M. mirabilis far apart from one another, so that they probably did not engage in interference competition for light or particle flux. In contrast to our fragments, resource capture in naturally occurring aggregates of M. mirabilis likely is allometric because interior polyps of branching aggregates experience decreased light, flow, and particle flux as a result of self-shading (Helmuth et al., 1997; Sebens et al., 1997). Therefore, the observation of isometric scaling of calcification in this study may apply only to individual branches (e.g., recruits, fragments) of M. mirabilis, rather than entire aggregates. Additionally, the thickness of the boundary layer will differ with branch size and could lead to allometry if the mass transfer characteristics of important metabolites are altered, but such effects were not apparent in the present study.
Although young fragments calcified faster than old fragments, there was no interactive effect of age and depth on calcification rates. Factorial analysis of variance commonly has been used to test for the plastic responses of several genotypes in a series of environments (Schlichting, 1986). The goal of this study was to investigate an age x environment interaction, to determine whether plasticity varied ontogenetically. Both young and old fragments in the 14-week experiment increased their calcification rates when transplanted to a shallower depth, whereas all corals in the 3-week experiment calcified similarly at both depths. The response of calcification rates to the shallow depth in only the 14-week experiment may reflect a temporal requirement of at least 3 weeks for full photoacclimation by the symbiotic zooxanthellae (Falkowski and Dubinsky, 1981). Importantly, there was no age-related difference in plasticity, even though a relative age difference of 1 to 2 years was enough to detect a difference in calcification rates between age classes. Although M. mirabilis exhibits genotype x environment effects with respect to morphological traits (Bruno and Edmunds, 1997), calcification rates of genets appear to be independent of the environment (Bruno and Edmunds, 1997; this study), age, and size (this study). The lack of genotype effects in the present study accentuates the importance of age and size in affecting the calcification rates of M. mirabilis and suggests that genets may be exposed to strong selective pressure to maintain similar growth rates (a well-known fitness correlate; Bruno and Edmunds, 1997) in different environments.
The causal basis for the main finding of this study, the putative effect of age on calcification, is unclear. The symbiosis between the coral and dinoflagellate may contribute to this age effect. For example, the symbiont may experience some negative consequence of increasing age, or the communication between the host and symbiont may degrade with age. The lack of studies regarding either of these hypotheses precludes a distinction between the roles played by either partner. However, with respect to the cnidarian host, differences in gastrovascular transport between modules of the young and old fragments of M. mirabilis may have contributed to the observed physiological differences. In support of this hypothesis, variation in gastrovascular pumping (Blackstone, 1996) may mediate age-dependent differences in growth and competitive ability of two hydrozoan species (Van Winkle and Blackstone, 2002). Stony corals are known to transport fluids among polyps through their gastrovascular cavities (Gladfelter, 1983), and the proposed age effect in this study is complicated by the integration of polyps along the distal and proximal portions of coral branches (Soong and Lang, 1992). The position of a polyp within a branch may dictate its calcification rate (Pearse and Muscatine, 1971), thereby influencing the overall morphogenesis of the colonial aggregate. The decreased magnitude of the age effect during the 14-week experiment relative to the 3-week experiment may reflect the gradual adjustment of polyp integration to the new colony morphology (i.e., the fragments). In other words, the polyps of old (proximal) fragments may eventually be "instructed" to calcify at rates commensurate with young (distal) fragments, but the duration of the current study was not sufficient to elicit such a response.
An alternative explanation for the present results relates to senescence of coral tissue (Meesters and Bak, 1995; Rinkevich and Loya, 1986). Previous authors (Meesters and Bak, 1995; Palumbi and Jackson, 1983) have noted that senescence in old, proximal modules of clonal organisms is phylogenetically widespread, and the same phenomenon has been reported in algae (Borowitzka and Larkum, 1976), plants (Leopold, 1961; Watt, 1947), fungi (Holliday, 1969), and several metazoan lineages (Campbell, 1968; Rinkevich et al., 1992; Ryland, 1979; Sabbadin, 1979). These observations suggest that a common, intrinsic cellular process explains modular senescence, even though physiological deterioration of proximal modules may be unrelated to senescence of the genet (Jackson and Coates, 1986). However, physiological impairment is coupled tightly with genotypic senescence in unitary, multicellular organisms and is likely caused by oxidative stress (Hughes and Reynolds, 2005; Sohal et al., 2002). In scleractinian corals, oxidative damage is well-known from studies of its role in the process of bleaching (Downs et al., 2002; Lesser, 1997). It is tempting to suggest that the modules of scleractinian corals cannot escape the somatic aging process observed in unitary animals because senescence likely evolved (Williams, 1957) prior to coloniality in metazoans (Martínez, 2002). Nevertheless, experiments explicitly addressing the oxidative stress hypothesis for senescence in corals are necessary, preferably using individuals whose absolute age can be measured accurately (e.g., sexual recruits).
Polyp senescence is in stark contrast to the observed longevity of some coral colonies in nature (Foster, 1979; Potts et al., 1985; Soong, 1993). Perhaps in these species, selection has favored the use of totipotent interstitial cells for periodic regeneration, but to our knowledge such rapid tissue renewal has been documented only in hydrozoans (Crowell, 1953; Martínez, 1998; Müller et al., 2004), where it may explain why Hydra is exempt from the constraints of senescence (Martínez, 2002). It is worth noting that the documented cases of colony longevity are apparently restricted to corals with a massive or mounding morphology. Such species typically compete for space by growing slowly and defending their position aggressively (Hughes, 1983), and thus they would benefit from polyp regeneration to prevent other sessile taxa from colonizing senescent tissue. In contrast, branching species acquire space through rapid growth and overtopping (Hughes, 1983) and are more ephemeral due to their susceptibility to fragmentation (Highsmith, 1982). Thus, senescence of proximal modules may have restricted the morphology of M. mirabilis and other branching scleractinians, or alternatively, it may be an adaptive feature. Slow tissue regeneration rates at the bases of Acropora palmata branches may facilitate bioerosion and subsequent fragmentation of branches large enough to enhance survivorship (Meesters and Bak, 1995). Likewise, the colonization of branch bases of M. mirabilis by boring sponges and algae (Bruno and Edmunds, 1997) may contribute to the generation of fragments typically larger than 5 cm, which appears to be a threshold size for increased survivorship (Bruno, 1998). The present study provides indirect evidence for this possibility, because very few of the old fragments of M. mirabilis extended new tissue over their broken tips during the 14-week experiment, and filamentous algae frequently settled onto this bare space. In contrast, 80% of the young fragments were able to form new tissue-covered branch tips. Although tissue-covered branch tips clearly are not a requirement for calcification in M. mirabilis, the apparent inability of old fragments to extend tissue over broken tips suggests that the age of tissue is an intrinsic influence on the apical growth observed in this species. In support of this hypothesis, the skeletal growth and form of Pocillopora damicornis branch tips are thought to be controlled by an intrinsic cycle in the overlying tissues (LeTissier, 1988).
In summary, the results of our study contrast markedly with the traditional assumption that age does not matter for scleractinian corals. In Madracis mirabilis, the age of coral tissue appears to have considerable biological importance, and the same is probably true for other coral species that have developmental gradients associated with a branching morphology (Soong and Lang, 1992). Together, the senescence of proximal modules reported in many other clonal organisms and the physiological patterns presented here may be a general feature of taxa sharing this body plan.
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Acknowledgments
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Special thanks to the staff at the Discovery Bay Marine Laboratory for facilitating the completion of this research, and to the Northeastern University Three Seas program for providing generous field and laboratory support. R.E. in particular would like to thank C. Buck, M. R. Murray, and students of the Three Seas XX program for field assistance. R. C. Carpenter, S. R. Dudgeon, B. Helmuth, and three anonymous reviewers improved earlier versions of this manuscript. We acknowledge additional support from PADI Project Aware, CSUN University Corporation (#620200), and Associated Students to R.E., and the Sea Grant Program of the University of Puerto Rico (#R-101-2-02) and an NSF- LTREB (DEB 03443570) to P.J.E. This work was submitted in partial fulfillment of the M.S. degree to R.E. at California State University, Northridge. This is contribution 716 of the Discovery Bay Marine Laboratory and contribution 138 of the CSUN Marine Biology Program.
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Footnotes
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Received 21 April 2006; accepted 16 October 2006.
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Literature Cited
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Anthony, K. R. N., and O. Hoegh-Guldberg. 2003a. Kinetics of photoacclimation in corals. Oecologia 134:23–31.[ISI][Medline]
Anthony, K. R. N., and O. Hoegh-Guldberg. 2003b. Variation in coral photosynthesis, respiration and growth characteristics in contrasting light microhabitats: an analogue to plants in forest gaps and understoreys? Funct. Ecol. 17:246–259.
Arnqvist, G., and F. Johansson. 1998. Ontogenetic reaction norms of predator-induced defensive morphology in dragonfly larvae. Ecology 79:1847–1858.
Barnes, D. J. 1973. Growth in colonial scleractinians. Bull. Mar. Sci. 23:280–298.
Blackstone, N. W. 1996. Gastrovascular flow and colony development in two colonial hydroids. Biol. Bull. 190:56–68.[Abstract]
Boardman, R. S., and A. H. Cheetham. 1973. Degrees of colony dominance in stenolaemate and gymnolaemate bryozoa. Pp. 121–220 in Animal Colonies: Development and Function Through Time, R. S. Boardman, A. H. Cheetham, and W. A. Oliver, eds. Dowden, Hutchinson & Ross, Stroudsburg, PA.
Borowitzka, M. A., and A. W. D. Larkum. 1976. Calcification in the green alga Halimeda. J. Exp. Bot. 27:864–878.[Abstract/Free Full Text]
Bradford, M. M. 1976. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248–254.[ISI][Medline]
Bruno, J. F. 1998. Fragmentation in Madracis mirabilis (Duchassaing and Michelotti): How common is size-specific fragmentation survivorship in corals? J. Exp. Mar. Biol. Ecol. 230:169–181.
Bruno, J. F., and P. J. Edmunds. 1997. Clonal variation for phenotypic plasticity in the coral Madracis mirabilis. Ecology 78:2177–2190.
Campbell, R. D. 1968. Colony growth and pattern in the two-tentacled hydroid, Proboscidactyla flavicirrata. Biol. Bull. 135:96–104.
Crowell, S. 1953. The regression-replacement cycle of hydranths of Obelia and Campanularia. Physiol. Zool. 26:319–327.
Davies, P. S. 1989. Short-term growth measurements of corals using an accurate buoyant weight technique. Mar. Biol. 101:389–395.
Dennison, W. C., and D. J. Barnes. 1988. Effect of water motion on coral photosynthesis and calcification. J. Exp. Mar. Biol. Ecol. 115:62–77.
Diekmann, O. E., J. L. Olsen, W. T. Stam, and R. P. M. Bak. 2003. Genetic variation within Symbiodinium clade B from the coral genus Madracis in the Caribbean (Netherlands Antilles). Coral Reefs 22:29–33.
Downs, C. A., J. E. Fauth, J. C. Halas, P. Dustan, J. Bemiss, and C. M. Woodley. 2002. Oxidative stress and seasonal coral bleaching. Free Radic. Biol. Med. 33:533–543.[ISI][Medline]
Falkowski, P. G., and Z. Dubinsky. 1981. Light-shade adaptation of Stylophora pistillata, a hermatypic coral from the gulf of Eilat. Nature 289:172–174.
Fang, L.-S., Y.-W. J. Chen, and C.-S. Chen. 1989. Why does the white tip of stony coral grow so fast without zooxanthellae? Mar. Biol. 103:359–363.
Foster, A. B. 1979. Phenotypic plasticity in the reef corals Montastraea annularis (Ellis & Solander) and Siderastrea siderea (Ellis & Solander). J. Exp. Mar. Biol. Ecol. 39:25–54.
Gattuso, J.-P., D. Allemand, and M. Frankignoulle. 1999. Photosynthesis and calcification at cellular, organismal and community levels in coral reefs: a review on interactions and control by carbonate chemistry. Am. Zool. 39:160–183.
Gladfelter, E. H. 1983. Circulation of fluids in the gastrovascular system of the reef coral Acropora cervicornis. Biol. Bull. 165:619–636.
Goreau, T. F., and N. I. F. Goreau. 1959. The physiology of skeleton formation in corals. II. Calcium deposition by hermatypic corals under various conditions in the reef. Biol. Bull. 117:239–250.[Free Full Text]
Helmuth, B. S. T., B. E. H. Timmerman, and K. P. Sebens. 1997. Interplay of host morphology and symbiont microhabitat in coral aggregations. Mar. Biol. 130:1–10.
Highsmith, R. C. 1982. Reproduction by fragmentation in corals. Mar. Ecol. Prog. Ser. 7:207–226.
Holliday, R. 1969. Errors in protein synthesis and clonal senescence in fungi. Nature 221:1224–1228.[Medline]
Hughes, K. A., and R. M. Reynolds. 2005. Evolutionary and mechanistic theories of aging. Annu. Rev. Entomol. 50:421–445.[ISI][Medline]
Hughes, R. N. 1983. Evolutionary ecology of colonial-reef organisms, with particular reference to corals. Biol. J. Linn. Soc. 20:39–58.
Hughes, R. N., and J. M. Cancino. 1985. An ecological overview of cloning in Metazoa. Pp. 153–186 in Population Biology and Evolution of Clonal Organisms, J. B. C. Jackson, L. W. Buss, and R. E. Cook, eds. Yale University Press, New Haven.
Hughes, T. P., and J. B. C. Jackson. 1980. Do corals lie about their age? Some demographic consequences of partial mortality, fission, and fusion. Science 209:713–715.[Abstract/Free Full Text]
Hughes, T. P., and J. B. C. Jackson. 1985. Population dynamics and life histories of foliaceous corals. Ecol. Monogr. 55:141–166.[ISI]
Huston, M. 1985. Variation in coral growth rates with depth at Discovery Bay, Jamaica. Coral Reefs 4:19–25.
Jackson, J. B. C., and A. G. Coates. 1986. Life cycles and evolution of clonal (modular) animals. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 313:7–22.
Jackson, J. B. C., L. W. Buss, and R. E. Cook, eds. 1985. Population Biology and Evolution of Clonal Organisms. Yale University Press, New Haven.
Johannes, R. E., and W. J. Wiebe. 1970. Method for determination of coral tissue biomass and composition. Limnol. Oceanogr. 15:822–824.
Kaandorp, J. A. 1999. Morphological analysis of growth forms of branching sessile organisms along environmental gradients. Mar. Biol. 134:295–306.
Kim, K., and H. R. Lasker. 1998. Allometry of resource capture in colonial cnidarians and constraints of allometric growth. Funct. Ecol. 12:646–654.
Kojis, B. L., and N. J. Quinn. 1985. Puberty in Goniastrea favulus age or size limited? Pp. 289–293 in Proc. 5th Int. Coral Reef Congr., Tahiti.
Leopold, A. C. 1961. Senescence in plant development. Science 134:1727–1732.[Free Full Text]
Lesser, M. P. 1997. Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16:187–192.[ISI]
LeTissier, M. D. A. 1988. The growth and formation of branch tips of Pocillopora damicornis (Linnaeus). J. Exp. Mar. Biol. Ecol. 124:115–131.
Marsh, J. A. 1970. Primary productivity of reef-building calcareous red algae. Ecology 51:255–263.
Martínez, D. E. 1998. Mortality patterns suggest lack of senescence in hydra. Exp. Gerontol. 33:217–225.[ISI][Medline]
Martínez, D. E. 2002. Senescence and rejuvenation in asexual metazoans. Pp. 115–140 in Progress in Asexual Reproduction, R. N. Hughes, ed. John Wiley, Chichester.
McCardle, B. H. 1988. The structural relationship: regression in biology. Can. J. Zool. 66:2329–2339.
Meesters, E. H., and R. P. M. Bak. 1995. Age-related deterioration of a physiological function in the branching coral Acropora palmata. Mar. Ecol. Prog. Ser. 121:203–209.
Müller, W. A., R. Teo, and U. Frank. 2004. Totipotent migratory stem cells in a hydroid. Dev. Biol. 275:215–224.[ISI][Medline]
Ostrowski, M.-F., P. Jarne, O. Berticat, and P. David. 2002. Ontogonetic reaction norm for binary traits: the timing of phallus development in the snail Bulinus truncatus. Heredity 88:342–348.
Palumbi, S. R., and J. B. C. Jackson. 1983. Aging in modular organisms: ecology of zooid senescence in Steginoporella sp. (Bryozoa: Cheilostomata). Biol. Bull. 164:267–278.[Abstract/Free Full Text]
Pearse, V. B., and L. Muscatine. 1971. Role of symbiotic algae (zooxanthellae) in coral calcification. Biol. Bull. 141:350–363.[Abstract/Free Full Text]
Pigliucci, M., and C. D. Schlichting. 1995. Ontogonetic reaction norms in Lobelia siphlitica (Lobeliaceae): response to shading. Ecology 76:2134–2144.
Potts, D. C., T. J. Done, P. J. Isdale, and D. A. Fisk. 1985. Dominance of a coral community by the genus Porites (Scleractinia). Mar. Ecol. Prog. Ser. 23:79–84.
Quinn, G. P., and M. J. Keough. 2002. Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge.
Rinkevich, B., and Y. Loya. 1986. Senescence and dying signals in a reef building coral. Experientia 42:320–322.
Rinkevich, B., R. J. Lauzon, B. W. M. Brown, and I. L. Weissman. 1992. Evidence for a programmed life span in a colonial protochordate. Proc. Natl. Acad. Sci. USA 89:3546–3550.[Abstract/Free Full Text]
Ryland, J. S. 1979. Structural and physiological aspects of coloniality in Bryozoa. Pp. 211–242 in Biology and Systematics of Colonial Organisms, G. Larwood and B. R. Rosen, eds. Academic Press, New York.
Sabbadin, A. 1979. Colonial structure and genetic patterns in ascidians. Pp. 433–444 in Biology and Systematics of Colonial Organisms, G. Larwood and B. R. Rosen, eds. Academic Press, New York.
Schlichting, C. D. 1986. The evolution of phenotypic plasticity in plants. Annu. Rev. Ecol. Syst. 17:667–693.[ISI]
Schlichting, C. D., and M. Pigliucci. 1998. Phenotypic Evolution: A Reaction Norm Perspective. Sinauer Associates, Sunderland, MA.
Schmidt-Nielsen, K. 1984. Scaling: Why is Animal Size So Important? Cambridge University Press, Cambridge.
Sebens, K. P., J. Witting, and B. Helmuth. 1997. Effects of water flow and branch spacing on particle capture by the reef coral Madracis mirabilis (Duchassaing and Michelotti). J. Exp. Mar. Biol. Ecol. 211:1–28.
Sohal, R. S., R. J. Mockett, and W. C. Orr. 2002. Mechanisms of aging: an appraisal of the oxidative stress hypothesis. Free Radic. Biol. Med. 33:575–586.[ISI][Medline]
Sokal, R. R., and F. J. Rohlf. 1981. Biometry. W. H. Freeman, New York.
Soong, K. 1993. Colony size as a species character in massive reef corals. Coral Reefs 12:77–83.
Soong, K., and J. C. Lang. 1992. Reproductive integration in reef corals. Biol. Bull. 183:418–431.[Abstract]
Van Winkle, D. H., and N. W. Blackstone. 2002. Variation in growth and competitive ability between sexually and clonally produced hydroids. Biol. Bull. 202:156–165.[Abstract/Free Full Text]
Watt, A. S. 1947. Contribution to the ecology of bracken. IV. The structure of the community. New Phytol. 46:97–121.
Williams, G. C. 1957. Pleiotropy, natural selection, and the evolution of senescence. Evolution 11:398–411.[ISI]
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Abstract
Introduction
