Biol. Bull. 206: 61-64. (April 2004)
© 2004 Marine Biological Laboratory
Size-Dependent Differences in the Photophysiology of the Reef Coral Porites astreoides
Peter J. Edmunds1,* and
Ruth D. Gates2
1 Department of Biology, California State University, 18111 Nordhoff Street, Northridge, California 91330-8303
2 The Hawai’i Institute of Marine Biology, University of Hawaii Manoa, P.O. Box 1346, Kaneohe, Hawai’i 96744
* To whom correspondence should be addressed. E-mail: peter.edmunds{at}csun.edu
The recruitment and survival of juvenile corals is central to the maintenance of coral reef communities and the repopulation of denuded reef substrata. Although it is widely accepted that the mortality of scleractinians is inversely proportional to size, the biotic and abiotic factors that drive this trend remain unclear. Here we measure the mortality of corals on the reefs of St. John (U.S. Virgin Islands) to demonstrate that small corals are more likely to die than their larger counterparts, and we explore whether the photophysiological performance of juveniles in two size classes can provide some insight into why smaller corals are so vulnerable. To evaluate photophysiological performance, we examined chlorophyll fluorescence in two size classes (mean diameters 15 mm and 45 mm) of juvenile colonies of Porites astreoides exposed for short periods to ambient and elevated temperatures. Our results show that the photophysiology of these size classes differs under ambient conditions, with dark-adapted quantum yield (Fv/Fm) being significantly higher in smaller compared to bigger juveniles. As expected, the photophysiology of both size classes is negatively impacted by thermal stress, and although size-related trends are evident in our data, the interaction between size and temperature is not statistically significant. Thus, while there is size dependency in the photophysiological performance of juvenile colonies of P. astreoides, the link between this aspect of scleractinian biology and the higher mortality of small juvenile corals in the face of high thermal stress remains unclear.
As a context for this study, we draw on mortality data for different size classes of corals at five sites on the shallow reefs of St. John. Between 1996 and 2002, the annual mortality of all juvenile corals <20 mm in diameter was 2-fold higher than for corals of 21–40 mm in diameter (Fig. 1), and in genera such as Porites, the smallest juveniles experienced a 4.3-fold higher mortality rate than their larger counterparts (Fig. 1). Using these data as a rationale, we compared the photophysiology of two size classes of juvenile colonies of Porites astreoides in January 2003. Corals were collected from 6–8 m depth on the west fore reef at Discovery Bay, Jamaica, to represent two significantly different size classes (t = 17.960, df = 26, P < 0.001) with mean diameters of 15 ± 2 mm and 45 ± 6 mm, hereafter described as sizes I and II, respectively. These corals were exposed to ambient (
27 °C) and elevated temperatures (31.6 °C) for 6 h in the light followed by 2 h in the dark, and the impact of these environmental conditions was evaluated by using pulse amplitude modulation (PAM) fluorometry to measure each coral’s photophysiological performance at the end of the 8-h incubation (Fig. 2). The duration of these experiments reflects previously published studies that show an 8-h exposure to high temperature to be sufficient to elicit a photophysiological response in reef corals (1, 2). Throughout the incubations the corals were inspected for signs of stress, such as the production of mucus or the loss of color, but no such responses were observed.
View larger version (34K):
[in this window]
[in a new window]
|
Figure 1. The mortality of juvenile corals at 5–6 m depth along the south coast of St. John, U.S. Virgin Islands. Juvenile corals at five sites were identified to genus, sized (diameter), and tagged. To determine mortality, each coral was relocated a year later and scored as dead or alive (12). Sample sizes and taxonomic composition of the corals varied each year, but most belonged to the genera Porites, Agaricia, Siderastrea, and Favia. Mortality was calculated for Porites spp. (including P. astreoides) and for juveniles pooled by taxon (11 genera), and was determined separately for corals  20 mm in diameter (small) and between 21 and 40 mm in diameter (big). Mean annual percentage mortality is displayed (±SE; n = 6 years), and differed significantly between small and big juveniles for both Porites (t = 2.306, df = 10, P = 0.044) and the pooled taxa (t = 3.076, df = 10, P = 0.012; statistical analyses were carried out with arcsine-transformed percentage mortality). Porites mortality was calculated using 58 corals between 1996 and 1997, 46 between 1997 and 1998, 28 between 1998 and 1999, 5 between 1999 and 2000, 17 between 2000 and 2001, and 37 between 2001 and 2002; the sample sizes for all juvenile corals were 395, 187, 105, 28, 57, and 92, respectively.
|
|
View larger version (19K):
[in this window]
[in a new window]
|
Figure 2. A comparison of the photophysiology of two size classes of juvenile colonies of Porites astreoides. Temperature treatments were established in 10-1 tanks placed in an air-conditioned room where they received sunlight from an adjacent window [119 ± 5 µmol photons · s–1 · m–2 (mean ± SD, n = 2), recorded with a spherical Li-Cor sensor at noon]. The tanks were aerated and filled with fresh seawater daily, and maintained at 26.1 ± 0.4 °C (mean ± SE, n = 6, ambient treatment; on reef 27 °C) and 31.6 ± 0.3 °C (mean ± SE, n = 6, elevated treatment). A randomized block experimental design was used to test for the effects of size and temperature, where each block corresponded to one day of experiments with one coral of each size class allocated to each treatment. Incubations began at noon, and after 6 h the tanks were covered and the corals dark-adapted for at least 2 h prior to assessing their photophysiology. A pulse amplitude modulation fluorometer (PAM-210, Walz GmbH) was used to quantify chlorophyll fluorescence in the dark-adapted state and at each of 11 standard light levels. Fluorescence measurements were obtained by positioning the sensor just above the tissue on the upper surface of a coral colony sitting in seawater at the appropriate incubation temperature. Two sets of recordings were obtained from different positions on each coral, and the average was used as a statistical replicate. Minimal and maximal fluorescences for dark-adapted corals (Fo and Fm, respectively) were measured, and the results displayed as PSII quantum yield [Fv/Fm = (Fm – Fo)/Fm; mean ± SE shown (n = 7)]. Fv/Fm differed significantly between size classes and treatments, but there was no statistical interaction between the two (Table 1).
|
|
The analysis of the photosynthetic performance of P. astreoides by means of PAM fluorometry revealed that the dark-adapted (maximal) quantum yield of photosystem (PS) II (calculated as Fv/Fm which is defined in Fig. 2), differed significantly between size classes and treatments, but that the interaction between size and treatment was not significant (Table 1, Fig. 2). At ambient temperatures, Fv/Fm was 3% to 6% higher in size I versus size II juvenile corals, and exposure to the elevated temperature reduced Fv/Fm by 10% in size I and 12% in size II juveniles. Because Fv/Fm measures the efficiency of exciting electrons with light energy in PSII, a decline in Fv/Fm reflects a reduction in the efficiency of the photochemical pathways culminating in carbon fixation (3). Thus, our results show that for P. astreoides, the photochemical pathways of smaller juveniles are slightly more efficient than those in their larger counterparts, but that their photophysiology is equally impaired by short exposures to elevated temperatures, at least in corals collected and analyzed in the winter.
View this table:
[in this window]
[in a new window]
|
Table 1 Results of a three-way randomized block ANOVA comparing dark-adapted quantum yield of PSII (Fv/Fm) between size classes (fixed factor I) and treatments (fixed factor II), with the block being the day that the experiment was completed
|
|
To explore these size-dependent differences in photophysiology in more detail, we examined nonphotosynthetic quenching in the same corals by qualitatively comparing rapid light curves. Nonphotosynthetic quenching (qN) is a measure of excess light energy absorbed by the PSII antenna system and dissipated as heat through photoprotective mechanisms such as xanthophyll cycling (3, 4); qN is calculated from the relationship qN = (Fm – Fm')/(Fm – Fo), where Fm and Fo are defined in Figure 2, and Fm' is the maximal fluorescence in the light. We selected qN because it is more sensitive to thermal stress than variable fluorescence [Fv (5)], and therefore is likely to display more subtle responses to high temperature than Fv/Fm. As expected, qN appears sensitive to a number of factors; however, most relevant to the current discussion are the differences in response of qN for sizes I and II juvenile corals under the same light and temperature conditions (Fig. 3). For example, when corals are exposed to elevated temperature at <120 µmol photons · s–1 · m–2, qN is more severely depressed in size I corals than in their larger counterparts (size II). Interestingly, at higher light intensities of 
367 µmol photons · s–1 · m–2, this trend is reversed and the size II juveniles incubated at the higher temperature exhibit a greater depression in qN than do size I corals. Although qualitative, the nuances in our results provide some evidence that the photophysiology of two size classes of juveniles of P. astreoides respond differently to the combination of light and temperature used in our experiments. The most parsimonious conclusion is that the two size classes are functionally different in photophysiology (as described by Fv/Fm and qN); it remains to be demonstrated whether these differences are reflected in their tolerance to thermal stress and in their inverse size-dependent mortality. Perhaps the smallest corals die faster than the bigger corals simply because they are so easily overwhelmed (and killed completely) by sources of mortality other than thermal stress, for example sedimentation or predation (6).
View larger version (20K):
[in this window]
[in a new window]
|
Figure 3. Quenching analyses for size I and size II juvenile corals exposed to ambient and elevated temperature treatments. Measurements were obtained using chlorophyll fluorescence after exposure to each of 11 irradiances for 1 min in the software-driven protocol supplied by the manufacturer (Run 9, Walz GmbH). Results are displayed for nonphotosynthetic quenching (qN) (mean ± SE, n = 7 for each datum) and allow for a qualitative comparison of relative photosynthetic performance between size classes and treatments. One important limitation of this analysis is that photosynthetic equilibrium is probably not achieved within the 1-min irradiance exposures employed.
|
|
The size-dependent differences in dark-adapted yield (Fig. 2) under ambient conditions likely reflect the functional implications of other well-known aspects of coral biology. For example, conspecifics belonging to different size classes may harbor distinct "types" of symbiotic zooxanthellae (7), each with the physiological characteristics and functional limits most suited to the ontogenetic rigors facing corals of a particular size. Alternatively, the symbionts harbored by size I and size II juvenile corals might be identical, but the communication between the symbiotic partners might be tailored to meet the unique demands of their specific developmental stage, such as the rapid growth necessary for small juveniles to escape the risks of overgrowth and predation (8). Or perhaps allometric scaling of biological traits (9) mediates the differences in photophysiology. For example, size-dependent changes in coral tissue biomass and thickness (9) could create variable shading of zooxanthellae through behavioral responses (10), and rapid protein metabolism in fast-growing small corals could reduce the nitrogen limitation of the symbiotic algae, thereby enhancing the efficiency of photochemical conversion (11). Regardless of the mechanisms underlying our results, we believe that further investigation of size-dependent variation in juvenile corals is likely to be valuable in understanding the environmental thresholds and biology of these complex symbiotic organisms.
 |
Acknowledgments
|
|---|
This research was facilitated by S. Genovese and the East/West Marine Biology Program of Northeastern University, and is dedicated to Mr. Brown, whose tireless spirit and hard work has done much to support our research in Jamaica for the last two decades. We thank R. C. Carpenter and J. Kübler for comments that improved earlier drafts of this paper. Funding was provided in part by the Sea Grant Program of the University of Puerto Rico (grant #R-101-2-02) and the Reef Assessment Program of the Virgin Islands National Park (both to PJE). This is contribution number 119 of the CSUN Marine Biology Program, 677 of the Discovery Bay Marine Laboratory and 1176 of the Hawai’i Institute of Marine Biology.
|
Footnotes
|
|---|
Received 10 October 2003; accepted 12 January 2004.
|
Literature Cited
|
|---|
 TOP
 Literature Cited
|
|---|
Jones, R. J., O. Hoegh-Guldberg, A. W. D. Larkum, and U. Shreiber. 1998. Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant Cell Environment 21: 1219–1230.
Warner, M. E., W. K. Fitt, and G. W. Schmidt. 1999. Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc. Natl. Acad. Sci. USA 96: 8007–8012.[Abstract/Free Full Text]
Maxwell, K., and G. N. Johnson. 2000. Chlorophyll fluorescence—a practical guide. J. Exp. Botany 51: 659–668.[Abstract/Free Full Text]
Brown, B. E., I. Ambarsari, M. E. Warner, W. K. Fitt, R. P. Dunne, S. W. Gibbs, and D. G. Cummings. 1999. Diurnal changes in photochemical efficiency and xanthophylls concentrations in shallow water reef corals: evidence of photoinhibition and photoprotection. Coral Reefs 18: 99–105.
Shreiber, U., U. Schliwa, and W. Bilger. 1986. Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynthesis Research 10: 51–62.
Hughes, T. P., and J. B. C. Jackson. 1985. Population dynamics and life histories of foliaceous corals. Ecol. Monogr. 55: 141–166.[ISI]
Coffroth, M. A., S. R. Santos, and T. L. Goulet. 2001. Early ontogenetic expression of specificity in a cnidarian-algal symbiosis. Mar. Ecol. Prog. Ser. 222: 85–96.
Jackson, J. B. C. 1977. Competition on marine hard substrata: the adaptive significance of solitary and colonial strategies. Am. Nat. 980: 743–767.
Vollmer, S. V., and P. J. Edmunds. 2000. Allometric scaling in small colonies of the scleractinian coral Siderastrea siderea (Ellis and Solander). Biol. Bull. 199: 21–28.[Abstract]
Brown, B. E., C. A. Downs, R. P. Dunne, and S. W. Gibb. 2002. Preliminary evidence for tissue retraction as a factor in photoprotection of corals incapable of xanthophyll cycling. J. Exp. Mar. Biol. Ecol. 277: 129–144.
Falkowski, P. G., Z. Dubinsky, L. Muscatine, and L. McCloskey. 1993. Population control in symbiotic corals. Bioscience 43: 606–611.[ISI]
Edmunds, P. J. 2000. Patterns in the distribution of juvenile corals and coral reef community structure in St. John, US Virgin Islands. Mar. Ecol. Prog. Ser. 202: 113–124.
