- Email: [email protected]
Morphological variation in the oral disc of the scleractinian coral Favia speciosa (Dana) at Indonesia
Computational Biology and Chemistry 32 (2008) 345–348
Contents lists available at ScienceDirect
Computational Biology and Chemistry journal homepage: www.elsevier.com/locate/compbiolchem
Research Article
Morphological variation in the oral disc of the scleractinian coral Favia speciosa (Dana) at Indonesia Tamir Caras a , Ami Bachar b , Zohar Pasternak c,∗ a
Department of Geography, Canterbury Christ Church University, North Holmes Road, Canterbury, Kent CT1 1QU, UK Department of Microsensors, Max Planck Institute for Marine Microbiology, Celsiustraße 1, Bremen 28359, Germany c Institute of Systems and Robotics, Department of Electrical and Computer Engineering, University of Coimbra, Coimbra 3030-290, Portugal b
a r t i c l e
i n f o
Article history: Received 9 June 2008 Accepted 22 June 2008 Keywords: Coral morphology Intraspecific variation Sedimentation Depth Autotrophy Heterotrophy
a b s t r a c t Photographic analysis was used to examine morphological differences in the oral disc of n = 1196 living polyps of Favia speciosa Dana (1846) sampled from four sites in the Wakatobi Marine National Park, Indonesia. Although oral disc size attributes differed significantly between the study sites, the geographic difference accounted for only a small fraction of the morphological variation and did not show a clear pattern of correspondence to sedimentation rates. A much higher fraction of the morphological variation was attributed to depth and so to incident light: oral discs grew significantly larger with increasing depth. These results suggest that for F. speciosa corals at Wakatobi, oral disc size may be optimised for heterotrophic nutrition under low light conditions, and photosynthesis in conditions where light is not limiting. Furthermore, the driving force for this phenotypic plasticity is more likely to be depth than sedimentation rate. © 2008 Elsevier Ltd. All rights reserved.
1. Introduction Intra-specific morphological variation is a pervasive feature in ecology, which can be attributed to genetic differentiation, phenotypic plasticity or a combination of both and is often environmentally correlated (Bradshaw, 1965; Pigliucci, 1996). Adaptive phenotypic plasticity, the differential expression of one genotype under varying environmental conditions, is a mechanism through which multi-cellular organisms can cope with changing environments when the scale of the temporal and/or spatial variability is smaller than the organism’s lifespan and/or dispersal range, respectively (Bradshaw, 1965; Foster, 1979). Two environmental factors are often considered as main driving forces of plasticity in coral morphology: ambient light level (McCloskey and Muscatine, 1984; Bosscher and Meesters, 1992) and sedimentation rate (Lasker, 1980; Dodge, 1982); this is because substantive growth of scleractinian reef corals depends primarily on high light availability for their symbiotic unicellular algae, the zooxanthellae (Barnes and Chalker, 1990; Muscatine, 1990). Increased depth, frequent re-suspension events (Larcombe et al., 1995), anthropogenic hypersedimentation (Todd et al., 2001) and increased concentrations of nutrients (Airoldi, 2003) may all result in higher attenuation and/or
∗ Corresponding author. Tel.: +351 239 796323; fax: +351 239 406672. E-mail address: [email protected] (Z. Pasternak). 1476-9271/$ – see front matter © 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.compbiolchem.2008.06.003
absorption of light, reducing light levels available to the coral (Kirk, 1994) and subsequent photosynthetic rates (Falkowski et al., 1990). In addition to autotrophy, corals are also heterotrophs and feed on a range of food types (e.g., zooplankton, Porter, 1974; bacteria, Bak et al., 1998; sediment, Stafford-Smith and Ormond, 1992). Thus, in deep or turbid waters where the rate of photosynthesis is compromised by low light levels, heterotrophy may be favoured (Tomascik and Sander, 1985; Ayling and Ayling, 1991; Anthony, 2000; Fabricius and Dommisse, 2000). Crabbe and Smith (2006) found evidence for such trophic plasticity by examining density and size of Galaxea fascicularis polyps at the Wakatobi National Marine Park, Indonesia, while Todd et al. (2001) discovered the same in Favia speciosa colonies at Singapore. The aim of the present work was to test the hypothesis that as depth and/or sedimentation rates increase, oral disc size increases in order to facilitate a trophic ‘shift’ from autotrophy to heterotrophy. To that end, the morphological variation of polyps from F. speciosa colonies were studied at Wakatobi located in different depths and exposed to different sedimentation rates. 2. Materials and Methods Four reef sites were studied at the Wakatobi National Marine Park, south-east Sulawesi, Indonesia (Table 1; for map locations see Fig. 1 of Crabbe and Smith, 2005): (1) Sampela, a shallow (maximal depth 12 m), slow sloping reef in close proximity to human
346
T. Caras et al. / Computational Biology and Chemistry 32 (2008) 345–348
Table 1 Environmental data and sampling scheme at the four reef sites (mean ± S.D. where applicable) Reef sites
Sampela
Mid-channel
Pak-kasim’s
Kaledupa
Colony depth (m) Estimated visibility (m) Sedimentation rate (g dry weight m−2 d−1 ) No. of colonies sampled No. of polyps sampled
7.8 ± 1.2 4–6 20.16 ± 1.71 7 260
15.2 ± 4.6 8–10 (no data) 8 316
14.2 ± 3.4 18–22 7.54 ± 0.76 6 255
12.9 ± 3.1 20–25 5.35 ± 0.68 10 365
Visibility was estimated using Secchi disc. Sedimentation rates are from Crabbe and Smith (2005).
of 10 cm × 10 cm was used for scale standardization. Images were computerized into MapInfo 5 (MapInfo, USA). Fully budded, nonfissioned polyps (i.e., completely isolated from their neighboring polyps and possessing complete walls and oral discs) within the 10 cm × 10 cm square were measured for oral disc area, oral disc circumference and oral disc maximum diameter (Fig. 1). These measurements were repeated a second time for a smaller, 5 cm × 5 cm square at the centre of each large 10 cm × 10 cm square. The measured oral disc size characters differed significantly between the large and small squares, suggesting that in the larger area, the colony’s curvature is distorting the measurements; as a result, only polyps in the smaller area were used in this study, thus minimizing the effect of colony curvature. Each character was checked for normality and homogeneity of variance, and was then tested for differences between colonies and between sites using ANOVA and post hoc Tukey tests (Table 2). As there is no link between any colonies on one reef to any colony on another reef, a nested ANOVA design was used: colonies were nested within sites and oral disc measurements were nested within colonies; this method allowed testing whether the variability in oral disc characteristics stems from differences between colonies or from differences between geographical reef sites. One characteristic, “Number of polyps”, was not nested, as there was only one statistic for each colony.
Fig. 1. Measured oral disc characters of Favia speciosa. (A) area; (B) circumference; (C) maximum diameter.
3. Results and Discussion habitation; it is a heavily used reef experiencing high sedimentation rates. (2) Mid-channel reef, a steep wall located at the centre of the channel between Sampela and Hoga Islands and characterised by strong currents. (3) Pak-Kasim’s reef, a steep wall with low sedimentation rate. (4) Kaledupa, an intact wall reef experiencing very little human pressure and a low sedimentation rate. The coral species studied was F. speciosa Dana (1846), possessing a high coral cover at the Wakatobi region. F. speciosa is widespread from the shallows to depths of 20 m, forming large (diameter > 30 cm) colonies with bi-coloured polyps, brown on the outside and green on the inside. Six to 10 (see Table 1) coral colonies were randomly selected, identified and photographed with a digital camera (Sony Cyber-shot DSC-P72). The camera was positioned perpendicularly to the coral surface and a slate frame
The three polyp size characters, polyp area, oral disc circumference and oral disc maximum diameter, differed significantly between sites and between colonies. When comparing the oral disc characters between sites (Fig. 2), the differences were small but statistically significant: both oral disc area and circumference were smallest at Sampela, larger at Kaledupa and Pak-kasim’s and larger still at the mid-channel ridge. At Sampela, where sedimentation rate is highest, oral disc diameter was significantly smaller than at the other reefs (where the sedimentation rates are significantly lower), while the number of polyps per cm2 did not differ significantly between the reefs. When comparing the oral disc characters between colonies, the differences were statistically significant (Table 2). The partial eta squared (H2 ) values indicate
Table 2 ANOVA results of the four characters measured Character
Effect
df
F
Significance
Partial H2
Oral disc area
Site Colony
3 30
21.2 15.6
P < 0.001 P < 0.001
0.06 0.32
Oral disc circumference
Site Colony
3 30
19.7 14.7
P < 0.001 P < 0.001
0.06 0.31
Oral disc maximum diameter
Site Colony
3 30
11.2 12.2
P < 0.001 P < 0.001
0.03 0.27
No. of polyps
Site
P = 0.646
–
3
0.56
df (degrees of freedom) equals the number of samples minus one (n − 1); ‘site effect’ is testing whether the character differs between the four sites, ‘colony effect’ is testing whether the character differs between the 31 colonies. F is the test statistic used to determine the statistical significance (P), a value of P < 0.05 means differences between samples are not likely to have happened by chance. Partial Eta-squared (H2 ) is comparable to R2 in correlation/regression analysis, denoting the proportion of variance explained by the model.
T. Caras et al. / Computational Biology and Chemistry 32 (2008) 345–348
Fig. 2. Oral disc characters (mean ± S.D.) and number of polyps of F. speciosa at the different sites. Units of the Y axis are cm2 for ‘area’, cm for ‘circumference’ and ‘maximal diameter’ and 1/cm for ‘no. of polyps’. Letters represent groups that are significantly different (P < 0.05) from one another; group lettering is in increasing order, e.g., group ‘a’ has significantly lower values than group ‘b’.
that the proportion of the total variance which is accounted for by the different colonies is much higher than the proportion of the total variance accounted for by the different sites; in other words, over 27% of the variance in oral disc size of F. speciosa at Wakatobi can be explained by differences between colonies, while very little of the variance (<6%) can be explained by differences between sites. According to the calculated partial H2 values, the differences between colonies are of much more consequence (more than five times greater) than the differences between sites. One important factor that distinguishes colonies from one another is their depth. Oral disc maximal diameter, circumference and area were all weakly, but significantly, correlated with depth (Spearman’s , 0.14 ≤ R2 ≤ 0.17, P < 0.05). This means that 14–17% of the variation in oral disc size can be reliably predicted by the changes in depth. All the size characters increased with increasing depth; since they were all also highly correlated to each other (R2 > 0.93, P < 0.01), and to avoid redundancy, Fig. 3 shows only one of these characters, oral disc area, increasing with increasing depth. This does not necessarily mean that the depth is the cause of 14–17% of the variance; it can be caused by other factors which are correlated to depth, notably incident light levels (Fig. 4). Plasticity of oral disc size, where oral discs become larger with increased sedimentation rates and/or decreased light levels, may have two possible reasons: greater physical defense against sediment settled on the coral, and increased heterotrophic feeding capability. Sediment settling directly on corals can cause stress and reduced growth (Rogers, 1990), and large polyps may offer an advantage in such habitats: larger polyp area, larger calice size,
Fig. 3. Oral disc area of F. speciosa colonies (mean ± S.D., total n = 1196) at different depths.
347
Fig. 4. Incident light levels (mean ± S.D., n = 5) at different depths on reef walls at three sites in the Wakatobi marine national park, Indonesia. Squares, Kaledupa; diamonds, Hoga; triangles, Sampela. The curves are logarithmic best fits to the data (reprinted with permission from Crabbe and Smith, 2006).
more tissue and greater distension potential positively correlate with rates of active sediment rejection (Hubbard and Pocock, 1972; Stafford-Smith and Ormond, 1992; Stafford-Smith, 1993), leading to greater survival rates and subsequent domination of areas with high sedimentation (Marshall and Orr, 1931; Hodgson, 1993; but see also Riegl, 1995). Todd et al. (2001) found that polyps of F. speciosa were larger in habitats with higher sedimentation rates, but did not speculate as to whether this phenomenon was due to the physical sediment load or the decreased light level. In the present study, oral discs of F. speciosa at Sampela, a reef suffering up to four times the sedimentation rates of the other reefs that were examined, not only did not show increased size but indeed were significantly smaller than in all other reefs. This result suggests that the driving force for the morphologic variation of F. speciosa oral disc size at Wakatobi is not the physical sediment load but rather the amount of light available for photosynthesis. Although research has demonstrated the influence of light on gross colony shape (Graus and Macintyre, 1982), little is known of its effect on polyp morphology (Foster, 1977, 1979). As the habitat of the colony becomes deeper, the amount of light available to the coral is reduced due to attenuation and/or absorption (Kirk, 1994); under these low light conditions, photosynthetic potential (i.e., the amount of energy that can be gained via photosynthesis) is also reduced (Verde and McCloskey, 2002). For cnidarians, there may be a great difference in the metabolism and utilization of carbon from heterotrophic and autotrophic sources (Bachar et al., 2007), and these results suggest that F. speciosa may adjust its mode of nutrition according to the amount of available light (e.g., Anthony and Fabricius, 2000): larger oral discs may optimise heterotrophic nutrition in low-light conditions, while smaller polyps may be optimal for photosynthesis in conditions where light is not limiting. Crabbe and Smith (2006) witnessed a similar pattern for G. fascicularis at Wakatobi, and suggested that small, tightly packed polyps increase the amount of surface area available for zooxanthellae, thereby maximizing photosynthetic potential in well-lit habitats. Conversely, individual polyps in lowlight environments may need to meet a greater proportion of their energetic requirements by heterotrophy, and therefore require better-developed food capturing body parts (larger oral discs and a larger number and size of tentacles). The mechanism enabling this apparent plasticity in the importance of heterotrophy and autotrophy may involve calcium uptake and oxygen secretion (Marshall and Clode, 2003), in which more polyps are produced and are done so more rapidly in colonies that are subjected to higher ambient light.
348
T. Caras et al. / Computational Biology and Chemistry 32 (2008) 345–348
Acknowledgments We would like to thank Operation Wallacea and the staff at Hoga Island who facilitated and hosted the fieldwork. References Airoldi, L., 2003. The effects of sedimentation on rocky coast assemblages. Oceanogr. Mar. Biol. Annu. Rev. 41, 161–236. Anthony, K.R.N., 2000. Enhanced particle-feeding capacity of corals on turbid reefs (Great Barrier Reef, Australia). Coral Reefs 19, 59–67. Anthony, K.R.N., Fabricius, K.E., 2000. Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. J. Exp. Mar. Biol. Ecol. 252, 251–253. Ayling, A.M., Ayling, A.L., 1991. The effect of sediment run-off on the coral populations of fringing reefs at Cape Tribulation. Research Publication no. 26, Great Barrier Reef Marine Park Authority, Townsville. Bachar, A., Achituv, Y., Pasternak, Z., Dubinsky, Z., 2007. Autotrophy versus heterotrophy: the origin of carbon determines its fate in a symbiotic sea anemone. J. Exp. Mar. Biol. Ecol. 349, 295–298. Bak, R.P.M., Joenje, M., de Jong, I., Lambrechts, D.Y.M., Nieuwland, G., 1998. Bacterial suspension feeding by coral reef benthic organisms. Mar. Ecol. Prog. Ser. 175, 285–288. Barnes, D.J., Chalker, B.E., 1990. Calcification and photosynthesis in reef-building corals and algae. In: Dubinsky, Z. (Ed.), Coral Reefs Ecosystems of the World, vol. 25. Elsevier, Amsterdam, pp. 109–131. Bosscher, H., Meesters, E.H., 1992. Depth related changes in the growth rate of Montastrea annularis. In: Proceedings of the 7th International Coral Reef Symposium, 1, pp. 507–512. Bradshaw, A.D., 1965. Evolutionary significance of phenotypic plasticity in plants. Adv. Gen. 13, 115–155. Crabbe, M.J.C., Smith, D.J., 2005. Sediment impacts on growth rates of Acropora and Porites corals from fringing reefs of Sulawesi, Indonesia. Coral Reefs 24, 437–441. Crabbe, M.J.C., Smith, D.J., 2006. Modelling variations in corallite morphology of Galaxea fascicularis coral colonies with depth and light on coastal fringing reefs in the Wakatobi Marine National Park (S.E. Sulawesi, Indonesia). Comput. Biol. Chem. 30, 155–159. Dodge, R.E., 1982. Effects of drilling mud on the reef-building coral Montastrea annularis. Mar. Biol. 71, 141–147. Fabricius, K.E., Dommisse, M., 2000. Depletion of suspended particulate matter over coastal reef communities dominated by zooxanthellate soft corals. Mar. Ecol. Prog. Ser. 196, 157–167. Falkowski, P.G., Jokiel, P.L., Kinzie III, R.A., 1990. Irradiance and corals. In: Dubinsky, Z. (Ed.), Ecosystems of the World, vol. 25. Elsevier, Amsterdam, pp. 89–107. Foster, A.B., 1977. Patterns of small-scale variation of skeletal morphology within the scleractinian corals, Montastrea annularis and Siderastrea siderea. In: Proceedings of the 3rd International Coral Reef Symposium, 2, pp. 409–415. Foster, A.B., 1979. Phenotypic plasticity in the reef corals Montastrea annularis and Siderastrea siderea. J. Exp. Mar. Biol. Ecol. 39, 25–54.
Graus, R.R., Macintyre, I.G., 1982. Variation in the growth forms of the reef coral Montastrea annularis (Ellis and Solander): a quantitative examination of growth response to light distribution using computer simulation. Smithson Contrib. Mar. Sci. 12, 441–464. Hodgson, G., 1993. Sedimentation damage to reef corals. In: Ginsberg, R.S. (compiler), Colloquium on global aspects of coral reefs: health, hazard, and history, Rosentiel School of Marine and Atmospheric Science, University of Miami, Miami. Hubbard, J.A.E.B., Pocock, Y.P., 1972. Sediment rejection by recent scleractinian corals: a key to paleoenvironmental reconstruction. Geol. Rundsch 61, 598–626. Kirk, J.T.O., 1994. Light and Photosynthesis in Aquatic Ecosystems. Cambridge University Press, Cambridge. Larcombe, P., Carter, R.M., Dye, J., Gagan, M.K., Johnson, D.P., 1995. New evidence for episodic post-glacial sea-level rise, central Great Barrier Reef, Australia. Mar. Geol. 127, 144. Lasker, H.R., 1980. Sediment rejection by coral reefs: the roles of behaviour and morphology of Montastrea cavernosa. J. Exp. Mar. Biol. Ecol. 47, 77–87. Marshall, A.T., Clode, P.L., 2003. Effect of increased calcium concentration in seawater on calcium cation and photosynthesis in the scleractinian coral Galaxea fascicularis. J. Exp. Biol. 205, 2107–2113. Marshall, S.M., Orr, A.P., 1931. Sedimentation on Low Isles reefs and its relation to coral growth. Great Barrier Reef Expedition 1928–29 Scientific Reports. Vol. I. British Museum (Natural History), London, pp. 93–132. McCloskey, L.R., Muscatine, L., 1984. Production and respiration in the Red Sea coral Stylophora pistillata as a function of depth. Proc. R. Soc. Lond. B Biol. Sci. 222, 215–230. Muscatine, L., 1990. The role of symbiotic algae in carbon and energy flux in reef corals. In: Dubinsky, Z. (Ed.), Ecosystems of the World, Vol. 25, Coral reefs. Elsevier, Amsterdam, pp. 75–87. Pigliucci, M., 1996. How organisms respond to environmental changes: from phenotypes to molecules (and vice versa). Trends Ecol. Evol. 11, 168–173. Porter, J.W., 1974. Community structure of coral reefs on opposite sides of the Isthmus of Panama. Science 186, 543–545. Riegl, B., 1995. Effects of sand deposition on scleractinian and alcyonacean corals. Mar. Biol. 121, 517–526. Rogers, C.S., 1990. Responses of coral reefs and reef organisms to sedimentation. Mar. Ecol. Prog. Ser. 62, 185–202. Stafford-Smith, M.G., 1993. sediment rejection efficiency of 22 species of Australian scleractinian corals. Mar. Biol. 115, 229–243. Stafford-Smith, M.G., Ormond, R.F.G., 1992. Sediment rejection mechanisms of 42 species of Australian scleractinian corals. Aust. J. Mar. Freshwater Res. 43, 683–705. Todd, P.A., Sanderson, P.G., Chou, L.M., 2001. Morphological variation in the polyps of the scleractinian coral Favia speciosa (Dana) around Singapore. Hydrobiologia 444, 227–235. Tomascik, T., Sander, F., 1985. Effects of eutrophication on reef-building corals. I. Growth rate of the reef-building coral Montastrea annularis. Mar. Biol. 87, 143–155. Verde, E.A., McCloskey, L.R., 2002. A comparative analysis of the photobiology of zooxanthellae and zoochlorellae symbiotic with the temperate clonal anemone Anthopleura elegantissima (Brandt). II. Effect of light intensity. Mar. Biol. 141, 225–239.
Contents lists available at ScienceDirect
Computational Biology and Chemistry journal homepage: www.elsevier.com/locate/compbiolchem
Research Article
Morphological variation in the oral disc of the scleractinian coral Favia speciosa (Dana) at Indonesia Tamir Caras a , Ami Bachar b , Zohar Pasternak c,∗ a
Department of Geography, Canterbury Christ Church University, North Holmes Road, Canterbury, Kent CT1 1QU, UK Department of Microsensors, Max Planck Institute for Marine Microbiology, Celsiustraße 1, Bremen 28359, Germany c Institute of Systems and Robotics, Department of Electrical and Computer Engineering, University of Coimbra, Coimbra 3030-290, Portugal b
a r t i c l e
i n f o
Article history: Received 9 June 2008 Accepted 22 June 2008 Keywords: Coral morphology Intraspecific variation Sedimentation Depth Autotrophy Heterotrophy
a b s t r a c t Photographic analysis was used to examine morphological differences in the oral disc of n = 1196 living polyps of Favia speciosa Dana (1846) sampled from four sites in the Wakatobi Marine National Park, Indonesia. Although oral disc size attributes differed significantly between the study sites, the geographic difference accounted for only a small fraction of the morphological variation and did not show a clear pattern of correspondence to sedimentation rates. A much higher fraction of the morphological variation was attributed to depth and so to incident light: oral discs grew significantly larger with increasing depth. These results suggest that for F. speciosa corals at Wakatobi, oral disc size may be optimised for heterotrophic nutrition under low light conditions, and photosynthesis in conditions where light is not limiting. Furthermore, the driving force for this phenotypic plasticity is more likely to be depth than sedimentation rate. © 2008 Elsevier Ltd. All rights reserved.
1. Introduction Intra-specific morphological variation is a pervasive feature in ecology, which can be attributed to genetic differentiation, phenotypic plasticity or a combination of both and is often environmentally correlated (Bradshaw, 1965; Pigliucci, 1996). Adaptive phenotypic plasticity, the differential expression of one genotype under varying environmental conditions, is a mechanism through which multi-cellular organisms can cope with changing environments when the scale of the temporal and/or spatial variability is smaller than the organism’s lifespan and/or dispersal range, respectively (Bradshaw, 1965; Foster, 1979). Two environmental factors are often considered as main driving forces of plasticity in coral morphology: ambient light level (McCloskey and Muscatine, 1984; Bosscher and Meesters, 1992) and sedimentation rate (Lasker, 1980; Dodge, 1982); this is because substantive growth of scleractinian reef corals depends primarily on high light availability for their symbiotic unicellular algae, the zooxanthellae (Barnes and Chalker, 1990; Muscatine, 1990). Increased depth, frequent re-suspension events (Larcombe et al., 1995), anthropogenic hypersedimentation (Todd et al., 2001) and increased concentrations of nutrients (Airoldi, 2003) may all result in higher attenuation and/or
∗ Corresponding author. Tel.: +351 239 796323; fax: +351 239 406672. E-mail address: [email protected] (Z. Pasternak). 1476-9271/$ – see front matter © 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.compbiolchem.2008.06.003
absorption of light, reducing light levels available to the coral (Kirk, 1994) and subsequent photosynthetic rates (Falkowski et al., 1990). In addition to autotrophy, corals are also heterotrophs and feed on a range of food types (e.g., zooplankton, Porter, 1974; bacteria, Bak et al., 1998; sediment, Stafford-Smith and Ormond, 1992). Thus, in deep or turbid waters where the rate of photosynthesis is compromised by low light levels, heterotrophy may be favoured (Tomascik and Sander, 1985; Ayling and Ayling, 1991; Anthony, 2000; Fabricius and Dommisse, 2000). Crabbe and Smith (2006) found evidence for such trophic plasticity by examining density and size of Galaxea fascicularis polyps at the Wakatobi National Marine Park, Indonesia, while Todd et al. (2001) discovered the same in Favia speciosa colonies at Singapore. The aim of the present work was to test the hypothesis that as depth and/or sedimentation rates increase, oral disc size increases in order to facilitate a trophic ‘shift’ from autotrophy to heterotrophy. To that end, the morphological variation of polyps from F. speciosa colonies were studied at Wakatobi located in different depths and exposed to different sedimentation rates. 2. Materials and Methods Four reef sites were studied at the Wakatobi National Marine Park, south-east Sulawesi, Indonesia (Table 1; for map locations see Fig. 1 of Crabbe and Smith, 2005): (1) Sampela, a shallow (maximal depth 12 m), slow sloping reef in close proximity to human
346
T. Caras et al. / Computational Biology and Chemistry 32 (2008) 345–348
Table 1 Environmental data and sampling scheme at the four reef sites (mean ± S.D. where applicable) Reef sites
Sampela
Mid-channel
Pak-kasim’s
Kaledupa
Colony depth (m) Estimated visibility (m) Sedimentation rate (g dry weight m−2 d−1 ) No. of colonies sampled No. of polyps sampled
7.8 ± 1.2 4–6 20.16 ± 1.71 7 260
15.2 ± 4.6 8–10 (no data) 8 316
14.2 ± 3.4 18–22 7.54 ± 0.76 6 255
12.9 ± 3.1 20–25 5.35 ± 0.68 10 365
Visibility was estimated using Secchi disc. Sedimentation rates are from Crabbe and Smith (2005).
of 10 cm × 10 cm was used for scale standardization. Images were computerized into MapInfo 5 (MapInfo, USA). Fully budded, nonfissioned polyps (i.e., completely isolated from their neighboring polyps and possessing complete walls and oral discs) within the 10 cm × 10 cm square were measured for oral disc area, oral disc circumference and oral disc maximum diameter (Fig. 1). These measurements were repeated a second time for a smaller, 5 cm × 5 cm square at the centre of each large 10 cm × 10 cm square. The measured oral disc size characters differed significantly between the large and small squares, suggesting that in the larger area, the colony’s curvature is distorting the measurements; as a result, only polyps in the smaller area were used in this study, thus minimizing the effect of colony curvature. Each character was checked for normality and homogeneity of variance, and was then tested for differences between colonies and between sites using ANOVA and post hoc Tukey tests (Table 2). As there is no link between any colonies on one reef to any colony on another reef, a nested ANOVA design was used: colonies were nested within sites and oral disc measurements were nested within colonies; this method allowed testing whether the variability in oral disc characteristics stems from differences between colonies or from differences between geographical reef sites. One characteristic, “Number of polyps”, was not nested, as there was only one statistic for each colony.
Fig. 1. Measured oral disc characters of Favia speciosa. (A) area; (B) circumference; (C) maximum diameter.
3. Results and Discussion habitation; it is a heavily used reef experiencing high sedimentation rates. (2) Mid-channel reef, a steep wall located at the centre of the channel between Sampela and Hoga Islands and characterised by strong currents. (3) Pak-Kasim’s reef, a steep wall with low sedimentation rate. (4) Kaledupa, an intact wall reef experiencing very little human pressure and a low sedimentation rate. The coral species studied was F. speciosa Dana (1846), possessing a high coral cover at the Wakatobi region. F. speciosa is widespread from the shallows to depths of 20 m, forming large (diameter > 30 cm) colonies with bi-coloured polyps, brown on the outside and green on the inside. Six to 10 (see Table 1) coral colonies were randomly selected, identified and photographed with a digital camera (Sony Cyber-shot DSC-P72). The camera was positioned perpendicularly to the coral surface and a slate frame
The three polyp size characters, polyp area, oral disc circumference and oral disc maximum diameter, differed significantly between sites and between colonies. When comparing the oral disc characters between sites (Fig. 2), the differences were small but statistically significant: both oral disc area and circumference were smallest at Sampela, larger at Kaledupa and Pak-kasim’s and larger still at the mid-channel ridge. At Sampela, where sedimentation rate is highest, oral disc diameter was significantly smaller than at the other reefs (where the sedimentation rates are significantly lower), while the number of polyps per cm2 did not differ significantly between the reefs. When comparing the oral disc characters between colonies, the differences were statistically significant (Table 2). The partial eta squared (H2 ) values indicate
Table 2 ANOVA results of the four characters measured Character
Effect
df
F
Significance
Partial H2
Oral disc area
Site Colony
3 30
21.2 15.6
P < 0.001 P < 0.001
0.06 0.32
Oral disc circumference
Site Colony
3 30
19.7 14.7
P < 0.001 P < 0.001
0.06 0.31
Oral disc maximum diameter
Site Colony
3 30
11.2 12.2
P < 0.001 P < 0.001
0.03 0.27
No. of polyps
Site
P = 0.646
–
3
0.56
df (degrees of freedom) equals the number of samples minus one (n − 1); ‘site effect’ is testing whether the character differs between the four sites, ‘colony effect’ is testing whether the character differs between the 31 colonies. F is the test statistic used to determine the statistical significance (P), a value of P < 0.05 means differences between samples are not likely to have happened by chance. Partial Eta-squared (H2 ) is comparable to R2 in correlation/regression analysis, denoting the proportion of variance explained by the model.
T. Caras et al. / Computational Biology and Chemistry 32 (2008) 345–348
Fig. 2. Oral disc characters (mean ± S.D.) and number of polyps of F. speciosa at the different sites. Units of the Y axis are cm2 for ‘area’, cm for ‘circumference’ and ‘maximal diameter’ and 1/cm for ‘no. of polyps’. Letters represent groups that are significantly different (P < 0.05) from one another; group lettering is in increasing order, e.g., group ‘a’ has significantly lower values than group ‘b’.
that the proportion of the total variance which is accounted for by the different colonies is much higher than the proportion of the total variance accounted for by the different sites; in other words, over 27% of the variance in oral disc size of F. speciosa at Wakatobi can be explained by differences between colonies, while very little of the variance (<6%) can be explained by differences between sites. According to the calculated partial H2 values, the differences between colonies are of much more consequence (more than five times greater) than the differences between sites. One important factor that distinguishes colonies from one another is their depth. Oral disc maximal diameter, circumference and area were all weakly, but significantly, correlated with depth (Spearman’s , 0.14 ≤ R2 ≤ 0.17, P < 0.05). This means that 14–17% of the variation in oral disc size can be reliably predicted by the changes in depth. All the size characters increased with increasing depth; since they were all also highly correlated to each other (R2 > 0.93, P < 0.01), and to avoid redundancy, Fig. 3 shows only one of these characters, oral disc area, increasing with increasing depth. This does not necessarily mean that the depth is the cause of 14–17% of the variance; it can be caused by other factors which are correlated to depth, notably incident light levels (Fig. 4). Plasticity of oral disc size, where oral discs become larger with increased sedimentation rates and/or decreased light levels, may have two possible reasons: greater physical defense against sediment settled on the coral, and increased heterotrophic feeding capability. Sediment settling directly on corals can cause stress and reduced growth (Rogers, 1990), and large polyps may offer an advantage in such habitats: larger polyp area, larger calice size,
Fig. 3. Oral disc area of F. speciosa colonies (mean ± S.D., total n = 1196) at different depths.
347
Fig. 4. Incident light levels (mean ± S.D., n = 5) at different depths on reef walls at three sites in the Wakatobi marine national park, Indonesia. Squares, Kaledupa; diamonds, Hoga; triangles, Sampela. The curves are logarithmic best fits to the data (reprinted with permission from Crabbe and Smith, 2006).
more tissue and greater distension potential positively correlate with rates of active sediment rejection (Hubbard and Pocock, 1972; Stafford-Smith and Ormond, 1992; Stafford-Smith, 1993), leading to greater survival rates and subsequent domination of areas with high sedimentation (Marshall and Orr, 1931; Hodgson, 1993; but see also Riegl, 1995). Todd et al. (2001) found that polyps of F. speciosa were larger in habitats with higher sedimentation rates, but did not speculate as to whether this phenomenon was due to the physical sediment load or the decreased light level. In the present study, oral discs of F. speciosa at Sampela, a reef suffering up to four times the sedimentation rates of the other reefs that were examined, not only did not show increased size but indeed were significantly smaller than in all other reefs. This result suggests that the driving force for the morphologic variation of F. speciosa oral disc size at Wakatobi is not the physical sediment load but rather the amount of light available for photosynthesis. Although research has demonstrated the influence of light on gross colony shape (Graus and Macintyre, 1982), little is known of its effect on polyp morphology (Foster, 1977, 1979). As the habitat of the colony becomes deeper, the amount of light available to the coral is reduced due to attenuation and/or absorption (Kirk, 1994); under these low light conditions, photosynthetic potential (i.e., the amount of energy that can be gained via photosynthesis) is also reduced (Verde and McCloskey, 2002). For cnidarians, there may be a great difference in the metabolism and utilization of carbon from heterotrophic and autotrophic sources (Bachar et al., 2007), and these results suggest that F. speciosa may adjust its mode of nutrition according to the amount of available light (e.g., Anthony and Fabricius, 2000): larger oral discs may optimise heterotrophic nutrition in low-light conditions, while smaller polyps may be optimal for photosynthesis in conditions where light is not limiting. Crabbe and Smith (2006) witnessed a similar pattern for G. fascicularis at Wakatobi, and suggested that small, tightly packed polyps increase the amount of surface area available for zooxanthellae, thereby maximizing photosynthetic potential in well-lit habitats. Conversely, individual polyps in lowlight environments may need to meet a greater proportion of their energetic requirements by heterotrophy, and therefore require better-developed food capturing body parts (larger oral discs and a larger number and size of tentacles). The mechanism enabling this apparent plasticity in the importance of heterotrophy and autotrophy may involve calcium uptake and oxygen secretion (Marshall and Clode, 2003), in which more polyps are produced and are done so more rapidly in colonies that are subjected to higher ambient light.
348
T. Caras et al. / Computational Biology and Chemistry 32 (2008) 345–348
Acknowledgments We would like to thank Operation Wallacea and the staff at Hoga Island who facilitated and hosted the fieldwork. References Airoldi, L., 2003. The effects of sedimentation on rocky coast assemblages. Oceanogr. Mar. Biol. Annu. Rev. 41, 161–236. Anthony, K.R.N., 2000. Enhanced particle-feeding capacity of corals on turbid reefs (Great Barrier Reef, Australia). Coral Reefs 19, 59–67. Anthony, K.R.N., Fabricius, K.E., 2000. Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. J. Exp. Mar. Biol. Ecol. 252, 251–253. Ayling, A.M., Ayling, A.L., 1991. The effect of sediment run-off on the coral populations of fringing reefs at Cape Tribulation. Research Publication no. 26, Great Barrier Reef Marine Park Authority, Townsville. Bachar, A., Achituv, Y., Pasternak, Z., Dubinsky, Z., 2007. Autotrophy versus heterotrophy: the origin of carbon determines its fate in a symbiotic sea anemone. J. Exp. Mar. Biol. Ecol. 349, 295–298. Bak, R.P.M., Joenje, M., de Jong, I., Lambrechts, D.Y.M., Nieuwland, G., 1998. Bacterial suspension feeding by coral reef benthic organisms. Mar. Ecol. Prog. Ser. 175, 285–288. Barnes, D.J., Chalker, B.E., 1990. Calcification and photosynthesis in reef-building corals and algae. In: Dubinsky, Z. (Ed.), Coral Reefs Ecosystems of the World, vol. 25. Elsevier, Amsterdam, pp. 109–131. Bosscher, H., Meesters, E.H., 1992. Depth related changes in the growth rate of Montastrea annularis. In: Proceedings of the 7th International Coral Reef Symposium, 1, pp. 507–512. Bradshaw, A.D., 1965. Evolutionary significance of phenotypic plasticity in plants. Adv. Gen. 13, 115–155. Crabbe, M.J.C., Smith, D.J., 2005. Sediment impacts on growth rates of Acropora and Porites corals from fringing reefs of Sulawesi, Indonesia. Coral Reefs 24, 437–441. Crabbe, M.J.C., Smith, D.J., 2006. Modelling variations in corallite morphology of Galaxea fascicularis coral colonies with depth and light on coastal fringing reefs in the Wakatobi Marine National Park (S.E. Sulawesi, Indonesia). Comput. Biol. Chem. 30, 155–159. Dodge, R.E., 1982. Effects of drilling mud on the reef-building coral Montastrea annularis. Mar. Biol. 71, 141–147. Fabricius, K.E., Dommisse, M., 2000. Depletion of suspended particulate matter over coastal reef communities dominated by zooxanthellate soft corals. Mar. Ecol. Prog. Ser. 196, 157–167. Falkowski, P.G., Jokiel, P.L., Kinzie III, R.A., 1990. Irradiance and corals. In: Dubinsky, Z. (Ed.), Ecosystems of the World, vol. 25. Elsevier, Amsterdam, pp. 89–107. Foster, A.B., 1977. Patterns of small-scale variation of skeletal morphology within the scleractinian corals, Montastrea annularis and Siderastrea siderea. In: Proceedings of the 3rd International Coral Reef Symposium, 2, pp. 409–415. Foster, A.B., 1979. Phenotypic plasticity in the reef corals Montastrea annularis and Siderastrea siderea. J. Exp. Mar. Biol. Ecol. 39, 25–54.
Graus, R.R., Macintyre, I.G., 1982. Variation in the growth forms of the reef coral Montastrea annularis (Ellis and Solander): a quantitative examination of growth response to light distribution using computer simulation. Smithson Contrib. Mar. Sci. 12, 441–464. Hodgson, G., 1993. Sedimentation damage to reef corals. In: Ginsberg, R.S. (compiler), Colloquium on global aspects of coral reefs: health, hazard, and history, Rosentiel School of Marine and Atmospheric Science, University of Miami, Miami. Hubbard, J.A.E.B., Pocock, Y.P., 1972. Sediment rejection by recent scleractinian corals: a key to paleoenvironmental reconstruction. Geol. Rundsch 61, 598–626. Kirk, J.T.O., 1994. Light and Photosynthesis in Aquatic Ecosystems. Cambridge University Press, Cambridge. Larcombe, P., Carter, R.M., Dye, J., Gagan, M.K., Johnson, D.P., 1995. New evidence for episodic post-glacial sea-level rise, central Great Barrier Reef, Australia. Mar. Geol. 127, 144. Lasker, H.R., 1980. Sediment rejection by coral reefs: the roles of behaviour and morphology of Montastrea cavernosa. J. Exp. Mar. Biol. Ecol. 47, 77–87. Marshall, A.T., Clode, P.L., 2003. Effect of increased calcium concentration in seawater on calcium cation and photosynthesis in the scleractinian coral Galaxea fascicularis. J. Exp. Biol. 205, 2107–2113. Marshall, S.M., Orr, A.P., 1931. Sedimentation on Low Isles reefs and its relation to coral growth. Great Barrier Reef Expedition 1928–29 Scientific Reports. Vol. I. British Museum (Natural History), London, pp. 93–132. McCloskey, L.R., Muscatine, L., 1984. Production and respiration in the Red Sea coral Stylophora pistillata as a function of depth. Proc. R. Soc. Lond. B Biol. Sci. 222, 215–230. Muscatine, L., 1990. The role of symbiotic algae in carbon and energy flux in reef corals. In: Dubinsky, Z. (Ed.), Ecosystems of the World, Vol. 25, Coral reefs. Elsevier, Amsterdam, pp. 75–87. Pigliucci, M., 1996. How organisms respond to environmental changes: from phenotypes to molecules (and vice versa). Trends Ecol. Evol. 11, 168–173. Porter, J.W., 1974. Community structure of coral reefs on opposite sides of the Isthmus of Panama. Science 186, 543–545. Riegl, B., 1995. Effects of sand deposition on scleractinian and alcyonacean corals. Mar. Biol. 121, 517–526. Rogers, C.S., 1990. Responses of coral reefs and reef organisms to sedimentation. Mar. Ecol. Prog. Ser. 62, 185–202. Stafford-Smith, M.G., 1993. sediment rejection efficiency of 22 species of Australian scleractinian corals. Mar. Biol. 115, 229–243. Stafford-Smith, M.G., Ormond, R.F.G., 1992. Sediment rejection mechanisms of 42 species of Australian scleractinian corals. Aust. J. Mar. Freshwater Res. 43, 683–705. Todd, P.A., Sanderson, P.G., Chou, L.M., 2001. Morphological variation in the polyps of the scleractinian coral Favia speciosa (Dana) around Singapore. Hydrobiologia 444, 227–235. Tomascik, T., Sander, F., 1985. Effects of eutrophication on reef-building corals. I. Growth rate of the reef-building coral Montastrea annularis. Mar. Biol. 87, 143–155. Verde, E.A., McCloskey, L.R., 2002. A comparative analysis of the photobiology of zooxanthellae and zoochlorellae symbiotic with the temperate clonal anemone Anthopleura elegantissima (Brandt). II. Effect of light intensity. Mar. Biol. 141, 225–239.