Journal of Experimental Marine Biology and Ecology 287 (2003) 57 78 www.elsevier.

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Photophysiological stress in scleractinian corals in response to short-term sedimentation

Eva Philipp a, Katharina Fabricius b,*
a

Alfred Wegener Institute for Polar and Marine Research, Columbusstr., 27568 Bremerhaven, Germany b Australian Institute of Marine Science, PMB No. 3, Townsville MC, Queensland 4810, Australia Received 15 August 2001; received in revised form 3 September 2002; accepted 28 October 2002

Abstract Effects of short-term sedimentation on common coastal coral species were investigated in laboratory and field experiments on the Great Barrier Reef (GBR) using pulse-amplitude modulated (PAM) chlorophyll fluorometry. In the laboratory, changes in maximal quantum yields of photosystem II ( Fv/Fm) in Montipora peltiformis were examined in response to the amount of sedimentation (79 234 mg cm 2) and duration of exposure (0 36 h). In control colonies, Fv/Fm ranged from 0.67 to 0.71, and did not show any temporal trend, while maximum yields of sedimentcovered fragments declined steadily and reached levels below 0.1 in most colonies after 36 h coverage. Maximal quantum yield in M. peltiformis declined linearly in relation to both the amount of sediment deposited per unit surface area and the duration of exposure. Zooxanthellae densities and chlorophyll concentrations per unit area of sediment-treated corals decreased in the same manner, however, their responses were not quite as strong as the changes in Fv/Fm. Within the ranges measured, sedimentation stress of colonies exposed to large amounts of sediment for short periods of time was similar to that exposed to low amounts of sediments for prolonged periods of time. Colonies were recovered from short-term, or low-level, sedimentation within < 36 h, whereas longterm exposure, or high levels of sedimentation, killed exposed colony parts. Field experiments comparing susceptibilities of common coastal coral species towards sedimentation showed significant reductions in effective quantum yields (DF/F m V ) in 9 out of 12 common coastal species after 22 h of exposure. Three out of twelve investigated species were not affected by the experimental application of sediments (Galaxea fascicularis, Fungia crassa, and Pectinia lactuca). Our results suggest that anthropogenic sediment deposition can negatively affect the photosynthetic activity of zooxanthellae and thus the viability of corals. However, the results also showed the ability of corals to compartmentalise sedimentation stress, as the photosynthetic activity only from tissues

* Corresponding author. Tel.: +61-7-4753-4444; fax: +61-7-4772-5852. E-mail address: k.fabricius@aims.gov.au (K. Fabricius). 0022-0981/02/$ - see front matter. Crown Copyright D 2002 Published by Elsevier Science B.V. All rights reserved. PII: S 0 0 2 2 - 0 9 8 1 ( 0 2 ) 0 0 4 9 5 - 1

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directly underneath the sediment declined, whereas that of adjacent clean tissues did not change measurably. Crown Copyright D 2002 Published by Elsevier Science B.V. All rights reserved.
Keywords: Photophysiological stress; Scleractinian corals; Short-term sedimentation

1. Introduction There is a significant natural variation in sedimentation on coral reefs, and tolerance to sedimentation varies widely among corals. Natural processes, such as resuspension from the sea floor and sediment imports from rivers, determine concentrations of suspended solids in the water column. However, excessive sedimentation constitutes one of the biggest sources of reef degradation from human activities (Rogers, 1990). The main sources of sedimentation due to human activities are dredging or drilling at sea and runoff from river catchments degraded by upstream deforestation, removal of riparian vegetation and s and Risk, mangroves, and agriculture in wetlands and floodplains (Guilcher, 1985; Corte 1985; Hubbard, 1986; van Katwijk et al., 1993; Brodie, 1995). If wave energy is low (e.g., during calm weather, on leeward sides, or at greater depths), the suspended sediment settles out of the water column, and is deposited on the sea floor and upon sea floor-inhabiting organisms. The effects of sedimentation on corals and their symbiotic algae have been investigated in a number of studies around the world (reviewed in Rogers, 1990). Some species are able to clean off deposits efficiently and show no damage due to sedimentation (Abdel-Salam and Porter, 1988; Stafford-Smith, 1993; Riegl, 1995; Wesseling et al., 1999). In other coral species, sedimentation depresses rates of photosynthesis and enhances respiration and mucus production (Riegl and Branch, 1995; Yentsch et al., 2002). With increasing sedimentation, growth rates decline, the corals loose their zooxanthellae, and the underlying tissue dies (Bak, 1978; Lasker, 1980; Rogers, 1983; Peters and Pilson, 1985). Sedimentation also negatively affects rates of survival and settlement of coral larvae (Babcock and Davies, 1991; Gilmour, 1999). In the longer term, high sedimentation regimes can influence coral cover as well as the species composition in communities due to s and differences in sediment tolerances between species (Dodge and Vaisnys, 1977; Corte Risk, 1985). In this study, we used the noninvasive pulse-amplitude modulated chlorophyll fluorometry (PAM) to quantify the build-up and recovery from photosynthetic stress in corals exposed to short-term (12 36 h) periods of high levels of sedimentation. A submersible PAM-instrument (Diving-PAM, Walz, Germany) enabled us to conduct measurements both in the laboratory and in the field. This instrument has previously been used on corals for in situ studies of reactions of symbiotic zooxanthellae to diurnal changes in light intensity or different water depth (Beer and Ilan, 1998; Ralph et al., 1999), and to detect stress caused by cyanide, heavy metals or temperature changes (Warner et al., 1996; Jones et al., 1999, 2000; Prange and Dennison, 2000). The aim of this study was, firstly, to investigate the short-term stress reaction of the coral Montipora peltiformis to sediment exposure and its potential to recover from such

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stress under controlled laboratory conditions. M. peltiformis is a foliose coral species, which occurs in high abundances on some turbid nearshore reefs of the central Great Barrier Reef (GBR). In particular, the effects of exposure to (a) different amounts of sediment for (b) different times on photosynthetic activity, zooxanthellae count, and chlorophyll concentration, were investigated. Secondly, the susceptibility of a range of coral species to sediment stress was assessed in the field. Responses were compared among reefs as well as among species, and it was tested whether the photosynthetic stress is confined to the coral surface directly underneath the sediment. The results of this investigation may help to understand the damage of corals caused by short-term exposure to high levels of sedimentation and potential shifts in community structure in relation to prolonged or repeated enhanced levels of sedimentation in coastal reefs of the Great Barrier Reef.

2. Materials and methods 2.1. Laboratory experiments 2.1.1. Experimental setup The effects of sediments on corals were studied in the outdoor flow-through aquarium system of the Australian Institute of Marine Science (AIMS) in January and February 2001. Fragments of the foliose coral M. peltiformis were sampled from 3 to 5 m water depth at Magnetic Island, a turbid nearshore fringing reef where this species occurs in high abundance (Fig. 1). Corals were transported to AIMS within 2 h of collection. Large coral pieces were split into fragments with a mean area of 33 cm2 ( F 8 SD) and left in a tank on plastic racks for 3 days to recover. The oval 1000-l tank had a continuous inflow of natural seawater at rate of 600 l h 1. A circular laminar flow of about 3 4 cm s 1 was created by a system of water and air hoses. The water temperature was around 29 jC, equivalent to that of the ambient sea. Corals were exposed to natural sunlight reduced by a 70% shade cloth to simulate natural conditions at f6 m water depth. Fine, muddy sediment was collected from 3 m water depth behind the breakwater wall of the AIMS jetty. It was sieved through a 3-mm mesh to remove coarse material, and aerated for two days. The sediment contained 2.37% carbon, 0.13% nitrogen, and 459 Ag/g phosphorous. When the experiments commenced, half of the coral fragments were temporarily removed from the tank and put into a holding tank of the same size, flow, and light exposure. After the incoming water was turned off in both tanks, the sediment was stirred and distributed as evenly as possible in the water column of the experimental tank. When the sediment had settled after 6 h, the inflow of seawater was turned on again, and the control corals were moved back from the holding tank into the experimental tank, and evenly distributed between the now sediment-loaded corals. 2.1.2. PAM chlorophyll fluorometry Photosynthetic activity was determined by measuring variable chlorophyll fluorescence of photosystem II (PS II), with a pulse-amplitude modulated chlorophyll

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Fig. 1. Map of the Great Barrier Reef showing the positions of AIMS, Magnetic Island, and the four reefs of the field experiments.

fluorometer (Diving-PAM; Schreiber et al., 1986). In dark acclimated corals, maximal quantum yield was calculated as the ratio of variable to maximum fluorescence ( Fv/Fm). For dark adaptation, coral fragments were kept in black boxes with running seawater for 30 min, while the sediment remained on the sediment-treated fragments. At the end of the dark period, the sediment was washed off each fragment and collected in separate vials for dry weight determination. Chlorophyll fluorescence was measured with the fiberoptics of the PAM chlorophyll fluorometer at 3-mm distance to the coral surface. F0 was measured by applying a pulsed measuring beam ( < 1 Amol quanta m 2 s 1), followed by a saturation pulse of white light to record Fm (>1000 Amol quanta m 2 s 1). Fifteen measurements, evenly distributed over the surface, were made on each fragment. 2.1.3. Calculation of sediment load The sediment retrieved from each fragment of M. peltiformis was dried in an oven at 60 jC until constant weight. The surface area of each of the foliose

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fragments was determined by tracing its outline onto paper, cutting and weighing the piece of paper, and using a calibration curve to convert paper weight to surface area. The amount of sediment retrieved from each coral was then normalised to their surface area. It averaged 151 F 37 mg DW cm 2 (range: 79 234 mg cm 2). 2.1.4. Determination of chlorophyll concentrations and zooxanthellae density Zooxanthellae densities and chlorophyll (chl a and chl c2) concentrations were analysed on subsamples of the frozen corals. The tissue was stripped from the skeleton with an airbrush using 60 100 ml filtered seawater. The water tissue solution was homogenised in a glass homogeniser, and five 10 ml subsamples were taken. To determine chlorophyll concentrations, three of the subsamples were centrifuged at 1500 g for 3 min. The supernatant was rejected and the tissue redissolved in 2 ml 100% acetone, sonicated for 1 min, and the chlorophyll extracted overnight in darkness at 4 jC. The next day, the samples were again centrifuged at 1500 g for 3 min, and the supernatant was transferred into vials and frozen at 20 jC. A second extraction was performed on the remaining tissue pellet, which was redissolved in 2 ml 100% acetone, and processed as described before. Both extracts were measured in a spectrophotometer at 630 and 663 nm, and chl a and chl c2 concentrations were calculated after Jeffrey and Humphrey (1975). Zooxanthellae densities in two subsamples of the homogenised water tissue solution were counted under the microscope using a haemocytometer slide (eight replicates) and counts were normalised to coral surface area. 2.1.4.1. Experiment 1.1: effects of amount and duration of sedimentation. After 0, 12, 18, 24, and 36 h, sediment-loaded and control fragments were removed from the experimental tank and carefully transferred into a darkened flow-through 10-l tank for Fv/Fm measurements. Two to five replicate fragments were analysed for each treatment and time. Subsequently, half of the fragments were frozen for analyses of chlorophyll and zooxanthellae densities (see above); the rest were moved back into the experimental tank to monitor their recovery from the treatment. 2.1.4.2. Experiment 1.2: effects of duration of exposure on recovery. Recovery from sedimentation was monitored for up to 7 days by repeated measurements of maximum PS II quantum yields ( Fv/Fm) of M. peltiformis fragments, which had been exposed to sediment for 0, 12, 18, and 24 h. 2.1.4.3. Experiment 1.3: effects of sedimentation on the adjacent tissue. To determine whether sediment stress in one area also affected the surrounding tissues, sediment was applied to about 50% of the surface of four colonies of M. peltiformis, while the remaining surface was left clean. After 48 h exposure, maximum quantum yields of the clean surfaces away from the sediment, as well as those along the edge of the sediment patch, were measured and compared with those of the colonies before sediment application. After sediment removal, Fv/Fm of the cleaned tissues was determined. This experiment was later repeated in the field on four colonies each of Echinopora lamellosa

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and massive Porites. These colonies were exposed to sediments for 22 h before effective quantum yield measurements. 2.2. Field experiments Field experiments were carried out on the windward sides of reefs at 6 8 m depth in February 2001. The reefs fringed four inshore islands located at 5 8 km off the coast. Two islands were in the northern Great Barrier Reef (Hay Island: 13j40VS, 143j42VE, and Wilkie Island: 13j47VS, 143j38VE), and two were in the Central GBR (Green Island: 16j46VS, 146j00VE, and Normandy Island: 17j12VS, 146j04VE) (Fig. 1). Sediment was freshly collected from 15 m depth at the study site in the beginning of the experiment. This provided a finer sediment fraction than found at the depth of the experimental corals. Sediment nutrient concentrations are listed in Table 1. The amount of sediment loaded onto the corals could not easily be quantified, but we aimed to apply amounts similar to those added in the laboratory experiments (about 200 mg cm 2). In the field experiments, advantage was taken of the fact that responses were confined to directly exposed tissues (see results to Experiment 1.3): we added the sediment to one portion of the investigated colonies and used other parts of the same colonies as controls (without sediment load; Fig. 2). This allowed us to eliminate potential between colony variability in effective quantum yields (DF/F m V ) caused by small-scale environmental heterogeneity (depth, flow exposure, shading by neighbours, etc.). 2.2.1. Experiment 2.1: comparison of sedimentation effects among reefs Replicate colonies of six common nearshore species (Pachyseris speciosa, massive Porites, E. lamellosa, Turbinaria peltata, Fungia crassa, Galaxea fascicularis) were measured on several of the four islands to compare responses to sediment application among different locations. After tagging the corals, effective quantum yields of the tissue were recorded with the Diving-PAM (about 30 measurements per colony). DF/F m V were measured across the whole colony surface at time zero because the exact position of the sediment deposit, and its edge, could not be fully controlled. One part of the colony surface was then covered with a thin layer of the freshly collected sediment. After 22 h, the effective quantum yield of the tissue in the area free of sediment was measured as control, then the sediment was removed from the remaining colony and DF/F m V of the cleaned tissue was recorded.

Table 1 Content of carbon (C), nitrogen (N) and phosphorous (P) in sediments of different reefs C (%) Hay Island Wilkie Island Normandy Island Green Island 10.33 9.89 9.68 11.08 N (%) 0.03 0.02 0.05 0.05 P (Ag/g) 320 864 291 286

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Fig. 2. Sediment-induced tissue discolouration in a massive Porites from Green Island, Great Barrier Reef. The dark circle marks an area on the colony surface that was covered with sediment for 22 h. The white circle shows a control patch that was not covered with sediment.

2.2.2. Experiment 2.2: comparison of sedimentation stress among coral species Colonies of 12 common nearshore species belonging to a range of families (Table 5) were tagged by scuba divers and treated as in Experiment 2.1. 2.3. Statistical methods 2.3.1. Experiment 1.1: effects of sedimentation dose and duration of exposure on yields A two-way analysis of variance was used to compare the changes in Fv/Fm of sediment exposed and control colonies over time in the laboratory experiments. Time (0, 12, 18, 24, and 36 h) and treatment (control versus sediment) were used as factors. The Fv/Fm data were heteroscedastic, and were stabilised by expressing them as proportion of maximum Fv/Fm (0.70) and arc sine square root transformed. The heteroscedascity was severe so the transformation was applied twice. The amount of sediment recovered from each fragment varied, and linear models were used to explain Fv/Fm as a function of the amount of sediment added (henceforth dose; 0 234 mg cm 2) and duration of exposure (time; 12, 18, 24, and 36 h). Linear regression was also used to determine the relationship between chlorophyll concentrations and zooxanthellae counts. The change over time in the ratio between Fv/Fm, and both chlorophyll concentration and zooxanthellae counts in sedimentexposed corals, was modelled as a linear regression model. 2.3.2. Experiment 1.3: effects of sedimentation on the adjacent tissue Changes in Fv/Fm and DF/F m V , in response to sedimentation, were investigated using analysis of variance. The factors in the model were species (M. peltiformis, E. lamellosa,

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and massive Porites), colonies nested within species, and treatments. The four treatments were (a) all tissues before sediment application, (b) non-sediment tissue after 22 h of sediment application, (c) tissue along the edge (about 5 mm away) of the sediment patch after 22 h, and (d) tissue directly under the sediment after sediment removal. Species and treatment were treated as fixed effects, and colonies nested in species were random. Single degree of freedom contrasts were used to compare Fv/Fm and DF/F m V values of the three types of tissues measured at the end of the experiment, with values of the control tissue at time zero. Data were expressed as proportion of maximum Fv/Fm or DF/F m V , and double arc sine square root transformed, as in Experiment 1.1, to stabilise error distributions. 2.3.3. Experiment 2.1: comparison of sedimentation effects among reefs An analysis of variance was used to test for differences in effective quantum yields of P. speciosa among reefs. The factors in the model were reef (Normandy, Green, and Hay Islands), colonies nested within reef, and treatments. The treatments were (a) all tissues before sediment application, (b) non-sediment tissue after 22 h of sediment application, and (c) tissue directly under the sediment after sediment removal. The analysis and data transformation were as for Experiment 1.3. 2.3.4. Experiment 2.2: comparison of sedimentation stress among coral species An analysis of variance was used to test for differences in responses to sedimentation among 12 species in the field. The factors in the model were species, colonies nested within species, and treatments. The treatments were (a) control tissues before sediment application, (b) non-sediment tissue after 22 h of sediment application, and (c) tissue directly under the sediment after sediment removal. The analysis and data transformation were as for Experiment 1.3. All analyses were done with S-Plus statistical software, Version 2000 (Statistical Sciences, 1999).

3. Results 3.1. Laboratory experiments 3.1.1. Observations The sediment remained on most of the coral fragments in a relatively thin and even layer during the experiment, and from visual observations, it was concluded that M. peltiformis appeared unable to remove significant amounts of it. After 12 18 h exposure to a mean load of 151 F 37 mg cm 2 of sediment (range: 79 234 mg cm 2), discolouration of the fragment surfaces was visible when the sediment was removed. In colonies covered for 24 36 h, the tissue was heavily bleached and showed signs of necrosis. 3.1.1.1. Experiment 1.1: effects of sediment exposure on Fv/Fm PAM chlorophyll fluorometry. In control colonies of M. peltiformis, maximum PS II quantum yields ( Fv/Fm) ranged from 0.67 to 0.71, and remained at this level

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Fig. 3. Effects of short-term sedimentation on the photophysiology of M. peltiformis. White circles: control corals without sediment; black circles: corals covered with 151 F 37 mg cm 2 sediment. Data are means F SE. (A) Fv/Fm (backtransformed), measured by PAM chlorophyll fluorometry (N = 4 11 colony fragments per treatment, 15 measurements per fragment). (B) Zooxanthellae density (N = 4 7 fragments per treatment, two subsamples with eight zooxanthellae counts each per subsample and fragment). (C) Chlorophyll concentration per unit surface area (N = 4 7 fragments per treatment, three replicates per fragment).

throughout the experiment. In fragments covered with sediment, Fv/Fm declined consistently and reached levels below 0.1 in most colonies after 36 h coverage (Fig. 3A). Both exposure time and treatment (sedimentation versus control) significantly influenced the photosynthetic activity (Table 2). Chlorophyll concentrations and zooxanthellae density. Sediment-covered fragments showed a continuous decline both in numbers of zooxanthellae and chlorophyll concentration per unit surface area with time after the onset of the experiment (Fig. 3B,C). The chlorophyll concentration in control corals ranged from 4.0 to 8.6 Ag cm 2 colony surface area, whereas those exposed to sediment for 36 h contained 1.3 2.5 Ag cm 2. Zooxanthellae densities of controls were 2.6 4.1 106 cells cm 2. In contrast, densities

Table 2 Analysis of variance for photosynthetic yields ( Fv/Fm) in M. peltiformis in response to treatment (control versus sediment) and duration of exposure (time) df Treatment Time Treatment:Time Residuals Sums of squares are sequential. 1 4 4 60 F 455.8 58.23 80.40 Pr( F) < 0.0001 < 0.0001 < 0.0001

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fell to 1.5 1.9 106 cells cm 2 after 36 h sediment exposure. Chlorophyll concentrations were strongly, linearly related to zooxanthellae densities in the tissues of M. peltiformis (R2 = 0.82, F(3,43) = 56.6, P < 0.0001), thus, the chlorophyll content per zooxanthellae did not change in response to the treatments. The ratio of yields and zooxanthella numbers of sediment-exposed corals declined monotonously with time (R2 = 0.44, F(1,19) = 14.88, P = 0.001), and the same pattern was found for the ratio of yields and chlorophyll, which also decreased monotonously within 36 h (R2 = 0.42, F(1,19) = 13.86, P = 0.0015). After 12 h exposure, yields were 82% of control values, whereas the number of zooxanthellae was still 94%. After 18 h, maximum PS II quantum yields were reduced to only 61% of controls, and the number of zooxanthellae was around 81% of control values. Fv/Fm reached baseline levels when the tissue still contained about 25% of initial zooxanthellae and chlorophyll concentrations. In the control corals, no significant change in chlorophyll concentration and zooxanthellae density was observed during the experimental run. Dose time relationship. The amount of sediment (dose) retrieved from the colonies varied from 79 to 234 mg cm 2 (mean = 151 mg cm 2). A series of linear models were used to further explore the relationship between Fv/Fm and dose and time. The initial model treated time as a factor and dose as numeric, and comprised different slopes and intercepts for each level of time. The slopes of this model were significantly different ( F(3,61) = 47.7, P < 0.0001), but the intercepts were not ( F(4,61) = 1.49, P = 0.246). A common intercept model was fitted and the four slopes of the time groups increased linearly (Fig. 4A). This suggested that the decline of Fv/Fm could be explained as a linear function of dose and dose time, and a test of this model against the four slopes model confirmed this ( F(2,65) = 0.62, P = 0.542). Finally, dose was dropped from the model ( F(1,66) = 2.62, P = 0.111), thus, the model simplified to decreasing Fv/Fm being a linear function of dose time (henceforth exposure; Fig. 4B). The same model (linear change with only exposure in the model) was best for explaining the numbers of zooxanthellae and chlorophyll concentrations (not shown). For all three models, the response depended only on the product of dose and time, and thus, for example, 12 h exposure to 200 mg cm 2 was equivalent to 24 h of 100 mg cm 2. The photophysiological stress in corals exposed to high levels of sedimentation for a short time period is therefore similar to that of corals exposed to low levels of sedimentation for extended periods of time. 3.1.1.2. Experiment 1.2: effects of exposure on recovery. All fragments of M. peltiformis, which were exposed to sediments for 12 and 18 h, recovered to normal Fv/Fm ratios within 24 36 h (Fig. 5A,B). After 24 h of exposure, one coral fragment loaded with 107 mg cm 2 sediment fully recovered to initial values within 48 h. Two other fragments, loaded for 24 h with 109 and 138 mg cm 2, respectively, showed further declines in Fv/Fm after the sediment was washed off, and died (Fig. 5C). Coral fragments covered with sediment for 36 h did not recover from the treatment. 3.1.1.3. Experiment 1.3: effects on tissues adjacent to a sediment deposit. In the laboratory experiments, about 50% of the surfaces of four M. peltiformis were covered by sediment for 48 h, the other surfaces remained sediment-free. Effects were confined

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Fig. 4. Photosynthetic yields in M. peltiformis in response to sedimentation. (A) Fv/Fm (backtransformed) as a function of the amount of sediment deposited and duration of sedimentation application (12 h: black squares; 18 h: white squares; 24 h: black triangles; 36 h: white triangles). (B) Fv/Fm (backtransformed) as a function of sediment exposure (duration dose). The solid line represents the mean; the dashed lines represent upper and lower 90% confidence intervals.

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Fig. 5. Recovery of Fv/Fm in M. peltiformis after 12 (A), 18 (B), and 24 h (C) sediment treatment, measured by PAM chlorophyll fluorometer. White circles: Fv/Fm in control corals (means of 4 11 fragments, each represented by about 15 measurements). Black circles: Fv/Fm of individual sediment-treated fragments (each represented by about 15 measurements). The dashed vertical line indicates the sediment removal and the beginning of the postburial time. Error bars are omitted for clarity.

to the tissue directly exposed to sedimentation, while tissue about 5 mm away from a sediment patch showed no difference in Fv/Fm or colouration to control fragments at time zero and after 48 h (Fig. 6). The same result was obtained in light-adapted E. lamellosa and massive Porites (Fig. 6) after 22 h of exposure in the field. In all

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Fig. 6. Effects of sediment exposure on DF/F m V in tissues of E. lamellosa, Porites massive, and Fv/Fm in M. peltiformis. Data are backtransformed mean DF/F m V or Fv/Fm F SE (three to four colonies per species). Abbreviations, C0: tissues before sediment exposure (white bars); C22 or 48: control areas at the end of the experiment after 22 or 48 h (dense-structured), E22 or 48: tissue along the boundary of a sediment patch (lightV or Fv/Fm structured); and S22 or 48: tissue that was sediment-covered for 22 or 48 h (black). About 30 DF/F m readings were taken from each colony and treatment.

species, effective quantum yields (DF/F m V ) were indistinguishable between tissues adjacent to a sediment patch at the end of the experiment, tissues away from the sediment at the end of the experiment, and tissues prior to the sediment application (Fig. 6, Table 3). 3.2. Field experiments 3.2.1. Observations Similar to the laboratory experiments, some of the corals, e.g., Porites massive, E. lamellosa, or Merulina scabricula, were heavily bleached and showed signs of necrosis. E. lamellosa and Montipora crassituberculata developed particularly thick and sticky mucus underneath the sediment, which made it difficult for the divers to fan off the sediment. 3.2.1.1. Experiment 2.1: comparison of sedimentation effects among reefs. The photophysiological stress response to sedimentation was similar among colonies of P. speciosa and did not vary among three reefs despite different levels of sedimentation and turbidity (Normandy Island being the most turbid and Green Island the clearest

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Table 3 Effects of sedimentation on the photosynthetic yields of coral tissues (A) Species Colonies/species Treatment Species:Treatment Residuals df 2 9 3 6 25 F 4.986 4.5751 251.6 9.111 Pr( F) 0.0349 0.0426 < 0.0001 < 0.0001

(B) (a) Cend Mean diff F SE T value P Mean diff F S.E. T value P Mean diff F S.E. T value P

Montipora peltiformis 0.079 F 0.047 1.661 0.109 0.050 F 0.046 1.084 0.289 0.78 F 0.046 16.99 < 0.0001

Echinopora lamellosa 0.086 F 0.041 2.094 0.047 0.011 F 0.041 0.2659 0.793 0.393 F 0.041 9.594 < 0.0001

Massive Porites 0.0026 F 0.041 0.0639 0.950 0.017 F 0.041 0.425 0.674 0.477 F 0.041 11.66 < 0.0001

(b) Eend

(c) Send

(A) Analysis of variance testing for differences in yields between four treatments (underneath the sediment patch at the end of the experiment, along the edges of the sediment patches at the end of the experiment, controls before sediment application, and controls at the end of the experiment away from the sediment patch), and in three species of corals (M. peltiformis, E. lamellosa, and massive Porites). (B) Single-contrast analysis of variances comparing control yields at the beginning of the experiment with yields at the end of the experiment of (a) tissue that remained free of sediment (Cend), (b) tissues not exposed to sediment along the edge of the sediment patch (Eend), and (c) tissue covered by sediment (Send).

reef, K. Fabricius, unpublished data). Twenty-two hours of sedimentation had significant effects on effective quantum yields (interaction treatment and time), but both baseline DF/F m V and the reduction in DF/F m V after sediment exposure neither differed among reefs nor among colonies (Table 4, Fig. 7). Similarly, neither differences among reefs nor colonies were found in other coral species (massive Porites, E. lamellosa, T. peltata, F. crassa, G. fascicularis; data not shown).

Table 4 Comparison of photosynthetic yields (DF/F V m ) in colonies of P. speciosa growing on three reefs of the Great Barrier Reef (Normandy Island, Green Island, Hay Island; see Fig. 7) df Reef Colonies/reef Treatments Reef:Treatments Residuals 2 4 2 4 8 F 0.465 4.23 134 2.47 Pr( F) 0.658 0.395 < 0.0001 0.129

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Fig. 7. Effects of 22 h sedimentation on the effective yield of P. speciosa at different reefs (see Table 5). Abbreviations and symbols, C0: tissues before sediment exposure (white bars); C22: control areas at the end of the experiment after 22 h (structured); and S22: underneath the sediment (black). Data are backtransformed means F SE of four to six colonies per reef. About 30 DF/F m V readings were taken from each colony and treatment. N = Normandy Island, G = Green Island, H = Hay Island.

3.2.1.2. Experiment 2.2: comparison of sedimentation stress among coral species. Sediment was added to 12 common coastal species of scleractinian corals at 6 8 m depth on coastal reefs (Table 5). In these species, DF/F m V ranged from 0.63 to 0.73 at the beginning of the experiment and did not differ from those of the controls at the end of the experiment (Fig. 8). Most corals were unable to remove the sediment within the 22 h of experimental run. Nine of the species showed minor to massive photophysiological stress responses to sedimentation, with DF/F m V being significantly reduced in the sediment-covered areas (Fig. 8, Table 6). DF/F m V reduction was greatest in E. lamellosa, P. speciosa, massive Porites, Turbinaria reniformis, and M. crassituberculata. In these species,

Table 5 List of coral species investigated and reefs on the Great Barrier Reef where field measurements were conducted Species Echinopora lamellosa Fungia crassa Galaxea fascicularis Montipora crassituberculata Montipora danae Montipora tuberculosa Reef N, W N, G N, G H W G Species Merulina scabricula Pachyseris speciosa Pectinia lactuca massive Porites Turbinaria peltata Turbinaria reniformis Reef H N, G, W H N, W, H W, H N

N = Normandy Island, G = Green Island, W = Wilkie Island, H = Hay Island.

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Fig. 8. Effects of 22 h sediment loading on the effective yields of 12 common inshore hard corals species, measured by PAM chlorophyll fluorometry in situ. The species names are listed in Table 5. Data are backtransformed mean DF/F m V F SE (N = 2 11 colonies per species) of: tissues before sediment exposure (white bars); tissues not exposed to sediments after 22 h at the end of the experiment (structured); and areas directly underneath the sediment (black). A mean of 30 measurements was taken from each colony and treatment. Species marked with asterisks showed significant changes in DF/F m V due to sedimentation.

DF/F m V values on sediment-loaded areas were only about 50% of control areas. Three species showed no differences in DF/F m V between the sediment-treated and control areas. These were G. fascicularis and F. crassa, which were both able to clean off the sediment, and Pectinia lactuca, which inflated the underlying tissues. The effects of sedimentation in three species of Montipora (the genus used in the laboratory experiments) were by no means extreme compared with other species.

Table 6 V ) in response to Results of an analysis of variance comparing changes in photosynthetic yields (DF/F m sedimentation among 12 coral species in the field df Species Colonies/Species Treatment Species:Treatment Residuals 11 46 2 22 92 F 25.8917 15.311 294.1645 11.6751 Pr( F) < 0.0001 < 0.0001 < 0.0001 < 0.0001

DF/F m V in tissues not exposed to sediment (control areas before and after 22 h of sediment application, and the sediment area before sediment application) varied greatly from yields in the sediment-exposed tissues. DF/F m V were not significantly different in controls before and after 22 h of sediment exposure in any of the 12 species, however DF/F m V varied significantly among colonies within some of the species, and among species.

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4. Discussion Short-term exposure to sedimentation under laboratory conditions severely affected the quantum yield of photosystem II, chlorophyll a and c2 concentrations, and zooxanthellae densities in M. peltiformis. The corals responded initially with discolouration. Severe bleaching and tissue necrosis occurred within 24 36 h of sediment exposure, indicating that such sedimentation inflicted irreversible damage to both the zooxanthellae and the animal. Comparisons with 12 other coral species in the field showed that the responses of M. peltiformis were typical for corals inhabiting turbid coastal reefs. Large differences among species in their ability to reject and survive from deposition of fine and coarse sediments have been described in previous studies (Lasker, 1980; Abdel-Salam and Porter, 1988; Rogers, 1983; Stafford-Smith and Ormond, 1992; Wesseling et al., 1999). Prolonged and severe sedimentation can lead to a shift in the species composition of reef communities (Dodge and Vaisnys, 1977). Bleaching and tissue necrosis caused by sediment loads of 30 4000 mg cm 2 for 2 40 days have been reported for scleractinian and alcyonacean corals (Bak and Elgershuizen, 1976; Rogers, 1983; Hodgson, 1990; Riegl, 1995; Wesseling et al., 1999). Our field measurements showed that the changes in photosynthetic yields in response to fine, muddy sediments differed also among common coastal corals. Particularly sensitive were foliose corals or corals with relatively small polyps, such as E. lamellosa, Montipora spp., and massive Porites. Sediment was firmly lodged on concave or flat coral surfaces, and the polyps appeared unable to remove or shift the sediment. In many of these species, DF/ Fm V was significantly reduced after less than 24 h of sediment exposure. In contrast, corals with bigger calyces or a more open skeletal structure, like F. crassa, G. fascicularis, or P. lactuca, were not affected by sedimentation. These corals were either able to clean off the sediment (F. crassa, G. fascicularis) or inflate the underlying tissue, probably to increase a gas exchange through the uncovered parts (P. lactuca). The specific causes of the severe decline in Fv/Fm in corals exposed to sedimentation remain unknown to date. Fv/Fm naturally varies by a few percent with light availability, declining from 0.62 to 0.57 after 4 h darkness, and increasing again with exposure to light or oxygen-enriched water (Jones and Hoegh-Guldberg, 2001), confirming that the availability of light and oxygen are major factors influencing the photosynthetic activity. However, sedimentation has significant energetic implications for corals, as it reduces photo- and heterotrophic energy acquisition, and increases energy expenditure. A sediment cover of 100 mg cm 2 reduces the available light by 75% (Riegl and Branch, 1995), depressing gross and net photosynthesis as well as oxygen evolution (Shashar et al., 1993; Kuhl et al., 1995; Riegl and Branch, 1995; Gardella and Edmunds, 1999). Sediment that interferes with the prey-capturing polyps also compromises the corals ability to heterotrophic energy gain. Furthermore, the energy required to produce mucus in corals, normally f35% of the daily net photosynthesis, increases to 65% at a sediment load of 200 mg cm 2 (Riegl and Branch, 1995). Consequently, the energy budget of a coral may reach the compensation point or even a deficit (Riegl and Branch, 1995; Yentsch et al., 2002). The negative energetic consequences of long-term exposure to sedimentation will be particularly severe for corals growing in deeper water where

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photosynthetic energy gain is low and sediment deposition is high (Anthony and Fabricius, 2000). The copious amounts of mucus, which were produced underneath the sediment by some corals, have often been interpreted as a cleaning mechanism. However, E. lamellosa and M. crassituberculata, which had particularly thick and sticky mucus, were among the most severely sediment-affected species. Our observations therefore support previous suggestions that mucus trapping of small particles on the coral surface contributes to anoxia and thus the death of underlying tissues (Bak and Elgershuizen, 1976; Stafford-Smith and Ormond, 1992). Sediment-covered corals treated with tetracycline suffer less from bleaching and tissue necrosis than sediment-covered corals not supplied with this antibiotic, which showed necrosis after 2 days and died after 7 days (Hodgson, 1990). This suggests that the expulsion of zooxanthellae and tissue necrosis may not be related to light reduction, whereas tetracycline-sensitive microorganisms and their metabolic products in the sediment-mucus layer may significantly contribute to it. Our study showed that the photosynthetic activity in M. peltiformis decreased linearly with both the amount of sedimentation and the time it remained on the tissues, which indicates that any threshold value for sedimentation tolerance has to incorporate both amount and time. The threshold level of M. peltiformis for recovery from sedimentation was around 24 h 0.11 g c 2.5 g h cm 2. Thus, that within the exposure range tested, low levels of sedimentation for extended periods of time altered the photophysiology of these corals as much as exposure to high amounts of sediment for short periods of time. For example, half the amount of sedimentation for twice the time had the same photophysiological effect as twice the amount of sediment for half the time. The linear effect of time and dose also indicated that planned sediment-suspending human activities such as dredging would cause least damage if they were to be conducted during conditions that promote resuspension (rather than deposition) of sediment from coral surfaces, e.g., if calm weather periods with low waves and weak tidal currents are avoided. M. peltiformis was able to recover to normal Fv/Fm values within 24 36 h after the removal of the sediment, if the duration was short ( < 24 h) or if doses were low. Recovery was possible even when yields had temporarily dropped to 60%, and zooxanthellae counts to 80% of initial numbers. Yields generally declined more rapidly than the number of zooxanthellae, and reached a baseline level when about 25% of zooxanthellae were still present. The linear correlation between chlorophyll concentrations and zooxanthellae densities demonstrated that chlorophyll contents per zooxanthellae remained unaltered, thus, reductions in zooxanthellae numbers, probably due to the expulsion of zooxanthellae, were responsible for the drop in tissue chlorophyll concentrations. Bleaching of corals (the loss of zooxanthellae from the host tissue) is known as a stress response to a range of environmental conditions such as high temperature, cyanide exposure, low salinity, or sedimentation (Bak, 1978; Thompson, 1980; Neudecker, 1981; Dallmeyer et al., 1982; Rogers, 1990; Jokiel and Coles, 1990). In a study of cyanide and heat-stressed corals, which showed a fast recovery of quantum yields, but a reduction in zooxanthellae densities, Jones et al. (1999) argued that a selective expulsion of damaged zooxanthellae (with lower yield) might give the impression of recovery by increasing the proportion of healthy algae (with higher

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yields) in the remnant algal population. This finding could explain the fast recovery of Fv/Fm in M. peltiformis in the present study, however, further research is necessary to understand the mechanisms leading to decreases in zooxanthellae yields and to death or fast recovery in coral tissue. Several reef around the world, including the fringing reefs of Magnetic Island where the experimental corals were collected, experience sedimentation rates in excess of 200 mg s and Risk, cm 2 day 1 for periods of days (Maragos, 1972; Mapstone et al., 1989; Corte 1984; Riegl, 1995). The sediment exposure threshold of 2.5 g h 1 cm 2 for M. peltiformis would be reached if a full days deposition of sediment remained on the surface for a further 12 h. Such exposure is feasible in particular on leeward reefs and at deeper depths where resuspension is low. And indeed, few corals grow on the leeward sides of Magnetic Island and similar reefs, and coral cover is often < 10% below 8 m depth on their windward sides (K. Fabricius, personal observations). On offshore reefs of the Great Barrier Reef, corals are not commonly exposed to natural sedimentation levels as high as those applied by us experimentally (151 F 37 mg cm 1). However, much higher sedimentation rates occur in areas of human activities (Rogers, 1990), and increasing sedimentation, resulting from anthropogenic sources, is of serious concern for coastal coral reefs worldwide (Wilkinson, 2000; Yentsch et al., 2002; Burke et al., 2002). Dredging and drilling suspend high levels of sediments, which can settle locally on the benthos (Bak, 1978). Sediment is resuspended by bottom trawl fishery (Riemann and Hoffman, 1991), and their potential contribution to the degradation of some inshore reefs has so far been little studied. However, of greatest concern are the terrigenous sediments eroding from cleared land (Burke et al., 2002). River plumes pass over large proportions of coastal coral reefs of the central Great Barrier Reef, carrying typically 5 50 mg l 1 of fine, organically, and nutrient-enriched suspended sediments, with maximum concentrations of up to 300 mg l 1 close to river mouths (Devlin et al., 2001). Effects of the freshly imported muddy sediments on benthic organisms can be more detrimental than that of old nutrient-poorer resuspended sea floor sediment, possibly due to enhanced organic and nutrient contents that promote microbial growth, stickiness, and flocculation (Fabricius and Wolanski, 2000; Fabricius et al., in press). Bleached patches caused by natural sedimentation were observed on a small proportion of corals during our study on the turbid inshore reefs of the GBR. Sediment-covered patches were particularly noticeable on colonies with concave surfaces such as Montipora spp. or E. lamellosa, and in grooves of massive Porites. Underneath the sediment, we found either bleached tissue or, more commonly, dead patches, whereas the surrounding tissues appeared to be healthy. Another commonly observed apparent outcome of sedimentation was colony fragmentation in foliose corals, when the central concave colony area was covered by sediment and dead, whereas the more peripheral parts survived. Our experiments demonstrated the ability of corals to compartmentalise sedimentation stress, as yields only from tissues directly underneath the sediment suffered, whereas those from adjacent clean tissues did not change measurably. Such compartmentalisation may be an important survival mechanism for corals growing in turbid environments: even if proportions of a colony are killed by sedimentation, the remaining colony surfaces remain physiologically unaffected and continue to contribute to the coral community.

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Acknowledgements The study was funded by the Commonwealth of Australia Cooperative Research Centres Program through the Cooperative Research Centre for the Great Barrier Reef World Heritage Area. It was supported by the Australian Institute of Marine Science and the Deutsche Akademische Austauschdienst (German Academic Exchange Organisation, DAAD). Many thanks to Glenn Death for his help with the statistical analyses. Thanks also to Emre Turak for helping to identify the hard coral species. We greatly appreciate comments and suggestions on the manuscript by David Barnes, Jon Brodie, and Kai Bischof. [SS]

References
Abdel-Salam, H.A, Porter, J.W., 1988. Physiological effects of sediment rejection on photosynthesis and respiration in three Caribbean reef corals. Proc. 6th Int. Coral Reef Symp., Townsville, vol. 2, pp. 285 292. 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, 221 253. Babcock, R., Davies, P., 1991. Effects of sedimentation on settlement of Acropora millepora. Coral Reefs 9, 205 208. Bak, R.P.M., 1978. Lethal and sublethal effects of dredging on reef corals. Mar. Pollut. Bull. 9, 14 17. Bak, R.P.M., Elgershuizen, J.H.B.W., 1976. Patterns of oil-sediment rejection in corals. Mar. Biol. 37, 105 113. Beer, S., Ilan, M., 1998. In situ measurements of photosynthetic irradiance responses of two Red Sea sponges growing under dim light conditions. Mar. Biol. 131, 613 617. Brodie, J., 1995. Terrestrial runoff and the Great Barrier Reef. Australas. Sci. 16, 23 25. Burke, L., Selig, E., Spalding, M., 2002. Reefs at Risk in Southeast Asia. World Resources Institute, Cambridge. 72 pp. s, N.J., Risk, M.J., 1984. The coral reef of the Cahuita National Park, Costa Rica. Revista De Biologia Corte Tropical. San Jose Rev. Biol. Trop. 32, 109 121. s, N.J., Risk, M.J., 1985. A reef under siltation stress: Cahuita, Costa Rica. Bull. Mar. Sci. 36, 339 356. Corte Dallmeyer, D.G., Porter, J.W., Smith, G.J., 1982. Effects of particulate peat on the behaviour and physiology of the Jamaican reef-building coral Montastrea annularis. Mar. Biol. 68, 229 233. Devlin, M., Waterhouse, J., Taylor, J., Brodie, J., 2001. Flood plumes in the Great Barrier Reef: spatial and temporal patterns in composition and distribution. Great Barrier Reef Marine Park Authority Report, Townsville. Dodge, R.E., Vaisnys, J.R., 1977. Coral populations and growth patterns: responses to sedimentation and turbidity associated with dredging. J. Mar. Res. 35, 715 730. Fabricius, K.E., Wolanski, E., 2000. Rapid smothering of coral reef organisms by muddy marine snow. Estuar. Coast. Shelf Sci. 50, 120 150. Fabricius, K.E., Wild, C., Wolanski, E., Adele, D., in press. Effects of transparent exopolymer particles (TEP) and muddy terrigenous sediments on the survival of hard coral recruits. Estuar. Coast. Shelf Sci. 57 (5). Gardella, D.J., Edmunds, P.J., 1999. The oxygen microenvironment adjacent to the tissue of scleractinian Dichocoenia stokesii and its effects on symbiont metabolism. Mar. Biol. 135, 289 295. Gilmour, J., 1999. Experimental investigation into the effects of suspended sediment on fertilisation, larval survival and settlement in a scleractinian coral. Mar. Biol. 135, 451 462. Guilcher, A., 1985. Nature and human changes of sedimentation in lagoons behind Barrier Reefs in the humid tropics. Proc. 5th Int. Coral Reef Congr., Tahiti, vol. 4, pp. 207 212. Hodgson, G., 1990. Tetracycline reduces sedimentation damage to corals. Mar. Biol. 104, 493 496. Hubbard, D.K., 1986. Sedimentation as a control of reef development: St. Croix, U.S.V.I. Coral Reefs 5, 117 125.

E. Philipp, K. Fabricius / J. Exp. Mar. Biol. Ecol. 287 (2003) 5778

77

Jeffrey, S.W., Humphrey, G.F., 1975. New spectrophotometric equitations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem. Physiol. Pflanzen 167, 191 194. Jokiel, P.L., Coles, S.L., 1990. Response of Hawaiian and other Indo Pacific reef corals to elevated temperature. Corals Reefs 8, 155 162. Jones, R.J., Hoegh-Guldberg, O., 2001. Diurnal changes in the photochemical efficiency of the symbiotic dinoflagellates (Dinophyceae) of corals: photoprotection, photoinactivation and the relationship to coral bleaching. Plant Cell Environ. 24, 89 99. Jones, R.J., Kildea, T., Hoegh-Guldberg, O., 1999. PAM Chlorophyll fluometry: a new in situ technique for stress assessment in scleratinian corals, used to examine the effects of cyanide from cyanide fishing. Mar. Pollut. Bull. 38 (10), 864 874. Jones, R.J., Ward, S., Amri, A.Y., Hoegh-Guldberg, O., 2000. Changes in quantum efficiency of Photosystem II of symbiotic dinoflagellates of corals after heat stress, and of bleached corals sampled after the 1998 Great Barrier Reef mass bleaching event. Mar. Freshw. Res. 51, 63 71. Kuehl, M., Cohen, Y., Dalsgaard, T., Joergensen, B.B., Revsbech, N.P., 1995. Microenvironment and photosynthesis of zooxanthellae in scleractinian corals studied with microsensors for O sub(2), pH and light. Mar. Ecol. Prog. Ser. 117 (1 3), 159 172. Lasker, H.R., 1980. Sediment rejection by reef corals: the roles of behaviour and morphology in Montastrea cavernosa (Linnaeus). J. Exp. Mar. Biol. Ecol. 47, 77 87. Mapstone, B.D., Choat, J.H., Cumming, R.L., Oxley, W.G., 1989. The fringing reefs of Magnetic Island: benthic biota and sedimentation. A baseline study. A report to the Great Barrier Reef Marine Park Authority, Townsville, 88 pp. Maragos, J.E., 1972. A study of the ecology of Hawaiian reef corals. PhD dissertation, University of Hawaii, Honolulu. Neudecker, S., 1981. Growth and survival of scleractinian corals exposed to thermal effluents at Guam. 4th Int. Coral Reef Symp., Manila, Philippines, pp. 173 180. Peters, E.C., Pilson, M.E.Q., 1985. A comparative study of the effects of sedimentation on symbiotic and asymbiotic colonies of the coral Astrangia danae (Milne Edwards and Haime, 1849). J. Exp. Mar. Biol. Ecol. 92, 215 230. Prange, J.A., Dennison, W.C., 2000. Physiological responses of five Seagrass species to trace metals. Mar. Pollut. Bull. 41, 327 336. Ralph, P.J., Gademann, R., Larkum, A.W.D., Schreiber, U., 1999. In situ underwater measurements of photosynthetic activity of coral zooxanthellae and other reef-dwelling dinoflagellate endosymbionts. Mar. Ecol. Prog. Ser. 180, 139 147. Riegl, B., 1995. Effects of sand deposition on scleratinian and alcyonacean corals. Mar. Biol. 121, 517 526. Riegl, B., Branch, G.M., 1995. Effects of sediment on the energy budgets of four scleractinian (Bourne 1900) and five alcyonacean (Lamouroux 1816) corals. J. Exp. Mar. Biol. Ecol. 186, 259 275. Riemann, B., Hoffman, E., 1991. Ecological consequences of dredging and bottom trawling in the Limfjord, Denmark. Mar. Ecol. Prog. Ser. 69, 171 178. Rogers, C.S., 1983. Sublethal and lethal effects of sediment applied to common Caribbean reef corals in the field. Mar. Pollut. Bull. 14, 378 382. Rogers, C.S., 1990. Responses of coral reefs and reef organisms to sedimentation. Mar. Ecol. Prog. Ser. 62, 185 202. Schreiber, U., Schliwa, U., Bilger, W., 1986. Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth. Res. 10, 51 62. Shashar, N., Cohen, Y., Loya, Y., 1993. Extreme diel fluctuations of oxygen in diffusive boundary layers surrounding stony corals. Biol. Bull. Mar. Biol. Lab., Woods Hole, vol. 185, pp. 455 461. 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. Freshw. Res. 43, 683 705. Statistical Sciences, 1999. S-PLUS, Version 2000 for Windows Statistical Sciences, a division of Mathsoft, Seattle, USA.

78

E. Philipp, K. Fabricius / J. Exp. Mar. Biol. Ecol. 287 (2003) 5778

Thompson Jr., J.H., 1980. Responses of selected scleratinian corals to drilling fluids used in the marine environment. PhD Dissertation. Texas A & M University, College Station, U.S.G.S. Rep. van Katwijk, M.M., Meier, N.F., van Loon, R., van Hove, E.M., Giesen, W.B.J.T., van der Velde, G., den Hartog, C., 1993. Sabaki River sediment load and coral stress: correlation between sediments and condition of the Malindi Watamu reefs in Kenya (Indian Ocean). Mar. Biol. 117, 675 683. Warner, M.E., Fitt, K.W., Schmidt, G.W., 1996. The effects of elevated temperature on the photosynthetic efficiency of zooxanthellae in hospite from four different species of reef coral: a novel approach. Plant Cell Environ. 19, 291 299. Wesseling, I., Uychiaoco, A.J., Alino, P.M., Aurin, T., Vermaat, J.E., 1999. Damage and recovery of four Philippine corals from short-term sediment burial. Mar. Ecol., Prog. Ser. 176, 11 15. Wilkinson, C. (Ed.), 2000. Status of Coral Reefs of the World: 2000. Australian Institute of Marine Science, Townsville, Australia. 364 pp. Yentsch, C.S., Yentsch, C.M., Cullen, J.J., Lapointe, B., Phinney, D.A., Yentsch, S.W., 2002. Sunlight and water transparency: cornerstones in coral research. J. Exp. Mar. Biol. Ecol. 268, 171 183.