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High-sediment tolerance in the reef coral Turbinaria mesenterina from the inner Great Barrier Reef lagoon (Australia)
Estuarine, Coastal and Shelf Science 78 (2008) 748–752
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High-sediment tolerance in the reef coral Turbinaria mesenterina from the inner Great Barrier Reef lagoon (Australia) Jeremy J. Sofonia, Kenneth R.N. Anthony * School of Marine Biology and Aquaculture, James Cook University, Townsville, Queensland 4811, Australia
a r t i c l e i n f o
a b s t r a c t
Article history: Received 2 May 2007 Accepted 19 February 2008 Available online 12 March 2008
Sedimentation is an important stressor on coral reefs subjected to run-off, dredging and resuspension events. Reefs with a history of high-sediment loads tend to be dominated by a few tolerant coral species. A key question is whether such species live close to their tolerance thresholds or near their niche optima. Here, we analyse experimentally the sediment tolerance of a spatially dominant coral, Turbinaria mesenterina (Dendrophylliidae), at nearshore reefs in the central Great Barrier Reef lagoon. Testing was conducted in a 5-week tank experiment under manipulated sediment loading and flow conditions. Physiological stress was assessed based on the behaviour of three key response variables: skeletal growth rate, energy reserves (lipid content) and photosynthetic performance. Because sediment effects are likely to vary between flow regimes, sediment and flow responses were tested using a full factorial design. Sediment loads greater than 110 mg cm2 had no effect on any of the physiological variables, regardless of flow (0.7–24 cm s1). Turbinaria mesenterina is thus tolerant to sediment loads an order of magnitude higher than most severe sediment conditions in situ. Likely mechanisms for such tolerance are that: (1) colonies covered in sediment (60–120 mm) in low-flow were able to clear themselves rapidly (within 4– 5 h); and (2) sediment provides a source of food. These results suggest that intensified sediment regimes on coastal reefs may shift coral communities towards dominance by a few well-adapted species. Ó 2008 Elsevier Ltd. All rights reserved.
Keywords: physiological tolerance stress growth rate lipid calcification Great Barrier Reef scleractinian coral Regional index terms: Australia Queensland Great Barrier Reef Cleveland Bay Magnetic Island Cockle Bay
1. Introduction Sedimentation is one of the most important disturbance factors on coastal coral reefs worldwide (Rogers, 1990; Brown, 1997). Rates of sedimentation and turbidity levels on coastal reefs have in many areas increased 5–10-fold during the past 2–3 decades, mainly due to increased run-off from the land to the sea (Wilkinson, 2002; McCulloch et al., 2003; Fabricius, 2005). However, in many coastal reef areas where high levels of run-off and resuspension are in part due to natural processes (Kleypas, 1996) reef assemblages have developed under high natural sediment loads for millennia (Larcombe et al., 1995). Often, coral assemblages on nearshore turbid-zone reefs differ in composition from that of more offshore clear-water reefs (e.g. Done, 1982; Acevedo et al., 1989), potentially reflecting differences in species niche characteristics (Anthony and Connolly, 2004).
* Corresponding author. Present address: Centre for Marine Studies, The University of Queensland, St Lucia, Queensland 4072, Australia. E-mail address: [email protected] (K.R.N. Anthony). 0272-7714/$ – see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2008.02.025
Coral species that are well adapted to high-sediment loads, for example by utilisation of particulate matter as a food source (Anthony, 1999; Rosenfeld et al., 1999), acclimatization to shifting light regimes (Anthony et al., 2004) or by energy-efficient mechanisms of sediment handling are likely to have a selective advantage on high-turbidity reefs (Lasker, 1980). As many coastal reefs become subjected to increasing sediment loads due to coastal developments, poor land use practices (e.g. Furnas, 2003; McKergow et al., 2005), and increased frequency of severe storms (e.g. Emanuel, 2005), reef communities may potentially shift towards assemblages dominated by sediment-tolerant species. Studies of phase shifts on coral reefs have mainly been concerned with transitions from coral to algal dominance (e.g. Hughes, 1994; McClanahan et al., 2002) and less so with mechanisms driving shifts in spatial dominance between coral taxa (Aronson et al., 1998). Here, we investigate experimentally the tolerance of the coral Turbinaria mesenterina to an extreme range of sediment loads. Colonies of T. mesenterina form whorls or plates (foliose) with pronounced ecomorph variation ranging from horizontal plates in deep water to tightly packed cones in shallow water (Anthony et al.,
J.J. Sofonia, K.R.N. Anthony / Estuarine, Coastal and Shelf Science 78 (2008) 748–752
2005). The species has been recorded along turbid reefs over a wide geographic area (Veron, 2000), ranging from Japan (Ueshima and Ohno, 1997) to southern China (Zou, 1982) and is spatially dominant on nearshore reefs in the central section of Australia’s Great Barrier Reef (Done, 1982; Van Woeski and Don, 1997). In the most turbid areas on the western (nearshore) side of Magnetic Island (Cleveland Bay, North Queensland), T. mesenterina covers nearly 100% of the reef from the crest to the deep slope (Fig. 1). To characterise in detail the physiological response profile of T. mesenterina to high-sediment loads we examined changes in three key physiological variables during a 5-week experiment: (1) skeletal growth rate; (2) maximum quantum yield (photosynthetic efficiency) of symbionts; and (3) lipid content (energy stores). Skeletal growth rate, as change in buoyant weight or linear extension, is the most commonly used metric for coral growth (e.g. Buddemeier and Kinzie, 1976; Spencer-Davies, 1989) and maximum quantum yield is a proxy for photosynthetic performance (e.g. Ralph et al., 1999). Lipid content provides an estimate of energy storage and is thus a proxy for the trophic value of the coral’s recent environmental conditions (Anthony and Fabricius, 2000; Grottoli et al., 2006). For example, a negative energy balance due to a greater expenditure on sediment handling than energy intakes via phototrophy and heterotrophy (Anthony and Connolly, 2004) will lead to depletion of lipid stores. Because effects of sediment loading on the coral biology are likely to vary with flow regime (i.e. as deposition under low-flow and resuspension under high-flow), each sediment
Fig. 1. (A) Central section of the Great Barrier Reef lagoon (North Queensland, Australia). The site of coral collecting and deployment of field controls in Cockle Bay (Magnetic Island) is marked x. (B) Turbinaria mesenterina, forming large stands with up to 90% cover in 1–5 m depth.
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treatment was conducted under stagnant as well as high-flow conditions. Key physiological processes such as rate of respiration, exchange rate of dissolved nutrients and particle encounter rates vary greatly with flow environment (e.g. Dennison and Barnes, 1988; Patterson et al., 1991). We test the hypotheses that: (1) all physiological response variables are reduced under extremely high-sediment loads, but that (2) sediment effects will be stronger in depositional (low-flow) compared to in resuspension (high-flow) regimes. By using sediment with low (<1%) organic carbon content, we did not expect particle heterotrophy to compensate for energy costs associated with any of the sediment regimes. 2. Materials and methods 2.1. Study site and coral collecting Corals were collected from the fringing reef in Cockle Bay on the western side of Magnetic Island, North Queensland, Australia (1911.21500 S, 146 48.95000 E) on May 5 (Austral winter), 2003 (Fig. 1). Cockle Bay is one of the most turbid reefs in the nearshore region of the Great Barrier Reef lagoon (Anthony et al., 2004), in part due to frequent resuspension of sediment deposits in the shallow Cleveland Bay (Larcombe et al., 1995) and downstream transport of mud from adjacent bays around Magnetic Island. Coral communities on the reef crest and slope (1–6 m depth) in Cockle Bay and adjacent bays are characterised by high abundance of Turbinaria mesenterina. In Cockle Bay in particular, this species forms large monospecific stands that may cover >90% of the reef (Fig. 1). Approximately 100 fragments (around 8 cm by 8 cm) were collected from large colonies of Turbinaria mesenterina, selected randomly, at 2–4 m depth (below lowest astronomical tides) in Cockle Bay. The fragments were cut from colony peripheries using surgical bone cutters. Based on colour morph variation among samples at least 10 different genotypes were represented. To ensure that all experimental corals had similar light history, corals were collected exclusively from colonies in open (unshaded) habitats. At the broken end of each fragment, a 2 mm hole was drilled through the coral and used for attachment to stands using a cable tie. Each stand consisted of an arched piece of PVC (8 cm by 8 cm) with a 2 mm hole in one end so the coral could be attached horizontally to the arched upper side of the stand. To allow the corals to recover from handling stress, they were left on racks (2–4 m depth) in the field for 9 weeks at which time new polyps had developed along the broken edges. During the recovery period and experimental phase, downwelling irradiance in situ at the level of the experimental colonies (fragments) ranged between 50 and 300 mmol quanta m2 s1 (daily averages), based on continuous monitoring using two light loggers (Dataflow 392 recorders with cosine corrected PAR sensors) attached to the coral racks. This was consistent with the long-term range for the location (Anthony et al., 2004). The sensors were equipped with automated wipers to prevent fouling. Rates of sedimentation at the site approximated 7– 12 mg cm2 d1 (dry weight of GF/C filtered material) estimated from weekly deployment of six sediment traps (3.25 cm diameter and 30 cm long, Jurg, 1996) and correspond to anticipated winter rates with no significant storm events (Larcombe et al., 1995, 2001; Anthony et al., 2004). Flow speeds in situ were estimated using dissolution rates of plaster blocks (e.g. Jokiel and Morrissey, 1993). Six hemispherical blocks (base diameter 53 mm) of known dry weights were placed on the coral racks at three occasions (1-day exposures). Dissolution rate was converted to flow speed after calibrating blocks in a flow chamber (n ¼ 8) with known flow velocities determined by particle tracking. Flow rates at the sites ranged from 3 to 11 cm s1.
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2.2. Laboratory experiment Eighty of the experimental coral colonies were transported to the research aquarium facility at James Cook University. The remaining 20 corals were left on the racks at the reef site as field controls. At the indoor experimental facility, 72 of the corals were randomly distributed among 18 tanks (25 l each, measuring 35 cm long, 25 cm wide and 20 cm tall) connected independently to an inflow of filtered seawater (35 ppt, 23–24 C). The remaining eight coral fragments were immediately frozen for later analysis for baseline lipid concentrations. An array of six metal halide lamps (each 400 W, EYE, Japan) was suspended 50 cm above the tanks to obtain a light level of w300 mmol m2 s1, which corresponds to the average growth irradiance at the field site (see also Anthony et al., 2004). The lamps were connected to timers set to a 10-h daylight cycle. The experimental design consisted of two fixed factors with three levels of sediment loading and two flow regimes. Tanks were arranged in a randomised block design to account for potential heterogeneity in light regime and water inflow among tank positions. Each treatment level was replicated by three tanks; each tank holding four corals. In each of the high-flow tanks, two recirculating pumps (w950 l h1, Aquaclear 402, Italy) generated a turbulent flow environment of 24 4 cm s1, sufficient to keep added sediment in suspension. In the low-flow tanks, flow speeds were 0.7 0.1 (SE) cm s1 due only to convection caused by inflow of seawater. Fine sediment was applied manually three times daily (at 7–8 AM; 12–1 PM; and 5–6 PM) to the sediment treatment tanks for 34 days. The sediment was collected from the surface layer near the field site in Cockle Bay using an airlift. Particle sizes ranged from 60 to 120 mm as determined by a laser particle sizer (Malvern Instruments, UK), representative of sandy silts (Larcombe et al., 2001). To avoid contamination of the aquarium system with organic material, and potential interactions with the flow and sedimentation effects, the sediment was rinsed in freshwater, stored dry and rehydrated 1 h prior to use. The processed sediment was therefore likely to have lower nutritional value than that in the field. Similar type sediment used in previous experiments had an organic carbon content of 0.5–1.5%, determined using a CHN Analyzer (Shimadzu 5000), and contained 0.1–0.2% nitrogen determined using an Antec 720 C/N Analyzer (Anthony, unpublished data). Six tanks were dosed with a high-sediment load of 110 27 mg cm2, six tanks with a moderate load of 16 4 mg cm2, and six tanks received filtered (5 mm) seawater only with a background sedimentation rate of 0.8 0.3 mg cm2. Sedimentation rates within the tanks were estimated using triplicate cylindrical sediment traps (3.6 cm diameter, 4.5 cm tall) placed between coral colonies on the tank floor. 2.3. Coral responses Coral stress responses were assessed using three physiological variables: (1) rate of skeletal growth; (2) tissue lipid content; and (3) maximum quantum yield (photosynthetic efficiency) of algal symbionts. Skeletal growth rates were determined as differences in buoyant weight between the first and last day of the experiment (Spencer-Davies, 1989). Tissue lipid content was determined using a technique modified from that of Harland et al. (1992) (see also Anthony and Fabricius, 2000). Pre-experimental lipid concentrations were obtained from assays of microcolonies selected randomly from the population of experimental corals on the first day of the experiment. Stress responses of dinoflagellate symbionts were assessed by estimating changes in the maximum quantum yield (Fv/Fm) of photosystem II (Hoegh-Guldberg and Jones, 1999; Jones et al., 1999; Ralph et al., 1999) using a pulse amplitude modulation (PAM)
fluorometer (DIVING PAM, Walz, Germany). PAM assays were conducted on dark-acclimated colonies (before sunrise) on the first and last days of the experiment. 2.4. Data analysis Data were analysed using two-way analysis of variance (ANOVA), using sediment and flow regime as main factors. Data for individual corals were pooled within each tank, thus using tanks as replicates. Analyses were followed by Tukey’s multiple comparison tests to identify significant differences between individual treatment groups. Assumptions of normality were tested using Kolmogorov–Smirnov one-sample tests and homogeneity of variances was tested using Levene’s test (Sokal and Rohlf, 1995). 3. Results and discussion None of the physiological stress/health indicators (skeletal growth rate, lipid content and maximum quantum yield) assayed for Turbinaria mesenterina showed significant responses to the sediment or flow treatments as main factors (Tables 1 and 2). Skeletal growth rates (as relative changes in buoyant weight, Table 1) varied marginally among three treatment combinations only: corals in the low-sediment/high-flow treatment had around 30% higher growth rates (3.9 0.1% month1) than corals in the high-sediment/low-flow (3.0 0.2% month1) and filtered/ high-flow (3.1 0.2% month1) groups. Enhanced growth rates in high-flow is consistent with predictions in environments where high convection leads to increased mass flux and thereby enhanced rates of photosynthesis (e.g. Patterson et al., 1991; Bruno and Edmunds, 1998). The marginally higher rate of calcification in the low (moderate) sediment regime under high-flow compared to the filtered/high-flow group may be due to enhanced uptake of inorganic carbon (e.g. Marubini and Thake, 1999) leaching from the sediment, and potentially due to the small amount of nitrogen and organic carbon bound to the sediment, providing a marginal food source (Anthony, 1999; Rosenfeld et al., 1999; Anthony and Fabricius, 2000). Buoyant weights could not be obtained for field controls on day 1 because weather conditions did not allow redeployment of weighed corals. Variation in lipid contents among sediment and flow treatments in the laboratory varied less than 4% (coefficient of variation,
Table 1 Physiological responses of Turbinaria mesenterina to 5 weeks of sediment and flow treatments. Colony growth was measured as the percent change in buoyant weight per month, and energy stores were measured as tissue lipid content on the last day of the experiment. Maximum quantum yield (Fv/Fm) was used as an indicator of the photosynthetic efficiency of symbiotic algae, also measured on the last day of the experiment. For comparison, lipid contents and Fv/Fm values for field controls on the last day are also depicted (field) but were not included in the analysis. See Table 2 for summary results of analyses Sediment load
Flow regime Low Mean SE
High n
Mean SE
n
Growth rate (% month1)
Filtered Low High
3.7 0.2 3.5 0.2 3.0 0.2
12 11 12
3.1 0.2 3.9 0.1 3.5 0.3
12 11 11
Energy stores (mg cm2)
Filtered Low High Field
7.7 0.6 8.5 0.9 7.4 0.6 8.8 0.6
11 12 12 20
6.9 0.7 8.0 0.6 7.6 0.8
11 11 12
Fv/Fm
Filtered Low High Field
0.59 0.02 0.60 0.01 0.60 0.02 0.55 0.01
36 35 34 80
0.61 0.01 0.59 0.02 0.59 0.01
33 36 33
J.J. Sofonia, K.R.N. Anthony / Estuarine, Coastal and Shelf Science 78 (2008) 748–752 Table 2 Summary results of two-way ANOVA for effects of sediment load and flow environment on the three key physiological responses in Turbinaria mesenterina. Data for each dependent variable were normally distributed and variances were homogeneous, hence data were analysed untransformed. Tanks (n ¼ 3) were used as replicates Source of variation
df
Skeletal growth rate (% weight increase)
Lipid contents (mg cm2)
F
P
F
P
F
P
Sediment Flow Sediment flow
2 1 2
2.34 0.25 4.57
0.129 0.624 0.033
0.70 0.25 0.12
0.515 0.628 0.888
0.83 1.63 0.91
0.459 0.226 0.428
Fv/Fm (dimensionless)
Tables 1 and 2). This is a surprising result given that previous studies have found that energy stores in particular are highly sensitive to environmental variation (Anthony et al., 2002; Rodrigues and Grottoli, 2007). Also, lipid contents of coral colonies in the experimental tank populations (7.4–8.5 mg cm2) were 3–16% lower than those of the field controls (8.8 2.7 mg cm2). Because clean sediment with low nutritional value was used in the laboratory, and corals were not fed zooplankton during the experiment, the higher lipid content in the field might reflect the greater availability of particulate organic matter (heterotrophic environment) in situ. The high concentrations of particulate matter on nearshore reefs in the Great Barrier Reef lagoon (e.g. Sammarco and Crenshaw, 1984; Larcombe et al., 1995) represent a significant food source for some coral species (Anthony, 1999), in Turbinaria and Acropora contributing to significantly higher lipid stores in nearshore compared to offshore conspecifics (Anthony, 2006). Lipid contents of experimental corals in the laboratory and in the field declined 13–27% relative to the lipid contents of field samples taken from large colonies at the initial day of collecting (10.1 2.7 mg cm2). This decline is most likely due to energy reserves allocated to healing of the injuries (Meesters et al., 1994; Hall, 1997) inflicted on the day of collecting. However, because the physical injuries were similar for all colonies used in the experiment, the lowered lipid levels were unlikely to bias the outcome of the experiment. Indeed, allocation of energy reserves to repair is likely to reduce the overall physiological resistance to stressors (by competing with resources for maintenance), and may have made the experimental corals more susceptible to sediment stress than unhandled coral colonies in situ. Similar to the pattern for the lipid contents, maximum quantum yield (Fv/Fm) showed no effect of sediment or flow treatments (Tables 1 and 2). Importantly, high values of Fv/Fm (0.60–0.75)
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across treatments were consistent with those of healthy (unstressed) symbioses reported in previous studies (Hoegh-Guldberg and Jones, 1999; Jones et al., 1999; Ralph et al., 1999). This is surprising, given that Fv/Fm has been shown to be sensitive to sediment stress for other coral species, mainly due to the shading effect of sediment deposited on the colony surface. For instance, Philipp and Fabricius (2003) observed a 50% decline in Fv/Fm of the plating Montipora peltiformis within 24–36 h of exposure to sediment loads (in stagnant conditions) similar to the maxima used in this study (w100 mg cm2). A likely explanation for the consistently high Fv/ Fm values in this study is that sedimentation does not produce significant damage to the photosystem of corals, unless the corals are unable to clear themselves of accumulated material and there is a corresponding onset of tissue necrosis. In this study, colonies of Turbinaria mesenterina were able to clear themselves within 4–5 h of sediment doses greater than 100 mg cm2 (Fig. 2). These sediment clearance rates are consistent with the highest rates reported for corals (Stafford-Smith, 1993). Such rapid sediment clearing is likely to prevent tissue damage and allows sufficient light to symbionts to alleviate stress from suboptimal shading. Observations suggested that sediment removal in T. mesenterina is both active, i.e. as cilia-mediated transport of sediment-laden mucus across the surface, as well as passive due to morphology, the latter reducing the energy cost associated with sediment clearing (Lasker, 1980). Specifically, corallites are raised 1–2 mm above the coenosarc (Veron, 2000), which facilitates gravity- or flow-induced removal of sediment from the polyps. In conclusion, our results demonstrate that Turbinaria mesenterina is physiologically tolerant to sediment loads an order of magnitude greater than those occurring during most resuspension episodes on turbid-zone reef areas of the nearshore Great Barrier Reef. Neither high-flow conditions (potentially causing scouring of coral tissues) nor stagnant conditions (leading to sediment deposition, reduced irradiance and reduced mass transfer) had adverse effects on coral physiology at high-sediment loads. The success of T. mesenterina in high-turbidity areas of the inner Great Barrier Reef, as manifest by extensive monospecific assemblages, is likely to be driven primarily by the high-sediment tolerance as found in this study, and secondarily by its ability to utilize sediment as an energy and nutrient source (Anthony, 2006). Other coral species have also demonstrated tolerance for high-sediment loads, such as Goniastrea retiformis which is abundant on muddy reef flats (Anthony and Fabricius, 2000). However, the strong photo-physiological stress responses reported for other coral species in compatible sediment experiments (Philipp and Fabricius, 2003) in comparison with the almost complete lack of physiological responses of T. mesenterina to
Fig. 2. Sediment clearing by Turbinaria mesenterina colony in the low-flow regime following application of a heavy sediment load (w100 mg cm2). Time sequence: (A) t ¼ 0 h, (B) t ¼ 1.5 h, and (C) t ¼ 4.5 h. All colonies in the trial (n ¼ 12) cleared themselves completely within 5 h.
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extreme sediment conditions in this study, suggests that T. mesenterina is one of the most well-adapted species to high-sediment environments. If sediment regimes on coastal reefs intensify due to increased erosion and export of terrigenous material from river catchments (e.g. Furnas, 2003; McCulloch et al., 2003; Fabricius, 2005; McKergow et al., 2005), and potentially increased frequency and severity of sediment resuspension events associated with intensified storm activity (e.g. Emanuel, 2005), coral taxa with highsediment tolerances, such as Turbinaria, are likely to be the key players on future coastal coral reefs. Acknowledgments This study was supported by a grant from the Australian Research Council to KRNA. We thank A. Pharaoh for help in the field, and B. Leggatt, T. Ridgeway, S. Weeks and G. Diaz-Pullido for comments on the manuscript. This is a contribution from the ARC Centre of Excellence for Coral Reef Studies. References Acevedo, R., Morelock, J., Olivieri, R.A., 1989. Modification of coral reef zonation by terrigenous sediment stress. Palaios 4, 92–100. Anthony, K.R.N., 1999. Coral suspension feeding on fine particulate matter. Journal of Experimental Marine Biology and Ecology 232, 85–106. Anthony, K.R.N., 2006. Enhanced energy status of corals on coastal, high-turbidity reefs. Marine Ecology Progress Series 319, 111–116. Anthony, K.R.N., Fabricius, K.E., 2000. Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. Journal of Experimental Marine Biology and Ecology 252, 221–253. Anthony, K.R.N., Connolly, S.R., 2004. Environmental limits to growth: physiological niche boundaries of corals along turbidity-light gradients. Oecologia 141, 373–384. Anthony, K.R.N., Connolly, S.R., Willis, B.L., 2002. Comparative analysis of energy allocation to tissue and skeletal growth in corals. Limnology and Oceanography 47, 1417–1429. Anthony, K.R.N., Ridd, P.V., Orpin, A., Larcombe, P., Lough, J.M., 2004. Temporal variation in light availability in coastal benthic habitats: effects of clouds, turbidity and tides. Limnology and Oceanography 49, 2201–2211. Anthony, K.R.N., Hoogenboom, M.O., Connolly, S.R., 2005. Adaptive variation in coral geometry and the optimization of internal colony light climates. Functional Ecology 19, 17–26. Aronson, R.B., Precht, W.F., Macintyre, I.G., 1998. Extrinsic control of species replacement on a Holocene reef in Belize: the role of coral disease. Coral Reefs 17, 223–230. Brown, B.E., 1997. Disturbances to reefs in recent times. In: Birkeland, C. (Ed.), Life and Death of Coral Reefs. Chapman and Hall Inc., New York, pp. 354–385. Bruno, J.F., Edmunds, P.J., 1998. Metabolic consequences of phenotypic plasticity in the coral Madracis mirabilis (Duchassaing and Michelotti) – the effect of morphology and water flow on aggregate respiration. Journal of Experimental Marine Biology and Ecology 229, 187–195. Buddemeier, R.W., Kinzie, R.A., 1976. Coral growth. Oceanographic and Marine Biology Annual Reviews 14, 183–225. Dennison, W.C., Barnes, D.J., 1988. Effects of water motion on coral photosynthesis and calcification. Journal of Experimental Marine Biology and Ecology 115, 67–77. Done, T.J., 1982. Patterns in the distribution of coral communities across the central Great Barrier Reef. Coral Reefs 1, 95–107. Emanuel, K., 2005. Increasing destructiveness of tropical cyclones over the past 30 years. Nature 436, 686–688. Fabricius, M., 2005. Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Marine Pollution Bulletin 50, 125–146. Furnas, M., 2003. Catchments and Corals: Terrestrial Runoff to the Great Barrier Reef. Australian Institute of Marine Science, Townsville, Australia, 320 pp. Grottoli, A.G., Rodrigues, L.J., Palardy, J.E., 2006. Heterotrophic plasticity and resilience in bleached corals. Nature 440, 1186–1189. Hall, V.R., 1997. Interspecific differences in the regeneration of artificial injuries on scleractinian corals. Journal of Experimental Marine Biology and Ecology 212, 9–23.
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Estuarine, Coastal and Shelf Science journal homepage: www.elsevier.com/locate/ecss
High-sediment tolerance in the reef coral Turbinaria mesenterina from the inner Great Barrier Reef lagoon (Australia) Jeremy J. Sofonia, Kenneth R.N. Anthony * School of Marine Biology and Aquaculture, James Cook University, Townsville, Queensland 4811, Australia
a r t i c l e i n f o
a b s t r a c t
Article history: Received 2 May 2007 Accepted 19 February 2008 Available online 12 March 2008
Sedimentation is an important stressor on coral reefs subjected to run-off, dredging and resuspension events. Reefs with a history of high-sediment loads tend to be dominated by a few tolerant coral species. A key question is whether such species live close to their tolerance thresholds or near their niche optima. Here, we analyse experimentally the sediment tolerance of a spatially dominant coral, Turbinaria mesenterina (Dendrophylliidae), at nearshore reefs in the central Great Barrier Reef lagoon. Testing was conducted in a 5-week tank experiment under manipulated sediment loading and flow conditions. Physiological stress was assessed based on the behaviour of three key response variables: skeletal growth rate, energy reserves (lipid content) and photosynthetic performance. Because sediment effects are likely to vary between flow regimes, sediment and flow responses were tested using a full factorial design. Sediment loads greater than 110 mg cm2 had no effect on any of the physiological variables, regardless of flow (0.7–24 cm s1). Turbinaria mesenterina is thus tolerant to sediment loads an order of magnitude higher than most severe sediment conditions in situ. Likely mechanisms for such tolerance are that: (1) colonies covered in sediment (60–120 mm) in low-flow were able to clear themselves rapidly (within 4– 5 h); and (2) sediment provides a source of food. These results suggest that intensified sediment regimes on coastal reefs may shift coral communities towards dominance by a few well-adapted species. Ó 2008 Elsevier Ltd. All rights reserved.
Keywords: physiological tolerance stress growth rate lipid calcification Great Barrier Reef scleractinian coral Regional index terms: Australia Queensland Great Barrier Reef Cleveland Bay Magnetic Island Cockle Bay
1. Introduction Sedimentation is one of the most important disturbance factors on coastal coral reefs worldwide (Rogers, 1990; Brown, 1997). Rates of sedimentation and turbidity levels on coastal reefs have in many areas increased 5–10-fold during the past 2–3 decades, mainly due to increased run-off from the land to the sea (Wilkinson, 2002; McCulloch et al., 2003; Fabricius, 2005). However, in many coastal reef areas where high levels of run-off and resuspension are in part due to natural processes (Kleypas, 1996) reef assemblages have developed under high natural sediment loads for millennia (Larcombe et al., 1995). Often, coral assemblages on nearshore turbid-zone reefs differ in composition from that of more offshore clear-water reefs (e.g. Done, 1982; Acevedo et al., 1989), potentially reflecting differences in species niche characteristics (Anthony and Connolly, 2004).
* Corresponding author. Present address: Centre for Marine Studies, The University of Queensland, St Lucia, Queensland 4072, Australia. E-mail address: [email protected] (K.R.N. Anthony). 0272-7714/$ – see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2008.02.025
Coral species that are well adapted to high-sediment loads, for example by utilisation of particulate matter as a food source (Anthony, 1999; Rosenfeld et al., 1999), acclimatization to shifting light regimes (Anthony et al., 2004) or by energy-efficient mechanisms of sediment handling are likely to have a selective advantage on high-turbidity reefs (Lasker, 1980). As many coastal reefs become subjected to increasing sediment loads due to coastal developments, poor land use practices (e.g. Furnas, 2003; McKergow et al., 2005), and increased frequency of severe storms (e.g. Emanuel, 2005), reef communities may potentially shift towards assemblages dominated by sediment-tolerant species. Studies of phase shifts on coral reefs have mainly been concerned with transitions from coral to algal dominance (e.g. Hughes, 1994; McClanahan et al., 2002) and less so with mechanisms driving shifts in spatial dominance between coral taxa (Aronson et al., 1998). Here, we investigate experimentally the tolerance of the coral Turbinaria mesenterina to an extreme range of sediment loads. Colonies of T. mesenterina form whorls or plates (foliose) with pronounced ecomorph variation ranging from horizontal plates in deep water to tightly packed cones in shallow water (Anthony et al.,
J.J. Sofonia, K.R.N. Anthony / Estuarine, Coastal and Shelf Science 78 (2008) 748–752
2005). The species has been recorded along turbid reefs over a wide geographic area (Veron, 2000), ranging from Japan (Ueshima and Ohno, 1997) to southern China (Zou, 1982) and is spatially dominant on nearshore reefs in the central section of Australia’s Great Barrier Reef (Done, 1982; Van Woeski and Don, 1997). In the most turbid areas on the western (nearshore) side of Magnetic Island (Cleveland Bay, North Queensland), T. mesenterina covers nearly 100% of the reef from the crest to the deep slope (Fig. 1). To characterise in detail the physiological response profile of T. mesenterina to high-sediment loads we examined changes in three key physiological variables during a 5-week experiment: (1) skeletal growth rate; (2) maximum quantum yield (photosynthetic efficiency) of symbionts; and (3) lipid content (energy stores). Skeletal growth rate, as change in buoyant weight or linear extension, is the most commonly used metric for coral growth (e.g. Buddemeier and Kinzie, 1976; Spencer-Davies, 1989) and maximum quantum yield is a proxy for photosynthetic performance (e.g. Ralph et al., 1999). Lipid content provides an estimate of energy storage and is thus a proxy for the trophic value of the coral’s recent environmental conditions (Anthony and Fabricius, 2000; Grottoli et al., 2006). For example, a negative energy balance due to a greater expenditure on sediment handling than energy intakes via phototrophy and heterotrophy (Anthony and Connolly, 2004) will lead to depletion of lipid stores. Because effects of sediment loading on the coral biology are likely to vary with flow regime (i.e. as deposition under low-flow and resuspension under high-flow), each sediment
Fig. 1. (A) Central section of the Great Barrier Reef lagoon (North Queensland, Australia). The site of coral collecting and deployment of field controls in Cockle Bay (Magnetic Island) is marked x. (B) Turbinaria mesenterina, forming large stands with up to 90% cover in 1–5 m depth.
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treatment was conducted under stagnant as well as high-flow conditions. Key physiological processes such as rate of respiration, exchange rate of dissolved nutrients and particle encounter rates vary greatly with flow environment (e.g. Dennison and Barnes, 1988; Patterson et al., 1991). We test the hypotheses that: (1) all physiological response variables are reduced under extremely high-sediment loads, but that (2) sediment effects will be stronger in depositional (low-flow) compared to in resuspension (high-flow) regimes. By using sediment with low (<1%) organic carbon content, we did not expect particle heterotrophy to compensate for energy costs associated with any of the sediment regimes. 2. Materials and methods 2.1. Study site and coral collecting Corals were collected from the fringing reef in Cockle Bay on the western side of Magnetic Island, North Queensland, Australia (1911.21500 S, 146 48.95000 E) on May 5 (Austral winter), 2003 (Fig. 1). Cockle Bay is one of the most turbid reefs in the nearshore region of the Great Barrier Reef lagoon (Anthony et al., 2004), in part due to frequent resuspension of sediment deposits in the shallow Cleveland Bay (Larcombe et al., 1995) and downstream transport of mud from adjacent bays around Magnetic Island. Coral communities on the reef crest and slope (1–6 m depth) in Cockle Bay and adjacent bays are characterised by high abundance of Turbinaria mesenterina. In Cockle Bay in particular, this species forms large monospecific stands that may cover >90% of the reef (Fig. 1). Approximately 100 fragments (around 8 cm by 8 cm) were collected from large colonies of Turbinaria mesenterina, selected randomly, at 2–4 m depth (below lowest astronomical tides) in Cockle Bay. The fragments were cut from colony peripheries using surgical bone cutters. Based on colour morph variation among samples at least 10 different genotypes were represented. To ensure that all experimental corals had similar light history, corals were collected exclusively from colonies in open (unshaded) habitats. At the broken end of each fragment, a 2 mm hole was drilled through the coral and used for attachment to stands using a cable tie. Each stand consisted of an arched piece of PVC (8 cm by 8 cm) with a 2 mm hole in one end so the coral could be attached horizontally to the arched upper side of the stand. To allow the corals to recover from handling stress, they were left on racks (2–4 m depth) in the field for 9 weeks at which time new polyps had developed along the broken edges. During the recovery period and experimental phase, downwelling irradiance in situ at the level of the experimental colonies (fragments) ranged between 50 and 300 mmol quanta m2 s1 (daily averages), based on continuous monitoring using two light loggers (Dataflow 392 recorders with cosine corrected PAR sensors) attached to the coral racks. This was consistent with the long-term range for the location (Anthony et al., 2004). The sensors were equipped with automated wipers to prevent fouling. Rates of sedimentation at the site approximated 7– 12 mg cm2 d1 (dry weight of GF/C filtered material) estimated from weekly deployment of six sediment traps (3.25 cm diameter and 30 cm long, Jurg, 1996) and correspond to anticipated winter rates with no significant storm events (Larcombe et al., 1995, 2001; Anthony et al., 2004). Flow speeds in situ were estimated using dissolution rates of plaster blocks (e.g. Jokiel and Morrissey, 1993). Six hemispherical blocks (base diameter 53 mm) of known dry weights were placed on the coral racks at three occasions (1-day exposures). Dissolution rate was converted to flow speed after calibrating blocks in a flow chamber (n ¼ 8) with known flow velocities determined by particle tracking. Flow rates at the sites ranged from 3 to 11 cm s1.
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2.2. Laboratory experiment Eighty of the experimental coral colonies were transported to the research aquarium facility at James Cook University. The remaining 20 corals were left on the racks at the reef site as field controls. At the indoor experimental facility, 72 of the corals were randomly distributed among 18 tanks (25 l each, measuring 35 cm long, 25 cm wide and 20 cm tall) connected independently to an inflow of filtered seawater (35 ppt, 23–24 C). The remaining eight coral fragments were immediately frozen for later analysis for baseline lipid concentrations. An array of six metal halide lamps (each 400 W, EYE, Japan) was suspended 50 cm above the tanks to obtain a light level of w300 mmol m2 s1, which corresponds to the average growth irradiance at the field site (see also Anthony et al., 2004). The lamps were connected to timers set to a 10-h daylight cycle. The experimental design consisted of two fixed factors with three levels of sediment loading and two flow regimes. Tanks were arranged in a randomised block design to account for potential heterogeneity in light regime and water inflow among tank positions. Each treatment level was replicated by three tanks; each tank holding four corals. In each of the high-flow tanks, two recirculating pumps (w950 l h1, Aquaclear 402, Italy) generated a turbulent flow environment of 24 4 cm s1, sufficient to keep added sediment in suspension. In the low-flow tanks, flow speeds were 0.7 0.1 (SE) cm s1 due only to convection caused by inflow of seawater. Fine sediment was applied manually three times daily (at 7–8 AM; 12–1 PM; and 5–6 PM) to the sediment treatment tanks for 34 days. The sediment was collected from the surface layer near the field site in Cockle Bay using an airlift. Particle sizes ranged from 60 to 120 mm as determined by a laser particle sizer (Malvern Instruments, UK), representative of sandy silts (Larcombe et al., 2001). To avoid contamination of the aquarium system with organic material, and potential interactions with the flow and sedimentation effects, the sediment was rinsed in freshwater, stored dry and rehydrated 1 h prior to use. The processed sediment was therefore likely to have lower nutritional value than that in the field. Similar type sediment used in previous experiments had an organic carbon content of 0.5–1.5%, determined using a CHN Analyzer (Shimadzu 5000), and contained 0.1–0.2% nitrogen determined using an Antec 720 C/N Analyzer (Anthony, unpublished data). Six tanks were dosed with a high-sediment load of 110 27 mg cm2, six tanks with a moderate load of 16 4 mg cm2, and six tanks received filtered (5 mm) seawater only with a background sedimentation rate of 0.8 0.3 mg cm2. Sedimentation rates within the tanks were estimated using triplicate cylindrical sediment traps (3.6 cm diameter, 4.5 cm tall) placed between coral colonies on the tank floor. 2.3. Coral responses Coral stress responses were assessed using three physiological variables: (1) rate of skeletal growth; (2) tissue lipid content; and (3) maximum quantum yield (photosynthetic efficiency) of algal symbionts. Skeletal growth rates were determined as differences in buoyant weight between the first and last day of the experiment (Spencer-Davies, 1989). Tissue lipid content was determined using a technique modified from that of Harland et al. (1992) (see also Anthony and Fabricius, 2000). Pre-experimental lipid concentrations were obtained from assays of microcolonies selected randomly from the population of experimental corals on the first day of the experiment. Stress responses of dinoflagellate symbionts were assessed by estimating changes in the maximum quantum yield (Fv/Fm) of photosystem II (Hoegh-Guldberg and Jones, 1999; Jones et al., 1999; Ralph et al., 1999) using a pulse amplitude modulation (PAM)
fluorometer (DIVING PAM, Walz, Germany). PAM assays were conducted on dark-acclimated colonies (before sunrise) on the first and last days of the experiment. 2.4. Data analysis Data were analysed using two-way analysis of variance (ANOVA), using sediment and flow regime as main factors. Data for individual corals were pooled within each tank, thus using tanks as replicates. Analyses were followed by Tukey’s multiple comparison tests to identify significant differences between individual treatment groups. Assumptions of normality were tested using Kolmogorov–Smirnov one-sample tests and homogeneity of variances was tested using Levene’s test (Sokal and Rohlf, 1995). 3. Results and discussion None of the physiological stress/health indicators (skeletal growth rate, lipid content and maximum quantum yield) assayed for Turbinaria mesenterina showed significant responses to the sediment or flow treatments as main factors (Tables 1 and 2). Skeletal growth rates (as relative changes in buoyant weight, Table 1) varied marginally among three treatment combinations only: corals in the low-sediment/high-flow treatment had around 30% higher growth rates (3.9 0.1% month1) than corals in the high-sediment/low-flow (3.0 0.2% month1) and filtered/ high-flow (3.1 0.2% month1) groups. Enhanced growth rates in high-flow is consistent with predictions in environments where high convection leads to increased mass flux and thereby enhanced rates of photosynthesis (e.g. Patterson et al., 1991; Bruno and Edmunds, 1998). The marginally higher rate of calcification in the low (moderate) sediment regime under high-flow compared to the filtered/high-flow group may be due to enhanced uptake of inorganic carbon (e.g. Marubini and Thake, 1999) leaching from the sediment, and potentially due to the small amount of nitrogen and organic carbon bound to the sediment, providing a marginal food source (Anthony, 1999; Rosenfeld et al., 1999; Anthony and Fabricius, 2000). Buoyant weights could not be obtained for field controls on day 1 because weather conditions did not allow redeployment of weighed corals. Variation in lipid contents among sediment and flow treatments in the laboratory varied less than 4% (coefficient of variation,
Table 1 Physiological responses of Turbinaria mesenterina to 5 weeks of sediment and flow treatments. Colony growth was measured as the percent change in buoyant weight per month, and energy stores were measured as tissue lipid content on the last day of the experiment. Maximum quantum yield (Fv/Fm) was used as an indicator of the photosynthetic efficiency of symbiotic algae, also measured on the last day of the experiment. For comparison, lipid contents and Fv/Fm values for field controls on the last day are also depicted (field) but were not included in the analysis. See Table 2 for summary results of analyses Sediment load
Flow regime Low Mean SE
High n
Mean SE
n
Growth rate (% month1)
Filtered Low High
3.7 0.2 3.5 0.2 3.0 0.2
12 11 12
3.1 0.2 3.9 0.1 3.5 0.3
12 11 11
Energy stores (mg cm2)
Filtered Low High Field
7.7 0.6 8.5 0.9 7.4 0.6 8.8 0.6
11 12 12 20
6.9 0.7 8.0 0.6 7.6 0.8
11 11 12
Fv/Fm
Filtered Low High Field
0.59 0.02 0.60 0.01 0.60 0.02 0.55 0.01
36 35 34 80
0.61 0.01 0.59 0.02 0.59 0.01
33 36 33
J.J. Sofonia, K.R.N. Anthony / Estuarine, Coastal and Shelf Science 78 (2008) 748–752 Table 2 Summary results of two-way ANOVA for effects of sediment load and flow environment on the three key physiological responses in Turbinaria mesenterina. Data for each dependent variable were normally distributed and variances were homogeneous, hence data were analysed untransformed. Tanks (n ¼ 3) were used as replicates Source of variation
df
Skeletal growth rate (% weight increase)
Lipid contents (mg cm2)
F
P
F
P
F
P
Sediment Flow Sediment flow
2 1 2
2.34 0.25 4.57
0.129 0.624 0.033
0.70 0.25 0.12
0.515 0.628 0.888
0.83 1.63 0.91
0.459 0.226 0.428
Fv/Fm (dimensionless)
Tables 1 and 2). This is a surprising result given that previous studies have found that energy stores in particular are highly sensitive to environmental variation (Anthony et al., 2002; Rodrigues and Grottoli, 2007). Also, lipid contents of coral colonies in the experimental tank populations (7.4–8.5 mg cm2) were 3–16% lower than those of the field controls (8.8 2.7 mg cm2). Because clean sediment with low nutritional value was used in the laboratory, and corals were not fed zooplankton during the experiment, the higher lipid content in the field might reflect the greater availability of particulate organic matter (heterotrophic environment) in situ. The high concentrations of particulate matter on nearshore reefs in the Great Barrier Reef lagoon (e.g. Sammarco and Crenshaw, 1984; Larcombe et al., 1995) represent a significant food source for some coral species (Anthony, 1999), in Turbinaria and Acropora contributing to significantly higher lipid stores in nearshore compared to offshore conspecifics (Anthony, 2006). Lipid contents of experimental corals in the laboratory and in the field declined 13–27% relative to the lipid contents of field samples taken from large colonies at the initial day of collecting (10.1 2.7 mg cm2). This decline is most likely due to energy reserves allocated to healing of the injuries (Meesters et al., 1994; Hall, 1997) inflicted on the day of collecting. However, because the physical injuries were similar for all colonies used in the experiment, the lowered lipid levels were unlikely to bias the outcome of the experiment. Indeed, allocation of energy reserves to repair is likely to reduce the overall physiological resistance to stressors (by competing with resources for maintenance), and may have made the experimental corals more susceptible to sediment stress than unhandled coral colonies in situ. Similar to the pattern for the lipid contents, maximum quantum yield (Fv/Fm) showed no effect of sediment or flow treatments (Tables 1 and 2). Importantly, high values of Fv/Fm (0.60–0.75)
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across treatments were consistent with those of healthy (unstressed) symbioses reported in previous studies (Hoegh-Guldberg and Jones, 1999; Jones et al., 1999; Ralph et al., 1999). This is surprising, given that Fv/Fm has been shown to be sensitive to sediment stress for other coral species, mainly due to the shading effect of sediment deposited on the colony surface. For instance, Philipp and Fabricius (2003) observed a 50% decline in Fv/Fm of the plating Montipora peltiformis within 24–36 h of exposure to sediment loads (in stagnant conditions) similar to the maxima used in this study (w100 mg cm2). A likely explanation for the consistently high Fv/ Fm values in this study is that sedimentation does not produce significant damage to the photosystem of corals, unless the corals are unable to clear themselves of accumulated material and there is a corresponding onset of tissue necrosis. In this study, colonies of Turbinaria mesenterina were able to clear themselves within 4–5 h of sediment doses greater than 100 mg cm2 (Fig. 2). These sediment clearance rates are consistent with the highest rates reported for corals (Stafford-Smith, 1993). Such rapid sediment clearing is likely to prevent tissue damage and allows sufficient light to symbionts to alleviate stress from suboptimal shading. Observations suggested that sediment removal in T. mesenterina is both active, i.e. as cilia-mediated transport of sediment-laden mucus across the surface, as well as passive due to morphology, the latter reducing the energy cost associated with sediment clearing (Lasker, 1980). Specifically, corallites are raised 1–2 mm above the coenosarc (Veron, 2000), which facilitates gravity- or flow-induced removal of sediment from the polyps. In conclusion, our results demonstrate that Turbinaria mesenterina is physiologically tolerant to sediment loads an order of magnitude greater than those occurring during most resuspension episodes on turbid-zone reef areas of the nearshore Great Barrier Reef. Neither high-flow conditions (potentially causing scouring of coral tissues) nor stagnant conditions (leading to sediment deposition, reduced irradiance and reduced mass transfer) had adverse effects on coral physiology at high-sediment loads. The success of T. mesenterina in high-turbidity areas of the inner Great Barrier Reef, as manifest by extensive monospecific assemblages, is likely to be driven primarily by the high-sediment tolerance as found in this study, and secondarily by its ability to utilize sediment as an energy and nutrient source (Anthony, 2006). Other coral species have also demonstrated tolerance for high-sediment loads, such as Goniastrea retiformis which is abundant on muddy reef flats (Anthony and Fabricius, 2000). However, the strong photo-physiological stress responses reported for other coral species in compatible sediment experiments (Philipp and Fabricius, 2003) in comparison with the almost complete lack of physiological responses of T. mesenterina to
Fig. 2. Sediment clearing by Turbinaria mesenterina colony in the low-flow regime following application of a heavy sediment load (w100 mg cm2). Time sequence: (A) t ¼ 0 h, (B) t ¼ 1.5 h, and (C) t ¼ 4.5 h. All colonies in the trial (n ¼ 12) cleared themselves completely within 5 h.
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