Sediment: stress factor or food source for reef corals

Anthony, Kenneth Roald Nies (1999) Sediment: stress factor or food source for reef corals. PhD thesis, James Cook University.

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Abstract

Nearshore reefs in many parts of the tropics are subject to high concentrations of suspended sediment, conditions that impose stress on symbiotic reef organisms by reducing light for photosynthesis and smothering of tissues. The formation of extensive fringing reefs in many nearshore turbid areas, however, challenges the dogma that reef corals need clear water and bright light for survival and substantive growth. The central hypothesis of this thesis is that suspended sediment is also a food source for corals. Specifically, I test the hypotheses that (1) corals ingest and assimilate suspended sediment in proportion to availability, (2) that corals from nearshore turbid habitats have higher sediment-feeding capacities than corals from offshore oligotrophic habitats in accordance with optimal diet theory, and (3) that high rates of sediment feeding by some species may energetically offset effects of reduced photosynthesis and sediment stress. The implications of these hypotheses are that sediment feeding may provide an energetic explanation for the presence of coral reefs in turbid environments.

To investigate the capacity of corals to utilise suspended particulate matter (SPM) as a food and energy source in different sediment regimes, I quantified ingestion and assimilation of ¹⁴4C-labelled SPM for four common species of scleractinian coral on the Great Barrier Reef (GBR) over a wide range of SPM concentrations (1-30 mg dry weight [dw]/L ). Ingestion rates of three species (Pocillopora damicornis, Montipora digitata, and Acropora millepora) increased linearly over the full range of SPM concentrations. Only one species (Pontes cylindrica) conformed to traditional saturation-kinetic models (Michaelis-Menten) with ingestion rates reaching maximum at moderate SPM concentrations (4-8 mg dw/L). All study species assimilated a major proportion of the ingested label, but assimilation efficiency was inversely related to SPM concentration in agreement with the findings of previous studies. At low SPM concentration (1 mg dw/L), assimilation efficiencies ranged from 89 to 95% of the ingested SPM, which are among the highest reported for suspension feeders, decreasing to 40-50% at the highest concentration.

The maximum rate of carbon assimilated from SPM can cover less than 5% of basic metabolic costs, which is not significantly different from reported contributions of zooplankton feeding to coral energy budgets. More importantly, SPM feeding at high particle concentrations may cover up to half of the carbon and a third of the nitrogen used in tissue growth.

In order to test the hypothesis that corals from turbid nearshore areas have greater capacity to utilise sediment as a food source than conspecifics from less turbid midshelf areas I used two common species with a widespread distribution across the GBR lagoon (P. damicornis and A. millepora). Samples from turbid reefs of both coral species fed 1-3 times more efficiently on SPM than did conspecifics from midshelf reefs. Rates of particle ingestion were a linear function of particle load for both inshore and offshore groups, indicating no significant saturation within the concentration range 1-30 mg dw/L. Assimilation efficiency of particulate ¹⁴4C was maximised for midshelf A. millepora at the lowest sediment concentration, suggesting a more efficient heterotrophy in oligotrophic habitats. Based on feeding-response curves, assimilation efficiencies, and published records of ambient particle concentrations, representatives of these species on turbid inshore reefs are 10-20 times more heterotrophic on suspended sediment than their conspecifics on less turbid midshelf reefs.

In a two-month experiment involving manipulated sediment and light treatments, I analysed experimentally the effects of different light and SPM regimes on the growth rates of two species of scleractinian coral. A ten-fold higher sediment-feeding capacity of G. retiformis compared to P. cylindrica provided an excellent opportunity to test the ecological and physiological implications of sediment feeding for the energy budgets of symbiotic cnidarians in turbid environments. To provide an energetic analysis of growth patterns across treatments, I quantified changes in the energetics of total tissue mass, lipid contents, and skeletal mass.

Shading corresponding to 16 mg dw SPM/L at 3-4 m depth resulted in reduced growth rates in both species. However, the two species showed contrasting patterns of energy investment across SPM treatments (<1, ~4, ~16 mg dw/L and controls ~2 mg dw/L). Growth rates of G. retiformis increased monotonically with SPM concentration, and growth rates at the maximum particle load were almost twice those of conspecifics in filtered seawater. Importantly, growth rates of shaded and unshaded G. retiformis did not differ significantly at high SPM concentrations, but growth rates of corals from both these treatment groups were significantly higher than those of shaded and unshaded corals in particle-depleted treatments. Conversely, P. cylindrica showed maximum growth rates at the intermediate SPM concentration (~4 mg/L), and the combination of shading and maximum particle load resulted in negative tissue growth in this species. Energy investment was strongly partitioned between tissue and skeletal growth in both species, with preference given to tissue growth in corals with high overall rates of energy investment. Minor differences in skeletal growth were primarily explained by differences in light level.

The results of this study indicate that high turbidity enhances growth in G. retiformis to the extent that it compensates for reduced light, whereas a similar high-turbidity regime causes stress in P. cylindrica. At intermediate sediment concentrations, however, the nutritional effect of sediment is greater than its stress effect on P. cylindrica.

As a corollary to the growth study, I investigated the physiological processes underlying the different growth patterns displayed by the two species. Specifically, I quantified the relative contributions of sediment feeding and photosynthesis to the energy budget in the range of turbidity regimes used in the growth study. Further, I analysed the importance of heterotrophic plasticity of corals in adapting to prevailing turbidity regimes with implications for the width of physiological niches.

In G. retiformis, sediment feeding more than compensated for the reduction in photosynthesis and sediment removal at high sediment concentrations (~16 mg dw/L), resulting in a positive total carbon balance despite shading (corresponding to 16 mg dw/L at 3-4 m depth). Part of this compensation was enabled by a doubling of the feeding capacity at a given particle availability in response to a history of shading, a mechanism not previously reported for symbiotic invertebrates. In contrast, the feeding capacity of P. cylindrica increased only marginally in response to high sediment loads and its total carbon budget remained in deficit in shaded treatments. Multiple regression analysis indicated that > 85% of the variation in energy investment into growth of G. retiformis was explained jointly by the variation in energy acquisition through sediment feeding (r-part = 72%) and photosynthesis (r-part = 92%). A similar analysis for P. cylindrica indicated an almost exclusive dependence on phototrophy. Using the data from the prolonged turbidity experiment, a predictive model of energy budgets as a function of SPM concentration and depth indicated that particle feeding by G. retiformis can effectively increase the depth at which the energy balance remains positive in a turbid environment.

In summary, SPM represents a quantitatively important food source for most coral species, but concentration thresholds at which SPM becomes a stress factor varies among species. Enhanced rates of sediment feeding in response to prolonged increased turbidity in some species suggest that corals are able to alter their trophic strategies to optimise the nutritional potential of their habitat. Heterotrophic plasticity of G. retzformis, P. damicornis and A. millepora may be important for maintaining the energy balance of corals on reefs that are subject to high or seasonally fluctuating sediment loads. Given that coral species with high sediment-feeding capacity should have selective advantage over poor sediment feeders in muddy environments, species-specific variation in heterotrophic plasticity undoubtedly contributes to inshore-offshore patterns in the composition of coral communities and may alter community structure if sedimentation regimes increase.

Item ID: 27400
Item Type: Thesis (PhD)
Keywords: sediment feeding; coral diet; nearshore turbidity; offset effects
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Additional Information:

Publications arising from this thesis are available from the Related URLs field. The publications are:

Anthony, Kenneth R.N., and Fabricius, Katharina E. (2000) Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. Journal of Experimental Marine Biology and Ecology, 252 (2). pp. 221-253.

Anthony, K.R.N. (1999) A tank system for studying benthic aquatic organisms at predictable levels of turbidity and sedimentation: case study examining coral growth. Limnology and Oceanography, 44. pp. 1415-1422.

Anthony, K.R.N. (2000) Enhanced particle-feeding capacity of corals on turbid reefs (Great Barrier Reef, Australia). Coral Reefs, 19 (1). pp. 59-67.

Anthony, K.R.N. (1999) Coral suspension feeding on fine particulate matter. Journal of Experimental Marine Biology and Ecology, 232(1). pp. 85-106.

Date Deposited: 25 Jun 2013 04:14
FoR Codes: 06 BIOLOGICAL SCIENCES > 0602 Ecology > 060205 Marine and Estuarine Ecology (incl Marine Ichthyology) @ 90%
06 BIOLOGICAL SCIENCES > 0603 Evolutionary Biology > 060303 Biological Adaptation @ 10%
SEO Codes: 96 ENVIRONMENT > 9608 Flora, Fauna and Biodiversity > 960808 Marine Flora, Fauna and Biodiversity @ 51%
97 EXPANDING KNOWLEDGE > 970106 Expanding Knowledge in the Biological Sciences @ 49%
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