Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis
Introduction
Around the world, water quality in coastal areas is changing in response to rapidly increasing fertiliser use and land clearing (Vitousek et al., 1997, Tilman et al., 2001, Smith et al., 2003). Annual nitrogen fertiliser use has increased globally more than sixfold since 1960 (Matson et al., 1997), land clearing continues at a rate of 1% of the earth’s surface per year (GESAMP, 2001), and coastal urbanisation is expanding disproportionally to human population growth. Oxygen-depleted seafloor zones, caused primarily by river-borne agricultural nitrogen and phosphorus, have doubled in number and expanded in size since 1990, presenting clear evidence that many coastal waters are becoming more eutrophic (GESAMP, 2001). Coastal coral reefs, like other marine coastal ecosystems, are increasingly exposed to growing loads of nutrients, sediments and pollutants discharged from the land. Terrestrial runoff is therefore a growing concern for most of the 104 nations endowed with coral reefs (Bryant et al., 1998, Spalding et al., 2001).
Field studies have provided a large body of information showing that sedimentation, nutrient enrichment and turbidity can degrade coral reefs at local scales (Table 1). At regional scales, it has often been difficult to assess causal relationships between increasing terrestrial runoff and reef degradation, because pollution effects and other disturbances are typically confounded, historical data are often missing, and reef communities change naturally along gradients from oceanic conditions (low siltation, high water clarity, generally low nutrient levels except during upwelling periods) to terrestrially influenced conditions (fluctuating salinity, variable or high silt and nutrient levels, variable or reduced water clarity). As nutrients increase, coral reef communities change from dominance of nutrient-recycling symbiotic organisms such as corals (in oligotrophic oceanic waters), to increasing proportions of macroalgae (on eastern continental margins naturally exposed to river runoff), and further to heterotrophic filter feeders (in nutrient-enriched areas of upwelling or lagoons) (Birkeland, 1987). Although coastal coral reefs can flourish at relatively high levels of particulate matter and siltation (Anthony, 1999), they tend to be restricted to the upper 10 m depth (in extreme cases 4 m depth) in turbid water, while extending to >40 m in clear oceanic waters (Yentsch et al., 2002).
This review compiles the current state of knowledge on runoff-specific responses in coral reefs, in order to aid assessment of the effects of terrestrial runoff at regional scales. Inorganic nutrients and particulate material, although not ‘classical’ pollutants, are arguably the most important contaminants at national and regional levels (GESAMP, 2001), and this review will focus on assessing the effects of these materials on reef communities. However, contamination by pesticides, heavy metals, hydrocarbons or other human-made pollutants can also significantly affect the health of reefs at local scales (Guzman and Holst, 1993). For example, heavy metals such as copper and zinc and some hydrocarbons have been linked to reduced fertilization, fecundity and growth in adult corals (Heyward, 1988, Brown, 1987, Loya and Rinkevich, 1987, GESAMP, 2001). Some herbicides (e.g., diuron and atrazin) cause rapid (but reversible) photophysiological stress in corals after short-term exposure at environmentally relevant concentrations of <1 μg l−1 (Owen et al., 2003, Jones and Kerswell, 2003, Jones et al., 2003, Negri et al., in press); their effects at chronic low-level exposures are still largely unknown. Other studies, too numerous to be listed here, document the uptake of a variety of human-made pollutants by adult corals; the effects of these substances on coral reefs are beyond the scope of this review.
This paper systematically reviews and synthesises the available information on the direct effects of terrestrial runoff on (1) calcification, tissue growth, zooxanthellae populations and photosynthesis in adult hard corals, (2) the six main stages of coral reproduction and recruitment, and (3) six groups of other reef organisms that affect hard coral abundances. The latter group includes those organisms that affect coral larval settlement, bioeroding filter feeders that weaken the structural strength of reefs, macroalgae, heterotrophic filter feeders and octocorals competing for space with corals, disease pathogens, and coral predators. Responses of each of these groups are assessed separately against exposure to the four main water quality parameters, namely: (1) dissolved inorganic nutrients, (2) suspended particulate organic matter, (3) light reduction from turbidity and (4) sedimentation. This separation disregards additive or synergistic effects, but helps to understand the mechanisms for change in the field where many contaminants and responses co-occur. Furthermore, the paper identifies geographic and biological properties influencing the level of resistance and resilience of reefs to degradation.
Section snippets
Dissolved inorganic nutrients
Considerable effort has gone into experiments studying the direct effects of elevated dissolved inorganic nitrogen (DIN, as nitrate or ammonium) and phosphate (DIP) on coral calcification, tissue growth and zooxanthellae. Table 2a, and detailed reviews by Dubinsky and Stambler (1996) and Szmant (2002) show that most experiments were conducted at environmentally unrealistically high levels, and that significant inconsistencies exist across studies that are as yet unresolved. Many studies found
Effects of terrestrial runoff on benthic organisms that affect corals and coral communities
Abundances of a large number of invertebrates and algae in coral reef communities change along environmental gradients influenced by terrestrial runoff. This section focuses on the responses of those organism groups that profoundly affect health and abundance of corals; hence changes in their abundances in response to terrestrial runoff induce secondary or indirect effects on corals. The six main groups of organisms are those that (1) facilitate coral settlement (especially crustose coralline
Reef properties related to resistance, resilience and risk
Inshore reefs vary considerably in their resistance against detrimental effects from terrestrial runoff and their resilience after exposure. Understanding properties of reefs or regions that contribute to their resistance and resilience could underpin management decisions, e.g., by prioritizing protection of reefs that have the greatest chance of withstanding degradation by terrestrial runoff. This section provides an assessment of the physical, hydrodynamic, spatial and biological properties
Conclusions
Models of the global scale of pollution around coral reefs estimate that 22% of all coral reefs worldwide are classified as at high (12%) or medium (10%) threat from inland pollution and soil erosion (Bryant et al., 1998). The percentage of reefs at risk is highest in countries with widespread land clearing, such as Taiwan and Vietnam with 50% of their reefs at risk from terrestrial runoff, or the Philippines with 35% (Bourke et al., 2002). The models also classify 30% of reefs as threatened
Acknowledgments
Many thanks to Pat Hutchings, Miles Furnas, Britta Schaffelke, Jon Brodie, Glenn De’ath, Craig Humphrey and Selina Ward for helpful comments on the manuscript. This study was funded by the Cooperative Research Centre for the Great Barrier Reef World Heritage Area (CRC Reef Research), and the Australian Institute of Marine Science (AIMS).
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