Journal of Experimental Marine Biology and Ecology 300 (2004) 217 – 252 www.elsevier.com/locate/jembe
Experimental biology of coral reef ecosystems Michael P. Lesser * Department of Zoology and Center for Marine Biology, University of New Hampshire, Durham, NH 03824, USA Received 23 November 2003; received in revised form 18 December 2003; accepted 28 December 2003
Abstract Coral reef ecosystems are at the crossroads. While significant gaps still exist in our understanding of how ‘‘normal’’ reefs work, unprecedented changes in coral reef systems have forced the research community to change its focus from basic research to understand how one of the most diverse ecosystems in the world works to basic research with strong applied implications to alleviate damage, save, or restore coral reef ecosystems. A wide range of stressors on local, regional, and global spatial scales including over fishing, diseases, large-scale disturbance events, global climate change (e.g., ozone depletion, global warming), and over population have all contributed to declines in coral cover or phase shifts in community structure on time scales never observed before. Many of these changes are directly or indirectly related to anthropogenically induced changes in the global support network that affects all ecosystems. This review focuses on some recent advances in the experimental biology of coral reef ecosystems, and in particular scleractinian corals, at all levels of biological organization. Many of the areas of interest and techniques discussed reflect a progression of technological advances in biology and ecology but have found unique and timely application in the field of experimental coral reef biology. The review, by nature, will not be exhaustive and reflects the author’s interests to a large degree. Because of the voluminous literature available, an attempt has been made to capture the essential elements and references for each topic discussed. D 2004 Elsevier B.V. All rights reserved. Keywords: Coral reef ecosystems; Experimental biology; Global climate change
Scleractinian, or reef-building corals, are a central component to coral reef ecosystems worldwide between 30jN and 30jS latitude and contribute to thousands of square kilometers of critical marine habitat. The prolific growth rates (3– 15 cm year 1) of reef-building corals in optically clear, oligotrophic tropical seas are responsible for the three-dimensional framework of coral reef systems (Fig. 1). While other organisms serve * Tel.: +1-603-862-3442; fax: +1-603-862-3784. E-mail address:
[email protected] (M.P. Lesser). 0022-0981/$ - see front matter D 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2003.12.027
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Fig. 1. Underwater photograph of coral reef in Indonesia with almost 100% cover of Acropora sp. (Photograph by M. Lesser).
to consolidate the framework of the reef structure together (e.g. calcareous algae) and use it as essential habitat (e.g. fish, algae, invertebrates and bacteria), corals are the functional group that has contributed significantly to coral reef ecosystems for at least 200 million years (Veron, 1995) and have built the primary structure of entire reefs, islands and such massive oceanic barriers as the barrier reefs of Mesoamerica and Australia. Coral reefs are a source of food and livelihood for at least 100 million people worldwide, support major industries (fishing and tourism), play a key role in stabilizing coastlines, and their high species and genetic diversity rivals that of tropical rainforests (Connell, 1978; HoeghGuldberg, 1999). This biodiversity is now just beginning to be exploited in the search for bioactive compounds that could benefit humankind (Quinn et al., 2002). Unfortunately, coral reefs are also experiencing unparalleled levels of anthropogenically induced stress. Current estimates on the rate of decline in the health of coral reefs and the loss or change in community structure of reefs are of worldwide concern (Wilkinson, 2000). It is estimated that a combination of physical, chemical and biological stresses will cause the decline of between 40% to 60% of the world’s coral reefs over the next 50 years unless appropriate steps are taken (Wilkinson, 2000). Until recently, global climate change was seen as just one of many factors (e.g., eutrophication, coastal development, sedimentation, over-fishing) responsible for the decline in the health of coral reefs (Wilkinson, 1999) while the time scales of change due to global climate effects were believed to be slow and other anthropogenic causes a higher priority for study. In 1998, however, an estimated 16% of the world’s living corals were eliminated in a single warming event related to El Nin˜o (Wilkinson, 2000). During this event, sea temperatures warmed to 2 –3 jC above long-
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term average summer temperatures and resulted in a catastrophic ‘‘bleaching’’ event that caused significant mortality of several species of coral (e.g., both the expulsion of zooxanthallae and host tissue death occurred). The impact of this thermal event on the percent cover of shallow coral reefs worldwide and the projection of continued rising sea temperatures under greenhouse warming (Hoegh-Guldberg, 1999) has radically changed the focus of a large proportion of the research community towards understanding the potential impact of greenhouse-driven climate change on the world’s coral reefs. Bleaching as a result of thermal stress is not the only threat from global climate change and coral reef biologists from around the world have had to use new experimental tools at all levels of biological organization in their efforts to understand how reefs work, determine which corals will survive anthropogenically driven change, and predict what reefs will look like at the end of the next century. In essence, who will be the winners and the losers (Loya et al., 2001)?
1. The coral–algal symbiosis Coral reef communities contain a wide variety of mutualistic associations none more important than the relationship between corals and their symbiotic dinoflagellates of the genus Symbiodinium sp., commonly referred to as zooxanthellae. Scleractinian corals first appeared in the Triassic (Veron, 1995), and it is widely accepted that their rapid ecological success was directly related to the acquisition of dinoflagellate endosymbionts that enabled the symbiosis to survive in oligotrophic and high solar irradiance habitats. Corals acquire the majority of their energetic and nutrient requirements by two mechanisms: photosynthesis by their zooxanthellae and heterotrophy, or the direct ingestion of zooplankton and other organic particles in the water column by the cnidarian host. The zooxanthellae reside within vacuoles in the cells of the host gastrodermis (Fig. 2a and b; Trench, 1979, 1987) where they serve as primary producers and supply their coral host with up to 95% of their photosynthetic products, such as sugars, amino acids, carbohydrates and small peptides (Trench, 1979; Muscatine, 1990) making corals autotrophic with respect to carbon in most habitats. These compounds provide the coral with energy for respiration, growth, and the deposition of its CaCO3 skeleton (Muscatine, 1990). Supplying translocated photosynthate to the host contributes significantly to the fitness of the symbiosis (Muscatine, 1990; Mueller-Parker and D’Elia, 1997) while in return the zooxanthellae receive essential nutrients such as ammonia, phosphate, and carbon dioxide from the metabolic wastes of the coral (Trench, 1979; Mueller-Parker and D’Elia, 1997). Additionally, photoautotrophy is not the only source of nutrition for corals. An increasing amount of experimental evidence continues to document that heterotrophy in corals is essential for providing nitrogen, phosphorus, and other nutrients which make it possible for the coral host to use the available carbon skeletons for protein synthesis and other essential metabolic requirements. Initially, the degree of heterotrophy appeared to be positively correlated with coral polyp size (Porter, 1976). Porter (1976) described a bathymetric gradient from autotrophy in shallow waters to heterotrophy in deeper waters that was correlated with polyp size in the Caribbean. Species with small polyps that were more dependent on autotrophy were found in shallow waters while more heterotrophic large polyp species of coral were found in deep waters (Porter, 1976). Clearly, heterotro-
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Fig. 2. (a) Electron micrograph of zooxanthellae in hospite. (b) Phase-contrast micrograph of zooxanthellae in tentacle squash preparation (Photographs by M. Lesser and T. LaJeuness).
phy in corals is important. Glynn (1973) described plankton depletion on a coral reef as water flowed past and Wellington (1982) provided experimental, multifactorial, evidence that supported Porter’s autotrophy to heterotrophy gradient, but also showed that heterotrophy did not compensate for the decrease in solar irradiance with depth when growth rates were measured. Recently, Sebens and colleagues (Sebens and Johnson, 1991; Johnson and Sebens, 1993; Sebens et al., 1996, 1998) have shown quite convincingly that both small and large polyped corals are successful at capturing certain size classes of zooplankton and that any differences in the efficiency of capture were due largely to the escape ability of the zooplankton. Whether from autotrophy or heterotrophy, the tight recycling of nutrients within the coral symbiosis and the close coupling between trophic levels at reasonably high
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efficiencies contribute to the very high productivity of corals (Muscatine and Porter, 1977; Falkowski et al., 1984; Muscatine, 1990; Mueller-Parker and D’Elia, 1997). Nutrient limitation imposed by the host on the algal symbionts is also believed to be part of a highly regulated control mechanism on the growth of zooxanthellae that would otherwise outdivide their host cells at rates approaching those of free-living phytoplankton (Muscatine and Porter, 1977). From an organismal and experimental perspective, it would appear that the role of autotrophy and heterotrophy in the energetics and nutrient metabolism of corals should be vigorously revisited. This will require simultaneous and interdisciplinary studies by groups of collaborators on a range of coral species in different habitats using a range of tools (e.g., fluorescence measurements, feeding studies, stable isotopes) to fill in what appear to be large gaps in our understanding. By definition mutualistic associations incur both benefits and costs for the partnered species. For any mutualistic symbiosis to develop and persist, a constant evaluation of the costs and benefits must be occurring such that the selective pressure favors those associations where the benefit to both partners outweighs the costs (Cushman and Beattie, 1991). Under the continuing scenario of rapid change on coral reefs, it is important to understand, at an organismal level, which species will survive in the broad range of trophic strategies that span the dependence on autotrophy versus heterotrophy.
2. Hurricanes, overfishing, eutrophication, bleaching, and community phase shifts Both the growth forms and species of corals show typical and well-described zonational patterns on reefs worldwide (Loya, 1972; Huston, 1985; Done, 1995). While heterogeneity exists, species diversity along a bathymetric gradient is predictable to a certain degree and reflects both biotic and abiotic processes. Much of the recent ecological work on coral reefs has been framed around the concept that reefs are non-equilibrium systems whose community structure and diversity are largely determined by the intensity and rate of disturbance as described in the intermediate disturbance hypothesis (Connell, 1978, 1997; Connell et al., 1997). Additionally, strong latitudinal and bathymetric gradients in abiotic factors such as solar irradiance, water flow, and calcium carbonate saturation state significantly influence the community structure, growth forms, and state of photoacclimatization over both small and large spatial scales (Falkowski et al., 1990; Done, 1995; Wilkinson, 1999; Lesser et al., 2000). The scale-dependent variability in coral reef community structure continues to be an important area of study for understanding not only the range of scales at which different patterns occur but also what processes at different scales may be driving that variability (Murdoch and Aronson, 1999). The current concern by coral reef biologists is that the periodicity and intensity of disturbance events, which now include a suite of anthropogenic factors over large (e.g., kilometer) spatial scales, is rapidly changing coral reefs and threatening their existence which is in juxtaposition to the long-term persistence of coral reefs over geological time scales (Pandolphi, 1999). Most coral reef biologists do agree that coral reefs are changing and will exist in the near future but they will not be the ‘‘coral reefs’’ we have come to know in many parts of the world (Knowlton, 2001). The outcome on each reef system will likely be determined by a combination of the number and severity of insults, but also which set of the
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unique and varied life-history traits will be able to cope with these stressors on ecological and evolutionary time scales (Hughes et al., 1992; Done et al., 1996). Jackson et al. (2001) demonstrate from several sources of historical data that a range of disturbances including overfishing and coastal development have consistently led to major changes in coral reefs ecosystem structure and health. The most poignant example of the effects of anthropogenic influences is the state of reefs in the Caribbean. A recent metaanalysis of coral cover throughout the Caribbean has shown an 80% decline in percent coral cover that has been both long-term (e.g., decadal) and region-wide (Gardner et al., 2003). Though many reefs worldwide have suffered similar reductions in coral cover (McClanahan, 2002), most Caribbean reefs have undergone a shift from being coraldominated to algal-dominated in this time period (Hughes, 1994). The causes of this shift vary from reef to reef but are the result of several types of disturbance that include hurricane damage (Hughes, 1994; Hughes and Connell, 1999), eutrophication (Lapointe, 1997), thermal stress resulting in coral bleaching (Hoegh-Guldberg, 1999; Aronson et al., 2000, 2002; Ostrander et al., 2000), coral diseases (Harvell et al., 2002; Richardson, 1998; Rosenberg and Ben-Haim, 2002), the transport and deposition of sand and dust from the Sahara in the Caribbean, which may be a factor that partially explains the increase in coral diseases (Shinn et al., 2000), and reduced herbivory from over-fishing compounded by an epizootic of unknown etiology that decimated Diadema populations in the 1980s (Carpenter, 1988; Hughes, 1994). Hughes (1994) described the rapid and significant ecological changes that occurred on coral reefs in Jamaica when herbivores were removed by fishing, to the point where reef resilience (i.e. ability to recover from a disturbance) was lost and a permanent phase shift to algal-dominated communities began. Additionally, natural factors conspired with anthropogenic stresses to produce this outcome. First, Hurricane Allen, a category five hurricane struck Jamaica after almost 40 years without any significant storm damage to coral reefs. While most of the damage occurred in shallow waters (
