Naturally, the economic impacts of reef decline will be greatest for developing nations, but this does not mean that the US will get by unscathed. Many of the reefs showing the most serious degradation are in US waters. Coral reefs from Florida, Puerto Rico, and the US Virgin Islands to Hawaii and former US protectorates in the Pacific region have all shown sharp declines in live coral cover and fish abundance. We know that in a general sense these declines are due to the combined effects of overfishing, coastal pollution, emergent diseases, global warming, and changes in atmospheric chemistry. What we do not know is how to translate our available science into policy, and in many places the scientific data are not yet convincing enough to justify the economic implications of effective mitigation measures. Nowhere is this more apparent than in the effects of elevated atmospheric carbon dioxide (CO2) on coral reef health.Since the industrial revolution the use of fossil fuels, coupled with deforestation, has increased the global atmospheric concentration of carbon dioxide by 75% (Whitfield 1974), with a projected level at Century's end of twice that of today. The atmosphere and oceans are intimately coupled. When atmospheric CO2 increases the amount of CO2 dissolved in the ocean is amplified, causing shifts in the ionic composition of seawater. With increased CO2 dissolved in the ocean, it becomes much more difficult for marine invertebrates to precipitate their limestone skeletons. This impacts all marine organisms that produce limestone (calcium carbonate)- seashells, seastars, sponges, sea urchins, crabs, lobsters and a myriad of other forms, huge to microscopic; let us not forget hard corals. The water also becomes more acidic, again making it harder for marine creatures to secrete their skeletons, and easier for skeletal material to dissolve back into the seawater (Skirrow and Whitfield 1975). Models suggest that in the next half century increased atmospheric CO2 will decrease the aragonite saturation state of seawater in the tropics (aragonite is the form of limestone produced by corals and is part of many seashells) by 30% (Gattuso et al. 1998, Kleypas et al. 1999), which would decrease calcification rates of corals and other organisms by 14-30% by 2050. Laboratory evidence confirms that coral calcification will be hard hit by these atmospheric changes (Marubini and Atkinson 1999, Marubini and Thake 1999, Leclercq et al. 2000).

While much attention is focused on the role of acute stressors on coral reefs - ship groundings, starfish outbreaks, and bleaching events - the various and complex effects of increased CO₂ (Done 1999) have taken a back seat. We feel that this is a grave error because, due to the frequency of acute events, what matters more than anything for the future of coral reefs is their ability to tolerate and rebound from natural and human disturbance. This power is directly related to coral growth and repair rates that are at risk from increased oceanic CO₂.

However, the coral/climate question is still more complex than this. Corals do not live in isolation, but rather are productive members of one of our planets most complex and diverse ecosystems; the coral reef. Corals compete for space and food, are eaten by fishes and invertebrates, and are a host for countless species of small invertebrates and microscopic organisms. Like all of our natural world, corals rest in some unknown balance with other members of their community.

When herbivorous fishes and invertebrates are eliminated from coral reefs – often from over fishing - algae can quickly outgrow and shade out corals (Lewis 1985, Hughes et al. 1987, Steneck 1988, McClanahan et al. 1994, Hixon and Brostoff 1996, Shulman and Robertson 1996, McClanahan and Muthiga 1998, Schmitt 1998, McClanahan et al. 1999). The presence of symbiotic crustaceans (Glynn 1983) and algae (McConnaughey et al. 2000) can affect coral calcification rates and their competition for space. On a microscopic scale, corals are constantly battling in a fight against fungi and bacteria that would hope to consume them (Le Campion-Alsumard et al. 1995, Bentis et al. 2000). This complex web of ecological relationships could either mediate or exacerbate the affects of increased CO₂.

In general, the complex nature of reef systems suggests there are any number of positive and negative feedbacks on increased atmospheric CO₂. Will photosynthetic rates increase to offset decreased calcification rates? Will new proteins evolve in corals quickly enough to compensate for decrease bicarbonate concentrations? Will some competitors be differentially affected by the changes? Like many complex questions, these answers will only come when we “take it to the numbers” so to speak. Our understanding of the precise affects of global climate change on coral reefs has yet to incorporate this ecosystem approach.

Work by our collaborators in the Biosphere2 mesocosm (www.bio2.edu) has corroborated earlier experiments in small-scale aquarium systems in demonstrating that elevated levels of CO₂ in seawater cause a profound reduction in the rates at which corals are able to secrete their calcium carbonate skeletons (Langdon et al. 2000). Our current collaboration in Biosphere2 is focused on the investigation of CO₂ levels and complex interactions between herbivores, coral, algae, and fungi.

CARBON DIOXIDE and the CARBONATE LIMITATION HYPOTHESIS

Corals are particularly fascinating in that their functional self consists of part animal (the coral itself) and part algae in the form of symbiotic dinoflagellates called Zooxanthellae. Corals collect organic material from the water to secure nutrients and minerals, but a large portion of the raw energy for life comes in the form of sugars created via photosynthesis by the algae. Zooxanthellae reside in the tissue space of the corals where nutrients vital to the photosynthetic pathway are readily available. The process of photosynthesis produces oxygen and consumes CO₂, and the interstitial concentration of CO₂ is driven down by the photosynthetic process.

In water, carbon dioxide gas absorbed from the atmosphere persists in very small quantities since the bulk of this material undergoes a rapid reaction with water

CO₂ + 2H₂O <-> H₂CO₃ <-> HCO₃^- + H⁺<-> CO²₃^- + 2H+                   (1)

Increased CO2 affects pH via the generation of the negative carbonate ions on the right side of equation 1. Inside corals, photosynthesis decreases CO₂ concentrations, increases pH, and increases the bicarbonate concentration. This vital function of Zooxanthellae, perhaps more important then the sugars they produce, facilitates the calcification process by which corals build their skeletal material (aragonite) via the reaction

            Ca²⁺ + 2HCO₃^- <-> CaCO₃ + CO₂ + H₂O                 (2)

During coral bleaching Zooxanthellae are ejected from the coral tissue due to some stressor, and the process of calcification becomes energetically impossible. Under natural conditions a battle exists between the decomposition of aragonite by environmental forces and its deposition by the calcification process. When calcification is halted, natural decomposition continues and so corals may actually shrink during bleaching events. Geography, light availability, nutrient concentrations, pH, dissolved CO₂, O₂, HCO₃^-, temperature, and salinity interact to determine “natural” or “background” rates of respiration, calcification, and degradation; the components of coral growth. Under normal conditions, within the biogeographical ranges of hermatypic corals, environmental conditions support rapid coral growth, allowing corals to compete successfully for space and survive natural disturbance.

Increased CO₂ concentrations push equation 1 towards the far right, forcing the dislocation of negative carbonate ions from their positive counterparts (be they H⁺ or Ca²⁺), and making the calcification process more energetically expensive (Marubini and Atkinson 1999, Marubini and Thake 1999). Decreased calcification rates upset the balance between growth and degradation, with potential system wide consequences. Rates of physical and biological erosion are large when compared to deposition, and a decrease in the rate of calcification of as little as 5% will lead to a net loss of calcium carbonate (Hoegh-Guldberg 1999), but even small scale changes in calcification may effect ecological relationships.

METHODOLOGY

In the Biosphere2 system, dissolved CO₂ concentrations are altered on a (approximately) quarterly basis between present, past, and predicted future levels. We use this manipulation to study the importance of interactions between herbivores, corals, and CO₂. In the oceanarium proper we maintain four arrays of Montipora and Porites nubbins, half of which are caged to exclude herbivores. As a control we maintain coral arrays in an adjacent flow-through facility at light levels equal to and greater then those experienced in the oceanarium. Half of those corals are “grazed” by hand to simulate the effects of fish herbivory. This design offers 6 treatments;

Oceanarium grazed

Oceanarium ungrazed

Low light grazed

Low light ungrazed

High light grazed

High light ungrazed

At the end of every CO₂ regime each nubbin is stained using Alizarin Red and photographed from four orthogonal directions. The growth rates of corals are estimated from the digital photographs using NIH Image software, and, when nubbins are removed from the experiment, the density of endolithic fungi is estimated using scanning electron microscopy of thin sections.

We monitor fish herbivory in the oceanarium via four underwater cameras that are trained on our coral arrays. Video from the cameras is transmitted over the Internet using an Axis 2100 video server, and we record fish behavior using a web-based ethology tool. In the coming months we would like to bring additional researchers into the project to assist with our observation of fish behavior, and we would like to collaborate with educators to use this Internet-based experiment as a teaching tool in classrooms around the world. Please take a moment to explore our ethology tools, get to know the biota of the Biosphere2 oceanarium, and observe our live web-casts. We look forward to comments and criticisms, and are excited to hear from potential collaborators.

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