Coral Reefs at the Crossroads

Coral reefs are complex systems that are difficult to fully understand when viewed from a single perspective. As we have separated ourselves into increasingly smaller and more specific disciplines, we often lose sight of important connections between physical and biological factors and how they can change over different spatial and temporal scales. As stresses on these robust yet fragile systems broaden and deepen, it is becoming increasingly important that we break down artificial disciplinary barriers and ask questions that are difficult to frame from a single scientific perspective. This chapter provides a jumping-off point to examine coral reefs – sitting at both a disciplinary and a temporal crossroads.

Over 60 years ago, the discovery that light increased calcification in the coral plant-animal symbiosis triggered interest in explaining the phenomenon and understanding the mechanisms involved. Major findings along the way include the observation that carbon fixed by photosynthesis in the zooxanthellae is translocated to animal cells throughout the colony and that corals can therefore live as autotrophs in many situations. Recent research has focused on explaining the observed reduction in calcification rate with increasing ocean acidification (OA). Experiments have shown a direct correlation between declining ocean pH, declining aragonite saturation state (Ω_arag), declining [CO₃ ²⁻] and coral calcification. Nearly all previous reports on OA identify Ω_arag or its surrogate [CO₃ ²⁻] as the factor driving coral calcification. However, the alternate “Proton Flux Hypothesis” stated that coral calcification is controlled by diffusion limitation of net H⁺ transport through the boundary layer in relation to availability of dissolved inorganic carbon (DIC). The “Two Compartment Proton Flux Model” expanded this explanation and synthesized diverse observations into a universal model that explains many paradoxes of coral metabolism, morphology and plasticity of growth form in addition to observed coral skeletal growth response to OA. It is now clear that irradiance is the main driver of net photosynthesis (P_net), which in turn drives net calcification (G_net), and alters pH in the bulk water surrounding the coral. P_net controls [CO₃ ²⁻] and thus Ω_arag of the bulk water over the diel cycle. Changes in Ω_arag and pH lag behind G_net throughout the daily cycle by two or more hours. The flux rate P_net, rather than concentration-based parameters (e.g., Ω_arag, [CO₃ ²⁻], pH and [DIC]:[H⁺] ratio) is the primary driver of G_net. Daytime coral metabolism rapidly removes DIC from the bulk seawater. Photosynthesis increases the bulk seawater pH while providing the energy that drives calcification and increases in G_net. These relationships result in a correlation between G_net and Ω_arag, with both parameters being variables dependent on P_net. Consequently the correlation between G_net and Ω_arag varies widely between different locations and times depending on the relative metabolic contributions of various calcifying and photosynthesizing organisms and local rates of carbonate dissolution. High rates of H⁺ efflux continue for several hours following the mid-day G_net peak suggesting that corals have difficulty in shedding waste protons as described by the Proton Flux Model. DIC flux (uptake) tracks P_net and G_net and drops off rapidly after the photosynthesis-calcification maxima, indicating that corals can cope more effectively with the problem of limited DIC supply compared to the problem of eliminating H⁺. Predictive models of future global changes in coral and coral reef growth based on oceanic Ω_arag must include the influence of future changes in localized P_net on G_net as well as changes in rates of reef carbonate dissolution. The correlation between Ω_arag and G_net over the diel cycle is simply the result of increasing pH due to photosynthesis that shifts the CO₂-carbonate system equilibria to increase [CO₃ ²⁻] relative to the other DIC components of [HCO₃ ⁻] and [CO₂]. Therefore Ω_arag closely tracks pH as an effect of P_net, which also drives changes in G_net. Measurements of DIC flux and H⁺ flux are far more useful than concentrations in describing coral metabolism dynamics. Coral reefs are systems that exist in constant disequilibrium with the water column.

Reef organisms are well known for engaging in photosymbiosis in which a heterotrophic protist or animal host partners with one or more kinds of photosynthetic microbes. This relationship provides metabolic advantages in nutrition and rapid calcification, often leading to secretion of massive skeletons in the host. In turn the symbiont receives protection, physical stability in the photic zone and direct access to the sun’s energy. On an evolutionary scale, this relationship provided strong selective pressures for producing the algal-host relationship and has occurred multiple times in geological history. Today, different kinds of algae (dinoflagellates, diatoms, chlorophytes, rhodophytes, and cyanobacteria) inhabit various hosts (foraminifera, corals, mollusks) in modern reefs, and multiple phylogenetically separate algae may have also inhabited phylogenetically distinct ancient animals and protists. The modern dinoflagellate photosymbiont Symbiodinium occurs in a wide variety of unrelated host organisms from protists to mollusks. Molecular data indicate this genus first evolved either after the end-Cretaceous mass extinction 65 my ago or in the Early Eocene some 55 my ago. Encysted dinoflagellates related to Symbiodinium have been traced to the Triassic, and photosymbiosis may have been involved in even earlier reef associations. In all fossils, however, the identity of ancient photosymbionts is difficult to establish because they rarely, if ever, fossilize. Nevertheless, indirect evidence indicates that photosymbiotic ecosystems existed at least as far back as the Cambrian. Inferential lines of evidence, including large colony size, massive skeletons, unusual or complex morphology, the biogeographic distribution of possible hosts and skeletal geochemistry are all consistent with active photosynthesis. In the following pages, we develop the hypothesis that photosymbiosis best explains both the successes and failures of reefs through geologic time. We then review the evidence that suggests photosymbiosis in reef organisms played significant roles through geologic time in both the evolution and extinction of organisms and the reefs they constructed.

Biological erosion (bioerosion) is a key ecological process on coral reefs. It occurs though the grazing activities of specific fish and sea urchin species, and as a result of the colonisation of reef substrates by endolithic species of sponges, bivalves, worms and microorganisms. This activity results either in the direct dissolution of reef (mainly coral) substrate and/or the conversion of this substrate to sediment. As a result, bioerosion plays a key role in defining the structure of the accumulating reef framework, is a key process dictating the balance between rates of carbonate production and erosion, and influences reef-carbonate budget states. This chapter initially explores the key biological agents responsible for reef bioerosion within Holocene reef systems, and the influence that these organisms exert on patterns and styles of reef development. However, in the context of the aims of this book, the most pertinent question is how are reef-bioeroding taxa responding to environmental and ecological change, and how are they interacting with reef substrates under changing conditions. We discuss the current state of knowledge regarding variations in bioerosion rates and the ways in which different bioeroding taxa use space within degrading reef systems. Although much is known about the key taxa that drive reef bioerosion, data on actual bioerosion rates are limited to a few well-cited studies, and information on how these rates vary across spatial and temporal scales is even more limited. Habitat-specific bioerosion budgets for most taxa are also rare. Addressing these knowledge gaps will be critical to predicting future changes in bioeroder abundance and their impacts on changing reef environments.

Histories of sponges and reefs have been intertwined from the beginning. Paleozoic and Mesozoic sponges generated solid building blocks, and constructed reefs in collaboration with microbes and other encrusting organisms. During the Cenozoic, sponges on reefs have assumed various accessory geological roles, including adhering living corals to the reef frame, protecting solid biogenic carbonate from bioeroders, generating sediment and weakening corals by eroding solid substrate, and consolidating loose rubble to facilitate coral recruitment and reef recovery after physical disturbance. These many influences of sponges on substratum stability, and on coral survival and recruitment, blur distinctions between geological vs. biological roles.

Biological roles of sponges on modern reefs include highly efficient filtering of bacteria-sized plankton from the water column, harboring of hundreds of species of animal and plant symbionts, influencing seawater chemistry in conjunction with their diverse microbial symbionts, and serving as food for charismatic megafauna. Sponges may have been playing these roles for hundreds of millions of years, but the meager fossil record of soft-bodied sponges impedes historical analysis.

Sponges are masters of intrigue. They play roles that cannot be observed directly and then vanish without a trace, thereby thwarting understanding of their roles in the absence of carefully controlled manipulative experiments and time-series observations. Sponges are more heterogeneous than corals in their ecological requirements and vulnerabilities. Serious misinterpretations have resulted from over-generalizing from a few conspicuous species to the thousands of coral-reef sponge species, representing over twenty orders in three classes, and a great variety of body plans and relationships to corals and solid carbonate substrata.

Dynamics of living sponges are difficult to document because most sponges heal after partial mortality and vanish quickly after death. Thus observations of localized increases or overgrowths of corals by a few unusual sponge species have led to recent assertions that sponges are in the process of overwhelming coral reefs. However, a consistent pattern of high mortality in the few long-term census studies done on full assemblages suggests that, perhaps for the first time in their long history, sponges may actually be unable to keep up with changes in the sea. Diminished sponge populations could have profound consequences, many of them negative, for corals and coral reefs.

Declining calcification and accelerating sea-level rise have brought us ever closer to the point where coral reefs may not be able to keep pace. Even if this is insufficient to change reef-community structure or totally overtop low reef islands in the twenty-first century, the impacts on reefs and the organisms that depend on them will still be profound. Patterns of sea-level rise have varied spatially in the past due to both local tectonics and regional crustal responses to deglaciation. The result has been regionally disparate sea-level histories that complicate our understanding of the links between past sea level and reef development.

At the same time, gaps remain in our understanding of how, and how fast, reefs build. Holocene reefs-accretion rates (generally <5 mm/year) are lower than previous estimates (10–15 mm/year), making coral reefs more vulnerable to rising sea level than has been assumed. Furthermore, the conflation of coral growth and reef accretion has provided an overly simplistic view of reef building that focuses on coral abundance and calcification. Protocols have been suggested to quantify the changing balance between carbonate production and bioerosion, but these still ignore the role of physical processes that redistribute and remove material from the reef, a scenario that will become even more important as the intensity of tropical storms increases. Holocene cores show that accretion does not mimic the depth dependence of calcification, suggesting that predictions based solely on biological assessments could be flawed.

Uniformitarianism, the idea that “the present is the key to the past”, has been a fundamental tool for geologists trying to unravel the development of ancient reefs using their modern counterparts. As we try to separate anthropogenic change from natural variability that operates on cycles longer than human lifetimes, we might consider whether this concept could be reversed to help predict the fate of coral reefs – or to at least examine some of our critical assumptions about reef accretion and sea-level rise. This chapter considers some of our long-standing models of sea level and reef building, using recent data to provide a more complete picture of the factors involved in both the recent geologic past and the immediate future. The goal is to provide a better understanding of interactions between the two that might allow better models of ancient reefs while also providing more realistic answers to the question, “Will coral reefs keep up with rising sea level in the twenty-first century?”

Two major hypotheses have been developed to explain the observed stability of reef assemblages through the Quaternary. The first invokes interspecific interaction or interdependence as an emergent property, which stabilizes community composition for long periods even in the face of environmental change. The second recognizes that the persistence of communities includes or implies persistently stable environments and faunal tracking of environments even when conditions vary. The null model for persistence-stability is that similar community types should recur whenever and wherever similar environmental conditions exist, so long as the same general species pool is available for recruitment.

Analyzing reef facies preserved within a sequence-stratigraphic framework allows us to test the null model on Quaternary reefs. We propose here that reassembly was unnecessary, because reef communities were able to track even the most rapid changes in sea level, producing recurrent biofacies largely through asexual and sexual recruitment from local populations. Analysis of climate change and accompanying tropical SSTs associated with glacial cycles shows they were not sufficient to cause coral populations or the coral reefs they build to disappear and then to reorganize anew. We are, therefore, unable to reject the null model. Incremental faunal tracking of suitable habitats through time and in regional space is the likely mechanism conferring persistence-stability in these coral assemblages.

Although reef-like structures formed in the Neoproterozoic, reefs built by metazoans did not appear until the early Paleozoic. From then until the Recent, reefs diversified, underwent extinctions many times and then diversified again. Reef-inhabiting organisms included many different groups from algae to vertebrates as well as enigmatic, extinct suprageneric taxa. Evolution of these groups continued unabated and sometimes resulted in significant changes in the communities making up reefs. These reef groups varied over geologic time with extinction events commonly marking dramatic changes in the biotas. Paleozoic reefs consisted of sponges, corals, foraminifera, algae, bryozoans, and brachiopods, among others. The major extinction event at the end of the Paleozoic eliminated these forms as reef constituents and new groups (e.g., the first scleractinian corals) appeared in the Triassic. The Mesozoic was dominated by sponges, corals, rudist bivalves, and algae, most of which were eliminated in the end-Cretaceous extinction event. The Cenozoic reef biotas included red algae, foraminifera, sponges, corals, various invertebrates, and fish.

Throughout the Phanerozoic, these biotas were eliminated by extinction events of differing magnitude. Each event corresponded to warming due to rising greenhouse gases (CO₂ and CH₄), and ocean acidification caused by lowered pH and anoxia of shallow waters that took severe tolls on reef organisms. These extinction events caused the decline of reef organisms and the reefs they built, resulting in decreased diversity and slower carbonate deposition. Photosymbiotic reef ecosystems failed during extinctions and these failures may have been driven, at least in part, by either the demise of the symbiosis or the extinction of symbionts.

Reefs were generally absent in post-extinction times due to different ecologies. The ancestors of the next radiation of reef organisms must have been present somewhere—perhaps in deeper water, remote seamounts or isolated shallow seas. These ancestral faunas gave rise to radiations of reef organisms following several million years of depauperate and unusual biotas. Once underway, these radiations were relatively rapid and were responses to an amelioration of the extinction conditions and an increase in ecological opportunities. They did not restore the same taxa; rather new organisms at the familial or generic levels commonly diversified in most groups.

The extinction events of the past do not bode well for the survival of modern reefs because of impending anthropogenic changes. Although humans have caused reef destruction through pollution, sedimentation, nutrient influx, and physical damage, increasing global warming and ocean acidification caused by CO₂ and CH₄ emissions are the principal threats to modern reef ecosystems with severe degradation or even extinction possibilities. Scientific and political will to change these inputs soon are essential to the survival of reefs, as well as other aspects of modern civilization.

Reef building has responded to changes in climate, ocean chemistry, and a variety of other physical and biological factors during the geologic past, as have the taxa involved. Many of the data revealed by the geologic record are also relevant to human impacts on coral reefs today and their success moving forward. This chapter reviews the responses of reefs and reef builders to environmental changes over Earth’s history and relates this information to projected changes due to anthropogenic activities going forward. These changes include increasing temperature, ocean acidification, more intense storms, sea-level rise, nutrification, and sedimentation. Past events provide some insights, but are somewhat limited proxies of future impacts, largely because of the perhaps unprecedented current rate of CO₂ release today. Present-day rates of climate change and ocean acidification may be higher than at any point in the geologic past, and may exceed the capacity for corals and other reef builders to tolerate or adapt to the changing environment.

Reefs are complex ecosystems on many scales and a host of simplifications, assumptions, and limitations are inherent in surveying and characterizing them. This chapter examines the techniques used to collect data on living and mineral reefs and asks what potential biases may arise from equating the two very different types of “reefs” (i.e., a living community vs. its mineral remains). Data from each of the two has its own limitations. Although fossil assemblages are famous for lost detail, vast amounts of ecological information are also lost when surveying living reefs. Despite inherent shortcomings, living and mineral reefs both provide important ecological context that is needed to address many of todays most relevant reef questions. While data on living organisms are the foundation for documenting the status of modern reefs, mineral reef deposits provide the baseline needed to put that information in a broader context.

Coral-reef ecosystems are declining worldwide, compromising their capacity to provide ecosystem services that include feeding hundreds of millions of people and protecting shorelines from erosion. The anthropogenic causes of reef degradation are complex and operate over a broad range of scales and hierarchical levels, but accelerating climate change and its collateral impacts are currently the strongest drivers. Deleterious trends in local-scale, ecological processes that occur within reef communities, such as declining herbivory and increasing eutrophication, generally play a subsidiary role at present, because their effects are overwhelmed by the impacts of climate change on many reefs. That does not mean local-scale ecology is irrelevant. Solving environmental problems at one scale or level will by default leave problems at the other scale as the new primary problems. If humanity is able to control climate change at the global level, then community-level processes will in general become limiting. Both local and global impacts must be mitigated and reversed if we are to save coral reefs.

What, exactly, is a coral reef? And how have the world’s reefs changed in the last several decades? What are the stressors undermining reef structure and function? Given the predicted effects of climate change, do reefs have a future? Is it possible to “manage” coral reefs for resilience? What can coral reef scientists contribute to improve protection and management of coral reefs? What insights can biologists and geologists provide regarding the persistence of coral reefs on a human timescale? What is reef change to a biologist… to a geologist?

Clearly, there are many challenging questions. In this chapter, we present some of our thoughts on monitoring and management of coral reefs in US national parks in the Caribbean and western Atlantic based on our experience as members of monitoring teams. We reflect on the need to characterize and evaluate reefs, on how to conduct high-quality monitoring programs, and on what we can learn from biological and geological experiments and investigations. We explore the possibility that specific steps can be taken to “manage” coral reefs for greater resilience.