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Coral reef baselines: How much macroalgae is natural?

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Highlights

  • Identifying the baseline state of an ecosystem is a critical step in conservation.

  • Some reef scientists believe that the baseline cover of seaweed was very low.

  • Evidence suggests that macroalgal biomass may have been higher than assumed.

  • Developing context-specific baseline distributions of seaweed is an important goal.

  • Uncertainties illustrate the difficulty of determining the baseline condition.

Abstract

Identifying the baseline or natural state of an ecosystem is a critical step in effective conservation and restoration. Like most marine ecosystems, coral reefs are being degraded by human activities: corals and fish have declined in abundance and seaweeds, or macroalgae, have become more prevalent. The challenge for resource managers is to reverse these trends, but by how much? Based on surveys of Caribbean reefs in the 1970s, some reef scientists believe that the average cover of seaweed was very low in the natural state: perhaps less than 3%. On the other hand, evidence from remote Pacific reefs, ecological theory, and impacts of over-harvesting in other systems all suggest that, historically, macroalgal biomass may have been higher than assumed. Uncertainties about the natural state of coral reefs illustrate the difficulty of determining the baseline condition of even well studied systems.

Introduction

To restore and manage ecosystems properly, we need to know what they looked like and how they operated before humans began to deplete, alter, and otherwise degrade them (Dayton et al., 1998). The pristine or natural state of a population or community is called the baseline in conservation biology, and it serves as a guide for setting conservation and restoration targets. Unfortunately, scientists rarely have reliable information on baselines because in most cases quantitative data are not collected until long after the resource has been modified (Pauly, 1995, Dayton et al., 1998). This is particularly true for marine communities, which can be difficult and expensive to monitor.

Ecologists use a variety of approaches and sources of information to estimate the baseline states of populations and communities: historical data such as ships’ logs and naturalists’ observations (Jackson, 1997), fossil and archeological information (Wing and Wing, 2001, Aronson et al., 2002), molecular-genetic techniques (Lessios et al., 2001, Roman and Palumbi, 2003), and even relationships between abundance and body mass (Levitan, 1992, Jennings and Blanchard, 2004). We have not, however, constructed a logical framework for choosing the target baseline for situations in which different techniques provide conflicting portraits of the pristine condition.

Here we illustrate this general problem by evaluating evidence from different methods of estimating the baseline state of coral reef communities, in terms of the abundance of seaweeds, or macroalgae. We use macroalgal cover as a key indicator of reef state, based on a broad consensus of coral reef scientists (Steneck, 1988, Liddell and Ohlhorst, 1992, Steneck and Dethier, 1994, Steneck and Sala, 2005). We define macroalgae as large, anatomically complex algal forms, including erect calcifying species but not filamentous algal turfs. Even erect, calcifying green algae, such as species of Halimeda, have increased on many reefs around the world over the last several decades and are thought to have a negative impact on coral populations (Szmant, 2001, Nugues et al., 2004, Smith et al., 2006, Birrell et al., 2008). Conceptual models of coral reef ecology frequently pool algae in this way (Hughes et al., 2010), rather than attempting to predict or depict the specific effect and dynamic of each coral-algal species pair. Algal turfs are not included in this category because far less is known about their effects on adult and juvenile corals (but see Birrell et al., 2005), and because their abundance and cover are rarely quantified accurately (Littler et al., 1987, Aronson et al., 1994, Miller et al., 2003).

Section snippets

Coral reef degradation and the missing baseline

Coral populations around the world began to decline several decades ago from a variety of causes including oceanic warming, storms, outbreaks of predators and diseases, and poor land-use practices that cause nutrient and sediment pollution. The loss of once-dominant corals, combined with the over-harvesting and die off of key grazers, has enabled seaweeds to increase in abundance on many reefs (McManus and Polsenberg, 2004). Seaweeds are perceived as harmful invaders because they can reduce

Estimating the seaweed baseline: The Jamaican prototype

One answer is based on historical surveys of a handful of reefs off Jamaica and St. Croix, U.S. Virgin Islands in the late 1970s and early 1980s (Adey and Steneck, 1985, Liddell and Ohlhorst, 1992, Hughes, 1994) from which average macroalgal cover was estimated to be approximately 2% (Côté et al., 2005, Schutte et al., 2010). These studies preceded the impacts of strong hurricanes on both islands in the 1980s and the regional mass mortality in 1983–1984 of the echinoid Diadema antillarum, an

Shifting Caribbean baselines

Because many reef scientists began their careers in the Caribbean during the 1970s, the field in general has largely adopted the condition of Caribbean reefs of this era – particularly Jamaican reefs – as the archetypal natural state (Côté et al. 2013). Caribbean reefs of the 1970s, however, were probably not representative of pre-human, pristine reefs. By the time scientists began studying coral reefs, people had been harvesting plants and animals from them for centuries (Wing and Wing, 2001,

Estimating the seaweed baseline: Quasi-pristine Pacific reefs

A second approach to understanding natural levels of seaweed abundance, which largely avoids this problem of shifting baselines, is to document the state of currently pristine or nearly pristine reefs (Vroom et al., 2006, Knowlton and Jackson, 2008, Sandin et al., 2008). As a consequence of their remote locations, and in some cases due to legal protection, fishing and other direct human impacts are minimal on certain reefs in the central Pacific (Knowlton and Jackson, 2008). The National

Baseline distributions

Reefs, like all communities, have always been disturbed. Even long ago in the pre-human past, reefs were dynamic, non-equilibrial systems and were not fixed in climax states of coral dominance (Woodley, 1992, Connell et al., 1997, Vroom et al., 2006). In his long-term monitoring study of shallow reefs on the Great Barrier Reef, Connell documented repeated fluctuations of macroalgal cover between 15% and 85% due to natural disturbances and community succession (Connell et al., 2004). Because

Trophic cascades and lessons from other systems

To investigate trophic cascades, ecologists experimentally remove carnivorous predators from model communities. Humans have effectively replicated this work in an uncontrolled fashion at far larger scales by removing carnivorous vertebrates for sustenance, profit, and sport from nearly every ecosystem on the planet. In most cases, the depletion of such predators weakens trophic cascades and reduces plant biomass. Marine examples include kelp forests, salt marshes and rocky subtidal habitats (

Conclusions

Different approaches to assessing the macroalgal baseline for the world’s coral reefs produce different baseline estimates – an unfortunate reality that leads to considerable ambiguity for managers and confusion in the literature (Bruno et al., 2009). Most reef scientists would agree that a reef with >50% seaweed coverage has been substantially degraded or has at least shifted to a macroalgal-dominated phase (Sandin et al., 2008, Houk and Musburger, 2013, Ruppert et al., 2013). But what about a

Acknowledgements

We thank Rusty Brainard, Katie DuBois, Les Kaufman, Judy Lang, Paul Sammarco, Brian Silliman, Robert Steneck, Hugh Sweatman, Maxwell Tice-Lewis, Jon Witman and several anonymous reviewers for their valuable help and advice and perspectives on coral reef baselines, and the CRED towed diver team for data collection. Support for this paper was provided by the University of North Carolina at Chapel Hill, the National Science Foundation and the NOAA Coral Reef Conservation Program. This is

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