How robust are estimates of coral reef shark depletion?
Introduction
Apex predators are large carnivores that occupy the top trophic level of food webs. They are typically characterized by conservative life history traits, such as slow growth rates, late sexual maturity, and low fecundity. These traits make them particularly susceptible to over-harvesting, and apex predators often are preferentially targeted by humans for food or game (e.g. Myers and Worm, 2003). Consequently, apex predators are typically the first to become extinct or locally extirpated. This loss of apex predators may have extensive, adverse effects on ecosystem structure and function. In terrestrial, marine and freshwater systems, for example, changes in apex predator abundance have affected herbivore populations, with substantial flow-on effects to plant communities that provide the primary production and habitat structure that support biodiversity in these ecosystems (Estes et al., 2011).
In marine food webs, sharks are common apex predators, and also are socio-economically valuable resources (Heithaus et al., 2008). This is most apparent in tropical ecosystems, such as coral reefs, where reef sharks are believed to play an important role in ecosystem resilience (e.g. Ruppert et al., 2013), and they generate ∼$1billion USD annually from ecotourism and fisheries (Cisneros-Montemayor et al., 2013). However, recent surveys of sharks of the Red Sea (Berumen et al., 2013), the Great Barrier Reef (GBR; Hisano et al., 2011, Robbins et al., 2006), the Indian Ocean (Graham et al., 2010), the Pacific Ocean (Nadon et al., 2012) and the Caribbean (Ward-Paige et al., 2010b) indicate substantial declines compared to estimated baseline populations, which have been primarily attributed to increased fishing pressure. Given the putative ecosystem functions provided by sharks, the need for accurate assessments of population status is crucial for effective coral reef management and to sustain the livelihoods of people who depend on their ecosystem goods and services.
Currently, the severity of shark population declines on coral reefs is disputed (e.g. Heupel et al., 2009). Differences in survey method selection are commonly cited as a potential cause for discrepancies in abundance estimates (e.g. Graham et al., 2010, Ruppert et al., 2013, Ward-Paige et al., 2010a). Sharks may respond variably to different stimuli such as noise, bait, divers, and boats, which are employed in different ways in different types of surveys (Cubero-Pardo et al., 2011, Fitzpatrick et al., 2011, Ward-Paige et al., 2010a). In addition, some methods, particularly diver-based counts, have been criticized for potentially producing biased estimates of differences in shark abundance along gradients of human interaction (Ward-Paige et al., 2010a). If sharks are less accustomed to people at unfished or remote locations, they may be more likely to approach divers, leading to over-estimates of abundance in those locations, relative to areas with more human activity (Graham et al., 2010).
Recent studies have concluded that reef shark populations in fished areas are severely depleted, and that low levels of poaching render no-take marine reserves much less effective than strictly enforced no-entry zones (Ayling and Choat, 2008, Robbins et al., 2006). Because estimates of population status in these studies have relied heavily on relative abundances from diver-based surveys, resolving the controversy about the validity of these approaches is crucial for evaluating the effectiveness of no-take marine protected areas for protecting apex predators with low intrinsic population growth rates, such as reef sharks, and for determining how best to assess the status of such populations. In particular, for estimates of baseline shark densities to be unbiased, sharks should neither actively avoid, nor approach, divers conducting surveys. Consequently, estimates of population depletion based on relative abundances estimated in fished and unfished areas, will be compromised if any such biases differ in magnitude in areas with different levels of fishing pressure. To date, the only study to investigate the performance of survey methods for sharks was undertaken at a single remote location (Palmyra Atoll, Line Islands) where sharks may be naïve towards humans (McCauley et al., 2012). Thus, an assessment of sharks’ responses to alternative survey methods across a gradient of human interaction, and the responses’ implications for estimates of absolute and relative abundance, is needed to assess the robustness of recent conclusions about the status of reef shark populations and their vulnerability to poaching in no-take marine reserves.
Here, we address this issue by comparatively evaluating four visual survey techniques that are commonly used for estimating shark abundance: (1) timed-swim, (2) towed-diver, (3) stationary-point-count (SPC), and (4) baited-remote-underwater-video (BRUV). In addition, we trialed a novel survey method, (5) audible-stationary-count (ASC), which uses low frequency sound to attract sharks to a stationary point. During each replicate survey, we recorded any observed behavioural response of sharks to divers, as well as the time at which each shark was observed. If sharks are attracted to divers, then we expect encounter rates with new individuals to be high when divers first enter the water to commence counting, and to decrease thereafter. Conversely, if sharks respond neutrally to divers, encounter rates should not increase or decrease over the course of a survey time. Each method was repeated across a gradient of human interaction in order to quantify whether any such biases vary, depending on the prevalence of human activity on the reef. To achieve this, we conducted our study in the Great Barrier Reef Marine Park (GBRMP), a system of spatial zoning that includes: (1) no-entry zones, which are strictly enforced exclusion areas; (2) no-take zones, which are conservation areas where fishing is prohibited, but non-extractive activities (e.g. diving) are allowed and where low levels of illegal fishing have been recorded (Davis et al. 2004); and (3) fished zones, which are general use areas that allow fishing and other extractive activities. Finally, we converted all shark counts to density estimates, and we tested for any differences between survey methods in shark abundance estimates, allowing for potential interactive effects with management zone and habitat type.
Section snippets
Study sites and species
Surveys were performed at Rib Reef (fished zone), Little Kelso Reef (no-take zone) and Bandjin Reef (no-entry zone) in the central Great Barrier Reef (GBR), and Northwest Reef (fished zone), Tryon Reef (no-take zone) and Wreck Reef (no-entry zone) in the southern GBR (Fig. 1). At each reef, zone boundaries are a minimum of 1–2 km from the reef edge. All six reefs are comparable in morphology and distance from shore, with a well-developed reef slope, reef flat and back reef, and each reef has an
Results
We found no direct observational evidence of differences in behavioural responses to divers across management zones. Individual sharks were found to be visibly unique (in terms of species, size, sex, colour patterns, scars, etc.) and no shark was knowingly observed more than once during a single survey. Frequency distributions of behavioural responses among management zones were homogeneous (, P > 0.25; Fig. 2). Across all management zones, only a small proportion of sharks were evasive
Discussion
While there is wide agreement that reef sharks are in decline in many regions of the world, the appropriateness of baseline population estimates and the effectiveness of no-take areas for protecting shark populations have been the subject of increasing debate, especially over the past five years (Heupel et al., 2009, Hisano et al., 2011, Nadon et al., 2012). Much of the controversy has revolved around the reliability of diver-based estimates of absolute and relative abundances of sharks in
Acknowledgements
We thank M. Cappo and M. Stowar of the Australian Institute of Marine Science for loan of BRUV equipment, B. Bergseth, M. Rocker, S. Sandin and one anonymous reviewer for useful comments on the manuscript and M. Hisano for help with data analysis. This research was undertaken with permission from the Great Barrier Reef Marine Park Authority (permit no. G11/34529.1). Funding was provided by the Australian Research Council Centre of Excellence for Coral Reef Studies and the School of Marine and
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These authors contributed equally to the research.