Current Biology 16, 2314–2319, December 5, 2006 ª2006 Elsevier Ltd All rights reserved DOI 10.1016/j.cub.2006.09.044 Report Ongoing Collapse of Coral-Reef Shark Populations William D. Robbins,1,* Mizue Hisano,1,2 most-abundant reef shark species, the whitetip reef Sean R. Connolly,1,2 and J. Howard Choat1 shark (Triaenodon obesus) and the gray reef shark 1 School of Marine and Tropical Biology (Carcharhinus amblyrhynchos), in four levels of coral- James Cook University reef management zones. These zones represent a gradi- Townsville, Queensland 4811 ent in fishing pressures because (1) no-entry zones are Australia aerially-surveyed, strictly-enforced exclusion areas (1% 2 Australian Research Council of total reef area on the GBR). (2) No-take zones cannot Centre of Excellence for Coral Reef Studies legally be fished, although fishing boats are permitted James Cook University to be present (30% of total reef area); moderate levels Townsville, Queensland 4811 of illegal fishing have been documented in these zones Australia [18]. (3) Limited-fishing zones have tight restrictions on the type and quantity of fishing gear permitted (4% of reef area). (4) Open-fishing zones have fewer gear re- Summary strictions on line fishing (60% of reef area) (Figure 1). We contrast reef shark abundances in these zones with Marine ecosystems are suffering severe depletion of those we found through comparative sampling at the apex predators worldwide [1–4]; shark declines are southern atoll of the Cocos (Keeling) Islands in the Indian principally due to conservative life-histories and fish- Ocean. This isolated Australasian atoll may be one of eries overexploitation [5–8]. On coral reefs, sharks the last pristine reefs in the world [19], with no recorded are strongly interacting apex predators and play a history of commercial shark fishing and negligible re- key role in maintaining healthy reef ecosystems [9– creational shark fishing. Its inclusion allows for an addi- 11]. Despite increasing fishing pressure, reef shark tional estimate of reef shark abundance under minimal catches are rarely subject to specific limits, with man- exploitation, to complement our estimates from no-entry agement approaches typically depending upon no- zones. take marine reserves to maintain populations [12–14]. We find substantially lower numbers of reef sharks Here, we reveal that this approach is failing by docu- outside no-entry zones than within them (Figure 2). No- menting an ongoing collapse in two of the most abun- entry reefs sustain shark abundances similar to the min- dant reef shark species on the Great Barrier Reef (Aus- imally fished shark populations in the Cocos (Keeling) tralia). We find an order of magnitude fewer sharks on Islands. Compared to the no-entry reefs, abundances fished reefs compared to no-entry management zones on reefs with the fewest fishing restrictions (open-fish- that encompass only 1% of reefs. No-take zones, which ing zones) are reduced by 80% for whitetip reef sharks are more difficult to enforce than no-entry zones, offer and 97% for gray reef sharks on the Great Barrier Reef almost no protection for shark populations. Population (Figure 2). Abundances on limited-fishing reefs are viability models of whitetip and gray reef sharks pro- nearly identical to those of open-fishing reefs. Surpris- ject ongoing steep declines in abundance of 7% and ingly, abundances on no-take reefs, where fishing boats 17% per annum, respectively. These findings indicate may anchor but fishing is illegal, were also heavily de- that current management of no-take areas is inade- pleted and remarkably similar to the legally fished quate for protecting reef sharks, even in one of the zones. These results indicate that not only are reef shark world’s most-well-managed reef ecosystems. Further populations heavily depleted on fished reefs but also steps are urgently required for protecting this critical that there is a dramatic difference in the effectiveness functional group from ecological extinction. of no-entry zones and no-take zones. Indeed, it is strik- ing that the abundance differences that we observe be- Results and Discussion tween no-entry and fished reefs are comparable in mag- nitude to differences in reef shark biomass documented The Australian Great Barrier Reef (GBR) is widely re- between lightly and heavily fished islands in Hawaii [10]. garded as one of the least-degraded reefs in the world One possible explanation for the marked difference in [15, 16]. It is regulated by a hierarchical series of manage- abundance between no-take and no-entry zones is that ment zones, the aim of which is to balance conservation sharks move from no-take to fished zones (where they with sustainable use [17]. The status of shark popula- are caught) more frequently than they move from no- tions in this system should therefore provide a conserva- entry to fished zones. However, although movements tive picture of the vulnerability of reef sharks worldwide of sharks may occur between reefs zoned for different as well as yield valuable insights into the efficacy of no- fishing levels [20], it is unlikely that reef sharks preferen- take zones as a management tool for high-trophic-level tially move out from areas of lower density (no-take predators. By using fisheries-independent underwater zones) at greater rates than from areas of higher density visual censuses, we surveyed populations of the two (no-entry zones). No-take and no-entry zones are often similar in size and similarly interspersed among open- fishing and limited-fishing zones (Figure 1). Indeed, no- *Correspondence: [email protected] entry reefs may be found within 1–2 km of open-fishing Ongoing Collapse of Coral-Reef Shark Populations 2315 Figure 1. Location of Great Barrier Reef Underwater Visual Censuses No-entry zone reefs surveyed were Carter (CT) and Hilder (HD) reefs; no-take zone reefs were Barnett Patches (BP), Coil (CL), De- tached (DT), MacGillivray (MG), No Name (NN), and Wheeler (WL) reefs; limited-fishing zone reefs were Bommie Bay (BB), Crystal Beach (CB), Myrmidon (MD), Needle (ND), Trunk (TK), and Washing Machine (WM) reefs; open-fishing zone reefs were Britomart (BM), Chicken (CH), Day (DY), Helix (HX), Hicks (HC), Knife (KF), and Yonge (YG) reefs. Cur- rent zonation of BB, CB, MG, and WM reefs was implemented in 1983; other listed north- ern reef zones were implemented in 1992. All listed central reef zones were implemented in 1987. reefs, yet we still find higher abundance levels on the no- (Table 1). Our results indicate very high probabilities of entry zone reefs. Moreover, the movements of reef population decline, with 98% and 100% of simulations sharks such as the whitetip reef shark are limited (0–3 yielding negative population growth for whitetip and km) [21], suggesting a high level of site fidelity. Conse- gray reef sharks, respectively. Moreover, the magnitude quently, the most likely explanation for the discrepancy of estimated population decline is severe: Median rates between no-entry and no-take reefs is that illegal fishing of population decline are 7% per annum for whitetip reef in no-take zones, which has been documented even on sharks and 17% for gray reef sharks (Figure 3). If current comparatively well-policed inshore reefs [18], has a population trends continue unabated, the abundance of highly deleterious effect on reef shark abundances. Sim- whitetip reef sharks and gray reef sharks present on le- ilar poaching problems appear to be common to many gally fished reefs will be reduced to only 5% and 0.1%, coral-reef marine reserve systems worldwide [22]. respectively, of their present-day no-entry abundance In principle, there are two ways in which fishing pres- levels within 20 years. The potential for further reduc- sure may produce the differences observed in shark tions in population growth rates at such low population abundance between no-entry and fished reefs: directly, densities (e.g., difficulty finding mates or other such through overfishing of sharks and indirectly, through Allee effects [24]) may well make this population collapse fishing of prey species, forcing sharks to seek prey on increasingly difficult to reverse as time progresses. unfished reefs. However, it is unlikely that indirect fishing The minimum change in mortality necessary to pro- pressures are responsible for the patterns we observe in duce a median estimated population growth rate of 1.0 these reef sharks. The preferred prey of both shark spe- (i.e., population stability) was calculated for each spe- cies includes benthic fishes (Scaridae and Acanthuri- cies. Analyses indicate that reductions in annual mortal- dae), cephalopods, and eels (Muraenidae) [21, 23], but ity by one-third (36%) for the whitetip reef shark and one- with the exception of cephalopods, these species are half (49%) for the gray reef shark would be required to neither commercially nor recreationally fished on the halt these ongoing declines. However, with commercial Great Barrier Reef. We conclude, therefore, that the catches of sharks nearly quadrupling on the Great Bar- most likely explanation for the differences in abundance rier Reef between 1994 and 2003 [13] and recreational between no-entry and fished zones is because of the fishing also removing large numbers of sharks in Aus- direct capture and removal of sharks. tralia [25], the trend is strongly in the opposite direction. To determine the sustainability of the two reef shark Recent attempts to quantify rates of shark population species, we conducted population viability analyses by decline [6, 7] have been criticized as overly pessimistic using independently obtained biological parameters because of their reliance on trends in catch rates re- from the same populations. Annual survival estimates corded in logbooks [26, 27]. Management plans have were calculated from the age-frequency distribution of called for more comprehensive data before drawing con- each species, and age-specific fecundities were calcu- clusions about population status [28].