Assessing the Ecacy of A Marine Reserve to Protect Sharks With Differential Habitat Use

Spatial management through the implementation of marine protected areas is one strategy to limit the extraction of sensitive marine species. Understanding the area used by marine life is thus a key step towards the evaluation of the management framework and ecacy of a protected area. To provide information of the protective coverage of the Galapagos Marine Reserve (GMR), we assessed the habitat utilization distribution (UD) of hammerhead and blacktip sharks in the GMR. Fifteen hammerhead sharks and 27 blacktip sharks were tagged with SPOT and SPLASH satellite tags in the north and south-central regions of the GMR between 2007 and 2012. Our results show nearly 90% of hammerhead shark’s UD was enclosed by the reserve boundary during the cold season (June-October), yet this decreased to only ~30% with the advent of the warm season (December-April). Conversely, blacktip sharks’ UD was 100% enclosed by the reserve boundaries in all seasons. Season and depth were the most important environmental parameters dening the UD of hammerhead sharks; whilst year and eddy kinetic energy were the most important parameters for blacktip sharks. These ndings suggest the size of the GMR may be effective for blacktip sharks but seasonally effective for hammerhead sharks.


Introduction
Despite the controversy around the magnitude of species' declines1 , 2, and the ecological effect such declines may produce3 , 4, it is accepted that over shing is the major cause of population decline among cartilaginous shes5 , 6. Sharks are mostly caught as by-catch in sheries targeting teleost sh species, such as tuna and marlin7. As such, sharks are being harvested under management regulations more suited to species with higher intrinsic rebound potential8 , 9. To avoid the collapse of shark populations, management should focus on reducing shing mortality to the population's rebuilding rate8.
Spatial closures are considered to be an important tool to aid the management of sheries targeting commercially and ecologically sensitive species10 , 11. Generally, spatial management is carried out through the implementation of xed marine protected areas (MPA), but it can also be implemented by seasonal12 or dynamic13 spatial closures. MPAs are increasingly becoming popular tools to limit the extraction of sensitive sh species and buffer the effects of sheries in surrounding marine ecosystems14 , 15. While there is substantial evidence supporting the implementation of MPAs in maintaining the biomass and diversity of coastal sh species16 , 17, their potential to protect highly mobile species is still the subject of debate18-20. Shark movements can exceed MPA boundaries and national jurisdictions21 , 22, making them vulnerable when migrating to unmanaged open-shing areas23. For wide-ranging species, MPAs should encompass a signi cant proportion of their life stages and movements, with emphasis on reproducing adults9.
Unfortunately, the lack of supporting evidence on the recovery of highly mobile sh species still limits a wider implementation of these reserves15.
The Galapagos Marine Reserve (GMR) is the second largest MPA in the Eastern Tropical Paci c Ocean (ETP), covering approximately 138000 km 2 of the pelagic environment surrounding the Galapagos Islands24. It lies in the con uence of three major currents, with marked seasonal gradients in current strength, sea surface temperature and productivity25. The reserve was created in 1998 with the main aim of protecting all the coastal marine ecosystems and a signi cant proportion of the pelagic waters surrounding the archipelago24. Theoretical approaches modelling the food-web interactions in the pelagic (open-water) Galapagos ecosystems, suggested that the pelagic and coastalpelagic shark species would be expected to have increased in biomass since the creation of the GMR26. However, contrasting the ecological knowledge of dive guides against empirical information about the relative sharks abundance demonstrates that this increases might only apply to certain coastal species, such as the blacktip shark (Carcharhinus limbatus) 27. Pelagic species such as the scalloped hammerhead shark (Sphyrna lewini) are reported to have declined by 50% in their relative abundance across the GMR27, which was also reported for other MPAs of the ETP28 , 29. Given the unknown spatial scale of the home range of shark species around Galapagos, there are concerns the size of the reserve may not adequately protect sensitive species like the critically endangered scalloped hammerhead shark30.
This study aimed to assess the protective coverage of the GMR over the home range of the scalloped hammerhead shark and the blacktip shark. Speci cally, this research is aimed to i) compare the environmental preferences of hammerhead and blacktip sharks in the GMR; ii) evaluate their spatial and temporal habitat utilization in relation to the size of the GMR; and iii) characterize the factors in uencing the selection of core areas (preferred habitat) within their utilization distributions.

Results
Relocation information was obtained from eight hammerheads (males = 6, females = 2), tracked for 5 to 148 days (average 48 days); and 18 blacktip (males = 2, females = 16) sharks tracked for 18 to 512 days (average 102 days) (  Hammerhead shark travel distance from the tagging location was signi cantly greater than for blacktip sharks (t-test p = 0.004). The average distance from the tagging location was 221 km (SD 191) for hammerhead sharks and 73.7 km (SD 76.2) for blacktip sharks. Hammerhead sharks travelled beyond the reserve boundaries although they did not migrate between the north and south of the GMR. In contrast, blacktip sharks remained within the reserve, particularly north of Santa Cruz Island, and migrated between regions within the GMR (  and extended away from the GMR boundaries in warmer seasons (Fig. 2). Approximately 90% of the estimated UD area of all hammerhead sharks was con ned within the GMR during the cold season; 65% in the transition period, and 30% in the warm season. Conversely, blacktip sharks' UD was completely con ned within the reserve across all seasons ( Fig. 2).
probability of the UD of hammerhead sharks ( Table 2). The best-t model explained 51.7% (R 2 = 0.493) of the total deviance and was obtained from the additive effects of depth, season, year and SST. Depth and season were the most important factors, followed by the year and SST. Despite the importance of chlorophyll a as a single factor, it did not have a major additive effect in the nal model. Partial response curves suggest hammerhead sharks remain during the colder months (June -October) in areas shallower than 1000 m where SST is lower than 25 o C (Fig. 3). In the case of blacktip sharks, all environmental predictors had a statistically signi cant in uence on their probability of UD, yet not all contributed to the top-tted models ( Table 2). The best-t model for this species explained 64.7% (R 2 = 0.493) of the total deviance and was built with four variables. Year and EKE were the most important factors in uencing the model, followed by SST and season. Partial response curves suggest blacktip sharks travelled farther distances during 2006 to 2012, but were staying closer to the core UD area towards 2015 (Fig. 3). GAM results suggest that core UD area of this species is characterized by EKE lower than 50 m 2 s 2 , sea oor depth less than 500 m and temperatures lower than

Discussion
Our results highlight the value of a MPA to protect shark species with coastal habitats and strong site delity, yet they also show that MPA size is less effective in the case of migratory coastal-pelagic species. While blacktip sharks movements were totally encompassed by the GMR size, hammerhead shark movements were mostly protected by the reserve boundary only during the cold season. that female blacktip sharks display strong philopatry to their nursery grounds found around the Caribbean and North-western Atlantic region. The occurrence of important nursery grounds in the south central GMR46 further supports this for the GMR. The presence of feeding grounds in the area, either via prey availability (e.g. whitetip reef sharks47, sealions48), or food provisioning from ships or shers49, could be also in uencing the strong delity observed around Santa Cruz Island.
The reported habitat use in addition to the recently reported relative abundance increase27 and identi ed nursery grounds for blacktip sharks46 indicate that the GMR provides adequate protection for the different life history stages.
By contrast, hammerhead sharks were reported to have declined by 50% within the GMR27, which in combination with our results suggest this species is not being effectively protected by this MPA. Although there are informal reports of juvenile hammerhead sharks, at present there is no scienti cally assessed hammerhead nurseries within the GMR. This suggests only adult and sub-adults individuals are bene ting from the reserve's protective coverage, particularly during the cold season. If fully functional nursery grounds were present, we'd expect UDs, especially of females, to show seasonal movement towards pupping grounds within the GMR. The apparent recovery of blacktip sharks and decline of hammerheads re ect these differing levels of protection in Galapagos. A similar scenario for both species has been reported for Cocos Island28, a smaller MPA also located the ETP.
The inadequacy of the reserve size to protect hammerhead sharks is of particular concern given this species' current global endangered status30. A revision of the management of this species in the ETP suggested the creation of several small non-take MPAs (which include the existent MPAs of the region) enclosed in a large special marine managed area from Galapagos to Costa Rica50. Such a special managed area would allow a considerably reduced shing effort and should be equal in size to the Exclusive Economic Zones of the countries with national jurisdiction in the region.
Achieving this complex spatial zoning, however, would require high levels of national and international agreements and would have important economic implications for the industrial shing operations in the area. Also, this will not stop interactions between sheries and hammerhead sharks whenever they leave the small non-take MPAs.
Alternatively, dynamic spatial closures extending the current xed GMR boundaries could reduce the susceptibility of 2014. All sharks were caught from a small boat using barbless circle hooks and nylon lines, with pieces of skipjack (Katsuwonus pelamis) or wahoo (Acanthocybium solandri) as bait. Once hooked, sharks were allowed to calm down prior to slowly being towed to a mother-vessel located less than 10 minutes away. Sharks were either brought on board using a sling and hydraulic crane, or drawn onto a platform that was lowered into the water and subsequently raised above sea level. On deck, sharks were immobilized, their eyes covered with a wet cloth, and seawater pumped continuously across their gills. All sharks were measured and sexed, after which either SPOT 5 or SPLASH (Wildlife Computers -Redmond, USA) satellite transmitter tags were attached to the dorsal n with nuts, bolts and rubber gaskets. These tags were con gured to send location data to Argos satellites whenever a shark's dorsal n breached the water surface.  on the adjusted Akaike's Information Criterion (AICc) and Bayesian Information Criterion (BIC) values to take into account differences in effective sample size and lack of t57 , 58. We followed a manual step-wise model construction and selection process. We built an initial model with predictors independent from each other, and then selected the best model using the lowest AIC and BIC. We continued building more complex models by adding each additional predictor considered one at a time. We favoured the parsimony principle and chose simpler over more complex models whenever we obtained competing models with similar AIC and BIC results.
Ethics Statement.
All research methods were carried out in accordance with relevant guidelines and regulations approved by the Galapagos Marine Reserve location and spatial extent of hammerhead sharks and blacktip sharks trajectories. Note: The designations employed and the presentation of the material on this map do not imply the expression of any opinion whatsoever on the part of Research Square concerning the legal status of any country, territory, city or area or of its authorities, or concerning the delimitation of its frontiers or boundaries. This map has been provided by the authors.

Figure 2
Hammerhead sharks and blacktip sharks habitat utilization distribution areas.