Managing Bite Risk for Divers in the Context of Shark Feeding Ecotourism: a T Case Study from French Polynesia (Eastern Paciﬁc)

Home , Galeocerdo, Negaprion, Sicklefin lemon shark

Tourism Management 68 (2018) 275–283

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Tourism Management

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Managing bite risk for divers in the context of shark feeding ecotourism: A T case study from French Polynesia (Eastern Paciﬁc)

∗ Eric E.G. Cluaa,b, a EPHE, PSL Research University, CRIOBE USR3278 EPHE-CNRS-UPVD, F-66860 Perpignan, France b Labex Corail, CRIOBE, 98729 Moorea, French Polynesia

GRAPHICAL ABSTRACT

ARTICLE INFO ABSTRACT

Keywords: Shark-based ecotourism has been recently expanding around the world. Provisioning sharks, however, is not Ecotourism management without risk and accidental bites on humans are regularly reported. Such events may jeopardise the shark Diving tourists safety ecotourism industry and local economies. Through a case study from French Polynesia, I investigated whether Provisioning and smelling changes in feeding practices of lemon sharks between the early 1990s and 2013 are related to recent accidental Agonistic behaviour bites of divers. Hand-feeding, ‘smelling’ and surface feeding facilitated the development of agonistic behaviour Sickleﬁn lemon shark in sharks, which resulted in accidental bites. The level of interaction between sharks and humans appears to be Negaprion acutidens. the most important driver for analysing bite-risk. This paper presents the very ﬁrst framework for risk-analysis and will allow managers to better manage the risk associated with current practices in shark-feeding around the world. The paper also provides technical guidelines for the design of adequate legal frameworks that will support any sustainable shark feeding operation.

1. Introduction as the central and north Atlantic (UK, Azores, Canary islands) (Gallagher & Hammerschlag, 2011; Topelko & Dearden, 2005). Glob- Shark-based ecotourism operations are widespread around the ally, c. 590,000 tourists participate in shark watching and spend USD world and occur in at least 40 diﬀerent countries mainly in tropical and 314 million per year, directly supporting 10,000 jobs (Cisneros- subtropical oceans in the Caribbean (Bahamas, Cuba, West Indies), Montemayor, Barnes-Mauthe, Al-Abdulrazzak, Navarro-Holm, & Central and South America (Costa Rica, Belize, Mexico, Ecuador), Sumaila, 2013). Although valuations made at the scale of single animals Southern and East-northern coasts of South Africa, Paciﬁc (Australia, are frequently based on assumptions that may not withstand critique Palau, Fiji, Hawaii and French Polynesia) (Brena, Mourier, Planes, & (Catlin, Hughes, Jones, Jones, & Campbell, 2013), Clua, Buray, Clua, 2015). Shark tourism, however, occurs even in cold oceans such Legendre, Mourier, and Planes (2011) estimated that each of the 13

∗ EPHE, PSL Research University, CRIOBE USR3278 EPHE-CNRS-UPVE, Université de Perpignan, 58 avenue Paul Alduy, Bâtiment R, F-66860 Perpignan, France. E-mail address: [email protected]. https://doi.org/10.1016/j.tourman.2018.03.022 Received 3 February 2015; Received in revised form 25 March 2018; Accepted 27 March 2018 0261-5177/ © 2018 Elsevier Ltd. All rights reserved. E.E.G. Clua Tourism Management 68 (2018) 275–283

Fig. 1. (A) Location of Bora-Bora in the eastern Central Paciﬁc. (B) The island is composed of a central islet surrounded by a medium-sized lagoon (78 km2)deﬁned by a large barrier reef that includes in the West a large passage (Teavanui pass) and several ‘motu’ (hard soil areas with trees on the barrier). Sites 1, 2 and 3 are dedicated to outer slope diving and snorkelling, targeting large sharks, while sites 4 and 5 are the most favoured lagoonal sites for small shark observations. Site 1, called ‘Tapu site’ and located at around 1000 m from the passage, has been and is still the most used site for both scuba-diving and snorkelling with large sharks.

lemon sharks most often observed at a feeding site off Moorea (French address the issue of bite-risk in order to minimise the danger and op- Polynesia) had an average contribution to the local economy of around timise the sustainability of these activities. More recently, Richards USD 315,000 per year. Similar results were found for Palau (South et al. (2015) interviewed 45 diving/snorkelling shark operators, and Pacific) where shark diving generates USD 1.2 million in salaries and found out that nine reported ‘troublesome behaviours’ from sharks, USD 1.5 million in taxes annually (Vianna, Meekan, Pannell, Marsh, & suggesting a more precautionary approach to provisioning. Meeuwig, 2012). In addition to economic benefits, there is also a view Sharks are probably one of the most demonised species groups in that non-consumptive wildlife tourism provides substantial conserva- human history. A number of newspaper articles and television pro- tion value to vulnerable and endangered species, through educating grams (CBS, 2001, Wordpress, 2007, Discovery channel, 2013) have tourists about the need for conservation of animals that play a critical specifically speculated that shark attacks are linked to the potential role in ecosystems (Bookbinder, Dinerstein, Rijal, Cauley, & Rajouria, conditioning of sharks to humans through chumming and feeding 1998; Heithaus, Frid, Wirsing, & Worm, 2008) and limiting pressure for during shark dives and/or simple observation from the surface. Due to extractive use of these species. the particular ‘hysteria’ that can surround sharks and diving with po- Although not all shark tourism involves scuba diving and feeding, tentially aggressive sharks, State interventions in terms of either ban- artificial provisioning is the most common form of interaction and takes ning the activity (such as in Florida, Hawaii, Maldives, California, etc.) several forms. Chumming (also called ‘berleying’) involves placing or using licensing (such as in the Commonwealth of Northern Mariana blood and/or liquidised fish parts in the water to create a slick that islands CNMI, South Africa, Australia, etc.) to control the activity are sharks can sense and follow to the chumming location (Laroche, Kock, becoming increasingly preferred options around the world (Dobson, Dill, & Oosthuizen, 2007). In many instances, animals are not fed 2006). When regulations take over on banning, the technical approach during chumming. In contrast, at many shark tourism sites, large pieces is either based on geographical considerations (feeding operations are of fish are fed to the sharks (Dobson, 2007, pp. 49–65, Clua, Buray, displaced far from other recreational marine activities, such as in Legendre, Mourier, & Planes, 2010, Clua et al., 2011). Such provi- Australia and French Polynesia) or on vague definitions of the concept sioning of animals over long time periods may lead to negative impacts of ‘feeding’ (such as in CNMI). Nowadays, governance regimes are to animals and humans (Brena et al., 2015; Dobson, 2006; Gallagher deeply affected by the quantity and quality of available scientific data et al., 2015; Newsome & Rodger, 2008). For example, based on a 5-year (Dobson, 2007, pp. 49–65; Techera & Klein, 2013). The identification of study of an aggregation of sicklefin lemon shark (N. acutidens)ata best practice legal regulation requires therefore scientific research and feeding site in Moorea (French Polynesia), Clua et al. (2010) showed objective data on biological and ecological issues that drive the real risk that intra- and interspecific aggression was witnessed, leading to a for human safety induced by shark-based ecotourism. potentially increased risk of severe bites to humans, mainly during and Here, I use a case study in French Polynesia to suggest how feeding immediately after the mating season. These findings potentially confirm practices influence and potentially increase bite risk for divers. I then the fact that shark feeding may pose significant safety hazards for re- propose a framework of risk-analysis associated with underwater creational divers (Orams, 2002). feeding practices in order to facilitate the management of bite risk Shark bites occur in the context of underwater provisioning activ- among feeding-based shark diving activities. ities. The International Shark Attack Files (ISAF) database (2016) reports 9 cases of shark attacks that occurred during feeding worldwide 2. Material and methods between 1971 and 2013. None of these cases were fatal, except one in 2008 in Bahamas (ISAF 2008). For the same period, the Global Shark 2.1. Description of the study site Attack File (GSAF) database reports 12 cases (GSAF 2017). However, it is likely that, due to the risk of a strong negative impact on the eco- French Polynesia encompasses 118 islands that are gathered in five tourism activity with subsequent economic impacts (Topelko & archipelagos across a 5.5 million km2 Exclusive Economic Zone in the Dearden, 2005), bites in the context of ecotourism are not publicised by Eastern Central Pacific(Fig. 1). The two main sources of income for a professionals and are globally under-reported. As a demonstrative ex- population below 260,000 inhabitants are the black pearl oyster in- ample, the analysis of 54 cases of shark bites (most not reported to dustry and tourism with an average of 180,000 visitors per year (IEOM international databases) that occurred between 1979 and 2001 in 2016). Reef scuba-diving represents around 20% of the leisure activities French Polynesia (Eastern Pacific) showed that up to 25 cases (45%) of tourists, but was threatened during the mid-and late 1990s after were actually linked to shark feeding (Maillaud & Van Grevelynghe, several catastrophic events degraded reefs. These included a crown-of- 2005). This under-reporting should not hamper the need to efficiently thorns starfish (Acanthaster planci) outbreak (1984) on the main diving

276 E.E.G. Clua Tourism Management 68 (2018) 275–283 destinations of Moorea and Bora-Bora that were also impacted by major 2.3. Data collection and analysis coral bleaching events in 1991 and 1994 and cyclones Wasa (December 1991), Martin (October 1997) and Osa (November 1997) (Adjeroud The results of this study can be considered as a synthesis of two et al., 2005). complementary approaches. Firstly, the above mentioned study (see To improve diving attractiveness, dive operators began artificial Clua et al., 2010) gave the author a privileged access to the observation provisioning of sharks in some areas where tourists were taken on an and understanding of lemon shark behaviour, both at an individual and almost daily basis. Partly because of some minor incidents in the early collective levels, in the context of artificial provisioning. This experi- 2000s, legislation was introduced in French Polynesia under article 3 of ence came in addition to more than 1000 h of shark scuba and free the Ministers' Council statement N°396 of 28 April 2006 which stipu- diving experience that he had previously performed. Secondly, a spe- lated that ‘in the lagoons, reef passages and (outer reef) in a radius of cific study was implemented in Bora-Bora where the author was asked 1 km centered on the axis of any passage, any activity, being free or (at the end of February 2013) to conduct a risk assessment, following a commercial, based on the observation of sharks attracted by humans, bite on a tourist that had taken place earlier in the month during a shark through in particular a provisioning process commonly named as dive. An on-site mission was conducted from 02 to 05 March 2013. ‘shark-feeding’, is prohibited’. This legislation impacted the islands of During this mission, interviews (see Appendix 1) were conducted of i) Rangiroa and Fakarava (Tuamotu Archipelago), but mainly the islands both the current and former presidents of the Bora-Bora Tourism Ac- of Tahiti, Moorea and Bora-Bora (Windward Islands) where the shark- tivities Board (BBTAB), who are both shark-based ecotourism operators, feeding activity was most developed. Moorea and Bora-Bora are high ii) four dive masters, two each from the two main dive operators in islands with an encircling coral reef with passages and emergent land Bora-Bora, including the one that registered the accidental bite, and iii) areas that support several high standard hotels. Shark feeding was de- a dive master who was bitten by a lemon shark in 2009. This dive veloped in both of them in the early 1990s and expanded considerably master provided several underwater videos taken in the Tapu site (see after 1997. From the beginning, provisioning of blacktip reef sharks Fig. 1) during the previous years. A meeting of 32 members of the (Carcharhinus melanopterus) was developed within the lagoon where BBTAB collectively discussed the history and present situation of shark- tourists can observe the sharks standing in ca. 1 m of water or while feeding operations in Bora-Bora, in presence of the author. All minutes snorkelling. At the same time, operators working on the outer reef slope of the 28 meetings of the BBTAB from April 2006 to March 2013 were began to attract larger species including grey reef sharks (Carcharhinus also investigated. Finally, two diving sessions were conducted at the amblyrhynchos) and, more commonly, sicklefin lemon sharks (Negaprion usual operating times with the two main diving operators on the acutidens). For the specific purpose and in the framework of this study, I feeding site of Tapu (Fig. 1). The analysis of data consisted of detecting, will focus on Bora-Bora island where in 2013 a dozen ecotourism op- through both interviews of divers and video footages, behavioural erators were involved in lagoon shark feeding and five operators in changes in the sicklefin lemon shark population (and potentially at an provisioning on the outer slope, respectively (Fig. 1). I will however individual level) visiting the Tapu site over the past two decades. Ad- also use the results of a previous study that was conducted in Moorea ditional Bora-Bora underwater videos were also obtained from Poly- island between 2005 and 2010. For details about the development of nesian divers and internet (www.youtube.com) to support the results. shark feeding in Moorea island, quite similar to the one of Bora-Bora, In parallel, the number of tourists involved in aquatic activities, the see Buray, Mourier, Planes, and Clua (2009) and Clua et al. (2010). spatial distribution of activities and the potential changes in feeding practices were compiled with an historic perspective. The data were considered as reliable when either several persons (at least two) or 2.2. Behavioural ecology of the sicklefin lemon shark video footage (properly dated) confirmed the same data. Through the approaches listed above, I adressed the following The sicklefin lemon shark Negaprion acutidens (Rüppell, 1837) is a questions: large (≤340 cm total length) shark found in tropical inshore waters of continental and insular shelves in the Indo-Pacific. Sicklefin lemon - Are the bites on divers linked to a general change in behaviour sharks are considered largely benthic, and rarely occur near the surface, within the lemon sharks population? Or, should we consider them as except in the context of feeding by humans (Compagno, 1984).The few isolated events perpetrated through stochastic and specific beha- data on diets suggest it is primarily piscivorous (Stevens, 1984). The viours of individual animals, that are both difficult and potentially sicklefin lemon shark is often considered potentially dangerous because impossible to manage. of its large size, but is normally inoffensive and sluggish except when - If they exist, can the changes of behaviour among the shark popu- provoked (Compagno, 1984). Adults are mostly solitary, except during lation be related to changes in feeding practices? Or, are these ac- the mating season when males are found following females. cidents linked to stochastic events favoured by an extended period Sicklefin lemon sharks have recently become a focal species in shark of shark feeding in a given shark population, regardless of the feeding activities in the eastern Paci fic, in particular in French practices implemented. Polynesia (Buray et al., 2009). Sicklefin lemon sharks are not, however, as gregarious as other shark species involved in shark feeding opera- 3. Results tions, such as the grey reef shark that naturally aggregate in large schools in confined areas (Compagno, 1984). Ecotourism and feeding, 3.1. History of feeding practices in Bora-Bora however, promote large aggregations of adult lemon sharks year round, that can involve more than 30 different animals, with up to a dozen When shark feeding for ecotourism started in Bora-Bora in the early present during a single session. Through 949 diving. 1990s, it was implemented by a small number of operators, but in- Surveys conducted over 44 months, Clua et al. (2010) investigated creased significantly in the late 1990s after cyclone Osea seriously da- the behavioural response of 36 photo-identified adult sicklefin lemon maged the Bora-Bora coral reefs in November 1997 and live coral cover sharks involved in daily provisioning in Moorea island. In the frame- dropped to 32% in 1998 (Adjeroud et al., 2005). This reduced the visual work of the Moorea study, they focused on the ecology and residence attractiveness of traditional diving and stimulated the development of patterns of these animals but data on the behaviour was also collected. shark feeding. At the end of the 1990s, two different types of shark- They noticed that during provisioning, intraspecific aggression could be feeding were ongoing, together attracting almost 100,000 tourists per observed, possibly due to competition for food and access to receptive year. Of these, 90% were bathers/snorkellers and the rest scuba-divers. females as well as potentially agonistic behaviour toward humans, The first activity occurred inside the lagoon where snorkellers were mainly around the mating season. brought on large pirogues taking up to 30 people, to observe blacktip

277 E.E.G. Clua Tourism Management 68 (2018) 275–283

1). - Phase 2: 2007–2008. Stationary viewing was abandoned by some operators who feared that it was not sufficiently stimulating to their clients. These operators used a technique called ‘smelling’, whereby fish flesh or entire sardines or anchovies were enclosed in a small plastic bag or a little pipe with holes and held by the dive master (under the Buoyancy Compensator –BC- vest) while the group swam. This practice was intended to permit a group of divers to swim around the reef slope, being escorted by large sharks, kept at short distances by the odour. During this phase, snorkelers mostly observed sharks attracted by scuba-divers either on the bottom or in the water column. Some operators did however start to implement some surface feeding to aggregate bony fishes (such as jacks) and blacktip reef sharks in the vicinity of the snorkellers. – Fig. 2. Gross evolution of numbers of tourists and recreational activities from - Phase 3: 2009 2013. The visitation to Tapu spot grew to an average 1998 to 2013 (divided in 4-year periods). The lagoonal dystrophic event in of 35,000 snorkellers and 7000 scuba-divers per year (source: 2001 led to a significant shift of ecotourism activities from the lagoon (where BBTAB) and new practices were implemented. First, hand feeding they represented 82% before 2002) to the outside reef (where they came up to (instead of ‘patch hiding’) was initiated by some scuba-diving op- 47% in 2002, and up to 49% after 2009). erators in order to increase the attractiveness of the underwater spectacle (Fig. 3B), but also to compete with the development of reef sharks in shallow waters (< 1.2 m depth) that were attracted by surface feeding by the snorkelling operators. The surface feeding fi small pieces of fish flesh. The second activity was based on provisioning focused on bony shes and blacktip reef sharks that were observed on the outer slope of the reef to attract either grey reef sharks or lemon by snorkellers who remained close to the pirogue, often holding a sharks (plus some blacktip reef sharks) to be observed by scuba-divers. wooden bar or special lines tied to the pirogue. However, some Until 2001, > 80% of the activity was based on inside lagoon watching, snorkelling operators also began free-diving with food in hand to whereas the rest was more or less equally shared between inside lagoon attract lemon sharks to the surface to allow closer viewing by scuba-diving (without shark-feeding) and outside reef snorkelling and snorkellers. These same free-diving operators were also grabbing fi fi scuba-diving (with shark-feeding) (Fig. 2). In 2001, the Bora-Bora la- some large sharks on the rst dorsal n to be drawn underwater by goon was hit by a dystrophic crisis, due to the heat and the lack of water several metres, to enhance the spectacle. Many freediving tourists – renewal, provoking a massive death of corals and reef-attached fauna. A imitated the guides, taking rides lasting up to 15 20 s (see video 2 major consequence of the phenomenon was a significant decrease (al- from http://dx.doi.org/10.17632/2k46dg6n8t.1). most 50%) of snorkelling inside the lagoon that was replaced by snorkelling outside the reef. In spite of a recovery of the lagoon landscape 3.2. Changes in shark behaviour concomitant to changes in provisioning and fauna, activities outside the reef remained common, in particular near Tapu (Fig. 2). When food was hidden under reef patches, lemon sharks typically In the context of Bora-Bora, ecotourism and shark diving can be approached the feeding spot sluggishly, a few minutes after the arrival divided into three different phases: of divers, swimming slowly near the bottom, without strong directional changes (see video 3 from http://dx.doi.org/10.17632/2k46dg6n8t.1). - Phase 1: early 1990s to 2005–2006. Feeding was based on pieces or It would often take sharks several minutes to locate the food. Once entire dead fish that were hidden by the dive operators under the located, the lemon sharks would swim around for several minutes, fi reef patches (‘patch hiding’), most of the time away from the pre- before one managed to extract the sh pieces from the hiding spot. sence of sharks (at least at the beginning). The scuba-divers were When multiple sharks were present, the shark with the food usually ff then positioned on the bottom several metres from the food antici- swam o , and showed zero interest in the divers (see video 4 from pating the arrival of the sharks before observing them moving http://dx.doi.org/10.17632/2k46dg6n8t.1). Based on video evidence around (Fig. 3A). During this period, snorkellers also used the area, and interviews, lemon sharks appeared shy during this phase, and at a couple of hundred metres from the feeding spot, without im- avoided any interaction with the nearby divers. plementing any feeding. They were able to observe some large Interviewees unanimously agreed that lemon shark behaviour ‘ ’ sharks from the surface even when sharks were swimming on the changed during the second phase of operations, when smelling tech- bottom (see video 1 from http://dx.doi.org/10.17632/2k46dg6n8t. niques were instituted. Within the feeding area, lemon sharks actively swam in the water column, up to several metres from the bottom, instead of remaining close to it. They were also much more inquisitive towards divers, particularly those carrying the smelling source (see video 5 from http://dx.doi.org/10.17632/2k46dg6n8t.1). Following the description provided by Smith, Scarr, and Scarpaci (2010), shark swimming behaviour included ‘milling’– a low level of activity with frequent directional changes within the same area. In stark contrast to shark behaviour during the first phase of operations, lemon sharks were present in the water column at the start of the dive, where they waited Fig. 3. (A) A tourist diver observing a (TL > 2.5 m) lemon sharks, Negaprion for the divers to enter the water and then closely followed them (see acutidens, feeding on a bait that was placed under a reef patch; this practice video 6 from http://dx.doi.org/10.17632/2k46dg6n8t.1). During this does not allow the perception by sharks of a strong link between divers and phase, lemon sharks still maintained a distance from divers. During the food, which would potentially increase the bite risk. (B) A diving operator hand third phase, however, hand feeding (see video 7 from http://dx.doi. feeding a (TL > 2.5 m) lemon sharks, Negaprion acutidens, in front of tourist org/10.17632/2k46dg6n8t.1) coincided with a decrease in the divers; this practice significantly promotes the direct link that sharks can make avoidance distance between lemon sharks and divers according to between food and divers, potentially facilitating involuntary stimuli by divers those interviewed. Besides the numerous and expected physical and accidental bites (Clua & Torrente, 2015). contacts between the feeder and the sharks, contact with non-feeding

278 E.E.G. Clua Tourism Management 68 (2018) 275–283 divers and free divers was frequent. In parallel, the addition of surface that the bitten diver had a watch on his wrist that may have been feeding created a second source of food with operators noting that targeted by the shark. Ten days prior to this incident two dive ‘feeding frenzies1’ occurred potentially as a result of food competition masters from the same dive company cut short a commercial dive at between some large bony fishes such as carangids, lutjanids and the same site because lemon sharks, in particular a male individual, blacktip reef or grey reef sharks (see video 8 from http://dx.doi.org/ were behaving aggressively towards divers. 10.17632/2k46dg6n8t.1). 4. Discussion 3.3. Description of the bites Section 3.2 describes changes in shark behaviour that were wit- Several minor bites, mainly on feeding divers' hands, occurred after nessed by several experienced and reliable professional divers. They 2007 according to interview subjects. These bites, however, were kept coincided with changes in feeding practices but, without any science- as confidential as possible among the professional divers, for fear of based framework, it was impossible to demonstrate a definitive caus- damaging shark-based ecotourism. A minor bite on a feeding diver's ality link between both processes. However, years of research experi- hand is mentioned in the minutes of the BBTAB of the 01 June 2007. ence on shark behaviour, with a particular focus on the lemon sharks of However, the direct interviews with the victim of an accident in 2009, Moorea (Clua et al., 2010), led to the hypotheses and subsequent field- and witnesses of another accident in 2013 provide insights into in- findings presented in this Bora Bora-based study, which potentially cidents at Bora-Bora's Tapu site. In order to capture the accidental confirm that certain shark-feeding methods lead to changes in shark nature of the bites and their direct link to the feeding activity, I provide behaviour and often result in accidental bites. In the following discus- here a detailed description: sion I will define the shark-feeding processes associated with an increase in bite risk, and will then present specific management measures - Accident 1 occurred at the Tapu site on April 2009 and involved a that should be considered to minimise this risk. French dive master from the Bora Diving Centre (BDC). The bite took place during the second morning dive (at around 11:00). The 4.1. Shark senses involved in provisioning processes Tapu site was under a moderate western swell. Two diving groups (each of 5–6 divers) dropped into the water with an underwater Sharks, like other organisms that inhabit complex environments, cameraman, under the supervision of two dive masters, that were should theoretically exhibit behavioural flexibility to enable them to both carrying fish pieces in their BCs (for smelling purposes). The function and survive by adapting to changing conditions and thereby lemon sharks were present in the water column, waiting for the maximise ecological fitness (Dill, 1983). Learning and memory are divers, as usual during this period. Sharks did not appear to be crucial means with which to facilitate such adaptation (Guttridge, showing any particular nervousness. After positioning the tourist Myrberg, Porcher, Sims, & Krause, 2009; Kimber, Sims, Bellamy, & Gill, divers on the bottom at a distance of 4–5 m from the feeding spot, 2014). Sharks are capable of adapting to a novel food source (provi- one of the dive masters and the cameraman went close to a reef sioning) most likely due to a flexible foraging strategy. For such a patch that was usually used for hiding fish. Both divers were face to purpose, they will use the panel of available senses to locate the source face, occupied by filming and hiding the fish, when the dive master of potential food. At great distances from the food (> 100 m), audition who had his back to the open water of the slope, was grabbed on his will play a critical role, in particular the reception of low frequency left calf by an adult lemon shark (∼2.5 m TL) which laterally shook sounds (Nelson, 1966). In the context of artificial provisioning, the the head three times before releasing the leg. The dive master was sounds in the range from 31 to 375 Hz (Corwin, 1981) can be linked to immediately taken to the surface and quickly stabilised. The phy- any anthropogenic source, such as divers jumping into the water or sical consequences were minor, after surgery, because there was even the sounds of a motor-boat (Meyer, Dale, Papastamatiou, Whitney, little tissue loss, and the divemaster was able to walk and dive again & Holland, 2009, Burgess, 1991). Olfaction plays a major role in the with no limitations. attraction of sharks, but in many instances, their rapid appearance - Accident 2 occurred at the Tapu site on February 2013 and involved precludes the possibility that olfactory substances, which are carried at a Canadian tourist diving with the Top Dive Centre. The bite took a relatively slow rate by currents, formed the initial stimulus. Recent place during the first morning dive (ca. 09:00). The Top Dive boat studies shows that sharks require both olfactory and lateral line input was apparently among the first professional boats to visit the spot for efficient and precise tracking of odour-flavoured wakes and that after seven days of strong western swell that prevented diving. Two visual input can improve food-finding performance when lateral line diving groups, each of five divers dropped into the water under the stimuli are not available (Gardiner & Atema, 2007). Olfaction, com- supervision of two dive masters, one of whom had 1-year of ex- plemented by the lateral line, would then take over from audition for perience shark diving in Bora-Bora and the other had no experience. food location at smaller distances (< 100 m). However, among elas- Right after entering the water, the divers were surrounded by mobranch cognitive ability, the visual discrimination to gain food re- blacktip reef sharks and three large lemon sharks, which were de- wards is well known and plays a critical role in the same ranges, when scribed as very inquisitive. The two groups split and one group, water clarity allows it (Clark, 1959; Graeber & Ebbesson, 1972; Wright including the victim and the inexperienced shark divemaster, pro- & Jackson, 1964). The last sense to play a role in the few metres sur- gressed off the bottom on the reef slope, in open water, at around rounding the potential source of food, is the shark capacity in detecting 15–20 m depth. One of the tourist divers had negative buoyancy and weak electro-magnetic fields, in particular those that are produced by instead of adjusting his buoyancy using his BC (by inflating it), was living prey (Kalmijn, 1982). However, in the case of provisioning based adopting a ‘parachute’ posture with arms extended out from the on inanimate flesh, as it is most of the time practiced, this sense is not body and shaking his hands to gain lift. A lemon shark came from supposed to play any particular role at short distances for the food lo- behind and grabbed his hand on the open-water side. The shark cation, opening the ground for the others, in particular vision. immediately released the hand and there was minimal loss of tissue. In the report for the insurance company, one dive master mentioned 4.2. Modified behaviour of fed sicklefin lemon sharks

Provisioning animals can involve ‘habituation’ whereby animals 1 Mono or multi-speciﬁc aggregations of aquatic predators, esp. sharks, which get ex- tolerate a human presence in return for the feeding opportunity. cited by a feeding stimulus, leading to frenetic and agonistic behaviours to access the ﬀ food, with a decreased level of vigilance, biting anything within biting range, including Provisioning uses the animals' attraction to food to o set their aversion other animals or inert materials (Clua et al. 2013). to humans (Knight, 2009). Although the lack of data does not allow to

279 E.E.G. Clua Tourism Management 68 (2018) 275–283 fully demonstrate it, habituation likely occurred at the Tapu site (Bora- sharks, are known to participate in them regularly. As shark density Bora) during the first phase of feeding when food was hidden in the increases around prey or food, competition also increases leading to patch reefs. Based on the testimonies of dive operators from Bora-Bora more active swimming and increased aggressive behaviours (particu- and our observation of a similar process in Moorea, lemon sharks larly from new arrivals) or reduced time to feeding via cyclical social started to increase in numbers and their natural avoidance toward reinforcement (Guttridge et al., 2013). However, this collective beha- humans declined. Food was not placed into the reef in the presence of viour temporarily increases the aggressiveness of participants toward sharks, which should have minimised the link that animals made be- conspecifics, other animals (including humans) or even inert devices tween food and divers. These points likely explain the apparent lack of (such as divers' flippers, boat motors, paddles, etc.) that are close to the major changes in behaviour during the first phase of operations. food source (Clua, Chauvet, Read, Werry, & Lee, 2013; Nelson & Based on studies conducted on white sharks in South Africa Johnson, 1980). Although it did not modify the lemon sharks beha- (Laroche et al., 2007), general conditions are rarely met for sharks to viour, the repetitive triggering at the surface of feeding frenzies invol- develop a learned response, indicating that moderate levels of tourism ving them, would definitely increase the bite risk for humans in close activity may not have a broad impact on shark behaviour across a wide proximity. range of spatial and temporal scales. However, in cases where rewards These are critical factors for the change in shark behaviour from are made readily available and learning can occur, the potential to 2009 and onward, likely contributing to the accidental bites I described. modify behaviours is increased (Guttridge et al. 2009; Orams, 2002). A visual stimulus appears to be important in both cases and may have The introduction of hand-feeding at specific locations of the Tapu site, been facilitated by uncovered skin, both on the leg and the arm, which and of smelling in the adjacent waters modified the behaviour of lemon may have been mistaken for fish flesh as no clear evidence of anything sharks. Hand-feeding probably allowed sharks to make a direct link other than monochromatic vision has been shown for the lemon shark between divers and food, likely facilitating a ‘begging’ process, not only (Van Eyk et al., 2011). In the context of the first accident, the presence toward feeders, but also towards divers in general. ‘Begging’ behaviour of food near the diver that was bitten also likely contributed. For the towards tourists is reported for a wide range of provisioned animals and second accident, the movements of the arm and hand were probably can be a first step that can lead to aggressive and violent behaviour triggers stimulating the bite. As far as it is known, attacks by sharks, toward people (Zhao & Deng, 1992). Furthermore and during the im- unlike barracudas (Wright, 1948), are not facilitated by flashy stimulus. plementation of hand-feeding, the sharks may have easily identified the The hypothesis of any contributing role of the watch the diver was end of the arms (the hands) as a potential source of food, as described wearing on his wrist is then highly improbable. by Clua and Torrente (2015). In addition, feeders often attract the at- tention of the shark by shaking the hand holding the food. Beside the 4.3. Lessons learnt from the Bora-Bora case: human-shark interactive vs association of food with the divers' hands, this specific human beha- non-interactive shark feeding viour then leads the shark to associate the movement of hands with a food reward. Even if smelling was not intended to reward the animals, There is a high probability that the risk of bites by lemon sharks has the way of practicing it in open water may have been a contributing increased off Bora Bora because of the changes in feeding practices factor to the development of a modified behaviour for lemon shark, through time. Bora-Bora is interesting as a case study because it shows, contributing to a higher risk of accidental bites on humans. The ago- over two decades, a range of situations of shark-feeding that started nistic behaviour of fishes may indeed be linked to the spatial context with practices that put the animals in situations close to natural pro- (Bolyard & Rowland, 1996). As a neritic fish which usually swims close cesses, and currently involves practices where human interaction is at to the bottom (see video 1 from http://dx.doi.org/10.17632/ the core of the experience. Based on a review of usual practices of 2k46dg6n8t.1), one could speculate that a lemon shark would likely feeding, this level of interaction between sharks and humans can feel less secure in the water column and would be more inclined to therefore be assessed in order to determine the level of associated risk instinctive and aggressive behaviours (Fig. 4) in this environment. (see Table 1 as a framework for risk analysis). Studies investigating this aspect of lemon shark behaviour are required Because of the limited number of incidents it is difficult to pin bites for further clarify this point. on specific causes, but from a management perspective it appears that The introduction and then intensification of surface feeding allowed there are ways of managing the risk. In case of detection of a risk such me to distinguish a third phase of operations. This practice may have as in the Bora-Bora situation, the managing body may consider different played a critical role in two ways. It first enhanced the attraction of options: lemon sharks towards the water column, leading them up to the surface to feed with the behavioural consequences that are mentioned above. - option 1: continue as currently practiced; the potential consequence Secondly, it potentially increased the aggressiveness of lemon shark would be to witness incidents as animals have habituated to the feeding through frequent ‘feeding frenzies’ that characterise this prac- situation; tice. ‘Feeding frenzies’ are natural events, and many animals like lemon - option 2: scale back to phase 1 practices at the current site; this comes with the risk of sharks looking for food from divers because of the past recent interactions; - option 3: implement a waiting period, hoping that sharks forget close encounters and resume at phase 1; - option 4: start phase 1 type activities but at a different site where sharks would not be present when food is hidden; that is only possible if a suitable spot exists, probably quite far from the current site to prevent interactions; - option 5: total ban of feeding; that would have heavy economic consequences.

However, in situations such as in Bora-Bora where the risk induced by the shark behaviour has reached concerning levels, options 1 and 2 should not be considered. The presence of a single passage (that boats Fig. 4. Chronological evolution of the bite risk in Tapu site, based on the heading to the outer slope must take) and the relatively small size of the chronological introduction and development of unsuitable feeding practices. island (allowing spatial connections with the existing feeding site),

280 ...Clua E.E.G.

Table 1 Description of driving factors for an assessment of the level of interactions between humans and sharks in the context of artificial provisioning, allowing an assessment of the level of increasing associated risk. From the top to the bottom, the learning criteria are developing along the association of food and the contacts with divers. A set of procedures may mix different factors (from columns 2, 3 and 4) belonging to different levels of interaction: the global level of interaction will then be a combination of all the factors. However, the global level in this case will remain the one of the highest level of interaction, even if the number of corresponding criteria is numerically inferior. NB: As described in Clua et al. (2010) the mating period of a given shark species would globally increase the level of risk, whatever the other parameters of the assessment.

Type of feeding Level of Criteria Time and location of the feeding Presentation of the food/Divers' behaviour Quantityf of food Bite risk level interaction

Non-interactive Nil Sharks hardly associate the presence Feeding spots are vary within a large The food is set down before the arrival of divers (no Low quantity (with no capacity of Low of food with the presence of divers given areaa temporal convergence) meeting the sharks' daily requirements) Feeding times vary among sessions The food is hidden from the sharks between the surface and the bottom (opaque container - no visual stimulus) The food is hermetically transported (sealed container - no olfactory stimulus) Feeding ceases for at least two days per The food is hidden in the substrate (natural situation) week and two months per yearb No physical contact between divers and sharks at any time Interactive Low/Medium Sharks associate the presence of food Feeding spots are globally the same Divers and food temporally coincide Medium quantity (aproaching the daily Medium with the presence of divers among sessions requirements of some animals) Feeding times vary among sessions Sharks can identify the food from the surface (through vision and/or smell) The food is contained in a cage (no access for sharks) Feeding occurs almost every day A diver is in contact with food at a certain stage and releases the food on the seabed (not directly by hand to 281 sharks) Feeding ceases during a given period of Few, short, physical contacts with sharks occur (< 3s) the year (min. one month) High Sharks may associate the body of the Feeding spots are strictly the same Divers and food temporally coincide and additional High quantity in scattered areas High divers with food among sessions stimulic allow shark to anticipate the encounter Sharks can easily identify the food from the surface (through vision and smell) Feeding times are strictly the same The food is not hermetically enclosed (pieces are released among sessions and shark can access the food) A diver keeps the food and directly gives it by handd Feeding is maintained all year long Physical contacts with sharks are frequent and longer (> 3–10s) Very high Sharks associate divers with food Same features as above plus surface The provisioning practice creates 'feeding frenzies'e High quantity (including largeg pieces) in Very high and beg feeding Physical contacts with sharks are frequent and very long a conﬁned area (> 10s)

a Feeding spots need to be far enough from each other to avoid aggregating the same animals.

b In particular during the mating season which adds sexual competition to the access to food (see Clua et al. 2010). Tourism Management68(2018)275–283 c Such as specific noises created by divers to advertise their presence. d See Clua and Torrente (2015) about the increase of bite risk linked to hand-feeding. However, if operated under strict, repetitive and fully controlled procedures, this technic can indeed be implemented with an acceptable level of risk (M. Newmann, Pers. Comm.). e See definition in Clua et al. (2013). In addition to the number of animals, which plays a facilitating role, the quantity and size of the food offered would play a critical role. f Based on either the quantity given by one operator or the sum of the food given by all operators working in a confined area. g A piece of food can be considered as 'large' when a shark of a given size is unable to directly ingest it, allowing other sharks to try to steal it. E.E.G. Clua Tourism Management 68 (2018) 275–283 make finding an appropriate alternative spot unlikely (option 4) could sensitiveness and economical weight of the issue, the name of the be found. A complete interruption of the feeding activity (option 3) people from Bora-Bora involved in the interviews will not be provided. I should then be implemented. A recent empirical study conducted by however warmly thank them for their involvement in the study, in Kimber et al. (2014) proved that a reinforcement of the operant fora- particular those from the Bora-Bora Tourism Activities Board. My warm ging response to an electric stimulus by rewarding with food clearly thanks also go to Dr Michael Heithaus (International University of altered the behaviour of catsharks Scyliorhinus canicula. The fact that Florida), Jeanine Almany (CRIOBE) and Dr Clive Wilkinson (Australian none of the learned and habituated behaviours were continued after a Reef and Rainforest Research Centre) and the two anonymous re- 3-week interval, and that behaviour levels were independent of whe- viewers for their valuable comments and improvements on the draft ther rewards were offered before or after the interval suggests that the version of this paper. Finally, I would like to aknowledge the Institut de memory window for these elasmobranchs is less than three weeks. la Statistique en Polynésie française (ISPF) that provided me with data However cognitive abilities are also likely to vary among elasmobranch for the purpose of my study. species. For example, inter-specificdifferences in visual learning have previously been observed between lemon and nurse (Clark, 1959) and Appendix A. Supplementary data lemon and bull sharks (Wright & Jackson, 1964). These findings prove that an interruption, at least of several weeks if not months, would Supplementary data related to this article can be found at http://dx. allow feeding activities to start again with an adequate control and doi.org/10.1016/j.tourman.2018.03.022. management. Following some authors' suggestions, another choice would be to ban the feeding activities as it was implemented in several References countries (see Introduction). To achieve this, humans would need to behave in such a way as to restore wildlife aversion to humans (what Adjeroud, M., Chancerelle, Y., Schrimm, M., Perez, T., Lecchini, D., Galzin, R., et al. one might call ‘reverse habituation’) and withdraw human food hand- (2005). Detecting the effects of natural disturbances on coral assemblages in French Polynesia: A decade survey at multiple scales. Aquatic Living Resources, 18, 111–123. outs while regenerating erstwhile feeding grounds in order to restore a Bolyard, K. J., & Rowland, W. J. (1996). Context-dependent response to red coloration in (mobility-based) foraging way of life (‘reverse provisioning’)(Knight, stickleback. Animal Behaviour, 52(5), 923–927. 2009). The choice of banning or maintaining feeding remains in the Bookbinder, M. P., Dinerstein, E., Rijal, A., Cauley, H., & Rajouria, A. (1998). Ecotourism's support of biodiversity conservation. Conservation Biology, 12, hands of political bodies. I nevertheless strongly believe that this study 1399–1404. can contribute to finding a compromise based on maintaining feeding Brena, P. F., Mourier, J., Planes, S., & Clua, E. (2015). Shark and ray provisioning: through a constraining legislation that relies on the avoidance of det- Functional insights into behavioral, ecological and physiological responses across – rimental provisioning practices that increase the accidental bite risk. multiple scales. Marine Ecology Progress Series, 538, 273 283. Bruce, B. D., & Bradford, R. W. (2013). The effects of shark cage-diving operations on the A more coordinated international regime for shark-based eco- behaviour and movements of white sharks, Carcharodon carcharias, at the Neptune tourism is needed to ensure the conservation of these iconic species Islands, South Australia. Marine Biology, 160(4), 889–907. Buray, N., Mourier, J., Planes, S., & Clua, E. (2009). Underwater photo-identification of (Techera & Klein, 2013), and there is a critical need for ensuring that fi fi fi sickle n lemon sharks, Negaprion acutidens, at Moorea (French Polynesia). Cybium, scienti c ndings are used in improving legal frameworks, rather than 33,21–27. anthropogenic reasons which are not scientifically demonstrated Burgess, G. H. (1991). Shark attack and the international shark attack file. In S. H. Gruber – (Dobson, 2007, pp. 49–65; Richards et al., 2015). I hope the technical (Ed.). Discovering sharks. American littoral society (pp. 101 105). New Jersey: Highlands. guidelines that I provide for better managing the underwater provi- Catlin, J., Hughes, M., Jones, T., Jones, R., & Campbell, R. (2013). Valuing individual sioning of sharks will contribute to such a need and outcome. There are animals through tourism: Science or speculation? Biological Conservation, 157,93–98. successful examples of such a process with the white shark cage diving CBS (2001). Feeding on the shark attack. CBSnews August, 10. Cisneros-Montemayor, A. M., Barnes-Mauthe, M., Al-Abdulrazzak, D., Navarro-Holm, E., industry around Neptune Island (South Australia). Following a sig- & Sumaila, U. R. (2013). Global economic value of shark ecotourism: Implications for nificant rise in cage diving effort in 2007, the local government laun- conservation. Oryx, 47(03), 381–388. ched a long consultative process with industry and other marine sectors Clark, E. (1959). Instrumental conditioning of lemon sharks. Science, 130, 217–218. 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Dr Eric CLUA is DVM, with a MsC in Environmental Maillaud, C., & Van Grevelynghe, G. (2005). Shark attacks and bites in French Polynesia. Economics and a PhD in Marine Biology. After a primary Journal Européen des Urgences, 18,37–41. focus on tropical fish ecology, he got specialized from 2005 Meyer, C. G., Dale, J. J., Papastamatiou, Y. P., Whitney, N. M., & Holland, K. N. (2009). in shark ecology and behaviour, with a special focus on Seasonal cycles and long-term trends in abundance and species composition of sharks attacks on humans (with several publications on the subject associated with cage diving ecotourism activities in Hawaii. Environmental in peer-reviewed forensic journals). He also published sev- Conservation, 36,1–18. eral papers on the effects of artificial provisioning on shark Nelson, D. R. (1966). Hearing and acoustic orientation in the lemon shark, Negaprion behaviour as well as papers on the economics of shark brevirostris (Poey), and other large sharks. Dissertation Abstracts, 27(1), 333B. feeding, contributing to the assessment of the non-con- Nelson, D. R., & Johnson, R. H. (1980). Behaviour of the reef sharks of Rangiroa, French sumptive direct use value of sharks. One of his present Polynesia. National Geographic research reports, 479–499. objectives is about developing ‘payment for ecosystem Newsome, D., & Rodger, K. (2008). To feed or not to feed: A contentious issue in wildlife services’ in the context of shark-based ecotourism. He also tourism. In D. Lunney, A. Munn, & W. Meikle (Eds.). Too close for comfort : Contentious implements an eco-anthropologic approach of shark per- issues in human-wildlife encounters (pp. 255–270). Mosman, Australia: Royal ception for improving shark conservation. Zoological Society of New South Wales. Orams, M. B. (2002). Feeding wildlife as a tourism attraction, a review of issues and

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