Article

# Hand feeding can periodically fuel a major portion of bull shark energy requirements at a provisioning site in Fiji

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## Abstract

Wildlife tourism is often extolled for its contribution to conservation. However, understanding the effects of tourism activities on the health of target animals is required to fully assess conservation benefits. Shark tourism operators often use food rewards to attract sharks in close proximity to tourists, but nothing is known about the contribution of these food rewards to the energetic requirements of target species. In this study, hand-feeding of bull sharks Carcharhinus leucas was directly observed on 36 commercial shark watching dives in the Shark Reef Marine Reserve (SRMR), Fiji. Mean number of tuna heads consumed per dive by focal individuals ranged from 1.3 to 3.7. Monitored bull sharks consumed an average of ~ 0.74 heads per provisioning day, and bioenergetics modelling suggests that some sharks might periodically be meeting their full energy requirement from provisioning at the SRMR. Knowing how much individual sharks consume at provisioning sites and how this relates to their energy requirements is crucial in order to better understand the effects of wildlife tourism and its contribution to conservation.

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... Given that tuna heads provided can fuel the energetic needs of bull sharks , we expect that tuna will make up a significant component of the diet of at least some bull sharks individuals. Note however that the study from Brunnschweiler et al. (2017) was conducted in 2008, and that the number of sharks attending the dive site in 2008 was lower than in 2015, when the present study was done (see Fig. 1). This means that in 2008 bait was shared among a smaller number of bull shark individuals and therefore that bait contribution could have been higher than in 2015, the year the present study was conducted. ...
... These regular movements out of the study area, coupled with the relative slow muscle turnover rate of large sharks (Logan and Lutcavage, 2010;MacNeil et al., 2006) can limit our ability to quantify a possible incorporation of bait based on stable isotope analysis. Therefore, the importance of bait for whitetip reef sharks, a resident shark species that is also an important focus of the shark dive at the Monthly mean ( ± SD) number of bull sharks sighted per dive for 2008 (when feeding rate data used in Brunnschweiler et al. (2017) was collected) and 2015 (when stable isotope data from the present study was collected). ...
... The lack of bait incorporation was somewhat surprising, particularly given the frequency of shark feeds (5 days/week, with 2 dives/ day) and bull shark encounter and feeding rates at the Shark Reef Marine Reserve (Brunnschweiler and Barnett, 2013;Brunnschweiler et al., 2017). Indeed, Brunnschweiler et al. (2017) estimated that one tuna head could meet the energy requirements of a 200 kg (corresponding to~2.8 m (Branstetter and Stiles, 1987)) bull shark for 3.1 days (2.3 heads/week). ...
Article
Wildlife tourism is a growing industry, with significant conservation and socio-economic benefits. Concerns have however been raised about the possible impacts of this industry on the long-term behaviour, health and fitness of the animal species tourists come to see (the target species), particularly when those species are regularly fed to improve the tourism experience. Information on the contribution of food rewards to the diet of the target species at feeding sites is critical to assess the dependency on handouts and to identify possible health/fitness problems that might be associated, if handouts become the main part of animals' diets. Here, we use stable isotopes (δ¹³C and δ¹⁵N) to evaluate the importance of handouts for a marine predator, the bull shark (Carcharhinus leucas), at a feeding site (Fiji) where shark feeds occur 5 days/week and sharks (up to 75 individuals/dive) are fed ~200 kg of tuna heads/day. There was no evidence of incorporation of food provided, even for individuals that regularly consume food rewards. Results, when combined with those from previous studies on bull shark movements and feeding rates at our study site, show that current levels of provisioning likely have no long-term impacts on bull shark diet or behaviour. This study also demonstrates the applicability of stable isotope analysis to assess and monitor the contribution of food rewards to wildlife, and highlights the benefits of using multi-sources of information to gain a holistic understanding of the effects of provisioning predators.
... In some ways, commercial shark feeding mimics natural exploitation of hyperabundant resources [15] as pelagic fish (tuna heads) are fed to the sharks, thus providing a human-facilitated trophic linkage between pelagic and near-shore systems. In fact, while a recent isotopic study suggested that trophic supplementation to bull sharks (Carcharhinus leucas) from tuna heads represented only a minor component of their diet [16], a bioenergetics model suggested that at least some sharks could meet or exceed their daily dietary requirements solely from provisioned food [17]. Thus at least on local time scales, tourism-based provisioning can provide an important role in the population ecology of reef apex predators. ...
... Our work represents an important first step in understanding how the ecology of coral reefs is impacted by tourism. Stable isotope studies have suggested that food provisioning at Beqa shark dive sites could meet daily nutritional diets for some bull sharks [17] Whether the tuna subsidy to smaller, opportunistically feeding species is energetically significant for other species remains an open question. ...
Article
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Tourism represents an important opportunity to provide sustainable funding for many ecosystems, including marine systems. Tourism that is reliant on aggregating predator species in a specific area using food provisioning raises questions about the long-term ecological impacts to the ecosystem at large? Here, using opportunistically collected video footage, we document that 61 different species of fish across 16 families are consuming tuna flesh at two separate shark dive tourism operations in the Republic of Fiji. Of these fish, we have resolved 55 to species level. Notably, 35 (63%) of the identified species we observed consuming tuna flesh were from ostensibly non-piscivorous fishes, including four Acanthuridae species, a group primarily recognized as browsers or grazers of algae and epibenthic detritus. Our results indicate that shark diving is having a direct impact on species other than sharks and that many species are facultatively expanding their trophic niches to accommodate the hyperabundance of resources provided by ecotourism.
... There is growing evidence to show that sharks are able to rapidly learn to take advantage of new food sources (Heinrich et al., 2021) and associate the presence of fishing vessels with the availability of hooked fish to feed on (Mitchell et al., 2020). This may lead to changes in the movement patterns and residency of sharks, where they increase the time spent in locations where fishing is occurring regularly, as reported at Lord Howe Island and is analogous to provisioning effects seen elsewhere, for example bull sharks fed for ecotourism in Fiji (Brunnschweiler and Baensch, 2011;Brunnschweiler et al., 2018). However, further research is needed to generate a greater understanding of how depredation may be influencing behaviour and movement patterns of different species of sharks that are responsible for depredation. ...
... It is currently unknown whether this provision of food would be frequent enough to benefit sharks at a population level, in terms of increased potential for breeding and survival of offspring. The beneficial effect of feeding on hooked and released fish is likely to be fairly localised although previous research has shown that where bull sharks were hand-fed regularly over many years for ecotourism activities, this provisioning can provide a major proportion of their energy needs, although only over short timescales (days) and the effect was highly variable between individual sharks (Brunnschweiler et al., 2018). ...
... pinnipeds). Whether the infrequent consumption of these baits provide sufficient energy to compensate for the increased energy expenditure associated with sharks interacting with the operators would depend on the calorific value of these baits and the frequency of white sharks successfully feeding on the baits, both of which are currently unknown (Brunnschweiler et al., 2017). Spending time interacting with cage-diving operators might also distract sharks from normal behaviours such as foraging on natural, energy-rich prey like pinnipeds. ...
... Future research should quantify the amount of time white sharks interact with cage-diving operators and estimate its effect on white sharks in relation to their daily energy budget. Estimation and comparison of the energy obtained from natural prey vs. bait would also facilitate a better understanding of the effect of the cagediving industry on the energy budget of white sharks (Brunnschweiler et al., 2017). Such information will enable managers to go beyond the use of presence/absence of cagediving vessels and sharks and account for the potential effect of wildlife tourism on the energy balance, fitness and ultimately population viability of this internationally threatened species. ...
Article
Full-text available
Anthropogenic activities are dramatically changing marine ecosystems. Wildlife tourism is one of the fastest growing sectors of the tourism industry and has the potential to modify the natural environment and behaviour of the species it targets. Here, we used a novel method to assess the effects of wildlife tourism on the activity of white sharks (Carcharodon carcharias). High frequency three-axis acceleration loggers were deployed on ten white sharks for a total of ~9 days. A combination of multivariate and univariate analysis revealed that the increased number of strong accelerations and vertical movements when sharks are interacting with cage-diving operators result in an overall dynamic body acceleration (ODBA) ~61% higher compared with other times when sharks are present in the area where cage-diving occurs. Since ODBA is considered a proxy of metabolic rate, interacting with cage-divers is probably more costly than are normal behaviours of white sharks at the Neptune Islands. However, the overall impact of cage-diving might be small if interactions with individual sharks are infrequent. This study suggests wildlife tourism changes the instantaneous activity levels of white sharks, and calls for an understanding of the frequency of shark-tourism interactions to appreciate the net impact of ecotourism on this species’ fitness.
... It is a global industry (Gallagher et al. 2015). Examples are the whale shark (Rhincodon typus) at Tofo Beach, Mozambique (Haskell et al. 2015), hand feeding (Carcharhinus leucas) in the Shark Reef Marine Reserve, Fiji (Brunnschweiler et al. 2018), tiger sharks (Galeocerdo cuvier) in the Aliwal Shoal Marine Protected Area, South Africa (Du Preez et al. 2012), and the white shark (Carcharodon carcharias) cage-diving in South Australia's Spencer Gulf important industry (Nazimi et al. 2018). ...
... Wildlife tourism may have the potential to contribute to conservation (Goodwin 1996;Börger et al. 2014;Saayman and Saayman 2017;Brunnschweiler et al. 2018). It is said to enhance environmental education, while providing local economic benefits (Grafeld et al. 2016;Nazimi et al. 2018). ...
Article
In the last few winters, shark communities have been aggregating near the Israeli Mediterranean coast, at a specific point, near the Hadera power station. This unusual phenomenon has fascinated residents, visitors, kayakers, divers, and swimmers. We analyze the effects of this intense human interest on the sharks, using contingent behavior, in Hadera and in Ashkelon, where sharks are present and there is available infrastructure for their observation. We also report on changes in shark behaviour due to changes in tourism intensity. We find a change of about ILS 4.1 million annually for both sites but a larger individual consumer surplus in Hadera, where sharks are currently observable. Touristic intensity crosses the threshold level by about 12% and making the socio-equilibrium sustainable for both humans and sharks would have a social cost of ILS 0.157 million. This paper, which is based on the assessment of conservation values to marine and coastal tourists, raises a need for spatial planning in order to protect this endangered species.
... Recent studies on elasmobranchs have shown that wildlife tourism can have a wide range of effects on focal and nonfocal species, including changes in seasonality, residency, abundance (Clarke, Lea, & Ormond, 2011;Meyer, Dale, Papastamatiou, Whitney, & Holland, 2009), space use (Bruce & Bradford, 2013;Brunnschweiler & Barnett, 2013;Fitzpatrick, Abrantes, Seymour, & Barnett, 2011;Huveneers et al., 2013), activity (Corcoran et al., 2013;Huveneers, Watanabe, Payne, & Semmens, 2018) and diet (Brunnschweiler, Payne, & Barnett, 2018;Meyer, Whitmarsh, Nichols, Revill, & Huveneers, 2020). Such effects are often accentuated by feeding the focal species to ensure reliable and close encounters (Brena, Mourier, Planes, & Clua, 2015;Gallagher et al., 2015). ...
... Barnett et al., 2016;Huveneers et al., 2018). This information is, however, crucial to understand the effects of wildlife tourism (Brown, Gillooly, Allen, Savage, & West, 2004;Brunnschweiler et al., 2018;Gallagher & Huveneers, 2018;Wilson et al., 2006). A study on whitetip reef sharks, Triaenodon obesus, at Osprey Reef (Great Barrier Reef, Australia) demonstrated that sharks subjected to regular feeding events showed elevated activity levels during the day when they would normally rest, resulting in a ca. ...
Article
Tourism-related feeding of wildlife can result in detrimental, human-induced changes to the spatial distribution, social behaviour and health of target species. The feeding of sharks as part of shark-viewing activities has become increasingly popular in recent years to ensure reliable and consistent encounters. A common limitation in determining how feeding affects individuals or populations is the lack of baseline data prior to the establishment of a feeding site. Here, we documented the residency, spatial distribution, activity patterns and daily metabolic rates of juvenile lemon sharks, Negaprion brevirostris, prior to initiating daily feeding for 27 days to assess the effect of short-term feeding. We implanted acoustic transmitters equipped with accelerometers to record movement and activity in six lemon sharks. Sharks progressively anticipated the feeding events during the 27 days of daily feeding, as shown by a change in activity and increased time spent near the feeding site 1 h prior to feeding events. Shark behaviour did not fully return to baseline levels within the documented 90 days of postfeeding recovery. However, neither spatial distribution outside the refuge nor mean daily activity was affected by feeding. Sharks decreased their metabolic rates over the course of the study, but this was probably due to falling water temperature rather than the effect of feeding. Overall, our study shows that anticipatory behaviour in juvenile lemon sharks can occur within 11 days of daily feeding events, but behavioural changes seem confined to fine-scale movement patterns and may not affect these sharks' daily energy needs. The ability to assess the effects of daily feeding at a site where tourism has not been occurring previously provides new information for operators and managers of wildlife tourism to account for and minimize potentially detrimental effects on the target species.
... It is a global industry (Gallagher et al. 2015). Examples are the whale shark (Rhincodon typus) at Tofo Beach, Mozambique (Haskell et al. 2015), hand feeding (Carcharhinus leucas) in the Shark Reef Marine Reserve, Fiji (Brunnschweiler et al. 2018), tiger sharks (Galeocerdo cuvier) in the Aliwal Shoal Marine Protected Area, South Africa (Du Preez et al. 2012), and the white shark (Carcharodon carcharias) cage-diving in South Australia's Spencer Gulf important industry (Nazimi et al. 2018). ...
... Wildlife tourism may have the potential to contribute to conservation (Goodwin 1996;Börger et al. 2014;Saayman and Saayman 2017;Brunnschweiler et al. 2018). It is said to enhance environmental education, while providing local economic benefits (Grafeld et al. 2016;Nazimi et al. 2018). ...
Article
In the last few winters, shark communities have been aggregating near the Israeli Mediterranean coast, at a specific point, near Hadera power station. This unusual phenomenon has fascinated residents, visitors, kayakers, divers, and swimmers. We analyse the effects of this intense human interest on the sharks, using contingent behaviour, in Hadera and in Ashkelon, where sharks are present and there is available infrastructure for their observation. We also report on changes in shark behaviour due to change in tourism intensity. We find a change of about ILS 4.1 million annually for both sites but a larger individual consumer surplus in Hadera, where sharks are currently observable. Touristic intensity crosses the threshold level by about 12% and making the socio-equilibrium sustainable for both humans and sharks would have a social cost of ILS 0.157 million. This paper, which is based on the assessment of conservation values to marine and coastal tourists, raises a need for spatial planning in order to protect this endangered species.
... When poorly managed, the potential economic and social benefits of elasmobranch tourism can be overshadowed by ecological consequences [10,[44][45][46]. To date research on the topic has mainly focused on identifying tourism driven changes in elasmobranch behaviour (e.g. ...
... Tourism activities at Grand Cayman Island are very intensive and have resulted in a number of long-term negative behavioural and physiological effects on the stingray species, Hypanus americanus [48,51]. In contrast, the strict self-imposed management actions and limited number of shark feeding operators at Shark Reef in Fiji, has resulted in minimal long-term effects on bull shark (Carcharhinus leucas) behaviour and diet, and is likely to have had no effects on health and fitness [45,52,53]. ...
Article
Elasmobranch tourism is a rapidly expanding global industry. While this industry can provide community and conservation benefits, it presents risks to target species, environments and humans when inappropriately managed. To ensure appropriate management is implemented, there is a need to identify the prevalence of elasmobranch tourism globally, the types of operations occurring and the controls used to mitigate risk. This study undertook a global literature review to develop an industry activity typology and establish the types of management controls present across elasmobranch tourism operations. In total, 151 unique species-activity-location conditions were identified, with four broad activity types categorised: diving, snorkelling, provisioning and cage diving. Spanning 42 countries and 49 different species, 32% of conditions identified lacked evidence of management. Further to this, many of the prevailing management controls in place (e.g. MPAs, shark sanctuaries, protected species status), were secondary in nature, having not been designed or implemented to manage elasmobranch tourism explicitly. Therefore, avoidable risks are likely widespread throughout the industry. Encouragingly, the application of activity specific management controls is likely to be effective at reducing risks across activity types. The theoretical case studies and management tools investigated herein provide operators and industry managers with guidance on how to reduce risk and safeguard industry benefits. With the elasmobranch tourism industry likely to continue expanding, it is important that appropriate management and regulatory frameworks are in place so that marine wildlife tourism can continue in a beneficial and sustainable manner.
... densities providing some of the foundational characterizations of such (Albo-Puigserver et al., 2017;Brunnschweiler et al., 2018;Hartman and Brandt, 1995). Thus, bomb calorimetry could be thought of as a starting point in conservation-based studies when dietary inputs for bioenergetic models are unknown (Glover et al., 2010;Johnson et al., 2017), especially as energy contents can vary between species, sex, age, and seasonality (Albo-Puigserver et al., 2017;Vollenweider et al., 2011;Wuenschel et al., 2006), which could have implications for model input estimates. ...
Chapter
Energy is a fundamental currency of life that can be quantified in organisms to understand how environmental conditions and anthropogenic stressors affect individuals, scaling up to populations and entire ecosystems. Bioenergetics studies have been conducted extensively on fishes, with an historical focus on lab-based experiments relevant to fisheries and aquaculture; however, recent methodological and technological advances are enabling more widespread applications in ecology and conservation including in situ measurement of various aspects of fish bioenergetics in aquatic ecosystems. Much of the utility of bioenergetics is based on a generalized mass-balance equation that describes energy allocation, and there are numerous advanced modeling techniques available to quantify how various environmental and intrinsic biological factors influence fish energetics, as well as relevant endpoints such as growth and reproduction. In this chapter, we discuss (1) key components of fish bioenergetics, (2) available measurement techniques, (3) common modeling techniques, and (4) case studies that highlight some key applications to date. We conclude by discussing current limitations and future research directions in this field. Bioenergetics is an increasingly powerful approach to build mechanistic connections between environmental conditions, stressors, and fish populations that is especially valuable for predicting the responses of fishes to rapidly changing conditions in the Anthropocene.
... operators to overcome the initial skepticism and resulted in a fruitful collaboration. We believe that deployments of clamps and harnesses would provide interesting insights to participate to the current debate on shark tourism, as the effects of attraction and/or provisioning on animal behaviour remain largely lacking (Brunnschweiler et al. 2017;Gallagher et al. 2015). ...
Article
Full-text available
Biologging technology has provided scientists with unprecedented tools to investigate the ecology and behaviour of marine animals, but tag deployment and attachment methods have lagged behind. Electronic tagging of elasmobranchs still essentially involves implanting anchors or drilling the fins of restrained animals. Here, we present two new non-invasive methods for deploying satellite and biologging tags on pelagic sharks and rays that do not require restraining or manipulation of the animals, nor the attachment of intramuscular anchors. The attachment of a modified fin clamp and a harness systems were tested on 12 blue sharks and four devil rays in the Azores, mid-north Atlantic. Clamps and harnesses were fitted with galvanic timed releases and deployed manually by a free diver or from the boat using a harness tagging pole. The tags remained on the animals over the entire short-term duration of the trials. Focal observations and deployment data suggest that both methods produce little or no adverse behavioural reaction on the animals, offering a valid alternative for short-term tagging of pelagic sharks and rays. Deployment length can be substantially increased by selecting longer duration galvanic timed releases.
... For example, Clua et al. (2010) observed a reduction in mobility, increased residency and greater levels of aggression in N. acutidens over a long-term (44 month) study, as a result of feeding by divers. Likewise, Clarke et al. (2011) recorded C. falciformis spending more time close to a reef site where feeding occurred regularly, and research has shown that provisioning can temporarily provide a substantial portion of the energy requirement of C. leucas in Fiji (Brunnschweiler et al. 2018), as well as leading to a change in their relative abundance and movement patterns (Brunnschweiler and Baensch 2011;Brunnschweiler and Barnett 2013). The use of accelerometers has identified substantial changes in the activity patterns and vertical movements of individual C. carcharias in the vicinity of cage-diving operations in South Australia (Huveneers et al. 2018). ...
Article
Full-text available
Shark depredation, where a shark partially or completely consumes an animal caught by fishing gear before it can be retrieved to the fishing vessel, occurs in commercial and recreational fisheries worldwide, causing a range of negative biological and economic impacts. Despite this, it remains relatively understudied compared to other fisheries issues. This is the first review of the literature relating to shark depredation, which also includes an overview of the potential mechanisms underlying its occurrence and options for mitigation. Furthermore, this review highlights key research gaps that remain to be investigated, thereby providing impetus for future research. In total, 61 studies have been published between 1955 and 2018, which include information on shark depredation. These studies recorded quantitative rates of depredation between 0.9 and 26% in commercial and recreational fisheries and during research fishing, identified 27 shark species from seven families that were responsible for depredation and discussed potential factors influencing its occurrence. Information from research into bycatch mitigation and the testing of shark deterrent approaches and technologies is also presented, in the context of applying these approaches to the reduction of shark depredation. This review presents an holistic overview of shark depredation in fisheries globally and, in doing so, provides a central resource for fisheries researchers and managers focusing on this topic to stimulate further collaborative research on this important fisheries issue.
... Whereas the value and benefits of the industry have been largely recognized and will continue to add information from regional studies, the overall impacts on shark behavior remain largely equivocal and an area of interest, with some studies showing impacts on physiology and behavior [20,4,10], whereas others do not [6,19,1]. Nevertheless, one can always expect some degree of impact from tourism practices involving wild animals [26], and as the public interest in sharks and shark-diving continue to grow, the adaptive management of emerging issues will become increasingly important for the overall sustainability and vitality of the industry, as well as the perceptions of sharks more broadly. ...
... Negative effects resulting from tourist activities have been observed in other marine protected species, such as marine birds and cetaceans, where interruptions in foraging and breeding have been linked to a higher use of energy (Green & Giese, 2004). Nevertheless, intentional and supplementary feeding would not necessarily affect the energy balance or feeding ecology in elasmobranchs, as it has been observed in bull sharks (Carcharhinus leucas) during the ecotourism in Fiji (Abrantes, Brunnschweiler, & Barnett, 2018;Brunnschweiler, Payne, & Barnett, 2018). However, the energy expenditure due to a lack of food reward is beyond the scope of this study and should be assessed in future research regarding baits and white shark physiology during ecotourist activities. ...
Article
1. Cage diving is the most important activity for the sustainable use of white sharks (Carcharodon carcharias). However, information related to their behaviour during ecotourism is scarce. 2. This study provides useful information for monitoring C. carcharias during cage‐ diving activities around Guadalupe Island, Mexico. Surface behaviour of 106 white sharks was recorded for 87 days on‐board six cage‐diving boats in 2012, 2013, and 2014. 3. Of the observed sharks, 63% were immature specimens (n = 67) and 37% were considered mature (n = 39). Seventy‐one per cent were males (n = 75) and 29% were females (n = 31). 4. Interactions were classified into one of the 11 behaviours: parading, close inspection, horizontal attack, vertical attack, bait catching, feeding, not feeding, buoy catching, encounter, escape, and staying. 5. Parading, close inspections, and horizontal attacks were performed more often by mature males, whereas immature females performed more vertical attacks, with no differences between mature and immature males. 6. A total of 1,542 ethograms were registered. Each ethogram consisted on average of 6.3 ± 5.6 behaviours with a significant transitional pattern from horizontal attacks to parading and close inspections, and from vertical and horizontal attacks to bait being caught. 7. A pattern related to feeding in a simple stimulus response reflex was observed. The shark's length seems to play an important role in the efficiency of the attacks, presumably resulting from the experience of mature individuals. Intentional feeding should be avoided to prevent negative effects related to ecotourism. 8. This study constitutes a baseline for future research on white shark behaviour. It can be applied in other regions regardless of environmental conditions, quantity and size of the boats, and types of bait. Using this standard method could improve the monitoring, management, and conservation of this vulnerable species.
... Large meals, such as those that might occur for bold sharks that consistently feed or sharks that gorge during competitive interactions, may reduce aerobic capacity by reducing the available AS for other oxygen-demanding processes (Norin and Clark 2017). Indeed, single provisioning events can satiate sharks for days (Brunnschweiler et al. 2018). Given concerns that human-wildlife encounters can have consequences for the health of sharks and rays (Semeniuk et al. 2010), _ MO 2 can be applied to quantify stress, especially in the context of bioenergetics, that is associated with ecotourism. ...
Article
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Elasmobranch populations face worldwide declines owing to anthropogenic stressors, with lethal and sub-lethal consequences. Oxygen uptake rates ($$\dot{M}$$O2, typically measured in mg O2 kg⁻¹ h⁻¹) can be quantified as proxies of whole-organism aerobic metabolic rates and are relevant to fisheries management and conservation through aerobic performance’s relationship with fitness and spatial ecology. The purpose of this review was to better understand how $$\dot{M}$$O2 has been and can be applied to predict how elasmobranch populations will respond to current and future anthropogenic stressors. We identified 10 studies spanning 9 elasmobranch species that quantified $$\dot{M}$$O2 to understand elasmobranch populations’ responses to exposure to anthropogenic stressors. Studies measuring responses to climate change stressors (ocean warming and acidification, declining oxygen content, increasing storm frequency) were most common. Studies with relevance to fisheries stressors used $$\dot{M}$$O2 to approximate energetic costs of capture and estimate recovery times in bycatch scenarios. Ecotourism encounters were investigated in the context of increases in energetic requirements owing to anthropogenic disruption of diel activity cycles. Furthermore, we discuss how an understanding of $$\dot{M}$$O2 in elasmobranchs has been and can be applied to predict populations’ responses to anthropogenic stressors with deliverables for improving species management and conservation. Specifically, $$\dot{M}$$O2 can be applied to predict population-level responses to stressors by quantifying associations between $$\dot{M}$$O2 and fitness-related processes, spatial ecology, and impact on ecosystem function (via bioenergetics modelling). This review is meant to serve as a call-to-action to further bridge the gap between experimental biology and elasmobranch conservation in the “good Anthropocene”.
... A convenience sampling method was used whereby all shark cage-diving participants, over grown rapidly since the early 1990s (Cater, 2008;Dearden, Topelko, & Ziegler, 2008) with an estimated 590,000 tourists participating in global shark watching activities in 2011 (Cisneros-Montemayor, Barnes-Mauthe, Al-Abdulrazzak, Navarro-Holm, & Sumaila, 2013). These tourist experiences range from diving in aquariums to snorkeling with whale sharks (Bentz, Dearden, Ritter, & Calado, 2014;García-Cegarra & Pacheco, 2017;Ziegler, Dearden, & Rollins, 2015), and in-water experiences observing large predatory species including bull sharks (Brunnschweiler, Payne, & Barnett, 2018), tiger sharks (Hammerschlag, Gutowsky, Gallagher, Matich, & Cooke, 2017), blue and shortfin mako sharks (Bentz et al., 2014), and white sharks (Huveneers et al., 2013). ...
Article
Management of protected areas is as much about understanding how society values these resources as it is about understanding ecological processes. Yet, in comparison to standard ecosystem monitoring and economic evaluation, social values are frequently overlooked because of the challenge to measure and define them. As marine protected areas are currently the fastest growing protected area type, this article argues the need to incorporate social value assessment in planning and policy decisions to improve ecological and social outcomes. This study surveyed 675 white shark ( Carcharodon carcharias ) cage-dive participants to investigate how tourists' value the Neptune Islands group (Ron and Valerie Taylor) Marine Park. Applying a value typology previously used in forests, respondents were able to identify with 13 distinct values. Results demonstrate that tourists hold biocentric, indirect use, and nonconsumptive values of the marine park as most important. The relevance of these results as an indicator of tourists' preference for management decisions is discussed.
... Coastal communities in Fiji, Palau, Maldives and the Philippines have realized the more sustainable perspective of exploiting shark species as non-consumptive tourism products rather than consumptive fishing products (Pine et al. 2007;Brunnschweiler 2010;Vianna et al. 2011;Gallagher et al. 2015). Ecotourism, however, can also have negative impacts on species, on public safety, and on the management of activities in marine areas, for example, due to feeding, chumming and excessive disturbance (Apps et al. 2015;Bradley et al. 2017;Brunnschweiler et al. 2018;Huveneers et al. 2018). In Australia, cage diving has been observed to influence the swimming behavior of white sharks, possibly impairing their fitness levels ). ...
Article
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The Mediterranean Sea is a hotspot for shark conservation. A decline in large pelagic shark populations has been observed in this vast region over the last 50 years and a lack of data on the local population status of various species has been pointed out. Throughout history, the relation between people and sharks has been revolving around a mixture of mystery, fear, and attraction. Recently, however, a remunerative ecotourism industry has been growing in areas of shark aggregation globally. This growth has been accompanied by the establishment of a citizen science (CS) movement aimed to engage and recruit ecotourists in data collection for shark research. Several CS projects have generated interesting results in terms of scientific findings and public engagement. In the Mediterranean Sea, shark aggregations are not as relevant to support locally-focused CS actions on shark diving sites as in other parts of the world. However, a series of other initiatives are taking place and CS could offer an excellent opportunity for shark conservation in the Mediterranean Sea. The dramatic decline of shark populations shown in the region calls for alternative ways to collect data on species distributions and abundance. Obtaining such data to set proper conservation and management plans for sharks in the Mediterranean Sea will be possible if existing CS initiatives collaborate and coordinate, and CS is widely acknowledged and deployed as a valuable tool for public education, engagement, and scientific discovery. After providing an overview of multiple facets of the relationship between humans and sharks, we focus on the possibility of exploiting new technologies and attitudes toward sharks among some groups of ocean users to boost participatory research. CS is a great opportunity for shark science, especially for areas such as the Mediterranean Sea and for large pelagic sharks whose populations are highly impacted.
... Fitzpatrick et al., 2011;Heinrich et al., 2021), increased locomotor activity levels (Barnett et al., 2016;Huveneers et al., 2018) and intra-and interspecific aggression (Clua et al., 2010). Furthermore, ecophysiological studies have indicated that provisioning can alter individual metabolic rate (Barnett et al., 2016;Heinrich et al., 2021) and dietary patterns (Brunnschweiler et al., 2018;Maljkovi c & Côt e, 2011). ...
Article
While a growing body of literature has shown that tourism provisioning can influence the behaviour of wildlife, how physiological state might be related to the nature and magnitude of these effects remains poorly understood. Physiological state, including reproductive and nutritional status, can have profound effects on an individual's behaviour and decision making. In the present study, we used multiple physiological markers related to reproductive (testosterone, 17β-oestradiol and progesterone), metabolic (corticosteroids) and nutritional ecology (stable isotopes and fatty acids), integrated with ultrasonography and passive acoustic telemetry to explore the possible relationship between physiological condition and space use of tiger sharks, Galeocerdo cuvier, exposed to dive tourism provisioning. Large, nongravid female tiger sharks, with higher plasma steroid levels (i.e. testosterone, 17β-oestradiol, relative corticosteroid), enriched δ¹⁵N and elevated nutritional status (in terms of fatty acids) spent proportionally more time at food provisioning sites compared to conspecifics. Testosterone levels also were positively correlated with the proportion of time spent at provisioning sites. Based on these results, we speculate that physiological condition plays a role in shaping the spatial behaviour of female tiger sharks within the context of food provisioning, whereby larger individuals, exhibiting higher testosterone levels and elevated nutritional status, show selective preferences for provisioning dive sites, where they outcompete conspecifics of relatively smaller size, lower testosterone levels and depressed nutritional state. While more studies are needed to explore whether sharks are making these decisions because of their physiological state or whether spending more time at provisioning sites results in altered physiological state, our findings highlight the importance of considering animal life stage, endocrine regulation, and nutritional condition when evaluating the biological impacts of provisioning tourism.
... Large meals, such as those that might occur for bold sharks that consistently feed or sharks that gorge during competitive interactions, may reduce aerobic capacity by reducing the available AS for other oxygen-demanding processes (Norin and Clark, 2017). Indeed, single provisioning events can satiate sharks for days (Brunnschweiler et al., 2018). Given concerns that human-wildlife encounters can have consequences for the health of sharks and rays (Semeniuk et al., 2010), ṀO2 can be applied to quantify stress, especially in the context of bioenergetics, that is associated with ecotourism. ...
Thesis
Myriad anthropogenic impacts drive declines in global shark populations; yet, the consequences of a newly recognised threat, global climate change, are poorly understood. This thesis tested the hypothesis that global change stressors (ocean acidification and warming) reduce fitness in tropical reef sharks via effects on physiological performance. My specific objectives were to define thermal performance in fitness-enhancing nursery areas, physiological performance in situ, associations between thermal performance, preference, and tolerance, and physiological performance under multiple global change stressors. I found that neonatal blacktip reef sharks (Carcharhinus melanopterus) have superior growth efficiency in nursery areas relative to other habitats, but ocean acidification and warming synergistically reduce performance. This thesis suggests that global change stressors reduce fitness in tropical reef sharks by acting on physiological traits that are associated with nursery areas.
... Previous studies with captive sharks have documented changes in behaviour consistent with the formation of behavioural associations (Clark, 1959;Guttridge et al., 2009;Guttridge and Brown, 2014;Vila Pouca and Brown, 2018). Provisioning of wild sharks has also been shown to result in changes in behaviour, diet and movement patterns in some cases (Johnson and Kock, 2006;Bruce and Bradford, 2013;Brunnschweiler and Barnett, 2013;Brunnschweiler et al., 2018;Brena et al., 2015;Barnett et al., 2016;Gallagher et al., 2015), although not in others (Laroche et al., 2007;Hammerschlag et al., 2012;Abrantes et al., 2018), and recent research in New Caledonia suggests increased wariness and a lower likelihood of sharks biting bait in fished areas close to populations centres (Juhel et al., 2019). However, the potential for behavioural associations to occur in the context of shark depredation has not been investigated empirically, therefore research into this behavioural process is necessary to understand the mechanisms underlying depredation. ...
Article
Baited video systems have been widely used to assess the relative abundance and diversity of sharks in locations around the world, however they provide limited information on behaviour. We developed and pilot tested a novel experimental approach to investigate whether repeated deployments of baited video systems in the same location could generate quantitative data on shark behavioural patterns, in the context of shark depredation (where sharks consume hooked fish). Specifically, we sought to test whether repeated exposure to boats and food in the same location would lead to a change in the arrival time and first feeding time of sharks, over a short timescale. We used the Ningaloo Marine Park (NMP) in Western Australia, a location where higher shark depredation rates have been identified in consistently fished areas, as a case study. A modified Baited Remote Underwater Video (BRUV) system was repeatedly deployed at two fished sites and two sites within a no-take marine reserve in the NMP, over six consecutive days, to mimic repeated recreational fishing and the availability of hooked fish for sharks to depredate. This approach was designed to investigate and disentangle the potential role of changes in behaviour versus variation in shark abundance, as a mechanism for how and why shark depredation can occur. Here, we report preliminary results from this methodological approach, where time of arrival and time of first feeding declined markedly in the fished site over 6 days of BRUV deployments, compared to the control site in the no-take marine reserve. A greater number of individuals from four carcharhinid species were observed at the fished site, compared to only three individuals from two species in the no-take marine reserve. The preliminary results from pilot testing of this novel experimental approach suggest that, with further modifications to identify individual sharks, and a greater spatial and temporal replication of sampling, it may be possible to identify behavioural changes occurring in sharks in the context of shark depredation. Understanding this mechanism can bring important benefits for fishers and managers, as it can lead to modifications in fishing methods designed at reducing the occurrence of behavioural changes in sharks, and thus mitigating shark depredation.
... If they are reducing the amount of time spent in the lagoon or increasing their activity, it can affect the time and energy allocated to gestation and could in turn have some implications for the fitness and survival of their pups, especially for a species with a relatively high turnover (1-year reproductive circle; 10-to 11-month gestation period; . Moreover, food from provisioning activities can induce trophic shifts in fed individuals and, in certain cases, can impact the health and the condition of an animal's body (Semeniuk, Speers-Roesch & Rothley, 2007;Semeniuk et al., 2009;Maljković & Côté, 2011;Brunnschweiler, Payne & Barnett, 2018). Yet, no negative effects have been reported so far on the reproduction of females using provisioning areas , although further detailed investigations are needed. ...
Article
While the negative effects of consumptive pressures on marine predators are well established, the effects of increasing non-consumptive activities such as wildlife tourism are still understudied. As such, the long-term effects of the provision of bait on shark behaviour are still unclear. Here, we assessed the effects of provi-sioning using a Control-Impact design on the spatial use and level of residency of the blacktip reef shark Carcharhinus melanopterus over a 2-year period. We used effect sizes to model the relative changes in residency between provisioning and non-provisioning sites. Sharks showed a high degree of residency and significant changes in their habitat use which persisted overnight while the activity ceased. We suggest that provisioning activities can affect species with high level of residency such as the blacktip reef shark. Further research is needed to better understand how these behavioural modifications can alter the fitness of this species. It is important to adapt shark provisioning activities to limit the induced changes in habitat use.
... Further, we expected to find differences in the time spent and the bait uptake at the dive site between sharks that were experienced (i.e., philopatric) vs. sharks that were new to the dive site. Finally, based on Brunnschweiler et al. (2018) and the frequency and intensity of provisioning dives in Bimini, we expected that some great hammerhead sharks were likely fulfilling a considerable amount of their daily ration through provisioned food. Such information will be important to find a balance between sustainable ecotourism protocols that minimize the potential impacts on the sharks and their ecological role, while maintaining tourism activities that are important for the local economy. ...
Article
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Wildlife provisioning is popular, economically valuable, and a rapidly growing part of marine tourism, with great potential to benefit conservation. However, it remains controversial due to limited understanding of its implications on the behavior and ecology of target species. In this study, we modeled how various abiotic and biotic factors influenced great hammerhead sharks' (Sphyrna mokarran) use of a recreational dive site in Bimini, the Bahamas, where shark-feeding has been conducted since 2012. Further, we calculated bioenergetic models to estimate their daily ration and examined if individual sharks fulfilled their daily energetic requirements from food uptake during dives. Between December 2016 and May 2017, we collected data during 104 provisioning dives in collaboration with a local dive operator. Twenty-eight individual great hammerhead sharks were observed, 11 were philopatric (i.e., identified at the dive site in previous years), and 17 were new (i.e., identified at the dive site for the first time during this study) individuals. On average, four sharks were observed daily, occasionally up to nine individuals, with some individuals spending more than 2 h attending each dive, consuming up to 4.75 kg of provisioned food per dive and returning repeatedly throughout the study period. When we grouped sharks based on their previous experience of the dive site (i.e., philopatric vs. new sharks), we found significantly higher attendance indices, i.e., the number of attended dives divided by the total number dives, and longer presence times during dives in philopatric sharks and different responses toward the number of boats and conspecifics between the two groups. Overall, great hammerhead sharks increased their bait uptake during longer dives and when more boats were present at the dive site. Finally, nine of 12 provisioned great hammerhead sharks were regularly able to fuel their daily energetic requirements from provisioned food alone, with two sharks doing so on 77.8% of all dives. Our study provides insights into how large-bodied marine predators react toward wildlife tourism associated provisioning and allows further discussion about daily energy uptake during provisioning dives, its potential impacts on the ecological role of the target species and associated management measures.
... However, heavy dependence has been observed in some other species, such as southern stingrays (Dasyatis Americana) (Semeniuk et al., 2007). This could be a sign of potential differential effects of artificial feeding depending on species and practices, which may as well occur at an intraspecific level (Brunnschweiler et al., 2017). Thus, it is expected that elasmobranchs that are fully dependent on daily provisioning activities continue to regularly visit the site, anticipating being fed. ...
Article
The tourism activities linked to artificial provisioning of blacktip reef sharks (Carcharhinus melanopterus) and pink whiprays (Pateobatis fai) on a specific site in French Polynesia were suddenly and completely stopped due to a COVID-19 lockdown that lasted 6 weeks from March 20 until April 30, 2020. Using both drone footage and underwater counting, we were able to track the abundance of those two species before, during, and after reopening and thus investigate the impact of provisioning on wild shark populations. The absence of any stimulus during this long period resulted in almost total desertion of the site by the elasmobranchs. However, 1 day prior to reopening, some individuals of both species positively reacted to the single acoustic stimulus of an engine boat, showing the resilience of conditioning, and some elasmobranchs reacted to acoustic and olfactive stimuli linked to the provisioning practice from the first day after reopening. During the first 2 weeks after reopening, the abundance of both species remained at reduced levels comparable to those observed between 2008 and 2010 for sharks; i.e., around 9 animals in the presence of local tourists. Pre-lockdown abundance levels, reaching approximatively 15 individuals for sharks and 10 for rays, were considered restored 1 and 2 months after reopening for blacktip reef sharks and pink whiprays, respectively. These findings improve our capacity to better understand the potential effects of artificial provisioning tourism on the abundance of elasmobranchs by showing that conditioning is resilient for several weeks, suggesting that intermittent interruption of elasmobranchs feeding would not really help to decrease its impact on animal welfare.
Chapter
Shark ecotourism has the potential to contribute significantly to local and national economies and conservation, though this depends on a concerted effort to implement evidence-based management. Sharks are key attractions at some of the most important marine ecotourism sites throughout Mexico, focusing particularly on whale sharks, white sharks, hammerhead sharks, and several other reef-associated and pelagic species. This generates important employment opportunities and millions of USD in revenue, but truly implementing ecotourism requires that education and conservation be a part of activities and that these benefit local communities, so that the industry can be socially, economically and ecologically sustainable. In Mexico, this includes addressing potential negative impacts from vessel overcrowding, provisioning, inequitable distribution of ecotourism and conservation benefits and costs, and a broader lack of governance capacity to ensure that coastal development is environmentally sustainable and socially equitable. In the context of a Blue Economy centred on sustainability and local benefits, ecotourism provides a key incentive and opportunity to improve ocean management.
Book
This is the second book in a series about the sharks of Mexico their biology, ecology and conservation. These are books in Elsevier's Advances in Marine Biology Series vol 83 (part A) and 85 (part B). Topics covered are: Shark movement patterns in the Mexican Pacific: A conservation and management perspective; Fisheries interactions and the challenges for target and nontargeted take on shark conservation in the Mexican Pacific; Shark ecotourism in Mexico: Scientific research, conservation, and contribution to a Blue Economy; and Conclusions:Doweeatthemorwatchthem, orboth?Challenges for conservation of sharks in Mexico and the NEP
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Marine protected areas (MPAs) effectively improve the biomass and diversity in heavily exploited marine systems, but often fail to reach their full potential because they require more space, time, and consistency of regulation. Recently, shark-based tourism, which utilises some of the remaining shark strongholds as tourism hotspots, has brought about increased awareness to exploited reef systems. In Fiji, specifically, shark diving companies include local community members in their operations to promote better understanding of their reefs. We seek to investigate whether seemingly denser shark populations during feeding times influence community composition and structure. Visual census data were collected from 50-m belt transects at four different reefs in Fiji: two MPAs with shark-based ecotourism with food provisioning, one MPA without shark-based ecotourism, and one unprotected area without shark-based tourism. Paradoxically, indices of evenness and diversity were highest in the non-protected site. However, there was significantly higher fish abundance and species diversity within reserves than outside of reserves. Within reserves, sites with shark feeding had lower fish abundance and higher richness, diversity, and evenness. Mean trophic level was highest at sites with shark feeding. Use of chum increased average fish abundance and diversity within shark-dive sites. These results indicate that there are evident differences between MPAs that do and do not offer trophic supplementation for shark-based ecotourism. Thus, tourism may be facilitating a shift of ecosystem composition in such areas. Furthermore, the results suggest that feeding methods may augment the impacts of shark-based tourism on the reef at large.
Article
Wildlife tourism uses various stimuli to attract species and facilitate close encounters. Such activities are often referred to as provisioning, however the term is used interchangeably, and sometimes erroneously, with attracting, feeding, luring, and chumming, all of which lack consistent definitions. Here, we review the current use of provisioning-associated terminology in marine bird, teleost (bony fish), marine mammal, marine reptile, ray and shark tourism, within the scientific literature and on tourism operator webpages. We then propose to reclassify provisioning into Feeding, Attracting, and Modifying habitat, providing eight specific terms that reflect: (1) if the stimulus exploits wildlife appetite or search for preferred habitat; (2) the nature of the attractant (consumable or not); (3) the intention of the activity if using consumable attractants (direct, indirect, or incidental feeding) or modified habitat (intentional or repurposed modification); and (4) which species are affected by the activity (target or non-target species). We applied these terms to wildlife tourism around the world to gain better insight into tourism practices across taxa. Clarifying the terminology describing these wildlife interactions ensures they can be accurately described in the scientific literature, which will in turn help resource managers and industry groups to systematically assess these diverse activities.
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The bull shark (Carcharhinus leucas Valenciennes, 1839) is a large, primarily coastally distributed shark famous for its ability to penetrate far into freshwater bodies in tropical, subtropical, and warm-temperate climates. It is a cosmopolitan species with a geographical range that includes the coastlines of all major ocean basins (Atlantic Ocean, Indian Ocean, Pacific Ocean). As a consequence, freshwater occurrences of C. leucas are possible everywhere inside its geographic range. Carcharhinus leucas is a fully euryhaline, amphidromous species and possibly the widest-ranging of all freshwater tolerating elasmobranchs. This species is found not only in river systems with sea access that are not interrupted by human impediments but in hypersaline lakes as well. Rivers and estuaries are believed to be important nursery grounds for C. leucas, as suggested by observations of pregnant females in estuaries and neonates with umbilical scars in rivers and river mouths. Due to the physical capability of this species to enter riverine systems, the documentation of its occurrence in fresh and brackish water is essential for future conservation plans, fishery inspections, and scientific studies that focus on the link between low salinity habitats, shark nurseries, and feeding areas. The author’s review of the available literature on C. leucas revealed the absence of a comprehensive overview of fresh and brackish water localities (rivers and associated lakes, estuaries) with C. leucas records. The purpose of this literature review is to provide a global list of rivers, river systems, lakes, estuaries, and lagoons with records and reports of this species, including a link to the used references as a base for regional, national, and international conservation strategies. Therefore, the objective of this work is to present lists of fresh and brackish water habitats with records of C. leucas as the result of an extensive literature review and analysis of databases. This survey also took into account estuaries and lagoons, regarding their function as important nursery grounds for C. leucas. The analysis of references included is not only from the scientific literature, but also includes semi-scientific references and the common press if reliable. The result of 415 global fresh and brackish water localities with evidence of C. leucas highlights the importance of these habitats for the reproduction of this species. Moreover, gaps in available distribution maps are critically discussed as well as interpretations and conclusions made regarding possible reasons for the distribution range of C. leucas, which can be interpreted as the result of geographic circumstances, but also as a result of the current state of knowledge about the distribution of this species. The results of the examination of available references were used to build a reliable and updated distribution map for C. leucas, which is also presented here.
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The use of olfactory stimuli and the provision of food are a common practice to prompt artificial aggregations of emblematic wild species and ensure the economic viability of the wildlife-watching industry. Several elasmobranch species have been targeted by such operations in a variety of locations for over four decades. A recent review succinctly addressed the potential effects of shark diving tourism, including shark provisioning, on shark individual behavior and ecology, but the general paucity of data on the ecology of elasmobranchs precluded general statements. By using a functional framework, we reviewed the findings of the 22 available studies that investigated the behavioral, physiological, and ecological response of 14 shark and three ray species targeted by artificial provisioning. Focusing on the underlying processes that rule the response of targeted elasmobranch species, we report further effects acting beyond the individual-scale and their cross-scale relationships. We suggest that the most commonly described alterations of individual movement patterns have cascading effects through the group and community-scale, ultimately resulting in altered health condition and individual behavior toward humans. We conclude by stressing the potential for provisioning activities to support the investigation of complex ecological and behavioral processes in elasmobranchs.
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Many shark populations are experiencing critical declines from overfishing, triggering potentially detrimental cascade effects on marine ecosystems. Silky sharks, Carcharhinus falciformis, have experienced some of the most severe declines, yet little information exists on their behavioural ecology to inform management decisions. In the present study, the movement patterns of a sexually segregated subpopulation of female silky sharks on reefs in the Central Red Sea were investigated using acoustic telemetry to characterise habitat-use and residency patterns. Frequent baiting of sharks at a particular reef-site significantly increased time spent in the vicinity, although no increases in use of other reef areas 5-10 and 50-60 km away were recorded, and regular use of all three reef areas persisted in the absence of bait. Observed residency patterns varied considerably, from being present almost year-round to visiting only intermittently. The sharks spent significantly longer times at study reefs during daylight hours, even within bait-free regions, suggesting the diel bias is normal. This pattern became less distinct nearer the full moon when there is more ambient light. The regular, perennial use of these reefs by mature and near-mature female silky sharks highlights the importance of this habitat in the Red Sea for recruitment into the local shark population.
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Body size and temperature are primary determinants of metabolic rate, and the standard metabolic rate (SMR) of animals ranging in size from unicells to mammals has been thought to be proportional to body mass (M) raised to the power of three-quarters for over 40 years. However, recent evidence from rigorously selected datasets suggests that this is not the case for birds and mammals. To determine whether the influence of body mass on the metabolic rate of vertebrates is indeed universal, we compiled SMR measurements for 938 species spanning six orders of magnitude variation in mass. When normalized to a common temperature of 38 degrees C, the SMR scaling exponents of fish, amphibians, reptiles, birds and mammals are significantly heterogeneous. This suggests both that there is no universal metabolic allometry and that models that attempt to explain only quarter-power scaling of metabolic rate are unlikely to succeed.
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This study represents the first description of whale sharks, Rhincodon typus, occurring at a provisioning site in Oslob, Cebu, Philippines. Frequent observations of sharks are often difficult, even at tourism sites, giving rise to provisioning activities to attract them. The present study provides repeated longitudinal data at a site where daily provisioning activities took place, and whale sharks were present every day. A total of 158 individual whale sharks were photographically identified between Mar 2012 and Dec 2013, with 129 males (82%), 19 females (12%) and 10 (6%) of undetermined sex. Mean estimated total length was 5.5 m (±1.3 m S.D.). Twenty individuals were measured with laser photogrammetry to validate researchers' estimated sizes, yielding a good correlation (r (2) = 0.83). Fifty-four (34%) individuals were observed being hand-fed by local fishermen (provisioned), through in-water behavioural observations. Maximum likelihood methods were used to model mean residency time of 44.9 days (±20.6 days S.E.) for provisioned R. typus contrasting with 22.4 days (±8.9 days S.E.) for non-provisioned individuals. Propeller scars were observed in 47% of the animals. A mean of 12.7 (±4.3 S.D.) R. typus were present in the survey area daily, with a maximum of 26 individuals (Aug 10 2013) and a minimum of 2 (Dec 6 2012). Twelve (8%) individuals were seen on at least 50% of survey days (n = 621), with a maximum residency of 572 days for one individual (P-396). Twenty four individuals were photographically identified across regional hotsposts, highlighting the species' migratory nature and distribution. Extended residency and differences in lagged identification rates suggest behavioural modification on provisioned individuals, underlying the necessity for proper management of this tourism activity.
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Tuna bioenergetics can be described by the following relationship: the energy available for growth is equal to the food energy minus all metabolic costs. These costs include routine metabolic rate, specific dynamic action, increased activity level, eliminated waste, and gonadal development. Captive populations of Pacific bluefin tuna (Thunnus orientalis) were held at ~ 20 °C in fiberglass tanks and fed on a regular schedule with a diet formulated to achieve an energetic content of 176 ± 36 kJ · kg− 1 of biomass · day− 1 (mean ± s.d.). To conduct a bioenergetic study, growth rates during the captive period and tissue energy values post-mortem were empirically determined. Daily growth rates were obtained from a von Bertalanffy growth function based on curved fork length (CFL) measurements of live fish and post-mortem morphometrics. The parameters obtained for the captive bluefin growth function were 225.13 cm straight fork length (SFL), 0.173, and − 0.497 years for L∞, k, and to, respectively. The growth equation, SFL = 225.13 · (1 −e(− 0.173(t-(− 0.497)))) in conjunction with the length-mass regression (where body mass M = 4.98 × 10− 6 × SFL 3.3186) gave a daily growth increase of 32.60 ± 2.40 g · day− 1 for Pacific bluefin tuna of 2.2 years of age and 11.4 ± 1.0 kg (the average age and mass of a fish in the study). The average tissue energy value from four sampled tuna was 7.66 ± 0.40 kJ · g− 1, and applying the daily growth increase estimate provides a daily energy gain of 249.7 kJ, which is 12.4% of an ingested meal's total energy content. A food conversion ratio of 17.8:1 is estimated for a meal consisting solely of sardines and 22.6:1 for a mixed diet consisting of sardines, squid, and a gelatin-vitamin mixture at the stated feeding regimen. This paper presents the first data on actual food conversion ratios and bioenergetic utilization for Pacific bluefin tuna.
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Diving with sharks, often in combination with food baiting/provisioning, has become an important product of today's recreational dive industry. Whereas the effects baiting/provisioning has on the behaviour and abundance of individual shark species are starting to become known, there is an almost complete lack of equivalent data from multi-species shark diving sites. In this study, changes in species composition and relative abundances were determined at the Shark Reef Marine Reserve, a multi-species shark feeding site in Fiji. Using direct observation sampling methods, eight species of sharks (bull shark Carcharhinus leucas, grey reef shark Carcharhinus amblyrhynchos, whitetip reef shark Triaenodon obesus, blacktip reef shark Carcharhinus melanopterus, tawny nurse shark Nebrius ferrugineus, silvertip shark Carcharhinus albimarginatus, sicklefin lemon shark Negaprion acutidens, and tiger shark Galeocerdo cuvier) displayed inter-annual site fidelity between 2003 and 2012. Encounter rates and/or relative abundances of some species changed over time, overall resulting in more individuals (mostly C. leucas) of fewer species being encountered on average on shark feeding dives at the end of the study period. Differences in shark community composition between the years 2004-2006 and 2007-2012 were evident, mostly because N. ferrugineus, C. albimarginatus and N. acutidens were much more abundant in 2004-2006 and very rare in the period of 2007-2012. Two explanations are offered for the observed changes in relative abundances over time, namely inter-specific interactions and operator-specific feeding protocols. Both, possibly in combination, are suggested to be important determinants of species composition and encounter rates, and relative abundances at this shark provisioning site in Fiji. This study, which includes the most species from a spatially confined shark provisioning site to date, suggests that long-term provisioning may result in competitive exclusion among shark species.
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Ecotourism operations which provide food to large predators have the potential to negatively affect their target species, by conditioning them to associate humans with food, or by generally altering their behavioural patterns, This latter effect could have potentially detrimental consequences for the ecosystem inhabited by the predator, because any behavioural changes could affect the species with which they interact. We present the results of an experimental study conducted from June to October 2004, which examined the effects of provisioning ecotourism on the behaviour of white sharks around a seal colony on a small island in South Africa. Although ecotourism activity had an effect on the behaviour of some sharks, this was relatively minor, and the majority of sharks showed little interest in the food rewards on offer. It is unlikely that conditioning would occur from the amount of ecotourism activity tested, because even those sharks identified supplying most of the data presented here (which may be more strongly predisposed towards conditioning, as their persistence around the boat is what allowed them to be identified) showed. a nearly ubiquitous trend of decreasing response with time. Furthermore, even the sharks frequently acquiring food rewards typically stopped responding after several interactions. Consequently, moderate levels of ecotourism probably have only a minor impact on the behaviour of white sharks, and are therefore unlikely to create behavioural effects at the ecosystem level.
Article
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Shark-based tourism that uses bait to reliably attract certain species to specific sites so that divers can view them is a growing industry globally, but remains a controversial issue. We evaluate multi-year (2004-2011) underwater visual (n = 48 individuals) and acoustic tracking data (n = 82 transmitters; array of up to 16 receivers) of bull sharks Carcharhinus leucas from a long-term shark feeding site at the Shark Reef Marine Reserve and reefs along the Beqa Channel on the southern coast of Viti Levu, Fiji. Individual C. leucas showed varying degrees of site fidelity. Determined from acoustic tagging, the majority of C. leucas had site fidelity indexes >0.5 for the marine reserve (including the feeding site) and neighbouring reefs. However, during the time of the day (09:00-12:00) when feeding takes place, sharks mainly had site fidelity indexes <0.5 for the feeding site, regardless of feeding or non-feeding days. Site fidelity indexes determined by direct diver observation of sharks at the feeding site were lower compared to such values determined by acoustic tagging. The overall pattern for C. leucas is that, if present in the area, they are attracted to the feeding site regardless of whether feeding or non-feeding days, but they remain for longer periods of time (consecutive hours) on feeding days. The overall diel patterns in movement are for C. leucas to use the area around the feeding site in the morning before spreading out over Shark Reef throughout the day and dispersing over the entire array at night. Both focal observation and acoustic monitoring show that C. leucas intermittently leave the area for a few consecutive days throughout the year, and for longer time periods (weeks to months) at the end of the calendar year before returning to the feeding site.
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Several methods to indirectly estimate metabolism of aquatic animals have been reported, including heart rate, electromyograms, video recording, and averaging velocity of an animal moving between two or more points. The present study carried out in the lagoon at Bimini Islands, Bahamas, used acoustic, speed-sensing transmitters to indirectly estimate energy consumption of 1.5–2 m subadult lemon sharks (Negaprion brevirostris). Speed records from three sharks tracked a total of 170 h, yielded average swimming speeds of 0.44–0.71 m s-1. These speeds were converted into energy consumption to obtain metabolism. By combining the estimates of metabolism with calculated values on assimilation and production, we are able to present a balanced bioenergetics model for the subadult lemon shark: 100C = 7P + 66M + 26E, where C = consumption, P = production, M = metabolism, and E = excretion. When comparing juvenile lemon sharks to subadults, an ontogenetic shift is seen: 0 to 2 yr olds allocate 22% of consumed energy to production and 50% to metabolism while 6 to 9 yr olds show values of 7% and 66%, respectively. We believe this to be the first field-based, balanced equation presented for any large elasmobranch.
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In the dive tourism industry, shark provisioning has become increasingly popular in many places around the world. It is therefore important to determine the impacts that provisioning may have on shark behaviour. In this study, eight adult whitetip reef sharks Triaenodon obesus were tagged with time-depth recorders at Osprey Reef in the Coral Sea, Australia. Tags collected time and depth data every 30s. The absolute change in depth over 5-min blocks was considered as a proxy for vertical activity level. Daily variations in vertical activity levels were analysed to determine the effects of time of day on whitetip reef shark behaviour. This was done for days when dive boats were absent from the area, and for days when dive boats were present, conducting shark provisioning. Vertical activity levels varied between day and night, and with the presence of boats. In natural conditions (no boats present), sharks remained at more constant depths during the day, while at night animals continuously moved up and down the water column, showing that whitetip reef sharks are nocturnally active. When boats were present, however, there were also long periods of vertical activity during the day. If resting periods during the day are important for energy budgets, then shark provisioning may affect their health. So, if this behaviour alteration occurs frequently, e.g., daily, this has the potential to have significant negative effects on the animals’ metabolic rates, net energy gain and overall health, reproduction and fitness. Keywords Triaenodon obesus –Ecotourism–Shark feeds–Depth use–Disturbance–Behavioural response–Provisioning–Sharks
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Shark tourism has become increasingly popular, but remains controversial because of major concerns originating from the need of tour operators to use bait or chum to reliably attract sharks. We used direct underwater sampling to document changes in bull shark Carcharhinus leucas relative abundance at the Shark Reef Marine Reserve, a shark feeding site in Fiji, and the reproductive cycle of the species in Fijian waters. Between 2003 and 2009, the total number of C. leucas counted on each day ranged from 0 to 40. Whereas the number of C. leucas counted at the feeding site increased over the years, shark numbers decreased over the course of a calendar year with fewest animals counted in November. Externally visible reproductive status information indicates that the species' seasonal departure from the feeding site may be related to reproductive activity.
Article
The increasing popularity of marine wildlife tourism (MWT) worldwide calls for assessment of its conservation outcomes and the development of appropriate management frameworks to ensure the conservation of the species and habitats involved as well as the long-term sustainability of this industry. While many studies have examined the positive and/or negative implications of particular forms of MWT, few have attempted to identify factors of concern shared across different types of marine tourism, or examine their implications for sustainability in a broader perspective. We reviewed the existing literature to highlight common impacts on animal behaviour, health and ecology, and to identify successful cases based on minimal negative affects and/or lack of chronic/irreversible impacts on target species or habitats. To ensure the achievement of both economic and ecologic objectives, the following steps should be integrated in MWT management: 1) Increase of research on the biology and ecology of target species/habitat and application of relevant information for the development of suitable policies, frameworks and management strategies; 2) Structured enforcement of existing policies and enhancement of ecological awareness of visitors through active education; 3) Application of an adaptive management framework to continuously improve the codes of conduct employed; 4) Involvement of different stakeholders and local communities in the development and improvement of the MWT activity. Combining these strategies with the extrapolation of frameworks and policies from cases where adverse ecological impacts have been addressed and successfully resolved can further contribute in ensuring the long-term health and conservation of the species/habitats involved in MWT activities.
Article
Wildlife tourism has been shown to cause behavioural changes to numerous species. Yet, there is still little understanding if behavioural changes have consequences for health and fitness. The current study combined accelerometry and respirometry to show that provisioning whitetip reef sharks (Trianadon obesus) for tourism increases their daily energy expenditure by elevating activity levels during periods when they normally rest. Field metabolic rate increased by 6.37% on provisioning days compared to non-provisioning days. Since metabolism is a key parameter influencing most biological and ecological processes, this represents some of the clearest evidence to date that ecotourism can impact critical biological functions in wild animals.
Article
The thermal dynamics of bomb calorimeters are modeled using a lumped heat transfer analysis in which heat is released in a pressure vessel/bomb immersed in a stirred water bath that is surrounded by a static air space bounded by an insulated (static) jacket, a constant/controlled temperature jacket (isoperibol), or a changing temperature (adiabatic) jacket. The temperature history of the water bath for each of these boundary conditions (methods) is well described by the two-term solution for the calorimeter response to a heat impulse (combustion), allowing the heat transfer coefficients and thermal capacities of the bomb and water bath to be determined parametrically. The validated heat transfer model provides an expression for direct calculation of the heat released in an arbitrary process inside a bomb calorimeter using the temperature history of the water bath for each of the boundary conditions (methods). This result makes possible the direct calculation of the heat of combustion of a sample in an isoperibol calorimeter from the recorded temperature history without the need for semi-empirical temperature corrections to account for non-adiabatic behavior. Another useful result is that the maximum temperature rise of the water bath in the static jacket method is proportional to the total heat generated, and the empirical proportionality constant, which is determined by calibration, accounts for all of the heat losses and thermal lags of the calorimeter.
Article
Body size is a key determinant of metabolic rate, but logistical constraints have led to a paucity of energetics measurements from large water-breathing animals. As a result, estimating energy requirements of large fish generally relies on extrapolation of metabolic rate from individuals of lower body mass using allometric relationships that are notoriously variable. Swim-tunnel respirometry is the ‘gold standard’ for measuring active metabolic rates in water-breathing animals, yet previous data are entirely derived from body masses <10 kg – at least one order of magnitude lower than the body masses of many top-order marine predators. Here, we describe the design and testing of a new method for measuring metabolic rates of large water-breathing animals: a c. 26,000 L seagoing ‘mega-flume’ swim-tunnel respirometer. We measured the swimming metabolic rate of a 2·1-m, 36-kg zebra shark Stegostoma fasciatum within this new mega-flume and compared the results to data we collected from other S. fasciatum (3·8–47·7 kg body mass) swimming in static respirometers and previously published measurements of active metabolic rate measurements from other shark species. The mega-flume performed well during initial tests, with intra- and interspecific comparisons suggesting accurate metabolic rate measurements can be obtained with this new tool. Inclusion of our data showed that the scaling exponent of active metabolic rate with mass for sharks ranging from 0·13 to 47·7 kg was 0·79; a similar value to previous estimates for resting metabolic rates in smaller fishes. We describe the operation and usefulness of this new method in the context of our current uncertainties surrounding energy requirements of large water-breathing animals. We also highlight the sensitivity of mass-extrapolated energetic estimates in large aquatic animals and discuss the consequences for predicting ecosystem impacts such as trophic cascades.
Article
The Shark Reef Marine Reserve in Fiji is an ecotourism project designed to protect a small reef patch and its fauna while preserving the livelihood of local communities. It involves the local communities by using a participatory business planning approach to Marine Protected Area management, generating income through diver user fees, distributed to the local villages that have exchanged their traditional fishing rights in the marine reserve for this new source of income. The Shark Reef Marine Reserve is a self-sustaining and profitable project, and is an example of a privately initiated, bottom-up approach, which includes all relevant stakeholders in an area where marine rights are finely subdivided into small units.
Article
Understanding the energy requirements for captive sharks is important for their successful long-term maintenance. This information is critical in assessing the health of the animals and the suitability of their environment. We studied five bull sharks (Carcharhinus leucas) for up to 7 years in a 2.5 × 106 liter oceanarium. Individual animal feedings provided information for food intake analysis. During the first 3 years, fork length increase was estimated to have averaged 1.9 cm/month (s.d. = 0.1), or 23.0 cm/year. Biannual measurements, begun in the fourth year, showed that growth rates decreased during the next 4 years to a mean rate of 0.6 cm/month (s.d. = 0.2), or about 7.0 cm/year. Mean food consumption from June 1988 to December 1992 was 3.4% body weight per week. Caloric conversion of weights incorporated into a simple bioenergetics model providing mean metabolic expenditures per animal was 5.7 (s.d. = 0.3) and 4 (s.d. = 0.5) kcal/kg/day for 1991 and 1992, respectively. © 1994 Wiley-Liss, Inc.
Article
Length at age and growth rates for 59 bull sharks, Carcharhinus leucas, collected from the northern Gulf of Mexico were estimated from the band patterns formed seasonally in the vertebral centra. The combined age at length data for both sexes were applied to a von Bertalanffy growth model producing parameter estimates of L = 285 cm TL, K = .076, t0 = –3.0 yr. Lengths at age for males and females were similar except that males did not attain as great a length as females. Growth was apparently slow and varied among individuals, but in general, was estimated to be 15–20 cm yr–1 for the first five years, 10 cm yr–1 for years 6–10, 5–7 cm yr–1 for years 11–16, and less than 4–5 cm yr–1 thereafter. Males mature at 210–220 cm TL or 14–15 yr of age; females mature at>225 cm TL or 18+ yr of age. The largest male (245 cm TL) was 21.3 yr old; the largest female (268 cm TL) was 24.2 yr old.
Article
Adult bull sharks Carcharhinus leucas were monitored with electronic tags to investigate horizontal and vertical movements in the Atlantic and Pacific Oceans. In both locations, C. leucas showed some fidelity to specific coastal areas with only limited horizontal movements away from the tagging sites after tag attachment. Fish tagged in the Bahamas were detected mostly in the upper 20 m of the water column in water 25-26° C, whereas C. leucas tagged in Fiji spent most of their time below 20 m in water usually >26° C. The results highlight the importance of coastal inshore habitats for this species.
Physiological energetics
• J R Brett
• D D Groves
Brett, J.R. & Groves, D.D. (1979). Physiological energetics. In Fish physiology: 279-352. Hoar, W.S., Randall, D.J. & Brett, J.R. (Eds). New York: Academic Press.