The surface presence of white sharks was similar regardless maturity, sex, or type of bait, suggesting a similar effectiveness in the attractant of sharks. In other ethological studies, the white shark has been suggested as a predator that evaluates the consumption of food through previous inspection and monitoring14,15,16. In this instance, the use of frozen or fresh bait had a similar effectiveness when attracting sharks, mainly due to the visual and olfactory stimuli inherent to the bait16,17,18. It is possible that the scent of the frozen bait was not significantly different from a fresh bait, since there is no nutritional differences between both treatments19. This has been observed in other pelagic species such as the yellow fin tuna T. albacares, where the catches are similar regardless of the freshness of the bait20. However, the smell would be the main sense involved in the attraction at distance, while the sight would be fundamental in the decision of the capturing of prey20,21.
In other aggregation sites, the use of bait has shown a minimum effect on the white sharks behaviour2,3. In South Africa, Laroche et al.1 suggest that the population of 64,000 Cape fur seals, Arctocephalus pusillus pusillus, generates a constant olfactory stimulus for the white sharks, so the use of bait is negligible for the attraction and conditioning of C. carcharias1,22. A similar effect occurs in Farallon Islands where cage diving is often difficult, probably explained by the presence of a high density of northern elephant seals Mirounga angustirostris4. The extension of both sites is 0.02 km2 for the South African site, and 0.42 km2 for the American one. If it is compared with the 241 km2 of Guadalupe Island, the density of pinnipeds could be much lower in this oceanic island. In this regard, the absence of a natural, intense, and permanent stimulus in Guadalupe Island could explain both the success to attract sharks to the boats and the inherent risk of conditioning.
The idea that a fresh stimulus could generate a greater number of sightings cannot be accepted according to the results of the present study, since all the baits showed a similar effect on the attraction of the sharks. This lack of preference for a particular attractant may be related to the opportunistic predation on dead animals such as whale carcasses that have been observed in mature and immature white sharks23,24,25,26. Future analysis involving the hour of arrival of each shark according to the type of bait could be useful to determine the effectiveness in terms of time, which could complement the information for boat owners during ecotourism.
There were significant differences in the observed behavioural patterns according to the type of bait. The behavioural patterns with the frozen bait with chum and fresh bait were related to the reception of stimuli and feeding, while the frozen bait did not generate a defined pattern. It is possible that the smell and appearance of a frozen bait generate an olfactory and visual attraction in the white sharks without aggressions16,21. In contrast, the use of fresh bait along with the stimuli of a recently captured animal could be part of the explanation for the violent behaviours observed with this type of bait14,17,18.
Contrary to the pattern observed with the use of fresh bait, the behavioural transitions towards aggressive displays were not detected during the use of a frozen bait. This lower number of agonistic displays could decrease the risk of accidents of white sharks that enter or hit the cages, as it is frequently observed during each cage diving season22. However, vigilance and specifications for the handling of the bait, as well as for the redesign of the cages are the first steps to reduce the incidence of accidents11,12,22.
The horizontal strike (HS) was the most frequent behaviour during the study period, as it has been similarly observed in Australia by Tricas27 and Strong14, and in South Africa by Sperone et al.15. The large number of foraging attempts with respect to the number of captures and consumptions was the cause of the low effectiveness of this behaviour. In comparison with the immature individuals, the mature sharks managed to capture and consume the bait more efficiently. This may be attributable to the experience and size of white sharks according to their age, since mature sharks perform a better evaluation of the conditions before ambushing their prey to efficiently manage their energy when compared to immature individuals22,28.
In previous research, a low effectiveness of the foraging attempts has been related to energy loss and a physiological imbalance that could affect the health of the sharks10,11,22. An evaluation of the effects on the metabolic rate of the white sharks could provide insights in terms of energy loss caused by ecotourism, as it has been observed in other species of sharks29,30. However, an energetic affectation is unlikely if there is a low conditioning in the sharks that interacted with the boats, as it was observed under the current ecotourism conditions of Guadalupe Island.
The development of a conditioning to the boats requires defined patterns for feeding, since the behaviours and stimuli must be constant for this learning1,31,32,33. The sharks that interacted with the frozen bait presented a diverse number of behaviours for the acquisition of food, so this high variability of displays would prevent the development of conditioning in the absence of a defined behavioural pattern. In contrast, chum and fresh baits did demonstrate a pattern directed toward aggressions and reception of stimuli. Unlike those observed by Laroche et al.1, it is possible that the baits such as chum or fresh tuna could generate a future change in the behaviour of C. carcharias in Guadalupe Island22. In this regard, trophic interactions of each white shark population should be considered for future comparative studies, as differences in diet could be involved in the response and conditioning to the used baits6,9.
It is improbable that the ecotourism generates a conditioning on the white sharks of Guadalupe Island. Although the used criteria underestimate the cognitive capacity of the white shark, there are five arguments that may explain the lack of conditioning in this aggregation site.
- 1.
Few visits of sharks. In other studies, conditioning was observed after 6 months of interaction with the constant provision of substantial food in training sessions that lasted more than 20 min32,34. In this study, most of the sharks were recorded in less than 5 days, so their low permanence would not allow a conditioning32,35,36.
- 2.
Duration of the season. Studies in captivity have shown that conditioning can persist after 10 weeks in the memory of sharks31. This conditioning arises after receiving a constant stimulus under controlled situations31,32,36. In Guadalupe Island, the stimuli granted by their natural prey availability5,37, the white shark migration habits and its local movements5,38, as well as the 8 months between seasons11 could affect the duration of conditioning in terms of the memory of the sharks31,32. Under this assumption, the shark’s attraction to the boats would be the result of a natural curiosity and not of acquired learning16,17,39.
- 3.
Low consumption of bait. In previous studies, the reception of “substantial” stimuli was one of the criteria necessary to determine a high risk of conditioning31,32,36. In the present research, the capture of at least one bait was considered as substantial and significant for the detection of conditioning in a precautionary measure to detect any indication of possible conditioning. Despite this, it was not possible to detect more than three sharks that fulfilled the bait intake, the number of visits and necessary interactions to determine a high risk of conditioning.
- 4.
Effectiveness. The effectiveness of the strikes or foraging attempts was low for the capture and consumption of bait, so this lack of stimuli could lead to the disappearance of the potential acquired response in conditioning. White sharks from Guadalupe did not have many reinforcements, and the amount of strikes in means of energy used to capture them may not be profitable for their energetics22. A conditioning is unlikely when not enough stimuli is received during the development or maintenance of learning31,33.
- 5.
Competition. The highest number of sightings was registered during the month of August and corresponded mostly to mature and immature males. It is possible that the presence of sharks of similar size favours the intraspecific interactions with respect to the bait, due to a greater tolerance on the part of the males of similar sizes22. However, the decrease in sightings during the following months could be related to the presence of larger sharks, which, given a hierarchy by size, would displace small sharks that could be more vulnerable to conditioning. In this manner, the segregated migration of mature sharks, the size hierarchy and competition would prevent immature individuals from developing a conditioning11,22,38.
In any case, the learning capacity of sharks could be higher during their juvenile stages32,34, so the monitoring of these individuals is essential to understand the possible changes in their presence or behaviour. A high number of immature males were observed during all season, so the vigilance in order to avoid the consumption of bait would represent a measure of precautionary management to prevent the conditioning of the white sharks11,22,32.
The study of the behaviour of sharks is necessary in the localities were ecotourism occurs. Although some activities like snorkelling, scuba diving or cage diving are considered as sustainable, there are few studies related to the negative effects of ecotourism in most shark populations2,29,30,40,41,42. The acquisition of data through science-based monitoring is a practical strategy that could improve the knowledge about the biology of the species, its relations with ecotourism and the correct decisions for good practices22. Some of the proper management regulations could include tourism seasonality, quantity of boats and the responsible use of organic attractants if these were needed9,22.
As a cosmopolitan species that is economically exploited in several countries, the presented results of the behaviour of white sharks could be useful in future comparisons with other populations6,22. This observational method is applicable without the need of invasive techniques or high economical resources, which could facilitate the obtention of data through the participation of trained observers and the tourism inclusion in scientific activities. This could lead to a significant contribution to local marine policies for efficient protection and sustainable use of the sharks, as it has been observed in other marine protected areas43,44.
Wildlife regulations during ecotourism are essential for the prevention of accidents between humans and sharks. The limited vigilance in Guadalupe Island, along with a lack of scientific evidence supporting some of the unfollowed regulations, were part of the cause for several accidents that occurred in 2016 and the years before, where several sharks and divers were harmed during ecotourism44, including the recent death of a white shark in 201912. Although these situations are scarce and could not be avoided in some cases, the information regarding the behaviour to specific type of baits is needed for the prevention of accidents through science-based decisions. In the present paper, the different short-term surface behaviours according to the type of bait are provided in order to prevent more accidents, as well as to improve the monitoring of this threatened species.
The creation of a standard governmental monitoring using the presented methods will be useful for the constant evaluation of this and other shark populations. Future studies should consider the effect of the environment, social behaviour, personalities of sharks, times of response to the bait and movements of the sharks by the use of other techniques such as drone video and acoustic tagging in relation to the boats, which could provide more insights about the effects of cage diving ecotourism2,42. Additionally, the use of genetics and other photo identification methods, such as the analysis of dorsal fins and mark-recapture studies, would be beneficial for the knowledge of the status of this white shark population45,46.
The improvement of monitoring through the participation of trained observers would allow the generation of scientific knowledge in terms of ecology, demography and ethology if the proper data are frequently obtained9,22,27. Research involving minimum invasive techniques as the one presented in this paper could be useful for the generation of such information, which in turn can be used for the improvement of the activity in terms of sustainability and the conservation of this threatened species. Specific recommendations for cage diving ecotourism could be the creation of emergency response protocols for stuck sharks and injured divers, as well as the implementation of a nautical video vigilance cameras onboard all boats. The latter could be useful for the governmental inspection of good practices and the obtention of data in one of the most profitable and sustainable activities with sharks worldwide6,9.
Source: Ecology - nature.com
