Associative conditioning of white sharks (Carcharodon carcharias) in a baited situation. R. L. Robbins.

Transcription

1 Associative conditioning of white sharks (Carcharodon carcharias) in a baited situation R. L. Robbins rachel@sharkfoundation.com Fox Shark Research Foundation, 17 Lowan Avenue, Glenalta, SA 5052 ABSTRACT This study investigated conditioning of white sharks to feeding by humans over a three-year period at the Neptune Islands, South Australia. Over half of the sharks (n = 69) were seen on one day only over the 3 year study, with the majority being observed for less than five days, thus discounting them from the risk of conditioning under the conditions outlined. The number of sharks at risk of conditioning was not statistically significant, with less than 5% of sharks falling into one or more high conditioning risk categories. Although not significant, signs of conditioning were evident in a few individuals, particularly those that were frequent visitors. Changes in the conduct of operators, such as bait limitations, were recommended to minimise the effects on the sharks behaviour. Keywords: white shark, behaviour, learning, conditioning, chumming 1

2 INTRODUCTION Conditioning is defined as "a form of associative learning that occurs when changes in thought or emotion are produced by temporal relations among events" (Roberts 1997). Since all vertebrates and many invertebrates can be conditioned under the right circumstances (Roberts 1997), it is possible that white sharks can be conditioned to associate humans with food. Conditioning has been demonstrated in a number of fishes, including the guppy, Poecilia reticulata (Swaney et al. 2001), the blue gourami fish, Trichogaster trichopterus (Hollis et al. 1997), and the goldfish, Carassius auratus (Manteifel & Karelina 1996). Within a species, juveniles and sub-adult teleost fish tend to learn faster than adults and older fish (Wright & Jackson 1964). Individuals belonging to social or schooling species tend to learn faster than solitary migrants (Laland & Williams 1997). Conditioning has been demonstrated in a captive situation in the lemon shark, Negaprion brevirostris (Clark 1959, Aronson et al. 1967, Wright & Jackson 1964) and the bull shark, Carcharhinus leucas (Wright & Jackson 1964), with juveniles responding more readily to conditioning than adults of the same species. Some species of shark are capable of being conditioned to the same level as some mammals (Aronson et al. 1967). Aronson et al. (1967) showed that it is possible to condition a shark to respond to a stimulus in as little as 3-5 days, provided the shark received numerous rewards in this time whenever it shows the conditioned response. Chumming is sometimes perceived as being responsible for attracting sharks to an area and leading to development of behavioural patterns where sharks approach vessels with the expectation of being fed (Presser & Allen 1995). There is concern that individuals may become conditioned to associate the vessel, cages and/or divers with a food source, which could pose a serious concern for water users near the cage-diving operations. White sharks often display curiosity towards new objects in their environment, a behaviour that would be advantageous to this highly opportunistic predator in exploiting new resources of food (Collier et al. 1996). They are also capable of learning from experience and altering their behaviour accordingly (Goldman & Anderson 1999). Very little research has been conducted in this area of white shark behaviour. The conditioning of white sharks to the baited situation presented by the operator would involve classical and operant conditioning. The shark would generalize its response to approach a boat (conditioned stimulus) because it always accompanies the presentation of food (unconditioned stimulus) and the sharks being attracted and feeding (unconditioned response) a form of 2

3 learning, referred to as classical conditioning. The interest in boats will only be maintained if food is presented and feeding occurs repeatedly while the boat is present (operant conditioning). The following criteria for judging the potential conditioning effects of cage diving operations, based on and corroborated by other research into conditioning in elasmobranchs, were used in this study: 1. Aronson et al. (1967) showed that, even under optimal conditions in a captive situation, it took a minimum of 3-5 days with substantial rewards to produce a conditioned response in nurse sharks (Ginglymostoma cirratum). Therefore, if a shark is present for less than 3-5 days, conditioning is not considered to be possible. Thus, sharks making less than four visits/year to cage-dive sites probably cannot be conditioned at all. 2. The studies conducted by Clark (1959) and Aronson et al. (1967) concluded that conditioning would only occur when the conditioning stimulus was applied at regular intervals and at optimal times for conditioning success. Therefore, sharks making 5-10 visits to cage-dive sites/year probably cannot be conditioned if their visits are irregular, punctuated by long absences and they don't receive a substantial number of positive reinforcements on each visit. 3. Experiments have shown the conditioned response in other species in as little as 5 days (Aronson et al. 1967) when rewards are regular and substantial. Clark (1959) also found that lemon sharks being fed once a day, 5 times a week, learned the conditioned response within one week. Classical conditioning has also been demonstrated in the lemon shark in as little as eight days of training (Gruber & Schneiderman 1975). Assuming white sharks learn at a similar rate to the species in these experiments, conditioning could occur under these conditions. Thus, sharks making 5-10 visits to cage-dive sites over a short period of time (e.g. a few weeks) could be at high risk of conditioning, especially if they receive substantial rewards during this period. In this study, a short period of time was classified as a 30-day period. 4. In addition to the findings presented above by Clark (1959) and Aronson et al. (1967), instrumental conditioning experiments showed young lemon sharks (Negaprion brevirostris) to be conditioned to a stimulus in under 14 days, with just minutes of training each day (Wright & Jackson 1964). Fur- 3

4 thermore, Clark (1959) found that the conditioned response persisted after a 10 week period of inactivity. Therefore, sharks making more than 10 visits to cage-dive sites/year can potentially be conditioned and should be carefully monitored for signs of conditioning. The criteria described were based on findings from conditioning studies in other shark species. Although these criteria can be used as a guideline for white shark conditioning, they also assume optimal conditions for learning. While this is impossible under natural conditions, and it is dangerous to extrapolate the behaviour of white sharks based on other species, these guidelines are based on assumptions that err on the side of safety for evaluating the potential of conditioning. These include the inference that white sharks learn as fast as other elasmobranch species, and that there is no interference by conspecifics during feeding bouts. For the purposes of this study, it was assumed that, when sharks were not visible on a particular day, they were not present. This can be assumed here as sharks cannot be conditioned if they are not receiving rewards and hence can be discounted from the study on days when there is no interaction, even if they had not moved away from the islands altogether. This study aims to test the hypothesis that white sharks do not visit the islands frequently enough to become conditioned to the boat and baits. Therefore, it can be determined whether the natural movements and behaviour of white sharks in the area are being changed. MATERIALS AND METHODS Expeditions were conducted from April 2001 until February 2004, encompassing 27 expeditions over 140 days. The duration of each trip was between four and eleven days to the Neptune Islands, which lie at the mouth of the Spencer Gulf off Port Lincoln, South Australia. Shark densities were estimated based on attraction to bait. Sharks were attracted to the boat by means of a standardised baiting method (Strong et al. 1992). A threedimensional odour corridor was discharged consisting of known amounts of unrefined fish oil, minced tuna, tuna blood and seawater, delivered at a low rate. Baits of whole salmon or tuna chunks (weighing about 1kg) were attached to a natural fibre bait line approximately 15m in length and allowed to drift from the stern of the boat. Once a shark arrived and showed interest in the baits, the baits were drawn closer to the boat by crewmembers to allow tagging, identification and photography to take place. When bait was removed or eaten by a shark, it was replaced with fresh bait. However, whenever possible, baits were removed from the water away from the shark on approach to avoid the shark feeding from the vessel. 4

5 A number of factors were recorded during each day for each shark in the vicinity of the vessel. The times of arrival and departure for each individual were recorded, as were the minutes of contact time with the vessel, cages and divers. The numbers of visits (and hence repeat visits over the course of the years of the study) were recorded, as well were the intervals between the visits. In analyses, a visit was defined as one day of observation. Daily contact time was defined as the sum of all the periods during the visit that the shark spent in close proximity to the boat (approximately 20m radius) or made a series of investigative passes at the bait, cage or divers. The number of rewards received was classified as the number of times in which a shark succeeded in biting the bait, regardless of whether the bait was ingested or not. A shark was considered to have received a reward every time it managed to mouth the bait, irrespective of whether it actually removed and swallowed tissue since the taste of bait would still have constituted a reward. An attempt was defined as an oriented pursuit of a bait or other object, whether or not that attack was successful or unsuccessful. An approach was defined as a pass of the boat or cage that was not oriented towards the bait. The percentage success rate was defined as the number of rewards received as a percentage of the number of attempts performed. From these measures, sharks that fell into the categories outlined above were selected for further analyses. Pearson correlations and linear regressions were conducted to investigate relationships between the number of rewards received with the number of days on location and contact time. ANOVAs were executed to determine differences between successful and unsuccessful attempts to determine if sharks received more positive than negative rewards. From the sharks that were considered cause for concern, the sharks that were determined to be most at risk were analysed in detail. The changes in the success rate and behaviour of these individuals over time were closely examined to determine if the sharks were becoming habituated. The rationale behind this method was that, if these sharks had not become habituated to the baited situation, then it was highly likely that none of the other sharks in the study would be either, since they all received less contact and reinforcement. RESULTS Number of sharks fulfilling the criteria for conditioning Sharks that made less than four visits per year to the vessel were discounted from analyses, since it is unlikely that these individuals could be conditioned in such a short period of time (conditioning criteria 1). Of the 126 individuals observed during the course of this study, 53% were seen on only one day throughout the three years 5

6 Number of sharks whilst 85% were sighted on four days or less (Figure 1). In terms of visits per year, 85% of white sharks in 2001 were seen for less than five days, 73% in 2002 and 100% in Number of days observed Figure 1. Frequency of white shark visits to the Neptune Islands for all three years of the study combined (n = 126 sharks). Observation at 37 days represents shark I 2. When comparing the individuals in each of the years, only 12.7% of individuals visited the vessel on five or more days per year. 2.4% could be eliminated from the conditioning study since their visits were irregular (they were observed for less than 4 days in each year) and did not receive a great number of positive reinforcements during the times observed. To satisfy criteria 3, white sharks making 5-10 visits (observed on 5-10 days) in a 30-day period were considered. 10.3% of white sharks were observed for five days or more in a 30-day period; and of these, 1.6% were observed in multiple 30-day periods. Therefore, of the total number of sharks in the study, 10.3% of sharks (or 13 of the sharks in this study) were classified as making regular visits and, if substantial rewards were received, 6

7 Mean number of rewards per day could be at high risk of developing conditioned behaviours. Since conditioning data were not recorded in 2001, the number of rewards that sharks obtained in this period could not be analysed. However, data were available for 10 of the 13 individuals. The number of rewards received in any one day by the ten at risk sharks ranged from 2 to 46 baits, which varied in quality and quantity. There was a significant relationship between the mean number of rewards received per day and the number of days an individual was encountered (linear regression R² = 0.90, p = , Figure 2). The contact time was also highly related to the mean number of rewards received per day (linear regression R² = 0.72, p = , Figure 3). Thus, the longer that sharks were in the vicinity of the vessel, the more rewards they received, as would be expected since the baits were not manipulated to create individual bias in any way. The number of rewards received reflected the amount of time spent in contact with the baits. Therefore, in analyses, the mean number of rewards received per hour of contact time was considered in order to remove biases caused by increased contact times. For all sharks in the conditioning study, the number of rewards received per hour of contact time ranged from 0 to 16.3, with a mean of 4.33 (SE 0.816). The 75 th percentile for these data was 6.0. Sharks receiving more Number of days present Figure 2. Relationship between the number of days present and the mean number of rewards per day received by white sharks at the Neptune Islands (R² = 0.90, p = ). 7

8 Mean number of rewards per day Contact time (min) Figure 3. Relationship between contact time (number of minutes observed around vessel) and the mean number of rewards received per day by white sharks at the Neptune Islands (R² = 0.72, p = ). than the 75 th percentile of 6.0 baits were defined as receiving substantial rewards. The number of rewards received per hour of contact time for the ten sharks pinpointed in at risk categories ranged from 0.9 to 8.39, with a mean of 5.16 (SE 0.66). Of the 10 white sharks being considered (7.9% of the total in the study), four sharks (40%) obtained more than 6.0 rewards per hour and therefore were classified as having received substantial rewards during the time in which they were observed. These four individuals therefore, were classified as being at high risk of being conditioned to the baited conditions. The final criteria stated that sharks making more than 10 visits to the vessel per year would be at high conditioning risk. Over the 3-year study, 3.2% of sharks fell into this category. Of these individuals, 1.6% were seen in two or more consecutive years. Therefore, 3.2% of sharks made 10 or more visits per year to the site, and 3.2% of sharks received substantial rewards in a short time interval. Of these two groups, 1.6% of sharks fell into both categories, leaving 4.7% of white sharks in total (six individuals) that would require monitoring for signs of conditioning when favourable circumstances existed (Table I). 8

9 Table I: Conditioning data for the white sharks considered to be at risk of habituation (n = 6 sharks). Shark ID Number of rewards received Number of days present Contact time (min) Rewards received per hour % success Archie I I I Ted Ratio of success to failure at attaining rewards For the six sharks outlined as at risk of conditioning, the staying time (time period they remained in the vicinity of the vessel) ranged from 1 to 585 minutes, with a mean of minutes per shark. However, the actual contact time involving direct interaction between the white shark and humans, bait or cages ranged from 1 to 30 minutes, with a mean of 9.94 minutes per shark. A total of 956 attempts to obtain baits were made by these sharks, with them collectively receiving a total of 237 rewards, resulting in one reward for every 4.03 passes (or a 40% success rate). It should be noted that the data may be somewhat biased since identification of individuals sometimes relied on scars or markings that could have faded or disappeared over time. The number of sharks that re -visited the area after long absences were therefore probably underestimated. Therefore, findings cited here are conservative. DISCUSSION The effect of chumming on shark behaviour and movements Less than 5% of sharks were seen to be at risk of conditioning, hence there was not a significant effect of chumming on shark behaviour. The majority of sharks were observed on one day only, despite the continued presence of chum. If white sharks had been conditioned to associate a vessel with a food source, it would be likely that they would remain in the vicinity of the vessel to exploit the food source for as long as it was available. A study into residency patterns at the Neptune Islands found that chumming days did not have a higher 9

10 number of white sharks present than non-chumming days (Bruce & Stevens 2003), and there was no evidence to suggest that white sharks remained in the area for longer periods during operator presence than they would otherwise. Over 50% of the white sharks in this study were seen on one day only, with 85% being observed for less than five days, and so they were excluded from the conditioning analyses. The large percentage of white sharks visiting for short periods at the Neptune Islands indicated that the majority of the individuals observed were transient, possibly due to competitive exclusion by the small semi-resident population that exists seasonally at the islands (Bruce & Stevens 2003). Since larger sharks were more successful at obtaining baits than smaller sharks, they may have been more susceptible to conditioning. Experience gained during natural predation by mature sharks may have resulted them being more adept at hunting than sub-adults, which would have only recently switched to hunting surfacedwelling seals as opposed to teleosts (Ainley et al. 1981, Casey & Pratt 1985, Malcolm et al. 2001). The occurrence of size-dependent hierarchies (Strong et al. 1992) would serve to further enhance the success of larger sharks. Sharks at high conditioning risk If sharks visited the vessel in a manner that was not influenced by the chumming operation, then a Poisson distribution would be expected. In general, this appeared to be the case, but peaks towards the end of the distribution curve (Figure 1) showed that some sharks no longer conformed to the behavioural patterns exhibited by the rest of the white sharks in the area. Six sharks were classified as being at high risk of conditioning and four sharks were classified as having received substantial rewards during the time in which they were observed. These substantial rewards may have been received during periods of reduced human vigilance, but it is more likely that these sharks were more adept at successfully pursuing baits than other sharks in the area. Signs of conditioning were evident in some individuals, particularly in those that were known to be frequent seasonal visitors. For example, when attacking baits, the reflexive eye-rolling behaviour was not exhibited by these individuals which, speculatively, could indicate that they had learnt that there was no need to protect the eye from the defensive blows of prey. The nictitating membrane response in lemon sharks has been able to be classically conditioned, with conditioning levels similar to those found in rabbits (Gruber & Schneiderman 10

11 1975). However, quantitative research would need to be conducted to confirm this observed behaviour, and this behaviour has also been exhibited in a non-baited environment when feeding on natural prey (Klimley personal communication). Conditioning to the baited situation does not necessarily equate to an association of divers with food by the sharks, and this association would be difficult to test on wild individuals (and in general since white sharks do not generally survive for long in captivity). Nevertheless, the fact that this species can become conditioned to the baited conditions leads to the inference that this species could form an association when the correct conditions are met. As the duration of visitation of white sharks cannot be controlled, it needs to be ensured that sharks do not receive substantial rewards when encountered, and, if possible, rewards should be withheld whenever possible. If the conditioned reflex is not maintained by regular positive reinforcement, it retards and is eventually lost altogether (Roberts 1997). So, withholding baits altogether from a previously conditioned animal would cause frustration and soon result in total extinction of the conditioned reflex. Despite the lack of statistical significance the conditioning effect demonstrated in this study, feeding of white sharks should be minimised and closely controlled. CONCLUSIONS For the majority of the white sharks encountered at the Neptune Islands, visits were too irregular or short-lived, or rewards were insufficient, for conditioning of sharks to the vessel, cage and/or divers to occur. In a small percentage of individuals however, the correct criteria were met to put them at a higher conditioning risk, and conditioning to the baited conditions were observed in some animals. ACKNOWLEDGEMENTS I thank P.A.D.I. Project A.W.A.R.E for partial funding of the project, R.Fox and A.Fox whom supplied the research platform. Also D. Booth and B.Bruce for guidance and assistance in the review of the paper. 11

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