Friday, December 24, 2010

The Shark Feeding Paper!

Here it is – finally!
This is now the published paper about Aleks’ work with the Caribbean Reefs.

Here she is talking to David, courtesy of SFS.

From the paper (highlights are mine).

Effects of tourism-related provisioning on the trophic signatures and movement patterns of an apex predator, the Caribbean reef shark

Aleksandra Maljković and Isabelle M. Côté

Department of Biological Sciences, Simon Fraser University, Burnaby, BC, Canada
Received 26 May 2010; revised 2 November 2010; accepted 28 November 2010.
Available online 18 December 2010.


Wildlife provisioning, i.e. the provision of bait to generate aggregations of charismatic megafauna as tourist attractions, occurs around the world.
This practice is often promoted as an economic incentive to conserve the focal species, yet has stimulated debate based on the potential for risks to human safety and perceptions of behavioural shifts in provisioned populations. We studied a population of Caribbean reef sharks (Carcharhinus perezi) in the Bahamas that has been subject to regular provisioning for >20 years.

We used a combination of focal observations of sharks during feeding events, remote acoustic telemetry and stable isotope analysis of shark muscle tissue to determine the impacts of provisioning on the trophic signatures and ranging behaviour of sharks in this population.
A small number of large sharks monopolised more than 50% of the bait on offer. These ‘fed’ individuals showed significant 15N enrichment in their tissues compared to conspecifics of the same size that failed to obtain bait at the feeding site, and un-provisioned sharks from a control site.

Despite the disparity in trophic signatures, fed, unfed and control sharks exhibited similar degrees of residency at their respective home receiver sites, and travelled similar daily minimum distances.
Thus, despite long-term provisioning of this Caribbean reef shark population, there is no evidence for shifts in the behaviours considered which might affect the ecological role of these sharks.

However, further research is required to examine potential indirect effects of shark provisioning on sympatric fauna and habitat before this activity can be placed within a sustainable marine conservation framework.

1. Introduction

Provisioning wildlife, as a means of enhancing nature-based tourism experiences, is a hotly debated issue (Newsome and Rodger, 2008) which becomes most controversial when involving the feeding of large predatory species (Burns and Howard, 2003; Perrine, 1989).
In these cases, human safety issues are usually at the forefront of the debate, with opponents of the practice claiming the potential for predators to learn to associate human presence and food rewards, and proponents citing a lack of empirical documentation of such links (Orams, 2002). Concerns have also been raised about impacts on the provisioned animals themselves, which have only begun to be empirically examined. Regular provisioning of various predators has been shown to lead to increased population densities and interference competition (Semeniuk and Rothley, 2008), increased frequency and duration of aggressive behaviours (Hodgson et al., 2004; Hsu et al., 2009), impoverished body condition and physiological indications of impaired health (Semeniuk and Rothley, 2009).

Shark-viewing tourism is the epitome of this controversy.
At over 40% of the 267 globally-distributed shark viewing sites detailed by Carwardine and Watterson (2002), some form of attractant (chum or decoys) or bait is used to increase encounter rates and keep the focal species within viewing distance of paying clients. Yet due to the longstanding difficulties associated with studying large marine predators, the basic ecology of most of these shark species, let alone their responses to provisioning, remains undocumented. Nevertheless, the full spectrum of arguments both for and against the practice of shark feeding has been discussed in several recent papers (Johnson and Kock, 2006; Laroche et al., 2007; Meyer et al., 2009).

The contentious nature of shark provisioning has prompted legislation abolishing the practice in several areas of the world, including Florida, Hawaii, the Cayman Islands and South Africa (Carwardine and Watterson, 2002), with mounting pressure for the activity to be banned in others regions (Topelko and Dearden, 2005).
However, the popularity of shark dives, and subsequent success of many shark encounter operations, now makes this activity a valuable source of revenue, particularly in countries that depend on tourism as a major source of foreign earnings (Green and Higgenbottom, 2000; Topelko and Dearden, 2005).

For example, an analysis of the economic impact of shark-related tourism in the Bahamas revealed that in 2007, operators facilitated more than 72 500 shark encounters, generating an estimated $ 78 207 338 input to the economy when all local services used by shark dive clients were considered (W. Cline, Cline Marketing Group, unpublished data).

The strong economic incentive to maintain, or even promote, shark-related tourism may therefore outweigh the perceived negative effects of this activity on sharks, particularly in light of the absence of strong evidence showing such effects.
Because a substantial part of the debate surrounding shark feeding centres on perceived shifts in the behaviour of sharks in response to provisioning (Guttridge et al., 2009), the aim of our study was to quantify the effects of tourism-related provisioning on the trophic signatures and movement patterns of sharks, i.e. factors for which data may be reliably collected and which are expected to reflect direct impacts of supplemental feeding.

We focused on Caribbean reef sharks (Carcharhinus perezi), which are frequently the focal species at shark dive sites in the Bahamas.
The relative abundance of this shark in accessible coral reef ecosystems of the tropical Western Atlantic makes it an ideal model system to examine the impacts of provisioning on apex predators. Specifically, we compared patterns of site fidelity, daily distances travelled and 15N-based trophic signatures of provisioned sharks with those of un-provisioned conspecifics to elucidate the effects of shark feeding on this species.

Our study provides data that are currently missing from attempts to weigh the benefits and disadvantages of wildlife provisioning.
Such information is essential to assess whether provisioning practices can be included in portfolios of management strategies that enhance apex predator conservation awareness and revenues while not conflicting with other preservation goals.

2. Methods

2.5. Data analysis

We categorised individual sharks as ‘fed’ or ‘unfed’ based on bait consumption (see Section 3.1). Fed sharks were those consuming 3% or more of the bait (n = 11 individuals), and unfed sharks were those consuming 1% or less (n = 37 individuals).
These cut-off values represented a natural break in the bait acquisition data (see Fig. 2a). To account for the possible effects of sex- or size-based differences on Caribbean reef shark behaviour, we restricted our analyses of trophic signatures and movement patterns
to female sharks (i.e. the most abundant gender) of more than 180 cm TL, with the stipulation that these individuals had to have attended at least 50% of the focal shark feeding events.

In addition, we included a control group of 10 Caribbean reef sharks to test whether the shark feeding activity per se influenced movement patterns and trophic signatures regardless of any bait consumption effect.
Sharks in the control group were all females of more than 180 cm TL and, as determined using acoustic telemetry, resided mainly near receiver C (Fig. 1), approximately 4.6 km from the shark feeding site. Eight of the sharks in the control group were sighted at shark feeds over the course of the study, but they attended very infrequently (ntotal = 51 sightings; or 0.4 ± 0.03 sightings per shark per month) and none took any of the bait on offer.

3. Results

3.1. Shark presence and behaviour at shark feeding dives

Between 24 May 2007 and 13 February 2009, 97 individual Caribbean reef sharks were identified during 293 shark feeding dives, i.e. 48% of all shark dives conducted during this period.
Of these sharks, 56 were externally tagged to aid identification. Sharks ranged in size from 90 to 280 cm TL (mean ± SD: 160 ± 35 cm), and the sex ratio was strongly female-biased (1:6.5). Overall, the number of sharks present at each feeding dive varied between seven and 55 individuals (mean ± SD: 34 ± 9 sharks), and individual sighting frequency varied widely (mean ± SD: 127 ± 84 sightings, range: 1–261 sightings, or 0.3–89% of feeding events surveyed).

Eleven sharks (11% of all individuals recorded; 2 males, 9 females) took over 50% of the bait on offer (ntotal = 3792 pieces), with no other single shark consuming more than 2% of the remainder.
The sharks eating the majority of the bait were significantly larger (mean ± SD: 198.18 ± 26.0 cm) than the remainder of the study population (155.47 ± 33.42 cm; independent t-test: t95 = 4.08, P < 28 =" 0.76," p =" 0.48;" 26 =" 2.26," p =" 0.12)," 26 =" 2.51," p =" 0.13;" 26 =" 0.98," p =" 0.39)." 28 =" 1.09," p =" 0.35;">

4. Discussion

Substantial tourism industries have developed around the world, which are centered on charismatic predatory species.
While such industries can provide an economic stimulus favouring the non-consumptive exploitation of the focal species, the cryptic nature and low abundance of most predators often necessitates the use of bait to generate larger aggregations and satisfactory viewing opportunities for tourists (Laroche et al., 2007).

The impacts of provisioning for wildlife viewing purposes are generally poorly known (Orams, 2002), and this is particularly true for marine predators such as sharks.
We examined the direct effects of provisioning on the behaviour of an inshore population of Caribbean reef sharks. We found that although a large number of sharks attended feeding events, a very small proportion of sharks acquired bait regularly. Bait consumption resulted in an elevated 15N signature of fed sharks relative to unfed and control sharks, but there was no statistically detectable variation in the extent of movement of individuals across groups.

Our results therefore suggest that the impacts of long-term, regular provisioning on this shark population may be limited, at least in terms of the parameters examined here.

4.1. Shark presence and behaviour at shark feeding dives

Attendance at feeding events varied widely among individual sharks.
Some of this variation, at a seasonal scale, is attributable to reproductive activity. A mass departure of near-term gravid females, followed quickly by many other females, occurred throughout June. None of the returning sharks, the majority of which reappeared at the feeding site in July, was visibly pregnant and most individuals exhibited extensive scars, usually obtained as a result of mating (Pratt and Carrier, 2001). However, some of the variation in daily individual attendance at feeding events also stems from differences in patterns of residency. Some sharks exhibited a strong degree of fidelity to the feeding area, but many sharks arrived at the site opportunistically, perhaps as a result of attraction to the bait or to the aggregation of conspecifics.

The proportion of Caribbean reef sharks successfully acquiring food rewards at shark feeds was very small.
Although this pattern has also been noted in studies of white shark provisioning (Johnson and Kock, 2006; Laroche et al., 2007), it seems surprising here given the larger numbers and tighter spatial aggregation of Caribbean reef sharks at feeding events. Close proximity potentially created the opportunity for multiple individuals to successfully compete for the proffered bait. The fact that only a few large sharks were repeatedly effective at taking the majority of bait suggests that in Caribbean reef sharks, as in many other shark species (Allee and Dickinson, 1954; Bres, 1993), social hierarchies exist in which larger sharks are dominant in competitive situations.

4.3. Residency and movement

Previous studies of animals subject to regular provisioning have shown marked changes in space use and movement of provisioned animals, including increases in the time spent at the site where food is provided and when it is provided (Hodgson et al., 2004; Milazzo et al., 2005; Newsome et al., 2004; Walpole, 2001).
Neither shift was evident in our study population. All sharks with transmitters spent a high proportion of their time near a single receiver, regardless of feeding status. Thus, overall, fed sharks did not spend more time at the provisioning site than unsuccessful individuals. In addition, fidelity to a single receiver was evident across the day. Fed, unfed and control group sharks in our study were detected at their respective home receiver sites equally during the morning and afternoon indicating that the regular acquisition of food, or even the potential to acquire food, does not influence the residency patterns of these sharks. Provisioning also did not appear to affect the extent of movement away from home receivers. All sharks travelled similar daily minimum distances suggesting that successful acquisition of bait did not lead to smaller foraging ranges.

Overall, both fed and unfed sharks in our study population exhibited movement patterns that were consistent with previous studies of habitat use in Caribbean reef sharks, which have shown that larger individuals (>110 cm TL) prefer ocean reef habitats near drop-offs (Pikitch et al., 2005) and exhibit site fidelity, but also make wide-ranging lateral (_50 km) and vertical movements (Chapman et al., 2005, 2007).

In light of the small estimated contribution of bait to the overall energetic budget of the majority of sharks, it is not surprising that shark movement patterns appear to be largely unaffected by provisioning.
However, our analyses were restricted to a specific subset of sharks (i.e. females > 180 cm TL) whose behaviour may not be representative of the population as a whole. Future telemetry studies should include a broader range of shark size classes and use active, rather than passive, monitoring to obtain more accurate estimates of daily space use.

Previous studies of the movement patterns of marine fish in response to provisioning have yielded conflicting results.
Fish abundance – the most commonly reported proxy for movement – is often higher at feeding sites than at control sites, or during feeding than at other times (Ilarri et al., 2008; Medeiros et al., 2007; Milazzo et al., 2005; Newsome et al., 2004; Semeniuk and Rothley, 2008), but this effect is highly variable among species.

Many taxa, in both tropical and temperate locations, show no change in abundance or biomass as a result of provisioning (e.g. Cole, 1994; Hawkins et al., 1999; Milazzo et al., 2005).
However, the lack of individual identification in these studies makes changes in individual movement impossible to measure. The most comparable study to our own is a telemetry study of provisioned and un-provisioned stingrays (Dasyatis americana) in the Cayman Islands. In contrast to our results, Corcoran (2006) found that stingrays, which are normally solitary foragers with large home ranges, showed strong site fidelity to the provisioning area and reduced activity, which resulted in aggregation. The lack of consensus among fish provisioning studies perhaps reflect differences in, for example, home range sizes, habitat associations, habituation thresholds or tolerance levels of the species at provisioning sites to repeated disturbances.

5. Conclusion: Provisioning as a tool for conservation management of apex predators

The development of effective conservation strategies for apex predators is a pivotal step in the movement towards ecosystembased environmental management (Pikitch et al., 2004; Wallach et al. 2010).
However, large and usually highly vagile predatory species pose a specific set of conservation challenges. For example, their home ranges frequently exceed the boundaries of protected areas (Chapman et al., 2005; Woodroffe and Ginsberg, 1998), increasing the likelihood of negative human-wildlife encounters and susceptibility to hunting or capture.

Given that economic factors play a fundamental role in driving the consumptive exploitation of many apex predators, both on land and in the sea, the key to reducing, or even reversing, population declines may therefore lie in raising the economic value of non-consumptive forms of exploitation.
Our study of Caribbean reef sharks – one of the most abundant apex predators remaining in the Caribbean – suggests that provisioning does not necessarily influence animal behaviour in detrimental ways (Orams, 2002). Because of this, we believe that provisioning, when carefully conducted, has the potential to be an effective strategy that can contribute to apex predator conservation.

Provisioning-based tourism, when accompanied by natural history information, can enhance public awareness of the conservation plight of apex predator populations (Carwardine and Watterson, 2002; Topelko and Dearden, 2005).
Moreover, wildlife-viewing tourism is an expanding and lucrative industry, which suggests good potential for shifting the relative economic gains from extractive to non-consumptive exploitation of apex predators (Clarke et al., 2006; Johnson and Kock, 2006; Meyer et al. 2009; Topelko and Dearden, 2005).

On a cautionary note, our conclusions may not necessarily be extrapolated to other provisioned species – either marine or terrestrial – owing to the potential effects of species-specific responses and differences in provisioning modes.
There may also be indirect effects of provisioning which were not considered here. For sharks, these include increases in diver-sustained damage to habitats at provisioning sites, as well as potential cascading effects of marked local increases in predator abundance.

However, healthy populations of apex predators have been shown to have positive impacts on biodiversity at lower trophic levels (Sergio et al. 2005), thus conservation of these species may deliver wider ecosystem-level benefits.
There is a clear need for further ecological research, coupled with studies of the socio-economic benefits of provisioning-related tourism, before this activity can be safely incorporated within a sustainable-use framework for conservation management of apex predators.

This is just great work, bravo!
I obviously like it because it proves, at least for this population of Caribbean Reefs at this specific feeding site with its specific procedures, that the provisioning has no notable effect on how the Sharks utilize their habitat, meaning that it dispels the myth that feeding Sharks harms the animals.
Bravo also to Stuart Cove who facilitated this!

I also like it because it’s so nifty.
Segregating different sub-groups based on their feeding and attendance patterns, and creating a control group in the process is very smart indeed! If you remember, the lack of control group was one of my principal reservations about the Clua paper on Lemons - and here, we’re being shown a smart way of obtaining that very result through careful observation and lateral thinking! Incidentally, I’m not the only one who took exception to some of the findings in the Lemon paper: some fellow Shark researchers have raised similar concerns, resulting in an interesting discussion – keep watching this space.

Finally, bravo for the caveat!
Indeed, the conclusions may not necessarily be extrapolated to other provisioned species – either marine or terrestrial – owing to the potential effects of species-specific responses and differences in provisioning modes! I really cannot agree more – especially considering the stupid reverse statements about feeding The Wildlife in general and Bears in particular that continue to haunt us!

Still, I do find plenty of similarities to our dive here in Fiji.
In view of the totally different species, I did not expect this and find it totally fascinating! We, too, have periods when the pregnant females leave, shortly followed by most other animals, male and female. We, too, observe different levels of residency, meaning that we have “regulars”, ‘strays” and individuals (e.g. Long John and Valerie) that only turn up during specific periods that appear unrelated to any sexual activity.

Also, we too know that specific individuals nearly always feed when present, whilst other regulars never do – although I could not confirm that successful feeding is liked to size in females. To me, rather than being hierarchical, it really appears to be an individual inclination.
My gut here is that contrary to Reefs where many species aggregate, maybe in family groups, Bulls are rather solitary and that as a consequence, their social etiquette is just not very pronounced – think Polar Bears in Churchill, Ontario. I just cannot see any advantage for such large Sharks to live in groups in a reef habitat where food does not come in large packages. This is contrary to the open ocean with its sporadic big schools of Fishes and Cephalopods where some form of cooperative hunting requiring a more pronounced social etiquette would likely facilitate predation.

Yes, I’m speculating as usual!
The good news being that Juerg is presently working his way through our gargantuan database and the results of years of acoustic tagging – so finally, we will be able to progress from observations, personal speculation and daring (and probably rather stupid) hypotheses by yours truly to proper peer reviewed conclusions!
Can’t wait!


BeachNomad said...

Read over the abstract and seems like a great piece of work. I'll read over it again after Christmas and give you some thoughts!

And Mike, as my advisor loves to remind any student who says that they "proved something" researchers never prove anything they just provide support for an idea :)

Merry Christmas!!


DaShark said...

Duly noted! :)

Full PdF on its way - you, too, MerryHappy!