Thursday, September 23, 2010

About feeding Lemons in Moorea

Well well.

May Monsieur Mourier have an agenda?
Check out his pre-emptive statements about Shark feeding here.

Then, compare to excerpts of this new paper he has co-authored.

Behavioural response of the sicklefin lemon shark Negaprion acutidens to underwater feeding for ecotourism purposes
Eric Clua*, Nicolas Buray, Pierre Legendre, Johann Mourier, Serge Planes

ABSTRACT: The feeding of marine predators is a popular means by which tourists and tour operators can facilitate close observation and interaction with wildlife.
Shark-feeding has become the most developed one around the world in spite of its controversial nature. Amongst other detrimental effects, the long-term aggregation of sharks can modify the natural behaviour of the animals, potentially increase their aggression toward humans, and favour inbreeding. During 949 diving surveys conducted over 44 months, we investigated the ecology and residence patterns of 36 photo-identified adult sicklefin lemon sharks (Negaprion acutidens). The group contained 20 females and 16 males. From this long-term survey, we identified 5 different behavioural groups that we described as “new sharks” (7), “missing sharks” (4), “resident sharks” (13), “unpredictable sharks” (5) and “ghost sharks” (7). In spite of in-and-out movements of some males and females, probably related to mating, the general trend is that residency significantly increased during the study, particularly in males, showing a risk of inbreeding due to the reduction of shark mobility. Intra and inter-specific aggression was also witnessed, leading to an increased risk of potentially severe bites on humans. Our findings suggest the need for a revision of the legal framework of the provisioning activity in French Polynesia, which could include a yearly closure period to decrease shark behavioural modifications due to long-term shark-feeding activities.

From the paper


Large predators, which are potentially dangerous to humans and often feared, account for a substantial proportion of ecotourism activities based on animal sightings.
However, because of their generally elusive nature and locally low population densities, such predators are often difficult to observe. Sharks are shy animals (Bres 1993), and provisioning is necessary to produce reliable and impressive aggregations of animals. The last decade has seen tremendous development of ecotourism based on the sighting of top marine predators (Orams 2002, Topelko & Dearden 2005). The practice of shark-feeding is widespread throughout the tropical and subtropical seas of the world, e.g. in the Bahamas, Fiji, South Africa, Australia and French Polynesia, and it is becoming controversial, with little consensus about how it should be managed.

Deliberate and long-term shark-feeding is suspected to generate problems for both animals and humans (Dobson 2006, Newsome & Rodger 2008).
It may alter the natural behavioural patterns of sharks, generating biological (for the animal themselves) and ecological (for the ecosystem) effects. Provisioning may cause habituation to human contact and increase aggression towards humans by associating divers with food (Burgess 1998, Orams 2002). However, feeding wildlife can be a positive tool for assisting in the conservation of vulnerable and endangered species, through attaching economic value to wildlife and educating tourists about the need for conservation (Bookbinder et al. 1998, Halpenny 2003); it can also increase the probability of a shark encountering a partner as a result of aggregation (Orams 2002).

Despite the controversy, few, if any, comprehensive reports have measured the impact of shark-feeding, which is now widespread and growing around the world.

To date, studies have been conducted on the effect of chumming on white shark Carcharodon carcharias in South Africa (Johnson & Kock 2006, Laroche et al. 2007), as well as sandbar Carcharhinus plumbeus and Galapagos C. galapagensis sharks in Hawaii (Meyer et al. 2009).
These studies all concluded that moderate levels of provisioning of cage-diving ecotourism probably had a minor impact on the behaviour of the sharks and no risk of increased attacks on humans in adjacent areas.

In South Africa, Johnson & Kock (2006) showed that conditioning only arises if white sharks gain significant and predictable food rewards, which only happens if operators contravene permit regulations prohibiting intentional feeding of sharks.
White sharks are lured to the boat with baits (typically, mashed sardines and fish oil; Laroche et al. 2007) that are significantly different from their usual prey in the area, Cape fur seals Arctocephalus pusillus pusillus (Ferreira & Ferreira 1996).

In Hawaii, Meyer et al. (2009) showed that cage-diving activities did not increase the number of attacks on humans, probably due to the fact that the shark tours use a small amount of fish scraps, mimicking the activities of crab fishing vessels which have been operating in the same area for over 40 yr.
In both cases, while some food is used to attract sharks to the cages for observation and photography, the quantities involved are small, so this activity cannot be considered as real ‘provisioning’.

Light baiting is also used at Aliwal Shoal (South Africa) for attracting tiger sharks Galeocerdo cuvier and allowing encounters with snorkelers in open water (Dicken & Hosking 2009).

However, the available scientific data focus on the economic value of the recreational activity, and do not address its effects on the behaviour of these potentially dangerous sharks (ISAF 2010).
Bull sharks Carcharhinus leucas, another dangerous species (ISAF 2010), have been attracted to an ecotourism site in Beqa (Fiji Islands) since 2002 through a real feeding and conditioning process based on the release of several tuna heads during each dive (E. Clua pers. obs.); here again, however, the only data provided are socio-economic (Brunnschweiler 2010), with no reference to the biological issues of provisioning of carnivorous animals.

Given the controversial nature of shark-feeding, there is a critical need for empirical studies that focus on potentially dangerous sharks, and address both the potential disruption of their natural behaviour, which underpins their resilience, and the increasing risk of fatal attacks on humans (Garrod & Wilson 2006).

In French Polynesia, sharks are fed daily during diving activities. The main species involved, the sicklefin lemon shark Negaprion acutidens, can reach over 3 m in length and is considered to be potentially dangerous to humans (Maillaud & Van Grevelynghe 2005, ISAF 2010). This coastal shark is widely distributed in the Indo-Pacific, from Eastern Africa to French Polynesia. However, very little is known about the ecology of the sicklefin lemon shark in the Central Pacific. Despite its commercial value (Compagno 1984), only a few studies have been conducted in the Indian Ocean (Stevens 1984) and in Western Australia (White et al. 2004) besides a recent global genetic study (Schultz et al. 2008). The ecology of its sister species, the Atlantic lemon shark N. brevirostris, has been well documented during past decades (Gruber 1982, Chapman et al. 2009), mostly in the central Western Atlantic Ocean. However, while its early life has been extensively studied (Morrissey & Gruber 1993, DiBattista et al. 2007), very little is known about the adult stages of N. brevirostris and even less about N. acutidens.

Moorea Island (French Polynesia) is among the few locations worldwide where it is possible and feasible to have daily encounters with several wild adult sicklefin lemon sharks in their natural environment.

This characteristic provided us with an opportunity to investigate the behaviour and residency pattern of an adult population of this reef shark species through daily underwater observations at a provisioning tourism location. Here, we describe the population size and structure of this species, aggregated for ecotourism purposes at a site on the northern outer reef of Moorea Island. We divided the population into co-occurrence groups and describe the residence patterns and behaviour of these groups. We also tested the hypothesis that shark-feeding increases the fidelity of lemon sharks to the site, and discuss the potential long-term effects on population resilience and behaviour, including the risk of increased interactions with humans.

From the


…. Assuming similarity in the natural behaviour of these 2 sister species (Editor: Common and Sicklefin Lemon Sharks), our findings could be linked to an aggregating effect of shark-feeding, which decreases the mobility of animals, mainly the males, and may contribute to increased inbreeding.
This trend may lead to long-term loss of genetic variability in the Polynesian lemon shark populations, even though natural philopatry in N. acutidens, which would have been a detrimental factor, seems to be low (Schultz et al. 2008).

Increasing residency was a general trend for the shark population.
For all groups except Group B, which was composed of animals that disappeared, the linear regressions had positive slopes (Fig. 4), indicating an increase in shark abundance over time, and their site fidelity increased over the 44 mo, particularly for the ‘resident’ subgroups, C1 and C2 (Table 1). This means that, despite some sharks leaving and others
arriving, the number of days with sharks present and the number of sharks at the site both increased. This trend is explained by the increased attraction of sharks by provisioning, suggesting that learning plays a strong role in optimising their food search (Guttridge et al. 2009). Our findings are consistent with similar situations where other elasmobranchs (rays) learned to associate specific locations with food rewards, with detrimental effects on their behaviour, and indirect effects on the surrounding marine ecosystems, leading to the concept of an ‘ecological trap’ (Corcoran 2006, Gaspar et al. 2008, Semeniuk & Rothley 2008).

In the case of lemon sharks, their increased site fidelity can have a negative effect on gene flow, as mentioned previously, and can also affect their role as top predators in the area, as shown for top terrestrial predators such as dragons Varanus komodoensis in the Komodo National Park, where provisioning was eventually banned (Walpole 2001).

Among the negative effects, we observed intraspecific interactions generated by the provision of a limited amount of food.

Not all sharks present during a dive acquired food, and this resulted in exacerbated competition among the animals. This pattern can lead to increasing the number of intraspecific dominance actions and the aggression of sharks to acquire food (Ritter 2001), as shown for rays (Semeniuk & Rothley 2008). Dominance is often driven by the size (length) of the sharks in social groups (Allee & Dickinson 1954, Myrberg & Gruber 1974). During several feeding sessions, the largest resident male, M04, appeared to be the most inquisitive, approaching the divers closer than any other individual did. Since males M07 and M18 were dominant in 2005, M04 definitely acquired increasing dominance behaviour with respect to other individuals, which turned into deliberate aggression towards other males when several of them were present.
As was previously observed in 2005 for its 2 predecessors, from 2006 onwards M04 often arrived in the morning with fresh scars or notches that can be attributed to intraspecific fights (N. Buray pers. obs.). Aggression increased significantly when resident males came back to the feeding site after the mating period, probably in the context of a reorganisation of the hierarchy, as shown by serious wounds on males that were quite different in their severity and locations from those inflicted on females during mating (Fig. 5).

In natural conditions, sicklefin lemon sharks cannot be considered a gregarious species (Stevens 1984), except during the mating period, and animals usually feed separately.
Therefore, intraspecific aggression linked to the feeding process, even though natural among carnivorous animals, can be interpreted as deviant behaviour, exacerbated by human activity.Although managers may consider this process of increasing intraspecific aggression to be acceptable among sharks, it represents a real issue regarding the safety of divers for whom the risk of accidental bites has increased critically (Burgess 1998). Between 1979 and 2001, 47% of shark bites in French Polynesia were experienced in the context of shark-feeding activities (Maillaud & Van Grevelynghe 2005). Although anecdotal, this was confirmed by a serious bite by shark M04 on the left hand, which was not holding any food, of the diver doing the feeding in January 2006 (N. Buray pers. obs.).

The results of this study indicate that in spite of the provisioning activity, several male and female sicklefin sharks seem to have left the study site while others came back to it for mating.
This positive aspect from the perspective of maintaining gene flow between this shark population and adjacent ones is mitigated by the increasing pattern of residency for the overall population during the study. At present, the population seems to be a balanced mix of resident and non-resident individuals, which favours population mixing. However, if the resident sharks increase their numbers and their attachment to the feeding site, group living can generate costs for animals which are normally solitary foragers, such as injuries, predation, increased stress hormone levels and exposure to parasites due to increased transmission rates between individuals (Semeniuk & Rothley 2008).If supplemental feeding can be perceived as an artificial support to sharks by providing easy-to-access resources (Milazzo et al. 2006, Laroche et al. 2007), and can allow increasing energy allocation to other fitness-related activities such as rest and reproduction (Orams 2002), long-term unnatural aggregation can also have long-term fitness consequences for the population.
Because the studied population is small, daily aggregations at the same location could result in increased social interactions and increased mating between close relatives, reinforcing the risk of inbreeding. As lemon sharks are known for their polyandry (Feldheim et al. 2004), the potential negative effect on gene flow linked to the increasing residency pattern might be buffered by the multiple paternity process; this needs to be thoroughly monitored.

This factor, added to the development of aggression and incremental risk of accidental bites to divers, should lead managers to seriously consider a revision of the regulations on shark-feeding in French Polynesia in order to reduce these risks. An annual cessation of the feeding activity for several months, preferably encompassing the mating period, is an obvious solution. Whereas our study allowed us to draw these preliminary conclusions, additional field investigations are required to better understand the long-term effects of provisioning on shark populations.
Further work may also enable us to better understand the risks induced by feeding predators.

Quick ‘n dirty assessment: interesting - but both prejudiced and highly speculative!

But first things first: this is what I like.
Scientists are finally discovering the Shark feeding industry and publishing a first set of baseline studies, of which this is a (I believe: rather poor) example. And although I do not concur with the conclusions, see below, I do commend the authors for having taken the time to compile and analyze a long term set of data. As the always brilliant CJA Bradshaw remarks, monitoring has long been the ugly cousin of the fashionable experimenting and is only now being recognized as an invaluable tool for trying to decipher complex systems where causal relationships are not immediate and thus difficult to manipulate selectively.

Which brings me straight to my principal critique.
Where is the control group, as in a comparable group of Lemons that are not being fed? If they got nothing to compare them to: how can the authors postulate that any of the described phenomena are caused directly by the human interference and not due to chance variability, or to natural fluctuations in population, or to climate fluctuations like ENSO or the like?

But let’s quickly examine the allegations.

The observed increased residency may lead to reduced gene flow and inbreeding.
Indeed, maybe! But many Shark species, among which Lemons, do wander off during mating season and indeed, so did the studied animals! The increased residency during the remainder of the year is utterly irrelevant in terms of gene flow as the animals do not mate during that time – or are we to believe that Lemon Sharks may engage in protracted dating prior to having sex?
Plus – was the increased residency the direct consequence of the feeding, see above?

Increased intra-specific aggression.
Here, the authors blame the limited amount of food leading to exarcerbated competition; and on the other hand, they seem to postulate (?) that a higher concentration of resident Sharks led to more hierarchical fights and subsequent wounds in males.
Probably! But having witnessed how fast Sharks recover from horrific wounds contracted during the mating season, what is the point? Did any of the bitten Sharks die or end up being permanently inconvenienced as a consequence - and how does that compare to the “natural” mortality and/or bite frequency of non fed Lemon Sharks?

Plus, what’s that tale about M04?
M04 often arrived in the morning with fresh scars or notches (that were hence not contracted during feeding time!) that can be attributed to intraspecific fights (N. Buray pers. obs.). Interesting – but is it science?
Knowing that all individual Sharks have different characters: was he maybe just a notorious brawler – and not a very successful one since it was him, the supposedly dominant Shark, coming back with those wounds and not his assumed victims? And who did he brawl with: females or males?

Increased inter-specific aggression - what is the other species: humans?
If so, we learn that 47% of shark bites in French Polynesia occur during Shark feeds and that M04 bit a feeder in the hand. Both, we learn, prove that the risk of accidental bites has increased critically.

Well, gee, what a mind-boggling insight!
Tremendous development of shark dives is leading to more bites!
I’ve blogged about it in extenso here and don’t need to repeat myself more than that: the precondition for a Shark bite is that a human and a Shark be in the same place at the same time (hellooooo…) and thus, feeding sharks does indeed increase the risk of getting bitten and more Shark feeds will indeed lead to more bites!
This is so trivial, it is painful!

By the same token, the act of commuting in aeroplanes increases the risk of fatal plane crashes - yes, believe it or not: it does!!!
So going back to square one: do we prohibit aviation as a consequence? No, we ask that anybody engaging in the activity, especially commercially, follow a regimen of strict safety protocols!

Now, it just so happen that I’ve done a multitude of Shark dives in French Polynesia.
Many of them were Shark feeds with mainly Greys and Silvertips - and yes, I’ve also witnessed several of the Moorea Lemon Shark feeds.

Any Shark bites?
Certainly: four of them, one by a Silvertip and three by Grey Reefs!
The cause: multi-user sites combined with Gallic panache and improvisation: poor Shark diving briefings leading to unpredictable behavior of the clients, ever changing procedures and feeders, creative chaos and heaps of bravado, zero protection of the feeders and clients alike – in brief, the recipe for certain disaster!
With that in mind, the described bite comes at no surprise whatsoever!

Was that bite by M04 really aggression – and if so, due to what? Did the behavior of the feeder piss off the Shark? Did the Shark mistake him for a competitor? Is aggression really the most plausible explanation?
Here in Fiji, all of our clients have to wear dark gloves. The reason is that anybody without gloves will get nailed by the ever greedy Giant Trevally and Red Bass who mistake the pasty hands sticking out of dark wetsuits for bait. This is not aggression, this is a mistake!
Would it not be much more plausible to assume that M04 might have made the exact same mistake when in a hurry due to a competitive situation?

Bull Sharks are not Sicklefin Lemons and anybody who knows about Sharks knows that different Shark species have very different behavioral traits and that one cannot make generic statements across species - and certainly not make comparisons to, of all animals, Komodo Dragons!

Case in point, this stellar interview with Aleks Makjkovic about her research with Caribbean Reefs in the Bahamas.

Keeping in mind the above caveat, this is what we do in Fiji in order to increase the safety of everybody:
- This is a one operator site, meaning that we can enforce a uniform protocol that is always highly predictable – for the animals, not us!
- By the same token, the people feeding are always the same, to the point that they have developed personal relationships with individual Sharks
- Feeders wear chain mail gloves and clients, full body dark wetsuits and black gloves
- There is separation between the large Bull Sharks and the customers (remember the precondition above!)
- There are extensive dive briefings so that the clients know exactly how to behave and don’t startle the animals
- There is ample food and the animals are conditioned to follow a set routine, meaning that we are trying to minimize competitive pressure. We also always control the amount of food being introduced, meaning that when we sense any incipient tension, we can discontinue the feed and wait until everybody has calmed down again.

Could some of it be replicated in Moorea! Sure!
Long story short: the obvious solution is not the annual cessation of the feeding activity for several months that implies the necessity to re-establish the feed, the relationships and the training of the animals - it is to improve the feeding protocols!

As to the other grievances about inbreeding and intra-specific aggression: not with our Bulls!

We’ve been keeping highly detailed tabs for 7 years now and none of the Bulls has taken up residency, let alone established a territory necessitating defense against conspecifics.
Instead, although the numbers continue to increase, we’re being faced with a continuous rotation of individuals who clearly lead a free life and are not dependent on Shark Reef for sustenance. Plus, they all vanish during the mating season which is a good indication for them doing plenty of walkabout and mixing of gene pools once they get horny!

The tally:
Bulls biting feeders: zero;
Bulls biting clients: zero;
Bulls biting Bulls: one documented case (we always have at least one camera rolling) where two homed in on a Tuna head and one very obviously missed the head and bit the other – yes, camera rolling! We have certainly never witnessed a single case of a Bull Shark resorting to biting in order to assert its dominance, and this in thousands of Shark dives – but then again, it’s a different species.
Fatalities among our 100 individually named animals, of a total of approx 300: only Jaws who has been missing since 2006.
All others are friendly, well fed and above all, locally protected - and I believe, perfectly happy!

Hence, what is the relevance of this paper to what we do and to Shark feeding in general?
You be the judge of that.


BeachNomad said...

Care to send the paper my way? Would love to read the whole thing before posting comments.

DaShark said...


Looking forward to your comments!

Johann MOURIER said...

Just wanted to say you that I'd like to reply to this interesting comments on our study.
But quickly, just want to say that our aims were not to say that feeding and diving industry is wrong (as our study was done with a diving instructor) and that it is a case study that would maybe different in Fidji or Bahamas... We tried to be the most objective as posible in our study, and it is good to discuss about it.
Anyway, DaShark: were can we send you a reply? I think that many of your points are interesting but I have additional information to better understand our case in Moorea that differ from Fidji from example.

DaShark said...

Bonjour Johann

STP écris-nous a

Merci, Mike

BeachNomad said...

Just after a quick review I have to say that I believe that the paper is a good start to what appears to be one of the first papers to look at the effects of shark diving (baiting/feeding) on Negaprion spp. However like Mike I do see some preliminary issues.

#1 being (as the authors state) the lack of information on the ecology/biology of Adult Lemons. Are these groups really a result of the feeding efforts or just normal behavior? It has been shown in juvenile N. brevirostris that sharks aged 2+ show a tedenacy towards social behavior (Guttridge et al. 2009, Reyier et al. 2007).

#2 is the lack of a control site. While this is inherently difficult because of the difficulty in locating another area where lemon sharks show high density especially if this group behavior is a result of the feeding. However research in the on N. brevirostris in the Atlantic has shown that such areas exist around nursery grounds so locating an area in the Pacific to use as a control site is conceivable.

I am interested to see the results in the DNA part of this study as this will actually give information on if the same sharks are coming back and what extent their offspring are related. The authors suggest that there may be loss of genetic diversity but that only occurs if the juveniles are following adults back to this feeding habitat and the adults only mate with the same individuals. From the paper it still appears that males are leaving the area which gives them ample opportunity to mate outside of these groups.

Hopefully the authors continue their research and address some of the questions raised by Mike and myself. Dr. Mourier if you don't mind I would be interested in your comments and I can be reached at

MooreaNaturalDiverLover said...

hello there,
why don't you study the video of bathys diving regarding the "attack" (as it is purely one) of the lemon shark on the feeder which haven't even started the hand feeding yet.
There will be no more question of if it due or not of misbehavior of the feeder.
Purely a change in shark behavior, scary ...
you can see a picture taken from that video on facebook on page "stop shark feeding in tahiti", the shark attack the feeder from behind after passing next to him and suddently making a turn and trying to make a big bite on his head !!!

Save turtles borneo said...

As a scientist from SE Asia I love the fact that you actually have sharks. 100 named identified sharks is awesome.
Please add some data to the global shark survey, we need bright spots to compare the death and destruction too. I have good shark abundances from Maldives seychelles and the Bahamas but nothing from Fiji or French Polynesia.
In SE Asia with baiting we see maybe 1 shark in 8h on any fished reef. With no baiting I have numbers like 2050h in a national park and no sharks seen.
one out of 5 national parks actually has sharks that can be seen by divers.

on dives without baiting how many sharks do you see. That is the data I want to use to convince fisheries and tourism ministers to think about protection for sharks.

Could someone send me the paper.


steve oakley
facebook/save sharks in sabah