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Behavioural response of sicklefin lemon sharks Negaprion acutidens to underwater feeding for ecotourism purposes

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Behavioural response of sicklefin lemon sharks Negaprion acutidens to underwater feeding for ecotourism purposes

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 provisioning activity around the world, despite 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 mo, 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 movements in and out of the area by some males and females, which were probably related to mating, the general trend was that residency significantly increased during the study, particularly in males, showing a risk of inbreeding due to the reduction of shark mobility. Intra- and interspecific aggression was also witnessed, leading to an increased risk of potentially severe bites to 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.
MARINE ECOLOGY PROGRESS SERIES
Mar Ecol Prog Ser
Vol. 414: 257266, 2010
doi: 10.3354/meps08746
Published September 13
INTRODUCTION
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 ani-
mals. The last decade has seen tremendous develop-
ment 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 Poly-
nesia, and it is becoming controversial, with little con-
sensus 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 habitua-
tion to human contact and increase aggression towards
humans by associating divers with food (Burgess 1998,
© Inter-Research 2010 · www.int-res.com*Email: ericc@spc.int
Behavioural response of sicklefin lemon sharks
Negaprion acutidens to underwater feeding for
ecotourism purposes
Eric Clua
1, 2,
*
, Nicolas Buray
3
, Pierre Legendre
4
, Johann Mourier
3
, Serge Planes
3
1
Secretariat of the Pacific Community, BPD5, 98848 Noumea, New Caledonia
2
Ministère de l’Agriculture et de la Pêche, 251 Rue de Vaugirard, Paris 15, France
3
Centre de Recherches Insulaires et Observatoire de l’Environnement (CRIOBE – USR 3278 EPHE CNRS), BP 1013,
98729 Moorea, French Polynesia
4
Département de sciences biologiques, Université de Montréal, CP 6128, succursale Centreville, Montréal,
Québec H3C 3J7, Canada
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 provisioning activity around the world, despite its controversial nature. Amongst other
detrimental effects, the long-term aggregation of sharks can modify the natural behaviour of the ani-
mals, potentially increase their aggression toward humans, and favour inbreeding. During 949 diving
surveys conducted over 44 mo, 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 movements in and out of the area by some males and females, which were
probably related to mating, the general trend was that residency significantly increased during the
study, particularly in males, showing a risk of inbreeding due to the reduction of shark mobility. Intra-
and interspecific aggression was also witnessed, leading to an increased risk of potentially severe
bites to humans. Our findings suggest the need for a revision of the legal framework of the provision-
ing activity in French Polynesia, which could include a yearly closure period to decrease shark
behavioural modifications due to long-term shark-feeding activities.
KEY WORDS: Shark-feeding · Provisioning · Human disturbance · Behaviour · Site residence
Resale or republication not permitted without written consent of the publisher
Mar Ecol Prog Ser 414: 257266, 2010
Orams 2002). However, feeding wildlife can be a posi-
tive 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 prob-
ably 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 sig-
nificant and predictable food rewards, which only hap-
pens if operators contravene permit regulations pro-
hibiting 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 & Fer-
reira 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, mimick-
ing 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 consid-
ered 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 eco-
nomic value of the recreational activity, and do not
address its effects on the behaviour of these potentially
dangerous sharks (ISAF 2010). Bull sharks Carcharhi-
nus leucas, another dangerous species (ISAF 2010),
have been attracted to an ecotourism site in Beqa (Fiji
Islands) since 2002 through a real feeding and condi-
tioning 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 bio-
logical 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 div-
ing 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 docu-
mented during past decades (Gruber 1982, Chapman
et al. 2009), mostly in the central Western Atlantic
Ocean. However, while its early life has been exten-
sively 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 char-
acteristic provided us with an opportunity to investi-
gate the behaviour and residency pattern of an adult
population of this reef shark species through daily
underwater observations at a provisioning tourism lo-
cation. 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 behav-
iour 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.
MATERIALS AND METHODS
Study implementation. The study was conducted at
Moorea Island (17° S, 149° W) in the Society Islands
Archipelago, French Polynesia. Shark-feeding activi-
ties started there in the late 1980s, in the lagoon,
passes and outer slope of the barrier reef. In October
2004, Moorea authorities implemented a Management
Plan for the Marine Environment (Plan de Gestion de
258
Clua et al.: Effects of feeding on shark behaviour
l’Espace Maritime, PGEM) that restricted shark-
feeding activities to 2 zones. Our specific study area
was located at Papetoai on the outer slope of the reef
(from 149° 50’ 670” to 149° 51’ 389” W); it was selected
for its abundance of sicklefin lemon sharks (Buray et al.
2009). At this site, 3 different diving centres feed the
sharks between 08:00 and 10:30 h. Our feeding ses-
sions were conducted in the presence of tourist divers
through dives at depths of 20 to 25 m, starting at
09:00 h and lasting 60 to 100 min. Sessions consisted of
placing a small cage containing tuna discards on the
substratum at the beginning of each dive to lure and
aggregate the sharks in the area. The food was re-
leased at the end of the dive for the benefit of 1 or
sometimes 2 sharks. Data on the presence or absence
of sharks were recorded on each dive using natural
identification marks on their bodies (Buray et al. 2009),
photographed with a digital camera when necessary.
Part of the identification process included the determi-
nation of sex from the presence or absence of claspers,
and total length, estimated visually. We cross-checked
the reliability of this visual assessment through a laser
measurement of some individuals, based on the pro-
jection of 2 laser light spots, 43 cm apart, onto the flank
of the shark as it was photographed (Bansemer &
Bennett 2008). DNA sampling with a biopsy probe
mounted on a spear gun was also conducted on 80% of
the sharks for paternity analysis (the subject of a com-
plementary study), which also allowed us to assess the
reliability of the photo-identification process through
genetic fingerprinting.
The data analysed in the present paper comprise 36
sicklefin lemon sharks observed during 949 dives
spanning 1338 d, or more than 3.5 yr. The study started
on 2 January 2005, and ran until 31 August 2008. The
animals are numbered F01 to M38 (F: female, M:
male). Sharks numbered 14 and 22 are not included in
the present study as they were photo-identified only
once in the provisioning area.
Statistical methods. Females F32 and F33 and males
M34 to M38 arrived at the study site late in the study
and were seldom seen (2 to 19 times each, for a total of
51 sightings of these 7 ind.), and never in groups. The
earliest sighting was on Day 692 of the study (animal
M34). These 7 ind. were excluded from the following
analyses; they were considered as a separate group.
For the 29 remaining sharks, we computed a square
(29 × 29) matrix showing how many times each pair of
animals was observed during the 949 dives. That value
is usually called a in descriptions of binary similarity
indices like the Jaccard and Sørensen coefficients
(Legendre & Legendre 1998); and we follow this usage
in this paper. This statistic can be tested for signifi-
cance against the null hypothesis H
0
that there is no
association between these 2 sharks. We developed an
R function to carry out the test of a by permutation, fol-
lowing the method originally proposed by Raup &
Crick (1979) and detailed by Legendre & Legendre
(1998, p. 273). The function produced 2 outputs: a (29 ×
29) matrix of coefficients a and a (29 × 29) matrix of
p values (after 9999 random permutations) associated
with the coefficients.
We used the matrix of p values to delineate groups of
lemon sharks. An initial total of 406 tests of signifi-
cance were computed. The Holm (1979) correction for
multiple testing was applied to the p values to obtain
an experiment-wise error rate of 5%. After correction,
the 52 pairs of animals that had a coefficients with orig-
inal p values of 0.0001 or less remained significant. Ag-
glomerative clustering methods were not useful for this
study because the groups were not clearly isolated
from one another and some individuals belonged to
2 groups. We therefore examined the connections
among animals on a graph obtained by principal coor-
dinate ordination of the matrix of significant p values
(Gower 1966, Legendre & Legendre 1998).
We used simple linear regression analysis to relate
the abundances of the sharks, globally and in groups,
to days since the beginning of the survey, in order to
determine which group, if any, displayed increased
fidelity to the site. The regression lines were plotted on
graphs showing how many sharks of each group were
observed during each dive.
RESULTS
Population size and structure
The 36 observed sharks comprised 20 females
(55.5%) and 16 males (44.5%). Total length (TL) of the
identified sicklefin lemon sharks ranged from 230 to
310 cm, with a mean of 273 ± 24 cm (95% confidence
interval, Fig. 1). The sex ratio was slightly in favour of
females all year long but varied during any given year,
with the number of males decreasing during the repro-
ductive season, around October (Fig. 2). Overall, this
population was made up of adults larger than 230 cm,
which are assumed to be sexually mature at that size
(Stevens 1984).
Residence patterns and grouping
Fig. 3 presents the co-occurrence links between sharks
in the principal coordinate ordination plot. The first
2 principal coordinate axes accounted for 21% of the
variance in the matrix of p values, which is sufficient
for such a representation. One can make out 5 groups,
with the largest possibly containing 2 subgroups.
259
Mar Ecol Prog Ser 414: 257266, 2010
Group A (51 sightings in total), designated ‘new
sharks’, comprised females F32 and F33 and males
M34 to M38. They arrived at the site late in the study
(first sighting on Day 692). These individuals were
seldom observed, and no more than one was seen dur-
ing a dive (Fig. 4A), as described in the statistical
methods above. Because of their peculiar time distrib-
ution, they displayed a strong significant increase with
time (Table 1). This grouping was more a result of late
occurrence than any real interaction grouping. How-
ever, it demonstrates a renewal of the pool that gained
7 new individuals (20%) in a single year.
260
Fig. 1. Negaprion acutidens. Size distribution of the 36 male
and female sicklefin lemon sharks at the Moorea shark-
feeding site. Individual sharks are identified in the histo-
gram bars
0
2
4
6
8
10
12
14
16
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
Number of sharks
Month
Females
Males
Fig. 2. Negaprion acutidens. Mean number of male and female sharks in each month of the year after 44 mo of observation with
95% confidence intervals (error bars)
F01
F02
M03
M04
M05
F06
M07
F08
M09
M10
F11
M12
F13
F15
F16
F17
M18
M19
F20
F21
F23
F24
F25
F26
F27
M28
F29
F30
M31
Group B
Group C2
Group C1
Group D
PCoA axis 1
–0.5 0.0 0.5
–0.6
–0.4
–0.2
0.0
0.2
0.4
PCoA axis 2
*
*
*
*
*
Fig. 3. Negaprion acutidens. Principal coordinate analysis
(PCoA) ordination showing the co-occurrence links among
sharks with a p value of 0.0001. The first 2 PCoA axes to-
gether account for 21% of the variation in the matrix of p val-
ues among the 29 sharks. Groups B, C1 and C2 are identified
by ellipses, and Groups D and E by asterisks and black dots,
respectively
Clua et al.: Effects of feeding on shark behaviour
261
0
2005 2006 2007 2008
400200 600 800 1000 1200 1400
0 200 400 600 800 1000 1200 1400
0 200 400 600 800 1000 1200 1400
0 200 400 600 800 1000 1200 1400
0 200 400 600 800 1000 1200 1400
0
0
1
2
1
2
3
4
0
4
8
12
0
1
2
3
Total Group D Total Group C Total Group B Total Group A
0
1
2
3
4
Days from beginning of survey
Total Group E
Fig. 4. Negaprion acutidens. Total number of sharks in a group (A to E are the group identifiers) observed during the 949 dives
(days from the beginning of the survey along the abscissa). The linear regression line is shown in each graph, except for Group E.
Vertical dashed lines are year divisions (2005, 2006, 2007, 2008)
Mar Ecol Prog Ser 414: 257266, 2010
Group B (246 sightings), called ‘missing sharks’, con-
tained the 4 strongly interconnected sharks (M05, F08,
F16, M28) at the bottom of Fig. 3. F27 was not included
in that group for 2 reasons: it was only associated with
F08 and it was seen at the site during the whole study,
whereas the members of Group B were only observed
up to Day 606 (Fig. 4B). This is the only group that dis-
played a strong significant decrease (Table 1): it was
present in 2005 but disappeared during 2006.
Group C (3739 sightings), designated ‘resident
sharks’, was the largest group, with 13 ind. (M03, M04,
M07, M10, F11, F15, M18, F20, F23, F24, F25, F29,
M31), and was composed of 2 subgroups. The pivotal
male M04 belonged to both subgroups C1 and C2. This
male showed some atypical dominance behaviour. As
the study progressed, in addition to a strong residency
pattern, this shark showed increasing aggression
towards its male and female conspecifics and, to a
lesser degree, toward divers (N. Buray pers. obs.).
Subgroup C1 (1877 sightings) contained 6 sharks
(M03, M04, M07, M10, M18, F25), all of which were
males except F25. It showed a slight but significant in-
crease in sightings over time (Table 1).
Subgroup C2 (2137 sightings) included 8 sharks
(M04, F11, F15, F20, F23, F24, F29, M31), all of which
were female except M04 and M31. It showed a strong
significant increase in sightings over time, particularly
in the last 2 yr (Table 1).
Group D (556 sightings), designated ‘unpredictable
sharks’, contained 5 loosely interconnected sharks
(F01, F02, F06, M12, F26) of which all were female ex-
cept M12. Female F06 played a pivotal role in this
group. The group showed a slight but significant in-
crease in sightings over time (Table 1).
Group E (617 sightings), designated ‘ghost sharks’,
contained 7 ungrouped individuals (M09, F13, F17,
M19, F21, F27, F30). All except F27 had no co-occur-
rence link at the 0.0001 significance level.
DISCUSSION
This is the first detailed study to
address the effects of provisioning on
sharks by providing observational data
which describe the response of these
predators to a multi-annual daily feed-
ing in a natural environment. It pro-
vides complementary information about
a different type of feeding (conducted
underwater), on a different species
(lemon shark), than previous studies
which addressed the effects of surface
chumming on white sharks in South
Africa (Laroche et al. 2007), or cage div-
ing on Galapagos and sandbar sharks in
Hawaii (Meyer et al. 2009).
Our statistical analysis allowed us to classify the 36
sharks into 6 groups (A, B, C1, C2, D, E), based on
the affinity between sharks and their fidelity to the
site. Groups A and E, each composed of 7 sharks,
were of limited interest, as they comprised sharks
that were either too late in coming to the feeding site
to determine any significant pattern, or displayed
unpredictable behaviour with no clear pattern. How-
ever, it is interesting to notice a clear turn-over in the
population with the arrival of new individuals that
became established. The 4 sharks composing Group
B had a resident pattern in 2005 but disappeared
from the study site during 2006. This may be
explained by death (i.e. M05, which appeared to be
old), stress due to shark intraspecific interactions (see
below) or just temporary disappearance (i.e. M28,
which re-appeared in 2008 after a 2 yr absence).
Group C, which comprised 13 ‘resident’ sharks,
showed a strong pattern of sexual segregation. Sub-
group C1 was mostly composed of males (5 males
and 1 female), and subgroup C2 was mostly com-
posed of females (6 females and 2 males), with male
M04 showing strong affinities with both subgroups.
This spatial and temporal sexual segregation is com-
monly encountered in carcharhinids (Klimley 1987,
Economakis & Lobel 1998) and other shark families
(Bansemer & Bennett 2008, Mucientes et al. 2009).
Male sharks of Subgroup C1 (1877 sightings) showed
strong residency during all 4 yr; their presence rate
decreased strongly in OctoberNovember, corre-
sponding with the mating period (Stevens 1984). This
trend may be due to a temporary migration for mat-
ing with females that do not belong to the studied
population. In fact, reproduction has been recognised
as a driving factor for spatial segregation between
sexes in other studies (Economakis & Lobel 1998).
Sharks from Subgroup C2 (2137 sightings) mostly
comprised females which seemed to aggregate at the
262
Slope p-value Interpretation
All sharks (n = 36) 0.00176 2.05 × 10
–12
Strong significant increase
Group A 1.542 × 10
–4
3.68 × 10
–16
Strong significant increase
Group B 8.588 × 10
–4
<2 × 10
–16
Strong significant decrease
Group C 0.00260 <2 × 10
–16
Strong significant increase
Group C1 0.00033 0.0151 Slight significant increase
Group C2 0.00252 <2 × 10
–16
Strong significant increase
Group D 1.677 × 10
–4
0.0103 Slight significant increase
Table 1. Negaprion acutidens. Simple linear regression results for the relation-
ships between the number of sharks, globally and in groups (except Group E),
observed during 949 dives, and the number of days since the beginning of
the survey. The slope values are very small because the day numbers range
from 2 to 1339
Clua et al.: Effects of feeding on shark behaviour
feeding site and leave for only a few days for parturi-
tion (easily detected by external shape of the belly),
as witnessed between August and October in 2005
and 2007 (for F11, F15 and F20), in September 2007
(F23) and in August and October 2008 (F24 and F29;
N. Buray pers. obs.).
We considered the ‘unpredictable’ sharks from
Group D, comprising 4 females and 1 male (556 sight-
ings), as ‘non-residents’. This term is based mainly on
the consideration of the cumulative number of days at
the site; it does not refer to a pattern of regular yearly
presence at the feeding site during the extended mat-
ing period (July to November). This pattern can be
seen as the inverse of the disappearance of the C1
sharks in OctoberNovember. As some ‘resident’
males were leaving the study site for mating, some
females may have arrived for the same purpose.
Genetic investigations on the lemon shark Negaprion
brevirostris in the Bahamas (Feldheim et al. 2002) have
shown that to avoid inbreeding problems within their
relatively small populations, they appear to have
developed a mating strategy. Whereas female lemon
sharks return to their natal grounds each year, males
remain nomadic, only infrequently returning to the
same mating group. In our study, we found a similar
pattern of ‘mixing population’ in N. acutidens, mainly
with females potentially coming back to their natal
grounds; however, unlike N. brevirostris in the Baha-
mas, males showed a strong residency and site attach-
ment over the years. Assuming similarity in the natural
behaviour of these 2 sister species, 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 vari-
ability 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), indicat-
ing 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 sit-
uations 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 pre-
viously, 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 intraspe-
cific interactions generated by the provision of a lim-
ited 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 ses-
sions, 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 pre-
sent. As was previously observed in 2005 for its 2 pre-
decessors, from 2006 onwards M04 often arrived in the
morning with fresh scars or notches that can be attrib-
uted to intraspecific fights (N. Buray pers. obs.). Ag-
gression increased significantly when resident males
came back to the feeding site after the mating period,
probably in the context of a reorganisation of the hier-
archy, 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 in-
creased 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 anec-
dotal, this was confirmed by a serious bite by shark
263
Mar Ecol Prog Ser 414: 257266, 2010
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 popula-
tion during the study. At present, the population seems
to be a balanced mix of resident and non-resident indi-
viduals, which favours population mixing. However, if
the resident sharks increase their numbers and their
attachment to the feeding site, group living can gener-
ate costs for animals which are normally solitary for-
agers, such as injuries, predation, increased stress hor-
mone levels and exposure to parasites due to increased
transmission rates between individuals (Semeniuk &
Rothley 2008). If supplemental feeding can be per-
ceived 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 re-
production (Orams 2002), long-term unnatural aggre-
gation 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 nega-
tive effect on gene flow linked to the increasing resi-
dency pattern might be buffered by the multiple pater-
nity 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 Polyne-
sia in order to reduce these risks. An annual cessation
of the feeding activity for several months, preferably
encompassing the mating period, is an obvious solu-
tion. Whereas our study allowed us to draw these pre-
liminary 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.
Acknowledgements. This study benefited from the financial
support of the Direction à l’Environnement (DIREN) of French
Polynesia and the scientific support of the Coordination Unit
of the Coral Reef Initiatives for the Pacific (CRISP Pro-
gramme), based in Noumea, New Caledonia. We thank the
private diving company Top Dive in Moorea for logistic sup-
port, and R. Galzin, Centre de Recherche Insulaire et Obser-
vatoire de l’Environnement (CRIOBE), J. Werry (University of
Griffith) and M. Francis (National Institute of Water and
Atmospheric Research), for scientific support.
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Editorial responsibility: Tim McClanahan,
Mombasa, Kenya
Submitted: March 11, 2010; Accepted: July 25, 2010
Proofs received from author(s): September 4, 2010
... The provisioning of sharks and rays also raises concerns regarding the potential ecological effects on the animals. Indeed, previous studies highlighted some negative impacts such as modification of the composition of elasmobranch communities (Brunnschweiler et al., 2014;Meyer et al., 2009), reduced mobility or habitat shifts (Bruce & Bradford, 2013;Clua et al., 2010;Corcoran et al., 2013;Huveneers et al., 2013;Mourier et al., 2021), altered activity patterns (Barnett et al., 2016;Bruce & Bradford, 2013;Corcoran et al., 2013), the transmission of ectodermal parasites (Semeniuk et al., 2009;Semeniuk & Rothley, 2008), alteration of physiological characteristics (Semeniuk et al., 2009), and elevated intra-and interspecific competition (Brunnschweiler et al., 2014;Clua et al., 2010;Newsome et al., 2004;Semeniuk & Rothley, 2008). However, other studies did not show any significant negative impacts on ecology and behavior of targeted elasmobranchs species including white sharks (Carcharodon carcharias) (Laroche et al., 2007), Caribbean reef sharks (Carcharhinus perezii) (Maljković & Côté, 2011), tiger sharks (Galeocerdo cuvier) (Hammerschlag et al., 2012), bull sharks (Carcharhinus leucas) (Abrantes et al., 2018;Brunnschweiler & Barnett, 2013), and juvenile lemon sharks (Negaprion brevirostris) (Heinrich et al., 2021). ...
... The provisioning of sharks and rays also raises concerns regarding the potential ecological effects on the animals. Indeed, previous studies highlighted some negative impacts such as modification of the composition of elasmobranch communities (Brunnschweiler et al., 2014;Meyer et al., 2009), reduced mobility or habitat shifts (Bruce & Bradford, 2013;Clua et al., 2010;Corcoran et al., 2013;Huveneers et al., 2013;Mourier et al., 2021), altered activity patterns (Barnett et al., 2016;Bruce & Bradford, 2013;Corcoran et al., 2013), the transmission of ectodermal parasites (Semeniuk et al., 2009;Semeniuk & Rothley, 2008), alteration of physiological characteristics (Semeniuk et al., 2009), and elevated intra-and interspecific competition (Brunnschweiler et al., 2014;Clua et al., 2010;Newsome et al., 2004;Semeniuk & Rothley, 2008). However, other studies did not show any significant negative impacts on ecology and behavior of targeted elasmobranchs species including white sharks (Carcharodon carcharias) (Laroche et al., 2007), Caribbean reef sharks (Carcharhinus perezii) (Maljković & Côté, 2011), tiger sharks (Galeocerdo cuvier) (Hammerschlag et al., 2012), bull sharks (Carcharhinus leucas) (Abrantes et al., 2018;Brunnschweiler & Barnett, 2013), and juvenile lemon sharks (Negaprion brevirostris) (Heinrich et al., 2021). ...
... 95% confidence intervals are highlighted for each curve foraging in the area. Such negative interactions have already been observed for sicklefin lemon sharks (Negaprion acutidens) in another feeding site in Moorea, located on the outer reef, where some animals were displaying wounds inflicted during fights for dominance (Clua et al., 2010). Particularly strong dominance interactions could have occurred after reopening, but then progressively attenuated with time, allowing coexistence of different individuals in the same area of interest, as has already been shown for tiger sharks (Galeocerdo cuvier) around a blue whale carcass (Clua et al., 2013). ...
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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.
... Behavioural changes detected have included aggregation of large solitary sharks at a small spatial scale (Bruce & Bradford, 2013;Brunnschweiler & Baensch, 2011), increased residency at provisioning sites (e.g. 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). ...
... Indeed, large gravid females had more variable spatial behavioural patterns compared to mature, but nongravid, females, suggesting that reproductive state and possibly plasma testosterone level influence behaviour (Fig. 8). For example, changes in shark behaviour associated with their reproductive cycle have been reported for provisioned sicklefin lemon sharks, Negaprion acutidens, in which males increase aggression during mating (Clua et al., 2010), probably associated with increased testosterone levels during this period (e.g. Awruch, 2013). ...
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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.
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... Individual fish can be identified by a combination of attributes, including natural markings, scars, or body size (e.g., Ang and Manica 2010;Brena et al. 2018;Perryman et al. 2019), or tagged (see section 16.2.2.2). Collecting data on other attributes such as sex, size, reproductive status, and boldness is useful because these traits can predict or influence social relationships (e.g., Clua et al. 2010;Maruska and Fernald 2010). Under laboratory conditions, it may be relatively easy to identify and record attribute data for all individuals. ...
Chapter
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... Field and laboratory studies have demonstrated that sharks learn to habituate food source with sensory cues [21,54]. For example, ecotourism operators use the incentive of food to attract some species of sharks [19,55,56]. Although not a deliberate attempt to feed sharks, recreational fishing may provide increased food provisioning that enables sharks to readily obtain prey. ...
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... Moreover, the presence of other sharks can increase competition and aggression (e.g. Clua et al., 2010) and in low visibility conditions (such as in Cid Harbour), sharks rely less on vision and more on other senses (electroreception, olfaction, lateral line, hearing) to detect prey (Gardiner et al., 2014). All these factors could have contributed to the Cid Harbour shark bites. ...
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... These activities can lead to nutritional problems and a higher risk of disease spread due to the increased concentration of animals in specific places (Miller et al., 2003;Orams, 2002). Food provisioning is also a form of behavioural conditioning in which animals learn to associate humans with food resources, which can disrupt their habitat use and behavioural budgets (Brunnschweiler et al., 2014;Hodgson et al., 2004;Fitzpatrick et al., 2011;Bejder & Samuels, 2002), promote aggression (Clua et al., 2010;Alves et al., 2013;Smith et al., 2008) and maladaptive behaviour (e.g. 'begging' for food handouts; Donaldson, Finn, & Calver, 2010;Powell & Wells, 2011). ...
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Food provisioning promotes close interaction with wildlife but can negatively impact the targeted species. Repeated behavioural disruptions have the potential to negatively impact vital rates and have population level consequences. In Bunbury, Western Australia, food-provisioned female bottlenose dolphins, Tursiops aduncus, suffer reduced reproductive success via lower calf survival. However, the proximal causes of this long-term negative effect remain unknown. To infer processes that could lead to fitness costs, we combined network analyses, Markov Chain, regression models and kernel density estimates to evaluate the social environment, behavioural budget and home range size of provisioned dolphins relative to their nonprovisioned counterparts. We found that provisioned dolphins spent significantly less time socializing and had smaller home ranges and weaker social associations than the nonprovisioned dolphins. Overall, these findings suggest that provisioned dolphins experience a more restricted social environment among themselves, which likely results from investing time in an unnatural foraging tactic around the provisioning site, in proximity to human activities. This modified social environment associated with food provisioning and begging behaviour, reinforced by the limited time spent socializing, could affect the opportunities of calves of provisioned females to acquire fitness-enhancing skills and form essential social bonds. This study highlights the need to consider the potential impact of human activities on the social environment of animals.
... A total of 125 references were cited from 2002 to 2018, with an average year of 2011. References with high citation in #3 mainly studied the extinction and protection of marine life such as sharks (Dulvy et al., 2014), as well as the economic value and ecological impact of shark ecotourism (Clua et al., 2010;Gallagher & Hammerschlag, 2011;Gallagher et al., 2015). The paper published by Gallagher et al. (2015) is both the highly cited reference and main citing article, mainly focusing on the impact of shark ecotourism. ...
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... Easy and concentrated access to introduced food can lead to unnatural aggregation at feeding sites, which can lead to higher pathogen transmission (avian populations) (Robb et al., 2008), and increased intraspecific and interspecific aggression (sicklefin lemon sharks, Negaprion acutidens) (Clua et al., 2010), all of which can result in stress to animals. Unexpectedly, in the present study corticosterone was generally lower for iguanas at sites with more tourist activity, but this varied depending on sex and season for both subspecies. ...
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To promote survival and fitness, organisms use a suite of physiological systems to respond to both predictable and unpredictable changes in the environment. These physiological responses are also influenced by changes in life history state. The continued activation of physiological systems stemming from persistent environmental perturbations enable animals to cope with these challenges but may over time lead to significant effects on the health of wildlife. In the present study, we tested how varying environmental perturbations driven by tourism and associated supplemental feeding affects the energetics, corticosterone and immunity of six discrete populations of the northern Bahamian rock iguana (Cyclura cychlura inornata and Cyclura cychlura figginsi). We studied populations within and outside the reproductive season and quantified tourist numbers during sample collection. Specifically, we measured clutch size, body condition, plasma energy metabolites, reactive oxygen species, baseline corticosterone concentrations and immune function of male and female iguanas from each population to address whether (i) disparate physiologies are emerging across a gradient of tourism and feeding, (ii) both subspecies respond similarly and (iii) responses vary with season/reproductive condition. We found significant effects of tourism level, season and their interaction on the physiology of both C. c. inornata and C. c. figginsi, supporting the idea that tourism is leading to the divergence of phenotypes. Specifically, we found elevated plasma energy metabolites, oxidative stress and a measure of innate immunity (bactericidal ability), but reduced corticosterone concentrations with increasing tourism in both subspecies of rock iguanas. These physiological metrics differ according to the level of tourism in both subspecies and persist across seasons despite variation with natural seasonal and reproductive changes. These findings suggest that anthropogenic disturbance results in disparate physiologies in northern Bahamian rock iguanas.
... These activities can lead to nutritional problems and a higher risk of disease spread due to the increased concentration of animals in specific places (Miller et al., 2003;Orams, 2002). Food provisioning is also a form of behavioural conditioning in which animals learn to associate humans with food resources, which can disrupt their habitat use and behavioural budgets (Brunnschweiler et al., 2014;Hodgson et al., 2004;Fitzpatrick et al., 2011;Bejder & Samuels, 2002), promote aggression (Clua et al., 2010;Alves et al., 2013;Smith et al., 2008) and maladaptive behaviour (e.g. 'begging' for food handouts; Donaldson, Finn, & Calver, 2010;Powell & Wells, 2011). ...
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