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Genetic Network and Breeding Patterns of a Sicklefin Lemon Shark (Negaprion acutidens) Population in the Society Islands, French Polynesia


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Human pressures have put many top predator populations at risk of extinction. Recent years have seen alarming declines in sharks worldwide, while their resilience remains poorly understood. Studying the ecology of small populations of marine predators is a priority to better understand their ability to withstand anthropogenic and environmental stressors. In the present study, we monitored a naturally small island population of 40 adult sicklefin lemon sharks in Moorea, French Polynesia over 5 years. We reconstructed the genetic relationships among individuals and determined the population's mating system. The genetic network illustrates that all individuals, except one, are interconnected at least through one first order genetic relationship. While this species developed a clear inbreeding avoidance strategy involving dispersal and migration, the small population size, low number of breeders, and the fragmented environment characterizing these tropical islands, limits its complete effectiveness.
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Genetic Network and Breeding Patterns of a Sicklefin
Lemon Shark (Negaprion acutidens) Population in the
Society Islands, French Polynesia
Johann Mourier
, Nicolas Buray
, Jennifer K. Schultz
, Eric Clua
, Serge Planes
1 LabEx «CORAIL» - USR 3278 CNRS-EPHE, Centre de Recherche Insulaire et Observatoire de l’Environnement (CRIOBE), Papetoai, Moorea, French
Polynesia, 2 National Marine Fisheries Service, Silver Spring, Maryland, United States of America, 3 Délégation Régionale à la Recherche et Technologie,
Haut-commissariat de la République française, Papeete, Tahiti, Polynésie Française, 4 Ministère de l’Agriculture et de la Pêche, Paris, France
Human pressures have put many top predator populations at risk of extinction. Recent years have seen alarming
declines in sharks worldwide, while their resilience remains poorly understood. Studying the ecology of small
populations of marine predators is a priority to better understand their ability to withstand anthropogenic and
environmental stressors. In the present study, we monitored a naturally small island population of 40 adult sicklefin
lemon sharks in Moorea, French Polynesia over 5 years. We reconstructed the genetic relationships among
individuals and determined the population’s mating system. The genetic network illustrates that all individuals, except
one, are interconnected at least through one first order genetic relationship. While this species developed a clear
inbreeding avoidance strategy involving dispersal and migration, the small population size, low number of breeders,
and the fragmented environment characterizing these tropical islands, limits its complete effectiveness.
Citation: Mourier J, Buray N, Schultz JK, Clua E, Planes S (2013) Genetic Network and Breeding Patterns of a Sicklefin Lemon Shark (Negaprion
acutidens) Population in the Society Islands, French Polynesia. PLoS ONE 8(8): e73899. doi:10.1371/journal.pone.0073899
Editor: Gabriele Sorci, CNRS, Université de Bourgogne, France
Received April 10, 2013; Accepted July 23, 2013; Published August 13, 2013
Copyright: © 2013 Mourier et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This study benefited from the financial support of the Direction à l’Environnement (DIREN) of French Polynesia and the scientific support of
Coordination Unit of the Coral Reef Initiatives for the Pacific (CRISP Programme), based in New Caledonia. The funders had no role in study design, data
collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
* E-mail:
Human population growth has fragmented the range of many
species [1], leading to significant declines in abundance, loss of
genetic diversity and an elevated risk of extinction [2,3]. Such
patterns are mainly reported from terrestrial systems [4], but
marine systems are now showing similar trends [5]. Isolation
and reduction in population size erode evolutionary potential
and raise the risk of extinction through inbreeding depression,
leading to the loss of genetic variation or the accumulation of
deleterious alleles [3,6]. To this end, many species have
developed inbreeding avoidance strategies [7], although some
animal populations naturally show low genetic variability [8,9].
Globally, sharks are threatened by overfishing [10–12]. While
these threats are evident for pelagic species [13] as by-catch of
commercial fisheries, populations of reef-associated species
are also declining [11,14]. Sharks appear to be particularly
vulnerable to over-exploitation because of their K-selected life-
history strategy (i.e., slow growth, late sexual maturity, long life
spans and low fecundity). As a result, overfished populations
may require several decades to recover [10,11,15]. Chronic
overfishing of sharks has diminished population sizes,
fragmented large populations into small, locally-isolated ones
[14], and led to trophic cascades [16]. Despite these rapid
declines, little is known about their ability to persist in smaller,
more fragmented populations and to recover from human-
induced bottlenecks [17]. In addition, there is a lack of
information about the fine-scale population genetic structure
and breeding patterns of most reef shark species (but see
18–21). As top predators, sharks frequently exhibit small
population sizes and are therefore a good model to investigate
the interactions between demographic parameters, genetic
population structure, mating system and levels of inbreeding in
natural small marine populations, especially in isolated insular
For 5 years, we monitored a small sicklefin lemon shark
(Negaprion acutidens) population around Moorea, French
Polynesia [22]. This species is a large (≤ 340 cm total length)
coastal shark that occurs in the Indo-Pacific region [23]. The
species is now listed as globally vulnerable on the IUCN
Redlist. It is a viviparous shark giving birth every second year
on average, between August and October, to 1-13 well-
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developed pups after a 10-11 month gestation period [23]. The
small population of Moorea [22] has not experienced a high
level of exploitation, as sharks are not of commercial interest or
traditionally fished locally, and sharks in French Polynesia have
been formally protected by law since 2006. Low densities may
therefore be a result of natural ecosystem equilibrium in an
isolated, fragmented, insular system and/or due to some recent
natural bottleneck [24]. Meanwhile this species supports part of
the diving industry in French Polynesia with special feeding
dives organised [22,25].
The aim of this study was to describe genetic relatedness
and assign parentage based on microsatellite DNA markers in
order to investigate the genetic makeup and mating output
within a small isolated shark population. Previous parentage
analyses of sharks were mostly based on the reconstruction of
parental genotypes from sampled offspring and, when possible,
included few opportunistic sampled adults in the analysis
[18–20]. The present approach differs since it combines a 5-
years monitoring of the population in Moorea together with a
genetic analysis of relationships among individuals within and
between generations.
Ethics Statement
All necessary permits were obtained for the described field
study from the French Polynesia Ministry of Research to the
authors. No specific permission was required for underwater
surveys as they were conducted at a commercial diving site
and only involved photo-identification surveys (see below).
Every shark species is protected under French Polynesian
laws, however, DNA samples were taken by non-invasive
methods approved and conducted under the French Polynesia
Ministry of Research permitting authority (Permit #
653/MRM/SPE/DEV), and no lethal sampling was conducted.
Juvenile sharks were captured with gillnets and released in the
water alive under good conditions and adults were remotely
sampled with a modified speargun with a biopsy tip.
Study background and tissue collection
Our study was conducted in French Polynesia, a fragmented
system of small islands and atolls separated by deep ocean
(depth 2 000 m), which is expected to increase the effective
isolation of reef-associated populations [26]. We monitored a
population of sicklefin lemon sharks (Negaprion acutidens)
visiting a recreational diving site during a 5-year period in
Moorea (17° S, 149° W; Figure S1). Diving surveys were
implemented on a daily basis representing 1058 days between
January 2005 and September 2009 [22]. Based on photo-
identification [27], we consistently identified 40 mature sharks
(18 males and 22 females ranging from 2.4 to 3.1 meters total
length), with an average of 26.75 ± 3.33 individuals sighted per
year (24 in 2005, 28 in 2006, 31 in 2007, 29 in 2008 and 24 in
2009). When possible, a fin clip was removed from the dorsal
fin of each new shark using a modified spear gun. As a result,
29 out of 40 individuals (72.5%) were sampled. All 11 non-
sampled sharks were observed only once or very few times
and disappeared before sampling. Additionally, 4 resident
females were sampled in Bora Bora (230 km from Moorea)
where only 12 females (but no males) have been observed.
From this survey, all sharks were classified into behavioural
groups based on the affinity between sharks and their fidelity to
the site [22] and were assigned to three categories:
Resident sharks of Moorea: composed of 7 males (M03,
M04, M05, M07, M10, M18 and M31) and 7 females (F08, F11,
F15, F20, F23, F25 and F29);
Non-resident sharks visiting Moorea occasionally:
composed of 6 males (M09, M12, M19, M34, M36 and M38)
and 9 females (F01, F02, F06, F13, F17, F21, F26, F27 and
Bora-Bora resident sharks: composed of 4 females only
sighted in Bora Bora (B1, B2, B3 and B4).
In addition to adults on Moorea and Bora-Bora sites we also
captured 52 newborn and immature sharks from different
cohorts between 2006 and 2009 in Moorea and three
neighbouring islands: Tetiaora (40 km), Tahaa (200 km) and
Rangiroa (330 km) (Figure S1). Annual sampling of juveniles
took place soon after pupping by adult females (between
December and February). Most newborn sharks (or age-0)
could be identified based on the presence of an open (or
recently closed) umbilical scar that closes few months after
birth. The age of sharks without umbilical scars was
determined based on body length, whose distribution is
generally non-overlapping between age-0, age-1 and age-2
(85<age-1<100 cm TL, 100<age-1<115 cm TL and
115<age-1<130 cm TL, respectively, as determined based on
ongoing growth calculations from capture-recapture data). This
was also confirmed with recapture of individuals in two
consecutive years. Sharks that were larger than 130 cm TL
were assigned to an unknown year of birth (‘other’). Tissues
were stored in 95% ethanol.
Underwater observations of reproductive status
During our underwater photo-identification surveys, we
reported the presence of dermal bite wounds and scars on
females’ body as a sign of mating activity [21,28]. Courtship
behaviour with males engaged in close following of females
was also reported with identification of male and female ID
when possible [29]. Finally, the period of parturition was
estimated based on the reappearance of newly slender female
after the pregnant female left the site for several days or weeks
DNA isolation and microsatellite genotyping
Genomic DNA was isolated from each fin-clip using a DNA
Purification Kit (Puregene). We isolated 2 species-specific
polymorphic microsatellite loci from Negaprion acutidens and
selected 14 polymorphic microsatellite loci developed for other
shark species (Table S1). All specimens (n = 85) were
genotyped at all 16 polymorphic microsatellite loci. PCRs were
conducted with forward primers labelled with Beckman Coulter
dyes D2, D3 or D4 (Table S1). Amplified fragments were
separated on a Beckman Coulter CEQ 8000 Genetic Analysis
System, with a 400-bp internal size standard. Genotypes and
allele sizes were scored using Beckman-Coulter CEQ TM 8000
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Genetic Analysis System-associated software. Allelic frequency
and expected heterozygosity under Hardy–Weinberg
equilibrium were calculated for each locus in GENALEX 6 [30].
The presence of null alleles was investigated using
MICROCHECKER [31]. Tests for Hardy-Weinberg and linkage
disequilibrium were conducted in GENEPOP 3.4 [32] and
significant levels were adjusted with sequential Bonferroni
corrections for multiple tests with P < 0.05. Of the 16
microsatellite loci, three did not satisfy Hardy-Weinberg and
linkage disequilibrium assumptions. To test our photo-
identification technique [27], GENALEX 6 [30] was used to
detect potential identical genotypes belonging to resampled
individuals. No identical genotype was found confirming the
accuracy of our photo-identification technique.
Relatedness and genetic network construction
Maximum likelihood estimates of pairwise relatedness
coefficients and genealogical relationships were calculated with
the software ML-RELATE [33] computing 5000 iterations. The
program calculates the maximum likelihood relationship
between individual pairs. It determines which of parent-
offspring (PO), full-sibling (FS), half sibling (HS) and unrelated
(U) categories yields the greatest likelihood.
Instead of trying to reconstruct an exact pedigree that is
challenging from genetic data alone in wild populations, we
built a genetic network using relatedness information [34].
Network analysis is now a common tool used to characterize
animal social associations [35] including sharks [36]. However,
it has rarely been used to illustrate the genetic relationships
between individuals in a population despite its advantage to
incorporate a large amount of data into a simple visual graph
[34]. The genetic network was built from the matrix of genetic
relatedness together with individual characteristics (size, sex
and group membership) using the programs SOCPROG [37]
and NETDRAW 2.123 [38]. Only the R values of first-order
genetic relationships (PO, FS and HS) inferred from ML-
RELATE were retained in this network for an easier
Parentage analysis
The program CERVUS [39] was first used to find highly
probable mother–offspring and father–offspring pairs.
Assignment to these potential parents was done under a strict
confidence level of 95%. These mother–offspring and father–
offspring pairs were then identified in the input file of COLONY [40] as known maternity and paternity. COLONY
[40] implements a full-likelihood approach to parentage
analysis and was shown to outperform other programs in cases
of less than 20 microsatellite markers [41]. We considered both
parent-offspring relationships and sibship amongst offspring.
Adults were separated by sex, and we assumed a polygamous
mating system for both sexes, therefore allowing the
assignment of half-siblings. We carried out a long-run with
medium likelihood precision and a genotyping error rate of 1%.
The prior probability that the true parent was present in the
sample was set to 0.5 for fathers and 0.25 for mothers based
on the proportion of sampled males and females that were
assigned to offspring by CERVUS. We conducted other runs
varying the input parameters such as the mating system for
each sex. For each analysis, 3 replicate runs were conducted
on the same data set. Each of the replicate runs used different
random number seeds to initiate the simulated annealing
processes. Parental genotype reconstruction was also
performed with COLONY allowing to infer the number of
breeders in the population. Therefore, total number of breeders
was assessed either by reconstructing males and females’
genotypes from young of the year half-sib groups or by directly
assigning parentage to offspring from sampled adults.
Inbreeding estimations
To test for inbreeding, we used a Monte Carlo simulation
implemented in STORM 1.0 [42]. This analysis generates
offspring internal relatedness (IR) values expected from the
gene pool if mating is random with respect to parental
relatedness. We calculated the average observed IR for all
offspring (n = 52) and adults (n = 33) sampled. We generated
simulated IR measures by sampling random males (n = 13)
and females (n = 20) with replacement. Each random mating
pair produces a simulated offspring whose internal relatedness
can be measured. The observed mean IR was then compared
with the distribution of average simulated IR produced from
1000 iterations. Potential bias of allelic diversity into IR
estimates was tested by resampling and recalculating IR
values on loci with 5 or more alleles.
Microsatellite summary statistics
Across all individuals of Negaprion acutidens collected for
this work, polymorphism varied from 2 to 15 alleles per locus.
Observed heterozygosity ranged from 0.365 to 0.871 per locus
and expected heterozygosity from 0.395 to 0.871 (Table S1).
Null alleles were detected at loci LS15 and Cli107, as
suggested by the general excess of homozygotes using
MICRO-CHECKER. Overall, significant heterozygote
deficiencies were found in three loci (LS15, Cli107 and Cpl169;
with all P < 0.05 following Bonferroni standard correction). We
therefore decided to remove both LS15 and Cli107 from
subsequent analyses due to evidence of null alleles. Once
analyzing together the remaining 14 loci, no significant
heterozygote deficiencies were observed in the global
population (P>0.05).
Adult population genetic structure
As expected in a wild population, the mean coefficient of
relatedness was low among adults, both within the overall
population of Moorea (mean R ± SD = 0.086 ± 0.137) and
when we included individuals from Bora Bora (mean R ± SD =
0.076 ± 0.128; Table S2). However, the genetic network
illustrates that all individuals are interconnected at least by one
first order genetic relationship except for female B4 from Bora
Bora that is isolated from the network (Figure 1). First order
genetic relationships (PO, FS and HS) accounted for 21.6% of
all pairwise relationships in Moorea and 17.6% when
individuals from Bora Bora are included (Figure 1). The number
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of connections a focal individual has in the network (genetic
degree) ranged from 0 to 11 among the 32 other members of
the network (mean ± SD = 5.6 ± 2.6; Figure 1C), indicating that
individuals have a high number of close relatives in the
population. Residency groups as well as sex categories were
also all genetically linked (Figure 1B). Within-group average
genetic relatedness was significantly different from between
group (P < 0.001) even when excluding resident sharks of Bora
Bora (P < 0.05; Table S2). There was no difference between
sex (P > 0.05; Table S2).
Visual information on reproductive status
Pre-copulatory and courtship behavior, characterized by a
male showing a close nose to tail behavior while following a
female (Figure 2F; Table S3; Video S1), started in August and
lasted until early November (first observation in August 20
last observation in November 1
), with a stable calendar each
Figure 1. Genetic network of the sicklefin lemon shark population from Moorea and Bora Bora. (A) Map of the study
location. (B) The genetic network of adult lemon sharks. Each individual is indicated by a node labelled by shark ID. Circles and
squares indicate females and males respectively and symbol size is indicative of the body length of the shark. Node colour
corresponds to the three defined residency groups. Dyads sharing a first-order genetic relationship are connected by a line, with line
thickness indicating the strength of the genetic relationship (proportional to R values). A ‘spring embedding’ algorithm with node
repulsion for laying out the nodes’ positions [38] was used to cluster densely connected nodes together with less connected nodes
placed around the edge. (C) Genetic degree (number of first-order genetic relationships an individual has) distribution within the
doi: 10.1371/journal.pone.0073899.g001
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year. Several males can be involved in courtship behavior at
the same time following the same female (Figure 2F; Table
S3). Females with specific mating scars were then observed
from the end of September throughout November (Figure 2C;
Table S4). Pregnancy in females became visually apparent in
February and progressed until being fully apparent in May
(Figure 2). Most females followed a 2 years reproductive cycle
(Figure 2A–D) with the exception of females F01 (Figure 2E)
and F21 that became pregnant on 2 consecutive years (Table
S4). Considering the reappearance at the site of newly slender
females together with first newborn sharks found in their
nursery in October, we determined that parturition occurs
between July and November (Figure 2E-F; Table S4).
Therefore, gestation is estimated to last 10 to 11 months.
Parentage analysis
Parentage analysis assigned 35 of the 52 genotyped
juveniles to at least one parent or a parent pair among the 33
sampled adults (Figure 3). In all case, the three runs gave
consistent results and mating system parameters did not
Figure 2. Inference of reproductive cycle from underwater surveys. (A–D) A two-year reproductive cycle as displayed by
female F11 which was pregnant in 2007 (A), then entered in a resting period (B) and mated in 2008 as shown by dermal bite
wounds on its flanks (C), and was pregnant again in 2009 (D). (E–F) Female F01 is pregnant in 2008 (E) and is followed by males
M10 and M31 in a courtship behavior just after parturition in 2008 (F).
doi: 10.1371/journal.pone.0073899.g002
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consistently change parentage assignment results. Of the 35
juveniles, 17 (49%) were assigned only to a female, 13 (37%)
only to a male and 5 (14%) to a parent pair. The two mating
pairs of sampled sharks were F11-M09 (Resident/Non-
resident) and F30-M09 (Non-resident/Non-resident). The 52
juveniles were assigned to 29 distinct litters across the years
(Figure 3). From the adult sharks sampled (13 males and 20
females), only 4 females and 8 males were assigned to a
juvenile. However, the genotype of 29 physically unsampled
sharks (12 males and 17 females) was reconstructed by
COLONY and assigned to a juvenile. No juvenile was assigned
to a female from Bora Bora. Therefore, a total of 41 adult
sharks including 20 males (8 sampled and 12 genetically
reconstructed fathers) and 21 females (4 sampled and 17
genetically reconstructed mothers) contributed to the
reproduction for our sampled juveniles (Table 1).
Female reproductive behaviour
Of the 21 females either sampled or genetically
reconstructed (Table 1), 15 gave birth in Moorea and 4 in
Tetiaroa (Figure 3). Six females returned to the same nursery
on multiple years to give birth, of which 4 returned on a two-
years cycle (F11, F30, #1 and #2; Figure 3) and 2 returned in
consecutive years (#3 and #13; Figure 3). Two litters were
made of juveniles sampled in different nurseries (Figure 3).
Seven (78%) of the 9 litters cumulating more than one young
were the result of polyandrous females with females mating
with 2 to 3 males (Figure 3). Most parturition events confirmed
the dermal bite wounds observed underwater (Figure 2) in the
year prior to parturition (Table S4).
Male reproductive behaviour
In our sample, 10 (50%) of the 20 fathers sired more than
one litter (Figure 3). Five males mated with multiple (2,3)
females in a single year (M09 in 2006; M04 and M09 in 2007;
*6 in 2008; *2 and *3 in 2009). Nine males sired a litter in
multiple years. Male M04 was assigned to offspring of two
different litters of female F30 (Figure 3). Male M05 sired 2
different litters in 2 different years (2008 and 2009) although
this shark has not been sighted in Moorea since early 2006.
Genetic diversity and inbreeding
The mean IR value of offspring was not significantly higher
than expected under random mating (Monte Carlo
randomization (x1000): mean IR ± 95% CI = 0.037 ± 0.056 and
mean simulated IR ± 95% CI = 0.009 ± 0.001, P = 0.142). IR
values calculated from loci with over 5 alleles were not different
from those calculated from all loci (mean IR ± 95% CI = 0.023 ±
0.047; P > 0.05) suggesting that our estimation of IR values
were not inflated by the presence of low allelic diversity at
some loci. Observed maximum IR value was 0.504, 13% (7/52)
of all offspring had IR values higher than 0.25 (the value
expected for offspring of half-sibling mating), and 36% (19/52)
had o-IR larger than 0.125 (Figure S2).
There was a significant inverse relationship between body
size (ca. age) and IR (y = -0.0005x+0.0780; R
= 0.0629; P =
0.011). This was confirmed by a significant difference in R
values between maturity status (F
= 3.248, P = 0.043);
offspring IR values being higher than IR of mature sharks (
P =
0.034; Figure 3A; Figure S2). Finally, offspring IR values did
not vary significantly across years (F
= 0.853, P = 0.472;
Figure 3B).
This study provides a unique case of long term (5 years)
monitoring and genetic survey used to construct the genetic
network and to infer the mating output of an island adult shark
population. This population is also unique since, unlike many
places in the world, it has been preserved from any human
exploitation, implying that low densities observed are normal
for this population. Our results demonstrate that this small
population displays patterns of connectivity throughout the
archipelago and dispersal which are used as a strategy to
avoid mating with closely related partners.
Population genetic structure and dispersal
Although the mean relatedness was low among adults of the
population, all sharks (but 1) were interconnected through
close to moderate genetic relationships. First order genetic
relationships accounted for 17.6% of all pairwise relationships,
reaching 21.6% when excluding individuals from Bora Bora.
The genetic network (Figure 1) illustrates that sharks from
different residency groups and islands are related, that is likely
a consequence of dispersal [37]. Our results also indicate that
sharks are migrating to breed outside their resident population
(Figure 2). While some individuals of its Atlantic sister species,
Negaprion brevirostris, appear to remain at their natal island,
others disperse before reaching maturity [43] to colonize other
islands. A similar situation is found in Negaprion acutidens, as
among four resident female sharks of Bora Bora, three (B1, B2
and B3) appeared genetically linked to sharks sighted in
Moorea (resident M03 and M05; non-resident M12 and M34;
Figure 1B). Also, direct migration evidence is available with
some individuals from Moorea being sighted in Tahiti both
within and outside the mating season (i.e. females F15, F20,
F23, F25 and F30; Figure 1A). Moreover, during each breeding
period (September–November), most resident males
disappeared from days to weeks [22] while non-resident males,
such as male M12, show up in in Moorea, presumably to mate
(Figure 1B). While adult sharks appear to migrate throughout
the archipelago, movement or dispersal in juvenile and
immature sharks may be limited as only two age-0 juveniles
were caught away from their littermates within the same island
(female J4A about 8 km away in Moorea and Tet9 about 1.5
Table 1.
Number of breeders determined by direct
parentage assignment and genotype reconstruction
conducted in program COLONY.
Mothers Fathers Total
Physically sampled 4 8 12
Genetically reconstructed 17 12 29
Total (Ne) 21 20 41
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Figure 3. Female reproduction inferred from parentage assignment. Litters are shown by years for each female with the
assigned father(s) and juvenile(s). Sampled individual adult sharks are indicated in bold. Mothers and fathers inferred through
genotype reconstruction by the program COLONY are identified by #ID and *ID, respectively. Colour of juveniles refers to their
sampling nursery site (Figure S1). Note that juvenile Tet5 was sampled in 2008 in Tetiaroa but was assigned to the birth year 2007
due to its size (110 cm) corresponding to an age-1 juvenile, while subadult Sub1 was sampled in 2008 at the size of 125 cm and
subsequently assigned to year of birth 2006. Finally, Tet1 was assigned to an unknown year as we were not able to determine its
year of birth.
doi: 10.1371/journal.pone.0073899.g003
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km away in Tetiaroa). However, female Tet1 (180 cm TL)
caught in Tetiaroa is an offspring of female 1 that gave birth in
Varari (Moorea) in 2007 and in 2009; therefore, this immature
shark can either correspond to a dispersal event from its birth
location or a change in nursery location of its mother (female 1)
for parturition. The paucity of studies on Negaprion acutidens
does not provide further information on the year of first
dispersal (or emigration from nursery) of juveniles, but a recent
study showed that among immature sharks (i.e., 141 < TL <
202 cm) the first sharks to leave the study area was about 150
cm TL [44]. Individual sharks have been shown to emigrate
from their nursery during their third year in the sister species
Negaprion brevirostris [43] and in their first year in
Carcharhinus melanopterus [45]. However, some species delay
their dispersal until reaching maturity [46]. Therefore, while
sicklefin lemon sharks may start emigration from nurseries
during their first year, dispersal rate in the population may
increase throughout the shark’s growth [43]. Overall, sicklefin
lemon sharks in the Society Islands appear to be structured as
a mixed population of individuals moving throughout the
archipelago (Figure 1; Figure 3).
Reproductive behaviour
From parentage analysis, we were able to investigate the
mating system and recruitment patterns of lemon sharks in the
archipelago. Like other reef sharks depending on nurseries for
recruitment [18,20,21], most females showed philopatry to
particular nurseries (Figure 3) although this was not the case
for all of them (Figure 3). Negaprion acutidens shares nursery
locations with Carcharhinus melanopterus in Moorea and
Tetiaroa [21,47]. As females mostly followed a biennial
reproductive pattern, some did not exhibit a two-year cycle
(Figure 2; Figure 3; Table S4). Therefore, females may follow
an average two-year reproductive cycle in this species, but like
female F01, may sometimes be mated to harassing males just
after parturition (Figure 2E-F; Table S3). Of the 20 genetically
sampled females, only 4 used one of our sampled nurseries.
Therefore, the other females either did not reproduce during
the study period or gave birth at different, unsampled nursery
locations (Table S4). Based on our parentage analysis and
genotype reconstruction, a total of 41 adult breeders (20 males
and 21 females; Table 1) were found in our system. Although
this may be an underestimate due to unsampled nursery
locations in our study area, the number of breeders is relatively
low. Most litters (78%) had multiple sires showing the
prevalence of polyandrous female mating as it is commonly
found in reef sharks [19,20]. This proportion may be
underestimated as the monogamous females had small,
potentially incompletely sampled litters. Male reproductive
success was highly skewed with few males siring litters on
multiple occasions within and across years (Figure 3),
potentially due to dominance hierarchy among them or
migratory strategies during the mating season [22].
Genetic diversity
The mean offspring internal relatedness (mean IR = 0.03)
was not significantly higher than expected under random
mating. However, maximum offspring IR values (IRmax = 0.50)
were higher than those found in offspring of its sister species
Negaprion brevirostris in the Bahamas (IRmax = 0.05 [48]). IR
values were lower to that of full-siblings (mean IR = 0.14) in
Squalus acanthias litters [49], although the estimates were
limited to 7 microsatellite markers. Even the critically
endangered Pristis pectinata did not reveal inbreeding (mean
IR = -0.02 [50]), perhaps due to the absence of migration
barriers of a continuous coastal environment. The same level
of inbreeding was found in Carcharhinus melanopterus,
another shark species of the Society Islands [21]. Negaprion
acutidens clearly developed some inbreeding avoidance
strategy by conducting specific behaviour including dispersal
and migrations across the archipelago. Polyandry is often
expected to effectively increase the cumulative genetic
variation in a single litter and therefore decrease inbreeding. At
the population level, this effect is likely to be mitigated by an
increased variance in male reproductive success [51].
Additionally, studies on Negaprion brevirostris [19,48]
suggested that high multiple paternity in lemon sharks is more
likely a result of convenience polyandry than of indirect genetic
benefits such as inbreeding avoidance. Therefore, it remains
unlikely that polyandry alone play a major role in inbreeding
avoidance mechanisms.
Considering these behaviours and the mating system
displayed by sicklefin lemon sharks to avoid inbreeding, the
observed degree of inbreeding is unusual for mobile free-living
marine species. Chapman et al. [50] argue that male-biased
dispersal from their natal area as well as no evidence that
certain males dominate paternity may reduce the likelihood of
inbreeding in K-selected elasmobranchs. These life history
characteristics and reproductive behaviour are less evident for
Negaprion acutidens in French Polynesia as: (1) a few males
appear to dominate paternity (Figure 3) (2), some males are
resident to an island and do not roam like other species do
[22], and (3) although evidence for dispersal was found,
individuals within the entire Archipelago remain closely related
(Figure 1). Another reason that may limit the effectiveness of
inbreeding avoidance may be the fragmented habitat in this
region which tends to isolate populations [26] and may reduce
the opportunity to find unrelated mates.
In addition, significantly higher IR values in juveniles than in
adults (Figure 4; Figure S2) demonstrate a temporal change in
inbreeding levels. Such a change, that suggests variation in
fitness through time can result either from individuals with
higher IR values progressively migrating away from their natal
site or some differential mortality with individuals with higher IR
values showing lower survival rate than juveniles with higher
genetic diversity. Longer monitoring and redundancy of such
pattern in inbreeding values will be necessary to determine
which hypothesis should be favored.
Individuals from this local population of sickefin lemon sharks
in the Society archipelago share many first-order genetic
relationships providing evidence that population size in this
species is fairly limited in the context of islands at least in
French Polynesia, but likely in isolated islands system of the
Relatedness and Reproduction in a Shark Population
PLOS ONE | 8 August 2013 | Volume 8 | Issue 8 | e73899
Pacific. This low genetic variability has encouraged sicklefin
lemon sharks to develop different strategies to avoid mating
between close relatives with evidence of migrations across
islands and atolls. The highly isolated and fragmented
environment of French Polynesia [26] may limit encounter rate
of unrelated mates despite dispersal and migrations across the
Society Islands. These results encourage for long-term
monitoring to survey the population response to increasing
anthropogenic factors [22] despite the economic importance of
these sharks in the local tourism industry [24].
Figure 4. Patterns of distribution in internal relatedness
values (IR). (A) IR values across the maturity stage of
individuals (categories: juvenile < 100 cm, immature = 100-199
cm and mature > 200 cm). (B) IR values of newborn sharks
(cohorts) across years. Box plots show the median (line within
the boxes), mean (white diamond) and interquartile ranges IQR
(boxes). Raw data points are indicated by black circles.
doi: 10.1371/journal.pone.0073899.g004
Supporting Information
Figure S1. Sampled nursery locations. (A) Map of French
Polynesia with sampled islands. (B) Sampled nursery locations
in Tetiaroa. (C) Nursery locations in Moorea. Circles are
coloured according to the nursery location used in the study
and black circles refers to adult sampling sites.
Figure S2. Distribution of internal relatedness values (IR)
of adult (black bars) and juvenile (grey bars) lemon sharks.
Table S1. Description of the 16 microsatellite loci used to
genotype sicklefin lemon sharks. Dyes: fluorescent
Beckman Coulter dyes labels; Ta: annealing temperature (°C);
N: number of individual scored; H
: observed heterozygosity;
: expected heterozygosity; k: number of alleles; Fis:
inbreeding coefficient; H–W: exact test for departure from
Table S2. Distribution of average relatedness values
across categories (sex and socio-residency groups). Mean
relatedness is displayed together with SD in parenthesis.
Table S3. Underwater observations of male courtship
behaviour in sicklefin lemon sharks in Moorea. For each
year, the females that each male was observed to follow is
Table S4. Underwater visual estimations of reproduction
timing in sicklefin lemon sharks in Moorea. DBW: Dermal
Bite Wound (dates of observations are indicated); P: Parturition
indicated in grey (estimated to have occurred during the time
the female was absent from the observation area; dates of
disappearance for pregnant females are indicated when
Video S1. Courtship behavior with female F01 is closely
followed by male M10 in 23 October 2008. Female F01 was
in near to term gestation in August 2008 (Figure 2E) and
presumably gave birth between August and October 2008
(Table S4). This female returned to our study site on 8 October
2008, was seen followed by male M10 in a courtship and then
joined by male M31 (Figure 2F). Note that both male M10 and
female F01 are focused in their courtship behavior and do not
pay attention to the diver.
We would like to thank the private diving company Top Dive in
Moorea for logistic support and René Galzin, Centre de
Relatedness and Reproduction in a Shark Population
PLOS ONE | 9 August 2013 | Volume 8 | Issue 8 | e73899
Recherche Insulaire et Observatoire de l’Environnement
(CRIOBE), Pablo Saenz-Agudelo, Thomas Vignaud and
Elisabeth Rochel, Centre de Biologie et d’Ecologie Tropicale et
Méditerranéenne (CBETM) for scientific and technical support.
Author Contributions
Conceived and designed the experiments: JM NB EC SP.
Performed the experiments: JM NB JKS EC SP. Analyzed the
data: JM SP. Contributed reagents/materials/analysis tools: JM
SP. Wrote the manuscript: JM NB JKS EC SP.
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... Negaprion acutidens on the other hand, are considered as rare, data deficient, and threatened List with local extinctions in South East Asia [IUCN 2003]) apex predators (maximum length of 3.5 m) with a fragmented distribution range and small breeding populations (Compagno et al., 2005;Schultz et al., 2008;Mourier et al., 2013a). Despite these distinctions, females of both species use shallow nearshore areas of islands, atolls and coastal bays as partition sites and nursery habitats (Stevens, 1984;Speed et al., 2011;Oh, 2016;Matich et al., 2017c). ...
... Despite these distinctions, females of both species use shallow nearshore areas of islands, atolls and coastal bays as partition sites and nursery habitats (Stevens, 1984;Speed et al., 2011;Oh, 2016;Matich et al., 2017c). In areas of sympatry, simultaneous parturition cycles can result in high numbers of morphologically similar sharks (size at birth 55 -66 cm for C. melanopterus; 33 -52 cm total length for N. acutidens; Mourier et al. 2013aMourier et al. , 2013b. Both species likely face unique foraging challenges when they aggregate in nearshore areas, because they are inexperienced, they typically have restricted home ranges and extended periods of residency, and may be frequented by large predatory sharks and teleosts (Heupel & Hueter, 2002;Bethea et al., 2004;Kinney et al., 2011;Tillett et al., 2014;Oh, 2016). ...
... Joseph Atoll, Moorea is populated, has a substantial infrastructure, and has an increasing number of visiting tourists each year. Juvenile C. melanopterus and juvenile N. acutidens are predominantly found across at least nine putative nursery sites (Mourier & Planes, 2013;Mourier et al., 2013bMourier et al., , 2013a, which are within or adjacent to a network of eight marine protected areas (MPA) with different levels of protection (de Loma et al., 2008). Importantly and similar to St. ...
In areas of sympatry, closely related and morphologically similar species are expected to occupy different ecological niches in order to avoid competition. However, without knowledge on competitive abilities (e.g. dominance hierarchies) and population characteristics (e.g. growth rates, fitness traits), the origin and the potential effects of niche pattern (segregation and overlap) are unknown. I found compelling evidence that juvenile blacktip reef sharks Carcharhinus melanopterus and juvenile sicklefin lemon sharks Negaprion acutidens from St. Joseph Atoll, Seychelles exhibit fine-scale segregation patterns as a means to avoid competition. In contrast, slight differences in population characteristics were more likely to be caused by prey availability, intraspecific competition, and anthropogenic impacts. This thesis highlights the need for multi-disciplinary investigations to unveil the underlaying mechanisms of coexistence.
... Spatial management is used increasingly in conjunction with fisheries management to project populations of marine species (Babcock et al., 2010). Data on how environmental factors such as tide (Pillans et al., 2009;Lyon et al., 2017), temperature (Bestley et al., 2013;Kessell et al., 2014), salinity as well biological factors such as food availability (Sims et al., 2006) and mating and reproduction (Mourier et al., 2013;Chapman et al., 2015;Heupel and Simpfendorfer, 2015) are therefore required to understand how management can be tailored to maximize effectiveness. ...
... There are few comparative studies on adult N. acutidens in the Indo-Pacific or N. brevirostris in the Atlantic. Using visual observations, Clua et al. (2010) demonstrated residence and site fidelity of some individual adult N. acutidens around a shark feeding site in Moorea with Mourier et al. (2013) providing additional support of high residency in the French Polynesia. Kessell et al. (2014) monitored movement of adult N. brevirostris with acoustic tags on the east coast of Florida and while estimates of home range were not made, they demonstrated high site fidelity of sharks to reefs off the Jupiter Inlet region. ...
... The movement of some adult females away from their area of residence during the reproductive season may be due to females returning to specific locations to pup. Similarly, movement of males away from resident areas has been documented in N. acutidens (Mourier et al., 2013) and other reef sharks (Heupel and Simpfendorfer, 2015) and is thought to be due to males searching for receptive females. At the onset of the reproductive season, some individual sharks (both males and females) were recorded moving repeatedly between groups of receivers at Mangrove Bay, Point Cloates and Coral Bay with animals moving several 100 km within a few days. ...
Full-text available
Knowledge of the movement patterns of the lemon shark Negaprion acutidens is poor in contrast to the allopatric N. brevirostis . Using acoustic telemetry, we investigated daily (diel and tidal) and seasonal patterns in residency, fidelity, home range, habitat preference, and migratory patterns along the Ningaloo coast, Australia. Thirty eight adult N. acutidens were monitored for up 6.1 years (mean 2.5 y) with 19 animals detected for more than 3 years and 5 for more than 5 y. Approximately 50% of the tagged animals remained within 10 km of their tagging location for more than 12 months (average core home range of 1.7 km ² ). Surprisingly, residency of adults was greater than juveniles in this known nursery area. Adults showed a strong preference for lagoon habitats and moved into shallow nearshore habitats at high tide and at night. During winter months, female sharks shifted their core home range 0.45 km further offshore into deeper lagoon areas, a shift which is likely due to behavioral thermoregulation. Space use by males and females within core areas was asynchronous indicating sexual segregation by resident sharks. Both resident and non-resident sharks were detected up to 140 km away. These highly directional (southerly) and rapid movements (140 km in 2 days) were largely correlated with the parturition and mating periods with males departing 1–2 months earlier than females. In females, periodicity of migrations was variable with evidence of annual and biannual patterns. Negaprion acutidens are highly susceptible to over-fishing and movement data are essential to quantify spatio-temporal overlap with fisheries and assist with developing spatially explicit stock assessment models.
... Climate changedriven impairments to the performance of species like blacktip reef sharks or sicklefin lemon sharks could have population-and ecosystem-level outcomes (Nagelkerken and Munday 2016;Rosa et al. 2017). Similar to previously studied tropical species, however, blacktip reef and sicklefin lemon sharks rely on shallow, nearshore habitats within lagoons as parturition grounds, and neonates appear site-attached to these-potentially shark nurseryhabitats (Mourier, Buray et al. 2013;Mourier, Mills et al. 2013). Blacktip reef and sicklefin lemon sharks are also site-attached for reproduction Mourier, Buray et al. 2013), such that it is unclear whether sharks can select new parturition grounds if conditions reduce survival of neonates and juveniles. ...
... Similar to previously studied tropical species, however, blacktip reef and sicklefin lemon sharks rely on shallow, nearshore habitats within lagoons as parturition grounds, and neonates appear site-attached to these-potentially shark nurseryhabitats (Mourier, Buray et al. 2013;Mourier, Mills et al. 2013). Blacktip reef and sicklefin lemon sharks are also site-attached for reproduction Mourier, Buray et al. 2013), such that it is unclear whether sharks can select new parturition grounds if conditions reduce survival of neonates and juveniles. Therefore, our objectives were to investigate anthropogenic and ecological sources of stress for neonatal and ju ven ile blacktip reef and sicklefin lemon sharks and to identify key stressors for targeted management. ...
... Through research efforts by the CRIOBE and Physioshark, a series of ecologic al and anthropogenic stressors were identified. The breeding populations of blacktip reef and sicklefin lemon sharks are small enough that inbreeding could affect the survival of offspring Mourier, Buray et al. 2013). Low interannual recapture rates and low juvenile abundance relative to neonate and adult populations suggest that survival of neonates within their first year of life is intrinsically low (Mourier, Mills et al. 2013). ...
Sharks and rays are among the most threatened aquatic vertebrate taxa. This is due to a combination of their slow generation times, exploitation within the fisheries, and habitat degradation. Climate change was added as an additional, major threat to sharks and rays in the first decade of the 21st century. While marine protected areas are becoming more widespread, managing and conserving sharks and rays is complicated. Yet, the conservation physiology toolbox can be used to address such challenges. Here, we highlight studies from the Physioshark project, a conservation physiology research programme initiated to understand how human-induced stressors, primarily climate change, will affect tropical sharks and rays and the consequences for the health and viability of populations. We also highlight how other research teams from around the world have taken physiological approaches to understanding conservation problems for sharks. We then emphasize the importance of public outreach and education about the conservation issues sharks encounter, the benefits of using social media to disseminate key concepts, publications, presentations, media, and successes, and we underscore the power of storytelling through digital media as an important means for attracting attention to research, which can result in support and action.
... Blacktip reef sharks take 4-8 years to reach sexual maturity (Chin et al., 2013), have litters of 3-4 pups after 10-11 months of gestation (Stevens, 1984;Porcher, 2005;Chin et al., 2013), achieve a maximum total length of 1.5 m (Papastamatiou et al., 2009a;Mourier et al., 2013b), and are considered high-level mesopredators as adults (Frisch et al., 2016;Roff et al., 2016). Sicklefin lemon sharks reach sexual maturity at approximately 2.2 m total length, have litters of up to 12 pups following 10-11 months of gestation (Stevens, 1984), achieve a maximum total length of at least 3 m and (Clua et al., 2010;Mourier et al., 2013a), as adults, are considered apex predators (Frisch et al., 2016). As neonates, however, both species occupy functional roles as mesopredators in their respective ecosystems . ...
... Further, neonates of these species co-occur across their range (Matich et al., 2017;Oh et al., 2017b;Weideli et al., 2019b), and their tendency to exhibit small home ranges (Papastamatiou et al., 2009a;Oh et al., 2017b;George et al., 2019) and predictable use of habitats as putative nursery areas Mourier et al., 2013a) means that both species can reliably be collected for use in laboratory experiments with sufficient replication. The small size of neonates (< 70 cm total length; Mourier et al., 2013b;Weideli et al., 2019), amenability to captivity Wells et al., 1992;Davie et al., 1993;Chin et al., 2015), and ability to actively ventilate via buccal pumping (personal observation) facilitate the use of these animals in laboratory experiments, including respirometry that restricts the capacity for swimming for ram ventilation. ...
... My study site is the island of Moorea in French Polynesia, where blacktip reef shark and sicklefin lemon shark populations have been extensively studied since 2007 Mourier et al., 2013a). Both populations are fragmented and have low genetic diversity Vignaud et al., 2014); adult populations of blacktip reef sharks and sicklefin lemon sharks around Moorea are made up of approximately 240 and 40 individuals, respectively (Mourier et al., 2012(Mourier et al., , 2013a. ...
Myriad anthropogenic impacts drive declines in global shark populations; yet, the consequences of a newly recognised threat, global climate change, are poorly understood. This thesis tested the hypothesis that global change stressors (ocean acidification and warming) reduce fitness in tropical reef sharks via effects on physiological performance. My specific objectives were to define thermal performance in fitness-enhancing nursery areas, physiological performance in situ, associations between thermal performance, preference, and tolerance, and physiological performance under multiple global change stressors. I found that neonatal blacktip reef sharks (Carcharhinus melanopterus) have superior growth efficiency in nursery areas relative to other habitats, but ocean acidification and warming synergistically reduce performance. This thesis suggests that global change stressors reduce fitness in tropical reef sharks by acting on physiological traits that are associated with nursery areas.
... Polyandry, which is widespread in taxa of live-bearing snakes [86], including the adder [87][88][89], may thus represent a protective mechanism against inbreeding [82,90]. Interestingly, Mourier et al (2013) described a very similar network pattern of extensive pairwise relatedness between individuals of the sicklefin lemon shark (Negaprion acutidens) in French Polynesia [91]. Despite the biological differences, there are clear similarities in the reproductive ecology between the taxa, the lemon shark also being viviparous, of low female fecundity, with a polyandrous mating system and limited distribution [91]. ...
... Interestingly, Mourier et al (2013) described a very similar network pattern of extensive pairwise relatedness between individuals of the sicklefin lemon shark (Negaprion acutidens) in French Polynesia [91]. Despite the biological differences, there are clear similarities in the reproductive ecology between the taxa, the lemon shark also being viviparous, of low female fecundity, with a polyandrous mating system and limited distribution [91]. ...
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Genetic factors are often overlooked in conservation planning, despite their importance in small isolated populations. We used mitochondrial and microsatellite markers to investigate population genetics of the adder (Vipera berus) in southern Britain, where numbers are declining. We found no evidence for loss of heterozygosity in any of the populations studied. Genetic diversity was comparable across sites, in line with published levels for mainland Europe. However, further analysis revealed a striking level of relatedness. Genetic networks constructed from inferred first degree relationships suggested a high proportion of individuals to be related at a level equivalent to that of half-siblings, with rare inferred full-sib dyads. These patterns of relatedness can be attributed to the high philopatry and low vagility of adders, which creates high local relatedness, in combination with the polyandrous breeding system in the adder, which may offset the risk of inbreeding in closed populations. We suggest that reliance on standard genetic indicators of inbreeding and diversity may underestimate demographic and genetic factors that make adder populations vulnerable to extirpation. We stress the importance of an integrated genetic and demographic approach in the conservation of adders, and other taxa of similar ecology.
... A conservative error rate of 0.01 was chosen, which is the equivalent of 1 error per 100 genotypes. As the error rate has little effect on the accuracy of the results (Ackerman et al. 2017), this error rate was chosen according to previous studies (Mourier et al. 2013, Pirog et al. 2017. Grey nurse sharks have multiple paternity (Chapman et al. 2013), so polygamy was chosen as the parameter to describe the mating system for both males and females. ...
The Australian gummy shark Mustelus antarcticus is distributed across southern and eastern Australian waters and is the main target of a large shark fishery. Commercial harvest of the species is considered sustainable based on biomass estimates that show recovery from past overexploitation. However, the effective population size and genetic-based assessments of stock structure remain unresolved. We evaluated the genetic structure and effective population size ( N e ) of the gummy shark using genome-wide single nucleotide polymorphisms. We found genetic divergence between individuals from the east coast and those along the south coast, resulting in 2 discrete populations with signatures of adaptive divergence. Spatial analyses revealed widespread gene flow within each of these populations, with some evidence for mild isolation-by-distance observed using individual-based tests. Demographic modelling of each population showed a comparatively rapid decline of N e in the most recent past compared to more historical projections, with evidence that such declines have occurred to the point where genetic variation could be at risk. The identification of 2 divergent populations of gummy shark suggests that management should consider each individually to ensure the long-term sustainability of the species.
... The current study provides the first coarse injury healing timeframe for whale sharks and can be used to infer the maximum number of days since an injury was obtained based on the healing status of a wound. For elasmobranch species in general, ecological applications of this information include evaluating wound characteristics to potentially deduce date of birth for neonatal sharks based on the healing status of their vitelline scar (Aubrey and Snelson, 2007;Rowat et al., 2007;Chin et al., 2015) and determining the timing of copulation (Chin et al., 2013;Mourier et al., 2013;Chin et al., 2015) or the location of key nursery areas (McCallister et al., 2013). Regrettably, these applications are difficult to apply to whale shark ecology given that encountering individuals at crucial life stages, such as adults engaged in mating activities or neonates, is extremely rare (Rowat et al., 2007;Ramírez-Macías et al., 2017). ...
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Wound healing is important for marine taxa such as elasmobranchs, which can incur a range of natural and anthropogenic wounds throughout their life history. There is evidence that this group shows a high capacity for external wound healing. However, anthropogenic wounds may become more frequent due to increasing commercial and recreational marine activities. Whale sharks are particularly at risk of attaining injuries given their use of surface waters and wildlife tourism interest. There is limited understanding as to how whale sharks recover from injuries, and often insights are confined to singular opportunistic observations. The present study makes use of a unique and valuable photographic data source from two whale shark aggregation sites in the Indian Ocean. Successional injury-healing progression cases were reviewed to investigate the characteristics of injuries and quantify a coarse healing timeframe. Wounds were measured over time using an image standardization method. This work shows that by Day 25 major injury surface area decreased by an average of 56% and the most rapid healing case showed a surface area reduction of 50% in 4 days. All wounds reached a point of 90% surface area closure by Day 35. There were differences in healing rate based on wound type, with lacerations and abrasions taking 50 and 22 days to reach 90% healing, respectively. This study provides baseline information for wound healing in whale sharks and the methods proposed could act as a foundation for future research. Use of a detailed classification system, as presented here, may also assist in ocean scale injury comparisons between research groups and aid reliable descriptive data. Such findings can contribute to discussions regarding appropriate management in aggregation areas with an aim to reduce the likelihood of injuries, such as those resulting from vessel collisions, in these regions or during movements between coastal waters.
Temperature and oxygen limit the distribution of marine ectotherms. Haematological traits underlying blood-oxygen carrying capacity are thought to be correlated with thermal tolerance in certain fishes, and this relationship is hypothesised to be explained by oxygen supply capacity. We tested this hypothesis using reef shark neonates as experimental models because they live near their upper thermal limits and are physiologically sensitive to low oxygen conditions. We first described in situ associations between temperature and oxygen at the study site (Moorea, French Polynesia) and found that the habitats for reef shark neonates (Carcharhinus melanopterus and Negaprion acutidens) were hyperoxic at the maximum recorded temperatures. Next, we tested for in situ associations between thermal habitat characteristics and haematological traits of neonates. Contrary to predictions, we only demonstrated a negative association between haemoglobin concentration and maximum habitat temperatures in C. melanopterus. Next, we tested for ex situ associations between critical thermal maximum (CTMax) and haematological traits, but only demonstrated a negative association between haematocrit and CTMax in C. melanopterus. Finally, we measured critical oxygen tension (pcrit) ex situ and estimated its temperature sensitivity to predict oxygen-dependent values of CTMax. Estimated temperature sensitivity of pcrit was similar to reported values for sharks and skates, and predicted values for CTMax equalled maximum habitat temperatures. These data demonstrate unique associations between haematological traits and thermal tolerance in a reef shark that are likely not explained by oxygen supply capacity. However, a relationship between oxygen supply capacity and thermal tolerance remains to be demonstrated empirically.
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The Southern Lanternshark, Etmopterus granulosus, is a deep-sea shark commonly found throughout the oceans of the southern hemisphere and frequently caught as bycatch in deep-sea fisheries. Despite its common occurrence, little is known about this species’ life history and reproductive biology. Here, we develop species-specific microsatellite markers to better understand the mating system of E. granulosus. Eighteen litters were opportunistically collected as bycatch along the Madagascar Ridge, Walter’s Shoal, and Southern Indian Ocean Ridge. Novel microsatellite loci were used to test for the presence and frequency of multiple paternity and morphological data were obtained from mothers to examine whether litter size or polyandry correlated with female size. Multiple paternity was found in 33% of litters, but no significant relationship between either litter size or the occurrence of polyandry and female size was found, although some adult individuals were found to have high internal relatedness. The frequency of multiple paternity in conjunction with these other factors could be indicators of mating between relatives or a reduction in population size due to fishing pressure.
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The smooth hammerhead shark Sphyrna zygaena is known to display a high degree of site fidelity to specific areas along the South African coastline. This species is vulnerable to overfishing and steep declines have been noted globally. In this study, a dual marker approach was used to investigate the spatial and temporal genetic variation of juvenile S. zygaena across the south and east coast of South Africa. Kinship of individuals was determined within and across cohorts from juvenile S. zygaena sampled in Mossel Bay, a putative pupping ground. Significant genetic differentiation (supported by F-statistics, multivariate analysis and Bayesian clustering) was evident between individuals sampled from the warm temperate south coast and the subtropical east coast, with asymmetric gene flow between regions. Distinct genetic composition was also revealed between sampling years, with different levels of relatedness within and among cohorts, indicating different temporal populations utilizing Mossel Bay annually. Based on these results, further investigation of S. zygaena populations across a wider region is warranted in order to make recommendations regarding conservation management of this vulnerable coastal shark.
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Understanding the movement behaviour of any species is important for developing species-specific management and conservation measures. In recent years, the sicklefin lemon shark Negaprion acutidens has shown rapid range reductions and has even disappeared altogether in certain areas. In this study, the area use patterns and site fidelity of the N. acutidens were assessed at the St. Joseph Atoll in the Seychelles. Passive acoustic telemetry methods were employed to monitor the movements of 19 tagged individuals for 1 year. Area use within the lagoon of the atoll was found to be highly restricted, with individuals typically utilising a small portion of the available area throughout the year. A high-use zone was apparent in the south-east of the atoll’s lagoon, which was shared by many of the monitored individuals. Fidelity to the study site was found to be extremely high, with the 79 % of tagged N. acutidens still present in the atoll at the end of the study. Individuals displayed both diel and tidal movements between the lagoon and surrounding habitats. The restricted area use and high site fidelity observed in this study highlight both the vulnerability of this species to rapid over exploitation and importance of remote habitats such as the St. Joseph Atoll in their future conservation. The results obtained here can be used to inform management decisions regarding the development and utilisation of similar atoll environments throughout the species’ range.
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Large, solitary, marine predators such as sharks have been observed to aggregate at specific areas. Such aggregations are almost certainly driven by foraging and behavioural strategies making space for diverse spatial organizations. Reef-associated shark species often show strong patterns of site fidelity that could be viewed as a prerequisite for sociality. However, there is limited empirical evidence that such aggregations are driven by intrinsic social factors. Association data for blacktip reef sharks, Carcharhinus melanopterus, were obtained from photoidentification surveys conducted in Moorea coral reefs (French Polynesia). We adapted a social network approach to demonstrate evidence of four main communities and two subcommunities within the population. We confronted the resulting structure with candidate explanatory variables. Sharks formed spatial groups characterized by nonrandom and long-term associations, despite opportunities for social relationships to develop between communities. Sex and length of sharks tended to influence assortment at the population and community levels. Individual space use also explained community structure, although spatial assortment was globally weaker than random expectations, suggesting that observed associations were not an artefact of the sampling design or spatial distribution of individuals. We conclude that the observed grouping patterns not only resulted from passive aggregations for specific resources, but rather the communities developed from an active choice of individuals as a sign of sociability. Individual preferences and adaptation to local conditions, as well as demographic, ecological and anthropogenic factors, may explain the social variability between communities. This suggests that a stable grouping strategy may confer substantial benefits in this marine predator.
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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.
Because sharks possess an unusual suite of reproductive characteristics, including internal fertilization, sperm storage, relatively low fecundity, and reproductive modes that range front oviparity to viviparity, they can provide important insight into the evolution of mating systems and sexual selection. Yet, to date, few studies have characterized behavioral and genetic mating systems in natural populations of sharks or other elasmobranchs. In this study, highly polymorphic microsatellite loci were used to examine breeding biology of a large coastal shark, the lemon shark, Negaprion brevirostris, at a tropical lagoon nursery. Over six years, 910 lemon sharks were sampled and genotyped. Young were assigned into sibling groups that were then used to reconstruct genotypes of unsampled adults. We assigned 707 of 735 young sharks to one of 45 female genotypes (96.2%), and 485 (66.0%) were assigned to a male genotype. Adult female sharks consistently returned to Bimini on a biennial cycle to give birth. Over 86% of litters had multiple sires. Such high levels of polyandry raise the possibility that polyandry evolved in viviparous sharks to reduce genetic incompatibilities between mother and embryos. We did not find a relationship between relatedness of mates and the number of offspring produced, indicating that inbreeding avoidance was probably not driving pre- or postcopulatory male choice. Adult male sharks rarely sired more than one litter at Bimini and may mate over a broader geographic area.
Connectivity between coastal habitats and mid-shelf and offshore coral reefs is a topical issue in the conservation and management of fishes and coastal ecosystems.Coastal habitats provide a range of ecosystem functions for sharks and rays and the use of coastal ecosystems by these species affects conservation and management outcomes. There is a growing need to better understand movement and habitat use patterns given recorded declines of many shark and ray species around the world.This study presents evidence of connectivity of blacktip reef sharks between coastal and offshore habitats, with juveniles dispersing from natal grounds at the onset of maturity and moving to new locations including offshore coral reefs.These dispersal patterns differ from previous accounts of reef shark movements and provide new evidence of connectivity among coastal habitats and offshore coral reefs.These large-scale movements may help to maintain genetic diversity of populations, and could increase the resilience of blacktip reef shark populations to localized pressures. These movement and connectivity patterns also illustrate the potential importance of coastal habitats to reef shark conservation. Copyright © 2013 John Wiley & Sons, Ltd.
Elasmobranch reproductive behavior has been inferred from freshly caught specimens, laboratory examinations of reproductive structures and function, or determined from direct observations of captive or free swimming wild animals. Several general behaviors have been described including seasonal sexual segregation, courtship and copulation. Courtship behavior was inferred for many species from the presence of scars and tooth cuts on the female's body, and noted in more detail from underwater observations. Copulation has been directly observed in captive settings for several species of elasmobranchs in large aquaria, and in the wild for three species of urolophids and for Triaenodon obesus and Ginglymostoma cirratum. A detailed ‘case history’ of nurse shark reproductive behavior is presented that may be used as a template for future work on shark reproductive behavior of other species. Our studies, using diver identifiable tags and in situ behavioral observations, provide unprecedented information on social structure and mating behavior in this species. Since 1993, 115 G. cirratum, 45 adults and 70 juveniles have been tagged in the Dry Tortugas, Florida. Observations show that adult males visit the study site every year with three males dominant. Individual adult females visit the study area to mate in alternate years. Polygyny and polyandry are common. Future research on reproductive behavior of elasmobranchs should address questions on male access to females, sexual selection and dominance hierarchies.
Most arguments invoked so far by the scientific community in favour of shark conservation rely on the ecological importance of sharks, and have little impact on management policies. During a 57-month study, we were able to individually recognise 39 sicklefin lemon sharks that support a shark-feeding ecotourism activity in Moorea Island, French Polynesia. We calculated the direct global revenue generated by the provisioning site, based on the expenses of local and international divers. The total yearly revenue was around USD5.4 million and the 13 sharks most often observed at the site had an average contribution each of around USD316 699. Any one of these sharks represents a potential contribution of USD2.64 million during its life span. We argue that publicising economic values per individual will be more effective than general declarations about their ecological importance for convincing policy makers and fishers that a live shark is more valuable than a dead shark for the local economy. Studies monitoring the potential negative ecological effects of long-term feeding of sharks should, however, be conducted to ensure these are also considered. Besides declarations about the non-consumptive direct-use value of sharks, as promoted by ecotourism, the calculation of their other economic values should also benefit shark conservation.