published online 25 February 2009
Gonzalo R Mucientes, Nuno Queiroz, Lara L Sousa, Pedro Tarroso and David W Sims
Sexual segregation of pelagic sharks and the potential threat
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Sexual segregation of
pelagic sharks and the
Gonzalo R. Mucientes1, Nuno Queiroz2,3,
Lara L. Sousa2, Pedro Tarroso2
and David W. Sims3,4,*
1Instituto de Investigaciones Marinas, CSIC, Eduardo Cabello 6,
36208 Vigo, Spain
2CIBIO—Universidade de Porto, Campus Agra ´rio de Vaira ˜o,
Rua Padre Armando Quintas, 4485-668 Vaira ˜o, Portugal
3Marine Biological Association of the United Kingdom, The Laboratory,
Citadel Hill, Plymouth PL1 2PB, UK
4School of Biological Sciences, University of Plymouth, Drake Circus,
Plymouth PL4 8AA, UK
*Author for correspondence (email@example.com).
Large pelagic sharks are declining in abundance
in many oceans owing to fisheries exploitation.
What is not known however is whether within-
species geographical segregation of the sexes
exacerbates this as a consequence of differential
exploitation by spatially focused fisheries. Here
we show striking sexual segregation in the fastest
swimming shark, the shortfin mako Isurus
oxyrinchus, across the South Pacific Ocean.
The novel finding of a sexual ‘line in the sea’
spans a historical longline-fishing intensity
gradient, suggesting that differential exploitation
of the sexes is possible, a phenomenon which
may underlie changes in the shark populations
Keywords: distribution; behaviour; sex ratio;
sexual harassment; overfishing; conservation
Pelagic sharks are facing widespread declines owing
to fisheries expansion into the open ocean within the
past few decades (Baum et al. 2003). Recent studies
have suggested that reductions in relative abundance
of up to 80 per cent have occurred in as little as
15 years for some species (Baum et al. 2003),
although lack of accurate harvest data hampers
quantitative stock assessments. Despite some fisheries
assessments showing less pronounced declines for
large sharks (Sibert et al. 2006), they are undoubtedly
particularly susceptible to over-harvesting because of
slow growth rates, a late age at maturity and low
fecundity (Compagno 2002).
Management of pelagic shark populations is poorly
developed and takes little account of behavioural
characteristics such as spatial and temporal movements
and distributions. Recent studies have shown that large
sharks cross national boundaries, exhibit sex-biased
dispersal and often return to favoured areas (Sims et al.
2000; Pardini et al. 2001; Southall et al. 2006).
Therefore, if high fishing activity occurs in key areas
where, for example, the majority of a population
aggregate for feeding or mating opportunities, or where
important components of a population (e.g. pregnant
females, juveniles) choose to remain, there is a potential
for increased rates of decline. A potential factor
exacerbating declines may be the sex-biased exploita-
tion as a consequence of within-species sex differences
in habitat use (Sims 2005).
Sexual segregation is a widespread behaviour in the
animal kingdom and can arise within a species owing
to, among other factors, sex differences in body size,
activity, behaviour, nutritional requirements and/or
habitat selection (Magurran & Macias Garcia 2000;
Wearmouth & Sims 2008). Habitat segregation by
sex appears common among sharks (Klimley 1987;
Wearmouth & Sims 2008), where adult males and
females within a species use different habitats either
within the same or different areas (Sims 2005).
Habitats may be selected differentially by the sexes
for social, thermal or forage-related reasons, for
example (Wearmouth & Sims 2008). However, the
potential role of sexual segregation in the over-
exploitation of shark populations remains an open
question because distinct boundaries in the ocean
between male and female sharks have not been docu-
mented in detail, or in relation to fisheries activity.
To investigate whether (i) sexual segregation in
open-ocean sharks is evident over medium time scales
(weeks to months) and (ii) population structuring by
sex may lead to differential availability of shark sexes
to the fishery, we made detailed observer records of
shortfin mako Isurus oxyrinchus and blue shark Prionace
glauca catches during commercial longlining in the
South Pacific Ocean.
2. MATERIAL AND METHODS
Shortfin mako and blue sharks (see the electronic supplementary
material for species biological information) were caught by a
Spanish commercial surface-longline vessel targeting swordfish
Xiphias gladius in the southeast Pacific Ocean between 20–408 S
and 100–1408 W, from 9 December 2004 to 9 March 2005
(summer season, December–February). A total of 89 longline sets
were deployed during the night at different depths, ranging from
20.1 to 27.4 m. Hooks (nZ172 878) were fixed to monofilament
lines and baited with mackerel Scomber scombrus. All sharks were
sexed on-board and the fork length was measured.
Capture locations were plotted as sex ratios with locations geo-
referenced using tools in ARCGIS v. 9.2 (http://www.spatialecology.
com/htools/). Sea surface temperature (SST) data were obtained
through the online Ocean ESIP Tool (POET; http://poet.jpl.nasa.gov/).
As an estimate of primary productivity, chlorophyll ‘a’ images
were derived from the Sea-viewing Wide Field of view Scanner
(http://oceancolor.gsfc.nasa.gov). Pearson’s correlation coefficients
were estimated between sexes (number of sharks caught per
individual longline set) and SST or chlorophyll a. Stomach
contents (nZ396 sharks) were analysed in situ during evisceration.
Items were identified to the lowest taxa possible and only the
presence/absence was recorded. A multivariate randomization
procedure (ANOSIM) was performed to test for diet differences
between the sexes.
Longline catch and yearly effort data aggregated by 5!5 degree
squares covering the whole Pacific Ocean between 1950 and
2004 were provided by the Secretariat of the Pacific Community
(http://www.spc.int/). Longlining data were used since purse-seine
fishery data for the western Pacific indicates low mako catches
(less than 2% of total by-catch; see the electronic supplementary
material). Effort data (number of hooks) for every visited square
were averaged and a t-test performed between the two main
Electronic supplementary material is available at http://dx.doi.org/
10.1098/rsbl.2008.0761 or via http://rsbl.royalsocietypublishing.org.
Received 11 December 2008
Accepted 12 January 2009
This journal is q 2009 The Royal Society
on 25 February 2009rsbl.royalsocietypublishing.orgDownloaded from
A total of 264 male and 132 female I. oxyrinchus were
captured. Data showed clear sexual segregation over
the four-month period with males occurring predomi-
nantly in the west and females mainly in the east
(figure 1a; electronic supplementary material, figure 1;
longitude; r2Z0.56, FZ88.34, p!0.0001). Based on
length measurements at sexual maturity (Compagno
2002), 84 per cent of males were considered adult,
compared with only 13 per cent of females, indicating
size, in addition to sexual, segregation (electronic
supplementary material, figure 2a). To examine this
striking separation, we mapped the capture locations
of the sexes on remote-sensing images of environ-
mental variables. These showed no significant corre-
lation between males and SST (rZ0.550, pZ0.670;
figure 1) or between male or female occurrence and
chlorophyll a (males: rZK0.165, pZ0.201; females:
rZK0.060, pZ0.674; electronic supplementary
material, figure 3) and the negative correlation of
female occurrence with SST was inconclusive
(see Results in the electronic supplementary material).
Examination of prey items in stomach contents showed
no difference in diet between the sexes (RZ0.017,
pZ0.195; electronic supplementary material, table 1).
Males were predominant in the area where longline
fishing intensity was historically higher (averaged over
55°W 100°W 140°W 150°W
average number of hooks
sea surface temperature (°C)
Figure 1. (a) Capture locations of male (white; nZ264) and female (black; nZ132) shortfin mako sharks in the southeast
Pacific with respect to a false colour remote-sensing image of SST. (b) Longline effort data averaged by 5!5 degree squares
for the Pacific from 1950 to 2004; class breaks were determined statistically by finding adjacent feature pairs between which
there was a relatively large difference in data valueKnatural breaks. Inset black boxes represent the survey area.
2G. R. Mucientes et al.Shark segregation and threat from fisheries
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a 55-yr period), whereas females dominated in the
area with lower historical effort (figure 1b); average
number of ‘historical’ longline hooks set in each
surveyed area was significantly different (t-test: tZ2.86,
The pattern of the blue shark sex distribution from
the same longline sets as shortfin mako indicated a
general bias towards mature males across the entire
area (figure 2; ratio, male : female, 1.00 : 0.34. Total
mature individuals: male, 425; female, 64; total
immature: male, 25; female, 167).
Clear population structuring in large, open-ocean
sharks at this scale is striking and has not been
previously reported. The sexual ‘line in the sea’ we
observed between male and female shortfin mako is
intriguing because this species is the world’s fastest
swimming shark (clocking speeds up to approx.
70 km hK1) and capable of long-distance movements.
Tagging shows trans-Atlantic migrations are rare
however (Casey & Kohler 1992), but with sufficient
genetic exchange among stocks for a single species
worldwide (Heist 2008). Nonetheless, this exploited
shark displays pronounced sex and size segregation at
the regional scale, which does not appear to closely
reflect prey, SSTor primary productivity, at least over
the time scale of this study. Furthermore, the
observed pattern appeared to be principally the result
of spatial rather than temporal effects because the
large changes in sex ratio were too abrupt (occurring
over 8 and 24 days) within the core summer months
to be consistent with large-scale, synchronous move-
ments of the sexes as the survey progressed, which
would be expected if segregation were wholly
temporally driven (see Discussion in the electronic
Numerous hypotheses have been proposed to
explain sexual segregation in animals, but how and
why it occurs remains controversial and largely
unresolved for many taxa (Wearmouth & Sims 2008).
For the sexually size dimorphic scalloped hammerhead
shark Sphyrna lewini (females grow larger), Klimley
(1987) proposed that females segregated from males
by moving to offshore habitat to feed on different, more
energy-rich prey that conferred increased growth rates,
such that maturity was reached at a larger body size
than similar aged males; a larger female body size is
necessary to support large, well-developed embryos.
It was suggested that this strategy would act to match
the reproductive lifetime of females with that of males
within the same cohort. Shortfin mako exhibit
sexual body size dimorphism with females growing up
to 4 m in length, some 30 per cent larger than
males, and giving birth to a few large young (embryo
at-birth length, approx. 0.7 m; frequency, 4–16 per
female; Compagno 2002). Although the present
study could not conclusively identify behavioural
mechanisms, our results indicate that mako sex segre-
gation is probably unrelated to different nutritional
requirements, because male and female diets were
not different and basal productivity between male
and female habitats was a poor predictor of the
Sexual segregation in mako shark in this study was
observable at the large spatial scale but was not
absolute because some mixing was evident. Males
and females were captured on the same longline sets
at a number of locations, principally around the line
separating western from eastern sectors, but also
along the thermal front boundary zone in the south
(figure 1a). Thermal fronts are often prey rich and
act to aggregate predators with greater apparent
mixing of the sexes owing to feeding or courtship
opportunities (Sims et al. 2000). Although we are
unable to provide an explanation for why shortfin
mako segregate sexually, it is possible that it occurs
owing to social factors. Courtship and mating in
sharks are highly aggressive during which (often
multiple) males inflict serious bite wounds on females
(Stevens 1974). It is possible that mako shark sexual
harassment (by males) results in fitness consequences
for females (Magurran & Seghers 1994), interactions
that manifest at the large geographical scale as sexual
55°W 100°W 140°W 150°W
Figure 2. Capture locations of male (white; nZ445) and female (black; nZ231) blue shark in the southeast Pacific with
respect to seabed bathymetry. Inset black boxes represent the survey area.
Shark segregation and threat from fisheries
G. R. Mucientes et al.
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segregation. That mature females were not captured
in large numbers (nZ15) suggests that they were
absent from the study area, which may also reflect
The finding of marked sexual segregation in a
fast-swimming, highly mobile pelagic shark at the
broad scale has implications for assessing fisheries
effects on shark populations. Complex structuring
coupled with region-specific fishing activities may
have disproportionate effects on different com-
ponents of shark populations. In support of this, we
found sex differences in potential exposure to fish-
ing effort for I. oxyrinchus owing to geographical
separation of the sexes (see Discussion in the
electronic supplementary material). For shortfin
mako in this study, we hypothesize that more
intense longlining in the west, if it occurs over the
shorter, seasonal term, has the potential for higher
relative catch rates of males but lower catches of
females. Exploitation of sharks exhibiting seasonal
sexual segregation could be a major contributor to
population declines. For example, the seasonal
capture of sex-specific schools of mature female
spurdog Squalus acanthias in the English Channel
may have resulted in stock collapse in just a few
years (Ford 1921).
We also found evidence for sexual segregation of
blue shark in the southeast Pacific region, since
catches were dominated by mature males, suggesting
that segregation occurs at a larger spatial scale than
the area studied here. Our findings are consistent
with tagging and surveys showing that blue shark
sexually segregated over very large, perhaps even
ocean-basin scales (Stevens 1990). Nevertheless, even
with sexual structuring at these scales, blue shark
populations may also be affected by sex differential
exploitation. For example, P. glauca in the western
Atlantic are thought to segregate sexually and our
proposal of sex-biased exploitation seems supported
80 per cent between 1977 and 1994 but no change
was discernible for females over the same period
(Simpfendorfer et al. 2002).
What these and the current study indicate is the
need for wide-scale, spatially referenced recording of
shark sexes by global high-seas fisheries. However,
given the lack of even the most basic shark catch
data for most fisheries, the potential problem we
highlight may already have impacted populations.
There is an urgent need for proper reporting by
high-seas fisheries of shark catches by species,
number of individuals and biomass, together with
The authors thank the captain and crew for scientific
access to commercially caught sharks and V. Wearmouth
for manuscript comments. N.Q. was supported by Funda-
c ¸a ˜o para a Cie ˆncia e a Tecnologia (FCT) grant SFRH/
BD/21354/2005 and D.W.S. by the UK Natural Environ-
ment Research Council (NERC) Oceans 2025 Strategic
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