Electronic Supplementary Material
Sexual segregation of pelagic sharks and the potential threat from fisheries
Gonzalo R. Mucientes, Nuno Queiroz, Lara L. Sousa, Pedro Tarroso, David W. Sims
1. Supplementary Methods
1.1 Study Species
The shortfin mako shark (Isurus oxyrinchus) is a large, warm-bodied pelagic shark found
in tropical and warm temperate seas circumglobally with a high-value to by-catch and
targeted longline fisheries where it occurs. Mako may be at particular risk from human
exploitation, with populations apparently diminished by some 25% since 1986 in the
western Atlantic (Baum et al. 2003). Its spatial ecology is little known although markrecapture tagging and fishery data provide coarse evidence for fidelity to geographic
regions and sexual segregation (Casey & Kohler 1992), suggesting the sexes’
susceptibility to fishery impacts may differ.
As a large, ectothermic shark with a wide geographical range across all oceans, the
blue shark (Prionace glauca) is one of the most important target and by-catch species in
high-seas fisheries. Tagging and survey data indicate males and females segregate
sexually in the North Atlantic (Stevens 1990; Simpfendorfer et al. 2002), but its spatial
dynamics in the southeast Pacific Ocean are not known.
1.2 Fisheries Jurisdictions in the Pacific Ocean
The Pacific Ocean is divided into two areas, the western area controlled by the Western
and Central Pacific Fisheries Commission (WCPFC) and the eastern by the InterAmerican Tropical Tuna Commission (IATTC). WCPFC provided the Secretariat of the
Pacific Community (SPC) data we used on fishing intensity (number of hooks deployed).
WCPFC has as members Australia, China, Canada, Cook Islands, European Union,
Federated States of Micronesia, Fiji, Japan, Kiribati, Korea, Republic of Marshall Islands,
Nauru, New Zealand, Niue, Palau, Chinese Taipei, Tonga, Tuvalu, USA and Vanuatu.
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Data provided were to be only for the western Pacific, however it also included data from
the eastern Pacific, so we assumed it included IATTC data.
1.3 Mako Shark Discards/By-catch in Pacific Fisheries
Discards and by-catch of shortfin mako shark (Isurus oxyrinchus) in the hand-line, poleand-line and troll fisheries are relatively minor (Bailey et al. 1996) and only purse-seines
and longline fisheries have a significant by-catch. However, detailed information on
shark by-catch is generally poor in global fishery reports. For the western Pacific Ocean
(WPO) the same SPC report (Bailey et al. 1996) states “There is no logsheet reporting of
shark catch, by species, in the tropical waters of the WPO...”. For the eastern Pacific
Ocean (EPO), the Fishery Status Report (2006) states that “Some information is available
on sharks that are retained by parts of the longline fleet. Information on by-catches and
discards is also available for large purse-seiners, and for some smaller ones”. However,
the same report affirms “Apart from the assessments of […] blue shark there are no stock
assessments available for these species [shark and other large fishes] in the EPO, and
hence the impacts of the by-catches on the stocks are unknown.”
Nonetheless, with the few available data (in minor reports) it is justifiable to conclude
shortfin mako shark were rarely caught by purse-seine fisheries (<2% of the total bycatch in the western Pacific; Bailey et al. 1996). Most of the shark purse-seine by-catch
was silky shark (Carcharhinus falciformis) and oceanic whitetip shark (Carcharhinus
longimanus). In the eastern Pacific, during a shark characteristics sampling programme in
the purse-seine fishery, the percentage of shortfin mako shark caught was 0.9% (RomanVerdesoto & Orozco-Zoller 2005). The same report also provides as an example the data
for the blue shark, stating that “the catch of blue sharks in the longline fishery constituted
about 41% of the entire shark catch […] whereas it represented less than 1% in the EPO
purse-seine shark by-catch during the shark characteristics sampling program.”
The importance of mako sharks as by-catch in the longline fishery is evident in the
literature, both in scientific journals and the ICCAT data for the Atlantic. Given the
above, it is justified to conclude that most of the shortfin mako by-catch in the Pacific is
due to longline fishing effort.
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2. Supplementary Results
Female shortfin mako shark occurrence appeared to correlate negatively with SST (r =
0.431, p = 0.002; Fig. 1a). The negative correlation of female occurrence with SST was
inconclusive however because the vessel moved north into warmer waters only in the
eastern sector where females predominated, which increases the likelihood of a
significant correlation that was not independent of the bias associated with the vessel’s
track.
3. Supplementary Discussion
3.1 Spatial and Temporal Segregation
Spatial sexual segregation is where the sexes differ in their area use, whereas temporal
sexual segregation is when sexes use the same area but at different times (Conradt 2005).
However, spatial and temporal segregation are not mutually exclusive as both types of
segregation have a spatial pattern albeit at different time scales. Where temporal
segregation occurs across a longer time frame, for example as a result of sex-specific
seasonal movements to feeding or breeding areas, a ‘spatial segregation’ pattern could
potentially emerge as a result of progressive sampling of temporally sexually segregated
individuals. Under such conditions, one might conclude that the sexes were spatially
segregated throughout the year, even if the pattern of sexual segregation observed were
actually produced by temporal effects.
In this study, differentiating between these segregation types is not straightforward
since pelagic shark sex ratios were not sampled at the same time at all locations
(something which no high-seas surveys can achieve for logistical reasons). Therefore,
even though our survey occurred over a 4-month period and, for all but a week at the start
of March, was within a single summer season (9th Dec 2004 to 9th Mar 2005), there is
still a chance, however small, that females, for example, were present in the western
sector of the total area along with males during December when we were not sampling
there, but were not present (presumably due to migration or dispersal) by the time we
reached that location. However, regardless of whether spatial sexual segregation in mako
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sharks is temporal in nature, males were more abundant in this area at this time, and so
the potential of sex-biased exploitation still exists.
The likelihood of such wide-ranging, synchronous mass movement by female mako
sharks within a season seems unlikely given what is known about movements of mako
sharks. Obviously it was not possible for us to sample all locations within our study area
at the same time using a single ship (the study area being larger than the size of the
continent of Australia, by comparison). However, we examined the transition periods
over which there was greatest change in sex ratio to determine the timescale over which
the switches from females to males and back again occurred (as the ship traversed the
study area). One interpretation would be that if transitions occurred over too short a time
period within the core summer months it would be unlikely to be consistent with a solely
temporal pattern of sexual segregation because the following would have to be supported:
when the ship started sampling in the eastern sector, males had already moved out
leaving mainly females, whereas when the ship arrived into the western sector the
majority of females were absent leaving predominantly males, which continued until the
northern part of the eastern sector was visited, by which time nearly all males assumed to
have been there, had moved somewhere else.
Analysis of sex ratio transitions showed the short temporal scale and relatively large
spatial scale over which major changes were observed (Supplementary Fig. 4). The
change from roughly equal numbers of males and females being captured (0.46
proportion female) on 10 Jan 2005 to zero proportion of females on 18 Jan 2005 (and
consistently thereafter) would imply, if temporal segregation were the primary
mechanism underlying the pattern, that over this eight day period all females in the
vicinity (at least 400 km) moved from the western half of the study area (Supplementary
Fig. 4). Similarly, the change from zero females to about a 0.7 proportion of females
occurred over a three-week period (24 days) and over a distance of nearly 1300 km
(Supplementary Fig. 4). This could imply that, not only had all the females returned to
the study site over this time, but that the majority of males moved out of the eastern half
of the study site.
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The putative large-scale movements of males and females over periods between 8 and
24 days within two core summer months (January and February) that would be needed to
support the idea of solely temporal sexual segregation accounting for our observations,
are inconsistent with the timing and scale of known mako movements and distribution
changes. Tagging studies in the North-west Atlantic show that although shortfin mako
sharks are capable of making extensive movements of up to 4,542 km, they occupy
specific areas seasonally with most recaptures (64 %) being made within 552 km of the
tagging site (Casey & Kohler 1992). In the North-west Atlantic during summer this
species remains on the eastern U.S. continental shelf between Cape Hatteras and the
southern Gulf of Maine, a region thought to comprise primary feeding grounds for mature
animals as well as for juveniles and subadults. Tagging data from the Pacific also show
extensive movements are possible, although most tag returns from New Zealand and
southeast Australia were restricted to the southwest Pacific (Stevens 2008, and references
therein). Although little is known about sex differences in distributions and movements,
the tagging studies suggest that rapid, highly synchronous, large-scale movements at the
temporal scale of 1 and 3 weeks within the core summer months have not been
demonstrated previously. Indeed, this specific type of within-summer migration as a
consequence of temporal sexual segregation or otherwise has not been observed, to our
knowledge, in any large, pelagic shark species (Camhi et al. 2008), even for those where
temporal sexual segregation was suggested to be a principal driving factor underlying
space use patterns (e.g. Robbins 2007). Therefore, it seems that spatial segregation, at
least at the seasonal scale, may be the main effect contributing to the observed pattern of
sexual segregation in mako shark, and which can most reasonably explain the abrupt sex
ratio transitions observed in this study. Although temporal effects cannot be entirely
discounted, they are unlikely to be dominant over the temporal scale investigated here.
3.2 Sexual Segregation and Fishing
It was not possible to match temporal scales of mako shark sexual segregation (observed
over 4 mo) with fishing activity (averaged over 55 yrs) due to a lack of data, so the
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fishing intensity gradient in the southeast Pacific could be less marked in the short term.
Nonetheless, fisheries are known to be spatially heterogeneous over seasonal scales (a
few months) (Witt & Godley 2007) so the potential for differential exploitation of mako
shark sexes is possible if the seasonal pattern occurs annually.
References
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tuna fisheries: a review of SPC data holdings and literature. Technical Report, Oceanic
Fisheries Programme No. 34. Noumea, New Caledonia: South Pacific Commission.
Baum, J. K., Myers, R. A., Kehler, D. G., Worm, B., Harley, S. J. & Doherty, P. A. 2003
Collapse and conservation of shark populations in the northwest Atlantic. Science 299,
389-392.
Camhi, M.D., Pikitch, E.K., Babcock, E.A., eds. 2008 Sharks of the open sea: biology,
fisheries and conservation. 502 pp. Oxford, UK: Blackwell.
Casey, J. G. & Kohler, N. E. 1992 Tagging studies on the shortfin mako shark (Isurus
oxyrinchus) in the western North Atlantic. Aust. J. Mar. Freshwater Res. 43, 45-60.
Conradt, L. 2005 Definitions, hypotheses, models and measures in the study of animal
segregation. In Sexual segregation in vertebrates: ecology of the two sexes (ed. K. E.
Ruckstuhl & P. Neuhaus), p.11-32. Cambridge, UK: Cambridge University Press.
Robbins, R.L. 2007 Environmental variables affecting the sexual segregation of great
white sharks Carcharodon carcharias at the Neptune Islands South Australia. J. Fish.
Biol. 70, 1350-1364.
Roman-Verdesoto, M. & Orozco-Zoller, M. 2005 Bycatches of sharks in the tuna purseseine fishery of the Eastern Pacific Ocean reported by observers of the Inter-American
Tropical Tuna Commission, 1993-2004. Inter-American Tropical Tuna Commission
(IATTC), Data Report 11. La Jolla, California: IATTC.
Simpfendorfer, C.A., Hueter, R.E., Bergman, U., Connett, S.M.H. 2002 Results of a
fishery-independent survey for pelagic sharks in the western North Atlantic, 1977-1994.
Fish. Res. 55, 175-192.
Stevens, J.D. 1990 Further results from a tagging study of pelagic sharks in the Northeast Atlantic. J. Mar. Biol. Ass. U.K. 70, 707-720.
Stevens, J.D. 2008 The biology and ecology of the shortfin mako shark, Isurus
oxyrinchus. In Sharks of the open sea: biology, fisheries and conservation (ed. M.D.
Camhi, E.K. Pikitch & E.A. Babcock), p. 87-94. Oxford, UK: Blackwell.
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Witt, M.J. & Godley, B.J. 2007 A step towards seascape scale conservation: Using vessel
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doi:10.1371/journal.pone.0001111.
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Table 1. Diet composition of male and female shortfin mako shark Isurus oxyrinchus
from the southeast Pacific Ocean. A multivariate randomisation procedure (ANOSIM)
showed no significant differences in diet between the sexes (R = 0.017, p = 0.195). Raw
data were used in the statistical test not the summary data given here.
Proportion of total stomach contents (%)
Prey type
Male (n = 264)
Female (n = 132)
Mean
S.D.
Mean
S.D.
Cephalopods
34
0.34
31
0.34
Pelagic fish
16
0.25
10
0.21
Tuna
12
0.21
17
0.27
Non-identified teleosts
24
0.29
22
0.30
Demersal fish
4
0.12
2
0.09
Invertebrates
4
0.12
3
0.12
Other remains
3
0.11
8
0.19
Cetaceans
3
0.11
7
0.17
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(a)
(b)
Supplementary Figure 1. (a) Histograms of number of male (white) and female (black)
shortfin mako sharks captured in each of 72 longline sets from 9th December 2004 to 9th
March 2005 in the southeast Pacific Ocean. (b) Linear regression of mako sex ratio
(presented as proportion female; all female = 1.0) against longitude showing a significant
shift from females in the east to males in the western part of the study area (linear
regression analysis: proportion female vs longitude; r2 = 0.56, F = 88.34, p < 0.0001).
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(a)
(b)
Supplementary Fig. 2. (a) Capture locations of adult male (white; n=227) and female
(black; n=15) shortfin mako shark and (b) adult male (white; n=420) and female (black;
n=64) blue shark in the southeast Pacific Ocean with respect to seabed bathymetry.
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Supplementary Figure 3. Capture locations of male (white; n=264) and female (black;
n=132) shortfin mako sharks in the southeast Pacific Ocean with respect to a false colour
remote-sensing image of chlorophyll ‘a’ concentration.
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Supplementary Fig. 4. Time scales and distances over which changes in the proportion
of female mako captured occurred showing two distinct, short-term (8 and 24 d)
transition periods (T1 and T2). Proportion female (all female = 1.0) is the running mean
of this measure across five consecutive longline sets.
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