1. 1 23
Coral Reefs
Journal of the International Society for
Reef Studies
ISSN 0722-4028
Coral Reefs
DOI 10.1007/s00338-016-1437-9
Indicators of fishing mortality on reef-
shark populations in the world’s first shark
sanctuary: the need for surveillance and
enforcement
Gabriel M. S. Vianna, Mark G. Meekan,
Jonathan L. W. Ruppert, Tova
H. Bornovski & Jessica J. Meeuwig

2. 1 23
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3. NOTE
Indicators of fishing mortality on reef-shark populations
in the world’s first shark sanctuary: the need for surveillance
and enforcement
Gabriel M. S. Vianna1,2 • Mark G. Meekan2 • Jonathan L. W. Ruppert3 •
Tova H. Bornovski4 • Jessica J. Meeuwig1
Received: 30 March 2015 / Accepted: 14 March 2016
Ó Springer-Verlag Berlin Heidelberg 2016
Abstract Shark sanctuaries are promoted as a manage-
ment tool to achieve conservation goals following global
declines of shark populations. We assessed the status of
reef-shark populations and indicators of fishing pressure
across the world’s first shark sanctuary in Palau. Using
underwater surveys and stereophotogrammetry, we docu-
mented large differences in abundance and size structure of
shark populations across the sanctuary, with a strong neg-
ative relationship between shark densities and derelict
fishing gear on reefs. Densities of 10.9 ± 4.7 (mean ± SE)
sharks ha-1
occurred on reefs adjacent to the most popu-
lated islands of Palau, contrasting with lower densities of
1.6 ± 0.8 sharks ha-1
on remote uninhabited reefs, where
surveillance and enforcement was limited. Our observa-
tions suggest that fishing still remains a major factor
structuring shark populations in Palau, demonstrating that
there is an urgent need for better enforcement and
surveillance that targets both illegal and licensed com-
mercial fisheries to provide effective protection for sharks
within the sanctuary.
Keywords Marine protected area Á Derelict fishing gear Á
IUU fishing Á Underwater visual survey Á Palau shark
sanctuary
Introduction
Growing recognition of the urgent need to conserve shark
populations has led some nations to declare nationwide
shark sanctuaries (Davidson 2012; Chapman et al. 2013).
Typically, these sanctuaries ban shark fishing, trade, and
exports of shark parts and products within parts or
throughout territorial waters and Exclusive Economic
Zones (EEZs) (Davidson 2012; Techera 2012). In general,
both traditional artisanal practices and fisheries targeting
other species of commercial importance such as tunas and
reef fish are still permitted within the sanctuary; however,
some of these fisheries may still capture sharks as bycatch.
The large spatial scale (thousands to millions of km2
) of
sanctuaries and the remoteness of their islands and reefs
from major centres of population present a challenge for
surveillance and enforcement. This can require a level of
infrastructure (vessels, planes, etc.) that is often beyond the
capacity of many of the small island nations where sanc-
tuaries have been established (Bergin 1988; Techera 2012).
In areas where enforcement is deficient, remoteness from
human populations might provide some degree of protec-
tion for sharks (Ward-Paige et al. 2010; Nadon et al. 2012).
However, modern fishing fleets can reach virtually any area
of the ocean, and illegal, unreported, and unregulated
Communicated by Ecology Editor Dr. Alastair Harborne
Electronic supplementary material The online version of this
article (doi:10.1007/s00338-016-1437-9) contains supplementary
material, which is available to authorized users.
& Gabriel M. S. Vianna
gabe.vianna@gmail.com
1
School of Animal Biology, The UWA Oceans Institute, The
University of Western Australia, 35 Stirling Hwy, Perth,
WA 6009, Australia
2
Australian Institute of Marine Science, The UWA Ocean
Institute (MO96), 35 Stirling Hwy, Perth, WA 6009,
Australia
3
Department of Renewable Resources, University of Alberta,
823 General Services Building, Edmonton, AB T6G 2H1,
Canada
4
Micronesian Shark Foundation, P.O. Box 964, Koror 96940,
Palau
123
Coral Reefs
DOI 10.1007/s00338-016-1437-9
Author's personal copy

4. (IUU) fishing is likely to be most intense in remote areas
that lack the capacity to enforce protection (Agnew et al.
2009).
Uncertainties about enforcement capacity have gener-
ated debate regarding the effectiveness of large sanctuaries
as a tool to protect sharks (Davidson 2012; Rife et al. 2012;
Chapman et al. 2013; Dulvy 2013), an issue that is fuelled
by the lack of baseline surveys of shark populations, fish
assemblages, and benthos within most sanctuaries. This
paucity of baseline data makes it very difficult to determine
whether the creation of a sanctuary has resulted in the
recovery of shark populations that were once subjected to
fishing and if so, whether there have been any concomitant
changes in the resilience or structure of reef communities.
In 2009, Palau declared the world’s first national shark
sanctuary, prohibiting commercial shark fishing within an
area of 629,000 km2
. Reefs and islands are spread
throughout much of this sanctuary, and it is situated in a
region of intense commercial fishing, where tuna and
sharks have been targeted by regional and international
fleets (Bromhead et al. 2012). Furthermore, Palau borders
Indonesia, a leading shark-fishing nation where shark
populations have been severely depleted, and cross-border
IUU fishing is a major problem (Agnew et al. 2009; Field
et al. 2009; Varkey et al. 2010). These factors suggest that
shark populations within the sanctuary in Palau may
experience some level of illegal fishing pressure, particu-
larly on isolated reefs where enforcement is costly and
logistically challenging.
Here, we used underwater surveys as a fishery-inde-
pendent method to assess the status of reef-shark popula-
tions in Palau 4 yr after the establishment of the shark
sanctuary. Our main objectives were to (1) quantify dif-
ferences in density and size of reef sharks across the
sanctuary, and (2) identify environmental and anthro-
pogenic variables that could potentially explain demo-
graphic patterns. Our study provides the first broad-scale
assessment of the status of reef-shark populations follow-
ing the establishment of a nationwide shark sanctuary.
Methods
Study area
Palau is an archipelago consisting of the Main Island
Group (MIG) and the Southwest Islands (SI), the latter a
collection of relatively isolated oceanic islands and atolls in
the southern part of the country (Fig. 1). The MIG is
comprised of a complex of volcanic and limestone islands
and a large shallow lagoon (*40 m deep) that is sur-
rounded by a barrier reef extending for approximately
260 km (Colin 2009). The SI are situated between 300 and
500 km from the MIG and are composed of a true atoll
(Helen Reef) and five low islands that are surrounded by
coral reefs with relatively narrow reef flats and steep
slopes. In 2012, the population of Palau was approximately
17,500 inhabitants and the country received 124,000 visi-
tors, almost all of whom stayed on the central part of the
MIG (Anon. 2013). Reports describe human populations in
the SI of several hundred people in the early 1900s (Jo-
hannes 1981); however, the current population in this
region is restricted to approximately 25 inhabitants, the
majority residing at Tobi Island (SEDAC 2013).
Sampling methodology
In June and October 2012, we sampled three reefs in the
MIG (North, Central, and South) and four reefs in the SI
(Helen, Tobi, Merir, and Pulo Anna). On each reef, we
conducted one belt transect dive at each selected site,
averaging 5.3 and 4.5 dives in the MIG (n = 16) and SI
(n = 18), respectively (Electronic Supplementary Material,
ESM, Fig. S1). Sites in the MIG were distributed to cover
the latitudinal range of the entire barrier reef (mainly on the
west side). Each belt transect was 300 m in length and was
placed on the fore reef at depths of 9–15 m. All shark
Fig. 1 Reefs and islands of the Main Island Group and Southwest
Islands in the Palau shark sanctuary
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5. density estimates were standardised by the area covered by
the belt transect (see ESM Additional methods). During the
dives, we employed stereo video cameras to collect footage
of all sharks sighted so that we could obtain accurate
measures of total length using the software EventMeasure-
Stereo (http://www.seagis.com.au). We were able to dif-
ferentiate among multiple sharks sighted on the same
transect in the video footage and therefore mitigate the risk
of counting of the same individuals multiple times.
Following the dives, we conducted 212 manta tow
transects to quantify the amount of derelict fishing gear
entangled on the reefs where belt transects were completed.
On each 5-min manta tow, the observer recorded the
number of distinct items of fishing gear entangled on the
reef at depths between 5 and 15 m. We estimated the
density of derelict fishing gear as the number of items
recorded in each transect divided by the area covered.
Anthropogenic and environmental variables
We calculated the total number of people living within a
radius of 10, 50, and 200 nautical miles (nm) of each reef
(SEDAC 2010) as a measure of potential anthropogenic
stressors on reef-shark populations. Mean density of
chlorophyll a (as an indicator of primary productivity),
yearly average sea surface temperature, and percentage
categorised benthic cover within each transect (see ESM
Additional methods) were used to assess the potential
influence of environmental variables and habitat on the
density and size of sharks.
Data analysis
We used permutated t tests (n = 9999) to investigate dif-
ferences in density and size structure (total length) of reef
sharks in the MIG and the SI. We only analysed size
structure data of grey reef sharks as the frequency of
sightings of other species within the SI was too low to
allow size comparisons between the two regions. We used
simple linear regression to model shark density (species
combined) as a function of the effects of environmental
parameters and anthropogenic stressors among reefs. Reef
sharks have home ranges in the order of tens of km2
(Speed
et al. 2010), meaning that for some of the reefs sampled in
our study, the home range might encompass the entire reef
(ESM Tables S1, S2). For this reason, the regression
analysis was conducted at the level of reef rather than site.
This was appropriate as data on human densities were also
available at the same scale. The MIG sites were divided
into three areas to reflect the considerable variation in
human density and possible environmental differences
among these areas. Finally, prior to analysis, shark densi-
ties were log-transformed to meet the assumptions of linear
regression (Zar 1999). All analysis was conducted in R
software (R Development Core Team 2010).
Results and discussion
We observed a mean density (species combined, ±SE) of
6.0 ± 2.4 sharks ha-1
across all sampled sites. The average
density of sharks in the SI (1.6 ± 0.8 sharks ha-1
) was
significantly lower (by an order of magnitude, t34 = 2.46,
p = 0.02) than in the MIG (10.9 ± 4.7 sharks ha-1
). The
mean total length of grey reef sharks (n = 47) was
121 ± 46 cm, with sharks from the SI significantly smaller
(85 ± 11 cm, t47 = 4.09, p = 0.003) than those in the
MIG (124 ± 5 cm).
Our analysis also revealed a strong and negative rela-
tionship between the density of reef sharks and derelict
fishing gear on reefs (p = 0.002, R2
= 0.85; Fig. 2). The
greatest density of derelict gear of 0.3–1 item ha-1
(25%
nets and 75% longlines; the latter were relatively free of
fouling) was associated with the lowest densities of sharks
of 0–0.7 sharks ha-1
at Pulo Anna and Helen Reef,
respectively. Conversely, we found little relationship
between shark densities and the remaining anthropogenic
and environmental variables at the whole-reef scale (ESM
Table S2).
Reductions in the density and mean size of individuals
are acknowledged indicators of fishing impacts on shark
populations (Stevens et al. 2000). Combined with our data
on derelict fishing gear, which is a useful proxy for illegal
fishing effort on coral reefs (Williamson et al. 2014), these
results suggest that fishing has been and may continue to be
a major factor shaping patterns in abundance and size
structure of the populations of sharks across the Palau
shark sanctuary.
It was not possible to determine whether our results
were a function of a legacy of fishing that predates
implementation of the sanctuary, or reflect an ongoing
issue. Given that many shark species have conservative life
history traits, it is likely that the short period of time since
implementation of the sanctuary (4 yr) may be insufficient
to allow the recovery of shark populations (Edgar et al.
2014), and thus the low densities of sharks in the remote
areas represent a legacy effect to some extent. However,
reports by local rangers of frequent sightings of IUU ves-
sels targeting reef fishes and sharks and the record of a
shark recently caught in derelict fishing gear on our surveys
(ESM Fig. S2) suggest that illegal fishing is causing
ongoing impacts on shark populations on remote reefs.
Our observations of greater shark densities on reefs
adjacent to relatively large human populations contrast
with surveys in the Pacific and Caribbean, where there are
usually negative correlations between the density of reef
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6. sharks and the presence of humans (Ward-Paige et al.
2010; Nadon et al. 2012). This may reflect differences in
human behaviour as local populations are engaged in shark
fishing in many countries across the Pacific and the Car-
ibbean. In Palau, fishing by the local population does not
generally target sharks, and the proximity of populated
areas, the presence of local boats, and vessel traffic may in
fact deter foreign vessels from fishing illegally. The pres-
ence of people may also explain the relatively high density
of sharks observed at Tobi (Fig. 2), the only island of the
SI that hosts a significant resident population. Furthermore,
the occurrence of regular shark-diving operations in the
MIG (Vianna et al. 2014) is also likely to reduce the risk of
illegal fishing in areas around dive sites (Steenbergen
2013). However, while the sale of shark products is illegal
in Palau, citizens are still permitted to fish for sharks within
most of the sanctuary. Since fisheries inspection and
enforcement is limited, the trade in shark products should
be monitored closely as local demand for products may
increase with growing tourism from Asia.
Similar to other island nations, Palau has limited
infrastructure capacity to enforce fishery regulations across
the entire EEZ, which places obvious restrictions on the
ability of the nation to apprehend illegal fishers. Moreover,
while the commercial tuna fishery operating in Palau is
forbidden from targeting and retaining sharks, relatively
high mortality of sharks as bycatch ([20%, including reef
sharks) is still likely to occur (Bromhead et al. 2012). Thus,
legal commercial fishing may also contribute to the patterns
in abundance of reef sharks we recorded. However, the very
low observer coverage of the international longline fleet
operating in Palau ([5% coverage; WCPFC 2015) prevents
determining the origin or the extent of this impact.
Our results are likely to be representative of other small
island states that have declared shark sanctuaries in the
Indo-Pacific (e.g., Maldives and Marshall Islands). Indeed,
Fig. 2 a Linear regression
showing the relationship
between log-transformed mean
density of reef sharks (species
combined) sighted in belt
transects and mean density of
derelict fishing gear entangled
on reefs (R2
= 0.85;
p = 0.002), MIG Main Island
Group. b Density of species of
reef shark on reefs in the MIG
and Southwest Islands
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7. issues involving IUU fishing, the enforcement of fishery
regulations, and the loss of shark resources may be even
greater in other nations, given that Palau is relatively
prosperous compared to many of its neighbours, and it has
a vibrant marine tourism industry where shark-diving
returns large amounts of revenue to the nation (Vianna
et al. 2012). Assuming that IUU fishing pressure has been
removed from a sanctuary, the recovery of reef-shark
populations in isolated areas, such as the SI in Palau, is
likely to be slow (decades) as a consequence of the low
rebound capacity of these species (Smith et al. 1998) and
the high levels of residency common to reef-shark popu-
lations (Vianna et al. 2013). Thus, although shark sanctu-
aries are a promising instrument for shark conservation,
there is an urgent need for better regulation, enforcement,
and surveillance that targets both illegal and licensed
commercial fisheries to provide effective protection for
sharks.
Lastly, baseline surveys must be an essential part of the
establishment of sanctuaries because without them, we lack
any means to judge the effectiveness of these areas as a
management tool or to identify problems that could be
hampering strategic goals. This point is relevant not just to
shark sanctuaries, but also to ongoing investment in the
establishment of large marine protected areas across the
world’s oceans.
Acknowledgments The authors acknowledge the Save Our Seas
Foundation and a private donor for financial support. We also thank
the staff and divers of Fish ‘n’ Fins and the Ocean Hunter III. We
acknowledge the support of Micronesian Shark Foundation and the
Koror State Rangers, in particular M. Moros, Bohemian Companies,
T. Wynn, and H. Wuyts. We are also thankful to N. Bornovski, J.
White, B. Oh, T. Hofmeister and F. Toribiong.
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