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RESEARCH ARTICLE
Satellite tagging of rehabilitated green sea
turtles Chelonia mydas from the United Arab
Emirates, including the longest tracked
journey for the species
David P. Robinson
1
*, Rima W. Jabado
2
, Christoph A. Rohner
3
, Simon J. Pierce
3
, Kevin
P. Hyland
4
, Warren R. Baverstock
1
1Jumeirah Group, Dubai, United Arab Emirates, 2Gulf Elasmo Project, Dubai, United Arab Emirates,
3Marine Megafauna Foundation, Truckee, California, United States of America, 4Wildlife Protection Office,
Dubai, United Arab Emirates
*sharkwatcharabia@gmail.com
Abstract
We collected movement data for eight rehabilitated and satellite-tagged green sea turtles
Chelonia mydas released off the United Arab Emirates between 2005 and 2013. Rehabilita-
tion periods ranged from 96 to 1353 days (mean = 437 ±399 days). Seven of the eight
tagged turtles survived after release; one turtle was killed by what is thought to be a post-
release spear gun wound. The majority of turtles (63%) used shallow-water core habitats
and established home ranges between Dubai and Abu Dhabi, the same area in which they
had originally washed ashore prior to rescue. Four turtles made movements across interna-
tional boundaries, highlighting that regional cooperation is necessary for the management
of the species. One turtle swam from Fujairah to the Andaman Sea, a total distance of 8283
km, which is the longest published track of a green turtle. This study demonstrates that sea
turtles can be successfully reintroduced into the wild after sustaining serious injury and
undergoing prolonged periods of intense rehabilitation.
Introduction
The green sea turtle Chelonia mydas (Linnaeus 1758) is found circumglobally in tropical and
subtropical waters. It is a highly migratory, long-lived species that is susceptible to anthropo-
genic pressures during all life-stages [1]. Green turtle populations around the world are declin-
ing due to harvesting for meat and eggs [2–6], incidental capture in both artisanal and
commercial fisheries [7,8], as well as habitat alteration, degradation and loss [9,10]. Despite
ongoing worldwide protection efforts spanning several decades, green turtles remain classified
as Endangered on the International Union for the Conservation of Nature (IUCN) Red List of
Threatened Species [1]. Furthermore, it has recently been suggested that traditional
approaches to estimation of numbers of nesting turtles may have led to a gross overestimation
by as much as 50%, further highlighting the ‘endangered’ status of this species [11]. On the
PLOS ONE | https://doi.org/10.1371/journal.pone.0184286 September 5, 2017 1 / 19
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OPEN ACCESS
Citation: Robinson DP, Jabado RW, Rohner CA,
Pierce SJ, Hyland KP, Baverstock WR (2017)
Satellite tagging of rehabilitated green sea turtles
Chelonia mydas from the United Arab Emirates,
including the longest tracked journey for the
species. PLoS ONE 12(9): e0184286. https://doi.
org/10.1371/journal.pone.0184286
Editor: Graeme Hays, Deakin University,
AUSTRALIA
Received: March 1, 2017
Accepted: August 20, 2017
Published: September 5, 2017
Copyright: ©2017 Robinson 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.
Data Availability Statement: All relevant data are
within the paper and its Supporting Information
files.
Funding: The Jumeriah Group provided support in
the form of research materials and salaries for
authors WRB and DPR but did not have any
additional role in the study design, data collection
and analysis, decision to publish, or preparation of
the manuscript. The specific roles of these authors
are articulated in the ‘author contributions section.
other hand, there have been a number of very encouraging conservation successes suggesting
upward trends in population sizes (e.g. Ascension Islands, [12]) and showcasing that reversing
declining trends in populations is possible.
The Arabian Gulf (hereby referred to as ‘the Gulf’) is located within a subtropical, hyper-
arid region. The Gulf is a shallow basin, bordered by Bahrain, Iran, Iraq, Kuwait, Oman,
Qatar, Saudi Arabia and the United Arab Emirates (UAE).
Within the Gulf, the green turtle has nesting sites in Saudi Arabia [13–15], Kuwait [16–18],
Iran [19], and the UAE [20]. The region is undergoing rapid economic growth, involving sub-
stantial construction in coastal and offshore regions [21]. The Gulf is the warmest sea in the
world [21] and environmental conditions within the Arabian Gulf are among the most
extreme on the planet [22].Although nesting sites have been monitored for many years, infor-
mation on the movement ecology of green turtles in Gulf waters is limited to a single study
that used satellite tracking in the northern waters of Kuwait [18]. Given that green turtles
spend the majority of their lives away from nesting sites, understanding their movements and
habitat use is essential to ensure appropriate management and protection for this Endangered
species [18,23].
Advances in satellite tracking technologies have led to improved insight into the life history
and behavior of many species [24,25] and facilitated the identification of critical habitats to
support management actions (e.g. [6,26–28]). For example, such studies have shown that
green turtles migrate from feeding grounds in Brazil to nesting grounds in the Ascension
islands, a distance of at least 2300 km [29–31]. Hays et al. [32] tracked eight green turtles from
the Chagos Archipelago and found that seven of them made journeys exceeding 1000km to
their foraging grounds.
Gilbert [33] states that the main objective of rehabilitating sea turtles is to contribute to
their conservation. Rehabilitation is particularly beneficial for sea turtles as they have a low
survival probability from egg to maturity; the rehabilitation of individuals that have survived
the high initial mortality rate is therefore considered demographically relevant [34]. However,
there is currently a gap in our understanding of post-rehabilitation integration back into the
wild and survival rate, with mixed results reported in the literature. Few studies have focused
on post-release behavior of rehabilitated turtles [33,34] with most turtle satellite tracking work
focusing on the post-nesting movements of adult females [25,35]. Godley et al. [35] suggest
that satellite tracking is a valid way of monitoring post-rehabilitation and release survival, and
that more information needs to be gathered on male and immature turtles. However, they
question the normality of the rehabilitated turtles’ post-release behaviour. Cardona et al. [36]
highlight the importance of understanding the ability of rehabilitated sea turtles to survive and
integrate back into the reproductive population successfully, not only to justify rehabilitation
efforts and costs, but also because rehabilitation centres often supply animals for satellite track-
ing studies [37,38]. Mestre et al. [34] state that post-release tracking of rehabilitated sea turtles
is a valid means to monitor the success of the rehabilitation process, while obtaining additional
information on their movements and behaviour.
Satellite tracking of rehabilitated turtles has produced mixed reports with regards to behav-
ior and integration back into the wild. Cardona et al. [36] satellite tracked 18 loggerhead Car-
etta caretta (Linnaeus, 1758) turtles off Spain, six of which had undergone ‘long and
complicated’ rehabilitation protocols. In a comparison to 12 control turtles, it was found that
two of the six rehabilitated animals did not differ from the control animals, but four animals
showed anomalies in one of the tested behavioral parameters. They concluded that rehabili-
tated turtles survive in the wild for at least a few months, but questioned their long-term re-
adaptation to natural conditions. Polovina et al. [39] found that satellite-tagged captive-raised
loggerhead turtles in Japan did not differ from wild individuals in their dispersal patterns.
Satellite tracking rehabilitated sea turtles in the UAE
PLOS ONE | https://doi.org/10.1371/journal.pone.0184286 September 5, 2017 2 / 19
WRB and DPR acted as independent researchers
throughout this study. The journal publication fees
for this manuscript were provided by the Jumeirah
Group. All other collaborators, had no role in the
preparation or decision to publish the manuscript.
Competing interests: The Jumeriah Group
provided support in the form of research materials
and salaries for authors WRB and DPR but did not
have any additional role in the study design, data
collection and analysis, decision to publish, or
preparation of the manuscript. The specific roles of
these authors are articulated in the ‘author
contributions section. WRB and DPR acted as
independent researchers throughout this study.
The journal publication fees for this manuscript
were provided by the Jumeirah Group. All other
collaborators, had no role in the preparation or
decision to publish the manuscript. The
commercial affiliation for this project does not alter
our adherence to PLOS ONE policies on sharing
data and materials.
Nichols et al. [40] reported that a loggerhead turtle, shown to be of Japanese origin through
genetic analysis but captured from the wild as a juvenile off the Pacific coast of Mexico,
migrated back to Japan from Mexico after 10 years in captivity. These studies generally indi-
cate that periods of captivity are unlikely to lead to major differences in post-release foraging
or navigation [36]. Rees et al. [18] tracked three green turtles in the Gulf, two of which were
rehabilitated animals, and found these turtles moved to foraging sites and developed similar
home ranges, suggesting survival and successful re-integration of the rehabilitated animals. In
addition, a large number of rehabilitated sea turtles have been satellite-tracked from Naples,
Italy and, these animals were used to investigate diving behaviour and seasonal changes
[38,41–43]. Mestre et al. [34] satellite tagged two green and one loggerhead turtle after long
periods of captivity (up to 30 years) off Portugal. These turtles moved towards known feeding
locations for both species, suggesting successful reintegration into the wild.
The Dubai Turtle Rehabilitation Project (DTRP), based in the UAE, has been running in its
current form since 2004 and receives and treats sick or injured turtles from countries sur-
rounding the Gulf [44]. Satellite-tagging of rehabilitated green turtles by the DTRP has been
ongoing since 2005. Here we present data on the spatial ecology, post-release behavior and
thermal environment data of eight rescued and rehabilitated sub-adult and adult green turtles
released after varying periods in captivity.
Materials and methods
Study area
The Gulf is a shallow, almost enclosed sea experiencing low precipitation and high evaporation
rates which lead to salinities reaching over 39 ppt. The average depth is 30 m, gradually becom-
ing deeper to 100 m as it approaches its entrance at the narrow Strait of Hormuz [45–47]. Air
temperatures in the region can drop to 0˚C in the winter and reach in excess of 50˚C in the
summer, resulting in fluctuations in nearshore waters of up to 29˚C over the year, from 10˚C
in winter to 39˚C in summer. Deeper waters vary between 18˚C and 33˚C [48]. Despite these
physical extremes, the Gulf is a highly productive and diverse basin, supporting important
habitats such as seagrass beds, mangroves, salt marshes and coral reefs [45,48]. The UAE lies
along the southeastern coast of the Gulf, and has two separate coastal areas: the low, sandy
Gulf coast, and the rocky and somewhat steep Gulf of Oman coast [49].
Study animals
Permissions for sea turtle rehabilitation work were given by the Dubai Wildlife Protection
Office with whom this work was conducted. Eight green turtles C.mydas were brought to the
DTRP between 2004 and 2011 for rehabilitation from debilitation or infection resulting from
‘cold stunning’ [50] in the winter months (n = 4); severe injuries (n = 3) thought to be caused
by propeller impact; intentional anthropogenic injuries or entanglement; and intestinal impac-
tion (n = 1) (Table 1).
Adult sea turtles are sexually dimorphic, with mature males possessing a long prehensile tail
[51]. After internal examination, tail length is the main secondary sexual characteristic of adult
sea turtles and has been routinely used to successfully determine the sex of mature animals
[52]. Miller (2011) summarized the morphometrics of nesting turtles from records of 2,844
nesting green turtles examined along the Saudi Arabian Gulf coast and found that the mean
curved carapace length (CCL) of these adult females ranged between 73–114cm CCL. Rees
et al. [18] recorded a CCL of 98.2 and 96cm for nesting females satellite tagged in Kuwait. Our
study animals were classified using their CCL and tail length as either sub-adult (<70 cm) or
Satellite tracking rehabilitated sea turtles in the UAE
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adult (>90 cm) females and ranged in weight from 25 to 150 kg. The adult turtles (n = 3) were
all female based on their short tails. Individuals deemed immature could not be sexed.
Rehabilitation and release
Turtles in this study underwent rehabilitation for 96 to 1353 days (mean = 437 ±399 days).
Individual rehabilitation protocols were determined by the ailment or injuries suffered, but
common treatments while in captivity included rehydration, force-feeding, antibiotic treat-
ment, vitamin and mineral treatment, anti-parasite treatment for debilitation [44], and surgi-
cal procedures as detailed in [53] and [54].
All animals were moved into a sea-fed outdoor enclosure and observed for at least two
months prior to release. Turtles were evaluated for active feeding and swimming ability, and
given a physical health assessment to ensure they met the criteria for release described in [55].
A blood sample was also taken from each turtle and tested for normal parameters using meth-
ods and tests reported in [44]. Each turtle was considered fit by all these standards at their time
of release.
Tag deployment
Turtles were released and tracked between January 2005 and April 2013. Sirtrack tags (n = 4)
were used until 2010, after which four Wildlife Computers SPOT5 back-mount tags were used.
Both tag models estimated location through the Argos satellite system operated by CLS Argos
(http://www.argos-system.org). Tags were attached to the carapace using a base of marine
putty and covered with a slow-hardening, low temperature-generating epoxy. Once the putty
and epoxy were hard, the tags and exposed epoxy were painted with a black copper-based
Table 1. Summary of rehabilitation information and resulting tracking data for green sea turtles C.mydas released in UAE waters. Minimum bound-
ing geometry (MBG) and percentage volume contours (PVC) are provided for turtles that remained in the Gulf.
Turtle
Name
Transient
/Resident
Sex / Life
Stage
Ailment
on receipt
Rehab
Duration
(days)
Release
Weight
(kg)
Curved
Carapace
Length
(cm)
Maritime
Boundaries
Entered
Tracking
Duration
(days)
Distance
traveled
(km)
MBG
(km
2
)
PVC
95%
(km
2
)
PVC
50%
(km
2
)
Dibba Transient Female /
Adult
Injury 546 80 93 ■UAE
■Oman
■Maldives
■Sri Lanka
■India
259 8283 NA NA NA
Maju Transient Unknown /
Sub-Adult
Infection 96 25 56 ■UAE
■Iran
■Pakistan
47 992 NA NA NA
Lepi Transient Unknown /
Sub-Adult
Injury 499 25 57 ■UAE
■Iran
284 1123 16382 657 69
Jade Resident Female /
Adult
Infection 275 150 115 ■UAE
■Iran
310 2450 18057 568 8
Moonlight Resident Unknown /
Sub-Adult
Infection 203 32 58 ■UAE 141 190 2564 709 56
Emerald Resident Unknown /
Sub-Adult
Injury 1353 37 70 ■UAE 220 1086 1591 529 61
Bahar Resident Unknown /
Sub-Adult
Infection 263 36 70 ■UAE 52 853 9635 5023 112
Belle Resident Female /
Adult
Impaction 262 58 90 ■UAE 112 9 1813 854 15
Mean for resident turtles 8340 ±
7514
2154
±
1783
29 ±
38
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antifouling paint produced by Interlux, leaving a non-painted distance of 1 cm around the
tag’s saltwater switches.
All tags had a 45 second Argos transmission repetition period with a limit of 250 transmis-
sions per day. Sirtrack tags were programmed by the manufacturer and duty cycled to transmit
at sunrise through to sunset for UAE local time. Deployed Sirtrack tags were not capable of
collecting information on temperature. Wildlife Computers SPOT5 tags were programmed
using the manufacturer-provided software and duty cycled to transmit from sunrise to sunset
for UAE local time. Each Wildlife Computers tag was programmed to record 12 temperature
bins ranging from 9˚C to 39˚C in 3˚C increments and form two sets of 12-hour histogram
data, one for local daylight hours and one during the hours of darkness. All temperatures
above 39˚C were included in the final temperature bin, while all temperatures below 12˚C
were included in the first bin.
Satellite-data filtering and analysis
Tags included an Argos transmitter and used standard Doppler-based geolocation to track the
position of the turtle. An accuracy estimate was assigned and a location class was then given by
the Argos system (A, B, 0, 1, 2, 3). Class A and B are not given an error estimate by the Argos
system, however, class 0, 1, 2 and 3 have an estimated accuracy of >1500 m, >1000 m, >500
m, >150 m, respectively. To facilitate regular data downloads from the Argos system, accounts
were set up through the www.seaturtle.org Satellite Tracking and Analysis Tool (STAT). The
STAT automatically collected daily Argos data and stored these data online. Data transmitted
by each satellite tag were checked for multiple daily and maximum transmission records and
static temperature data that could be indicative of a floating tag. The STAT bathymetry data
were then used to calculate the distance travelled between transmission points and to extrapo-
late the water depth at the location of tag transmission.
The Douglas filter was applied to the data in Movebank (www.movebank.org) to further
improve the accuracy of location data [56]. This filter is based on a Maximum Redundant Dis-
tance (MRD) to remove unrealistic locations and in addition a Distance, Angle and Rate (DAR)
filter was used. The MRD filter retains locations that are near-consecutive within a defined dis-
tance threshold [56]. All Argos locations B grade and more accurate were included in the analy-
sis with locations given an accuracy estimate of 1, 2 and 3 always retained. Locations with
duplicate timestamps were removed. A MRD radius of 10 km was set along with a maximum
realistic rate of movement was set at 5km/h as recommended in [57]. A turning angle filter of
25˚ was also used to remove any extreme changes in direction as in [18,58–61]. A mean of 5 ±
4% of outlying data were removed by the filter (n = 8; median = 5%; range 1 – 13%).
Home range analysis
All filtered tag locations were input to ArcGIS 10.2.1 from Movebank. The “kernel density
tool” was used to calculate percentile kernels of location density. Percentage Volume Contours
(PVC) representing 50% and 95% of locations were produced in ArcGIS 10.2.1 from the previ-
ously produced kernels, using the “Spatial Analyst” and “Reclassify tool” and, following meth-
odology outlined in [62]. The “map algebra” and “raster calculator” tools in ArcGIS 10.2.1
were used to investigate how many individuals used a specific location within their home
ranges as described in [62]. Turtles were categorised as transient if they moved out of UAE
waters for 10 or more days, or resident if they stayed within the UAE’s maritime boundaries.
Part of the final home range of one turtle (‘Bahar’) was been excluded from these analyses
since this individual was recovered from the western region of the UAE after washing up on
the shore with a fatal injury thought to be from a speargun.
Satellite tracking rehabilitated sea turtles in the UAE
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Temperature
Water temperature was collected daily in the early morning by internal thermometer in front
of the extraction point from the Dubai Madinat Jumeirah coastal water pumps, located ~100
m from the shoreline and intake, from a depth of ~10 m. To investigate temperature related
movements in coastal locations, a linear regression was fitted to daily coastal water tempera-
ture data and water depth at transmission locations (n = 327) for all five resident green turtles.
Results
Tracking
Tracking duration ranged between 47 and 310 days with a mean of 178 ±104 days
(median = 181, n = 8) and distances travelled ranged between 190 and 8283 km with a mean of
1988 ±926 km (median = 1039, n = 8) (Table 1). Minimum bounding geometry for turtles
that remained within the Gulf ranged between 1591 and 18057 km
2
with a mean of 8340 ±
7514 (median = 6100, n = 6). For approximately three days’ post-release, turtles usually trav-
elled slowly or stayed offshore of the release point. After this period, most turtles moved away
in an increasingly focused direction.
Horizontal movements
Seven turtles were recovered from the west coast of the UAE and released back into the same
body of water (Gulf) while one turtle was recovered from, and released on, the east coast (Gulf
of Oman). Five turtles remained resident in UAE waters over the duration of tracking. Four of
these, ‘Emerald’, ‘Belle’, ‘Bahar’ and ‘Moonlight’, chose core habitats on the coast of the UAE
between Abu Dhabi and Dubai and did not leave the area.
The home range area for resident turtles ranged between 529 and 5023 km
2
with a mean of
1536 ±1953 km
2
(median = 709, n = 5). The core habitat area for resident turtles ranged
between 8 km
2
and 112 km
2
with a mean of 50 ±42 km
2
(median = 56, n = 5). Transient ani-
mals did not form a definitive home range or core habitat area. Both transient (197 ±130,
median = 259 days, n = 3) and resident (167 ±100, median = 141 days, n = 5) turtles had a sim-
ilar mean tracking duration.
The female adult turtle, ‘Jade’, also formed a small core habitat (8 km
2
) in the Ghantoot
area. During her tracking, she made a highly directional journey across the Gulf to Qeshm
Island in Iranian waters (Fig 1B). The crossing took 11 days, following which she spent 14 days
around Qeshm Island. She then travelled back to her previous small core habitat area over a
period of 10 days. Tracking ended 18 days after Jade’s return to her Ghantoot core habitat
area. This journey resulted in a large minimum bounding geometry (18057 km
2
) and home
range (568 km
2
) for this individual.
Sub-adults ‘Lepi’ and ‘Maju’ were transient: ‘Lepi’ crossed the Gulf, spending a significant
amount of time in Iranian waters, while ‘Maju’ crossed the Gulf into Iranian waters, then trav-
elled through the Strait of Hormuz and out into the Gulf of Oman. ‘Maju’ remained close to
the coastline, and the last transmission was made just after crossing the maritime boundary
into Pakistani waters (Fig 1A).
Dibba
‘Dibba’ was found on the east coast of the UAE in August 2006 with massive head trauma,
believed to be intentional and anthropogenic in origin, and was close to death upon arrival at
the DTRP. Her rehabilitation took 546 days with treatment given for both the original injury
and subsequent illnesses associated with her head trauma. After being monitored for several
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months in a large sea-fed enclosure, ‘Dibba’ was released close to the area where she was found
in February 2008. ‘Dibba’ travelled 8283 km from the UAE, to Omani waters, crossing the Ara-
bian Sea to the Maldives, before proceeding to Sri Lanka and entering the Bay of Bengal where
the last transmission was made close to the Andaman and Nicobar Islands (Fig 2). Tag trans-
missions were not received on a consistent daily basis, message numbers were inconsistent
and, the location accuracies of the Argos plots varied throughout the deployment indicating
that the turtle was healthy, making dives and travelling independently. The tag is thought to
have stopped transmitting at the end of the deployment due to the battery running out.
Seasonal habitat usage
Green turtles used most of the coastline from Abu Dhabi through to Ras Al Khaimah within
the UAE (Fig 3). Overlapping core habitats of two or more turtles occurred offshore of Abu
Dhabi and Jebel Ali. The Ghantoot area was utilised heavily with three core home ranges
overlapping.
Turtles were released at different times throughout the year and had different data transmis-
sion periods. Both coastal water temperature (F-statistic: 0.5226 on 1 and 325 DF, p-value =
Fig 1. Horizontal movements of seven rehabilitated green sea turtles satellite tagged and released in Dubai, UAE. Fig 1A shows the tracks for
‘transient’ turtles and Fig 1B shows the tracks for turtles considered ‘resident’.
https://doi.org/10.1371/journal.pone.0184286.g001
Fig 2. Horizontal movements of ‘Dibba’, a rehabilitated green sea turtle released on the east coast of the UAE in February 2008.
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0.4703) and sea surface temperature (F-statistic: 0.066 on 1 and 325 DF, p-value = 0.80) had no
influence on the sea floor depth where turtles made transmissions, showing that resident green
sea turtles made no temperature related movements to deeper water.
All core habitats of resident turtles were in coastal, shallow waters within known seagrass
areas (Fig 4). The only core habitat of a turtle that was not immediately coastal, although still
in water less than 10 m in depth, was observed in ‘Bahar’. This turtle’s core habitat included
two separate areas, one immediately coastal and one area approximately 50 km from the coast-
line (Fig 4). The core habitats of two turtles, ‘Bahar’ and ‘Belle’ fell within current protected
areas, although at the time of tagging the Bul Syayeef Marine Protected Area (MPA) had not
yet been declared.
Tag-recorded temperatures
No notable thermoregulatory movements were noted during summer. The major temperature
bin recorded by turtle-borne tags was similar to the mean water temperatures recorded daily
at 10 m depth in Dubai. The highest temperatures experienced by these turtles varied between
the 36–39˚C data bin in August and the 21–24˚C temperature bin in the cooler winter months
(December to April). In summer, the prevalent temperature bin experienced was between 30–
Fig 3. Overlapping home range usage for seven green sea turtles within the United Arab Emirates.
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33˚C, although time was spent in each bin. In winter, turtles experienced the normal range of
temperatures associated with coastal waters, from 20˚C to 34˚C (Fig 5).
Fig 4. Fifty percent (core habitat) and 95% percentage volume contours (PVC) for all turtles that remained within the Gulf.
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Discussion
Post-release movements
All eight green turtles C.mydas included in this study showed a successful integration back
into the wild after long periods of rehabilitation. This builds on the successful rehabilitation
efforts documented in previous studies from other areas [18,33,34]. Turtles in this study
returned to either known feeding areas or undertook large-scale migrations, indicating they
were fit to resume normal behaviours. Rehabilitation efforts thus were a direct benefit to these
individuals, contributing to the survival of this endangered species and thereby supporting
conservation efforts. The associated post-release tracking also provided information on the
lack of obvious thermoregulatory behavior of green turtles in an water body subject to extreme
water temperature variation.
There are limited previous satellite-tagging data on the movement of green turtles in the
Arabian region. Rees et al. [58] satellite-tagged two nesting adult green turtles from the Island
of Masirah, Oman that travelled into the Red Sea. Journeys were reported to be a minimum of
2400 km and 2500 km, respectively, crossing maritime boundaries including Yemen, Eritrea
and the Red Sea coast of Saudi Arabia. Rees et al. [18] tracked three adult females from Kuwaiti
waters of the Gulf, one post-nesting and two rehabilitated. The rehabilitated turtles displayed
no notable difference in post-tagging behavior when compared to the nesting female. Unlike
studies focused on nesting females, rehabilitated turtles are typically from unknown origin,
with no data on their birthplace, nesting location and migration routes. The turtles included in
Fig 5. Overall percentage of time spent at temperature for all SPOT tagged turtles, split into months, compared to average monthly water
temperatures taken in coastal Dubai at 10 m depth (black dots). No tags were active during the month of November.
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this study spanned a range of ages, injuries, and ailments. This could explain why some of the
animals tagged were transient to UAE waters, whereas others remained ‘resident’. Transient
turtles could have been injured while moving through UAE waters on a larger-scale migration,
which they resumed after successful rehabilitation.
‘Jade’ was the only resident turtle to leave UAE waters for a short period of time and then
return to her previous core habitat foraging area. On July 25 2010, ‘Jade’ made a directional
movement across the Gulf to Qeshm Island, and then returned to her preferred core habitat
area. This movement was highly directional, and could possibly represent movement towards
a nesting area or a quest to find a mate. Spotila [63] reported that green turtles lay up to three
nests in a season and have an inter-nesting interval of 12–14 days. ‘Jade’s’ CCL on release was
115 cm, indicating she was mature, and she spent 14 days around Qeshm. This could have
been sufficient time to lay two batches of eggs before returning to her foraging habitat around
Ghantoot. Although there are no previous reports of green turtles nesting on Qeshm Island,
Jade’s movement was during the summer months of July and August when green turtles nest
within Gulf waters [18]. Nesting could not be confirmed through temperature or ‘dry’ time as
the tag used was not capable of collecting temperature or ‘haul out’ information. However,
movement for foraging was unlikely due to the long transit times (11 days to Qeshm and 10
days on the return to Ghantoot) and the known productivity of her core habitat.
‘Dibba’ was the only turtle to be found and released on the east coast of the UAE. The lon-
gest reported post-nesting movement by an adult green turtle is from the Chagos Archipelago
to mainland Africa, a distance of 3979 km [64]. ‘Dibba’ moved more than twice this distance
travelling 8283 km and was still travelling when the tag stopped transmitting. This journey is
comparable to the trans-oceanic movements known to be made by loggerhead turtles migrat-
ing across the Pacific Ocean at different stages of their life [40].
This highlights the exceptional abilities of green turtles to travel and navigate over long dis-
tances across large expanses of open ocean. Karl & Bowen [65] conducted a global study on
green turtles from 15 major rookeries around the world, categorising haplotypes into two
groups corresponding to major oceanic basins: the Atlantic and the Indo-Pacific. The latter
included turtles sampled from the Ras Al Hadd rookery in Oman. They demonstrated that
there was population substructure within each basin, suggesting natal homing by female green
turtles, but they also noted haplotype connection among the Indian and Pacific Ocean rooker-
ies suggesting some degree of interchange. Although ‘Dibba’ was found and released on the
east coast of the UAE, and not in the Gulf itself, Dibba’s journey away from the region may not
be unusual and we hypothesize that it is unrelated to her previous injuries and rehabilitation.
Aloia & Al-Ghais [66] investigated population genetics of foraging green turtles in the Gulf
and mtDNA results suggested that at least two populations occur in this area. They proposed
that these turtles may be from nesting and wintering populations and could have travelled
from as far as the Seychelles, Pakistan, India or the Maldives. We show here that green turtles
leave the Gulf, and it is equally possible that they move into the Gulf from Omani waters [67].
Carr [30] stated that the occurrence of wandering and straying must happen and that such
occurrences are advantageous for green turtle colonies. We suggest that further study into the
regional movements and population genetics of green turtles should be conducted to expand
on our knowledge of their movements from this region.
Post-release residency in foraging areas
Our results show that sub-adult and adult green turtles use the same near-shore habitat, with
some home ranges directly overlapping. Luschi et al. [68] suggested that sub-adults of most
turtle species recruit to neritic habitats after some years of pelagic life to complete their
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development. The authors highlighted that these areas are either shared with adults (who use
them as foraging grounds) or can be frequented only by sub-adults that later shift to a different
adult feeding area [69]. Another study by [70], where two sub-adult green turtles were tagged
after rehabilitation, found that the turtles remained close to the release site. They suggested
that these turtles did not need to move far because of the habitat suitability around the release
site. Similarly, [34] indicated that two green turtles tagged after rehabilitation undertook
coastal movements as an optimum strategy to increase their chances of finding food. Since all
sub-adult turtles in our study were transient, it is likely they were still undertaking their devel-
opmental migrations and heading towards their late developmental habitats, which are likely
to be closer to their natal beaches [68].
Adults in our study were residents and utilised most of the coastal region of the UAE from
Ras Al Khaimah to Abu Dhabi waters. Overlapping areas, where two or more turtles were pres-
ent, were mostly located south of Dubai and north of Abu Dhabi with Ghantoot being the most
frequented. Ghantoot is a small area that encompasses a large expanse of seagrass beds where
foraging green turtles are frequently sighted (RWJ pers. obs). Upon leaving a nesting area, adult
turtles usually swim towards a fixed feeding area, generally a neritic environment, where they
remain for a long time, possibly for the entire inter-reproductive period [68]. A similar behavior
was noted by [18] where rehabilitated green turtles in Kuwait established long-term residencies
around the areas they were released and were believed to be foraging there. Although females
were resident in UAE waters, they are not known to nest in these coastal areas. They are there-
fore using these habitats during their inter-reproductive period and then presumably move to
other areas within or outside the Gulf to nest. Gaining a better understanding of the use of this
foraging habitat is needed to ensure targeted management actions can be developed.
Home ranges of turtles utilising neritic foraging habitats are not well understood [71].
Aloia & Al-Ghais [66] proposed that Gulf green turtles are from two genetic populations, ‘nest-
ing’ and ‘wintering’, and could have travelled from the wider Indian Ocean. By tagging both
‘transient’ and ‘resident’ animals in our study, a more detailed outline of habitat use and move-
ments is being developed for animals that utilise our study region but may not nest in the local
area. Although it appears that sub-adults are more ‘transient’ than mature animals, the small
sample size means than further tracking and genetic analysis, targeting both adult and sub-
adult animals, is required to gain a better understanding of their behavior.
Home ranges of turtles that remained in the Gulf were generally large, ranging between 529
and 5023 km
2
with a mean of 1390 ±1783 (median = 683, n = 6). These home range estimates
are likely to be impacted by the low accuracy of Argos locations and therefore, so are compari-
sons between individual animals and other studies. Broderick et al. [72] tagged 10 post-nesting
green turtles in the Mediterranean and found turtles formed home ranges of less than 77 km
2
.
Rees et al. [18] reported similar home ranges of below 76 km
2
. Of the resident turtles in this
study, all home ranges were in excess of 500 km
2
, suggesting that turtles in the Gulf waters of
the UAE utilize much larger areas. Schofield et al. [73] found that loggerheads in the Mediter-
ranean dispersed widely, with females dispersing further than males. This extensive dispersal
was attributed to the widespread availability of foraging grounds throughout the Mediterra-
nean. The coastal waters of the UAE have suitable green turtle habitat spread along the entire
Gulf coast which may similarly explain the large home range sizes.
Rees et al. [18] reported core habitat area from two rehabilitated turtles in Kuwaiti waters of
the Gulf as 15 km
2
and 8 km
2
, and from one post-nesting female at 5 km
2
(mean = 9 ±3). In
comparison, the core habitat area for our resident turtles ranged between 8 km
2
and 112 km
2
with a mean of 50 ±42 km
2
(median = 56, n = 5), notably larger, although [18] reported that a
low number of transmitted locations were used for the tracked nesting female which may have
reduced the calculated core area size. Two adult females (‘Jade’ and ‘Belle’) formed small core
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home ranges (<16 km
2
) but three others (‘Bahar’, Emerald and ‘Moonlight’) formed larger
core habitats (<112 km
2
) within the same local area between Dubai and Abu Dhabi. Four tur-
tles, ‘Bahar’, ‘Moonlight’, ‘Belle’ and ‘Emerald’ formed home ranges within the Ghantoot area,
known to have healthy sea grass beds and supporting a sizeable population of green sea turtles.
This wide-ranging availability of food within their home range may explain why core habi-
tat area was large and why, during their tracked time, they did not venture far. Seminoff et al.
[71] tracked 12 sub-adult and adult green turtles in Mexican waters, and reported kernel den-
sity home ranges with one to three activity centers or core habitats ranging in area from 0.038
to 6.42 km
2
(mean = 1.788 ±0.62 km
2
) it was reported that green turtles displayed small and
defined home ranges which were dependent on the extent of suitable habitat and concluded
that there was no evidence that size, sex and duration of tagging had an effect on the area uti-
lised. Makowski et al. [74] tracked six juvenile green sea turtles from Atlantic waters around
Florida, core areas from kernel density ranged from 0.18 and 1.17 km
2
(mean = 0.49 ±0.39
km
2
). Both studies have notably smaller core habitat areas than our resident turtles which may
be attributed to a larger area of suitable and productive habitat along the UAE Gulf coastline.
Thermoregulatory behavior
Observations by the DTRP of turtles kept in sea-fed outside enclosures over the summer
months showed that when the water temperature reached 34˚C, the smaller juvenile hawksbill
turtles E.imbricata (<10kg) started to show signs of heat stress as displayed by lethargy and a
reduction in feeding (DTRP, unpub. data). Once these turtles were relocated to cooler, temper-
ature-controlled holding facilities, normal feeding and behaviour resumed. The heat stress
symptoms were only displayed in juvenile hawksbills whilst larger individuals of the same spe-
cies and of green turtles of all life stages did not display these symptoms even though the water
during the summer months can exceed 36˚C. These observations suggest that the upper ther-
mal tolerance levels of juveniles may differ from sub-adults and adults in some turtle species.
They also show that green sea turtles can tolerate very warm water. Spotila et al. [75] suggested
that thermoregulatory capabilities in sea turtles increase with body size, which may explain
why coastal areas are frequented by sub-adults and adults, while juveniles are rarely encoun-
tered. Mestre et al. [34] and [76] suggested that sea water temperature was a variable of minor
importance in regard to the movement paths chosen by green turtles in the Atlantic Ocean
including the Caribbean Sea. However, the Gulf is probably the warmest sea in the world [21]
and turtles in this region are likely exposed to the highest seawater temperatures. Resident
green turtles tagged and released during this study encountered water temperatures in excess
of 36˚C whilst within their coastal core habitats.
Pilcher et al. [77] reported a short-term behavioural response to remotely sensed Sea Sur-
face Temperature (SST) in Gulf hawksbills. Their results suggest that hawksbills moved
towards deeper and cooler waters in the summer months. We saw no such thermoregulatory
movements away from the coast in the summer months using tag collected temperature data,
indicating that the upper-temperature tolerance level for green turtles is more than 36˚C. This
apparent resilience to high water temperatures has further implications for studies on climate
change and its effect on turtle behaviour in other regions as sea temperatures rise. Pilcher et al.
[78] found no indication of extreme sex bias in both hawksbill and green turtle populations
from Qatari waters of the Gulf, even with the extreme high temperatures experienced and it is
suggested that marine turtles in the Gulf may be able to adapt to these warmer conditions.
Although our study indicates that sub-adult and adult green turtles may display resilience to
increasing sea temperatures, this may not be the case for all stages of their embryonic develop-
ment and life cycle stages and further research is suggested.
Satellite tracking rehabilitated sea turtles in the UAE
PLOS ONE | https://doi.org/10.1371/journal.pone.0184286 September 5, 2017 14 / 19
Conservation implications
Green turtles face many threats in UAE waters, including collisions with vessels, direct and
incidental take, as well as habitat destruction and degradation from coastal development. The
fate of Bahar in this study exemplifies the ongoing anthropogenic threats to wild turtles in
UAE waters, even though all sea turtle species are protected under UAE law. Our results show
that some coastal waters in the UAE are important habitats for green turtles throughout the
year and as such, should be considered for further protection.
Rehabilitation efforts were successful, with sea turtles surviving in the wild after long peri-
ods of captivity. This provides support to the premise that rehabilitated animals are potential
candidates for ecological tracking studies. Sea turtle tracking studies are heavily biased towards
nesting females. Rehabilitated turtles offer the opportunity to track members of other demo-
graphic groups and therefore support our understanding of these species.
Four of the eight turtles remained in UAE waters over the period of tracking, highlighting
the country’s critical role in managing and protecting green turtles and the habitats they uti-
lize. However, movements across international maritime boundaries were frequent for
released turtles and included movements into the waters of Iran, Pakistan, Oman, Maldives,
Sri Lanka and India. Mitigation measures for threats they might face during their travels are
crucial and require broad, cross-boundary and collaborative sea turtle management on a
regional scale to ensure their effectiveness.
Supporting information
S1 Fig. An image of ‘Dibba’ being released from a beach in the UAE.
(TIF)
S1 Data. The individual post-filtered satellite transmitted data for each sea turtle included
in this study.
(XLS)
Acknowledgments
This project was kindly supported by His Highness Mohammed Bin Rashid Al Maktoum,
Vice-President and Prime Minister of the United Arab Emirates and Ruler of Dubai. We
would like to thank the Dubai Falcon Hospital and the Central Veterinary Research Labora-
tory (CVRL) for their ongoing support of the Dubai Turtle Rehabilitation Project. We thank
the Jumeirah Group for providing the funding for satellite tags and data related costs. We
would like to thank Kevin Lay from Wildlife Computers for his assistance with satellite track-
ing. We thank all individuals and organisations who have rescued sick turtles in the UAE and
brought them to the DTRP for treatment. We also thank the Dubai Municipality, the Ministry
of Climate Change and Environment, Environment Agency Abu Dhabi and the Emirates
Marine Environmental Group for their support and for rescuing sea turtles in the UAE. Fig-
ures throughout this manuscript were created using ArcGIS software by Esri, please visit www.
esri.com. We acknowledge the use of free vector and raster map data sourced from www.
naturalearthdata.com.
Author Contributions
Conceptualization: David P. Robinson, Kevin P. Hyland, Warren R. Baverstock.
Data curation: David P. Robinson, Kevin P. Hyland, Warren R. Baverstock.
Satellite tracking rehabilitated sea turtles in the UAE
PLOS ONE | https://doi.org/10.1371/journal.pone.0184286 September 5, 2017 15 / 19
Formal analysis: David P. Robinson, Rima W. Jabado, Christoph A. Rohner, Simon J. Pierce,
Kevin P. Hyland, Warren R. Baverstock.
Funding acquisition: David P. Robinson, Kevin P. Hyland, Warren R. Baverstock.
Investigation: David P. Robinson, Simon J. Pierce, Kevin P. Hyland, Warren R. Baverstock.
Methodology: David P. Robinson, Kevin P. Hyland, Warren R. Baverstock.
Project administration: David P. Robinson, Kevin P. Hyland, Warren R. Baverstock.
Resources: David P. Robinson, Kevin P. Hyland, Warren R. Baverstock.
Software: David P. Robinson, Kevin P. Hyland, Warren R. Baverstock.
Supervision: David P. Robinson, Simon J. Pierce, Kevin P. Hyland, Warren R. Baverstock.
Validation: David P. Robinson, Kevin P. Hyland, Warren R. Baverstock.
Visualization: David P. Robinson, Kevin P. Hyland, Warren R. Baverstock.
Writing – original draft: David P. Robinson, Rima W. Jabado, Christoph A. Rohner, Simon J.
Pierce, Kevin P. Hyland, Warren R. Baverstock.
Writing – review & editing: David P. Robinson, Rima W. Jabado, Christoph A. Rohner,
Simon J. Pierce, Kevin P. Hyland, Warren R. Baverstock.
References
1. Seminoff JA (2004) Chelonia mydas. IUCN Red List of Threatened Species. Version 2011.
2. Parsons JJ (1962) The green turtle and man. University of Florida Press.
3. Horikoshi K, Suganuma H, Tachikawa H, Sato F, Yamaguchi M (1994) Decline of Ogasawara green tur-
tle population in Japan. In Proceedings of the fourteenth annual symposium on sea turtle biology and
conservation: 1–5.
4. Chaloupka M, Osmond M, Kaufman G (1999) Estimating seasonal abundance trends and survival prob-
abilities of humpback whales in Hervey Bay (east coast Australia). Marine Ecology Progress Series
184: 291–301.
5. Frazier J (2003) Prehistoric and ancient historic interactions between humans and marine turtles. The
biology of sea turtles 2: 1–38.
6. Troe
¨ng S, Rankin E (2005) Long-term conservation efforts contribute to positive green turtle Chelonia
mydas nesting trend at Tortuguero, Costa Rica. Biological Conservation 121: 111–116.
7. NRC (1990) Decline of the Sea Turtles: Causes and Prevention. Washington, DC, USA. National
Academies Press
8. Hall MA, Alverson DL, Metuzals KI (2000) By-catch: problems and solutions. Marine Pollution Bulletin
41: 204–219.
9. Miller RR, Williams JD, Williams JE (1989) Extinctions of North American fishes during the past century.
Fisheries 14: 22–38.
10. Gardner TA, Co
ˆte
´IM, Gill JA, Grant A, Watkinson AR (2003) Long-term region-wide declines in Carib-
bean corals. Science 301: 958–960. https://doi.org/10.1126/science.1086050 PMID: 12869698
11. Esteban N, Mortimer JA & Hays GC (2017) How numbers of nesting sea turtles can be overestimated
by nearly a factor of two. Proceedings of the Royal Society: Biological Sciences 284: doi 20162581.
12. Broderick AC, Frauenstein R, Glen F, Hays GC, Jackson AL, Pelembe T, et al. (2006) Are green turtles
globally endangered? Global Ecology and Biogeography 15: 21–26
13. Basson PW, Burchard JE, Hardy JT, Price ARG (1977) Biotopes of the Western Arabian Gulf: Marine
Life and Environments of Saudi Arabia. Aramco Department of Loss Prevention and Environmental
Affairs: Dhahran, Saudi Arabia.
14. Al-Merghani M, Miller JD, Al-Mansi A, Pilcher N (2000) The green and hawksbill turtles in the Kingdom
of Saudi Arabia: Synopsis of nesting studies 1986–1997. Fauna of Arabia 18: 369–384.
15. Pilcher NJ (2000) The green turtle, Chelonia mydas, in the Saudi Arabian Gulf. Chelonian Conservation
and Biology 3: 730–734.
Satellite tracking rehabilitated sea turtles in the UAE
PLOS ONE | https://doi.org/10.1371/journal.pone.0184286 September 5, 2017 16 / 19
16. Al-Mohanna SY, Meakins RH (1998) Study of the biology of marine turtles and their marine environment
in Kuwait. Final Report KFAS Project: 1–96.
17. Al-Mohanna SY, Al-Zaidan ASY, George P (2014) Green turtles (Chelonia mydas) of the north-western
Arabian Gulf, Kuwait: the need for conservation. Aquatic Conservation: Marine and Freshwater Ecosys-
tems. 24: 166–178.
18. Rees AF, Al-Hafez A, Lloyd JR, Papathansopoulou N, Godley BJ (2013) Green Turtles, Chelonia
mydas, in Kuwait: Nesting and Movements. Chelonian Conservation and Biology 12: 157–163.
19. Frazier J (1980) Exploitation of marine turtles in the Indian Ocean. Human Ecology 8: 329–370.
20. Al Suweidi AS, Wilson KDP, Healy T, Vanneyre L (2012) First Contemporary Record of Green Turtle
(Chelonia mydas) nesting in the United Arab Emirates. Marine Turtle Newsletter 133: 16–17.
21. Sheppard C, Al-Husiani M, Al-Jamali F, Al-Yamani F, Baldwin R, Bishop J, et al. (2010) The Gulf: A
young sea in decline. Marine Pollution Bulletin 60: 13–38. https://doi.org/10.1016/j.marpolbul.2009.10.
017 PMID: 20005533
22. Wilson S, Fatemi SMR, Shokri MR, Claereboudt M (2002) Status of coral reefs of the Persian/Arabian
Gulf and Arabian Sea region. Status of coral reefs of the world: 53–62.
23. Miller G (2012) Marine and Coastal Reptiles in Marine Atlas, Western Arabian Gulf. 2nd Ed. Loughland
R, Khaled AA eds. Saudi Arabia: Saudi Aramco Environmental Protection.
24. Block BA, Teo SLH, Walli A, Boustany A, Stokesbury MJW, Farwell CJ, et al. (2005) Electronic tagging
and population structure of Atlantic bluefin tuna. Nature 434: 1121–1127. https://doi.org/10.1038/
nature03463 PMID: 15858572
25. Jeffers VF, Godley BJ (2016) Satellite tracking in sea turtles: How do we find our way to the conserva-
tion dividends? Biological Conservation 199: 172–184.
26. Horrocks JA, Vermeer LA, Krueger B, Coyne M, Schroeder BA, Balazs GH (2001) Migration routes and
destination characteristics of post-nesting hawksbill turtles satellite-tracked from Barbados, West
Indies. Chelonian Conservation and Biology 4: 107–114.
27. James MC, Ottensmeyer CA, Myers RA (2005) Identification of high-use habitat and threats to leather-
back sea turtles in northern waters: new directions for conservation. Ecology letters 8: 195–201.
28. Blumenthal JM, Solomon JL, Bell CD, Austin TJ, Ebanks-Petrie G, Coyne M, etal. (2006) Satellite track-
ing highlights the need for international cooperation in marine turtle management. Endangered Species
Research 2: 51–61.
29. Koch AL, Carr A, Ehrenfeld DW (1969) The problem of open-sea navigation: the migration of the green
turtle to Ascension Island. Journal of Theoretical Biology 22: 163–179. PMID: 5797566
30. Carr A (1975) The Ascension Island green turtle colony. Copeia: 547–555.
31. Mortimer JA, Carr A (1987) Reproduction and migrations of the Ascension Island green turtle (Chelonia
mydas). Copeia: 103–113.
32. Hays GC, Dray M, Quaife T, Smyth TJ, Mironnet NC, Luschi P, et al. (2010) Movements of migrating
green turtles in relation to AVHRR derived sea surface temperature. International Journal of Remote
Sensing 22: 37–41.
33. Gilbert J (2011) Current Threats to Marine Turtles and Post Rehabilitation Success with Satellite Track-
ing. Queensland Coastal Conference, Australia.
34. Mestre F, Braganca MP, Nunes A, dos Santos ME (2014) Satellite tracking of sea turtles released after
prolonged captivity periods. Marine Biology Research 10: 996–1006.
35. Godley BJ, Blumenthal J, Broderick A, Coyne M, Godfrey M, Hawkes LA, et al. (2008) Satellite tracking
of sea turtles: Where have we been and where do we go next? Endangered Species Research 4: 3–22.
36. Cardona L, Ferna
´ndez G, Revelles M, Aguilar A (2012) Readaptation to the wild of rehabilitated logger-
head sea turtles (Caretta caretta) assessed by satellite telemetry. Aquatic Conservation: Marine and
Freshwater Ecosystems 22: 104–112.
37. Godley BJ, Broderick AC, Glen F, Hays GC, (2003) Post-nesting movements and submergence pat-
terns of loggerhead marine turtles in the Mediterranean assessed by satellite tracking. Journal of Exper-
imental Marine Biology and Ecology 287: 119–134.
38. Hochscheid S, Bentivegna F, Bradai MN, Hays G (2007) Overwintering behavior in sea turtles: dor-
mancy is optional. Marine Ecology Progress Series 340: 287–298.
39. Polovina J, Uchida I, Balazs G, Howell EA, Parker D, Dutton P (2006) The Kuroshio Extension Bifurca-
tion Region: A pelagic hotspot for juvenile loggerhead sea turtles. Deep-Sea Research Part II: Topical
Studies in Oceanography 53: 326–339.
40. Nichols WJ, Resendiz A, Seminoff JA, Resendiz B (2000) Transpacific migration of a loggerhead turtle
monitored by satellite telemetry. Bulletin of Marine Science 67: 937–947.
Satellite tracking rehabilitated sea turtles in the UAE
PLOS ONE | https://doi.org/10.1371/journal.pone.0184286 September 5, 2017 17 / 19
41. Hochscheid S, Bentivegna F & Hays GC (2005) First records of dive durations for a hibernating sea tur-
tle. Biology letters 1: 82–86. https://doi.org/10.1098/rsbl.2004.0250 PMID: 17148134
42. Hochscheid S, Bentivegna F, Hamza A & Hays GC (2010) When surfacers do not dive: multiple signifi-
cance of extended surface times in marine turtles. Journal of Experimental Biology 213: 1328–1337.
https://doi.org/10.1242/jeb.037184 PMID: 20348345
43. Hochscheid S (2014) Why we mind sea turtles’ underwater business: A review on the study of diving
behavior. Journal of Experimental Marine Biology and Ecology 450: 118–136.
44. Caliendo V, McKinney P, Robinson D, Baverstock W, Hyland K (2010) Plasma Biochemistry and Hema-
tology Values in Juvenile Hawksbill Turtles (Eretmochelys imbricata) Undergoing Rehabilitation. Jour-
nal of Herpetological Medicine and Surgery 20: 117–121.
45. Sheppard C, Price A, Roberts C (1992) Marine ecology of the Arabian region-patterns and processes in
extreme tropical environments. Academic Press, London.
46. Al-Gahtani AS, Maslehuddin M (2002) Characteristics of the Arabian Gulf environment and its impact
on concrete durability-an overview. In The 6th Saudi Engineering Conference, KFUPM, Dhahran, Saudi
Arabia: 169–184.
47. Nadim F, Bagtzoglou AC, Iranmahboob J (2008) Coastal management in the Persian Gulf region within
the framework of the ROPME programme of action. Ocean & Coastal Management 51: 556–565.
48. Jabado R, Cecile J (2012) Marine Ecosystems in the United Arab Emirates. Emirates Marine Environ-
mental Group (EMEG).
49. Carpenter KE, Krupp F, Jones DA, Zajonz U (1997) The Living Marine Resources of Kuwait, Eastern
Saudi Arabia, Bahrain, Qatar, and the United Arab Emirates. Rome: FAO.
50. Mrosovsky N (1980) Thermal biology of sea turtles. American Zoologist: 531–547.
51. Wibbels T (1999) Diagnosing the sex of sea turtles in foraging habitats. Research and management
techniques for the conservation of sea Turtles. IUCN/SSC Marine Turtle Specialist Group Publication
4: 139–143.
52. Casale P, Freggi D, Basso R, Argano R (2005) Size at male maturity, sexing methods and adult sex
ratio in loggerhead turtles (Caretta caretta) from Italian waters investigated through tail measurements.
The Herpetological Journal 15: 145–148.
53. Hampel MR, Robinson DP, Baverstock WR, Hyland KP (2008) Repair of a fractured plastron in a green
turtle (Chelonia mydas). Wildlife Middle East News 3: 5.
54. Baverstock W, Robinson D, Hyland KPC (2008) Rehabilitation and satellite-tracked release of a green
turtle, Chelonia mydas. Wildlife Middle East News 3: 6.
55. Bluvias JE (2008) Marine Turtle Trauma Response Procedures: A Husbandry Manual. Durham, NC:
Nicholas School of the Environment and Earth Sciences. Duke University.
56. Douglas DC, Weinzierl R, Davidson C, Kays R, Wikelski M, Bohrer G (2012) Moderating Argos location
errors in animal tracking data. Methods in Ecology and Evolution 3: 999–1007
57. Luschi P, Hays GC, Del Seppia C, Marsh R & Papi F (1998) The navigational feats of green sea turtles
migrating from Ascension Island investigated by satellite telemetry. Proceedings of the Royal Society:
Biological Sciences 265: 2279–2284.
58. Rees A, Al-Kiyumi F, Broderick A, Papathanasopoulou N, Godley BJ (2012) Each to Their Own: Inter-
Specific Differences in Migrations of Masirah Island Turtles. Chelonian Conservation and Biology 11:
243–248.
59. Rees A, Margaritoulis D, Newman R, Riggall TE, Tsaros P, Zbinden JA et al. Ecology of loggerhead
marine turtles Caretta caretta in a neritic foraging habitat: Movements, sex ratios and growth rates.
Marine Biology 160: 519–529.
60. Coyne MS, Godley BJ (2005) Satellite Tracking and Analysis Tool (STAT): an integrated system for
archiving, analyzing and mapping animal tracking data. Marine Ecology Progress Series 301: 1–7.
61. Hawkes LA, Witt MJ, Broderick AC, Coker JW, Coyne MS, Dodd M, et al (2011) Home on the range:
Spatial ecology of loggerhead turtles in Atlantic waters of the USA. Diversity and Distributions 17: 624–
640.
62. MacLeod C (2013) An Introduction To Using GIS In Marine Ecology 2nd ed. Glasgow: Pictish Beast
Publications.
63. Spotila JR (2004) Sea turtles: A complete guide to their biology, behavior, and conservation, JHU
Press, USA.
64. Hays GC, Mortimer JA, Lerodiaconou D, Esteban N (2014). Use of Long-Distance Migration Patterns of
an Endangered Species to Inform Conservation Planning for the World’s Largest Marine Protected
Area. Conservation Biology 28: 1636–1644. https://doi.org/10.1111/cobi.12325 PMID: 25039538
Satellite tracking rehabilitated sea turtles in the UAE
PLOS ONE | https://doi.org/10.1371/journal.pone.0184286 September 5, 2017 18 / 19
65. Karl SA, Bowen BW (2010) Evolutionary Significant Taxonomy: Molecular systematics of an endan-
gered sea turtle. Conservation Biology 13: 990–999.
66. Aloia MD, Al-Ghais SM (2013) Preliminary genetic analysis of the Green Turtle, Chelonia mydas, in the
Arabian Gulf using mitochondrial DNA. Zoology in the Middle East: 37–41.
67. Ross JP (1985) Biology of the green turtle, Chelonia mydas, on an Arabian feeding ground. Journal of
Herpetology: 459–468.
68. Luschi P, Hays GC, Papi F (2003) A review of long-distance movements by marine turtles, and the pos-
sible role of ocean currents. Oikos 103: 293–302.
69. Musick JA, Limpus CJ, Lutz PL, Musick JA (1997) Habitat utilization and migration in juvenile sea tur-
tles. The biology of sea turtles 1: 137–163.
70. Pelletier D, Roos D, Ciccione S (2003) Oceanic survival and movements of wild and captive-reared
immature green turtles (Chelonia mydas) in the Indian Ocean. Aquatic Living Resources 16: 35–41.
71. Seminoff JA, Resendiz A, Nichols WJ (2002) Home range of green turtles Chelonia mydas at a coastal
foraging area in the Gulf of California, Mexico. Marine Ecological Progress Series 242: 253–265.
72. Broderick AC, Coyne MS, Fuller WJ, Glen F, Godley BJ (2007) Fidelity and over-wintering of sea turtles.
Proceedings of the Royal Society of London: Biological Sciences 274: 1533–1539
73. Schofield G, Dimadi A, Fossette S, Katselidis KA, Koutsoubas D, Lilley KS, et al. (2013) Satellite track-
ing large numbers of individuals to infer population level dispersal and core areas for the protection of
an endangered species. Diversity and Distributions 19: 834–844.
74. Makowski C, Seminoff JA, Salmon M (2006) Home range and habitat use of juvenile Atlantic green tur-
tles (Chelonia mydas) on shallow reef habitats in Palm Beach, Florida, USA. Marine Biology 148:
1167–1179.
75. Spotila JR, O’Connor MP, Paladino FV (1997) Thermal biology. In: The biology of sea turtles. Lutz PL,
Musick J (eds), CRC Press, Boca Raton, FL: 297–314.
76. Hays GC, Åkesson S, Godley BJ, Luschi P, Santidrian P (2001) The implications of location accuracy
for the interpretation of satellite-tracking data. Animal Behaviour 61: 1035–1040.
77. Pilcher NJ, Perry L, Antonopoulou M, Abdel-Moati MA, Al Abdessalaam TZ, Albeldawi M, et al. (2014)
Short-term behavioural responses to thermal stress by hawksbill turtles in the Arabian region. Journal of
Experimental Marine Biology and Ecology 457: 190–198.
78. Pilcher NJ, Al-Maslamani I, Williams J, Gasang R, Chikhi A (2015) Population structure of marine turtles
in coastal waters of Qatar. Endangered Species Research 28: 163–174.
Satellite tracking rehabilitated sea turtles in the UAE
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