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Ecology and conservation of green turtles in Guinea-Bissau

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  • Faculty of Sciences of the University of Lisboa
102 Testudo Vol. 9 No. 3
Ecology and conservation of green turtles in
Guinea-Bissau
Ana R. Patrício1,2*, Castro Barbosa3, Paulo Catry1 and Aissa Regalla3
1MARE – Marine and Environmental Sciences Centre, ISPA – Instituto
Universitário de Ciências Psicológicas, Socias e da Vida, Lisbon, 1149 –
041, Lisboa, Portugal
2Centre for Ecology and Conservation, University of Exeter, Cornwall
Campus, Penryn TR10 9FE, UK
3Instituto da Biodiversidade e das Áreas Protegidas, Dr. Alfredo Simão
da Silva (IBAP), CP70, Bissau, Guiné-Bissau
*Corresponding author: Ana R. Patricio, email: R.Patricio@exeter.ac.uk
Introduction
Green turtle, a great traveller
Green turtles (Chelonia mydas) are a highly migratory species, establishing
connectivity between distant areas (Scott et al. 2014a). They venture into
their first great migration as soon as they emerge from their nests at sandy
beaches and crawl into the sea, where they associate with prevalent currents
to disperse into the open ocean (Putman et al. 2010; Scott et al. 2014b).
During this oceanic period, they can travel several thousand kilometres, living
an epipelagic life-style, which can last 3-5 years (Reich et al. 2007). After
this stage, juvenile turtles recruit to shallow coastal foraging areas, where
they may remain resident until adulthood, or travel between nearby feeding
grounds (Bolten et al. 2003).
During the dispersal stage of green turtles, in the first years of life, animals
from various populations mix with the help of ocean currents (Patrício et al.
2017). As a result, in coastal feeding areas, it is common to have aggregations
composed of animals from several nesting beaches (mixed stocks; Bolker et
al. 2007). It is essential to know the origin of these animals, to understand
the threats to which they are subjected throughout their life cycle, and to
establish collaborations between countries that share this resource. Through
genetic characterisation of individual turtles, it is possible to compare mixed-
stock foraging aggregations with nesting populations, to estimate their
rookery origin.
Finally, as adults, they perform cyclic breeding migrations, every two to
five years on average (Seminoff et al. 2015), between nesting beaches and
neritic foraging grounds, covering hundreds to thousands of kilometres each
time (Scott et al. 2014a). For such a vagrant animal as the green turtle, the
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effective conservation of populations depends highly on understanding the
links established between the different areas occupied throughout their life
cycle, so that the full-range of threats can be identified and addressed.
Conservation challenges
After centuries of overexploitation for the consumption of meat, eggs, oil
and soup (Rieser 2012), the green turtle has been recovering in most of its
distribution range, thanks to decades of conservation efforts (Mazaris et al.
2017). However, this species is now facing several different anthropogenic-
induced threats, with bycatch (Wallace et al. 2010), plastic pollution (Wilcox
et al. 2018; Duncan et al. 2019) and coastal development (Biddiscombe et al.
2020) having the greatest impact. Green turtles are also highly vulnerable to
upcoming climate change (Varela et al. 2018; Patrício et al. 2021) and these
pressures can act synergistically, further enhancing negative impacts.
The conservation challenges are ever greater, as the aforementioned threats
are ubiquitous in our seas and coastal habitats, and even more so because
the source/s of some threats are impossible to pinpoint (e.g. plastic pollution
or climate change). Ensuring the protection of a range of suitable habitats
to allow populations to thrive and adapt is, thus, a priority for population
continuity. However, to define which areas are key to protect we must first
understand the spatial distribution of populations and the connectivity they
establish, through dispersal and migration, between breeding and foraging
sites. This is particularly urgent for areas that are poorly known, due to
limited research in the past, such as West Africa.
Major population of green turtles in West Africa
West Africa is a region of global importance for green turtles, hosting one
of the largest populations globally (SWOT 2011; Patrício et al. 2019). The
core breeding rookery for this population is located at Poilão Island, in the
southeast limit of the Bijagós Archipelago, Guinea-Bissau (Catry et al. 2009;
Barbosa et al. 2018), where an average of 27,251 clutches are laid annually
(2013-2017; Broderick & Patrício 2019). Lower numbers of nesting occur
on several other islands of the archipelago and on the northern continental
coast of Guinea-Bissau (Catry et al. 2002). There is also nesting in other
countries of the region, but in much lower numbers (~10 to ~100 nests/year;
Agyekumhene et al. 2017).
Foraging aggregations are also known to occur across the Bijagós (Barbosa
pers. comm.), with an important developmental area around the islands of
Unhocomo and Unhocomozinho (Catry et al. 2010), which has yet to be
genetically characterized. Important green turtle foraging areas are also
known at Cabo Verde (Marco et al. 2011; Monzón-Argüello et al. 2010),
at the National Park of the Banc d’Arguin (PNBA), in Mauritania (Cardona
© British Chelonia Group + Ana R. Patrício,
Castro Barbosa, Paulo Catry and Aissa Regalla 2021
104 Testudo Vol. 9 No. 3
et al. 2009; Godley et al. 2010), around the Bijol Islands, in The Gambia
(Hawkes et al. 2008) and in Guinea (Fretey et al. 2008). Additionally, bycatch
data support the presence of foraging green turtles in other countries of the
region (e.g. Ghana, Togo and Benin; Agyekumhene et al. 2017).
Potentially, several of the foraging aggregations in West Africa are linked
to the major rookery of the Bijagós, yet there is a paucity of tracking and of
genetic data to confirm this hypothesis. The exception is the connectivity with
the PNBA, which was confirmed through satellite tracking of post-breeding
females from Poilão Island (Godley et al. 2010). However, the sample size for
this study was limited (n = 4) and a more recent work suggests the existence
of plasticity in foraging strategies for this population (Patrício et al. 2019),
possibly associated with multiple post-breeding destinations.
Study aims
Considering the challenges intrinsic in the conservation of migratory species,
and the knowledge gaps in the study region, we set out to understand the
spatial distribution of green turtles nesting at Poilão Island, and the connectivity
between juvenile green turtles from the Bijagós and Atlantic rookeries.
Specifically, we use 1) genetic analyses to assess the origin of the juvenile
green turtles foraging in the Bijagós archipelago, and 2) satellite telemetry
to investigate the inter-nesting spatial distribution, the post-breeding
migrations and the foraging habitat use by green turtles that nest at Poilão
Island. Ultimately, our results will provide the scientific basis to inform marine
spatial planning and other conservation measures in the region, aimed at
protecting this resource.
Study site
The Bijagós is a deltaic archipelago west of the mainland coast of Guinea-Bissau.
It comprises 88 islands and islets and covers an area of 10,000km2. Only 21 of
the islands are permanently inhabited, with a human population of ca. 25,000,
mostly from the Bijagó ethnic group (Campredon & Catry 2016). Some of the
uninhabited islands are considered sacred and only accessed during religious
and social ceremonies. These traditional restrictions have contributed to the
protection of the archipelago's remarkable biodiversity, which includes several
other charismatic species besides the green turtle, notably the West African
manatee (Trichechus senegalensis), the Atlantic humpback dolphin (Sousa
teuszii) and the ‘marine’ hippopotamus (Hippopotamus amphibious). A large
part of the islands is surrounded by mangroves and extensive mudflats, which
provide shelter and developmental areas for many species of fish, molluscs,
and crustaceans, and feeding grounds for wintering shorebirds. In addition
to the green turtle, three other species of sea turtle nest on the beaches
of the archipelago: the olive ridley (Lepidochelys olivacea), leatherback
© British Chelonia Group + Ana R. Patrício,
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(Dermochelys coriacea), and hawksbill (Eretmochelys imbricata). Loggerhead
turtles (Caretta caretta) are present in the surrounding waters, but do not
nest in Guinea-Bissau. This rich biodiversity led to the establishment of three
marine protected areas (MPAs) within the archipelago, and to the designation
of the Bijagós-Bolama Biosphere Reserve by UNESCO in 1996.
It is within one of the archipelago’s MPAs, the João Vieira-Poilão Marine
National Park (PNMJVP in its Portuguese acronym), in the southeast limit of
the Bijagós, at Poilão Island, that the main green turtle rookery is located
(Fig. 1a). Poilão (N 10.87°, W 15.72°) is a low-lying small island, with an area
Fig. 1. Upper, right to left: location of the Bijagós Archipelago in West Africa and zoomed
map of the Bijagós Archipelago showing the location of the study sites; a. Poilão Island and
b. Unhocomo and Unhocomozinho Islands (U&U). Dashed line shows limits of the João-Vieira
Poilão National Marine Park (PNMJVP). Lower, right to left: a. Outer limits and delineation of
the no-take zone (central zone) of the PNMJVP, and islands within the MPA, including Poilão
(yellow diamond); b. Unhocomo and Unhocomozinho Islands (U&U) and in-water capture
locations (yellow diamonds).
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106 Testudo Vol. 9 No. 3
of 43ha, covered by undisturbed tropical forest, and surrounded by a rocky
subtidal zone. It has a tropical climate, with the rainy season between May
and November, peaking in August, coinciding with the peak of the nesting
season.
Besides Poilão, this MPA has three other islands – João Vieira, Cavalos
and Meio – and three islets – Cabras, Águias and Baixo de Gaivotas. After
Poilão, most nesting occurs on Cavalos (2,507 nests in 2016), followed by
Meio (2,063 nests in 2016) and João Vieira (596 nests in 2011; Barbosa et al.
2018). Although there is marked interannual variability in nesting numbers,
the relationship of nesting abundance (absolute number of nests) among
these islands has been consistent over the years. Nesting density (nests per
square metere) is very high at Cabras Islet, but nesting abundance has yet to
be quantified there. The other two islets are submersed during high tide and
thus not suitable for nesting.
The main green turtle feeding and developmental grounds in the Bijagós
are located at the westernmost limit of the archipelago, in the shallow waters
surrounding the islands of Unhocomo and Unhocomozinho (N 11.31º, W
16.40º; Fig. 1b). These feeding grounds are characterized by areas of rocky
seabed covered with algae (Caulerpa sp., Sargassum sp. and Dictyota sp.),
adjacent to mangroves (Rhizophora sp.) and sandy areas, with low-density
seagrass patches (Halodule sp.) and sparse rocks covered in algae. The sea
surface temperature average is 27.3°C (ranging from 25.1°C to 29.5°C).
To assess the connectivity of green turtles from the Bijagós, we collected
biopsy samples from juvenile green turtles foraging around Unhocomo and
Unhocomozinho and deployed satellite tags on females found nesting at
Poilão Island. We also continued the standard monitoring of nesting activities
and report the nesting number estimates for the last 15 years.
Methods
Monitoring of nesting activities
Since 2007, IBAP has used a standard protocol to monitor the nesting activities
of green turtles at Poilão. Because the island is, for its most part, surrounded
by intertidal rocks which are exposed at low tide (Fig. 2), the turtles must wait
for high tide to access the beach to nest. It is therefore around the peak of
the night high tide that IBAP patrols the 2km beach to assess the number of
nesting females. In the early morning, there is an additional survey to count
tracks from the previous night, and to count the number of turtles that are
stranded on the intertidal rocks. These turtles usually rest in intertidal pools,
where they can keep their body temperatures within tolerable limits before
returning to the sea with the high tide.
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Testudo Vol. 9 No. 3 107
Monitoring is conducted annually from August to November, to encompass
the nesting distribution. Because nesting density at Poilão is too high to allow
counting all the nests, we estimate the number of clutches laid per season
by multiplying the number of nesting female emergences by 0.813, to adjust
for nesting success in Poilão (Catry et al. 2009).
Genetic assessment
We collected biopsy samples from the epidermis of juvenile green turtles found
foraging at Unhocomo and Unhocomozinho for genetic analysis. The number
of biopsy samples collected was minimal without jeopardising statistically
valid results, and the sampling techniques chosen have been refined over the
years of practice to minimise impact on animals (e.g. reduced handling time,
reduced size of samples). All procedures used are widely applied in the field
of sea turtle research and were carried out by trained personnel following
recommended guidelines (NMFS-SFC, 2008) in order to reduce stress to the
animals and ensure their welfare.
To capture turtles, we used an entanglement net (800m long, 20cm mesh
size) which was deployed from a pirogue operated by Bijagós fishers. Water
depth varied from 4-1m. Each net set lasted one hour, and we swam the
length of the net throughout this period to look for entangled turtles (i.e.
three people started at equidistant points along the net and kept swimming
to ensure that turtles were released from the net as fast as possible). Most
turtles did not get entangled; instead, they would swim along the net trying
to find a way out, and were captured by hand. Once captured, we brought
the turtles to a logistic vessel anchored next to the net.
Once at the logistic vessel, we measured the curved carapace length (CCL)
using a flexible metric tape to the closest millimetre for each individual and
tagged both front flippers with uniquely numbered, self-piercing Inconel tags
(©National Band & Co). We used sterile biopsy punches (6mm diameter) to
Fig. 2. Left: Poilão Island, in the Bijagós Archipelago, Guinea-Bissau, with intertidal rocks
exposed due to low tide. Right: green turtles waiting for high tide to return to the sea.
Photos by IBAP (left) and Rita Patricio (right).
© British Chelonia Group + Ana R. Patrício,
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108 Testudo Vol. 9 No. 3
collect skin samples from the right shoulder, after disinfecting the area with
a diluted povidone-iodine solution. We used single-use surgical gloves and
biopsy punches for each new sample. Samples were stored in 96% ethanol,
inside 2ml Eppendorf tubes uniquely labelled.
We will extract the DNA of samples and amplify specific regions of the
mitochondrial DNA (i.e. ~860bp fragment from control region and short
tandem repeats; Shamblin et al. 2012; Tikochinski et al. 2018), used in sea
turtle population genetic assessments and shown to improve resolution
of connectivity studies (Shamblin et al. 2012; Tikochinski et al. 2018). We
will then compare the haplotypes found in the Bijagós with haplotypes
throughout Atlantic green turtle rookeries, to estimate the contribution of
each putative source to this foraging aggregation.
Satellite tracking
During the 2018 to 2020 nesting seasons at Poilão Island, we deployed
45 satellite tags on nesting females (Fig. 3) to study their movements. We
also applied flipper tags and passive integrated transponders (PIT) tags to
each turtle. To deploy the satellite transmitters, we waited for the turtles to
start laying their eggs and then executed the attachment procedure within
20 minutes, while the turtle continued to lay. First, we sanded the second
vertebral scute where the tag was to be attached and cleaned it with acetone.
Then we applied a base of fibreglass and fast-dry epoxy (®Devcon-5min
Epoxy) and allowed it to dry for five minutes. A ‘cushion’ for the tag was then
made with magic metal (®Loctite) before we pressed the tag gently on top
of the fibreglass base and allowed ten minutes for it to dry further. For the
last step, we applied again fibreglass with epoxy around the tag to secure
it, and allowed five minutes for the second fibreglass and epoxy application
to dry. All turtles continued with their nesting activity throughout the tag
application, successfully laid their eggs, and covered and camouflaged the
nest; therefore, we are confident that the procedure did not disturb them.
Preliminary results
This population shows high inter-annual variability in nesting numbers (Fig.
4), and the year 2020 was a record year, with over 60,000 clutches estimated
at Poilão Island alone (Fig. 4). This variability in nesting numbers across years is
common among sea turtle populations, particularly among green turtles, and
it is potentially linked to the availability of food resources at foraging areas, in
addition to the natural reproductive cycle of breeding females (Broderick et al.
2001). The very high number of clutches in 2020 reinforces the importance
of this population for the maintenance of foraging aggregations across the
West Africa region, and potentially, the Atlantic.
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At Unhocomo and Unhocomozinho we captured a total of 103 green turtles,
of which 99 were immatures, ranging from recruit (i.e. a turtle that recently
moved from oceanic to neritic waters) to subadult sizes (CCL: 35-79cm; Fig. 5),
indicating that this is mainly a developmental site. We also caught four adults,
two females and two males (CCL: 87.5-97.0cm). The genetic assessment
at Unhocomo and Unhocomozinho will allow us to estimate the origin of
this foraging aggregation, and estimate the connectivity between Atlantic
nesting beaches and this juvenile developmental area, further highlighting the
importance of the Bijagós Archipelago for Atlantic green turtles.
Thanks to satellite tracking technology, we have obtained daily movements
of green turtles from this large population and have some very interesting
findings. The spatial distribution during the inter-nesting intervals will be key
to understanding whether the current limits of the PNMJVP ensure adequate
protection to turtles during the nesting season. Tracking data from their post-
nesting migrations will allow us to understand the connectivity established
between Poilão and foraging grounds along West Africa. We have found
that this population feeds in coastal areas in Guinea-Bissau, Senegal, The
Gambia and Mauritania. Knowledge of the spatial distribution of this
Fig. 3. Green turtle with ®Wildlife Computers Spot tag, at Poilão Island, Guinea-Bissau.
Photo by Rita Patricio.
© British Chelonia Group + Ana R. Patrício,
Castro Barbosa, Paulo Catry and Aissa Regalla 2021
110 Testudo Vol. 9 No. 3
Fig. 4. Estimated number of green turtle clutches at Poilão Island, in the Bijagós Archipelago,
Guinea-Bissau.
Fig. 5. Size-classes of green turtles found foraging at the water surrounding the islands of
Unhocomo and Unhocomozinho, in the Bijagós Archipelago, Guinea-Bissau. Dark blue: recruits
(i.e., turtles that have recently moved from oceanic to neritic waters); light blue: resident
juveniles; yellow: subadults; orange: adults.
© British Chelonia Group + Ana R. Patrício,
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population outside the breeding period will allow us to understand the range
of threats that this population may be exposed to, including identifying
areas of conflict with fishing activities. Ultimately, these results should help
establish collaborations among sea turtle conservation projects within the
region, and potentially help define areas in need of protection.
Acknowledgements
This work is conducted through a partnership between the MARE – ISPA,
Instituto Universitário and the Instituto da Biodiversidade e das Áreas
Protegidas Dr. Alfredo Simão da Silva (IBAP), and it is funded by the MAVA
Foundation and the Regional Partnership for Coastal and Marine Conservation
(PRCM), through the projects ‘Consolidation of sea turtle conservation at the
Bijagós Archipelago, Guinea-Bissau’ and ‘Survie des Tortues Marines’, with
additional support from the Rufford Foundation and the British Chelonia
Group, to whom we are deeply thankful. Research permits for this work
were obtained from national and local authorities in Guinea-Bissau, namely
the Instituto da Biodiversidade e das Áreas Protegidas, Dr. Alfredo Simão da
Silva (IBAP), which was also involved in fieldwork and in all outputs related
to this research. Fieldwork was also conducted with the collaboration of
members from local communities of the Bijagós, particularly from the islands
of Canhabaque, Unhocomo and Unhocomozinho.
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... The increase in conservation efforts is driving the recovery of some species, for example the humpback whales (Megaptera novaeangliae), which then leads to an increase in reported sightings [19]. New areas of sea turtle occurrence and nesting in the Mediterranean region [3,4,17,18], and on the west African coast [19][20][21][22][23][24][25], have been recorded due to an increase in conservation efforts, increasing monitored areas and improving staff training. ...
... Specifically, the olive ridley, loggerhead and leatherback turtles are categorized as vulnerable, the green turtle as endangered and the hawksbill turtle as critically endangered [27]. In this region, the most important nesting ground for green turtles is located in Guinea Bissau, with more than 30,000 nests annually [24] and for loggerhead turtles is in Cabo Verde with more than 100,000 nests annually [25]. ...
... In addition, juveniles of olive ridleys have also never been reported in the region [48]. The closest established green turtle nesting ground to Cabo Verde is 950 km away in the Bijagos archipelago of Guinea Bissau, one of the largest green turtle populations in the world [24,56]. The nearest olive ridley population is approximately 750 km away, in The Gambia, although with lower nesting activities [19]. ...
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