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ORIGINAL ARTICLE
Demographic and tumour prevalence data for juvenile green turtles at the
Coastal-Marine Protected Area of Cerro Verde, Uruguay
Milagros Lpez-Mendilaharsua,b, Gabriela M. Vlez-Rubioa,c,d, Cecilia Lezamaa,e, Anita Aisenberga,f,
Antonia Bauza, Laura Berrondoa, Victoria Calvoa, Noel Caraccioa, Andrs Estradesa, Martn Hernndeza,g,
Martn Laportaa,g, Gustavo Martnez-Souzaa,h, Melisa Moralesa, Vernica Quiricii, Mariana Rosj and
Alejandro Fallabrinoa
Karumb NGO, Zoo Villa Dolores, Montevideo, Uruguay; bFundao Pr-TAMAR, Salvador, Bahia, Brazil; cMarine Zoology Unit, Cavanilles
Institute of Biodiversity and Evolutionary Biology (ICBIBE), University of Valencia, Valencia, Spain; dGrupo de Investigacin y Formacin de
Recursos Humanos en Biodiversidad, Centro Universitario Regional del Este (CURE), Universidad de la Repblica, Campus de Maldonado,
Punta del Este, Uruguay; eDireccin Nacional de Recursos Acuticos (DINARA-MGAP), Montevideo, Uruguay; fLaboratorio de Etologa,
Ecologa y Evolucin, Instituto de Investigaciones Biolgicas Clemente Estable, Montevideo, Uruguay; gSeccin Gentica, Facultad de
Ciencias, UDELAR, Montevideo, Uruguay; hInstituto de Cincias Biolgicas, Universidade Federal do Rio Grande, Brazil; iDepartamento de
Ecologa y Biodiversidad, Facultad de Ecologa y Recursos Naturales, Universidad Andres Bello, Santiago, Chile; jrea de Biodiversidad y
Conservacin, Museo Nacional de Historia Natural, Montevideo, Uruguay
ABSTRACT
ARTICLE HISTORY
Marine Protected Areas are increasingly considered in coastal areas as an instrument to preserve
threatened fauna and fragile habitats from the detrimental effects of human activities. For this
reason baseline data are of utmost importance for the evaluation of the outcomes of ongoing
conservation efforts. Along the Uruguayan coast, the area of Cerro Verde (declared protected
since 2011) represents the most important foraging and development area for green turtles
(Chelonia mydas). Between 2002 and 2009, a long-term capture-mark-recapture programme
for green turtles was developed to gather data on demography, ecology and status of the
species in the area. Turtles captured were juveniles ranging from 28.8 to 64.3 cm in length over
the curve of the carapace (n = 514), and results indicated a size-based habitat segregation.
Tumour prevalence was 5.3% (n = 27) and was positively correlated with carapace length.
The mean body condition index was 1.25 0.14 (n = 494). From the total number of tagged
turtles 10.6% were recaptured during the study period. Green turtles showed high site
delity; 81% of the turtles were recaptured within the same season and 76% were
recaptured in different seasons but were found at the original capture spot. Mean annual
growth rate was 1.6 0.9 cm year1. The catch per unit effort of 2008 differed from 2009,
higher in 2009, but also signicantly different between capture spots. The present study
constitutes a baseline dataset for future monitoring of green turtles in the area and provides
valuable information for wider analyses of population dynamics in the Southwestern Atlantic
Ocean.
Introduction
The green turtle, Chelonia mydas (Linnaeus, 1758), has a
circum-global distribution and inhabits neritic foraging
areas in tropical, subtropical and temperate waters
(Hirth 1997). Recently, Wallace et al. (2010) established
Regional Management Units (RMUs), aiming to provide
a framework for study and conservation of marine
turtles in units of protection above the level of
nesting populations, but below the level of species,
within regional entities. This proposal was based on
updated studies on sea turtle biogeography, including
site-based monitoring, genetic analyses, mark-recapture studies and telemetry. In particular, 17 RMUs
were identied for the green turtle and the Southwest
CONTACT Gabriela M. Vlez-Rubio
gabriela.velez@uv.es
RESPONSIBLE EDITOR
Leandro Bugoni
KEYWORDS
Southwest Atlantic;
protected areas; site delity;
size distribution; health
condition
M. LPEZ-MENDILAHARSU ET AL.
Methods
Study area
The CMPA of Cerro Verde (3356 S, 5330 W) is located
on the northern coast of Uruguay in the Rocha Department encompassing 17 km2 of mainland and 73 km2 of
marine surface comprising a complex of islands (Figure
1). This region contains tropical and subtropical waters
and is inuenced by the cold Malvinas Current in winter
and autumn and the warm Brazilian Current in spring
and summer, and is subject to great variations in temperature (range 927C) and salinity (1530) throughout
the year (Acha et al. 2004; Defeo et al. 2009). The CMPA
harbours rich hard-substrata benthic communities
dominated by mussels and macro-algae (Borthagaray
& Carranza 2007), offering suitable conditions for
green turtle foraging. The insular ecosystem and its
marine surroundings contain a high biodiversity,
including many migratory and threatened species of
marine mammals such as the Rio de La Plata dolphin,
Pontoporia blainvillei (Gervais & dOrbigny, 1844) and
the seabirds Cabots tern, Thalasseus acuavidus (Cabot,
1847) and Royal tern, Thalasseus maximus (Boddaert,
1783). The study was conducted at three different sites
within the study area: Punta Coronilla (PC), Cerro Verde
(CV) and Coronilla Islands (CI) (Figure 1).
Figure 1. Location of the Coastal Marine Protected Area (CMPA) of Cerro Verde in the northeast coast of Uruguay. PC: Punta Coronilla, CV: Cerro Verde, CI: Coronilla Islands.
Population structure
For the analysis of population structure only rst captures were considered in order to avoid bias introduced
by multiple recaptures. Since green turtles from multiple populations are found in foraging grounds
(Lahanas et al. 1998; Caraccio et al. 2008; MonznArgello et al. 2010; Prosdocimi et al. 2011; NaroMaciel et al. 2012) and since marine turtles from different populations may reach sexual maturity at different
sizes, the minimum size of nesting females recorded
among the main contributors to this foraging ground
was CCL = 90 cm, corresponding to a nesting female
from Trindade Island, Brazil (Almeida et al. 2011). In
order to evaluate size-based habitat segregation, data
from the three capture sites were tested for signicant
differences using a KruskalWallis test.
M. LPEZ-MENDILAHARSU ET AL.
2010). The photo-ID methodology can be used for recognition of individuals by comparing the shape and
arrangement of facial scutes (Reisser et al. 2008). Even
though only two turtles were identied using this
methodology in the present study, we have a large
photographic catalogue of known turtles, all of which
have been validated as they were also marked with
external ipper tags. To determine the yearly growth
rate only recaptured turtles from different sampling
seasons were considered and the longest recapture
interval was considered in cases of multiple recaptures.
Growth rate was calculated as follows: (CCLnal
CCLinitial)/recapture interval in years.
Relative density
For the 2008 and 2009 sampling seasons relative
density was studied through the CPUE at the PC and
CV sampling sites, using standardized capture conditions. One effort unit was dened as deploying
30 3 m of net during 1 h. CPUE was calculated by
dividing the total number of turtles captured during
each sampling period by the effort units. Annual differences in CPUE and spatial differences in CPUE between
PC and CV were analysed using the MannWhitney
U-test. All statistical analysis was carried out using the
software package BioEstat 3.0 (Ayres et al. 2003), with
a signicance level of alpha = 0.05.
Results
Population structure
All green turtles captured during the present study
were juveniles ranging from 28.8 to 64.3 cm CCL
(mean SD = 40.8 5.5 cm; n = 514). While no signicant differences were found in the size distribution
among years (KruskalWallis, H = 8.4; P = 0.21), size distributions differed signicantly among the three
studied areas (KruskalWallis, H = 35.6; P = 0.0001),
being smaller at PC (39.3 4.7 cm; n = 207) and larger
at CV (41.5 5.9 cm; n = 236) and CI (43.1 5.1 cm; n
= 71) (Figure 2).
Body condition
Relative density
During 2008 and 2009, 260 capture events were
recorded, including 37 recaptures comprising 531
effort units. The sampling effort was homogeneous
for both years, being 278 units of effort in 2008 and
253 units of effort in 2009. CPUE during 2009 (1.56
2.61 turtles effort unit1, n = 50) was signicantly
higher than in 2008 (0.95 1.82 turtles effort
unit1, n = 74) (MannWhitney, U = 1307, P = 0.005).
Signicant differences were found in CPUE between
sites during both sampling periods (MannWhitney,
U = 325.5, P = 0.0004 and U = 197.0, P = 0.04, respectively), being higher at Cerro Verde (Table II).
Discussion
Figure 3. (A) Number of green turtles (Chelonia mydas) examined among years (grey bars) and variation in the prevalence
(%) of tumours (black line), (B) Size class distribution of
green turtles (grey bars) and variation in prevalence (%) of
tumours for each size class (black line).
M. LPEZ-MENDILAHARSU ET AL.
Tagged
Recaptured
% Recaptures
2003
2004
2005
2006
2007
2008
2009
Total
33
47
62
28
68
61
210
509
0
0
2
3
7
10
32
54
0
0
3.2
10.7
10.3
16.4
15.2
10.6
Site
2008
Punta
Coronilla
Cerro Verde
Punta
Coronilla
Cerro Verde
2009
No.
trials
Turtles
captured
Effort
units
CPUE (mean
SD)
28
17
187.90
0.15 0.48
46
30
48
120
90.16
198.28
1.44 2.15
0.93 1.52
20
75
54.51
2.52 3.54
recruited juvenile green turtles (SCL <82 cm) in the Caribbean Sea. Data on annual growth rates for green
turtles in the SWAO are scarce. Annual growth rates
recorded in the state of Esprito Santo, Brazil, for juvenile green turtles ranging from 28 to 57 cm of CCL, was
3.5 cm year1 (Torezani et al. 2010). However, it is
worth nothing that in the latter case the study area
encompassed the efuent discharge channel of a
steel company characterized by high water temperatures (mean = 32C). Seasonal differences in growth
rates have been documented in studies of green
turtles from temperate regions (Koch et al. 2007;
McMichael et al. 2008). For example, Koch et al.
(2007) in Baja California recorded similar growth rates
(1.62 cm year1) for green turtles recaptured at intervals greater than 11 months. However, they found
that the growth was strongly seasonal, with growth
rates being over three times greater in summer than
in winter.
The CMPA of Cerro Verde is a warm-temperate foraging ground with low water temperatures during
winter (914C, from July to September). While some
turtles migrate to lower latitudes during cold months,
others remain in the area as evidenced by turtles
recorded during winter (Lpez-Mendilaharsu et al.
2006). Thus, the observed differences in growth rates
compared with other studies could have been caused
by different factors such as water temperature, food
availability and quality, population density and
reduced metabolism and activity during winter
(Felger et al. 1976; Bjorndal et al. 2000).
Green turtles recaptured across different years displayed feeding site delity, with 76% recaptured at
exactly the same location as the original capture. Very
few turtles were recaptured at a different site than
the original location, and the distance between these
sites was less than 2.5 km. Also all turtles recaptured
at a different location were found in deeper and
higher-energy areas, which agrees with the size-based
segregation structure found in the present study. In
contrast, the majority of captured turtles were not
seen again after the initial capture. Thus, animals that
were not recaptured could be those that (1) have low
site delity and utilize neritic habitats throughout
their distribution range, (2) have some site delity,
but were not captured again as they migrated to or
from preferred sites, or (3) have site delity to the
area, but failed to be recaptured in the sampling
nets. Two green turtles tracked by satellite telemetry
migrated to warmer waters in Brazil during winter
and returned to the study area at the end of spring
(Milagros Lpez-Mendilaharsu, unpublished data),
which suggests that the two latter options could be
Acknowledgements
We would like to thank all Karumb members, volunteers and
our families. Especially we thank Carlos Romero (sherman)
for his unconditional support throughout these years.
Thanks to the Army Park Service (Ministry of Defence) for
lodging us during the rst years of monitoring. We are very
grateful to Coronillas people who have supported Karumb
since the beginning of its activities in the area. We also
thank Luciana Alonso who provided valuable assistance in
the eld, laboratory and data analysis. Thanks to Alvar Carranza for his comments on the previous versions of the manuscript. This research was conducted under license (No. 200/
M. LPEZ-MENDILAHARSU ET AL.
Disclosure statement
No potential conict of interest was reported by the authors.
Funding
This work was supported by the Conservation Leadership Programme (Future Conservationist, Follow-up and Leadership
Awards) under grant no. 001404F; National Fish and Wildlife
Foundation; Peoples Trust for Endangered Species; Rufford
Small Grants; Idea Wild; PADI Foundation; International
Fund for Animal Welfare; Green Grants; and Project Aware
Foundation.
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