Marine Biology Research

ISSN: 1745-1000 (Print) 1745-1019 (Online) Journal homepage: http://www.tandfonline.com/loi/smar20

Demographic and tumour prevalence data for

juvenile green turtles at the Coastal-Marine
Protected Area of Cerro Verde, Uruguay
Milagros Lpez-Mendilaharsu, Gabriela M. Vlez-Rubio, Cecilia Lezama,
Anita Aisenberg, Antonia Bauz, Laura Berrondo, Victoria Calvo, Noel
Caraccio, Andrs Estrades, Martn Hernndez, Martn Laporta, Gustavo
Martnez-Souza, Melisa Morales, Vernica Quirici, Mariana Ros & Alejandro
Fallabrino
To cite this article: Milagros Lpez-Mendilaharsu, Gabriela M. Vlez-Rubio, Cecilia Lezama,
Anita Aisenberg, Antonia Bauz, Laura Berrondo, Victoria Calvo, Noel Caraccio, Andrs
Estrades, Martn Hernndez, Martn Laporta, Gustavo Martnez-Souza, Melisa Morales,
Vernica Quirici, Mariana Ros & Alejandro Fallabrino (2016): Demographic and tumour
prevalence data for juvenile green turtles at the Coastal-Marine Protected Area of Cerro Verde,
Uruguay, Marine Biology Research, DOI: 10.1080/17451000.2016.1169294
To link to this article: http://dx.doi.org/10.1080/17451000.2016.1169294

Published online: 27 May 2016.

Submit your article to this journal

View related articles

View Crossmark data

Full Terms & Conditions of access and use can be found at

http://www.tandfonline.com/action/journalInformation?journalCode=smar20
Download by: [201.159.189.48]

Date: 27 May 2016, At: 14:47

MARINE BIOLOGY RESEARCH, 2016

http://dx.doi.org/10.1080/17451000.2016.1169294

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

Downloaded by [201.159.189.48] at 14:47 27 May 2016

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.

Received 24 June 2015

Accepted 16 March 2016

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

2016 Informa UK Limited, trading as Taylor & Francis Group

RESPONSIBLE EDITOR

Leandro Bugoni
KEYWORDS

Southwest Atlantic;
protected areas; site delity;
size distribution; health
condition

Atlantic RMU (including the Uruguayan Coast) was

assessed as one of the healthiest sea turtle RMUs
(Wallace et al. 2011). Furthermore, it has been shown
that the juvenile stage is a key target for the global conservation of sea turtles (Crouse et al. 1987).
Available knowledge on the distribution of the globally endangered green turtle in the Southwestern
Atlantic Ocean (SWAO) suggests that the distribution
limit for this species most likely is located around
40S (see e.g. Gonzlez-Carman et al. 2012). Immature
green turtles occurring along this area recruit from
nesting populations, mainly from Ascension Island
(UK) but also from Trindade Island (Brazil), Aves Island
(Venezuela), Surinam and Guinea Bissau (Africa) (see

Karumb NGO, Av Rivera 3245, Montevideo 11600, Uruguay

Downloaded by [201.159.189.48] at 14:47 27 May 2016

M. LPEZ-MENDILAHARSU ET AL.

Caraccio 2008; Naro-Maciel et al. 2012). In the SWAO

important foraging grounds for green turtles have
been identied (Bellini & Sanches 1996; Marcovaldi &
Marcovaldi 1999; Gallo et al. 2006; Lpez-Mendilaharsu
et al. 2006; Bondioli et al. 2008; Gonzlez-Carman et al.
2012; Reisser et al. 2013). The main threats for this
species are incidental capture in sheries (e.g. gillnets),
and entanglement and ingestion of marine debris
(Bugoni et al. 2001; Laporta et al. 2006; Tourinho
et al. 2010). Another threat to the survival of green
turtles is the disease bropapillomatosis (FP) that
causes tumours on the skin. These tumours can
inhibit a turtles ability to swim, eat or see, depending
upon where the tumours grow; the tumours can also
grow internally, causing other health problems (Rodenbusch et al. 2014). Its prevalence in Brazilian waters,
and the high levels of incidence mainly in degraded
environments, suggest that FP might affect green
turtle survival in the region (Baptistotte 2007; Mascarenhas & Iverson 2008; Santos et al. 2010; Rodenbusch
et al. 2014; Zwarg et al. 2014).
In Uruguay, juvenile green turtles have a continuous
distribution along the Rio de la Plata estuary and Atlantic coast where important foraging grounds have been
documented, all of them characterized by rocky capes
and sandy beach arcs with high abundance and diversity of macro-algae (Lpez-Mendilaharsu et al. 2006).
The most important green turtle foraging ground is
located along the countrys northeast Atlantic coast,
in the area of Cerro Verde (Lpez-Mendilaharsu et al.
2006; Vlez-Rubio et al. 2013), which was declared a
Coastal-Marine Protected Area (CMPA) by the government of Uruguay (Decree 68/2011) in 2011. Over
several decades the Cerro Verde area was under
intense degradation, principally due to waste water
runoff from agriculture, illegal shing and overexploitation of marine resources (Fallabrino & LpezMendilaharsu 2008). Therefore, the creation of this
CMPA and subsequent integration of other marine
areas to the National System of Protected Areas
(Sistema Nacional de reas Protegidas, SNAP) were
important steps towards the reduction of threats
along this critical foraging habitat (Lpez-Mendilaharsu
et al. 2006; Vlez-Rubio et al. 2013).
Marine Protected Areas (MPAs) are quickly gaining
popularity as a management tool for marine conservation, sheries and leisure activities (Halpern 2003;
Mazaris et al. 2014). In this way data collected in an
area prior to establishment of an MPA serves as a reference point for future evaluations of the effectiveness
of the area in protecting habitats and species of
special concern (Katselidis et al. 2013; Moland et al.
2013; Schoeld et al. 2013). Besides providing this

kind of baseline data for future assessments, this

study provides valuable information for wider analyses
on green turtle ecology and health status in the SWAO.
Specically, this study focused on: (1) the green
turtle size distribution and size variations among different years and sites; (2) the prevalence of tumours, body
condition index and annual growth rate as indicators of
population health; (3) the site delity through markrecapture data; and (4) the catch per unit effort
(CPUE) to infer relative density and its variations
among years and sites within the study area.

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).

Turtle capture and measurements

Between 2002 and 2009 and from December to April
(warm months), green turtles were captured at the
three sites, PC, CV and CI, using entanglement nets
made of monolament (30 3 m, mesh size = 32 cm
stretched). Nets were deployed during daylight hours
in areas that did not exceed 5 m depth and monitored
at 30-minute intervals. Soak time was recorded and
limited by oceanographic conditions. Nets were
always deployed at the same location at the three
sites and marked with GPS coordinates (Garmin handheld GPS unit). Incidentally captured turtles by a local

Downloaded by [201.159.189.48] at 14:47 27 May 2016

MARINE BIOLOGY RESEARCH

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.

sherman at PC, who used an entanglement net with the

same characteristics, were also included in the analysis.
Turtles recaptured at their original capture site, i.e. less
than 30 m apart (which is the length of the entanglement net), were considered to have high site delity.
Upon capture at CV and PC, turtles were taken to the
beach, where they were measured, weighed, tagged
and released. Turtles captured at CI were transported
to PC (< 2.5 km), where they were released after data
collection.
General health and external abnormalities (missing
ippers and presence of external tumours) were
recorded. Curved carapace length (CCL) from the
nuchal notch to the posteriormost portion of the rear
marginal was measured using a exible tape ( 0.1
cm) (Bolten 1999), calibrated each day before measurements. Turtles were weighed to the nearest 0.5 kg
using a spring balance, which was calibrated before
each use. Each turtle was identied and Inconel tags
(style #681, National Band and Tag, Kentucky, USA)

were attached to the trailing edge of the second

large proximal scale of both front ippers.

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.

Downloaded by [201.159.189.48] at 14:47 27 May 2016

Body condition and growth

Prevalence of tumours for each sampling year and size
class was calculated as the percentage of turtles that
had evidence of tumours among the total number of
turtles examined. All green turtles captured at the
three sampling locations were examined for external
and oropharyngeal tumours; however, we considered
them as bropapillomatosis (FP) on the basis of previous studies that conrmed the presence of FP
tumours in the area (Pastorino et al. 2007). Differences
between annual and size class prevalence of tumours
were analysed with the Chi-square test.
The CCL was converted to straight carapace length
(SCL) using the equation described by Bjorndal &
Bolten (1989), and the body condition index (BCI) was
calculated using the following formula (Bjorndal et al.
2000): BCI = (Weight/SCL3)10,000; SCL in cm and
weight in kg. For the CCL and the BCI, statistical differences between turtles with and without tumours were
analysed using the MannWhitney U-test.
Each recaptured turtle was identied by the tags or
photo-ID when tags were lost and the scar present
(Reisser et al. 2008; Schoeld et al. 2008; Jean 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

Figure 2. Size distribution of juvenile green turtles (Chelonia

mydas) across the different capture sites in the CMPA of
Cerro Verde: (A) Punta Coronilla, (B) Cerro Verde, (C) Coronilla
Islands.

A total of 514 green turtles were captured, 490 turtles

using direct capture methods and 24 incidentally captured by local sherman. Among the incidentally captured turtles 25% (n = 6) were drowned.
Eleven turtles (2%) had injuries caused by natural
and/or anthropogenic causes. A total of six turtles
had lost a fore or hind limb, while the other ve

MARINE BIOLOGY RESEARCH

Downloaded by [201.159.189.48] at 14:47 27 May 2016

showed direct evidence of interaction with shing gear,

such as monolament shing lines, hook and lines and
cotton ropes entangled around the body.
Tumours were recorded predominantly on the inguinal and axillaries region. Tumour prevalence for the
whole studied period was 5.3% (n = 27) and did not signicantly differ between years (Chi-square test 2 =
8.53; df = 6; P = 0.2) (Figure 3A). Mean CCL for turtles
without tumours differed signicantly from those
with tumours (40.3 4.9 cm, n = 482; 50.3 6.7 cm, n
= 27, respectively; MannWhitney, U = 1303; P =
0.0001) and augmented with the increase in size of
the turtles ( 2 = 98.41; df = 7; P = 0) (Figure 3B).
The mean body condition index of green turtles
ranged between 0.65 and 1.77 (1.25 0.14, n = 494)
and we did not nd signicant differences between
BCI for individuals with and without tumours (Mann
Whitney, U = 4126.5; P = 0.25).

Annual growth rate and site delity

From December 2002 to April 2009, 509 green turtles
were tagged with metal tags and released in the
study area. A total of 43 green turtles were recaptured
54 times: 35 turtles were recaptured once, six turtles
twice, one turtle three times and one turtle four
times (Table I). From the recaptured events, 52 were

identied by metal tags, while two were identied by

photo-ID, due to loss of both tags. The percentage of
green turtle recaptures was 10.6% (Table I). Of the 43
recaptured turtles, 17 had recapture intervals 11
months and were thus considered in growth rate analysis. From this subsample (n = 17) a total of 15 turtles
resulted in growth rate measurements, while two
were excluded from the analysis because they were
not measured at the rst or last capture. Juvenile
green turtles ranged in size from 35.1 to 50.7 cm CCL
(41.0 5.0 cm, n = 15) at initial capture. Recapture
intervals varied from 11 to 47 months. Growth rates
ranged from 0.3 to 2.9 cm year1 and the mean
annual growth rate was 1.6 0.9 cm year1.
From the 54 recapture events, the majority (80.0%,
n = 43) occurred at the original capture location.
Specically 81.0% (30 out of 37) of the recapture
events were recorded within the same sampling
season and 76.0% (13 out of 17) identied during previous years showed high site delity. It is worth noting
that the remaining recapture events (n = 11) corresponded to turtles originally captured at Punta Coronilla and recaptured at Cerro Verde (2.2 km apart)
and Coronilla Islands (2.5 km apart) or rst captured
at Cerro Verde and recaptured at the Coronilla Islands
(2.0 km apart). Mean distance SD between recaptures
at different locations was 2.4 0.2 km.

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).

Green turtle populations in the Atlantic Ocean recruit

from oceanic to neritic habitats (pelagic to benthic
phase) when they reach a size of 2535 cm straight carapace length for the North Atlantic Ocean (Bjorndal
et al. 2000), although recent studies suggest that they
are not strictly neritic in the temperate SWAO (Gonzlez-Carman et al. 2012). The results show that the
CMPA of Cerro Verde provides a habitat for juvenile

M. LPEZ-MENDILAHARSU ET AL.

Table I. Number of juvenile green turtles (Chelonia mydas)

tagged and recaptured, including multiple recaptures, and
percentage of recaptures for each sampling period.

Downloaded by [201.159.189.48] at 14:47 27 May 2016

Number of green turtles

Year

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

green turtles in the early neritic phase (i.e. 2964 cm)

with a size distribution strongly skewed towards
smaller turtles from 35 to 45 cm. The absence of
larger turtles (>65 cm) may be associated with an ontogenic shift in habitat preferences and further developmental migrations to other foraging grounds,
eventually closer to their natal beaches (Bjorndal
et al. 2000; Meylan et al. 2011).
The results of this study showed size-based habitat
segregation similar to other foraging populations
(Lpez-Mendilaharsu et al. 2005; Koch et al. 2007;
Lpez-Castro et al. 2010). Turtles captured at Punta Coronilla were smaller than turtles captured at less protected and deeper areas such as Cerro Verde and the
Coronilla Islands. Although the reasons for this segregation remain unknown, Koch et al. (2007) studying
green turtle ecology in Baha Magdalena, Mexico,
suggested that diet preferences may play a role in
the spatial pattern observed with larger turtles
feeding on sea grass and smaller turtles on algae. In
the study area the green turtles diet is primarily based
on macroalgae (Lpez-Mendilaharsu et al. 2006;
Vlez-Rubio et al. 2016) which is present throughout
the area; thus, the size-based segregation seems to be
related to the physical features and environmental conditions of the different sites, e.g. protected and shallow
versus exposed and deeper habitats. For example, as
has been reported for other reptiles (Wikelski et al.

Table II. Summary of capture data of green turtle (Chelonia

mydas) for Punta Coronilla and Cerro Verde during 2008 and
2009, including number of trials, number of turtles captured,
total effort units, dened as 30 3 m of net during 1 h, and
average CPUE (mean standard deviation).
Year

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

1993), smaller turtles may have higher energy

demands, due to their relatively higher mass-specic
metabolic rate and lower digestive efciency. Thus,
they may prefer sheltered areas where the net energy
expenditure during foraging activities is less than in
high-energy zones (Lpez-Mendilaharsu et al. 2005).
Tumour prevalence at the studied area (5.3%) falls
within the range recorded in other foraging areas in
the SWAO. In Brazil, tumour prevalence, conrmed as
bropapillomatosis, ranges between 3.4 and 58.3%
off the mainland. The higher proportion corresponds
to the state of Esprito Santo where the disease is
endemic since it was rst documented in 1986,
whereas it is absent from oceanic islands like Fernando
de Noronha and Atol das Rocas (Baptistotte 2007;
Santos et al. 2010). Absence of tumours among
smaller turtles as well as the increase in prevalence
with size agreed with previous results from other foraging grounds in Brazil (Baptistotte 2007; Proietti et al.
2007; Rodenbusch et al. 2014). According to Baptistotte
(2007) there is an increase in tumour prevalence, as size
increases, up to 80 cm. However, Santos et al. (2010)
recorded lower prevalence in size classes larger than
50 cm and suggested that mortality prior to reaching
this size or the ability to recover from the disease
may explain this result. The increasing prevalence
also among 5065 cm size classes recorded during
the present study is in agreement with the rst hypothesis; however, the absence of larger turtles (CCL >65
cm) in the study area prevents full comparisons with
other studies.
Analyses of stranding data in the area have indicated that sheries interaction and anthropogenic
debris consumption are by far the most important
threats affecting green turtles in Uruguayan waters
(Vlez-Rubio et al. 2013). Evidence of interaction with
sheries was noted for some of the green turtles captured (n = 11). However, incidence of human impact
may be higher due to hook or debris ingestion that
could not be determined by external examination
alone (Vlez-Rubio et al. 2013).
The mean BCI (1.25) was within the range recorded
by Bjorndal et al. (2000), which varied among years
between 1.2 and 1.3 for Caribbean green turtles. The
lack of signicant differences in the BCI of the turtles
with tumours and those without them may indicate
that the FP is not yet affecting the growth and survival
of green turtles in the area.
The mean annual growth rate recorded in the
present study, 1.6 cm year1 (1.5 cm year1, converted
to SCL as described by Bjorndal & Bolten (1989)) was
below the one recorded by Bjorndal et al. (2000),
who estimated a mean of 4.3 cm year1 for post

Downloaded by [201.159.189.48] at 14:47 27 May 2016

MARINE BIOLOGY RESEARCH

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

more likely. Future telemetry studies could help

address these questions.
CPUE results for 2008 and 2009 showed that green
turtle density between years and sites is not homogeneous, with higher densities of green turtles in
Cerro Verde. Future studies should include environmental and oceanographic variables, as well as food
resource availability and distribution, to possibly identify the causes of the observed results. Despite the fact
that the CPUE was higher during 2009, the short duration of the study does not allow identifying trends
in green turtles densities. Nevertheless, this index provided useful data about relative density and constitutes
a baseline data set against which to compare future
juvenile green turtle abundance and trends.
This study provides important information on the
ecology and health condition of green turtles from a
region where long-term in-water studies are scarce.
Although green turtles are abundant in coastal habitats
along the SWAO, there have been very few long-term
mark-recapture studies of the species in the region
(Gallo et al. 2006; Torezani et al. 2010; Colman et al.
2015). Thus, the maintenance of long-term standardized monitoring programmes like the present one
brings the opportunity to improve our knowledge on
life history traits of green turtles in the temperate
SWAO. In addition, further in-water studies on abundance trends, habitat use and preferences will serve
to better understand the population dynamics at different green turtle foraging areas in the SWAO.
In summary, the Coastal-Marine Protected Area of
Cerro Verde not only provides protection to green
turtles within its boundaries but also has served as a
model for the integration of new MPAs within the
countrys National System of Protected Areas, beneting local aggregations of green turtles associated
with rocky capes along the coast of Uruguay (Fallabrino
& Lpez-Mendilaharsu 2008). In this way it is imperative
to continue monitoring the abundance trends in the
region to be able to evaluate the outcome of the
ongoing conservation efforts.

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.

04, 073/08 and 323/11) from the Fauna Department Ministry

of Cattle, Agriculture and Fishing of Uruguay.

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.

Downloaded by [201.159.189.48] at 14:47 27 May 2016

References
Acha EM, Mianzan HW, Guerrero RA, Favero M, Bava J. 2004.
Marine fronts at the continental shelves of austral South
America: physical and ecological processes. Journal of
Marine Systems 44:83105. doi:10.1016/j.jmarsys.2003.09.005
Almeida AP, Moreira LMP, Bruno SC, Thom JCA, Martins AS,
Bolten AB, et al. 2011. Green turtle nesting on Trindade
Island, Brazil: abundance, trends, and biometrics.
Endangered Species Research 14:193201. doi:10.3354/
esr00357
Ayres M, Ayres Junior M, Ayres DL, Santos AS. 2003. BioEstat
3.0: aplicaes estatsticas nas reas das cincias
biolgicas e mdicas. Belm, Brazil: Sociedade Civil
Mamirau. Computer program.
Baptistotte C. 2007. Caracterizao Espacial e Temporal da
Fibropapilomatose em Tartarugas Marinhas da Costa
Brasileira. PhD Thesis. University of So Paulo, Piracicaba,
Brazil. 63 pages.
Bellini C, Sanches TM. 1996. Reproduction and feeding of
marine turtles in the Fernando de Noronha Archipelago,
Brazil. Marine Turtle Newsletter 74:1213.
Bjorndal KA, Bolten AB. 1989. Comparison of straight-line and
over-the-curve measurements for growth rates of green
turtles, Chelonia mydas. Bulletin of Marine Science
45:18992.
Bjorndal KA, Bolten AB, Chaloupka MY. 2000. Green turtle
somatic growth model: evidence for density dependence.
Ecological Applications 10:26982.
Bolten AB. 1999. Techniques for measuring sea turtles. In:
Eckert KL, Bjorndal KA, Abreu-Grobois FA, Donnelly M,
editors. Research and Management Techniques for the
Conservation of Sea Turtles, IUCN/SSC Marine Turtle
Specialist Group Publication No. 4. Washington, DC: SSC/
IUCN Marine Turtle Specialist Group, p 11014.
Bondioli ACV, Nagaoka SM, Monteiro-Filho D. 2008. Chelonia
mydas: habitat and occurrence. Herpetological Review
39:213.
Borthagaray AI, Carranza A. 2007. Mussels as ecosystem
engineers: their contribution to species richness in a
rocky littoral community. Acta Oecologica 31:24350.
doi:10.1016/j.actao.2006.10.008

Bugoni L, Krause L, Petry MV. 2001. Marine debris and human

impacts on sea turtles in Southern Brazil. Marine Pollution
Bulletin 42:133034. doi:10.1016/S0025-326X(01)00147-3
Caraccio MN. 2008. Anlisis de la Composicin Gentica de
Chelonia mydas (Tortuga Verde) en el rea de
Alimentacin y Desarrollo de Uruguay. MSc Thesis.
Science Faculty, University of the Republic, Montevideo,
Uruguay. 89 pages.
Caraccio MN, Domingo A, Mrquez A, Naro-Naciel E, Miller P,
Pereira A. 2008. Las aguas del Atlntico sudoccidental y su
importancia en el ciclo de vida de la tortuga cabezona
(Caretta caretta): evidencias a travs del anlisis del
ADNmt. Collective Volume of Scientic Papers, ICCAT
62:183137.
Colman LP, Patrcio ARC, McGowan A, Santos AJB, Marcovaldi
MA, Bellini C, et al. 2015. Long-term growth and survival
dynamics of green turtles (Chelonia mydas) at an isolated
tropical archipelago in Brazil. Marine Biology 162:11122.
doi:10.1007/s00227-014-2585-5
Crouse DT, Crowder LB, Caswell H. 1987. A stage-based population model for loggerhead sea turtles and implications
for conservation. Ecology 68:141223. doi:10.2307/
1939225
Defeo O, Horta S, Carranza A, Lercari D, de lava A, Gmez J,
et al. 2009. Hacia un Manejo Ecosistmico de Pesqueras.
reas Marinas Protegidas en Uruguay. Montevideo:
Facultad de Ciencias-DINARA. 122 pages.
Fallabrino A, Lpez-Mendilaharsu M. 2008. Juvenile green
turtles as a agship species: starting point for the rst
marine protected area in Uruguay. Marine Turtle
Newsletter 122:1617.
Felger RS, Cliffton K, Regal PJ. 1976. Winter dormancy in sea
turtles: independent discovery and exploitation in the
Gulf of California, Mexico by two local cultures. Science
191:28385. doi:10.1126/science.191.4224.283
Gallo BMG, Macedo S, Giffoni BB, Becker JH, Barata PCR. 2006.
Sea turtle conservation in Ubatuba (Southeastern Brazil), a
feeding area with incidental capture in coastal sheries.
Chelonian Conservation and Biology 5:93101. doi:10.
2744/1071-8443(2006)5[93:STCIUS]2.0.CO;2
Gonzlez-Carman V, Falabella V, Maxwell S, Albareda DA,
Campagna C, Mianzan H. 2012. Revisiting the ontogenetic shift paradigm: the case of juvenile green turtles in
the SW Atlantic. Journal of Experimental Marine Biology
and Ecology 429:6472. doi:10.1016/j.jembe.2012.06.007
Halpern BS. 2003. The impact of marine reserves: do reserves
work and does reserve size matter? Ecological Applications
13:11737. doi:10.1890/1051-0761(2003)013[0117:TIOMRD]
2.0.CO;2
Hirth HF. 1997. Synopsis of the Biological Data on the Green
Turtle Chelonia mydas (Linnaeus, 1758). Biological report
submitted to the US Fish and Wildlife Service, 97(1).
Washington, DC: Fish and Wildlife Service. 120 pages.
Jean C, Ciccione S, Talma E, Ballorain K, Bourjea J. 2010. Photoidentication method for green and hawksbill turtles rst
results from Reunion. Indian Ocean Turtle Newsletter
11:813.
Katselidis KA, Schoeld G, Dimopoulos P, Stamou GN, Pantis
JD. 2013. Evidence based management to regulate the
impact of tourism at a key sea turtle rookery. Oryx
47:58494. doi:10.1017/S0030605312000385

Downloaded by [201.159.189.48] at 14:47 27 May 2016

MARINE BIOLOGY RESEARCH

Koch V, Brooks LV, Nichols WJ. 2007. Population ecology of

the green/black turtle (Chelonia mydas) in Baha
Magdalena, Mexico. Marine Biology 153:3546. doi:10.
1007/s00227-007-0782-1
Lahanas PN, Bjorndal KA, Bolten AB, Encalada SE, Miyamoto
MM, Valverde RA, et al. 1998. Genetic composition of a
green turtle (Chelonia mydas) feeding ground population:
evidence for multiple origins. Marine Biology 130:34552.
doi:10.1007/s002270050254
Laporta M, Miller P, Ros M, Lezama C, Bauz A, Aisenberg A,
et al. 2006. Conservacin y manejo de tortugas marinas en
la zona costera uruguaya. In: Menafra R, Rodrguez-Gallego
L, Scarabino F, Conde D, editors. Bases para la Conservacin
y el Manejo de la Costa Uruguaya. Montevideo, Uruguay:
Vida Silvestre Uruguay, p 25969.
Lpez-Castro MC, Koch V, Mariscal-Losa A, Nichols WJ. 2010.
Long-term monitoring of black turtles (Chelonia mydas)
at coastal foraging areas off the Baja California Peninsula.
Endangered Species Research 11:3545. doi:10.3354/
esr00264
Lpez-Mendilaharsu M, Gardner SC, Seminoff JA, RiosmenaRodriguez R. 2005. Identifying critical foraging habitats of
the green turtle (Chelonia mydas) along the Pacic coast
of the Baja California peninsula, Mexico. Aquatic
Conservtion 15:25969. doi:10.1002/aqc.676
Lpez-Mendilaharsu M, Estrades A, Caraccio MA, Calvo V,
Hernndez M, Quirici V. 2006. Biologa, ecologa y
etologa de las tortugas marinas en la zona costera uruguaya. In: Menafra R, Rodrguez-Gallego L, Scarabino F,
Conde D, editors. Bases para la Conservacin y el Manejo
de la Costa Uruguaya. Montevideo, Uruguay: Vida
Silvestre Uruguay, p 24757.
Marcovaldi MA, Marcovaldi GG. 1999. Marine turtles of Brazil:
the history and structure of Projeto TAMAR-IBAMA.
Biological Conservation 91:3541. doi:10.1016/S00063207(99)00043-9
Mascarenhas R, Iverson PJ. 2008. Fibropapillomatosis in
stranded green turtles, Chelonia mydas, in Paraiba State,
northeastern Brazil: evidence of a Brazilian epizootic?
Marine Turtle Newsletter 120:36.
Mazaris AD, Almpanidou V, Wallace B, Schoeld G. 2014. A
global gap analysis of sea turtle protection coverage.
Biological Conservation 173:1723. doi:10.1016/j.biocon.
2014.03.005
McMichael E., Seminoff J, Carthy R. 2008. Growth rates of wild
green turtles, Chelonia mydas, at a temperate foraging
habitat in the northern Gulf of Mexico: assessing shortterm effects of cold-stunning on growth. Journal of Natural
History 42:2793807. doi:10.1080/00222930802357335
Meylan PA, Meylan A, Gray JA. 2011. Ecology and migrations
of sea turtles 8. Tests of the developmental habitat hypothesis. Bulletin of the American Museum of Natural History
357:170. doi:10.1206/357.1
Moland E, Moland OE, Knusten H, Garrigou P, Heiberg ES, Ring
KA, et al. 2013. Lobster and cod benet from small-scale
northern marine protected areas: inference from an
empirical beforeafter control-impact study. Proceedings
of the Royal Society B 280:20122679. 9 pages. doi:10.
1098/rspb.2012.2679
Monzn-Argello C, Rico C, Naro-Maciel E, Varo-Cruz N, Lopez
P, Marco A, et al. 2010. Population structure and conservation implications for the loggerhead sea turtle of the Cape

Verde Islands. Conservation Genetics 11:187184. doi:10.

1007/s10592-010-0079-7
Naro-Maciel E, Bondioli ACV, Martin M, Almeida AP,
Baptistotte C, Bellini C, et al. 2012. The interplay of
homing and dispersal in green turtles: a focus on the
southwestern Atlantic. Journal of Heredity 103:792805.
doi:10.1093/jhered/ess068
Pastorino V, Aguirre A, Caraccio N, Hernndez M, Fallabrino A,
Moraa JA. 2007. First histopathological conrmation of
bropapillomatosis in juvenile green turtles in Uruguay.
In: Mast RB, Hutchinson BJ, Hutchinson AH, editors.
Proceedings of the 24th Annual Symposium on Sea
Turtle Biology and Conservation, NOAA Tech. Memo.
NMFS-SEFSC 567, p 145.
Proietti MC, Reisser JW, Kinas PG. 2007. Avaliao preliminar
da ocorrncia de bropapilomatose em tartarugas-verdes
(Chelonia mydas) incidentes na Reserva Biolgica Marinha
do Arvoredo, SC. In: XII Congresso Latino-Americano de
Cincias do Mar. Florianpolis, Brazil: Asociacin Brasilea
de Oceanografa, p 18.
Prosdocimi L, Carman VG, Albareda DA, Remis MI. 2011.
Genetic composition of green turtle feeding grounds in
coastal waters of Argentina based on mitochondrial DNA.
Journal of Experimental Marine Biology and Ecology
412:3745. doi:10.1016/j.jembe.2011.10.015
Reisser J, Proietti MC, Kinas PG, Sazima I. 2008. Photographic
identication of sea turtles: method description and validation, with an estimation of tag loss. Endangered
Species Research 5:7382. doi:10.3354/esr00113
Reisser J, Proietti M, Sazima I, Kinas P, Horta P, Secchi E. 2013.
Feeding ecology of the green turtle (Chelonia mydas) at
rocky reefs in western South Atlantic. Marine Biology
160:316979. doi:10.1007/s00227-013-2304-7
Rodenbusch CR, Baptistotte C, Werneck MR, Pires TT, Melo
MTD, de Atade MW, et al. 2014. Fibropapillomatosis in
green turtles Chelonia mydas in Brazil: characteristics of
tumors and virus. Diseases of Aquatic Organisms
111:20721. doi:10.3354/dao02782
Santos RG, Martins AS, Torezani E, Baptistotte C, Faria JN,
Horta PA, et al. 2010. Relationship between bropapillomatosis and environmental quality: a case study with Chelonia
mydas off Brazil. Diseases of Aquatic Organisms 89:8795.
doi:10.3354/dao02178
Schoeld G, Katselidis KA, Dimopoulos P, Pantis JD. 2008.
Investigating the viability of photo-identication as an
objective tool to study endangered sea turtle populations.
Journal of Experimental Marine Biology and Ecology
360:10308. doi:10.1016/j.jembe.2008.04.005
Schoeld G, Scott R, Dimadi A, Fossette S, Katselidis KA,
Koutsoubas D, et al. 2013. Evidence-based marine protected area planning for a highly mobile endangered
marine vertebrate. Biological Conservation 161:10109.
doi:10.1016/j.biocon.2013.03.004
Torezani E, Baptistotte C, Mendes SL, Barata PR. 2010. Juvenile
green turtles (Chelonia mydas) in the efuent discharge
channel of a steel plant, Esprito Santo, Brazil, 20002006.
Journal of the Marine Biological Association of the United
Kingdom 90:23346. doi:10.1017/S0025315409990579
Tourinho PS, Ivar do Sul JA, Fillmann G. 2010. Is marine debris
ingestion still a problem for the coastal marine biota of
southern Brazil? Marine Pollution Bulletin 60:396401.
doi:10.1016/j.marpolbul.2009.10.013

10

M. LPEZ-MENDILAHARSU ET AL.

Downloaded by [201.159.189.48] at 14:47 27 May 2016

Vlez-Rubio GM, Estrades A, Fallabrino A, Toms J. 2013.

Marine turtle threats in Uruguayan waters: insights from
12 years of stranding data. Marine Biology 160:2797811.
doi:10.1007/s00227-013-2272-y
Vlez-Rubio GM, Cardona L, Lpez-Mendilaharsu M, Martnez
Souza G, Carranza A, Gonzlez-Paredes D, et al. 2016.
Ontogenetic dietary changes of green turtles (Chelonia
mydas) in the temperate Southwestern Atlantic. Marine
Biology 163:57. 16 pages. doi:10.1007/s00227-016-2827-9
Wallace BP, DiMatteo AD, Hurley BJ, Finkbeiner EM, Bolten AB,
Chaloupka MY, et al. 2010. Regional management units for
marine turtles: a novel framework for prioritizing conservation and research across multiple scales. PLoS ONE 5:
e15465. 11 pages. doi:10.1371/journal.pone.0015465

Wallace BP, DiMatteo AD, Bolten AB, Chaloupka MY,

Hutchinson BJ, Abreu-Grobois FA, et al. 2011. Global conservation priorities for marine turtles. PLoS ONE 6:e24510.
14 pages. doi:10.1371/journal.pone.0024510
Wikelski M, Gall B, Trillmich F. 1993. Ontogenetic changes in
food intake and digestion rate of the herbivorous marine
iguana (Amblyrhynchus cristatus, Bell). Oecologia 94:373
79. doi:10.1007/BF00317112
Zwarg T, Rossi S, Sanches TC, Cesar M, Werneck MR,
Matushima ER. 2014. Hematological and histopathological
evaluation of wildlife green turtles (Chelonia mydas) with
and without bropapilloma from the north coast of So
Paulo State, Brazil. Pesquisas Veterinarias Brasileiras
34:68288. doi:10.1590/S0100-736X2014000700013