Download Hawksbill turtle (Eretmochelys imbricata Linnaeus 1766) and green

Amphibia-Reptilia 27 (2006): 539-547
Hawksbill turtle (Eretmochelys imbricata Linnaeus 1766) and green
turtle (Chelonia mydas Linnaeus 1754) nesting activity (2002-2004)
at El Cuyo beach, Mexico
Raquel Xavier1,2 , Andre Barata3 , Leopoldo Palomo Cortez4 , Nuno Queiroz1 , Eduardo Cuevas4
Abstract. The Yucatan Peninsula nesting hawksbill turtles’ population (Eretmochelys imbricata Linnaeus 1766) is the biggest
in the Caribbean and fourth in the world; within the Ría Lagartos Biosphere Reserve, at El Cuyo beach both hawksbill and
green turtle (Chelonia mydas Linnaeus 1754) nest. In the present study, the nesting trend and reproductive output of both
species during three consecutive nesting seasons (2002-2004) was evaluated. Night patrols from mid April to September
allowed the collection of data on number of nests, nest location and size of females. The number of hawksbill and green
turtles’ nests decreased along these seasons. No differences were found in mean length of female turtles of both species
between nesting seasons. Both species showed high nest site fidelity with average distance between nests of 3 km for
Hawksbill and 1.8 km for Green turtles. The regression analysis between size and fecundity was significant (p < 0.05)
for both species. The spatial variation of laid nests was also analyzed revealing that both species nested mainly on the dune
zone. Predation has risen on El Cuyo beach, affecting mostly hawksbills nests. Hurricane Ivan destroyed the majority of green
turtles nests in 2004.
Introduction
The green turtle (Chelonia mydas) is currently
listed as Endangered by the IUCN Red List
Book while the hawksbill turtle (Eretmochelys
imbricata) is listed as Critically Endangered
(Baillie and Groombridge, 1996). Both species
are also included in the Appendix I of the
Convention on International Trade of the Endangered Species and Wild Fauna and Flora
(CITES, 2005).
Estimating population size for long-lived animals, such as sea turtles, is important for assessing their risk of extinction, since such populations decline more rapidly and recover slower
than those of short-lived species (Musick, 1999;
Alvarado and Murphy, 1999; Gerrodette and
1 - CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Campus Agrário de Vairão, 4485-661
Vairão, Portugal
Corresponding author’s e-mail: [email protected]
2 - Departamento de Zoologia e Antropologia, Faculdade
de Ciencias da Universidade do Porto, 4099-022 Porto,
Portugal
3 - Faculdade de Ciências da Universidade de Lisboa, Departamento de Biologia Animal, Campo Grande, 1749016 Lisboa, Portugal
4 - Pronatura Península Yucatán, Calle 32 n◦ 269, Col. Pinzon II, Mérida, CP 97207, Yucatán, México
Taylor, 1999). Considering that both green and
hawksbill turtles are endangered species it is important to monitor changes in population structure. Sea turtles are difficult to census because
they have a complex life cycle which includes
different habitats such as pelagic for hatchlings,
benthic habitats for juveniles and adult ones.
They also disperse over a wide area and are difficult to detect in the water, making it extremely
difficult to estimate the size of this part of the
population (Gerrodette and Taylor, 1999). Thus,
the most common and feasible method for monitoring population trends is by counting nesting
females on the beaches (Meylan and Donnely,
1999).
The number of females nesting and reproductive output (number of nests and number of
eggs) are dependent on many endogenous factors, such as genetics, body size and condition
(Broderick et al., 2001). Several exogenous factors, such as climate, migratory distance, and
food quality are also likely to affect reproduction (Hamann et al., 2003; Broderick et al.,
2003). The interaction of both factors will also
induce variations in reproductive output. For example, in reptiles, body size limits the number of eggs produced by a female although this
© Koninklijke Brill NV, Leiden, 2006. Also available online - www.brill.nl/amre
540
limit may not be reached if conditions in foraging areas are sub-optimal and body condition
is low (Shine, 1992). It is thought that endogenous energy reserves play a vital role in both
intra and interannual reproductive effort in both
sexes, especially in the case of the herbivorous
green turtles because they are at a lower trophic
level than hawksbills are (Broderick et al., 2001;
Hamann et al., 2003).
There are several natural mortality factors
for both eggs and hatchlings on the beach:
(1) high tides and storms that may drown eggs
and wash away nests, (2) egg predation and
(3) hatchling predation, generally by nocturnal animals (Georges et al., 1993; Milton and
Lutz, 2003). Determining clutch size (or fecundity) and hatching success provides fundamental data for the conservation and management of
sea turtles because these data are essential for
understanding the beach or hatchery suitability
and the general health of the nesting population
(Miller, 1999).
The population of hawksbill turtles nesting in
the Yucatan Peninsula increased from 1990 until
1999 (Garduño-Andrade et al., 1999), due to
the start of conservation programs in the middle
of the 1970’s and the total ban imposed on sea
turtle exploitation in Mexico in 1990 (GarduñoAndrade et al., 1999; Meylan, 1999).
With this work we are updating the insights
on a number of important aspects on the reproduction of both hawksbill and green turtles at El
Cuyo beach given by Garduño-Andrade (1999)
and Salum-Fares (2001), as well as to postulate
hypothesis explaining the major changes to the
patterns reported by these authors.
Material and Methods
This study took place in El Cuyo beach (21◦ 31 N, 87◦ 41 W),
in the Ría Lagartos Biosphere Reserve, a RAMSAR site,
located in the Yucatan state of Mexico, which is one of
only two beaches where green turtles nest in this state
(Carabias et al., 1999). The study was conducted under the
“Conservation Program of marine turtles in the north coast
of the Yucatan Península” for which Pronatura Península
Yucatán is responsible in this Reserve (Register CONVDGVS/CPCTM-004-YUC-002). The study area comprises
R. Xavier et al.
two portions of beach, divided by the town’s harbour, the
nesting beach extends for 13 km east from the harbour and
11 km west of the harbour. The nesting season for Hawksbill turtles’ at El Cuyo begins in April and finishes in September (Garduño-Andrade et al., 1999; Fares, 2003) and
for Green turtles begins in June and finishes in September
(Hernandez-Guzmán, 2003).
Data on nests and females were collected on night patrols, (minimum of two observers per night) with an All
Terrain Vehicle (ATV) between 2200 and 0400 (local time),
every night, during nesting seasons from 2002 to 2004.
Every female found was measured and tagged after
oviposition to ensure minimum disturbance (Broderick and
Godley, 1999). Standard curved carapace length (CCL) was
measured from the anterior point at midline (nuchal scute)
to the posterior pit of the supracaudal (Bolten, 1999). Inconel “ear tags” (model 681 National Band and Tag Company) were applied. The sizes of nesting females arriving at
El Cuyo beach during the three nesting seasons were compared with the Kruskall-Wallis non parametric test for independent samples using Statistica 6.0 (StatSoft).
The position of every nest was recorded using a GPS
Garmin Etrex summit and location on the beach was classified as: dune, beach platform and washing zone. Several
nests were only spotted by turtle prints on the sand and track
morphology was used to identify the species, since this is
a differentiating characteristic between these two species:
green turtle make a symmetrical crawl track, whereas that
of hawksbill is markedly asymmetrical (Broderick and Godley, 1996); their identification could be confirmed by the
presence of hatchlings in most nests, thus we assume that
all identifications were made correctly. Non-nesting emergences, such as tracks entering and immediately exiting the
beach or the presence of small beds, were often easy to identify. Nonetheless in some occasions nests initially considered as real were subsequently discarded from the data sets
when no signs of eclosion were visible at the end of incubation period. In other cases, nests originally considered nonnesting emergences were later regarded as true nests since
hatching was detected and included in the analyses. Due to
hurricane Ivan in September of 2004, almost all of the nests
still in the incubation period were lost and the detection of
false nests was impossible onwards. To avoid double counting, tracks were subsequently raked over with the ATV.
The internesting interval was calculated based on the interval (days) between one nesting episode and the next nesting attempt (Alvarado and Murphy, 1999). Any observed
internesting intervals exceeding 25 days were discarded and
corrected with an estimated interval based on the average internesting period reported for these species, since it is more
likely that there was an unobserved nest laid (Alvarado and
Murphy, 1999; Broderick et al., 2003; Hernandez-Guzmán,
2003). In these cases, the average clutch frequency (average number of nests laid by female per year) was calculated
based on the assumption that nesting occurs at the average
interval.
At the end of the incubation period (60 days) every nest
was re-visited, excavated by hand and the fate of every nest
recorded. Four mutually exclusive categories were considered: (1) hatched, (2) predated, (3) flooded or (4) destroyed
541
Nesting of hawksbill and green turtles in El Cuyo
Table 1. Internesting intervals (days), distance between
nests (km) of a same turtle of both species at El Cuyo beach
in the three nesting seasons.
Figure 1. Number of nests (nests) of hawksbill and green
turtles throughout the nesting seasons studied in El Cuyo
beach.
by another turtle. In order to ascertain individual fecundity (F), hatching success (HS) and emergence success (ES)
every egg was included in one of the following categories:
hatchlings alive or dead inside or outside the nest (Ain , Aout ,
Din or Dout ), hatched eggs (H), hatchlings hatching alive
or dead (EA or ED) (Balazs, 1999; Broderick and Godley,
1999). Unhatched eggs were opened and their contents categorized as “with embryonic development” (WED), as “with
no apparent embryonic development” (NED) or as rotten
eggs (RE). It is difficult to determine the number of unhatched eggs containing fertilized embryos (Miller, 1997),
so the number of NED eggs is probably underestimated. Fecundity, hatching success and emergence success were calculated using the following equations (Miller, 1999; SalumFares, 2003):
F = H + WED + NED + RE + EA + ED
HS =
ES =
H + EA + ED
F
H − Ain − Din
F
× 100
× 100
A Kruskall-Wallis test and linear regression analysis
were performed in order to compare the relation between
females’ size and fecundity.
Results
Number of nests, internesting intervals, clutch
frequency and estimates on number of breeding
females
In this beach track morphology was successfully used in classifying the turtles’ species.
Non-nesting emergences were not considered in
the analyses.
Species
Internesting
intervals
(days)
Distance
between
nests
(km)
Hawksbill Mean
N = 27
turtle
(± s.d.)
Min
Max
Mode
17.5 (±2.4)
3.0 (±2.9)
13
22
20
0 (±0.1)
10.2 (±0.1)
1 (±0.1)
Mean
N = 52
(± s.d.)
Min
Max
Mode
11.5 (±1.8)
1.8 (±2)
10
20
10
0 (±0.1)
6.6 (±0.1)
0 (±0.1)
Green
turtle
Hawksbill turtles usually started nesting at
the end of April and beginning of May and most
nests (65%) were laid in May and June. Green
turtles started nesting in June and the majority
of the nests (73%) were laid in July and August. The number of hawksbill’s nests in 2002
was 373 while in 2003 this value decreased to
311. In 2004, 217 nests were registered for this
species. This represents a 40% decrease when
compared with 2002 (fig. 1). A total of 390
green turtle nests were found in 2002, in the following year there were only 157 registered nests
and in 2004 the number of nests increased to
172, which represents a decrease of about 55%
from 2002 (fig. 1).
Hawksbill’s average internesting interval was
of 17.5 ± 2.4 days and for green turtles this interval was of only 11.5 ± 1.8 days. The hawksbills’ clutch frequency (number of clutches laid
by each female within each season) based on actual recaptures of tagged females and corrected
with the average nesting interval (table 1) was
2.16 ± 0.38 (n = 24), 2.88 ± 1.05 (n = 9) and
2.25 ± 0.5 (n = 4) in 2002, 2003 and 2004,
respectively. For the same individual, the number of nests per season ranged from two to a
maximum of five. The clutch frequency of green
turtles, based on actual recaptures and corrected
with the average nesting interval, was 3.12±0.4
(n = 30) nests in 2002, 2.33 ± 0.51 (n = 6)
542
nests in 2003 and 2.75 ± 0.61 (n = 16) nests in
2004. The minimum number of laid nests was
two and maximum six. The estimated number of
hawksbill females in 2002 was approximately
172 ± 25, and in 2003 this number decreased to
108 ± 28 and the following year only 92 ± 8 females nested in El Cuyo. For green turtles the
number of females ranged from 177 ± 25 in
2002 to 67±12 in 2004, while in 2003 this value
was 62 ± 4 females.
Nest spatial variation
Both species showed preference for nesting on
the dune or vegetation zone (73% and 76% respectively) in 2003 and 2004, although in 2002
both nested evenly above the tide line and in
the dune zone. The nest density (nests/ km)
varied between the species and sampled seasons. High nest density was observed on the
tips of both portions of the beach (farther away
from the village). Green turtles nested almost
exclusively on the west beach while hawksbills nested evenly on both sides. Green turtles
showed higher nest-site fidelity between nests
laid in the same season than hawksbill turtles.
Maximum distance between green turtles’ nests
was of 6.6 km while in hawksbill this value
reached 10.2 km (table 1).
Female size
The mean CCL of hawksbill turtle increased
slightly from 2002 (94.1 ± 4.2 cm) to 2004
(95.2 ± 3.9 cm) although Kruskall-Wallis test
showed no significant differences (H (2, N =
81) = 1.337, p = 0.51). The modes in 2002 and
2004 were the same (94 cm) and in the middle
year of 2003 the mode was higher (97 cm). Minimum size of nesting females varied from year
to year but differences between 2002 and 2004
were insignificant (table 2). Kruskall-Wallis test
showed no significant differences in the mean
CCL of green turtles between the different years
(H (2, N = 282) = 2.05, p = 0.35). Minimum size of nesting females increased in 2003
and 2004 compared with 2002. Similarly with
R. Xavier et al.
hawksbills the mode in 2002 coincided with the
one in 2004 (table 2).
Fecundity and relation size/fecundity
The mean fecundity found for hawksbill turtles
in 2002 was 148 ± 26 (n = 171) eggs per nest,
while in 2003 was 153 ± 21 (n = 174) eggs
per nest, and in 2004 mean fecundity per nest
was 146 ± 31 eggs (n = 110). No significant
differences were found, using Kruskall-Wallis
test, between the years (H (2, N = 455) =
5.258; p = 0.07).
The mean fecundity for green turtles was similar in 2002 and 2003 (131 ± 23 (n = 165) and
131 ± 25 (n = 75) eggs respectively), and in
2004 decreased to 127 ± 27 (n = 35) eggs per
nest. There were no differences in fecundity in
the three years, using the Kruskall-Wallis test
(H (2, N = 275) = 0.435; p = 0.79). The linear regression analysis for hawksbills between
fecundity and CCL showed a very weak correlation between variables (R 2 = 0.04, p = 0.027),
with only 4% of the variation being explained
by this model (fig. 2). For green turtles this regression showed a stronger correlation between
variables (R 2 = 0.27, p < 0.0001) (fig. 3).
Incubation success and fate of the nests
For hawksbill turtles the HS in 2002 was 88%
(n = 171) and ES 76% (n = 171). In 2003 HS
was 92% (n = 174) and ES was 87% (n = 174).
In 2004 HS was 87% (n = 110) and ES of 60%
(n = 110). For green turtles in 2002 HS was
92% (n = 165) and ES 87% (n = 165). In 2003
HS was of approximately 89% (n = 75) and ES
87% (n = 75) and in 2004 HS 86% (n = 35)
and ES 80% (n = 35). The majority of the nests
of hawksbill and green turtles hatched (80%
and 97%, respectively) in 2002, and the major
cause for embryo mortality for both species was
predation from foxes and racoons, followed by
destruction by other turtles. In 2003 predation
pressure increased for both species and in 2004
the majority of eggs did not hatch, only 41% of
hawksbill and 31% of green turtles nests were
543
Nesting of hawksbill and green turtles in El Cuyo
Table 2. Size of female hawksbill and green turtles throughout the seasons of 2002-2004
Species
Hawksbill
turtle
Green
turtle
Mean CCL
(± s.d.) (cm)
CCL min (cm)
CCL max (cm)
Mode (cm)
N = 81
Mean CCL
N = 282
(± s.d.) (cm)
CCL min (cm)
CCL max (cm)
Mode (cm)
2002
2003
2004
94.2 (±4.2)
95.1 (±3.9)
95.2 (±3.9)
87
119
94
83
106.5
97
88
101
94
107.9 (±6.1)
106.6 (±7.2)
107.3 (±5.5)
91
122
108 and 109
95
120.5
103
95
120
109
Figure 2. Linear regression of size with fecundity for nesting hawksbill turtles. With N = 127, the expression of the equation
is y = 68.633 + 0.630x, R 2 = 0.0382, F = 4.999; p = 0.027.
left undisturbed. Green turtles’ eggs were lost
due to flooding of the beach and to a minor
extent due to predation by foxes. In the case
of hawksbill the majority of eggs were lost
mainly due to predation by foxes and raccoons,
by flooding of the beach or destroyed by other
turtles.
Discussion
A 25-year report for El Cuyo beach area comprising data from 1977 to 1996 (based on studies from Federal, State and Municipal Government Agencies, academic institutions and NGO
programs), considered the hawksbill nesting
population in the Yucatan Peninsula the largest
in the western Atlantic and one of the largest
worldwide (Garduño-Andrade et al., 1999). The
same study reported that the state of Campeche
registered the highest nest density recorded in
1996, followed by the state of Yucatan where
an average of 659 nests/km were observed in El
Cuyo beach, the second highest density in the
Peninsula (Garduño-Andrade et al., 1999). Recent data from a study where the same methodology was employed, points to a decrease in the
number of nests at El Cuyo beach between 1999
and 2001, where close to 300 hawksbill turtle’s nests were observed (Salum-Fares, 2003).
In the present work, the number of nests re-
544
R. Xavier et al.
Figure 3. Linear regression between size and fecundity for nesting green turtles. With N = 102, the expression of the
equation is y = −86.15 + 2.028x, R 2 = 0.2686, F = 36.72, p < 0, 0001.
corded in 2004 (n = 217) was the lowest since
1995. Estimated number of females nesting also
diminished for both hawksbill and green turtles. At the state of Campeche, a decrease in
hawksbill and green turtles’ nests was also noticed from 2000 to 2003 (Hernandez-Guzman,
2003). Although these findings seem alarming,
there are several aspects of sea turtles’ biology
that need to be taken into account before making any further considerations on these populations’ status; first, only a part of the population (mature females) is being monitored at the
beach, so the observed decrease in number of
nests and females may not represent the trend of
the entire green and hawksbill populations. Secondly, any species with delayed sexual maturity has many year-classes of sub adults (Bjorndal, 1999) hence, further considerations made in
this work concern only the number of nests and
population size of breeding females and not the
entire population. The third factor to be considered is the ability of sea turtles to vary the interval between successive breeding seasons (Broderick et al., 2001; Hamann et al., 2003). This
interval is likely to reflect changes in feeding
ground conditions (food abundance and quality)
which can affect breeding rates in sea turtles and
produce greater variability in nesting numbers
(Hays, 2000; Broderick et al., 2001).
Although both species demonstrate nest-site
fidelity, green turtles have higher precision
when compared with hawksbills. Since 1995
until 2002 both species showed a preference for
nesting just above the high tide line, although in
2003/2004 both species preferred nesting in the
dune area. This change may have been caused
by possible modifications in the width of the
beach, forcing female turtles to go further inland to lay their eggs, since nesting in the dune
diminishes the risk of inundation and washing
of the eggs. Variation in longitudinal nest densities was observed between species and among
the different nesting seasons, particularly for
hawksbills. This species seems to prefer the east
part of the beach to nest and in both beaches
nest density was higher further from the village.
However green turtles seldom nested in the east
section of the beach and within the west section they preferred the kilometres far from the
village. Although preferences were consistent
over different seasons, it is important to continue generating density maps. Otherwise, longitudinal preferences and/or habitat suitability
are likely to change unnoticed from year to year.
Nesting of hawksbill and green turtles in El Cuyo
Even though the mean CCL of hawksbill turtles was not significantly different between the
studied seasons, 2002 and 2004 modes were the
same, which could indicate that many of the
females that nested in 2002 returned in 2004.
According to Garduño-Andrade et al. (1999),
there is a 65% probability for that to happen.
In 1998 an average CCL of 90 cm was reported
(Garduño-Andrade, 1998); data from the last
three years present in this study showed that
nesting hawksbill turtles were larger (94-95 cm)
than the individuals reported in previous years
strongly indicating that recruitment of newly
matured females decreased. Similarly, female
green turtles failed to show significant differences in mean size between years and the mode
in 2004 coincides with the one in 2002 suggesting that this species may also have a biannual nesting behaviour (Zurita et al., 2002, unpublished data; Bagley et al., 1997, unpublished
data).
When comparing hawksbill’s fecundity with
previous studies for El Cuyo, a difference of no
more than 20 eggs per nest per female is noticeable (Rodriguez and Zambrano, 1991; GarduñoAndrade, 2000). Green turtles’ fecundity coincided with previous observations for the area
(Rodriguez and Zambrano, 1991). The relation
between hawksbills’ size and fecundity reported
in this study coincides with that observed by
Garduño-Andrade (2000) in the neighbouring
beach of Coloradas. For green turtles this relation is stronger than for hawksbill turtles but this
value could not be compared with other studies.
The hatching success could be considered
high for both species. Emergence success was
generally high with the exception of the 2004
season, indicating that this beach is a suitable
hatchery as previously stated by Miller (1999).
In 2004, hurricane Ivan, affected the beach with
high tides and caused complete nest inundation
in mid September. Adding to this, the number
of predated nests increased.
Coupled together, the above mentioned factors, i.e. decreasing numbers of nesting females
in the lasts seasons, low hatchling emergence in
545
2004 and high predation on eggs will probably
have a negative impact on the hawksbill population. According to Georges et al. (1993), an
even greater predation on hatchlings is likely
to occur at sea. Similar declines were observed
in many other Yucatan beaches as presented in
the regional meeting on conservation programs
(WWF, 2004, unpublished data).
A decreasing trend in green turtles nesting events was only observed in El Cuyo and
Isla Aguada, Campeche (Hernandéz-Guzmán,
2003) so it is not appropriate to suggest a
decline for this population. Possibly this decrease in the number of nests only reflects an
adaptation to environmental changes in foraging
grounds or to other stochastic factors and not a
decrease in green turtle’s population size.
Reductions in the number of nest and females
in these latter seasons may be related to a number of aspects, or a synergy between them:
(1) A destructive event at the end of the
1980’s, e.g. flooding caused by hurricane
Gilberto in 1988, could have led to low
hatchling rates, and subsequently, low recruitment levels of newly matured females 15-25 years later, since the success of a rookerie depends on environmental parameters such as beach stability
(Georges et al., 1993). This hypothesis is
based on the period of time needed for
sea turtles to reach maturation (GarduñoAndrade, 1998) and on the natal homing
model, and is supported by the observed
increase in female size, indicative of low
recruitment rates.
(2) Green turtles, being exclusively herbivorous, could have been seriously affected
by Hurricane Isidoro in 2002 which may
have altered the bottom of the sea changing sea grass areas and destroying some
coral reefs, thus preventing turtles from
spending energies in reproduction. Because these effects are greater at lower
trophic levels (Limpus and Chaloupka,
1997; Brainard et al., 2002), a variation
in the number of clutches laid in a sea-
546
son and a change the interval between
laying seasons is more likely to be observed in green turtles (Broderick et al.,
2001). This is supported by the present
study, since in 2002 clutch frequency corresponded to approximately 3 nests per
female, while in 2003, it decreased to 2
nests per female.
During the study period, the hawksbills’
clutch frequency did not vary much and
the values obtained were higher than the
minimum number of 2.1 nests per female previously considered for this population (Garduño-Andrade et al., 1999).
However, the fact that the internesting
interval for green and hawksbill turtles
(17.5 and 11.5 days, respectively) was
higher than previously recorded by other
authors (Garduño-Andrade et al., 1999;
Hernandez-Guzmán, 2003) indicates that
females are laying fewer nests per season.
(3) Several studies report that seismological experiments caused an increase in
the swimming time and erratic swimming in turtles (McCauley et al., 2000).
Such experiments conducted for the petroleum industry (late 2003 and the beginning of 2004) near mating areas may
have caused turtles’ disorientation and
decreased mating events. According to
Hernandéz-Guzmán (2003) these experiments caused the death of several juvenile and adult turtles on Campeche
beach.
Acknowledgements. All the volunteers, R. Teja, E. Galicia,
P. Ribeiro, Banamex, Hewlett Packard, Fundación Azteca,
CALICA, U.S. Fish and Wildlife Service, National Fish and
Wildlife Foundation, PEMEX and PRODEP III.
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