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Amphibia-Reptilia 28 (2007): 337-346

Spatial characterization of a foraging area for immature hawksbill


turtles (Eretmochelys imbricata) in Yucatan, Mexico

Eduardo Cuevas1 , María de los Ángeles Liceaga-Correa1 , Mauricio Garduño-Andrade†2

Abstract. The submarine habitats in the Rio Lagartos Sea Turtle Sanctuary, Mexico, are an important feeding and
development area for juvenile Hawksbill turtles (Eretmochelys imbricata). The characterization of these critical habitats is an
important and urgent issue to attend for the conservation of this species in Mexico. The objective of this study is to identify,
locate and describe the marine benthic habitats in this area, and explain the distribution of the juvenile Hawksbill turtles in
the study area. We used submarine techniques such as videotransects and spot checks to characterize the bottom types in the
area, and geostatistic techniques to elaborate thematic maps of the different benthic components, integrating all of them into a
GIS. We obtained the bottom type map with eight submarine habitats at different depth ranges. We found juvenile Hawksbill
turtles distributed mainly on hard bottom sites covered by octocorals, such as Pseudopterogorgia, and sponges of the genera
Chondrilla and Spheciospongia. We estimated habitat ranges for the captured turtles and the bottom types occupied by them,
then we calculated the distribution densities of juvenile Hawksbill turtles by bottom type. We concluded that the combination
of spatial techniques and multivariate statistics is efficient for mapping the marine bottom types in the area, and recommend
the generation of specific conservation strategies to protect this area because of the natural marine resources and process
ocurring in it.

Introduction pattern can be easier seen considering that we


are only assessing less than the 0.05% of the
The Hawksbill turtles (Eretmochelys imbricata,
sea turtle’s life cycle, making it more important
Linnaeus 1766) is a pantropical critically endan-
and urgent to assess critical habitats such as the
gered species in the world occupying different
feeding and developing grounds for the Hawks-
marine habitats including beaches, coral reefs,
seagrasses and oceanic areas; making it an im- bill turtles.
portant species to investigate as well as the criti- The Yucatan Peninsula harbors the biggest
cal habitats used by it (Meylan et al., 1997; Bail- nesting population of Hawksbill turtles (E. im-
lie et al., 2004). bricata) in the Caribbean, and the fourth one
For more than ten years, the conservation ef- in the world; being one of the first in the
forts on sea turtles in Mexico had been merely Caribbean to register a significant increase of
oriented towards the nesting beaches, mainly the Hawksbill nests by 1999 (Garduño-Andrade
because of an easier access to the beaches than et al., 1999; Meylan, 1999; Meylan and Don-
to marine areas where you need specialized nelly, 1999).
equipment and staff at a higher amount of finan- Yet even though the importance and urgence
cial funds. to locate and characterize the feeding and devel-
The last fact has provoked a limited approach opment areas for the Hawksbill (E. Imbricata)
to the sea turtles’ life cycle producing severe turtles, there are only a few ecological stud-
lacks of information about these species in the ies attending feeding areas for hawksbill tur-
region (Abreu-Grobois et al., 2005). The last tles, except for the one conducted by Garduño
et al. (2000), who assessed the population dy-
1 - Centro de Investigación y de Estudios Avanzados, IPN, namics of immature Hawksbill populations in
Unidad Mérida, México. Km 6 Antig Carr a Prog., the Rio Lagartos area, and Guzmán et al. (com.
Cordemex, C.P. 97310. A. P. 73 “Cordemex” pers., 2003) who captured and tagged immature
e-mail: ecuevas@pronatura-ppy.org.mx
2 - Programa de Protección de Tortugas Marinas. Departa- Hawksbill turtles in the nearshore marine areas
mento de Vida Silvestre, SEMARNAT, México in the Campeche Bank.

© Koninklijke Brill NV, Leiden, 2007. Also available online - www.brill.nl/amre


338 E. Cuevas, M. de los Á. Liceaga-Correa, M. Garduño-Andrade

Table 1. Pearson correlation analysis results using the different biotic and abiotic variables. The correlation
values (r) in black are significative p < 0.05, N = 45.

Sand Calcareous Floor Rubish Seagrass Gorgonians Sponges

Sand 1
Calcareous Floor −0.52 1
Single rocks −0.20 −0.14 1
Seagrass 0.42 −0.48 −0.23 1
Gorgonians −0.49 0.14 −0.06 −0.42 1
Sponges −0.18 −0.04 0.14 −0.24 −0.08 1

Ecological characterization for the Hawks- Spatial and ecological characterization


bill’s critical areas may be expressed using spa- The marine habitats were ecologically characterized using
tially explicit products (maps), making it eas- two standardized methods: submarine videotransects (Aron-
ier for decision makers to design and imple- son and Swanson, 1997), and spot checks (Kenchington,
1978), both appropriate techniques for surveying wide ma-
ment conservation and management strategies rine areas.
in the area. Techniques such as geostatistics and The survey sites were systematically selected along per-
GIS are being used to generate management pendicular transects to the line coast, taking into account the
variation in the distribution of the marine organisms accord-
tools with punctual data inputs coming from ing to the depth. In May and August 1999, we surveyed 45
field work, then processed using algebraic and sites obtaining submarine videos and coverages employing
logic operations. The map overlayings, based on an adapted and standardized cover percentages scale (Bello-
Pineda, 1998).
specific criteria established by the reserve man- We generated a basic matrix data considering 6 variables
agers, land users and scientists together, are an (sponges, seagrasses, gorgonians, calcareous floor, sand,
single rocks) for the 45 survey sites. Next we performed a
important step in the creation of this powerful
correlation analysis using the Pearson-moment test to assess
spatial tool, aiding in the zoning and manage- the level of correlations among the variables here considered
ment processes for the natural protected areas. (Zar, 1985).
The resulting matrix was later used to perform spatial
The objective of this study was to character-
analyses (by the kriging method) to generate maps for the
ize the marine benthic habitats in the Rio La- six different variables. The maps were generated using the
gartos Sea Turtles Sanctuary, Yucatan, Mexico, Geostatistcal for Environmental Science™ program apply-
ing different statistical models depending on the correlation
a critical area for immature and adult Hawksbill
parameter and the cross-validation value used for each case.
turtles. Subsequently, we divided the newly generated maps in
two groups: biotic and abiotic ones, having the pixels in
their respective maps containing the cover value for each
variable. For the next step, we proceed to conjunct the
Materials and methods three different maps in each group overlaying them and
employing basic arithmetic operations (scaling and adding)
Study area in the GIS:
The Rio Lagartos Sea Turtle Sanctuary (RLSTS) (21.58◦ N Vi = V1i + (V2i ∗ 10) + (V3i ∗ 100) (1)
87.9◦ W) in Yucatan, Mexico, harbors submarine habitats
such as seagrass beds and wide areas covered by octoco- where V1i is the cover value of the variable 1 in the pixel
rals. This marine landscape is an important forage and de- i. Specifically, at each pixel i the cover value Vi indicates
the cover percentage range for each variable integrating the
velopment area for the population of immature hawksbill
map.
turtles (E. imbricata) in the Yucatan Peninsula. Considering
After this, we applied a refining procedure to better de-
there is genetic evidence showing a relative closed Hawks-
fine the representative classes in the maps using multivari-
bill population in Mexico (Abreu et al., 2003) and that the ate cluster analysis (WPGMA, Gower similarity index), fed
adjacent beaches to this development area were one of the with the new values at each pixel in the two new maps,
first in the Caribbean to register a significant increase of to identify the similar classes (clumps) at a 80% similitude
the Hawksbill nests (Meylan et al., 1997; Garduño et al., value, becoming the final classes for the new biotic and abi-
1999); this area is specially important to characterize be- otic maps (fig. 1).
cause of its ecological roll for the Hawksbill populations in After this, we used a second map overlaying procedure
the region (Frazier and Rodríguez, 1991; Maldonado and using the biotic and abiotic maps to obtain the final bot-
Garduño, 1999; Abreu et al., 2005). tom types map (Chuvieco, 1990). The bottom type map’s
Foraging areas in hawksbill turtles 339

Figure 1. Stepwise scheme showing the bottom type map elaboration using geostatistics, multivariate statistics and GIS.
340 E. Cuevas, M. de los Á. Liceaga-Correa, M. Garduño-Andrade

accuracy was checked establishing 30 random survey sites the seagrass’ cover also decreased as the cal-
and visiting them using the checkpoint technique for thruth- careous floor cover increased (r = −0.48).
validation, and finally making an error matrix to obtain the
global accuracy index kappa. From the geostatiscal analyses we obtained
the semivariogram for each variable, showing
Juvenile hawksbill turtle ecology that in all cases the here studied variables were
We captured 10 juvenile Hawksbill turtles inside our study
spatially structured,with the spherical model ex-
area, making it possible to employ them in our analyses by plaining the most of the spatial variations.
integrating them as a layer in the GIS and determine habitat In the process to build the bottom types map,
preference for them.
we overlaid the three maps of the biotic and abi-
For habitat preference we also took into account a pre-
vious experimental work made in this same study area otic groups, respectively, and using the equa-
by Cuevas and Maldonado (1999), who tracked a juvenile tion (1) we obtained one map for each of the
Hawksbill turtle for a 24 h period, obtaining periodic move- two groups, with six new classes in the abiotic
ments for it, allowing for calculation of its home range
by using the Animal Movement extension for ArcViewTM map and eight for the biotic one. After overlay-
(Hooge et al., 1999), by the Minimum Convex Polygon ing and properly mixing these two new maps
(MCP) and Kernel methods, both methods have been re- (multivariate techniques), we used a variation of
cently incorporated in the sea turtle research (Worton, 1989;
Seminoff et al., 2002). The MCP has the bias that is highly equation (1) for only two maps:
sensitive to outliers in the analyzed data and does not have
the capability of identifying spatial patterns inside the de-
Vi = V1i + (V2i ∗ 10) (2)
fined home range. In the other hand, the Kernel is a non-
parametric method capable of identifiying areas with differ-
to obtain the final map whose new classes were
ent use intensity within the defined home range, attributing filtered having the criteria of similarity percent-
to them probabilistic values for the animal usage, features age (78%) and the minimum covered area by
that makes it one of the most recomended technique for
the classes (1%), we produced the new and fi-
home range estimations (Worton, 1989; Seamen and Pow-
ell, 1996; Seminoff et al., 2002). The later method have been nal bottom types map containing eight different
highly recomended because of its versatility in the analysis classes (fig. 2).
as well as the amount and quality of information obtained In order to assess the accuracy of this bot-
using it; however, despite its biological and statistical limita-
tions, the MCP is still recomended because it is more widely tom types map, we visited 30 truthing field loca-
used for home range estimations thus enabling comparisons tions, finding that 25 of them (83.33%) agreed
with other similar studies, but it is always recommended to with the map, giving a value of 76% as an accu-
employ in the analisis an extra technique besides the MCP
one (Seminoff et al., 2002). racy value for this map (kappa index).
We made a buffer layer for the 10 captured turtles using
an average home range diameter based on the previous Ecological characterization
home range analysis. Thanks to the last step we were able to
learn their habitat preference inside their foraging area, and The octocoral colonies are the most abundant
to use a contingency table analysis to statistically assessed
and common biological group in the study area,
their habitat preferences.
hence the bottom types where they were the
dominant group were divided according to their
covered area (fig. 2). The bottom type with
Results
the highest amount of area was the octocorals
When comparing the six studied biotic and abi- covering between 20% and 40% with 19.14% of
otic variables, we found five correlations that the total study area; followed by the octocorals
were statistically significant (at least P < 0.05, mixture on hard bottoms with 18.00%.
n = 45) (table 1). Observing these relation- We identified eight different bottom types de-
ships, among the three highest correlation val- scribed as follows. The bare substratum, cover-
ues we found that the sand cover decreases ing the 9.86% of the total area, is a submarine
when the calcareous floor increases (Pearson- habitat where there are not any relevant topo-
moment r = −0.52); the gorgonian cover also graphic features and is merely formed by bare
decreases when the sand cover increased; and sandy or hard bottom areas, in some cases with
Foraging areas in hawksbill turtles 341

Figure 2. Bottom types map and immature hawksbill turtles capture sites in 1998 and 1999 and their habitat range (Capture
sites taken from Garduño et al., 2000).

a small amount of unattached algae (Phaeophyta gorgia, which is a common symbiotic group
and Chlorophyta). This bottom type is com- in shallow areas with medium strength cur-
monly found at areas up to 5 m depth. rents. Among these octocoral colonies we found
The habitat of sponges dominating hard bot- high amounts of macroalgae (Phaeophyta and
toms are places where these organisms cover Rhodophyta, mainly); and often we found me-
more than 20% of the sites, harboring ge- dium size rocks (50 cm-300 cm diameter), as
nera such as Spheciospongia and Chondrilla. In well as some characteristic elevations of the cal-
many cases, these sponges are accompanied by careous floor forming little caves of 30 cm-60
small hard corals and macroalgae of the Phaeo- cm height running parallel to the shoreline. This
phyta and Rhodophyta divisions. This bottom complexity harbored a variety of reef fishes,
type covers 9.32% of the total area and is com- spiny lobsters as well as some juvenile Hawks-
monly located in areas up to 5 m depth. bills. These bottom types were characteristic in
The bottom types dominated by octocorals areas between 6-12 m depth in the study area.
were divided in five different categories: octoco- The last bottom type is the seagrass beds,
rals covering up to 20.00% of the sites, covering where more than half the cover consisted of sea-
between 20% and 40%, 40%-65%, 65%-100% grasses Thalassia testudinum and Syringodium
and octocorals mixture on hard bottoms where filiforme (mainly), mostly on a sandy bot-
there are variable cover values. All these covers tom mixed with macroalgae belonging to the
are on a hard substratum with a soft slope har- Chlorophyta and Phaeophyta Divisions. This
boring octocoral colonies up to 70 cm height. bottom type covers the 9.00% of the total area
The dominant genus was the Pseudoptero- and was found in places up to 6 m depth.
342 E. Cuevas, M. de los Á. Liceaga-Correa, M. Garduño-Andrade

Figure 3. Night and day movements during 24 hs tracking an immature. Hawksbill turtle in Las Coloradas (taken from Cuevas
and Maldonado, 1999).

Juvenile hawksbill turtle’s ecology detailed home range for the tracked juvenile
turtle during day and night (fig. 4). It is pretty
We caught ten juvenile hawksbill turtles in the evident the bigger area (0.124 km2 ) used by the
study area. One individual was found on a bot- turtle during the day than the area used at the
tom with sponges on a calcareous floor, another night (0.021 km2 ), shedding some light about
one in octocoral habitat <20%, five on octoco- its habits in a common foraging area.
rals 20% and 40% cover, two on octocorals 40% We assessed the habitat preference of the
and 65% cover and the last one on octocorals juvenile Hawksbill sea turtles and we did not
mixture (fig. 2). find statistical significant preference (X 2 =
Analyzing the movements of the juvenile 1.53; n = 10, P = 0.68). However, we did find
Hawksbill turtle tracked by Cuevas and Mal- differences in habitat preference between day
donado (1999), we obtained a map with the dif- and night, with the tracked juvenile Hawksbill
ferent trends and movement of the turtle in re- turtle during the day mainly occupying habitats
lation to the bottom types map (fig. 3). In this with octocoral cover between 20% and 40% of
figure we are able to observe the different habi- the site, and during the night having a trend to
tats visited by the turtle during 24 hrs of track- occupy bare substratum areas (fig. 3).
ing. Employing the Minimum Convex polygon
for home-range assessment (Hooge et al., 1999)
we obtained an average home range of 1.2 km in Discussion
diameter, which was expressed on the sea turtle
capture sites map (fig. 2). The geostatistic analyses have not been com-
We also obtained a probabilistic home-range monly used for sea bottom characterization be-
area employing the Kernel method proposed by cause of the disadvantages they have in com-
Worton (1989), by which we generated a more parison with the remote sensing ones (Dustan et
Foraging areas in hawksbill turtles 343

Figure 4. Home range estimations using the Minimum Convex Polygon and the Kernel method for the day and night
movements of one juvenile Hawksbill turtle in front of the port Las Coloradas, Yucatan (Adapted from Cuevas and
Maldonado, 1999).

al., 2001). However, given the conditions of this grass beds, and at the east we find the octo-
study area (mainly water transparency) and the coral communities dominating the colonization
type of available data, we implemented an un- of the hard calcareous substrata. They seem to
common and innovative combination of meth- distribute according to the dominant superficial
ods to generate bottom type maps including currents and the sediment types in the zone;
a mixture of statistical techniques, similitude this hypothesis has been built merely empiricaly
analyses, geostatistics and GIS. since we observed, at field and satellite images,
The obtained statistically significant corre- a higher energy regime in the sea at the eastern
lations between variables, such as the positive zone than in the western one, condition which
ones for the seagrass and sand, octocorals and could be favoring the dominance of the octoco-
the calcareous substratum are completely ex- rals in the east zone because of the feeding strat-
pected due to the biological needs for these ma- egy of these organisms (filtering) (Chang-Feng
rine organisms, soft and hard substratum respec- and Ming-Chao, 1993; Gili and Coma, 1998).
tively, and have already been reported by sev- The different bottom types presented specific
eral authors for the Caribbean (Jordán, 1989; depth ranges, this pattern has already been re-
Sponaugle, 1991; Márquez, Lozada and Ro- ported by Jordan (1989) for the Yucatan Penin-
dríguez, 1997; van Tussenbroek et al., 2000). sula, Goldberg (1973) for the Florida Penin-
The significant correlations suggest the ex- sula, Lasker and Coffroth (1983) for Belize and
istence of two different ecotones in the study Márquez, Lozada and Rodríguez (1997) for the
area: at the west of the study area we find sea- Caribbean sea at Venezuela.
344 E. Cuevas, M. de los Á. Liceaga-Correa, M. Garduño-Andrade

The study area covers all the characteristic conservation of this large hawksbill foraging
features for a sea turtle foraging area accord- area.
ing to Meylan and Meylan (1998), we can find The habitat range here used with 600 m of
juvenile Hawksbill turtles in shallow habitats radius estimated for the juvenile Hawksbill tur-
where the individuals recruit at 20-30 cm cara- tles slightly differ from the one recorded by van
pace length and leave when they reach about Dam and Diez (1998) of a habitat range ra-
50 cm carapace length, and the most of them is dius of 450 m for Puerto Rico; Leon and Diez
expected come from the same haplotype (MX1) (1999) reported a 360 m radius habitat range in
(Abreu-Grobois et al., 2003). Dominican Republic; making a proper use of
The specific depth range where the juvenile the calculus made by Cuevas and Maldonado
Hawksbill turtles were captured varied from (1999), which seem consistent with these other
four to seven meters with hard substratum, just ecological studies.
as Garduño, Maldonado and Lope (2000) re- In this study area we found hawksbill turtles
ported for the region. The bottom type where the foraging items, such as the sponge genera Chon-
most of the turtle captures were made (five) was drilla, the algae genera Dictyota, Dictyopteris,
the one with octocorals covering 20%-40%, us- Hypnea, Jania, Laurencia, Ceramium, Codium
ing a capture effort of 13 checked hectares. Con- and Gracilaria. Several of these marine organ-
sidering the exisitng cover of this bottom type in isms have been reported as some preferred feed-
the area (5,600 ha) we assume an estimated ju- ing items for E. imbricata, such as León and
venile Hawksbill density, for this bottom type, Diez (1999).
of 0.38 individuals/ha (38 juvenile Hawksbill In summary, the combination of geostatistic
turtles/km2 ). The next Hawksbill turtle’s pre- and multivariate techniques resulted to be effi-
ferred bottom type was the one with octoco- cient for mapping marine benthic habitats, ob-
rals covering 40%-65% where we had a 10 ha taining good accuracy. The difference between
capture effort. In a similar way, considering its this study and others is that this one made a spa-
covering area (5,200 ha) we estimated a den- tial description of the bottom types in the study
sity of 0.30 individuals/ha (30 juvenile Hawks- area explicitly expressed in a map, in contrast
bill turtles/km2 ). to previous studies in the zone which just de-
These last densities are not far from the scribed the bottom area.
densities reported in other studies for juvenile We contribute with basic maps for the scien-
Hawksbill turtles in similar bottom types. Gar- tific community, the users of this area as well
duño et al. (2000) reported a general estima- as for the decision makers, helping to make an
tion for the juvenile Hawksbill population in easier management and zonification of the area,
this area of 4,289 individuals with a density of since there is enough evidence to support that
25.90 juvenile Hawksbill turtles/km2 . León and this is an important foraging and developmental
Diez (1999) reported a juvenile Hawksbill tur- area for Hawksbill turtles.
tles’ density of 35.10 individuals/km2 in the Na- These results are a strong argument to con-
tional Park of Jaragua in Dominican Republic. sider the protection of this marine area because
Such calculations are extrapolations based of the resources and processes in it, in addition
on the captures made and the GIS integrated to the Ria Lagartos wetland (Biosphere Reserve
here and meant as a tool to direct subsequent Ria Lagartos) which it interacts with.
capture efforts for juvenile Hawksbill turtles
in the study area, leading to higher success in
Acknowledgements. We thank CONABIO for the funding
the capture rate than in previous studies. In the
given for the project L269. We are also indebted to H.
same way we contribute with spatially explicit Cárdenas, N. Cárdenas, M. Zapata for their help in the sea,
inputs for future habitat management and proper to the fishermen Willy and Jonás for their valuable help,
Foraging areas in hawksbill turtles 345

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