1. Introduction
The
queen conch (Lobatus
gigas) is a large gastropod which used to represent an important
food and economic resource in the Caribbean [1].
The life cycle of the conch is complex, presenting an extensive pelagic larval
stage, an in faunal stage and an epibenthic stage, which complicates the assessment of stocks by traditional methods used in
fishery biology [2,3].
Furthermore, each stage of its life cycle is subject to a variety of factors which influence the abundance and distribution of this
species (CFMC 1999) [4].
The queen conch performs several migrations throughout its life
and at least two have been documented in the literature. The first
systematic observations on conch mobility were made by Hesse (1979) [5]
who documented that habitat use increased with body size. Furthermore, this
author documented seasonal adult movements, which have also been documented by
other authors and are thought to be associated with reproductive behavior [6-9]. The second type of migration reported in the
literature consists of the mass movement of small
juveniles, which is hypothesized to represent the dispersal of newly emerged
classes (>1 year) classes from the centres of larval recruitment [10]. Ddescription of migrations of even smaller
juveniles with shell lengths between 50-100 mm, believed to represent shifts
from post-settlement habitats to nurseries have
been studied [11,12]. Juveniles
are predominantly found in certain areas characterized by soft sediments [5], Appeldoorn & Ballantine 1983) [13], while larger juveniles and adults are
much more mobile and are found across a large variety of habitats [14]. Nevertheless, the characteristics
of the benthic environment such as sea grass density, depth and sediment type
are not good predictors for suitable habitats for this species [15]. Sampling of L. gigas populations
is often biased either towards or against juveniles [14].
Most studies solely address ecologic aspects of juveniles [10,16,17] or adults [18,19]
and rarely asses’ complete life cycles or the connectivity between both stages.
This is probably due to the spatial segregation of life stages, which is rarely
considered in experimental designs.
The
body size of an organism is a key aspect of its ecology, determining its
ability to exploit resources and its susceptibility to predation [20]. Many species undergo extensive ontogenetic
shifts in food or habitat use as they increase in size, known as ontogenic
niche shifts, a phenomena especially well documented in aquatic communities [20].
Nurseries
are habitats where juvenile fish or invertebrate species occur at higher
densities, suffer lower rates of predation or have higher rates of growth in
comparison with other habitats where juveniles are found [21]. However, these criteria cannot predict whether
these juvenile habitats successfully transfer juvenile biomass to adult
populations [21]. Hence, it is vital that
studies assess take into account movements from juvenile to adult habitats, a
link which is currently missing in our understanding of nurseries. L. gigas nursery locations provide
for high juvenile growth, as a resulting of high macro algal production and low
mortality. The nurseries persist where competent
larvae are concentrated by tidal circulation and where settlement occurs selectively
[15]; hence they depend directly on adult
distribution and are determined by the intersection of habitat features and
ecological processes which combine to yield high rates of recruitment and
survivorship [15].
The
Xel-Ha inlet is an enclosed coastal lagoon, which has been used since 1995 as a
park for ecotourism. It has a persistent population of queen conch, composed of
juveniles, sub adults, reproductive and old adults [22],
as well as pelagic larvae [23,24]. Furthermore,
the occurrence of mating and spawning activity in the lagoon [25], suggests that the conch completes its whole
lifecycle within the limits of the inlet. In terms of growth and survival,
Xel-Ha presents several features of a nursery [26].
The
aims of this study were to describe habitat shifts of L. gigas related
to size and determine the seasonality of these shifts. This work demonstrates
the effects of body size on habitat use and may be of great interest for
management, since it documents that different life stages have different
habitat requirements. Furthermore, this work demonstrates that behavior may be
used as a non-invasive assessment tool to determine sexual maturation, an
aspect of fundamental importance for fishery management.
2. Materials
and Methods
The Xel-Ha
inlet is a coastal lagoon located on the east coast of the
Yucatan Peninsula (20°19'15''-20°18'50''N
and
87°21'41''-87°21'15''W)
which consists of a mix of fresh ground water,
supplied by underground rivers, and seawater.
The inlet is connected to the Caribbean Sea by a100 m
wide and 170 m long channel and has a total surface of 14 ha with a central
area and three appendices: Mouth/channel,
north-arm
and south-arm.
Its
depth ranges from 0.5-4.5 m.
Tidal variations may range from 36 cm at the mouth and up to 53 cm at the
south-arm. Four sites were surveyed within the inlet: Cueva, Centro, Bocana and
Brazo Norte.
Cueva (6,000 m²) is located in the south-arm of the inlet
and
includes a small bay surrounded by mangroves (Rhizophora mangle)
and several underground caves with up welling of cold
freshwater, forming a
stable thermo-and
halocline
at about 1.25 m depth, with salinities ranging from 35 at the bottom to 10 at
the surface. The site has a depth of 1-3
m. The bottom is composed of fine muddy sediment, sand, fragments of calcareous
algae, small rocks,
and dense isolated patches
of macro algae (e.g. Padina sp, Calimesa sp, Penicillus sp, Amphiroa sp, Acanthophora sp, Caulerpa sp, Dictyota sp) Decaying
mangrove leaves and inverted jelly fish (Cassiopea sp.) may
also be found. Centro is located in
the center area of the inlet and was the most extensive sampling site with a
total area of 23,000 m2. The site
consists of an extensive coarse sand plain, parts of which are covered with sea
grass (Halodule sp). Close
to the shore, the bottom is rocky with macro algae growing on it. As in the
case of Cueva, the water column is highly stratified. The sampling site Bocana includes part of the channel that
connects the inlet with the Caribbean Sea and the adjacent zone in the interior
of the inlet. The bottom is composed of coarse sand, coral fragments and small
rocks. Isolated patches of sea grass (Thalassia sp) and
coral may be found. Brazo Norte is located in the north-arm of the inlet. The
sampled surface area was 6,000 m². The bottom is
composed of fine muddy sediment, large rocks which form several channels, and
has very dense macro algae coverage (see Cueva), as well as many inverted
jellyfish (Cassiopea sp). The water
column is less stratified than in Cueva, but also presents a halo and
thermocline at a depth of about 1.25 m with salinities ranging from 15 at the
surface to 30 at the bottom.
Between January
2005 and September 2011, a total of 26 surveys
were conducted at Cueva, Centro and Bocana, sampling a total
area of 39,000 m².
In 2009, Brazo Norte was included in the sampling efforts, expanding the
surveyed area to 45,000 m².
In
2005 surveys were carried out monthly, and from 2006 to 2011 samples were collected
taken every two months. At each of the four sampling sites all possible
as many organisms as possible were collected by free-diving by
three divers during three hours. We used the capture-mark-recapture
method,
tagging all individuals with a consecutively numbered plastic Dymo® tag, which allowed the
identification of each individual. The tag was fixed to the
spire of the conch with a plastic zip tie. Shell
length and lip thickness were
determined for each individual, using a precision
caliper accurate to ±1 mm.
All animals were released in the location where they were found.
For
each site, the number of juveniles, sub adults and adults was determined. Since
shell length is not a good indicator of age [27,28],
lip thickness was used to establish size classes. A juvenile was defined as a
conch with not lip, while conches with a formed lip, but thinner than 5 mm were
classified as sub adults, and an adult was defined as a conch with a lip
thickness≥5 mm, based on histological evidence
proposed by Appeldoorn (1988) and Aldana-Aranda & Frenkiel (2007) [27,28].
In
order to detect dispersal and movement, tag recovery was analyzed, counting and
classifying all conch that were recaptured at a site different from the one
they were initially tagged at, using the same classification criteria as
explained before.
In
order to determine if whether were any significant differences between the
source population and the population of emigrant conch, a Chi-square test with
a 95% confidence level was carried out using R [29].
Analysis
of variance (ANOVA) with a confidence level of 95% was used to determine if
whether there were significant differences in the shell length and lip
thickness, and the redistribution of conch throughout the inlet. Finally, the
direction and seasonality of movements was evaluated, counting the total number
of conch that moved in the dry-+rainy- and winter season. Frequency and
goodness of fit test were used to determine frequency of these movements from
the original site to a destination site showed significant differences between
seasons.
3.
Results
Figure 1 shows
the population structure (number of juveniles, sub adults and adults) at each
of the four source sites (site where the conchs were originally tagged), the
number of juveniles, sub adults and adults which leave each source site, and
the redistribution of conch in the inlet according to their life stage
(juvenile, sub adult and adult).
At
Cueva a total of 2,558 individuals
were tagged throughout the duration of this study (Figure.
1), 85% were juveniles (2184), 6% (149 individuals) were sub adults and
9% (225 individuals) were adult conchs. The emigration of 366 individuals from Cueva was detected. More than half (212 individuals) of the
emigrants were adults. The emigrant conch population composition was
significantly different from the source population (χ²calc=725.0544>χ² [0.95;2] =5.991;
P< 0.001), which suggests that dispersal was not random. Juveniles and sub adults
were mainly reencountered in Centro,
while the most of the adults (112 individuals) were found at Bocana, the site where the inlet connects to
the ocean.
At
Centro a total of 2,846 animals were tagged, of
which 73% (2,089 individuals) were juveniles, 15% (430 individuals) were sub adults
and 12% (327 individuals) adult conchs (Figure 1).
Emigration of 1,064 conchs was registered. Despite the fact that the source
population consisted mainly of juveniles, 72% (762 individuals) of the emigrant
conchs were adults, and significant differences between the source- and
emigrant population were found (χ²calc=1393.756>χ² [0.95;2] =5.991;
P< 0.001), suggesting non-random dispersal. The majority of the movements
(87%) were directed towards Bocana, where 979 individuals from Centro were recaptured.
At
Bocana a total of 1,292 conchs were tagged, of which 666 were adults (Figure 1).
Nevertheless,
only 30 (2.3%) conchs were found to move towards the interior of the inlet and
83% of them were recaptured at the adjacent sampling site Centro.
At
Brazo Norte 1,598 conchs were tagged (Figure 1). As
in the case of Cueva and Centro, the source population was mainly composed of
juveniles (81%). A total of 245 conchs were recaptured at other sites within
the inlet. The majority (63%) of the emigrant conch were adults. The
composition of the emigrant conch was significantly different from the
composition of the population at the source site (χ²calc=586.9287>χ² [0.95;2] =5.991; P< 0.001),
suggesting non-random dispersal. Most of the juveniles (33 out of 41
individuals) and sub adults (42 out of 44 individuals) were recaptured at Centro,
while 92 (60%) of the adults were found at Bocana.
Figure 2 shows the average
shell length and lip thickness of emigrant conch and the respective destination
of migrations in the inlet. In the case of conch emigrating from Cueva, Brazo
Norte and Centro, the average size ranged from 205 to 215 mm. There were no
significant differences between shell length and final destination of the
conch. In the case of conchs emigrating from Bocana, shell length was much more
variable. Nevertheless, we detected significant differences (P> 0.001) in
lip thickness, depending on the destination of migrations; conch reencountered
at Bocana generally had thicker lips.
The animals’
movements also showed seasonality (Figure 3)
with conch emigrating from Cueva, Centro and Brazo Norte. Significant
differences were observed between seasons (P< 0.001), and the animals
presented higher mobility during the rainy season, with lower mobility during
winter (corresponding to November-February). In the case of animals emigrating
from Bocana, no significant
differences between the frequencies of movements were detected among seasons (P = 0.219).
4. Discussion
The conch population at Xel-Ha was mainly composed of juveniles.
Furthermore, we detected a biased distribution of juveniles and adults
throughout the inlet, observing mainly adults at Bocana and juveniles or sub adults
in the rest of the inlet. These results were consistent with previous
observations made by Aldana-Aranda, et al. (2005) [30],
who reported 79.2% juveniles and
sub adults at this study site in the period from 2001-2003. Moreover, the
authors reported 76% juveniles in Cueva and 82% adults in Bocana during
2001-2003. The impact of fishing causes a decrease in the population
adult [31,32]. On the other
hand, [5] described populations with a
juvenile-adult ratio of 3:1, which could be explained by increased mobility of adults. Fishing is prohibited in Xel-Ha,
suggesting that the population composition found in this study is natural and
can be described to other factors, such as habitat shift, as this study
suggests.
Mobility and redistribution of conch in the inlet appeared to be related
to size, explaining the size segregated population distribution. Our finding seems
to be consistent with observations made by Hesse (1979), reporting that
mobility increases in conch > 170 mm.
In the case of Xel-Ha, the average size of mobile conch was ~210 mm, although redistribution in the inlet was mostly related to
lip thickness, with mainly reproductive
adult conch (lip thickness ≥ 5 mm) in Bocana.
Alcolado (1979) [7] and Stoner & Ray (1996) [33] determined that nurseries are usually restricted to
certain sites with special environmental features. Corporal size of
an organism is a key aspect of its ecology, determining its ability to exploit resources
and its susceptibility to predation [20]. Organisms that undergo large changes in body size typically
display pronounced changes in resource use between birth and maturation, known
as ontogenetic niche shifts, which often manifest as shifts in habitat use or
diet with increasing body size [20,34,35]. This
can generate complex interactions and dynamics within communities [20]. One of the key features of an ontogenic niche is
segregation of the population by size. This phenomenon is especially well
documented in aquatic communities [20], as for
example in the Caribbean spiny lobster Panulirus
argus [ 36] or
Archaster typicus,
a common sea star of the Indo Pacific regions [37].
Ontogenetic niche shifts are
particularly important for organisms for which resource use, growth rates, and
predation risk are strongly related to body size [20,38],
as in the case of S. gigas, given that juveniles are highly vulnerable to
predation and
that mortality decreases dramatically with size [39-42].
Lobsters for example, attain partial refuge from predation in size, allowing
the ontogenetic niche shift from full-time algal dwelling to diurnal crevice
sheltering and nocturnal foraging [36]. The
common Indo Pacific sea star A. typicus, is found to be associated with
intertidal mangrove prop roots, sea grass meadows, sandy beaches, and shoals.
Small specimens occur with higher densities in intertidal mangrove prop roots.
High organic matter in sediment and a relatively low predation rate seems to
support juvenile life among mangroves. Size and density analyses provide
evidence that individuals gradually move to seagrass, sandy habitats, and
shoals as they age, allowing an ontogenetic habitat shifts for sea stars to be
documented, providing new biological information as a basis for management of
harvested A.
typicus populations [37]. On the other hand, spatial aggregations by age
and sex have been described for S. luhuanus, a close relative of L. gigas from the Indo-pacific. Four types of discrete
aggregations have been identified for this species: mixed age-class, juveniles,
mating and cluster [42], which also indicates
that population aggregation or segregation may be a common social feature of Strombus
species.
The
ecological processes operating in nursery habitats, compared to other habitats,
must support greater contributions to adult recruitment from any combination of
four factors: (1) density, (2) growth, (3) survival of juveniles, and (4)
movement to adult habitats [21]. In the case of
Xel-Ha, the first three aspects have already been identified successfully [44], while the present study supports evidence for
the migration of juveniles to adult habitats. This suggests that the sites in
the interior of the inlet probably function as nurseries, whereas Bocana may be associated with reproductive activity, where spawning
aggregations have been observed from June to October [45].
Mobility of L. gigas in the
Xel-Ha inlet increased during the rainy season, corresponding to the summer
months. This has previously been reported by. Furthermore, the conch reproductive season has been
associated with increasing temperatures [5,18,45-47],
and as mentioned before, spawning conch have been observed in the inlet from June to October.
Our
study provides evidence of spatial segregation of life stages, and coupled with
previous studies on growth, survival and density [26],
we conclude that the Xel-Ha inlet can be considered a true nursery,
successfully transferring individuals from juvenile habitats to adult
populations. Furthermore, we propose that the queen conch S. gigas performs ontogenic niche
shifts related to size. The seasonality of the habitat shift from juvenile to
adult habitats, strongly suggests that these are related to reproductive
activity, hence conch mobility could be used as an indicator for sexual
maturity.
4.
Acknowledgments
We
thank Xel-Há Park’s administration and staff,
for logistical support during our field work. Thanks to CONACYT for the
economic support through the scholarship Conacyt 24210 and The Grant The pink
snail as an indicator of climate change in the Caribbean: ocean acidification
and warming (CB‐2012‐01/181329). Thanks
to Ph.D. Gemma Franklin, a native speaker for revision of this manuscript.
research paper 
