osystem &

Ec

Ec
Arellano-Méndez et al. J Ecosys Ecograph 2011, S1
f

Journal of Ecosystem & Ecography

J ournal o

og r
DOI: 10.4172/2157-7625.S1-001
aphy
ISSN: 2157-7625

Research Article Open

OpenAccess
Access

Morphometric Trait Variation in Thalassia testudinum (Banks ex Konig)

Associated to Environmental Heterogeneity in a Subtropical Ecosystem
Leonardo Uriel Arellano-Méndez*, Jorge Alfredo Herrera-Silveira*, Jorge Luis Montero- Muñoz and María De los Angeles Liceaga-Correa
Departamento de Recursos del Mar, CINVESTAV-IPN, Unidad Mérida, USA

Abstract
In order to advance on the understanding of the morphology plasticity of Thalassia testudinum at different
hydrochemical conditions, the size–frequency distributions of shoot- specific and area-specific characteristics were
investigated in five hydrochemical regions of Bahía de la Ascension, a non-disturbed coastal bay in the Mexican
Caribbean region. At Bahía de la Ascension was observed that the size-frequency distributions of the morphometric
characteristic of Thalassia testudinum were registered in the lowest modal classes, the only exception was the
maximum leaf length. All the morphometric variables analyzed showed differences among hydrochemical regions,
indicating the plasticity of this seagrass according to site-specific water quality conditions, suggesting its utility as
ecoindicator, and confirm the hydrochemical zoning of Bahía de la Ascension. The results of the multivariate analysis
used to establish the association among the hydrochemical regions and the morphometric trait variation of Thalassia
testudinum indicate that the best shoot-specific and area-specific characteristics were registered in environmentally
stable areas across time and with relatively high nutrient concentrations, high transparency and salinity ranging from
25 to 35, which demonstrate the sensitivity of size–frequency distributions characteristics to environmental variability,
indicating that T. testudinum morphology responds strongly to local and regional hydrochemical heterogeneity.

Keywords: Thalassia testudinum; Morphometric; Size-frequency
distribution; Ecoindicator; Multivariate analysis
Introduction
Under natural conditions, coastal ecosystems are recognized as
highly productive and resilient systems which represent feeding and
reproductive grounds, as well as refuge for numerous species [1-6].
Moreover, these ecosystems provide environmental services to humans
both directly (i.e., fisheries) or indirectly (i.e., recreation) [7]. Because
these systems are located at the land-ocean interface, they are highly
dynamic and heterogeneous and species that inhabit them develop
diverse strategies to cope with such high levels of environmental
variation. This environmental scenario favors phenotypic plasticity
in many of these species, which results in greater levels of variation
at different levels of organization (biochemical, individual, population
or community-level) [8]. Seagrasses are an important structural
and functional component of coastal ecosystems because they act
as sediment traps and stabilizers that improve water quality. They
also represent a direct and indirect source of organic matter for
many organisms, provide a habitat or refuge for fauna, and are
remarkably efficient nutrient recyclers [9,10]. On the other hand,
changes in seagrasses spatial and temporal distribution have been
commonly linked to environmental heterogeneity, as well as natural
or anthropogenic impacts [11,12]. As a result, seagrasses has been
commonly used as an environmental indicator [13-15]. Nonetheless,
it has been found that seagrass responses to environmental variation
across physical and chemical hydrological gradients are not always
linear [16]. This has stimulated a great deal of research in order to
better understand and characterize seagrasses responses to different
types of impact, and in this way generate more precise predictions
of human impacts on coastal ecosystems, as well as serve to support
both conservation or restoration programs. Thalassia testudinum
Banks ex König is a long-lived tropical seagrass specie that requires
specific hydrological conditions for its survival and development. Such
niche specificity is one of the main reasons why it has been used as
bioindicator of “ecosystem health” in coastal tropical and subtropical
ecosystems [17]. Specifically, several morphometric and anatomical
traits of this species such as leaf length and width, leaf specific area and
above ground biomass have been used to estimate habitat complexity
[18], as well as they served as ecological indicators of environmental
changes [17]. The Bahía de la Ascension is a coastal ecosystem located
inside the “Sian Ka´an” Biosphere Reserve (RBSK) that is situated
south of Cancun (SE Mexico). The Bahía de la Ascension is recognized
by having a relatively good conservation status [19]. It constitutes a
highly heterogeneous ecosystem from a hydrochemical stand point;
up to five different hydrochemical regions have been identified in this
system. These five regions were identified through grouping stations
according to differences and similarities in salinity, temperature,
dissolved inorganic nutrients and Chl-a, using a data matrix which
include 85 sampling station and samplings in 3 different seasons
and two times each one. Spatial variation in the freshwater inputs
and water interchange with the sea are forcing functions to favor the
spatial heterogeneity and the seasonal variations of the hydrochemical
behavior in Bahía de la Ascension [20]. Such conditions make a
suitable system to examine the relationship between morphometric/
structural traits in T. testudinum and hydrochemical variability under
*Corresponding author: Leonardo Uriel Arellano-Mendez, Departamento de
Recursos del Mar, CINVESTAV-IPN, Unidad Mérida , Carretera Antigua a Progreso
km. 6, Mérida Yucatán C.P. 97310, México Tel: 0152-942-9400 ext. 2528; Fax:
0152- 981-2334; E-mail: leonardo@mda.cinvestav.mx
Jorge Alfredo Herrera-Silveira, Departamento de Recursos del Mar, CINVESTAV-
IPN, Unidad Mérida , Carretera Antigua a Progreso km. 6, Mérida Yucatán C.P.
97310, México. Tel: 0152-942-9400 ext. 2528; Fax: 0152- 981-2334; E-mail:
jherrera@mda.cinvestav.mx
Received August 02, 2010; Accepted August 22, 2011; Published August 25,
2011
Citation: Arellano-Méndez LU, Herrera-Silveira JA, Montero- Muñoz JL, De
los Angeles Liceaga-Correa M (2011) Morphometric Trait Variation in Thalassia
testudinum (Banks ex König) Associated to Environmental Heterogeneity in a
Subtropical Ecosystem. J Ecosys Ecograph S1:001. doi:10.4172/2157-7625.S1-
001
Copyright: © 2011 Arellano-Méndez LU, et al. This is an open-access article
distributed under the terms of the Creative Commons Attribution License, which
permits unrestricted use, distribution, and reproduction in any medium, provided
the original author and source are credited.

J Ecosys Ecograph
ISSN:2157-7625 JEE, an open access journal Special Issue 1 • 2011
Citation: Arellano-Méndez LU, Herrera-Silveira JA, Montero- Muñoz JL, De los Angeles Liceaga-Correa M (2011) Morphometric Trait Variation
in Thalassia testudinum (Banks ex König) Associated to Environmental Heterogeneity in a Subtropical Ecosystem. J Ecosys Ecograph
S1:001. doi:10.4172/2157-7625.S1-001

Page 2 of 13

conditions of low (direct) human impact. In this way, the present study
intends to contribute to the establishment of a reference framework
that serves to determine the relationship between variation in seagrass
morphometric traits and different hydrochemical conditions. Such
framework should be useful to determinate the ecosystem condition in
tropical coastal regions, as well as to determine which hydrochemical
variables are more strongly related to such seagrass characteristics, and
thus suitable to detect anthropogenic impacts on water quality in such
systems.
Study area
The Bahia de la Ascension was selected as study system to carry
out the present work. It occupies an area of 740 km², and is located
within the limits of the RBSK (Figure 1). The RBSK is situated in
Quintana Roo state, at southeast Mexico, on the Caribbean coast,
covering a total of 5,281,470 km², including a wide variety of terrestrial
and marine ecosystems. Samples were sorted by species (Thalassia
testudinum and macroalgaes) and only live plant material was used

Figure 1: Geographic localization of the study site and sampling stations in Bahia de la Ascension, Quintana Roo. México.

HchR Temperature (°C) Salinity DIN (μmol l-1) SRP (μmol l-1) SRSi (μmol l-1) Chl-a (mg m-3)
1 27.0 (25.5-31.5) 32.0 (26.5-32.5) 1.48 (1.38-2.95) 1.00 (0.60-1.40) 22.5 (13.5-29.5) 0.40 (0.23-0.65)
2 26.7 (25.0-30.0) 25.5 (18.5-34.0) 1.11 (0.65-3.03) 1.05 (0.45-1.40) 23.5 (16.5-29.5) 0.46 (0.26-0.75)
3 28.2 (26.0-30.5) 27.5 (15.0-36.0) 1.06 (0.91-3.50) 0.95 (0.45-1.75) 24.0 (12.0-29.0) 0.39 (0.27-0.74)
4 29.0 (25.5-32.0) 20.0 (5.4-36.0) 1.23 (1.03-3.62) 0.90 (0.50-1.90) 18.5 (10.5-28.0) 0.37 (0.23-0.69)
5 27.3 (26.5-31.5) 33.5 (22.0-38.5) 1.34 (1.18-3.1) 1.10 (0.95-1.90) 24.5 (12.5-29) 0.41 (0.25-0.69)

Table 1: Mean and range values of the physical and chemical variables from the Hidrochemical Regions (HchR) in Bahía de la Ascension. Dissolved inorganic nitrogen
DIN, (NO2+NO3+NH4), soluble reactive phosphorus (SRP), soluble reactive silica (SRSi), and Chlorophyll-a (Chl-a), (Arellano-Méndez, 2004).

HcR 1 HcR 2 HcR 3 HcR4 HcR5 Other sites

Leaves per shoot 6 ± 0.42 4 ± 1.44 6 ±0.76 3 ± 0.52 6 ± 0.33 4 ± 0.95 (b)
Density (shoots m-2) 233 ± 14 165 ± 50 230 ± 25 87 ± 18 249 ± 12 494 ± 49 (a)
Max Leaf Long (cm) 21 ± 2.73 17.7 ± 2.4 13.7 ± 1.41 2.93 ± 0.22 18.7 ± 2.4 13.3 ± 1.8 (b)
Max Leaf Width (mm) 7.6 ± 0.24 5.83 ± 0.49 5.36 ± 0.15 4.87 ± 0.02 6.6 ± 0.15 4 ± .2 (b)
Leaf Area Index (m2m-2) 1.2 ± 0.12 0.93 ± 0.67 1.24 ± 0.22 0.60 ± 0.19 1.52 ± 0.09 2.8 ± 0.5 (b)
Aboveground Biomass (g DW m ) -2
184.5 ± 20.6 53.22 ± 6.5 95.5 ± 10.1 42.3 ± 7.1 168.3 ± 16.15 76 ± 9 (a)
Total Biomass (g DW m-2) 989.4 ± 89.1 366.5 ± 53.9 547.5 ± 78.38 274.8 ± 47.5 910.2 ± 68.7 584 ± 103 (a)
Above:Belowground Biomass ratio 0.31 ± 0.02 0.27 ± 0.07 0.31 ± 0.04 0.20 ± 0.03 0.27 ± 0.02
a
Data from other authors cited by Terrados et al. [81].
b
Data from diferente authors: Castillo-Torres, [69], Díaz et. al., 2003, Hackney and Durako, [21], Guzmán et al. [7], Fonseca et al. [71].
Table 2: Comparison of the different morphometric characteristics of Thalassia testudinum in the five Hydrochemical Regions (HcR) in Bahía de la Ascención, (Q. Roo,
México) in 2006-2007 and other locations.

J Ecosys Ecograph
ISSN:2157-7625 JEE, an open access journal Special Issue 1 • 2011
Citation: Arellano-Méndez LU, Herrera-Silveira JA, Montero- Muñoz JL, De los Angeles Liceaga-Correa M (2011) Morphometric Trait Variation
in Thalassia testudinum (Banks ex König) Associated to Environmental Heterogeneity in a Subtropical Ecosystem. J Ecosys Ecograph
S1:001. doi:10.4172/2157-7625.S1-001

Page 3 of 13

for analyses. Thalassia testudinum consists of a horizontally creeping
rhizome (long-shoot), lateral short-shoots (or vertical rhizomes),
formed by monopodial branching of the rhizome apex, arise at regular
intervals from the rhizome. Short-shoots produce leaves, consisting of
a colourless sheath, and a green photosynthetic blade. The following
measures were recorded for each short-shoot: total number of leaves,
leaf length (cm) from point of attachment to the short-shoot leaf tip,
and leaf width (cm) just above the sheath (protective cover consisting
of dead leaves) of all green leaf blades. Each sample was divided in
two portions: above-ground (consisting of green leaves from which
epiphytes were carefully removed) and below-ground (short-shoot
and live rhizomes and roots), both of which were dried to constant
weight at 60°C and then weighed to measure standing crop. Based
on Hakney and Durako [21] approach, data recorded for each of the
two sample portions were used to describe two types of morphometric
characteristics in T. testudinum: shoot-specific traits and area-specific
traits. The following shoot-specific traits were measured: leaves per
shoot, maximum shoot leaf length, maximum leaf width, and shoot-
specific leaf area (the sum of the leaf area of a short-shoot in cm2). The
area-specific traits measured were: short-shoot density (shoots m-2),
Leaf Area Index (LAI; mean shoot- specific leaf area x short-shoot
density, m2 m−2), standing crop (g m−2), and the ratio of above- to
below-ground biomass.The basin of the Bahía de la Ascension has an
area of approximately 2,950 km², and Multivariate statistical analyses
were conducted to test for differences in T. testudinum shoot-specific
and area-specific characteristics across hydrochemical regions. This
was done by comparing the frequency distribution patterns of the T.
testudinum variables. In order to evaluate the effect of hydrochemical
characteristics on variation of T. testudinum morphometric variables,
we used a constrained ordination method. First, the longitude of the

Figure 2: Variation of the morphometric characteristics as number of leaf per shoot-1 and maximum leaf width (cm) of T. testudinum, in Bahía de la Ascension.

J Ecosys Ecograph
ISSN:2157-7625 JEE, an open access journal Special Issue 1 • 2011
Citation: Arellano-Méndez LU, Herrera-Silveira JA, Montero- Muñoz JL, De los Angeles Liceaga-Correa M (2011) Morphometric Trait Variation
in Thalassia testudinum (Banks ex König) Associated to Environmental Heterogeneity in a Subtropical Ecosystem. J Ecosys Ecograph
S1:001. doi:10.4172/2157-7625.S1-001

Page 4 of 13

Figure 3: Variation of the morphometric characteristics of Leaf Area Index (LAI; m2 m-2) and maximum leaf length (cm) of T. testudinum, in Bahía de la Ascension.

gradient (measured in standard deviations; SD) of the response matrix
(structural and morphometric characteristic of T. testudinum) was
estimated by means of a Detrended Correspondence Analysis (DCA),
where <3 SD (standard deviation) was considered a short response
gradient while >4 SD was considered a unimodal response gradient
[22]. When the gradient is of short response, a redundancy analysis
(RDA) is recommended, which assumes a linear relationship between
predictor variables (hydrological matrix) and response variables
(structural and morphometric matrix). Morphometric data were
log n +1 transformed. The procedure to select significant variables
(alpha level set at 0.05) was the forward selection by means of the
Monte Carlo permutations test (999 permutations), which provides
estimates of the marginal and conditional variance for each of the
selected variables. Following recommendations from ter Braak and
Similauer [22], only variables with a Variance Inflation Factor (VIF)
smaller than 20 (indicating non collinearity among selected variables)
were considered for analysis. The value of the all canonical eigenvalues
sum was reported in all cases. Results from the constrained ordination
(RDA) are represented through “biplots”, using hydrochemical regions
as supplementary variables in the graph.
Results
The observed range of values for shoot-specific and area-specific
characteristics in Thalassia testudinum at Bahía de la Ascension did
not differ from those observed at other localities of the sub-tropical
region (Table 2). At the overall Bahía de la Ascension data, the
frequency distribution of shoot-specific and area-specific trait values
described a positive tendency for which most of the observations fell
in a region of low values (Figures 2, 3, 4 and 5); the only exception
to this pattern was given by maximum leaf length (Figure 2a), which

J Ecosys Ecograph
ISSN:2157-7625 JEE, an open access journal Special Issue 1 • 2011
Citation: Arellano-Méndez LU, Herrera-Silveira JA, Montero- Muñoz JL, De los Angeles Liceaga-Correa M (2011) Morphometric Trait Variation
in Thalassia testudinum (Banks ex König) Associated to Environmental Heterogeneity in a Subtropical Ecosystem. J Ecosys Ecograph
S1:001. doi:10.4172/2157-7625.S1-001

Page 5 of 13

Figure 4: Variation of the morphometric characteristics of leaf area shoot-1 (cm2) and standig crop (g DW m-2) of T. testudinum, in Bahía de la Ascension.

showed a nearly symmetrical distribution. The observed frequency
distribution patterns at the spatial scale of Bahía de la Ascension varied
considerably. Specifically, 85% of the values for number of leaves per
shoot fell inside modal classes of 4 and 5 leaves shoot (Figure 2b),
while 68% of maximum leaf width values fell inside modal classes of
0.5, 0.6 and 0.7 cm; maximum leaf width was 1.5 cm (Figure 3a). In
addition, 34% of the LAI values fell inside modal classes 0.4 to 0.8 m2
m-2 (Figure 3b); less than 1% of the LAI values fell inside the greatest
modal classes (3-4-5 m2 m-2). Finally, 50% of the maximum shoot leaf
length values fell inside modal classes 10 to 18 cm (Figure 2a), with
maximum leaf length falling inside the modal class of 70 cm; 56% of
leaf area per shoot values (cm2) fell inside modal classes 10 to 25 cm2,
and less than 0.5% of the values fell in the greatest modal class (264
cm2; Figure 4a). Biomass was analyzed in two ways: above-ground
biomass and above- ground:below-ground biomass ratio. Specifically,
9.4 % of standing crop values fell inside 7 the modal class of 70 gr m-2
(Figure 4b), while the frequency of values falling inside the greatest
modal classes (i.e., 700 gr m-2) was of 1.4%; the highest biomass value
was of 1960 gr m-2. On the other hand, 28% of the above-ground:below-
ground biomass ratio values fell inside modal class 0.125-0.175 (Figure
5a), while most of shoot density values (31%; Figure 5b) were found
inside the modal class of 200 shoot m-2. With respect to trait variation
across hydrochemical regions, the number of leaves per shoot showed
to be more variable in zones 1, 4 and 5, while for zones 2 and 3 all of
the values for this trait were distributed in 3 modal classes of which the
class of 3 leaves shoot-1 held the greatest number of values. However,
hydrochemical region-2 showed a negative distribution with 2 leaves
shoot-1 as the minimum, while hydrochemical region-3 registered

J Ecosys Ecograph
ISSN:2157-7625 JEE, an open access journal Special Issue 1 • 2011
Citation: Arellano-Méndez LU, Herrera-Silveira JA, Montero- Muñoz JL, De los Angeles Liceaga-Correa M (2011) Morphometric Trait Variation
in Thalassia testudinum (Banks ex König) Associated to Environmental Heterogeneity in a Subtropical Ecosystem. J Ecosys Ecograph
S1:001. doi:10.4172/2157-7625.S1-001

Page 6 of 13

Figure 5: Variation of the morphometric characteristics of above:below-ground biomass relation and Shoot density (m2) of T. testudinum, in Bahía de la Ascension.

a positive distribution with 5 leaves shoot-1 as the maximum (Figure
6a). Hydrochemical region-5 showed more variability in the number
of leaves shoot-1, with values of up to 10 leaves shoot-1. On the other
hand, maximum leaf width (Figure 6b) showed to be most variable for
zones 1 and 5, and more than 50% of the measurements recorded for
this variable fell inside the class interval 0.5 to 0.7 cm; hydrochemical
region-2 and 3 showed a less number of classes dominating the modal
class of 0.6 cm. Finally, maximum leaf length was more variable in
hydrochemical region-1, with values ranging from 8 to 70 cm, and
the modal class at 20cm; values were less variable at hydrochemical
region-3 and 4, although they showed the same modal class (20cm).
This trait did not show a clear pattern for hydrochemical region-2
(Figure 7a). The LAI was more variable at hydrochemical region-1 and
5, the modal class of 0.2 m2 m-2 being dominant. Patterns were unclear
for other zones (Figure 7b). Standing crop frequency distribution on
the other hand, exhibited a positive pattern for all hydrochemical
regions except region 2 (Figure 8a). This variable showed its highest
mean values (> 600 g m-2) at hydrochemical region-1, 2 and 5. On the
other hand, the above-ground:below-ground biomass ratio (Figure 8b)
was more variable at hydrochemical region-1 and 5 with more classes,
and more than 50% of the data falling inside modal classes 0.1 and 0.2;
this variable showed a positive frequency distribution pattern at these
zones, which differed from that observed for other zones which did not
show any type of tendency. Hydrochemical region-2 showed a narrow
range of values and 29% of the data was distributed in modal classes 0.2
and 0.4. Shoot density (Figure 9a) values showed a positive distribution
at all zones except hydrochemical region-3 where the data exhibited a
central tendency towards the modal class of 300 shoots m-2; the greatest

J Ecosys Ecograph
ISSN:2157-7625 JEE, an open access journal Special Issue 1 • 2011
Citation: Arellano-Méndez LU, Herrera-Silveira JA, Montero- Muñoz JL, De los Angeles Liceaga-Correa M (2011) Morphometric Trait Variation
in Thalassia testudinum (Banks ex König) Associated to Environmental Heterogeneity in a Subtropical Ecosystem. J Ecosys Ecograph
S1:001. doi:10.4172/2157-7625.S1-001

Page 7 of 13

Figure 6: Interzone (Hidrochemical Regions) comparison of the morphometri characteristics variation of number of leaf per shoot-1 and maximum leaf width (cm) of
T. testudinum in Bahía de la Ascension.

Figure 7: Variation of the morphometric characteristics of maximun leaf length (cm) and Leaf Area Index (LAI; m2 m-2) of T. testudinum, in Bahía de la Ascension.

level of variation for this trait was observed at hydrochemical region-5,
while the dominant modal class was that of 200 shoots m-2. In order to
identify the relationship among regions, hydrochemical variables and
T. testudinum morphometric traits, a multivariate analysis approach
was conducted. The first step was to determine the length of the
gradient from a DCA (detrended correspondence analysis) which is
an indirect ordination technique that shows the maximum dispersion
(using standard deviations) of the sample scores. As the first ordination
axis was <4 Standard Deviation (0.123 SD), and a redundancy analysis
(RDA) was then chosen to analyze the data [22]. Figure 10 shows that
temperature, salinity, nitrites, nitrates, ammonium, soluble reactive
phosphorus (SRP) and soluble reactive silica (SRSi) explain ≈85%
(84.87%) of the variance in T. testudinum morphometric variables
(Table 3). The eigenvalues of the first two constrained axes were
0.666 (1st) and 0.140 (2nd), respectively, while the sum of all canonical
eigenvalues was 0.047.
The Monte Carlo permutations test indicated which of the
selected variables had the strongest and most significant (P<0.05)
correlation with the environmental variables. On the other hand,
no multicollinearity among the selected variables (all of them had
values < 10) was identified among the data, VIF values (Table 3). The
relationship between T. testudinum traits, environmental variables and
the five hydrochemical regions was statistically significant (P<0.05).
Figure 10 show the triplot generated from the RDA which indicated

J Ecosys Ecograph
ISSN:2157-7625 JEE, an open access journal Special Issue 1 • 2011
Citation: Arellano-Méndez LU, Herrera-Silveira JA, Montero- Muñoz JL, De los Angeles Liceaga-Correa M (2011) Morphometric Trait Variation
in Thalassia testudinum (Banks ex König) Associated to Environmental Heterogeneity in a Subtropical Ecosystem. J Ecosys Ecograph
S1:001. doi:10.4172/2157-7625.S1-001

Page 8 of 13

Figure 8: Variation of the morphometric characteristics of standig crop (g DW m-2) and above:belowground biomass of T. testudinum, en Bahía de la Ascension.

Figure 9: Interzone (Hidrochemical Regions) comparison of the morphometric characteristics variation of shoot density (m2) of T. testudinum in Bahía de la
Ascension.

that the hydrochemical regions-1 and 3 were associated with shoot-

Figure 10: RDA’s Biplot of the two first axes from selection variables with
Monte-Carlo’s test (structure variables–shot density, above-ground:below-
ground biomass, max leaf width and max leaf length-; and hydrological
variables–salinity, temperature and inorganic nitrogen), with Hidrochemical
Regions (HcR) like centroids.
specific characteristics (length and width maximums), high salinity
and ammonium concentrations. On the other hand, hydrochemical
region-4 was associated to the amount of standing crop and high water
temperatures, while hydrochemical regions-4 and 5 were linked to area-
specific characteristics. Given that, the triplot was constructed based
on centered and standardized variables, the position of hydrochemical
region-5 suggests this environmental scenario as the most favorable
for T. testudinum development, due to in it was registered the best
shoot-specific and area-specific characteristics of this seagrass in the
entire system. The most important gradients which characterized the
hydrochemical regions were: salinity (for the first constrained axis),
and above-ground:below-ground biomass ratio, standing crop and
temperature (the last three in the case of the second constrained axis).
Discussion
The observed size-frequency distributions of some morphometric
characteristics in T. testudinum at Bahía de la Ascension according
to the natural hydrochemical variability of this system, suggest
that phenotipic plasticity and spatial distribution of T. testudinum
according to the environmental gradients are higher than registered
before at other localities in Gulf of Mexico and Caribbean (Table 2)
[23-26].

J Ecosys Ecograph
ISSN:2157-7625 JEE, an open access journal Special Issue 1 • 2011
Citation: Arellano-Méndez LU, Herrera-Silveira JA, Montero- Muñoz JL, De los Angeles Liceaga-Correa M (2011) Morphometric Trait Variation
in Thalassia testudinum (Banks ex König) Associated to Environmental Heterogeneity in a Subtropical Ecosystem. J Ecosys Ecograph
S1:001. doi:10.4172/2157-7625.S1-001

Page 9 of 13

Variable F λm λc λexp P VIF

Seagrass variables
Max leaf width 6.228 0.262 0.020 35.94% 0.0010 0.2108
Max leaf long 3.057 0.192 0.001 26.33% 0.0025 0.3035
Above-ground biomass 0.169 0.125 0.002 17.15% 0.0054 0.5675
Below-ground biomass 1.283 0.098 0.002 13.44% 0.0057 0.6731
Standing crop 0.628 0.014 0.003 1.92% 0.0080 1.5408
Total Explicate Variance percentage 94.78%
Environmental variables
Temperature 7.335 0.267 0.267 43.41% 0.0020 1.4833
Salinity 4.921 0.107 0.513 17.40% 0.0060 2.3788
Nitrites 3.865 0.054 0.321 8.78% 0.0087 1.4196
Nitrates 3.155 0.050 0.371 8.13% 0.0210 1.1681
Amonium 2.528 0.023 0.406 3.74% 0.0340 1.2912
SRP 1.114 0.012 0.383 1.95% 0.0400 1.4445
SRSi 1.098 0.009 0.359 1.46% 0.0430 1.3211
Total Explicate Variance percentage 84.87%

Table 3: RDA values from selected variables by Monte Carlo test with 999 permutations, with their values of F (permutated), λm (marginal variance), λc (cumulative
variance), λexp (explicate variance), P-values and VIF (Valor Inflation Factor), with a Total Explicate Variance of 94.78% of 0.729 Total Variance of seagrasses and
84.87% of Total Explicate Variance of 0.615 Total Variance of environmental variables, with a probability valor p<0.01, in both cases.

The observed modal classes for T. testudinum of maximum leaf
length and width, number of leaves per shoot, and above-ground
biomass at Bahía de la Ascension are higher than those reported for
this specie at Florida Bay (FB) [21]. Such differences suggest that water
quality and sediment variables at Bahía de la Ascension are probably
better for the development of T. testudinum compared to those found
at FB. This could be is strengthened due to FB has suffered hydrological
changes favoring massive die- off of the T. testudinum [27,28].
The results for all of the morphometric traits analyzed for T.
testudinum at Bahía de la Ascension indicated patterns associated with
the hydrochemical variability observed in this system, supporting that
this species could occupy different habitats in ecosystems that show
high environmental heterogeneity due to it strong phenotypic plasticity
of this specie. Seagrasses display an extraordinarily high degree of
phenotypic plasticity, adapting rapidly to changing environmental
conditions by means of which it has adapted in terms of growth to specific
conditions found at each hydrochemical regions. These findings may
be useful to define range values for T. testudinum morphometric traits
that should be useful as reference hydrochemical conditions at Bahía de
la Ascension (i.e., be used as eco-indicator variables). Several authors
demonstrated that several structural and dynamic characteristics of T.
testudinum are affected by environmental conditions and reproductive
efforts, as the positive correlation between biomass and water
transparency [17,29-32]. Spatially, the hydrochemical region-4 was
the most different respect to the other zones in terms of T. testudinum
morphometric trait values, it is probably due to this zone receives
freshwater and sediment inputs from land run-off, favoring low salinity
and water transparency as well as major seasonal variability (Table 1)
[20]. T. testudinum has been recognized to be a plastic species in terms
of its responses to environmental changes, considered a climax seagrass
species in the Caribbean, and showing high sensitivity to salinity and
water transparency changes [33].
T. testudinum meadows at hydrochemical regions-1 and 5 showed
the greatest mean biomass, number of leaves per shoot, as well as
the longest and widest leaves (Figures 2, 3, 4 and 5), suggesting that
environmental conditions at these zones are particularly favorable
for this species development. Variables as sediment characteristics
and water transparency are similar in both zones [34,20], and the
RDA biplot (Figure 10) suggest that both are more quite similar
between than among the other zones. Both zones are located in
areas relatively near from coral reef barrier, islands or mangroves,
being protected from mechanical damage caused by waves and tides
[35]. The maximum values of number of leaves per shoot, density
and biomass in the region 5 (Figures 6, 7, 8 and 9), should be related
with the nutrients and sediments inputs from mangroves connected
with the seagrass meadows in this area, the nutrients source and
water transparency changes could favored the leaves production
increasing the above biomass [36]. The association observed between
T. testudinum and morphometric trait values at both these sites should
be useful in order to establish reference values for a hydrochemical
range of variations for this species and being used as an ecological
indicator in these subtropical ecosystem. However, other variables as
sediment characteristics and hydrodynamic must be added in order to
establishment connection between ecosystem health and T. testudinum
morphometric variables. Overall, these results show that the structure
of biological components in coastal ecosystems responds strongly to
local and regional forcing functions [37], and thus the magnitude of
anthropogenic impacts and natural events such as hurricanes could be
evaluated by using biological indicator species such as seagrasses [38].
T. testudinum morphometric trait values at hydrochemical region-3
and 4 were mostly distributed in the lower value modal classes (Figures
6, 7, 8 and 9), suggesting that the environmental conditions at these
zones were not the best for T. testudinum development. Hydrochemical
region-3 is characterized by high salinity values, and strong changes
of the water transparency (Table 1), and the bottom is dominated by
limestone with low percentage of sandy sediments [34,39]. This region
is located in the central portion of Bahía de la Ascension where marine
currents dynamic is intense and do not provide sediment conditions

J Ecosys Ecograph
ISSN:2157-7625 JEE, an open access journal Special Issue 1 • 2011
Citation: Arellano-Méndez LU, Herrera-Silveira JA, Montero- Muñoz JL, De los Angeles Liceaga-Correa M (2011) Morphometric Trait Variation
in Thalassia testudinum (Banks ex König) Associated to Environmental Heterogeneity in a Subtropical Ecosystem. J Ecosys Ecograph
S1:001. doi:10.4172/2157-7625.S1-001
that are stable enough for the anchorage of T. testudinum structures
and rhizome dispersion [40]. In the region-4, the low mean water
salinity (Table 1) is probably the main environmental variable driving
a major frequency of low values in T. testudinum morphometric traits
[41], except for shoot density values (Figure 9a). Is interesting to
observe shoots of T. testudinum in salinities as lower as 5, when the
reports indicate the this specie is estenohaline with optimus neares to
marine salinity [42-44].
The use of multivariate statistical tools in the present study has been
useful to define ecological zones [45,46] within the study area through
the associations between hydrochemical variables and morphometric
traits of T. testudinum. Specifically, these tools help us to describe the
environmental complexity of the study system by linking different
combinations of morphometric variables in T. testudinum according
to the hydrochemical heterogeneity of Bahía de la Ascension, the latter
being driven mainly by spatial and temporal changes in marine and
freshwater inputs, as well as nutrient and sediment changes. Overall
mean shoot density for T. testudinum at Bahía de la Ascension was <200
shoots m-2, while at FB more than 50% of the densities values fell inside
the modal class of 500 shoots m-2 [21]. Nonetheless, biomass and leaf
size were greater at Bahía de la Ascension, where 50% of the sampling
sites exhibited values in modal classes between 50-200 gr m-2, while
at FB up to 80% of the sampling sites had biomass values <40 gr m-2.
Although Bahía de la Ascension shows lower mean shoot density of T.
testudinum, the leaves are of greater size, this leave’s size suggests that
photosynthetic efficiency will be reflected in development of the foliage
of the plants due to the amount of light entering the water column,
with an average of 2.75 URT [20] equivalent to a transparency-2.04m-1
(Wet Labs Inc, 1998), likewise, the size of the leaves indicate the use
of inorganic carbon in this type of karst environments have available
[20,19,47,48], as have mechanisms seagrass carbonate absorption and
conversion of carbon dioxide, which are near the surface of the leaf
[49,50], and this will be reflected in the further development of the
aboveground biomass of T. testudinum, this combination of factors
are an hydrochemical indicator of better general environmental
conditions and ecosystem heath of Bahía de la Ascension than FB, and
support use the structural development of T. testudinum as ecological
indicator in these coastal ecosystems as in the FB has not been seen this
same combination of factors, because here there is a greater turbidity
[51,21], coupled with a scheme by salinity stress, being in large central
area concentrations close to 70 during prolonged droughts, as well
as changes in the discharge of freshwater and saltwater exchange for
the dredging of mouths to the sea [52-54]. On the other hand, this
combination of hydrochemical factors (good transparency, adequate
discharge of carbon) will be reflected in the Leaf Area Index Index
values were greater at Bahía de la Ascensión than FB (where there is
a greater turbidity and therefore less photosynthesis), the first show
the most sampling sites in a LAI >18-20 m2 m-2, while in the second
more than 70% of the sampling sites had values within modal classes <
2m2m-2. The RDA analysis indicate an environmental gradient strongly
associated to salinity values and inversely temperature values (high
temperature and low salt concentrations in the inner bay toward the
mouth where there are low temperature and high salt concentrations),
this gradient is related to heavy freshwater discharge in the system and
breadth of the mouth of the Bay [53,40], where a positive association
of salinity, because this area is in the mouth of the bay with direct
contact with the entry of sea water and thus cooler waters and dynamic,
allowing optimum light input and the partnership is seen as a reflection
on morphometric characteristics of T. testudinum [54]. These gradient
J Ecosys Ecograph
ISSN:2157-7625 JEE, an open access journal
Page 10 of 13
and its associated to high shoot density and leaf length / width
values Recorded at Hydrochemical region 1 (Figure 10), these same
characteristics of T. testudinum, are associated with the hydrochemical
region 3, but here is related to nutrients (Table 1) presented by a
contribution due to runoff and transparency [20], especially in the
margin coastal waters where they are slower and allow for better
settling and therefore greater transparency [34,20,40], as well as the
remineralization of organic matter [55,56] as the grouping of these
variables (nutrients, transparency) are ones that cause the association
with morphometric characteristics of productivity [54]. On the other
hand, salinity and ammonium conditions observed at hydrochemical
region-1 and 3 were associated to long and wide leaves, probably as
a result of nutrient inputs from organic matter remineralization
[56], given that this zone is characterized by silty- clay sediments
[34]. According to the RDA analysis, hydrochemical region-5
showed strongest association between environmental variables and
morphometric characteristics of T. testudinum, suggesting that this
zone showed the most favorable environmental conditions for this
species development. This finding has important management and
conservation implications for the region, due this zone should be have
a seagrass management program.
The association between hydrochemical and biological variables
such as morphometric characteristics in T. testudinum, should
consider the spatial dependence between these two groups of variables,
which cannot be treated by a classic statistic [57,58]. The RDA results
support the hypothesis that the association between hydrochemical
variables and morphometric characteristics in T. testudinum should be
directly related to local conditions of each hydrochemical region, but
not just this, even sediments conditions are important for the spatial
distribution, growing, and development of seagrasses [53,54,59].
The frequency distributions of the T. testudinum variables measured
in this study, indicate a base-line of spatial pattern in the distribution,
abundance and morphometric differentiation of T. testudinum
characteristic in Bahia de la Ascension, supports that this species is
highly plastic and adaptable to different hydrological conditions as water
transparency, temperature and salinity, as observed in other coastal
ecosystems [60-63]. However, the same variables could act as limiting
factors for the establishment, permanency and development of this
specie, probably the in any specific area of the Bay. These observations
suggest a healthy environment (from a hydrochemical standpoint)
which favors a well developed T. testudinum meadows which in turn
will be able to better respond to changing conditions, especially to
extreme events such as the hurricanes, or environmental fluctuations
due to climatic change. On the other hand, the data analysis conducted
here allowed identifying local sources of environmental variation in
Bahía de la Ascension, which would have not been detected if only the
central tendency of the data had been taken into account during the
analysis. Overall, our results indicate differences across hydrochemical
regions, which resulted in corresponding differences in morphometric
characteristics for T. testudinum, affecting local morphological patterns
in this seagrass.
Findings from this study show that T. testudinum is sensitive to
the hydrochemical variability registered at each hydrochemical regions
of Bahía de la Ascension, and its presumably high level of plasticity
allows it to establish and develop across a wide range of conditions
and thus be distributed practically throughout the entire Bay, despite
strong environmental differences across sites. Together with findings
from studies conducted in other areas [21], the present work suggests
Special Issue 1 • 2011
Citation: Arellano-Méndez LU, Herrera-Silveira JA, Montero- Muñoz JL, De los Angeles Liceaga-Correa M (2011) Morphometric Trait Variation
in Thalassia testudinum (Banks ex König) Associated to Environmental Heterogeneity in a Subtropical Ecosystem. J Ecosys Ecograph
S1:001. doi:10.4172/2157-7625.S1-001
that long-term monitoring in spatially-heterogeneous systems (i.e.,
across latitudinal gradients) will offer the best experimental layout
to obtain T. testudinum reference values that can be used to define
the health condition of tropical and subtropical coastal ecosystems.
The estimation of these reference values should be done at the
appropriate spatial scale (i.e., at a site- specific level). Same plasticity
has been observed in other species such as sea grass Zostera noltii
in Portugal, which has a considerable plasticity along an intertidal
gradient, showing changes in morphometric structural level, both
environmental variability that determines the structure and level of
plasticity, eg large and broad leaves found on plants to low intertidal
zone, which occurs according to observations at other sites intertidal
and depth gradients [64,65], the same effect in the leaves were observed
in Ascension Bay with respect to the gradient of salinity and depth.
This effect was interpreted as an adaptation to irradiance. It also has
been reported to Z. noltii under a strong hydrodynamic reduces the
size and shape of the shoots [66,67]. All these evidences suggest that the
plasticity found in the leaves of Z. noltii, are due to effects of emersion
/ drying and light, rather than hydrodynamic effects. With respect to
P. oceanica, also presents a plasticity in the space (4 sites) and time (3
years of sampling) to hydrodynamic effects with respect to density, with
respect to the gradient of depth and transparency, since the density has
an enormous variability but remains stable over time with respect to
the number of sheets per bundle (6 in average) and the length of them
(average 18.5cm), maintained with little variation (ranging from 5 to 7
sheets beam and 17 to 20cm with respect to length, Borg et al., 2006).
With regard to this study, the results show that the effects of plasticity
in the leaves of T. testudinum in Bahía de la Ascension are due more
to the hydrodynamic effects (the gradient of salinity, transparency
and temperature in particular). Several morphometric characteristics
of T. testudinum in some basins of Bahia de Ascension were higher
than other Caribbean and Gulf of Mexico sites (Table 2); leaves per
shoot, maximum leaf long, maximum leaf width, total biomass were
two times the average recorded previously for this species. The HcR1
and HcR5 showed the highest values of the last variables. However, the
mean values of the same T. testudinum variables in the HcR4 were the
lowest among regions and among sites. This range of variation about
the response of T. testudinum to environmental gradients reflect their
plasticity, however, it is not just related to water quality conditions,
suggesting that the specific vegetative development of T. testudinum
might be driven too by conditions related with physical processes as
light availabil1ty, sediments characteristics, and the intensity and
frequency of natural events as hurricanes.
The variability in size-frequency distributions for structural and
morphometric characteristics in T. testudinum across hydrochemical
regions at Bahía de la Ascension could be used as indicator of
environmental heterogeneity of this coastal system, and probably
this favored more resilience to the submerged aquatic vegetation
component of this ecosystem.
This present study has been established an ecological baseline
to define the magnitude of medium and long-term changes in T.
testudinum populations at the Bahia de la Ascension driven by natural
hydrochemical variation, human impacts, as well as natural events
such as hurricanes. Seagrass population data such as that presented
here (i.e., together with findings from similar studies), will useful to
define the range of environmental conditions which characterize
healthy Caribbean coastal ecosystems, assuming these species can
act as ecological indicators. Future research effort should focus on
the relationship between variations in seagrass morphometric size-
J Ecosys Ecograph
ISSN:2157-7625 JEE, an open access journal
Page 11 of 13
frequency distributions and ecosystem functional traits such as
productivity and nutrient dynamics, as well as biodiversity associated
to seagrass meadows and the sediment settings.
Acknowledgements
This work is part of the Doctoral thesis of Leonardo Arellano at CINVESTAV-
IPN, U. Mérida. We acknowledge, Javier Ramírez, Israel Medina, Jorge Trejo,
Ileana Osorio, Jose Cámara, Elsy Alvarado, Juan Ascencio, Lucio Loman y Sara
Morales for helping in sampling and for assistance in measurements. This work
was financially supported by Primary Production Laboratory and The Nature
Conservancy (MxSomex0106070CINVETSAC-Pastos Marinos). Thanks to
personal of the “Area Natural Protegida de Sian Ka´an”.
References
1. Marguillier S, van der Velde G, Dehairs F, Hemminga MA, Rajagopal S (1997)
Trophic relationships in an interlinked mangrove-seagrass ecosystem as traced
by delta 13C and delta 15N. Mar Ecol Prog Ser 151: 115-121.
2. De Troch M, Mees J, Wakwabi EO (1998) Diets of abundant fishes from beach
seine catches in seagrass beds of a tropical bay (Gazi Bay, Kenya). Belg J
Zool 128: 135-154.
3. Nagelkerken I, Dorenbosch M, Verberk WCEP, Cocheret de la Moriniere E,
et al. (2000a) Day-night shifts of fishes between shallow-water biotopes of a
Caribbean bay, with emphasis on the nocturnal feeding of Haemulidae and
Lutjanidae. Mar Ecol Progr Ser 194: 55-64.
4. Nagelkerken I, Dorenbosch M, Verberk WCEP, Cocheret de la Moriniere E,
van der Velde G (2000b) Importance of shallow water biotopes of a Caribbean
bay for juvenile coral reef fishes: patterns in biotope association, community
structure and spatial distribution. Mar Ecol Prog Ser 202: 175-192.
5. Nagelkerken I, van der Velde G, Gorissen MW, Meijer GJ, van’t Hof T et al.
(2000c) Importance of mangroves, seagrass beds and the shallow coral reef
as a nursery for important coral reef fishes, using a visual census technique.
Estuar Coast Shelf Sci 51: 31-44.
6. Nagelkerken I, van der Velde G, Cocheret de la Moriniere E (2001) Fish feeding
guilds along a gradient of bay biotopes and coral reef depth zones. Aquat Ecol
35: 73-86.
7. Guzman HM, Barnes PAG, Lovelock CE, Feller IC (2005) A site description of
the CARICOMP Mangrove, Seagrass and Coral reff sites in Bocas del Toro,
Panama. Carib J Sci 41: 430-440.
8. Cottingham KL, Schindler DE (2000) Effects of grazer community structure on
phytoplankton response to nutrient pulses. Ecology 81: 183-200.
9. Attrill MJ, Power M, Thomas RM (1999) Modelling estuarine Crustacea
population fluctuations in response to physico-chemical trends. Marine Ecology
Progress Series 178: 89-99.
10. Hemminga MT,Duarte CM (2000) Seagrass Ecology. Cambridge University
Press.
11. Hobbs NT (1990) Diet selection by generalist herbivores: to test of the to line
programming model. In: Hughes RN (ed), Behavioural mechanisms of food
selection (BORN THIS WAY series, Vol: 20). Springer, Berlin Heidelberg New
York.
12. Field CB, Randerson JT, Malmström CM (1995) Global net primary production:
Combining ecology and remote sensing. Remot Sens Environ 51: 74-88.
13. Wang PF, Martin J, Morrison G (1999) Water quality and Eutrophication in
Tampa Bay, Florida. Est Coastal Shelf Sci 49: 1-20.
14. Tomasko DT, Corbett CT, Greening HS, Raulerson GY (2005) Spatial and
temporary variation in seagrass coverage in southwest Florida: Assessing the
relative effect of anthropogenic nutrient lauds reductions and rainfall in four
contiguous estuaries. Mar Pollut Bullet 50: 797-805.
15. Romero J, García Y, Manzanera M, Archers Y(2007) Impact of the brine from
to desalination plant on to shallow seagrass (Posidonia oceanica) meadow.
Estuar Coast Shelf Sci 72: 579-590.
16. Nichols PB, Couch JD, Al-Hamdani SH (2000) Selected physiological
responses of Salvinia minima to different chromium concentrations. Aqu Bot
68: 313-319.
17. Durako MJ, Moffler MD (1987) Factors affecting the reproductive ecology of
Thalassia testudinum. Aqu Bot 27: 79-95.
Special Issue 1 • 2011
Citation: Arellano-Méndez LU, Herrera-Silveira JA, Montero- Muñoz JL, De los Angeles Liceaga-Correa M (2011) Morphometric Trait Variation
in Thalassia testudinum (Banks ex König) Associated to Environmental Heterogeneity in a Subtropical Ecosystem. J Ecosys Ecograph
S1:001. doi:10.4172/2157-7625.S1-001
18. Heck KL Jr, Wetstone GS (1977) Habitat complexity and invertebrate species
richness and abundance in tropical seagrass meadows. J Biogeography 4:
135-142.
19. Herrera-Silveira JA (2006) Coastal lagoons of Yucatan (SE, México):
Investigation, Diagnostic and Management. ECOTROPICOS 19: 94-108.
20. Arellano-Méndez LU (2004) Space-Temporary Analysis of the Hydrological
Variables: Detection of Heterogeneity to Space Great Scale. Center
of Investigation and of Advanced Studies of the Polytechnic National
(CINVESTAV-IPN) Institute. Master thesis, Unit Merida, Yucatan, Mexico.
21. Hackney JW, Durako MJ (2004) Size-frequency patterns in morphometric
characteristics of the seagrass Thalassia testudinum reflect environmental
variability. Ecol Ind 4: 55-71.
22. ter Braak CJF, Smilauer P (2002) Canoco 4.51. Biometris-Plant Research
International, Wageningen, the Netherlands.
23. McMillan C (1978) Morphogeographic variation under controlled conditions in
five seagrasses, Thalassia testudinum, Halodule wrightii, Syringodium filiforme,
Halophila engelmannii, and Zostera marine. Aqu Botan 4: 169-189.
24. Back HP (1980) Age populations and biometrics in eelgrass, Zostera marina L.
Ophelia 19: 155-162.
25. Heij H, Neinhuis PH (1992) Intraspecific variation in isozyme patterns of
phenotypically separated populations of Zostera marina L., in the Southwestern
Netherlands. J Exp Mar Biol Ecol 161: 1-14.
26. Alcoverro T, Duarte CM, Romero J (1995) Annual growth dynamics of oceanic
Posidonia: contribution of large-scale versus local factors to seasonality.
Marine Ecol Prog Ser 120: 210-230.
27. Fourqurean JW, Robblee MW (1999) Florida Bay: to history of recent ecological
changes. Estuaries 22: 345-357.
28. Koch MS, Schopmeyer SA, Nielsen OI, Kyhn-Hansen C, Madden CJ (2007)
Conceptual model of seagrass die-off in Florida Bay: Links to biogeochemical
processes. J Exp Mar Biol Ecol 350: 73-88.
29. Dawes CJ, Tomasko DA (1988) Depth distribution of Thalassia testudinum
in two meadows on the west coast of Florida; a diffrerence in effect of light
availability. PSZN Mar Ecol 9: 123-130.
30. Harrison PG, Durance C (1992) Variation in clonal structure in an eelgrass
(Zostera marina) meadow on the Pacific coast of Canada. Can J Bot 70: 653-
657.
31. Lee KS, Dunton KH (1997) Effects of in situ light reduction on the maintenance,
growth and partitioning of carbon resources in Thalassia testudinum Banks ex
König. J Exp Mar Biol Ecol 210: 53-73.
32. Hernández-Delgado EA, Lassus J, Martinó D, Lucking MA, Márquez J, et al.
(2003) Caracterización de la comunidad de hierbas marinas en la reserva
natural del canal de Luis Peña, Culebra, Puerto Rico. En: Memorias del XXII
Simposio de la Flora y Fauna del Caribe. Universidad de Puerto Rico en
Humacao. Puerto Rico.
33. Galician ME, Merino M, Marbà N, Duarte CM (1993) Biomass and dynamics of
Thalassia testudinum in the Mexican Caribbean: elucidating rhizome growth.
Mar Ecol Prog Ser 95: 185-192.
34. Mexicano-Cintora G, Liceaga-Cintora MA, Arellano-Méndez LU, Hernández-
Núñez H (2003) Space and Systematic Characterization of the Superficial Silts
of Bay of the Ascension, Quintana Roo. National Congress of Science and
Technology of the Sea. 16 at 18 October, Boca del Rio, Veracruz.
35. Hale JA , Frazer TK, Tomasko DA, Hall MO (2004) Changes in the distribution
of seagrass species along Florida’s Central Gulf Coast: Iverson and Bittaker
revisited. Estuaries and Coasts 27: 36-43.
36. Valiela I, Cole ML (2002) Comparative Evidence that Salt Marshes and
Mangroves May Protect Seagrass Meadows from Land-derived Nitrogen
Loads. Ecosyst 5: 92-102.
37. Twilley RR (1995) Properties of mangrove ecosystems related to the energy
signature of coastal environments. In: Hall, C (ed) Maximum Power Boulder,
Colorado: University of Colorado Press.
38. Stewards JS, Virnstein RW, Lasi MA, Morris LJ, Miller JD, et al. (2006) The
impacts of the 2004 Hurricanes on hydrology, water quality and seagrass in
the Central Indian River Lagoon, Florida. Estuar Coast Mar Sci 29: 954-965.
J Ecosys Ecograph
ISSN:2157-7625 JEE, an open access journal
Page 12 of 13
39. Liceaga-Correa MA (2003) Final Report. Ecological, Current and Retrospective
characterization, of the Habitats Bénticos and their Relationship with the
Fishery of the Lobster Panulirus argus. Bay of the Ascension, Reserves of the
Biosphere of Sian Ka’an. Project SISIERRA 20000706005.
40. Medina-Gómez I (2010) Characterization of Karst Coastal Ecosystem in the
Mexican Caribbean: Assessing the influnces of the coastal hydrodynamics and
the submerged groundwater discharges on the seagrass habitat, Department
of Oceanography. Texas A&M University, College Station, TX.
41. Kelble CR, Ortner PB, Hitchcock GL, Boyer JN (2005) Attenuation of
photosynthetically available radiation (EVEN) in Florida Bay: potential for light-
limitation of primary producers. Estuaries 28: 560-571.
42. Zieman C (2000) The Biology of Thalassia: Paradigms and Recent Advances
in research. Seagrasses.Ecology. Hemminga M. A. and C. M. Duarte. (Eds.).
Cambridge University Press, Cambridge 298 .
43. den Hartog C (1970) Seagrasses of the World. North Holland Publ Co
Amsterdam.
44. In Van Tussenbroek B, Vonk JA, Stapel J, Erftemeijer PLA, Middelburg JJ,
Gómez-López (eds). 2003. Las praderas de pastos marinos de Colombia:
Estructura y distribución de un ecosistema estratégico. INVEMAR. Serie
Publicaciones Especiales No. 10, Santa Marta 160pp.
45. Wanless HR, Taggett MG (1989) Origin, growth and evolution of carbonates
mudbanks in Florida Bay. Bulletin of Marine Science 44: 454-489.
46. Zieman JC, Fourqurean JW, Iverson RL (1989) Distribution, abundance and
productivity of seagrasses and macroalgae in Florida Bay. Bull Mar Sci 44:
292-311.
47. Medina-Gómez I, Herrera-Silveira JA (2003) Spatial characterization of
water quality in a karstic coastal lagoon without anthropogenic disturbance: a
multivariate approach Estuarine. Coastal Shelf Sci 58: 455-465.
48. Medina-Gómez I, Herrera-Silveira JA (2006) Primary production dynamics in
a pristine groundwater influenced coastal lagoon of the Yucatan Peninsula.
Contin Shelf Res 26: 971-986.
49. Björk M, Weil A, Semesi S, Beer S (1997) Photosynthetic utilization of inorganic
carbon by seagrasses from Zanzibar, East Africa. Mar Biol 129: 363-366.
50. In Larkum AW, Drew EA, Ralph RJ (2000) Photosynthesis and Metabolism on
Seagrasses at the Cellular Level. Seagrasses. Ecology. Hemminga MA and
Duarte CM (Eds). Cambridge University Press, Cambridge 298.
51. Durako MJ (1996) Indicators of seagrasses ecological condition: an assessment
based on spatial and temporal changes. In: Dyers, K. R. and R. J. Orth (Eds).
Changes in Fluxes in Estuaries Olsen & Olsen Denmark 261.
52. Light SS, Dineen JW (1994) Water control in the Everglades: a historical
perspective. 47-84. In Davis SM, Ogden JC (Eds.) Everglades: the Ecosystem
and Its Restoration. St. Lucie Press, Delray Beach, FL, USA.
53. Nuttle WK, Fourqurean JW, Cosby BJ, Zieman JC, Robblee M (2000) Influence
of net freshwater supply on salinity in Florida Bay. Water Resour Res 36: 1805-
1822.
54. Rudnick DT, Ortner PB, Browder JA, Davis SM (2005) A Conceptual Ecological
Model of Florida Bay. Wetlands 25: 870-883.
55. Suttle CA, Harrison PJ (1988) Ammonium and phosphate uptake rates, N: P
supply ratios, and evidence for N and P limitation in some oligotrophic lakes.
Limnol Oceanogr 33: 186-202.
56. Suttle CT, Fuhrman JT, Capone DG (1990) Rapid ammonium cycling and
concentration-dependent partitioning of ammonium and phosphate: implications
for coal transfer in plankton communities. Limnol Oceanogr 35: 424-433.
57. Legendre P, Legendre L (1998) Numerical Ecology. Elsevier Amsterdan.
58. Liebhold M, Gurevitch J (2002) Integrating the statistical analysis of spatial
dates in ecology. Ecography 25: 553-557.
59. Carlson PR, Yarbro LA, Barber TR (1994) Relationship of sediment sulfide to
morality of Thalassia testudinum in Florida Bay. Bull Mar Sci 54: 733-774.
60. Duarte CM (1991) Seagrass depth limits. Aquat Bot 40: 363-377.
61. Fourqurean JW, Boyer JN, Durako MJ, Hefty LN, Peterson BJ (2003)
Forecasting responses of seagrass distributions to changing water quality
using monitoring data. J Appl Ecol 13: 474-489.
Special Issue 1 • 2011
Citation: Arellano-Méndez LU, Herrera-Silveira JA, Montero- Muñoz JL, De los Angeles Liceaga-Correa M (2011) Morphometric Trait Variation
in Thalassia testudinum (Banks ex König) Associated to Environmental Heterogeneity in a Subtropical Ecosystem. J Ecosys Ecograph
S1:001. doi:10.4172/2157-7625.S1-001
62. Borg JA, Micallef MA, Schembri YPJ (2006) Spatio-temporal variation in the
structure of a deep water Posidonia oceanica meadow assessed using non-
destructive techniques. Mar Ecol 27: 320-327.
63. Cabaço S, Machás R, Santos YR (2009) Individual and population plasticity
of the seagrass Zostera noltii along a vertical intertidal gradient. Estuarine,
Coastal and Shelf Sciences 82: 301-308.
64. Peralta G, Pérez-Llórens JL, Hernández I, Brun F, Vergara JJ, et al. (2000)
Morphological and physiological differences between two morphotypes of
Zostera noltii Hornem. from the south-western Iberian Peninsula. Helgoland
Mar Res 54: 80-86.
65. Tanaka Y, Nakaoka YM (2004) Emergence stress and morphological
constraints affect the species distribution and growth of subtropical intertidal
seagrasses. Mar Ecol Prog Ser 284: 117-131.
66. Schanz A, Asmus YH (2003) Impact of hydrodynamics on development and
morphology of intertidal seagrasses in the Wadden Sea. Mar Ecol Prog Ser
261: 123-134.
67. Peralta G, Brun FG, Pérez-Lloréns JL, Bouma YTJ (2006) Direct effects of
current velocity on the growth, morphometry and architecture of seagrasses: a
case study on Zostera noltii. Mar Ecol Prog Ser 327: 135-142.
68. Buia MC, Mazzella YL (1991) Reproductive phenology of the Mediterranean
seagrasses Posidonia oceanica (L.) Delile, Cymodocea nodosa (Ucria)
Aschers, and Zostera noltii Hornem. Aqu Bot 40: 343-362.
69. Castillo-Torres P (2002) Caracterización estructural y evaluación del estado
ambiental de las praderas de pastos marinos del Caribe colombiano. Trabajo
de grado (Biólogo Marino), Universidad Jorge Tadeo Lozano. Facultad de
Biología Marina. Área de Ingeniería y de Recursos Naturales. Santa Marta,
Colombia.
70. Durako MJ, Kunzelman JI (2002) Photosynthetic characteristics of Thalassia
testudinum measured in situ by press-amplitude modulated (PAM) fluorometry:
methodological and scale-based considerations. Aquat Bot 73: 173-185.
71. Fonseca AC, Nielsen V, Cortés J (2007) Monitoreo de pastos marinos en
Perezoso, Cahuita, Costa Rica (sitio CARICOMP). Rev Biol Trop 55: 55-66.
72. Gutierrez A (1986) Caracterización Geológica de la Zona Marina y Estuarina de
la reserve de la Biosfera de SIAN KA’AN, Quintana Roo. Reporte de Avance.
CIQROO.
J Ecosys Ecograph
ISSN:2157-7625 JEE, an open access journal
Page 13 of 13
73. Lipkin Y, Beer S, Zakai YD (2003) The seagrasses of Eastern Mediterranean
and Red Sea. In: Green E.P., Short F.T. (Eds). World Atlas of Seagrasses.
University California Press, CA: 65-73.
74. Mazzella L, Buia MC, Gambi MC, Lorenti M, Russo GF, et al. (1992) Plant–
animal trophic relationship in the Posidonia oceanica ecosystem of the
Mediterranean Sea: a review. In: John DM, Hawkins SJ, Price JH (Eds) Plant–
Animal Interaction in the Marine Benthos. Systematic Association special
volume. Clarendon Press, Oxford: 165-187.
75. Animal Interaction in the Marine Benthos. Systematic Association special
volume. Clarendon Press, Oxford: 165-187.
76. Paynter CK, Cortés J, Engels YM (2001) Biomass, productivity and density of
the seagrass Thalasassia testudinum at three sites in Cahuita National Park,
Costa Rica. Rev Biol Trop 49: 265-272.
77. Procaccini G, Buia MC, Gambi MC, Mez M, Pergent G, et al. (2003) The
seagrasses of the Western Mediterranean. In: Green EP, Short FT, World Atlas
of Seagrasses. University California Press, CA: 48-73.
78. Revilla N, Camarena L, Aguilar P, Aguilar D (1990a) Tipos de fondos de
un sector de Bahía de la Ascension, Quintana Roo, México, aplicando
teledetección. Academy of Sciences of Cuba. Fund of Publications 23-29.
79. Revilla N, González S, Álvarez R, Páez J, Hernández L et al. (1990b) Dynamics
of the system lagunar of the Cautious one, Cuba using teledetection methods.
Academy of Sciences of Cuba. Fund of Publications.
80. Scardi M (2003) Neural network applications in Coastal Ecological Modeling.
In: Lakhan C (Ed) Advances in Coastal Modeling. Elsevier Oceanogr Ser 67:
505-532.
81. Terrados J, Ramírez-García P, Hernández-Martínez O, Pedraza K, Quiroz A
(2008) State of Thalassia testudinum Banks ex König meadows in the Veracruz
Reef System, Veracruz, México. Aquatic Botany 88: 17-26.
82. Wet Labs Inc (1998) C Star Transmisometer User´s Guide Version 2.0.
Philomath, Oregon 21.
83. Zieman JC (1975) Seasonal variation of turtle grass, Thalassia testudinum
(König), with reference to temperature and salinity effects. Aquat Bot 1: 107-
123.
84. Kelble CR, Ortner PB, Hitchcock GL, Boyer JN (2005) Attenuation of
photosynthetically available radiation (EVEN) in Florida Bay: potential for light-
limitation of primary producers. Estuaries 28: 560-571.
Special Issue 1 • 2011