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Morphometric Trait Variation in Thalassia testudinum (Banks ex Konig) Associated to Environmental Heterogeneity in a Subtropical Ecosystem | OMICS International
ISSN: 2157-7625
Journal of Ecosystem & Ecography

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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

*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: [email protected]
*Corresponding Author:
Jorge Alfredo Herrera-Silveira
Departamento de Recursos del Mar
Carretera Antigua a Progreso km. 6
Mérida Yucatán C.P. 97310, México
Tel: 0152-942-9400 ext. 2528
Fax: 0152- 981-2334
E-mail:[email protected]

Received date: August 02, 2010;Accepted date: August 22, 2011; Published date: 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 and source are credited.

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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.


Thalassia testudinum; Morphometric; Size-frequency distribution; Ecoindicator; Multivariate analysis


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 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 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 shootspecific 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 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.


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


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 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:belowground 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 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 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.

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 HcR 4 HcR 5 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  

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.

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.


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.


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.


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.


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.


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.


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.


Figure 10: RDA’s Biplot of the two first axes from selection variables with Monte-Carlo’s test (structure variables–shot density, above-ground:belowground biomass, max leaf width and max leaf length-; and hydrological variables–salinity, temperature and inorganic nitrogen), with Hidrochemical Regions (HcR) like centroids.

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 that the hydrochemical regions-1 and 3 were associated with shootspecific 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 areaspecific 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).


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].

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].

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 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 [19,20,47,48], 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 [21,51], 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 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 [20,34,40], 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 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 frequency distributions and ecosystem functional traits such as productivity and nutrient dynamics, as well as biodiversity associated to seagrass meadows and the sediment settings.


This work is part of the Doctoral thesis of Leonardo Arellano at CINVESTAVIPN, 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".


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