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Benthic community response to habitat variation: A case of study from a natural protected area, the Celestun coastal lagoon
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Continental Shelf Research 27 (2007) 2523–2533 www.elsevier.com/locate/csr
Benthic community response to habitat variation: A case of study from a natural protected area, the Celestun coastal lagoon Daniel Pech, Pedro-Luis Ardisson, Norma A. Herna´ndez-Guevara Departamento de Recursos del Mar, Cinvestav, Carretera Antigua a Progreso km 6, Apdo. Postal 73, Cordemex, 97310 Me´rida, Yucata´n, Me´xico Received 31 October 2006; received in revised form 21 June 2007; accepted 28 June 2007 Available online 22 July 2007
Abstract Little information currently exists on spatial and temporal benthic community variations in tropical coastal lagoons. Here, the benthic community response to habitat variation in the Celestun coastal lagoon, northwest Yucatan peninsula, was seasonally examined during the 1994–1995 climatic cycle into a grid of 12 sampling sites distributed along the salinity gradient of the lagoon. Habitat variation was assessed through physical factors associated both to the water column (e.g. salinity) and the bottom sediment (e.g. sand, silt and clay fractions). The benthic community response was assessed through species diversity measures and abundance. Under the influence of climatic seasonality, variations in habitat conditions followed by changes in the benthic community characteristics were expected. Results from two-way ANOVAs showed that for the period of study, Celestun lagoon was more heterogeneous along the spatial axis of variability than along the temporal one. Multiple regression analysis showed that salinity was spatially the main factor influencing the benthic community characteristics. Temporally, the sediment characteristics were observed to exert significant effects on the species diversity characteristics but not on abundance. Other variables assessed (dissolved oxygen, pH, temperature and water column transparency) exhibited no significant covariance with species diversity and abundance. Since generated from historical data, these results have the potential to be useful as a benchmark to the establishment of monitoring programs in the light of the increasing anthropogenic pressure on the natural resources of the lagoon and surrounding coastal area. r 2007 Elsevier Ltd. All rights reserved. Keywords: Coastal lagoons; Habitat; Benthos; Species diversity; Variability
1. Introduction Tropical coastal ecosystems such as sandy beaches, estuaries, and coastal lagoons, are among the world’s most jeopardized environments due to the increase in the intensity of use of their natural Corresponding author. Tel.: +52 999 1242100x2574; fax: +52 999 9812917. E-mail address: [email protected] (D. Pech).
0278-4343/$ - see front matter r 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.csr.2007.06.017
resources. These ecosystems are persistently exposed to anthropogenic activities that cause negative impacts on biodiversity and habitat suitability (Carr et al., 2003; Hughes, 1994). Celestun coastal lagoon, on the northwest Yucatan peninsula, is an example of a tropical ecosystem exposed to increasing human pressure. In this coastal lagoon, the local economy relies on the exploitation of natural resources in two different ways. On the one hand, its high biological productivity sustains artisanal
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fisheries exploiting organisms such as shrimps and fishes and, on the other hand, its scenic value allows the development of tourist activities such as the observation of the American flamingo Phoenicopterus ruber ruber. In spite of its importance, it is only recently that research has provided scientific evidence on the dynamics of this ecosystem in order to implement management strategies to assure its sustainability (e.g. Baldassarre et al., 1997; Pe´rezCastan˜eda and Defeo, 2003). The research conducted on this coastal lagoon has been mainly focused on the description of the hydrological (e.g. Herrera-Silveira, 1994), trophic (Vega-Cendejas, 2003), parasites (e.g. Vidal-Martinez et al., 2002) and shrimp species (e.g. Pe´rezCastan˜eda and Defeo, 2005) dynamics. Even though some of these studies have considered the submerged aquatic vegetation as a crucial factor determining the abundance and spatial distribution of shrimps (e.g. Pe´rez-Castan˜eda and Defeo, 2004), the study of the benthic habitat and its importance on the maintenance of the whole benthic community have been up to now overlooked. It is known that changes in the habitat characteristics have a great influence on the ecosystem functionality. For example, eutrophication of bottom habitats reduces the production of demersal fishes (Powers et al., 2005) and species diversity of the benthic community (Trush et al., 2001). Celestun coastal lagoon is a dynamic ecosystem showing natural significant intra annual variability in the water column characteristics mainly derived from seasonal rainfall, winds and temperature regimes prevailing in the zone. The regional climatic conditions have led to define three seasons for the study area whose temporal limits are not always well defined: the dry season from March to May, the rainy season from June to October and the winter frontal storms (nortes) season from November to February (Fuentes-Yaco et al., 2001). Accordingly, marked changes are expected both spatially and temporally in the bottom conditions followed by changes in the benthic community characteristics. Here, by using historical data, we explore the relationship between habitat quality (water column and sediment physical and chemical) characteristics and soft bottom benthic community (species richness, diversity, evenness and abundance) characteristics along the salinity gradient of the coastal lagoon during a complete climatic cycle. Historical data are useful to establish biological reference criteria to better understand the transient character-
istics of the benthic community and help to define the current status of the ecosystem health. In the absence of sound evidence demonstrating that the ecosystem changes are driven by human disturbance, results are discussed under the assumption that the dynamics of the benthic community is controlled mainly by natural climatic variability occurring during the period when the sampling program was carried out. 2. Materials and methods 2.1. Study site Celestun is a tropical coastal lagoon located in the northwest of the Yucatan peninsula (201450 N, 901250 W) as part of the Celestun biosphere reserve. The karstic nature of the site allows the input of freshwater from groundwater discharges that vary according to the rainfall regime (Herrera-Silveira et al., 1999). After the hydrological characteristics of the water column, the lagoon is divided in three main zones: seaward, middle, and inner (Herrera-Silveira, 1994). 2.2. Sampling procedure Sampling was carried out seasonally during the 1994–1995 climatic cycle into a grid of 12 sampling sites distributed along the lagoon salinity gradient (Fig. 1). Benthic samples were collected by triplicate using a Birge-Ekman stainless steel grab (15 cm 15 cm 15 cm). Once collected, samples were passed through a sieve of 500 mm mesh size and the organisms retained in the mesh were identified to the lowest possible taxonomic category. The sediment from each sample was taken apart to determine directly in the field its pH (potentiometer Corning pH-103) and interstitial salinity (portable refractometer portable S-100). Sediment subsamples were preserved at a temperature of 4 1C and transported to the laboratory for organic carbon determination (Walkley and Black, 1934), porosity (percentage volume) and particle size analysis (percentage of sand, silt and clay fractions). For this last analysis, the sand fraction was obtained passing the dry sediment through a sieve of 63 mm mesh. The silt and clay fractions were determined by the wet sieving analysis described in Holme and McIntyre (1984). Salinity, pH, temperature (analogical thermometer) and transparency (Secchi disc) of the water column were also registered in situ.
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was used to reduce the irrelevant explanatory factors susceptible to decrease the precision of the estimated coefficients and predicted values. The APS procedure fits all regressions involving one factor, two factors, three factors and son on. Then, selection criterion is recorded for each single regression test. Once the procedure finishes, the model for each variable subset is shown. The optimum subset of factors to be used in the multiple regression models is determined when the r-square values stabilize. 3. Results 3.1. Physical habitat factors
Fig. 1. Position of the sampling sites along the estuarine gradient in the Celestun coastal lagoon.
Additionally, dissolved oxygen was measured following the Winkler titration method (Parsons et al., 1984). 2.3. Data analysis Abundance (N. Ind. 0.25 m2), species richness (species number), species diversity (H0 ), and evenness (J0 ) were the four characteristics used to assess the spatial and temporal variability trends of the benthic community. Two-way ANOVAs were used to test for differences in the physical habitat factors and community characteristics among sampling sites and sampling seasons. When the normality assumption of the variables was not satisfied, the Kruskal–Wallis nonparametric test was carried out. The spatial resemblance in the habitat physical factors was described on a seasonal basis using the unweighted arithmetic average clustering (UPGMA). Cluster groups were obtained using a 50% similarity threshold value. Next, an ordination in reduced space procedure by principal component analysis (PCA) was used to determine the relationship among physical and biological variables. Multiple regression analysis was performed in order to obtain the best physical factors explaining the seasonal benthic community characteristics. Previous to the application of this last analysis, the ‘All possible regressions procedure (APS, NCSS 1999)’
Water salinity, sediment salinity, sand and silt were the factors that showed significant differences among sampling sites and sampling seasons. Organic matter and clay, on the contrary, showed significant differences only among sampling sites. Transparency showed significant differences among seasons. Finally, dissolved oxygen, pH and porosity data did not show significant differences neither in space or time (Tables 1 and 2). As expected water and sediment salinities increased seaward (Fig. 2c), while porosity and pH kept steady along the estuary gradient (Fig. 2a and d). The rest of the factors did not show any definite trends of variation. Cluster analysis, on the basis of the physical habitat factors, showed that the lagoon is structured in two main zones (Fig. 3). Roughly, the first zone corresponds to the sampling sites located in the inner and middle zones (sampling sites 1–8), and the second one corresponds to the sampling sites located in the seaward zone of the estuary gradient (sampling sites 9–12). This sampling sites array was better defined during the rainy and dry seasons; in the nortes season, the ecological resemblance among contiguous sampling sites tended to be not so clearly ordered. Modifying the similarity criterion from 50% to 70% permitted to observe three clusters of sampling sites located in the inner, middle and seaward zones of the estuary gradient; here again, this sampling sites array was more defined during the rainy and dry seasons. 3.2. Benthic community characteristics One hundred and five infaunal species were observed along the estuarine gradient during the fourth sampling periods. The most abundant taxa
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Table 1 Mean values of physical factors by sampling season
Organic matter (%) Dissolved oxygen (mg l1) Sand (%) Silt (%) Clay (%) Transparency (cm) Porosity (%) Water salinity Sediment salinity Sediment pH
Rainy 1994
Nortes 1994
Dry 1995
Rainy 1995
17.7 8.13 23.7 36.1 40.6 40 76.7 24.7 20.5 7.68
17.5 7.79 30.6 31.6 37.7 30.83 78.8 21.3 18.7 7.64
19.9 9.00 38.1 22.8 39.1 62.6 78.3 26.8 32.4 8.12
15.6 6.71 34.5 27.4 37.8 36.1 81.0 15.3 14.5 7.79
(2.76) (3.47) (17.2) (6.6) (13.3) (14.45) (7.63) (6.31) (6.46) (0.09)
(5.54) (2.07) (19.8) (7.72) (12.6) (12.9) (5.26) (0.24) (5.54) (0.24)
(11.6) (2.20) (25.8) (10.2) (19.5) (21.8) (8.34) (8.81) (5.89) (1.08)
(4.66) (0.77) (22.6) (9.73) (15.4) (14.7) (5.49) (6.85) (6.06) (0.20)
Number in parenthesis represents 71 S.D.
Table 2 Two-way ANOVAs (F) and Kruskal–Wallis (H) tests used to look for differences in physical habitat and benthic community characteristics as function of sampling site and season Site (A)
Season (B)
AB
Physical factor Organic matter (%) Sand (%) Silt (%) Clay (%) Transparency (cm) Dissolved oxygen (mg l1) pH Water salinity Sediment salinity Porosity (%)
F11,33 ¼ 1.95 F11,33 ¼ 28.08 F11,33 ¼ 6.91 F11,33 ¼ 17.89 F11,33 ¼ 0.80 H11,96 ¼ 9.21 H11,96 ¼ 12.71 H11,96 ¼ 24.81 H11,96 ¼ 19.78 H11,96 ¼ 2.93
F3,33 ¼ 0.86 F3,33 ¼ 6.90 F3,33 ¼ 11.54 F3,33 ¼ 0.31 F3,33 ¼ 8.38 H3,96 ¼ 7.45 H3,96 ¼ 2.51 H3,96 ¼ 11.43 H3,96 ¼ 23.74 H3,96 ¼ 3.21
F11,33 ¼ 6.74 F11,33 ¼ 3.53 F11,33 ¼ 2.07 F11,33 ¼ 3.10 F11,33 ¼ 2.09
Community characteristic Diversity (H0 ) Evenness (J0 ) Richness (species number) Abundance (N. Ind. 0.25 m2)
F11,33 ¼ 11.68 F11,33 ¼ 2.24 F11,33 ¼ 6.71 F11,33 ¼ 2.90
F3,33 ¼ 6.16 F3,33 ¼ 7.43 F3,33 ¼ 12.98 F3,33 ¼ 0.96
F11,33 ¼ 1.78 F11,33 ¼ 1.62 F11,33 ¼ 3.62 F11,33 ¼ 6.19
Term significant at alpha ¼ 0.05.
were Mollusca (40.4%), Polychaeta (29.4%) and Crustacea (25.8%). Echinodermata, Clitellata, Sipunculida and Nemertea represented together the remaining 4.3%. Species richness (Fig. 4a), species diversity (Fig. 4b) and, to a lesser extent, species evenness (Fig. 4c) increased from the inner to the seaward zone, while abundance (Fig. 4d) showed the opposite trend. The two-way ANOVAs showed that in almost all the cases, these community characteristics differed significantly among sampling seasons and sampling sites. Evenness was the sole characteristic that did not show significant differences among sampling sites and abundance was the sole one that did not show significant
differences among sampling seasons (Table 2; Fig. 4c and d). The highest values for species diversity and richness for the entire sampling area were registered during the 1995 dry season. The lowest values were registered in the 1994 nortes season. Highest and lowest values of evenness did not occur consistently during any particular season. Abundance presented similar values during the four sampling seasons as shown in the two-way ANOVAs. The composition of the major taxonomic groups showed significant changes among sampling sites (F ¼ 14.50, p ¼ 0.00) and sampling seasons (F ¼ 12.95, p ¼ 0.00). Polychaeta was the most dominant group during the two rainy seasons and
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Fig. 2. Spatial variability of organic matter, porosity (a), sediment texture (b), salinity (c), pH (d), dissolved oxygen (e), and water transparency (f) in the Celestun coastal lagoon. Histogram bars represent 71 S.D.
Fig. 3. UPGMA cluster analysis of the sampling sites in each season. Benthic habitat characteristics were used to associate the sampling sites. Cluster groups were obtained using a 50% similarity threshold value.
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Fig. 4. Spatial and seasonal variability of species richness (a), species diversity (b), abundance (c), and evenness (d) in the Celestun lagoon. Histogram bars represent 71 S.D.
Fig. 5. Spatial and seasonal variability of abundances of the major taxonomic groups in the Celestun lagoon. Histogram bars represent 71 S.D. The abundance of ‘‘Others’’ comprises Echinodermata, Sipunculida, Nemertea, and Clitellata pooled together.
Mollusca during nortes, while in the dry season not a dominant group was apparent (Fig. 5). Crustacea was the second dominant group during all seasons,
showing a higher stability than the all other groups. Even if all groups showed high temporal variability, Polychaeta was the only group almost disappearing
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during the nortes season (Fig. 5). On the whole, stations located in the inner zone showed higher abundances than the ones situated in the middle and seaward zones. The middle zone exhibited higher abundances than the other zones only during the 1994 rainy season. No group presented a clear trend of dominance for a particular zone, excepting perhaps Mollusca that were mostly limited to the inner lower salinity zone.
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3.3. Relationship among physical and biological characteristics The principal component analysis shows that in all cases, the first two principal components accounted for more than 90% of the variance (Fig. 6). The overall dispersal of physical and biological variables in the reduced space, shows that for all seasons and along the first principal
Fig. 6. Results from principal component analysis per climatic season. In all cases, the first two components accounted for more than 90% of the variance in the multivariate reduced space. OrMa, organic matter; WaSa, water salinity; SeSa, sediment salinity; Poro, porosity; DiOx, dissolved oxygen; Trans, transparency; Abund, abundance; Rich, species richness; Dive, species diversity, Evenn, species evenness.
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component, the species diversity measures (strongly and negatively related to water salinity, sediment salinity and, to a lesser extent, sand), were spatially discriminated from abundance (not clearly related in turn to any physical factor, excepting perhaps organic matter during the 1994 rainy season). On the contrary, for all seasons and along the second principal component, species evenness was clearly discriminated from species diversity, species richness and abundance. Along this principal component, species evenness was weakly and positively related to water salinity, sediment salinity and, to a lesser extent, pH in nortes 1994 and dry 1995, and unrelated to any other physical factor in the two remaining seasons. No more than two factors were retained by the multiple regression models in each sampling season (Table 3). In models in which only one factor was retained, these ones explained up to 58% of the observed variance. In the cases where two factors were retained, these ones explained more than 60% of the observed variance. Species diversity was better explained by water salinity alone or in
combination with porosity (rainy 1994) or sand (nortes 1994). In the meantime, species richness was better explained by silt in most seasons, but by clay in the nortes 1994 season. In an analogous way, abundance was better explained by the combination of water salinity and sediment salinity but only in the nortes 1994 and dry 1995 seasons. In the rainy 1994 and 1995 seasons, there were no factors retained by the models for explaining abundance. 4. Discussion Benthic community characteristics are expected to vary in keeping with spatial and seasonal variability. However, results do not totally sustain this assumption. Data analysis showed that for the period of study Celestun coastal lagoon was more heterogeneous along the spatial axis of variability than along the temporal one. Spatially salinity was the main factor influencing the benthic community characteristics. Temporally, the physical habitat characteristics were observed to exert significant effects on the species diversity measures but not on
Table 3 Multiple regression analysis per sampling season
Rainy 94
Diversity Richness Evenness Abundance
‘‘Nortes’’ 94
Diversity Richness Evenness Abundance
Factor
Slope
r2
SS
F
p
Water salinity Porosity Water salinity Silt Sediment salinity Porosity ——
+ + + + + + ——
0.66 0.13 0.25 0.48 0.36 0.22 ——
1.44 1.70 64.29 12.56 0.11 0.96 ——
9.13 11.27 12.85 9.45 5.38 4.09 ——
0.00 0.04 0.00 0.02 0.00 0.03 ——
Water salinity Sand Clay Water salinity Water salinity Sediment salinity
+ + + +
0.28 0.32 0.40 0.58 0.30 0.44
0.91 1.04 48.92 4.43 4.60 6.64
11.14 4.85 6.07 11.03 3.64 21.31
0.01 0.00 0.01 0.00 0.00 0.00
Dry 95
Diversity Richness Evenness Abundance
Water salinity Silt pH Water salinity Sediment salinity
+ +
0.47 0.48 0.54 0.33 0.27
1.52 58.26 0.18 4.99 4.09
9.12 9.26 5.63 3.31 10.06
0.02 0.03 0.00 0.02 0.00
Rainy 95
Diversity Richness
Sediment salinity Silt Sediment salinity Sand ——
+ + ——
0.48 0.48 0.19 0.50 ——
1.54 59.81 23.73 0.34 ——
6.22 4.25 3.98 4.90 ——
0.04 0.00 0.04 0.00 ——
Evenness Abundance
Regression models include the combination of factors that best accounted for the variation of each community characteristic. Only the significant results are showed (po0.05).
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abundance. Macrofauna responded to environmental variability by modifying the dominance relationships of the major taxonomic faunistic groups present in the community. Along the spatial axis of variability, Mollusca was the most abundant group in the inner zone during all seasons. Polychaeta, when present, was dominant in the middle zone, while in the seaward zone, no dominant group was present. Along the temporal axis of variability, Mollusca was dominant during both the nortes and dry seasons, and Polychaeta was the dominant one during the rainy season. Crustacea was the second dominant group during the whole period. The most remarkable feature of this dynamic scenario was the disappearance of Polychaeta during the nortes season, with a recovery in abundance throughout the rainy season, suggesting thus that this group respond sensibly to natural environmental disturbances. Dissolved oxygen, porosity and pH were the three factors that did not show significant differences along the temporal axis of variability. The karstic characteristic of the site probably acts as a buffer mechanism to maintain stable the mean values of pH. Constancy in porosity (percentage volume of pore space) indicates that texture and hydraulic conductivity of sediment kept roughly steady during the study period. Dissolved oxygen, usually variable both spatially and temporally (Herrera-Silveira et al., 2002), kept relatively steady during the whole period of interest. Rainfall in the study area, in addition to vary seasonally, varies also on a yearly basis. The data used in this study were obtained just after one of the most severe dryness periods recorded in the area during the last quarter century (Fig. 7). The relatively high and seasonally even values of dissolved oxygen probably denote the
Fig. 7. Historical annual mean precipitation in Celestun area. Dotted line represents 71 S.D.
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influence of the recovery period during which rainfall increased, illustrating by this mean the climatic forcing to which the study site is exposed. 4.1. Spatial variability trends The analysis of the data sustains the view that the species diversity measures and abundance mainly respond to changes in the salinity gradient of the lagoon (Nicolaidou et al., 2006). However, whereas species diversity and species richness correlated positively with salinity, abundance did the opposite. It has been already argued that salinity is the most important factor affecting submerged aquatic vegetation and shrimp abundance distribution in the Celestun coastal lagoon (Pe´rez-Castan˜eda and Defeo, 2003). This fact seems also true for the overall invertebrate benthic community and it is in the middle zone of the lagoon that the effects of this factor become more apparent. The middle zone corresponds to a mixed portion of the lagoon characterized by intermediate values of water salinity (Pe´rez-Castan˜eda and Defeo, 2003) and sediment salinity (this study). The main inflexion points in species diversity and species richness (increase), as well as in abundance (decrease) along the estuarine gradient occur precisely in this zone (Fig. 4). Whereas the lowest species diversity and species richness (higher dominance) observed in the inner zone could be associated with the natural physical stress prevailing in the freshwater zone (Arias and Drake, 1994), the lowest abundance (higher evenness) observed in the seaward zone could be associated with the increase in predation pressure of organisms that rely on benthic species as its principal food resource (juvenile shrimps, fishes), at least on a seasonal basis (Pe´rez-Castan˜eda and Defeo, 2005; Vega-Cendejas, 2003). The most abundant species observed in the inner zone were those that can tolerate low salinity values such as Assiminea succinea (Gastropoda), Hargeria rapax (Tanaidacea) and Leitoscoloplos fragilis (Polychaeta). In addition to salinity, benthic communities from coastal lagoons are deeply influenced by the granulometric characteristics (Beukema and Flach, 1995) and organic matter content (Jayaraj and Jayalakshmi, 2007) of sediment. The sediment of sampling sites 1–8 (Fig. 1) contained a major proportion of clay and silt. In the last four sampling sites, located in the seaward zone, the sediment was predominantly sandy, with a lesser proportion of
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silt and clay (Fig. 2b). Results from PCA and multiple regression analysis showed that sediment texture was the second more important factor explaining species diversity and species richness variance (Table 3; Fig. 6). Multiple regression analysis showed that species diversity was positively correlated with porosity and sand while species richness was mostly negatively correlated with silt and clay. Organic matter content did not appear to be related to any benthic community characteristic, probably because over time it was relatively invariant and over space its absolute content values did not represent a limiting resource for deposit feeders but at the same time did not represent either a risk of dystrophy for the system. 4.2. Temporal variability trends The physical habitat factors did not show marked seasonal variability. After ANOVA results, organic matter, dissolved oxygen, pH, sediment porosity and clay did not show significant differences among sampling seasons. The same result was obtained on the mean values of species abundance. In addition, none of the physical habitat factors mentioned above was retained in the regression models to explain abundance variability. On the contrary, it was observed that water salinity and sediment salinity were the factors affecting negatively abundance but only during the dry and nortes seasons. This suggests that for these factors and seasons, a feedback mechanism regulating abundance was underway, probably via the presence of marine predators entering the lagoon when the freshwater outflow was low or when the salt water entrance was forced during storm events. A critical aspect to be considered when examining the temporal variability in the benthic community response to environmental changes is that of sampling design in relation to scale. If environmental change and the subsequent temporal response of the benthic community occur at temporal scales shorter than our temporal sampling resolution (seasonal), these could get stabilized by the resilience of the system and pass unnoticed. For certain processes, the opposite is also susceptible to occur. Gonneea et al. (2004), tracing organic matter in mangrove sediments over the past 160 years, suggest that major fluctuation in the entire Celestun lagoon occurs at temporal scales higher that 10 years, a period much larger that the one examined in this study.
Water salinity, sediment salinity, as well as s and and silt sediment fractions, varied significantly on a seasonal basis (Table 2). After the multiple regression analysis, these four factors appeared responsible for the seasonal variability observed in species diversity and species richness, whose maximum values were observed during the dry season (Fig. 4). In keeping with these results, the lowest species diversity and species richness were expected to occur during the rainy season when salinity decreases due to the freshwater input and, to a lesser degree, during the nortes season when stability of the water column decrease by effect of the wind stress. In conclusion, seasonality only caused significant changes in 50% of the physical factors measured in this study. Among these, changes in salinity due to variations in the freshwater and saltwater balance seem to be the most important single factor inducing changes in the benthic community characteristics. Further studies connecting salinity to changes in this and other components of the lagoon such as fishes and submerged vegetation are needed to understand the role of salinity in this system. Effective management of the lagoon’s biological resources requires a sensitive indicator of the response to fresh or saltwater inflow that has ecological significance. Such kind of indicators has been already explored in the literature (e.g. Jassby et al., 1995) and could be profitably explored for the understanding of the dynamics of this coastal lagoon. In the last 25 years, there have been many efforts to maintain the Celestun coastal lagoon as an unaltered ecosystem. As part of these efforts, since 1979 this coastal lagoon makes part of a wildlife refuge, upgraded in 2000 to a biosphere reserve, and presently being integrated into the Mexican system of natural protected areas possessing its own management plan. However, anthropogenic activities within the lagoon and in the surrounding area have not ceased to increase during the same period. Among other threats, recent studies have reported the recurrent occurrence of harmful algal blooms in the Yucatan coastal zone caused by an increase in dissolved nutrients in the water column (Ghinaglia et al., 2004; Aranda-Cirerol et al., 2006). On the basis of the recognition of these threats, we are entitled to infer that the maintenance of the integrity of this ecosystem will be in the coming years a major challenge. It is exactly in this context that the soft bottom benthic community could be an appropriate
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tool for monitoring the habitat quality of the lagoon in the light of an increasing anthropogenic pressure on the natural resources of the nearshore coastal zone and, particularly, of this relatively healthy natural protected area. Acknowledgments We thank DUMAC (Ducks Unlimited) for providing field facilities in Celestun. Special thanks are due to the ‘Laboratorio de Bentos’ staff, Cinvestav, for field and laboratory assistance. This research was supported by funds from CONABIO to P.L.A. and a Cinvestav postodoctoral fellowship to D.P.
References Aranda-Cirerol, N., Herrera-Silveira, J.A., Comin, F.A., 2006. Nutrient water quality in a tropical coastal zone with groundwater discharge, northwest Yucatan, Mexico. Estuarine, Coastal and Shelf Science 68, 445–454. Arias, A.M., Drake, P., 1994. Structure and production of the benthic macroinvertebrate community in a shallow lagoon in the bay of Cadiz. Marine Ecology Progress Series 115, 151–167. Baldassarre, G.A., Arengo, F., Galicia, E., 1997. Habitat use and conservation of American flamingos (Phoenicopterus ruber ruber) and associated wetlands in Yucatan, Mexico. Final Report submitted to the United States and Wildlife ServiceNorth American Wetland Conservation Council and Secretarı´ a de Medio Ambiente, Recursos Naturales y Pesca, Mexico. State University of New York, Syracuse. Beukema, J.J., Flach, E.C., 1995. Factors controlling the upper and lower limits of the intertidal distribution of two Corophium species in the Wadden sea. Marine Ecology Progress Series 125, 117–126. Carr, M.H., Neigel, J.E., Estes, J.A., Andelman, S., Warner, R.R., Largier, J.L., 2003. Comparing marine and terrestrial ecosystems: implications for the design of coastal marine reserves. Ecological Applications 13, 90–107. Fuentes-Yaco, C., de Leon, D.A.S., Monreal-Gomez, M.A., 2001. Environmental forcing in a tropical estuarine ecosystem: the Palizada River in the southern Gulf of Mexico. Marine and Freshwater Research 52, 735–744. Ghinaglia, L.T., Herrera-Silveira, J.A., Comin, F.A., 2004. Structural variations of phytoplankton in the coastal seas of Yucatan, Mexico. Hydrobiologia 519, 85–102. Gonneea, M.E., Paytan, A., Herrera-Silveira, J.A., 2004. Tracing organic matter sources and carbon burial in mangrove sediments over the past 160 years. Estuarine, Coastal and Shelf Science 61, 211–227. Herrera-Silveira, J.A., 1994. Spatial heterogeneity and seasonal patterns in a tropical coastal lagoon. Journal of Coastal Research 10, 738–746.
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Herrera-Silveira, J.A., Martin, M., Diaz-Arce, V., 1999. Phytoplankton variations in four coastal lagoons, Yucatan, Mexico. Revista de Biologı´ a Tropical 47, 47–56. Herrera-Silveira, J.A., Medina-Gomez, I., Colli, R., 2002. Trophic status based on nutrient concentration scales and primary producers community of tropical coastal lagoons influenced by groundwater discharges. Hydrobiologia 475/ 476, 91–98. Holme, N.A., McIntyre, A.D., 1984. Methods for the Study of Marine Benthos. Blackwell, Oxford. Hughes, T.P., 1994. Catastrophes, phase-shifts, and large-scale degradation of a Caribbean coral-reef. Science 265, 1547–1551. Jassby, A.D., Kimmerer, W.J., Monismith, S.G., Armor, C., Cloern, J.E., Powell, T.M., Schubel, J.R., Vendlinski, T.J., 1995. Isohaline position as a habitat indicator for estuarine populations. Ecological Applications 5, 272–289. Jayaraj, K.A., Jayalakshmi, K.V., 2007. Influence of environmental properties on macrobenthos in the northwest Indian shelf. Environmental Monitoring and Assessment 127, 459–475. Nicolaidou, A., Petrou, K., Kormas, K.A., Reizopoulou, S., 2006. Inter-annual variability of soft bottom macrofaunal communities in two Ionian Sea lagoons. Hydrobiologia 555, 89–98. Parsons, T., Maita, Y., Lally, C., 1984. A Manual of Chemical and Biological Methods of Seawater Analysis. Pergamon Press, Oxford. Pe´rez-Castan˜eda, R., Defeo, O., 2003. Influence of estuarine zonation on exploited shrimp populations in a Mexican biosphere reserve: a feature for management and conservation. Journal of Marine Biology Assessment 83, 781–784. Pe´rez-Castan˜eda, R., Defeo, O., 2004. Spatial distribution and structure along ecological gradientes: penaeid shrimps in a tropical estuarine habitat of Mexico. Marine Ecology Progress Series 273, 173–185. Pe´rez-Castan˜eda, R., Defeo, O., 2005. Growth and mortality of transient shrimp populations (Farfatepenaeus spp.) in a coastal lagoon of Mexico: role of environmental and density dependence. Journal of Marine Science 62, 14–24. Powers, S.P., Peterson, C.H., Christian, R.R., Sullivan, E., Powers, M.J., Bishop, M.J., Buzelli, C.P., 2005. Effects of eutrophication on bottom habitat and prey resources of demersal fishes. Marine Ecology Progress Series 302, 233–243. Trush, S.F., Hewitt, J.E., Funell, G.A., Cummmings, V.J., Ellis, J., Shcultz, D., Talley, D., Norkko, A., 2001. Fishing disturbance and marine biodiversity: the role of habitat structure in simple soft-sediment systems. Marine Ecology Progress Series 223, 277–286. Vega-Cendejas, M.E., 2003. Trophic dynamics of a mangrove ecosystem in Celestun lagoon, Yucatan Peninsula, Mexico. Fisheries Centre Research Reports 1, 237–243. Vidal-Martinez, V.M., Jimenez-Cueto, A.M., Sima-Alvarez, R., 2002. Parasites and symbionts of native and cultured shrimps from Yucatan, Mexico. Journal of Aquatic Animal Health 1, 51–64. Walkley, A., Black, I.A., 1934. An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Science 37, 29–38.
Continental Shelf Research 27 (2007) 2523–2533 www.elsevier.com/locate/csr
Benthic community response to habitat variation: A case of study from a natural protected area, the Celestun coastal lagoon Daniel Pech, Pedro-Luis Ardisson, Norma A. Herna´ndez-Guevara Departamento de Recursos del Mar, Cinvestav, Carretera Antigua a Progreso km 6, Apdo. Postal 73, Cordemex, 97310 Me´rida, Yucata´n, Me´xico Received 31 October 2006; received in revised form 21 June 2007; accepted 28 June 2007 Available online 22 July 2007
Abstract Little information currently exists on spatial and temporal benthic community variations in tropical coastal lagoons. Here, the benthic community response to habitat variation in the Celestun coastal lagoon, northwest Yucatan peninsula, was seasonally examined during the 1994–1995 climatic cycle into a grid of 12 sampling sites distributed along the salinity gradient of the lagoon. Habitat variation was assessed through physical factors associated both to the water column (e.g. salinity) and the bottom sediment (e.g. sand, silt and clay fractions). The benthic community response was assessed through species diversity measures and abundance. Under the influence of climatic seasonality, variations in habitat conditions followed by changes in the benthic community characteristics were expected. Results from two-way ANOVAs showed that for the period of study, Celestun lagoon was more heterogeneous along the spatial axis of variability than along the temporal one. Multiple regression analysis showed that salinity was spatially the main factor influencing the benthic community characteristics. Temporally, the sediment characteristics were observed to exert significant effects on the species diversity characteristics but not on abundance. Other variables assessed (dissolved oxygen, pH, temperature and water column transparency) exhibited no significant covariance with species diversity and abundance. Since generated from historical data, these results have the potential to be useful as a benchmark to the establishment of monitoring programs in the light of the increasing anthropogenic pressure on the natural resources of the lagoon and surrounding coastal area. r 2007 Elsevier Ltd. All rights reserved. Keywords: Coastal lagoons; Habitat; Benthos; Species diversity; Variability
1. Introduction Tropical coastal ecosystems such as sandy beaches, estuaries, and coastal lagoons, are among the world’s most jeopardized environments due to the increase in the intensity of use of their natural Corresponding author. Tel.: +52 999 1242100x2574; fax: +52 999 9812917. E-mail address: [email protected] (D. Pech).
0278-4343/$ - see front matter r 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.csr.2007.06.017
resources. These ecosystems are persistently exposed to anthropogenic activities that cause negative impacts on biodiversity and habitat suitability (Carr et al., 2003; Hughes, 1994). Celestun coastal lagoon, on the northwest Yucatan peninsula, is an example of a tropical ecosystem exposed to increasing human pressure. In this coastal lagoon, the local economy relies on the exploitation of natural resources in two different ways. On the one hand, its high biological productivity sustains artisanal
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fisheries exploiting organisms such as shrimps and fishes and, on the other hand, its scenic value allows the development of tourist activities such as the observation of the American flamingo Phoenicopterus ruber ruber. In spite of its importance, it is only recently that research has provided scientific evidence on the dynamics of this ecosystem in order to implement management strategies to assure its sustainability (e.g. Baldassarre et al., 1997; Pe´rezCastan˜eda and Defeo, 2003). The research conducted on this coastal lagoon has been mainly focused on the description of the hydrological (e.g. Herrera-Silveira, 1994), trophic (Vega-Cendejas, 2003), parasites (e.g. Vidal-Martinez et al., 2002) and shrimp species (e.g. Pe´rezCastan˜eda and Defeo, 2005) dynamics. Even though some of these studies have considered the submerged aquatic vegetation as a crucial factor determining the abundance and spatial distribution of shrimps (e.g. Pe´rez-Castan˜eda and Defeo, 2004), the study of the benthic habitat and its importance on the maintenance of the whole benthic community have been up to now overlooked. It is known that changes in the habitat characteristics have a great influence on the ecosystem functionality. For example, eutrophication of bottom habitats reduces the production of demersal fishes (Powers et al., 2005) and species diversity of the benthic community (Trush et al., 2001). Celestun coastal lagoon is a dynamic ecosystem showing natural significant intra annual variability in the water column characteristics mainly derived from seasonal rainfall, winds and temperature regimes prevailing in the zone. The regional climatic conditions have led to define three seasons for the study area whose temporal limits are not always well defined: the dry season from March to May, the rainy season from June to October and the winter frontal storms (nortes) season from November to February (Fuentes-Yaco et al., 2001). Accordingly, marked changes are expected both spatially and temporally in the bottom conditions followed by changes in the benthic community characteristics. Here, by using historical data, we explore the relationship between habitat quality (water column and sediment physical and chemical) characteristics and soft bottom benthic community (species richness, diversity, evenness and abundance) characteristics along the salinity gradient of the coastal lagoon during a complete climatic cycle. Historical data are useful to establish biological reference criteria to better understand the transient character-
istics of the benthic community and help to define the current status of the ecosystem health. In the absence of sound evidence demonstrating that the ecosystem changes are driven by human disturbance, results are discussed under the assumption that the dynamics of the benthic community is controlled mainly by natural climatic variability occurring during the period when the sampling program was carried out. 2. Materials and methods 2.1. Study site Celestun is a tropical coastal lagoon located in the northwest of the Yucatan peninsula (201450 N, 901250 W) as part of the Celestun biosphere reserve. The karstic nature of the site allows the input of freshwater from groundwater discharges that vary according to the rainfall regime (Herrera-Silveira et al., 1999). After the hydrological characteristics of the water column, the lagoon is divided in three main zones: seaward, middle, and inner (Herrera-Silveira, 1994). 2.2. Sampling procedure Sampling was carried out seasonally during the 1994–1995 climatic cycle into a grid of 12 sampling sites distributed along the lagoon salinity gradient (Fig. 1). Benthic samples were collected by triplicate using a Birge-Ekman stainless steel grab (15 cm 15 cm 15 cm). Once collected, samples were passed through a sieve of 500 mm mesh size and the organisms retained in the mesh were identified to the lowest possible taxonomic category. The sediment from each sample was taken apart to determine directly in the field its pH (potentiometer Corning pH-103) and interstitial salinity (portable refractometer portable S-100). Sediment subsamples were preserved at a temperature of 4 1C and transported to the laboratory for organic carbon determination (Walkley and Black, 1934), porosity (percentage volume) and particle size analysis (percentage of sand, silt and clay fractions). For this last analysis, the sand fraction was obtained passing the dry sediment through a sieve of 63 mm mesh. The silt and clay fractions were determined by the wet sieving analysis described in Holme and McIntyre (1984). Salinity, pH, temperature (analogical thermometer) and transparency (Secchi disc) of the water column were also registered in situ.
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was used to reduce the irrelevant explanatory factors susceptible to decrease the precision of the estimated coefficients and predicted values. The APS procedure fits all regressions involving one factor, two factors, three factors and son on. Then, selection criterion is recorded for each single regression test. Once the procedure finishes, the model for each variable subset is shown. The optimum subset of factors to be used in the multiple regression models is determined when the r-square values stabilize. 3. Results 3.1. Physical habitat factors
Fig. 1. Position of the sampling sites along the estuarine gradient in the Celestun coastal lagoon.
Additionally, dissolved oxygen was measured following the Winkler titration method (Parsons et al., 1984). 2.3. Data analysis Abundance (N. Ind. 0.25 m2), species richness (species number), species diversity (H0 ), and evenness (J0 ) were the four characteristics used to assess the spatial and temporal variability trends of the benthic community. Two-way ANOVAs were used to test for differences in the physical habitat factors and community characteristics among sampling sites and sampling seasons. When the normality assumption of the variables was not satisfied, the Kruskal–Wallis nonparametric test was carried out. The spatial resemblance in the habitat physical factors was described on a seasonal basis using the unweighted arithmetic average clustering (UPGMA). Cluster groups were obtained using a 50% similarity threshold value. Next, an ordination in reduced space procedure by principal component analysis (PCA) was used to determine the relationship among physical and biological variables. Multiple regression analysis was performed in order to obtain the best physical factors explaining the seasonal benthic community characteristics. Previous to the application of this last analysis, the ‘All possible regressions procedure (APS, NCSS 1999)’
Water salinity, sediment salinity, sand and silt were the factors that showed significant differences among sampling sites and sampling seasons. Organic matter and clay, on the contrary, showed significant differences only among sampling sites. Transparency showed significant differences among seasons. Finally, dissolved oxygen, pH and porosity data did not show significant differences neither in space or time (Tables 1 and 2). As expected water and sediment salinities increased seaward (Fig. 2c), while porosity and pH kept steady along the estuary gradient (Fig. 2a and d). The rest of the factors did not show any definite trends of variation. Cluster analysis, on the basis of the physical habitat factors, showed that the lagoon is structured in two main zones (Fig. 3). Roughly, the first zone corresponds to the sampling sites located in the inner and middle zones (sampling sites 1–8), and the second one corresponds to the sampling sites located in the seaward zone of the estuary gradient (sampling sites 9–12). This sampling sites array was better defined during the rainy and dry seasons; in the nortes season, the ecological resemblance among contiguous sampling sites tended to be not so clearly ordered. Modifying the similarity criterion from 50% to 70% permitted to observe three clusters of sampling sites located in the inner, middle and seaward zones of the estuary gradient; here again, this sampling sites array was more defined during the rainy and dry seasons. 3.2. Benthic community characteristics One hundred and five infaunal species were observed along the estuarine gradient during the fourth sampling periods. The most abundant taxa
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Table 1 Mean values of physical factors by sampling season
Organic matter (%) Dissolved oxygen (mg l1) Sand (%) Silt (%) Clay (%) Transparency (cm) Porosity (%) Water salinity Sediment salinity Sediment pH
Rainy 1994
Nortes 1994
Dry 1995
Rainy 1995
17.7 8.13 23.7 36.1 40.6 40 76.7 24.7 20.5 7.68
17.5 7.79 30.6 31.6 37.7 30.83 78.8 21.3 18.7 7.64
19.9 9.00 38.1 22.8 39.1 62.6 78.3 26.8 32.4 8.12
15.6 6.71 34.5 27.4 37.8 36.1 81.0 15.3 14.5 7.79
(2.76) (3.47) (17.2) (6.6) (13.3) (14.45) (7.63) (6.31) (6.46) (0.09)
(5.54) (2.07) (19.8) (7.72) (12.6) (12.9) (5.26) (0.24) (5.54) (0.24)
(11.6) (2.20) (25.8) (10.2) (19.5) (21.8) (8.34) (8.81) (5.89) (1.08)
(4.66) (0.77) (22.6) (9.73) (15.4) (14.7) (5.49) (6.85) (6.06) (0.20)
Number in parenthesis represents 71 S.D.
Table 2 Two-way ANOVAs (F) and Kruskal–Wallis (H) tests used to look for differences in physical habitat and benthic community characteristics as function of sampling site and season Site (A)
Season (B)
AB
Physical factor Organic matter (%) Sand (%) Silt (%) Clay (%) Transparency (cm) Dissolved oxygen (mg l1) pH Water salinity Sediment salinity Porosity (%)
F11,33 ¼ 1.95 F11,33 ¼ 28.08 F11,33 ¼ 6.91 F11,33 ¼ 17.89 F11,33 ¼ 0.80 H11,96 ¼ 9.21 H11,96 ¼ 12.71 H11,96 ¼ 24.81 H11,96 ¼ 19.78 H11,96 ¼ 2.93
F3,33 ¼ 0.86 F3,33 ¼ 6.90 F3,33 ¼ 11.54 F3,33 ¼ 0.31 F3,33 ¼ 8.38 H3,96 ¼ 7.45 H3,96 ¼ 2.51 H3,96 ¼ 11.43 H3,96 ¼ 23.74 H3,96 ¼ 3.21
F11,33 ¼ 6.74 F11,33 ¼ 3.53 F11,33 ¼ 2.07 F11,33 ¼ 3.10 F11,33 ¼ 2.09
Community characteristic Diversity (H0 ) Evenness (J0 ) Richness (species number) Abundance (N. Ind. 0.25 m2)
F11,33 ¼ 11.68 F11,33 ¼ 2.24 F11,33 ¼ 6.71 F11,33 ¼ 2.90
F3,33 ¼ 6.16 F3,33 ¼ 7.43 F3,33 ¼ 12.98 F3,33 ¼ 0.96
F11,33 ¼ 1.78 F11,33 ¼ 1.62 F11,33 ¼ 3.62 F11,33 ¼ 6.19
Term significant at alpha ¼ 0.05.
were Mollusca (40.4%), Polychaeta (29.4%) and Crustacea (25.8%). Echinodermata, Clitellata, Sipunculida and Nemertea represented together the remaining 4.3%. Species richness (Fig. 4a), species diversity (Fig. 4b) and, to a lesser extent, species evenness (Fig. 4c) increased from the inner to the seaward zone, while abundance (Fig. 4d) showed the opposite trend. The two-way ANOVAs showed that in almost all the cases, these community characteristics differed significantly among sampling seasons and sampling sites. Evenness was the sole characteristic that did not show significant differences among sampling sites and abundance was the sole one that did not show significant
differences among sampling seasons (Table 2; Fig. 4c and d). The highest values for species diversity and richness for the entire sampling area were registered during the 1995 dry season. The lowest values were registered in the 1994 nortes season. Highest and lowest values of evenness did not occur consistently during any particular season. Abundance presented similar values during the four sampling seasons as shown in the two-way ANOVAs. The composition of the major taxonomic groups showed significant changes among sampling sites (F ¼ 14.50, p ¼ 0.00) and sampling seasons (F ¼ 12.95, p ¼ 0.00). Polychaeta was the most dominant group during the two rainy seasons and
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Fig. 2. Spatial variability of organic matter, porosity (a), sediment texture (b), salinity (c), pH (d), dissolved oxygen (e), and water transparency (f) in the Celestun coastal lagoon. Histogram bars represent 71 S.D.
Fig. 3. UPGMA cluster analysis of the sampling sites in each season. Benthic habitat characteristics were used to associate the sampling sites. Cluster groups were obtained using a 50% similarity threshold value.
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Fig. 4. Spatial and seasonal variability of species richness (a), species diversity (b), abundance (c), and evenness (d) in the Celestun lagoon. Histogram bars represent 71 S.D.
Fig. 5. Spatial and seasonal variability of abundances of the major taxonomic groups in the Celestun lagoon. Histogram bars represent 71 S.D. The abundance of ‘‘Others’’ comprises Echinodermata, Sipunculida, Nemertea, and Clitellata pooled together.
Mollusca during nortes, while in the dry season not a dominant group was apparent (Fig. 5). Crustacea was the second dominant group during all seasons,
showing a higher stability than the all other groups. Even if all groups showed high temporal variability, Polychaeta was the only group almost disappearing
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during the nortes season (Fig. 5). On the whole, stations located in the inner zone showed higher abundances than the ones situated in the middle and seaward zones. The middle zone exhibited higher abundances than the other zones only during the 1994 rainy season. No group presented a clear trend of dominance for a particular zone, excepting perhaps Mollusca that were mostly limited to the inner lower salinity zone.
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3.3. Relationship among physical and biological characteristics The principal component analysis shows that in all cases, the first two principal components accounted for more than 90% of the variance (Fig. 6). The overall dispersal of physical and biological variables in the reduced space, shows that for all seasons and along the first principal
Fig. 6. Results from principal component analysis per climatic season. In all cases, the first two components accounted for more than 90% of the variance in the multivariate reduced space. OrMa, organic matter; WaSa, water salinity; SeSa, sediment salinity; Poro, porosity; DiOx, dissolved oxygen; Trans, transparency; Abund, abundance; Rich, species richness; Dive, species diversity, Evenn, species evenness.
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component, the species diversity measures (strongly and negatively related to water salinity, sediment salinity and, to a lesser extent, sand), were spatially discriminated from abundance (not clearly related in turn to any physical factor, excepting perhaps organic matter during the 1994 rainy season). On the contrary, for all seasons and along the second principal component, species evenness was clearly discriminated from species diversity, species richness and abundance. Along this principal component, species evenness was weakly and positively related to water salinity, sediment salinity and, to a lesser extent, pH in nortes 1994 and dry 1995, and unrelated to any other physical factor in the two remaining seasons. No more than two factors were retained by the multiple regression models in each sampling season (Table 3). In models in which only one factor was retained, these ones explained up to 58% of the observed variance. In the cases where two factors were retained, these ones explained more than 60% of the observed variance. Species diversity was better explained by water salinity alone or in
combination with porosity (rainy 1994) or sand (nortes 1994). In the meantime, species richness was better explained by silt in most seasons, but by clay in the nortes 1994 season. In an analogous way, abundance was better explained by the combination of water salinity and sediment salinity but only in the nortes 1994 and dry 1995 seasons. In the rainy 1994 and 1995 seasons, there were no factors retained by the models for explaining abundance. 4. Discussion Benthic community characteristics are expected to vary in keeping with spatial and seasonal variability. However, results do not totally sustain this assumption. Data analysis showed that for the period of study Celestun coastal lagoon was more heterogeneous along the spatial axis of variability than along the temporal one. Spatially salinity was the main factor influencing the benthic community characteristics. Temporally, the physical habitat characteristics were observed to exert significant effects on the species diversity measures but not on
Table 3 Multiple regression analysis per sampling season
Rainy 94
Diversity Richness Evenness Abundance
‘‘Nortes’’ 94
Diversity Richness Evenness Abundance
Factor
Slope
r2
SS
F
p
Water salinity Porosity Water salinity Silt Sediment salinity Porosity ——
+ + + + + + ——
0.66 0.13 0.25 0.48 0.36 0.22 ——
1.44 1.70 64.29 12.56 0.11 0.96 ——
9.13 11.27 12.85 9.45 5.38 4.09 ——
0.00 0.04 0.00 0.02 0.00 0.03 ——
Water salinity Sand Clay Water salinity Water salinity Sediment salinity
+ + + +
0.28 0.32 0.40 0.58 0.30 0.44
0.91 1.04 48.92 4.43 4.60 6.64
11.14 4.85 6.07 11.03 3.64 21.31
0.01 0.00 0.01 0.00 0.00 0.00
Dry 95
Diversity Richness Evenness Abundance
Water salinity Silt pH Water salinity Sediment salinity
+ +
0.47 0.48 0.54 0.33 0.27
1.52 58.26 0.18 4.99 4.09
9.12 9.26 5.63 3.31 10.06
0.02 0.03 0.00 0.02 0.00
Rainy 95
Diversity Richness
Sediment salinity Silt Sediment salinity Sand ——
+ + ——
0.48 0.48 0.19 0.50 ——
1.54 59.81 23.73 0.34 ——
6.22 4.25 3.98 4.90 ——
0.04 0.00 0.04 0.00 ——
Evenness Abundance
Regression models include the combination of factors that best accounted for the variation of each community characteristic. Only the significant results are showed (po0.05).
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abundance. Macrofauna responded to environmental variability by modifying the dominance relationships of the major taxonomic faunistic groups present in the community. Along the spatial axis of variability, Mollusca was the most abundant group in the inner zone during all seasons. Polychaeta, when present, was dominant in the middle zone, while in the seaward zone, no dominant group was present. Along the temporal axis of variability, Mollusca was dominant during both the nortes and dry seasons, and Polychaeta was the dominant one during the rainy season. Crustacea was the second dominant group during the whole period. The most remarkable feature of this dynamic scenario was the disappearance of Polychaeta during the nortes season, with a recovery in abundance throughout the rainy season, suggesting thus that this group respond sensibly to natural environmental disturbances. Dissolved oxygen, porosity and pH were the three factors that did not show significant differences along the temporal axis of variability. The karstic characteristic of the site probably acts as a buffer mechanism to maintain stable the mean values of pH. Constancy in porosity (percentage volume of pore space) indicates that texture and hydraulic conductivity of sediment kept roughly steady during the study period. Dissolved oxygen, usually variable both spatially and temporally (Herrera-Silveira et al., 2002), kept relatively steady during the whole period of interest. Rainfall in the study area, in addition to vary seasonally, varies also on a yearly basis. The data used in this study were obtained just after one of the most severe dryness periods recorded in the area during the last quarter century (Fig. 7). The relatively high and seasonally even values of dissolved oxygen probably denote the
Fig. 7. Historical annual mean precipitation in Celestun area. Dotted line represents 71 S.D.
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influence of the recovery period during which rainfall increased, illustrating by this mean the climatic forcing to which the study site is exposed. 4.1. Spatial variability trends The analysis of the data sustains the view that the species diversity measures and abundance mainly respond to changes in the salinity gradient of the lagoon (Nicolaidou et al., 2006). However, whereas species diversity and species richness correlated positively with salinity, abundance did the opposite. It has been already argued that salinity is the most important factor affecting submerged aquatic vegetation and shrimp abundance distribution in the Celestun coastal lagoon (Pe´rez-Castan˜eda and Defeo, 2003). This fact seems also true for the overall invertebrate benthic community and it is in the middle zone of the lagoon that the effects of this factor become more apparent. The middle zone corresponds to a mixed portion of the lagoon characterized by intermediate values of water salinity (Pe´rez-Castan˜eda and Defeo, 2003) and sediment salinity (this study). The main inflexion points in species diversity and species richness (increase), as well as in abundance (decrease) along the estuarine gradient occur precisely in this zone (Fig. 4). Whereas the lowest species diversity and species richness (higher dominance) observed in the inner zone could be associated with the natural physical stress prevailing in the freshwater zone (Arias and Drake, 1994), the lowest abundance (higher evenness) observed in the seaward zone could be associated with the increase in predation pressure of organisms that rely on benthic species as its principal food resource (juvenile shrimps, fishes), at least on a seasonal basis (Pe´rez-Castan˜eda and Defeo, 2005; Vega-Cendejas, 2003). The most abundant species observed in the inner zone were those that can tolerate low salinity values such as Assiminea succinea (Gastropoda), Hargeria rapax (Tanaidacea) and Leitoscoloplos fragilis (Polychaeta). In addition to salinity, benthic communities from coastal lagoons are deeply influenced by the granulometric characteristics (Beukema and Flach, 1995) and organic matter content (Jayaraj and Jayalakshmi, 2007) of sediment. The sediment of sampling sites 1–8 (Fig. 1) contained a major proportion of clay and silt. In the last four sampling sites, located in the seaward zone, the sediment was predominantly sandy, with a lesser proportion of
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silt and clay (Fig. 2b). Results from PCA and multiple regression analysis showed that sediment texture was the second more important factor explaining species diversity and species richness variance (Table 3; Fig. 6). Multiple regression analysis showed that species diversity was positively correlated with porosity and sand while species richness was mostly negatively correlated with silt and clay. Organic matter content did not appear to be related to any benthic community characteristic, probably because over time it was relatively invariant and over space its absolute content values did not represent a limiting resource for deposit feeders but at the same time did not represent either a risk of dystrophy for the system. 4.2. Temporal variability trends The physical habitat factors did not show marked seasonal variability. After ANOVA results, organic matter, dissolved oxygen, pH, sediment porosity and clay did not show significant differences among sampling seasons. The same result was obtained on the mean values of species abundance. In addition, none of the physical habitat factors mentioned above was retained in the regression models to explain abundance variability. On the contrary, it was observed that water salinity and sediment salinity were the factors affecting negatively abundance but only during the dry and nortes seasons. This suggests that for these factors and seasons, a feedback mechanism regulating abundance was underway, probably via the presence of marine predators entering the lagoon when the freshwater outflow was low or when the salt water entrance was forced during storm events. A critical aspect to be considered when examining the temporal variability in the benthic community response to environmental changes is that of sampling design in relation to scale. If environmental change and the subsequent temporal response of the benthic community occur at temporal scales shorter than our temporal sampling resolution (seasonal), these could get stabilized by the resilience of the system and pass unnoticed. For certain processes, the opposite is also susceptible to occur. Gonneea et al. (2004), tracing organic matter in mangrove sediments over the past 160 years, suggest that major fluctuation in the entire Celestun lagoon occurs at temporal scales higher that 10 years, a period much larger that the one examined in this study.
Water salinity, sediment salinity, as well as s and and silt sediment fractions, varied significantly on a seasonal basis (Table 2). After the multiple regression analysis, these four factors appeared responsible for the seasonal variability observed in species diversity and species richness, whose maximum values were observed during the dry season (Fig. 4). In keeping with these results, the lowest species diversity and species richness were expected to occur during the rainy season when salinity decreases due to the freshwater input and, to a lesser degree, during the nortes season when stability of the water column decrease by effect of the wind stress. In conclusion, seasonality only caused significant changes in 50% of the physical factors measured in this study. Among these, changes in salinity due to variations in the freshwater and saltwater balance seem to be the most important single factor inducing changes in the benthic community characteristics. Further studies connecting salinity to changes in this and other components of the lagoon such as fishes and submerged vegetation are needed to understand the role of salinity in this system. Effective management of the lagoon’s biological resources requires a sensitive indicator of the response to fresh or saltwater inflow that has ecological significance. Such kind of indicators has been already explored in the literature (e.g. Jassby et al., 1995) and could be profitably explored for the understanding of the dynamics of this coastal lagoon. In the last 25 years, there have been many efforts to maintain the Celestun coastal lagoon as an unaltered ecosystem. As part of these efforts, since 1979 this coastal lagoon makes part of a wildlife refuge, upgraded in 2000 to a biosphere reserve, and presently being integrated into the Mexican system of natural protected areas possessing its own management plan. However, anthropogenic activities within the lagoon and in the surrounding area have not ceased to increase during the same period. Among other threats, recent studies have reported the recurrent occurrence of harmful algal blooms in the Yucatan coastal zone caused by an increase in dissolved nutrients in the water column (Ghinaglia et al., 2004; Aranda-Cirerol et al., 2006). On the basis of the recognition of these threats, we are entitled to infer that the maintenance of the integrity of this ecosystem will be in the coming years a major challenge. It is exactly in this context that the soft bottom benthic community could be an appropriate
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tool for monitoring the habitat quality of the lagoon in the light of an increasing anthropogenic pressure on the natural resources of the nearshore coastal zone and, particularly, of this relatively healthy natural protected area. Acknowledgments We thank DUMAC (Ducks Unlimited) for providing field facilities in Celestun. Special thanks are due to the ‘Laboratorio de Bentos’ staff, Cinvestav, for field and laboratory assistance. This research was supported by funds from CONABIO to P.L.A. and a Cinvestav postodoctoral fellowship to D.P.
References Aranda-Cirerol, N., Herrera-Silveira, J.A., Comin, F.A., 2006. Nutrient water quality in a tropical coastal zone with groundwater discharge, northwest Yucatan, Mexico. Estuarine, Coastal and Shelf Science 68, 445–454. Arias, A.M., Drake, P., 1994. Structure and production of the benthic macroinvertebrate community in a shallow lagoon in the bay of Cadiz. Marine Ecology Progress Series 115, 151–167. Baldassarre, G.A., Arengo, F., Galicia, E., 1997. Habitat use and conservation of American flamingos (Phoenicopterus ruber ruber) and associated wetlands in Yucatan, Mexico. Final Report submitted to the United States and Wildlife ServiceNorth American Wetland Conservation Council and Secretarı´ a de Medio Ambiente, Recursos Naturales y Pesca, Mexico. State University of New York, Syracuse. Beukema, J.J., Flach, E.C., 1995. Factors controlling the upper and lower limits of the intertidal distribution of two Corophium species in the Wadden sea. Marine Ecology Progress Series 125, 117–126. Carr, M.H., Neigel, J.E., Estes, J.A., Andelman, S., Warner, R.R., Largier, J.L., 2003. Comparing marine and terrestrial ecosystems: implications for the design of coastal marine reserves. Ecological Applications 13, 90–107. Fuentes-Yaco, C., de Leon, D.A.S., Monreal-Gomez, M.A., 2001. Environmental forcing in a tropical estuarine ecosystem: the Palizada River in the southern Gulf of Mexico. Marine and Freshwater Research 52, 735–744. Ghinaglia, L.T., Herrera-Silveira, J.A., Comin, F.A., 2004. Structural variations of phytoplankton in the coastal seas of Yucatan, Mexico. Hydrobiologia 519, 85–102. Gonneea, M.E., Paytan, A., Herrera-Silveira, J.A., 2004. Tracing organic matter sources and carbon burial in mangrove sediments over the past 160 years. Estuarine, Coastal and Shelf Science 61, 211–227. Herrera-Silveira, J.A., 1994. Spatial heterogeneity and seasonal patterns in a tropical coastal lagoon. Journal of Coastal Research 10, 738–746.
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Herrera-Silveira, J.A., Martin, M., Diaz-Arce, V., 1999. Phytoplankton variations in four coastal lagoons, Yucatan, Mexico. Revista de Biologı´ a Tropical 47, 47–56. Herrera-Silveira, J.A., Medina-Gomez, I., Colli, R., 2002. Trophic status based on nutrient concentration scales and primary producers community of tropical coastal lagoons influenced by groundwater discharges. Hydrobiologia 475/ 476, 91–98. Holme, N.A., McIntyre, A.D., 1984. Methods for the Study of Marine Benthos. Blackwell, Oxford. Hughes, T.P., 1994. Catastrophes, phase-shifts, and large-scale degradation of a Caribbean coral-reef. Science 265, 1547–1551. Jassby, A.D., Kimmerer, W.J., Monismith, S.G., Armor, C., Cloern, J.E., Powell, T.M., Schubel, J.R., Vendlinski, T.J., 1995. Isohaline position as a habitat indicator for estuarine populations. Ecological Applications 5, 272–289. Jayaraj, K.A., Jayalakshmi, K.V., 2007. Influence of environmental properties on macrobenthos in the northwest Indian shelf. Environmental Monitoring and Assessment 127, 459–475. Nicolaidou, A., Petrou, K., Kormas, K.A., Reizopoulou, S., 2006. Inter-annual variability of soft bottom macrofaunal communities in two Ionian Sea lagoons. Hydrobiologia 555, 89–98. Parsons, T., Maita, Y., Lally, C., 1984. A Manual of Chemical and Biological Methods of Seawater Analysis. Pergamon Press, Oxford. Pe´rez-Castan˜eda, R., Defeo, O., 2003. Influence of estuarine zonation on exploited shrimp populations in a Mexican biosphere reserve: a feature for management and conservation. Journal of Marine Biology Assessment 83, 781–784. Pe´rez-Castan˜eda, R., Defeo, O., 2004. Spatial distribution and structure along ecological gradientes: penaeid shrimps in a tropical estuarine habitat of Mexico. Marine Ecology Progress Series 273, 173–185. Pe´rez-Castan˜eda, R., Defeo, O., 2005. Growth and mortality of transient shrimp populations (Farfatepenaeus spp.) in a coastal lagoon of Mexico: role of environmental and density dependence. Journal of Marine Science 62, 14–24. Powers, S.P., Peterson, C.H., Christian, R.R., Sullivan, E., Powers, M.J., Bishop, M.J., Buzelli, C.P., 2005. Effects of eutrophication on bottom habitat and prey resources of demersal fishes. Marine Ecology Progress Series 302, 233–243. Trush, S.F., Hewitt, J.E., Funell, G.A., Cummmings, V.J., Ellis, J., Shcultz, D., Talley, D., Norkko, A., 2001. Fishing disturbance and marine biodiversity: the role of habitat structure in simple soft-sediment systems. Marine Ecology Progress Series 223, 277–286. Vega-Cendejas, M.E., 2003. Trophic dynamics of a mangrove ecosystem in Celestun lagoon, Yucatan Peninsula, Mexico. Fisheries Centre Research Reports 1, 237–243. Vidal-Martinez, V.M., Jimenez-Cueto, A.M., Sima-Alvarez, R., 2002. Parasites and symbionts of native and cultured shrimps from Yucatan, Mexico. Journal of Aquatic Animal Health 1, 51–64. Walkley, A., Black, I.A., 1934. An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Science 37, 29–38.