Abstract
Landlocked lagoons are naturally stressed environments. They are strongly influenced by freshwater input which not only varies naturally, but which is also impacted by anthropogenic activities. This study investigated the direct influence of freshwater discharges on the distribution patterns and abundance of benthic communities in two neighbouring landlocked coastal lagoons, assessing the whole system and the confluence area of each tributary. Sampling occurred in the wet and dry seasons of 2011 at two distances from freshwater discharge locations. Both lagoons were colonized by species from two different pools, freshwater and marine. Freshwater flow rates had a direct influence on the spatial structure of the benthic communities of brackish-water/freshwater interface areas, where also specific taxa can act as early indicators of freshwater input variations. The intensity of this influence is highly dependent on lagoon size, creating spatial heterogeneity or affecting the entire system. The benthic fauna at the confluence of the tributary that depends almost exclusively on groundwater showed the lowest variability, suggesting that the biogeochemical nature of the groundwater may be a central cause for setting specific ecotones. The results suggest that benthic communities of landlocked coastal lagoons can be highly impacted by flow reduction from freshwater aquifers under drought conditions or water abstraction activities.
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Introduction
Coastal lagoons are highly productive brackish-water systems that provide a wide range of natural services, granting them a high level of importance, both economical and ecological (Kjerfve, 1994). Despite their significance to human societies, these are highly stressed systems that constrain the establishment of biological communities, not only due to their natural variability, but also due to the anthropogenic pressures they are exposed to. These particular characteristics require the management of these systems, which poses several difficulties (Viaroli et al., 2010) and needs scientific support. Scientific knowledge on coastal lagoons has been increasing, but mostly focused on open lagoons, leaving a gap as to the functioning of lagoons that are closed, i.e. that have short period or no connection to the adjoining sea, termed as landlocked or enclosed lagoons (Bamber et al., 2001; Beer & Joyce, 2013). This knowledge gap is particularly significant with regard to the factors that modulate the dynamics of the system and how they affect the biological communities and, more importantly, if those factors are subject to human exploitation, like water abstraction activities (Correia et al., 2012; Félix et al., 2013a).
Landlocked coastal lagoons are typically shallow and confined brackish-water systems at the interface between the continent and sea (Healy, 2003), highly dependent on freshwater discharges, either from run-off or groundwater. Freshwater inputs, which vary naturally in their flow rates and biogeochemical characteristics, are important drivers for the settlement and structure of biological communities of these enclosed systems (Cancela da Fonseca et al., 2001a; Basset et al., 2006; Cañedo-Argüelles & Rieradevall, 2010). However, the level of their impact is also highly dependent on the morphological characteristics of each lagoon, such as the surface area or depth (Basset et al., 2006; Cañedo-Argüelles & Rieradevall, 2010). Thus, each lagoon can have its particular traits and biological role. Most studies on enclosed lagoons have focused mainly on the nutrient enrichment provided by freshwater sources and very little on the direct impact on the ecosystems and biological communities. Although it has been suggested that freshwater inputs can have a high impact in the settlement and composition of biological communities (e.g. Cañedo-Argüelles & Rieradevall, 2010), no information on the direct influence and impact on the stream/lagoon interface areas is available. Hence, the biodiversity in different confluence areas (different streams can discharge into a single lagoon) might be influenced by the biogeochemical processes due to freshwater discharge. This influence is expected to decrease gradually with increasing distance from the confluence, due to the dilution effect of brackish water. The hydraulic management of these basins and groundwater exploitation policies are particularly difficult to manage due to the lack of knowledge on the influence of freshwater inputs into the lagoonal system and its ecological susceptibility (cf. Smith, 1994). This may be particularly relevant in years of drought or heavy rainfall and in medium- and long-term scenarios of reduced rates of aquifer recharge, caused by increasing effects of climate change.
Enclosed lagoons are also the final reservoir of continental watershed material, which is transported by freshwater and accumulate. This adds to the lagoons own decay products, due to active beach ridges, resulting in high primary production conditions and consequent eutrophication (see Beer & Joyce, 2013). These phenomena lead to a natural ageing process in most landlocked coastal lagoons, i.e. towards eutrophicated freshwater ponds (Heydorn & Tinley, 1980). In some Portuguese SW coastal lagoons this process is prevented by man-made openings of the sand barrier, typically conducted once a year, according to management decisions. The opening connects the lagoons to the sea promoting the export of nutrients and organic matter and the modification of physical, chemical and biological conditions (Cancela da Fonseca et al., 2001a; Costa et al., 2003). On the other hand, freshwater discharges are the main water input during the isolation period from the sea. This freshwater input is important for setting ecotones in enclosed lagoons, by influencing parameters like salinity, sediment type or organic matter. Additionally, it determines the colonization of the lagoon by freshwater species, particularly benthic invertebrates (Cancela da Fonseca et al., 2001a; Basset et al., 2006; Oyedele & Momoh, 2009; Cañedo-Argüelles & Rieradevall, 2010).
Benthic macroinvertebrates play an important role in the metabolism of aquatic ecosystems and are a key biological group in the energy flow of these brackish-water systems (Casagranda et al., 2006). The marine colonization of landlocked coastal lagoons with periodic openings to the sea occurs essentially during these openings, after which diversity is mainly determined by the plasticity of the species, based on their tolerance to variations of environmental factors. The colonization by freshwater macroinvertebrate species, mainly aquatic insects, also occurs in these lagoons and depends mostly on less constant abiotic factors, like salinity, which varies considerably on both temporal and spatial scales (Cancela da Fonseca et al., 1989; Correia et al., 2012; Beer & Joyce, 2013; Félix et al., 2013a).
This study addressed the influence of freshwater inputs and associated environment on the distribution and abundance of macroinvertebrates in two neighbouring enclosed coastal lagoons, located in the southwest region of Portugal. The hypotheses tested are the following: (1) there were differences in the structure of benthic communities between freshwater confluence areas and the lagoonal environment; (2) there was temporal variation (between wet and dry seasons) of benthic communities within confluence areas—both testing the spatial distribution patterns of the benthos, as a consequence of freshwater inputs—and (3) there were differences in the abundance of individual species/taxa between freshwater confluence areas and the lagoonal environment—the latter hypothesis will identify which specific species or taxa can be early indicators of freshwater input variations within these interface areas.
Differences in the benthic communities and individual taxa between the confluence areas and lagoonal environments are expected to occur in both lagoons, particularly marked after the wet season, due to increased freshwater inputs (groundwater and run-off). The reduced freshwater flow during the dry season should allow a brackish-water intrusion into the confluence areas, increasing the similarities between both areas. Understanding if freshwater has an influence on the biological communities is of particular importance in groundwater-dependent systems, tributaries that commonly sustain human exploitation through water abstraction activities.
Materials and methods
Study area
Melides (38°08′N, 8°47′W) and Santo André (38°6′N, 8°48′W) are small coastal lagoons—with an average area of 0.4 and 2.5 km2, respectively—located in the southwest of continental Portugal (Fig. 1), 2.5 km apart, with catchment areas of 63 and 96 km2, respectively. Melides Lagoon has one major tributary, the Melides stream, and an adjacent groundwater outflow, Unnamed outflow, while three major tributaries, namely Badoca/Ponte, Serradinha and Cascalheira streams, and an adjacent groundwater outflow, Caniços outflow, discharge into Santo André Lagoon. Most tributaries depend on base flow and on the top detritic layer of the Sines aquifer system. In addition, the Melides stream is highly dependent on the deep carbonate aquifer (Monteiro et al., 2008). Both lagoons are isolated from the sea (Atlantic Ocean) by sand barriers, except for a short period, during early spring (coinciding with the end of the rainy season), when the connection to the sea is artificially made by the opening of an inlet in the sand barrier. Brief periods of sea-lagoon connection can also occur during occasional sand-barrier overwash episodes, which may not occur every year, but are typical of the late summer/early autumn spring tides (after the dry season). The inlet, which persists for a variable period (a few days to a few weeks) until its sealing off by waves and currents, provides the main exchange pathway between the lagoons and the sea allowing discharge of retained materials and recruitment of marine species (Cancela da Fonseca et al., 1989; Costa et al., 2003). In 2011, during which the present study was made, Melides Lagoon remained open for 3 days in April and Santo André Lagoon remained open for 56 days, between March and May. At least one overwash episode was reported for each lagoon, during a spring tide in late August 2011.
Sampling
Sampling was carried out twice during the closed period of each lagoon, in May (end of wet season) and September (end of dry season) 2011, corresponding to two periods of the same hydrological year, with different environmental conditions. The location of known freshwater discharges was termed as Confluence. In the Melides Lagoon, there are two known Confluences: Melides stream and an Unnamed outflow, and in Santo André Lagoon, there are four: Badoca, Serradinha and Cascalheira streams, and Caniços outflow (Fig. 1). Sampling was conducted at two distances from the freshwater discharge point, specifically 50 m from freshwater discharge (FW) and 200 m from the freshwater discharge (LG) (depicted in Fig. 1). This experimental design assumed that benthic communities were directly influenced by freshwater at FW sites and not directly influenced by the freshwater inputs at LG sites.
Three random replicates were collected at each sampling station (site) using a van Veen grab (0.05 m2). The samples were sieved in situ with a 500-μm mesh sieve, and subsequently fixed in a 4% formalin solution buffered with borax and stained with Rose Bengal. In the laboratory, samples were rinsed to remove excess formalin and sediment, the organisms were hand sorted into major taxonomic groups and preserved in 70° ethanol. All specimens were identified to the lowest possible taxonomic level (frequently species level) and counted. Several environmental parameters were measured in the water, namely bottom temperature, dissolved oxygen (DO), total dissolved solids (TDS), pH and salinity, during each sampling event and at each sampling station, using a multi-parametric sonde. Bottom water samples were also collected at each site using an adapted horizontal van Dorn water sampler for the determination of nutrient (NO3, NO2, NH4, P, PO4) and chlorophyll a (Chla) concentrations. The Chla was determined by Spectrophotometry, using the method by Lorenzen (1967) and nitrates, nitrites and ammonium by Segmented Flow Analyser using the Skalar continuous flow system (autoanalyzer) (Grasshoff et al., 1983). The orthophosphate concentration was measured through colorimetry using the ascorbic acid method (Grasshoff et al., 1983). All analyses were run by the accredited laboratory of Administração da Região Hidrográfica do Alentejo.
Additional grab samples were collected at each site for determination of total organic matter (TOM), which was obtained by loss on ignition (480°C), and sediment grain size. The latter was determined using 63 µm to 2 mm sieves to separate, respectively, the silt–clay, sand and gravel fractions. Each fraction was dried and weighed, and sediments assorted according to their percentages and classified with Shepard diagrams. Sediments were then grouped as follows: Mud < 63 µm; 0.063 mm ≤ Muddy sand/Sandy mud < 0.2 mm; 0.2 mm ≤ Sand < 2 mm; Gravel > 2 mm, following the classification system adopted in the sediment charts of the Portuguese Navy Hydrographic Institute (Moita, 1985).
Data analysis
The spatial and temporal differences in benthic macroinvertebrate communities were assessed using a Permutational Analysis of Variance—PERMANOVA (Anderson, 2001), with four factors: Lagoon (fixed with two levels, Melides and Santo André), Period (fixed with two levels, May and September), Distance (fixed with two levels, FW and LG) and Confluence (each FW/LG pair) nested in Lagoon (random with two levels in Melides Lagoon: Melides stream and Unnamed outflow; and with four levels in Santo André Lagoon: Badoca, Serradinha and Cascalheira streams and Caniços outflow) (see Fig. 1). The abundance data was log (X + 1) transformed and Bray-Curtis similarity coefficient was used as a resemblance measure. The Monte Carlo permutations (P(MC)) were used whenever there were not enough possible permutations (number of possible permutations <100) to get a reasonable test in PERMANOVA. The PERMDISP routine tested the dispersion of the data and the Pair-Wise tests were run as a posteriori comparisons of levels for single factors, in the case of significant interactions or significant main effects. The SIMPER routine was used to identify which taxa and environmental variables (normalized) provided discrimination between any differing factors, with a cut-off level selected wherever the individual contribution of variables was higher than 10% or at a major leap between high and low percentage of individual contribution. A multi-dimensional scaling (MDS) ordination was performed using benthic abundance data, and environmental variables most likely to influence the benthic structure were superimposed on the MDS (bubble plots). All statistical analyses were run in Primer 6 + PERMANOVA (Clarke & Gorley, 2006; Anderson et al., 2008).
A non-parametric Wilcoxon test was used to analyse differences in each species’ abundance between sampling sites located closer to the freshwater discharges (FW) and those located farther apart (LG), using Statistica v11 (Statsoft®). These tests were run independently for each lagoon and each sampling period.
Results
A total of 78799 macroinvertebrate specimens of 80 different taxa was collected, 32 in Melides Lagoon and 68 in Santo André Lagoon, with 20 taxa common to both systems (Table 1). Most consisted of typical lagoonal taxa and Chironomidae, Ostracoda, Peringia ulvae, Oligochaeta, Lekanesphaera hookeri and Abra segmentum, accounted for about 90% of the total average abundance observed in both lagoons.
In Melides Lagoon, 24 taxa were recorded in May and 18 in September, with 10 common taxa between periods and with most Insecta families occurring only in September. Thus, there was a species reduction and also a shift in community composition (described below) between sampling at the end of the wet and dry seasons, and hence between periods, differing according to freshwater input. A similar trend was observed in Santo André Lagoon, with 49 and 42 taxa registered, respectively in May and September and with 23 common taxa between periods. Several marine Bivalvia species were registered exclusively in this lagoon and only in May, just after the closure of the inlet (see Table 1), all of which were only present in the downstream area of the lagoon.
The MDS ordination of the biological assemblages indicates a clear separation between the benthic communities of both lagoons (Fig. 2a), corroborated by the PERMANOVA results (Table 2). Up to 74% of the dissimilarity between lagoons was explained by (i) the exclusive occurrence of A. segmentum and Desdemona ornata in Santo André; (ii) higher abundance of Oligochaeta and Peringia ulvae in Santo André and; (iii) higher abundance of Ostracoda, Chironomidae, Lekanasphera hookeri and Hediste diversicolor in Melides(SIMPER analysis). Environmental variables that most discriminated the two lagoons (up to 80%, SIMPER results) were salinity, temperature and percentage of gravel, all higher in Santo André Lagoon; and depth, percentage of mud (negatively correlated to % of gravel) and total orthophosphate (PO4) concentration, higher in Melides Lagoon (Fig. 2).
The PERMANOVA results also showed a significant interaction between the factors Period, Distance and Confluence (Table 2). The PERMDISP routine indicated that the significance found in the interaction of factors is not the result of heterocedasticity (P(perm) = 0.352). The Pair-wise tests performed within this interaction to factors Period and Distance have shown that the benthic communities of Melides Lagoon did not vary significantly between periods in any of the sampling sites (either FW or LG). However, in Santo André Lagoon, significant variations between wet and dry seasons were found in all FW and LG sites, except in Badoca LG. In this lagoon, there were several taxa that explained this dissimilarity (up to 74%, SIMPER results) and that were more abundant in September, namely A. segmentum, Oligochaeta, Ostracoda, D. ornata, Chironomidae, P. ulvae, Polydora cornuta and Cerastoderma glaucum. The environmental conditions showing a variation between wet and dry seasons at Santo André Lagoon were Chla, TOM and Gravel showing higher values in May (wet season), while DO was higher in September (dry season) (up to 73%, SIMPER results).
In Melides Lagoon, no effect of freshwater was found, as there were no differences in the benthic communities between FW and LG sites. In Santo André Lagoon, there were significant differences between FW and LG in two confluence areas, the Caniços outflow (p < 0.04) and the Serradinha stream. However, in the latter these differences were only evident in May (P = 0.009). Although in the Caniços outflow there were consistent differences between FW and LG, the species that explained those dissimilarities (75%, SIMPER results) fluctuated. In May, the Caniços LG site showed higher abundance of D. ornata, P. ulvae, Foraminifera, Harpacticoida, Cerastoderma edule, A. segmentum and Chironomidae, while FW showed higher abundance of C. glaucum. On the other hand, in September, LG showed higher abundances of Oligochaeta, P.cornuta, Capitella capitata, P. ulvae, Ostracoda, Harpacticoida and C. glaucum and FW of Chironomidae. The differences between FW and LG concerning the Serradinha stream (in May) are explained by the higher abundance of Chironomidae, P. ulvae, Ostracoda, Gammarus chevreuxi in FW and A. segmentum in LG. In the Caniços outflow, that showed consistent biological differences, the most important abiotic parameters discriminating sites were depth, DO and temperature, all higher in FW (up to 94% of SIMPER results).
The lagoonal bivalve A. segmentum was the taxon with a more consistent presence and higher abundance at LG sites. Most taxa that gave higher contributions to dissimilarities found between different periods (from the SIMPER results), varied considerably on a spatial and temporal scale. The taxa Ostracoda, P. ulvae and Chironomidae had their highest abundance either in LG or FW sites, depending on the season.
Wilcoxon tests showed that there were significant differences in the abundance of individual taxa between FW and LG sites, as listed in Table 3. In Melides Lagoon, differences were only found in May for H. diversicolor and Ostracoda, which were more abundant in LG locations while in Santo André Lagoon there were significant differences for Chironomidae and P. cornuta in September, which were more abundant in FW and LG locations, respectively.
Discussion
The present study indicates that freshwater inputs influence the structure of benthic communities and spatial distribution of specific taxa, but that influence seems to depend on the characteristics of the lagoonal system, i.e. significant differences between FW and LG occurred, but only in Santo André lagoon. Although both studied lagoons are neighbouring systems, their benthic communities are dissimilar, suggesting that specific morphological and dynamic characteristics of each lagoon might determine the settlement of different species. Corroborating previous studies, benthic communities, as well as other biological groups, seem to be particularly dependent on the lagoon size (Félix et al., 2013a, b), where smaller lagoons show less evident macrobenthic zonation, as found in Melides Lagoon (see also Cancela da Fonseca et al., 2001b; Félix et al., 2013a). In these smaller enclosed systems occasional phenomena like heavy or abrupt freshwater inputs can have a widespread effect across the entire system. Santo André lagoon, on the other hand, appears to buffer freshwater input and displays a certain degree of zonation (e.g. Elliott & Whitfield, 2011; Correia et al., 2012; Félix et al., 2013a, b).
Seawater intrusion into landlocked lagoons allows the colonization of marine species and, hence, potentially modifies the influence of freshwater input. After the wet season, seawater entered the lagoon through the artificial opening and in late summer through an overwash episode. During the former there is persistent influence and a high input of seawater whilst, in the latter, seawater intrusion is occasional and has a lower input. Thus, one might expect a higher pressure of marine tidal forces on the confluences in May. However, this was not the case. After the rainy season (in May) freshwater taxa (e.g. Chironimidae, G. chevreuxi) expanded further into the Santo André lagoonal environment (LG) despite the opening of the sand barrier. In contrast, a large portion of marine/brackish taxa was found in September, (from the overwash) and the presence of freshwater taxa was more confined to FW areas. This indicates that freshwater flow rate is the main factor determining the extent to which seawater incursion affects community structure. In summary, the temporal shift in the community composition suggests that stream/lagoon interface areas are dynamic and dependent on freshwater flow rates. This may allow freshwater species to colonize areas further into the lagoon or be more confined to confluence areas, depending on the higher or lower freshwater flow rate, respectively.
Like the freshwater flow rate, the geochemical nature of freshwater input can also affect several other key parameters such as nutrients, Chla and silicates (Duarte et al., 2006; Medina-Gómez & Herrera-Silveira, 2006; Young et al., 2008). The structure of the benthic community in the Caniços outflow, opposing other tributaries, showed no variation between periods. This singularity could likely be related to the biogeochemical nature of the freshwater, as it is the only tributary whose flow depends almost exclusively on groundwater, potentially contributing for the establishment of specific ecotones.
The analysis of individual taxa, support the hypothesis that some taxa may be good early indicators of flow rate changes. Some of the species with marine affinities, like H. diversicolor and P. cornuta, were generally more abundant in LG sites while Chironomids, typical of freshwater habitats, were more abundant in FW areas. Although also significant in this analysis, considerations about the Ostracoda distribution would require identifications to the species level, to determine their optimal habitat type, as this group can cover a relatively wide range of ecotones (e.g. Loureiro et al., 2009; Martins et al., 2010). The fact that these differences for individual taxa were found in May for Melides and September for Santo André Lagoon is consistent with the results obtained for the spatial distribution of the benthic community in both lagoons, suggesting that these were the most heterogeneous periods in each lagoon. This pattern enhances the higher heterogeneity of a small lagoon (Melides) after inlet opening and higher patchiness of a wider lagoon (Santo André) after the dry season. Again, a reduction in the flow rate of tributaries seems to reduce the area under the effect of freshwater modifying the distribution boundaries for several species.
The present results showed that, like in open brackish systems, such as estuaries (Silva et al., 2012), the structure of benthic communities is strongly associated and dependent of freshwater inputs. Thus, and although additional information is required to quantify this relationship, it is reasonable to consider that unsustainable groundwater abstraction can have a strong impact on the biological communities of enclosed lagoons. Considering the fact that groundwater is subject to human exploitation, future research should aim to understand the real ecological importance of these systems, as it may require specific exploitation policies. Additionally, severe reductions in freshwater flow rate may cause sea water intrusion, with strong effects on the interface areas (Oyedele & Momoh, 2009) and, like any other abrupt environmental shift in a system, may impair the ecosystem dynamics.
It is therefore recommended that the exploitation of the aquifers ensure a sustainable management, particularly in years of drought that can be aggravated in the medium- and long-term by the effects of climate change (Klein Tank & Können, 2003). In conclusion, a science-based groundwater management of groundwater-dependent ecosystems, such as enclosed lagoons, is particularly relevant for the sustainability of these sensitive habitats.
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Acknowledgments
The authors acknowledge the research funding of the project GroundScene—“Modeling scenarios of exploitation in coastal aquifers: effects on biodiversity of lagoons and their streams as groundwater dependent ecosystems” (PTDC/AAC-AMB/104639/2008), the Strategic Project (PEst-OE/FIS/UI0275/2011) and the Post Doc fellowship SFRH/BPD/29579/2006 all funded by FCT (Fundação para a Ciência e Tecnologia).
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Félix, P.M., Correia, M.J., Chainho, P. et al. Impact of freshwater inputs on the spatial structure of benthic macroinvertebrate communities in two landlocked coastal lagoons. Hydrobiologia 758, 197–209 (2015). https://doi.org/10.1007/s10750-015-2290-5
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DOI: https://doi.org/10.1007/s10750-015-2290-5