Nutrient retention in the sediments and the submerged aquatic vegetation of the coastal lagoon of the Ria de Aveiro, Portugal

Journal of Sea Research 62 (2009) 276–285

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Journal of Sea Research j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / s e a r e s

Nutrient retention in the sediments and the submerged aquatic vegetation of the coastal lagoon of the Ria de Aveiro, Portugal J. Figueiredo da Silva a,⁎, R.W. Duck b,1, J.B. Catarino a a b

Departamento de Ambiente e Ordenamento, Universidade de Aveiro, 3810-193 Aveiro, Portugal School of Social and Environmental Sciences, University of Dundee, Dundee, DD1 4HN, Scotland, UK

a r t i c l e

i n f o

Article history: Received 1 August 2008 Received in revised form 20 May 2009 Accepted 26 June 2009 Available online 5 July 2009 Keywords: Seagrasses Nanozostera noltii Macroalgae Sediments Nutrients Ria de Aveiro

a b s t r a c t A decrease in the areas covered by seagrasses within the Ria de Aveiro, Portugal, has been observed over the past five decades, resulting in a corresponding increase of the areas of uncovered sediment supporting the growth of sparse macroalgae populations only. Presently, several macroalgae (Ulva spp., Gracilaria sp.) and one seagrass species (Nanozostera noltii (Hornem.) Toml. & Posl.) comprise the submerged aquatic vegetation (SAV) adapted to this shallow, high-energy environment, characterised by fast tidal currents and turbid waters and in which large areas of the bed are exposed during low tide. This study shows that there is a strong inter-relation between the SAV and the surface sediment in intertidal areas. The sediment covered by N. noltii was finer (median grain size 95 µm) and had a high percentage of organic matter (mean value 7.6%), compared with the sediment colonised by macroalgae (median grain size 239 µm; mean organic content 3.2%). The concentrations of both total nitrogen and phosphorous were significantly greater (P b 0.001) in surface sediments covered by N. noltii. Thus, sediments within N. noltii appear to act as a large reservoir of N and P by accumulating greater concentrations of fine sediment particles (silt and clay) and organic matter when compared with the coarser sediment covered with macroalgae only. Hence, the reduction in the area covered by seagrasses will likely result in a gradual loss of nutrients and fine sediment from the Ria de Aveiro channels. © 2009 Elsevier B.V. All rights reserved.

1. Introduction Nutrient enrichment has been reported in many coastal and estuarine systems (Boesch, 2002). Increased inputs from inland areas can promote both nutrient accumulation in the bottom compartment and higher concentrations in the water column. However, long-term accumulation depends on factors controlling nutrient cycling; the interaction between aquatic vegetation and sediment is important for the bioavailability of nutrients. Submerged aquatic vegetation (SAV) communities, comprising seagrasses and macroalgae, support sediment and nutrient filtration, sediment stabilisation and contribute to a complex trophic food web (Short and Wyllie-Echeverria, 1996). Besides supplying organic carbon to consumer populations, SAV growth changes the physical and hydrodynamic conditions at the bed and in the water column, thereby creating specific habitats (e.g. Menéndez and Comín, 2000). Seagrasses can also develop large intertidal populations, although not all species are able to withstand exposure to air, and only few are com-

⁎ Corresponding author. Tel.: +351 234 370928. E-mail addresses: [email protected] (J. Figueiredo da Silva), [email protected] (R.W. Duck). 1 Tel.: +44 1382 384528. 1385-1101/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.seares.2009.06.007

mon in the intertidal. For example, Nanozostera noltii (Hornem.) Toml. & Posl. (= Zostera noltii Hornem.) is particularly widespread in the intertidal zone of the coasts of Western Europe and North-West Africa (Hemminga and Duarte, 2000). In consequence, changes in SAV cover may have a strong impact on coastal ecosystems. One type of change that is commonly reported is the reduction in the abundance of seagrasses (Hall et al., 1999), often accompanied by an increase in the growth of certain macroalgal species (Curiel et al., 2004). The proliferation of macroalgae has been observed in many lagoons, bays and estuaries (Menéndez and Comín, 2000; Morand and Briand, 1996). Furthermore, the relative abundance of seagrasses and macroalgae has been related to hydromorphological conditions and nutrient loading in the aquatic system (e.g. Bachelet et al., 2000). Nedwell et al. (2002), studying a nutrient-enriched estuary with limited hard substrate for the growth of macroalgae, observed mats of Ulva spp. at the edges of salt marshes where the plants provided the necessary attachment points. Macroalgae were not found over mud or sand. Thus, these authors concluded that the availability of suitable attachment points exerts a strong control on the growth of macroalgae when the nutrient concentrations are high. However, some macroalgae species, particularly Ulva spp., can grow in drifting mats and bloom when the light and nutrients are abundant in supply. Such macroalgal blooms can blanket the bed and impact on the benthic species by providing large amounts of organic carbon and nutrients to

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the bottom compartment (Pihl et al., 1999). Thus, macroalgal mats represent a stock of nutrients, which becomes available to bacterial decomposer populations associated with organic-enriched sediments. Subsequently, the nutrients released from the sediment can be taken up by new macroalgae growing on the sediment. Tyler et al. (2001) have shown that Ulva lactuca takes up N from the water column and the sediment and releases organic N to the water column and to the sediment, following senescence, thus playing an important role in the transformation and retention of N in coastal lagoons. Pihl et al. (1999), working in the nutrient-enriched waters of the Swedish west coast, have observed the growth of filamentous green algae covering up to 50% of the shallow water area characterised by soft substrates. The patterns of algal abundance were related to wind, wave and current exposure, but not to the local nutrient loading. Bedforms can also influence the distribution of seaweed. Aníbal et al. (2007) observed that Ulva intestinalis is the only species of macroalgae present on soft sediment in areas of bed with a convex shape, whereas concave areas have a more varied biomass. The sediments in the areas covered by macroalgal mats are enriched in organic carbon and nutrients; remineralisation promotes future algal growth in the areas where tidal exchange is limited. During the 1980s, very high biomass density of Ulva rigida, up to 25 kg m− 2, was recorded in large areas of the Venice Lagoon. Curiel et al. (2004) and Sfriso and Facca (2007) documented a large reduction in the biomass of these algae during the 1990s, after an extensive harvesting programme in the late 1980s. Several factors are believed to have contributed to the major reduction in Ulva biomass, with importance being attributed to the particular climatic conditions and lower nutrient inputs. The harvesting of the macroalgae, thereby removing the nutrients that would have previously been remineralised in the sediment, may also have been an important factor. In the Venice lagoon, the reduction of macroalgae biomass has triggered an increase in suspended mater concentration and water turbidity (Sfriso and Marcomini,1996), which further reduces the growth of SAV. While macroalgae have limited capacity to grow on soft substrates, seagrasses are important stabilisers of soft bottom sediments. Water flow velocities within seagrass canopies become slowed down, thereby reducing sediment resuspension (Peralta et al., 2008). Relationships between sedimentation patterns and seagrass occurrence can provide a useful tool to understand coastal sedimentary regime processes and their ecological significance. Indeed, the loss of seagrass beds has often been related to modifications of sedimentary regimes as well as to a general deterioration in coastal water quality (De Falco et al., 2000). Seagrass meadows improve water quality by reducing particle concentrations in the water column and by absorbing dissolved nutrients. By extracting nutrients from sediments and supporting epiphytes that fix nitrogen, seagrasses provide a pathway for nutrients to enter the water column (Rutkowski et al., 1999). Duarte et al. (2005) have shown that seagrasses play a significant role in global carbon and nutrient cycling. Seagrass biomass, together with that of long-lived macroalgae, has been identified as an important sink of carbon in the ocean (Hemminga and Duarte, 2000). The major requirements for the growth of seagrasses in the marine environment are the presence of adequate rooting substrate, the sufficiency of immersion in seawater and the light needed to maintain growth (Hemminga and Duarte, 2000). Light availability, which constrains the maximum depth of growth, is influenced by the suspended sediment concentration (De Boer, 2007). Hydrodynamics control sediment resuspension, but seagrasses strongly interact with these factors resulting in a self-organisation of seagrass beds (Fonseca et al., 2007). Comparing the dynamics of N. noltii in two coastal lagoons, PergentMartini et al. (2005) concluded that, although light and temperature are the two major factors controlling the growth of this plant, nutrient availability is a positive factor provided that there are shallow depth areas suitable for supporting N. noltii beds. Changes in SAV communities, in response to salinity variation and increase in suspended

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sediment concentration, have also been observed in other shallow lagoons (Sfriso and Marcomini, 1996; Charpentier et al., 2005; Erftemeijer and Lewis, 2006). Decline of seagrasses is now reported as a widespread phenomenon (Hemminga and Duarte, 2000; Orth et al., 2006) and environmental changes that lead to reductions in available light have been implicated in seagrass declines worldwide (Hall et al., 1999). Study of the SAV in the Ria de Aveiro of northern Portugal has shown that this shallow estuarine ecosystem is no exception. Silva et al. (2004) identified a pattern in the change of seagrass populations that can be related to changes in the physical forcing associated with increased tidal wave penetration. The induced resuspension, transport and redistribution of coarser, sandy sediment increase turbidity in the water column and sedimentation in vegetated areas, which have contributed to seagrass decline. Building upon the preliminary work of Silva et al. (2004), this paper presents the results of a study of the relationships between SAV and nutrient retention in the sediments of this shallow coastal lagoon. The aim is to improve understanding of the evolution of the ecosystem's SAV communities, which comprise dominantly N. noltii (Hornem.) Toml. & Posl. (= Z. noltii Hornemann), together with the green macroalgae, Ulva spp. (including the species U. intestinalis L., U. compressa (L.) Nees, U. lactuca L. and U. rigida C. Agardh) and the red macroalgae Gracilaria gracilis (Stackhouse) Steenoft, Irvine et Farnham (= Gracilaria verrucosa (Hudson) Papenfuss). 1.1. The study area The Ria de Aveiro, located in northern Portugal at approximately 40.7°N, 8.7°W, comprises a shallow estuary-coastal lagoon system with a complex morphology and productive ecosystem. The physical system is characterised by many branching channels that are connected to the Atlantic Ocean by a single tidal channel, via an intervening tidal lagoon (Fig. 1). The area below mean sea level, presently c. 50 km2, has suffered erosion over the last few decades, causing the deepening of major channels (Silva and Duck, 2001). Until the 1960s, a large part of this area had a dense coverage of SAV including Potamogeton pectinatus, Ruppia cirrhosa, N. noltii and several macroalgae taxa. The dense coverage of SAV, stabilising shallow water sediments, promoted the retention of fine particles and nutrients entering the lagoon via the inflows of four rivers and several streams. A decrease in the areas covered by seagrasses within the Ria de Aveiro has been observed over the past five decades (Silva et al., 2004), resulting in a corresponding increase of the areas of uncovered sediment supporting the growth of sparse macroalgae populations. The loss of vegetation sheltering the sediment, can thus lead to a gradual loss of the fine particles and nutrients accumulated in the sediment. This paper aims to document the effect of SAV change, in relation to nutrient accumulation, and its implications for the eutrophication process in the Ria de Aveiro. 2. Methods 2.1. Field methods Frequently, studies of SAV combine in situ observations of the vegetation with remote observations either by aerial photography or satellite images. The areas covered by SAV appeared darker in the images used by Gullström et al. (2006). Bernard et al. (2007) also verified that darker areas in the bottom of a coastal lagoon correspond to N. noltii beds, allowing the mapping of the area of seagrasses and long-term changes. Airborne colour photography, obtained from a light aircraft flying at 500–1000 m, was used for identification of vegetated areas in the Ria de Aveiro. The intertidal areas covered by seagrasses and macroalgae appear in dark green tones when observed from the air. The remote observations were repeated six times in order to identify

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were determined with Magellan® Promark X-CM GPS (accuracy of c.10 m). Above and below ground biomass of N. noltii or the macroalgae attached to the sediment were hand collected from an area of 0.25 m2. In the areas with N. noltii the surface layer of sediment was removed in order to permit the collection of the below ground parts of the plants. Plant samples were washed in the field to remove sediment and shells. Surface sediment samples, to approximately 3 cm in depth, were also collected at the same points, after removing the plants in order to minimise the inclusion of live plant material. Some short cores (0.2 m length, 0.1 m diameter) were also obtained, from which to determine the variation of organic content and nutrient concentration with depth. The temperature and the salinity of water, close to the sampling points, were measured at low stages of the tide using a WTW LF330 conductivity meter. One sample of seagrass, plus any macroalgae present, was collected at each sampling point in the areas with N. noltii, for each sampling date, resulting in a maximum of eight samples per point; a few samples were missed when some points could not be reached at low tide. The number of macroalgae samples collected from points outside the N. noltii bed was lower, because occasionally macroalgae were not present at some locations. Whenever a biomass sample was collected, the surface sediment in the same area was also sampled. The sediment cores were collected in January and May 2004, at the sampling points with N. noltii. 2.2. Laboratory methods

Fig. 1. The Ria de Aveiro showing the distribution of the main vegetated areas. The intertidal areas covered by seagrass or macroalgae are shown in grey and the numbered sampling points represented by black dots. Note the single inlet/outlet channel to the Atlantic Ocean (west side) and the five main channels: A. Canal de Ovar; B. Canal da Murtosa; C. Canal do Parrachil; D. Canal de Ílhavo and E. Canal de Mira. The grid shows UTM co-ordinates (km).

changes in the distribution of the SAV (data obtained in September 2002, January 2003, April 2003, May 2003, July 2003 and September 2003). The boundaries of the vegetated areas, persisting in all the surveys, were then overlain onto a map representing the lagoon channels, drawn based on photomaps (dated 2005), and shown schematically in Fig. 1. Ten sampling points were located inside the intertidal areas with N. noltii beds, as well as in adjacent locations with sparse macroalgae coverage. Three additional sampling points (7, 9, and 11) were located in the Canal de Ovar (Fig. 1), in subtidal areas that had important seagrass beds, but now support macroalgae only. The criteria for selection considered both the need for general coverage in the lagoon and also the size of the areas persistently covered by SAV, as observed in the remote images. The sampling programme began in October 2002 and continued until December 2004, including eight campaigns (October 2002, February 2003, June 2003, September 2003, January 2004, May 2004, September 2004 and December 2004). These dates span both the variation of natural hydrological conditions and the natural change in the abundance of vegetation through the year. All sampling locations

In the laboratory, plant samples were separated by species, followed by the determination of the wet weight and dry weight. Sub-samples, obtained by cutting the plants, were taken for determination of the dry weight at 60 °C, volatile content (combustion at 550 °C), total nitrogen and total phosphorus. The plant sub-samples were digested for total nitrogen by the Kjeldahl method, adapted from Eaton et al. (1995). Total phosphorus concentration was obtained by a colorimetric method, adapted from Eaton et al. (1995), after digesting the plant material with nitric and sulphuric acids. Whenever a sample concentration of N or P was not measured, the mean contents for that type of plant biomass were used in the calculation of nutrients mass per unity of area. The sediment samples were analysed to determine the moisture content by drying at 105 °C and the organic matter content by combustion for 1 h at 550 °C. Sediment samples were also digested for total nitrogen and total phosphorus, by the same analytical procedures used for the plants. The contents of N and P, obtained as a mass fraction of dry weight, were used for the calculation of nutrient mass contained in the surface sediment layer corresponding to 30 L m− 2 (3 cm deep). The dry weight of sediment in this layer was calculated assuming that the particle density was 2.5 and using the moisture content measured as proxy for porosity. Laser granulometry analysis (Beckman Coulter LS230) was used to obtain grain size distributions from which the percentages of sand (2 mm to 63 µm), silt (63 µm to 4 µm) and clay (b4 µm) were calculated. 2.3. Data analysis The dataset derived during this study was sub-divided into two classes for the calculation of mean values and standard deviations: one class relating to samples from locations where N. noltii growth was observed and the other from locations in the study area without N. noltii and where only macroalgae were present. The dataset was organised into a series of values for each of the different sampling locations at the different sampling dates. For each location, from six to eight samples (points with N. noltii) plus up to seven samples (points with macroalgae) were collected on the different sampling dates. The total number of samples, for each class, is given in Tables 1 and 2. Student's t-test was used to compare the statistical significance of the differences in the mean values of the parameters measured in the plants and in the sediments, after verifying the homogeneity of

J. Figueiredo da Silva et al. / Journal of Sea Research 62 (2009) 276–285 Table 1 Mean values and standard deviations of biomass density (ash free dry weight per unit area) for N. noltii and for the main macroalgae taxa. Ash free dry weight (g m− 2) N. noltii Gracilaria U. intestinalis U. lactuca

Areas with N. noltii

Areas with macroalgae only

110 ± 50 (n = 74) 13 ± 25 (n = 74) 3 ± 9 (n = 48) 3 ± 13 (n = 69)

8 ± 12 (n = 55) 4 ± 9 (n = 57) 2 ± 7 (n = 57)

Numbers of samples for each taxon include only the results from points where it was present at least once. Results are aggregated in each area class (with N. noltii and with macroalgae only). Sampling period was October 2002 to December 2004.

variance by the F-test. Where the population variances were equal, the standard error of the differences was computed based on the pooled variance. Where the population variances were not equal, the standard error of the differences was calculated from the two variances and the appropriate formula for the number of degrees of freedom was used. One way analysis of variance (ANOVA), performed with SPSS software, was used to determine statistically significant spatial differences among the data, considering the various sampling dates as replicates. Normality and homogeneity of variances were verified for the results presented; the Tukey test was selected for the identification of significantly different sampling locations. Multiple regression analysis was used to verify if biomass on N. noltii was correlated with grain size, clay content or organic content of the sediment. 3. Results 3.1. Distribution of seagrasses and macroalgae The results of the sets of airborne remote observations of the Ria de Aveiro are combined in Fig. 1 to show the extent of the areas with a dense coverage of submerged vegetation. The grey areas represent the intertidal zones that are vegetated by vascular plants and macroalgae. The total area is c.3 km2, which corresponds to c. 5% of the area of the lagoon. As illustrated in Fig. 1, the distribution is not uniform; the most important vegetated areas are located in the central parts of the lagoon, on the sediment banks in the lower intertidal zone (tidal flats), extending to the limit of the salt marsh areas. The tidal flats supporting N. noltii are frequently less exposed to tidal currents than lower areas with macroalgae only. The spatial distribution of sampling points, which includes all the major channels in the Ria de Aveiro, permits a characterisation of the temperature and salinity conditions in the water supporting the vegetation. Both parameters showed a small spatial variation with a seasonal trend. The water temperature in vegetated areas was lowest in January varying from 11 °C near the inlet channel to 9 °C in the inner parts of the lagoon. Between May and September the water temperature ranged from 18 to 25 °C. The lowest salinities were recorded in February, ranging from 9 psu in the inner parts of the lagoon to 27 psu at sampling points near to the inlet channel. In September, salinity remained close to oceanic values at all points, varying from 30 to 36 psu.

Table 2 Variation in bed surface sediment grain size distribution according to vegetation cover in the Ria de Aveiro (mean values, standard deviations and number of samples). Vegetation cover

% Sand

% Silt

% Clay

Median grain size (µm)

Areas with N. noltii

59.2 ± 17.4 (n = 74) 86.9 ± 11.9 (n = 52)

37.8 ± 16.2 (n = 74) 11.9 ± 11.0 (n = 52)

2.9 ± 1.8 (n = 74) 1.2 ± 1.1 (n = 52)

95 ± 65 (n = 74) 239 ± 110 (n = 52)

Areas with macroalgae only

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The only seagrass species observed within the Ria de Aveiro was N. noltii and only three macroalgae species were also abundant: G. gracilis, U. intestinalis and U. lactuca. Some other macroalgae species were identified (Cladophora sp., Chaetomorpha sp., Ulva sp., Blidingia sp., Bryopsis sp., Ceramium rubrum, Polysiphonia sp., Bostrychia scorpioides, and Goniotrichum sp.), however they were present in insignificant quantities during most of the year. On the building stones of man-made seawalls other macroalgae, especially Fucus spiralis and Sargassum muticum, were also observed attached to structures. 3.2. Plant biomass The results presented in Fig. 2 show that the mean total plant biomass (ash free dry weight of N. noltii including rhizomes plus macroalgae), determined for each sampling location where N. noltii was present in the Ria de Aveiro, varies through the range 86–170 g m− 2. By one way analysis of variance, it was observed that N. noltii biomass varies significantly (1-way ANOVA, P b 0.001) between sampling locations. The lower values of N. noltii biomass (post-hoc Tukey test, P b 0.05) were observed in the north of the lagoon (10-Torreira, 12-Ovar and 13-Carregal, Fig. 2). In the adjacent points with only macroalgae, the mean plant biomass was much lower, varying from 3 to 28 g m− 2. In most locations and sampling dates the macroalgae biomass was low, but high values (over 100 g m− 2) were measured at some locations, which are attributed to the occasional accumulation of drifting macroalgae. The macroalgae biomass dataset did not satisfy the prerequisites for applying ANOVA. The areas covered with N. noltii had a higher total plant biomass, per unit area, compared with areas covered with macroalgae only (Table 1). The total macroalgae biomass in the areas with N. noltii was not significantly different (t-test, P N 0.05) from that in areas with macroalgae only. This shows the importance of N. noltii, presently the only vascular plant contributing to the plant biomass in the Ria de Aveiro. With reference to the importance of the major macroalgae taxa, Gracilaria was the most abundant and was present in most of the samples from areas with N. noltii; U. intestinalis was the most frequent species in areas without N. noltii but with a low biomass density; U. lactuca had a lower abundance and was frequently not present in the samples. However, it was present occasionally in large masses. In addition to the spatial variation between the sampling points, the seasonal change in plant biomass was also monitored. The mean values of total biomass, at both sets of locations (i.e. with N. noltii and with macroalgae only), were calculated for different times in the year (Fig. 2). The maximum values of total biomass in both types of vegetation coverage occurred in September 2003 and 2004, corresponding to the end of summer, and the minimum values occurred in February 2003 and January 2004, corresponding to the end of winter. Mean total biomass values for N. noltti plus macroalgae are significantly (t-test, P b 0.001) greater in September than in January/February. Mean biomass of macroalgae is also significantly higher (t-test, P b 0.01) in late summer. 3.3. Sediment The grain size results (Table 2) show that the bottom sediment of the Ria de Aveiro comprises mainly sand mixed with a variable finer fraction and so should form a suitable substrate for seagrass populations. However, the coarser deposits, characterised by ripple and dune bedforms caused by currents and wave-induced bedload transport, revealed a high mobility that may render them unsuitable to support plant growth. Observations showed that, in the Ria de Aveiro, N. noltii survives only in sediment that contains a significant mud (i.e. silt plus clay) component, while coarser substrates, characterised by ripples and dunes, support macroalgae only. In addition, the organic and nutrient content of the bottom sediments are related to the characteristics of the colonising vegetation.

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Fig. 2. Mean values and standard deviations of plant biomass (ash free dry weight — g− 2) derived from the samples collected at each intertidal location in the Ria de Aveiro. A — Results for each of the sampling stations shown in Fig. 1. B — Results for each sampling date.

The grain size distributions within the c. 20 cm long sediment cores showed, in general, very little variation with depth (data not shown). In consequence, the results of grain size analyses presented here correspond to sediment collected from the uppermost 3 cm of the bed. The granulometry results for samples collected over the entire lagoon, between October 2002 and December 2004, showed a clear differentiation between the bottom sediments characterising the two types of vegetation cover (Table 2). Surface sediment covered with N. noltii contained more silt and clay than the sediment where only macroalgae (mainly U. intestinalis) were present. The mean values of these two types of sediment correspond to median grain sizes ( ± standard deviation) of 95 ± 65 µm (n = 74) and 239 ± 110 µm (n = 52), respectively, which are significantly different (t-test, P b 0.001). The observed spatial and temporal variation in median grain size (Fig. 3) can be attributed to the location of the main river inputs, in the centre of the lagoon, and to the mobility of fine particles according to seasonally changing environmental conditions, respectively. The mean organic content of the sediment supporting N. noltii (7.6 ± 2.1%) was considerably higher than that supporting macroalgae only (3.2 ± 2.2%). The organic matter content varied significantly (1-way ANOVA, P b 0.001) in the sediment of the areas with N. noltii between sampling locations (Fig. 4), while in the sediment supporting macroalgae only, equally large temporal variations were observed. Multiple regression analysis was carried out using N. noltii biomass as the dependent variable and sediment median grain size, clay and organic content, as predictor variables; only 3% of the sample variance

is predicted by the linear regression model. The correlations with any of the predictor variables are weak and not statistically significant (Pearson correlation, P N 0.1). The correlations among the predictor variables are statistically significant (Pearson correlation, P b 0.001) indicating that a smaller median grain size correlates with higher concentrations of clay and organic material in the sediment. 3.4. Storage of nutrients The two types of vegetation have very different capacities for nutrient retention, both in the plants themselves and also in the sediment substrate (Tables 3 and 4). The total amount of nutrients present in the benthic compartment was divided into the part contained in the plants (including the below ground tissues) and the part contained in the sediment, including any microalgae and dead organisms. The mean N and P contents (% dry weight) determined in the vegetation samples (Table 3) showed that N. noltii contained significantly less N (t-test, P b 0.001), compared with macroalgae, whilst the P content, was generally higher (t-test, P b 0.025). The N and P content in the sediment were typically 10 times lower than in the plant material. Both N and P in the sediment from areas with N. noltii were significantly higher (t-test, P b 0.001) than in areas with macroalgae only. The mass of nutrients present per unit area (g m− 2) of each of the two vegetation types was also calculated in order to evaluate their importance in storing nutrients in the estuarine system. Equivalent analyses were also undertaken for the sediment samples (uppermost 3 cm), to elucidate any relationship between the substrate and the

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Fig. 3. Median grain size of the bed surface sediments of the Ria de Aveiro (mean values and standard deviations of samples collected at all locations). A — Results for each of the sampling stations shown in Fig. 1. B — Results for each sampling date.

colonising intertidal vegetation. The mean N contents in the vegetation and in the sediment (g m− 2), for each sampling period, in the areas with N. noltii and in those with macroalgae only are shown in Fig. 5. The most remarkable difference relates to the vegetation coverage in the sampled areas. Where N. noltii was present, N contents were significantly higher (t-test, P b 0.001) both in the plants and in the bed sediment. Comparing the N contents (g m− 2) in the vegetation with those in the surface sediment, the latter retained 12 times (areas with N. noltii) to 43 times (areas with macroalgae) the amount of N in the vegetation (Table 4). Fig. 6 shows the seasonal variation of P content in the vegetation and in the surface sediment. In the areas colonised by N. noltii, the concentrations of P in the vegetation were greater (t-test, P b 0.001) than in areas with macroalgae only (Fig. 6). A similar difference (t-test, P b 0.001) in P concentration occurred in the surface sediments from these areas (Fig. 6). A comparison of the P concentrations in the plants with those in the bed surface sediment showed that the latter is a much larger P reservoir than the former, especially in the areas colonised by macroalgae only, retaining 16 times (areas with N. noltii) to 180 times (areas with macroalgae) the amount of P in the vegetation (Table 4). 4. Discussion and conclusions The results from the airborne observations, combined with the results of direct sampling (Fig. 1), allow the comparison between the present distribution of vegetation in the Ria de Aveiro with that

observed in 1980 (Silva et al., 2004). The decline of seagrasses in the Ria de Aveiro is now well established. Since the 1980s, reductions in both species number and abundance have been observed in the lagoon, in particular within the subtidal areas in the Canal de Ovar. Although, in the past, the collection of seagrasses and macroalgae had great social and economic importance, there are today no such activities remaining in the ria. Several factors have been suggested to explain seagrass decline in the Ria de Aveiro, including increased salinity, siltation and turbidity, associated with faster tidal flows, which are related to changes in the physical forcing in the system (Silva et al., 2004). A major consequence of changes occurring over the last 50 years has been the disappearance of subtidal meadows of Zostera, Ruppia and Potamogeton species. The only submerged vascular plant still present in the Ria de Aveiro is N. noltii, which is restricted to some intertidal areas that are usually less exposed to tidal currents than adjacent areas. The macroalgae Ulva and Gracilaria are sparsely present over a large area of the shallow water and intertidal areas. The reasons for this loss of rooted plant species are most likely related to the changes in the salinity and in the physical conditions in the ria. Our results also suggest that the presence of N. noltii is related to the distribution of appropriate sediment types. Sediment samples obtained at points with and without the growth N. noltii, separated by distances of typically no more than 100 m, are of very different types. Measurements of water temperature and salinity carried out during the sampling programme revealed the maximum temperature (25.8 °C) in May 2004 and the minimum (9.1 °C) in January 2004. The

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Fig. 4. Organic matter content in bed surface sediments of the Ria de Aveiro (mean values and standard deviations of samples collected at all locations). A — Results for each of the sampling stations shown in Fig. 1. B — Results for each sampling date.

present conditions of tidal forcing inside the Ria de Aveiro cause the low salinities to occur only during the transient high river flows, so only those plants adapted to high salinity water can thrive. The seasonal change in total plant biomass observed at some sampling locations, with a minimum in winter, can be attributed to reduced incident irradiance and temperature. However, the patterns of seasonal changes, varying with the location and exposure to the river inputs, result in no significant (1-way ANOVA, P N 0.05) difference in overall N. noltii biomass through time. As noted above, the biomass of N. noltii showed a significant variation (1-way ANOVA, P b 0.001) between the sampling locations. The low values recorded at point 10 (Torreira), where the vegetated

Table 3 Mean percentages dry weight (% d.w.) and standard deviations of N and P in the samples of N. noltii, macroalgae and sediment in the Ria de Aveiro. Vegetation type Areas with N. noltii

N. noltii Macroalgae Sediment

Areas with macroalgae only

Macroalgae Sediment

Mean N (% d.w.)

Mean P (% d.w.)

2.09 ± 0.48 (n = 55) 3.64 ± 2.14 (n = 23) 0.20 ± 0.06 (n = 68) 2.84 ± 1.09 (n = 37) 0.08 ± 0.06 (n = 54)

0.39 ± 0.10 (n = 53) 0.30 ± 0.18 (n = 23) 0.05 ± 0.01 (n = 67) 0.23 ± 0.10 (n = 37) 0.03 ± 0.01 (n = 54)

area was located at a lower level than the other sampling stations and thus was exposed only briefly during low water, were due to reduced light availability. It is of interest to note that the northern zone of the Ria de Aveiro was, until the 1980s, the richest in terms of seagrass abundance and species diversity in the subtidal areas. It was also in this area that, when still abundant, the collection of seagrasses had the greatest social and economic importance (Silva et al., 2004). The areas where N. noltii shoots grow have a high standing biomass, when compared with the intertidal areas covered with macroalgae only. The total biomass observed in both types of vegetation cover is significantly different (t-test, P b 0.001) and, in the case of

Table 4 Mean mass of N and P per unit area (g m− 2) in the plants and the sediment according to vegetation type in the Ria de Aveiro. Vegetation type Areas with N. noltii

N. noltii Macroalgae Sediment

Areas with macroalgae only

Macroalgae Sediment

N per unit area (g m− 2)

P per unit area (g m− 2)

3.8 ± 1.7 (n = 67) 0.7 ± 1.4 (n = 69) 53 ± 11 (n = 62) 0.7 ± 0.8 (n = 57) 30 ± 18 (n = 52)

0.69 ± 0.31 (n = 67) 0.06 ± 0.13 (n = 69) 12 ± 2 (n = 62) 0.05 ± 0.07 (n = 57) 9±3 (n = 52)

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Fig. 5. Seasonal variation of N content (g m− 2) in the vegetation (A) and in the surface sediments (B) of the Ria de Aveiro (mean values and standard deviations of samples collected at all locations).

N. noltii, varied trough the range 86–170 g m− 2 (dry weight), which is similar to the values measured in other lagoons (Pergent-Martini et al., 2005). The nutrient stock in the vegetation is significantly smaller (t-test, P b 0.001) compared with the storage in the bed surface sediment, however the presence of N. noltii significantly increases the content of nutrients and organic matter per unit area. Usually organic matter concentrations in sediment supporting seagrass growth are b6% dry weight (Hemminga and Duarte, 2000). However, in the case of the Ria de Aveiro, bed surface sediment colonised by N. noltii contains 7.6 ± 2.1% of organic matter. The sediment with macroalgae only, contains less organic material, with a mean value of 3.2 ± 2.2%. There is also a clear difference between the nutrient retention in areas covered with N. noltii, compared with those areas characterised by the presence of macroalgae only. The surface sediment supporting N. noltii acts as a large reservoir of N and P and accumulates greater concentrations of fine particles (silt and clay) and organic matter compared with the coarser sediment covered with macroalgae only. Thus, the effect of the presence of seagrasses in relation to nutrient retention is to promote accumulation in the sediment rather than in the plant biomass. Authors studying submerged macrophytes at other locations verified a complex interaction between the plants and the sediment. The sediment sheltering effect, provided by seagrasses, is more effective in relation to tidal induced flow than for wave-induced currents (Madsen et al., 2001). In the case of N. noltii the flexible shoots are

easily bent over the sediment, reducing the canopy water flow (Morris et al., 2008). Thus the sediment under the shoots of N. noltii is effectively protected from tidal currents capable of causing sediment transport (Peralta et al., 2008). However, the protective effect, which depends on the shoot density, can vary seasonally. Presently, in the Ria de Aveiro, N. noltii grows only in intertidal flat areas characterised by fine sediment with a high organic fraction (intertidal mud flats). The N. noltii standing biomass density varies within these areas, but no significant correlation with the sediment median grain size, clay and organic content was found in the results obtained for mud flats supporting the seagrasses. It can be concluded that the availability of areas with this type of sediment is a prerequisite for the establishment of N. noltii populations in the Ria de Aveiro. It also is known that N. noltii has a limited capacity for vertical rhizome growth (Brun et al., 2005) and fast burial by a layer of sediment results in a reduction of shoot density leading to the death of this plant (Cabaço and Santos, 2007). Thus, the conditions for the growth of seagrass populations in the Ria de Aveiro are strongly related to the sediment dynamics, and the evolution of areas with N. noltii will depend principally on the sedimentary regime to which they are subjected. This paper supports the findings of Silva et al. (2004), that seagrass decline was associated with an increased transport and redistribution of sandy sediment induced by increased tidal wave penetration after dredging works. The paper has, furthermore, demonstrated the

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Fig. 6. Seasonal variation of P content (g m− 2) in the vegetation (A) and in the surface sediments (B) of the Ria de Aveiro (mean values and standard deviations of samples collected at all locations).

relationships between sediment characteristics and SAV type in the Ria de Aveiro and in this way contributes to improved understanding of the evolution of seagrass communities in the system. The challenge that still remains is how to prevent further decline in seagrasses, thereby preventing further ecosystem change, a goal that is currently the subject of ongoing research. The observed relationship between sediment characteristics and the presence of N. noltii shows the importance of changes in the sedimentary regime, in limiting the distribution of SAV in the Ria de Aveiro. Silva and Duck (2001) observed that past engineering works have caused an increase in tidal amplitude within the lagoon, resulting in erosion in many areas. Thus, further canalisation of major channels will potentially impact the N. noltii populations. Seagrass decline was not accompanied by a large increase in macroalgae populations, although the nutrient inputs from rivers were large (Silva et al., 2002). As observed in other areas, the macroalgae biomass was probably limited by the availability of attachment points and by the action of tidal currents, which prevent the accumulation of drifting mats. Kamer et al. (2004) observed that adding estuarine sediment, with a fine fraction of about 40%, increases the growth of macroalgae when nutrients are scarce in the water column. In the Ria de Aveiro, a lower retention of fine sediment and the large reduction of seagrass beds could also decrease the availability of nutrients when other inputs are low and reduce the summer growth of macroalgae. Thus, the evolution of the vegetation and of the

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