Scientia Marina 73(2) June 2009, 307-318, Barcelona (Spain) ISSN: 0214-8358 doi: 10.3989/scimar.2009.73n2307
Spatial and temporal patterns of benthic invertebrates in the Tagus estuary, Portugal: comparison between subtidal and an intertidal mudflat Susana França 1, Catarina Vinagre 1, Miguel A. Pardal 3 and Henrique N. Cabral 1,2 1 Instituto
de Oceanografia, Faculdade de Ciências da Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal. E-mail:
[email protected] de Biologia Animal, Faculdade de Ciências da Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal. 3 IMAR – Institute of Marine Research, Department of Zoology, University of Coimbra, 3004-517 Coimbra, Portugal.
2 Departamento
SUMMARY: Intertidal mudflats are a dominant feature in many estuarine systems and may be a significant component of the feeding grounds available for many fish and bird species. Therefore, it is crucial to determine the importance and role that this particular habitat plays for the different estuarine communities. Spatial and temporal dynamics of macrobenthic communities in an intertidal mudflat of the Tagus estuary were assessed in order to determine the role of this habitat in the whole estuarine functioning. Benthic macroinvertebrate communities were sampled monthly in two intertidal areas (upper and lower) and in the adjoining subtidal area for one year. Macroinvertebrate density and biomass in the intertidal mudflat were higher than in the subtidal area, but no clear trends were found between the lower and upper intertidal area. Spatial patterns in the community were more pronounced than seasonal patterns. This benthic community was characterised by high densities of Pygospio elegans, Scrobicularia plana, Cyathura carinata, Hydrobia ulvae and Nereis diversicolor. Abundance and biomass values in this intertidal mudflat were considered low in comparison with other estuarine habitats, namely seagrass beds. Nevertheless, this habitat plays an important role for the main species present in the community, acting as a key area for recruitment, with high concentrations for many invertebrate species. Keywords: benthic macroinvertebrates, community structure, intertidal mudflat, subtidal, Tagus estuary. RESUMEN: Pautas de distribución espacio temporales de invertebrados bentónicos en el estuario del Tajo, Portugal: comparación entre marismas intermareales y submareales. – Las marismas intermareales son características de muchos sistemas estuáricos y pueden abarcar un componente significativo de las áreas de alimentación disponibles para muchas especies de peces y aves. Por tanto, es crucial determinar la importancia y el papel que juega este hábitat para las diferentes comunidades estuarinas. Se evaluaron las dinámicas espaciales y temporales de las comunidades macrobentónicas en una marisma intermareal del estuario del Tajo, determinando el papel de este hábitat en el conjunto del funcionamiento de estuario. Las comunidades de macroinvertebrados bentónicos se muestrearon, mensualmente durante un año, en dos áreas intermareales (superior e inferior) y en las áreas submareales adyacentes. La densidad y la biomasa de los macroinvertebrados en las marismas intermareales fueron superiores que en el área submareal, y no se encontraron claras tendencias entre el intermareal superior e inferior. Los patrones espaciales en la comunidad fueron más pronunciados que los estacionales. Esta comunidad bentónica estuvo caracterizada por altas densidades de Pygospio elegans, Scrobicularia plana, Cyathura carinata, Hydrobia ulvae y Nereis diversicolor. Los valores de abundancia y biomasa en esta marisma intermareal fueron considerados bajos cuando se comparan con otros hábitats estuarinos como las praderas de fanerógamas. No obstante, este hábitat juega un importante papel para las principales especies presentes en la comunidad, actuando como un área clave para el reclutamiento, con altas concentraciones de muchas especies de invertebrados. Palabras clave: macroinvertebrados bentónicos, estructura de la comunidad, marismas intermareales, submareales, estuario del Tajo.
308 • s. frança et al.
INTRODUCTION Coastal transition ecosystems such as estuaries and coastal lagoons are recognised worldwide as the most productive and valuable aquatic ecosystems on Earth (Costanza et al., 1997). These transitional environments are characterised by a unique biodiversity and perform several vital functions, e.g. as nursery areas for fish, feeding areas for migrating and wintering birds and migration routes for anadromous and catadromous fish (Odum, 1983; McLusky, 1989). One of the most important characteristics of estuaries is the fact that they form a mosaic of inter-linked habitats that should not be considered in isolation (Morrisey et al., 2003). Each one is of particular value for the different species that use it. The assessment of the importance, dynamics and functions of each estuarine habitat, as well as their ecological connectivity, is still poorly understood (Elliott and Hemingway, 2002). Intertidal mudflats are a dominant habitat in many estuarine systems, often covering a considerable part of their area (Morrison et al., 2002). They have long been recognised as a key habitat for the estuarine food web because of their disproportionately high productivity in comparison with subtidal areas (Reiser, 1985; Michaelis et al., 1992; Wanink and Zwarts, 1993; Elliott and Dewailly, 1995), and an increasing number of studies considering their dynamics have been published recently (Dittmann, 2000; Boer and Prins, 2002; Dolbeth et al., 2003; Melville and Connolly, 2005; Rodrigues et al., 2006; Cardoso et al., 2008). The first studies on intertidal mudflats focused mainly on macro benthic communities, so their distribution in this habitat is well known for temperate areas (Dittman, 2000). The spatial heterogeneity of macrobenthos along the estuarine gradient is traditionally described in relation to salinity and sediment composition (Ysebaert et al., 2003). However, the depth gradient from high intertidal to deep subtidal areas also has a pronounced effect on macrobenthic species distribution within the estuary (Ysebaert et al., 2002), with the highest values for density and biomass being registered at intertidal sites (Ysebaert et al., 2000). Intertidal mudflats also play an important role as a preferential recruitment habitat for several macroinvertebrate species when adjacent seagrass habitats are available and show higher species richness and abundances (Heck et al., 1995).
The present study was conducted in the Tagus estuary, one of the largest estuaries on the Atlantic coast of Europe. Despite being subjected to intense human disturbance, the Tagus estuary contains a high biodiversity, mainly because many different habitats are available for biological communities (Bettencourt et al., 2001). Intertidal mudflats occupy 40% of the total estuarine area and are mainly located within the nature reserve of the Tagus estuary. They are used as feeding areas, maintaining large populations of resident and migratory birds (Moreira,1999). The Tagus estuary plays a functional role as a nursery area for many commercially important fish species (Costa and Bruxelas, 1989; Costa and Cabral, 1999), with intertidal mudflats maintaining suitable conditions for this nursery function, as previously reported for this area (Cabral, 2000; Vinagre et al., 2006; França et al., 2008). Despite the recognised importance of the benthic macrofauna of these areas, the most extensive study on the Tagus estuary intertidal benthic macroinvertebrates, which dates from the early 1980s (Calvário, 1982), is qualitative and fails to cover the most important areas. Recent studies on this area described the structure of the benthic invertebrate community and evaluated its relationship with several environmental factors and the dynamics of this community (Rodrigues et al., 2006; Silva et al., 2006). However, none of these studies dealt with the importance of this vertical gradient from high intertidal to subtidal areas and the differences between their communities. In this study both intertidal and subtidal habitats were sampled, with the main goal of determining the assemblage structure and the spatial and seasonal distribution of macrobenthic communities in the upper and lower part of the intertidal mudflat and in the subtidal area adjacent to it. Special emphasis is placed on differences between communities through this tidal gradient. The crucial role that this intertidal mudflat plays in the global dynamics and functioning of the Tagus estuary is also discussed. MATERIAL AND METHODS Study Area The Tagus estuary (38º40’N 9º15’W) is 50 km long and occupies an area of 325 km2. The system has a tidal amplitude of 4 m and the intertidal
SCI. MAR., 73(2), June 2009, 307-318. ISSN 0214-8358 doi: 10.3989/scimar.2009.73n2307
Benthic invertebrate patterns in an intertidal mudflat • 309
Sampling and laboratory procedures
Fig. 1. – Location of sampling areas in the Tagus estuary: A, upper intertidal; B, lower intertidal; C, subtidal.
and saltmarsh areas account for 40% of the total estuarine area (Bettencourt et al., 2001). The average estuarine depth is ca. 10 m and the maximum depth is 40 m near the mouth of the estuary. The river flow varies both seasonally and annually, with a mean discharge of 400 m3 s-1 (Bettencourt and Ramos, 2003). The Tagus estuary includes several special areas that are protected because of their biological diversity, one of the most important being the Tagus Estuary Nature Reserve, with an area of 14560 ha (Farinha et al., 2001). This area is mainly composed of mudflats that become emerged at low tide, playing an important role as feeding grounds for wintering birds that use the area as a stopover site during their winter migrations (Moreira, 1999). The present study was undertaken at an area located in the upper estuary in a sheltered south branch, located near Alcochete (Fig. 1). The study sites are located in a large mudflat intertidal area, with an adjacent channel representing the subtidal area. These mudflat areas are completely drained for two periods daily. According to the elevation of the two intertidal sampled areas, the mean emersion times for both areas were calculated using the synoptic equations for the water level. The obtained estimations were 17 hours day-1 for the upper part of the mudflat and 14 hours day-1 for its lower part. The subtidal area (channel) is always submerged. Salinity in this area varies from 4 in winter to nearly 30 in summer, while water temperature ranges from 8 to 26ºC (Cabral et al., 2001).
Quantitative sampling of macrobenthic organisms was carried out monthly from January to December 2004, covering three main areas: upper intertidal (A), low intertidal (B) and subtidal (C). Samples were taken during high water, at neap tides. In each area 10 replicates were randomly sampled using a Van Veen grab (0.05 m2). In a preliminary study in the same area, the number of replicates per sample was established using the rank-frequency diagram method (Frontier, 1983) for stabilising variability. All samples were sieved using a 0.5 mm mesh size sieve and fixed in 10% formalin solution. A sediment sample was obtained for determination of grain size composition. In the laboratory samples were sorted after being stained with rose Bengal and organisms were counted and identified to the lowest taxonomic level. Measures were taken from the most abundant species: total shell length for the bivalve Scrobicularia plana (da Costa, 1778) and total body length for the worm Nereis diversicolor (O.F. Muller, 1776) and for the isopod Cyathura carinata (Krøyer, 1847). Biomass values were determined as gram ash free dry weight (g AFDW), directly measured as the difference between the dried (80ºC for minimum 48 h) and ashed (560ºC for 2 h) weight. In order to obtain grain size composition, sediment samples were dried at 60ºC and a 100 g subsample was wet-sieved through a 0.063 mm mesh sieve and dried. The remaining sediment was sieved through a four-sieve column. The weight of the residue remaining in each sieve was then expressed as a percentage of the initial subsample weight and the 2 mm) (0.5-2 mm) Upper intertidal Low intertidal Subtidal
0.04 0.29 29.76
0.51 0.33 40.27
station for analysis. The aim of the analysis was to investigate the distribution patterns of species in the three areas considered (upper intertidal, low intertidal and subtidal), and to determine the differences in the spatial and seasonal changes in the community structure between them throughout the sampling year. In order to describe these differences the biological data were submitted to correspondence analysis, using CANOCO 4.5 software (Ter Braak and Šmilauer, 2002). RESULTS Sediment analysis Mud was the predominant fraction found on the intertidal mudflat (Table 1). The annual mean percentage of mud in the upper intertidal area was 98.9%. Similar percentages of mud were found in the lower part of the intertidal mudflat, with a yearly mean value of 98.4% (Table 1). The subtidal area sediment was primarily composed of coarse sand (40.3%), followed by gravel and mud, which represented 29.8% and 29.4% of the total sediment, respectively. Macrofauna analysis During the present study, a total of 8 species and three higher taxa groups were recorded among 58 778 individuals collected from 360 samples. Some individuals were identified only to genus (particularly amphipods), while other organisms, such as oligochaetes, were only identified to class level and may have consisted of more than one species. Mean density (ind m-2) and biomass (g AFDW m-2) values for each species in the three sampled areas are presented in Table 2. The macrobenthic community of the study area was characterised mainly by high densities of four taxa: Scrobicularia plana, Pygospio elegans, Oligo-
Sand Medium Fine (0.125-0.5 mm) (0.063-0.125 mm) 0.14 0.13 0.04
0.36 0.82 0.58
Mud (
