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Colonization process by macrobenthic infauna after a managed coastal realignment in the Bidasoa estuary (Bay of Biscay, NE Atlantic)
Estuarine, Coastal and Shelf Science 84 (2009) 598–604
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Estuarine, Coastal and Shelf Science journal homepage: www.elsevier.com/locate/ecss
Colonization process by macrobenthic infauna after a managed coastal realignment in the Bidasoa estuary (Bay of Biscay, NE Atlantic) Mikel A. Marquiegui a, *, Florencio Aguirrezabalaga a, b a b
S.C. INSUB, Museo Okendo, Zemoria, 12, Apdo 3223, 20013 Donostia, Spain ˜ati plaza 3, 20018 Donostia, Spain University of the Basque Country EHU/UPV, Donostiako Irakasleen Eskola, On
a r t i c l e i n f o
a b s t r a c t
Article history: Received 4 February 2009 Accepted 3 August 2009 Available online 11 August 2009
The colonization process by macrobenthic infauna after the completion of managed realignment on the fertile plain of Jaitzubia, along the Bidasoa estuary, is assessed here. The benthic invertebrate fauna was sampled annually for three years in the newly recovered intertidal areas. The results show a rapid colonization process. Six months after the completion of the restoration works, all the stations exhibited a large number of small opportunistic benthic species, as well as some large individuals of Hediste diversicolor, that dominated the biomass of the community. One year later, a new stage of development or succession towards the settlement of the Scrobicularia plana–Cerastoderma edule community was observed, showing a reduction of both abundance and species richness, and an increase in biomass, mainly due to the presence of individuals of S. plana (which were absent previously). The following year, a further reduction in the abundance and number of species was observed, as well as an increase in biomass, but on this occasion S. plana was the main contributor to community biomass. Evidence of the importance of passive or active dispersion in the adult stage of the species H. diversicolor and S. plana in the recovery process was also observed. Ó 2009 Elsevier Ltd. All rights reserved.
Keywords: benthic invertebrates managed realignment colonization estuary Hediste diversicolor Scrobicularia plana
1. Introduction Estuaries are ecological systems with intense biological activity and high levels of ecological production (Wolf, 1983; McLusky, 1989), and, historically, have provided many goods, uses and services to human populations which have settled nearby. As a consequence of the demographic increase, the biodiversity of these habitats has declined, mainly due to anthropogenic pollution and land reclamation (Costanza et al., 1997). Habitat loss has occurred over the past 300 years in many estuaries and coastal areas in developed countries through land claim for agriculture, port development, harbours, housing and infrastructure (Evans et al., 1998; Atkinson, 2003; McLusky and Elliott, 2004). Although in recent years they have been the sites of habitat gain, albeit to date on a smaller scale than the previous loss, 50–80% of wetlands have been lost from many estuaries along NW European and North American coastlines (Elliot and Cutts, 2004). It is now universally accepted, and in many cases legally demanded, that the long-standing adverse effects of human activities require that mitigation and/or compensation measures
* Corresponding author. E-mail address: [email protected] (M.A. Marquiegui). 0272-7714/$ – see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2009.08.001
are carried out (Madgwick and Jones, 2002). This constitutes the Response part of the DPSIR framework (Driving-Pressures-StateImpacts-Responses) (McLusky and Elliott, 2004). Added to this continuing anthropogenic loss there is also the potential for climate change and sea level rise to have an effect in the long term (Cardoso et al., 2008). As a result, it will be necessary to face new challenges to mitigate the effects of both direct habitat loss and these changing environmental conditions (Atkinson, 2003). Within the management action to restore or recreate estuarine habitats, managed realignment is growing in popularity, since the early 1990s, in its dual role of habitat restoration and as a ‘‘soft engineering’’ solution for the protection of estuaries in the face of sea level rise due to global warming (French, 2006; Garbutt et al., 2006; Elliott et al., 2007). The underlying rationale of the technique in the estuarine context is simple, i.e. to return land to the estuary, so as to allow salt marsh and intertidal mudflats to develop landward of those already in existence. The science of restoring coastal habitats which has been developed for three decades worldwide has largely focused on efforts to create and restore tidal wetlands (e.g. Zedler, 2001). In NW Europe the experience of creating new habitat, especially mudflats, is fairly limited and the majority of papers about managed realignment have concerned non-biological processes
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(e.g. Pethick, 1993; Watts et al., 2003). Studies involving the fauna of managed realignment sites have largely related to utilisation by fish (e.g. Colclough et al., 2005) and birds (Atkinson et al., 2004; Mander et al., 2007). Research on managed realignment sites of colonization by macrobenthic infauna and community development has been studied by Evans et al., 1998; Atkinson et al., 2004; French, 2006; Mazik et al., 2007. Other studies also briefly refer to invertebrate communities (e.g. Garbutt et al., 2006) but they are generally not the primary focus of most research. The River Bidasoa, a natural boundary between France and Spain in the Basque Country, has not escaped the effects of the human pressure. In the 17th century marsh reclamation was initiated and during the last century the estuarine areas have supported the construction of large railway stations on marsh and sandy areas on both sides of the border and The Hondarribia International Airport on an inter- and supra-tidal sandy area (Cearreta et al., 2004). The Bidasoa estuary currently covers less than 40% of its original surface area since post-Flandrian times (Rivas and Cendrero, 1992). The Bidasoa estuary received a high load of pollutants until the end of the 1990s generally from wastewater discharged from industrial installations and municipal sewage. Between 1995 and 2003, several water treatment programmes have been undertaken and the estuary has shown a progressive improvement in its ‘‘ecological status’’ (Uriarte and Borja, 2009; Borja et al., 2009), although important pressures and impacts still exist, including high population density, industry and port development (Borja et al., 2006). Despite these anthropogenic impacts, the Bidasoa estuary includes wetlands of great ecological value, especially for migratory birds, which have been left out of the urban development of the cities of Hondarribia and Irun, being a designated Wetland of International Importance by the Ramsar Convention, and Site of Community Importance and a Bird Special Protection Area in the Natura 2000 Network.
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Since September 2001, the Bidasoa estuary has been subject to ´n major transformations, including the project entitled ‘‘Restauracio Ambiental de Marismas de la Vega de Jaitzubia’’. As part of this project, 25 ha of farm land were restored mainly to salt marshes under tidal influence and to small fresh water wetlands. From 2004 to 2006, some studies on the river-bed and recovered areas were carried out in the area, including tidal dynamics and water, sediment and faunal analyses. The present paper focuses on invertebrate colonization and the development of the macrofaunal communities within the managed realignment site. 2. Material and methods 2.1. Study area The fertile plain of Jaitzubia (43 21 N, 148 W) is located in the middle region of the Bidasoa estuary (Fig. 1). Until the 18th century, this extensive flat area (70 ha) was under tidal influence, forming an arm of salt marshes with extensive reed-beds (Rivas and Cendrero, 1992). Subsequently, most of this area was dried out, forming a mosaic of Atlantic prairies and cultures, together with reed-beds along its borders and some small marshy areas. The primary aim of managed realignment was the establishment of salt marsh in their original conditions under tidal influence. The restoration project was started in November 2003 and concluded in October 2004. Existing dikes were demolished and sediment withdrawn to a 1.2–1.6 m tidal level. Tides in the Biscay bay are semidiurnal and its maximum range during spring tides reaches 4.5 m. 2.2. Sediment and faunal analysis Six stations (C1–C6) inside the managed realignment site were chosen to study benthic macroinfauna and sediment, each one
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situated in the recovered areas (Fig. 1). Samples were collected annually for three years, in June. In 2004 and 2005 samples were collected at all the stations. In 2006 benthic macrofauna sampling effort was reduced to three stations (C2, C3 and C4), situated in the central part of the area and with similar characteristics. Benthic macroinfauna was sampled using a 16 cm i.d. corer, i.e. 200 cm2 surface area to a depth of 20 cm. Five replicates were taken randomly at each station, separating the top layer of the sample (0–5 cm) from the remaining 15 cm (bottom layer). Each subsample thus obtained was kept separately and sieved through a 0.5 mm mesh sieve for the top layer and through a 1 mm for the bottom layer. This method, previously used in the same area (Garmendia et al., 2003), is considered as a good approximation of sieving the whole sample through a 0.5 mm mesh. Rodrigues et al. (2007) also consider this approximation as being efficient to characterize the macrofauna community basing on abundance, biomass and structure, in areas dominated by small individuals, thus minimizing the sample processing effort. The residue was preserved in 4% buffered formalin and stained with rose Bengal. The macrofauna was sorted then preserved in 70% ethanol. Specimens were identified to species level whenever possible, counted and preserved in 70% ethanol. The biomass of the macrofauna specimens was estimated as ash free dried weight, after ignition at 560 C for 6 h. The age of the individuals of Hediste diversicolor was estimated from the width of the 10th chaetiger (parapodia included). For individuals of Scrobicularia plana the age was estimated on the basis of their shell width. At each station (2004, 2005 and 2006) a single sediment sample was collected from the upper 5 cm, for particle size characterization and determination of organic matter content. The samples were dried at 105 C, for 24 h, then passed through a column of six sieves (aperture size from 2 mm to 0.063 mm) and, finally, the percentage of gravel (>2 mm), sand (2 mm – >0.063 mm) and mud (<0.063 mm) was calculated. Organic matter content was calculated using the loss-on-ignition method, by combusting the dry sample at 520 C, for 6 h. The sediment classification followed Larsonneur (1977) criteria for the fines content (below 5% – clean sand; 5–25% – muddy sand; 25–50% – sandy-mud, above 50% mud). Shannon–Wiener diversity index (Shannon and Weaver, 1963) and Pielou evenness index (Pielou, 1966) were calculated for each sampling event. A multivariate analysis of data was performed using the statistical software Primer (Clarke and Warwick, 2001). The Bray–Curtis measure of similarity on square root transformed data based on species biomass in each station was used to attain the matrix of similarity among stations. 3. Results
(SD 3.57). At all stations, with the exception of C5, a decrease in mud content and an increase in sand was observed during the study period. 3.2. Fauna A total number of 24 326 individuals belonging to 29 different taxa were collected in the 75 samples analyzed (5 replicates in each of the 15 stations analyzed in the three years, see Electronic supplementary material). 3.2.1. 2004 3.2.1.1. Density, biomass, composition and diversity. Six months after the completion of the restoration work benthic infauna was well represented in all stations: density varied between 15 320 and 26 740 ind. m2; species richness between 5 and 13 taxa and biomass between 0.74 and 7.67 g m2. Annelids were the dominant group, accounting for 94.8% of the total abundance in all the stations and 97.1% of the total biomass. Within this group, oligochaetes were most abundant in all stations, accounting for 89.2% of the total fauna and the 14.8% of the total biomass, while the polychaete Hediste diversicolor, found at the first four stations (C1–C4), accounted for 81.1% of the total biomass and only the 0.6% of the total abundance. As a consequence, Shannon– Wiener diversity (H0 ) and Pielou eveness (J) values were very low: H0 for the abundance between 0.14 and 1.00 bit, and between 0.15 and 0.99 bit for the biomass; J for the abundance between 0.08 and 0.31, and between 0.05 and 0.35 for the biomass. In addition, seven small opportunistic polychaete species (Manayunkia aestuarina, Polydora ligni, Polydora hoplura, Streblospio shrubsolii, Capitella capitata, Alkmaria romijni and Desdemona ornata) were collected. Estuarine crustaceans were poorly represented; only 8 individuals from 5 identified taxa (Carcinus maenas, Corophium multisetosum, Lekanesphaera rugicauda, Cyathura carinata and Talitridae) were collected. Insects represented more than half of all arthropods found, with Chironomid larvae being the most abundant arthropod. The gastropod Hydrobia ulvae was the only mollusc collected at the six stations studied 6 months after completion of the restoration works. Most of infaunal specimens were collected in the top layer (0– 5 cm) of the sample (between 93.37% and 99.03% of individuals in the stations C1–C5, and 81.52% in C6) while the bottom layer (to 20 cm) of the stations C1–C4 included the bulk of overall biomass (between 83.46% and 94.46%), due to the presence of large specimens of Hediste diversicolor in the bottom layer of these stations. No specimens of H. diversicolor were collected in the stations C5 and C6, so the bottom layer of these stations included a lower proportion of biomass (24.73% and 37.73%, respectively) than the top layer.
3.1. Sediment The sediment mud content of the 2004 campaign varied between 39.15% and 82.92% and, according to the Wentworth scale (Doeglas, 1968; Larsonneur, 1977), was classified as sandy-mud (C1, C5) and mud (C2, C3, C4 and C6). The organic matter content oscillated between 4.03% and 7.75%, with a mean of 5.47% (SD 1.62). In 2005, the mud content varied between 25.37% and 74.12% and sediments from the first five stations (C1–C5) were classified as sandy-mud. Sediment from C6 was classified as mud. The mean organic matter content oscillated between 3.35% and 10.04%, with a mean of 5.87% (SD 2.70). In 2006, the mud content varied between 10.02% and 37.54% and sediments were classified as muddy sand at stations C1–C4 and as sandy-mud at stations C5 and C6. The mean organic matter content oscillated between 3.81% and 13.21%, with a mean of 6.60%
3.2.1.2. Colonization by Hediste diversicolor. The individuals of Hediste diversicolor collected were relatively large, bearing in mind the short time that had elapsed between the completion of the restoration work and the sampling date (the recovered areas were flooded between January and February 2004, while sampling was conducted in June 2004, about 5–6 months later). The average weight of these individuals per replicate (0.0275 g; S.D. 0.0283) was much greater than that of individuals collected during the same period from river-bed samples (0.0030 g; S.D. 0.0049). The age of the colonizers H. diversicolor was estimated on the basis of their total length; however, due to the fact that many of them were fragmented, the total length was estimated from the width of the 10th chaetiger (parapodia included). The relationship between the width of the 10th chaetiger and other parameters, such as the total length and biomass, has been used in numerous studies on this ˜ ez, 1990; Sola, pers. comm.). In more than 60% species (Sola and Iban
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of H. diversicolor individuals, the width of the 10th chaetiger was greater than 4 mm. Based on the relationship between the width of the 10th chaetiger and the total length estimated by Sola (pers. comm.), these individuals of H. diversicolor would have a total length close to or longer than 100 mm. In the Bay of Txingudi, H. diversicolor specimens reach a mean body length of 48.4 mm in their first year (Sola, pers. comm.), much shorter than our large individuals of great body size. This would indicate that these individuals were clearly older than one year, probably close to 2 years or even older. In general, this species has been assigned a life cycle of 2 years, although exceptions exist with life cycles of 1 or 3 years (Sola, pers. comm.). This suggests that most of the H. diversicolor specimens colonizing these areas did so by means of the active or passive migration of adults from nearby areas. 3.2.1.3. Macrofauna assemblages. The analysis of the classification dendrogram of the samples in accordance with biomass (Fig. 2a) identified two sample clusters. First group is formed by the inner stations, C5 and C6. The community inhabiting these sites is dominated by oligochaetes and small arthropods as insect larvae. The second group is formed by the rest of the stations (C1–C4). Infaunal community is characterized by the presence of typical estuarine species (Hediste diversicolor, Manayunkia aestuarina, Polydora ligni, Hydrobia ulvae, Streblospio shrubsolii) that were absent in the other two stations. 3.2.2. 2005 3.2.2.1. Density, biomass, composition and diversity. One year later, benthic infauna was well represented in all stations: density (with the exception of station C6) varied between 3940 and
12 270 ind. m2; species richness between 7 and 12 taxa, and biomass between 4.04 and 36.85 g m2. In general, density values were lower, taxa number a little higher and biomass values clearly higher than those registered in 2004 samples. As in 2004, annelids dominated the community, accounting for 90.9% of the total abundance and 72.9% of the total biomass. Oligochaetes were most abundant at the inner stations (C4–C6), especially at station C6, where they reached a density of 82 980 ind. m2. Nevertheless, their number showed an important reduction compared to 2004, mainly at the stations C1, C2, C4 and C5. The polychaete Hediste diversicolor increased its distribution to five stations (C1–C5) and also increased its abundance in comparison with the previous year (66 ind. in 2004; 1036 ind. in 2005) and accounted for 62.6% of the total biomass. The bivalve mollusc Scrobicularia plana, absent from the 2004 samples, was detected at three stations (C2–C4), with a mean density of 183 ind. m2 and a mean biomass of 9.06 g m2. It accounted for 27.1% of the total faunal biomass. Shannon–Wiener diversity (H0 ) and Pielou evenness (J) values were low but higher than previous year, except at station C6 where values were very low due to the high abundance of oligochaetes. At stations C1–C5, H0 values for the abundance were between 1.16 and 2.12 bit, and between 0.5 and 1.25 bit for the biomass; J for the abundance was between 0.35 and 0.64, and between 0.17 and 0.37 for the biomass. Most of infaunal specimens were collected in the top layer (between 74.38% and 90.38% of individuals in the stations C1–C5, and 97.29% in C6) while the bottom layer of the stations C1–C5 included most of total biomass (between 80.3% and 93.92%), due to the presence of large specimens of Hediste diversicolor and
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Fig. 2. Similarities dendrogram of macrobenthic infauna for the biomass: a) Samples of 2004; b) Samples of 2004 and 2005; c) Samples of 2004–2006; d) Samples of the stations C2–C4 of 2004–2006.
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Scrobicularia plana in the bottom layer of these stations. All the specimens of S. plana collected were included in the bottom layer. No specimens of H. diversicolor or of S. plana were collected at the station C6 and, consequently, the bottom layer of C6 station included a very low proportion of biomass (2.89%). 3.2.2.2. Colonization by Scrobicularia plana. As with Hediste diversicolor in the samples from 2004, many of the 55 individuals of Scrobicularia plana collected in 2005 were larger than might be expected from a larval-settlement colonization of new intertidal areas. According to the life cycle of this species described by Sola (pers. comm.), the recruitment of S. plana in the Bay of Txingudi begins in July and finishes between October and January. Over wintering individuals (class 0þ) reach a maximum width of 12 mm at the beginning of the next summer, a maximum of 27 mm during the second summer (class1þ) and 32 mm during the third summer (class 2þ). The width of the measured individuals (Table 1) indicates that most belong to class 1þ or are older. Thus, the colonization of these areas by many of the S. plana individuals can be attributed to active or passive dispersal of adults from nearby areas. 3.2.2.3. Macrofauna assemblages. The analysis of the classification dendrogram of all the samples collected in 2004 and 2005 in accordance with biomass (Fig. 2b) identified three groups of samples. The first group is formed by the stations C5 and C6 of 2004 and C6 of 2005. The community inhabiting these sites is dominated by Oligochaetes and small arthropods as insect larvae. Second group is formed by the stations C1–C4 of 2004 and C5 of 2005. Infaunal community is characterized by the dominance of Oligochaetes, the presence of typical estuarine species as Hediste diversicolor, Hydrobia ulvae, Streblospio shrubsolii, Manayunkia aestuarina, Polydora ligni and the absence of Scrobicularia plana. The third group is formed by the stations C1–C4 of 2005 and the community is characterized by the dominance of species typical of the S. plana–Cerastoderma edule community, H. diversicolor, S. plana, H. ulvae, S. shrubsolii, Cyathura carinata.. Although S. plana was not collected at station C1, other typical species of this community (i.e. H. diversicolor, H. ulvae and C. carinata) are present in high densities.
than 76% of abundance. Oligochaetes abundance was very low in comparison with previous years. As a consequence, Shannon– Wiener diversity (H0 ) and Pielou evenness (J) values for the abundance were clearly higher than previous year, while values for the biomass were lower. H0 values for the abundance were comprised between 1.98 and 2.51 bit, and between 0.38 and 0.52 bit for the biomass; values of J for the abundance were between 0.77 and 0.79, and between 0.13 and 0.15 for the biomass. The abundance of infaunal specimens was more or less equally distributed in both layer (between 36.32% and 66.67% of individuals in the top layer; between 33.33% and 63.68% of individuals in the bottom layer) while almost all the biomass were included in the bottom layer (between 97.28% and 98.64%), due to the presence of large specimens of Scrobicularia plana in the bottom layer. 3.2.3.2. Macrofauna assemblages. The analysis of the classification dendrogram of all the samples collected in the three years in accordance with biomass (Fig. 2c) identified three groups of samples. The first and second groups are the same identified in the classification of samples of 2004 and 2005. The three new samples (C2–C4 in 2006) are included in the third group together with the stations C1–C4 of 2005. The community is characterized by the dominance of species typical of the Scrobicularia plana–Cerastoderma edule community, Hediste diversicolor, S. plana, Hydrobia ulvae, Streblospio shrubsolii and Cyathura carinata. 3.2.4. Stations C2–C4 in the study period (2004–2006) When the analysis is carried out using only stations C2–C4 (stations sampled yearly) (Fig. 2d), the classification dendrogram reveals three sample groups, each composed by samples from the same year, indicating the colonization process of the central part of the study area by benthic infauna from a community of transition to the Scrobicularia plana–Cerastoderma edule community (2004) to a typical S. plana–C. edule community (2005 and 2006). Moreover, the similarity between stations increased with time; thus indicating that they underwent a parallel evolution as regards their faunal composition and community structure. 4. Discussion
3.2.3. 2006 3.2.3.1. Density, biomass, composition and diversity. In 2006 only stations C2–C4 were sampled. In total, 655 specimens belonging to 10 taxa were obtained from the samples analyzed. Density varied between 2040 and 2390 ind. m2; species richness between 6 and 9 taxa; and biomass between 26.02 and 44.03 g m2. Density values and taxa number were lower than those registered in 2005 samples and biomass values clearly higher. Hediste diversicolor was the most abundant species and accounted for 32.1% of individuals. Scrobicularia plana was the second most abundant species (24.3%), but the most important one in terms of biomass (93%). Together with H. diversicolor (6.1% of the total biomass), both species accounted for more than 99% of the biomass of the community, and together with Hydrobia ulvae more Table 1 Scrobicularia plana abundance (ind. 0.1 m2) in different sizes and age classes and estimated age in the Bidasoa estuary. Stations
C2 C3 C4 Total Class Age
Size (mm) 4–8
8–12
12–16
16–20
20–24
24–28
– 2 –
1 2 1
1 4 3
2 2 4
2 3 4
1 2 7
6 0þ 0–1 year
35 1þ 1–2 year
28–32
32–36
– – – – 2þ 2–3 year
– 1 1 2 3þ >3 year
The results obtained in 2004 shown that the initial colonization of the newly created sites was rapid. 5–6 months after the completion of the recovery work, all the stations were inhabited by an infaunal community composed predominantly of early colonizing species including oligochaetes, insect larvae, and small polychaetes. Species typical of intertidal areas of the middle Bidasoa estuary as Hediste diversicolor, Hydrobia ulvae and Cyathura carinata were also present, mainly in the outer stations, but in very low abundance. The reasons why invertebrate colonization of newly created areas, is rapid in some cases but severely delayed in others are poorly understood (Atkinson et al., 2001). Colonization of a newly created site appears to be related to the availability of suitable sediments (Garbutt et al., 2006). Compaction of sediment caused by the earth-moving equipment may mean that the colonization of a created area by invertebrates is slower than expected (Evans et al., 1998). The presence of large individuals of H. diversicolor in the bottom layer of the sample suggests that from the beginning sediment characteristics were suitable for macrofauna to bury sufficiently deep in the sediment to avoid mortality by hard frosts or desiccation (Evans et al., 1998). In addition, the season of flooding, in spring, could have helped in the rapid colonization, because adults of some species (Hydrobia, Hediste) can disperse at that time (Evans et al., 1998). The 2005 results indicated a new step in the colonization process by invertebrate macrofauna. The overall abundance
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Peninsula (Junoy and Vie´itez, 1990; Curras and Mora, 1991; Borja et al., 2004) and dominates extensive intertidal areas of the Bidasoa estuary (Borja, 1988). The dominant taxa found in the core samples (S. plana, Hediste diversicolor, Streblospio shrubsolii, Cyathura carinata, and oligochaetes) are characteristic of the S. plana–C. edule community, and this composition is similar to that found in other intertidal areas of the same estuary, including the river-bed outside of the realignment site (Fig. 3). The rate of establishment of intertidal invertebrates can be related to their mobility both as adults and as juveniles where many have planktonic phases. Mobile species, and those that have planktonic larval stages, such as Hediste and other polychaetes, and Hydrobia, colonize more quickly than bivalves and other species that have no planktonic larval stage or take time to grow to a suitable size (Atkinson et al., 2001). Bivalves and the sediment they live in may be re-suspended and transported short distances through the water column or may travel along the bottom as bed load transport (Commito et al., 1995; Turner et al., 1997). These colonization steps, first by Hediste diversicolor and later by Scrobicularia plana, are similar to those described by Lewis et al. (2002, 2003) in Ireland after the defaunation caused by a pipeline construction in the estuary of Clonakilty Bay, show evidence of active or passive migration in the adult stage by H. diversicolor and S. plana. Adult migration has been demonstrated to be the predominant recovery mechanism following large-scale disturbances (Zajac et al., 1998). Hediste diversicolor is capable of active migration through the water column (Beukema et al., 1999), and although S. plana is capable of migrating horizontally (Hughes, 1970), sediment mobilization and deposition may have been an
decreased (the abundance of Oligochaetes and the polychaete Manayunkia aestuarina reduced considerably, and small polychaetes as Polydora ligni, Polydora hoplura and Desdemona ornata disappeared) whilst total biomass increased (the abundance of the polychaete Hediste diversicolor increased and several specimens of the bivalve Scrobicularia plana appeared for the first time) indicating that the small bodied, early colonizing species were being replaced by smaller numbers of larger bodied organism. These differences suggest a degree of development or succession within the macrobenthic community (Mander et al., 2007). In 2006 (stations C2–C4) the abundance and number of species continued to decline and the biomass continued to increase, however, with Scrobicularia plana now being the species that most contributed to the community biomass (>90%). More than 99% of the total biomass was made up by just two species S. plana and Hediste diversicolor. In the middle region of the Bidasoa estuary, S. plana is the dominant species in terms of biomass and, together with H. diversicolor, determines the biomass of the community of the S. plana–Cerastoderma edule (Sola, 1997). However, pollution caused by sewage discharges may result in the total or adult disappearance of S. plana and the proliferation of H. diversicolor (Garmendia et al., 2003). The biomass dominance transfer observed in the study period from H. diversicolor to S. plana is similar to that described by Garmendia et al., (2003) and indicates a better community structure at the end of the period. The parameters of the community structure indicated a successional step towards the typical characteristics of the Scrobicularia plana–Cerastoderma edule community. This community is well represented along the Cantabrian and Atlantic coasts of the Iberian
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Fig. 3. Similarities dendrogram of macrobenthic infauna for the biomass. C1–C6, samples of the managed realignment site of 2004–2006; R1–R6, samples of the river-bed, out of the realignment site of 2004 and 2005; St 8–12, samples of the middle region of the estuary of 2002 (Garmendia et al., 2003); St 4, sample of the middle region of the estuary of 2009 (Canto´n, pers. comm.).
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important cue for this species. The present study this provides further evidence of the role of adult migration in the re-establishment of the fauna of areas of managed realignment. Acknowledgements This study was supported by the Biodiversity Bureau of the Basque Government Environment Department and partially funded by Txingudi Zerbitzuak S.A. Thanks are due to Igor Cruz, Jose´ Marı´a Ruiz, Lourdes Canto´n and Maite Margeli for their contributions to the development of this project. We would also like to thank Fe´lix Izco (from the Gipuzkoa Provincial Government) for the loan of sampling equipment. Finally, our thanks to the staff of Plaiaundi Parke Ekologikoa for their helpful contributions. Appendix. Supplementary data The supplementary data associated with this article can be found in the on-line version at doi: 10.1016/j.ecss.2009.08.001. References Atkinson, P.W., Crooks, S., Grant, A., Rehfisch, M.M., 2001. The Success of Creation and Restoration Schemes in Producing Intertidal Habitat Suitable for Water Birds. English Nature Research Report No. 425. English Nature, Peterborough. Atkinson, P.W., 2003. Can we create or restore intertidal habitats for shorebirds? Wader Study Group Bulletin 100, 67–72. Atkinson, P.W., Crooks, S., Drewitt, A., Grant, A., Rehfisch, M.M., Sharpe, J., Tyas, C.J., 2004. Managed realignment in the UK – the first 5 years of colonization by birds. Wader Study Group Bulletin 146, 101–110. Beukema, J.J., Flach, E.C., Dekker, R., Starink, M., 1999. A longterm study of the recovery of the macrozoobenthos on large defaunated plots on a tidal flat in the Wadden Sea. Journal of Sea Research 42, 235–254. Borja, A., Aguirrezabalaga, F., Martı´nez, J., Sola, J.C., Garcı´a-Arberas, L., Gorostiaga, J.M., 2004. Benthic communities, biogeography and resources management. In: Borja, A., Collins, M. (Eds.), Oceanography and Marine Environment of the Basque Country. Elsevier Oceanography Series, vol. 70. Elsevier, Amsterdam, pp. 455–492. Borja, A., Galparsoro, I., Solaun, O., Muxika, I., Tello, E.M., Uriarte, A., Valencia, V., 2006. The European Water Framework Directive and the DPSIR, a methodological approach to assess the risk of failing to achieve good ecological status. Estuarine, Coastal and Shelf Science 66, 84–96. Borja, A., Muxika, I., Rodrı´guez, J.G., 2009. Paradigmatic responses of marine benthic communities to different anthropogenic pressures, using M-AMBI, within the European Water Framework Directive. Marine Ecology 30, 214–227. Borja, A., 1988. Estudio de los moluscos bivalvos de la rı´a de Fuenterrabı´a (N ˜ a), en mayo de 1987. Iberus 8, 187–202. Espan Cardoso, P.G., Raffaelli, D., Pardala, M.A., 2008. The impact of extreme weather events on the seagrass Zostera noltii and related Hydrobia ulvae population. Marine Pollution Bulletin 56, 483–492. Cearreta, A., Irabien Ma, J., Pascual, A., 2004. Human activities along the Basque coast during the last two centuries: geological perspective of recent anthropogenic impact on the coast and its environmental consequences. In: Borja, A., Collins, M. (Eds.), Oceanography and Marine Environment of the Basque Country. Elsevier Oceanography Series, vol. 70. Elsevier, Amsterdam, pp. 27–50. Clarke, K.R., Warwick, R.M., 2001. Change in Marine Communities. An Approach to Statistical Analysis and Interpretation, second ed. Primer-E Ltd, Plymouth. Commito, J.A., Thrush, S.F., Pridmore, R.D., Hewitt, J.E., Cummings, V.J., 1995. Dispersal dynamics in a winddriven benthic system. Limnology and Oceanography 40, 1513–1518. Colclough, S., Fonseca, L., Astley, T., Thomas, K., Watts, W., 2005. Fish utilisation of managed realignments. Fisheries Management and Ecology 12, 351–360. Costanza, R., d’Arge, R., de Groot, R., Farber, S., Grasso, M., Hannon, B., Naeem, S., Limburg, K., Paruelo, J., O’Neill, R.V., Raskin, R., Sutton, P., Van den Belt, M., 1997. The value of the world’s ecosystem services and natural capital. Nature 387, 253–260. Curras, A., Mora, J., 1991. Comunidades bento´nicas de la rı´a del Eo (Galicia–Asturias, ˜ a). Cahiers de Biologie Marine 32, 57–91. NW Espan Doeglas, D.J., 1968. Grain-size indices, classification and environment. Sedimentology 10, 83–100. Elliot, M., Cutts, N.D., 2004. Marine habitats: loss and gain, mitigation and compensation. Marine Pollution Bulletin 49, 671–674.
Elliott, M., Burdon, D., Hemingway, K.L., Apitz, S.E., 2007. Estuarine, coastal and marine ecosystem restoration: confusing management and science – a revision of concepts. Estuarine, Coastal and Shelf Science 74, 349–366. Evans, P.R., Ward, R.M., Bone, M., Leakey, M., 1998. Creation of temperate–climate intertidal mudflats: factors affecting colonization and use by benthic invertebrates and their bird predators. Marine Pollution Bulletin 37, 535–545. French, P.W., 2006. Managed realignment e the developing story of a comparatively new approach to soft engineering. Estuarine, Coastal and Shelf Science 67, 409–423. Garbutt, R.A., Reading, C.J., Wolters, M., Gray, A.J., Rothery, P., 2006. Monitoring the development of intertidal habitats on former agricultural land after the managed realignment of coastal defences at Tollesbury, Essex, UK. Marine Pollution Bulletin 53, 155–164. Garmendia, L., Marquiegui, M., Agirrezabalaga, F., Cruz, I., Canto´n, L., 2003. Efecto de la desaparicio´n de los vertidos de aguas residuales urbanas sobre la comunidad reducida de Macoma en las islas del estuario del Bidasoa (Golfo de Vizcaya). ˜ ol de Oceanografı´a 19, 265–281. Boletı´n del Instituto Espan Hughes, R.N., 1970. Population dynamics of the bivalve Scrobicularia plana (da Costa) on an intertidal mud-flat in North Wales. Journal of Animal Ecology 39, 333–356. Junoy, J., Vie´itez, J.M., 1990. Macrozoobenthic community structure in the Rı´a de Foz, an intertidal estuary (Galicia, Northwest Spain). Marine Biology 107, 329–339. Larsonneur, C., 1977. La cartographie des depots muebles sur le plateau continental français: me´thode mise au point et utilise´e en Manche. Journal de Recherche Oce´anographique 2, 33–39. Lewis, L.J., Davenport, J., Kelly, T.C., 2002. A study of the impact of a pipeline construction on estuarine benthic invertebrate communities. Estuarine, Coastal and Shelf Science 55, 213–221. Lewis, L.J., Davenport, J., Kelly, T.C., 2003. 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Muller) en el estuario del Bidasoa. Bentos 6, 69–79. Sola, J.C., 1997. Dina´mica de la comunidad reducida de Macoma en el estuario del Bidasoa, Guipu´zcoa (golfo de Vizcaya). Publicaciones Especiales del Instituto ˜ ol de Oceanografı´a 23, 83–92. Espan Turner, S.J., Grant, J., Pridmore, R.D., Hewitt, J.E., Wilkinson, M.R., Hume, T.M., Morrisey, D.J., 1997. Bedload and water-column transport and colonization processes by post-settlement benthic macrofauna: does infaunal density matter? Journal of Experimental Marine Biology and Ecology 216, 51–75. Uriarte, A., Borja, A., 2009. Assessing fish quality status in transitional waters, within the European Water Framework Directive: setting boundary classes and responding to anthropogenic pressures. Estuarine, Coastal and Shelf Science 82, 214–224. Watts, C.W., Tolhurst, T.J., Black, K.S., Whitmore, A.P., 2003. In situ measurements of erosion shear stress and geotechnical shear strength of the intertidal sediments of the experimental managed realignment scheme at Tollesbury, Essex, UK. Estuarine, Coastal and Shelf Science 58, 611–620. Wolf, W.J., 1983. Estuarine benthos. In: Ketchum, B.H. (Ed.), Ecosystems of the World. Estuaries and Enclosed Seas, vol. 26. Elsevier, Amsterdam, pp. 151–182. Zajac, R.N., Whitlatch, R.B., Thrush, S.F., 1998. Recolonization and succession in softsediment infaunal communities: the spatial scale of controlling factors. Hydrobiology 375376, 227–240. Zedler, J.B., 2001. Handbook for Restoring Tidal Wetlands. CRC Press, New York. pp. 439.
Contents lists available at ScienceDirect
Estuarine, Coastal and Shelf Science journal homepage: www.elsevier.com/locate/ecss
Colonization process by macrobenthic infauna after a managed coastal realignment in the Bidasoa estuary (Bay of Biscay, NE Atlantic) Mikel A. Marquiegui a, *, Florencio Aguirrezabalaga a, b a b
S.C. INSUB, Museo Okendo, Zemoria, 12, Apdo 3223, 20013 Donostia, Spain ˜ati plaza 3, 20018 Donostia, Spain University of the Basque Country EHU/UPV, Donostiako Irakasleen Eskola, On
a r t i c l e i n f o
a b s t r a c t
Article history: Received 4 February 2009 Accepted 3 August 2009 Available online 11 August 2009
The colonization process by macrobenthic infauna after the completion of managed realignment on the fertile plain of Jaitzubia, along the Bidasoa estuary, is assessed here. The benthic invertebrate fauna was sampled annually for three years in the newly recovered intertidal areas. The results show a rapid colonization process. Six months after the completion of the restoration works, all the stations exhibited a large number of small opportunistic benthic species, as well as some large individuals of Hediste diversicolor, that dominated the biomass of the community. One year later, a new stage of development or succession towards the settlement of the Scrobicularia plana–Cerastoderma edule community was observed, showing a reduction of both abundance and species richness, and an increase in biomass, mainly due to the presence of individuals of S. plana (which were absent previously). The following year, a further reduction in the abundance and number of species was observed, as well as an increase in biomass, but on this occasion S. plana was the main contributor to community biomass. Evidence of the importance of passive or active dispersion in the adult stage of the species H. diversicolor and S. plana in the recovery process was also observed. Ó 2009 Elsevier Ltd. All rights reserved.
Keywords: benthic invertebrates managed realignment colonization estuary Hediste diversicolor Scrobicularia plana
1. Introduction Estuaries are ecological systems with intense biological activity and high levels of ecological production (Wolf, 1983; McLusky, 1989), and, historically, have provided many goods, uses and services to human populations which have settled nearby. As a consequence of the demographic increase, the biodiversity of these habitats has declined, mainly due to anthropogenic pollution and land reclamation (Costanza et al., 1997). Habitat loss has occurred over the past 300 years in many estuaries and coastal areas in developed countries through land claim for agriculture, port development, harbours, housing and infrastructure (Evans et al., 1998; Atkinson, 2003; McLusky and Elliott, 2004). Although in recent years they have been the sites of habitat gain, albeit to date on a smaller scale than the previous loss, 50–80% of wetlands have been lost from many estuaries along NW European and North American coastlines (Elliot and Cutts, 2004). It is now universally accepted, and in many cases legally demanded, that the long-standing adverse effects of human activities require that mitigation and/or compensation measures
* Corresponding author. E-mail address: [email protected] (M.A. Marquiegui). 0272-7714/$ – see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2009.08.001
are carried out (Madgwick and Jones, 2002). This constitutes the Response part of the DPSIR framework (Driving-Pressures-StateImpacts-Responses) (McLusky and Elliott, 2004). Added to this continuing anthropogenic loss there is also the potential for climate change and sea level rise to have an effect in the long term (Cardoso et al., 2008). As a result, it will be necessary to face new challenges to mitigate the effects of both direct habitat loss and these changing environmental conditions (Atkinson, 2003). Within the management action to restore or recreate estuarine habitats, managed realignment is growing in popularity, since the early 1990s, in its dual role of habitat restoration and as a ‘‘soft engineering’’ solution for the protection of estuaries in the face of sea level rise due to global warming (French, 2006; Garbutt et al., 2006; Elliott et al., 2007). The underlying rationale of the technique in the estuarine context is simple, i.e. to return land to the estuary, so as to allow salt marsh and intertidal mudflats to develop landward of those already in existence. The science of restoring coastal habitats which has been developed for three decades worldwide has largely focused on efforts to create and restore tidal wetlands (e.g. Zedler, 2001). In NW Europe the experience of creating new habitat, especially mudflats, is fairly limited and the majority of papers about managed realignment have concerned non-biological processes
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(e.g. Pethick, 1993; Watts et al., 2003). Studies involving the fauna of managed realignment sites have largely related to utilisation by fish (e.g. Colclough et al., 2005) and birds (Atkinson et al., 2004; Mander et al., 2007). Research on managed realignment sites of colonization by macrobenthic infauna and community development has been studied by Evans et al., 1998; Atkinson et al., 2004; French, 2006; Mazik et al., 2007. Other studies also briefly refer to invertebrate communities (e.g. Garbutt et al., 2006) but they are generally not the primary focus of most research. The River Bidasoa, a natural boundary between France and Spain in the Basque Country, has not escaped the effects of the human pressure. In the 17th century marsh reclamation was initiated and during the last century the estuarine areas have supported the construction of large railway stations on marsh and sandy areas on both sides of the border and The Hondarribia International Airport on an inter- and supra-tidal sandy area (Cearreta et al., 2004). The Bidasoa estuary currently covers less than 40% of its original surface area since post-Flandrian times (Rivas and Cendrero, 1992). The Bidasoa estuary received a high load of pollutants until the end of the 1990s generally from wastewater discharged from industrial installations and municipal sewage. Between 1995 and 2003, several water treatment programmes have been undertaken and the estuary has shown a progressive improvement in its ‘‘ecological status’’ (Uriarte and Borja, 2009; Borja et al., 2009), although important pressures and impacts still exist, including high population density, industry and port development (Borja et al., 2006). Despite these anthropogenic impacts, the Bidasoa estuary includes wetlands of great ecological value, especially for migratory birds, which have been left out of the urban development of the cities of Hondarribia and Irun, being a designated Wetland of International Importance by the Ramsar Convention, and Site of Community Importance and a Bird Special Protection Area in the Natura 2000 Network.
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Since September 2001, the Bidasoa estuary has been subject to ´n major transformations, including the project entitled ‘‘Restauracio Ambiental de Marismas de la Vega de Jaitzubia’’. As part of this project, 25 ha of farm land were restored mainly to salt marshes under tidal influence and to small fresh water wetlands. From 2004 to 2006, some studies on the river-bed and recovered areas were carried out in the area, including tidal dynamics and water, sediment and faunal analyses. The present paper focuses on invertebrate colonization and the development of the macrofaunal communities within the managed realignment site. 2. Material and methods 2.1. Study area The fertile plain of Jaitzubia (43 21 N, 148 W) is located in the middle region of the Bidasoa estuary (Fig. 1). Until the 18th century, this extensive flat area (70 ha) was under tidal influence, forming an arm of salt marshes with extensive reed-beds (Rivas and Cendrero, 1992). Subsequently, most of this area was dried out, forming a mosaic of Atlantic prairies and cultures, together with reed-beds along its borders and some small marshy areas. The primary aim of managed realignment was the establishment of salt marsh in their original conditions under tidal influence. The restoration project was started in November 2003 and concluded in October 2004. Existing dikes were demolished and sediment withdrawn to a 1.2–1.6 m tidal level. Tides in the Biscay bay are semidiurnal and its maximum range during spring tides reaches 4.5 m. 2.2. Sediment and faunal analysis Six stations (C1–C6) inside the managed realignment site were chosen to study benthic macroinfauna and sediment, each one
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Fig. 1. Map of the study area showing sampling stations.
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situated in the recovered areas (Fig. 1). Samples were collected annually for three years, in June. In 2004 and 2005 samples were collected at all the stations. In 2006 benthic macrofauna sampling effort was reduced to three stations (C2, C3 and C4), situated in the central part of the area and with similar characteristics. Benthic macroinfauna was sampled using a 16 cm i.d. corer, i.e. 200 cm2 surface area to a depth of 20 cm. Five replicates were taken randomly at each station, separating the top layer of the sample (0–5 cm) from the remaining 15 cm (bottom layer). Each subsample thus obtained was kept separately and sieved through a 0.5 mm mesh sieve for the top layer and through a 1 mm for the bottom layer. This method, previously used in the same area (Garmendia et al., 2003), is considered as a good approximation of sieving the whole sample through a 0.5 mm mesh. Rodrigues et al. (2007) also consider this approximation as being efficient to characterize the macrofauna community basing on abundance, biomass and structure, in areas dominated by small individuals, thus minimizing the sample processing effort. The residue was preserved in 4% buffered formalin and stained with rose Bengal. The macrofauna was sorted then preserved in 70% ethanol. Specimens were identified to species level whenever possible, counted and preserved in 70% ethanol. The biomass of the macrofauna specimens was estimated as ash free dried weight, after ignition at 560 C for 6 h. The age of the individuals of Hediste diversicolor was estimated from the width of the 10th chaetiger (parapodia included). For individuals of Scrobicularia plana the age was estimated on the basis of their shell width. At each station (2004, 2005 and 2006) a single sediment sample was collected from the upper 5 cm, for particle size characterization and determination of organic matter content. The samples were dried at 105 C, for 24 h, then passed through a column of six sieves (aperture size from 2 mm to 0.063 mm) and, finally, the percentage of gravel (>2 mm), sand (2 mm – >0.063 mm) and mud (<0.063 mm) was calculated. Organic matter content was calculated using the loss-on-ignition method, by combusting the dry sample at 520 C, for 6 h. The sediment classification followed Larsonneur (1977) criteria for the fines content (below 5% – clean sand; 5–25% – muddy sand; 25–50% – sandy-mud, above 50% mud). Shannon–Wiener diversity index (Shannon and Weaver, 1963) and Pielou evenness index (Pielou, 1966) were calculated for each sampling event. A multivariate analysis of data was performed using the statistical software Primer (Clarke and Warwick, 2001). The Bray–Curtis measure of similarity on square root transformed data based on species biomass in each station was used to attain the matrix of similarity among stations. 3. Results
(SD 3.57). At all stations, with the exception of C5, a decrease in mud content and an increase in sand was observed during the study period. 3.2. Fauna A total number of 24 326 individuals belonging to 29 different taxa were collected in the 75 samples analyzed (5 replicates in each of the 15 stations analyzed in the three years, see Electronic supplementary material). 3.2.1. 2004 3.2.1.1. Density, biomass, composition and diversity. Six months after the completion of the restoration work benthic infauna was well represented in all stations: density varied between 15 320 and 26 740 ind. m2; species richness between 5 and 13 taxa and biomass between 0.74 and 7.67 g m2. Annelids were the dominant group, accounting for 94.8% of the total abundance in all the stations and 97.1% of the total biomass. Within this group, oligochaetes were most abundant in all stations, accounting for 89.2% of the total fauna and the 14.8% of the total biomass, while the polychaete Hediste diversicolor, found at the first four stations (C1–C4), accounted for 81.1% of the total biomass and only the 0.6% of the total abundance. As a consequence, Shannon– Wiener diversity (H0 ) and Pielou eveness (J) values were very low: H0 for the abundance between 0.14 and 1.00 bit, and between 0.15 and 0.99 bit for the biomass; J for the abundance between 0.08 and 0.31, and between 0.05 and 0.35 for the biomass. In addition, seven small opportunistic polychaete species (Manayunkia aestuarina, Polydora ligni, Polydora hoplura, Streblospio shrubsolii, Capitella capitata, Alkmaria romijni and Desdemona ornata) were collected. Estuarine crustaceans were poorly represented; only 8 individuals from 5 identified taxa (Carcinus maenas, Corophium multisetosum, Lekanesphaera rugicauda, Cyathura carinata and Talitridae) were collected. Insects represented more than half of all arthropods found, with Chironomid larvae being the most abundant arthropod. The gastropod Hydrobia ulvae was the only mollusc collected at the six stations studied 6 months after completion of the restoration works. Most of infaunal specimens were collected in the top layer (0– 5 cm) of the sample (between 93.37% and 99.03% of individuals in the stations C1–C5, and 81.52% in C6) while the bottom layer (to 20 cm) of the stations C1–C4 included the bulk of overall biomass (between 83.46% and 94.46%), due to the presence of large specimens of Hediste diversicolor in the bottom layer of these stations. No specimens of H. diversicolor were collected in the stations C5 and C6, so the bottom layer of these stations included a lower proportion of biomass (24.73% and 37.73%, respectively) than the top layer.
3.1. Sediment The sediment mud content of the 2004 campaign varied between 39.15% and 82.92% and, according to the Wentworth scale (Doeglas, 1968; Larsonneur, 1977), was classified as sandy-mud (C1, C5) and mud (C2, C3, C4 and C6). The organic matter content oscillated between 4.03% and 7.75%, with a mean of 5.47% (SD 1.62). In 2005, the mud content varied between 25.37% and 74.12% and sediments from the first five stations (C1–C5) were classified as sandy-mud. Sediment from C6 was classified as mud. The mean organic matter content oscillated between 3.35% and 10.04%, with a mean of 5.87% (SD 2.70). In 2006, the mud content varied between 10.02% and 37.54% and sediments were classified as muddy sand at stations C1–C4 and as sandy-mud at stations C5 and C6. The mean organic matter content oscillated between 3.81% and 13.21%, with a mean of 6.60%
3.2.1.2. Colonization by Hediste diversicolor. The individuals of Hediste diversicolor collected were relatively large, bearing in mind the short time that had elapsed between the completion of the restoration work and the sampling date (the recovered areas were flooded between January and February 2004, while sampling was conducted in June 2004, about 5–6 months later). The average weight of these individuals per replicate (0.0275 g; S.D. 0.0283) was much greater than that of individuals collected during the same period from river-bed samples (0.0030 g; S.D. 0.0049). The age of the colonizers H. diversicolor was estimated on the basis of their total length; however, due to the fact that many of them were fragmented, the total length was estimated from the width of the 10th chaetiger (parapodia included). The relationship between the width of the 10th chaetiger and other parameters, such as the total length and biomass, has been used in numerous studies on this ˜ ez, 1990; Sola, pers. comm.). In more than 60% species (Sola and Iban
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of H. diversicolor individuals, the width of the 10th chaetiger was greater than 4 mm. Based on the relationship between the width of the 10th chaetiger and the total length estimated by Sola (pers. comm.), these individuals of H. diversicolor would have a total length close to or longer than 100 mm. In the Bay of Txingudi, H. diversicolor specimens reach a mean body length of 48.4 mm in their first year (Sola, pers. comm.), much shorter than our large individuals of great body size. This would indicate that these individuals were clearly older than one year, probably close to 2 years or even older. In general, this species has been assigned a life cycle of 2 years, although exceptions exist with life cycles of 1 or 3 years (Sola, pers. comm.). This suggests that most of the H. diversicolor specimens colonizing these areas did so by means of the active or passive migration of adults from nearby areas. 3.2.1.3. Macrofauna assemblages. The analysis of the classification dendrogram of the samples in accordance with biomass (Fig. 2a) identified two sample clusters. First group is formed by the inner stations, C5 and C6. The community inhabiting these sites is dominated by oligochaetes and small arthropods as insect larvae. The second group is formed by the rest of the stations (C1–C4). Infaunal community is characterized by the presence of typical estuarine species (Hediste diversicolor, Manayunkia aestuarina, Polydora ligni, Hydrobia ulvae, Streblospio shrubsolii) that were absent in the other two stations. 3.2.2. 2005 3.2.2.1. Density, biomass, composition and diversity. One year later, benthic infauna was well represented in all stations: density (with the exception of station C6) varied between 3940 and
12 270 ind. m2; species richness between 7 and 12 taxa, and biomass between 4.04 and 36.85 g m2. In general, density values were lower, taxa number a little higher and biomass values clearly higher than those registered in 2004 samples. As in 2004, annelids dominated the community, accounting for 90.9% of the total abundance and 72.9% of the total biomass. Oligochaetes were most abundant at the inner stations (C4–C6), especially at station C6, where they reached a density of 82 980 ind. m2. Nevertheless, their number showed an important reduction compared to 2004, mainly at the stations C1, C2, C4 and C5. The polychaete Hediste diversicolor increased its distribution to five stations (C1–C5) and also increased its abundance in comparison with the previous year (66 ind. in 2004; 1036 ind. in 2005) and accounted for 62.6% of the total biomass. The bivalve mollusc Scrobicularia plana, absent from the 2004 samples, was detected at three stations (C2–C4), with a mean density of 183 ind. m2 and a mean biomass of 9.06 g m2. It accounted for 27.1% of the total faunal biomass. Shannon–Wiener diversity (H0 ) and Pielou evenness (J) values were low but higher than previous year, except at station C6 where values were very low due to the high abundance of oligochaetes. At stations C1–C5, H0 values for the abundance were between 1.16 and 2.12 bit, and between 0.5 and 1.25 bit for the biomass; J for the abundance was between 0.35 and 0.64, and between 0.17 and 0.37 for the biomass. Most of infaunal specimens were collected in the top layer (between 74.38% and 90.38% of individuals in the stations C1–C5, and 97.29% in C6) while the bottom layer of the stations C1–C5 included most of total biomass (between 80.3% and 93.92%), due to the presence of large specimens of Hediste diversicolor and
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Scrobicularia plana in the bottom layer of these stations. All the specimens of S. plana collected were included in the bottom layer. No specimens of H. diversicolor or of S. plana were collected at the station C6 and, consequently, the bottom layer of C6 station included a very low proportion of biomass (2.89%). 3.2.2.2. Colonization by Scrobicularia plana. As with Hediste diversicolor in the samples from 2004, many of the 55 individuals of Scrobicularia plana collected in 2005 were larger than might be expected from a larval-settlement colonization of new intertidal areas. According to the life cycle of this species described by Sola (pers. comm.), the recruitment of S. plana in the Bay of Txingudi begins in July and finishes between October and January. Over wintering individuals (class 0þ) reach a maximum width of 12 mm at the beginning of the next summer, a maximum of 27 mm during the second summer (class1þ) and 32 mm during the third summer (class 2þ). The width of the measured individuals (Table 1) indicates that most belong to class 1þ or are older. Thus, the colonization of these areas by many of the S. plana individuals can be attributed to active or passive dispersal of adults from nearby areas. 3.2.2.3. Macrofauna assemblages. The analysis of the classification dendrogram of all the samples collected in 2004 and 2005 in accordance with biomass (Fig. 2b) identified three groups of samples. The first group is formed by the stations C5 and C6 of 2004 and C6 of 2005. The community inhabiting these sites is dominated by Oligochaetes and small arthropods as insect larvae. Second group is formed by the stations C1–C4 of 2004 and C5 of 2005. Infaunal community is characterized by the dominance of Oligochaetes, the presence of typical estuarine species as Hediste diversicolor, Hydrobia ulvae, Streblospio shrubsolii, Manayunkia aestuarina, Polydora ligni and the absence of Scrobicularia plana. The third group is formed by the stations C1–C4 of 2005 and the community is characterized by the dominance of species typical of the S. plana–Cerastoderma edule community, H. diversicolor, S. plana, H. ulvae, S. shrubsolii, Cyathura carinata.. Although S. plana was not collected at station C1, other typical species of this community (i.e. H. diversicolor, H. ulvae and C. carinata) are present in high densities.
than 76% of abundance. Oligochaetes abundance was very low in comparison with previous years. As a consequence, Shannon– Wiener diversity (H0 ) and Pielou evenness (J) values for the abundance were clearly higher than previous year, while values for the biomass were lower. H0 values for the abundance were comprised between 1.98 and 2.51 bit, and between 0.38 and 0.52 bit for the biomass; values of J for the abundance were between 0.77 and 0.79, and between 0.13 and 0.15 for the biomass. The abundance of infaunal specimens was more or less equally distributed in both layer (between 36.32% and 66.67% of individuals in the top layer; between 33.33% and 63.68% of individuals in the bottom layer) while almost all the biomass were included in the bottom layer (between 97.28% and 98.64%), due to the presence of large specimens of Scrobicularia plana in the bottom layer. 3.2.3.2. Macrofauna assemblages. The analysis of the classification dendrogram of all the samples collected in the three years in accordance with biomass (Fig. 2c) identified three groups of samples. The first and second groups are the same identified in the classification of samples of 2004 and 2005. The three new samples (C2–C4 in 2006) are included in the third group together with the stations C1–C4 of 2005. The community is characterized by the dominance of species typical of the Scrobicularia plana–Cerastoderma edule community, Hediste diversicolor, S. plana, Hydrobia ulvae, Streblospio shrubsolii and Cyathura carinata. 3.2.4. Stations C2–C4 in the study period (2004–2006) When the analysis is carried out using only stations C2–C4 (stations sampled yearly) (Fig. 2d), the classification dendrogram reveals three sample groups, each composed by samples from the same year, indicating the colonization process of the central part of the study area by benthic infauna from a community of transition to the Scrobicularia plana–Cerastoderma edule community (2004) to a typical S. plana–C. edule community (2005 and 2006). Moreover, the similarity between stations increased with time; thus indicating that they underwent a parallel evolution as regards their faunal composition and community structure. 4. Discussion
3.2.3. 2006 3.2.3.1. Density, biomass, composition and diversity. In 2006 only stations C2–C4 were sampled. In total, 655 specimens belonging to 10 taxa were obtained from the samples analyzed. Density varied between 2040 and 2390 ind. m2; species richness between 6 and 9 taxa; and biomass between 26.02 and 44.03 g m2. Density values and taxa number were lower than those registered in 2005 samples and biomass values clearly higher. Hediste diversicolor was the most abundant species and accounted for 32.1% of individuals. Scrobicularia plana was the second most abundant species (24.3%), but the most important one in terms of biomass (93%). Together with H. diversicolor (6.1% of the total biomass), both species accounted for more than 99% of the biomass of the community, and together with Hydrobia ulvae more Table 1 Scrobicularia plana abundance (ind. 0.1 m2) in different sizes and age classes and estimated age in the Bidasoa estuary. Stations
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8–12
12–16
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1 4 3
2 2 4
2 3 4
1 2 7
6 0þ 0–1 year
35 1þ 1–2 year
28–32
32–36
– – – – 2þ 2–3 year
– 1 1 2 3þ >3 year
The results obtained in 2004 shown that the initial colonization of the newly created sites was rapid. 5–6 months after the completion of the recovery work, all the stations were inhabited by an infaunal community composed predominantly of early colonizing species including oligochaetes, insect larvae, and small polychaetes. Species typical of intertidal areas of the middle Bidasoa estuary as Hediste diversicolor, Hydrobia ulvae and Cyathura carinata were also present, mainly in the outer stations, but in very low abundance. The reasons why invertebrate colonization of newly created areas, is rapid in some cases but severely delayed in others are poorly understood (Atkinson et al., 2001). Colonization of a newly created site appears to be related to the availability of suitable sediments (Garbutt et al., 2006). Compaction of sediment caused by the earth-moving equipment may mean that the colonization of a created area by invertebrates is slower than expected (Evans et al., 1998). The presence of large individuals of H. diversicolor in the bottom layer of the sample suggests that from the beginning sediment characteristics were suitable for macrofauna to bury sufficiently deep in the sediment to avoid mortality by hard frosts or desiccation (Evans et al., 1998). In addition, the season of flooding, in spring, could have helped in the rapid colonization, because adults of some species (Hydrobia, Hediste) can disperse at that time (Evans et al., 1998). The 2005 results indicated a new step in the colonization process by invertebrate macrofauna. The overall abundance
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Peninsula (Junoy and Vie´itez, 1990; Curras and Mora, 1991; Borja et al., 2004) and dominates extensive intertidal areas of the Bidasoa estuary (Borja, 1988). The dominant taxa found in the core samples (S. plana, Hediste diversicolor, Streblospio shrubsolii, Cyathura carinata, and oligochaetes) are characteristic of the S. plana–C. edule community, and this composition is similar to that found in other intertidal areas of the same estuary, including the river-bed outside of the realignment site (Fig. 3). The rate of establishment of intertidal invertebrates can be related to their mobility both as adults and as juveniles where many have planktonic phases. Mobile species, and those that have planktonic larval stages, such as Hediste and other polychaetes, and Hydrobia, colonize more quickly than bivalves and other species that have no planktonic larval stage or take time to grow to a suitable size (Atkinson et al., 2001). Bivalves and the sediment they live in may be re-suspended and transported short distances through the water column or may travel along the bottom as bed load transport (Commito et al., 1995; Turner et al., 1997). These colonization steps, first by Hediste diversicolor and later by Scrobicularia plana, are similar to those described by Lewis et al. (2002, 2003) in Ireland after the defaunation caused by a pipeline construction in the estuary of Clonakilty Bay, show evidence of active or passive migration in the adult stage by H. diversicolor and S. plana. Adult migration has been demonstrated to be the predominant recovery mechanism following large-scale disturbances (Zajac et al., 1998). Hediste diversicolor is capable of active migration through the water column (Beukema et al., 1999), and although S. plana is capable of migrating horizontally (Hughes, 1970), sediment mobilization and deposition may have been an
decreased (the abundance of Oligochaetes and the polychaete Manayunkia aestuarina reduced considerably, and small polychaetes as Polydora ligni, Polydora hoplura and Desdemona ornata disappeared) whilst total biomass increased (the abundance of the polychaete Hediste diversicolor increased and several specimens of the bivalve Scrobicularia plana appeared for the first time) indicating that the small bodied, early colonizing species were being replaced by smaller numbers of larger bodied organism. These differences suggest a degree of development or succession within the macrobenthic community (Mander et al., 2007). In 2006 (stations C2–C4) the abundance and number of species continued to decline and the biomass continued to increase, however, with Scrobicularia plana now being the species that most contributed to the community biomass (>90%). More than 99% of the total biomass was made up by just two species S. plana and Hediste diversicolor. In the middle region of the Bidasoa estuary, S. plana is the dominant species in terms of biomass and, together with H. diversicolor, determines the biomass of the community of the S. plana–Cerastoderma edule (Sola, 1997). However, pollution caused by sewage discharges may result in the total or adult disappearance of S. plana and the proliferation of H. diversicolor (Garmendia et al., 2003). The biomass dominance transfer observed in the study period from H. diversicolor to S. plana is similar to that described by Garmendia et al., (2003) and indicates a better community structure at the end of the period. The parameters of the community structure indicated a successional step towards the typical characteristics of the Scrobicularia plana–Cerastoderma edule community. This community is well represented along the Cantabrian and Atlantic coasts of the Iberian
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important cue for this species. The present study this provides further evidence of the role of adult migration in the re-establishment of the fauna of areas of managed realignment. Acknowledgements This study was supported by the Biodiversity Bureau of the Basque Government Environment Department and partially funded by Txingudi Zerbitzuak S.A. Thanks are due to Igor Cruz, Jose´ Marı´a Ruiz, Lourdes Canto´n and Maite Margeli for their contributions to the development of this project. We would also like to thank Fe´lix Izco (from the Gipuzkoa Provincial Government) for the loan of sampling equipment. Finally, our thanks to the staff of Plaiaundi Parke Ekologikoa for their helpful contributions. Appendix. Supplementary data The supplementary data associated with this article can be found in the on-line version at doi: 10.1016/j.ecss.2009.08.001. References Atkinson, P.W., Crooks, S., Grant, A., Rehfisch, M.M., 2001. The Success of Creation and Restoration Schemes in Producing Intertidal Habitat Suitable for Water Birds. English Nature Research Report No. 425. English Nature, Peterborough. Atkinson, P.W., 2003. Can we create or restore intertidal habitats for shorebirds? Wader Study Group Bulletin 100, 67–72. Atkinson, P.W., Crooks, S., Drewitt, A., Grant, A., Rehfisch, M.M., Sharpe, J., Tyas, C.J., 2004. Managed realignment in the UK – the first 5 years of colonization by birds. Wader Study Group Bulletin 146, 101–110. Beukema, J.J., Flach, E.C., Dekker, R., Starink, M., 1999. A longterm study of the recovery of the macrozoobenthos on large defaunated plots on a tidal flat in the Wadden Sea. Journal of Sea Research 42, 235–254. Borja, A., Aguirrezabalaga, F., Martı´nez, J., Sola, J.C., Garcı´a-Arberas, L., Gorostiaga, J.M., 2004. Benthic communities, biogeography and resources management. In: Borja, A., Collins, M. (Eds.), Oceanography and Marine Environment of the Basque Country. Elsevier Oceanography Series, vol. 70. Elsevier, Amsterdam, pp. 455–492. Borja, A., Galparsoro, I., Solaun, O., Muxika, I., Tello, E.M., Uriarte, A., Valencia, V., 2006. The European Water Framework Directive and the DPSIR, a methodological approach to assess the risk of failing to achieve good ecological status. Estuarine, Coastal and Shelf Science 66, 84–96. Borja, A., Muxika, I., Rodrı´guez, J.G., 2009. Paradigmatic responses of marine benthic communities to different anthropogenic pressures, using M-AMBI, within the European Water Framework Directive. Marine Ecology 30, 214–227. Borja, A., 1988. Estudio de los moluscos bivalvos de la rı´a de Fuenterrabı´a (N ˜ a), en mayo de 1987. Iberus 8, 187–202. Espan Cardoso, P.G., Raffaelli, D., Pardala, M.A., 2008. The impact of extreme weather events on the seagrass Zostera noltii and related Hydrobia ulvae population. Marine Pollution Bulletin 56, 483–492. Cearreta, A., Irabien Ma, J., Pascual, A., 2004. Human activities along the Basque coast during the last two centuries: geological perspective of recent anthropogenic impact on the coast and its environmental consequences. In: Borja, A., Collins, M. (Eds.), Oceanography and Marine Environment of the Basque Country. Elsevier Oceanography Series, vol. 70. Elsevier, Amsterdam, pp. 27–50. Clarke, K.R., Warwick, R.M., 2001. Change in Marine Communities. An Approach to Statistical Analysis and Interpretation, second ed. Primer-E Ltd, Plymouth. Commito, J.A., Thrush, S.F., Pridmore, R.D., Hewitt, J.E., Cummings, V.J., 1995. Dispersal dynamics in a winddriven benthic system. Limnology and Oceanography 40, 1513–1518. Colclough, S., Fonseca, L., Astley, T., Thomas, K., Watts, W., 2005. Fish utilisation of managed realignments. Fisheries Management and Ecology 12, 351–360. Costanza, R., d’Arge, R., de Groot, R., Farber, S., Grasso, M., Hannon, B., Naeem, S., Limburg, K., Paruelo, J., O’Neill, R.V., Raskin, R., Sutton, P., Van den Belt, M., 1997. The value of the world’s ecosystem services and natural capital. Nature 387, 253–260. Curras, A., Mora, J., 1991. Comunidades bento´nicas de la rı´a del Eo (Galicia–Asturias, ˜ a). Cahiers de Biologie Marine 32, 57–91. NW Espan Doeglas, D.J., 1968. Grain-size indices, classification and environment. Sedimentology 10, 83–100. Elliot, M., Cutts, N.D., 2004. Marine habitats: loss and gain, mitigation and compensation. Marine Pollution Bulletin 49, 671–674.
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