Recent environmental evolution of regenerated salt marshes in the southern Bay of Biscay: Anthropogenic evidences in their sedimentary record

Journal of Marine Systems 109–110 (2013) S203–S212

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Recent environmental evolution of regenerated salt marshes in the southern Bay of Biscay: Anthropogenic evidences in their sedimentary record A. Cearreta a,⁎, A. García-Artola a, E. Leorri b, M.J. Irabien c, P. Masque d a

Micropaleontología, Facultad de Ciencia y Tecnología, Universidad del País Vasco/EHU, Apartado 644, 48080 Bilbao, Spain Department of Geological Sciences, East Carolina University, Graham Building, Room 103b, Greenville, NC 27858-4353, USA Mineralogía y Petrología, Facultad de Ciencia y Tecnología, Universidad del País Vasco/EHU, Apartado 644, 48080 Bilbao, Spain d Institut de Ciència i Tecnologia Ambientals & Departament de Física, Universitat Autònoma de Barcelona, 08193 Bellaterra, Spain b c

a r t i c l e

i n f o

Article history: Received 27 September 2010 Received in revised form 6 June 2011 Accepted 28 July 2011 Available online 22 August 2011 Keywords: Salt marshes Sedimentary record Human occupation Natural regeneration Environmental management Sea-level rise

a b s t r a c t Short sediment cores (up to 44 cm long) taken from salt marshes regenerated during the last 60 years in the Urdaibai Biosphere Reserve have been interpreted on the basis of microfaunal and geochemical determinations and historical data. Agricultural soils in the middle and upper estuary reaches were abandoned during the 1950s and entrance of estuarine water provoked a rapid natural environmental transformation of these anthropogenic areas. Increasing amounts of sand and benthic foraminifera were deposited at a very high sedimentation rate (average 16 mm yr −1) during the 1950s and 1960s allowing well developed regenerated salt marshes to be rapidly established in these formerly occupied areas. During recent decades much lower sedimentation rates (average 2.5 mm yr−1), abundant agglutinated foraminiferal assemblages and enrichment of heavy metals (Pb, Zn, Cu, Ni and Cr) due to industrialization are characteristic of these already regenerated environments. This rapid regeneration process (less than 10 years) is of great interest for environmental management of modern coastal zones where extensive reclaimed land could be easily restored to tidal wetlands under the current scenario of accelerating sea-level rise. © 2011 Elsevier B.V. All rights reserved.

1. Introduction Although land loss continues to be the most pervasive threat to coastal areas and salt marshes in Europe, in some regions anthropogenic actions such as drainage and embankment construction have been stopped and even reversed (Airoldi and Beck, 2007). This is the case of some coastal wetlands in the southern area of the Bay of Biscay, which were drained at the beginning of the 18th century for agricultural purposes and malaria eradication and subsequently abandoned during the mid 1900s due to rural migration to the cities (Cearreta et al., 2002). This abandonment and lack of dyke maintenance provoked the entrance of tidal, estuarine water and allowed their natural regeneration. There is considerable international interest in restoring tidal flow to dyked salt marshes (Portnoy, 1999; Sinicrope et al., 1990) in order to reestablish important wetland functions (waste processing, nutrient cycling and fertility, biodiversity, biological regulation or recreational among others) elucidated over the past few decades (Lotze et al., 2006). Worldwide experiences have noted previously that some accidentally restored sites, such as the abandoned agricultural fields, were colonized by marsh vegetation as rapidly as highly engineered projects ⁎ Corresponding author. Tel.: + 34 946 012 637; fax: + 34 946 013 500. E-mail addresses: [email protected] (A. Cearreta), [email protected] (A. García-Artola), [email protected] (E. Leorri), [email protected] (M.J. Irabien), [email protected] (P. Masque). 0924-7963/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.jmarsys.2011.07.013

(Williams and Faber, 2001). Observation of the rapid evolution of restoration sites where natural physical processes were unimpeded has now led practitioners to rely on encouraging natural physical processes (rather than engineered projects) as much as possible to restore ecologic functions in these environments (Williams and Faber, 2001). Zedler and Callaway (1999) concluded that soil organic matter in constructed wetlands would not reach the values of the reference natural salt marshes, and Craft et al. (2003) observed that constructed salt marshes were less effective in sequestering total organic carbon over the long term than natural salt marshes. Current concerns regarding global sea-level rise (GSLR) associated with anthropogenic warming of the atmosphere and oceans and its societal and physical impacts on the coastal areas have resulted in increased interest on past environmental changes recorded in coastal environments. In fact, GSLR is affecting coastal geomorphology, erosion, and most specially wetland loss (Leatherman, 2001; Nicholls, 2004). The GSLR rate for the last century has been estimated at 19 cm based on a number of high-quality tide gauge records (Bindoff et al., 2007; Church et al., 2004; Church and White, 2006), which is three times higher than the previous century (Jevrejeva et al., 2008). More recent estimates of GSLR about ~3 mm yr−1 became available based on satellite altimetry data beginning in 1993 (Cabanes et al., 2001; Cazenave and Nerem, 2004; Leuliette et al., 2004) suggesting even a greater acceleration over the last decades. This sea-level rise acceleration is increasingly stressing coastal ecosystems (Church et al., 2008). Potentially,

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sea-level rise would: 1) increase salt water intrusion landward, producing salinification of coastal aquifers and affecting the species composition and the ecologic function of wetlands; 2) enhance tidal creek incision and beach erosion, potentially forcing a coastal retreat; and 3) increase the potential impact of future storms. Under this scenario, wetlands appear to be especially vulnerable to sea-level rise (Harvey and Woodroffe, 2008). The study of regenerated wetlands over time in response to tidal inundation and sea-level rise can potentially provide key information of future trends of coastal evolution under the current climatic scenario of global warming and accelerating sea-level rise. The southern Bay of Biscay (Fig. 1) is formed by rocky cliffs interrupted by small estuaries where salt marsh environments develop. During the last centuries these salt marsh ecosystems have been occupied initially with agricultural purposes and lately to support modern urban and industrial development. These human activities have provoked their destruction, size reduction or degradation of their environmental quality. Rivas and Cendrero (1991) concluded that human occupation of salt marshes and other intertidal areas can be considered as the main geomorphological process in the southern Bay of Biscay during the last two centuries. The first significative change took place at the beginning of the 18th century when the need for fertile land and malaria eradication were powerful reasons to drain salt marshes. Then, the Cambó Law of 1918 promoted additional desiccation of coastal wetlands based on their suspected insalubrity (Gogeascoechea and Juaristi, 1997). During the 1950s these reclaimed areas were abandoned due to rural migration to the cities, and the lack of dyke maintenance provoked the entrance of tidal, estuarine water and allowed their natural regeneration. Natural, regenerated and still-reclaimed salt marshes represent around 65% of the whole estuarine area of the Urdaibai Biosphere Reserve. Consequently, an adequate scientific knowledge of the recent geological processes acting on these areas is of maximum importance to the correct management of this protected environment. This study uses a combined high-resolution microfaunal–geochemical approach to examine the recent history of salt marsh evolution and environmental regeneration in the Urdaibai estuary. The main aim of this work is the identification and assessment of natural versus anthropogenic processes in this area by means of benthic foraminifera and heavy metal contents from sediment cores collected from previously reclaimed salt marshes. 210Pb and 137Cs determinations have also been undertaken to provide a chronology for environmental changes recorded in the Urdaibai estuary salt marshes. The response of previously reclaimed areas to tidal inundation is of great interest in order to plan scientifically sound adaptation measures to face current sea-level rise. Cearreta et al. (2002) initiated the geological study of natural regeneration process of previously reclaimed areas in the Basque coast focused on the nearby Plentzia estuary, and Santín et al. (2009) studied the consequences of the reclamation and regeneration processes on the organic matter content of different salt marsh areas in the Urdaibai estuary. This joint microfaunal–geochemical approach is very cost effective and of wide applicability to all temperate coastal wetlands. 2. Materials and methods 2.1. Study area The Urdaibai estuary (northern Spain) is formed by the tidal part of the Oka river (Fig. 1). The estuary covers an area of 765 ha, and occupies the flat bottom of the 12.5 km long, 1 km wide alluvial valley. It is a mesotidal area with semidiurnal tides ranging from 4.5 m

during spring tides to less than 1.0 m during neap conditions (Leorri and Cearreta, 2009a; Monge-Ganuzas et al., 2008; Villate et al., 1990). During the last 300 years, the natural features of the Urdaibai estuary have been modified by extensive reclamation of salt marshes for agricultural purposes on both the middle and upper estuarine areas. Following agricultural decline during the second half of the 20th century, the salt marshes have experienced natural progressive regeneration, and it has been calculated that these renewed environments represent around 300 ha of the modern estuary. Furthermore, another 200 ha of reclaimed land could be easily restored to tidal wetlands (Gobierno Vasco, 1998). The studied salt marshes are located in the middle reaches of the estuary (Fig. 1) with the Busturia salt marsh characterized by Halimione portulacoides and Puccinellia maritima vegetation, and Isla and Baraizpe salt marshes dominated by H. portulacoides, Elymus pycnanthus and Juncus maritimus vegetation (Benito and Onaindia, 1991). The estuary represents the most extensive and best preserved tidal area on the entire Basque coast and it constitutes part of the Urdaibai Biosphere Reserve declared by UNESCO in 1984. 2.2. Sampling Sediment cores were collected from three different recently regenerated salt marshes of the Urdaibai estuary in March 2003 (Busturia), February 2008 (Isla) and March 2008 (Baraizpe). A small unvegetated area surrounded by halophytic vegetation was chosen in the central part of each marsh (Fig. 1). Two 50-cm long PVC tubes (12.5 cm diameter) were inserted by hand into the sediment at each sampling point in order to obtain sufficient material to determine grain size, benthic foraminiferal content, sediment geochemistry, and isotopic composition. Core penetration was limited to 37 cm in Busturia, 44 cm in Isla and 24 cm in Baraizpe due to increasing soil resistance with depth. Compaction of the sediment during sampling was negligible. Each core was divided in two halves, described and photographed before being sliced into successive 1-cm samples. In all, four identical halves were obtained at any sampling point, one for each analytical method. Precise elevation of each sampling point above local ordnance datum (LOD) was obtained in the field using a GPS-RTK and a total station. 2.3. Analyses 2.3.1. Foraminiferal assemblages Core samples analyzed for foraminiferal content (one every two samples for each core) were sieved through 1 mm (to remove large organic fragments) and 63-micron sieves, washed to remove clay material and dried at 50 °C. Foraminifera were concentrated by flotation in trichlorethylene as described by Murray (1979). Tests were picked until a representative amount of more than 300 individuals for each assemblage was obtained. Otherwise, all the available tests were picked and studied under a stereoscopic binocular microscope using reflected light. Altogether, 58 samples and around 10,600 foraminifera were examined. All foraminiferal species identified in the samples are listed in Appendix 1. Complete foraminiferal census data are listed as Appendix 2 and placed in the JMS online repository at doi:10.1016/ j.jmarsys.2011.07.013. Foraminiferal assemblages have been long studied in the region (Cearreta, 1988, 1989). More recently, foraminiferal distributions have been analyzed in relation to diverse environmental parameters using different statistical approaches. These studies established the correlation between foraminiferal assemblages and two main environmental parameters: elevation and salinity that represent the main control of their distribution (Leorri et al., 2008b; Leorri and Cearreta, 2009b).

Fig. 1. Geographic location of the studied salt marshes in the Urdaibai estuary, showing position of the cores in both historical (1957; left side) and modern (2008; right side) photographs: Busturia (top pictures), Isla (middle pictures), and Baraizpe (bottom pictures). Scale bar represents 100 m.

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Instead, in areas that were subject of heavy pollution, oxygen water levels seemed to be the main control (Irabien et al., 2008; Leorri et al., 2008a). Foraminiferal assemblages described here represent marsh settings dominated by elevation in relation to the tidal frame as described in the literature for this region and the SW European coast (Leorri et al., 2010). In order to support the identification of the different depth intervals (DI) dominated by different foraminiferal assemblages, cluster analysis (CA) and detrended corresponded analysis (DCA) were used (see Leorri et al., 2008b and Pruitt et al., 2010 for discussion about the methods) but statistical analyses only confirmed previously identified changes and are not subsequently discussed. 2.3.2. Short-lived radionuclides The concentration profiles of 210Pb (T1/2: 22.3 yr) and 137Cs (T1/2: 30 yr) were used to derive sedimentation rates over the last decades. The activities of 137Cs and 226Ra were determined by γ spectrometry using calibrated geometries in a coaxial high-purity Ge detector (EG&G Ortec). Samples were sealed at least 3 weeks prior to counting, to allow equilibrium between 226Ra and its short lived daughters. The 226 Ra activity was determined from 214Pb through its 351 keV gamma emission. Determination of total 210Pb activities was carried out through the measurement of its daughter nuclide 210Po by alpha spectrometry, following the methodology described in SanchezCabeza et al. (1998). Excess 210Pb activities ( 210Pbxs) were determined by subtracting the 226Ra activity (assumed to equal the supported 210 Pb activity) from the total 210Pb activity. Given its half-life (22.3 yr), 210Pb is especially useful to assess sedimentary processes on time scales of about 100–150 years: 210Pb is continuously introduced into the aquatic environments via atmospheric deposition, after decay from 222Rn exhaled from the continental crust, as well as from in situ decay of dissolved 226Ra in the water body. 210 Pb efficiently adsorbs to particulate matter, leading to find it in excess with respect to 226Ra in sediments. The excess 210Pb concentration profiles can then be used to estimate recent sedimentation and mixing rates through the implementation of appropriate mathematical models (i.e. Appleby and Oldfield, 1992; Cochran and Masque, 2005). As Smith (2001) pointed out, it is generally recommended to use independent evidence to confirm the validity of the results obtained from 210Pb methodologies. Some artificial radionuclides, such as 137Cs, were introduced in the environment in the 1950–1960s as a consequence of the detonation of nuclear weapons in the atmosphere (UNSCEAR, 2000). The Chernobyl accident also contributed significantly to the total 137Cs inventory in the Northern Hemisphere. Given the remote position of the study area from major nuclear facility discharges (e.g. Sellafield, La Hague), the 137Cs activity profiles in the sediment cores could provide with up to three independent chronostratigraphic events: the beginning of atmospheric nuclear tests in 1954, the peak of nuclear detonations in 1963, and the Chernobyl accident in 1986. However, no significant impact of the Chernobyl accident derived deposition occurred in the Iberian Peninsula, and thus 137Cs in the studied salt marshes is likely to be dominantly derived from nuclear weapons testing. 2.3.3. Heavy metals Geochemical analyses were performed by Activation Laboratories Ltd. (Actlabs, Ontario, Canada). Elemental determinations were carried out using Inductively Coupled Plasma-Optic Emission Spectrometry (ICP-OES) after digestion with aqua regia. This extraction technique is considered a suitable method for monitoring heavy metal contents in environmental materials (Sastre et al., 2002) and has been widely used for the analysis of recent sediments (Balls et al., 1997; Baptista Neto et al., 2000; Sarkar et al., 2004). Quality control was done by analyzing duplicate samples and blanks to check precision, whereas accuracy was obtained by using certified standards (GXR-1, GXR-4 and GXR-6; e.g. Gladney and Roelandts, 1990). Detection limits were 0.01% for Al and K, 0.1 mg kg −1 for Sc, 1 mg kg −1 for Zn, Cu and Ni, and 2 mg kg −1 for Pb and Cr. A common

method to compensate for grain-size effects in sediments is to normalize metal concentrations to a conservative element such as Al (Ackermann, 1980; Cundy et al., 2003; Mil-Homens et al., 2006; OSPAR, 1998). As in the sediments analyzed in this work (n = 52) this element shows a very close relationship with K and Sc (r = 0.994 and 0.928 respectively, P b 0.0001) and it appears as a good proxy of the clay fraction, mainly composed by illite (Irabien and Velasco, 1999). Therefore, results are represented normalized to Al. In order to support DI identification and correlation with foraminiferal data principal component analysis (PCA) was used (see Cearreta et al., 2008 for discussion about the methods) but statistical analysis only confirmed previously identified changes and are not subsequently discussed. 2.3.4. Organic and sand contents Organic content was measured by Neiker (Derio, Spain) following the Walkey method (Hesse, 1971) at 2 cm intervals only in the Busturia core. Sand content in all cores was determined by wet sieving at 63 μm during the sample preparation for foraminifera. 3. Results and discussion Relevant information on the temporal environmental changes occurred recently in response to anthropogenic land reclamation and natural environmental regeneration of salt marshes can be obtained by studying variations in foraminiferal assemblages and geochemical composition of short sediment cores. All cores were obtained from small salt-pans surrounded by halophytic vegetation located at the lower end of the high marsh environment with less than 13 cm of vertical difference among them (Fig. 1, Table 1). The cores were composed of silty clay with small sand content which increased generally upwards and presented evident burrows of polychaetes (Hediste diversicolor) concentrated at the top. At the Busturia site (core BU; coordinates X: 525420.688, Y: 4802512.496, Z: 3.722 m above LOD) 37 cm was recovered that in photography showed the sediments to be finely-laminated, with burrows throughout the upper 30 cm (Fig. 2). At the Isla site (core IS; coordinates X: 526567.318, Y: 4800781.350, Z: 3.599 m above LOD) 44 cm was recovered with the bottom being black in color and the upper 18 cm brown in response to evident burrows of polychaetes (Fig. 3). Finally, the Baraizpe core (core BA; coordinates X: 527558.441, Y: 4800144.724, Z: 3.659 m above LOD) presented 24 cm of dark gray sediments with the upper 5 cm almost black in color (Fig. 4). 3.1. Busturia core The number of benthic foraminifera present in the Busturia core was high in the upper half of the sequence and scarce in the lower part. In total, 3185 foraminiferal tests were obtained in the 19 samples analyzed. Foraminiferal results are expressed as percentage or as number of foraminiferal tests per 50 g of dry sediment for standardization. Although irregular, the data show a general upward increase in foraminiferal abundance. Ten different species were found in this core (Appendix 1) but only Jadammina macrescens was dominant throughout (Fig. 2). Three distinct depth intervals (DI) were distinguished in the core in terms of presence, abundance and dominance of foraminiferal species (Table 1). The basal 10 cm (DI3) was characterized by the absence of foraminifera and a very low sand content (average 1%). It is likely to represent the anthropogenic deposit introduced during the reclamation period. The following 8 cm was characterized by DI2 and exhibited very low numbers of foraminiferal tests (average 31 tests), species (average 2 species) and sand content (average 8%) in comparison with the upper DI1. Consequently it is interpreted as a zone deposited during the regeneration process from the agricultural soil (DI3) to the regenerated marsh (DI1). This upper interval of 19 cm was clearly dominated

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Table 1 Summary of core and microfaunal data. The single value represents the average and those in parentheses give the range. Busturia core

Isla core

Baraizpe core

DI 1 Thickness: 19 cm Lithology: burrowed brown silty clay 12 (7–30)% sand 2.2 (3.4–1.1)% organic matter Elevational range: 3.722–3.532 m Estimated age: 1960–2003 476 (100–2150) tests 5 (3–9) species J. macrescens 86 (47–98)% C. williamsoni 4 (0.3-23)% T. inflata 3 (0.4-6)% H. moniliforme 2 (0–16)%

DI 1 Thickness: 13 cm Lithology: brown burrowed silty clay 16 (14–18)% sand

DI 1 Thickness: 5 cm Lithology: black burrowed silty clay 9% sand

Elevational range: 3.599–3.469 m Estimated age: 1960–2008 1285 (710–1750) tests 6 (4–8) species J. macrescens 57 (37–73)% H. moniliforme 31 (15–49)% T. inflata 8 (4–16)% A. mexicana 2 (0–5)%

Elevational range: 3.659–3.609 m Estimated age: 1960s–2008 274 (107–402) tests 6 (3–8) species J. macrescens 58 (31–72)% M. fusca 20 (1–58)% C. oceanensis 8 (0–13)% T. inflata 7 (4–11)% H. moniliforme 6 (0–10)%

DI 2 Thickness: 8 cm Lithology: burrowed brown silty clay 8 (6–10)% sand 2.0 (2.2–1.7)% organic matter Elevational range: 3.532–3.452 m Estimated age: 1954–1960 31 (17–56) tests 2 species Few foraminifera

DI 2 Thickness: 19 cm Lithology: black and brown silty clay 13 (5–19)% sand

DI 2 Thickness: 4 cm Lithology: dark gray burrowed silty clay 1 (1–2)% sand

Elevational range: 3.469–3.279 m Estimated age: 1950s–1960 310 (100–630) tests 4 (2–5) species J. macrescens 94 (90–99)% H. moniliforme 3 (0–16)%

Elevational range: 3.609–3.569 m Estimated age: 1950s–1960s 38 (15–66) tests 5 species Few foraminifera

DI 3 Thickness: 10 cm Lithology: black silty clay 1 (0.5–1)% sand 1.8 (1.9–1.6)% organic matter Elevational range: 3.432–3.352 m Estimated age: 1954–1900s No foraminifera

DI 3 Thickness: 12 cm Lithology: black silty clay 5 (2–7)% sand

DI 3 Thickness: 15 cm Lithology: dark gray burrowed silty clay 2 (1–4)% sand

Elevational range: 3.279–3.159 m Estimated age: 1950s–1900s No foraminifera

Elevational range: 3.569–3.419 m Estimated age: 1950s–1900s 304 (136–757) tests 3 (2–4) species J. macrescens 98 (97–99)% C. oceanensis 1 (0–3)% T. inflata 1 (0–3)%

by agglutinated foraminifera (average 92%) with J. macrescens (average 86%) as the main species. The calcareous hyaline species Cribroelphidium williamsoni and other agglutinated species as Trochammina inflata and Hormosina moniliforme were present throughout this interval as secondary forms. Foraminiferal

density/50 g showed a general increasing tendency upwards with an average number of individuals of 476. The sand content was low (average 12%) and species diversity was very small (average 5 species). This zone represents the modern regenerated salt marsh environment (Fig. 2 and Table 1).

Fig. 2. Core photograph, sand content (%), main foraminiferal species (1: H. moniliforme; 2: J. macrescens; 3: T. inflata; 4: C. williamsoni), total 210Pb (dots) and 137Cs (squares) concentrations (Bq kg−1), Al-normalized Pb distribution, and organic matter content (%) with depth (cm) in the Busturia salt marsh core (Urdaibai estuary). Black dots in the foraminiferal distribution represent presence of scarce tests. Defined depth intervals (DIs) are also shown.

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Fig. 3. Core photograph, sand content (%), main foraminiferal species (1: A. mexicana; 2: H. moniliforme; 3: J. macrescens; 4: T. inflata), total 210Pb (dots) and 137Cs (squares) concentrations (Bq kg−1), and Al-normalized Pb and Zn distributions with depth (cm) in the Isla salt marsh core (Urdaibai estuary). Defined depth intervals (DIs) are also shown.

The Busturia core shows the presence of 210Pbxs (less than 100 yr) and 137Cs (present since 1954) in depth intervals DI1 and DI2 (Fig. 2) suggesting the beginning of the salt marsh regeneration process during the second half of 1950s, in accordance with the historical records that show the contemporaneous presence of both agricultural fields and salt marsh channels in the area by 1957 (Fig. 1). A maximum abundance in the 137Cs profile is located at 14 cm depth that can be considered as the peak of 1963. All this suggests a very rapid sedimentation rate during the regeneration process (around 14 mm yr −1) that slowed down greatly during the development of the regenerated salt marsh (around 3.5 mm yr −1). The 210Pbxs contents detected in DI3 indicate an age younger than 100 yr although the mixed nature of an agricultural soil does not allow a precise age determination for this basal interval. Range of concentrations of Pb, Zn, Cu, Ni and Cr are indicated in Table 2. As vertical profiles displayed by Al-normalized concentrations in the Busturia core are very similar in shape, only Pb/Al has been represented in Fig. 2. All of them exhibit low and fairly constant levels in DI3 and DI2, whereas enhanced contents can be observed only in DI1 (see discussion below). On the other hand, organic matter content in this core shows very low values throughout and a general decreasing trend with depth (Fig. 2; Table 1), probably related to the rapid decomposition of the organic constituents of the sediments as detected previously in other salt marshes from the same Basque coast (Cearreta et al., 2002; Santín et al., 2009).

3.2. Isla core The benthic foraminiferal content in the Isla core was very high, except for the basal 12 cm. In total, 4429 foraminiferal tests were obtained in the 22 samples analyzed. Foraminiferal abundance in Table 1, although irregular, showed a general upward increase in the core. Eleven different species were found (Appendix 1) with J. macrescens as dominant species throughout (Fig. 3). Three distinct depth intervals were distinguished in this core. The lowermost 12 cm (DI3) was characterized by the absence of foraminifera and a very low sand content (average 5%). Historical records and the concentration profiles of 210 Pb and 137Cs (Fig. 3) suggest this zone as an anthropogenic deposit introduced during the reclamation period. The following 19 cm (DI2) contained moderate numbers of foraminiferal tests (average 310 tests), low species numbers (average 4 species) and increasing upwards sand contents (average 13%). The only dominant species was agglutinated J. macrescens (average 94%). H. moniliforme was a secondary species. Using historical pictures and the sediment accretion rates derived from the short-lived radionuclides profiles, this interval is interpreted as being deposited during the regeneration process of the previously reclaimed agricultural soil. The upper 13 cm (DI1) was highly dominated by agglutinated foraminifera (average 99%). J. macrescens (average 57%), H. moniliforme (average 31%) and T. inflata (average 8%) were the main species. Arenoparrella mexicana was a secondary species. The sand content increased (average 16%) in comparison with previous intervals. The foraminiferal density/

Fig. 4. Core photograph, sand content (%), main foraminiferal species (1: H. moniliforme; 2: J. macrescens; 3: M. fusca; 4: T. inflata; 5: C. oceanensis), total 210Pb (dots) and 137Cs (squares) concentrations (Bq kg−1), and Al-normalized Pb and Zn distributions with depth (cm) in the Baraizpe salt marsh core (Urdaibai estuary). Black dots in the foraminiferal distribution represent presence of scarce tests. Defined depth intervals (DIs) are also shown.

A. Cearreta et al. / Journal of Marine Systems 109–110 (2013) S203–S212 Table 2 Ranges of metal concentrations in the analyzed cores (all values in mg kg−1).

Busturia core (n = 16) Isla core (n = 16) Baraizpe core (n = 14)

Pb

Zn

Cu

Ni

Cr

16–53 14–53 20–172

77–148 37–153 67–103

15–29 17–52 22–34

16–32 21–44 28–42

15–36 41–134 45–62

50 g showed an average number of individuals of 1285. Average number of species was 6. This uppermost interval represents the modern regenerated salt marsh environment (Fig. 3 and Table 1). As shown in Fig. 1, the presence of well developed salt marsh channels over a previous agricultural exploitation in the Isla area by 1957 is evident, suggesting environmental regeneration already in progress. Then, if agricultural soil represented by interval DI3 is previous to 1950s and the 137Cs maximum abundance detected at 8 cm depth in DI1 would represent the 1963 peak, a very rapid sedimentation rate can be deduced during the regeneration process (around 18 mm yr−1), together with deposition of increasing amounts of sand during this transitional interval DI2 (Fig. 3). As in the Busturia location, the sedimentation rate decreased severely during the development of the regenerated salt marsh environment (around 1.7 mm yr−1). Distribution of Al-normalized contents of metals with depth in Isla (Fig. 3) displays the same general behavior that was determined previously in Busturia (Fig. 2). Intervals DI3 (anthropogenic deposit) and DI2 (rapidly regenerating salt marsh during the 1950s–60s) are characterized by low concentrations of metals, whereas DI1 (regenerated salt marsh) exhibits increased values. Although this pattern suggests that sediments from DI2 could represent pre-industrial materials deposited before significant anthropogenic inputs, historical data indicate that metal processing factories have been working in this estuarine area since the beginning of the 1910s. Therefore, this enrichment is more likely related to the abovementioned decrease in sediment deposition, given that high sedimentation rates may “dilute” contaminant loads due to mixing with coarse sedimentary particles or non-polluted materials (Valette-Silver, 1993).

3.3. Baraizpe core Benthic foraminifera showed a moderate abundance throughout the Baraizpe core with an intermediate lower abundance interval. In all, 2966 foraminiferal tests were analyzed in the 17 samples studied. Nine different species were found in this core (Appendix 1) but only J. macrescens was always dominant (Fig. 4). Three distinct depth intervals were distinguished. The basal 15 cm was entirely dominated by agglutinated foraminifera (average 99%) with very abundant J. macrescens (average 98%), together with minor Cribroelphidium oceanensis and T. inflata. This DI3 contained a variable number of individuals/50 g (average 304) and very low species diversity (average 3 species). The sand content was also very low (average 2%). By comparison with modern assemblages of the same Basque coast (Cearreta et al., 2002), this depth interval can be interpreted as deposited under a high salt marsh environment. The following 4 cm was characterized by DI2. This zone of the core contained very low amounts of foraminiferal tests (average 38) and sand (average 1%). Using historical records and the sediment accretion rates derived from 210Pb and 137Cs contents (Figs. 1 and 4), this interval is interpreted as an anthropogenic deposit introduced during the reclamation period but partially mixed with salt marsh sediments. The upper 5 cm (DI1) was dominated by a mixture of agglutinated (average 91%) and hyaline (average 9%) foraminifera. J. macrescens (average 58%), Miliammina fusca (average 20%), C. oceanensis (average 8%), T. inflata (average 7%) and H. moniliforme (average 6%) were the main species (Fig. 4 and Table 1). The sand content (average 9%) and species diversity (average 6 species) were higher than in previous intervals. The foraminiferal density/50 g showed an

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average number of individuals of 274. This interval represents the modern regenerated salt marsh environment. In Baraizpe, the concentration profile of 210Pbxs suggests a record younger than 100 yr for this core (Fig. 4). Absence of 137Cs in basal DI3 indicates this salt marsh interval as older than 1950s, suggesting a recent human occupation of this estuarine area. Interval DI2 contains both 210Pbxs and 137Cs but the mixed nature of this agricultural soil avoids any precise age determination. Historical photography (Fig. 1) shows the existence of a well developed agricultural exploitation in this area by 1957. The topmost DI1 exhibits at the base a 137Cs peak that, together with elevated concentrations of heavy metals and benthic foraminifera contents (Fig. 4), indicates the development of the modern regenerated salt marsh since the late 1960s with a relatively slow sedimentation rate (around 0.9 mm yr−1). As in the other two cores, increased contents of heavy metals appeared only in the topmost DI1 (Fig. 4). In these near-surface sediments concentrations of Pb exceeded the Action Level I proposed in the Recommendations for the management of dredged materials from the Spanish ports published by CEDEX (1994). Therefore, they should be classified as moderately contaminated and a special authorization including further studies should be required to allow dumping in the sea. 3.4. Interpretation of the sedimentary record As observed previously by Cearreta et al. (2002) and Fernández et al. (2010), the main constituents of the sedimentary sequences in the salt marshes of the southern Bay of Biscay are detrital materials deposited from estuarine waters whereas organic materials from the vegetated surface are rapidly consumed during burial. Organic matter contents in the Busturia core were very low and exhibited a progressive decrease with depth, in accordance with previous studies in other regenerated and natural salt marshes from the same coastal area (Cearreta et al., 2002). This fact reflects the abundant regional input of detrital materials to the studied area, which exceeds by far the contribution of organic material from plant detritus. Gerritsee and Van Driel (1984) suggested that adsorption of metals in soils and sediments is mainly dominated by organic matter. However, the lack of significant correlations between organic matter and metals in the Busturia core prevents confirmation of a significant role of organic matter in the retention of metals. Three different environments have been identified in the studied sequences (reclaimed agricultural soil, regenerating salt marsh, and regenerated/well developed salt marsh) exhibiting an increasing amount of sand in their sediments as a consequence of the entrance of sandy materials from the estuarine environment during the regeneration process. Together with detrital materials, these minerogenic sediments contain also increasing amounts of foraminiferal tests both agglutinated and calcareous as the regeneration process is taking place, from their absence in the agricultural soil to very abundant assemblages in the regenerated salt marsh. Knowledge of modern assemblages is indispensable for the correct interpretation of the buried microfaunas (de Rijk and Troelstra, 1997; Phleger and Walton, 1950; Scott and Medioli, 1986), and simultaneously paleoenvironmental reconstructions must also rely on the assumption that buried microfaunas are closely similar to modern microfaunas (Guilbault et al., 1995; Jennings and Nelson, 1992). The distribution of modern microfaunas in the Basque salt marshes has been studied previously by Leorri et al. (2008b) who demonstrated the presence of well defined assemblages that occupy clear elevation subenvironments related to degree or duration of exposure to tidal inundation. Furthermore, microfaunas (both agglutinated and calcareous) are well preserved and abundant in the subsurface sediments due to supply of abundant calcium carbonate to the environment by regional rocks (Cearreta and Murray, 2000). This good preservation of the complete modern assemblages (calcareous component

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included) is of great advantage in the paleoenvironmental interpretation of buried sequences. Consequently, modern assemblages seem good analogs for the interpretation of well preserved buried assemblages and can be used on a comparative basis to interpret the temporal paleoenvironmental changes registered in the Urdaibai short cores (Figs. 2, 3 and 4). In particular, modern foraminifera from the Busturia salt marsh were described by Leorri et al. (2008b) based on the analysis of living and dead assemblages from 9 different surface samples taken at various altitudes above LOD. Nevertheless, dead assemblages are considered to be a better analog for interpreting patterns of foraminiferal distribution in buried microfaunas since they represent a time-averaged accumulation of foraminiferal tests (Horton, 1999; Murray, 1991). In this salt marsh environment, species diversity and calcareous tests decreased with increasing elevation. The most abundant species found in the vegetated marsh were agglutinated J. macrescens (average 81%) and T. inflata (average 17%) followed by very scarce calcareous Ammonia tepida (average b1%). The studied profiles present a consistent pattern with similar studies elsewhere, where lower elevations contain greater mixed layer thickness (i.e., Isla core with greater mixed layer [11.5 cm] has the lowest elevation). Intermediate elevations present smaller mixed layer thickness (e.g., Baraizpe and Busturia have 5 and 6.5 cm mixed layers respectively) and higher elevations present negligible mixed layers (see the profile presented by García-Artola et al. (2009) from the highest high marsh of Kanala in this Urdaibai estuary). Consequently, the mixed layer thickness is controlled by the elevation above mean high water level (MHW), in which the low marsh accumulates relatively quickly while the high marsh remains in “equilibrium” with MHW (Goodman et al., 2007; Temmerman et al., 2004). This mixed layer thickness corresponds to the upper zone of root growth and oxygenation, zone of sulfate reduction, redox potential discontinuity and decomposition of organic input from halophytic plants (Howarth and Teal, 1979; Lord and Church, 1983; Rhoads and Boyer, 1982). The reported values here are similar to ranges reported in the literature for the mid-Atlantic coast of the United States (Koretsky et al., 2005; Koretsky and Van Cappellen, 2002; McCraith et al., 2003) and the worldwide average for marine environments of 9.8 ± 4.5 cm for the mixed layer thickness (Boudreau, 1998; Wheatcroft and Drake, 2003; Leorri et al., 2009 for discussion). On the other hand, the sedimentary sequences analyzed here present the expected 210Pb profiles of sediments containing anthropogenic deposits, due to the mixed nature of the materials and the extremely short time intervals to analyze. Combination of these data with 137Cs evidences contributed efficiently to support historical records in the time location of the studied cores. Sedimentation rates have been associated to elevation with respect to local tidal range (Goodman et al., 2007; Temmerman et al., 2004). Thus, high sedimentation velocities detected during the regeneration process (intervals DI2 in Busturia and Isla cores) seem to be related to their low position, whereas equivalent sedimentation rates have not been observed in the topographically higher interval DI1 of Baraizpe (Table 1). Roman et al. (1984) found that tidal restriction of a former salt marsh area by embankment causes a decline in the elevation of the marsh surface that Portnoy (1999) quantified in 10–20 cm below that of unrestricted salt marshes. In summary, sedimentary records of the analyzed salt marshes were very young (less than 100 years) and in general presented three distinct intervals that reflected the regeneration process experienced by these salt marsh areas in the Urdaibai estuary as a consequence of the recent abandonment of previous agricultural soils. These soils at the base of the sequences could not be dated due to the mixed nature of these anthropogenic altered materials, although historical records showed these areas to be in regeneration already by the late 1950s. The regenerating process was characterized by the presence of increasing amounts of sand and benthic foraminifera (progressively more

abundant and diverse) that were deposited at a very high sedimentation rate (14–18 mm yr−1) during the 1950s and 1960s due to the entrance of estuarine waters. Then, during the last decades well developed regenerated salt marshes established in these areas exhibiting much lower sedimentation rates (0.9–3.5 mm yr−1), abundant agglutinated foraminiferal assemblages and elevated contents of heavy metals. However, Santín et al. (2009) observed in this Urdaibai estuary that despite similar edaphic characteristics and the same vegetation cover, natural salt marshes accumulated twice the amount of organic matter at the surface than the regenerated salt marshes. These authors concluded that soil organic matter requires a long time to achieve natural levels. A rapid regeneration process (less than 10 years) as a consequence of very high sedimentations rates (average 15 mm yr −1) during tidal inundation of previously reclaimed agricultural areas is of great interest for environmental management of coastal zones, particularly in protected areas as the Urdaibai Biosphere Reserve where extensive reclaimed land could be easily restored to tidal wetlands (Gobierno Vasco, 1998) and under the current climatic scenario of accelerating sea-level rise on the Basque coast (Leorri et al., 2008b). This seems to imply that at least in this region salt marshes will have the ability to respond to a sea-level rise acceleration by accreting very fast until they reach the equilibrium with the tidal frame. In this way, rapid salt marsh regeneration would represent a valid adaptation strategy to be implemented as a natural coastal defense. These systems have been naturally colonized by marsh vegetation as rapidly as highly engineered projects elsewhere. However, it is important to account for the necessary time-frame (i.e., 10 years or more) if successful restorations are going to be achieved, as some regulatory agencies realized already by the late 1980s (e.g. San Francisco Bay estuarine area; Williams and Faber, 2001). In addition, results obtained in Baraizpe salt marsh indicate that anthropogenic inputs may alter to a variable extent the geochemical quality of the accumulating sediments in these regenerated environments. These results are in accordance with the conclusions obtained by Atkinson et al. (2001) who reported that whereas vegetation, invertebrates and bird fauna often respond relatively quickly to reflooding of former reclaimed areas, geochemical cycling restoration often takes longer and can act as an important source of toxic elements. 4. Conclusions Rapid natural salt marsh regeneration during recent tidal inundation of previously reclaimed agricultural areas has been observed in the southern Bay of Biscay. This process is of great interest for environmental management of coastal zones, particularly in those areas where extensive reclaimed land is still present and could be easily restored to tidal wetlands, as these environments accrete sediment very fast to reach equilibrium with the tidal frame. Recent reviews on the performance of anthropogenically managed salt marshes worldwide are not confident on their long term effectiveness and ecological value compared to naturally restored environments. Observation of the rapid evolution of regenerated sites has now led practitioners worldwide to encourage natural physical processes as much as possible to restore ecological functions in salt marshes. Particularly under the current scenario of sea-level rise, rapid salt marsh restoration would represent a valid adaptation measure to be favored in suitable coastal areas. Acknowledgments This research was funded by the projects UNESCO06/08, K-Egokitzen II (Climate Change: Impact and Adaptation, Etortek 2010), TANYA (MICINN, CGL2009-08840) and IT365-10 (Basque Government). Ane García-Artola received a doctoral grant from the Basque Government (BFI08.180) and Dr. Eduardo Leorri was awarded a Ralph E. Powe Junior Faculty Enhancement Award. Support for the research of

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Dr. Pere Masque was received through the prize ICREA Academia funded by the Generalitat de Catalunya. Julia Fielitz (European Class 2003) and Itxaso Vicente (Master BEZ 2007–08) prepared and studied micropaleontological samples from the Busturia and Isla marsh cores respectively. Prof. Jesús Soto (University of Cantabria, Spain) analyzed 210 Pb and 137Cs contents from the Busturia core. Ana Aizpurua carried out the organic content analyses at NEIKER (Instituto Vasco de Investigación y Desarrollo Agrario). Iratxe Iriondo (Mendi Topografia) determined the topographic location of the Isla and Baraizpe and Joseba Abaitua carried out the topographic study of Busturia. Dr. Manuel R. Monge (Technical Office of the Urdaibai Biosphere Reserve) supplied the historical photographs and helped in the field (Busturia). Dr. Susana Fernández (University of Oviedo, Spain) and an anonymous reviewer are thanked for their helpful and critical comments on the original manuscript. This is a contribution to IGCP Project 588 and Northwest Europe working group of the INQUA Commission on Coastal and Marine Processes. It represents Contribution #1 of the Geo-Q Research Unit (Joaquín Gómez de Llarena Laboratory). Appendix 1 Microfaunal reference list. BU: Busturia salt marsh core; IS: Isla salt marsh core; BA: Baraizpe salt marsh core. 1. Ammonia tepida (Cushman) = Rotalia beccarii (Linné) var. tepida Cushman, 1926 (BU, IS, BA) 2. Arenoparrella mexicana (Kornfeld) = Trochammina inflata (Montagu) var. mexicana Kornfeld, 1931 (IS, BU) 3. Cibicides lobatulus (Walker and Jacob) = Nautilus lobatulus Walker and Jacob, 1798 (IS) 4. Cribroelphidium oceanensis (d'Orbigny) = Polystomella oceanensis d'Orbigny, 1826 (IS, BA) 5. Cribroelphidium williamsoni Haynes, 1973 (BU, IS, BA) 6. Haplophragmoides wilberti Andersen, 1953 (IS, BA) 7. Haynesina germanica (Ehrenberg) = Nonium germanicum Ehrenberg, 1840 (BU, IS, BA) 8. Hormosina moniliforme (Siddall) = Reophax moniliforme Siddall, 1886 (BU, IS, BA) 9. Jadammina macrescens (Brady) = Trochammina inflata (Montagu) var. macrescens Brady, 1870 (BU, IS, BA) 10. Miliammina fusca (Brady) = Quinqueloculina fusca Brady, 1870 (BU, IS, BA) 11. Quinqueloculina seminula (Linné) = Serpula seminulum Linné, 1758 (BU) 12. Textularia earlandi Parker, 1952 (BU) 13. Trochammina inflata (Montagu) = Nautilus inflatus Montagu, 1808 (BU, IS, BA) Appendix 2. Supplementary data Supplementary data to this article can be found online at doi:10. 1016/j.jmarsys.2011.07.013. References Ackermann, F., 1980. A procedure for correcting the grain size effect in heavy metal analysis of estuarine and coastal sediments. Environmental Technology Letters 1, 518–527. Airoldi, L., Beck, M.W., 2007. Loss, status and trends for coastal marine habitats in Europe. Oceanography and Marine Biology: An annual review 45, 345–405. Appleby, P.G., Oldfield, F., 1992. Applications of 210Pb to sedimentation studies, In: Ivanovich, M., Harmon, R.S. (Eds.), Uranium-series Disequilibrium. Applications to Earth, Marine and Environmental Sciences, second ed. Oxford Science, Oxford, pp. 731–778. Atkinson, P.W., Crooks, S., Grant, A., Rehfisch, M.M., 2001. The success of creation and restoration schemes in producing intertidal habitat suitable for waterbirds. English Nature Research Reports 425, 1–166. Balls, P.W., Hull, S., Miller, B.S., Pirie, J.M., Proctor, W., 1997. Trace metal in Scottish estuarine and coastal sediments. Marine Pollution Bulletin 34, 42–50.

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