Climate and anthropogenic factors influencing an estuarine ecosystem from NW Iberia: new high...

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Climate and anthropogenic factors inuencing an estuarine ecosystem from NW Iberia: new high resolution multiproxy analyses from San Simón Bay (Ría de Vigo) Castor Muñoz Sobrino a, * , Iria García-Moreiras a , Yoel Castro a , Natalia Martínez Carreño b , Esther de Blas a , Carlos Fernandez Rodríguez c , Alan Judd d , Soledad García-Gil b a Departamento de Bioloxía Vexetal e Ciencias do Solo, Facultade de Ciencias, Universidade de Vigo, Campus de Marcosende s/n., E-36310 Vigo, Spain b Departamento de Xeociencias Mariñas, Facultade de Ciencias, Universidade de Vigo, Campus de Marcosende s/n., E-36310 Vigo, Spain c Departamento de Historia, Fac. de Filosofía y Letras, Universidad de León, Campus de Vegazana s/n, 24071, Spain d Alan Judd Partnership, High Mickley, Northumberland, UK article info Article history: Received 15 November 2013 Received in revised form 20 March 2014 Accepted 21 March 2014 Available online 14 April 2014 Keywords: Pollen analyses Dinocyst record Geochemistry North Atlantic oscillation Chestnut cultivation Historic period abstract Two sedimentary sequences (coastal and subtidal) were studied in San Simón Bay (Ría de Vigo), situated on the Atlantic coast of NW Iberia. The coastal record is a shallowing upward sequence which evidences a locally-developed low marsh, situated below the current beach, and dated at the second half of the 4th century. During the following decades this low marsh was progressively replaced by an alder swamp which formed on it. This suggests an apparent stabilisation or slow-down of the relative sea-level (RSL), in this site, at the beginning of the Dark Ages (DA). The subtidal sequence studied reects the main changes in the landscape, the hydrological conditions, climate and RSL affecting this part of NW Iberia during the last 1250 years. Evidence of changing dinocysts content in the sediment reveals that two centennial or decadal-scale episodes existed of shelf marine waters more intensely penetrating inside the bay: between the 15 th -18th centuries and at ca 1800e1930 AD. Besides, we related different proxies with the occurrence of four main climatic stages, namely the previously described Dark Ages (DA, ca 350e750 AD), the Mediaeval Climatic Anomaly (MCA, ca 750e1100 AD) and the Little Ice Age (LIA. ca 1500e1930 AD); in addition we propose a regional MCA/LIA transition (ca 1100e1500 AD) that it has not been previously described. Our environmental characterization indicates a persistent North Atlantic Oscilla- tion (NAO) negative mode domain in Ría de Vigo during the MCA, but this became weaker during the LIA and, probably, also during the earlier DA. NAO mode become more irregular during the MCA/LIA tran- sition, generally persisting in dominant negative mode except for a phase of minor upwelling intensi- cation, at ca 1150e1350 AD, which mainly affected the external parts of the ria. We postulate that an almost simultaneous phase (ca 1100e1350 AD) of stronger continental contribution in the sediments may be related to increasing storm intensities, probably linked to a reinforcement of the Easter Atlantic (EA) pattern; and also that the intertidal/supratidal ecosystems inside San Simón Bay may have extended further in the past, at least towards the end of the 5th century, and between ca 1050e1350 AD and ca 1450e1750 AD. A number of local historical references are consistent with our palaeoecological data and so support the chronology proposed as well as many of the environmental changes reconstructed. This good agreement will help in the interpretation of other analogous sequences extending back in time. Ó 2014 Elsevier Ltd. All rights reserved. 1. Introduction Estuarine wetlands are dynamic coastal landforms moulded in the transition between the continental and the marine realms (Perillo et al., 2009). Typically they consist of a complex of natural habitats situated between the freshwater coastal ecosystems and the subtidal zone, forming ecotones of notable productivity and * Corresponding author. Tel.: þ34 (9) 86 812007; fax: þ34 (9) 86 812624. E-mail address: [email protected] (C. Muñoz Sobrino). Contents lists available at ScienceDirect Quaternary Science Reviews journal homepage: www.elsevier.com/locate/quascirev http://dx.doi.org/10.1016/j.quascirev.2014.03.021 0277-3791/Ó 2014 Elsevier Ltd. All rights reserved. Quaternary Science Reviews 93 (2014) 11e33

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Quaternary Science Reviews 93 (2014) 11e33

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Quaternary Science Reviews

journal homepage: www.elsevier .com/locate/quascirev

Climate and anthropogenic factors influencing an estuarine ecosystemfrom NW Iberia: new high resolution multiproxy analyses from SanSimón Bay (Ría de Vigo)

Castor Muñoz Sobrino a,*, Iria García-Moreiras a, Yoel Castro a, Natalia Martínez Carreño b,Esther de Blas a, Carlos Fernandez Rodríguez c, Alan Judd d, Soledad García-Gil b

aDepartamento de Bioloxía Vexetal e Ciencias do Solo, Facultade de Ciencias, Universidade de Vigo, Campus de Marcosende s/n., E-36310 Vigo, SpainbDepartamento de Xeociencias Mariñas, Facultade de Ciencias, Universidade de Vigo, Campus de Marcosende s/n., E-36310 Vigo, SpaincDepartamento de Historia, Fac. de Filosofía y Letras, Universidad de León, Campus de Vegazana s/n, 24071, SpaindAlan Judd Partnership, High Mickley, Northumberland, UK

a r t i c l e i n f o

Article history:Received 15 November 2013Received in revised form20 March 2014Accepted 21 March 2014Available online 14 April 2014

Keywords:Pollen analysesDinocyst recordGeochemistryNorth Atlantic oscillationChestnut cultivationHistoric period

* Corresponding author. Tel.: þ34 (9) 86 812007; fE-mail address: [email protected] (C. Muñoz Sobr

http://dx.doi.org/10.1016/j.quascirev.2014.03.0210277-3791/� 2014 Elsevier Ltd. All rights reserved.

a b s t r a c t

Two sedimentary sequences (coastal and subtidal) were studied in San Simón Bay (Ría de Vigo), situatedon the Atlantic coast of NW Iberia. The coastal record is a shallowing upward sequence which evidences alocally-developed low marsh, situated below the current beach, and dated at the second half of the 4thcentury. During the following decades this low marsh was progressively replaced by an alder swampwhich formed on it. This suggests an apparent stabilisation or slow-down of the relative sea-level (RSL),in this site, at the beginning of the Dark Ages (DA). The subtidal sequence studied reflects the mainchanges in the landscape, the hydrological conditions, climate and RSL affecting this part of NW Iberiaduring the last 1250 years. Evidence of changing dinocysts content in the sediment reveals that twocentennial or decadal-scale episodes existed of shelf marine waters more intensely penetrating inside thebay: between the 15th-18th centuries and at ca 1800e1930 AD. Besides, we related different proxies withthe occurrence of four main climatic stages, namely the previously described Dark Ages (DA, ca 350e750AD), the Mediaeval Climatic Anomaly (MCA, ca 750e1100 AD) and the Little Ice Age (LIA. ca 1500e1930AD); in addition we propose a regional MCA/LIA transition (ca 1100e1500 AD) that it has not beenpreviously described. Our environmental characterization indicates a persistent North Atlantic Oscilla-tion (NAO) negative mode domain in Ría de Vigo during the MCA, but this became weaker during the LIAand, probably, also during the earlier DA. NAO mode become more irregular during the MCA/LIA tran-sition, generally persisting in dominant negative mode except for a phase of minor upwelling intensi-fication, at ca 1150e1350 AD, which mainly affected the external parts of the ria. We postulate that analmost simultaneous phase (ca 1100e1350 AD) of stronger continental contribution in the sedimentsmay be related to increasing storm intensities, probably linked to a reinforcement of the Easter Atlantic(EA) pattern; and also that the intertidal/supratidal ecosystems inside San Simón Bay may have extendedfurther in the past, at least towards the end of the 5th century, and between ca 1050e1350 AD andca 1450e1750 AD. A number of local historical references are consistent with our palaeoecological dataand so support the chronology proposed as well as many of the environmental changes reconstructed.This good agreement will help in the interpretation of other analogous sequences extending back in time.

� 2014 Elsevier Ltd. All rights reserved.

ax: þ34 (9) 86 812624.ino).

1. Introduction

Estuarine wetlands are dynamic coastal landforms moulded inthe transition between the continental and the marine realms(Perillo et al., 2009). Typically they consist of a complex of naturalhabitats situated between the freshwater coastal ecosystems andthe subtidal zone, forming ecotones of notable productivity and

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remarkable biodiversity (Paterson et al., 2011). Nevertheless,coastal areas have become heavily populated since prehistorictimes, with most of the population currently living in the coastalfringe and consuming its natural resources (Kent, 2000; EEA, 2006).Therefore, numerous coastal marshes have been threatened, havedeteriorated or destroyed by changes in the inputs of freshwaterand sediment transported from the catchments to the coastal zone(e.g. Shabman and Batie, 1987; Reed, 2000; Silva et al., 2007).Currently, estuarine wetlands are exceptionally vulnerable todegradation due to the combined effects of pre-existing stressmechanisms associated with anthropogenic activity and acceler-ated sea-level rise caused by global climate change (Watson andByrne, 2009).

Sea-level oscillations, i.e. the level of the sea surface withoutreference to the land, are not always equivalent to the relative sea-level (RSL), i.e. the level of the sea as observed at the coastline (e.g.Smith et al., 2011). RSL may be affected by a number of factors,including climatically induced global/eustatic variations in oceanwater volume, tectonic subsidence or uplift of the crust, and glacio-and/or hydro-isostatic adjustment. The regional palaeogeographyand palaeobathymetry also may be influential by determining

Fig. 1. A. Map of the Atlantic coast of NW Iberia showing the Atlantic Galician coast, the sitother geographical sites referenced in the text. B. General map of the Ría de Vigo and its sushallow gas fields, with the location of the discussed sites: CS-6, CORE-8, and other nearby(Desprat et al., 2003); TR (Pérez-Arlucea et al., 2007); CIES (Costas et al., 2009); Ss3 (Álvar

changes in the tidal range (Shennan and Horton, 2002; Vink et al.,2007). Therefore, most of the modern reconstructions of changes inthe RSL are based on the identification and description of usefulregional index points in coastal areas, which are preferentially thindatable basal peats, intercalated in the sedimentary sequences, butpractically unaffected by compaction. They enable comparisonswith other nearby points which are susceptible to compaction (e.g.Gehrels, 1999), and are more frequently interpreted as phases ofstillstands or slow-downs during the sea-level rise (Bungenstockand Schäfer, 2009).

Northwestern Iberia (Fig. 1A) is sensitive to the major climaticoscillations detected in both the subtropical (deMenocal et al.,2000) and the boreal North Atlantic (Johnsen et al., 1992); andmarine conditions in the area governed postglacial inland vegeta-tion dynamics (van der Knaap and van Leeuwen, 1997; Roucouxet al., 2001; Muñoz Sobrino et al., 2005, 2009, 2013). However,the postglacial transgression and the human transformation of thecoastal wetlands limit the useful records near the coastline to someinactive organic deposits of Pleistocene age (e.g. Gómez-Orellanaet al., 2007, 2012) and to some active supralittoral systems (estu-aries, lagoons, etc.), which usually result in rather short and

uation of the Ría de Vigo, the pollen site of BUDIÑO (Gómez-Orellana et al., 1996), andrroundings, showing its bathymetry and the main river drainage areas. C. Ría de Vigo,data Vir-94 (Muñoz Sobrino et al., 2012); ZV-01 (Muñoz Sobrino et al., 2007); Vir-18

ez-Iglesias et al., 2006); SsMP (Álvarez-Iglesias et al., 2007).

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discontinuous Holocene records (e.g. Bao et al., 2007; Danielsen,2008; Costas et al., 2009).

Studies of palynomorphs in shallow, fully marine environmentsmay be a useful alternative for the reconstruction of the mainchanges affecting the estuarine wetlands, because deposition ratesare higher and almost continuous in the deepest parts of the basins,and they combine data from both continental and marine realms(Muñoz Sobrino et al., 2007).

Here we present and discuss two sedimentary sequences ob-tained, respectively, from the intertidal-supratidal fringe and thenearby subtidal area of an inner embayment in NW Iberia, SanSimón Bay (Fig. 1B), a site of community importance (SCI) due to itsnatural values (Ramil Rego et al., 2008). These may complementdata obtained previously from a core (Vir-94, see Fig. 1C) taken inthe adjacent ria, i.e. a submerged unglaciated river valley, wherethe main environmental changes that occurred during the mid-Holocene were condensed. The Vir-94 stratigraphic record weresubsequently disrupted by the downlapping progradation occurredduring the past two millennia (see Muñoz Sobrino et al., 2012).Here, an organic-rich section (CS-6, Fig. 1C) from the intertidal zoneis described, revealing a regional oscillation in the RSL. This is

Fig. 2. A. Schematic representation of the system of currents offshore western Iberia. B. Vertet al. (2004), and others cited by them. C. Schematic representation, simplified from Oterogenerated by along shore winds interacting with the NW Iberia coastal topography: 1) southcoast; 2) the WIBP expands when the downwelling phase declines by relaxation of the winnortherly winds. The 35.6 isohaline (coarse line) is marked as reference of the limit of the2000 m.

compared with pollen evidence from a nearby subtidal record(CORE-8, Fig. 1C) that indicates the principal changes affecting theregional vegetation landscape and hydrology, during historic times.This evidence is combined with other regional data and historicalinformation. Our main objectives are to reconstruct the majorchanges (environmental, climatic, oceanic or human activities)affecting an estuary from NW Iberia during the past two millennia,a period of absolute sea-level rise (e.g. Kemp et al., 2011), to discusstheir causes (natural or anthropogenic) and to evaluate theirenvironmental and social consequences. These goals will providean objective basis for estimating the potential risks for the man-agement of these very sensitive ecosystems.

2. Settings

2.1. North-western Iberia current system

Surface waters offshore western Iberia (Fig. 2AB) are dominatedby the Portugal Current System (PCS) flowing equatorward in latespring and summer, but poleward in autumn and winter (e.g.Sprangers et al., 2004; Otero et al., 2008). The Eastern North

ical distribution of the marine waters in front of the Galician coast, following Sprangerset al. (2008) of three different situations (distributions of surface current and salinity)erly winds promote a confinement of the Western Iberian Buoyant Plume (WIBP) to thed; 3) the WIBP reaches its maximum development offshore by upwelling promoted bybuoyant plume in all maps. Marked isobath (white) lines are 100, 200, 500, 1000 and

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Atlantic Central Water (ENACW) flows under the PCS, but is dividedin an ENACWst subtropical branch (lighter and relatively warm),and another ENACWsp subpolar branch (less saline and colder).ENACWst may be replaced westward by a southward extension ofthe North Atlantic Current, called West North Atlantic CentralWater (WNACW). The Mediterranean Water (MW), highly salineand relatively warm, flows northwards along the Iberian coast,between ca 550e1600 m depth. The deepest waters offshore arenutrient-rich and oxygen- poor bottom masses, like the NorthAtlantic Deep Water (NADW) and the lower-saline Labrador SeaWater (LSW).

2.2. Ría de Vigo: regional framework

Ría de Vigo (175 km2) is the southernmost drowned ungla-ciated river valley (ria) on the temperate and humid GalicianAtlantic coastline of NW Iberia. The connection of the ria with theopen sea is partially blocked by the Cíes Islands, a natural barrierthat controls the oceanographic and sedimentary processeswithin the ria. Rande Strait, a narrow channel 600 m across and1.5 km long, connects the outer ria to San Simón Bay, a NeSorientated, almost landlocked, shallow basin 10 km long and 4 kmwide (Fig. 1).

At the present-day, most of the basin is quite densely populatedbut it consists of a complex mosaic of urban soil, repopulations(mainly Eucalyptus spp. and Pinus spp.) and scrubs (Erica spp.,Calluna (L.) Hull., Ulex spp.), with scarce stands of deciduous oakforest (Quercus robur L., Betula alba L., Corylus avellana L.) and ri-parian woodlands (Salix spp., Alnus glutinosa (L.) Gaertn., Fraxinusexcelsior L., F. angustifolia Vahl.).

The main factors controlling the stratigraphic evolution andsedimentary facies distribution in the ria are the orographic andgeological frameworks (granites and metamorphosed Palaeozoicsediments), the climate, the oceanographic conditions and the RSLvariations (García-Gil et al., 1999; García-García et al., 2003, 2005).Mixed siliciclastic and skeletal gravels prevail on the present seafloor both in the outer ria area and along the coastal margins. Incontrast, the central and inner parts are dominated by clay and silt,rich in organics (Vilas et al., 1995). The use of high-resolutionseismic profiling has revealed acoustic turbidity caused by thepresence of shallow gas in some of these fine-grained sedimentaryareas (e.g. García-Gil, 2003, see Fig. 1C).

San Simón Bay (Fig. 3) has a 2.2 m median tidal range (Pérez-Arlucea et al., 2007). Sedimentary environments in the bay arecontrolled largely by tidal processes, with total organic carbon(TOC) in superficial sediments ranging from 2 to 8% (García-Gilet al., 2011). Muddy sediments dominate the subtidal areas,which cover 12.3 km2. The intertidal area extends to about 7.2 km2,mainly in the middle-northern part of the bay; it includes marshes,sandy intertidal flats, estuarine deltaic complexes, beaches andmuddy intertidal flats. Coarse-grained sediments (sand andgravels) are only found close to the river mouths (Fig. 3B; Pérez-Arlucea et al., 2007; Muñoz Sobrino et al., 2012).

2.3. Ría de Vigo: hydrological setting

Surface-water temperatures from outer to inner parts of the riavary from 11e12 �C in winter to 19e20 �C in summer. The averagesalinity inside Ría de Vigo decreases from 36 psu in the fully marineouter part of the ria to 31e32 psu at the entrance of San Simón Bay,and goes down further inside the bay because of freshwater inputs(Fig. 3A). The average fluvial discharge to the bay is 20 m3 s�1, thatis, 75% of the total freshwater input to the whole ria (Pérez-Arluceaet al., 2005). During periods of high river discharge, particularly inspring, vertical salinity gradients develop whereby a thin surface

layer of low-salinity water extends seawards of the Rande Straitinto the main ria.

The ria behaves as a partially mixed estuary with a two-layeredpositive residual circulation pattern, maintained in winter by thefreshwater flow and in summer by upwelling (e.g. Villacieros-Robineau et al., 2013). Along-shore winds interact with thecoastal topography to generate upwellingedownwelling dynamicson the continental shelf that drive the ria’s water circulationpattern (e.g. Souto et al., 2003; Cerralbo et al., 2013). A low-salinitylens formed by river discharge and continental run-off extendsalong the shelf off Northwest Iberia, being the Western IberianBuoyant Plume (WIBP) behaviour mainly determined by the di-rection, intensity and event duration of the wind-induced Ekmantransport (Otero et al., 2008). During downwelling periods, south-erly winds promote a confinement of theWIBP to the coast; but theplume expands when the downwelling phase declines by relaxa-tion of the wind, and reaches its maximum development offshoreby upwelling promoted by northerly winds (Fig. 2C).

Northerly winds prevail in spring and summer, when upwellingforces a two layer density-induced positive circulation in the rias.This is characterised by the outflow of surface water and thecompensating inflow of upwelled water at the bottom. The tran-sition to seasonal (autumn and winter) downwelling, which co-incides with the rapid change to southerly winds, establishes acirculation during which surface coastal water enters the rias todevelop a downwelling front at the location where it meets thewaters from the inner ria which have a higher continental influence(Crespo et al., 2006). The intrusion of nutrient-rich coastal waters atthe seabed increases biological productivity in the ria, and consis-tently enhances the flow of organic matter (OM) towards the seafloor. Nevertheless, anthropogenic activities are also influential andhave increased historically (Méndez Martínez et al., 2011);currently they contribute a significant proportion (>70%) of OM(Evans et al., 2011).

3. Materials and methods

Pollen analyses were performed on two sedimentary records.The first was a trench (CS-6) cut in the intertidal zone of CesantesBeach, where the building of a breakwater modified the sedimen-tary dynamics during the second half of the 20th century (Fig. 3A).Materials studied are peat and mud layers appearing below thepresent-day beach as the sand was progressively removed. Theprofile lies directly on the altered granitic basement and was cut toa depth of 42 cm. Samples were collected at regular 2 cm intervalsand the pollen residue extracted using HCl treatment (Moore et al.,1991). Coarse (>250 mm) and fine fraction (<10 mm) were elimi-nated by sieving. Themountingmediumwas glycerol liquid and theslides were analysed using an Olympus BH2 microscope at 400 and600�magnifications. Themean pollen count per samplewas of 328grains (minimum 124, maximum 496), and a variable number ofnon-pollen palynomorphs (NPP) was identified. Both the pollenand NPP percentages were calculated for CS-6 using the criteriaexplained below. The P/NPPs ratio was defined as the ratio (rangingbetween 0 and 1) of pollen to NPP counts excluding dinocysts andphytoliths.

Pollen, size particle and geochemical analyses was also per-formed in a series of gravity cores (CORE-8, including several rep-licas) that were taken from the survey ship B.O. Mytilus, in a waterdepth of 7.6m, within the gassy zone inside San Simón Bay (Fig.1C).These results are considered in the context of the earliergeochemical studies presented in García-Gil et al. (2011) and thoserelating to previous investigations (Fig. 1C): vibrocores ZV-01 andVir-94, both obtained from the Rande Strait (see Muñoz Sobrinoet al., 2007, 2012). CORE-8, used for pollen analyses, penetrated

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Fig. 3. A. Map of San Simón Bay and its surrounding area showing the location of the analysed sites: CS-6, CORE-8, the modern coast-line, the old seaport of Redondela and othersites referred in the text, and the set of surface samples discussed in García-Moreiras (2013). Dashed lines into the bay represent the main fresh water sources. B. Distribution of themain habitat types present in the site of community importance (SCI) ES1140016-Enseada de San Simón (see Muñoz Sobrino et al. (2012).

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to 356 cm below the present seabed (b.p.s.b.). This is below the topof the acoustic turbidity (i.e. the acoustic gas front) which, at thislocation, occurs at 100 cm b.p.s.b. (García-Gil et al., 2011; Martínez-Carreño and García-Gil, 2013).

Particle size distribution (established at 10 cm intervals alongthe core, see Fig. 4) was determined after adding hydrogenperoxideto destroy the organic matter and sodium hexametaphosphate todisperse the clay. The suspension was then sieved (63 mm) toseparate the sandy fraction (>63 mm) from the clay and silt frac-tions; large pieces of shell material were excluded so as to avoidbiasing the data. The sandy fractionwas dried at 60 �C andweighed.The suspension containing clay and silt was added to a volumetricflask and made up to 1 l with water. Finally, the suspension washomogenized and the particle size was determined by sedimen-tation analysis based upon Stokes’ Law using a MicromeriticsSediGraph 5100. Nitrogen (N), Sulphur (S) and Total Organic Carbon(TOC) concentrations were determined at 5 cm intervals by com-bustion with an elemental analyser (Carlo Erba-EA1108). Thesamples for TOC analysis were first acidified with 30% HCl, and thenmeasured by combustion with a ThermoFinnigan FlashEA 1112analyser. The pH and redox potential (Eh) were determined at10 cm intervals along the core at the time of sampling. The pH wasdetermined with a combination pH electrode and the Eh with aSenso-Direct Oxi-200 electrode. Methodology used for methaneextraction and quantification are detailed in García-Gil et al. (2011).

Pollen samples of 2.5 (or 5 in some cases) cm3 fresh sedimentwere prepared using HCl þ HF treatment (Moore et al., 1991) andthe same sieving and mounting methods described above. Most ofthe core was subsampled at regular 10 cm intervals, with severaladditional samples taken at 2, 4 or 6 cm to get higher resolution and

Fig. 4. CORE-8: lithology, results of the textural analysis and its correlation with some releMethane Transition Zone (SMTZ) is also shown.

to verify the reliability of a number of major changes observed inupper and deeper sections of the core. Samples from the upper296 cm were also spiked with Lycopodium spores for absolutepollen analysis. More than 825 palynomorphs per sample wereanalysed at each of 68 levels. A mean of 264 grains of pollen wascounted per sample (minimum 211, maximum 347). Terrestrialpollen percentages were calculated on the basis of the sum ofterrestrial pollen; these ranged between 193 and 311 pollen grainsper sample. Non-pollen palynomorphs (NPPs) include micro-foraminiferal linings (Stancliffe, 2002), and fungal and fresh/brackish-water algae remains (van Geel et al., 1989; van Geel,2003). Their percentages are based on total pollen þ NPPs. Themean number of dinocysts counted per sample was 316 (minimum210, maximum 647). The percentages of the different types ofdinocysts (identified groups follow Marret and Zonneveld, 2003;Sprangers et al., 2004) were calculated in relation to the totaldinocyst count. Pollen/dinocyst accumulation rates (respectivelyPAR/DAR, expressed as number of grains [or cysts] cm�2 yr�1) werealso calculated for the samples from the upper 296 cm section.Finally, the ratio of dinocysts to pollen þ spores þ dinocyst count(the D/P ratio, ranging between 0 and 1, see McCarthy and Mudie,1998) was calculated for each sample, to show their temporalvariation.

Two radiocarbon dates (Table 1) were obtained on terrestrialcharred material found in the profile CS-6. They were calibratedusing the INTCAL13 curve (Reimer et al., 2013). The polynomialmethod (Blaauw and Heegaard, 2012) was used for the age-depthmodel (Fig. 5). The temporal scales in full marine sediments arecommonly based on radiocarbon dating of biogenic carbonatesbecause radiocarbon dates of bulk sediment may be largely

vant geochemical data previously published in García-Gil et al. (2011). The Sulphatee

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Table 1Radiocarbon dates. (1) Radiocarbon age from García-García et al., 2003, dating the Pinus pollen expansion in at 21 cm depth in ZV-01 (see the text, Muñoz Sobrino et al., 2007).(2) Depth of Pinus pollen expansion observed in CORE-8.* Two-sigma confidence interval used in the age-models.

Site Depth (cm) Date 14C (a BP) Lab. Code Material C13/c12 (&) Calibration curve Cal age AD (1s) Relative area Cal age AD (2s) Relative area

ZV-01(1) 37(2) 500 � 30 Geochron Shell e MARINE13 1940epost 19501713e1895

0.0500.950*

1648- post 1950 1*

CORE-8 272.5 1430 � 30 Beta-320479 Shell þ2.4 MARINE13 845e1056 1 746e1170 1*CORE-8 351 1970 � 40 Beta-275715 Organic sediment �23.6 MARINE/INTCAL13 217e398 1 98e466 1*CS-6 11 1630 � 50 Beta-219290 Charred �25.8 INTCAL13 354e366

380e434452e470487e534

0.0600.5030.0960.341

326e549261e278

0.978*0.022

CS-6 35 1700 � 50 Beta-219291 Charred �17.0 INTCAL13 257e285321e399287e295

0.2200.7270.053

221e430518e528493e510

0.983*0.0060.011

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unreliable (e.g. Colman et al., 2002; Megens et al., 2002). However,it is difficult to find datable carbonates within muddy sediments inthe Ría de Vigo, because the diagenesis of OM and the fluvial inputspromote carbonate dissolution (Álvarez-Iglesias et al., 2006).Therefore, the chronology of CORE-8 (located inside a shallow gasfield) was primarily supported by only three radiocarbon dates: oneof them determined on a shell found about 273 cm depth, anotherobtained on bulk sediment at 351 cm depth; and the third

Fig. 5. A. Ageedepth models performed for cores CS-6 and CORE-8, constructed using theconfidence interval also shown) in Table 1; black symbols correspond with pollen eventsrespectively used for build them. Three different models are presented in the case of CORE(green); and pollen markers and biogenic radiocarbon dates (red). The radiocarbon age obtaithe text). B. Cluster analysis (CONISS) revealing the dissimilarity existing between the CORgraphically constrained statistical analysis was produced using the square-root transformaticounts. The lower depth was used when codifying samples. (For interpretation of the referarticle.)

estimated from a shell which dated the Pinus pollen expansion inthe nearby ZV-01 core (Fig. 1C, see Muñoz Sobrino et al., 2007), andsubsequently transposed to date the same pollen event (37 cmdepth) in CORE-8 (Table 1, Fig. 5A). The ages of biogenic carbonateswere calibrated using the CALIB 7.0 software (Stuiver et al., 1986e2013) and the MARINE13 curve (Reimer et al., 2013), applying alocal marine reservoir correction of DR ¼ �7�90 (Stuiver et al.,1986e2013). Although the bay has a fully marine water column,

chronological benchmarks: white squares are the radiocarbon dates (two-sigma agenumbered in Table 2. Polynomial method (CS-6) and LOWESS splines (CORE-8) were-8, respectively including all the radiocarbon dates (dotted line); pollen markers onlyned from bulk sediment in the base of CORE-8 has been considered to be an outlier (seeE-8 (CRR) and CS-6 (CS) samples at the point indicated by the broken line. The strati-on (Edwards and Cavalli-Sforza’s chord distance) of the terrestrial vascular plant pollenences to colour in this figure legend, the reader is referred to the web version of this

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Table 2Pollen criteria and radiocarbon dates used to establish the relative chronology of the pollen profile CORE-8, obtained inside the gas field, and their synchronization with otherpublished subtidal pollen records in Ría de Vigo: Vir-94 (Muñoz Sobrino et al., 2012); ZV-01 (Muñoz Sobrino et al., 2007); Vir-18 (Desprat et al., 2003). The age of the historicalevents used are discussed in the text.

No pollenevent inFig. 4

Age AD Age cala BP

Vir-18depth(cm)

ZV-01depth(cm)

Vir-94depth(cm)

CORE-8depth(cm)

Pollen event/Radiocarbon date References

1 1960 �10 19 5 2 Extensive reforestation with Eucalyptus Ramil-Rego et al. (2012)2 1930 20 46 35 8 Modern reforestations since 1930s López Torre (2009)e 1800 150 73 21 55 37 14C; start of Pinus pollen expansion Muñoz Sobrino et al. (2007)3 1720 230 101 41 77 Regional reintroduction of pinewoods Bouhier (2001)4 1600 350 71 Early introduction of Zea mays L. Vazquez Marinelly et al. (2007)5 1400 550 142 141 182 Forest exploitation, AP decrease Muñoz Sobrino et al. (2012)6 1300 650 172 171 65 212 Decline in arable farming; AP increase Peña Santos et al. (1999)7 1100 850 216 >95 232 Beginning of modern increase in Castanea Muñoz Sobrino et al. (2012)e 960 990 273 14C This papere 870 1080 227 14C Desprat et al. (2003)8 750 1200 303 352 First mediaeval increase in Castanea Muñoz Sobrino et al. (2012)

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the carbon in bulk sediment was derived from a mixture ofterrestrial and estuarine material (plants, algae, microbial mats,invertebrates). Hence, it was calibrated by running a 50:50 mixedmarine-terrestrial model using the Mixed Marine & NH Atmo-sphere dataset (Table 1). The chronological control of CORE-8 wasalso independently determined using the same combination ofpollen markers and historical information (Table 2) used previouslyby Muñoz Sobrino et al. (2007, 2012). Thus, three different age-models were finally performed by LOWESS splines (Blaauw andHeegaard, 2012), respectively using: 1) the radiocarbon datesonly, 2) the pollen markers only, and 3) the pollen markers com-bined with the two biogenic carbonate radiocarbon ages (Fig. 5A).

The program TILIA 1.7.14 (Grimm, 1990e2011) was used forprocessing the data and preparing diagrams. Pollen and dinocystdiagrams were independently zoned using a Constrained Incre-mental Sum of Squares (CONISS) cluster analysis (Figs. 6e10). Asimilar analysis was used to compare the two terrestrial pollenrecords, in order to discuss the synchronicity between the CS-6record and the basal horizons in CORE-8 (Fig. 5B).

4. Results

4.1. CS-6 Lithology and chronology

The 42 cm deep profile CS-6 (Fig. 6) consists of 12 cm of peatover a basal clayey layer 30 cm thick. The peat is a dark alder swampdeposit which is rich in humic material and has abundant charcoaland plant remains. The basal layer has less organic material and55e75% clay. Radiocarbon dating of the base of the peat (11 cmdepth) reveals a 14C age of 1630 � 50 yr BP (2s: 325e550 AD),whilst organic matter from 35 cm provided 14C age of 1700 � 50 yrBP (2s: 220e430 AD). Base and top CS-6 ages (ca 300 and 475 AD,respectively) were estimated by interpolation of the polynomialmodel obtained (Fig. 5).

4.2. CS-6 Palynological analyses

The palynological zones described below were identified usingcluster analysis performed on the pollen and NPP records. Threelocal pollen assemblage zones (LPAZs) have been recognized. Somehave been subdivided to highlight particular facts related to theregional vegetation dynamics or the sedimentary conditions in thearea (see Figs. 6 and 7).

LPAZ-1 (42e24 cm). e This entire zone is characterized bymoderate percentages of tree taxa (<40%), the continuous presenceof different types of thickets (Erica, Helianthemum-type, Ulex-type)and crops (Cerealia-type), and the notable development of herbs

(Poaceae), green algae (Chloroccocales) and cyanophyta (Gloeo-capsa, Gloeotrichia). Subzone LPAZ-1a reflects the highest repre-sentation of different freshwater or brackish taxa, includingvascular aquatics (Ranunculaceae, Potamogeton-type, Isoetes) butalso dinocysts, central diatoms and green algae. Quercus reaches arelative maximum in the subsequent LPAZ-1b, where there are alsoincreases in the abundance of Cyperaceae, some fungal remains(Type-200) and the spicules of freshwater poriferae. Poaceae,Armeria and the coenobial form Gloeocapsa peak in LPAZ-1c, whichalso has the highest percentages of dinocysts found in this profile(Fig. 7).

LPAZ-2 (24e12 cm). e This zone is characterized by a slightreduction in the proportion of total tree pollen (AP) and increases inherbs (Poaceae), ferns (Pteridium, Monolete-type) and Gloeotrichia;central diatoms and dinocycsts are present throughout.

LPAZ-3 (12e0 cm). e This zone records the decline of thicketsand the recovery of total tree pollen; Quercus and riparian trees(Alnus, Salix) account for the majority of this recovery, but notCastanea, whose percentages decline. A rapid development ofCyperaceae occurs in subzone LPAZ-3a, where other vascularaquatics (e.g. Myriophyllum, Typha, Nymphaea) also increase. Aprogressive disappearance of dinocysts and the substitution ofcentral diatoms by others with stronger freshwater affinities(Navicula, Fragillaria, Diploneis) was also observed. Noticeable peaksof Gloeotrichia and phytoliths were also recorded in this earlysubzone, whilst the greatest abundances of Alnus, Typha, Salix andSordariaceous ascospores were recorded in the later subzone,LPAZ-3b.

4.3. CORE-8 Lithology, geochemistry and chronology

The whole of CORE-8 is comprised of fine-grained mud withmore or less equal proportions of silt and clay, without evidence ofbioturbation; it is mainly greenish black in colour, with some black(Munsell Soil Colour Chart, 1998). The coarse (sand) fraction ismostly bioclastic, with bivalve and gastropod fragments morefrequently found between 87 and 150 cm (sandy mud), and onlyoccasionally appearing below this horizon. Gas bubble voids areapparent in the sediment between 85 and 140 cm depth (Fig. 4).The pH values oscillate between 6.30 and 7.72 in the upper 80 cm ofthe core, but become more stable, close to neutral (ca 7.2), belowthis. The measured Eh values were always negative, ranging be-tween e137 and e306 mV. Sulphate concentrations decrease lin-early from 35mM at 5 cm core depth to 6 mM at 55 cm; and almostdisappear below 75 cm. Methane was the only gas detected in thesamples. It is absent in the top 55 cm, but its concentration sharplyincrease to 0.86 mM at 90 cm, and remains between 0.52 and

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0.86 mM below this (Fig. 4). Both percentages of total organiccarbon (TOC%) and N% show similar patterns of variations. TOC%varies from 4.33 to 10.04 wt% and the ratio of TOC/N from 11 to 21(Fig. 11). The highest TOC% values (7.22e9.38 wt%) were recordedbetween 80 and 160 cm, although some high values (<8.73 wt%)were also registered between 190 and 250 cm, with a peak(10.04 wt%) near the bottom of the core (at 346 cm). The carbonisotopic compositions of TOC (d13C) vary between e21.5 and e

23.6& (García Gil et al., 2011). The chronology estimated for thecore differs notably betweenmodels: ca 1650 yr BP using all the 14Cages, but ca 1250 yr BP when the 14C age of the bulk sediment isexcluded (Fig. 5A).

4.4. CORE-8 Palynological analyses

The palynological zones described below, and illustrated inFigs. 8e10, were identified using cluster analysis.

4.4.1. Pollen and NPP recordSeven local pollen assemblage zones (LPAZs) have been recog-

nized, some of them subdivided (see Figs. 8 and 9).LPAZ-1 (356e348 cm). e This zone evidences the regional

occurrence of crops (Cerealia-type), with relatively low percentagesof deciduous oak (<15%) but successive peaks of Poaceae (25%) andCastanea (ca 30% at 352 cm depth). Some aquatic taxa (Cyperaceae,Equisetum, Sphagnum) and fungal remains (mainly hyphae remains,Sordariaceous ascospores Type-55 and Conidia Type-200) are alsonotably represented.

LPAZ-2 (348e296 cm). e This entire zone is characterised by anAP of approximately 30%, mainly due to the co-dominanceobserved between Quercus and Castanea. Furthermore, there is anincrease in other taxa that may be associated with the regionaldeciduous/riparian forests (e.g. Alnus, Salix, Hedera, Osmunda). Inspite of this, an intermediate LPAZ-2b subzone is recognized whereAP declines slightly and there are higher percentages of grasses(Poaceae), heath (Erica), shrubs (Ulex-type), ferns (Pteridium) andfungal spores (e.g. Gelasinospora sp., Phragmospores, Type-200).

LPAZ-3 (296e252 cm). e The regional recovery of the deciduous(Quercus) and riparian (Alnus) forests is represented by this zone,with AP reaching its maximum (over 50%) in spite of the reductionof Castanea (10%). Minimum percentages of Sordariaceous asco-spores Type-55 and an increasing proportion of algal remains(Botryococcus, pennate diatoms) are also recorded.

LPAZ-4 (252e152 cm). e This large zone is characterized by anew, significant increase of Castanea (about 30% after 232 cmdepth) and the decline of other regional deciduous/riparian trees(Quercus, Alnus). The greatest chestnut percentages are reached insubzone LPAZ-4a, along with noticeable increases of Pteridium andfungal remains (Phragmospores, Type-55, Type-200). Castaneapercentages decline in the subsequent LPAZ-4b, where the mini-mum of Cerealia-type occurs (212 cm depth), and there is also anincrease of Erica, Poaceae, Monolete-type spores and Botryococcus.

LPAZ-5 (152e62 cm). e Globally this zone confirms the retreat ofCastanea and also the decline of the regional deciduous forest atca 182 cm depth. Early subzone LPAZ-5a shows a partial recovery ofsome regional tree taxa (Quercus, Alnus) and increases of Pteridiumand several groups of fungal remains (Hyphae remains, Type-55,Type-200). The AP minimum is recorded when Cerealia-type rea-ches its maximum (about 4%) in the subsequent LPAZ-5b.

LPAZ 6 (62e10 cm). e The first recognized pollen is evidence ofthe introduction of Zea mays within this zone; AP remains low(<40%) throughout and thickets (Erica, Ulex-type, Helianthemum-type) and herbs (e.g. Poaceae, Compositae) achieve their maximumdevelopment. At the end of this zone the first evidence of modernrepopulations with pine appears at 37 cm depth.

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LPAZ 7 (10e0 cm). e Pinus percentages increase noticeably at8 cm depth in this last zone, with chestnut percentages decliningtowards their recorded minimum, and also the appearance ofpollen evidence of the regional introduction of Eucalyptus (2 cmdepth).

4.4.2. Dinocyst recordLingulodinium machaerophorum is the more abundant type

throughout the record, usually representing almost 90% of thedinocysts (Fig. 10A) but its highest DAR values recorded at ca 50 cmand ca 275 cm depth (Fig. 10B). The D/P ratio was generally higherthan 0.5 and shows several peaks about 0.7, the exceptions beingthe intervals 192e242 and 72e152 cm, where relative pollenabundances are substantially higher and the D/P ratio declinesbelow 0.4 and 0.2, respectively. Other several minor declines in theD/P ratio also occur in the upper 50 cm and below 250 cm depth.Four main dinocyst assemblage zones (DAZs) were recognized(Fig. 10).

DAZ-1 (424e288 cm). e Several less abundant forms areconsistently present in subzone DAZ-1a, like Operculodinium (bothO. centrocarpum and those with short processes), Bitectatodiniumtepikiense, Selenopemphix spp, Brigantedinium spp. or Impagidiniumspp. Some of them (Selenopemphix spp, Brigantedinium spp.,Impagidinium spp.) disappear in the susbsequent DAZ-1b, when L.machaerophorum slides and O. centrocarpum and Votadinium spi-nosum increase.

DAZ-2 (288e145 cm). e L. machaerophorum recovers its highestvalues but O. centrocarpum retreats along this zone. Subzones DAZ-2b and DAZ-2d represent moderate increases of Spiniferites spp., B.tepikiense and V. spinosum; and some rise of Operculodinium shortprocesses is observed in DAZ-2c.

DAZ-3 (145e75 cm). e A noticeable decline in L. machaer-ophorum is recorded while others forms increase, like B. tepikiense,Selenopemphix spp, Brigantedinium spp., V. spinosum, and Nem-atosphaeropsis labyrinthus; and particularly, Spiniferites spp., whichpeaks near 20%.

DAZ-4 (75e0 cm). e L. machaerophorum increases again, but notin subzone DAZ-4b, where there are new increases in Spiniferitesspp, B. tepikiense, Selenopemphix spp, and V. spinosum.

5. Discussion

5.1. Chronologies and correlation between sequences

Radiocarbon dates established that the most probable age forthe peat layer in CS-6 is between the 4th and 5th centuries; andsimilar radiocarbon ages are attributed to the organic muds fromthe lower part of CORE-8 (Table 1, Fig. 5). Thus, the start of thesubtidal sequence might be nearly contemporaneous with thecoastal record. However, a number of lines of evidence contradictedthis. Firstly, the three radiocarbon ages available for CORE-8 predictthat significant changes occurred in the sedimentation rates at thebottom of the sequence. The presence of gas in the upper sedimentmakes it impossible to identify the lower unconformable seismicreflectors (Martínez-Carreño and García Gil, 2013), but there is notextural (Fig. 4) or palynofacies evidence (Fig. 11) to indicate theoccurrence of an erosive event (cf. Muñoz Sobrino et al., 2012). Onthe other hand, CONISS analysis confirms that there are large dif-ferences between the terrestrial pollen assemblages obtained fromboth apparently contemporaneous CS-6 and CORE-8 sections(Fig. 5B), suggesting that the landscape in the surrounding areaswas significantly different when they were deposited. Besides, thereliability of the basal CORE-8 radiocarbon date may be consideredlow. Stable and radioactive carbon isotopic compositions of particlesize fractions vary considerably with particle size in estuarine

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Fig. 8. CORE-8: A) Results of the pollen analysis and D/P ratio. Only selected percentages curves are shown. Hatching denotes �10 magnification of the x-axis values. Roman numerals correspond to the historical events described inTable 3. B) PAR (grains cm�2 yr�1) of selected pollen types. Green and orange shading respectively represent the stages of partial recovery of the deciduous forest, and the stages of deciduous forest declining discussed in the text. (Forinterpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

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sediments (Megens et al., 2002); and organic carbon from bulksediment commonly yields older ages than the biogenic carbonates(Colman et al., 2002). Furthermore, lipids and biomass of certainarchaea/sulfate-reducing bacteria aggregates, which are commonin both quiescent sediment and dynamic methane seeps, are highlydepleted in 13C and 14C (e.g. Pearson et al., 2005; Kessler et al.,2008; Alperin and Hoeler, 2010). Molecular evidence of the exis-tence of this type of microorganisms has been recently identified inCORE-8 by Luis et al. (2012). A reliable explanation for this chro-nological inconsistency may be that the microorganisms thatinhabit methane-rich sediments had affected the apparent radio-carbon age obtained from the organic mud. Therefore, the radio-carbon date obtained from the CORE-8 organic mud at 351 cmdepth has been considered as an outlier and was not subsequentlyused in the age model (Fig. 5).

Our CORE-8 chronology was finally constructed using theradiocarbon ages of the two shells included in the mud (272.5 and27 cm depth), combined with pollen markers dating certain hori-zons (see Table 2, Fig. 5). This pollen chronology is based on theactualization of the same criteria previously used inMuñoz Sobrinoet al. (2012), namely the arrival of new crops to this region duringthe first decades of the 17th century (e.g. Z. mays L.) and themodernrepopulations with pines and Eucalyptus (cf. López Torre, 2009;Ramil-Rego et al., 2012). Furthermore, we assume that the medi-aeval chestnut exploitation presumably began in this region fromthe end of the 8th century onwards (vanMourik,1986), and that theage of the most recent Castanea pollen increase can be mostprobably dated between the 12th century and the first decades ofthe 15th century. In the meantime, there was a period in the 14thcentury that was characterized by the abandonment of some of thepreviously cultivated areas and the recovery of the regional de-ciduous forest (see Muñoz Sobrino et al., 2012). The age of eachpollen event adopted in the age-depth model was established byusing the historical information in its most conservative approach,i.e. considering the oldest year of the range indicated by theavailable references as the tie point (e.g. 750 AD for the second halfof the 8th century; 1700 AD for the first decades of 18th century; or1960 AD for the early sixties). We assume that the dating error ofthese points oscillates between a few years and several decades;but it is always comparable with (or lower than) the error associ-ated to the radiocarbon ages used in the model (�30 years).

This chronology (Table 2, Fig. 5) suggests that the CORE-8sediment probably accumulated between the 8th and the 20thcentury; and therefore, there may be a gap of about three centuriesbetween the two sections analysed. Sedimentation rates calculatedfor both sequences by using these age attributions (2.4 and2.8 mm year�1) are consistent with those calculated by Álvarez-Iglesias et al. (2007), using 210Pb and 137Cs, in the modern inter-tidal mud flat of the Bay (Fig. 1C). However, noticeable discrep-ancies have been described between the sedimentation ratepredicted by radionucleide method and that obtained by radio-carbon, due to an expected lack of compaction of the most recentsediments or eventual changes of the sedimentation rates overtime (e.g. Leroy et al., 2007). To evaluate this possible source oferror, other available historical data (that were not primarilyincluded in our age-model) are utilized later in the discussion of theresults for assessing the environmental changes described by ourrecords and testing the proposed chronologies (Table 3). None-theless, note here that the histories of the nobility and the eccle-siastic domains that historically met around San Simón Bay are

Fig. 9. CORE-8: A) Results of the NPP analysis and D/P ratio. Only selected percentages curvecorrespond to the historical events described in Table 3. B) NPP accumulation rates (grains cshading respectively represent the stages of partial recovery of the deciduous forest, and threferences to colour in this figure legend, the reader is referred to the web version of this

incompletely known because archives were almost completelydestroyed when the village of Redondela (Fig. 3A) was sacked in1702, during the naval Battle of Rande (Abelleira Méndez et al.,2002), and also in 1809, during the Battle of River Oitavén(Martínez Crespo, 2000).

5.2. An ancient continental organic horizon at the current seashore

Coastal microbial mats, built on cyanobacteria (Stal et al., 2010),contribute to the stabilization of the sediments on which saltmarshes subsequently formed; and consequently they have animportant morphodynamic role (e.g. Bolhuis and Stal, 2011). Also,these microbial mats typically vary in composition according to thetidal gradient because of a relationship with salinity. Diatoms aremore abundant in the low stations that stay unvegetated andpermanently exposed to the tide (Severin and Stal, 2010). Incontrast, cyanobacteria are usually the most conspicuous micro-organisms in mats on intertidal and supratidal sandy beaches. Thegreatest diversity of filamentous and unicellular types of cyano-bacteria, particularly Gloeocapsa, appears in the young supratidaldunes, which are only occasionally inundated by sea water(Dijkman et al., 2010). Sheaths of another type, Gloeotrichia, appearduring the early stages of an aquatic succession (Chmura et al.,2006), such as shallow, ephemeral, intra-dune ponds (Costaset al., 2009). Otherwise, the algal mats are relatively abundant inthe mud flats, with the fungal spores increasing in the salt-marshcommunities (e.g. Solomon et al., 2000; Al-Nasrawi and Hughes,2012).

Analyses of palynofacies performed on the CS-6 sequence,which is situated below the current Cesantes beach (Fig. 3A), haveshown that the less-organic sediments at the bottom of the profileare progressively enriched in marine diatoms, green algae, fungalremains and cyanobacteria, whereas pollen noticeably increasestowards the top of the record (Figs. 6 and 7). Such results indicatethe development of a consistent ecological succession (i.e. theprogressive transition from the upper-intertidal/lower-supratidallow marsh environments towards the upper-supratidal/highmarsh ecosystems, and the ultimate formation of a freshwaterswamp), just after the end of the Roman Period, at the northernside of the mouth of the River Alvedosa (Fig. 3A). This successioncorresponds with a shallowing upward sequence that may havebeen mediated by different causes.

The freshwater peat could have formed at approximately thelevel of mean high water spring tides (MHWST) or an unknownheight above that level (Shennan and Horton, 2002). Nevertheless,freshwater peats are not always necessarily directly linked to sea-level fluctuations because of specific regional palaeogeographicconditions (Baeteman, 1999). When sediment supply exceeds thecreation of accommodation space by RSL rise, tidal basins willrapidly accrete sediment to high-water levels. As a consequence,the frequency of tidal inundation declines and drainage networksare liable to become redundant and silt up. Eventually, salt marshesencroach upon mudflats, followed, if sufficient time is available, bypeat accumulation (Baeteman et al., 2011).

Therefore, our evidences may have implications, at least, for thereconstruction of some apparent sea-level oscillations inside theBay. The age of the freshwater swamp peat (ca 420e470 AD) is alimiting date in that regional RSL must have been at or below thelevel at which the peat layer was found (e.g. Shennan and Horton,2002; Baeteman et al., 2011). Thus, an apparent regression occurred

s are shown. Hatching denotes �10 magnification of the x-axis values. Roman numeralsm�2 yr�1) of selected NPP types and for the total identified remains. Green and orangee stages of deciduous forest declining discussed in the text. (For interpretation of thearticle.)

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Fig. 10. CORE-8: A) Results of the dinocysts analysis and D/P ratio. Only selected curves of percentages are shown. Hatching denotes �10 magnification of the x-axis values. Romannumerals correspond to the historical events described in Table 3. B) DAR (cysts cm�2 yr�1) of selected dinocysts types and PAR/DAR. Yellow and blue shading respectively representpredominately oligotrophic stages and periods tending towards the eutrophication. The last are defined by lower D/P ratios and decreasing L. machaerophorum accumulation rates(see the text). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

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in San Simón Bay at the end of the Roman Period, by an amount thatmay have been at least equal to the difference between the swamppeat situated over the MHWST and the low marsh environmentsaffected by the mean high water (MHW). Currently, the differencebetween MHWST and MHW inside San Simón Bay is as much as1.8 m (Pérez-Arlucea et al., 2007). In our profile, without consid-ering any possible compaction, we can determine that a verticalaccretion of at least 30 cm occurred between the beginning of the4th century and the first half of the 5th century (Figs. 6 and 7). Inview of the modern configuration of the site, we assume that the

RSL rose at some moment after the 5th century, until an intertidalbeach was formed on the former swamp.

5.3. Seabed taphonomy: geochemical and pollen evidence

Sedimentation rates deduced for CORE-8 during the last 1250years (2.8 mm year�1) are relatively constant (Fig. 5), being onaverage quite similar (ca 2.5e3 mm year�1) to those estimated byÁlvarez-Iglesias et al. (2006, 2007) in adjacent cores and a coastalmud layer (Fig. 1C). CORE-8 analyses reported by García-Gil et al.

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Fig. 11. CORE-8: Summary of the most relevant percentages (%) and [concentrations] (bars) data in the CORE-8 sequence, and the TOC, TOC/N and TOC/S curves described in García-Gil et al. (2011). Blue shading indicates the threeepisodes of lower D/P ratio, respectively dated at ca 1150e1350 AD, 1450e1750 AD and 1800e1930 AD. The two last were also the periods of stronger upwelling increase inside the Bay (UW), but the first mostly affected the externalparts of the ria. Orange shading represent the stages of deciduous forest declining (ca 1050 to 1350 AD, and ca 1450e1750 AD). Grey shadings represent the three stages (ca 750 AD, ca 1100e1300 AD, ca 1500e1750 AD) with highercontribution of continental OM (see the text). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

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Table 3Historical events described in the literature reviewed, which may be supported by the environmental reconstruction resulting from the analyses performed in CORE-8. Romannumerals correspond to the historical events described in Figs. 8e10.

No Figs. 8e10 Age AD Historical events References

(XIV) 1900e1930 Sardine relatively abundant in the Galician coast Valdés Hansen (2004); Vázquez Marinelly et al. (2007)(XIII) 1830e1890 Abundance of sardine decreases Vázquez Marinelly et al. (2007)(XII) 1850 Chestnut stands begun to decline due to fungal diseases Azcárate Luxan (1996)(XI) 1830e1860 Abundance of sardine increases Vázquez Marinelly et al. (2007)(X) 1765e1802 Sardine very scarce, spectacular increase of prices Vázquez Marinelly et al. (2007)(IX) 1702 Naval Battle of Rande, barrier of logs closing S. Simón Abelleira Méndez et al. (2002)(VIII) 1530e1650 The old seaport of Redondela began to collapse.

Chestnut commercialization is locally regulatedMartínez Crespo (2007)

(VII) since 1500 More intense rains described. New fishing techniques Martínez Crespo (2000); Peña Santos et al. (1999)(VI) 1460e1470 New civil disturbances affecting this region Vila (2010)(V) Since ca 1400 Salted fishing exported towards the Mediterranean Martínez Crespo (2000)(IV) 1200e1300 First historical references of coastal fishing nets

and taxes in the regionPeña Santos et al. (1999); Martínez Crespo (2000)

(III) 1200e1450 Social stability increases around S. Simón Bay González-Paz (2009)(II) 950e1200 Military actions and social instability affecting

the bottom of the bayCarballeira Debasa (2007); González-Paz (2009)

(I) <1070 (?) Benedictine Monastery at Cesantes Freire Camaniel (1998)

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(2011) revealed that TOC values in the sediment comprised be-tween 4 and 10%wt, and they concluded that most of the OManalysed along the profile has a mixed (continental and marine)origin (Fig. 11). The palynological studies reported here confirmthis, and also make more apparent new details about the envi-ronmental conditions of sedimentation (Fig. 11). As many as threestages with greater contributions of continental OM have now beenidentified. These occur at the bottomof the core, about 190e250 cmdepth, and between ca 75e150 cm depth. At these levels the TOC/Nratios are higher and the D/P ratio lower than 0.5, whilst the con-centrations of dinocysts in the sediment decrease and are notablylower than those of the fungal remains (concentrations are notavailable for the basal levels). In contrast, the proportion of OM ofmarine origin increases at ca 360e250 cm depth, ca 150e190 cmdepth, and also in the upper 75 cm (Fig. 11).

Higher Eh values and the availability of dissolved sulphate(Fig. 4) indicate that the utilisation of OM is dominated by sulphatereduction above the sulphate methane transition zone (SMTZ,García Gil et al., 2011). A selective preservation of palynomorphsshould be dismissed because of the anoxic conditions that prevailbelow the SMTZ, and because no type of bioturbationwas apparentalong the profile (Fig. 4). On the other hand, it is noted that thereare very high abundances of certain palynomorphs in our record(e.g. Castanea and Pteridium, but also several types of fungal re-mains), which are most probably over-represented (Figs. 8 and 9)when compared with continental pollen curves (e.g. MuñozSobrino et al., 2005). In other coastal areas, it has been demon-strated that the pollen signal may be linked to the whole drainagebasin and that it is mediated by a fluvial influence (e.g. Beaudouinet al., 2007). Accordingly, a previous study (García-Moreiras, 2013)concluded that pollen grains found in the subtidal sediments of SanSimón Bay are widely transported by the river plumes, with veryhigh relative pollen abundances (P/NPP) at the mouth of the RiverRedondela, but pollen concentrations in the sediment decreasingtowards the external part of the Bay (Fig. 3A).

5.4. The anthropogenic landscape since the 4th century

The subtidal Vir-94 sequence (Fig. 1C) previously obtainedoutside Rande Strait (Muñoz Sobrino et al., 2012) was less conclu-sive than this study about the historic period owing to hiatuses.Nevertheless, it revealed that the surroundings of San Simón Baywere progressively deforested since ca 4000 cal yr BP (ca 2050 BC),with chestnut stands being recorded in the area between 3000 and

2500 cal yr BP (1050e550 BC). Other data obtained from nearbyvalleys (Budiño, Fig.1A) also serve to support the same conclusions;and furthermore, they suggest that the coastal area was notablydeforested from the Iron Age onwards (Gómez-Orellana et al.,1996). The two sequences analysed here shed new light on thesepoints. Low AP percentages observed in our coastal CS-6 sequence(Fig. 6) indicate that, just after the end of the Roman Period, theregional forest remained quite open and the hygrophilous alderforest was probably overrepresented. At this time cereals weremost probably cultivated in the surroundings of San Simón Bay. TheCastanea pollen curve remained continuous but always below 15%,yet it may be overrepresented (see above) and therefore it is weaklyjustifiable to conclude that chestnut cultivation was widely estab-lished at this time. Alternatively, chestnut cultivation is clearlyidentified in CORE-8 as occurring during the second half of the 8thcentury, when the Castanea pollen percentages (>25%) exceedsthose of the remaining tree taxa (<25%). After this, the regionaldeciduous forest experienced two stages of partial recovery, duringthe 10the11th centuries and at ca 1350e1550 AD. In the meantime(ca 1050e1350 AD), the chestnut may have been enhanced locallyagain by removing the deciduous woodland. Later, the strongesthistorical deforestation in the area occurred between ca 1550e1750AD, affecting both Castanea and the other deciduous trees(Fig. 8AB). In this connection, the AP minimum found in our record(IX, see roman numerals in Table 3 and Fig. 8) may be associatedwith the blocking of the entrance to San Simón by a barrier of logsduring the naval battle which occurred in 1702 (Abelleira Méndezet al., 2002).

These two historical phases of intensive destruction of thenatural tree canopy (ca 1050e1350 AD and 1550e1750 AD) areapparently linked to strong increases (both percentages and con-centrations) in fungal remains appearing in the subtidal sedimentsof San Simón (particularly Type-55, Type 200 and undifferentiatedhyphae remains) and also two conspicuous D/P ratiominima; but infact they are not synchronic (Fig. 11). Sordariaceous ascosporesType-55 and Conidia Type-200 may be saprophytic fungi which areassociated with herbivorous dung and dead wood. They arefrequently interpreted as being linked towoodland destruction andincreased grazing (Carrión, 2002; van Geel, 2003), but some recentreviews suggest that sometimes this positive association withherbivory is not so obvious (see Baker et al., 2013). In CORE 8, pollenevidence of an early woodland decline with increase of fungioccurred ca 50 years before the first D/P retreat; but the D/P min-imum occurs simultaneously with the second woodland decline

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Fig. 12. Correlation between the two sequences (CS-6, CORE-8) obtained inside SanSimón Bay (Ría de Vigo), and other regional proxies represented during the past twomillennia. A. Black line is the d18O record from the GRIP core represented as a 10-sample running average, using the GICC05 in Vinther et al. (2006) and Rasmussenet al. (2006). Dotted line is the subtropical sea-surface temperature warm anomalies(�C) reconstructed by deMenocal et al. (2000). Grey shading represents the regionalwarmer stages proposed in this paper. They are intercalated by several recognisedstages of upwelling intensification (blue shading), which are interpreted as regionallycooler. Yellow shading represents stages of relaxation of the coastal upwelling system(predominantly oligotrophic). Below, a correlation with the principal climatic stagesdescribed in the literature is proposed. B. Roman Warm Period (RWP), Dark Ages (DA),Mediaeval Warm Period (MWP), Little Ice Age (LIA) following Alvarez et al. (2005). C.Chronology of the Mediaeval Climate Anomaly (MCA) as originally described in Trouetet al. (2009). D. Chronologies for the MCA and LIA in the Iberian Peninsula described byMoreno et al. (2012). E. New age limits proposed for the MCA and LIA in Trouet et al.(2012). (For interpretation of the references to colour in this figure legend, the reader isreferred to the web version of this article.)

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and ca 50 years before the new peak of fungi (Fig. 11). The exper-imental framework developed by García-Moreiras (2013) withmodern sediments in San Simón Bay revealed that the highestabundances of Sordariaceaous ascospores (Type-55), Phragmo-spores/conidia (Types 173, 200, 201 and others) and undifferenti-ated fungal hyphae occur in Juncus or Phragmites communitieslocated in the middle and high marsh, but decreases in the subtidalsamples (Fig. 3A). Hence, we hypothesize that part of these fungalforms might be also associated with Ascomycetous fungi andCoelomycetes, which are the principal decomposers of both certainbrackish and salt-marsh communities, because of their ability towithstand flooding cycles and to decompose relatively recalcitrantmaterial (van Ryckegem and Verbeken, 2005; Al-Nasrawi andHughes, 2012). Therefore, it is proposed here that the environmentsof sedimentation providing these type of pollen assemblages(intertidal/supratidal ecosystems inside San Simón Bay) may befurther extended in the past and, at least, during three stagesthroughout the historic period: towards the end of the 5th century(Figs. 6 and 7), between ca 1050e1350 AD and between ca 1500e1750 AD (Fig. 11). These expansions of the salt-marshes may berelated to the increasing supply of sediments that silted some partsof the estuary but also with climatic reversals, e.g. Dark Ages, LittleIce Age (see discussion below).

5.5. Pollen evidence versus other available historical data

In order to test the age-depth model assumed and the hypoth-eses associated, there is some historical information available thatmay be usefully compared with our own data, i.e. that describinglocal incidents which should be connected with the regional

landscape dynamics, the development of crops, etc. (see romannumerals in Table 3, Figs. 8 and 9). Only imprecise references havebeen preserved about a Benedict Monastery (I, chestnut cultivationand others, Fig. 8) that existed in Cesantes, likely before the 11thcentury (Freire Camaniel, 1998). However, it is well-known that thebridge crossing the mouth of the Oitavén-Verdugo fluvial system(Fig. 3A) was a strategic site during the Middle Ages, because itenabled the terrestrial communication with the booming towns ofPontevedra and Santiago de Compostela (Fig. 1A), and it was just onthe boundary between the domains of the Archbishop of Santiagoand the manors of Pontesampaio and Soutomaior (this since the12th century). There was a small fortification (see González-Paz,2009) named Castellum Sancti Pelagii de Luto, located at the endof the San Simón embayment, on a coastal island near the bridge(Fig. 3A). First references to this stronghold suggest that in the year997 AD it was destroyed for the first time during the invasion of theMuslim Army headed by Almanzor (Carballeira Debasa, 2007). Itmay have been rebuilt subsequently because new references to itappeared at the beginning of the 12th century. In the year 1111 ADSancti Pelagii de Luto was besieged by troops of the ArchbishopDiego Gelmirez, and it was also blockaded by a fleet. The strongholdwas finally conquered and transferred to the loyal local nobility, butduring the following decades it was blockaded again at least threetimes: in 1115, 1125 and 1197 AD. After this long period of disputes(II, AP declines in Fig. 8), the area apparently enjoyedmore stability,during the next few centuries (III, chestnut cultivation increasesagain in Fig. 8) when the stronghold was mentioned only in someadministrative documentation (González-Paz, 2009).

Vila (2010) maintained that the lower valley of the RiverOitavén, also known as ‘o Val do Souto’ (¼ valley of the chestnutgrove), was a sparsely populated, densely forested in 1147 AD (seeFig. 8). At this time, King Alfonso VII bequeathed it on Men PaesSorredea, and his heirs were named the Lords of Soutomaior.During the following centuries the feudal Lords of Soutomaior builttheir main castle a few kilometres upstream (Fig. 3A), and SanctiPelagii de Luto was almost completely destroyed by them, mostprobably, towards the middle of the 15th century (González-Paz,2009). Civil disturbances (VI, partial abandonment of crops, andcertain recovery of regional forest showed in Fig. 8) also occurred inGalicia after the famine of 1465e1467, and this included the siege ofthe castle of Soutomaior (Vila, 2010).

It is also known that the old seaport of Redondela (Fig. 3A) beganto be blocked bymud towards themiddle of the 15th, a process thatincreased during the next century when the rainfall was moreintense (VII, Figs. 8 and 9) and the landscape became almostdeforested (Martínez Crespo, 2000). At the beginning of the 17thcentury the local authorities were still trying to build a newmooring quay to solve that problem, while a series of bylawsexisted that regulated, amongst other things (VIII, Figs. 8 and 10),the commercialization of fish, cereals, wine and chestnut (MartínezCrespo, 2007). The southernmost part of Cesantes beach still isnamed Castañal beach in modern maps (Fig. 3A). Some ancientwoody remains of chestnut trees still appear at the site of Casti-ñeiras, beside the River Alvedosa, and stands of chestnut treespersist on terraces at the southern margin of the Rande Strait(Fig. 3A). The occurrence of these nearby stands may explain theoverrepresentation of Castanea in our pollen sequences, becausethey are on slopes that drain towards the fluvial plume feeding oursite. In this connection, it may be noted that some chestnut pollenpellets (probably staminate catkin remains) have been found inCORE-8. Finally, the occurrence since the middle of the 19th cen-tury (Azcárate Luxan, 1996) of new fungal diseases may also berelated to the modern decline of Castanea (XII, Fig. 8). Thus, duringthe last thousand years there is a noticeable synchronization be-tween independent historical events and our own proxy data,

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Fig. 13. Correlation between the pollen data obtained inside San Simón Bay (Ría deVigo) and other regional proxies represented during the past 1200 years. A. Black lineis the d18O record from the GRIP core represented as a 10-sample running average,

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which apparently supports the usefulness of the age-modeladopted.

5.6. Hydrological conditions inside the Bay

The dinocyst record shows that L. machaerophorum was themost abundant form in the subtidal sediments of San Simón Bayduring the past 1250 years, but it shows a number of minor declines(both percentages and DAR) which are notably associated withdecreasing D/P ratios (Fig. 10). L. machaerophorum tolerates a verybroad salinity range (e.g. Lewis and Hallett, 1997; Marret andZonneveld, 2003; Holzwarth et al., 2010), but it typically prefersregions with strong (seasonal) variability in the trophic state of theupper waters, namely upwelling areas with eutrophic conditionsprevailing only at times of active upwelling, upwelling relaxation orwhen they are crossed by upwelling filaments; and where oligo-trophic conditions exist during time intervals when upwelling isreduced or absent (e.g. Zonneveld et al., 2013). The highest relativeabundances of L. machaerophorum occur in the vicinity of the activeupwelling cells and near river mouths; but seasonal productionarises when stratified upper waters develop after a time of turbu-lence, e.g. at times of upwelling relaxation (Zonneveld et al., 2013).Increases in sea surface temperature (SST) may also force the rise ofL. machaerophorum percentages and concentration (Leroy et al.,2013a). According to the available data, SST is negatively associ-ated with the upwelling in the Atlantic Iberian coast (Alvarez et al.,2011); and in our case, it may be another concurrent factor (Figs. 12and 13ABC).

These ecological requirements agree with the conditions pre-vailing in the Ría de Vigo, but evidence from CORE-8 indicates thatsome noticeable variations occurred inside San Simón Bay duringthe historic period. Most notably, two conspicuous maxima of PAR/DAR ratio exist at ca 1150e1350 AD and ca 1500e1700 AD (Fig.10B).Besides, DAR data reveal two mayor blooms of L. machaerophorum,respectively occurring at ca 950 AD and after 1930 AD; and otherfour relative maxima dated at ca 1050e1150 AD, ca 1350e1500 AD,ca 1700e1800 AD, and ca 1850 AD. Otherwise, its lower accumu-lation rates occurred during the interval 1500e1700 AD, whenthere was significant increase in other forms, namely: Spiniferitesspp., B. tepikiense, Selenopemphix spp., Brigantedinium spp.,V. spinosum and N. labyrinthus. Most of them, with the exception ofBrigantedinium spp. and N. labyrinthus, experienced other minorincreases between ca 1800e1930 AD (Fig. 10).

In Ría the Vigo, those stages in which open-sea dinocysts (most,apart from L. machaerophorum) increase may be indicative ofincreased upwelling, with offshore marine waters penetrating intothe ria and bringing from the shelf some assemblages of dinofla-gellate cysts which are richer in Spiniferites spp. and others (Muñoz

using the GICC05 in Vinther et al. (2006) and Rasmussen et al. (2006). Dotted line is thesubtropical sea-surface temperature warm anomalies (�C) reconstructed by deMenocalet al. (2000). B. L. machaerophorum accumulation rates and DAR (�10) for other forms(Spiniferites spp., B. tepikiense, Selenopemphix spp., Brigantedinium spp., V. spinosum andN. labyrinthus) registered in CORE-8. C-E. Main dinocyst types (%) as respectivelyrecorded in C) CORE-8, D) ZV-01 and E) Vir-94 (Muñoz Sobrino et al., 2007, 2012), Ríade Vigo. F. D/P ratio �10 obtained in CORE-8, ZV-01 y Vir-94. G. Total tree pollen sum (%AP) and %AP-% Castanea in CORE-8. H. Total tree pollen sum in ZV-01. I. Total treepollen sum in Vir-94. J. Total tree pollen sum in Vir-18 (Desprat et al., 2003). K. %Castanea as recorded in all the pollen sequences discussed in Ría de Vigo (CORE-8, ZV-01, Vir-94, Vir-18). Blue shading indicates periods of probable increasing upwelling,with þ, þþ and þþþ representing a growing scale (see the text). Original data weresmoothed using the spline interpolation function in Microsoft Excel. Synchronizationof the most relevant dinocyst and pollen curves published in Ría de Vigo (also thechronology of Vir-18, see the text), was performed following the criteria shown inTable 2. (For interpretation of the references to colour in this figure legend, the readeris referred to the web version of this article.)

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Sobrino et al., 2012). Particularly, B. tepikiense appears offshore NWIberia during the Heinrich-like periods (Eynaud et al., 2000); alsothe highest abundances of Selenopemphix spp. may be associatedwith upwelling in coastal areas (Marret and Zonneveld, 2003).

A number of experimental studies (e.g. Doval et al., 1998;deCastro et al., 2004) have determined that the southern GalicianRías behave like an extension of the shelf during the upwellingseason (MarcheOctober), when northerly winds promote the up-welling of ENACW (Fig. 2). Nevertheless, it seems that the ENACWinfluence hardly reaches the seaward side of the Rande Strait(Tilstone et al., 1994; Montero Vilar, 1999, see Fig. 1B). Intensifica-tion of the upwelling regime during the Little Ice Age (LIA) has beenobserved previously in the middle-inner part of the ria (Fig. 13,Muñoz Sobrino et al., 2007). Nevertheless, the data presented hereshows that the upwelling influence extended into San Simón Bayduring most of the LIA, but it was particularly strong betweenca 1500e1700 AD; and to a minor degree, between ca 1800e1930AD, this last including an intervening period of upwelling relaxa-tion at ca 1850 AD (Fig. 10B).

Whereas V. spinosum is characteristic of fully marine, oligotro-phic/mesotrophic environments, both Brigantedinium spp. andN. labyrinthus may be associated with highly productive surfacewaters (Marret and Zonneveld, 2003). In our record, evidence ofthese dinocysts (Fig. 10) suggest that productivity increased afterca 950 AD, that it was it maximum during the interval 1500e1700AD, and it again increased during the first half of the 19th century(Fig. 10B). A number of historical documents support this inter-pretation (see roman numerals in Fig. 10 and Table 3). Fishing hasbeen an important economic activity in the area since prehistory(e.g. Antela Bernárdez, 2009) and the local inhabitants have tradi-tionally exploited the appearance of sardine shoals in the Ría,stimulated by vertical water movements (Margalef and Andreu,1958). The first historical references to coastal fishing nets in thisregion (IV) appear in fueros dating back to the 13th century (PeñaSantos et al., 1999). In Redondela (Fig. 3A), fishing taxes levied bythe Archbishop are known since 1304 AD, while surplus fish weresalted and exported to the Mediterranean (V), since at least theearly decades of 15th century (Martínez Crespo, 2000). Neverthe-less, the highest peak of fishing occurred during the 16th century(VII), when new fishing techniques were introduced in the AtlanticRías (Peña Santos et al., 1999). The sardine catchwas irregular in thefollowing centuries, but in general terms it declined during the17the18th centuries, with a spectacular increase in price (X)registered between 1765 and 1802 AD (Vázquez Marinelly et al.,2007). Even so, the abundance of sardines increased (XI) duringthe period 1830e1860 AD, declined from 1860 to 1890 AD (XII), andrecovered during the early decades (XIV) of the 20th century(Vázquez Marinelly et al., 2007). These tendencies may be partlyrelated to the political instability, over-exploitation and thecompetence of coastal cetaceans (e.g. Valdés Hansen, 2004); butalso with the changing environmental conditions. With respect tothis, these historical lines of evidence are largely consistent withthe stages of relatively low/high biological productivity predictedby our own data, the higher productivity apparently being linked tothose episodes of lower D/P ratios, when also the percentages andconcentration of L. machaerophorum decrease (Fig. 10AB).

5.7. Climate and regional relative sea-level oscillations

The variability of the main synoptic weather types on Galiciamay be explained by a combination of four large scale atmosphericmodes, namely: the North Atlantic Oscillation (NAO), the Scandi-navian Pattern (SCA), the Eastern Atlantic (EA), and the EasternAtlantic/Western Russia (EA/WR), with one hemispheric mode, theNorth Hemisphere Annular Mode (NAM). Cyclonic, western and

southwestern weather types explain the most important quantityof rain throughout the year. A positive NAO index greatly reducesthe appearance of cyclonic weather inwinter; but an EA pattern hasa positive annual correlation with W and SW weather types, andexplains increasing rainfall in spring, summer and autumn (see e.g.Lorenzo et al., 2008). On the other hand, the influence of upwellingis particularly intense in the western Iberian coast, where observedSST trends are attributed to changes in radiative or atmosphericheat fluxes, but also due to changes in upwelling dynamics (Alvarezet al., 2011; Alves and Miranda, 2013).

In the regional literature, the climate of Western Europe duringthe last two millennia was previously described (e.g. Álvarez et al.,2005) as having two warmer periods (Fig. 12B): the Roman WarmPeriod (RWP, 250 BC to 450 AD, ca 2200e1500 cal yr BP) and theMediaeval Warm Period (MWP, 950 to 1400 AD, ca 1000e550 cal yrBP), alternating with two colder stages: the Dark Ages (DA, 450e950 AD, ca 1500e1000 cal yr BP) and the Little Ice Age (LIA, 1400e1900 AD, ca 550e50 cal yr BP). The Mediaeval Climate Anomaly(MCA, ca 800e1300 AD, ca 1150e650 cal yr BP) was subsequentlyproposed as the most recent pre-industrial warm period. Innorthern Europe the MCA would have been driven by persistentpositive NAO conditions that became weaker with the onset of theLIA (Trouet et al., 2009).

Moreno et al. (2012) reviewed MCA evidence from the IberianPeninsula and found some local differences, some chronologicalinconsistences, and unequal climatic responses (Fig. 12D). Inparticular, data suggest that although the MCA was a dry period inthe Mediterranean area, the humidity increased in the AtlanticOcean side. Even so, they maintained that the data they reviewedhighlight the unique characteristics of the MCA relative to theearlier DA (ca 500e900 years AD, ca 1450e1050 cal yr BP) and thesubsequent LIA (ca 1300e1850 years AD, ca 650e100 cal yr BP)colder periods; and they concluded that those data support thehypothesis of Trouet et al. (2009), that a persistent positive mode ofthe North Atlantic Oscillation (NAO) dominated the MCA. However,this generalization overlooks minor scale fluctuations which areindicated by contrasting hydrographic and climatic scenariosrecorded simultaneously at different latitudes along the AtlanticIberian shore (Lebreiro et al., 2006; Moreno et al., 2012).

The more recent review of Trouet et al. (2012) proposed twoalternatives explaining the transition between MCA (1000e1300AD, ca 950e650 cal yr BP) and LIA (1400e1800 AD, ca 550e150 calyr BP) (Fig. 12E). One hypothesis postulates that the MCA/LIAtransition included a weakening of the Atlantic Meridional Over-turning Circulation (AMOC) and a transition tomore negative NorthAtlantic Oscillation (NAO) conditions, resulting in a strong coolingof the North Atlantic region but increasing precipitation in SWEurope. The alternative proposes an MCA/LIA shift to an increasednumber of storms over the North Atlantic linked to increased mid-latitude cyclogenesis and hence a pervasive positive NAO state.Following Trouet et al. (2012), these two competing hypothesesmay be reconciled: whilst an increase in storm frequency impliespositive NAO, increased intensity would be consistent with nega-tive NAO during the LIA. Such an increase in cyclone intensity couldhave resulted from the steepening of the meridional temperaturegradient from the MCA into the LIA.

The palynological data obtained in the innermost part of Ría deVigo combine information on terrestrial and marine realms andsupport the existence of a direct seaeland interaction. Therefore,they may help clarify the regional conditions in NW Iberia from theend of the Roman Period to the LIA. Pollen data (Fig. 6) indicate thatthe tree canopy in the surroundings of San Simón Bay were quiteopen at the end of the Roman Period (Gómez-Orellana et al., 1996);and they also were basically deforested for a period of almost 300years before the 20th century (Fig. 8). The tree canopy also decayed

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since the 11th and 15th centuries, when only the chestnut planta-tions were apparently preserved, and between ca 1550e1750 AD.Probably, all these environmental crises were essentially promotedby human disturbances; but notably, the increase of continentalOM being supplied to the shallow marine sediments at ca 1500 to1750 AD starts about 50 years before the beginning of the greatestdeforestation that occurred in the basin (Fig. 11).

With respect to the marine realm, we provide local evidencethat an apparent stabilisation or slow-down in the Holocene RSLrise occurred during the transition between the end of the RomanPeriod and the DA (Figs. 6 and 7). Subsequently, dinocyst assem-blages reveal century or decadal-scale anomalies during the last1250 years (Fig. 10), which may be related to stronger upwellingregimes and higher productivity affecting the ria (Fig. 11). The mostrelevant stage occurred from 1500 to 1700 AD, with another lessintense episode between 1800 and 1930 AD. Furthermore, anotherpossible but less apparent stage of eutrophication (increasing per-centages of other forms different to L. machaerophorum, but nottheir accumulation rates, see Fig. 10) is dated at ca 1150e1350 ADinside the bay (Fig. 11). Synchronization between CORE-8 and otherdinocyst records obtained outside the Rande Strait (see Fig. 1C)suggests that: 1) D/P ratios are consistently lower in shallowerwaters (Fig. 13f); 2) the D/P ratio retreats when the upwelling in-tensifies, in all the cases; 3) a minor upwelling intensificationprobably occurred at ca 1150e1350 AD, but it is better defined inthe external parts of the ria (only percentages available) than insideSan Simón Bay (Fig. 13BeE).

In NW Iberia, a stronger positive NAO results in intensificationsof the regional upwelling regime. In turn, this may drive the SSTandthe Sea Surface Height (SSH, Miranda et al., 2013), which might berelated with some minor regional sea-level oscillations (e.g. MuñozSobrino et al., 2009, 2012). For instance, it is well known that thepresent day seasonal tidal regime inside Ría de Vigo promotes aclear decrease of sea-level in the summer time, and an increase inthe autumn season, with a difference of ca 20 cm between thehighest autumn-winter tides and those for the period of upwelling(Lavín and García, 1992).

The two lowest D/P ratio stages described from the CORE-8sequence correspond to the highest abundances of fungal re-mains in the sediments (Fig. 11). Nevertheless, there is a significantdifference between the two stages: dinocyst assemblages suggestthat the more recent episode (ca 1500e1700 AD) may be linked tostronger upwelling regimes, but the earlier (ca 1150e1350 AD)stage occurred during a period of rather persistent downwellingconditions prevailing inside the Bay (Figs. 11 and 13).

Therefore, on one hand our regional climatic characterizationreinforces other previous data from the Galician rias (see Morenoet al. 2012) by indicating that a persistent negative mode NAOdomain dominated in Ría de Vigo during the MCA, and that itbecameweaker during the LIA and, probably, also during the earlierDA (Figs.12 and 13). On the other hand, our results are supportive ofthe alternative hypothesis developed by Trouet et al. (2012), sug-gesting that increased storm intensities during the MCA/LIA tran-sition may help to explain both the low D/P ratio, the higher fungalcontribution observed at ca 1150e1350 AD, and also that uncleartendency towards the eutrophication of the baywaters (Figs. 11 and13BC).

Differences of about two hundred years exist between thechronologies proposed in the literature for the different climaticstages described (Fig. 12). A plausible explanation for most of thepunctual discrepancies between our own data and other re-constructions performed in Ría de Vigo (Diz et al., 2002; Despratet al., 2003; Álvarez et al., 2005; Moreno et al., 2012) is that theprimary chronology used for the Vir-18 (Fig. 12B) was constructedwhen the seismic stratigraphic control of the basin was still not

very exhaustive (Fig. 1C) and it was based on the radiocarbon age ofa shell founded at the bottom of the core, where sand, gravels andbioclastic fragments were very abundant (see Diz et al., 2002). Mostrecent studies have shown that this particle-size distribution maybe associated with the existence of relevant erosive episodes,particularly the 2.8 ka event (see García-Gil et al., 2011; MuñozSobrino et al., 2012). In this connection, a modified Vir-18 chro-nology (only for the upper 3 m) is proposed here. It has beenestablished using only the radiocarbon age originally obtained at227 cm depth, and the same pollen chronology described in Table 1.Following these criteria, the derived sedimentation rates seem tobe quite constant, and the original Vir-18 pollen record is consistentwith the other sequences obtained in the ria (Fig. 13).

6. Conclusions

Pollen data let us reconstruct the landscape dynamics aroundSan Simón Bay (Ría de Vigo); and prevalent NAO conditions havebeing directly inferred from local marine evidence, making thismultiproxy approach possible to develop a more detailed recon-struction of the environmental conditions affecting the Atlanticcoast of NW Iberia during the historic period. Synchronizationbetween all the subtidal sequences available along the inner part ofRía de Vigo (Fig 1C): CORE-8 (ca 8 m of water depth), Vir-94 (ca 20m of water depth) and ZV-01 (ca 26 m of water depth), reveals thatseveral stages of relatively intense upwelling regimes affected theria during the past 1250 years, but only the two most intense LIAsub-stages (ca 1450e1750 AD and ca 1800e1930 AD) reached itsinnermost part, San Simón Bay (Fig. 13). We characterized them bydecreasing abundances of L. machaerophorum (percentages andconcentration) and lower D/P ratios. D/P ratio values are consis-tently lower in shallower waters from Ría de Vigo (Fig. 13), whichagrees with previous results obtained in other regions (e.g. Leroyet al., 2011, 2013b). This suggests that the D/P ratio may be pri-marily controlled by the proximaledistal relation; but also,partially, by the water-depth. Nevertheless, comparison betweensequences also shows that other regional environmental factorsmay be involved: e.g. the loss of the regional tree canopy (itsdestruction modified runoff and affected the sediment supply), theoccurrence of storms, the decreasing influence of the freshwaterplume towards the external part of the bay, or the eventualmodification of the coastal drainage and tidal inundation. Fourmain climatic episodes may be recognised during the last twomillennia, namely DA, MCA, MCA/LIA transition and LIA. Our cli-matic characterization reinforces other previous data from theGalician rias supporting the interpretation that a negative modeNAO domain dominated in Ría de Vigo during the MCA, but thatthis became weaker during the LIA and, probably, also during theearlier DA. Furthermore, we characterize a period (ca 1100e1300AD) when there was a stronger continental contribution to thesediment. This could be linked to the occurrence of increased stormintensities during the MCA/LIA transition perhaps promoted by andEA reinforcement (Fig. 13). Related to this, the intertidal/supratidalecosystems inside San Simón Bay may have extended further intothe past; at least three stages occurred during the historic period:end of the 5th century, 11th to 14th and 16th to 18th centuries.These may be connected to an apparent stabilisation or slow-downof the RSL which was mediated by a combination of more adverseclimate (DA, LIA), changes in the regional hydrology (upwellingintensification) and anthropogenic deforestation of the catchment.A number of local historical references are consistent with thepalaeoecological data obtained, and such agreement may serve tosupport the chronology proposed and many of the environmentalchanges envisaged. This good agreement will help in the inter-pretation of other analogous sequences extending back in time.

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Acknowledgements

This work was funded by the Spanish Ministry of Educationand Science under research projects Plan Nacional de I þ D þ I(2008e2011) CTM2009e13926-C02-01, CTM2009- 08158-E andCGL2012-33584 (co-financed with EFRD funds) and Xunta deGalicia 10MDS310020PR. N. Martínez-Carreño was funded by theFPI Ministerio de Ciencia e Innovación research program (BES-2010-037268) and I. García-Moreiras by the Xunta de Galicia PhDfellowship program (PRE/2013/404). Climatic data were obtainedfrom the World Data Centre-A for Palaeoclimatology, NationalGeophysical Data Centre, Boulder, Colorado. The authors thankuseful comments from anonymous referees.

Appendix A. Supplementary data

Supplementary data related to this article can be found at http://dx.doi.org/10.1016/j.quascirev.2014.03.021.

References

Abelleira Méndez, S., de Arce Andratschke, A., Saavedra Torreiro, C. (Coord), 2002.Compilación documental sobre la Batalla de Rande. Consorc. Zona Franca Vigo,Vigo, 533 pp.

Al-Nasrawi, H.G., Hughes, A.R., 2012. Fungal diversity associated with salt marshplants Spartina alterniflora and Juncus roemerianus in Florida. Jordan J. Biol. Sci.5, 247e254.

Alperin, M., Hoehler, T., 2010. The ongoing mystery of sea-floor methane. Science329, 288e289. http://dx.doi.org/10.1126/science.1189966.

Álvarez, M.C., Flores, J.A., Sierro, F.J., Diz, P., Francés, G., Pelejero, C., Grimalt, J.O.,2005. Millennial surface water dynamics in the Ría de Vigo during the last 3000years as revealed by coccoliths and molecular biomarkers. Palaeogeogr. Palae-oclimatol. Palaeoecol. 218, 1e13.

Alvarez, I., Gomez-Gesteira, M., deCastro, M., Lorenzo, M.N., Crespo, A.J.C., Dias, J.M.,2011. Comparative analysis of upwelling influence between the western andnorthern coast of the Iberian Peninsula. Cont. Shelf Res. 31, 388e399. http://dx.doi.org/10.1016/j.csr.2010.07.009.

Álvarez-Iglesias, P., Rubio, B., Pérez-Arlucea, M., 2006. Reliability of subtidal sedi-ments as “geochemical recorders” of pollution input: San Simón Bay (Ría deVigo, NW Spain). Estuar. Coast. Shelf Sci. 70, 507e521.

Álvarez-Iglesias, P., Quintana, B., Rubio, B., Pérez-Arlucea, M., 2007. Sedimentationrates and trace metal input history in intertidal sediments from San Simón Bay(Ría de Vigo, NW Spain) derived from 210Pb and 137Cs chronology. J. Environ.Radioact. 98, 229e250.

Alves, J.M.R., Miranda, P.M.A., 2013. Variability of Iberian upwelling implied by ERA-40 and ERA-Interim reanalyses. Tellus 65, 19245. http://dx.doi.org/10.3402/tellusa.v65i0.19245.

Antela Bernárdez, B., 2009. A pesca na Gallaecia Romana. Toxosoutos, Noia, 58 pp.Azcárate Luxan, I., 1996. Plagas agrícolas y forestales en España en los siglos XVIII y

XIX. Ministerio de Agricultura, Pesca Y Alimentación, Secretaría General Técn-ica, Madrid, 439 pp.

Baeteman, C., 1999. The Holocene depositional history of the IJzer palaeovalley(western Belgian coastal plain) with reference to the factors controlling theformation of intercalated peat beds. Geol. Belg. 2, 39e72.

Baeteman, C., Waller, M., Kiden, P., 2011. Reconstructing middle to late Holocenesea-level change: a methodological review with particular reference to ‘A newHolocene sea-level curve for the southern North Sea’ presented by K.-E. Behre.Boreas 40, 557e572. http://dx.doi.org/10.1111/j.1502-3885.2011.00207.

Baker, A.G., Bhagwat, S.A., Willis, K.J., 2013. Do dung fungal spores make a goodproxy for past distribution of large herbivores? Quat. Sci. Rev. 62, 21e31.

Bao, R., Alonso, A., Delgado, C., Pagés, J.L., 2007. Identification of the main drivingmechanisms in the evolution of a small coastal wetland (Traba, Galicia,NWSpain) since its origin 5700 cal yr BP. Palaeogeogr. Palaeoclim. Palaeoecol. 247,296e312.

Beaudouin, C., Suc, J.P., Escarguel, G., Arnaud, M., Charmasson, S., 2007. The sig-nificance of pollen signal in present-day marine terrigenous sediments: theexample of the Gulf of Lions (western Mediterranean Sea). Geobios 40, 159e172.

Blaauw, M., Heegaard, E., 2012. Estimation of age-depth relationships. In:Birks, H.J.B., Lotter, A.F., Juggins, S., Smol, J.P. (Eds.), Tracking EnvironmentalChange Using Lake Sediments, Data Handling and Numerical Techniques, vol. 5.Springer, Dordrecht, pp. 379e413.

Bolhuis, H., Stal, L.J., 2011. Analysis of bacterial and archaeal diversity in coastalmicrobial mats using massive parallel 16S rRNA gene tag sequencing. ISME J. 5,1701e17012. http://dx.doi.org/10.1038/ismej.2011.52.

Bouhier, A., 2001. Galicia. Ensaio Xeográfico de Análise e Interpretación dun VelloComplexo Agrario. Xunta de Galicia, Santiago de Compostela, 1407 pp.

Bungenstock, F., Schäfer, A., 2009. The Holocene relative sea-level curve for the tidalbasin of the barrier island Langeoog, German Bight, Southern North Sea. GlobalPlanet. Change 66, 34e51.

Carballeira Debasa, A.M., 2007. Galicia y los gallegos en las fuentes árabes medie-vales. Instituto de Estudios Gallegos Padre Sarmiento, Madrid, 251 pp.

Carrión, J.S., 2002. Patterns and processes of Late Quaternary environmental changein a montane region of southwestern Europe. Quat. Sci. Rev. 21, 2047e2066.

Cerralbo, P., Grifoll, M., Espino, M., López, J., 2013. Predictability of currents on amesotidal estuary (Ria de Vigo, NW Iberia). Ocean. Dyn. 63, 131e141. http://dx.doi.org/10.1007/s10236-012-0586-9.

Chmura, G.L., Stone, P.A., Ross, M.S., 2006. Non-pollen microfossils in Evergladessediments. Rev. Palaeobot. Palynol. 141, 103e119.

Colman, S.M., Baucom, P.C., Bratton, J.F., Cronin, T.M., McGeehin, J.P., Willard, D.A.,Zimmerman, A.R., Vogt, P.R., 2002. Radiocarbon dating, chronologic framework,and changes in accumulation rates of Holocene estuarine sediments fromChesapeake Bay. Quat. Res. 57, 58e70.

Costas, S., Muñoz Sobrino, C., Alejo, I., Pérez-Arlucea, M., 2009. Holocene evolutionof a rock-bounded barrier lagoon system, Cíes Islands, northwest Iberia. EarthSurf. Process. Landf. 34, 1575e1586.

Crespo, B.G., Figueiras, F.G., Porras, P., Teixeira, I.G., 2006. Downwelling and domi-nance of autochthonous dinoflagellates in the NW Iberian margin: the exampleof the Ría de Vigo. Harmful Algae 5, 770e781.

Danielsen, R., 2008. Palaeoecologial development of the Quiaios-Mira dunes,northern-central littoral Portugal. Rev. Palaeobot. Palynol. 152, 74e99.

deCastro, M., Gómez-Gesteira, M., Alvarez, I., Prego, R., 2004. Negative estuarinecirculation in the Ría of Pontevedra (NW Spain). Estuar. Coast. Shelf Sci. 60,301e312.

deMenocal, P.B., Ortiz, J., Guilderson, T., Sarnthein, M., 2000. Coherent high- andlow-latitude climate variability during the Holocene warm period. Science 288,2198e2202.

Desprat, S., Sánchez Goñi, M.F., Loutre, M.F., 2003. Revealing climatic variability ofthe last three millennia in northwestern Iberia using pollen influx data. EarthPlanet. Sci. Lett. 213, 63e78.

Dijkman, N.A., Boschker, H.T.S., Stal, L.J., Kromkamp, J.C., 2010. Composition andheterogeneity of the microbial community in a coastal microbial mat asrevealed by the analysis of pigments and phospholipid-derived fatty acids.J. Sea Res. 63 (1), 62e70. http://dx.doi.org/10.1016/j.seares.2009.10.002.

Diz, P., Francés, G., Pelejero, C., Grimalt, J.O., Vilas, F., 2002. The last 3000 years in theRía de Vigo (NW Iberian Margin): climatic and hydrographic signals. Holocene12, 459e468.

Doval, M.D., Nogueira, E., Pérez, F.F., 1998. Spatio-temporal variability of the ther-mohaline and biogeochemical properties and dissolved organic carbon in acoastal embayment affected by upwelling: the Ría de Vigo (NW Spain). J. Mar.Syst. 14 (1e2), 135e150.

European Environmental Agency (EEA), 2006. The Changing Faces of Europe’sCoastal Areas. EEA Report No 6/2006. Copenhagen, 107 pp.

Evans, G., Prego, R., Marshall, J.E., 2011. Organic matter in Ria sediments: relevanceof terrestial sources and temporal variations in rates of accumulation. Estuar.Coast. Shelf Sci. 94, 246e254.

Eynaud, F., Turon, J.L., Sanchez-Goñi, M.F., Gendreau, S., 2000. Dinoflagellate cystevidence of ‘Heinrich-like events’ off Portugal during the marine isotopic stage5. Mar. Micropaleontol. 40, 9e21.

Freire Camaniel, J., 1998. El Monacato Gallego en la Alta Edad Media. Fund. PedroBarrié la Maza, A Coruña, 1095 pp.

García-García, A., García-Gil, S., Vilas, F., 2003. Monitoring the Spanish gas fields inthe Ría de Vigo (1991e2001). Geo-Mar. Lett. 23, 200e206.

García-García, A., García-Gil, S., Vilas, F., 2005. Quaternary evolution of the Ría deVigo, Spain. Mar. Geol. 220, 153e179.

García-Gil, S., 2003. A natural laboratory for shallow gas: the Rías Baixas (NWSpain). Geo-Mar. Lett. 23, 215e229.

García-Gil, S., Vilas, F., Muñoz, A., Acosta, J., Uchupi, E., 1999. Quaternary sedi-mentation and thermal diapirism in the Ría de Pontevedra (Galician), North-west Spain. J. Coast. Res. 15, 1083e1090.

García-Gil, S., de Blas, E., Martínez-Carreño, N., Iglesias, J., Rial-Otero, R., Simal-Gándara, J., Judd, A.G., 2011. Characterisation and preliminary quantification ofthe methane reservoir in a coastal sedimentary source: San Simón Bay, Ría deVigo, NW Spain. Estuar. Coast. Shelf Sci. 91, 232e242.

García-Moreiras, I., 2013. Pollen Analysis of Modern and Fossil Samples Obtainedfrom Different Intertidal- subtidal Environments, in the Ría de Vigo (NW Iberia)(MSc thesis). Facultade de Bioloxía, Universidade de Vigo.

Gehrels, W.R., 1999. Middle and late Holocene sea-level changes in eastern Mainereconstructed from foraminiferal salt-marsh stratigraphy and AMS 14C dates ofbasal peat. Quat. Res. 52, 350e359.

Gómez-Orellana, L., Ramil-Rego, P., Aira Rodríguez, M.J., 1996. Cronología ydinámica de los humedales y lagunas existentes en las depresionessedimentarias de Galicia. In: Ruiz Zapata, B. (Ed.), Estudios Palinológicos1. Servicio de Publicaciones, Universidad de Alcalá, Alcalá Henares,pp. 63e67.

Gómez-Orellana, L., Ramil-Rego, P., Muñoz Sobrino, C., 2007. The Würm in NWIberia, a pollen record from Area Longa (Galicia). Quat. Res. 67, 438e452.

Gómez-Orellana, L., Ramil-Rego, P., Muñoz Sobrino, C., 2012. The response ofvegetation at the end of the last glacial period (MIS 3 and MIS 2) in littoral areasof NW Iberia. Boreas 42, 729e744. http://dx.doi.org/10.1111/j.1502-3885.2012.00310.x.

Page 22: Climate and anthropogenic factors influencing an estuarine ecosystem from NW Iberia: new high resolution multiproxy analyses from San Simón Bay (Ría de Vigo)

C. Muñoz Sobrino et al. / Quaternary Science Reviews 93 (2014) 11e3332

González-Paz, C.A., 2009. A medieval stronghold in the Portuguese way to saintjames of compostela: Castellum Sancti Pelagii de luto. Cuad. Estud. Gallegos 56,151e170.

Grimm, E., 1990e2011. TILIA and TILIA.GRAPH: PC spreadsheets and graphicssoftware for pollen data. INQUA Commission for the study of the HoloceneWorking Group Data Handling Methods. Newsletter 4, 5e7.

Holzwarth, U., Esper, O., Zonneveld, K.A.F., 2010. Organicwalled dinoflagellate cystsas indicators of oceanographic conditions and terrigenous input in the NWAfrican upwelling region. Rev. Palaeobot. Palynol. 159, 35e55.

Johnsen, S.J., Clausen, H.B., Dansgaard, W., Furher, K., Gusdestrup, N., Hammer, C.U.,Iversen, P., Jouzel, J., Stauffer, B., Steffensen, J.P., 1992. Irregular glacial in-terstadials recorded in a new Greenland ice core. Nature 359, 311e313.

Kemp, A.C., Horton, B.P., Donnelly, J.P., Mann, M.E., Vermeer, M., Rahmstor, S., 2011.Climate related sea-level variations over the past two millennia. Proc. Natl.Acad. Sci. U. S. A. 108, 11017e11022. http://dx.doi.org/10.1073/pnas.1015619108.

Kent, D.M. (Ed.), 2000. Applied Wetlands Science and Technology. CRC Press, BocaRaton, 472 pp.

Kessler, J.D., Reeburgh, W.S., Valentine, D.L., Kinnaman, F.S., Peltzer, E.T.,Brewer, P.G., Southon, J., Tyler, S.C., 2008. A survey of methane isotope abun-dance (14C, 13C, 2H) from five nearshore marine basins that reveals unusualradiocarbon levels in subsurface waters. J. Geophys. Res. 113, C12021. http://dx.doi.org/10.1029/2008JC004822.

Lavín, A., García, M.J., 1992. Mean sea level along the North Atlantic spanish coast,1980e1989. ICES Mar. Sci. Symp. 195, 187e192.

Lebreiro, S., Francés, G., Abrantes, F., Diz, P., Bartels-Jonsdottir, H., Stroynowski, Z.N.,Gil, I., Pena, L.D., Rodrigues, T., Jones, P.D., Nombela, M.A., Alejo, I., Briffa, K.R.,Harris, I., Grimalt, J.O., 2006. Climate change and coastal hydrographic responsealong the Atlantic Iberian margin (Tagus Prodelta and Muros Ría) during thelast two millennia. Holocene 16, 1003e1015.

Leroy, S.A.G., Marret, F., Gibert, E., Chalié, F., Reyss, J.-L., Arpe, K., 2007. River inflowand salinity changes in the Caspian Sea during the last 5500 years. Quat. Sci.Rev. 26, 3359e3383.

Leroy, S.A.G., Lahijani, H.A.K., Djamali, M., Naqinezhad, A., Moghadam, M.V.,Arpe, K., Shah-Hosseini, M., Hosseindoust, M., Miller, ChS., Tavakoli, V.,Habibi, P., Naderi, M., 2011. Late Little IceAge palaeoenvironmental records fromthe Anzali and Amirkola lagoons (south Caspian Sea): vegetation and sea levelchanges. Palaeogeogr. Palaeoclimatol. Palaeoecol. 302, 415e434.

Leroy, S.A.G., Lahijani, H.A.K., Reyss, J.-L., Chalié, F., Haghani, S., Shah-Hosseini, M.,Shahkarami, S., Tudryn, A., Arpe, K., Habibi, P., Nasrollahzadeh, H.S.,Makhlough, A., 2013a. A two-step expansion of the dinocyst Lingulodiniummachaerophorum in the Caspian Sea: the role of changing environment. Quat.Sci. Rev. 77, 31e45.

Leroy, S.A.G., Kakroodi, A.A., Kroonenberg, S., Lahijani, H.A.K., Alimohammadian, H.,Nigarov, A., 2013b. Holocene vegetation history and sea level changes in the SEcorner of the Caspian Sea: relevance to SWAsia climate. Quat. Sci. Rev. 70, 28e47.

Lewis, J., Hallett, R., 1997. Lingulodinium polyedrum (Gonyaulax polyedra) ablooming dinoflagellate. Oceanogr. Mar. Biol. Annu. Rev. 35, 96e161.

López Torre, R., 2009. De la reforestación de Pontevedra. El gran proyecto de Danielde la Sota hecho realidad, 1927e1958. Diputación de Pontevedra, 245 pp.

Lorenzo, M.N., Taboada, J.J., Gimeno, L., 2008. Links between circulation weathertypes and teleconnection patterns and their influence on precipitation patternsin Galicia (NW Spain). Int. J. Clim. 28, 1493e1505. http://dx.doi.org/10.1002/joc.1646.

Luis, J.R., García-Gil, S., Sanjúan, A., de Carlos, A., 2012. Microbial communities in thesediments of the Ría de Vigo, Spain. In: Abstracts of the 11th InternationalConference on Gas in Marine Sediments, 4e7 September 2012, Nice, France,pp. 130e131.

Margalef, R., Andreu, B., 1958. Componente vertical de los movimientos del agua enla ría de Vigo y su posible relación con la entrada de sardina. Investig. Pesq. 11,105e126.

Marret, F., Zonneveld, K.A.F., 2003. Atlas of modern organic walled dinoflagellatecyst distribution. Rev. Palaeobot. Palynol. 125, 1e200.

Martínez Crespo, J., 2000. Redondela y Vigo frente a la luctuosa y el diezmo ecle-siástico: la sentencia arbitral de 1494. Cuad. Estud. Gallegos 47, 76e137.

Martínez Crespo, J., 2007. Ordenanzas municipales de las Villas de Redondela yVilavella del año 1605. Gallaecia 26, 365e384.

Martínez-Carreño, N., García-Gil, S., 2013. The Holocene gas system of the Ría deVigo (NW Spain): factors controlling the location of gas accumulations, seepsand pockmarks. Mar. Geol. 344, 82e100.

McCarthy, F.M.G., Mudie, P.J., 1998. Oceanic pollen transport and pollen:dinocystratios as markers of late Cenozoic sea level change and sediment transport.Palaeogeogr. Palaeoclimatol. Palaeoecol. 138 (1e4), 187e206. http://dx.doi.org/10.1016/S0031-0182(97)00135-1.

Megens, L., van der Plicht, J., de Leeuw, J.W., Smedes, F., 2002. Stable carbon andradiocarbon isotope compositions of particle size fractions to determine originsof sedimentary organic matter in an estuary. Org. Geochem. 33, 945e952.

Méndez Martínez, G., Pérez-Arlucea, M., González-Villanueva, R., OvejeroCampos, A., 2011. Anthropogenic influence on the Holocene sedimentationprocess along the Atlantic coast of Galicia (NW Iberian Peninsula). J. Coast. Res.64, 1788e1792.

Miranda, P.M.A., Alves, J.M.R., Serra, N., 2013. Climate change and upwelling:response of Iberian upwelling to atmospheric forcing in a regional climatescenario. Clim. Dyn. 40, 2813e2824.

Montero Vilar, P., 1999. Estudio de la hidrodinámica de la Ría de Vigo mediante unmodelo de volúmenes finitos (PhD. thesis). Universidad de Santiago, 178 pp.

Moore, P.D., Webb, J.A., Collinson, M.E., 1991. Pollen Analysis. Blackwell, London,216 pp.

Moreno, A., Pérez, A., Frigola, J., Nieto-Moreno, V., Rodrigo-Gámiz, M., Martrat, B.,González-Sampériz, P., Morellón, M., Martín-Puertas, C., Corella, J.P.,Belmonte, A., Sancho, C., Cacho, I., Herrera, G., Canals, M., Grimalt, J.O., Jiménez-Espejo, F., Martínez-Ruiz, F., Vegas-Vilarrúbia, T., Valero-Garcés, B.L., 2012. TheMedieval Climate Anomaly in the Iberian Peninsula reconstructed from marineand lake records. Quat. Sci. Rev. 43, 16e32.

Muñoz Sobrino, C., Ramil-Rego, P., Gómez-Orellana, L., Díaz Varela, R.A., 2005.Palynological data on major Holocene climatic events in NW Iberia. Boreas 34,381e400.

Muñoz Sobrino, C., García-Gil, S., Diez, J.B., Iglesias, J., 2007. Palynological charac-terization of gassy sediments in the inner part of Ría de Vigo (NW Spain). Newchronological and environmental data. Geo-Mar. Lett. 27, 289e302.

Muñoz Sobrino, C., Ramil-Rego, P., Gómez-Orellana, L., Ferreiro da Costa, J., DíazVarela, R.A., 2009. Climatic and human effects on the post-glacial dynamics ofFagus sylvatica L. in NW Iberia. Plant Ecol. 203, 317e340.

Muñoz Sobrino, C., García-Gil, S., Iglesias, J., Martínez Carreño, N., Ferreiro daCosta, J., Díaz Varela, R.A., Judd, A., 2012. Environmental change in the Ría deVigo, NW Iberia, since the mid-Holocene: new palaeoecological and seismicevidence. Boreas 41, 578e601.

Muñoz Sobrino, C., Heiri, O., Hazekamp, M., van der Velden, D., Kirilova, E.P., García-Moreiras, I., Lotter, A.F., 2013. New data on the Lateglacial period of SW Europe:a high resolution multiproxy record from Laguna de la Roya (NW Iberia). Quat.Sci. Rev. 80, 58e77.

Munsell Soil Colour Charts. Munsell colour, Macbeth Division of Kollmorgen Cor-poration, 1998. Maryland, USA.

Otero, P., Ruiz-Villarreal, M., Peliz, A., 2008. Variability of river plumes off NorthwestIberia in response to wind events. J. Mar. Syst. 72, 238e255.

Paterson, D.M., Hanley, N.D., Black, K., Defew, E.C., Solan, M. (Eds.), 2011. Biodiver-sity, Ecosystems and Coastal Zone Management: Linking Science and Policy.Mar. Ecol. Prog. Ser. vol. 434, 201e301. http://dx.doi.org/10.3354/meps09279.

Pearson, A., Seewald, J.S., Eglinton, T.I., 2005. Bacterial incorporation of relict carbonin the hydrothermal environment of Guaymas Basin. Geochim. Cosmochim.Acta 69, 5477e5486.

Peña Santos, A., Sánchez Bargiela, R., González Fernández, J.M., RodríguezTeijeiro, J.D., 1999. Historia de Vigo. Via Láctea, A Coruña, 347 pp.

Pérez-Arlucea, M., Méndez, G., Clemente, F., Nombela, M.A., Rubio, B., Filguiera, M.,2005. Hydrology, sediment yield, erosion and sedimentation rates in theestuarine environment of Ría de Vigo, Galicia, Spain. J. Mar. Syst. 54, 206e226.

Pérez-Arlucea, M., Álvarez-Iglesias, P., Rubio, B., 2007. Holocene evolution of estu-arine and tidal-flat sediments in San Simón Bay, Galicia, NW Spain. J. Coast. Res.50, 163e167.

Perillo, G.M.E., Wolanski, E., Cahoon, D.R., Brinson, M.M. (Eds.), 2009. CoastalWetlands: An Integrated Ecosystem Approach. Elsevier, Amsterdam, 941 pp.

Ramil Rego, P., Rodríguez Guitián, M.A., Ferreiro Da Costa, J., Rubinos Román, M.,Gómez-Orellana, L., de Nóvoa Fernández, B., Hinojo Sánchez, B.A., MartínezSánchez, S., Cillero Castro, C., Díaz Varela, R.A., Rodríguez González, P.M., MuñozSobrino, C., 2008. Os Hábitats de Interese Comunitario en Galicia. FichasDescritivas. In: Monografías do IbaderUniversidade de Santiago de Compostela,Lugo, 627 pp.

Ramil-Rego, P., Muñoz Sobrino, C., Gómez-Orellana, L., Rodríguez Guitián, M.A.,Ferreiro da Costa, J., 2012. Configuración y transformación del paisaje del NWibérico durante el final de los tiempos glaciares, el Holoceno y el Antropoceno.Recur. Rurais 6, 19e62.

Rasmussen, S.O., Andersen, K.K., Svensson, A.M., Steffensen, J.P., Vinther, B.M.,Clausen, H.B., Siggaard-Andersen, M.L., Johnsen, S.J., Larsen, L.B., Dahl-Jensen, D., Bigler, M., Röthlisberger, R., Fischer, H., Goto-Azuma, K.,Hansson, M.E., Ruth, U., 2006. A new Greenland ice core chronology for the lastglacial termination. J. Geophys. Res. 111, D06102. http://dx.doi.org/10.1029/2005JD006079.

Reed, D.J., 2000. Sea-level rise and coastal marsh sustainability: geological andecological factors in the Mississippi delta plain. Geomorphology 48, 233e243.

Reimer, P.J., Bard, E., Bayliss, A., Beck, J.W., Blackwell, P.G., Bronk Ramsey, C.,Buck, C.E., Cheng, H., Edwards, R.L., Friedrich, M., Grootes, P.M., Guilderson, T.P.,Haflidason, H., Hajdas, I., Hatté, C., Heaton, T.J., Hogg, A.G., Hughen, K.A.,Kaiser, K.F., Kromer, B., Manning, S.W., Niu, M., Reimer, R.W., Richards, D.A.,Scott, E.M., Southon, J.R., Turney, C.S.M., van der Plicht, J., 2013. IntCal13 andMARINE13 radiocarbon age calibration curves 0e50000 years cal BP. Radio-carbon 55. http://dx.doi.org/10.2458/azu_js_rc.55.16947.

Roucoux, K.R., Shackleton, N.J., de Abreu, L., Schönfeld, J., Tzedakis, P.C., 2001.Combined marine proxy and pollen analyses reveal rapid Iberian vegetationresponse to North Atlantic millennial-scale climate oscillations. Quat. Res. 56,128e132.

Severin, I., Stal, L.J., 2010. Diazotrophic microbial mats. In: Seckbach, J., Oren, A.(Eds.), Microbial Mats. Springer, The Netherlands, pp. 321e339.

Shabman, L.A., Batie, S.S., 1987. Mitigating damages from coastal wetlands devel-opment: policy, economics and financing. Mar. Resour. Econ. 4, 227e248.

Shennan, I., Horton, B., 2002. Holocene land- and sea-level changes in Great Britain.J. Quat. Sci. 17 (5e6), 511e526.

Silva, J.P., Phillips, L., Jones, W., Eldridge, J., O’Hara, E., 2007. LIFE and Europe’swetlands. Restoring a Vital Ecosystem. Office for Official Publications of theEuropean Communities, Brussels, 68 pp.

Smith, D.E., Harrison, S., Firth, C.R., Jordan, J.T., 2011. The early Holocene sea-levelrise. Quat. Sci. Rev. 30, 1846e1860.

Page 23: Climate and anthropogenic factors influencing an estuarine ecosystem from NW Iberia: new high resolution multiproxy analyses from San Simón Bay (Ría de Vigo)

C. Muñoz Sobrino et al. / Quaternary Science Reviews 93 (2014) 11e33 33

Solomon, S., Mudie, P.J., Cranston, R., Hamilton, T., Thibaudeau, S.A., Collins, E.S.,2000. Characterization of marine and lacustrine sediments in a drownedthermokarst embayment, Richards Island, Beaufort Sea, Canada. Int. J. Earth Sci.89, 503e521.

Souto, C., Gilcoto, M., Farina-Busto, L., Pérez, F.F., 2003. Modelling the residual cir-culation of a coastal embayment affected by wind driven upwelling: circulationof the Ría de Vigo (NW Spain). J. Geophys. Res. e Oceans 108 (C11), 3340. http://dx.doi.org/10.1029/2002JC001512.

Sprangers, M., Dammers, N., Brinkhuis, H., van Weering, T.C.E., Lotter, A.F., 2004.Modern organic-walled dinoflagellate cyst distribution offshoreNWIberia;tracing the upwelling system. Rev. Palaeobot. Palynol. 128, 97e106.

Stal, L.J., Severin, I., Bolhuis, H., 2010. The ecology of nitrogen fixation in cyano-bacterial mats. Adv. Exp. Med. Biol. 675, 31e45.

Stancliffe, R.P.W., 2002. Microforaminiferal linings. In: Jansonius, J., McGregor, D.C.(Eds.), Palynology: Principles and Applications 1. American Association ofStratigraphical Palynologists Foundation, Dallas, TX, pp. 373e379.

Stuiver, M., Reimer, P.J., Reimer, R.W., 1986e2013. CALIB 7.0. Available at: http://www.calib.qub.ac.uk/calib/.

Tilstone, G.H., Figueiras, F.G., Fraga, F., 1994. Upwellinge downwelling sequences inthe generation of red tides in a coastal upwelling system. Mar. Ecol.-Progr. Ser.112, 241e253.

Trouet, V., Esper, J., Graham, N.E., Baker, A., Scourse, J.D., Frank, D.C., 2009. Persistentpositive North Atlantic oscillation mode dominated the medieval climateanomaly. Science 324, 5923. http://dx.doi.org/10.1126/science.1166349.

Trouet, V., Scourse, J.D., Raible, C.C., 2012. North Atlantic storminess and AtlanticMeridional Overturning Circulation during the last Millennium: reconcilingcontradictory proxy records of NAO variability. Global Planet. Change 84e85,48e55.

Valdés Hansen, F., 2004. El problema pesquero con los delfines y su persecución engalicia(siglos XIII al XX). Cuad. Estud. Gallegos 117, 313e362.

van der Knaap, W.O., van Leeuwen, J.F.N., 1997. Late Glacial and Early Holocenevegetation succession altitudinal vegetation zonation, and climatic change inthe Serra da Estrela, Portugal. Rev. Palaeobot. Palynol. 97, 239e285.

van Geel, B., 2003. Non pollen palynomorphs. In: Smol, J.P., Birks, H.J.B.,Last, W.M. (Eds.), Tracking Environmental Change Using Lake Sediments 3,Terrestrial, Algal and Siliceous Indicators. Kluwer Academic, Dordrecht,pp. 99e120.

van Geel, B., Coope, G.R., van der Hammen, T., 1989. Palaeoecology and stratigraphyof the Lateglacial type section at Usselo (The Netherlands). Rev. Paleobot.Palynol. 60, 25e129.

van Mourik, J.M., 1986. Pollen profiles of slope deposits in the Galician area (N.W.Spain). Nederl. Geogr. Stud. 12, 1e171.

van Ryckegem, G., Verbeken, A., 2005. Fungal ecology and succession on Phragmitesaustralis in a brackish tidal marsh. I. Leaf sheaths. Fungal Divers. 19, 157e187.

Vázquez Marinelly, C., Moreira Pumar, J., Rodal González, M., 2007. Historia deCangas. Deputación de Pontevedra, 645 pp.

Vila, S., 2010. A casa de Soutomaior (1147e1532). Ed. Toxosoutos, Noia. 662 pp.Vilas, F., Nombela, M.A., García-Gil, E., García-Gil, S., Alejo, I., Rubio, B., Pazos, O.,

1995. Cartografia de Sedimentos Submarinos. Ría Vigo 1:50.000. Xunta deGalicia, Conselleria de Pesca, Marisqueo e Acuicultura, Vigo.

Villacieros-Robineau, N., Herrera, J.L., Castro, C.G., Piedracoba, S., Roson, G., 2013.Hydrodynamic characterization of the bottom boundary layer in a coastal up-welling system (Ría de Vigo, NW Spain). Cont. Shelf Res. 68, 67e79.

Vink, A., Steffen, H., Reinhardt, L., Kaufmann, G., 2007. Holocene relative sea-levelchange, isostatic subsidence and the radial viscosity structure of the mantleof northwest Europe (Belgium, the Netherlands, Germany, southern North Sea).Quat. Sci. Rev. 26, 3249e3275.

Vinther, B.M., Clausen, H.B., Johnsen, S.J., Rasmussen, S.O., Andersen, K.K.,Buchardt, S.L., Dahl-Jensen, D., Seierstad, I.K., Siggaard-Andersen, M.L.,Steffensen, J.P., Svensson, A.M., Olsen, J., Heinemeier, J., 2006. A synchronizeddating of three Greenland ice cores throughout the Holocene. J. Geophys. Res.111, D13102. http://dx.doi.org/10.1029/2005JD00 6921.

Watson, E.B., Byrne, R., 2009. Abundance and diversity of tidal marsh plants alongthe salinity gradient of the San Francisco Estuary: implications for globalchange ecology. Plant Ecol. 205, 113e128.

Zonneveld, K.A.F., Marret, F., Versteegh, G.J.M., Bogus, K., Bonnet, S.,Bouimetarhan, I., Crouch, E., de Vernal, A., Elshanawany, R., Edwards, L.,Esper, O., Forke, S., Grøsfjeld, K., Henry, M., Holzwarth, U., Kielt, J.-F., Kim, S.-Y.,Ladouceur, S., Ledu, D., Liang, C., Limoges, A., Londeix, L., Lu, S.-H.,Mahmoud, M.S., Marino, G., Matsuoka, K., Matthiessen, J., Mildenhal, D.C.,Mudie, P., Neil, L.H., Pospelova, V., Qi, Y., Radi, T., Richerol, T., Rochon, A.,Sangiorgi, F., Solignac, S., Turon, J.-L., Verleye, T., Wang, Y., Wang, Z., Young, M.,2013. Atlas of modern dinoflagellate cyst distribution based on 2405 datapoints.Rev. Palaeobot. Palynol. 191, 1e197.