Foraminiferal biotopes and their distribution control in Ria de Aveiro (Portugal): a multiproxy approach

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Foraminiferal biotopes and their distribution control in Ria de Aveiro (Portugal): a multiproxy approach Maria Virgínia Alves Martins, Fabrizio Frontalini, Lazaro L. M. Laut, Frederico S. Silva, João Moreno, Silvia Sousa, et al. Environmental Monitoring and Assessment An International Journal Devoted to Progress in the Use of Monitoring Data in Assessing Environmental Risks to Man and the Environment ISSN 0167-6369 Environ Monit Assess DOI 10.1007/s10661-014-4052-7

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Author's personal copy Environ Monit Assess DOI 10.1007/s10661-014-4052-7

Foraminiferal biotopes and their distribution control in Ria de Aveiro (Portugal): a multiproxy approach Maria Virgínia Alves Martins & Fabrizio Frontalini & Lazaro L. M. Laut & Frederico S. Silva & João Moreno & Silvia Sousa & Noureddine Zaaboub & Monia El Bour & Fernando Rocha

Received: 30 October 2013 / Accepted: 11 September 2014 # Springer International Publishing Switzerland 2014

Abstract Ria de Aveiro, which is located in the centre of Portugal (40° 38′ N, 8° 45′ W), is a well-mixed and complex coastal lagoon that is separated from the sea by a sandy barrier and connects with the Atlantic through an artificial inlet. Tidal currents are the main factor controlling the lagoon’s hydrodynamics and, to a great extent, the sedimentary dynamic. The inner lagoonal zones receive input from several rivers and experience

the pressure caused by the accumulation of organic matter and pollutants (namely, trace metals) from diverse anthropic activities. This paper is the first piece of work aiming to recognize, characterize and explain the main benthic foraminiferal biotopes in Ria de Aveiro. To provide a broad overview of this kind of setting, our results are compared to those of previous published studies conducted in similar transitional

Electronic supplementary material The online version of this article (doi:10.1007/s10661-014-4052-7) contains supplementary material, which is available to authorized users. M. A. Martins (*) Faculdade de Geologia, Departamento de Estratigrafia e Paleontologia, Universidade do Estado do Rio de Janeiro, Av. São Francisco Xavier, 524, sala 4037 F, Maracanã, 20550-013 Rio de Janeiro, RJ, Brasil e-mail: [email protected] M. A. Martins : F. Rocha GeoBioTec, Dpto. Geociências, Universidade de Aveiro, Campus de Santiago, 3810-193 Aveiro, Portugal

F. S. Silva Laboratório de Palinofácies & Fácies Orgânicas – LAFO, Universidade Federal do Rio de Janeiro – UFRJ, Rio de Janeiro, Brasil

J. Moreno Faculdade de Ciências, Centro e Departamento de Geologia, Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal

M. A. Martins CESAM, Dpto. Geociências, Universidade de Aveiro, Aveiro, Portugal F. Frontalini DiSTeVA, Facoltà di Scienze e Tecnologie, Università degli Studi di Urbino “Carlo Bo”, Urbino, Italy L. L. M. Laut Laboratório de Micropaleontologia – LabMicro, Universidade Federal do Estado do Rio de Janeiro – UNIRIO, Rio de Janeiro, Brasil

S. Sousa Instituo Oceanográfico, Universidade de São Paulo, São Paulo, Brasil

N. Zaaboub : M. El Bour Institut des Sciences et Technologies de la Mer, Salammbô, Tunis, Tunisie

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environments. The research is based on an investigation of 225 sites spread throughout this ecosystem. Utilizing a statistical approach, this study analyses the details of dead benthic foraminiferal assemblages composed of 260 taxa, the texture and composition (mineralogical and geochemical) of the sediment and physicochemical data. On the basis of the results of R-mode and Q-mode cluster analyses, several different biotopes can be defined as marsh biotope/near-marsh biotope; marginal urban/marginal urban mixing biotope; inner-outer lagoon biotope or enclosed lagoon; outer lagoon biotope, mixed sub-biotope; and outer lagoon, marine sub-biotope. These biotopes are related to foraminifera assemblages and substrate type and are influenced by local currents, water depth, chemical and physicochemical conditions, river or oceanic proximity, and anthropogenic impact, as evidenced by the mapping of the six factor loadings of the principal component analysis conducted herein. Based on a similar methodology of analysis as that applied in previous studies in the Lagoon of Venice, comparable biotypes were identified in Lagoon of Aveiro. Keywords Benthic foraminifera . Sediments . Texture . Mineralogy . Geochemistry . Pollution . Statistical analysis . Coastal lagoon

Introduction Coastal zones are commonly fragile ecosystems (Miller and Auyong 1991; Mee 2012) that are being, and will be, exposed to increasing risks, including coastal erosion, over the coming decades due to climate change and sea level rises (Nicholls et al. 2007). The probability of catastrophic inundations of maritime origin due to the present tendency for rises in sea level and climatic change associated with exponential urban growth near the littoral (Oliver-Smith 2009; Komar 2011; Ramieri et al. 2011); the consequent intensification of domestic, economic and industrial activities (Ducrotoy et al. 2000; Clark 2001; Dolbeth et al. 2007); and the input of sewage into the environment, causing pollution (e.g. Beltrame et al. 2009; Covelli et al. 2011; Giuliani et al. 2011; Green-Ruiz and Páez-Osuna 2011), is contributing to the vulnerability of these ecosystems and having a negative impact on living organisms (Micheletti et al. 2007; Ponti et al. 2009; Ameur et al. 2012; Cravo et al. 2012; Nilin et al. 2012; León et al. 2013).

Moreover, human activities such as dredging and the construction of ports, marinas and coastal defences (Allersma et al. 1993; Anthony 2008) in river catchment areas (dams), estuaries and along coasts generate changes in hydrodynamic conditions (Gong et al. 2008; Moreno et al. 2010; Duck and Figueiredo da Silva 2012) and are causing rapid changes in these ecosystems (Pérez-Ruzafa et al. 2007). These dynamic coastal ecosystems often have complex, non-linear morphological responses to change (Dronkers 2005). Significant time lags frequently involve the evolution of the erosion, transportation and deposition of sediment in these environments due to local or regional development patterns (Brunsden 2001). Climate change in estuaries may also result in alterations to physical mixing characteristics caused by variations in the freshwater runoff (Scavia et al. 2002), with consequences for water quality. Freshwater inflows into the estuaries influence water residence time, nutrient delivery, vertical stratification, and phytoplankton growth rates (Nicholls et al. 2007). Meanwhile, increased water temperature could also affect algal production and lead to changes in the availability of light, oxygen and carbon, thus affecting living beings (Short and Neckles 1999). In order to assess the evolution of transitional coastal ecosystems, many studies have been performed utilizing different methodologies (e.g. Harris et al. 2001; De Pippo et al. 2004; Madricardo et al. 2007; Le Roy et al. 2008; Fornari et al. 2010; Duck and Figueiredo da Silva 2012; Fortunato et al. 2013; Maccotta et al. 2013), including the use of biological organisms like benthic foraminifera as indicators of environmental and paleoenvironmental changes (e.g. Serandrei Barbero et al. 1997; Armynot du Châtelet et al. 2005; Serandrei-Barbero et al. 2006; Nichol et al. 2007; Boski et al. 2008; Bony et al. 2011; Caruso et al. 2011; Koukousioura et al. 2012; Cosentino et al. 2013). Benthic foraminifera are increasingly being used in these kinds of study and, for several key reasons, are one of the most commonly used bioindicators in research into environmental quality and paleoenvironmental evolution (Schönfeld et al. 2012). The distribution of foraminiferal species is often related to abiotic factors, such as the natural boundaries of water masses, runoff influence, current activity, substrate type, elevation relative to sediment surface, nutrient flux, temperature, salinity, anthropogenic contamination, and biogeochemical processes, as well as biotic factors such as nutrients, competition and predation (e.g. Schafer and Cole 1974;

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Murray 1991, 2006; Yassini and Jones 1995; Hayward et al. 1997a; Hayward et al. 1999; Horton and Murray 2007). After their death, tests of these organisms are preserved in the sediment and can also ultimately fossilize. Moreover, due to their abundance, ecological behaviour and the possibility of the preservation of their tests in the sedimentary record, foraminifera are a useful tool when it comes to reconstructing recent and ancient marine environmental conditions (Murray 2000). In this context, this paper reports, for the first time, results based on a multiproxy approach and statistical analysis that aims to identify biotopes and their spatial distribution within the Lagoon of Aveiro. The research also aims to delineate the ecological and environmental factors that contribute to biotope distributions by comparing previous, similar studies, such as those concerning the Lagoon of Venice, where similar methodologies of analysis were applied (e.g. Serandrei Barbero et al. 1989; 1999; Albani et al. 1991, 1998, 2007, 2010). The opportunity to identify various biotopes in very complex environments like that of Ria de Aveiro allows us to evaluate its current environmental and ecological conditions and to define the baseline reference conditions for ecological studies. It also provides a unique opportunity to improve our understanding of transitional marine environments by using benthic foraminifera to develop an environmental management plan in this valuable, but poorly known, area; and establish proxies with which will be possible to study the evolution of the lagoon since the time it was formed in the X century (Dias et al. 2012).

Study area Ria de Aveiro is a well-mixed water coastal lagoon totalling an area of 83 km2 in high tide conditions and 66 km2 in low tide conditions, with a maximum length and width of 45 and 10 km, respectively (Dias et al. 2000). The lagoon is formed by four main channels (Mira, São Jacinto, Ílhavo and Espinheiro), which are intercepted by a complex system of channels and islands with extensive mudflats, salt marshes and old salt pans that give it an irregular geometry (Dias et al. 1999) (Fig. 1). The depth of the lagoon drops from being about 30 m at the lagoon inlet that is used for navigation to less than 3 m in the other channels (average depth of about 1 m).

The marine influence is relatively strong near the mouth of the lagoon and lessens towards the inner areas where the contributions of several rivers and riverine waters, namely, the Vouga and Antuã rivers (Moreira et al. 1993), are higher. The river flow depends on rainfall that is usually higher in winter than in summer. The contributions of rivers affect the circulation of the lagoon after periods of heavy rainfall (Dias et al. 2003), also causing plumes of low salinity in the sea in front of the lagoon (Peliz et al. 2002). Longitudinal salinity gradients occur from the mouth to the inner areas depending on the balance between the fresh and salty marine water inputs (Vaz et al. 2005). Normally, these gradient patterns vary, with tidal cycles and rainfall intensity affecting some organisms, such as molluscs (Génio et al. 2008). Water circulation in the lagoon is partly influenced by the wind and river runoff but is almost completely dependent on tidal energy that is predominantly semidiurnal with a mesotidal regime (Dias et al. 2000; Vaz and Dias 2008). Tides penetrate into the lagoon through the inlet and propagate along the channels, becoming delayed in the extremities of the Mira and Ovar channels, where the delay can be about 5 h (Vicente 1985; Araújo et al. 2008). The amplitude varies near the mouth of the lagoon by approximately 0.6 m in the neap tides and 3.2 m in the spring tides (average 2 m; Dias et al. 1999). The velocities of the tidal currents are very strong near the mouth and can reach speeds of about 2 m s−1, but these are much less active in the innermost part of the lagoon and the mudflats (Dias et al. 2000). The Vouga and Antuã rivers contribute with large amounts of sediment, introducing into the lagoon mostly silt and clay particles as coarse grained sediments are deposited in or near their mouths. Mud corresponds to the size of the sediment on the mudflats, marshes and harbours (Dias et al. 2001). In dry periods, erosion by tides is the dominant process that determines the transport of suspended sediment in the lagoon. The highest values of sediment concentration are found in the northern channels, due to erosion induced by a high current velocity in the shallow areas (Lopes et al. 2006). The Lagoon of Aveiro has high bioproductivity, supporting abundant populations of microalgae and bacteria (Cunha et al. 1999; Lopes et al. 2007), invertebrate fauna (Rodrigues et al. 2011), and fish populations (França et al. 2012) that are used by local people for their supply. Foraminifera are also an important

Author's personal copy Environ Monit Assess Fig. 1 a Location of the study area at Iberian Peninsula; b Lagoon of Aveiro map showing the main river basins and also salt marshes surrounding the lagoon and lowland areas marked in light grey (areas of higher altitude are marked in dark grey scale); c Lagoon of Aveiro map indicating the sampling stations (points), the main channels, cities and harbour areas

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b

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component of the benthic fauna in this lagoon (Martins et al. 2010, 2011a). Surrounding the Ria de Aveiro are 11 cities and a population greater than 300,000 people who are involved in a number of commercial activities, such as chemical plants, mussel and fish farming, and large boat and recreational traffic, all of which contribute domestic, agricultural and industrial waste (Barrosa 1985) and affect this coastal ecosystem. The lagoon has been the final recipient of all kinds of pollution discharge, as there were no infrastructures/wastewater treatments in place to protect it. The recent construction (1999) of the SIMRIA, a system for the collection, treatment and disposal of domestic and industrial effluent, has promoted the environmental rehabilitation of this ecosystem. However, in several places, the surface sediments are still polluted (Martins et al. 2013a). As a consequence, several studies have been performed on the accumulation of metals in some parts of Ria de Aveiro (e.g. Pereira et al. 1998a, b, 2009; Nunes et al. 2007; Reis et al. 2009; Pastorinho et al. 2012), and the negative effects thereof on several kinds of living beings (e.g. Pereira et al. 2005, 2006; Fonseca et al. 2011; Cardoso et al. 2013), in particular benthic foraminifera (Martins et al. 2010, 2011a).

Material and methods Sampling and data acquisition A total of 225 sites were sampled (2006/2007) in the sub-tidal, intertidal, mudflat zones, near marshes and salt pan areas of the Ria de Aveiro channels and margins, at water depths varying between 0 and ∼28 m (Fig. 1; Appendix A.1). Some samples were collected at the centre of the channels, mostly near the lagoon mouth. However, as these zones are subjected to very strong hydrodynamism and have low substrate stability (Plecha et al. 2012) avoiding the development of benthic foraminifera assemblages and the retention that registry (due to erosion as shown by Martins et al. 2011b), thus in most other places, the least hydrodynamic side of the channels was chosen for the sampling. A bathymetric map of the Ria de Aveiro is provided by Lopes et al. (2005). As observed by these authors, the Ria de Aveiro is a very shallow lagoon (average depth of 1 m). Our deepest stations are confined to the inlet channel and to small areas close to the lagoon mouth (12–28 m). The

stations located in the inner parts of the lagoon rarely are deeper than 3 m. Sediment samples were collected using an adapted Petit Ponnar sampler (with two openings). The uppermost part (∼2 cm) of the sediment was collected for geochemical, mineralogical and grain size analyses in each station and was cool preserved once on board. The thickness of 2 cm of sediment should correspond to about 1 year of sedimentation (as can be estimated by the chronology presented in Martins et al. (2013c) and other not published data). Thus, the studied assemblages of foraminifera which are also compared with sedimentological data may correspond to a memory of up to 1 year. Physicochemical parameters such as temperature, salinity/conductivity, pH and Eh were measured at each site in both the water and the sediment. The sediments for the benthic foraminifera analysis were preserved and stained with Rose Bengal and dissolved in alcohol (2 g l−1) to distinguish the biocoenosis from the thanatocoenosis. Homogenized portions of about 150–250 g of the dried sediment samples collected in each site were used for textural analysis. The fine fraction was separated from the sand fraction by wet sieving using a 63-μm screen. The sediment fraction coarser than 63 μm was dry sieved through a series of sieves (125, 250, 500, 1,000 μm). The sediment mean grain size (SMGS) and sorting were determined using the Folk and Ward method (Folk and Ward 1957). The mineralogical composition of the sediment was analysed by X-ray diffraction (XRD) techniques in the sediment fractions
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