**2. Case study: Aveiro Lagoon (Portugal)**

The Aveiro Lagoon is located on the Western Atlantic coast of Portugal (40°38′N, 8°45′W, **Figure 1**). It is 45 km long and 10 km wide and covers an area between 66 and 83 km2 at low and high spring tides, respectively [25]. It is composed by a series of channels among intertidal areas such as mudflats, salt marsh, and old saltpans. It is connected to the ocean through a single artificial inlet (∼350 m wide and 2 km long) fixed by two jetties (**Figure 1**). Four main channels radiate of the lagoon mouth: Mira, S. Jacinto/Ovar, Ílhavo, and Espinheiro channels (**Figure 1**), with lengths of 20, 29, 15, and 17 km, respectively. The inner lagoonal area receives the contribution of several rivers. The freshwater is supplied mainly by Vouga and Antuã rivers with average flows over 50 and 5 m3 s<sup>−</sup><sup>1</sup> , respectively [26] and in less way by small rivers such as Boco river, which flows into the south Ílhavo channel, and the Caster river, which flows into the north of Ovar channel, with an

#### **Figure 1.**

*(a) Aveiro Lagoon location; (b) samples location in Aveiro Lagoon; (c) a detail of the lagoon mouth (adapted from Google Earth).* 

average flow less than 1 m3 s<sup>−</sup><sup>1</sup> [25]. According to Dias et al. [27], each of the main channels may be considered as presenting features of separate estuaries, owing to typical estuarine longitudinal gradients of water salinity and temperature, with values close to the characteristics of the oceanic water near the inlet and close to freshwater furthest upstream.

 The average depth of the lagoon is approximately 1 m relative to the local chart datum (2.0 m below mean sea level) [27] although there are deeper areas close to the lagoon mouth, where depths may reach values of ≈30 m. Nevertheless, the bathymetry in this zone has changed over time due to both natural and anthropogenic causes [28].

The Ria de Aveiro is a tide-dominated lagoon with minimum tidal range of 0.6 m (neap tides) and maximum tidal range of 3.2 m (spring tides). Near the lagoon entrance, tidal current velocities are strong [29], but they weaken in more internal lagoon areas. Furthermore, the noticeable wind effect can have an important influence on the lagoon circulation. Particular circulation patterns mainly in shallow areas and wide channels can be induced by strong winds [25].

Regarding the environmental quality of the lagoon, in internal areas near the river mouth, there are high concentrations of metals and organic matter [18]. The Laranjo Bay area (**Figure 1**) is also polluted owing to release wastewaters of plants of the chemical complex of Estarreja [30].

#### **2.1 Methods applied in Aveiro Lagoon**

 The case study of Aveiro Lagoon, commonly known as Ria de Aveiro, was based on the analysis of geochemical, sedimentological, and environmental parameters combined with living benthic foraminifera. Environmental parameters and some foraminiferal data were based on Martins et al. [18, 31, 32]. The sediments were collected, in Aveiro Lagoon channels, in 255 stations, in 2006/2007 with an adapted Petit Ponar Grab sampler (opening at both extremities), and using a ZOE I boat (**Figure 1**), they were analyzed. Water depth was measured with the boat sonar, and the stations were located with a GPS. The upper sediment layer (about 1 cm) was scraped for textural, geochemical, and microfaunal (living benthic foraminifera) analyses at each site. The sediments sampled for geochemical analysis were immediately cool preserved on board. The samples collected for foraminifera studies were kept in alcohol (90%) stained with Rose Bengal (2 g of Rose Bengal in 1000 ml of alcohol). Rose Bengal was used to differentiate between living and dead foraminifera [33]. Temperature, salinity, pH, and potential redox (Eh) were measured in water and sediments in each site.

 Samples for grain size and geochemical analysis were dried to constant weight in an oven for about 72 h, at 45°C, and stored for subsequent analysis. The procedures used for sedimentological and geochemical analyses are described in detail in Martins et al. [18, 31, 32]. The description of the foraminiferal analysis can be observed in Martins et al. [18, 31, 32]. The number of species per sample (S) and the diversity index of Shannon (H′) [34] were determined. The equitability also was determined according to Pielou [35] and S is the total number of species in a sample [36].

#### **2.2 Results obtained in Aveiro Lagoon**

#### *2.2.1 Abiotic data*

Sedimentary samples were collected at water depths varying between 0.5 and 30 m. Water temperatures varied between 10.5 and 26.0°C and salinity from 6.2 to 33.7. Higher temperatures were recorded in the innermost part of the main channels *Response of Benthic Foraminifera to Environmental Variability: Importance of Benthic… DOI: http://dx.doi.org/10.5772/intechopen.81658* 

 and salinities near the lagoon mouth and in the channels with strong marine influence. In sediments, Eh values ranged from 134 to −222 mv, and pH between 4.2 and 10.9. The lower Eh values were found in Aveiro City canals and Murtosa channel. Some sites of Murtosa channel also have low pH values.

Sediment mean grain size (SMGS) varied between 19.7 and 3660.2 μm and fine fraction (fines; <63 μm) between 0 and 97.7%. Total organic matter (TOC) content in dry sediments ranged from 0.1 to 7.7% (**Figure 1**). Concentrations of potentially toxic elements (PTEs) varied for Zn 2-684 mg kg<sup>−</sup><sup>1</sup> ; Pb 7-851 mg kg<sup>−</sup><sup>1</sup> ; Cu 0.03- 121 mg kg<sup>−</sup><sup>1</sup> ; As 03-119 mg kg<sup>−</sup><sup>1</sup> , and Cr 78-0.03 mg kg<sup>−</sup><sup>1</sup> . The highest TOC and PTEs contents were found in protected areas.

### *2.2.2 Foraminiferal assemblages*

 Living specimens density (no per gram of sediment fraction 63–500 μm) were < 2300 n°/g. Higher densities were found in protected areas of channels with a good connection with marine waters. Ninety species of living foraminifera were found in the Aveiro Lagoon. Number of species per sample (SR) varied from 0 to 28 and Shannon index values (H) were < 2.8. The most frequent species in living foraminiferal assemblages of Aveiro Lagoon are *Ammonia tepida* (<40%) and *Haynesina germânica* (<40%), which were found in all of the sites. Other species also reach relatively high relative abundance, at least locally, such as *Elphidium margaritaceum* (<54%), *Lepidodeuterammina ochracea* (<52%), *Lobatula lobatula*  (<45%), *Rotaliammina concava* (<32%), *Bolivina ordinaria* (<31%), *Cibicides ungerianus* (<19%), *Planorbulina mediterranensis* (<17%), *Cribroelphidium excavatum*, *Elphidium gerthi* (<14%), *Elphidium complanatum* (<14%), *Bolivina pseudoplicata* (<13%), *Remaneica helgolandica* (<13%), *Bulimina elongata/B. gibba*  (<10%), *Elphidium williamsoni* (<6%)*, Gavelinopsis praegeri* (<6%), *Trochammina inflata (<5%)*, *Elphidium crispum* (<6%), *Cribroelphidium excavatum* (<5%), *Quinqueloculina seminula* (<5%), and *Cribrostomoides jeffreysii* (<5%). Other species, such as *Buliminella elegantissima*, *Miliammina fusca*, *Haplophragmoides manilaensis*, *Entzia macrescens*, *Tiphotrocha comprimata*, *Ammoscalaria pseudospiralis*, *Arenoparrella mexicana*, *Siphotrochammina lobata*, *Ammobaculites balkwilli*, and *Eggerelloides scaber*, occur in general with percentages less than 5%.

#### **2.3 Discussion of the results obtained in Aveiro Lagoon**

 The higher values of SMGS are common in samples collected along the inlet and S. Jacinto channels where the tidal currents are stronger and reach frequently velocities >2 m s<sup>−</sup><sup>1</sup> [29], and in stations of other channels due to stronger currents activity in interaction with local topographic effects. Tidal currents affect not only the sediments' texture but also their chemical composition in Aveiro Lagoon [37, 38]. The sediments are coarse-grained and have low organic matter content where the currents are strong. Under low currents activity, fine-grained sediments enriched in organic matter are accumulated. The heterotrophic activity in Aveiro Lagoon is intense [39], resulting in negative sedimentary redox potential values in many areas mostly where fine sediments and high organic matter contents are accumulated. As the region surrounding the Aveiro Lagoon is densely populated, in the most confined areas located near cities and villages or close to the rivers' mouths, higher available concentrations of PTE (such as Cr, Cu, Ni, Pb, and Zn) can be found. Highest PTE values were found, for instance, in Aveiro city and Murtosa Channel and the lowest values in the lagoon entrance.

In Aveiro Lagoon, in addition to the salinity and organic matter contents, the hydrodynamical conditions have an important influence in the pattern of distribution of benthic foraminifera assemblages. Living foraminifera density tends to increase in fine-grained sediments enriched in organic matter.

Most of the living species found in the Ria de Aveiro are typical of European estuarine environments [40, 41], of worldwide transitional environments [42], and some are present in the nearby continental shelf [43, 44]. Species such as *H. germanica*, *A. tepida*, *C. excavatum*, and *T. inflata* are typical of coastal and transitional environments [45, 46] and are quite common in Ria de Aveiro.

In Aveiro Lagoon, the agglutinated species that are known to be well adapted to a wide range of salinities [47] predominate in different ecological niches, all of them characterized by high environmental stress. *Lepidodeuterammina ochracea* and *Rotaliammina concava* dominate in very strong hydrodynamical conditions at the lagoon entrance. Instead *Miliammina fusca*, *Haplophragmoides manilaensis*, *Entzia macrescens*, *Tiphotrocha comprimata*, *Ammoscalaria pseudospiralis*, *Arenoparrella mexicana*, *Siphotrochammina lobata*, and *Ammobaculites balkwilli* reach the highest relative abundance but have low densities in low salinity waters near the rivers' mouth and in sediments with relatively low Eh and pH values, where the abundance of calcareous species decline [23, 37]. According to Fatela et al. [21], the low pH values in sediment pore water limit the episodic presence of calcareous foraminifera. Low pH levels coupled with the reactivity of biogenic carbonates may promote dissolution and destruction of calcareous tests [48].

 The diversity and species richness tend to increase in the deeper areas under greater oceanic influence where there is also an increase of, for instance, *E. margaritaceum*, *L. ochracea*, *L. lobatula*, *R. concava*, *B. ordinaria*, *C. ungerianus*, *P. mediterranensis*, *E. gerthi*, *E. complanatum*, *B. pseudoplicata*, *B. elongata*/*B. gibba*, *G. praegeri*, *E. crispum*, and *C. jeffreysii*. These species seem to prefer more saline and oxygenated waters and less impacted environments and thus are named as "marine species" [43, 44].

 Excess of organic matter linked with fine-grained sediments can lead to depressed levels of oxygen in the sediment pore waters, which may cause stress to benthic foraminifera [49]. However, *H. germanica, A. tepida, Bolivina ordinaria, Bolivina pseudoplicata*, *T. inflata*, and *C. excavatum,* for instance, can occur in such conditions, which means that they tolerate better the negative effects of eutrophication than, for example, *L. ochracea*, *L. lobatula*, *R. concava*, *C. ungerianus*, *P. mediterranensis*, and *G. praegeri.* However, it is known that benthic foraminifera are very tolerant to oxygen depletion, and some species appear to be resistant to hypoxic and periodic anoxic conditions [50].

 According to Armynot du Châtelet et al. [51], the relative abundance of *A. tepida*  is typically favored by an increase of total organic matter, meaning food resources. *Ammonia tepida* has been invariably reported as a potential bioindicator of pollution at the majority of the coastal polluted sites [1]. In general, the sites polluted with sewage rich in toxic metals had low foraminiferal abundance, high percentages of *A. tepida*, low percentage of epiphytic species, and more deformed fauna [46]. In this work, *A. tepida* is present in the most polluted sediments of the Aveiro Lagoon, but it seems to be not firstly related to the PTE enrichment. According to Armynot du Châtelet et al. [51], the relative abundance of *A. tepida* is typically favored by an increase of total organic matter, meaning food resources. A few workers, however, suggested that the preference of *A. tepida* for fine-grained organic carbon-rich sediments may be the reason for its dominance in polluted regions [1].

In Aveiro Lagoon, *H. germanica* is mostly associated with confined lagoonal sites with high content in organic matter under low currents activity and waters with relatively high salinity. This species probably displays an opportunist behavior benefiting of the organic matter supply (food) and tolerating low levels of oxygen. *Haynesina germanica* is a mid-latitudinal, temperate, and euryhaline species that

#### *Response of Benthic Foraminifera to Environmental Variability: Importance of Benthic… DOI: http://dx.doi.org/10.5772/intechopen.81658*

populates shallow water muddy and phytal environments of salt marshes, intertidal habitats with salinities that generally range between 1 and 30, and optimal temperatures between 12 and 22°C [52]. Armynot du Châtelet et al. [10] have also shown that *H. germanica* is a successful pioneer species in polluted estuarine environments and in rich organic matter sediments and is tolerant to heavy metals. This species seems to be quite tolerant to higher concentrations of metals, namely Zn, Pb, and Cu, in Aveiro Lagoon.

The results obtained in Aveiro Lagoon also indicate that most of the species that live in this lagoon, mainly those that drive to the most internal and confined areas of the lagoon, should tolerate the stress caused by eutrophication and relatively high concentrations of PTE, namely *H. germanica*.

In general, the density and diversity of foraminifera are low in the lagoon. However, in the most impacted zones the density and diversity of foraminifera become even smaller. In fact, the increase in pollutants has been reported in general, as being marked by a decrease in species diversity with increased abundance of stress-tolerant species and high percentage of abnormalities [45, 46].

It is known that the distribution of the living assemblages is strongly affected by the estuarine dynamic, since foraminifera react within less than 1 month to changes of environmental conditions [17]. The distribution of the living foraminifera species results in several blooms throughout the year, for this reason the abundance and diversity of foraminifera is naturally temporally variable [17]. Living assemblages of foraminifera can be quite variable over time depending on the variability of the physicochemical parameters (according to weather changes). Therefore, monitoring studies may provide data not only on the response of species to the variation of environmental parameters but also on the gradients of natural and/or anthropogenic environmental impact.
