Living and dead foraminifera assemblages as environmental indicators in the Almada River Estuary, Ilhéus, northeastern Brazil

Highlights

• Evaluation of environmental and ecological conditions in the Almada River Estuary.

• Characterization of impacted areas with few or none foraminiferal specimens.

• Recognition of bioindicators species of organic matter accumulation.

• Identification of pollution and hydrodynamic bioindicator assemblages.

Abstract

Analyses of living (L) and dead (D) foraminifera assemblages associated to environmental parameters were applied at the Almada River Estuary, aiming for assessments concerning local biodiversity, hydrodynamic sector and environmental quality. A total of 27 species were identified in the living assemblage and 35 in the dead, with the predominance of Ammonia tepida and Cribroelphium excavatum. A DCA for the living fauna demonstrated that C. excavatum Adelosina milletti, Elphidium discoidade, Rosalina bradyi and Triloculina oblonga were associated to shallow areas with muddy sediment and under marine influence in the estuary. Laryngosigma lactea and Pyrgo oblonga were associated to deep areas with sandy sediment under marine influence. All agglutinated species and the calcareous D. nitida and Miliolinella subrotunda were associated with organic matter and high chlorophyll levels from mangrove areas. A cluster analysis performed for L and D revealed five estuary regions: I - composed predominantly by D transported from the inner shelf; II - composed by L marine species; III - composed by D transported from region II and the inner shelf; IV - composed by living agglutinated species that delimit the beginning of the upper estuary area; and V - composed by transported agglutinated foraminifera and some calcareous species transported during storm episodes The present study was efficient in the environmental characterization of the Almada River Estuary and can be used as a baseline to understand natural or anthropic impacts in this ecosystem.

Introduction

Estuaries are characterized as the final region of the hydrographic basin, where seawater is mixed with fluvial waters. These hydrodynamic interactions create horizontals and verticals environmental parameter gradients, such as salinity, pH and dissolved oxygen (Simenstad and Yanagi, 2012). Estuaries provide invaluable ecosystem services essential for life-support processes on which all organisms depend on (Daily et al., 1997). When these ecosystems are associated with salt marshes and mangrove forests, they act as significant environment filters, providing ecosystem services, such as water filtration and habitat protection (USEPA, 2004).

Due to significant biodiversity and adequate geomorphological conditions, human communities use estuaries as fishing sources and harbour areas, as well as for transportation and recreation, among others. As a result, these areas concentrate the largest urban agglomerations. It is estimated that 22 of the largest cities in the world are located in estuarine zones (Ross, 1995). Increasing human occupation in fluvial and estuarine systems has led to alterations in their natural conditions, intensifying the range of anthropogenic stressors, including industrialization, urbanization, tourism, agriculture, fishing and resource overexploitation. These stressors can lead to pollution and species and habitat losses, as well as ecosystem degradation and fragmentation (Laut et al., 2017; Raposo et al., 2018; Belart et al., 2019).

The Almada River Estuary is located in southern Bahia, a state located on the northeastern coast of Brazil. The southern Bahia region comprises the largest and richest coral reefs in the South Atlantic, the largest rhodolite bank described in the world and a significant mangrove forest area (Dutra et al., 2005; Amado-Filho et al., 2012). This region has increasingly suffered high anthropic impacts due to the increase of unplanned urbanization since the 1990s, which intensified due to the rural population migration occurred during the cacao crisis in Brazil (PNRH, 2005). However, few studies concerning the identification of environmental impacts and monitoring of this region have been performed.

Environmental characterization is a fundamental step for environmental monitoring and management. It can be performed through differentiated approaches based on physical (hydrology, geomorphology, sedimentology and pedology, among others) or biological (fauna and flora) aspects, as well as the assessment of natural and anthropogenic pressures (Franco et al., 2009).

Resolution No. 357 of 2005 of the Brazilian National Environment Council (CONAMA) recommends the use of bioindicators to assess environmental water quality, as physical and chemical monitoring is not efficient in detecting changes in biological communities (Goulart and Callisto, 2003).

Studies on foraminifera associations have been applied in the last decades as tools for the environmental diagnosis of coastal regions. These organisms exhibit quick responses to environmental changes, display a short life cycle, are widely distributed and their shells are preserved in the sediment surface layer (Murray, 1991, 2006; Scott et al., 2002). In addition, they also display well-defined ecological and biological characteristics (Alve, 1995; Frontalini and Coccioni, 2011; Schönfeld et al., 2012).

The composition and distribution of foraminifera communities are associated to variation in environmental parameters such as oxygen, depth, grain size and organic matter supply, heavy metals and hydrocarbons, among others (Schafer et al., 1991Schafer et al., 1991; Alve, 1995). Therefore, it is possible to compartmentalize an estuary based on assemblage distribution and identify regions undergoing disturbances caused by natural and/or anthropic factors (Laut et al., 2014, 2016a). However, few studies have been carried out on living foraminifera in Brazilian estuaries (Laut et al., 2007, 2011; 2016b; Souza et al., 2010; Rodrigues et al., 2020). This knowledge gap reduces the possibility of using these organisms for biomonitoring efforts. So far, the number of species living in Brazilian estuaries is unknown, especially in the northeast, and their relationship with environmental parameters that determine their distribution is still under-explored. Another challenge concerning the use of foraminfera as bioindicators in coastal areas is the establishment of sampling, laboratory and taxonomy methodologies (Sousa et al., 2020).

This study is the first assessment performed in South Bahia in order to characterize foraminifera communities, both living and dead, and associate them to physical-chemical and sedimentological parameters at the Almada River Estuary, in order to recognize possible hydrodynamic and/or environmental impact bioindicators. Understanding concerning foraminifera biodiversity and hydrodynamic compartments is an invaluable tool for the development of management programs and the elaboration of public policies for the conservation of the Almada River region. The use of standardized methodologies intends to contribute to knowledge concerning foraminifera as bioindicators in coastal areas.