Metabolic and physiological responses of a coastal fish in highly and lightly impacted habitats

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Highlights

  • Estuary studied is higher impacted than coastal zone by human activities.

  • Feeding activity and diet composition showed differences between areas studied.

  • Somatic indexes and enzymatic activity registered are associated with the diet composition.

  • Biologic responses of sentinel species are correlated with the natural environment stressors.

Abstract

Coastal and estuarine zones are used by fish as nursery, spawning and feeding grounds. However, these essential habitats are characterized by the presence of both natural and anthropogenic stressors that may represent potential threats for the wellbeing of aquatic organisms, particularly fish. The main objective of this study was to evaluate and understand the effects of environmental stressors, both natural and anthropogenic, on coastal fish species using Ramnogaster arcuata as bioindicator. Fish were captured in two zones with different human activity levels: a highly impacted zone in Bahía Blanca Estuary (BBE) and a lightly impacted zone in the adjacent coastal zone (ACZ). Various indicators were used to determine fish responses to environmental stress. Main differences found between fishes from the two zones were in the condition index, trophic ecology (including feeding activity and diet composition) and liver metabolic biomarkers (ALT/AST enzymes, protein levels and lipid peroxidation). On the other hand, metal concentration levels analyzed in muscle did not show important differences between both environments. Physiological responses of R. arcuata from both zones were strongly correlated with natural stressors.

Introduction

Coastal waters and estuaries are ideal spawning and nursery habitats for many marine fish species, as they provide high food availability, shelter and other services that make optimal growth and survivability of early life stages possible (Whitfield and Elliot, 2002; Elliott et al., 2007; Seitz et al., 2014). Historically, humans have settled alongside rivers and coastal environments, which in turn have resulted in these habitats being widely modified and impacted by a multitude of human activities (Vasconcelos et al., 2017). Several of these activities cause loss, modification and fragmentation of aquatic coastal environments by changing the hydrological dynamics of the systems. Other terrestrial and coastal activities (e.g. industry and agriculture) introduce a variety of xenobiotic compounds, which impact regular physiological processes of fish and other organisms across different trophic levels (Brown et al., 2018).

Marine fish species are commonly dependent on different habitats during their life cycle. Estuaries, among other habitats, play a significant role in the recruitment success of many commercially valuable species (Elliott et al., 2007; Seitz et al., 2014). How alterations produced in these environments affect the ecological functions of fish, is a question on which extensive research is being conducted (Brown et al., 2018). Biological indicators based on fish communities are recognized as useful tools to assess anthropogenic impacts on estuaries, and they have been used to assess individual and population status as well as habitat quality (Vasconcelos et al., 2017). Fish inhabiting estuarine and coastal zones have been proposed as bioindicators for pollution monitoring, as the assessment of sensitive metabolic and physiological responses can be carried out via biomarker evaluation. Biomarkers represent any biochemical, physiological, behavioral or morphological alteration that can modify the well-being of an organism (van der Oost et al., 2003). Condition indices, oxidative stress, metabolic enzymes, histopathology and DNA damage are examples of biomarkers (Hook et al., 2014). These biomarkers are related to the organisms' ability to respond to the environment at different time scales (Harrison and Whitfield, 2006) and are triggered by endogenous or exogenous disturbances (van der Oost et al., 2003).

Bahia Blanca Estuary (BBE), located in the Southwest Atlantic Ocean, is a typical example of an estuary affected by its nearby human settlement. Environmental impacts in BBE due to anthropic activity are well-documented, which makes it an interesting study zone. The presence of heavy metals (such as Cr, Ni, Pb and Zn) and organic compounds (polycyclic aromatic hydrocarbons and pesticides) have been recorded in sediment and water column, ranging from low to very high concentrations in certain hotspots, according to international guidelines and regulations (Botté et al., 2007, Botté et al., 2010; Arias et al., 2010; Oliva et al., 2015; La Colla et al., 2017, La Colla et al., 2018). In order to monitor this environment, the Jenyns' sprat Ramnogaster arcuata (Teleostei: Clupeidae) has recently been proposed as a bioindicator fish (Ronda et al., 2019). This species has a wide distribution in coastal zones from the Southwestern Atlantic Ocean. It can be found from southern Brazil (estuary of the Patos Lagoon) to Tierra del Fuego in southern Argentina (Lopez Cazorla et al., 2011). R. arcuata is an estuarine-dependent species that carries out its entire life cycle in BBE (Lopez Cazorla and Sidorkewicj, 2009) and is also found in the adjacent coastal zone (ACZ) of this estuary. Several aspects of R. arcuata have been studied, including geographical distribution (Cione et al., 1998), trophic ecology (Lopez Cazorla et al., 2011) and other key population biology traits (Lopez Cazorla and Sidorkewicj, 2009). The present study aimed at comparing the body condition and physiological responses of a coastal fish species between two zones with high (HI) and least (LI) human-activity intensity. The concentration of metals in muscle and the trophic ecology of R. arcuata were employed as a proxy for both anthropogenic and natural environmental stressors, respectively.

Section snippets

Study area

BBE is located between 38°30′–39°25′S and 61°15′–63°00′W (Fig. 1) and is the second largest estuary of Argentina, covering an area of 750 (low tide) to 1900 (high tide) km2, with a mean depth of 10 m. This environment is under progressive impact from human activity due to the growing development of urban and industrial activities near and onto the watershed (Botté et al., 2007; Arias et al., 2010; López Abbate et al., 2012; Fernández Severini et al., 2013; Dutto et al., 2014; La Colla et al.,

General status of fish

The K index showed statistical differences between HI and LI zones (t = −3.36, df = 21, p value = .003), located in BBE and ACZ, respectively; being higher in HI individuals (K = 0.80 ± 0.03) than in LI (K = 0.74 ± 0.02). In addition, differences in K were not found between HI-1 and HI-2 nor between LI-1 and LI-2 (Table 3 and Fig. 2). The length-weight relationship of R. arcuata from HI (intercept = 1.36 × 10−6; slope = 3.28) and LI (intercept = 2.04 × 10−6; slope = 3.21) zones were not

Discussion

Coastal and estuarine areas are essential habitats that fish utilize as nursery, spawning and feeding grounds. However, they are characterized by the presence of both natural and anthropogenic multiple interacting stressors, which can represent potential threats towards aquatic organisms (Beck et al., 2001). A comparison of habitats exposed to differential anthropogenic pressures provides a means to distinguish between natural and anthropogenic stressors (Whitfield and Elliot, 2002). Various

Declaration of competing interest

The authors have no conflict of interest to declare.

Acknowledgments

The funds provided by Consejo Nacional de Investigaciones Científicas y Técnicas, Agencia Nacional de Promoción Científica y Tecnológica (project PUE 22920160100057CO), Universidad Nacional del Sur (Projects PGI 24/B231, PGI 24/ZB59 and PGI 24/ZB83) and Programa de Monitoreo de la Calidad Ambiental de la Zona Interior del Estuario de Bahía Blanca of Municipalidad de Bahía Blanca are gratefully acknowledged. We also thank Alberto Conte and Enio Redondo (Instituto Argentino de Oceanografía) for

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