Status of studies about Brazilian bioindicator fishes, a reviewAbstract:
Aim The freshwater environment is indeed diverse and complex, and it faces numerous challenges due to human activities. One approach to evaluating these human interventions is through the use of bioindicators, with fish being one of the key groups studied in the aquatic environment. However, the existent studies report that only a limited number of Brazilian ichthyofauna species have been investigated as potential bioindicators.
Methods The data present here were organized through a bibliographic review that adopts an exploratory and descriptive approach, focusing on articles published between the years 2000 and 2022, utilizing terms such as “bioindicators,” “Brazilian fish,” and “aquatic ecosystem” in both Portuguese and English languages.
Results Despite Brazil having the most diverse ichthyofauna on the planet, the research has focused on only 45 species thus far. Among these, Rhamdia quelen (Quoy & Gaimard, 1824) emerged as the most frequently studied species. The analysis of gill and liver tissues was found to be the most common method employed in these studies, while other tissues received relatively little attention. Moreover, the distribution of studies on bioindicator species was uneven, with the Upper Paraná ecoregion having the highest number of species investigated. This suggests that research efforts in this field have not been uniformly distributed across Brazil.
Conclusions The patchy nature of studies on bioindicators of the Brazilian ichthyofauna highlights the need for greater incentives and support for research in this area. With Brazil's exceptional ichthyofauna diversity, there is ample potential to identify and utilize additional species as environmental indicators. By expanding the scope of studies and addressing the geographical imbalance, a more comprehensive understanding of the impacts of human activities on freshwater ecosystems in Brazil can be achieved. This knowledge is vital for effective conservation and management efforts to protect and sustain the country's valuable aquatic resources.
Keywords: Brazilian fish; aquatic ecosystem; ecoregions; degradation; biomarkers
Resumo:
Objetivo O ambiente de água doce é amplamente diverso e complexo, e devido às atividades e intervenções antrópicas, enfrenta numerosos desafios. Uma das abordagens utilizada para avaliar essas intervenções humanas é através do uso de bioindicadores, sendo os peixes um dos principais grupos estudados no ambiente aquático. Entretanto, os trabalhos disponíveis relatam que apenas um número limitado de espécies da ictiofauna brasileira foi investigado como potenciais bioindicadores.
Métodos Os dados do presente trabalho foram organizados por meio de uma revisão bibliográfica que adota abordagem exploratória e descritiva, com foco em artigos publicados entre os anos de 2000 e 2022, utilizando termos como “bioindicadores”, “peixes brasileiros” e “ecossistema aquático” tanto em língua portuguesa quanto inglesa.
Resultados Apesar de o Brasil ter a ictiofauna mais diversificada do planeta, a pesquisa se concentrou em apenas 45 espécies até o momento. Dentre estas, Rhamdia quelen (Quoy & Gaimard, 1824) emergiu como a espécie mais estudada. A análise dos tecidos branquiais e hepáticos foi considerada o método mais comum empregado nesses estudos, enquanto outros tecidos receberam relativamente pouca atenção. Além disso, a distribuição dos estudos sobre espécies bioindicadoras foi desigual, sendo a ecorregião do Alto Paraná a que apresentou o maior número de espécies investigadas.
Conclusões Isso sugere que os esforços de pesquisa na área da ictiofauna como bioindicador não têm sido distribuídos uniformemente pelo Brasil. A natureza fragmentada dos estudos sobre bioindicadores da ictiofauna brasileira destaca a necessidade de maiores incentivos e apoio à pesquisa nesta área. Com a excepcional diversidade da ictiofauna do Brasil, há amplo potencial para identificar e utilizar espécies adicionais como indicadores ambientais. Ao ampliar o escopo dos estudos e abordar o desequilíbrio geográfico, pode-se alcançar uma compreensão mais abrangente dos impactos das atividades humanas nos ecossistemas de água doce no Brasil. Este conhecimento é vital para esforços eficazes de conservação e gestão para proteger e sustentar os valiosos recursos aquáticos do país.
Palavras-chave: peixes brasileiros; ecossistema aquático; ecorregiões; degradação; biomarcadores
1. Introduction
The complexity and diversity of the aquatic environment are easily observable. It encompasses a wide range of ecosystems such as rivers, lakes, lagoons, estuaries, and oceans (Rand et al., 1995). Furthermore, this environment is characterized by its openness and dynamism, consisting of various elements, both living (biotic) and non-living (abiotic). Consequently, it is continuously subjected to alterations and influences that impact its composition (Costa et al., 2008; Rand et al., 1995).
The constant changes occurring in the environment are primarily caused by various human activities. These activities encompass mining, urbanization, construction of dams and reservoirs, alterations in natural river courses, unregulated disposal of industrial and domestic waste, deforestation, pollution, unsustainable land use, introduction of non-native species, and the implementation of fish farming systems (Baptista et al., 2003; De Filippo, 2000; Goulart & Callisto, 2003; Langeani et al., 2007; Reis et al., 2016). Consequently, these actions bring about alterations in the physical, chemical, and biological characteristics of the environment, directly impacting the aquatic ecosystem and resulting in a loss of biodiversity (Clements, 2000) as well as a decline in water quality (Costa et al., 2008; Goulart & Callisto, 2003).
Water pollution and eutrophication are significant concerns in the degradation of aquatic ecosystems. The sources of pollution can be broadly categorized into three main areas. Firstly, agricultural activities contribute to pollution through the leaching process, where pesticides and fertilizers are transported by rainwater (Baptista et al., 2003; Cerejeira et al., 2003). Secondly, households discharge untreated wastewater, while industries release chemical and mining waste, as well as waste from slaughterhouses and farms (De Filippo, 2000). These multiple sources of pollution exacerbate the degradation of water quality and pose a threat to the health of aquatic ecosystems.
Pollution can manifest in various forms, including physical, chemical, and biological alterations within the aquatic environment (De Filippo, 2000). Physical pollution encompasses changes in temperature, brightness, turbidity, water velocity, and sedimentation, among others. Chemical pollution involves shifts in pH levels, dissolved salts, and other chemical constituents. Biological pollution refers to changes in the composition of the ecological community (De Filippo, 2000).
In contrast, eutrophication occurs when the aquatic ecosystem experiences an excess of nutrients, resulting in the rapid proliferation of algae and aquatic plants (De Filippo, 2000). This process, as described by Smith and Schindler (2009), can lead to noticeable changes in the taste, odor, and color of the water. Additionally, eutrophication can cause a decrease in dissolved oxygen levels and a decline in aquatic biodiversity, further exacerbating the negative impacts on the ecosystem (Smith & Schindler, 2009).
Organisms are commonly employed to determine and assess various degradation processes. According to Markert's (1994) definition, organisms (or parts thereof) are classified as bioindicators if they carry information that can evaluate the quality of an environment. In the context of the aquatic environment, fish (Chovanec et al., 2003; Freitas & Siqueira-Souza, 2009), crustaceans, aquatic plants, mammals, birds, algae, mollusks, and other organisms are considered bioindicators (Baptista et al., 2003; Lins et al., 2010; MacKenzie et al., 1995; Printes & Callaghan, 2003; Vital et al., 2011). Organisms positioned at the top of the food chain are often utilized as bioindicators due to their consumption of organisms at lower trophic levels, leading to the accumulation and concentration of contaminating substances (Lins et al., 2010). Additionally, a bioindicator must possess the capability to thrive in a healthy environment and endure exposure to contaminants (Barbieri et al., 2022; Chovanec et al., 2003). The research approach for a bioindicator can be classified as toxicological (e.g. sensitivity to metals and pesticides) (Braga et al., 2015; Silva et al., 2015; Florêncio et al., 2014; Martinez & Cólus, 2002; Moraes et al., 2012), morphological (e.g. analyses of gonadal diameter, hepatosomatic index, condition factor)(Arias et al., 2007; Barrilli et al., 2015; Morado et al., 2017; Schulz & Martins-Junior, 2001) histopathological (e.g. tissue analyses)(Amadeo et al., 2013; Martinez & Cólus, 2002; Miranda et al., 2008; Sousa et al., 2013) or physiological (e.g. enzymatic activity and blood tests) (Arias et al., 2007; Miranda et al., 2008; Morado et al., 2018; Rodrigues & Castilhos, 2003; Tortelli et al., 2006). Fish have traditionally been widely used as bioindicators in aquatic ecosystems (Chovanec et al., 2003; Martinez & Cólus, 2002), and there are several reasons why they are widely used to determine the natural characteristics of aquatic habitats and to assess their condition (Chovanec et al., 2003). The fish community includes several species scattered between trophic levels, with some species at the top of the chain, capable of accumulating contaminating substances that indicate and interferm in the occurrence of environmental disturbances (Freitas & Siqueira-Souza, 2009; Martinez & Cólus, 2002).
Certain species exhibit greater sensitivity to chemical and physical alterations, including changes in pH and dissolved oxygen, which can be attributed to shifts in environmental quality (Chovanec et al., 2003; Freitas & Siqueira-Souza, 2009). In comparison to other groups, such as invertebrates, fish offer a greater capacity to provide insights into the environmental conditions within their habitat due to their ease of identification and capture (Freitas & Siqueira-Souza, 2009).
Despite Brazil being recognized as the country with the highest biodiversity worldwide (Calixto, 2003; Mittermeier et al., 2005), research focused on utilizing ichthyofauna as bioindicators is often limited in scope and encompasses only a limited number of species. Recognizing the necessity to consolidate groups with the capacity to assess and evaluate aquatic environmental conditions due to their extensive utilization, the objective of this study is to assemble a comprehensive collection of Brazilian fish species that possess the potential to serve as bioindicators, using an approach that refers to the focal species and their corresponding toxicological, morphological, histopathological and physiological analyzes in response to anthropogenic interventions.
2. Material and Methods
The present study is a bibliographic review that adopts an exploratory and descriptive approach to investigate the Brazilian ichthyofauna as potential bioindicators. The dataset was compiled by conducting a search on the Google Scholar and SciELO platforms, focusing on articles published between the years 2000 and 2022.
To gather relevant articles, search terms such as “bioindicators,” “Brazilian fish,” and “aquatic ecosystem” were utilized in both Portuguese and English languages. These terms were combined in various combinations using the AND/OR conjunctions, and the searches were conducted to include singular, plural, and variant forms of the terms.
Following the identification of articles containing the targeted search terms, a citation and reference check was conducted to supplement the progress and requirements of the present study.
The results were gathered in a table whose validated potential refers to rather the species were submitted or not to tests capable to determinate whether it is a bioindicator. If the species has validated potential, it means that it has been subjected to testes, whether morphological, physiological, toxicological or histological. To develop the map, the Brazilian freshwater ecoregion presented by Abell et al. (2008) were used. These freshwater ecoregions are based on the distribution and composition of freshwater fish species, incorporating key ecological and evolutionary patterns.
3. Results
The bibliographic survey conducted in this study identified a total of 45 species of Brazilian ichthyofauna that have been recognized as potential bioindicators. These findings are based on the analysis of 39 articles (refer to Table 1 for a comprehensive list of the identified species). It is important to note that unpublished works and studies mentioning variations in the composition of ichthyological communities as bioindicators were excluded from the bibliographic analysis.
The individual capacity of each species to serve as a bioindicator was prioritized in this study, as suggested by Viana et al. (2010). Gills and muscles were the most commonly studied animal tissues for bioindicator analysis.
Among the identified species, Rhamdia quelen (Quoy & Gaimard, 1824), Hoplias malabaricus (Bloch, 1794), Geophagus brasiliensis (Quoy & Gaimard, 1824), Poecilia reticulata (Peters, 1859) and the genus Astyanax were the most frequently cited as bioindicators (refer to Table 1). Some species listed in the table have not been yet validated but hold potential as bioindicators according to the criteria proposed by Johnson et al. (1993). These criteria include easy recognition, cosmopolitan distribution, numerical abundance, limited mobility, well-known ecological characteristics, and suitability for laboratory studies.
The distribution of bioindicator species shows a significant disparity (Figure 1). The Upper Paraná ecoregion stands out with 18 bioindicator species, while several other ecoregions lack substantial research indicating species with bioindicator potential.
Reported distribution map of bioindicator species in Brazilian freshwater ecoregions. The map shows the distribution of species in South American freshwater ecoregions highlighted in color, marked by numbers, according to Abell et al. (2008). The uncolored and unnumbered regions did not show records of bioindicator species. The regions highlighted in gray are not part of the territory addressed in this work.
4. Discussion
Scientific literature underscores the significance of national-level scientific research in fostering innovation and driving economic development. Nevertheless, recent studies reveal an uneven distribution of scientific development within Brazil, primarily favoring regions in the south and southeast (Melo et al., 2019). This concentration of scientific activities has resulted in regional disparities in development and underscores the association between resource allocation and the economic capacity of specific regions (Melo et al., 2019; Mowery & Sampat, 2009). The ramifications of this centralized approach to scientific development are potentially detrimental to various domains of scientific research, including the study of biodiversity and the distribution of ichthyofauna.
The Upper Paraná watershed is recognized for its rich diversity of scientifically validated bioindicator species (Figure 1). However, this basin is facing substantial anthropic disturbances, making it one of the most impacted regions in the area (Agostinho et al., 2003; Castro & Arcifa, 1987). Despite extensive research conducted in Brazil, there still exists a significant number of species within this ecoregion that remain unknown or understudied (Agostinho & Júlio Júnior, 1999; Langeani et al., 2007). Molecular studies and identification efforts have highlighted this knowledge gap (Pereira et al., 2013), emphasizing the vulnerability of the ichthyofauna in the area. It is important to note that this situation may be even more critical in regions with higher biodiversity, where studies on fish as bioindicators are scarce or virtually non-existent.
Castro and Polaz (2020) highlight the limited translocation capacity of small species in aquatic environments, which leads to their local endemism as they do not migrate extensively between ecoregions during their life cycle. However, Poecilia reticulata, a small species (Lucinda, 2003), has been intentionally introduced for vector control and has achieved a widespread geographic distribution across various water bodies (Graça & Pavanelli, 2007). The broad distribution of P. reticulata presents significant potential for conducting comparative studies in degraded regions, especially when compared to locally distributed species. P. reticulata has the ability to indicate negative environmental disturbances in its habitat due to its high resilience to anthropogenic changes (Souza & Tozzo, 2013). However, it is important to consider that despite its bioindicator characteristics, these attributes may ultimately contribute to environmental issues for small aquatic communities (Souza & Tozzo, 2013; Widianarko et al., 2000).
Rhamdia quelen, a nocturnal species, displays a generalist feeding strategy, with a tendency towards omnivory. Small individuals primarily consume insects, while adults predominantly feed on fish (Casatti & Castro, 1998; Gomiero & Braga, 2008; C. C. G. F. Pereira et al., 2004). This species has a wide distribution (Albert et al., 2020) and is commonly found in fish farming, particularly in southern Brazil (Gomes et al., 2000; Marchioro & Baldisserotto, 1999). It exhibits remarkable resilience to environmental stressors, including temperature fluctuations and low salinity levels (Marchioro & Baldisserotto, 1999). Considering its morphological and physiological characteristics, R. quelen is regarded as a valuable bioindicator species (Chovanec et al., 2003; Johnson et al., 1993). However, taxonomic investigations have revealed that R. quelen represents a complex taxonomic scenario encompassing multiple species (Albert et al., 2020; Ríos et al., 2020; Scaranto et al., 2018; Silfvergrip, 1996). As different species may respond differently to the same environmental stimuli, studies employing R. quelen as a bioindicator must be conducted with care, preferably focusing on regional scopes, as observed in the studies included in this review (Table 1). Consequently, the ability to make comparisons between distant ecoregions, as is the case with Poecilia reticulata, may be compromised.
Several tissues have been tested for their bioindicator potential, but their use has proven to be limited, making comparisons between species and regions challenging (Table 1). Among the tissues, the branchial and hepatic tissues stand out as the most promising. Not only are they the most extensively studied, but they also possess characteristics that favor their use. The gills, being directly exposed to substances in the aquatic environment, are the first to experience the negative effects of pollution (Batista et al., 2014; Chovanec et al., 2003; Lins et al., 2010; Stagg & Shuttleworth, 1982). On the other hand, the liver receives a majority of circulating pollutants through the bloodstream, resulting in a higher accumulation of pollutants in liver tissue and making the organ more susceptible to damage (Batista et al., 2014; Chovanec et al., 2003; Lins et al., 2010). In addition to the average number of studies indicating the use of fish and their tissues as bioindicators, some authors have tested enzymes as biomarkers for individuals and environmental contamination (e.g., mercury and pesticides) (Batista et al., 2014; Braga et al., 2015; Menezes et al., 2011; Queiroz et al., 2019; Klemz & Assis, 2005; Moraes et al., 2012; Sinhorin et al., 2014; Tortelli et al., 2006).
In conclusion, this study highlights the incomplete nature of research on bioindicators of the Brazilian ichthyofauna, considering the vast number of species in existence. Currently, only a limited number of species have been studied, and research efforts are unevenly distributed. As a result, only a few species and a small number of tissues have been investigated. It is crucial to expand studies in this field to explore the bioindicator potential of species residing in other regions, such as the Amazon and the São Francisco region. Additionally, given the importance of ichthyofauna in assessing environmental quality, the scientific community should prioritize and conduct more studies focused on utilizing ichthyofauna as bioindicators.
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Cite as: Batista, C.P., Ferreira, A.A. and Silva, G.J.C. Status of studies about Brazilian bioindicator fishes, a review. Acta Limnologica Brasiliensia, 2024, vol. 36, e14. https://doi.org/10.1590/S2179-975X8723
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Edited by
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Associate Editor: Ronaldo Angelini.
Publication Dates
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Publication in this collection
20 May 2024 -
Date of issue
2024
History
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Received
18 Sept 2023 -
Accepted
25 Mar 2024
