(Eco)toxicological studies frequently evaluate the effects of chemicals in one life stage of organisms, but the use of these outcomes can only partially estimate populational effects. In this regard, multi- and/or transgenerational studies should be performed in order to provide information on contaminant effects in a populational functioning context. The present review aimed to summarize and critically evaluate the current knowledge regarding multi- and/or transgenerational effects of traditional and emerging environmental chemicals on mollusks. Results showed that these kinds of studies were performed in aquatic mollusks (bivalve and gastropod), being Gastropoda the mollusk Class most frequently studied. Additionally, freshwater species and multigenerational studies were more common for this class. For the Bivalvia class, only marine species were evaluated, and transgenerational exposure was more commonly assessed. The effects were reported for 15 species, highlighting the marine bivalves Crassostrea gigas and Saccostrea glomerata, and the freshwater gastropod Lymnaea stagnalis. Multi- and transgenerational effects were described for 8 environmental chemical groups, mainly metals, pesticides, and pharmaceuticals. In general, multi- and transgenerational exposure induced biometric, developmental, and reproductive impairments in mollusks, indicating that environmental chemicals might lead to generational impairments, reduced population growth and reproductive capacity, and decreased fitness. The current study indicated that bivalves and gastropods are suitable organism models to assess the multi- and transgenerational adverse effects induced by traditional and emerging environmental chemicals.
Despite the relevance of multi- and transgenerational evaluations, these kinds of studies are not part of standard ecotoxicity tests with mollusks (Bouly et al., 2022; Reátegui-Zirena et al., 2017; Salice et al., 2010). This most likely occurs due to characteristics that are required to conduct such experiments. For example, freshwater gastropods are suitable model systems to be used in multi- and transgenerational exposures due to the fact that they are easy to culture, have a small size, reach reproductive age early, reproduce continuously under laboratory conditions, have high egg production, and have a short embryonic development period (Ubrihien et al., 2022). Taking these desired characteristics into consideration, a limitation in the number of species that are suitable candidates for this type of study appears. Nevertheless, both multi- and transgenerational studies should be considered by policymakers in their decisions, as they highlight effects on the population level, which is more ecologically relevant. In fact, the Organization for Economic Co-operation and Development (OECD) recently published a new guideline that considered multiple generations of the fish Japanese Medaka (Oryzias latipes; OECD, 2023), evidencing the progress of assessments for fish, but not for mollusks.
Despite the growing number of review articles on the use of mollusks (i.e., bivalves and gastropods) as model systems in ecotoxicological studies, environmental risk assessments, and biomonitoring programs (Beyer et al., 2017; Caixeta et al., 2022, 2020; Curpan et al., 2022; Rocha et al., 2015; Rodrigues et al., 2023), the knowledge concerning multi- and/or transgenerational effects of chemicals on this group remains scarce. Therefore, the current review aimed to evaluate the current state of knowledge regarding multi- and/or transgenerational effects on mollusks exposed to different environmental chemicals. A scientometric and systematic review was performed, and data were then summarized and critically discussed. Additionally, gaps in knowledge and recommendations for future studies were identified herein.
Numerous synthetic chemicals are produced annually and, eventually, released into the aquatic environment (Naidu et al., 2021). Due to their different purposes and properties, both fauna and flora might be affected by the presence of these chemicals in their habitat. In order to prevent irreversible environmental damage and impacts on human health, guidelines were created to lead policymakers in their decisions (Villa and McLeod, 2002). Besides tests from guidelines, different (eco)toxicological studies are conducted to understand the effects of environmental chemicals and their mechanisms of action and toxicity. Among aquatic organisms, mollusks are frequently used in (eco)toxicological studies with traditional and emerging pollutants and environmental monitoring programs due to their ecological, medical, and economic value (Caixeta et al., 2022; Harayashiki et al., 2020; Rocha et al., 2015).
Regardless of the importance of mollusks in (eco)toxicological studies, most experiments only considered one life stage of these organisms, disregarding the possible effects on the whole life cycle and population (Bouly et al., 2022; Reátegui-Zirena et al., 2017). In this regard, multi- and transgenerational studies might answer the questions regarding this subject. In multigenerational studies, several generations are exposed to the same pollutant and, most of the time, to the same concentrations. This allows the observation of possible adaptive mechanisms to that particular pollutant, that would increase the survival success of that population in an environmental pollution scenario, or it might reveal aggravated or delayed effects of pollutants, which could endanger the local population (Salice et al., 2009; Ubrihien et al., 2022). While transgenerational studies allow the understanding of how the following generations might be affected by parental exposures (Po and Chiu, 2018; Reátegui-Zirena et al., 2017; Yingprasertchai et al., 2017). As the observed effects cannot be ascribed to the direct contact of these organisms to the pollutant (Perez and Lehner, 2019). In addition, it is possible to evaluate if these effects in the offspring are temporary or permanent, and if there is an increase in the pollutant tolerance in this type of study (Reátegui-Zirena et al., 2017; Yingprasertchai et al., 2017).
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