Progestogen-induced alterations and their ecological relevance in different embryonic and adult behaviours of an invertebrate model species, the great pond snail (Lymnaea stagnalis)

Abstract

The presence of oral contraceptives (basically applying estrogens and/or progestogens) poses a challenge to animals living in aquatic ecosystems and reflects a rapidly growing concern worldwide. However, there is still a lack in knowledge about the behavioural effects induced by progestogens on the non-target species including molluscs. In the present study, environmental progestogen concentrations were summarised. Knowing this data, we exposed a well-established invertebrate model species, the great pond snail (Lymnaea stagnalis) to relevant equi-concentrations (1, 10, 100, and 500 ng L−1) of mixtures of four progestogens (progesterone, drospirenone, gestodene, levonorgestrel) for 21 days. Significant alterations were observed in the embryonic development time, heart rate, feeding, and gliding activities of the embryos as well as in the feeding and locomotion activity of the adult specimens. All of the mixtures accelerated the embryonic development time and the gliding activity. Furthermore, the 10, 100, and 500 ng L−1 mixtures increased the heart rate and feeding activity of the embryos. The 10, 100, and 500 ng L−1 mixtures affected the feeding activity as well as the 1, 10, and 100 ng L−1 mixtures influenced the locomotion of the adult specimens. The differences of these adult behaviours showed a biphasic response to the progestogen exposure; however, they changed approximately in the opposite way. In case of feeding activity, this dose-response phenomenon can be identified as a hormesis response. Based on the authors’ best knowledge, this is the first study to investigate the non-reproductive effects of progestogens occurring also in the environment on molluscan species. Our findings contribute to the global understanding of the effects of human progestogens, as these potential disruptors can influence the behavioural activities of non-target aquatic species. Future research should aim to understand the potential mechanisms (e.g., receptors, signal pathways) of progestogens induced behavioural alterations.

Tyrosine hydroxylase messenger RNA corroborates protein localization in the nervous system of the pond snail, Lymnaea stagnalis

“…Embryos <4 days old (E45 as per the staging method employed in Voronezhskaya et al, 1999) exhibited no signal with respect to TH expression (data not shown). Four‐day‐old larvae began to develop eyes, and the development of the foot and shell became distinct (Hohagen & Jackson, 2013; Ivashkin et al, 2015; Jackson et al, 2016; Mescheryakov, 1990; Morrill, 1982; Svigruha et al, 2021). TH expression became detectable in two cells in the anterior region of the head at 5 days after first cleavage (Figure 2A–C), in the remnants of the apical organ of the larval nervous system, which is present only prior to metamorphosis (Nielsen, 2005).…”

Presence, Variation, and Potential Ecological Impact of Microplastics in the Largest Shallow Lake of Central Europe

“…From these stock solutions, 100 ng mL −1 working solutions were prepared in ethanol and then added in the appropriate volume to the experimental glass beakers to reach the desired nominal equi-concentration of 10 ng L −1 (mixture of progestogens) (≤ 0.01 % final solvent concentration). The 10 ng L −1 concentration value represents the detectable concentration level of the three compounds in Lake Balaton and its catchment area (Avar et al, 2016b;Maasz et al, 2019) as well as reflects to the average global concentration values (Svigruha et al, 2021a).…”

“…Previous environmental analytical studies revealed the presence of many PhACs in Lake Balaton and its catchment area (Avar et al, 2016a;Avar et al, 2016b;Maasz et al, 2019;Maasz et al, 2021;Molnar et al, 2021). Moreover, of the detected PhACs, previous studies investigated the impact of progestogens (progestogen and its synthetic analogues) on invertebrate (water flea [Daphnia magna] and the great pond snail [Lymnaea stagnalis]) and vertebrate (roach [Rutilus rutilus]) aquatic species representing the ecosystem of Lake Balaton and demonstrated several effects from the behavioral to the molecular level (Maasz et al, 2017;Svigruha et al, 2021b;Svigruha et al, 2021a;Zrinyi et al, 2017). However, similar surveys regarding MPs have not yet been carried out.…”

From polyethylene waste bottles to UIO-66 (Zr) for preconcentration of steroid hormones from river water

“…Steroid hormones are known as active chemical compounds that are involved in all the significant physiological roles in the body of living organisms 1 . These roles include the development of sexual characteristics, regulation of cell activity, mood control, water balance in the body, stimulation of the metabolism activities and growth, among others 2 – 4 . Steroid hormones are classified into four groups based on their structural variation and affinities 5 .…”