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All issues No 425 (2024) Knowl. Manag. Aquat. Ecosyst., 425 (2024) 3 Full HTML
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Knowl. Manag. Aquat. Ecosyst.
Number 425, 2024
Biological conservation, ecosystems restoration and ecological engineering
Article Number 3
Number of page(s) 4
DOI https://doi.org/10.1051/kmae/2023025
Published online 23 January 2024

© D. Halabowski et al., Published by EDP Sciences 2024

Licence Creative CommonsThis is an Open Access article distributed under the terms of the Creative Commons Attribution License CC-BY-ND (https://creativecommons.org/licenses/by-nd/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. If you remix, transform, or build upon the material, you may not distribute the modified material.

The European bitterling Rhodeus amarus (Bloch, 1782) is a freshwater fish that exhibits a spawning relationship with freshwater mussels. Females bitterling develop long ovipositors to place their eggs inside the gills of a mussel through its exhalant aperture. The male releases its sperm in front of the inhalant aperture, and the fertilised eggs subsequently complete their development inside the mussel gill, bitterling juveniles emerging after approximately a month (Smith et al., 2004). Freshwater mussels require suitable fish hosts for the successful development of their own larvae, called glochidia. Depending on the mussel species, glochidia must spend time attached to a fish host to undergo metamorphosis into juvenile mussels and complete their life cycle, relying on food resources obtained from the host. Freshwater mussels employ a myriad of strategies to infest their hosts (Barnhart et al., 2008; Modesto et al., 2018) and some of them, such as Unio crassus Philipsson, 1788, have evolved species-specific behaviours to attract fish (Aldridge et al., 2023). However, the roles of host and parasite in the relationship between freshwater mussels and bitterling have been shown to be variable, and can potentially be reversed (Reichard et al., 2012). R. amarus is rarely a host for the glochidia of European freshwater mussels, and the presence of bitterling embryos in mussels is associated with physiological costs to the mussel host (Smith et al., 2001; Mills et al., 2005; Prié, 2017; Methling et al., 2019). Bitterling embryos compete with the mussel hosts for oxygen, damage the gills and disrupt filtration (Stadnichenko and Stadnichenko, 1980; Smith et al., 2001), potentially also competing for nutrients (Spence and Smith, 2013). The presence of developing bitterling embryos in the gills may also adversely affect host growth (Reichard et al., 2006). Therefore, the European bitterling should be regarded as a mussel parasite (Sousa et al., 2020; Brian et al., 2022). As such, the degree of historical coexistence between bitterling and mussel populations in Europe is crucial to the understanding of their relationship from an evolutionary viewpoint (Van Damme et al., 2007).

Here, we report that a rare European unionid, Pseudanodonta complanata (Rossmässler, 1835), serves as a host for bitterling, and further discuss research directions to address the consequences for P. complanata and other mussel populations of the expansion of R. amarus in Europe. Until now, a single documented instance of R. amarus utilising P. complanata as a host is based on a specimen from the River Cam in the United Kingdom in 1995 (Smith et al., 2004).

During a survey of the River Warta in Poland in July 2023, we examined 25 individuals of P. complanata and found one specimen that hosted a single bitterling embryo (visually identified) at the eyed stage (Fig. 1). We additionally checked for the presence of bitterling embryos in the other freshwater mussel species found at this site: for Anodonta anatina (Linnaeus, 1758), one individual contained a bitterling embryo, for Unio pictorum (Linnaeus, 1758) four individuals contained bitterling embryos and eggs, and for U. tumidus (Philipsson, 1788) 12 individuals contained bitterling embryos and eggs (Tab. 1). These results match previous studies, as it is known that A. anatina, U. pictorum, and U. tumidus are hosts for the European bitterling (Balon, 1962; Wiepkema, 1961; Reynolds et al., 1997). Furthermore, it is also known to date that among co-occurring mussel species U. crassus (Tatoj et al., 2017), A. cygnea (Linnaeus, 1758) (Reynolds et al., 1997), Pseudunio auricularius (Spengler, 1793) (Soler et al., 1999), Microcondylaea bonellii (Férussac, 1827) (Sousa et al., 2020), U. mancus Lamarck, 1819, and Potomida litoralis (Cuvier, 1798) are suitable native European hosts for the European bitterling (Prié, 2017).

This study reinforces the hypothesis of Soler et al. (2019), stating that Rhodeus amarus can utilise all European unionid species within its current range, including rare European species as occasional hosts, including Unio crassus (Tatoj et al., 2017; Lewisch et al., 2023) and Pseudanodonta complanata (Smith et al., 2004; this study). However, despite their capacity for using a wide range of hosts, field and laboratory studies show that European bitterling are choosy about which species of freshwater mussel they use for oviposition (Balon, 1962; Aldridge, 1997; Kondo et al., 1984; Smith et al., 2000; Reichard et al., 2010, 2015; Soler et al., 2019; Sousa et al., 2020). It has been demonstrated that both the number of previously laid eggs and mussel species affect oviposition decisions, although not the number of eggs laid by the female bitterling when oviposition occurs (Smith et al., 2000). Smith et al. (2000) showed that among four mussel species (Anodonta anatina, A. cygnea, U. tumidus, U. pictorum), female bitterling can distinguish between host species and also the ‘quality’ of the host based on the number of previously laid eggs. A. anatina was the most frequently chosen species, while bitterling avoided spawning in A. cygnea, and relatively few A. cygnea released young bitterlings. Moreover, embryo mortality occurred at different rates in different mussel species. Yet, in water bodies where only A. cygnea was present, bitterling readily utilised this species as a host. As a result, bitterling appear to select hosts depending on mussel availability, but modulate host preference based on temporal variation in mussel quality (Smith et al., 2000). Therefore, in the presence of other species of freshwater mussels, A. cygnea and other rare mussel species are only occasional hosts for the European bitterling. This is consistent with our results as, while the relative abundance of P. complanata (22%) in our studied site was higher than for U. pictorum (18%), the latter was utilised more often by bitterlings.

The presence of R. amarus in Central and West Europe may be relatively recent (Reichard et al., 2007; Van Damme et al., 2007). A comprehensive study of historical records suggests a rapid expansion of R. amarus from the Pontic region (Van Damme et al., 2007). Climate change has been identified as a significant factor influencing the spread of invasive fish species, as it can create favourable conditions for the establishment and expansion of invasive fish populations, including bitterling (Van Damme et al., 2007; Rahel and Olden, 2008; Hellmann et al., 2008). Additionally, intentional or accidental introductions of R. amarus to new regions cannot be excluded (e.g., waterways connecting previously separated systems, releases by hobbyists and anglers). Considering the potential further expansion of R. amarus in Europe and its negative impact on the physiological condition of mussels, along with the threatened status of freshwater mussels in Europe (Lopes-Lima et al., 2017; Sousa et al., 2023), efforts to introduce or conserve R. amarus in some locations, especially in areas where mussels are endangered, should be discouraged. Indeed, a reconsideration of the protective status of R. amarus in Europe appears necessary (Van Damme et al., 2007). For example, in Poland, where R. amarus is under partial protection (Regulation, 2016), R. amarus is the fourth most abundant fish species in inland waters (The Chief Inspectorate of Environmental Protection; Ichthyofaunal monitoring results from 2011-2022), its range expands and local populations steadily increase, making it the most abundant species among the protected freshwater fishes. In the Czech Republic, R. amarus is listed as a near-threatened species on the Red List (Lusk et al., 2017) and, at the same time, is considered a non-native species (Barankiewicz et al., 2021). Despite its expanding range in Europe, there is currently no evidence that R. amarus has contributed to the decline of freshwater mussel populations, though this may reflect a lack of appropriate research to address this question.

Although freshwater mussels have evolved to mitigate the impacts of parasitism by bitterling (Smith et al., 2000; Reichard et al., 2010), freshwater mussel species that have no exposure to bitterling may not have appropriate adaptive responses to cope with parasitism. Therefore, there is an urgent need to determine the potential threat to native mussels from R. amarus (Rouchet et al., 2017; Sousa et al., 2020), which may contribute to the conservation of European mussel species.

Acknowledgements

This study was funded by the Polish National Science Grant 2021/41/B/NZ8/02567. All procedures were carried out in accordance with permission from the Regional Directorate of Environmental Protection (WPN.6401.325.2022.BWo.3).

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Cite this article as: Halabowski D, Reichard M, Pyrzanowski K, Zięba G, Grabowska J, Smith C, Przybylski M. 2024. The depressed river mussel Pseudanodonta complanata as an occasional host for the European bitterling Rhodeus amarus. Knowl. Manag. Aquat. Ecosyst., 425. 3.

All Tables

Table 1

Mussels utilised by bitterlings at the studied site.

In the text

All Figures

thumbnail Fig. 1

A − Sampling site on the River Warta, Poland (coordinates: N 51.968589, E 18.793521; photo by G. Zięba); B − Shell of Pseudanodonta complanata infested by bitterling embryo (photo by D. Halabowski); C − The bitterling embryo in the gills of P. complanata (photo by D. Halabowski).
In the text

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