Knowl. Manag. Aquat. Ecosyst.
Number 425, 2024
Biological conservation, ecosystems restoration and ecological engineering
Article Number 3
Number of page(s) 4
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 (, 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.


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).


  • Aldridge DC, Brian JI, Ćmiel A, et al. 2023. Fishing for hosts: larval spurting by the endangered thick-shelled river mussel, Unio crassus. Ecology 104 (5): 4026. [CrossRef] [Google Scholar]
  • Aldridge DC. 1997. Reproductive ecology of bitterling (Rhodeus sericeus Pallas) and unionid mussels, PhD thesis. Cambridge: Cambridge University. [Google Scholar]
  • Balon EK. 1962. Note on the number of Danubian bitterlings developmental stages in mussels. Věstník Československé Společnosti Zoologické 26: 250–256. [Google Scholar]
  • Barankiewicz M, Svobodová J, Picek J, Semerádová S, Beránková T, Musil J. 2021. Metodika regulace an eradikace invazních druhů ryb: výběr vhodných metod v závislosti na charakteru vodního útvaru. Výzkumný ústav vodohospodářský, T. G. Masaryka, v.v.i., Praha, 61 p. [Google Scholar]
  • Barnhart MC, Haag WR, Roston WN. 2008. Adaptations to host infection and larval parasitism in Unionoida. J N Am Benthol Soc 27: 370–394. [CrossRef] [Google Scholar]
  • Brian J, Reynolds S, Aldridge DC. 2022. Parasitism dramatically alters the ecosystem services provided by freshwater mussels. Funct Ecol 36: 2029–2042. [CrossRef] [Google Scholar]
  • Hellmann J, Byers J, Bierwagen B, Dukes J. 2008. Five potential consequences of climate change for invasive species. Conserv Biol 22 (3): 534–543. [CrossRef] [PubMed] [Google Scholar]
  • Kondo T, Yamashita J, Kano M. 1984. Breeding ecology of five species of bitterling (Pisces: Cyprinidae) in a small creek. Physiol Ecol Jpn 21: 53–62. [Google Scholar]
  • Lewisch E, Arnold F, Fuehrer HP, Harl J, Thielen F, El-Matbouli M. 2023. Parasites and their impact on thick-shelled river mussels Unio crassus from two populations in Luxembourg. Dis Aquat Organ 153: 31–43. [CrossRef] [PubMed] [Google Scholar]
  • Lopes-Lima M, Sousa R, Geist J, et al. 2017. Conservation status of freshwater mussels in Europe: state of the art and future challenges. Biol Rev 92: 572–607. [CrossRef] [Google Scholar]
  • Lusk S, Hanel L, Lojkásek B, Lusková V, Muška M. 2017. Červený seznam ohrožených druhů České republiky. Příroda 34: 51–82. [Google Scholar]
  • Methling C, Douda K, Reichard M. 2019. Intensity-dependent energetic costs in a reciprocal parasitic relationship. Oecologia 191 (2): 285–294. [CrossRef] [PubMed] [Google Scholar]
  • Mills SC, Taylor MI, Reynolds JD. 2005. Benefits and costs to mussels from ejecting bitterling embryos: a test of the evolutionary equilibrium hypothesis. Anim Behav 70: 31–37. [CrossRef] [Google Scholar]
  • Modesto V, Ilarri M, Souza AT, et al. 2018. Fish and mussels: Importance of fish for freshwater mussel conservation. Fish Fish 19: 244–259. [CrossRef] [Google Scholar]
  • Prié V. 2017. Newly overlapping ranges: first records of Potomida littoralis (Cuvier, 1798) infestation by the European Bitterling Rhodeus amarus (Bloch, 1782). J. Conchol 42: 381–382. [Google Scholar]
  • Rahel F, Olden J. 2008. Assessing the effects of climate change on aquatic invasive species. Conserv Biol 22 (3): 521–533. [CrossRef] [PubMed] [Google Scholar]
  • Regulation 2016. Rozporządzenie Ministra Środowiska z dnia 16 grudnia 2016 r. w sprawie ochrony gatunkowej zwierząt. Available from (Accessed 24.10.2023). [Google Scholar]
  • Reichard M, Douda K, Przybylski M, et al. 2015. Population-specific responses to an invasive species. Proc Royal Soc B 282: 1–8. [Google Scholar]
  • Reichard M, Liu H, Smith C. 2007. The co-evolutionary relationship between bitterling fishes and freshwater mussels: insights from interspecific comparisons. Evol Ecol Res 9: 1–21. [Google Scholar]
  • Reichard M, Ondračková M, Przybylski M, Liu H, Smith C. 2006. The costs and benefits in an unusual symbiosis: experimental evidence that bitterling fish (Rhodeus sericeus) are parasites of unionid mussels in Europe. J Evolution Biol 19: 788–796. [CrossRef] [PubMed] [Google Scholar]
  • Reichard M, Polačik M, Tarkan AS, et al. 2010. The bitterling-mussel coevolutionary relationship in areas of recent and ancient sympatry. Evolution 64: 3047–3056. [Google Scholar]
  • Reichard M, Vrtílek M, Douda K, Smith C. 2012. An invasive species reverses the roles in a host-parasite relationship between bitterling fish and unionid mussels. Biol Lett 8: 601–604. [CrossRef] [PubMed] [Google Scholar]
  • Reynolds JD, Debuse VJ, Aldridge DC. 1997. Host specialization in an unusual symbiosis: European bitterlings spawning in freshwater mussels. Oikos 78: 539–545. [CrossRef] [Google Scholar]
  • Rouchet R, Smith C, Liu H, et al. 2017. Avoidance of host resistance in the oviposition-site preferences of rose bitterling. Evol Ecol 31: 769–783. [Google Scholar]
  • Smith C, Reichard M, Jurajda P, Przybylski M. 2004. The reproductive ecology of the European bitterling (Rhodeus sericeus). J Zool 262 (2): 107–124. [CrossRef] [Google Scholar]
  • Smith C, Reynolds JD, Sutherland WJ, Jurajda P. 2000. Adaptive host choice and avoidance of superparasitism in the spawning decisions of bitterling (Rhodeus sericeus). Behav Ecol Sociobiol 48 (1): 29–35. [CrossRef] [Google Scholar]
  • Smith C, Rippon K, Douglas A, Jurajda P. 2001. A proximate cue for oviposition site choice in the bitterling (Rhodeus sericeus). Freshwater Biol 46: 903–911. [CrossRef] [Google Scholar]
  • Spence R, Smith C. 2013. Rose bitterling (Rhodeus ocellatus) embryos parasitise freshwater mussels by competing for nutrients and oxygen. Acta Zoologica 94: 113–118. [CrossRef] [Google Scholar]
  • Soler J, Wantzen KM, Araujo R. 2019. Rhodeus amarus (Bloch, 1782): a new potential threat for Margaritifera auricularia (Spengler, 1793) (Unionoida, Margaritiferidae). Freshw Sci 38: 406–411. [Google Scholar]
  • Sousa R, Bogan AE, Gonçalves DV, et al. 2020. Microcondylaea bonellii as a new host for the European bitterling Rhodeus amarus. Knowl Manag Aquat Ecosyst 421: 4. [CrossRef] [EDP Sciences] [Google Scholar]
  • Sousa R, Zając T, Halabowski D, et al. 2023. A roadmap for the conservation of freshwater mussels in Europe. Conserv Biol 37 (2): 13994. [CrossRef] [Google Scholar]
  • Stadnichenko AP, Stadnichenko YA. 1980. The effect of bitterling larvae on the lamellibranch mollusc Unio rostratus gentilis Haas. Gidrobiologicheskii Zhurnal 17: 57–61. [Google Scholar]
  • Tatoj K, Ćmiel AM, Kwaśna D, Lipińska AM, Zając K, Zając T. 2017. The endangered thick-shelled river mussel (Unio crassus): a new host species for the European bitterling (Rhodeus amarus). Biodivers Conserv 26: 1217–1224. [CrossRef] [Google Scholar]
  • Van Damme D, Bogutskaya N, Hoffmann RC, Smith C. 2007. The introduction of the European bitterling Rhodeus amarus to west and central Europe. Fish Fish 8: 79–106. [CrossRef] [Google Scholar]
  • Wiepkema PR. 1961. An ethological analysis of the reproductive behaviour of the bitterling (Rhodeus amarus Bloch). Archives Néerlandaises de Zoologie 14: 103–199. [Google Scholar]

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.

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

Current usage metrics show cumulative count of Article Views (full-text article views including HTML views, PDF and ePub downloads, according to the available data) and Abstracts Views on Vision4Press platform.

Data correspond to usage on the plateform after 2015. The current usage metrics is available 48-96 hours after online publication and is updated daily on week days.

Initial download of the metrics may take a while.