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All issues No 426 (2025) Knowl. Manag. Aquat. Ecosyst., 426 (2025) 4 Full HTML
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Knowl. Manag. Aquat. Ecosyst.
Number 426, 2025
Riparian ecology and management
Article Number 4
Number of page(s) 5
DOI https://doi.org/10.1051/kmae/2024026
Published online 27 January 2025

© M. Pfeiffer et al., Published by EDP Sciences 2025

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); hereafter simply referred to as bitterling unless otherwise specified) is the only bitterling species native to Central and West Europe (Kottelat and Freyhof, 2007). It has a unique strategy for reproduction: Bitterlings rely heavily on the presence of live freshwater mussels from the Unionoidea superfamily (mainly species from the Unionidae family, and to a lesser extent on bivalves from the Margaritiferidae family; reviewed in Smith et al., 2004) for reproduction. Females use long ovipositors to deposit their eggs in the gills of a clam through the clam's exhalation siphon (Aldridge, 1999; Smith et al., 2004). Bitterling embryonic development takes place inside the mussel, where the embryos remain for approximately one month.

Many of the 16 freshwater bivalves of the Unionoidea superfamily that occur naturally in Europe are in severe decline and are therefore considered highly endangered (Lopes-Lima et al., 2017). Due to the unique spawning symbiosis between bitterlings and Unionid mussels, the distribution of European bitterlings should also be restricted in the absence of their hosts. However, it can be observed that the bitterlinǵs distribution area in the Upper Rhine valley has continuously increased over the last decade, despite the steady decline of unionid mussel species in the same area (Dußling et al., 2018; Büro Gobio, 2022). This contradictory trend is difficult to explain, given that the European bitterling is dependent on Unionid host mussels for its development.

Like the European bitterling, the East Asian freshwater mussel Corbicula fluminea (O. F. Müller, 1774) has also been steadily spreading into the Upper Rhine Valley since the late 19th century. Some bitterling species in Asia and Europe use freshwater mussels outside the Unionoidea superfamily. For example, the Asian bitterling Sinorhodeus microlepis is specialised in using only C. fluminea for sexual reproduction (Li et al., 2017). As the cyprinid subfamily Acheilognathinae is mainly distributed in Asia (Fricke et al., 2023), it is conceivable that there is a causal relationship between the mutual dispersal of R. amarus and C. fluminea in Europe. Although oviposition of R. amarus in the invasive zebra mussel Dreissena polymorpha was observed by Bartáková and Reichard (2017), breeding success has not been documented. It is currently unknown whether the genus Corbicula also serves as a host for the European bitterling.

We tested the theory that bitterlings select Corbicula as potential hosts for their progeny. Furthermore, it is not clear whether the evolved defences of Asian Corbicula against bitterling parasitism will also result in the successful expulsion of bitterling eggs and embryos. Theoretically, the bitterling offspring could successfully develop in Corbicula mussels.

To test our hypothesis, we kept European bitterlings and Asian C. fluminea together in a tank for several weeks and recorded their behaviour. Our experimental animals originate from an area where both species co-exist, the Dreisam-Glotter drainage in south-west Germany. Ten individuals of young European bitterling fishes were caught in the river Glotter in summer 2019. Specimens of C. fluminea were collected from Lake Moosweiher in January 2020. Both species were kept in a 50-litre tank. Bitterlings were fed daily with standard fish food. The bitterling's behaviour was recorded when clear signals for prespawning behaviour were observed, such as mussel inspection, head-down posture, skimming, sperm release, quivering, female leading of the male, and spawning. If oviposition was successful, the C. fluminea individuals were removed, opened, and inspected for bitterling eggs in the inner tissue of the clam using a stereomicroscope (Nikon SMZ 1500).

To determine the preferred host of R. amarus when coexisting, we combined two individuals of U. crassus and three individuals of C. fluminea with ten bitterlings from the Glotter river in a 50-litre tank. The U. crassus and C. fluminea individuals were collected in April 2020 from the Krebsenbächle stream in the north of Freiburg. This location was chosen because R. amarus is absent, ensuring that no mussels were already infected with bitterling eggs. Once again, the behaviour of the bitterlings was recorded when clear signals of pre-spawning behaviour were observed.

Another experiment investigated the host preferences of R. amarus in their natural environment. The Schutter and the Herrenmühlebach are two rivers in the Upper Rhine Valley where live specimens of C. fluminea, R. amarus, and the thick-shelled river mussel (Unio crassus) coexist. Thus, bitterlings can use either U. crassus or C. fluminea as a host at both locations. In April and May, the bitterling fish were in their mating season, as indicated by their bright nuptial coloration. It is likely that the bitterlings have already deposited their eggs in their host mussel.

In April 2020, we collected 47 living C. fluminea from the Schutter. In May 2020, a further 18 C. fluminea individuals were taken from the Herrenmühlebach. In the laboratory, the collected C. fluminea individuals were opened and examined for bitterling eggs or embryos in the inner tissue of the mussel. In April 2020, we collected one individual of U. crassus from the Schutter. The two valves were carefully opened on-site without causing any damage. The inner tissue was examined for bitterling eggs or embryos, and subsequently, U. crassus was returned to the Schutter.

Shortly after the fish were placed in the aquarium, the male bitterlings developed their nuptial colouration. This change in colour persisted for several weeks even in the absence of a host clam. Subsequently, males showed mating behaviour (males frequently chasing females), albeit with a reduced spectrum. Female bitterlings also developed an ovipositor, but it was regularly retracted and not ready to spawn.

Shortly after placing C. fluminea individuals in the aquarium, both male and female bitterlings approached the clams and examined them by facing the siphons (head down posture); see supplementary video). Soon after, the female ovipositor extended to its maximum length. Both sexes showed clear signals of pre-spawning behaviour as described in Duyvené de Witt (1955) and Wiepkema (1961):

  1. quivering of the male in front of the female,

  2. frequent pursuance of females by males,

  3. male leading the female to the mussel,

  4. skimming (male and female dip forward frequently over the mussel).

The skimming behaviour can be considered as failed spawning (female misses the exhalant siphon with its ovipositor) and sperm release attempts (Smith et al., 2001). At one instance, sperm release of the male and immediate successful spawning of the female could be recorded (see supplementary video). These spawning periods (when the males showed a bright mating dress, the females extended their ovipositor and both sexes showed distinct behaviour) alternated with periods of inactivity. During the inactive periods, the nuptial coloration and ovipositor length were reduced.

The presence of bitterling eggs was confirmed by dissection of the C. fluminea specimens used. However, living embryos have never been found on the gills, only embryos that have not developed any further (Fig. 1). Additionally, we did not observe any juvenile bitterlings that had successfully developed and been released into the open water.

When both U. crassus and C. fluminea are present, bitterlings clearly prefer U. crassus for oviposition. Additionally, R. amarus larvae were only found in the two U. crassus individuals (Fig. 2), indicating a preference for this species over C. fluminea.

None of the 47 C. fluminea individuals collected from the Schutter, nor the 18 from the Herrenmühlebach, hosted bitterling eggs or embryos. In the gills of C. fluminea, gelatinous oval structures measuring 1–2 mm were occasionally observed (Fig. 3). Whether these objects were bitterling eggs or simply fat globules could not be determined. On the other hand, live bitterling embryos were found in the few U. crassus collected at the same location in the river Schutter (Fig. 3). This observation supports the results of the laboratory tests.

Our results indicate that C. fluminea is not a preferred host for the European bitterling. This is evidenced by the fact that C. fluminea is only used in the absence of unionid mussels. While European bitterlings occasionally use C. fluminea individuals for reproduction, this does not result in successful larval development within the mussel body. In accordance with the host preference and host suitability hypothesis evidenced by Reichard et al., (2007a), the general anatomy of C. fluminea seems to be unsuitable for successful bitterling embryo development. In the study by Reichard et al., (2007a), the authors found no bitterling eggs or embryos in C. fluminea.

Thus, the current range extension of the European bitterling appears not to be associated with the substantial spread of C. fluminea in Europe. It is more likely that R. amarus benefits from a general temperature rise caused by climate change (van Damme et al., 2007; Hellmann et al., 2008; Rahel and Olden, 2008), potentially resulting in an extension of the spawning season, faster larval/juvenile development, and improved habitat suitability. With a prolonged breeding season, a single unionid individual (like Unio crassus in the Schutter) might be used several times for oviposition.

Almost all bitterling species in the subfamily Acheilognathinae − including the genus Rhodeus − are restricted to Asia (Arai, 1988; Okazaki et al., 2001) and share a long co-evolution with native Asian mussel species. This led to the development of defence mechanisms against bitterling infection in Asian freshwater mussels (e.g. egg/embryo ejection and others; Reichard et al., 2006), reported for Sinanodonta woodiana (Reichard et al., 2007b). However, Unionid mussels native to Europe have not yet developed measures to avoid bitterling oviposition. Given that R. amarus is considered to be a parasite on European unionid bivalves with likely detrimental effects on its hosts (Reichard et al., 2006, 2007a; Sousa et al., 2020), further expansion and population growth of R. amarus must be viewed critically, especially given that all unionid bivalves in Europe are highly threatened (Lopes-Lima et al., 2017; Sousa et al., 2023).

The introduction and subsequent dispersion of the Asian clam Corbicula fluminea outside its native range (Southeast Asia) is one of the most dramatic events of non-indigenous invasive species (NIS) success in aquatic ecosystems (Crespo et al., 2015; Nentwig et al., 2018). These NIS, whether introduced accidentally or deliberately, are considered the most devastating environmental problem today, causing high ecological, economic, and conservation costs. The first records of C. fluminea in Europe date back to the early 1980s (Mouthon, 1981). It was introduced by cargo shipping upstream of the Rhine River as a stowaway in ballast water. Since then, it dispersed inexorably in Germany, now colonizing e.g. the entire Rhine and many connected water bodies up to the Lake Constance, Neckar, Oder, Weser, Elbe, and Danube (Alf, 1991; Kinzelbach, 1991; Boschert et al., 1996; Rey and Ortlepp, 1997; Titttizer and Taxacher, 1997; Schniebs and Winkelmann, 2001; Jueg and Zettler, 2004; Werner and Mörtl, 2004; Wilke, 2007).

The high reproductive fitness of C. fluminea (short generation times, rapid growth, rapid sexual maturity, and great fecundity) enabled this species to frequently predominate the benthic substrate of populated streams (Sousa et al., 2008; Geist et al., 2023). C. fluminea seems to prevail over the native unionid mussels regarding interspecific competition for the same resources (Ferreira-Rodríguez et al., 2018). Therefore, C. fluminea represents a significant threat to the continued existence of all European unionid bivalves and the implementation of urgent conservation measures is imperative.

It is unknown whether conservation efforts for unionid mussels will be successful in the future (Lopes-Lima et al., 2017), but on a local scale, many populations in Southwestern Germany are facing extinction. However, if a local population of Unionids becomes extinct, the socially connected bitterling population in the same location will also die. It is therefore highly likely that the European expansion of R. amarus will slow down or even come to a halt.

Supplementary Material

Movie S1. The video presents a series of oviposition attempts by Rhodeus amarus in Corbicula fluminea. Access here

References

  • Aldridge DC. 1999. Development of European bitterling in the gills of freshwater mussels. J Fish Biol 54: 138–151. [CrossRef] [Google Scholar]
  • Alf A. 1991. Neu- und wiedergefundene Arten des Makrozoobenthon im Neckar. Lauterbornia 8: 71–76. [Google Scholar]
  • Arai R. 1988. Fish systematics and cladistics. In Uyeno T and M, eds. Ichthyology Currents, Asakura Shoten, Tokyo, 4–33. [Google Scholar]
  • Araujo R, Moreno D, Ramos M. 1993. The Asiatic clam Corbicula fluminea (Müller, 1774) (Bivalvia: Corbiculidae) in Europe. Am Malacol Bull 10 1: 39–49. [Google Scholar]
  • Bartáková V, Reichard M. 2017. No effect of recent sympatry with invasive zebra mussel on the oviposition decisions and reproductive success of the bitterling fish, a brood parasite of unionid mussels. Hydrobiologia 794: 153–166. [CrossRef] [Google Scholar]
  • Boschert M, Heitz A, Heitz S, Laufer H, Münch C, Josef Ruf J, Rademacher M, Saumer F, Schneider F, Uhl A, Westermann K, Westermann S, Hanspeter Zimmermann H. 1996. Die Körbchenmuscheln Corbicula fluminea und Corbicula fluviatilis am südlichen Oberrhein − Dokumentation der Neufunde. Naturschutz südlicher Oberrhein 1: 211–225. [Google Scholar]
  • Büro Gobio 2022. Die Kleine Flussmuschel, Unio crassus (PHILIPSSON, 1788), in Baden-Württemberg, available at https://www.gobio-online.de/forschung.php − 2024/06/19. [Google Scholar]
  • Crespo D, Dolbeth M, Leston S, Sousa R, Pardal MÂ. 2015. Distribution of Corbicula fluminea (Müller, 1774) in the invaded range: a geographic approach with notes on species traits variability. Biol Invasions 17: 2087–2101. [CrossRef] [Google Scholar]
  • den Hartog C, van den Brink FWB, van der Velde G. 1992. Why was the invasion of the river Rhine by Corophium curvispinum and Corbicula species so successful? J Nat Hist 26: 1121–1129. [CrossRef] [Google Scholar]
  • Dußling U, Baer J, Gaye-Siessegger J, Schuman M, Blank S, Brinker A. 2018. Das große Buch der Fische Baden-Württembergs. Ministerium für Ländlichen Raum und Verbraucherschutz Baden-Württemberg, Stuttgart, 372 p. [Google Scholar]
  • Duyvené de Wit JJ. 1955. Some observations on the European bitterling (Rhodeus amarus). Suid-Afrikaanse Joernaal van Wetenskap 51: 249–251. [Google Scholar]
  • Ferreira-Rodríguez N, Sousa R, Pardo I . 2018. Negative effects of Corbicula fluminea over native freshwater mussels. Hydrobiologia 810: 85–95. [CrossRef] [Google Scholar]
  • Fricke R, Eschmeyer WN, Van der Laan R. 2023. Eschmeyer's catalog of fishes: Genera, species, references. Available from: http://researcharchive.calacademy.org/research/ichthyology/catalog/SpeciesByFamily.asp#Acheilognathidae [Google Scholar]
  • Geist J, Benedict A, Dobler AH, Hoess R, Hosse P. 2023. Functional interactions of non-native aquatic fauna with European freshwater bivalves: implications for management. Hydrobiologia 1: 1–24. [Google Scholar]
  • 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. [CrossRef] [EDP Sciences] [Google Scholar]
  • Hellmann JJ, Byers JE, Bierwagen G, Dukes JS. 2008. Five potential consequences of climate change for invasive species. Conserv Biol 22: 534–543. [CrossRef] [PubMed] [Google Scholar]
  • Jueg U, Zettler ML. 2004. Die Molluskenfauna der Elbe in Mecklenburg-Vorpommern mit Erstnachweis der Grobgerippten Körbchenmuschel Corbicula fluminea (O. F. Müller 1756). Mitteilungen der Naturforschenden Gesellschaft Mecklenburg 41: 85–89. [Google Scholar]
  • Kinzelbach R. 1991. Die Körbchenmuscheln Corbicula fluminalis, Corbicula fluminea und Corbicula fluviatilis in Europa (Bivalvia: Corbiculidae). Mainzer Naturwissenschaftliches Archiv 29: 215–228. [Google Scholar]
  • Kottelat M, Freyhof J. 2007. Handbook of European freshwater fishes. Kottelat, Cornol & Freyhof, Switzerland and Berlin, 646 p. [Google Scholar]
  • Li F, Liao T-Y., Arai R, Zhao L. 2017. Sinorhodeus microlepis, a new genus and species of bitterling from China (Teleostei: Cyprinidae: Acheilognathinae). Zootaxa 4353: 69. [PubMed] [Google Scholar]
  • Lopes-Lima M, Sousa R, Geist J, Aldridge DC, Araujo R, Bergengren J, Bespalaya Y, Bódis E, Burlakova L, Van Damme D, Douda K, Froufe E, Georgiev D, Gumpinger C, Karatayev A, Kebapçi Ü, Killeen I, Lajtner J, Larsen BM, Lauceri R, Legakis A, Lois S, Lundberg S, Moorkens E, Motte G, Nagel KO, Ondina P, Outeiro A, Paunovic M, Prié V, von Proschwitz T, Riccardi N, Rudzīte M, Rudzītis M, Scheder C, Seddon M, Şereflişan H, Simić V, Sokolova S, Stoeckl K, Taskinen J, Teixeira A, Thielen F, Trichkova T, Varandas S, Vicentini H, Zajac K, Zajac T, Zogaris S. 2017. Conservation status of freshwater mussels in Europe: state of the art and future challenges. Biol Rev 921: 527–607. [Google Scholar]
  • Mouthon J. 1981. Sur la presence en France et au Portugal de Corbicula (Bivalvia, Corbiculidae) originaire d'Asie. Basteria 45: 109–116. [Google Scholar]
  • Nentwig W, Bacher S, Kumschick S, Pyšek P, Vilà M. 2018. More than “100 worst” alien species in Europe. Biol Invasions 20: 1611–1621. [Google Scholar]
  • Nesemann H. 2018. Corbicula largillierti im Oberrhein (Hessen), neu erkannt in Deutschland. Mitteilungen der Deutschen Malakozoologischen Gesellschaft 98: 65–68. [Google Scholar]
  • Okazaki M, Naruse K, Shima A, Arai R. 2001. Phylogenetic relationships of bitterlings based on mitochondrial 12S ribosomal DNA sequences. J Fish Biol 58: 89–106. [CrossRef] [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]
  • 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 Evol Biol 19: 788–796. [CrossRef] [PubMed] [Google Scholar]
  • Reichard M, Liu H, Smith C. 2007a. The co-evolutionary relationship between bitterling fishes and freshwater mussels: insights from interspecific comparisons. Evol Ecol Res 92: 239–259. [Google Scholar]
  • Reichard M, Przybylski M, Kaniewsk P, Liu, H, Smith C. 2007b. A possible evolutionary lag in the relationship between freshwater mussels and European bitterling. J Fish Biol 70: 709–725. [CrossRef] [Google Scholar]
  • Rey P, Ortlepp J. 1997. Koordinierte biologische Untersuchungen im Hochrhein 1995; Makroinvertebraten. Schriftenreihe Umwelt 283: 115 p. [Google Scholar]
  • Schniebs K, Winkelmann C. 2001. Erste Nachweise der Körbchenmuschel Corbicula fluminea in Sachsen. Lauterbornia 41: 53–54. [Google Scholar]
  • Smith C, Rippon K, Douglas A, Jurajda P. 2001. A proximate cue for oviposition site choice in the bitterling (Rhodeus sericeus). Freshw Biol 46: 903–911. [CrossRef] [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]
  • Sousa R, Bogan AE, Gonçalves DV, Lajtner J, Prié, V, Riccardi, N, Lopes-Lima M. 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]
  • Sousa R, Antunes C, Guilhermino L. 2008. Ecology of the invasive Asian clam Corbicula fluminea (Müller, 1774) in aquatic ecosystems: an overview. Ann Limnol 44, 2: 85–94. [CrossRef] [EDP Sciences] [Google Scholar]
  • Titttizer T, Taxacher M. 1997. Erstnachweis von Corbicula fluminea/fluminalis (Müller 1774) (Corbiculidae, Mollusca) in der Donau. Lauterbornia 31: 103–107. [Google Scholar]
  • Turner H, Kuiper JGJ, Thew N, Bernasconi R, Rüetschi, J, Wüthrich M, Gosteli M. 1998. Fauna Helvetica 2: Atlas der Mollusken der Schweiz und Liechtensteins. Eidgenössische Forschungsanstalt für Wald, Schnee und Landschaft: 527 p. [Google Scholar]
  • Van Damme D, Bogutskaya N, Hoffmann R, Smith C. 2007. The introduction of the European bitterling (Rhodeus amarus) to west and central Europe. Fish Fish (Ox) 8: 79–106. [CrossRef] [Google Scholar]
  • Werner S, Mörtl M. 2004. Erstnachweis der Fluss-Körbchenmuschel Corbicula fluminea im Bodensee. Lauterbornia 49: 93–97. [Google Scholar]
  • Wiepkema PR. 1961. An ethological analysis of the reproductive behaviour of the bitterling (Rhodeus amarus Bloch). Arch Neerl Zool 14: 103–199. [Google Scholar]
  • Wilke H-J. 2007. Erstnachweis von Corbicula fluminea in der Hohensaaten-Friedrichsthaler-Wasserstraße/Oder (Brandenburg). Lauterbornia 59: 63–65. [Google Scholar]

Cite this article as: Pfeiffer M, Mildner M, Günter CP, Leschner M. 2025. The Asian clam Corbicula fluminea, an accidental host for the European bitterling Rhodeus amarus. Knowl. Manag. Aquat. Ecosyst., 426, 4. https://doi.org/10.1051/kmae/2024026.

All Figures

thumbnail Fig. 1

Bitterling embryo that has not developed further in the gills of Corbicula fluminea (photo by M. Pfeiffer).
In the text
thumbnail Fig. 2

Bitterling embryo that has not developed further in the gills of Corbicula fluminea (photo by M. Pfeiffer).
In the text
thumbnail Fig. 3

Gelatinous oval structures (bitterling eggs or fat globules) in the gills of Corbicula fluminea (photo by M. Pfeiffer).
In the text

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