Knowl. Manag. Aquat. Ecosyst.
Number 425, 2024
Anthropogenic impact on freshwater habitats, communities and ecosystem functioning
Article Number 5
Number of page(s) 5
Published online 26 February 2024

© T. Konno et al., published by EDP Sciences, 2024

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Recently, occurrences of native symbionts (including parasites) in introduced species (Kelly et al., 2009) or non-native symbionts in native species (Lymbery et al., 2014) have been reported. Because the presence or absence of symbionts often affects host behaviour and survival (Adamo, 2002; Prenter et al., 2004; Poulin, 2010; James et al., 2015), identifying secondary, often overlooked invasions and host shifts is important for the conservation and management of native ecosystems.

Some crayfish species are some of the most successful invaders due to anthropogenic translocations, and their range continues to expand globally (Lodge et al., 2012; Twardochleb et al., 2013). Crayfish in the Northern Hemisphere often carry branchiobdellidans (Annelida: Clitellata: Branchiobdellida), ectosymbiotic crayfish worm (Gelder and Williams, 2016), and new symbiotic relationships have been created as a result of translocations of the host crayfish and/or secondary invasions of the symbionts (Gelder, 2020). In Europe, several studies have documented the occurrence of native branchiobdellidans on invasive crayfish (Gelder et al., 1999; Vogt, 1999; Ďuriš et al., 2006; Blaha et al., 2018). In North America, three species of native branchiobdelidans were found on non-native crayfish, where the native Signal Crayfish, Pacifastacus leniusculus (Dana 1852), and the non-native Snake River Pilose Crayfish, Pacifastacus connections (Faxon, 1914), are sympatric (Williams and Weaver, 2021). On the other hand, there is only one published report on the transfer of branchiobdellidans from non-native crayfish to native crayfish (Parpet and Gelder, 2020). Host transfer of branchiobdellidans typically occurs during aggressive or mating behaviour among host individuals (Hunt et al., 2018) or by indirect transmission via substrates (Gelder and Williams, 2016).

Pacifastacus leniusculus has been extensively introduced across Japan (Nakata et al., 2010; Usio et al., 2016), and secondary introductions of its branchiobdellidans have also been observed (Kawai et al., 2004; Ohtaka et al., 2005; Nakata et al., 2010). Pacifastacus leniusculus is a cold-water crayfish and new populations have been widely established in Hokkaido, one of the coldest regions of Japan (Usio et al., 2016). The native and endangered Japanese Crayfish, Cambaroides japonicus (De Haan, 1841), is present in Hokkaido, but P. leniusculus is competitively dominant and has displaced C. japonicus in some sites (Kawai et al., 2002; Nakata et al., 2004). While direct interactions between the native and non-native crayfish have been suggested (Usio et al., 2001; Nakata and Goshima 2003), no evidence has been reported regarding the transfer of native and non-native crayfish worms to each crayfish species.

In Japan, 11 valid species of branchiobdellidans have been found on C. japonicus (Ohtaka et al., 2023; Ohtaka et al., 2024). The Red List published by the Japanese Ministry of the Environment lists all these species as being at a higher risk of extinction than their host, C. japonicus (Ministry of the Environment, 2020). Biological invasions have a serious impact not only on C. japonicus but also on its branchiobdellidans. In the Atsubetsu River in Sapporo, Japan (mainstem, Site 1, Fig. 1), we found suspected Japanese and North American branchiobdellidans on two individuals of P. leniusculus collected on August 5, 2021. Therefore, we investigated the prevalence and species composition more detail. We also examined branchiobdellidans on native C. japonicus. We particularly focused if a transfer of the symbionts occurred between the two host species.

We performed this study using the following methods. We collected P. leniusculus in the Atsubetsu River on August 30, 2022 (Fig. 1, Tab. 1), using a cage trap, hand nets and backpack electrofisher (model 20B; Smith-Root Inc., Vancouver, WA, USA). Sardine heads and entrails were used as bait in the cage trap (50 cm [L] × 25 cm [W] × 25 cm [H], 2 mm mesh), and 100 V was used for electric fishing. The post-orbital carapace length, wet weight and sex of 14 captured P. leniusculus were recorded (Tab. 2), and each individual was fixed in 80% ethanol. Later, the fixative ethanol from each sample container was filtered through a 63 μm mesh, and the number of branchiobdellidans was counted. The species of all obtained branchiobdellidans were identified according to Yamaguchi (1934) and Holt (1981). Although Cirrodrilus cirratus Pierantoni, 1905 and Cirrodrilus uchidai (Yamaguchi, 1932) were described as separate species (Pierantoni, 1905; Yamaguchi, 1932; Gelder, 1987), recent studies have argued that the overlap in taxonomic traits between the two species makes it doubtful whether they are valid species or species complex (Ohtaka et al., 2023). Therefore, in this study, we did not distinguish between the two species and considered C. cirratus complex.

From August 2021 to July 2022, we also surveyed the population of C. japonicus at four sites (tributaries, Site 2-5) near the site where P. leniusculus was found (Fig. 1; Tab. 1). Hand collecting was conducted for 30-100 minutes per site, with 2-3 people searching under stones and trees. Captured C. japonicus were temporarily submerged in 70% ethanol for a short time (30 s) to remove branchiobdellidans. This method can remove more than 90% of the attached branchiobdellidans without the death or growth reduction of the host crayfish (T. Konno, in preparation). The collected branchiobdellidans were preserved in 70% ethanol and brought back to the laboratory, and the species were identified according to Yamaguchi (1934). Host C. japonicus was rereleased at the site where they were captured.

From both surveys, we obtained the following results. A total of 75 individuals of P. leniusculus were captured in the mainstem of the Atsubetsu River (Site 1), while no C. japonicus was found in the mainstem (Fig. 1, Tab. 1). Individual information on 14 captured P. leniusculus and the number of branchiobdellidans from each host are summarised in Table 2. Two crayfish supported more C. cirratus complex than S. tetrodonta. The maximum number of C. cirratus complex on the host was 232, which was close to the number of S. tetrodonta on the same host individual.

Cambaroides japonicus was found in four small tributaries (Site 2-5) near the site of the mainstem (Site 1) where P. leniusculus was captured (Fig. 1, Tab. 1). The density of C. japonicus was very low in every site we surveyed. No sympatric sites were observed between the native and non-native crayfish. Japanese branchiobdellidans were found in three populations of C. japonicus (Site 2-4), and all were identified as Cirrodrilus digitatus (Pierantoni, 1906) based on the morphology of the jaws.

This is the first record of a native branchiobdellid species being found on a non-native host in Japan. The symbiotic relationships of branchiobdellidans and P. leniusculus have been studied at 21 sites in Japan, but only historically associated ectosymbionts, S. tetrodonta and Xironogiton victoriensis Gelder and Hall, 1990, were detected (Kawai et al., 2004; Ohtaka et al., 2005; Nakata et al., 2010). One of the reasons why Japanese branchiobdellidans have not been found on P. leniusculus in past studies could be that it has been a long time since crayfish was introduced (e.g., 70–80 yr after initial introduction (Usio et al., 2007)). For example, Ďuriš et al. (2006) reported that four species of native branchiobdellidans – Branchiobdella italica Canegallo, 1923, Branchiobdella pentadonta Whitman, 1882, Branchiobdella parasita (Braun, 1805) and Branchiobdella hexadonta Grube, 1883 – were found on the non-native crayfish Faxonius limosus (Rafnesque, 1817) in 2001. However, only B. italica was observed in 2003, and no branchiobdellidans were detected in subsequent surveys. This suggests that novel symbiotic relationships between crayfish and branchiobdellidans may not last long. The population of P. leniusculus was established in the Atsubetsu River system relatively recently (less than 10 yr ago, K. Tanaka, unpublished data). Not much time has been passed since the first interactions between the non-native and native crayfish, and the branchiobdellidans population might have been transiently supported by P. leniusculus.

No individuals of C. cirratus complex were found on C. japonicus during this study. Because we investigated only four populations of C. japonicus, exploring more sites in this river system may identify the source population of the branchiobdellidans transmitting to P. leniusculus from C. japonicus. However, the very low densities of C. japonicus in the studied area suggest that the host population from which the source of C. cirratus complex might have been already extinct, or that C. cirratus complex became extinct before C. digitatus due to the decline of host crayfish. Hinosawa et al. (2023) estimated that C. japonicus in northern Honshu Island in Japan will be largely extinct by 2050, suggesting that C. japonicus is at a greater risk of extinction than previously thought. In Hokkaido, population extinction has already been confirmed at several sites (Kawai et al., 2002; Nakata et al., 2004), and the estimation in Hinosawa et al. (2023) could apply to Hokkaido populations as well. Since symbionts are known to go extinct earlier than their hosts in some cases (Rózsa and Vas, 2005; Lafferty, 2012), it is highly possible that the extinction of C. cirratus complex occurred earlier than that of C. japonicus in the Atsubetsu River system.

Japanese branchiobdellidans are specifically ectosymbiotic with C. japonicus and could only live in lakes or small streams near water sources inhabited by this host. On the other hand, P. leniusculus can inhabit mainstems, and C. cirratus complex could permanently use P. leniusculus as a host; they have expanded their habitat range to mainstem reaches, where it was originally difficult for them to inhabit. This finding is a unique example of a native symbiont that would normally be lost along with its native host as a result of biological invasions avoiding extinction by shifting hosts to the invasive species as well as expanding the living area of the river due to the high dispersal ability of the new host.

When native endangered symbiotic species transfer to non-native hosts, the removal of non-native species means driving the endangered species to extinction at the hands of humans. This finding suggests that there is a dilemma between the extermination of non-native species and the protection of symbionts caused by an overlooked host shift. Nevertheless, the main goal of the management of introduced species is to eradicate or reduce their population sizes, which leads to the restoration of native biodiversity (Hulme, 2006; Prior et al., 2017). A proper understanding of complex ecosystems includes symbiotic organisms and clarifying on what to conserve and what to eliminate, sometimes at the expense of native species, is important for ecosystem management.


We are grateful to Dr. Akifumi Ohtaka (Hirosaki University) for teaching us the methods of branchiobdellidan identification. The authors also thank to Nobuhiro Sato (Sapporo Salmon Museum), Hiroki Terashima, Ayami Ohkuma (Sapporo Environmental Bureau), Wei Jia (Hokkaido University), Kazunobu Sakamaki, Satoshi Noguchi, Genji Takemon (Civil Engineering & Eco-Technology Consultants Co., Ltd.) and Masato Kataoka (Sapporo Maruyama Zoo) for supporting our crayfish sampling.


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Cite this article as: Konno T, Tanaka K, Koizumi I. 2024. Host shift to non-native species or ecological dead end? Endangered branchiobdellidans (Annelida: Clitellata) found on introduced Signal Crayfish in Japan. Knowl. Manag. Aquat. Ecosyst., 425, 5.

All Tables

Table 1

Number of crayfish captured at each site and the species of branchiobdellidans in the Atsubetsu River system.

Table 2

Number of branchiobdellidans on individuals of P. leniusculus from Site 1 in the Atsubetsu River system.

All Figures

thumbnail Fig. 1

Crayfish were captured in the Atsubetsu River system at the numbered sites. The collection area is indicated by a rectangle on the map of Hokkaido Island; insert bottom right.

In the text

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