Plankton Benthos Res 12(2): 123–128, 2017 Plankton & Benthos Research © The Japanese Association of Benthology

Long-anticipated new records of an ectosymbiotic branchiobdellidan and an ostracod on the North American red swamp crayfish, Procambarus clarkii (Girard, 1852) from an urban stream in Tokyo, Japan

1, 2 3 Akifumi Ohtaka *, Stuart R. Gelder & Robin J. Smith

1 Department of Natural Science, Faculty of Education, Hirosaki University, Hirosaki, Aomori 036-8560, Japan 2 Department of Math-Science, University of Maine at Presque Isle, 181 Main Street, Presque Isle, Maine 04769-2888, U.S.A. 3 Lake Biwa Museum, Kusatsu, Shiga 525-0001, Japan Received 16 January 2016; Accepted 16 March 2017 Responsible Editor: Shigeaki Kojima

Abstract: Two North American ectosymbionts, a cambarincolid branchiobdellidan, Cambarincola mesochoreus, and an entocytherid ostracod, Ankylocythere sinuosa, were recorded for the first time in Japan, on the red swamp crayfish, Procambarus clarkii, from an urban stream in Tokyo. Although the immediate origin of the hosts and ectosymbionts is unknown, it is highly probable that they were recently imported into Japan. A single C. mesochoreus was also found on an alien atyid , Neocaridina davidi, in the same stream as the infected Pr. clarkii. This demonstrates the possibil- ity that C. mesochoreus may find this shrimp to be a new potential host.

Key words: alien symbionts, Ankylocythere sinuosa, Cambarincola mesochoreus, Japan, Procambarus clarkii

on other crustaceans such as , isopods and amphipods Introduction (Hart & Hart 1974). Freshwater crayfishes have many symbionts ranging The red swamp crayfish, Procambarus clarkii (Girard, from viruses to metazoans (Edgerton et al. 2002; Longshaw 1852), is native to northeast Mexico and south-central 2011). Some crayfish are of commercial value, USA, but has now been introduced onto every continent, and they have long been recognized as unintentional in- except Australia and Antarctica, for aquaculture and the troducers of their symbionts to other continents follow- pet industry (Huner 2002). In its native region, Pr. clarkii ing translocations. Of their many symbionts, two notable is a host to branchiobdellidans (Gelder et al. 2002) and groups are the ectosymbiotic clitellate in the order entocytherids (Hart & Hart 1974). However, surprisingly, Branchiobdellida, and the crustacean ostracod family En- there are only a few records of their endemic ectosym- tocytheridae. Branchiobdellidans have a disjunct Holarctic bionts in the many reported alien locations. Among the distribution, consisting of North and Central America, Eu- branchiobdellidans, Cambarincola mesochoreus Hoff- rope and East Asia, and although the worms live mainly on man, 1963 was found in northern Italy (Gelder et al. 1994, astacoidean crayfish, a few species have used freshwater 1999) and southwest France (J-F Parpet unpublished data), crabs, , and isopods as hosts (Gelder & Williams whereas this species and Cambarincola pamelae Holt, 2015). There are, in total, 200 species of entocytherids, 1984 were observed to have relocated onto the blue , which have been reported mainly from North and Central Rathbun,1896, in the Chesapeake Bay, America, Europe, and Australia, with additional isolated Maryland, USA (Gelder & Messick 2006). Reports of records from Hawaii, Japan, Papua New Guinea, India, transported entocytherids are also sparse, and limited to New Zealand, and South Africa (Mestre et al. 2014). Al- two species in Spain, France, Germany, the Netherlands, though their primary host is crayfish, they are also found the UK, the Czech Republic, and Japan (Smith & Kami- ya 2001; Aguilar-Alberola et al. 2012; Mestre et al. 2013; * Corresponding author: Akifumi Ohtaka; E-mail, ohtaka@hirosaki-u. Huys et al. 2014). ac.jp Pr. clarkii was introduced into Japan almost 90 years 124 A. Ohtaka et al. ago for commercial reasons, and its history in Japan has on the host. In addition, alien atyid shrimps, Neocaridina been traced through archival records and oral reports davidi (Bouvier, 1904), were examined from the same lo- (Kawai et al. 2003; Kawai & Kobayashi 2006, 2011). Re- cations as the crayfish for any ectosymbionts. search has concluded that Pr. clarkii was introduced only once into Japan in 1927, to provide food for rearing bull- Materials and Methods frogs, Rana catesbeiana Shaw, 1802 (Kawai et al. 2003). The crayfish were purchased in Louisiana, USA, placed Five specimens of Pr. clarkii were collected by Mr. in beer barrels, and transported on the mail ship “Taiyo- Norio Kobayashi between October 21 and 24, 2015 from Maru” from New Orleans, Louisiana, USA to Yokohama each of the following three locations: Site 1 (35°42′27.34″N, Port, Kanagawa Prefecture, Japan. Approximately 100 139°35′58.54″E), Site 2 (35°41′56.57″N, 139°37′13.57″E), crayfish started the journey alive, but only about 20 in- located 2 km downstream of Site 1, in the Zenpukuji-gawa dividuals survived (Kawai et al. 2003). These individu- Stream, and Site 3 (35°40′31.22″N, 139°37′36.38″E) in the als were taken to a farm in Kamakura City, Kanagawa neighboring Kanda-gawa Stream, all of which are located Prefecture, Japan, and released into ponds where they in Suginami-ku, an urban area of Tokyo, in the Arakawa successfully reproduced. Within 30 years, they had been River basin (Fig. 1). Crayfish were collected and immedi- transported all over the Japanese archipelago (Kawai et ately placed in individual containers filled with 80% etha- al. 2003; Kawai & Kobayashi 2011). This most likely ac- nol solution. In the laboratory, carapace length (measured counts for the low genetic diversity found in the current from ocular socket to the posterior margin of carapace) and Japanese Pr. clarkii population as demonstrated by the un- sex were recorded for each crayfish, and all ectosymbionts published works of K. Uehara and N. Ushio et al. Given on the crayfish and those in the containers’ bottom de- the harsh conditions in the barrels during transportation, bris were counted. In addition, ten specimens of the alien it is almost certain that all ectosymbionts were killed en shrimp, Neocaridina davidi (Bouvier, 1904) sensu Klotz route, even though a few crayfish did survive (Kawai & et al. (2013) were collected from each site and preserved Kobayashi 2011). This assessment was supported by the in the same manner, prior to the removal of any ectosym- lack of any record of branchiobdellidans or entocytherids bionts. on Pr. clarkii following the 1927 introduction. Branchiobdellidans were dehydrated whole in 100% During benthological studies of urban streams in Tokyo ethanol, cleared in methyl salicylate, mounted in Canada in 2015, Mr. N. Kobayashi found many branchiobdellidans balsam on microscope slides, and identified using Gelder and entocytherids on Pr. clarkii. Such a duel ectosymbiotic et al. (1994). Entocytherids were dissected in glycerol, infection on this crayfish species had not been previously mounted on microscope slides and identified using Hart & recorded in Japan. The present paper identifies the ecto- Hart (1974) and Aguilar-Alberola et al. (2012). One mount- symbionts and records their composition and abundance ed specimen of a branchiobdellidan and that of a copulat-

Fig. 1. Map of sampling sites for the red swamp crayfish Procambarus clarkii in an urban area of Tokyo. Symbionts on Procambarus clarkii from Japan 125 ing couple of entocytherid have been deposited in the In- Discussion vertebrate Collection of the Hokkaido University Museum, Sapporo, Japan (ICHUM 5337 and 5338). The present study records Cambarincola mesochoreus and Ankylocythere sinuosa from Japan for the first time. It is unlikely that these ectosymbionts had been overlooked Results in the past, as researchers have repeatedly searched for any Both male and female crayfish were collected, and cara- ectosymbionts when Pr. clarkii were examined in Japan pace lengths ranged from 22 to 37 mm. The size of these (Kawai & Kobayashi 2006, 2011; Ohtaka 2010; Smith, un- crayfish, based on carapace length, showed no significant published). Except for our report of the alien Pr. clarkii, differences by site (ANOVA, P>0.05). All of the bran- there has been no record of either native or alien species chiobdellidans recovered were Cambarincola mesochoreus of crayfish in the Tokyo area, making it almost certain Hoffman, 1963, and all of the entocytherids were Ankylo- that they and their ectosymbionts were introduced recently cythere sinuosa (Rioja, 1942) (Fig. 2). Branchiobdellidans, as an assemblage into Japan. Finding a single juvenile C. both mature and juveniles, along with a large numbers of mesochoreus on an atyid shrimp at a site surrounded by cocoons were found on all crayfish from sites 1 and 2 in a large population of adult branchiobdellidans on crayfish the Zenpukuji-gawa Stream, wherein the maximum inten- indicates the worms were not attracted to the shrimp as sity was 555 (Table 1). Adult and juvenile entocytherids alternative hosts, but neither were they repelled. Further were also found on all crayfish collected from the Zenpu- studies are required to determine if C. mesochoreus would kuji-gawa Stream, except for one juvenile at site 2; their use an atyid shrimp as an acceptable host, particularly in highest observed intensity was 21 (Table 1). No significant the absence of crayfish. However, based on current in- correlations were found between the carapace length of formation, there is no justification to doubt that the two Pr. clarkii and the numbers of branchiobdellidans or en- ectosymbionts arrived in Japan on recently imported Pr. tocytherids (Spearman’s correlation coefficient, P>0.05). clarkii. In contrast, neither branchiobdellidans nor entocytherids International trade of live crayfish and shrimp is grow- were found on any crayfish from site 3 in the Kanda-gawa ing rapidly in the aquarium industry, owing to their popu- Stream. larity as domestic pets (Faulkes 2015; Patoka et al. 2015, From the 30 atyid shrimp of N. davidi that were collect- 2016). Although several countries have imposed restric- ed, only one individual from site 1 was found to carry one tions on the importation and transport of crustaceans, juvenile C. mesochoreus, whereas no entocytherids were North American crayfish continue to be traded between found. However, this is the first record of C. mesochoreus Europe and East and Southeast Asia (Kawai, person- on a shrimp host. al communication). Because of the complicated and of-

Fig. 2. Fixed-slide specimen of Cambarincola mesochoreus (A; ICHUM 5337), and Ankylocythere sinuosa (B; ICHUM 5338) from Procambarus clarkii collected from Site 1 in the Zenpukuji-gawa Stream, Suginami-ku, Tokyo, on 21st October 2015.

Table 1. Summary in occurrence of ectosymbionts on Procambarus clarkii from Tokyo in Oct. 2015. Cambarillcola mesochoreus Ankylocythere sinuosa Locality No. Prevalence % Mean intensity* (range) Prevalence % Mean intensity* (range) Site 1; Zenpukuji-gawa Strcam 5 100 136.2 (66–222) 100 6.8 (1–21) Site 2; Zenpukuji-gawa Strcam 5 100 182.2 (42–555) 80.0 8.0 (1–16) Site 3; Kanda-gawa Stream 5 0 0 0 0 * mean number of ectosymbionts per infected hosts 126 A. Ohtaka et al. ten inconsistent international regulations for transporting jita et al. 2010; Tanaka et al. 2016). Branchiobdellidans crustaceans, it is highly unlikely that Pr. clarkii and their have shown a surprising degree of flexibility, with spe- ectosymbionts found in Tokyo can be traced through docu- cies adopting either an alien crayfish host from a different mentation back to their point of origin. However, it could continent (Ďuriš et al. 2006; Vogt 1999) or a non-crayfish be possible to trace the histories of host and ectosymbionts crustacean host altogether (Gelder & Messick 2006). by studying and comparing their DNA markers with previ- Five species of entocytherids have been reported on ously published sequences. Pr. clarkii (Hart & Hart 1974), but only one of these, A. As the alien host and ectosymbiont association has only sinuosa, has been found in invasive populations of Pr. recently been found in two of the three closely situated clarkii, namely in Spain, England and the Czech Repub- locations, it might be too early to discuss the possible ex- lic (Aguilar-Alberola et al. 2012; Mestre et al. 2013; Huys tent of the invasion. However, because populations of both et al. 2014). Another species of invasive entocytherid, ectosymbionts contain juveniles and adults, plus bran- Uncinocythere occidentalis (Kozloff and Whitman 1954), chiobdellidans cocoons, they are well established on the was introduced to Japan through the translocation of Pa. crayfish at Sites 1 and 2. The absence of ectosymbionts on leniusculus (Smith & Kamiya 2001), the UK (Huys et al. a nearby population of crayfish is not unusual, although an 2014), Spain, France, the Netherlands and Germany (Mes- explanation for such a phenomenon is not known. tre et al. 2013). Commercial freshwater crayfish from the northern In the review of entocytherid ostracods by Hart & hemisphere have generally consisted of the signal crayfish Hart (1974), 40 species/subspecies were listed as hosts of Pacifastacus leniusculus (Dana, 1852) and the red swamp Ankylocythere sinuosa: Procambarus (25 species/subspe- crayfish Pr. clarkii from North America, and the narrow- cies), Oroconectes (six species), Cambarus (four species) clawed crayfish Astacus leptodactylus Eschscholtz, 1823 Fallicambarus (two species), Cambarellus (one species), from Europe (Souty-Grosset et al. 2006). The endemic Faxonella (one species) and Pacifastacus (one species). branchiobdellidans on these and other commercial North However, most entocytherid species have far fewer known American crayfishes were summarized by Gelder (2004), hosts, with approximately 50% being known from only and therefore these species would be expected as potential one or two host species (Mestre et al. 2014). The low host alien ectosymbionts when their hosts were translocated. specificity of A. sinuosa suggests a high propensity of Reports of alien branchiobdellidans in Japan are not new this particular species to translocate to different host spe- (Niwa et al. 2005; Ohtaka et al. 2005), and a recent inter- cies, as demonstrated by its ability to translocate from Pr. est in branchiobdellidans has shown a larger number of clarkii to a native European crayfish (Austropotamobius introductions than previously thought (Gelder et al. 2012; italicus (Faxon, 1914)) in laboratory experiments (Mestre Vedia et al. 2014). Pacifastacus leniusculus accounts for et al. 2015). Additionally, A. sinuosa is reported to be able four alien species (Cambarincola gracilis Robinson, 1954, to survive for up to 10 months in the absence of a host, al- Cambarincola okadai Yamaguchi, 1933, Xironogiton vic- though successful reproduction appears to take place only toriensis Gelder and Hall, 1990, and Sathodrilus attenu- when a host is present (Young 1971). Considering the low atus Holt, 1981) being introduced into Europe (Gelder et host specificity and ability to survive extended periods off- al. 2012). The last three species have also been reported host, the potential invasiveness of this species in Japan following Pa. leniusculus introductions into Japan (Yama- must be considered high. guchi 1933; Ohtaka et al. 2005). Although Pr. clarkii has Studies on populations of A. sinuosa collected from in- been more widely introduced around the world than Pa. vasive Pr. clarkii in Spain revealed that higher water tem- leniusculus, reports of its endemic branchiobdellidans are peratures had a positive impact and higher conductivity a unexpectedly few. These include C. mesochoreus in north- negative impact on population sizes; dissolved oxygen lev- ern Italy (Gelder et al. 1994, 1999) and southwest France els had no significant effect (Castillo-Escrivá et al. 2013). (J-F Parpe, unpubished data), while this species and Cam- Potentially suitable areas for A. sinuosa in Europe were barincola pamelae were observed in central California, subsequently identified with ecological niche modelling USA (Gelder 1991). The same two species on Pr. clarkii and concluded that A. sinuosa is mainly restricted by its were released into areas adjacent to the Chesapeake Bay, own limitations to minimum temperatures in western and Maryland, USA, where the interactions of swamp crayfish northern Europe and higher seasonal precipitation in cir- with blue crabs resulted in the branchiobdellidans trans- cum-Mediterranean areas (Mestre et al. 2013). Climatically ferring to the crabs (Gelder and Messick 2006). A similar suitable areas for A. sinuosa in Europe were predicted to situation has also been reported on the northern coast of be smaller than those of its host Pr. clarkii in these areas the Gulf of Mexico (Overstreet 1983). (Mestre et al. 2013). Therefore in Japan, the area that A. Branchiobdellidans are known to find some non-crayfish sinuosa could potentially invade may not correspond en- crustaceans as acceptable hosts, mainly south of the cray- tirely to the distribution of its host. However, the discovery fish’s southern distribution limit in Central America (Holt of A. sinuosa in Britain, outside of its postulated suitable 1973; Gelder et al. 2002), southern China (Liang 1963; areas in Europe (Huys et al. 2014), suggests that the areas Ohtaka et al. 2012), and central and southern Japan (Fu- of future expansion of this species may be difficult to pre- Symbionts on Procambarus clarkii from Japan 127 dict. lidans (Annelida: ). Can Field-Nat 105: 390–391. Given the location in Tokyo of the alien Pr. clarkii and Gelder SR (2004) Endemic ectosymbiotic branchiobdellidans its ectosymbionts, it is most likely that the crayfish either (Annelida: Clitellata) reported on three “export” species of escaped or were discarded after being purchased as pets North American crayfish (Crustacea: Astacoidea). Freshwat or fishing bait. 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