JapaneseJapaneseSociety Society ofSystematicof Systematic Zoology

Species Diversity, 2006, 11, 359-365

New Record of Propappus volki (Annelida: Clitellata: Propappidae) from

Takaaki Torii

ll)Et`I CDnsuttants inc., 1334-5Riemon, Oigawa. Shida, Shizuoka, 421-CL212 .lapan E-mail: [email protected]

(Received 1 November 2005; Accepted 11 July 2006)

A species of freshwater oligochaete, PrQpoppus volki Michaelsen, 1916, is newly recorded from sand and gravel bottoms of several unpolluted streams in , Japan. The present material agrees well with the previous de- scriptiens of this species except that the spermathecal ampulla is shorter

and the proboscis is more elomgate than those described earlier. This is the first record of the family Propappidae Coates, 1986 (New Japanese name: Ko- himemimizu-ka) and the genus Prql)qppus Miehaelsen, 1905 (New Japanese narne: Ko-himemimizu-zoku) in Japan. It provides evidence that the oligochaete fauna in Japan is more closely related to the Holarctic than to

the Sino-Indian zoogeographical region, PrQpqppus votici can be regarded as a good bio-indicator fbr unpolluted water. Key Words: oligochaetes, Clitellata, Propappidae, Propappus volki, new

record, Japan.

Introduction

The genus PrQpqppus was erected by Michaelsen (1905) fbr PrQpappus gtandu- losus Michaelsen, 1905 in the family Enchytraeidae. Afterwards Coates (1986) cre- ated the family Propappidae for the single genus PrQpappus on the basis of a unique combination of setal and genital characteristics distinctly different from those ef the Enchytraeidae. Only three species of Propampus have so far been described from freshwater habitats of the Palaearctic region, Among them, Prqpqppus glandulosus has been recorded from Lake Baikal and the Angara and Yenisey Rivers in central Russia (Michaelsen 1905; Coates 1986), PrQpqppus arhynchotus Sokolskaja, 1972 has been recorded only from the Kamchatka Peninsula and Amur basin in the Russian Far East (Timm 1994, 1999a). On the other hand, another species, PrQpQppus volki Michaelsen, 1916 originally described by Michaelsen (l916a) from Hamburg, Ger- many, has been recorded from numerous localities extending from western Europe through the Russian Far East (Bird 1982; Coates 1986; Timm et al. 1996) as well as the St. Lawrence River in Canada (K. A. Coates, pers. comm,), In the course of benthological surveys in Japanese rivers by the author and colleagues, many propappid worms were found, as the such records from this country, They were identified as R volki and are described in the present paper,

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Materials and Methods

Speeimens were collected from four rivers in central Japan, Live specimens

were fixed in either 10t)i, formalin or 709I] ethanol solutions, after being anes-

thetized in low concentrations of ethanol, when available. Specimens mounted whole on slides in Canada balsam were examined after having been dehydrated in a graded series of ethanol and water solutions, and then cleared in methyl salicy- late. The specimens examined are stored at IDEA Consultants Inc., Shizuoka, Japan, except fbr one slide which has been deposited in the Division ef Biologieal Science, Graduate School of Seience, University (ZIHU). At the collec- tien site of P. volki in the Tooyama River, the composition of the coexisting ben- thic macroinvertebrates was examined.

Taxonomy

PrQpmppus votki Michaelsen, 1916 [New Japanese name: Nagahana-ko-himemimizu] (Fig, 1)

Prcrpqppus volki Michaelsen, 1916: 51-55; Cernosvitov 1937: 273, figs 1, 2; Wachs 1967: 322, fig. 9; Bird 1982: 67-75; Coates 1986: 423-425, fig, 3; Timm et al. 1996: 27. See Coates (1986) for other synonyms and references.

Material exarnined. Thirty mature specimens, , Kodako, Kamiyahagi Town, , Japan (35o15'39"N, 137e29'24"E), 11 February 2004, T. Torii coll, (1 mature specimen registered as ZIHU 3176); 1 mature and 2 im- mature specimens, Tooyama River, Minamishinano Village, Shimoina County, , Japan (35023'13"N, 138001'41"E), 8 August 2004, T. Torii coll.; 1 mature and 10 immature specimens, , Hodaka Town, Kitaazumino County, Nagano Prefecture, Japan (36022'21.8"N, 137S52'49,2"E), 10 December 2002, C. Sato coll.; 3 mature specimens, , Okutsu Town, Okayama Prefec- ture, Japan (35"10'46"N, 133054'21"E), 21 March 2004, T, Shimizu colL Description of new material. Body white or pale yellowish when living. Fol- Iowing measured numerical values all taken from fixed mature specimens, Body length 5.4-7.8mm (rnean± SD: 6.6± O.8, n-18), with 38-50 (most often 42-45) seg- ments. Pharyngeal glands absent. Pharyngeal pad slightly thickened, Clitellum in segments XII-XIV. Clitellar gland cells small, 7.5-16.3ptm long (13.1± 4.1, n-:4), 3.0-4.3ptm wide (3.7± O,5, n==4), oval and arranged transversely. Head and dorsal pores absent. Brain 87.5-135,Opm long (105.5± 15.1, n=12), 75.0-80.0pm wide (76.6± 2.1, n-=5) anteriorly, 40.0-42.5um wide (41,4± 1.0, n=5) posteriorly. Brain rounded anteriorly, deeply incised with dorsal bloed vessels posteriorly. Pros- tomium tbrming proboscis, latter 45.0-I25.0um long (96,6± 21.4, n=-39), 24.0-36,Opm wide (30.0± 4.2, n-10) anteriorly and 25.e-37.5#m longwide (31.1± 4.2, n-=10) at base; length of proboscis about O.5 times greater than posterior width of segment III. Both dorsal and ventral setal bundles beginning in segment II. All setae closely similar in number, length, and fbrm throughout body. Setae three per bundle (Fig. IA), 4,5-80"m long (most often 65 77um); each setae sigmoid in shape with bifid

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Propoppus votki from Japan 361

.t.t C ttt/ tt l/ ttttt .t ';'/"/-)..//･kt"･I"'itti'= tt .. t'1/;/t' " A {-'H,"tit,'llikyk"/..I.../ .- ,. 'itt'1.1 ",'t' '? "z ,t ' //./ ,1 ,'-. ?,,',.., u,/ J- .L.....-" ../ . Lt2I.t:::]Opm

D l･lt

// .t .. fF" ,'' ttltt'/'''/' '' ' L:2:-:::-iOpm

'f""' B ir-,,, Xlt xl i,e' ,･', XHI x t/ // '',11J.ls) !ii･t Ntii, t'f''' :'t' '1/ SP xi}e･..,,gift-..･.i･i,･/i:I$･lll/{･lii't /' E ,g' , .g i ttt""-/'-/'l/s･" t ttt [-,1 t.tttt ltttttltttt..tt.;t g .-1･llte･tttl tttttt ttt h t l ,/ ..11.tl.,.,1, 1 'L ,, ...,-,-,,v･,,.-, .I.,-E:lift-- "':' i t sy 1･k,vd mp i ; o

2oe "m - 2eo pm[

Fig. 1. PrQpampus volki Michaelsen, 1916, mature specimen from Yahagi River, Gifu Prefec-

ture, Japan, A, Anterior ventral setae; B, reproductive organs in segments X-XIII, side view; C, vas deferens, sperm funnel, and penis; D, vas deferens, side view; E, anterior body and spermathecae, horizontal ventral view. Abbreviationsi fs, filiform spermatozoa; mp, male pore; o, ovary; sa, spermathecal ampulla; st sperm funnel; sg, setal gtand; sp, spermathecal pore; sv, seminal vesicle; t, testis; vd, vas deferens.

distal ends, lower tooth slightly thicker and about twice as long as upper tooth. Seta1 glands (Fig. IB, E, sg) flask-shaped, with narrow neck, 42.5-77.5pm long (57.9± 10.1, n==12), 20.0-35,O ptm (26,5± 4,5, n-12) wide in anterior segments. Nephridia from intersegmental boundary 5/6. Seminal vesicle unpaired, ex- tending from segment VI or VII to XIII. Spermathecal pores (Fig. IE, sp) paired, located in anterior part of segment IV ventrolaterally, 5,O-10.0pm in diame-

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ter (6.0± 2.0, n-6). Spermatheeal ectal ducts ca, 25CF500ptm long, 12.5-18.8pm (16.0± 2,2, n=10) in minimum width, without ectal glands. Spermathecal ampullae bead-shaped, with several swellings, ca. 375-640pam long, 70.0-147,5pm (90.9± 22.1, n= 11) in maximum width, extending from segment V or VI to as far as segments VII-X and not connected with gut, Walls of spermathecal ampullae only 2.0-6.3"m thick (3.6± 1,4, n-10). Swollen parts of spermathcal ampullae fi11ed with filiform masses of spermatozoa. One pair of testes located at posterior face of intersegmen- tal beundary 10/11 ventrolateraly. Thick bundles of filiform spermatozoa present in front of sperm funnel and around testes. Sperm funnels (Fig. IB, C, sD on ante- rior faee of intersegmental boundary 11/12, thick and conical in shape, becDming thinner posteriorly, 52.5-105.0pm (75.7± 20.2, n-7) in diameter at ental margin. Vasa deferentia (Fig. IB, C, D, vd) in segment XII, thick-walled entally, becoming thinner and irregularly coiled ectally. Total length of vasa deferentia and sperm funnels ca, 500-800"m. Minimum width of vasa deferentia 12,5-16.31im (14.3± 1,3, n=9). Male pores locatedjust posterier to ventral setal bundles in segment XII, Pro- trusive penes 10,O-26.3"m long (20.1+8.8, n=3), Penial bulb 27.5-37,5ptm wide (32,3± 4.2, n-7), Pair of large ovaries (Fig, IB, o) located in segment XIII, some- times extending into segment XIV or XV. Alimentary canal without diverticula,

abruptly widening in segment XV or XVI. Habitat. The present specimens were collected from 10-30cm below the bot- tom sutace in sand and gravel at the end of a sandbar, downstream ef which sub- soil water fiowed in and eut (=:hyporheic zone), Current velocities were 4(>-60 cm/s and the water depths were 20-50cm. The minimum water temperature during the year was 2.0oC, and the maximum 23,60C, at the lecality in the Yahagi River. The

fo11ewing macroinvertebrates were collected together with P. volki at the locality in the Tooyama River: Arais communis Piguet, 1906 (Clitellata, Oligochaeta); llphemera jqponica Mclaehlan, 1875, Drunetta tshlyamana, Matsumura, 1931, Alainites yoshinensis (Gose, 1980), Baetielta jcrponica (Imanishi, 1930), Baetis thernzi- cus Ueno, 1931, Ec(tvonurus viridis (Matsumura, 1931), liipeorus curvatulus Mat- sumura, 1931, and llipeorus nipponicus (Ueno, 1931) (Ephemeroptera); Ktimimuria quadrata (Klapalek, 1907) and Ptxragnetina tinctipennis (McLachlan, 1875) (Ple- coptera); l]lydropsyche orientalis Martynov, 1934, Stenopsyche marmorata Navas, 1920, and Eobrachycentrus sp. (Trichoptera); Blqpharocera shirakii (Alexander, 1922) (Diptera, Blephariceridae); Sim"tium sp. (Diptera, Simuliidae); Antocha sp. (Diptera, Tipulidae); and Atherix ibis Fabricius, 1798 (Diptera, Athericidae). An- nual average values ef BOD at each locality in 2003 were as fOllows: Yahagi River, O.6mgfL; Tooyama River, O.5mglL; Takase River, O,5mg/L; Yoshii River, 1.6mg/L (Natjonal Institute fbr Environmental Studies Website 2005). Remarks. The length of the proboscis in the present material was variable, ranging from 45-125pm ameng all localities. The Gifu specimens had the longest probosees, 105.8± 12.8ptm (mean± SD). According to Coates (1986), proboscis length of Baikal specimens (38.5± 5.4um) is distinctly shorter than in French and English specimens (56.2± 11,2pm and 64,6 ± 15,9um, respectively). The present Japanese specimens have much longer probosces than those firom England, France, or Lake Baikal. Wachs <1967, Fig. 9) shows the spermathecal ampullae of specimens from Ger- many extending from segment V as far back as segment IX or X. Coates (1986) de- scribed the spermathecal ampullae extending frorn intersegmental boundary 4/5

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Propappus votki from Japan 363

as far back as segment X or XII in European and Lake Baikal specimens. The pres- ent Japanese specimens have spermathecal ampullae extending from segment V or

VI as far baek as segments VII to X, in many cases from segments VI to VIII. Lengths of spermathecal ampullae and probosces may vary depending on lo- cality and state of fixation and maturity of specimens. The following combination

of diagnostic characters in the Japanese material agreed well with the original de- scription (Michaelsen 1916) and redescriptions (Wachs 1967; Coates 1986): setae with bifid ectal ends, usually three per bundle; setal glands in association with every setal bundle; spermathecal pores at intersegmental boundary 3f4; prosto- mial probpscis elongated anteriorly. I therefore conclude that the Japanese speci- mens are conspecific with the previous]y reported continental populations of Propappus volki.

Discussion

Species of Propappidae are widely distributed in the Holarctic region, but this is the first record of the family Propappidae in Japan. Propoppus volki js widely distributed in the Holarctic (Coates 1986 and pers. comm.) but so far is not known frem any other zoogeographical region (Timm 1999b). Timm (1997) suggested that the Amur-Japanese freshwater zoogeographical subregion, transitional between the Holarctic and Sino-Indian regions, is more closely related to the former region. The new record of P. volki from Japan supports his opinion, Lafbnt and Malard (2001) suggested that Prqpcrppus volki originated as a groundwater species and reproduces in the hyporheic zone. Mature specimens were recorded from superficial coarse and sandy sediment during all sampling sea- sons (June to November 1997) in a glacial river in Switzerland. The Japanese mate- rial was collected from 20-30cm below the riverbed surface in upwelling ground- water, and this tends to corroborate the suggested hyporheic nature of this species. It has been widely recognized that benthic macroinvertebrates can be used as bioindicators of water quality, In the United Kingdom, Chandler (1970> proposed "average the score per taxon" (ASPT) to estimate water quality and Chester (1980) developed this into the Biological Monitoring Working Party (BMWP) score, whereby the total score is based on the types of invertebrate organisms present, The ASPT method was tried in Japan by the Environment Agency, Government of Japan (1992) and the Collaborative Study Group of Environmental Biology in Envi- ronmental Laboratories Association (1995), and many Japanese macroinvertebrate taxa thus have been scored from 1 to 10 according to the water quality of their habitats (BOD, DO, T-P, and T-N). In this system, all the oligochaetes were treated ``1" together and scored as the most tolerant taxon. According to Bird (1982), P, volki has a preference for clean gravel and sand usually associated with high cur- rent velocities and is almost entirely absent from slightly to heavily silted sand. The present specimens of Japanese P. volki were a!so collected from non-silted sand and gravel bottoms, and the river water at these localities was not organically polluted, with BOD values of O,5-1.5mg/L (National Institute for Environmental Studies Website 2005). As scored by the Environment Agency, Government of Japan (1992), all the species of aquatic insects fbund coexisting with P. volki jn the present localities are into}erant taxa (scores from 6 to 10); it can be supposed,

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therefore, that P. js also an intolerant species and a good bio-indicator for un- polluted waters.volki

Acknowledgements

I am greatful to Drs Akifumi Ohtaka (Hirosaki University, Aomori, Japan) and Tarmo Timm (V6rtsiarv Centre fbr Limnology, Estonia) fbr their invaluable sug- gestions concerning the taxonomy of oligochaetes, Dr Kathryn A. Coates (Bermuda Biological Station fbr Research, Bermuda) fbr providing me with valuable infor- mation, and Ms Chiharu Sato (Akita-Minami Senior High school, Akita, Japan) and Dr Takao Shimizu (Freshwater Benthos Associates Inc., Nagano, Japan) fbr

the specimens used in this study. Thanks are also due to Ms Masako Torii (Shizuoka, Japan) for assistance in the field and linguistic help.

References

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Chester, R. K. 1980. Biological Monitoring Working Party. The 1978 national testing exercise.

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