CRUSTACEANRESEARCH ，NO. 26:10 3-108 ，1997

Sacculina polygenea，anew species of rhizocephalan (Cirripedia: ) n ・omJapan，parasitic on the intertidal (De Haan，1835) (Decapoda: Brachyura: Grapsidae)

Jorgen Lutzen and Tohru Takahashi

Abstract. - A new species of rhizo- any known taxon，they are here described cephalan，Sacculina polygeneα，is de- as anew speCles. scribed and illustrated on basis of material from the Amakusa Islands， Materials 田 ld Methods Kyushu Japan. Although previously ， Almost all specimens were collected at recorded as alocally common parasite of Inuki，Oyano Island，Am akusa Islands， the littoral crab Hemi psus s<α nguineus gra. Kyushu. Nearly all the specimens repre- (de Haan 1835) it has remained un- ， ， ， senting every size were studied alive. A described. especies is compared with ， Th number were preserved in Bouin's fluid S. senta Boschma 1933 and S. nigra ， (sea water formula) and embedded in Shiino 1943 which parasitize the same ， ， tissuemat and cut into 10μm thick serial crab. Upto 5concentric cuticular rings sections. The sections were stained with surround the stalk and adjacent part of hematoxylin and eosin (H E).Thin (2 the body. Such rings have never before + μm ) toluidine-blue stained sections of the beenob舵 rved in any sp回 ies ofthe colleteric glands，receptacles and special and are probably evidence that S. poly- parts of the mantle were prepared from geneαm o u l t s its outer cuticle up to 5 Bouin-preserved material that was em- times. bedded in araldite. The mantle cuticle was studied from lactic acid preparations. Introduction On many boulder beaches of S. W. Kyushu，Jap田 1，one of the most common Sα cculinαpolygeneαn e w species shore ，Hemigrapsus sanguineus (De (Figs.1-4) Haan 1835) is infected with aspecies of ， ， Type-materia Holotype (from Sα cculinα. Although the parasite has l.- Inuki) infesting amale crab CW28.5 been the subject of several studies (Taka- ， mm，Apri19 ，1997 and aparatype (I nuki) hashi，1991; Takahashi & Matsuura， from afemale crab，CW 2 1. 0mm ，April 1994; Y 田 naguchi et αl. 1994; Yamaguchi ， 11，1997 ，are deposited in the National & atake 1997 Takahashi et αl. 1997) Ar ， ， ， Science Museum Tokyo. oparatypes it has remained unidentified until now. ， Tw (also from lnuki) are kept in the Zoologi- The purpose of the present study is to cal Museum University of Copenhagen clarify its specific status. It is based on ， ， Denmark (catalogue numbers CRU-3060 specimens provided by Dr. T. Yamaguchi ， and CRU-3061). Aitsu Marine Biological Station，Kuma- moto University，or collected by our- Description. - The body is regularly selves. As they could not be referred to oval，dorsal and ventral halves usually of 104 J.LUTZEN &T .TAKAHASHI

Fig. 1. Sα cculinαpolygeneαn e w species，two extemae on abdomen of afemale Hemigrapsus sanguineus (De Haan). Drawn by Beth Beyerholm.

same size. Theposterior margin on either 出 1 average diameter of 20-25μm (Fig. 3). side is produced into around lobe. The The receptacles are spherical or mantle opening is situated on top of a shortly ovoid (Fig. 4) .They are placed， relatively short prominence.The stalk close together，outside the visceral mass has abroad base but tapers towards the and included in the mantle above the body. The mantle is thin and transpar- stalk. Theright receptacle is usually dis- ent. The external cuticle is generally placed somewhat posteriorly and dorsally smooth.I旬 surface is divided into m I1l ute to the left one. irregular squares with interdigitating The latter is located superficially borders. Small papillae may，however ， within the left mantle and clearly visible mαIr in smaller 町 eas ofthe cuticle. Upto from outside. Both receptacles are milky- five sinuous cuticul町 lines circumscribe white in live specimens. The receptacle concentrically 也 eupperpa此 ofthe stalk ducts form very narrow tubes that curve and/or the adjacent part of the body slightly in aposterior and ventral direc- (Fig. 2). Thelines are finely serrated. tion .They are distinctly set off from the Retinac叫 ae are apparently absent 合om receptacles .Their length is equal to the the interior mantle cuticle . longer diameter of the receptacles.In sec- Each colleteric gland occupies an area tions they are seen to have smooth，never of the anterior pa此 of the visceral mass， folded，interior walls. that is ill-defined from outside. In a medium-sized specimen it measures 1.0 Coloration. - The color of live speci- x1. 7mm in dimension. The maximum mens is different shades ofyellow，lighter number of glandular canals in sections is in immature than in mature specimens. 25-30 arranged in two-four layers，with Extemae with nauplii are light brown or S.POLYGENEA ，A NEW RHIZOCEPHALAN 105 purple. Virginal extemae are whitish.

Size. ー Dorso-ventral height of single externae may reach 20 mm，maximum length 14.0 mm; the thickness is by com- parison moderate (ca .2.0-4.0 mm). Vir- ginal externae are from 2.0 to 3.5 mm V d high. Position on host. - Ventrally on the first four abdominal segments.Th epref- erential attachment to the segments of male and female crabs has been analyzed by Yamaguchi & Aratak. e(1997). Biology. -A characteristic feature of S. polygeneαi s the fact that multiple ( externae per host (up to 8) occur fre- quently，and at some localities even as often as single ones (Yama郡lchi et al .， 1994). Uniquely among sacculinids，when Fig. 2. Sα cculinαpolygeneαn e w species. A ， the externa(e) of this species die after anatomy ofmature externa seen 企omleft side; having spawned afew times the host B，virginal externa. cg，colleteric gland with ， opening; d，dorsal side; lr ，left receptacle; me， crab moults afew weeks or months later mesentery; mo，mantle opening; rd，receptacle which is inevitably followed by the duct (ofleft side); 1・r，right receptacle; st ，stalk; appe訂 ance of one，or afew ，new extemae v，ventral side; vm，visceral mass with ovarγ. (Takahashi，1991; Takahashi & Matsu- Note the cuticular moult lines (arrowheads). ura，1994). Drawn by Beth Beyerholm. Distribution. - S. polygeneαi s until Sections of the rings show them to now known only 仕omKyushu，except for have exactly the same profile as the an・ asingle record from the Pacific coast of nuli or growth rings which mark lines Nor emHonshu( cculina sp. Naga- ， ， 血 部品 ， along which the outer cuticle ruptures sawaet 1. α ，1996). when，unlike the stalk cuticle ，it is shed at Variations. - Special attention was amoult .Th eir position is also the same as paid to the cuticular lines at the con- that 血 which they are found in species of fluence of stalk and body，as similar Peltogastridae and Lernaeodiscidae structures have never been noticed in any (Lutzen，1987) . species of before. Their Species of Sacculinidae are generally number vary between 1and 5，with 3or 4 believed never to shed the external being most frequently recorded. Small， mantle cuticle except once，namely at the 吋rginal，extemae have either no lines or moult which in the virginal externa re- only asingle one forming aring around sults in the functional opening of the the upper part of the stalk (Fig. 2B). mantle aperture (Hoeg，1987). 明白moult Among 7externae believed to be imma- is evidently represented by the single line ture (4.0-6.0 mm)，there were 1-3 lines， which we observed in 6of 9virginal 2being the most common. In mature externae examined and by the posterior- (ovigerous) extemae the number of lines ， most ofthe 1血es ，when more than one are 3-5，seems not to be correlated with body present. The occurrence of additional slze . rings in S .polygene αi n d i c a t e s that the 106 J.LUTZEN &T .TAKAHASHI

Figs. 3& 4.Sα cculinαpolygeneαn e w species. - Fig.3. Longtitudinal section through both colleteric glands (cg) .- Fig. 4.Lo ngtitudinal section through right receptacle and duct (π ，rd) ， cross section of left receptacle duct (l d) .- mc，mantle cavity; ms，muscle sheath around recep- tacle; sp，sperm producing tissue; vm，visceral mass. 10μm thick tissuemat-sections stained with H+ E. Scale bars 100μm (3) and 300μm (4).

cuticle in this species is shed three or four the rudimentary receptacle，may often more times during the life of an externa， fai l. Size reduction，or degeneration，of even if there is no direct observation of either right or left receptacle is therefore the moulting. That moulting may some- apoor diagnostic character，although it times occur in post-virginal externae of has often been used as such at the time Sacculinidae is indicated by several when the receptacles were believed to observations of 2or 3successive layers of represent the rhizocephalan testes. external cuticles that were reviewed by Etymology. - The species name is Boschma (1947). derived 企ompolys，Gk ，meaning several， Themutual size of the two receptacles andgeneα，Gk ，for descent，in allusion to may di首位 in many sacculinids. In 21 the fact that when the externa(e) of this specimens of S. polygeneαb o t h recep- species die they are constantly being tacles were more or less similarly devel- ， replaced by ageneration of new ones as oped; in 9other specimens one of them ， ， shown by Takahashi Matsuura 994). usually the right one，was degenerate or & (1 had almost vanished，while the other in Remarks. - Theexamined species has contrast was generally above average remained unidentified (Takahashi，1991; size. Theexplanation is that implantation Yamaguchi et al .，1987 ，1994) or mis- by trichogon larvae (Veillet ，1985; Hoeg， identified as Sα cculinαsentαB o s c h m a ， 1987)，which triggers the development of 1933 (Takahashi，1990; Takahashi & S. POLYGENEA，A NEW RHIZOCEPHALAN 107

Matsuura，1994). Although the recep- helped us in the field collections. The tacles of S. sentαr e s e m b l e those of S. travel of J. L. to Japan was funded by a polygeneαi n most details including their grant from the Danish Natural Science position outside the visceral mass the Research Council. outer mantle cuticle of S. sentαi s pro- vided with m 出 ly close-set papillae which Literature Ci句d possess stiff little spines. Sacculinαn恕rα Shiino 1943 is also aparasite of Japanese Boschma，H .，1947. Three successive layers of ， external cuticle in Sacculina leptodiαe . H. sanguineus，but differs from S. poly- Koninklijke Nederlandsche Akademie van geneαi n that the exterior of its two Wetenschappen，50: 3-9. cuticular layers has well-developed ridges Hoeg，J. ，1987 .Male cyprid metamorphosis that contain pigment displaying an ir- and anew male larval form，the trichogon， in the parasitic Sα cculina cα rcini re伊 lar arborescent colour pattern. One (Crustacea: Cirripedia: Rhizocephala). side of the body of S. nigrαi s more ex- Philosophical Transactions of the Royal panded than the other，while the body of Society of London，B 317 :47 -63. S. polygeneαi s more or less symmetrical. Lutzen，J. ，1987 .Life history parameters Structure and position of the receptacles calculated 企omgrowth rings in parasitic of the family Peltogastridae ofthe two species，however ，are very simi- (Crustacea: Cirripedia: Rhizocephala). lar. Cuticular rings surrounding the st alk. Journal ofCrustacean Biology，7: 493-506. region have never been observed in either Miyake，S. ，1983. Japanese deca- S. sentαn o r S. nigrα，，although they may pods and stomatopods in color .Vo l. II. have escaped notice. In Japan H. sαngui- Brachyura (crabs) .viu +277 pp. ，Hoik 田 ha， Osaka. (In Japanese) neus is also claimed to be parasitized by Nagasawa，K.， Lutzen，J. ，& Kado，R. ，1996. Sα cculinαconfrαgosαB o s c h m a ，1933 Parasitic Cirripedia (Rhizocephala) and (Nishimura & Suzuki，1971; Suzuki， Isopoda 企ombrachyuran and anomuran 1979; Miyake，1983; U 出 lomi，1983; Nishi- crabs of the Pacific Coast of Northern mura，1995) ，but this information is Honshu，Japan .Bulletin of the Biogeo- graphical Society of Japan 51: 1 probably not based upon thorough identi- ， -6. Nishimura，S. (ed.) ，1995. Guide to seashore fication of the material. Thetwo parasites of Japan with color pictures and illustrated by Nishimura (1 995，Pl. 78，3) keys. 663 pp. ，Hoikusha ，Osaka. (In Japa- and identified as S. conf同 gosαs h o w a nese) striking similarity to S. polygeneαe v e n if Nishimura，S .，& Suzuki，K.， 197 1.， Common sea shore animals of Japan in color .(super- the host is obviously Hemigrapsus penicil- vised by Utinomi，H.) 196 pp. ，Hoikusha ， lα tus (De Haan，1835). It is therefore Osaka. (In Japanese) possible that Sαcculinαs p . reported by Shimoizumi，M .，1970 .Effects of Sα cculinαo n Shimoizumi (1970，1973) 企omH. penicil- the external characters of the brackish- latus ，although from abrackish water water crab，Hemigr αpsus penicillαtus . habitat (Yoshiro River Shikoku) maybe Journal of Gakugei，Tokushima Univer- ， ， sity ，20: 1-6. identical with S. polygeneα. 一一一一， 1973. Effects of Sα:cculinαo n the inter ・ nal organs of the brackish-water crab， Acknowledgments Hemigrαpsus penicillatus. Journal of Gakugei，Tokushima University，24: 11- Weare much indebted to Dr. Takao 18. Yamaguchi，Ai tsu Marine Biological Sta- Suzuki，S. ，1979. Marine invertebrates of tion，Kumamoto University，for having Yamagata Prefecture .Tamakibi-kai ，Y 佃 la- collected some of the material and for gata. 370 pp. ，22 pls. (In Japanese). Takahashi，T .，199 1. Molting and growth of excellent professional assistance during the sacculinized shore crab，Hemigrapsus our visit to the Laboratory. Mr. Junichi sα nguineus and pα，chygrαpsus crassipes Nakagawa，Kumamoto University，kindly (preliminarγreport). Annual Report Ma- 108 J.LUTZEN &T. TAKAHAS田

rine Ecosystem Research Center，Chiba polygeneαi n Hemigrapsus sαnguineus (De University，No. 11:19-28. (In Japanese) Haan) (Brachyura: Grapsidae). Crusta司 一一一一， & Matsuura，S. ，1994. Laboratory cean Research，26: 125-145. studies on molting and growth of the shore Yamaguchi，T. ，Harada ，K.， Takeda，M. ，& crab，Hemigr α，:p sus sanguineus De Haan， Kikuchi，T. ，1987. Crab fauna ofthe Ama- parasitized by arhizocephalan barnacle. kusa Islands. Calanus (Bulletin of Aitsu Biological B 叫letin，186: 30仏- 3 08. Marine Biological Station，Kumamoto 一一一一， Iwashige，A. ，& Matsuura，S. ，1997. University)，10: 1-71. (In Japanese) Behavioral manipulation of the shore crab Yamaguchi，T. ，Tokunaga ，S. ，& Ar atake，H. ， Hemigrapsus sanguineus by the rhizo- 1994. Contagious infection by the rhizo- cephalan barnacle，Sacculina polygenea. cephalan parasite Sαcculinαs p . in the Crusta四 anResea四 h ，26: 153-161. grapsid crab Hemigrapsus sαnguineus (De Utinomi，H. ，1983. Sacculinαconfragosa. In: Haan). Crustacean Research，23: 89-101. H. Utinomi (ed.) ，The Aquatic Lower Ani- mals of Japan. p. 210，Gakken. Tokyo. (In Japanese) Addresses: (JL) Department of Cell Biology Veillet，A. ，1985. Note preliminaire sur la and Anatomy，Zoological Institute，Univer- phase larvaire male qui suit la fixation des sity of Copenhagen，Universitetsparken cypris male chez les Rhizoc岳phales. Bulle- 15，DK ・2100 Copenhagen o，Denmark; tin de la Societe Lorraine des Sciences，24: (TT) Department of Fisheries，Kyushu 141-146. University，Hakozaki ，Fukuoka 812 Japan. Yamaguchi，T .，& Ar atake，H. ，1997. Morpho・ E-mails:(JL)[email protected]; (TT) takahasi logical modifications caused by Sαcculinα @agr.kyushu-u.ac.jp