Diseases of Echinodermata. 11. Agents metazoans (Mesozoa to Bryozoa)

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1 Vol. 2: DISEASES OF AQUATIC ORGANISMS Dis. aquat. Org. I Published July 30 REVIEW Diseases of Echinodermata. 11. Agents metazoans (Mesozoa to Bryozoa) Michel Jangoux Laboratoire de Biologie marine (CP 160), Universite Libre de Bruxelles, Ave F. D. Roosevelt 50, B-1050 Bruxelles, Belgium ABSTRACT: The only species of Mesozoa known to parasitize echinoderms is clearly pathogenic; it causes the regression of ovaries of infested ophiuroids. Symbiotic turbellarians have been reported for each echinoderm group; they mainly infest the gut and coelom of aspidochirote holothuroids and regular echinoids. Echinoderms generally act as second intermediary host for trematodes; the latter are known mostly from echlnoids and ophiuroids which constitute the most frequent echinoderm prey for fishes. Records of echmodem-infeslng nematodes are rather scarce; they usually infest either the coelom or the gonads of their host. Many eulimid gastropods have been reported to parasitize echinoderms; however, most of them do not seem to seriously alter the echinoderm life cycle. They are no bivalves parasitic on echinodems except a few species inhabiting the gut of holothuroids. Associations between echinoderms and sponges, cnidarians, entoprocts or bryozoans have been casually reported in the literature. INTRODUCTION The present paper is the second of a series of 4 that review the diseases of Echinodermata. It considers the disease agents belonging to the Mesozoa, Parazoa, Cnidaria, Acoelomata (Turbellaria and Trematoda), Nematoda, Mollusca (Gasteropoda and Bivalvia), Entoprocta and Bryozoa. As discussed in Part I (Jangoux 1987), I have adopted the definition of parasites proposed by Kinne (1980, p. 19) and used it in a very broad sense, considering dsease agents (parasites sensu lato) to represent any kind of a harmful associate which affects, if even slightly, the echinoderm's tissues or internal fluids (i.e. coelomic and hemal fluids). DISEASES CAUSED BY METAZOANS Agents: Mesozoa The Mesozoa, a small group of uncertain taxonomic affinity, comprise about 50 species of minute animals parasitic on marine invertebrates. One species, Rhopalura ophiocornae, parasitizes ophiuroids. Its most frequent host is the small cosmopolitan incubating amphiurid Amphipholis squamata (Caullery & Mesnil. 1901, Kozloff 1969, Rader 1982) but it may - if very rarely - also affect other ophiurid species, namely Ophiothrix fragilis and Ophiura albida (respectively Fontaine 1968, Bender 1972). R. ophiocornae is mostly known from European localities (Atlantic coast of France, North Sea, northwest Mediterranean Sea; for reviews see Kozloff 1969, Bare1 & Kramers 1977), and also from 2 Pacific localities along the coast of Washington (Kozloff 1969, Rader 1982). Structure and life cycle of Rhopalura ophiocomae were studied intensively at the begining of this century, mainly by Caullery & Mesnil (1901) and Caullery & Lavallee (1908, 1912) (Fig. 1). Mature adults of R. ophiocomae are free living. Adults, either male or female, develop in Arnphipholis squamata and are emitted through the ophiuroid's bursal slits. Their life span is short (a few days) and they give rise to ciliated larvae. These infesting larvae penetrate the ophluroid bursal slits and intimately contact the outer epithelium of the bursae. Soon afterwards, small parasitic 'plasmodia' occur withln the epithelium. Subsequently, plasmodia migrate to the coelomic side of the bursae where they remain close to the ovaries. At that time plasmodia often protude into the coelomic cavity. They C2 Inter-Research/Pnnted m F. R. Germany

2 206 Dis. aquat. Org , 1987 l \ 'l' I FREE, I PARASITIC A, Fig. 1. Rhopalura ophiocomae. Ife-cycle of a mesozoan parasite of the ophiuroid AmphiphoLis squamata (not to scale). (A) Male and female mesozoans emitted through the genital slits of an infested ophiuroid; (B) fecondation; (C) infesting mesozoan larvae; (D) release of infesting larvae from a female mesozoan. (E) infestation of ophiuroid genital slits; (F) penetration of the larvae in the ophiuroid bursal epithelium; (G to I) developing plasmodia; (J) male and female plasmodia. (After Caullery & Lavallee 1912) are completely surrounded by an epithelia1 layer presumably formed by host mesothelium (Caullery& Mesnil 1901, Rader 1982). Whether each plasmodium derived from a whole larva or from one or more cells of that larva is not known. The plasmodia grow and some of them move along the coelomic lining. Fully developed plasmodia consist of an enlarged cytoplasmic (?) mass surrounded by an epithelium of host ongin. Each plasmodial mass contains numerous small nuclei (the 'plasmodic' or 'vegetative' nuclei), some germ cells (sometimes called 'agametes') and a few embryos at different developmental stages. These are either males or females, embryos of both sexes within the same plasmodium belng exceptional. When mature, the plasmodium presumably disintegrates and numerous adult R. ophiocomae are emitted into the outer medium through the host's bursal slit. The pathogenicity of Rhopalura ophiocomae is unquestionable. Its most obvious effect is the regression of host ovaries, while the testes - as noted by several authors - remain functional (Amphipholis squamata is hermaphroditic). The parasite does not consume the ovaries; these regress as soon as small plasmodia invade the bursal wall. Ovarian regression implies that infested ophiuroids never harbor incubated embryos. Other consequences of the disease are a decrease in the ophiuroid's regenerative abilities, as well as probably a decrease in its growth rate (Rader 1982). Agents: Parazoa There are only 2 sponge species known to parasitize echinoderms. Clark (1896, 1898) reported the occurrence of a Grantia-like species firmly attached to the outer body surface of several individuals of the holothuroid Synapta vivipara. The sponges always were seen at the base of the holothuroid buccal tentacles. Antarctic ophiuroids of the genus Ophiurolepis are very often parasitized by the sponge Iophon radiatus (Mortensen 1936, Fell 1961). The parasite fixes itself on the ophiuroid, and infestation is generally very extensive, the whole disc and the basal parts of the arms being involved. As shown by Mortensen (1932), the bizarre sponge Microcordyla asteriae described by Zirpolo (1926) as an

3 Jangoux: Diseases of Echi nodermata: agents metazoans 207 ectoparasite of the asteroid Coscinasterias tenuispina, actually represents a globiferous pedicellaria of the echinoid Sphaerechinus granularis. The pedicellariae probably were detached in a defensive reaction of S. granularis (globiferous pedicellariae of echinoids autotomize easily). Agents: Cnidaria Several sea anemones attach to the body surface of echinoderms. Gravler (1918) noted the occurrence of the actinid Sicyopus coinmensalis partly embedded in the body wall of the deep-sea holothuroid Pseudostichopus villosus. Kropp (1927) reported echinoids of the genus Diadema with the sea anemone Aptasia tagetas firmly attached to their body surface near the anal cone. Other cnidarians may incidentally parasitize echinoderms, namely hydrozoans which live attached to the stem or the cirri of cnnoids. Four crinoid-associated hydrozoans are known: Calycella syringa, Cuspidella sp., Lafoea fruticosa, and Stegoporna fastigiata (Clark 1921). A case of symbiosis between the hydrozoan Hydractinia vallini and several species of the Antarctic ophiuroid genus Theodoria has been reported by Smirnov & Stepanyants (1980). This symbiosis is similar to the one between Antarctic ophiuroids and sponges. The single known case of hydrozoans living on asteroids was reported by Madsen (1961) who recorded unidentified athecate hydroids attached to the penstome of the deep-sea asteroid Eremicaster gracilis. Agents: Turbellaria While Turbellaria are mainly free-living, each order has developed representatives living in close association with other organisms. Symbiotic turbellarians were reviewed by Jennings (1971) (see also Stunkard & Corliss 1951) who noted that echinoderms represent preferential shelters for turbellarians. Table 1 lists symbiotic turbellarians living with echinoderms; of the 68 species, 9 are Acoela, 58 Rhabdocoela (52 species belonging to the family Umagillidae) and 1 Polycladida. With very few exceptions (Euplana takewalui and Acholades asteris; respectively Kato 1935, Hickman & Olsen 1955), almost all echinoderm-associated turbellarians live either within the digestive tract or within the coelomic cavity of their host. Symbiotic turbellarians have been reported for each echinoderm group, but most of these associates live in aspidochirote holothuroids (mainly Holothuriidae and Stichopodidae) or in regular echinoids. As noted in Table 1, massive turbellarian infestations occur rather frequently in echinoderms. There is, however, no information on the effect of parasitic Turbellaria on the echinoderm life cycle. Gut-associated umagillids may either occur all along the digestive tract (Smith 1973) or be more or less restricted to some digestive areas (Bare1 & Kramers 1971, Shinn 1981, Cannon 1982; see also Table 1). Holt & Mettnck (1975) reported that Syndisyrinx franciscanus from the gut of Strongylocentrotus purpuratus feeds mostly on associated ciliates, harbored by the digestive tract of the echinoid. Snyder (1980) could deternline neither beneficial nor detrimental effects due to the occurrence of gut-associated umagillids. He concluded that these symbiotes should be considered simply conlmensals. In contrast Shinn (1981) reported that the gut-associated umagillids always compete with their host for nutrients and thus may exert adverse effects. He noted that all the umagillids studied by him ingest intestinal host tissue - one of them subsisted entirely on that tissue (see also Cannon 1982). Shinn suggested that gut umagillids parasitise their host to varying degress. Giese (1958) noted that the infestation level of S. franciscanus in the gut of S. purpuratus remains constant throughout the year and does not differ whatever the size, sex or gonadal stage of the echinoid. In contrast, Wahlia pulchella inhabiting the intestine of Stichopus californicus displays a distinct annual cycle of infestation related to the annual feeding cycle of its host (worms do not occur in S. caljfornicus in fall and winter when the host's vlscera are resorbed) (Shlnn 1986b). According to Shinn (1980, ) egg capsules of the gut-associating S. franciscanus leave the host gut with fecal material. Embryogenesis within capsules lasts approximately 2 mo, and fully-formed embryos (infesting embryos) can survive in their capsule for about 10 additional mo (Fig. 2). Embryos hatch after the capsules were ingested by an echinoid. Hatching is induced by some property of the host's digestive fluid and performed presumably owing to a hatching enzyme secreted by the embryos (Shinn , 1986a). Coelomic umagillids swim in the host's body cavity, seemingly without any particular intracoelomic location. Coelomic umagillids directly depend on their host for nutrition - they ingest the host's coelomic fluid together with coelomocytes (Jennings & Mettrick 1968, Shnn 1983b) - or on other coelom-associated organisms such as ciliates (Mettrick & Jennings 1969, Jennings 1980). Egg-capsules of intracoelomic umagillids of holothuroids frequently occur within brown bodies (Briot 1906a, b, Arvy 1957, Changeux 1961, Jespersen & Lutzen 1971, Shinn , 1985a). They are thought to be released into the outer medium through host evisceration (Changeux 1961, Jespersen & Lutzen 1971). Shinn (1985a) reported, however, that brown

4 208 DIS. aquat. Org. 2: , 1987 Table 1. Turbellarians associated with echinoderms (compiled from the sources indicated). Turbellarian species names according to Cannon (1982). Hosts A, asteroid; C, crinoid; E, echlnoid; H, holothuroid, 0, ophiuroid Turbellarian Host Location in host Remarks Geographical area Source I. Acoela Aechrnalotus pyrula Aphanastoma pallidurn Aphanostoma sanguineum Avagina glan duhfera Avagina incola Avagina incola Avagina vivipara Faerla echinocardil Meara stichopi Meara stichopi Meara stichopi Eupyrgus scaber (H) Digestive tract and respiratory trees Barents Sea Beklemlshev (1915) (Murmansk coast) blynotrokus rink (H) D~gestive tract Barents Sea Beklemtshev (1915) (Murmansk coast) Chirodota laevis (H) Spa tangus purpureus (E) Echrnocardiurn cordatum (E) Echinocardium flavescens, Spatanguspurpureus (E) Ecl~inocardiurn flavescens (E) Spatangus pupureus (E) Echinocardic~m corda turn (E) Echinocardium flavescens (E) ParasOchopus tremulus (H) Parastichopus trem ulus (H) Mesothuna intestinalis (H) Posterior part of the digestive tract Digestive tract S~phon (accessory canal) Digestive tract D~gestive tract Many echinoids infested 5 % of the ech~no~d population Infested Average infestahon : 50 worms echinoid-l 3 to 14 worms echinoid-' (50 echinotds investigated) Barents Sea Beklemishev (1915) (Murmansk coast) English Channel Westblad (1953) (Plymouth) NE Atlanhc Leiper ( ) (Millport) North Sea (Bonden. Karling (in Westblad Noway) 1948) North Sea Westblad (1948) (Norwegian coast) Digestive tract North Sea (Norwegian Westblad (1948, 1953) coast); English Channel (Plymouth) Esophagus 2 to 5 worms echinoid-' (18 infested/68 investigated) SW lndian Ocean Hickman (1956) (Ralph's Bay, Tasman~a) Unspecified 1 North Sea Dorjes (1972) (Nonvegian coast) Anterior intestine; coelomic cavity OctocoeLis chirodota Chirodota laevis (H) Anterior part of digestive tract l to 8 worms holothuroid~' North Sea (Norwegian Westblad ( ) coast: Herdla, Trondhjem) Esophagus North Sea (Oslofjord) Jespersen & Llitzen (1.971) Coelomic cavity Single observahon North Sea Westblad (1926, 1949) (Norwegian coast) Barents Sea Beklemishev (1915) (Murmansk coast) 11. Rhabdoecoela (I. umagillidae) Anoplodiera voluta Parastichopus Lrernulus (H) Anoplodiera voluta Anoplodiera sp. Parastichopus trernulus (H) Holoth uria arenicola (H) Anoplodiopsis gracilis Holothuria forskal~ (H) ~noplodiurn' ch~rodotae Ct~~rodota pellucida (H) Anoplodium evelinae Unidentified holothuroid Anoplodium graffi Holothur~a impatiens (H) Anoplodiurn hymanae Parastichopus califon~icus (H) Digestive tract Anterior part of dlgeslive tract Up to 90 worms holothurold-' Pharynx Average infestation: 7 worms holothuro~d-: (9 1nfested/l2 investigated) North Sea (Nonvegian Westblad ( ) coast: Herdla, Trondhjern) North Sea (Oslofjord) Jespersen & Ltitzen (1971) Tropical MIAtlantic Snyder (1980) (Bermuda) Coelomic cavity Up to 9 worms holothuroids-i (11 infested/47 investigated) (Wahl 1906) Mediterranean Sea (Naples) WahI(1906, 1909). Westblad (1953) Coelomic cavltv Species of doubtful Wh~te Sea Sabussow (1900, generic afflruty quoted by Barel & Kramers, 1977) Coelomic cavity Coelomic cavity Coelomic cavtty Up to 50 worms holothurold-l l to 51 (average l51 worms holothuroitff1 (25 infested/27 Investigated) SW AUantic (Brazil: Santos Bay) Mediterranean Sea (Naples) NE Pac~f~c (Washington coast: Cowlitz Bay1 Marcus (1949) Mont~celli (18921, Wrstblad (1953) Sh~nn fl983a; see also Sh~nn 1985bl

5 Jangoux: Diseases of Echinodermata: agents metazoans 209 Table l (continued) Turbellarian Host Location in host Remarks Geographical area Source Anoplodium Actinopyga sp. (H) Unspecified - SW Jndian ocean Hyman (1960) long~ductun? (Madagascar: Nossy-Be) Anoplodium Stichopus Coelomic cavlty - hw Pacific (Japan: Ozah (1932) mediale japonicus (H) Hiroshima) Anoplodium Myriotrochus Digestive tract Infestation frequent Arctic Seas Barel & Kramers m yriotrochi nncki (H) (Spitzbergen) (1977) Anoplodium parasita Holotl~una tubulosa, Coelomic cavlty, rare- 14 worms Mediterranean Sea Schneider (1858), Holothuria poh and ly digestive tract or holothuro~d-' (16 in- (Banyuls, Naples, Monticelli (1892), Holothuria stellah (H) respiratory trees fested/26 ~nvesti- Trieste) Bnot (1906b), Wahl gated) (Changeux) (1906). Westblad (1953), Changeux (1961) Anoplodium ramosurn Stichopus Unspecified - SW Indian Ocean Hyman (1960) vanega tus (H) (endoparas~bc) (Madagascar- Nossi-Be) Anoplodjum stichopi Parastichopus Coelomic cavity Up to 30 worms North Sea Bock (1926), Westblad tremulus (H) holothuroid-' (Norwegian coast) (1926). Jespersen & (Westblad) Liitzen (1971) Anoplodium Holoth uria Digestive tract - English Channel Westblad (1953) tubiferurn forskali (H) (Plymouth) 'Anoplodium'sp.~ Leptosynapta bergen- Digestive tract Rather frequent NE Atlanhc Cuenot (19121, Bare1 & sis. Leptosynapta (Plynlouth, Roscoff) Krarners (1970, 1977), galliennei, Leptosy- Kramers (1971) napta inhaerens (H) Bicladusmetacrini Metacrinus Digestive tract 'Occur m enormous N Pacific (Japan: Kaburaki (1925) rotundus (C) number' Sagami Sea) Cleistogamia Holothuria atra, Anterior to midpart of - Great Barrier Reef Cannon (1982) heronensis Holothuna leucospdo- digest~ve tract (Australia) ta (HI Clelstogamia Achnopyga Digestive tract 50 worms In a s~ngle NE Indian Ocean Faust (1924, 1927), holothun'ana mauritiana (H) individual (Faust) (Andaman Islands) Baer (1938) Clejstogamia Actinop yga Unspecified - SW Indian Ocean Hyman (1960) holothunana echinites (H) (endoparasitic) (Madagascar: Nossi-Be) Clejstogarnia Sbcl~opus chloronotus, Anterior to m~dpart of Great Barrier Reef Cannon (1982) long~c~rrus Sbchopus horrens, digestive tract (Australia) Shchopus van'egatus (H) Cleistogamia louftia Holothuria sp. Unspecified - Red Sea Khalil(l938. quoted (endoparasitic) by Stunkard & Corliss 1951) Cleistogamia pallii Bohadsch~argus (H) Antenor to rnidpart of - Great Barrier Reef Cannon (1982) digestive tract (Australia) Clelstoyamia pulchra Actinopyga echinltes, Midpart of digesbve - Great Barner Reef Cannon (1982) Actinopyga lecanora, tract (Australia) Actinopyga mitiaris (H) Cleistogamia Holothuria Antenor part of - Great Barrier Reef Cannon (1982) pyriformis impatiens (H) digestive tract (Australia) Desrnote mops Horornetra Digestive tract 10 to 30 worms NE Pacific (British Kozloff (1965) serratissima (C) crinoid-l (49 infested/ Columbia: satellite 60 investigated) Channel) Desmote vorax Heliometra Unspecified 1 to 20 worms crinoid-' Barents Sea Beklem~shev (1916) gla cialis (C) (endoparasitic) (9 infested/100 inves- (Kola Bay) tigated) Fallacohospes Horometra Digestive tract 2 to 15 worms crinoid-' NE Pacific (British Kozloff (1965) inchoatus serrabssirna (C) (59 infested160 inves- Columbia: satellite tigated) Channel) Macrogynium ovalis lsosbchopus Coelomic cavity; dl- 15 worms Tropical W Atlantic Meserve (1934), badionotus (H) gestive tract holothuroid-' (average (Bermuda) Snyder (1980) number); 36 holothuroids investigated (Snyder)

6 210 Dis. aquat. Org , 1987 Table l (continued) Turbellanan Host Locahon in host Remarks Geographical area Source Monticellina longituba2 ~VotoLhrix inquilina Holothuria ~mpatiens, Coelomic camty Holothuria poli (H) Mensaman'a Digestive tract thornpsoni (H) (anterior part) Ozametra arborum Stichopus D~gestive tract japonlcus (H) Ozametra sp. Parastichopus Digestive tract californicus (H) Paranotothrix Actinopyga echinites, Posterior part of clueenslandensis Actinopyga miliaris. digestive tract Bohadschia argus, Holothuria atra, Holothuria hilla, Holothuna impa tiens, Holothuna leucospilota, Stichopus chloronotus, Stichopus horrens, Stlchopus vanegatus, Thelonota ananas (H) SeriOa elegans Parastichopus D~gestive tract trem ulus (H) (anterior part) Sen'tia striata Stichopus Digestive tract mollis (H) (anterior part) Syndesmis alcalai Heterocen trotus D~gestive tract and mamn~illatus (E) coelornic cavity Syndesmis compacta Echinometra D~gestive tract and oblonga (E) coelomic cavity Syndesrnis dendrastrornum Dendraster excenmcus (E) D~gestive tract Syndesmis echinorum Echin us acutus, Digestive tract and Echjnus esculentus, coelornic camty Paracentrotus livldus. Psarnmechinus rnicrotu berculalvs, Psammechinus miliaris, Sphaerechin us granularis, Strongylocen trotus droebachiensis (E) Syndesrnis aff Strongylocentrotus Digestive tract echinorurn droebachiensis, Strongylocentrotus pallidus (E) Syndesmis glandulosa Diadema setosum. Digestive tract and Echinothriv coelornic cavity calamaris (E) Syndesrnis Echinometra Digestive tract and rnarnmillata oblonga (E) coelormc cavity Syndesmis phdippinens~s Echlnometra oblonga (E) D~geshve tract and coelornic ca%itx Evechinus chloroocus, Digestive tract Hebocidaris erythrogramrna (E) Up to 22 worms holothuroid-' (121 investigated/5 1 infested) Rather frequent Up to 23 worms echinoid-' (Smith); worms consistently present in large number (Orihel) Infestation rate highly variable (see Barel & Kramers 1977) Mediterranean Sea (Naples) Tasmania NW Pacific (Japan Hiroshima) Pacific coast of N America Great Bamer Reef (Australia) North Sea (Norwegian coast) Tasmania NW Pacific (Phihppines: Sumilon Island) NW Pacific (Phd~ppines: Cebu Provmce) E Pacific (California; Washington State) European Seas NE Pacific (Washington: San Juan Island) SW Indlan Ocean (Madagascar Nossi- BC) NW Panfic (Philippines: Negros Oriental Province) NW Pacific (Philippines: Negros Onental Province) Westblad (1953) Hickman (1955) Ozaki (1932) Kozloff in Shinn (1983a) Cannon (1982) Westblad (1926, 1953), Jespersen & Lutzen (1971) Hickman (1955) Komschlies & Vande Vusse (1980a) Komschhes & Vande Vusse (l980b) Stunkard & Corliss (1950, 1951). Orihel (1952), Smith (1973), Shinn (1981) Silliman (1881), Francois (1886), Cuenot (1891). Shipley (19011, Briot (1906b). Westblad (1926). Barel & Kramers (1970, 1977), Lama Seco & Rodriguez Bab~o (1978) Shinn (1981) Hyman (1960), Komschhes & Vande Vusse (l 980a) Komschlies & Vande Vusse (l980a) Komschlies & Vande Vusse (l980a) New Zealand McRae (1959)

7 Jangoux: Diseases of Echinodermata: agents metazoans 211 Table l (continued) Turbellarian Host Locat~on in host Remarks Geographical area Sourcr Syndrs)'r~nx Diadema antillarum Coelo~ni cavlty anmarurn (E) Syndisyrinv Lytechnus Digestive tract and antillarurn vanegatus (E) coelomic cavity Syndisyrinx Echinometra Digestive tract and antillarum vindis (E) coelomic cawty Syndisynnx Spatangus Digest~ve tract atn'ovillosa purpureus (E) Syn disyrinx Strongylocentrotus Digestive tract franciscan us franciscanus, Strong).- locentrotuspurpuratus, Strongylocentrotus droebachlensis, Strongylocentrotus pallidus, Lytechinus anamesus (E) S yn dis yrinx Allocen trotus Digeshve tract franciscanus fragilis (E) SyndisyniLv Lytechn us Digestive tract and francrscanus vanegatus (E) coelomic cavity Syndisyrinx pallida Echinocardiurn Digestive, tract cordatum (E) Syndisyrinxpurucea Helioc~ar~s erythro- Dlgestlve tract gramma, Amblypneustes ovum (E) Umagilla forkalensis Holothuria Digestive tract forskaii (H) Wahlia macrostylifera Isostichopus tremulus (H) Digestive tract Wahlia macrostyhfera Parastichopus Digesbve tract and badionotus (H) coelom~cavlty Wahlia pulchella Stichopus Anterior part of invescaliformcus (H) tine Wahlia stichopi Stichopus chloronotus, Anterior to midpart of Stichopus horrens, Igestlve tract Thelonota ananas (H) 60 worms echinoid-' (average number; 3 infested19 invest)- gated) (Snyder) Troplcal Atlantic (off Flonda: Bermuda) Up to 205 worms ech.inoidci (475 investigatedl350 infestcd) Up to 5 worms Jamaica echinoid-' (219 investigatedl87 infested) Enghsh Channel (Plymouth) Often up to 30 womu in infested echinoid (Lehman, Shinn) Pacific coast of N America (California, Washington) Powers (l 935), Stunkard & Corliss (1951), Mettrick & Jennings (1969), Snyder (1980) Nappi & Crawford (1984) Nappi & Crawford (1984) Westblad (1953) Lehman (1946). Stunkard & Corliss (1951). Giese (1958). Jennings & Mettrick (1968), Bames (1969), Mettrick & Jennings (1969), Mettnck & Boddington (1972). Holt & Mettrick (1975), Shinn ( b) Clese (1958). Hyman (1960) h4aximurn 3 worms NE Pacihc (off Califorech~noid-' (5 mfestedl nian coast) 75 investigated) (Giese) 29 worms echinoid-' Tropical W Atlantic Jennings & Mettnck (average number) (Jamaica) (1968), Jones & Canton (1970) 1 to 4 worms echlnoid-' (l0 infested/68 investigated) Infestation very frequent: up to l8 worms echinoid- ' Up to 14 worms holothuroidc' (29 infestedl47 investigated) (Wahl 1909) Infestation rather frequent Tasman~a (Ralph's Bay) SE In&an Occan (Tasmania: Ralph's Bay) Mediterranean Sea (Naples); North Sea (Nonuegian coast); Enghsh Channel (Plymouth) North Sea (Norwegian coast) 15 worms holo- Tropical M/ Atlantic thuroid-' (average (Bermuda) number) (33 infested1 36 investigated) 2 to 5 worms NE Pacific (coast of holothuroid-' (infesta- Washington) tion level: 62 to 100 % m spri.ng & summer; 0 % in fall and wlnter when host's vlscera are resorbed) Wahl( ). Westblad (1953) Westblad ( ). Jespersen & Liitzen (1971) Snyder (1980) Shinn (1986b) Great Bamer Reef Cannon (1982) (Australia) 111. Rhabodocoela (f. acholadidae and pterastericolidae) Acholades asteris Coscinastenas Encysted in tube feet calamaria (A) wall 20 or more worms as- SW Indian Ocean teroid-' (216 mfectedl (Tasmania: D'Entre- 267 investigated) casteaux Channel) Hickman & Olsen (1955)

8 212 Dis. aquat. Org. 2: , 1987 Table l (continued) Turbellanan Host Location ~n host Remarks Geographical area Source - Plerastencola Pat~nella calcar(a) Pyloric caeca Up to 10 worms as- Hasting Po~nt (New Jennings & Cannon a ustralis teroid-' (407 investi- South Wales, (1985) gated/28 infested) Australia) Pterastencola fedotovi Pterastermil~taris, Unspecified - Barents Sea (Mur- Beklemishev (1916), Pteraster obscurus, (endoparasitic) mansk); White Sea Karling (1970) Pteraster pulvillus (A) (Kandalaksha Bay) Pterastencola Acanthasterplanci (A) Pyloric caeca Infested asteroid may W Pacific (Australia: Cannon (1978), Jenvivipara have large number of central Great Barrier nings & Cannon worms Reef) (1985) Triloborhynchus Astropecten Pyloric caeca 5 to l0 worms per py- North Sea (Norwegian Bashimdin & Karling astropectenis irregularis (A) lonc caecum in in- and Swedish coasts); (1970). Jennings & tested asteroid English Channel (Ply- Cannon (1985) mouth) Tdoborhynchus psilastencola Psilaster andromeda (A) Pyloric caeca, coelomic cavity ljuvenlle forms) Infestation frequent (sometimes more than 10 worms asteroid-') North Sea (Oslo fjord) Jespersen & Liitzen (1972) IV. Polycladida Euplana takewakii Ophioplocus Bursae 20 infested / 200 in- NW Pacific (Japan: Kato (1935) japonicus (0) vestigated Mitsui) ' Species of doubtful validty (Shinn pers. comm.) Synonym of Umagilla forskalens~s, according to Cannon (1982) bodies containing egg capsules of the coelom-associat- hymanae lasts about 1 mo, and embryos remain quiesing Anoplodium hyrnanae may pass out of intact hosts cent in their capsule until they are ingested by a - the holothuroid Parastichopus californicus - through holothuro~d (developed embryos can survive in their any of a series of pores that connect the coelom to the capsules for 10 to 11 mo; Shinn ). Hatching is posterior end of the rectum. Embryogenesis of A. stimulated by some property of the host's digestive Fig. 2. Syndisyrinx franciscanus, a symbiotic turbellarian from the intestine of echlnoids (Strongylocentrotus spp.). (A).Ventral view of a live adult individual. cg: cement glands; ec: bulb of egg capsule; f: filament of egg capsule; fa: female antrum; gp: location of common gonophore; p: pharynx; t: left testis; v: vitellaria. Insert: egg capsule showing bulb and filament. (B) Bulb of a newly produced egg capsule. (C) Bulb of a 2 rno old egg capsule containing 6 fully developed embryos (arrows). (After Shinn )

9 Jangoux: Diseases of Echinodermata: agents metazoans 213 Fig. 3. Anoplodium hyrnanae. Life cycle of a coelom-associated umagillid from the holothuroid Parastichopus californicus. (A) Release of umagillid egg capsules into the host's coelom; (B) ensheathment of egg capsules into brown bodies; (C) completion of embryos' development outside the host; (D) ingestion by the new host of egg capsules containing embryos; (E) hatching of larvae in the upper intestine; (F) migration of larvae towards the respiratory trees; (G) larvae penetrate the wall of the respiratory trees and enter the coelom. (After Shinn 1985b) fluid. Larvae penetrate the wall of the posterior intestine or, more commonly, that of the respiratory trees to reach the coelom (Fig. 3). As demonstrated by Shinn (1985b), the size of A. hymanae infesting P. californicus varies seasonally and is correlated with the seasonal feeding behavior of the host. Investigations by Shinn (1983b, 1985a, b, 1986b) on echinoderm-associated umagillids showed that hatchings are not adversely affected by the host's digestive fluids whatever the final location of the worms in the host. However, adult worms of coelom-inhabiting species are killed by the host's digestive fluid but appear to have some mean of avoiding attack by coelomocytes. Considering the number of species of umagillids that are reported to inhabit both the coelom and gut of the host (see Table l), careful re-examination is needed 'to determine if the worms clearly are adapted to inhabiting very differents sites in their hosts, or whether the reports are the results of improper dissection techniques' (Shinn 1985b, p. 213). Non-umagillid rhabdocoels associated with echinoderms have been reported only from asteroids (Table 1). The acholadid Acholades asteris was always found encysted in the connective tissue layer of the tube feet of Coscinasterias calamaria. Nothing is known on the life cycle of this aberrant rhabdocoel. All pterastericolids found thus far were associated with asteroid pyloric caeca on which they feed (feeding on energy-rich epithelia1 cells; Cannon 1975, 1978, Jennings & Cannon 1985) (Fig. 4 & 5). According to Jennings & Cannon (1985), the occurrence of pterastericolids is independent of host size and sex. These workers noted that the worms neither affect the host's reproductive potential nor produce any marked damages to the asteroid's pyloric caeca. Digestion in Fig. 4. Triloborhynchus psilastencola. Ventral view of a turbellarian parasite of the pyloric caeca of the asteroid Psilaster andromeda. a: entrance to apical organ; bu: bursa; ca: caudal adhesive disk; CO: copulatory bul'b; e: egg capsule in uterus, gp: common genital pore; 1. intestine; m. mouth; o: ovary; p- pharynx; pr: prostatic glands; sh: shell glands; t: testis; v: yolk glands. (After Jespersen & Liitzen 1972) asteroid pterastericolids is predominantly intracellular (their gut is deprived of gastrodermal glands), and Jennings & Cannon suggest this would be 'an adaptative simplification related to the particular diet of host

10 214 Dis. aquat. Org. 2: , 1987 storage and digestive cells, which provides all necessary polyclad species known to be an echinoderm parasite, dietary components plus the enzymes necessary for Euplana takewakii, feeds on ophiuroid gonads, the their digestion a.nd assimilation' (p. 211). The only infested bursae always being castrated (Kato 1935). Pig. 5. Infestation of asteroid pyloric caeca by pterastericolid turbellarians. (A) Psilaster andromeda. Section through pyloric diverticulum containing 3 specimens (A, B, C) of Triloborhynchus psilastencola. ca: caudal adhesive disk; e: egg capsule in uterus; i: intestine; o: ovary; p: pharynx; v: yolk glands; large arrow: area of pyloric diverticulum demolished by specimen; small arrow: piece of ingested tissue from pyloric diverticulum. (B) Acanthaster planci. Section through a pyloric diverticulum showing an individual of Pterastericola vivipara ingesting pyloric tissues. P: pharynx. ([A] after Jespersen & Liitzen 1972; [B] after Cannon 19781

11 Jangoux: Diseases of Echinodermata: agents metazoans 215 Table 2. Parasitic trematodes from echinoderms (compiled from the sources indicated). Hosts: C, crinoid; E, echinoid; H, holothuroid; 0, ophiuroid Trematocle Host Locat~on in host Primary host Remarks Geograph~cal area Source Diph terostomum brusinae Himasthla leptosoma 'Metacercaria psammechini Monorchis monorchis ZNidrosra ophiurae2 Paralepidapedon hoplognathi Proctoeces maculatus Protoeces sp. 2Tetrarhynchus holothuriae3 Zoogonoides viviparud Zoogonoides viviparus Antedon medrterranea (C) lns~de crinoid calyx Several species of (within connective benthic fishes tissue stnngs) Ophiura albida, In wall of digestive Fishes (Anarrhicas Ophjura sarsi (0) sac lupus, Plalessa piatessa; Mortensen) Leptosynapta galliennei, Leptosynapta inhaerens (H) Psammechinus microtubercula tus, Sphaerechrnus granularis (E) Antedon mediterranea (C) In body wall, at base of buccal tentacles; sometimes withm coelomic brown bodies Sea birds (Tringa variabilis, CaD'dns leucophoea) In muscles of Aris- Presumably totle's lantern echmo~d-eating fishes of the family Labridae Inside crinoid calyx Sparid fishes, in (withln connective parocular Spondytissue strings) liosoma cantharus 1 to 15 trematodes crinoid-l; first intermedlary host would be a gastropod mollusc (Nassa sp., Naoca SP.) 1 to 13 trematodes ophiuroid-l: the first intermediary host is bivalve hlucula nucula (Chubdk) Alternative intermediary hosts: bivalve Scrobicularia tenuis, polychete Arenicola manna. sipunculid Phascolosoma vulgare (Cuenot 1912) Infestation may be very heavy 5 to 60 trematodes crinoid-' (17 infestedll51 investigated) Mediterranean Sea Prevot (1966a; see (Marseille) also Palomb~ 1930) Barents Sea (Kola Tauson (1917). Bay); North Sea Mortensen (1921a). (Gullmarfjord) Chubrik (1952, see also Barel & Kramers NE Atlantic (Ar- Cuenot (1892, cachon. Roscoff) 1912). Timon- David (1938) Mediterranean Sea Timon-David (Banuyls, (1934, 1938) Marseille) Mediterranean Sea Prevot (1966a, b) (Marse~lle) Ophiura sarsi (0) In gonads - North Sea (Trond- Mortensen (1933a) hjem fjord) Anthocjdaris Mostly in gonads; Fish Hoplognathus 1 to 66 trematodes Misaki (Japan) crassispina (E) also in muscles of Aristotle's lantern and in ampullae of tube feet Anthocidans In gonads crassispina, Diadema setosum, Nemicen trotus pulchemmus (E) StrongyIocentrotus In gonads intermedjus (E) Molpadra sp (H) Body wall (7) punctatus Ophiura albida, In gonads and Ophiothrix fragilis, coelom wall of Leptosynapta ophiuroids; in body galliennei, Lep- wall of tosynapta in- holothuroids (at haerens (0. H) base of buccal tentacles) Ophiura albida; Mostly behveen F~shes: posterior rarely Ophiura tex- arm vertebrae intestme and recturata and Ophiura (natural infesta- tum of plaice, robusta (0) tion); also within flounder, dab and disc (gonads, water long rough dab vascular system, from Oresund mesenteries) (experimental infestation) echinoid-l (22 infestedi29 investigated) Gastropod Halrotis discus hannal IS alternative intermediary host - M~ght also occur in Mysis sp First intermediary host is gastropod Buccinum undatum, 0. albida is the most important second interme&- ary host. 1 to 30 trematodes ophiuroid-'; up to 250 in experimentally infested ones Misaki (Japan) Shimazu & Shimura 1984 Shimazu & Shimura (1984) Japan Sea (off Shimazu (1979) Maehama. Hokkaido) NE Indian Ocean Shipley (1903) (Malaysian coast) NE Atlantic (Ar- Cuenot (1892, cachon, Roscoff) 1912) North Sea (Kattegat. 0resundl K~ie (1976)

12 216 Dis. aquat. Org. 2: , 1987 Table 2 (continued) Trernatode Host Locat~on ~n host Pnrnary host Remarks Geographcal area Source Zoogonusmlrus Arbac~a Lixula, Pa- In muscles of Ans- Fishes: Labrus 1 to 30 trematodes Mediterranean Sea T~rnon-Damd racentrotus lividus, totle's lantern merula (natural in- ech~noid-', heavy (Banyuls, (1933, 1934, Sphaerechln us festahon), Blenn~us lnfestahon w~th P Marseille) 1938) granulans (E) gattoruglfie (ex- liwdus, slight inperimental mfesta- festahon with hon) A, hula Zoogonus rubellus Arbac~a Presumably ln Eel (natural infes- First intermediary NW Atlant~c Stunkard (1941, punctulata (E) muscles of Aris- tation); toadf~sh host gastropod (Woods Hole) see also Stunkard totle's lantern (experimental ~ n- Nassa obsaleta; 1938) festahon) usual second mtermed~ary hostpolychete Nerels wens Expenrnental use of A. punctulata as alternahve second lntermedary host was partly successful Zoogonus sp Psarnmechmus In muscles of Ans- - l to 36 trematodes North Sea Stunkard (1941) mllians (E) totle's lantern echmo~d-' (Boulogne, Wunereux) ' Previously ]dentdied by Tauson (1917) as Adolescana ophurae The paraslte has been tentatively ascribed to trematodes by Mortensen; it causes destruction of ~nfested gonads Described as encysted larvae of cestode (Shlpley 1903) " Idenhhed by Cuenot ( ) as Cercaria capriciosa Agents: Trematoda Trematodes reported from echmoderms are listed in Table 2. Unidentifed metacercanae were noted by Schneider (1858), in the body cavity of Holothuria tubulosa; by Schurig (1906), in the gut of a deep-sea echinoid; by Ohshima (1911), in stomach and mesenchyme of a planktonic holothuroid larva; by Mortensen (1921b), in gonads of the Japanese echinoid Mespilia globulus; and by Johnson (1971), in gonads of Strongylocentrotus purpuratus. Echnoderms generally act as second intermediary host (Fig. 6). The echinoderm's reaction to invading cercanae or to encysted metacercariae is largely unknown. According to Prevot (1966a) host tissues form a 'xenocyst' of dense connective tissue around metacercanae (Fig.?), but Ksie (1976) reported that infested ophiuroids do not respond to trematode cysts. Effects of metacercanae on their echmoderm host appear to be rather unimportant. According to Ksie (19?6), heavily infested Ophiura albida tend to autotomize their arms. This is presumably linked to the cysts' location at the joints between the arm vertebrae. One may also suggest that, when heavily infested, the jaw muscles of echinoids become less functional (Table 2; Zoogonus rnirus and Zoogonus sp.); thus the cysts may affect echinoid feedng. The location of metacercanan cysts (in muscles or with the body wall) may partly explain why relatively few species of echinoderm-infesting trematodes have been recorded. Whatever the cause, it seems rather obvious that echinoderms are very suitable intermediary hosts for marine digenlc trematodes. Not only do echinoderms occur frequently in very dense population~, but some of their representatives also form part of the &et of many fishes. As seen in Table 2, most echinoderm-infesting trematodes are known from echinoids and ophiuroids which constitute the most frequent echinoderm prey for fishes. The role of echinoderms as potential vectors of trematode-caused fish diseases requires further attention. Agents: Nematoda Rather few nematodes have been reported to occur in echnoderms (e.g. Fig. 8). In addition to the species listed in Table 3, unidentified - and presumably undescribed - nematodes were found inside the host's body (mostly the coelomic cavity): Antarctic asteroids Hymenaster perspicuus and Diplasterias luetkeni (see Ludwig 1903); echinoids Echinus esculentus and Brissopsis lyrifera (respectively Shipley 1901, Brattstrom 1946); holothuroids Leptosynapta spp., Holothuria spp. and Aslia lefevrei (respectively Monticelli 1892, Briot 1906a, Herouard 1923); and North Sea ophiuroids Asteronyx loveni and Ophiura albida (respectively Jungersen 1912, Mortensen 1921a).

13 Jangoux: Diseases of Echinodermata. agents metazoans 217 Fig. 6. Fellodistornum fellis. Lifecycle of a marine digemc trematode with 2 intermediary hosts: bivalve mollusc Nucula tenuls and ophiuro~d Ophlura sarsi. (A) Redia; (B) cercaria; (C) metacercaria; (D) late metacercaria and adult worm. (After Chubnk 1952) F1g. 7. Monorchis rnonorchis (Trema ~toda). Metacercariae encysted witlun connectlve tissue strings of the calyx of the cornatulid crinold Antedon rnediter- ranea. cariae; e: encysted metacerg: gut of the crinoid. (After Prevot 1966a) Intense infestations by juvenile nematodes also occur- ably act as intermediary host, the primary host being red within the digestive wall of the abyssal fishes. This was suggested by Ward (1933) and demonholothuroids Kolga hyalina, Trochostoma thompsoni strated by Pearse & Timm (1971) who identified the and Elpidia glacialis (Danielssen& Koren 1882, Massin pnmary host of the echinoid parasite Echinocephalus pers. comm.). pseudouncinatus as the California horned shark As seen from Table 3 echinoderm-associated Heterodontus fi-ancisci. Host reactions were noted only nematodes are mostly juveniles. Echinoderms presum- by Pearse & Timm (1971) who reported the encystment

14 218 Dis. aquat. Org. suppressed in the infested tubules, especially above the parasite, viz. in the oral or distal part of the tubule. Pearse & Timm suggested that encysted juveniles block the passage through the tubules of some hormonal substance that regulates echinoid gametogenesis. Hagen (1985)implied that infestation of Strongylocentrotus droebachiensis by the nematode Philotrema sp. (= Echinomermella sp.) could be lethal for the echinoid upon hatching of the juvenile nematodes. Agents: Mollusca. Gastropoda Fig. 8. Thalassonerna ophioctinis, a nematode parasite of the ophiuroid Ophiocten amitinum. (A) Oral view of ophiuroid showing ends of nematode protruding through the wall of disc; (B) 5 nematodes coiled within the ophiuroid body cavity. (After Ward 1933) of juvenile nematodes within echinoid gonads. The cyst is host-produced and made of dense connective tissue. Effects of nematodes on their hosts are obvious when the worms destroy the echinoderm's body wall, an injury reported by Ludwig (1903), Ward (1933) and Rubstov (1977). Another, less conspicuous, effect was noted by Pearse & Timm (1971) on gonads of Centrostephanus coronatus: growing juvenile nematodes progressively invaded the gonadal tubules (small juveniles are confined to the gonad wall) and negatively affected host gametogenesis. Gametogenesis is Gastropods living symbiotically with echinoderms belong almost exclusively to the family Eulimidae. According to Waren (1984) there are about 800 species (43 genera) of extant eulimids of which all except 2 are associated with echinoderms. Table 4 lists both ectoand endoparasitic eulimids (species classified as ectoparasites clearly behave as parasites or entertain morphological relations with their host which imply parasitism). Most ectoparasitic eulimids live attached to the echinoderm's body surface, by either their snout or their proboscis (Vaney 1915, Waren 1984). They feed on the host's tissues or fluids using their proboscis which penetrates more or less deeply into the echinoderm's body wall or crosses it to reach the coelomic cavity, the water-vascular system, or the hemal system. However, unattached ectoparasites also occur, e.g. Pulicicochlea calamaris and Vitreobalcis temnopleuncola which browse over the epidermis of the echinoids Echinothrix calamaris and Temnopleurus toreumaticus (Ponder & Gooding 1978, Fujioka 1985, respectively) and Peastilifer nitidulus which moves over the entire body surface of Holothuxia atra, periodically puncturing the body wall of its host (Hoskin & Cheng 1970). Some attached ectoparasitic eulimids are said to feed exclusively on echinoderm dermal tissues. Among them are those belonging to the gallicole genus Stilifer (Tullis & Cheng 1971, Warh 1980a) (Fig. g), as well as representatives of the genera Pelseneena (Koehler & Vaney 1908) and Monogamus (Lutzen 1976). These authors reported that the proboscis is inserted into the dermis but they did not discuss the way in which the dermal tissue is ingested. Dermaltissue-feeding eulimids may induce conspicuous host reactions (Liitzen 1976): the formation of swollen areas which are basically disorganized outgrowths of the connective tissue upon which the parasite feed (Fig. 10). Fluid-feeding ectoparasitic eulimids have also been reported (e.g. Waren 1981~). According to Bacci (1948)

15 Jangoux: Diseases of Echinodermata: agents metazoans 219 Table 3. Parasitic nematodes from echinoderms (compiled from the sources indicated). Hosts: A, asteroid; E, echinoid; 0, ophiuroid Nematode Host Location in host Remarks Geographical area Source Ananus asteroideus Diplopteraster Coelomic cavity One nematode in Antarctic seas (off Rubstov (1977) perigrinator (A) each asteroid arm Kerguelen Islands) Echjnocephalus Arbacia Gonad Only juvenile NW Atlantic Hopkins (l935), pseudouncinatus punctulata (E) nematode observed (Woods Hole) Mlllemann (1951) Echinocephalus Centrostephanus Gonads Most infested E Pacific (Southern Pearse & Timm pseudouncinatus coronata (E) echino~ds had sev- California: Santa (1971) era1 juvenile Catalina Island) nematodes in each of their 5 gonads (142 infested/213 investigated) Marim ermis Hippas feria Coelomic cavity - kerguelensi hyadesi (A) Onchaleimus Echinus Digestive tract - echini esculentus (E) Antarctic seas (off Rubstov & Platono Kerguelen Islands) va (1974) - Leydig (1854) Phllometra grayi Echin us Coelomic cavity 1 to 4 nematodes Around British Isles Gemmil (1901), esculentus (E) echinoid-'; infesta- Gemmil & von Lintion relatively rare stow (1902), Irving (1910), Ritchie (1910, see also Bare1 & Kramers 1977) Philometra sp. Strongylocentrotus Coelomic cavity Infestation level: North Sea (Vest- Hagen [l 983, 1985) droebachiensis (E) 20 30% fjorden, Norway) Thalassonema Ophiacantha an- Coelomic cavity - Antarctic Seas Rubstov (1985) ephiacan this taretica (0) Thalassonema Ophiocten Coelomic cavity 1 to 5 juvenile SW Indian Ocean Ward (1933) ophioctinis arnitium (0) nematodes (South Africa: ophiuroid-' (4 in- Glendower fested/37 investi- Beacon) gated) the proboscis of Melanella comatulicola reaches the coelomic canal of its crinoid host's arm and sucks up coelomic fluid. Cabioch et al. (1978) found that Balcis alba - a temporary holothuroid ectoparasite - penetrates the host's body wall via its proboscis. Aquarium observations have shown that the proboscis does not seek out a specific organ or tissue. It moves actively within the holothuroid coelomic cavity and pumps off coelomic fluid. Aquarium observations further revealed that the point of penetration of the proboscis is not restricted to any part of the body surface. In the field however, it was invariably located immediately below the buccal tentacles. Smith (1984) observed that the -L proboscis of B. alba is unfolded when penetrating the 0 1 2mm holothuroid integument, and that the proboscis Fig. 9. StiD'fer linckiae. Position of 2 specimens of a parasitic epithelium releases secretory material which appears gastropod in a gall in the arm of the asteroid L~nclua laevigata. to bring about a rapid loosening of the host's connec- (After Liitzen 1972a) tive tissue. Fluid-feeding was inferred also with EchineuLima spp., OphieuLima minima and Peastilifer (respectively Liitzen & Nielsen 1975, Waren & Sibuet eduljs, as the proboscis of individuals of these species 1981, Hoskin & Waren 1983). Egloff (1966) and Waren was observed inserted into the host's body cavity (1980a) reported that the proboscis of adult Thyca crys-

16 220 Dis. aquat. Org. 2: , 1987 Table 4. Parasitic gastropods from echinoderms (compiled from the sources indicated). Species names of gastropods according to Waren (1984) Gastropod Host Locatlon in host Remarks Geograph~cal area Source I. Parasites of crinoids Annulobalc~s Crotalometra Attached between 2 specimens known New Zealand (off Waren (1981a) marshalli rustica arm ossicles from slngle host Mayor Island) Balcis devians Antedon bifida Attached to base of Only 1 specimen North Sea (Plymouth) Fretter (1955) pinnule found Eulima ptdocrinida Ptdocnnuspinnatus Proboscis deeply in- - NE Paclfic (off British Bartsch (1907) serted In side of the Columbia) crinoid calix Goodingia varicosa Capillasler Attached to aboral 4 specimens known NE Indian Ocean Lutzen (1972b) multiradiatus side of arms from 2 hosts (New Gu~nea) Melanella Antedon Attached to pinnules, l to l8 gastropods Mediterranean Sea Graff (1874); Bacci coma t ulicola medjterraneas also to calyx or anal clinoid-' (27 infested/ (Naples. Banyuls) (1948); Changeux cone 65 investigated) (1956) Mucronalia Capillaster Attached to the oral - Indian Ocean (Red Bartsch 11909), F~shelcapillastericola multiradjatus side of arms Sea, Singapore) son (1973,1974) Tropiometricola Tropiornelra afra Galls on arms Japan Sea (Honshu) Habe ( ), sphaeroconchus macrod~scus Waren (1981b) 11. Parasites of holothuroids Balcis acicula Stichopus chloronotus Body surface or Tropical W Pacific Habe (1952) coelom~cavity (Fiji, Hawau, Palao) Balcis alba Neopentadacfyla Body surface, near Up to 6 gastropods on NE Atlantic Cabioch et al. (1978) rnhta tentacles single host (aquarium (Irish coast] observation) Balcis catalinensis Fiolothuria arenicola Body surface or Stomach of infested Tropical E Pacific Brand & Ley (1980) stomach hosts harbors 9 to 26 (Mexico: Bay of La gastropods according Paz) to holothuroid size; percentage of infestation 66 to 100 % depending on locality Balcisintermedia Holothuria glaberrirna Firmly attached to out- 1 to 3 gastropods Tropical E Pacific Caso (1968) er body surface holothuroid-' (12 in- (Mexico: Vera Cruz) fested/35 investigated) Diacolax cucumariae Cucumana mendax Parasite protrudes Only 1 specimen Southern Atlantic Mandahl-Barth (1945) outside host body with known (51> 10's. 64> 15'W) its rostrum deeply inserted lnto the holothuroid's coelomic cavity Enteroxenos bouvieri Holothuna atra Coelornic cavity - Tropical W Pacif~c Risbec (1953) (New Caledonia) En teroxenos Parastichopus &re- Mostly hanging in 5 gastropods North Sea Bonnevie (1902). Oesoestergeni rnultls coelomic cavity, holothuroid-l (average (Scandinavian coast) tergren (1938), Liitzen attached to esopha- number) (537 rn- (1979) gus, rarely to stomach fested/l515 investior intestine. Some live gated) (Lutzen) free in coelomic cavity En teroxenos Hanglng in coelorn~c Ca 3 gastropods NE Pacific (Wash~ng- Tikas~ngh (1961, parastichopoli cavity, attached to holothuroid" (average ton: Puget Sound) 1962), Kmcaid (1964). esophagus number) (37 ~nfestedl Lutzen (1979) 244 investigated) (Lutzen) Entocolax chirodotae Chjrodata pellucida Hanging In coelomic - Sea of Japan Skarlato (1951) cavity, attached to body wall (anterior part) En tocolax ludwigl ~4yriotrochus nnki Hanging in coelomic cavity, attached to body wall (anterior part) Behnng Sea (Lorenz Bay)

17

18 222 Dis. aquat. Org. 2: , 1987 Table 4 (continued) Gastropod Host Locatlon in host Remarks Geograplucal area Source Megaden us voeltzko wi Holothuna pardahs Attached to pen-esophagial ring (presumably water-vascular ring) Cloaca Only 1 speclmen known Megadenus sp. Holothuna atra 1 to 3 gastropods holothuroid-' (8 infested/1359 investigated) Melanella muelleriae Molpadicola orien talis Mucronalia varia bilis Paedophorus dicoelobius Actinopyga mauritiana, Holothuria pervicax, Holothuria cmarescens, Holothuria arenicola Molpadia sp. Synapta ooplax Eupyrgus pacificus Projecting from body wall Coelornic cavity Free on host body surface, or in host digestive tract In Polian vesicles or respiratov trees Some indivtduals infested 12 gastropods collected from 3 infested holothuroids (80 inveshgated) Tropical W Indian Ocean (Zanz~bar) Scheprnan & Nierstrasz (1914) NE Indian Ocean Jones & Jarnes (1970) Central Ind~an Ocean (Aldabra) Okhotsk Sea (deep sea) SW Indan Ocean (Zanzibar) NW Paclfic (Peter the Great Bay) Sloan et al. (1979) Grusov (1957) Vaney (l913), Schepman & Nierstrasz (1914) Ivanov (1933,1937) 111. Parasites of echinoids Euchineuluna Chaetodiadema Attached to oral side 1 to 4 gastropods eburnea granulatum, Astropy- of body surface echlnoid-' ga radiata, Astropyga pulvinata. Heterocentrotus mammillatc~s, Heterocentrotus trigonana Euchineulima mittrei Echinothriw diadema, Attached to oral side l to 6 gastropods Echinothriw calamaris, of body surface echinoid-i Diadema setosum, Diadema mexicanum, Diadema savignyi Euchu~eul~rna ponden Parasalen~a gratiosa Attached to penstorne Only 2 speamens from slngle host Luetzenia Asthenosoma sp. Attached to peristome Only 2 spec~rnens asthenosorna trom single host Megadenus cysticolal Stylocidaris tiara Galls in primary 1 to 7 gastropods spines echlnoid-l Monogamus entopodia Monogamus mterspinea Monogamus parasalen~ae Pelseenaria media Pelseenana mlnor Pelseenan-a profunda Echinometra rnathaei Echinometra mathael Tube feet wall 21 gastropods from 10 infested echinolds 2 gastropods from 2 Infested ech~noids (55 mvestigated) Tropical Indo-Pacific Circumtropical Tropical W Pacific (Great Barrier Reef: Lizard Island) SW Paclfic (Austraha: New South Wales) E Indian Ocean (off Ceylon) Red Sea (Gulf of Aqaba) SW Indlan Ocean (Ambolna) Liitzen & Nielsen (1975) Lutzen & Nielsen (1975) Waren (1980a) Waren (1980b) Koehler ( ); Koehler & Vaney (1925) Lutzen (1976) Buned ln skin Liitzen (1976) Parasalenia grariosa Stylocidarrs tiara, Galls In spines Attached to body sur- 2 gastropods from single host - Troplcal Pacific (Tonga Islands) E Indian Ocean (Cey- Stereocidaris indica face, producing con- Ion, Bay of Bengal) sp~cuous test deformations Echlnus affinls Attached to body sur- NE Atlantic (off face Azores: deep sea) Echinus affim's Genocidaris maculata Attached to body surface Attached to body surface 11 echinoids infested (several hundred Investigated) North Sea (Banc de Selne) NE AUantic (off Azores deep sea) Waren (1980b) Koehler (1927) Koehler & Vaney (1908) Koehler & Vaney (1908) Koehler & Vaney (1908)

19 Jangoux: Diseases of Echinodermata: agents metazoans 223 Table 4 (continued) Gastropod Host Location in host Remarks Geographical area Source Pelseenaria stilifera Strongylocentrotus Attached to body 4 gastropods from Balt~c Sea Ankel (1938). droebachiensis, surface s~ngle host (Ankel) (Knstlnenberg) Montensen (1940) Echinus esculentus Pul~cochlea calamaris Echinothrix calamans Free on body surface Rather frequent infes- Troplcal W Pacific Ponder & Gooding Latlon (Hawau, Papua New (1978) Gumea. New Caledonia) Pulicochlea fusca Diadema setosum Free on body surface Numerous gastropods Tropical W Pacific Ponder & Gooding collected (Papua New Guinea (1978) and adjacent islands) Roblllardia cernlca Echinometra mathaei, Attached to wall 1 to 2 gastropods Indian Ocean (Red Gooding & Liitzen Echinon~etra insularis of rectum echinoid-l (54 ~ n- Sea, Mauritius, Am- (1973) fested/l85 Invesh- boma); SW Pacific gated) (Easter Island) SabmeUa mfrapatula Ogmocidaris benhami Attached to body sur- Only l lndivldual SW Pacific (New Zea- Waren (l98la) face. close to periproct found land: off Major Island) Sabinella troglodytes2 Eucjdans tribuloides Galls in primary Infestation relatively Tropical Atlantic Thiele (1925). Pilsbry spines rare (33 infested11467 (Cape Verde lslands, (1956). McPherson investigated) Florida) (1968) (McPherson) Trochostilifer Prionocidaris australis Galls in primary 1 gall with 2 gas- Tropical M' Pacific Waren (1980b) mortenseni spines tropods in each in- (New Caledonia) fested echinoid Vitreobalcis Temnopleurus Attached to body Infestation rate varied Inland Sea (Japan) Fujioka & Habe temnopleuricola toreumaticus surface from 5.3 to 50 de- (1983), Fujioka (1984. pending on host popu- 1985) lation and season IV. Parasites of asteroids Apicalia palmipedis Palmipesrosaceus Attached to body sur- 1 to 2 gastropods per NW Indian Ocean Koehler (1910), face (oral side) infested asteroid (Ceylan, Singapore) Koehler & Vaney (1912), Waren (l98lb) Asterolarnia Craspidaster hesperus Attached to side of - NW Pacific Waren (1980b) c~ngula tus body (marginal plates) (Hong Kong) Asterolamia h~ans Astropecten indicus Attached to aboral Trop~cal Pacific (Great Waren (1980b) body surface, among Bamer Reef) pax~llae Asterophdalapon~ca PediceUastermagis- Coelomic cavity 10 to 29 % asteroids N Pac~fic (off Japan. Randall & Heath ter, Ctenodiscus cris- attached to the body ~nfested depending on Asiahc coast, Alaska) (191 l), Grusov (1965), patus, Leptastenas wall locality (Hoberg et a1 ) Hoberg et a1 (1980) polans, Leptastenas arctica Paramegadenus Anthenoides Open gall on body Tropical \V Pacific Kanazawa & Habe arrhynchus rugulosus surface (aboral side) (Philippines: near (1979). Waren (1980b) Cebu) Paramegadenus Stellasterincei On tube feet Tropical W Pacific Waren (1980b) scu tell~cola (Great Bamer Reef) Parvioris eques~s Stellaster incei Attached to body sur- Indo-West Pacific (An- Koehler (1910). face (marginal plates) daman Islands. Java Koehler & Vaney Sea. Great Barrier (1912). Waren (1981b) Reef] Panrioris morton? Archaster typicus Attached to body sur- 1 to 4 gastropods NW Pacific Morton (1976). face (aboral or lateral asteroid-' (75 infested/ (Hong Kong) Waren (1981b) side) 396 investigated) Stiliferastericola Heliastercumingi Gall in body wall Up to S gastropods E Pacific (Galapagos) Liitzen (1972.a) asteroid-' SLilifer infla tus Linckia laevigata Gall in body wall Only 1 specimen Tropical W Pacific Waren (1980a) known (Great Barrier Reef) Stilifer linckiae Linckia mulbfora Gall in body wall 1 to 2 galls asteroid-' Tropical lndo-west Sarasin & Sarasin (54 mfested/665 inves- Pacif~c (Oman Sea, (1887), Davis (19671, tigated) (Dams) Ceylan, Great Barrier Tullis & Cheng (l971), Reef. Hawau) Lutzen (1972a), Waren (1980a)

20 224 Dis. aquat. Ory. 2, , 1987 Table 4 (continued) l C.;iistropod Host Location ~n host Rcmdrks Geographical arm Source Stil~fer Ophidiaster cribranus, Gall in body wall - oph~diast~ncola Ophld~astcrlor~oli, Ophidldster confestus, Ophldiastergranlfrr Stilifer ovoideus4 Certonardoa semire- Gall in body wall - gulans, Ophid~aster granifer, Tamana dubiosa Stilifer utinornl Linckra guildlng~, Gall in body wall - Linckia laevigata Stilifer sp. Ophldlastergranifer Gall in body wall Up to 4 gastropods asteroid-' (26 mvestigated/8 infested) Thyca callista Phatana unifascialis, Attached to body 1 to 3 gastropods as- Pharia pyrarnldata surface teroid-', infestation rather rare Thyca cristald'na Linck~a rnuldfora, Attached to body Infestation rate vari- Linckia laevigata surface able: from 14 to 62 % depending on localities Thyca ectoconcha Linckia multifora, Attached to body Infestation rate ca 3 % Linckja guildingi surface (MacNae& Kalk) Thyca stellasteris Stellaster equestris Attached to body - surface Troptcal Indo-Paclfic Habe (1976) (Indonesia to SW Japan) Tropical Indo-Pacific Hirase ( ). (Indonesia to SW Lutzen (1972a), Habe Japan) (1976) Troplcal W Pacific Habe (1952), (Great Barier Reef, SW Lutzen (1972a) Japan) Tropical W Pacific Yamaguchi & Lucas (Guam) (1984) Tropical E Pacific (coast of Mexico and central America) Tropical Indo-West Paclf~c (Indonesia, Papua New Guinea. Great Bamer Reet, Fiji) Indian Ocean (Ceylon. Mozambique coast) Indian Ocean (Andaman Islands. West Australia, Red Sea) Berry (1959), Shasky (1961). Bertsch (1975) Egloff (19661, Elder (1979). Waren (1980a). Bouillon & Jangoux (1984) Sarasin & Sarasin (1887). MacNae & Kalk (1962) Koehler (1910). Koehler & Vaney (1912), Waren (1980a) V. Parasites of ophiuroids Fuscapex Ophlocantha sp. Attached to body surophiocan thicola face (oral side). covering bursal slits Ophjeulirna armigen Ophiornc~sium Attached to body surarmigerum face (or4 side), near bursal slits Ophieulima Oph~actisprofundi Attd hed to body surfuscoapica ta face (radial shields) Ophieutima minima Opl~iactis abyssicola Attachcc1 to body sur- - face (aboral side) 3 gastropods from single host Up to 5 gastropods ophlurotd-i (23 infestedlmore than 3000 investigated) 2 gastropods from single host Ophioarachnicola Ophroarachna Attached to bodv sur- Only 1 gastropod hjformis incrassdta face (oral side of arm) found Punctifera Ophlomoensprojecta Open galls (aboral 2 gastropods from ophiomoerae side of the disc) s~ngle host Generic position unclear (see Waren 1980b) Identified as Mucronalia nidorurn by Pilsbry (1956) and McPherson (1968)(see hrarpn 1980b) Idcntifi~d as Eulirna shopldndib) Morton (19761(see Waren 1981b) ' Identified as Stil~fercelebensis by H~rase (1927, 1932) (see Waren 1980a) SW Pacific (off Ker- Waren (1981a) madec Islands, deep sea) NW Atlantic Waren & Carney (off Virgin~a) (1981) SW Pacific (off Ker- Waren (1981a) madec Islands, deep sea) N Atlantic (deep-sea: Waren & Sibuet (1981) off Ireland, off Iceland. Bay of Biscay) Tropical W Pacific (Salornon Islands) SW Pacific (off Kerrnadec Islands: deep sea) Waren (1980b) Waren (1981a) tallina passes through the asteroid's body wall to reach the radial (water-vascular) canal. One may wonder, however, if the ambulacral or coelomic fluids together with coelomocytes can ensure sufficient nutrients for parasites. As noted by Liitzen & Nielsen (1975), additional predation upon internal organs presumably occurs. Other fluid-feeding eulimids insert their pro- boscis into the hemal lacunae of holothuroids (their hemal system has energy-rich contents). Such a symbiosis has been documented by Bouchet & Liitzen (1976, 1980) who studied relations between Pisolamia brychius and the deep-sea holothuroid Oneirophanta mutabilis (Fig. 11). Ectoparasitic gastropods may also feed directly on Internal organs (i.e. digestive organs);