Diseases of Echinodermata. 11. Agents metazoans ... - Inter Research

Vol. 2: 205-234.1981 

REVIEW 

DISEASES OF AQUATIC ORGANISMS 

Dis. aquat. Org. I Published July 30 

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. Associa- 

tions 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 (Jan- 

goux 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, Rhopa- 

lura ophiocornae, parasitizes ophiuroids. Its most fre- 

quent host is the small cosmopolitan incubating 

C2 Inter-Research/Pnnted m F. R. Germany 

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 cen- 

tury, 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 'plas- 

modia' 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

206 Dis. aquat. Org. 2. 205-234, 1987 

l \ 'l' I 

FREE , PARASITIC 

I 

are completely surrounded by an epithelia1 layer pre- 

sumably formed by host mesothelium (Caullery & Mes- 

nil 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 cytoplas- 

mic (?) mass surrounded by an epithelium of host on- 

gin. 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 regres- 

sion 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 

' @ 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) infes- 

tation of ophiuroid genital slits; (F) pene- 

tration of the larvae in the ophiuroid bur- 

sal epithelium; (G to I) developing plas- 

modia; (J) male and female plasmodia. 

(After Caullery & Lavallee 1912) 

plasmodia invade the bursal wall. Ovarian regression 

implies that infested ophiuroids never harbor incu- 

bated 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 occur- 

rence 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 tenta- 

cles. 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

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 auto- 

tomize 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 Pseudo- 

stichopus 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-associ- 

ated hydrozoans are known: Calycella syringa, Cuspi- 

della sp., Lafoea fruticosa, and Stegoporna fastigiata 

(Clark 1921). A case of symbiosis between the hydro- 

zoan Hydractinia vallini and several species of the 

Antarctic ophiuroid genus Theodoria has been 

reported by Smirnov & Stepanyants (1980). This sym- 

biosis is similar to the one between Antarctic 

ophiuroids and sponges. The single known case of 

hydrozoans living on asteroids was reported by Mad- 

sen (1961) who recorded unidentified athecate hy- 

droids 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 associa- 

tion 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 sym- 

biotic turbellarians living with echinoderms; of the 68 

species, 9 are Acoela, 58 Rhabdocoela (52 species 

belonging to the family Umagillidae) and 1 Poly- 

cladida. With very few exceptions (Euplana takewalui 

and Acholades asteris; respectively Kato 1935, Hick- 

man & Olsen 1955), almost all echinoderm-associated 

turbellarians live either within the digestive tract or 

within the coelomic cavity of their host. Symbiotic tur- 

bellarians 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 

Jangoux: Diseases of Echi nodermata: agents metazoans 207 

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 francis- 

canus 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 feed- 

ing cycle of its host (worms do not occur in S. caljfor- 

nicus in fall and winter when the host's vlscera are 

resorbed) (Shlnn 1986b). According to Shinn (1980, 

198313) egg capsules of the gut-associating S. francis- 

canus leave the host gut with fecal material. Embryo- 

genesis 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 

198313, 1986a). 

Coelomic umagillids swim in the host's body cavity, 

seemingly without any particular intracoelomic loca- 

tion. 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 organ- 

isms such as ciliates (Mettrick & Jennings 1969, Jen- 

nings 1980). Egg-capsules of intracoelomic umagillids 

of holothuroids frequently occur within brown bodies 

(Briot 1906a, b, Arvy 1957, Changeux 1961, Jespersen 

& Lutzen 1971, Shinn 198313, 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

208 DIS. aquat. Org. 2: 205-234, 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 

Eupyrgus scaber (H) Digestive tract and 

respiratory trees 

Barents Sea Beklemlshev (1915) 

(Murmansk coast) 

blynotrokus rink (H) D~gestive tract 

Barents Sea 


Beklemtshev (1915) 

Chirodota laevis (H) Posterior part of the 

digestive tract 

Spa tangus 

Digestive tract 

purpureus (E) 

Echrnocardiurn 

cordatum (E) 

Avagina incola Echinocardium flavescens,Spatanguspurpureus 

(E) 

Ecl~inocardiurn flavescens 

(E) 

Avagina incola Spatangus 

pupureus (E) 

Avagina vivipara Echinocardic~m 

corda turn (E) 

Faerla echinocardil Echinocardium flaves- 

cens (E) 

Meara stichopi ParasOchopus 

tremulus (H) 

Meara stichopi Parastichopus 

trem ulus (H) 

Meara stichopi Mesothuna 

intestinalis (H) 

S~phon (accessory 

canal) 


Many echinoids 

infested 

5 % of the ech~no~d 

population Infested 

Average infestahon : 

50 worms echinoid-l 

D~gestive tract 3 to 14 worms 

echinoid-' 

(50 echinotds investigated) 

Barents Sea Beklemishev (1915) 


English Channel 

(Plymouth) 

Westblad (1953) 

NE Atlanhc 

(Millport) 

Leiper (1902. 1904) 

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 

11. Rhabdoecoela (I. umagillidae) 

Anoplodiera voluta Parastichopus 

Lrernulus (H) 

Anoplodiera voluta Parastichopus 

trernulus (H) 

Anoplodiera sp. Holoth uria 

arenicola (H) 

Anoplodiopsis gracilis Holothuria 

forskal~ (H) 

~noplodiurn' Ct~~rodota 

ch~rodotae pellucida (H) 

Anoplodium evelinae Unidentified 

holothuroid 

Anoplodium graffi Holothur~a 

impatiens (H) 

Anoplodiurn hymanae Parastichopus 

califon~icus (H) 

l to 8 worms 

holothuroid~' 

North Sea (Norwegian Westblad (1926. 1949) 

coast: Herdla, 

Trondhjem) 

Esophagus North Sea (Oslofjord) Jespersen & Llitzen 

(1.971) 

Coelomic cavity Single observahon North Sea 


Westblad (1926, 1949) 

Digestive tract Up to 90 worms 

holothurold-' 

Anterior part of dlges- 

live tract 

Pharynx Average infestation: 7 

worms holothuro~d-: 

(9 1nfested/l2 investi- 

gated) 

Barents Sea Beklemishev (1915) 


North Sea (Nonvegian Westblad (1926. 1930) 

coast: Herdla, Trondhjern) 

North Sea (Oslofjord) Jespersen & Ltitzen 

(1971) 

Tropical MIAtlantic Snyder (1980) 

(Bermuda) 

Coelomic cavity Up to 9 worms Mediterranean Sea WahI(1906, 1909). 

holothuroids-I (11 infested/47investigated) 

(Wahl 1906) 

(Naples) Westblad (1953) 

Coelomic cavltv Species of doubtful Wh~te Sea Sabussow (1900, 

generic afflruty 

quoted by Barel & 

Kramers, 1977) 

Coelomic cavity Up to 50 worms SW AUantic (Brazil: Marcus (1949) 

holothurold-l Santos Bay) 

Coelomic cavity 

Mediterranean Sea Mont~celli (18921, 

(Naples) 

Wrstblad (1953) 

Coelomic cavtty l to 51 (average l51 NE Pac~f~c (Washing- Sh~nn fl983a; see also 

worms holothuroitfF1 ton coast: Cowlitz Sh~nn 1985bl 

(25 infested/27 Investigated) 

Bay1

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, Leptosynapta 

inhaerens (H) 

Kramers (1971) 

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 

ta (HI 

(Australia) 

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, 

Shchopus van'egatus 

(H) 

digestive tract (Australia) 

Cleistogamia louftia Holothuria sp. Unspecified - Red Sea Khalil(l938. quoted 

(endoparasitic) by Stunkard & Corliss 

1951) 

Cleistogamia pallii Bohadsch~a 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, 

Actinopyga mitiaris 

(H) 

tract (Australia) 

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 investigated) 

(Kola Bay) 

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) 

number); 36 

holothuroids investigated 

(Snyder) 

Snyder (1980)

210 Dis. aquat. Org. 2. 205-234, 1987 


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 

japonlcus (H) 

D~gestive tract 

Ozametra sp. Parastichopus 

californicus (H) 


Paranotothrix 

clueenslandensis 

Actinopyga echinites, Posterior part of 

Actinopyga miliaris. digestive tract 

Bohadschia argus, 

Holothuria atra, 

Holothuria hilla, 

Holothuna impa tiens, 

Holothuna leucospilo- 

ta, 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 D~gestive tract 

excenMcus (E) 

Syndesmis echinorum Echin us acutus, Digestive tract and 

Echjnus esculentus, 

Paracentrotus livldus. 

Psarnmechinus rnicrotu 

berculalvs, 

Psammechinus 

miliaris, 

Sphaerechin us 

granularis, Strongylocen 

trotus 

droebachiensis (E) 

coelornic camty 

Syndesrnis aff Strongylocentrotus Digestive tract 

echinorurn 

droebachiensis, Strongylocentrotus 

pallidus 

(E) 

Syndesmis glandulosa Diadema setosum. Digestive tract and 

Echinothriv 

calamaris (E) 

coelornic cavity 

Syndesrnis 

Echinometra Digestive tract and 

rnarnmillata 

oblonga (E) coelormc cavity 

Syndesmis 

phdippinens~s 

Echlnometra D~geshve tract and 

oblonga (E) coelornic ca%itx 

Evechinus chloroOcus, Digestive tract 

Hebocidaris erythro- 

gramrna (E) 

Up to 22 worms 

holothuroid-' (121 

investigated/5 1 

infested) 

Mediterranean Sea 

(Naples) 

Tasmania 

NW Pacific (Japan 

Hiroshima) 

Pacific coast of 

N America 

Great Bamer Reef 

(Australia) 

Rather frequent North Sea 



echinoid-' (Smith); 

worms consistently 

present in large 

number (Orihel) 

Infestation rate highly 

variable (see Barel & 

Kramers 1977) 

Tasmania 

NW Pacific (Phihppines: 

Sumilon Island) 

NW Pacific (Phd~ppines: 

Cebu Provmce) 

E Pacific (California; 

Washington State) 


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) 

European Seas Silliman (1881), Francois 

(1886), Cuenot 

(1891). Shipley (19011, 

Briot (1906b). Westblad 

(1926). Barel & 

Kramers (1970, 1977), 

Lama Seco & Rodriguez 

Bab~o (1978) 

NE Pacific (Washing- 

ton: San Juan Island) 

SW Indlan Ocean 

(Madagascar Nossi- 

BC) 

NW Panfic (Philippines: 

Negros Oriental 

Province) 

NW Pacific (Philippines: 

Negros Onental 

Province) 

Shinn (1981) 

Hyman (1960), 

Komschhes & Vande 

Vusse (l 980a) 


Vusse (l980a) 


Vusse (l980a) 

New Zealand McRae (1959)



Turbellarian Host Locat~on in host Remarks Geographical area Sourcr 

Syndrs)'r~nx Diadema antillarum Coelo~nic 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 erythrogramma,Amblypneustes 

ovum (E) 

Dlgestlve tract 

Umagilla forkalensis Holothuria 

forskaii (H) 


Wahlia macrostylifera Isostichopus Digestive tract 

tremulus (H) 

Wahlia macrostyhfera Parastichopus Digesbve tract and 

badionotus (H) coelom~c cavlty 

Wahlia pulchella Stichopus Anterior part of inves- 

califormcus (H) tine 

Wahlia stichopi Stichopus chloronotus, Anterior to midpart of 

Stichopus horrens, Igestlve tract 

Thelonota ananas (H) 

111. Rhabodocoela (f. acholadidae and pterastericolidae) 

Acholades asteris Coscinastenas Encysted in tube feet 

calamaria (A) wall 

60 worms echinoid-' 

(average number; 

3 infested19 invest)- 

gated) (Snyder) 


ech.inoidCi (475 investigatedl350 

infestcd) 

Up to 5 worms 

echinoid-' (219 investigatedl87 

infested) 

Often up to 30 womu 

in infested echinoid 

(Lehman, Shinn) 

Troplcal Atlantic (off 

Flonda: Bermuda) 

Powers (l 935), Stunkard 

& Corliss (1951), 

Mettrick & Jennings 

(1969), Snyder (1980) 

Nappi & Crawford 

(1984) 

Jamaica Nappi & Crawford 

(1984) 

Enghsh Channel 

(Plymouth) 

Pacific coast of N 

America (California, 

Washington) 

h4aximurn 3 worms NE Pacihc (off Califor- 

ech~noid-' (5 mfestedl nian coast) 

75 investigated) 

(Giese) 

29 worms echinoid-' Tropical W Atlantic 

(average number) (Jamaica) 

1 to 4 worms 

echlnoid-' (l0 infested/68investigated) 

Infestation very frequent: 

up to l8 worms 

echinoid- ' 


holothuroidC' (29 infestedl47investigated) 

(Wahl 1909) 

Infestation rather 

frequent 

Tasman~a (Ralph's 

Bay) 

SE In&an Occan (Tas- 

mania: Ralph's Bay) 

Mediterranean Sea 

(Naples); North Sea 

(Nonuegian coast); 

Enghsh Channel (Ply- 

mouth) 

North Sea 


15 worms holo- Tropical M/ Atlantic 

thuroid-' (average (Bermuda) 

number) (33 infested1 


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) 


Lehman (1946). 

Stunkard & Corliss 

(1951). Giese (1958). 

Jennings & Mettrick 

(1968), Bames (1969), 

Mettrick & Jennings 

(1969), Mettnck & 

Boddington (1972). 

Holt & Mettrick 

(1975), Shinn (1981. 

1983b) 

Clese (1958). Hyman 

(1 960) 

Jennings & Mettnck 

(1968), Jones & Canton 

(1 970) 

Wahl(1906. 1909). 


Westblad (1926. 1930). 

Jespersen & Liitzen 

(1971) 

Snyder (1980) 

Shinn (1986b) 

Great Bamer Reef Cannon (1982) 

(Australia) 

20 or more worms as- SW Indian Ocean 

teroid-' (216 mfectedl (Tasmania: D'Entre- 

267 investigated) casteaux Channel) 

Hickman & Olsen 

(1955)

212 Dis. aquat. Org. 2: 205-234, 1987 


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 Psilaster Pyloric caeca, Infestation frequent North Sea (Oslo fjord) Jespersen & Liitzen 

psilastencola andromeda (A) coelomic cavity (sometimes more than (1972) 

ljuvenlle forms) 10 worms asteroid-') 

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 quies- 

ing 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 198513). 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 

198313)

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 intes- 

tine; (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 intes- 

tine 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 hatch- 

ings 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-examina- 

tion 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. 2 13). 

Non-umagillid rhabdocoels associated with echino- 

derms 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, Jen- 

nings & Cannon 1985) (Fig. 4 & 5). According to Jen- 

nings & Cannon (1985), the occurrence of pteras- 

tericolids 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 tur- 

bellarian 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 adapta- 

tive simplification related to the particular diet of host

214 Dis. aquat. Org. 2: 205-234, 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


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 

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, Lep- 

tosynapta in- 

haerens (H) 

Psammechinus 

microtubercula tus, 

Sphaerechrnus 

granularis (E) 

Antedon 

mediterranea (C) 

In body wall, at Sea birds (Tringa 

base of buccal ten- variabilis, CaD'dns 

tacles; sometimes leucophoea) 

withm coelomic 

brown bodies 

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 Spondy- 

tissue strings) liosoma cantharus 

1 to 15 trematodes 

crinoid-l; first in- 

termedlary host 

would be a gas- 

tropod mollusc 

(Nassa sp., Naoca 

SP.) 


ophiuroid-l: the 

first intermediary 

host is bivalve 

hlucula nucula 

(Chubdk) 

Alternative inter- 

mediary hosts: 

bivalve 

Scrobicularia 

tenuis, polychete 

Arenicola manna. 

sipunculid Phas- 

colosoma vulgare 

(Cuenot 1912) 

Infestation may be 

very heavy 


crinoid-' (17 in- 

festedll51 investi- 

discus hannal IS al- 

ternative inter- 

mediary host 

- 

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 & Kra- 

mers 19771 

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) 

gated) 

ZNidrosra 

Ophiura sarsi (0) In gonads - North Sea (Trond- Mortensen (1933a) 

ophiurae2 

hjem fjord) 

Paralepidapedon Anthocjdaris Mostly in gonads; Fish Hoplognathus 1 to 66 trematodes Misaki (Japan) Shimazu & Shimhoplognathi 

crassispina (E) also in muscles of punctatus echinoid-l (22 in- 

ura 1984 

Aristotle's lantern 

festedI29 investiand 

in ampullae of 

tube feet 

gated) 

Proctoeces Anthocidans In gonads 

Misaki (Japan) Shimazu & Shimmaculatus 

crassispina, Diadema 

setosum, 

Nemicen trotus 

pulchemmus (E) 

ura (1984) 

Protoeces sp. StrongyIocentrotus In gonads 

Gastropod Halrotis Japan Sea (off Shimazu (1979) 

intermedjus (E) 

Maehama. 

Hokkaido) 

2Tetrarhynchus 

holothuriae3 

Zoogonoides 

viviparud 

Zoogonoides 

viviparus 

Molpadra sp (H) Body wall (7) 

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, 

mesenteries) (experimentalinfestation) 

from Oresund 

M~ght also occur in 

Mysis sp 

First intermediary 

host is gastropod 

Buccinum un- 

datum, 0 . albida is 

the most important 

second interme&- 

ary host. 1 to 30 

trematodes 

ophiuroid-'; up to 

250 in experimen- 

tally infested ones 

NE Indian Ocean Shipley (1903) 

(Malaysian coast) 

NE Atlantic (Ar- Cuenot (1892, 

cachon, Roscoff) 1912) 

North Sea K~ie 

(1976) 

(Kattegat. 

0resundl

216 Dis. aquat. Org. 2: 205-234, 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, 1936. 

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~aryhostpolychete 

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 (1892. 1912) 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 mesen- 

chyme of a planktonic holothuroid larva; by Mortensen 

(1921b), in gonads of the Japanese echinoid Mespilia 

globulus; and by Johnson (1971), in gonads of Strongy- 

locentrotus 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 auto- 

tomize 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 unde- 

scribed - 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, Bratt- 

strom 1946); holothuroids Leptosynapta spp., 

Holothuria spp. and Aslia lefevrei (respectively Mon- 

ticelli 1892, Briot 1906a, Herouard 1923); and North 

Sea ophiuroids Asteronyx loveni and Ophiura albida 

(respectively Jungersen 1912, Mortensen 1921a).

Fig. 6. Fellodistornum fellis. Life- 

cycle of a marine digemc tre- 

matode with 2 intermediary hosts: 

bivalve mollusc Nucula tenuls and 

ophiuro~d Ophlura sarsi. (A) Re- 

dia; (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 rnediterranea. 

e: encysted metacercariae; 

g: gut of the crinoid. (After 

Prevot 1966a) 

Jangoux: Diseases of Echinodermata. agents metazoans 217 

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 demon- 

holothuroids 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

218 Dis. aquat. Org. 

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 Centro- 

stephanus coronatus: growing juvenile nematodes 

progressively invaded the gonadal tubules (small 

juveniles are confined to the gonad wall) and nega- 

tively affected host gametogenesis. Gametogenesis is 

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 hor- 

monal substance that regulates echinoid gameto- 

genesis. Hagen (1985)implied that infestation of Stron- 

gylocentrotus droebachiensis by the nematode 

Philotrema sp. (= Echinomermella sp.) could be lethal 

for the echinoid upon hatching of the juvenile 

nematodes. 

Agents: Mollusca. Gastropoda 

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 197 1, 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)


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 

nematodes in each 

of their 5 gonads 

(142 infested/213 

investigated) 

Catalina Island) 

Antarctic seas (off Rubstov & Platono 

Kerguelen Islands) va (1974) 

- Leydig (1854) 

Marim ermis Hippas feria Coelomic cavity - 

kerguelensi hyadesi (A) 

Onchaleimus Echinus Digestive tract - 

echini esculentus (E) 

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 investigated) 

Beacon) 

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 

proboscis of B. alba is unfolded when penetrating the 

-L 

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 connective 

tissue. Fluid-feeding was inferred also with 

(After Liitzen 1972a) 

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-

220 Dis. aquat. Org. 2: 205-234, 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~shel- 

capillastericola multiradjatus side of arms Sea, Singapore) son (1973,1974) 

Tropiometricola Tropiornelra afra Galls on arms Japan Sea (Honshu) Habe (1974.1976), 

sphaeroconchus macrod~scus Waren (1981b) 

11. Parasites of holothuroids 

Balcis acicula Stichopus chloronotus Body surface or Tropical W Pacific Habe (1952) 

coelom~c 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 infesta- 

tion 66 to 100 % de- 

pending 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 investi- 

gated) 

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 in- 

serted lnto the 

holothuroid's coelomic 

cavity 

Enteroxenos bouvieri Holothuna atra Coelornic cavity - Tropical W Pacif~c 

(New Caledonia) 

Risbec (1953) 

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 investi- 

En teroxenos 

or intestine. Some live gated) (Lutzen) 

free in coelomic cavity 

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) 

Lutzen (1979) 

Entocolax chirodotae Chjrodata pellucida Hanging In coelomic 

cavity, attached to 

body wall (anterior 

part) 

- Sea of Japan Skarlato (1951) 

En tocolax ludwigl ~4yriotrochus nnki Hanging in coelomic 

Behnng Sea 

cavity, attached to 

body wall (anterior 

part) 

(Lorenz Bay)

222 Dis. aquat. Org. 2: 205-234, 1987 


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 

Melanella muelleriae Actinopyga mauritiana, 

Holothuria pervicax, 

Holothuria 

cmarescens, 

Holothuria arenicola 

Molpadicola 

Molpadia sp. 

orien talis 

Mucronalia varia bilis 

Paedophorus 

dicoelobius 

Projecting from body 

wall 

Synapta ooplax Free on host body surface, 

or in host digestive 

tract 

In Polian vesicles or 

respiratov trees 

holothuroid-' (8 in- 

fested/1359 investi- 

gated) 

Some indivtduals in- 

fested 

Tropical W Indian 

Ocean (Zanz~bar) 

Scheprnan & Nier- 

strasz (1914) 

NE Indian Ocean Jones & Jarnes (1970) 

Central Ind~an Ocean 

(Aldabra) 

Coelornic cavity Okhotsk Sea 

(deep sea) 

Eupyrgus pacificus 12 gastropods col- 

lected from 3 infested 

holothuroids (80 in- 

veshgated) 

111. Parasites of echinoids 

Euchineuluna Chaetodiadema Attached to oral side 1 to 4 gastropods 

eburnea granulatum, Astropyga 

radiata, Astropyga 

pulvinata. Heterocentrotus 

mammillatc~s, 

Heterocentrotus 

trigonana 

of body surface echlnoid-' 

Euchineulima mittrei Echinothriw diadema, Attached to oral side l to 6 gastropods 

Echinothriw calamaris, of body surface 

Diadema setosum, 

Diadema mexicanum, 

Diadema savignyi 

echinoid-I 

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 

Echinometra rnathaei 

Echinometra mathael 

Tube feet wall 21 gastropods from 10 

infested echinolds 

2 gastropods from 2 

Infested ech~noids (55 

mvestigated) 

SW Indan Ocean 

(Zanzibar) 

NW Paclfic (Peter the 

Great Bay) 

Sloan et al. (1979) 

Grusov (1957) 

Vaney (l913), Schepman 

& Nierstrasz 

(1914) 

Ivanov (1933,1937) 

Tropical Indo-Pacific Liitzen & Nielsen 

(1975) 

Circumtropical Lutzen & Nielsen 

(1975) 

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) 

Waren (1980a) 

Waren (1980b) 

Koehler (1924. 1927); 

Koehler & Vaney 

(1925) 

Lutzen (1976) 

Buned ln skin Liitzen (1976) 

Monogamus 

Parasalenia grariosa Galls In spines 2 gastropods from Troplcal Pacific Waren (1980b) 

parasalen~ae 

single host 

(Tonga Islands) 

Stylocidarrs tiara, Attached to body sur- - 

E Indian Ocean (Cey- Koehler (1927) 

Stereocidaris indica face, producing consp~cuous 

test deformations 

Ion, Bay of Bengal) 

Pelseenaria media Echlnus affinls Attached to body sur- 

NE Atlantic (off Koehler & Vaney 

face 

Azores: deep sea) (1908) 

Pelseenana mlnor Echinus affim's Attached to body sur- 

North Sea (Banc de Koehler & Vaney 

face 

Selne) 

(1908) 

Pelseenan-a profunda 

Genocidaris maculata Attached to body sur- 11 echinoids infested NE AUantic (off Koehler & Vaney 

face 

(several hundred Investigated) 

Azores deep sea) (1908)



Gastropod Host Location in host Remarks Geographical area Source 

Pelseenaria stilifera Strongylocentrotus Attached to body 4 gastropods from Balt~c Sea Ankel (1938). 

droebachiensis, 

Echinus esculentus 

surface s~ngle host (Ankel) (Knstlnenberg) Montensen (1940) 

Pul~cochlea calamaris Echinothrix calamans Free on body surface Rather frequent infes- Troplcal W Pacific Ponder & Gooding 

Latlon (Hawau, Papua New 

Gumea. New 

Caledonia) 

(1978) 

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) (1 968) 

(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 

Asterolarnia Craspidaster hesperus Attached to side of - NW Pacific 

(1912), Waren (l98lb) 

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 

pax~llae 

Bamer Reef) 

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 

polans, Leptastenas 

arctica 

wall locality (Hoberg et a1 ) Hoberg et a1 (1980) 

Paramegadenus Anthenoides Open gall on body Tropical \V Pacific Kanazawa & Habe 

arrhynchus rugulosus surface (aboral side) (Philippines: near 

Cebu) 

(1979). Waren (1980b) 

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)

224 Dis. aquat. Ory. 2, 205-234, 1987 


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 

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 sur- 

fuscoapica ta face (radial shields) 

Ophieutima minima Opl~iactis abyssicola Attachcc1 to body surface 

(aboral side) 

- 

3 gastropods from 

single host 

Up to 5 gastropods 

ophlurotd-I (23 in- 

festedlmore 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) 

Troptcal Indo-Paclfic Habe (1976) 

(Indonesia to SW 

Japan) 

Tropical Indo-Pacific Hirase (1927. 1932). 

(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 (Anda- 

man 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) 

SW Pacific (off Ker- Waren (1981a) 

madec Islands, deep 

sea) 

NW Atlantic Waren & Carney 

(off Virgin~a) (1981) 


madec Islands, deep 

sea) 

N Atlantic (deep-sea: Waren & Sibuet (1981) 

off Ireland, off Iceland. 

Bay of Biscay) 

Tropical W Pacific Waren (1980b) 

(Salornon Islands) 


rnadec Islands: 

deep sea) 

tallina passes through the asteroid's body wall to reach boscis into the hemal lacunae of holothuroids (their 

the radial (water-vascular) canal. One may wonder, hemal system has energy-rich contents). Such a sym- 

however, if the ambulacral or coelomic fluids together biosis has been documented by Bouchet & Liitzen 

with coelomocytes can ensure sufficient nutrients for (1976, 1980) who studied relations between Pisolamia 

parasites. As noted by Liitzen & Nielsen (1975), addi- brychius and the deep-sea holothuroid Oneirophanta 

tional predation upon internal organs presumably mutabilis (Fig. 11). Ectoparasitic gastropods may also 

occurs. Other fluid-feeding eulimids insert their pro- feed directly on Internal organs (i.e. digestive organs);

226 Dis. aquat. Org. 2: 205-234, 1987 

this has been suggested by Waren (1980b) for 2 species 

of Asterolamia. 

Little information is available on the feeding biology 

of intradigestive eulimids. An unusual feeding habit 

was reported for 2 unattached species of holothuroid- 

associated snails, Mucronalia variabilis and Balcis 

catalinensis, symbiotic with Synapta ooplax and 

Holothuria arenicola (respectively Vaney 1913, Brand 

& Ley 1980). The snails move freely on the body surface 

of their host but may enter the host's digestive tract in 

order to feed by puncturing the digestive wall. The 

presence of several individuals of B. catalinensis in the 

stomach of H. arenicola does not cause significant 

effects on the absorption efficiency of the host (Brand & 

Ley 1980). Gooding & Liitzen (1973) provide evidence 

that Robillardia cernica, which inhabits the rectum of 

the echinoid Echinometra insularis, feeds on host 

gonads, using its elongated proboscis. Megadenus 

oneirophantae lives in cyst-like swellings in the diges- 

tive wall of a deep-sea holothuroid. According to 

Bouchet & Lutzen (1980), it supposedly feeds on con- 

tent of the digestive hemal lacunae. A most unusual 

feeding habit is that of Megadenus cantharelloides: it 

attaches to the digestive wall of Stichopus chloronotus 

- the visceral mass of the parasite protruding into the 

digestive cavity - with its proboscis crossing both 

digestive wall and coelomic cavity and penetrating the 

host's body wall, in order to feed on dermal tissue 

(Humphreys & Lutzen 1972). 

Oral feeding by intracoelomic eulimids has been 

inferred only for Gasterosiphon deimatis which inserts 

its proboscis into digestive hemal lacunae (Koehler & 

Vaney 1903). Other intracoelomic forms (viz. the 

aberrant Entocolax and allied genera, i.e., the former 

Entoconchidae; e.g. Tikasingh & Pratt 1961, Liitzen 

1968, 1979, Byrne 1985) are believed to derive their 

energy from the host's coelomic fluid by direct absorp- 

tion of nutrients through their body wall. Intracoelomic 

parasitic gastropods occur only in asteroids (eulimid 

genus Asterophila) and in holothuroids (eulimid genera 

Diacolax, Enteroxenox, En toconcha, Gasterosiphon, 

Molpadicola, Paedophorus, Thyonicola) (Table 4; Fig. 

12 & 13). Most of them are attached to the coelomic side 

of either digestive tract or body wall of their host by a 

hollow stalk or by a siphon. Although some authors 

have suggested that feeding could take place through 

that duct (Heath 1910, Tikasingh 1962), such a 

hypothesis has not been accepted generally. 

Harmful effects of parasitic gastropo!~ are not 

restricted to their feeding activities. Ectoparasitic 

eulimids may produce clearly definable attachment 

lesions (Liitzen & Nielsen 1975, Liitzen 1976, Elder 

1979). Host reactions produce conspicuous soft swel- 

lings of the dermal tissue in parasitized echinoid tube 

feet (Lutzen 1976) and in infested crinoid pinnules 

oct 

Fig. 12. Enteroxenos oestergreni, an intracoelomic gastropod 

parasite of the holothuroid Stichopus tremulus. ct: ciliated 

tubule; m: modified male implanted in receptaculum mas- 

culinum; p: pit in the wall of host's esophagus; rs: remains of 

stalk of another individual; S: stalk; oct: opening of ciliated 

tubule, ot: ovarian tubules; ou: opening of uterus; ov: oviduct, 

U: uterus. (After Lutzen 1979) 

(Bacci 1948, Fretter 1955). Gallicole eulimids (e.g. 

Stilifer spp., Puctifera ophiomoerae, Tropiornetncola 

sphaeroconchus; Table 4) produce spectacular hard 

swellings or galls in the body wall of asteroids, 

ophiuroids and cnnoids. These galls resemble those 

induced by myzostomids on crinoid arms. Whether or 

not they involve particular modifications of host skele- 

ton has not been investigated. According to Davis 

(1967) S. linckiae suppresses the autotomizing capabil- 

ity of the asteroid arm in which it is located. Other 

gallicole species modify primary spines of cidaroid 

echinoids (Koehler & Vaney 1925, Koehler 1927, Pils- 

bry 1956, Waren 1980b). In most cases the snails bore 

into the distal part of spines which then enlarges. 

Sometimes spine-dwelling gastropods appear to

Fig. 13. Myriotrochus rinki. Holothuroid parasitized by 3 

ovigerous specimens of the intracoelomic gastropod Entocolax 

ludwigi. 1: oral end; 2: ovary; 3: oviduct; 4: part of the body 

containing intestine; 5: pseudopallium with egg capsules; 6: 

siphon. (After Liitzen 1979) 

induce a conspicuous regression of the host skeleton, 

the spine being reduced to its swollen basal part 

(Koehler & Vaney 1925). Nothing is known of the 

feeding habits of these spine-associated eulimids. The 

host skeleton is also affected by non-gallicole species. 

Fishelson (1973, 1974) reported that Mucronalia 

capillastericola attaches to crinoid arms and causes a 

prononced twist and degeneration of the arm skeleton 

above the place of attachment. Koehler & Vaney (1912) 

and Vaney (1913) drew attention to the particular gaps 

occurring in the marginal skeleton of asteroids infested 

by Parvioris equestris. According to them, the absence 

of marginal plates is the consequence of the early 

attachment of parasitic snails which had inhibited 

skeletal growth. Eulimids parasitizing cidaroid 

echinoids may induce conspicuous test swellings im- 

plying deformations of the test skeleton (Doderlein 

1906, Koehler 1927) (Fig. 14). Pyriform test deforma- 

tions caused by a Mucronalia-like species were 

reported by Mortensen (1943) for the echinoid Salmacis 

bicolor. According to Byrne (1985) the intracoelomic 

eulimid Thyonicola arnericana for the most part did not 

appear to affect its holothuroid host Eupentacta quin- 

quesemita. She noted, however, that heavily para- 

sitized hosts could be detected by their apparent inabil- 

ity to keep their tentacles fully retracted and that, in 

some cases of mass infestation, the parasites may inter- 

Jangoux: Diseases of Echinodermata agents n-~etazoans 227 

Fig. 14, Stereocjdaris tricarinata. Oral view of cidaroid 

echinoid showing test deformations produced by parasitic 

gastropods (Stilifer sp.). (After Doderlein 1906) 

fere with the use of the holothuroid's tentacles for 

suspension feeding. 

That parasitic eulimids may produce partial castration 

of the host was considered by Gooding & Liitzen 

(1973). They found the size of the gonads in echinoids 

infested by Robillardia cernica to be usually smaller 

than in uninfested echinoids. According to Heding & 

Mandahl-Barth (1938), intracoelomic Entocolax spp. 

may castrate their host; in contrast Liitzen (1979) 

reported that Enteroxenox oestergreni is not likely to 

influence the fecundity of the holothuroid Paras 

tichop us trem ul us. 

Few host reactions have been reported from 

echinoderms parasitized by gastropods, except the 

induction of dermal swellings and galls. This does not 

imply of course that echinoderms do not react to snail 

infestations. A particular host-parasite relation must be 

noted, namely the constant presence of a host envelope 

surrounding the intracoelomic entoconchid eulimids 

from holothuroids (Vaney 1913, Tikasingh 1962, 

Wright 1974). This envelope consists of an outer 

mesothelial layer and of an inner connective tissue 

layer. Considering the unsolved question of entoconchid 

nutrition, it would be worth investigating whether 

or not host hemal lacunae occur within the inner layer 

of the envelope. A similar envelope was found around 

individuals of Asterophila japonica, an intracoelomic 

entoconchid from asteroids (Hoberg et al. 1980). The 

mesothelial cover surrounding intracoelomic gas-

228 Dis. aquat. Org. 2: 205-234, 1987 

tropods should occur presumably around any part of 

the parasitic snail which permanently crosses the 

coelomic cavity (a mesothelial covering of the parasite 

proboscis has been noticed by Waren [1980b] for 

Asterolamia hians). 

So far there are practically no data indicating that 

parasitism by eulimids can seriously alter the 

echinoderm life cycle. Eulimids do not - or only excep- 

tionally - produce host castration, nor do they have any 

measurable effect on the biology of their host, not even 

when mass infestations occur. (It may be presumed, 

however, that eulimids involving skeletal deformations 

are rather constraining for the echinoderms.) All these 

facts suggest that the ecological consequences of para- 

sitism due to eulimid gastropods may be quite limited 

for the echinoderms involved. 

Agents: Mollusca. Bivalvia 

Bivalves associated with echinoderms have been 

recorded almost exclusively from echinoids and 

holothuroids (Boss 1965). Most echinoid-associated 

bivalves are simply attached to the host's spines 

through byssal threads (e.g. Gage 1966, Barel & Kra- 

mers 1977). However, Bernard (1895, 1896) described a 

species (Scioberetia australis) which lives in the brood 

pouches of the Antarctic spatangoid Abatus caver- 

nosus. According to Bernard, only females of A. caver- 

nosus without S. australis had developing embryos in 

their brood pouches. This might imply that the bivalves 

inhibit the development of embryos or prevent their 

settlement in brood pouches. 

A few bivalve species live ectosymbiotically on 

synaptid holothuroids. They attach to the synaptid 

body surface through their spade-shaped creeping 

foot. It is generally agreed that creeping bivalves do not 

affect their host, except that they may slightly erode its 

skin (Anthony 1916, Popham 1940). Three species of 

endosymbiotic bivalves have been reported from 

holothuroids. There is almost no information on the 

relations between Holothuria fuscocinena and 

Entovalva major which is said to supposedly live in the 

holothuroid cloaca (Bruun 1938). Entovalva mirabilis 

and Cycladoconcha amboinensis inhabit small pouches 

dug into the digestive wall of synaptid holothuroids 

(respectively Voeltzkow 1890, Schepman & Nierstrasz 

1914; Sparck 1931). These 3 species are presumably 

typical suspension feeders. 

Agents: Entoprocta 

A few Loxosomatidae appear to be relatively com- 

mon symbiotes of crinoids and ophiuroids, especially in 

polar and subpolar areas. Mortensen (1910, 1911) 

reported the occurrence of Loxosomella antedonis on 

cirri of Poliometra prolixa and Heliometra glacialis. L. 

antedonis appears to secrete a cement on the surface of 

the crinoid cirri and then attach to its host. The 

ophiuroid Amphiocnida pilosa often supports individu- 

als of Loxosoma sp. attached to various places of the 

oral side of its disc and arms (Mortensen 1924). Accord- 

ing to Moyano & Wendt (1981) the entoproct Barentsia 

discreta may attach to the bivium of the Antarctic 

holothuroid Psolus charcoti. 

Agents: Bryozoa 

Bryozoans may be found firmly attached to the body 

surface of comatulid crinoids, mostly to their arms or 

cirri. They were recorded by Mortensen (1910) on 

PoLiometra prolixa, and by Gautier (1959) on Lep- 

tometra phalangium. According to Gautier, about 25 % 

of the cnnoid population was infested (6 different 

species of bryozoans were associated with L. phalan- 

gium). Moyano & Wendt (1981) report that up to 4 

different species of Bryozoa were seen attached to the 

outer body surface of the Antarctic holothuroid Psolus 

charcoti. 

Acknowledgements. I thank Drs. J. Jennings, 0. Kinne, J. M. 

Lawrence. G. Shinn and A. Waren for information and criti- 

cism; Dr. C. Massin for helping with literature research; and 

N. Biot, Dr. G. Coppois. M. Doize, and J. Harray for assisting 

In the preparation of the manuscript and ilIustrations. 

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