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

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Diseases of Echinodermata. 11. Agents Metazoans (Mesozoa to Bryozoa) DISEASES OF AQUATIC ORGANISMS Vol. 2: 205-234.1981 Published July 30 Dis. aquat. Org. I 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. Associa- tions between echinoderms and sponges, cnidarians, entoprocts or bryozoans have been casually reported in the literature. INTRODUCTION amphiurid Amphipholis squamata (Caullery & Mesnil. 1901, Kozloff 1969, Rader 1982) but it may - if very The present paper is the second of a series of 4 that rarely - also affect other ophiurid species, namely review the diseases of Echinodermata. It considers the Ophiothrix fragilis and Ophiura albida (respectively disease agents belonging to the Mesozoa, Parazoa, Fontaine 1968, Bender 1972). R. ophiocornae is mostly Cnidaria, Acoelomata (Turbellaria and Trematoda), known from European localities (Atlantic coast of Nematoda, Mollusca (Gasteropoda and Bivalvia), France, North Sea, northwest Mediterranean Sea; for Entoprocta and Bryozoa. As discussed in Part I (Jan- reviews see Kozloff 1969, Bare1 & Kramers 1977), and goux 1987), I have adopted the definition of parasites also from 2 Pacific localities along the coast of proposed by Kinne (1980, p. 19) and used it in a very Washington (Kozloff 1969, Rader 1982). broad sense, considering dsease agents (parasites Structure and life cycle of Rhopalura ophiocomae sensu lato) to represent any kind of a harmful associate were studied intensively at the begining of this cen- which affects, if even slightly, the echinoderm's tissues tury, mainly by Caullery & Mesnil (1901) and Caullery or internal fluids (i.e. coelomic and hemal fluids). & Lavallee (1908, 1912) (Fig. 1). Mature adults of R. ophiocomae are free living. Adults, either male or female, develop in Arnphipholis squamata and are DISEASES CAUSED BY METAZOANS emitted through the ophiuroid's bursal slits. Their life span is short (a few days) and they give rise to ciliated Agents: Mesozoa larvae. These infesting larvae penetrate the ophluroid bursal slits and intimately contact the outer epithelium The Mesozoa, a small group of uncertain taxonomic of the bursae. Soon afterwards, small parasitic 'plas- affinity, comprise about 50 species of minute animals modia' occur withln the epithelium. Subsequently, parasitic on marine invertebrates. One species, Rhopa- plasmodia migrate to the coelomic side of the bursae lura ophiocornae, parasitizes ophiuroids. Its most fre- where they remain close to the ovaries. At that time quent host is the small cosmopolitan incubating plasmodia often protude into the coelomic cavity. They C2 Inter-Research/Pnnted m F. R. Germany 206 Dis. aquat. Org. 2. 205-234, 1987 l \'l' I ' @ A, FREE , PARASITIC I 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) are completely surrounded by an epithelia1 layer pre- plasmodia invade the bursal wall. Ovarian regression sumably formed by host mesothelium (Caullery & Mes- implies that infested ophiuroids never harbor incu- nil 1901, Rader 1982). Whether each plasmodium bated embryos. Other consequences of the disease are derived from a whole larva or from one or more cells of a decrease in the ophiuroid's regenerative abilities, as that larva is not known. The plasmodia grow and some well as probably a decrease in its growth rate (Rader of them move along the coelomic lining. Fully 1982). developed plasmodia consist of an enlarged cytoplas- mic (?) mass surrounded by an epithelium of host on- Agents: Parazoa gin. Each plasmodial mass contains numerous small nuclei (the 'plasmodic' or 'vegetative' nuclei), some There are only 2 sponge species known to parasitize germ cells (sometimes called 'agametes') and a few echinoderms. Clark (1896, 1898) reported the occur- embryos at different developmental stages. These are rence of a Grantia-like species firmly attached to the either males or females, embryos of both sexes within outer body surface of several individuals of the the same plasmodium belng exceptional. When holothuroid Synapta vivipara. The sponges always mature, the plasmodium presumably disintegrates and were seen at the base of the holothuroid buccal tenta- numerous adult R. ophiocomae are emitted into the cles. Antarctic ophiuroids of the genus Ophiurolepis outer medium through the host's bursal slit. are very often parasitized by the sponge Iophon The pathogenicity of Rhopalura ophiocomae is radiatus (Mortensen 1936, Fell 1961). The parasite fixes unquestionable. Its most obvious effect is the regres- itself on the ophiuroid, and infestation is generally very sion of host ovaries, while the testes - as noted by extensive, the whole disc and the basal parts of the several authors - remain functional (Amphipholis arms being involved. squamata is hermaphroditic). The parasite does not As shown by Mortensen (1932), the bizarre sponge consume the ovaries; these regress as soon as small Microcordyla asteriae described by Zirpolo (1926) as an Jangoux: Diseases of Echi nodermata: agents metazoans 207 ectoparasite of the asteroid Coscinasterias tenuispina, echinoderms. There is, however, no information on the actually represents a globiferous pedicellaria of the effect of parasitic Turbellaria on the echinoderm life echinoid Sphaerechinus granularis. The pedicellariae cycle. probably were detached in a defensive reaction of S. Gut-associated umagillids may either occur all along granularis (globiferous pedicellariae of echinoids auto- the digestive tract (Smith 1973) or be more or less tomize easily). restricted to some digestive areas (Bare1 & Kramers 1971, Shinn 1981, Cannon 1982; see also Table 1). Holt & Mettnck (1975) reported that Syndisyrinx francis- Agents: Cnidaria canus from the gut of Strongylocentrotus purpuratus feeds mostly on associated ciliates, harbored by the Several sea anemones attach to the body surface of digestive tract of the echinoid. Snyder (1980) could echinoderms. Gravler (1918) noted the occurrence of deternline neither beneficial nor detrimental effects the actinid Sicyopus coinmensalis partly embedded in due to the occurrence of gut-associated umagillids. He the body wall of the deep-sea holothuroid Pseudo- concluded that these symbiotes should be considered stichopus villosus. Kropp (1927) reported echinoids of simply conlmensals. In contrast Shinn (1981) reported the genus Diadema with the sea anemone Aptasia that the gut-associated umagillids always compete tagetas firmly attached to their body surface near the with their host for nutrients and thus may exert adverse anal cone. Other cnidarians may incidentally parasitize effects. He noted that all the umagillids studied by him echinoderms, namely hydrozoans which live attached ingest intestinal host tissue - one of them subsisted to the stem or the cirri of cnnoids. Four crinoid-associ- entirely on that tissue (see also Cannon 1982). Shinn ated hydrozoans are known: Calycella syringa, Cuspi- suggested that gut umagillids parasitise their host to della sp., Lafoea fruticosa, and Stegoporna fastigiata varying degress. Giese (1958) noted that the infestation (Clark 1921). A case of symbiosis between the hydro- level of S. franciscanus in the gut of S. purpuratus zoan Hydractinia vallini and several species of the remains constant throughout the year and does not Antarctic ophiuroid genus Theodoria has been differ whatever the size, sex or gonadal stage of the reported by Smirnov & Stepanyants (1980). This sym- echinoid. In contrast, Wahlia pulchella inhabiting the biosis is similar to the one between Antarctic intestine of Stichopus californicus displays a distinct ophiuroids and sponges. The single known case of annual cycle of infestation related to the annual feed- hydrozoans living on asteroids was reported by Mad- ing cycle of its host (worms do not occur in S. caljfor- sen (1961) who recorded unidentified athecate hy- nicus in fall and winter when the host's vlscera are droids attached to the penstome of the deep-sea resorbed) (Shlnn 1986b). According to Shinn (1980, asteroid Eremicaster gracilis. 198313) egg capsules of the gut-associating S. francis- canus leave the host gut with fecal material. Embryo-
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