Nemerteans as hosts for symbionts: a review

Nemerteans utilize other animals as hosts in a variety of well‐studied, symbiotic relationships, but relatively little is known concerning nemerteans as hosts for other organisms. Only three haplosporidians, one microsporidian, two gregarines, three ciliates, five mesozoans, one mite and one copepod have been identified to species from nemerteans, whereas 34 nemertean species (one Archinemertea, 17 Heteronemertea, 15 Hoplonemertea, one Bdellonemertea) have been recorded as hosts. The majority of recorded nemertean symbionts are endoparasitic protozoans and orthonectids. Among the Haplosporidia, there are three species of Haplosporidium. The hyperparasite, Nosemoides vivieri, from an unidentified gregarine, is the only known microsporidian associated with a nemertean. Within the phylum Apicomplexa, besides the two species of gregarines from three species of nemerteans, there are 11 other species of nemerteans with unidentified gregarines. One species of nemertean has been found with an unidentified coccidian parasite. ‘Sporozoan‐like’ parasites, however, are known from three other species of nemerteans, two of which are pelagic polystiliferans. Two endosymbiotic and one ectosymbiotic species of ciliates have been identified from three species of nemerteans. At least five species of mesozoans (Orthonectida) infect nine species of nemerteans. Unidentified cestode, trematode and nematode juveniles, using nemerteans as intermediate hosts, have been recorded rarely and have not been linked to any life cycles. An ectosymbiotic mite and a copepod from two species of nemerteans are likely incidental associates. The nature of the host–symbiont relationships has been rarely reported. Castration of hosts by haplosporidians and orthonectids, and tissue damage by an unidentified coccidian and some gregarines, are known to occur. The suitability of nemerteans as hosts for parasites, hypersymbioses and approaches for future studies of parasite prevalence and host–parasite relationships are discussed.

[1]  H. Kajihara,et al.  A new genus and species of monostiliferous hoplonemertean (Nemertea: Enopla: Monostilifera) from Japan , 2001, Hydrobiologia.

[2]  J. Moore,et al.  Terrestrial nemerteans thirty years on , 2001, Hydrobiologia.

[3]  J. McDermott Status of the Nemertea as prey in marine ecosystems , 2001, Hydrobiologia.

[4]  J. Norenburg,et al.  Morphology and taxonomic distribution of a newly discovered feature, postero-lateral glands, in pelagic nemerteans , 2001, Hydrobiologia.

[5]  J. McDermott Nemertea inhabiting the Haploops (Amphipoda) community of the northern Øresund with special reference to the biology of Nipponnemertes pulcher (Hoplonemertea) , 1993, Hydrobiologia.

[6]  A. Kuris Life cycles of nemerteans that are symbiotic egg predators of decapod Crustacea: adaptations to host life histories , 1993, Hydrobiologia.

[7]  I. Varndell Catechol oxidase activity associated with sporogenesis inHaplosporidium malacobdellae, a balanosporidan endoparasite of the hoplonemerteanAmphiporus lactifloreus , 1981, Zeitschrift für Parasitenkunde.

[8]  I. Varndell A histochemical study ofHaplosporidium malacobdellae, a balanosporidan endoparasite of the hoplonemerteanAmphiporus lactifloreus , 1981, Zeitschrift für Parasitenkunde.

[9]  J. Moore,et al.  Further observations on the genus Geonemertes with a description of a new species from the Philippine Islands , 2004, Hydrobiologia.

[10]  J. Norenburg,et al.  Reproductive biology of several species of recently collected pelagic nemerteans , 2004, Hydrobiologia.

[11]  J. Norenburg,et al.  Observations on musculature in pelagic nemerteans and on pseudostriated muscle in nemerteans , 2004, Hydrobiologia.

[12]  J. O. Wern An enigmatic heteronemertean from the Gulf of Mexico , 2004, Hydrobiologia.

[13]  J. Shields CD-ROM REVIEW , 2001 .

[14]  J. Shields OVICIDES JULIEAE N. GEN., N. SP. (NEMERTEA: CARCINONEMERTIDAE) ON XANTHID CRABS FROM THE GREAT BARRIER REEF, AUSTRALIA , 2001 .

[15]  G. Vernet,et al.  Avance dans la connaissance des mésozoaires. Etude de la spécificité d'Intoshia linei, Orthonectide parasite de Némertes linéides , 1997 .

[16]  G. Vernet,et al.  Rhopalura sanguinea sp. nov. nouvel Orthonectide parasite de l'Hétéronémerte Lineus sanguineus , 1996 .

[17]  Ray Gibson,et al.  Nemertean genera and species of the world: an annotated checklist of original names and description citations, synonyms, current taxonomic status, habitats and recorded zoogeographic distribution , 1995 .

[18]  P. Sundberg,et al.  The nemerteans (Nemertea) of Rottnest Island, Western Australia , 1995 .

[19]  E. Kozloff The Structure and Origin of the Plasmodium of Rhopalura ophiocomae(Phylum Orthonectida) , 1994 .

[20]  G. Vernet,et al.  Avance dans la connaissance des mésozoaires. Etude de la spécificité d'Intoshia linei (Orthonectide) par greffe interspécifique de tronçons de Lineus (Heteronemertes) parasites sur des sujets sains , 1994 .

[21]  G. Vernet,et al.  Avance dans la connaissance des mésozoaires, morphologie et anatomie des adultes de Rhopalura linei (Orthonectides) , 1993 .

[22]  E. Kozloff The genera of the phylum Orthonectida , 1992 .

[23]  M. Slattery,et al.  Energetic composition, biomass, and chemical defense in the common antarctic nemertean Parborlasia corrugatus McIntosh , 1991 .

[24]  E. Kozloff Malacobdella siliquae sp.nov. and Malacobdella macomae sp.nov., commensal nemerteans from bivalve molluscs on the Pacific coast of North America , 1991 .

[25]  C. Langlet,et al.  Reactions of Linues ruber to orthorectids in various stages of development , 1989 .

[26]  J. Norenburg Redescription of a brooding nemertine, Cyanophthalma obscura (Schultze) gen. et comb.n., with observations on its biology and discussion of the species of Prostomatella and related taxa * † , 1986 .

[27]  R. Gibson Redescription and taxonomic reappraisal of Nemertopsis actinophila Bürger, 1904 (Nemertea: Hoplonemertea: Monostilifera) , 1986 .

[28]  R. Gibson Antarctic nemerteans: Heteronemertea– descriptions of new taxa, reappraisals of the systematic status of existing species and a key to the heteronemerteans recorded south of latitude 50oS , 1985 .

[29]  W. Kem Structure and Action of Nemertine Toxins , 1985 .

[30]  J. H. Stock Redescription et statut générique de Pseudanthessius nemertophilus (Gallien, 1936), copépode poecilostomatoïde associé a Lineus longissimus des côtes de la Manche , 1985 .

[31]  John J. Lee,et al.  An illustrated guide to the protozoa , 1985 .

[32]  J. McDermott The feeding biology of Nipponnemertes pulcher (Johnston) (hoplonemertea), with some ecological implications , 1984 .

[33]  E. Egan The seasonal reproductive cycle of the nemertean Gononemertes australiensis Gibson in relation to that of its ascidian host, Pyura pachydermatina (Herdman) , 1984 .

[34]  R. Gibson Craticulïneus novaezealandiae gen. et sp. nov., a new lineid heteronemertean from the South Pacific (Nemertini) , 1984 .

[35]  R. Gibson Nemerteans of the Great Barrier Reef: 5. Enopla Hoplonemertea (Monostilifera) , 1982 .

[36]  S. P. Parker Synopsis and classification of living organisms , 1982 .

[37]  R. Gibson Nemerteans of the Great Barrier Reef: 2. Anopla Heteronemertea (Baseodiscidae) , 1981 .

[38]  I. Varndell The Occurrence, Life History and Effects of Haplosporidium malacobdellaeJENNINGS and GIBSON in a New Host, the Monostiliferous Hoplonemertean Amphiporns lactifloreus (JOHNSTON) , 1980 .

[39]  P. Sundberg Tubulanus annulatus, an aposematic nemertean? , 1979 .

[40]  J. Moore,et al.  Haplosporidium prostomae sp. nov., a New Sporozoan from the Freshwater Hoplonemertean Prostoma eilhardi (Montgomery) , 1979 .

[41]  E. Egan,et al.  The Reproduction of the Entozoic Nemertean Gononemertes australiensis Gibson (Nemertea: Hoplonemertea : Monostylifera)–Gonads, Gametes, Embryonic Development and Larval Development , 1979 .

[42]  P. Roe LIFE HISTORY AND PREDATOR-PREY INTERACTIONS OF THE NEMERTEAN PARANEMERTES PEREGRINA COE , 1976 .

[43]  D. Vinckier Nosemoides gen. n., N. vivieri (Vinckier, Devauchelle & Prensier, 1970) comb. nov. (Microsporidie); Etude de la Différentiation Sporoblastique et Genèse des Différentes Structures de la Spore* , 1975 .

[44]  R. Gibson A new species of commensal hoplonemertean from Australia , 1974 .

[45]  J. Moore,et al.  A new genus of freshwater hoplonemertean from New Zealand , 1973 .

[46]  G. Prensier,et al.  Nosema vivieri n. sp. (Microsporidae, Nosematidae) hyperparasite d'une grégarine vivant dans le coelome d'une némerte. , 1970 .

[47]  R. Gibson Studies on The Biology of The Entocommensal Rhynchocoelan Malacobdella Grossa , 1968, Journal of the Marine Biological Association of the United Kingdom.

[48]  R. Gibson Occurrence of the entocommensal rhynchocoelan, Malacobdella grossa, in the oval piddock, Zirfaea crispata, on the Yorkshire coast , 1967, Journal of the Marine Biological Association of the United Kingdom.

[49]  T. Fenchel Ciliates from Scandinavian molluscs , 1965 .

[50]  L. Laubier Parhalixodes travei n.g., n.sp., a new Halixodinae (Halacarids) ectoparasite of Nemerte in occidental Mediterranean , 1960 .

[51]  J. B. Jennings OBSERVATIONS ON THE NUTRITION OF THE RHYNCHOCOELAN LINEUS RUBER (O. F. MÜLLER) , 1960 .

[52]  W. S. Hunter The nemertean, Cerebratulus lacteus, as an intermediate host for cestode larvae. , 1950, The Journal of parasitology.

[53]  W. McIntosh,et al.  A Monograph of the British Annelids , 2011, Nature.