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Epizoic and Parasitic Rotifers Hydrobiologia 186/187: 59-67, 1989. C. Ricci, T. W. Snell and C. E. King (eds), Rotifer Symposium V. 59 © 1989 Kluwer Academic Publishers. Printed in Belgium. Epizoic and parasitic rotifers Linda May Institute of Freshwater Ecology, Edinburgh Research Station, Bush Estate, Penicuik, Midlothian EH26 OQB, Scotland, UK Key words: epizoic, parasitic, rotifers Abstract Many rotifer species live in close association with plants or other animals. Most of these associations are of a commensal or synoecious nature, some rotifer species having lost the ability to live independently. Few rotifers are true parasites, actually harming their hosts. The Seisonidae, Monogononta and Bdelloidea include epizoic and parasitic species. The most widely known are probably the parasites of colonial and filamentous algae (e.g. Volvox, Vaucheria). However, rotifers are also found on a wide range of invertebrates: colonial, sessile Protozoa; Porifera; Rotifera; Annelida; Bryozoa; Echinodermata; Mollusca, especially on the shells and egg masses of aquatic gastropods; Crustacea, including the lower forms (e.g. Daphnia, Asellus, Gammarus) and in the gill chambers of Astacus and Chasmagnathus; the aquatic larvae of insects. There appear to be few records of epizoic or parasitic rotifers among vertebrates, apart from Encentrum kozminskii on carp, Limnias ceratophylli on the Amazonian crocodile, Melanosuchus niger, and an unidentified Bdelloid apparently living as a pathogenic rotifer in Man. Introduction This paper reviews the literature which de- scribes parasitic or epizoic associations between Rotifers have long been known to live in close rotifers and other organisms. Much of this litera- association with other organisms, but little is ture was published in the late 1800's and early known of the types of relationships involved. It is 1900's, when naturalists spent many hours ob- difficult to judge from the literature whether these serving the behaviour of live specimens. Many of associations are parasitic, symbiotic, commensal, the species names given by the original authors epiphytic or epizoic. Many of the records are are now out-of-date; these have been updated, as simply anecdotal and, while some authors have far as possible, according to Harring (1913), guessed at the type of relationship involved, few Bartos (1951), Kutikova (1970) and Koste (1978). have based their guesses on careful biological This review is not exhaustive and, in many observation. For the purposes of this paper, a ways, adds little to the information given by parasitic rotifer is considered to be one which Budde (1925) because the topic has received so lives in or on a plant or animal species, feeding on little attention since that time. Hopefully, how- its host and completing its life cycle in that envi- ever, the details given below, organised according ronment. In contrast, an epizoic rotifer is defined to the type of host, will renew interest in this much as a rotifer which lives on another animal for all neglected area of rotifer research. The text is or part of its life, but does not feed on its host. divided into sections according to the kingdom 60 and, in some cases, the phylum (after Barnes 1984) by P. werneckii has been recorded in a variety of to which the various 'host' organisms belong. Vaucheria species, including V. prona, V. gemina- ta, V. dillwynii, V. erythrospora, V. ?racemosa and V. canalicularis (Davis & Gworek, 1973; Ott, Parasitic and epizoic associations 1977; Christensen, 1987). In general, the rotifer enters the developing gametophore of the Vauche- Protistaand Monera ria filament where it induces gall formation. Here it feeds on the cytoplasm of the host by breaking Rotifer parasites are common among colonies of the tonoplast and ingesting the cytoplasmic orga- Volvox, especially V. globator (Williams, 1852; nelles. The rotifer deposits its eggs within the Gosse, 1852; Hood, 1895; Galliford, 1946), galls; these hatch and the emergent rotifers escape V. aureus (Rousselet, 1911; Sauer, 1978), and to parasitise more filaments (Davis & Gworek, V. tertius (Ganf et al., 1983). These rotifers have 1973; Ott, 1977). been identified as Proales parasita (Ehr.) (Wil- Many rotifers are thought to be parasitic on liams, 1852; Thompson, 1892; Rousselet, 1911, protozoa, including Dicranophorus difflugarium 1914; Harring & Myers, 1922; Rich & Pocock, (Penard) on Difflugia acuminata var. inflata (Pen- 1933; Hollowday, 1949; Wulfert, 1960; Sauer, ard, 1914; Koste, 1978), Brachionus rubens Ehrb. 1978), Ascomorphella volvocicola (Plate) (Gosse on colonies of Carchesium, Proalesparasita and 1852; Hood, 1895; Murray, 1906; Galliford, Pleurotrochapetromyzonon colonies of Ophridium, 1946; Ganf et al., 1983) and, more rarely, Cepha- and Albertia vermisculus Dujardin on Limax lodella catellina volvocicola (Zawadovsky) (Ed- species (Koste, 1978). In contrast, Eosphora gibba mondson & Hutchinson, 1934). Parasitism in Garner seems to have a commensal association Ascomorphella volvocicola seems to be specific to with colonies of Carchesium and Vorticella, the Volvox species, as this rotifer has never been ob- rotifer benefiting from the food carried towards it served on other phytoplankton species, or living in the strong water currents generated by the freely (Ganf et al., 1983). The mature rotifer enters protozoa (Hollowday, 1949). the Volvox colony and feeds on the cells causing extensive damage (Hood, 1895; Hollowday, 1949; Ganf et al., 1983). Whether this actually Fungi causes the Volvox population to decline is un- certain (Ganf et al., 1983). Garner (1937) records Macrotrachela fungicola Rotifers have also been recorded as parasites Garner living in the gelatinous, orange-yellow on other colonial algae, Ptygura melicerta (Ehrb.) fungus Dacrymyces deliquescens on decayed on Gloeotrichia(Edmondson, 1940; Koste, 1978), wood, in Britain. M.fungicola is probably an Proalesparasita on Uroglenopsis americana (Car- ectoparasite of this fungus, but the exact relation- lin, 1939), Proales uroglena and P. parasita on ship between the species is unclear. Uroglena (Koste, 1978). Little is known of the relationships between these species. Rotifers have long been known to parasitise Plantae Vaucheria filaments (Lister, 1884; Thompson, 1892; Brain, 1894; Wollny, 1879), although these Bryophyta early authors were unsure of the identification of Although bdelloid rotifers are often found living the rotifer species involved. Later descriptions among mosses, few could be thought of as para- showed that Vaucheria filaments are usually para- sites. Habrotrocha roeperi (Milne) and Habrotro- sitised by Proales werneckii (Ehrb.) (Jennings, cha reclusa (Milne) may be the exceptions, as they 1894; Harring & Myers, 1922; Davis & Gworek, actually live inside the outer cells of submerged 1973; Ott, 1977; Christensen, 1987). Parasitism branches of Sphagnum (Milne, 1888; Bartos, 61 1951). Whether they simply live inside the empty trophi to suck out the body fluids. Among these cells, filtering food from the surrounding water parasites are Cephalodella parasitica (Jennings), (Milne, 1888), or whether they are true parasites, found on a variety of freshwater oligochaetes (e.g. is unknown. Vejdovkyella comata, Stylaria lacustris, Chaetogas- ter spp., Nais spp.) (Jennings, 1894; Beauchamp, 1905; Koste, 1972, 1978), and Drilophaga buce- Animalia phalus Vejdovsky, found on oligochaetes (e.g. Lumbriculus variegatus, Rhynchelmis sp., Stylodril- Porifera us sp., Nais elinguis) (Vejdovsky, 1883; Koste, Several rotifer species have been found living in 1978) and the body and posterior sucker of close association with the freshwater sponge leeches (e.g. Herpobdella octoculata, H. nigricollis, Spongilla lacustris in lakes of southern Sweden H. testacea and Hirudo medicinalis) (Pawlowski, (Berzins, 1950). The first, Ptygura melicerta 1935; Koste, 1978). Murray (1906) also records (Ehrb.) does not seem to injure the sponge in any Proales daphnicola as living epizoically on oligo- way and appears to have a commensal asso- chaetes. However, his identification of the rotifer ciation with its host. This species is invariably species in thought to be incorrect (Dr W Koste, found around the pores and oscula of the sponge, pers. comm.). taking advantage of the increased food supply Endoparasitic rotifers of worms were originally carried in the water currents generated by its host. discovered by Dujardin (1838) who found Albertia However, Lecane clara (Bryce) and Lepadella vermisculus in the expressed body fluids of triba Myers, do appear to be true parasites. They earthworms and slugs. The parasites live in the graze on the sponge itself, leaving furrows up to gut of their host and most belong to the genera 50 m deep in the surface tissues. Neither of these Albertia (A. vermisculus, A. crystallina Schuiltze, species appears to be an obligate parasite, as both A. naidis Bousfield, A. reichelti Koste, A. bernhar- are also found swimming freely and have no di Hlava) and Balatro (B. calvus Claparede, B. fri- particular adaptation to a parasitic way of life. dericiae Kunst, B. anguiformis Issel, B. aciliatus (Radkevitsch)). The hosts of Albertia species in- Rotifera clude the freshwater oligochaetes Stylaria spp. Records of rotifers parasitising other rotifer (e.g. S. proboscidae, S. lacustris) (Levander, 1894; species are rare. However, it has been noted that Hlava, 1905; Murray, 1906; Koste, 1969, 1970), Acyclus inquietus Leidy is parasitic on colonies of Nais species (Hudson & Gosse, 1886; Bilfinger, Sinatherina socialis
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