Epizoic and Parasitic Rotifers

Home , Albertia, Callidina, Eurotatoria, Rotaria, Rotifer

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 describes 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 Many of the records are are now out-of-date; these have been updated, as simply anecdotal and, while some authors have far as possible, according to Harring (1913), guessed at the type of relationship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, Eosphoragibba 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 parasites. 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 (Linne) (Koste, 1968), while 1894; Koste, 1969, 1978), Paranaislitoralis, Ripis- Proales decipiens (Ehrb.) attacks Stephanoceros tis parasita (Koste, 1978), and the earthworm fimbriatus (Goldfusz) (Stevens, 1907). In the for- Allolobophora caliginosa(Rees, 1960), while Bala- mer case, the parasite feeds on the newly hatched tro species are more commonly found in the guts young of its host. In the latter, P. decipiens, only of Henlea ventriculosa, H. perpusila, Fridericiabul- one tenth the size of Stephanoceros, enters the bosa, F. perrieri, Trichodrilus sp., Buchholzia ap- protective tube and feeds on the adult and its pendiculata, Enchytraeus buchholzi and E. albidus developing eggs. The parasite lays its own eggs (Claparede, 1868; Hudson & Gosse, 1886; within the tube and these subsequently hatch, and Koste, 1978). The rotifers attach themselves firm- leave in search of new hosts. ly to the intestine of their host by grasping, with their trophi, the small papillae of the intestinal Annelida mucosa (Rees, 1960). A firm attachment is essen- Segmented worms and leeches have both ecto- tial to prevent the rotifer being dislodged by the and endo-parasitic rotifers. The ecto-parasites peristaltic movements of the intestine, and the live on the epidermis of the host, feeding on the pressure of food moving along the gut. A detailed epidermal cells and piercing the skin with their study of Albertia naidis in the gut of Nais elinguis 62 has shown that the rotifer feeds on cells from the tomentosa (Pfeiffer) in Australia. This author con- intestine wall of its host and does not ingest any cluded that the many rotifer species found in the of the algal remains passing through the worms natural habitats, and in laboratory cultures, of digestive tract (Coineau & Kunst, 1964). these snails had no harmful effects. Had he looked more closely at the egg masses, his con- Mollusca clusions may well have been different. One of the first records of rotifers parasitising Freshwater snails (e.g. Lymnaea tomentosa, freshwater snails was published by Glascott Biomphalariaalexandrina, B. galbrata,B. pfeifferi, (1893), who observed the rotifer Notommata gi- Bulinus truncatus) are of particular interest to gantea Glascott, inside the eggs of the common researchers because of their associations with water snail. Stevens (1912) also observed this parasitic infestations such as schistosomiasis, bil- rotifer in the eggs of Limnaea auriculariaL. and harzia, and liver flukes. Many workers in this area Paludina vivipara L., although he concluded that have complained of infestations of rotifers in their it belonged to another genus and renamed it experimental cultures which have caused a variety Proales gigantea (Glascott). Stevens (1912) de- of problems (Stirewalt & Lewis, 1980; Hassan scribed the rotifer in detail, including an interest- etal., 1985; J.M. Jewsbury, pers. comm.; G.J. ing account of its life history. The adult nibbles Greer, pers. comm.). Stirewalt & Lewis (1980), through the outer shell of the snail egg, wriggles for example, describe how Rotaria rotatoriaPallas through the hole and enters the shell. It then and Philodina acuticornis Murray colonize the begins to feed on the fluid surrounding the snail snail shells, beginning at the centre of the whorl embryo, killing the embryo within a few days. The and developing over the entire surface. A serious adult rotifer lays up to 13 eggs, one at a time, infestation can result in snails looking as though inside the snail egg. She then moves on to parasi- they are 'wearing fur coats' (J.M. Jewsbury, pers. tise a new egg, or dies and is eaten by her progeny. comm.). These rotifers seem to live commensally The developing eggs hatch and the first to hatch on the adult snails, but, like Proalesgigantea, their feed on the remains of the snail egg before escap- main effect is on the egg masses. Hassan et al. ing to parasitise another egg. Those which hatch (1985) have recorded up to 100% mortality later tend to starve. P. gigantea seems to be a true among young snails (up to the blastula stage) in parasite, spending most of its life cycle inside the rotifer-infested cultures. The reason for this is snail egg. It was only found outside an egg for unclear, but the authors suggest that it may be due short periods as it travelled through the jelly-like to an irritating effect of the rotifer, or to the effect substance of the egg mass to parasitise another of its excretory products on the ootheca of the egg egg. mass and on the embryo it contains. These results Similar observations were made by Giard have led the authors to propose that rotifers could (1908) & Nekrassow (1928), who also noticed be used in the biological control of these snails. that the eggs of several other snail species (e.g. A further effect of parasitic rotifers on disease- Lymnaea stagnalis L., L. auriculariaL., L. ovata spreading snails is described by Stirewalt & Lewis Drap., Myxas glutinosa Mall., and Physafontinalis (1980). They found that, in their studies of L.) were similarly parasitised by P. gigantea. Nek- Biomphalaria galbrata infected with Schistosoma rassow (1928) also noted that L. stagnalis eggs mansoni, cercariae production fell from 3123 cer- were parasitised less often than those of other cariae/snail/day to 591 cercariae/snail/day when species, and suggested that this may be because their cultures became infested with Rotaria rota- the outer shell of its eggs is tough and difficult to toria and Philodina acuticornis. They also found penetrate. that the cercariae which did emerge showed re- These early observations on Proales gigantea duced motility and infectivity. This effect occur- appear to be in contrast to the later findings of red not only in the presence of rotifers, but also Boray (1964), from ecological studies of Lymnaea in rotifer-conditioned water from which the roti- 63 fers themselves had been removed. The swimming water currents generated during swimming and activity (speed and distance) of the cercariae was filter feeding (Viaud, 1947). The rotifer attaches greatly depressed and their ability to penetrate the itself by its foot to the carapace of its host, and skin of their potential hosts (mice) was reduced by apparently benefits from this association by 50%, compared to the penetration rate of 'non- feeding on the excrement of the cladoceran rotifer cercariae'. (Schltiter, 1984). Another rotifer which is often found on the Bryozoa carapace of Daphnia is Proales daphnicola Philodina megalotrocha Ehrb. is the only rotifer (Thompson, 1892; Harring & Myers, 1922; Beau- which has been recorded as living on Bryozoa. champ, 1923; Galliford, 1946; Hollowday, 1949; This species was found in clusters around the Koste, 1968). This rotifer attaches itself firmly to upper parts of Lophopus crystallinus by Pittock its host by means of its pedal cement glands; it (1894). The authors notes that even newly hatch- also fixes its eggs to the carapace. P. daphnicola ed young polypides were heavily infested. Col- appears to gain nothing from the association, onies of this rotifer seemed to establish themselves apart from transportation (Hollowday, 1949). on the shoulders of the bryozoan in order to take Other rotifers which are also epizoic on Clado- advantage of the plentiful food supply drawn into cera, but occur less frequently, include Testudinel- the area by the bryozoan's feeding activity; a la epicopta Myers on Acantholeberis curvirostris colony of Lophopus creates a strong vortex in the (Myers, 1934), Brachionus variabilis (Hempel) on surrounding water which brings food particles Daphnia longispina and Ceriodaphnia longispina towards it. There was no evidence that Philodina (Hempel, 1896; Ahlstrom, 1940), Collotheca volu- was actually parasitic on the Lophopus itself, but tata var. sessilis Sebestyen on Monospilus dispar the rotifer seemed to gain considerable benefit (Sebestyen, 1937) and Brachionusnovaezealandiae from the association (Pittock, 1894). (Morris) on Pseudomonia lemnae, Daphnia carina- ta and Ceriodaphnia species. Crustacea Rotifers also occur as ectoparasites on species Epizoic and parasitic rotifers have often been of the marine opossum shrimp Nebalia. Koste found on marine and freshwater Crustacea. They (1975) found Seison annulatus Claus among the are particularly common among freshwater Cla- thoracic appendages which the shrimp uses to docera, where some rotifer species occur on a filter organic detritus. The rotifer also attaches its wide variety of hosts. Brachionussessilis Varga has eggs to the base of the gills of its host. Paraseison been found on Diaphonosoma excisum Sars in nudus Plate, P. proboscideus Plate and P. ciliatus India and Sri Lanka (Chengelath etal., 1973; Plate have also been found attached to the bran- Sharma, 1979), on Diaphanosomasarsii Riahrd in chial lamellae of Nebalia species (Plate, 1888). India (Sharma, 1979) and on Diaphanosomabra- These rotifers attach themselves by means of chyurum Lieven in Hungary (Varga, 1931); this mucus secreted from their pedal gland. rotifer species has always been found on the same Rotifers have been found on the thoracic and genus of cladoceran over a wide geographical area abdominal appendages, and the branchial plates, (Chengelath et al., 1973). In contrast, Brachionus of the freshwater louse Asellus aquaticus (Giglioli, rubens is more widely distributed among the Cla- 1863; Hudson & Gosse, 1886; Bilfinger, 1894; docera. Although mostly found on Daphnia Hood, 1895; Rousselet, 1898; Murray, 1906; species (e.g. D. magna, D. pulex, D. longispina) Hofsten, 1909; Galliford, 1946; Hollowday, (Bryce, 1924; Galliford, 1946; Viaud, 1947; Hal- 1949; Bartos, 1951). Most of these rotifers belong bach, 1973; Koste, 1978; Schliter, 1984), it has to 3 main genera, namely Rotaria (R. socialis also been recorded on the carapace of Moina recti- Kellicott, R. magna-calcarata Parsons), Testudi- rostris and Polyphemus pediculus (Koste, 1978). nella (T. elliptica (Ehr.), T. truncata (Gosse), The rotifer is attracted towards a Daphnia by the T. caeca (Parsons)) and Embata (E. parasitica 64

(Giglioli), E. laticeps (Murray), E. commensalis glass, the rotifers often expelled epithelial cells (Western)). These rotifers do not appear to cause ingested from the hosts gills. These observations any harm to their host and are generally consider- indicated a parasitic association between the ed to be epizoans, gaining nothing but transpor- species. The type of association between the tation from their association with Asellus. species mentioned earlier is not known. The branchial plates and appendages of Gam- marus pulex are another common site for epizoic Uniramia rotifers (Gigliolo, 1863; Hudson & Gosse, 1886; Many rotifers live epizoically on the aquatic larvae Plate, 1886; Hood, 1895; Murray, 1906; Varga, of insects, especially those of the dragonfly (Ro- 1931; Bartos, 1951; Koste, 1968, 1978). These are taria rotatoria, Brachionus rubens, B. caudatus mostly of the genus Embata (E. parasitica(Giglio- Barrois) (Chandra& Kameswara, 1976; Sharma, li), E. laticeps (Murray), E. hamata), although 1979), damselfly (Lepadella ovalis Mller, Proales daphnicola, Philodina convergens Murray, B. caudatus) (Chandra & Kameswara, 1976; Dicranophorus hauerianus var. siedleckii Sharma, 1979) and mayfly (Philodina convergens, Wiszniewski and Encentrum grande (Western) Murray) (Bartos, 1951). Epizoic rotifers have also have also been found. Again, none of these been found on the cases of caddis larvae (Rotaria species seems to have adverse effects on the host. tardigrada Ehr., Embata parasitica, Habrotrocha A variety of rotifer species are commonly found collarisEhrb.) (Scherren, 1897; Bartos, 1951) and in the branchial cavities of the freshwater crayfish, attached to the body and legs of the waterboat- Astacus species (Carlin, 1939; Koste, 1978). man, Corixa sp. (Albertia naidis Bousfield, B. ru- These include Lepadella astacicola Hauer, bens) (Varga, 1931; Koste, 1978). Little is known L. branchiola Hauer, L. parasiticaHauer, L. bor- of the relationship between these rotifers and their ealis Harring, L. Wiszniewski, Cephalodella cras- hosts, but the associations are not thought to be sipes (Lord) and several varieties of Dicranophorus truly parasitic. hauerianus Wiszniewski (Carlin, 1939; Koste, 1978). L. borealis, L. astacicola, L. lata and Echinodermata D. hauerianus have also been found in the gill Zelinkiella synaptae (Zelinka) has been found in cavity of the crayfish Cambarus affinis (Carlin, great abundance living in the body cavities of the 1939; Wulfert, 1957; Koste, 1978). Little is echinoderms Synapta inhoerens and S. digitata known of the relationship between these species, (Lankester, 1868 (?); Zelinka, 1888; Cuenot, but the rotifers may well be true parasites of these 1892). No detailed information of this relation- Crustacea. ship is given, but Cuenot (1892) suggests that Rotifers have also been found in the branchial Zelinkiella is commensal on the integument of the chambers of both freshwater and marine crabs. Echinoderm, and is unlikely to be a true parasite. Piovanelli (1903) describes two bdelloids, Macro- trachela cancrophila (Piovanelli) and Anomopus Chordata telphusae (Piovanelli), from the branchial chamber An extensive search of the literature revealed only of Telphusa fiuviatilis, while Man-Garzon and one record of a rotifer which was either parasitic Montero (1973) record another, Anomopus chas- or epizoic on fish. This was described by magnathi (Man6-Garzon & Montero), from the Wiszniewski (1946), who found the cold sten- branchial chamber of Chasmagnathus granulata. othermal species Encentrum kozminskii In addition, Proales paguri Thane-Fenchel was Wiszniewski on the skin and gills of carp from fish found on the gills of the hermit crab Pagurus culture ponds. The author describes the species as bernhardus (L.) (Thane-Fenchel, 1966). In the a true parasite which feeds on the mucus, and latter case, the rotifers were seen browsing on the probably the epithelium, of its host. He concludes gills and sucking the epithelium tissue of their that such an infestation could be harmful to the host. When lightly compressed under a cover- fish, but this has not been confirmed. 65

Rotifers have rarely been found living in close illoricate, within the Bdelloidea, Monogononta association with reptiles. However, Magnusson and Seisonidae. The relationships between these (1985) found the giant (up to 1500 gtm) rotifer rotifers and their hosts may be specific or non- Limnias ceratophylli Schrank living on the trunk, specific, obligate or opportunistic. Their method limbs, tail and jaws of the Amazonian crocodile, of attachment varies - some are attached by the Melanosuchus niger. The author suggests that this foot, others by the mouthparts. However, little is association is species specific, as the rotifer was known of the relationships between the species not found on other crocodile species in the area involved. Clearly, this interesting but neglected (Caiman crocodilus,Paleosuchus trigonatus, P. pal- area of rotifer research warrants further attention. pebrosus). M. niger did not seem to suffer any ill effects from the association, indicating that the rotifer was simply epizoic on the crocodile. How- Acknowledgements ever, the author did express the concern that heavy infestations could reduce the value of the I wish to thank Dr. A. E. Bailey-Watts for reading crocodile hide. and improving the manuscript, Mrs. L. A. Dick- Giesen (1934) published what appears to be the son for help in obtaining the literature and Mrs. only recorded case of a parasitic rotifer in mam- M. J. Ferguson who kindly typed the manuscript. mals. He found a considerable number of bdelloids in urine samples from a seriously ill woman whose symptoms included sore throat, aching joints, stomach disorders, exhaustion, References semi-coma and an enormous increase in blood leucocytes. Although Giesen (1934) suggests that Ahlstrom, E. H., 1940. A revision of the Rotatorian genera this is 'an apparent case of a pathogenic rotifer in Brachionus and Platyias with descriptions of one new species and two new varieties. Bull. amer. Mus. nat. Hist. man', this has never been confirmed. 77: 148-184. Barnes, R. S. K., 1984. A Synoptic Classification of Living Organisms. Blackwell Scientific Publications, Oxford, Discussion 273 pp. Bartos, E., 1951. The Czechoslovak Rotifers of the order Bdelloidea. Vestnik. Cs. zool. spol. 15: 241-500. Many rotifers live in close association with plants Beauchamp, P. M. de, 1905. Remarques sur deux Rotiferes and other animals, but few are true parasites and parasites. Bull. Soc. zool. Fr. 30: 117-124. actually harm their hosts. Most simply take ad- Beauchamp, P. de, 1923. Courtes notes sur les Rotiferes. vantage of increased food supplies and transpor- Ann. Biol. lac. 12: 221-228. tation provided by their host. However, some Berzins, B., 1950. Observations on rotifers on sponges. Trans. am. microsc. Soc. species are truly parasitic, feeding on the tissues, 69: 189-193. Bilfinger, L., 1894. Zur Rotatorien fauna Wirttembergs. 2. mucus or body fluids of their host. This is espe- Beitrag. Jahresh. d. Verf. f. vaterland. Naturk. Wirttem- cially true of the parasites of worms and leeches, bergs 50: 35-65. but is also occurs among algae, sponges, crustac- Boray, J. C., 1964. Studies on the ecology of Lymnaea tomen- eans, and fish. The damage to these hosts is rarely tosa, the intermediate host of Fasciola hepatica. I. History, geographical distribution and environment. Aust. J. Zool. fatal, in contrast to the situation in snails and 12: 217-230. rotifers. Few attempts have been made to quantify Brain, J. L., 1894. An inhabitant of Vaucheria. Science Gossip effects of parasitic rotifers on host populations, 1: 201-202. although these effects could be considerable. Bryce, D., 1924. The Rotifera and Gastrotricha of Devil's and Epizoic and parasitic rotifers are found in Stump Lakes, North Dakota, U.S.A. J. Quekett microsc. freshwater and marine environments, and in suf- Club, Ser. 2, 15: 81-108. Budde, E., 1925. Die parasitischen Radertiere mit besonderer ficiently humid terrestrial environments. They be- Beriicksichtigung der in der umgegend von minden I.W. long to a variety of genera, both loricate and beobachteten Arten. Z. Morph. u. Okol. Tiere 3: 706-785. 66

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