ZOBODAT - www.zobodat.at Zoologisch-Botanische Datenbank/Zoological-Botanical Database Digitale Literatur/Digital Literature Zeitschrift/Journal: Denisia Jahr/Year: 2005 Band/Volume: 0016 Autor(en)/Author(s): Tops Sylvie, Okamura Beth Artikel/Article: Malacosporean parasites (Myxozoa, Malacosporea) of freshwater bryozoans (Bryozoa, Phylactolaemata): a review 287-298 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at Malacosporean parasites (Myxozoa, Malacosporea) of freshwater bryozoans (Bryozoa, Phylactolaemata): a review S. TOPS & B. OKAMURA Abstract: Myxozoans belonging to the recently described class Malacosporea parasitise freshwater bryo- zoans during at least part of their life cycle. There are two malacosporeans described to date: Budden- brockia plumatellae and Tetracapsuloides bryosalmonae, the causative agent of salmonid proliferative kid- ney disease (PKD). Almost nothing is known about the ecology of malacosporeans and their interac- tions with bryozoan hosts. Here we review recent advances in our knowledge of malacosporean biology, development and life cycles. Key words: Malacosporeans, Tetracapsuloides bryosalmorwe, Buddenbrockia plumatellae, Proliferative Kidney Disease. Introduction vertebrates, primarily freshwater and marine teleosts (LOM 1984), but are also recorded as Freshwater bryo:oans (Phylum Bryozoa, parasites of amphibians (e.g. UPTON et al. Class Phylactolaemata) are common, fre- 1992; MCALLISTER et al. 1995), reptiles (see quently abundant, sessile, colonial inverte- LOM 1990), ducb (LOWENSTINE et al. 2002) brates. Phylactolaemates have a world-wide and moles (FRIEDRICH et al. 2000). They ha- distribution and are found inhabiting both ve even been recorded as persisting within lotic and lentic environments of varying wa- immuno-compromised humans (MONCADA ter quality (JOB 1976; WOOD 2001). Most et al. 2001), possibly through ingestion of species of freshwater bryozoans overwinter infected fish. Annelid worms are known to as dormant, encapsulated, yolk-filled buds, act as hosts in the life cycle of some myxo- known as statoblasts. These seed-like struc- zoans (KENT et al. 2001). tures serve as a refuge in both space and ti- me, and are the primary means of bryozoan There are currently approximately 1350 dispersal between waterbodies. described myxozoan species, in 55 genera (KENT et al. 2001). Some of these are the Despite their ubiquitous distribution causative agents of economically important and great abundance, freshwater bryozoans fish diseases, however, the majority of spe- remain relatively poorly studied. However, cies exert innocuous effects on their hosts the recent discovery that these organisms (LOM 1990). With the global expansion of are hosts to several myxozoan parasites, one marine and freshwater fish farming many of which is the causative agent of an econo- myxozoan diseases have gained prominence mically important fish disease, has led to (MOSER & KENT 1994), although the effect greater research interest in these animals. of myxozoan diseases on wild fish remains largely unknown. The phylum Myxozoa Myxozoans have been long classed as The phylum Myxozoa GRASSE 1970 is protozoans, although several independent comprised of microscopic, multicellular, attempts have been made to reclassify them spore-forming endoparasites. Myxozoans are as metazoans (Stolk 1899; Emery 1909; Ike- Denisia 16, zugleich Kataloge der OÖ. Landesmuseen best known as parasites of poikilothermic da 1912; Weil 1938; cited in CANNING & Neue Serie 28 (2005), 287-298 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at Fig. 1: Portion of a colony of Fredericella sultana, showing open lophophores (L) of individual zooids; scale bar = 500 pm. OKAMURA 2004)- These calls for reclassifi- 1881 and Actinosporea NOBLE 1980. These cation were primarily based on the multicel- classes were based on differing spore mor- lular nature of the group and phylogenetic phology. When actinosporeans infecting affinities. Although myxozoans were accor- oligochaete annelids were identified as sta- ded their status as phylum by GRASSE 1970, ges in the life cycle of the myxosporean M>- relatively recent publications continue to xobolus cerebralis (MARKIW & WOLF 1983), classify them as protists (BRUSCA & BRUSCA the class Actinosporea was suppressed lea- 1990; GILBERT & GRANATH 2003). Compel- ving only one class (the Myxosporea) wit- ling evidence that myxozoans should be of- hin the phylum (KENT et al. 1994a). To da- te about 25 life cycles of myxozoans have ficially reclassified as a metazoan phylum been resolved and these involve infection of now exists, again on the basis of the multi- annelid worms and fish hosts (listed in KENT cellularity of their spores, as well as molecu- et al. 2001). lar phylogenetic studies (e.g. SMOTHERS et al. 1994; SIDDALL et al. 1995; KENT et al. The discovery and description of a my- 2001, SCHLEGEL et al. 1996; ZRZAV? 2001, xozoan parasite infecting freshwater bryozo- ZRZAVI & HYPSA 2003; OKAMURA & CAN- ans in 1996 (CANNING et al. 1996; OKAMU- NING 2003, CANNING & OKAMURA 2004). RA 1996) led CANNING et al. (2000) to pro- While the metazoan nature of myxozoans is pose a new class - the Malacosporea - wit- now widely accepted, their phylogenetic hin the phylum Myxozoa. This class incor- status within the Metazoa has been strongly porates myxozoan parasites which include debated (see discussion in section on Bud- freshwater bryozoans in at least part of their denbrockia plumateVae). life cycle, but to date no complete malacos- porean life cycle has been resolved. The long-standing taxonomic dispute regarding the phylum Myxozoa has not me- rely been limited to higher-level phylogene- The class Malacosporea tic affinities. Prior to 1994, two classes exis- There is a great paucity of data on mala- ted within the group: Myxosporea BÜTSCHLI cosporean biology and ecology. One member 288 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at of the Malacosporea, Tetracapsuloides bryosd- Tab. 1: Species of bryozoans and fish, which have been identified as hosts to species of malacosporean. monae, is now recognised as the causative agent of proliferative kidney disease (PKD) Buddenbrockia plumatellae Tetracapsuloides bryosalmonae in salmonid fish (ANDERSON et al. 1999a, b; Bryozoan hosts Bryozoan hosts Fish hosts CANNING et al. 1999; FEIST et al. 2001). Lophopodella carterii Pectinatella magnifica Oncorhynchus mykiss Hyalinella punctata Fredericella sultana Salmo trutta Malacosporeans form an ancient clade Stolella evelinae Plumatella rugosa Salmo salar Pluma tella repens Plumatella emarginata Oncorhynchus tshawytscha of myxozoan parasites, which on the basis of Cristatella mucedo* Cristatella mucedo Oncorhynchus kisutch 18S rDNA sequences, appear to have diver- PI u mat el la fungosa Oncorhynchus clarki ged early in the evolution of the Myxozoa Rutilus rutilus * sac-like stages only Salvelius alpinus (ANDERSON et al. 1999a, b; KENT et al. Thymallus thymallus 1998, 2001). Two species of malacosporean Esox lucius have so far been described. One is Budden- cells, moving in the coelom of a bryozoan in brockia plumatellae SCHRÖDER 1910 (former- Belgium. Studies conducted on bryozoans ly Tetracapsula bryozoides; cp. CANNING et al. infected with B. plumatellae in Germany led 2002) and the other is Tetracapsuloides bryo- SCHRÖDER (1910) to name the species. He salmonae (formerly Tetracapsula bryosalmo- initially proposed that these 'worms' were nae; cp. CANNING et al. 2002). Despite the mesozoans, but later revised his opinion sug- relatively recent description of the class, gesting a nematode affinity, due to the pre- myxozoans appear to have been observed in sence of the four blocks of longitudinal mus- several early studies of phylactolaemate cles characteristic of this species (SCHRÖDER bryozoans. Thus, malacosporeans appear to 1912). The phylogenetic placement of Bud- be figured in various illustrations (e.g. ALL- denbrockia remained obscure, and, until re- MAN 1856; COOKE 1906). cently, it had never been assigned to an an- There are several distinctive diagnostic imal phylum, nor had a monotypic phylum features of malacosporeans infecting bryozo- been erected for it (MONTEIRO et al. 2002). an hosts, which indicate that they are not In fact, it was included as one of the 'five actinosporean stages of the class Myxospo- enigmatic taxa' by NIELSEN (2001) in his rea (CANNING et al. 2000). The most pro- text on animal evolution. minent attribute is the lack of hardened spo- Since the early studies conducted by re valves, a characteristic which led to the SCHRÖDER, B. plumatellae has been encoun- naming of the class (CANNING et al. 2000). tered parasitising several bryozoan genera In addition, spore development occurs wit- (Tab. 1) across a broad geographic distribu- hin closed sacs or hollow 'worms' encasing tion (OKAMURA et al. 2002). In spite of this, spores (CANNING et al. 2000). Since sexual the vermiform parasite is still rarely encoun- reproduction of malacosporeans has been tered. As such, little is known regarding the shown to occur in the bryozoan phase of ma- ecology and life cycle of this malacosporean. lacosporean life cycles, bryozoans are consi- dered as the true (definitive) hosts of these There has been a resurgence in interest enigmatic parasites (CANNING et al. 2000). in B. plumatellae in recent years. Molecular For a comprehensive review see CANNING & and ultrastructural evidence suggests that B. OKAMURA (2004). Although there are ob- plumateliae occurs