sign in sign up
<<
Home , Annelid, Cristatella, Fredericella, Myxozoa, Phylactolaemata, Plumatella

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 (, Malacosporea) of freshwater bryozoans (, ): 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 Malacosporea parasitise freshwater bryo- zoans during at least part of their cycle. There are two malacosporeans described to date: Budden- brockia plumatellae and 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 , development and life cycles.

Key words: Malacosporeans, Tetracapsuloides bryosalmorwe, Buddenbrockia plumatellae, Proliferative Kidney Disease.

Introduction , primarily freshwater and marine teleosts (LOM 1984), but are also recorded as Freshwater bryo:oans ( Bryozoa, parasites of (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 of freshwater bryozoans overwinter infected . are known to as dormant, encapsulated, -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 . 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 -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 sultana, showing open (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 of the group and phylogenetic phology. When actinosporeans infecting affinities. Although myxozoans were accor- oligochaete 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 (BRUSCA & BRUSCA the class Actinosporea was suppressed lea- 1990; GILBERT & GRANATH 2003). Compel- ving only one class (the ) 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 , 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 magnifica Oncorhynchus mykiss punctata Fredericella sultana Salmo trutta Malacosporeans form an ancient clade Stolella evelinae rugosa Salmo salar Pluma tella repens Plumatella emarginata Oncorhynchus tshawytscha of myxozoan parasites, which on the basis of mucedo* Cristatella mucedo Oncorhynchus kisutch 18S rDNA sequences, appear to have diver- PI u mat ella 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 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 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 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 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 as both -like and vious similarities between the two malacos- sac-like stages within bryozoan hosts as is porean species, they differ in their spore de- shown in Figure 2 (MONTEIRO et al. 2002; velopment, ecology and possibly also their OKAMURA et al. 2002). Both stages produce life histories. Therefore, they will be discus- infective spores, but the longitudinal mus- sed separately in the following sections. cles are absent in sacs (OKAMURA et al. 2002; CANNING et al. 2002). The sac-like stages were initially described as Tetracapsu- Buddenbrockia plumatellae la bryozoides (CANNING et al. 1996), but 18S The first record of Buddenbrockia pluma- rDNA sequences and ultrastructural simila- tetiae is that by DU MORTIER & VAN BENEDEN rities, including spore and (1850), reporting worm-like (vermiform) polar capsule structure, resulted in the sac- creatures, about 0.1 mm long and filled with like T. bryozoides being placed in synonymy

289 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at

Fig. 2: Buddenbrockia plumatellae infections; a: vermiform stage of B. plumatellae exiting from the of a zooid; scale bar = 200 urn; b: sac-like stages of B. plumatellae (arrows) infecting a colony of Cristatella mucedo; L - lophophore; scale bar = 200 urn.

with Buddenbrockia plumatellae (CANNING et her-level phylogeny of the Myxozoa persists, al. 2002). As mentioned above, the vermi- with some authors remaining steadfast in form stage of B. plumatellae has been found the belief that myxozoans are degenerate infecting several bryozoan species (CAN- cnidarians (SlDDALL et al. 1995; ZRZAvt et NING et al. 2002; MoNTElRO et al. 2002), but al. 1998; KENT et al. 2001). it is interesting to note that the sac-like sta- ges have only been observed parasitizing one Tetracapsuloides bryosalmonae bryozoan - Cristatella mucedo. PKD has been recognised as a serious The discovery that B. plumateliae is a salmonid fish disease since the early part of myxozoan, has generated debate over the the 20th century, but the etiological agent phylogenetic affinities of the Myxozoa. Its had never been identified and had conse- with four longitudinal muscle quently been referred to as PKX ('X' imply- blocks and a lack of gut lends support to a ing organism unknown) (SEAGRAVE et al. bilaterian placement of this phylum. Loss of 1980). The myxozoan traits of PKX were re- the gut is a feature of other lower metazoan cognised by KENT & HEDRICK (1986). The organisms which have become parasitic, discovery of an alternate worm host in the such as the Rhombozoa, and life cycle of the myxozoan cere- some species of Nematoda (OKAMURA & brdis (MARKIW & WOLF 1983, WOLF & CANNING 2003). A triploblastic nature for MARKIW 1984) prompted research to identi- myxozoans was previously suggested on the fy an host for PKX (LONGSHAW basis of 18S rDNA phylogenies (e.g. SMO- & FEIST 2000, LONGSHAW & FEIST, unpu- THERS et al. 1994; HANELT et al. 1996; blished data cited in FEIST et al. 2001; MOR- SCHLEGEL et al. 1996; KIM et al. 1999) and RIS D.J. et al. 1999). These searches were the presence of central class Hox genes unsuccessful until molecular data identified (ANDERSON et al. 1998). Support is therefo- freshwater bryozoans as hosts of PKX (AN- re mounting for placing the Myxozoa within DERSON et al. 1999a, b), which finally allo- the , with myxozoans showing an wed the species to be described as Tetracop' extreme secondary reduction in body plan, sula bryosalmonae (CANNING et al. 2000). due to their parasitic life-style (OKAMURA et Confirmation that T. bryosalmonae is the al. 2002). However, the debate over the hig- causative agent of PKD was subsequently

290 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at obtained by transmission studies (FEIST et al. (KENT et al. 1994b). Econo- 2001). Formerly named Tetracapsula bryosal- mic costs to the U. K. industry monae, this species was renamed when T. have been put at £1.8 million annually, as a bryozoides was placed in synonymy with result of stock losses, decreased food conver- Buddenbrockia plumatelhe (see MONTEIRO et sion rates and increased labour costs al. 2002) and the new generic name of Te- (MONTGOMERY 2000). In intensive farming tracapsidoides was proposed for Tetracapsula situations, mortalities of up to 95-100 % of bryosalmonae (see CANNING et al. 2002). stock have been recorded (HEDRICK et al. 1993) and, even when mortality is low, mor- Most salmonid fish species and many bidity can reach 100 % (CLIFTON-HADLEY et species of freshwater bryozoan are suscepti- al. 1984). Wild salmonids are known to be ble to infection by Tetracapsuloides bryosal- susceptible to the disease, but there is a pau- monae (Tab. 1). Interestingly, pike (Esox lu- city of data on its impact on wild stocks eins), which is not a salmonid fish species, is (BÜCKE et al. 1991; FEIST & BuCKE 1993, also capable of contracting PKD. However, FEIST 1999, FEIST et al. 2002). It has been pike are found within the same clade as sal- suggested that recent declines in brown monids (NELSON 1994; BERRA 2001). trout populations in Switzerland may be due While five species of bryozoan have to PKD (WAHLI et al. 2002). been confirmed as hosts of T. bryosalmonae PKD primarily affects underyearlings (Tab. 1) on the basis of 18S rDNA sequen- (KENT & HEDRICK 1985) and an acquired ce information, only one species (Fredericel- immunity follows infection (FERGUSON & la sultana; Fig. 1) has been confirmed BALL 1979; Foorr & HEDRICK 1987). Natu- through transmission studies (FEIST et al. ral outbreaks of the disease seldom occur at 2001). It remains unclear whether all fresh- water temperatures below 15 °C (FERGUSON water bryozoan species are susceptible to T. 1981), which lend a highly seasonal aspect bryosalmonae infection. On the basis of a to the disease (FERGUSON & BALL 1979). survey conducted in parts of Europe and The seasonality is thought to relate to the North America, OKAMURA & WOOD immune system offish, rather than the avai- (2002) concluded that members of the ge- lability of infective spores in the water, sin- nera Fredericella and Plumatella are the most ce the presence of infective T. bryosalmonae important hosts of Tetracapsuloides bryosal' spores capable of inducing PKD in rainbow monae, since they were most commonly as- trout has been shown to persist throughout sociated with fish farms that sustained out- the year (GAY et al. 2001). However, the breaks of PKD. biology of freshwater bryozoans is also cha- racterised by extreme seasonal growth and Importance and distribution proliferation (BuSHNELL 1966). of proliferative kidney disease (PKD) Malacosporean life cycles

A comprehensive review of PKD was The fact that phylactolaemate bryozo- presented by HEDRICK et al. (1993). The di- ans are the source for the causative agent of sease was first recorded from Germany as PKD in salmonids is now well established 'Amöbeninfection der Niere' by Plehn in (ANDERSON et al. 1999a, b; FEIST et al. 1924 (cited in HEDRICK et al. 1993). The 2001). However, whether stages that deve- distribution of PKD is limited to the nor- lop in and are released by fish are capable of thern hemisphere where it is found in many infecting bryozoans has so far not been de- countries in Europe and mainly in the wes- monstrated. TOPS et al. (2004) undertook tern states of North America (KENT & HE- extensive transmission studies to elucidate DRICK 1986). Due to the great economic los- the life cycle of malacosporeans. In particu- ses to aquaculture industries, PKD has been lar, they investigated transmission of the pa- identified as one of the most economically rasite from salmonids to bryozoans. None of important diseases affecting cultured salmo- the 15 transmission trials were successful, nids fisheries in Europe, including the U. K. indicating that there may be another host in (CLIFTON-HADLEY et al. 1984), and in the life cycle of malacosporean parasites.

291 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at

Fig. 3: Sacs of Tetracapsuloides bryosalmonae (arrows) infecting a branch of Fredericella sultana; scale bar = 200 ym.

MORRIS D.C. et al. (2002) and MORRIS hosts (MACCONNELL et al. 1989). However, DJ. et al. (2002) reported possible transmis- previous to the description of the Class Ma- sion of T. bryosalmonae and Buddenbrockia lacosporea (CANNING et al. 2000), resear- plumatellae from fish to bryozoans. The stu- chers expected final spore development to dies were uncontrolled. Their results may terminate in stages with hardened valves have reflected previous development of the consistent with myxosporeans. The possibi- parasite in bryozoans in the field or PCR lity that fish are not aberrant hosts is sup- amplification of residual DNA that had ad- ported by the release of apparently functio- hered to bryozoans or of undetected, infec- nal malacosporean-like spores in fish ted . It is, however, known that (HEDRICK et al. 2004). However, the presen- PKD is not transmitted from fish to fish ce of T. bryosalmonae has been confirmed (FERGUSON & BALL 1979; D'SILVA et al. from bryozoan populations collected from si- 1984). tes devoid of salmonids (OKAMURA et al. Certain observations have been cited as 2001). This suggests that fish may, at best, evidence that salmonids may be aberrant be facultative hosts. It also suggests that raa- hosts for Tettacapsuloides bryosalmonae. The- lacosporeans may be able to exploit the clo- se include the severe inflammatory response nal growth of bryozoans and remain as cryp- offish kidneys, as well as apparently incom- tic latent infections in bryozoan popula- plete spore development within salmonid tions.

292 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at

Thus far no host has been tions of malacosporeans in bryozoan hosts al- identified for Buddenbrockia plumatetiae. Al- low for a long-term persistence of the para- though, organisms with distinctly malaco- sites within the environment. sporean features have been described in pil- The long-term persistence of infections lar cells and endothelial cells of common could explain many aspects of the Tetracap- carp, Cyprinus carpio (VORONIN 1993, VOR- suloides bryosalmonae life cycle, especially ONIN & CHERNYSHEVA 1993), the precise when infecting Fredericella sultana (see Fig. nature of these stages is yet to be identified. 3). This species of bryozoan can overwinter as live colonies and may thus provide a win- Development of ter refuge for cryptic parasitic stages. Nota- malacosporean parasites bly, a survey of bryozoan species associated infecting bryozoan hosts with water courses enzootic for PKD over a wide geographic range, identified F. sultana The development of sacs and spores of as one of the most commonly found species both malacosporean species in bryozoans of bryozoan to be collected in PKD areas have been studied through ultrastructure (OKAMURA & WOOD 2002). Overwintering (CANNING et al. 1996, 2000, 2002; OKAMU- in the widely available live F. sultana colo- RA et al. 2002). Mature infections manifest nies would not only allow the persistence of themselves as spore-filled sacs. The sac-like infections through unfavourable periods, forms tumble within the coelom of the bryo- but also provide an explanation for the per- zoans, moving with the coelomic fluid. The sistence of annual outbreaks of PKD infec- vermiform stages of Buddenbrockia are capa- tions in consecutive years at some fish ble of independent movement due to the farms. Long-term cryptic infections in F. possession of 4 longitudinal muscle groups. sultana would also provide a means of dis- Recently, there has been an increase in our persal for the malacosporean. Fredericella knowledge of the early development of ma- sultana colonies become brittle as they grow lacosporeans infecting their invertebrate and branches detach, drift downstream and hosts. reattach elsewhere (WOOD 1973). This frag- Molecular, histological and ultrastructu- mentation strategy could allow for cryptic ral investigations have revealed that cryptic malacosporean stages to be transported to stages in the body wall are a feature of mala- new habitats within their host. cosporean infections of bryozoans (CAN- Since malacosporeans do not produce NING et al. 2002; TOPS & OKAMURA 2003). hardened, resistant spores there has been Cryptic stages have similarly been identified much speculation regarding what happens from myxosporean parasites infecting tubifi- to the parasites during the winter months, cid worms ( tubifex). The discovery of since most bryozoan species regress and these stages suggests that infections of bryo- overwinter as dormant statoblasts. One pos- zoans may be able to persist within bryozoan sibility is that malacosporeans are capable of populations as cryptic, latent infections, on- overwintering as cryptic stages in statoblasts ly proliferating into spore-filled sacs when (OKAMURA & WOOD 2002). This strategy the conditions are appropriate. would not only allow for the survival The inclusion of a latent period in the through periods which are not permissive life cycle of malacosporeans could play a sim- for host growth, but would also provide a ilar role to the inclusion of dormant, resist- means of dispersal of the parasite, since sta- ant stages in other pathogens. Such resistant toblasts are the dispersal stage of bryozoans. stages include occlusion bodies in the case of There is a growing body of evidence that some baculoviruses (BURDEN et al. 2003) and waterfowl act as dispersal vectors of bryozo- hardened spores as in the myxosporean an statoblasts, which lends credence to this stages of myxozoans (CANNING & OKAMURA possibility. Evidence includes ongoing gene 2004). These stages allow for the long-term flow amongst sites traversed by migratory persistence of pathogens by providing envi- waterfowl (FREELAND et al. 2000), the pre- ronmental reservoirs of infection (BURDEN et sence of intact statoblasts in waterfowl di- al. 2003). Perhaps long-term cryptic infec- gestive tracts and faeces (FlGUEROLA et al.

293 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at

2003) and the viability of some statoblasts, whether it is reduced in bryozoans with which hatched following ingestion and ex- cryptic infections is unknown. cretion by waterfowl (CHARALAMBIDOU et al. 2003). GILBERT & GRANATH (2003) ha- Vermiform and sac stages ve similarly speculated that the myxozoan may undergo dispersal Molecular and ultrastructural evidence thorough the dormant cysts of Tubifex tubi- has suggested that sac-like and vermiform (ex. stages are common in the life cycle of Bud- denbrockia plumatellae (MONTEIRO et al. It can be predicted that the life history 2002; OKAMURA et al. 2002). Nevertheless, of bryozoans plays an important role in the sacs and worms have not been found to coe- maintenance and spread of cryptic malacos- xist in any host. In addition, although nu- porean infections without the necessity of merous bryozoan species are recorded as regular transmissions from any other hosts. hosts to the vermiform stage, the sac stage Should malacosporeans possess the ability to has only been encountered in Cristaiella mu- proliferate as the host colony grew, they wo- uld be able to ensure that all regions of co- cedo (CANNING & OKAMURA 2004). It is possible that the life cycle of Buddenbrockia lonies became infected. In addition, Freden- cella sultana itself overwinters as live colo- plumacellae entails obligate cycling between life history stages or that these different nies (WOOD 1973; RADDUM &. JOHNSEN 1983), providing the parasite with a winter- morphologies represent facultative stages, refuge, thus allowing cryptic infections to be the expression of which is controlled by an maintained year-round in this species (GAY unidentified cue. Alternatively, they may et al. 2001). Finally, should cryptic stages represent different but closely related spe- infect dormant bryozoan statoblasts, infec- cies. tions could be passed to new colonies Observations have shown that narrow through hatching from statoblasts. All of branching species of bryozoans are able to these processes could promote long-term in- seal off infected portions of colonies, thus li- fections in bryozoan populations without miting the infection to a portion of the bry- the need for regular transmissions from any ozoan colony (CANNING et al. 2002; MORRIS other hosts. This could explain the high D.J. et al. 2002). Vermiform stages, capable prevalence of mature T. bryosalmonaeAnfec- of independent movement, may reduce the tions in bryozoan populations early in the likelihood of becoming trapped and may growing season (LONGSHAW et al. 1999; promote exit from the host (CANNING et al. Tops & Okamura unpubl. data). 2002, OKAMURA & CANNING 2003).

If cryptic stages of T. bryosalmonae are There has been speculation regarding capable of infecting bryozoan statoblasts, the possible existence of a vermiform stage then the maintenance of infections in some of Tetracapsuloides bryosalmonae (OKAMURA sites may simply be explained by coloniza- &. CANNING 2003; TOPS et al. 2004). In a tion through infected statoblasts and the study assessing statoblasts collected from subsequent spread of infection in the bryo- areas enzootic for PKD, TATICCHI et al. zoan population through proliferation of pa- (2004) observed vermiform stages emerging rasites within clonally reproducing hosts. from KOH treated statoblasts. They hypo- Furthermore, waterfowl-mediated dispersal thesised that these could be worm-like sta- of possibly infected statoblasts, followed by ges of T. bryosalmonae, but the study lacked the proliferation of in the bryozo- molecular and ultrastructural confirmation. an population provides one explanation for To date there is no evidence for different the presence of infected bryozoan popula- morphotypes in T. bryosalmonae. tions in sites lacking salmonids (TOPS et al. 2004). It is interesting to note that statob- Conclusions and future work last production is reportedly reduced, but not precluded in bryozoans with overt mala- As a result of ongoing debate regarding cosporean infections (OKAMURA 1996; the phylogenetic affinities of the Myxozoa MORRIS DJ. et al. 2002; Tops pers. obs.), but (CANNING et al. 2002; MONTEIRO et al.

294 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at

2002; OKAMURA et al. 2002) there has been freshwater bryozoan Cristatella mucedo a resurgence of interest in the study of the (Bryozoa: Phylactolaemata). — Folia Parasitol. 43:249-261. Buddenbrockia (MORRIS D.J. et al. 2002; ZRZAVY 2001, ZRZAV? & HYPSA 2003). CANNING E.U., TOPS S., CURRY A., WOOD T.S. & B. OKA- MURA (2002): Ecology, development and pa- In addition, PKD appears to be increasing in thogenicity of Buddenbrockia plumatellae many places (WAHLI et al. 2002). In light of SCHRÖDER, 1910 (Myxozoa, Malacosporea) these basic and applied issues, we can expect (syn. Tetracapsula bryozoides) and establish- further work on bryozoans and their parasi- ment of Tetracapsuloides n. gen. for Tetra- capsula bryosalmonae. — J. Eukaryot. Micro- tes. biol. 49: 280-295.

CHARALAMBIDOU I.C., SANTAMARIA L. & J. FIGUEROLA References (2003): How far can the freshwater bryozoan Cristatella mucedo disperse in duck guts? — ALLMAN GJ. (1856): A Monograph of the Fresh-wa- Arch. Hydrobiol. 157: 547-554. ter Polyzoa. — Ray Society, London: 1-119. CUFTON-HADLEY R.S., RICHARDS R.H. & D. BUCKE (1984): ANDERSON C.L., CANNING E.U. & B. OKAMURA (1998): A Experimental transmission of proliferative triploblast origin for Myxozoa. — Nature kidney disease: Preliminary report. — Vet. 392: 346. Rec. 114:90.

ANDERSON C.L., CANNING E.U. & B. OKAMURA (1999a): COOKE M.C. (1906): Ponds and Ditches. — Natural 18S rDNA sequences indicate that PKX orga- History Rambles. Society for Promoting Chris- nism parasitizes Bryozoa. — Bull. Eur. Ass. Fish tian Knowledge, London: 1-254. Pathol. 19: 94-97. D'SILVA J., MULCAHEY M.F. & P. DE KiNKEUN (1984): Ex- ANDERSON C.L., CANNING E.U. S B. OKAMURA (1999b): perimental transmission of proliferative kid- Molecular data implicate bryozoans as hosts ney disease in , Salmo gairdneri of PKX (Phylum Myxozoa) and identify a cla- RICHARDSON. — J. Fish Dis. 7: 235-239. de of bryozoan parasites within the Myxozoa. DU MORTIER B.C. & P.J. VAN BENEDEN (1850): Histoire — Parasitology 119: 555-561. naturelle des polypes composes d'eau douce. BERRA T.M. (2001): Freshwater Fish Distribution. — — Nouv. Mem. Acad. Roy. Sei. Belles-Lettres Academic Press, San Diego, California: 1-576. Bruxelles 16: 33-96.

BRUSCA R.C. & G.J. BRUSCA (1990): Invertebrates. — FEIST S.W. (1999): Effects of PKD on wild fish po- Sinauer Associates, Sunderland, Mass.: 1-922 pulations in the U.K. — In: MONTGOMERY C,

BUCKE D., FEIST S.W. & R.S. CUFTON-HADLEY (1991): FEIST S.W. & M. LONGSHAW (Eds.): Proliferative The occurrence of proliferative kidney disea- Kidney Disease (PKD) in Wild and Farmed Sal- se (PKD) in cultured and wild fish: Further ob- monids: Draft report of the first workshop: servations. — J. Fish Dis. 14: 583-588. 15-17 November Weymouth, UK: 35-39.

BURDEN J.P., NIXON C.P., HODGKINSON A.E., POSSEE R.D., FEIST S.W. & D. BUCKE (1993): Proliferative kidney SAU S.M., KING LA. & R.S. HAILS (2003): Covert disease in wild salmonids. — Fish. Res. 17: 51- infections as a mechanism for long-term per- 58.

sistence of baculoviruses. — Ecol. Lett. 6: 524- FEIST S.W., LONGSHAW M., CANNING E.U. & B. OKAMU- 531. RA (2001): Induction of proliferative kidney di- BUSHNELL J.H.J. (1966): Environmental relations of sease (PKD) in rainbow trout Oncorhynchus Michigan Ectoprocta and dynamics of natural mykiss via the bryozoan Fredericella sultana populations of Plumatella repens. — Ecol. infected with Tetracapsula bryosalmonae. — Monogr. 36: 95-123. Dis. Aquat. Org. 45: 61-68.

CANNING E.U., CURRY A., FEIST S.W., LONGSHAW M. & B. FEIST S.W., PEELER E.J., GARDINER R., SMITH E. & M. OKAMURA (1999): Tetracapsula bryosalmonae LONGSHAW (2002): Proliferative kidney disease n. sp. For PKX organism, the cause of PKD in and renal myxosporidosis in juvenile salmo- salmonid fish. — Bull. Eur. Ass. Fish Pathol. nids from rivers in England and Wales. — J. 19: 203-206. Fish Dis. 25:451-458.

CANNING E.U., CURRY A., FEIST S.W., LONGSHAW M. & B. FERGUSON H.M. (1981): The effects of water tempe- OKAMURA (2000): A new class and order of my- rature on the development of proliferative xozoa ns to accommodate parasites of bryo- kidney disease in rainbow trout, Salmo gaird- zoans with ultrastructural observations on Te- neri RICHARDSON. — J. Fish Dis. 4: 175-177. tracapsula bryosalmonae (PKX organism). — FERGUSON H.M. & H.J. BALL (1979): Epidemiological J. Eukaryot. Microbiol. 47: 456-468. aspects of proliferative kidney disease in rain- CANNING E.U. & B. OKAMURA (2004): Biodiversity and bow trout, Salmo gairdneri RICHARDSON in Nor- evolution of the Myxozoa. — Adv. Parasit. 56: thern Ireland. — J. Fish Dis. 2: 219-225. 44-130. FIGUEROLA J., GREEN A.J. & L. SANTAMARIA (2003): Pas- CANNING E.U., OKAMURA B. & A. CURRY (1996): Deve- sive internal transport of aquatic organisms lopment of a myxozoan parasite Tetracapsula by waterfowl in Donana, south-west Spain. — bryozoides gen. n. et sp. n. parasitic in the Global Ecol. Biogeogr. 12: 427-436.

295 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at

FOOTT J.S. & R.P. HEDRICK (1987): Seasonal occurren- nomenclatural revisions proposed for the ce of the infectious stage of proliferative kid- Phylum Myxozoa GRASSE, 1970. — Ca- ney disease (PKD) and resistance of rainbow nad. J. Zool. 72: 932-937. trout, Salmo gairdneri RICHARDSON, to reinfec- KENT M.L., MARGOUS L., WHITAKER DJ., HOSKINS G.E. & tion. — J. Fish Biol. 30: 477-483. T.E. MCDONALD (1994b): Review of Myxospo- FREEIAND J.R., NOBLE L.R. & B. OKAMURA (2000): Ge- rea of importance in salmonid fisheries and netic consequences of the metapopulation aquaculture in British Columbia. — Folia Pa- biology of a facultatively sexual freshwater rasitol. 41: 27-37. invertebrate. — J. Evol. Biol. 13: 383-395. KIM J., KIM W. & C.W. CUNNINGHAM (1999): A new FRIEDRICH C, INGOUC E., FREITAG B., KASTBERGER G., perspective on lower metazoan relationships HOHMANN B., StcofrrscH G., NEUMEISTER U. & O. from 18S and DNA sequences. — Mol. Biol. KEPKA (2000): A myxozoan-like parasite cau- Evol. 16: 423-427. sing xenomas in the of the mole, Talpa LOM J. (1984): Revised classification of the class europaea I., 1758 (Vertebrata, Mammalia). — Myxosporea BOTSCHU, 1881. — Folia Parasitol. Parasitology 121: 483-492. 31: 193-205.

GAY M., OKAMURA B. & P.D. KINKEUN (2001): Eviden- LOM J. (1990): Phylum Myxozoa. — In: MARGUILIS L., ce that the infective stages of Tetracapsula CORUSS J.O., MELKONIAN M. & D.J. CHAPMAN bryosalmonae for rainbow trout, Oncoryn- (Eds.): Handbook of the Protoctista: The chus mykiss, are present throughout the year. structure, cultivation, habitats, and life histo- — Dis. Aquat. Org. 46: 31-40. ries of the eukaryotic microorganisms and GILBERT M.A. & W.O. Jr. GRANATH (2003): Whirling their descendants, exclusive of animals, disease of salmonid fish: life cycle, biology, and funghi: A guide to algae, , and disease. — J. Parasitol. 89: 658-667. formanifera, sporozoa, water molds, slime molds, and the other protoctists. Jones & HANELT B., VAN SCHYNDEL D., ADEMA CM., LEWIS L.A. & Bartlett, Boston: 36-52. E.S. LOKER (1996): The phylogenetic position of Rhopalura ophiocomae (Orthonectida) ba- LONGSHAW M. & S.W. FEIST (2000): The agent of pro- sed on 18s ribosomal DNA sequence analysis. liferative kidney disease (PKD) requires a bry- — Mol. Biol. Evol. 13: 1187-1191. ozoan in its lifecycle. — Trout News 29: 24-27.

HEDRICK R.P., BAXA D.V., DE KINKEUN P. & B. OKAMURA LONGSHAW M., FEIST, S.W. CANNING E.U. & B. OKAMURA (2004): Malacosporean-like spores in urine of (1999): First identification of PKX in bryozo- rainbow trout react with antibody and DNA ans from the United - molecular probes to Tetracapsuloides bryosalmonae. — evidence. — Bull. Eur. Ass. Fish Pathol. 19: Parasitol. Res. 92: 81-88. 146-148.

LOWENSTINE L.J., RlDEOUT B.A., GARDNER M., BUSCH M., HEDRICK R.P., MACCONNELL E. & P. DE KINKELIN (1993): Proliferative kidney disease of salmonid fish. MACE M., BARTHOLOMEW J. & C.H. GARDINER (2002): Myxozoanosis in waterfowl: A new — Ann. Rev. Fish Dis. 3: 277-290. host record? — Proc. Amer. Soc. Zoo Veteri- JOB P. (1976): Intervention des populations de Plu- narians, Proc. Ann. Meeting, Milwaukie: 86- matella fungosa (PALLAS) (Bryozoaire Phylac- 87. toleme) dans I'autoepuration des eaux d'un etang d'un ruisseau. — Hydrobiologia 48: MACCONNELL E., SMITH C.E., HEDRICK R.P. S CA. SPEER (1989). Cellular inflammatory response of 257-261. rainbow trout to the protozoan parasite that KENT M.L. & R.P. HEDRICK (1985): PKX, the causative causes proliferative kidney disease. — J. agent of proliferative kidney disease (PKD) in Aquat. Animal Health 1: 108-118. pacific salmonid and its affinities with MARKIW M.E. S K. WOLF (1983): Myxosoma cere- the Myxozoa. — J. Protozool. 32: 254-260. bralis (Myxozoa: Myxosporea) etiological KENT M.L. & R.P. HEDRICK (1986): Development of agent of salmonid whirling disease requires the PKX myxosporean in rainbow trout Salmo tubificid worm (Annelida: ) in its gairdneri. — Dis. Aquat. Org. 1: 169-182. life cycle. — J. Protozool. 30: 561-564.

KENT M.L., ANDREE K.B., BARTHOLOMEW J.L., EL-MAT- MCALLISTER CT., BURSEY C.H., UPTON S.J., TRAUTH S.E. BOUU M., DESSER S.S., DEVUN R.H., FEIST S.W., HE- & D.B. CONN (1995): Parasites of Desogathus DRICK R.P., HOFFMANN R.W., KHATTRA J., HALLETT brimleyorum (Caudata: Plethodontidae) from S.L., LESTER R.J.G., LONGSHAW M., PALENZEULA O., the Ouachita mountains of Arkansas and SIDDALL M.E. & C.X. XIAO (2001): Recent advan- Oklahoma. — Comp. Parasitol. 62: 150-156. ces in our knowledge of the Myxozoa. — J. MONCADA L.I., LOPEZ M.C., MURCIA M.I., NICHOLLS S., Eukaryot. Microbiol. 48: 395-413. LEON F., Gulo O.L. & A. CORREDOR (2001): Myxo- KENT M.L., KHATTRA J., HERVIO D.M.L. & R.H. DEVUN bolus sp., another opportunistic parasite in (1998): Ribosomal DNA sequence analysis of immunosuppressed patients? — J. Clin. Mi- isolates of the PKX myxosporean and their re- crobiol. 39: 1938-1940. lationship to members of the genus Sphae- MONTEIRO A.S., OKAMURA B. S P.W.H. HOLLAND rospora. — J. Aquat. An. Health 10: 12-21. (2002): Orphan worm finds a home: Budden- KENT M.L., MARGOUS L & J.O. CORLISS (1994a): The brockia is a myxozoan. — Mol. Biol. Evol. 19: demise of a class of protists: Taxonomic and 968-971.

296 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at

MONTGOMERY C. (2000): Workshop on proliferative pens L. und PI. fungosa PALL. — Z. Wiss. Zool. kidney disease (PKD) in wild and farmed sal- 96: 525-537. monids. — Trout News 30: 25-27. SCHRÖDER O. (1912): Weitere Mitteilungen zur MORRIS D.C., MORRIS DJ. & A. ADAMS (2002): Mole- Kenntnis der Buddenbrockia plumatellae Ol. cular evidence of release of Tetracapsula bry- SCHRÖDER. — Verh. Natur-Med. Ver. Heidelb. osalmonae, the causative organism of prolife- 11:230-237. rative kidney disease from infected salmonids SEAGRAVE C.P., BÜCKE D. & DJ. ALDERMAN (1980): into the environment. — J. Fish Dis. 25: 501- Ultrastructure of a haplosporean-like orga- 504. nism: The possible causative agent of prolife- MORRIS D.I.. LONGSHAW M., ADAMS A., FEIST S.W. & rative kidney disease in rainbow trout. — J. R.H. RICHARDS (1999): Is an oligochaete invol- Fish Biol. 16:453-459. ved in the life cycle of PKX? — In: Brit. Soc. SIDDALL M.E., MARTIN D.S., BRIDGE D., DESSER S.S. & Parasitol. (B.S.P.): Spring Meeting Abstracts, D.K. CONE (1995): The demise of a phylum of University of Warwick: 32. protists: Phytogeny of Myxozoa and other pa- MORRIS D.J., MORRIS D.C. & A. ADAMS (2002): Deve- rasitic . — J. Parasitol. 81: 961-967. lopment and release of a malacosporean (my- SMOTHERS J.F., VON DOHLEN CD., SMITH L.H. Jr. & R.D. xozoan) from Plumatella repens (Bryozoa: SPALL (1994): Molecular evidence that the my- Phylactolaemata). — Folia Parasitol. 49: 25- xozoan protists are metazoans. — Science 34. 256: 1719-1721. MOSER M. & MX. KENT (1994): Myxosporea — In: TATKCHI M.I., GUSTINELU A., FIORAVANTI M.L., CAFFARA KREIER J.P. (Ed.): Parasitic . Vol. 8. M., PIERONI G. & M. PREARO (2004): Is the worm- Academic Press, San Diego, CA: 265-318. like organism found in the statoblasts of Plu- NELSON J.S. (1994): Fishes of the World. — Wiley, matella fungosa (Bryozoa, Phylactolaemata) New York: 1-600. the vermiform phase of Tetracapsuloides bry- NIELSEN C. (2001): Animal Evolution. Interrelations- osalmonae (Myxozoa, Malacosporea). — Ital. hips of the Living Phyla. 2nd ed. — Oxford Uni- J. Zool. 71: 143-146. versity Press, Oxford: 1-578. TOPS S. & B. OKAMURA (2003): Infection of bryozo- OKAMURA B. (1996): Occurrence, prevalence and ef- ans by Tetracapsuloides bryosalmonae at sites fects of the myxozoan Tetracapsula bryozoi- endemic for salmonid proliferative kidney di- des parasitic in the freshwater bryozoan Cri- sease. — Dis. Aquat. Org. 57:221-226.

statella mucedo (Bryozoa: Phylactolaemata). TOPS S., BAXA D.V., MCDOWELL T.S., HEDRICK R.P. S B. — Folia Parasitol. 43: 262-266. OKAMURA (2004): Evaluation of malacospore-

OKAMURA B., ANDERSON C.L., LONGSHAW M., FEIST S.W. an life cycles through transmission studies. — & E.U. CANNING (2001): Patterns of occurrence Dis. Aquat. Org. 60: 109-121.

and 18S rDNA sequence variation of PKX (7e- UPTON S.J., FREED P.S., FREED D.A., MCALLISTER C.T.& tracapsula bryosalmonae), the causative S.R. GOLDBERG (1992): Testicular myxosporidai- agent of salmonid proliferative kidney disea- asis in the flat-backed toad, Bufo maculatus se. — J. Parasitol. 87: 379-385. (Amphibia: Bufonidae), from Cameroon, Afri- OKAMURA B. & E.U. CANNING (2003): Orphan worms ca. — J. Wildlife Dis. 28: 326-329. and homeless parasites enhance bilaterian di- VORONIN V.N. (1993): PKX-like organism in common versity. — Trends Ecol. Evol. 18: 633-639. carp during swimbladder inflammation: Furt-

OKAMURA B., CURRY A., WOOD T.S. & E.U. CANNING her evidence of an association with the my- (2002): Ultrastructure of Buddenbrockia iden- xosporean Sphaerospora renicola. — Bull. tifies it as a myxozoan and verifies the bilate- Eur. Ass. Fish Pathol. 13: 127-129. rian origin of the Myxozoa. — Parasitology VORONIN V.N. & N.B. CHERNYSHEVA (1993): An intra- 124:215-223. cellular parasite as the possible causative OKAMURA B. & T.S. WOOD (2002): Bryozoans as hosts agent of mortality during swim-bladder in- for Tetracapsula bryosalmonae, the PKX or- flammation in , Cyprinus carpio ganism. — J. Fish Dis. 25: 469-475. L — J. Fish Dis. 16:609-611.

RADDUM G.G. & T.M. JOHNSEN (1983): Growth and WAHU T., KNUESEL R., BERNET D., SEGNER H., PUGNOVKIN feeding of Fredricella sultana (Bryozoa) in the D., BURKHARDT-HOLM P., ESCHER M. & H. SCHMIDT- outlet of a humic acid lake. — Hydrobiologia POSTHAUS (2002): Proliferative kidney disease 101: 115-120. in Switzerland: Current state of knowledge. — J. Fish Dis. 25:491-500. SCHLEGEL M., LOM J., STECHMANN A., BERNHARD D., LEI- PE D., DYKOVÄ I. & M.L. SOGIN (1996): Phyloge- WOLF K. & M.E. MARKIW (1984): Biology contrave- netic analysis of complete small subunit and nes in the Myxozoa: New discove- ribosomal RNA coding region of Myxidium ries show alternation of invertebrate and ver- lieberkuehni: Evidence that Myxozoa are tebrate hosts. — Science 225: 1449-1452. Metazoa and related to the Bilateria. — Arch. WOOD T.S. (1973): Colony development in species Protistenkd. 147: 1-9. of Plumatella and Fredericella (Ectoprocta: SCHRÖDER O. (1910): Buddenbrockia plumatellae, Phylactolaemata). — In: BOARDMAN T.S., CHEE- eine neue Mesozoenart aus Plumatella re- THAM A.H. S W.A.J. OLIVER (Eds.): Development

297 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at

and Function of Animal Colonies Through Ti- me. Dowden, Hutchinson & Ross, Strouds- burg, PA: 395-432.

WOOD T.S. (2001): Bryozoans. — In: THORP J.H. & A.P. COVICH (Eds.): Ecology and Classification of North American Freshwater Invertebrates. Academic Press, San Diego: 505-525.

ZRZAVY J. (2001): The interrelationships of metazo- an parasites: A review of phylum and higher- level hypotheses from recent morphological and molecular phylogenetic analyses. — Folia Parasitol. 48: 81-103.

ZRZAVY J. & V. HYPSA (2003): Myxozoa, , and the origin of the Bilateria: The phyloge- netic position of 'Endocnidozoa' in light of the rediscovery of Buddenbrockia. — Cladis- tics19: 164-169.

ZRZAVY J., MIHULKA S., KEPKA P., BEZDEK A. & D. TIETZ (1998): Phylogeny of the Metazoa based on morphological and 18s ribosomal DNA evi- dence. — 14: 249-285.

Address of authors: Dr. Sylvie TOPS & Dr. Beth OKAMURA Department of School of Animal & Microbial Sciences University of Reading Whiteknights PO Box 228 Reading RG6 6AJ E-Mail: [email protected]

298