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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
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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),
the class Actinosporea was suppressed lea-
classify them as protists (BRUSCA & BRUSCA
ving only one class (the Myxosporea) wit-
1990; GILBERT & GRANATH 2003). Compel-
hin the phylum (KENT et al. 1994a). To da-
ling evidence that myxozoans should be of-
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
life cycle, but to date no complete malacos-
denbrockia plumateVae).
porean life cycle has been resolved.
The long-standing taxonomic dispute
regarding the phylum Myxozoa has not me-
The class Malacosporea
rely been limited to higher-level phylogene-
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
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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 ell a 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 as both worm-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 morphogenesis 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
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Fig. 2: Buddenbrockia plumatellae infections; a: vermiform stage of B.
plumatellae exiting from the lophophore of a Plumatella fungosa 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 host - 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-
body plan 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, Orthonectida and life cycle of the myxozoan Myxobolus 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 invertebrate 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 Bilateria, 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
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obtained by transmission studies (FEIST et al. North America (KENT et al. 1994b). Econo-
2001). Formerly named Tetracapsula bryosal- mic costs to the U. K. aquaculture 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 Tetracapsulasituations, 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
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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 urine
ted invertebrates. 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.
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Thus far no vertebrate 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 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
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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
Myxobolus cerebralis 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-
cedo (CANNING & OKAMURA 2004). It is
uld be able to ensure that all regions of co-
possible that the life cycle of Buddenbrockia
lonies became infected. In addition, Freden-
plumacellae entails obligate cycling between
cella sultana itself overwinters as live colo-
life history stages or that these different
nies (WOOD 1973; RADDUM &. JOHNSEN
morphologies represent facultative stages,
1983), providing the parasite with a winter-
the expression of which is controlled by an
refuge, thus allowing cryptic infections to be
unidentified cue. Alternatively, they may
maintained year-round in this species (GAY
represent different but closely related spe-
et al. 2001). Finally, should cryptic stages
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 parasitism 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.
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2002; OKAMURA et al. 2002) there has been freshwater bryozoan Cristatella mucedo
(Bryozoa: Phylactolaemata). — Folia Parasitol.
a resurgence of interest in the study of the
43:249-261.
genus 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.
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