Bryozoan Hosts Research Articles

Development and Phenotypic Plasticity of Tubes and Tubaria of the Living Graptolite Rhabdopleura recondita (Pterobranchia, Hemichordata)

The extant graptolite Rhabdopleura recondita has been so far recorded only as inhabiting a bryozoan skeleton. Its larval settlement and metamorphosis are possible in the absence of a bryozoan zoarium, whereas further colony development may require that the larva is hidden inside the bryozoan host. This dependence may constrain the development of R. recondita tube and tubaria compared to the other Rhabdopleura species that develop without a host. We report here on larval settlement and metamorphosis in the absence/presence of a bryozoan host skeleton. We also make the first attempt to test the phenotypical response of R. recondita tubes and tubaria under variable hydrodynamic regimes in laboratory conditions. After 40 days, no significant variation was detected in the number or length of the newly formed tubes. These findings suggest that R. recondita eventually resides in a narrow velocity range and that tube and tubarium development is largely invariable.

Identification of in vivo induced antigens of the malacosporean parasite Tetracapsuloides bryosalmonae (Cnidaria) using in vivo induced antigen technology.

Tetracapsuloides bryosalmonae is a malacosporean endoparasite that causes proliferative kidney disease (PKD) in wild and farmed salmonids in Europe and North America. The life cycle of T. bryosalmonae completes between invertebrate bryozoan and vertebrate fish hosts. Inside the fish, virulence factors of T. bryosalmonae are induced during infection or interactions with host cells. T. bryosalmonae genes expressed in vivo are likely to be important in fish pathogenesis. Herein, we identify in vivo induced antigens of T. bryosalmonae during infection in brown trout (Salmo trutta) using in vivo induced antigen technology (IVIAT). Brown trout were exposed to the spores of T. bryosalmonae and were sampled at different time points. The pooled sera were first pre-adsorbed with antigens to remove false positive results. Subsequently, adsorbed sera were used to screen a T. bryosalmonae cDNA phage expression library. Immunoscreening analysis revealed 136 immunogenic T. bryosalmonae proteins induced in brown trout during parasite development. They are involved in signal transduction, transport, metabolism, ion-protein binding, protein folding, and also include hypothetical proteins, of so far unknown functions. The identified in vivo induced antigens will be useful in the understanding of T. bryosalmonae pathogenesis during infection in susceptible hosts. Some of the antigens found may have significant implications for the discovery of candidate molecules for the development of potential therapies and preventive measures against T. bryosalmonae in salmonids.

Current and projected impacts of the parasite Tetracapsuloides bryosalmonae (causative to proliferative kidney disease) on Central European salmonid populations under predicted climate change

Abstract Proliferative kidney disease (PKD) caused by the myxozoan parasite Tetracapsuloides bryosalmonae is an emerging salmonid disease implicated in recent declines in salmonid populations. Laboratory experiments have shown that the clinical symptoms of PKD exacerbate with increasing temperature. However, empirical evidence for a relationship between climate change and PKD driven declines in wild salmonid stocks is scarce. The current study uses both empirical data and ecological niche modelling to extrapolate future changes in temperature and precipitation on the spread of PKD in relation to changes in suitability of rivers for its primary bryozoan and secondary salmonid hosts. A 20‐year dataset on brown trout density using standardised method shows a decline of more than 50% in the population of the river Wutach, south‐western Germany at 536–755 m elevation. The decline coincides with higher prevalence of PKD. This decline was temperature related and driven by reduced local survival of parr to yearlings. Kidney hyperplasia was highest at low elevations and correlated negatively with trout density. Niche models based on state‐wide data show strong overlap in the areas suitable for T. bryosalmonae and its primary bryozoan hosts, and a strong link with temperature. Projections based on moderate to high emission‐case climate change scenarios predict a 50%–82% decrease in the area suitable for salmonids within this century, linked to PKD. The empirical data identify temperature‐mediated PKD as the underlying cause of the population decline. This relationship was corroborated by the niche modelling results. The highest losses are expected in projected salmonid suitable areas where salmonid habitats currently overlap with areas suitable for T. bryosalmonae. With ongoing climate change, both current and future populations are at severe risk to T. bryosalmonae and its associated disease PKD. Conservation efforts of salmonid stocks are dependent on climate mitigation and measures to help salmonids adapt to the disease.

An eDNA-based method for monitoring a salmonid infectious disease: Development and application

In the current context of global change, freshwater species are increasingly exposed to emerging infectious diseases (Okamura and Feist 2011). As an example, the Proliferative Kidney Disease (PKD) has emerged in salmonid fish during the last two decades, both in Europe and North America, causing important losses in aquaculture and worrying declines of several wild salmonid populations (Sudhagar et al. 2019). It is caused by Tetracapsuloides bryosalmonae, a myxozoan parasite with a complex life cycle involving two hosts: salmonids (intermediate host) and bryozoans (primary host). As PKD development strongly depends upon water temperature and quality, it is expected that global change could lead to more outbreaks (Okamura et al. 2011). Current monitoring of fish parasite load and infection status relies on histological observation or T. bryosalmonae DNA amplification out of kidney samples, involving fish euthanasia, and thus relatively small sample sizes when inferring infection prevalence. As large-scale screening of this parasite infections are required to better understand PKD dynamics, we have developed a non-lethal method for T. bryosalmonae detection in fish host based on the biological fact that T. bryosalmonae spores can be excreted from infected fish into the water through urine (Hedrick et al. 2004). This novel approach based on the detection of T. bryosalmonae DNA in fish urine was developed on wild brown trout (Salmo trutta), a species known to be an intermediate host of T. bryosalmonae and for releasing infective spores (only towards bryozoan host) through urine (Okamura et al. 2011). Applying this method, we have been able to map wild brown trout infection prevalence across 50 sites at the foothill of French Pyrenees and to identify the main environmental drivers of this disease.

Caupokeras badalloi, a new ichnospecies of impedichnia from the Lower Devonian of Spain. Palaeoecological significance

ABSTRACT A new ichnospecies, Caupokeras badalloi, is here erected from the Emsian (Lower Devonian) Aguión Formation of Asturias, NW Spain. It is a bioclaustration structure produced by the host-specific symbiotic intergrowth of two host bryozoan species, Leioclema elegans and Loxophragma cf. leptum, and a soft-bodied modular symbiont, possibly a hydroid. The distinctiveness of this bioclaustration structure creates the need for a new ichnotaxonomic name. The settlement and development of the symbiont on living colonies of bryozoan hosts formed sets of tubes with terminal openings that do not occur in non-symbiotic bryozoans, thus modifying the normal growth of its living substrate. Consequently, C. badalloi n. isp. is considered herein as belonging to the ethological category of impedichnia in the absence of a universally accepted criterion on the status of bioclaustration structures. The diagnosis of the ichnogenus Caupokeras is emended.

First evidence of virus-like particles in the bacterial symbionts of Bryozoa

Bacteriophage communities associated with humans and vertebrate animals have been extensively studied, but the data on phages living in invertebrates remain scarce. In fact, they have never been reported for most animal phyla. Our ultrastructural study showed for the first time a variety of virus-like particles (VLPs) and supposed virus-related structures inside symbiotic bacteria in two marine species from the phylum Bryozoa, the cheilostomes Bugula neritina and Paralicornia sinuosa. We also documented the effect of VLPs on bacterial hosts: we explain different bacterial ‘ultrastructural types’ detected in bryozoan tissues as stages in the gradual destruction of prokaryotic cells caused by viral multiplication during the lytic cycle. We speculate that viruses destroying bacteria regulate symbiont numbers in the bryozoan hosts, a phenomenon known in some insects. We develop two hypotheses explaining exo- and endogenous circulation of the viruses during the life-cycle of B. neritina. Finally, we compare unusual ‘sea-urchin’-like structures found in the collapsed bacteria in P. sinuosa with so-called metamorphosis associated contractile structures (MACs) formed in the cells of the marine bacterium Pseudoalteromonas luteoviolacea which are known to trigger larval metamorphosis in a polychaete worm.

A checklist of ciliate epibionts (Ciliophora) found on bryozoans.

A compilation of the ciliate (Ciliophora) species found on marine and fresh water bryozoans as epibionts has been carried out based on published records. The checklist includes the taxonomic position of each species of epibiontic ciliate, the species of basibiont bryozoans, localities and the bibliographic references. Altogether 40 ciliate species from classes Spirotrichea (two species); Suctorea (sixteen species); Oligohymenophorea, subclass Peritrichia (sixteen species) and Heterotrichea, family Folliculinidae (six species) were listed. Among registered species, six were reported on bryozoans only. Only one species of peritrich ciliate Ellobiophrya conviva adapted to inhabit on tentacles of bryozoans with special adhesive organelle (cinctum or adhesive ring) indicate a possible specific to bryozoan host.

PCR-RFLP: a targeted method to reveal host specific malacosporean infection profiles (Cnidaria: Myxozoa: Malacosporea).

Malacosporeans are a group of endoparasitic cnidarians (Myxozoa) that use freshwater bryozoans and fish as final and intermediate hosts, respectively. The malacosporean Tetracapsuloides bryosalmonae causes proliferative kidney disease (PKD), an emerging disease in aquaculture and wild fish populations, including threatened salmonids in Europe and the USA. Mixed infections of malacosporeans are often encountered, and a monitoring tool for screening of multiple malacosporean species in either their fish or bryozoan hosts is therefore desirable. We describe an inexpensive method that combines PCR amplification of the partial 18S rRNA gene (~260 bp) and a single-step restriction fragment length polymorphism (RFLP) method for identification of 10 malacosporean lineages and species. We demonstrate and test this methodology on a set of DNA extracted from malacosporeans infecting fish kidney and tissues sampled from bryozoan colonies and compare the results with Sanger sequencing of the same parasite DNA isolates. The PCR-RFLP and Sanger sequencing methods agreed in 100% of cases. The PCR-RFLP method offers a number of opportunities, including screening large panels of host tissue samples to gain insights into infection patterns, characterizing mixed infections, and confirming highly pathogenic T. bryosalmonae infections. The method can also be further refined as new sequence data become available for malacosporeans.

Life in a living substrate: Modular endosymbionts of bryozoan hosts from the Devonian of Spain

A new bioclaustration structure is described from the Emsian (Lower Devonian) Aguión Formation of Asturias, NW Spain. It is the result of intergrowth of two bryozoan species, Leioclema elegans and Loxophragma cf. leptum, hosting an unknown soft-bodied modular symbiont. These structures point to the development of host-specific symbiotic associations in which both partners grew simultaneously. The association is tentatively assessed as commensalism; no evidence suggesting parasitism or mutualism has been found. A revision of the existing literature on Devonian bryozoans reveals that tubular structures similar to those described herein have been observed in different regions of the world. Only a few trepostome genera developed this kind of association during the Devonian, and Leioclema seems to have been a suitable partner in intergrowths with a range of soft-bodied and skeletonized organisms. It is suggested that the association described herein was relatively common during the Devonian and that molecular factors such as chemical mediation may have played a role in conducting the development of these specific intergrowths.

The Malacosporean Myxozoan Parasite Tetracapsuloides bryosalmonae: A Threat to Wild Salmonids.

Tetracapsuloides bryosalmonae is a myxozoan parasite responsible for proliferative kidney disease (PKD) in a wide range of salmonids. PKD, characterized by high mortality and morbidity, is well known for affecting aquaculture operations and wild salmonid populations across Europe and North America. The life cycle of T. bryosalmonae revolves around freshwater bryozoan and salmonid fish hosts. In recent years, T. bryosalmonae has been reported among wild salmonids from the European countries where it has not been reported previously. T. bryosalmonae is believed to be a possible reason for the diminishing wild salmonid populations in the natural water bodies of many European countries. Climate crisis driven rising water temperature can further accelerate the distribution of T. bryosalmonae. Expansion of the geographical distribution of T. bryosalmonae may further advocate the decline of wild salmonid populations, especially brown trout (Salmo trutta) in their habitats. Mathematical models are used to understand the pattern and distribution of T. bryosalmonae among the host in the natural water bodies. The present manuscript not only summarizes the incidences of T. bryosalmonae among the wild salmonid populations, but also discusses the contemporary understanding about the development of T. bryosalmonae in its hosts and the influences of various factors in the spread of the disease in the wild.

A rugose coral – bryozoan association from the Lower Devonian of NW Spain

A new rugose coral-cystoporate bryozoan association is here described from the Devonian of NW Spain. This is the first evidence of intergrowths between Devonian rugose corals and bryozoans. In this case bryozoans provided a suitable substrate for the settlement of corals, which were subsequently encrusted by the bryozoans. The hypothesis of intergrowth between living organisms is supported by the absence of encrustation of the rugose coral calices by the cystoporates. We suggest that the association was specific and developed through chemical mediation. This symbiosis was facultative for the bryozoans but likely not for the corals. The association provided the bryozoan host with additional substrate for encrustation as well as protection from various predators, and it allowed the rugose corals to grow in a muddy environment and benefit from the feeding currents of the bryozoans.

Symbiosis of conulariids with trepostome bryozoans in the Upper Ordovician of Estonia (Baltica)

The trepostome bryozoans Diplotrypa abnormis, D. bicornis, D. petropolitana, Esthoniopora communis, E. subsphaerica, Mesotrypa excentrica, M. expressa, M. raritabulata, and Monotrypa jewensis have symbiotic associations with the conulariid Climacoconus bottnicus in the Upper Ordovician of Estonia. All bryoimmured conulariids are very small and oriented perpendicular (or nearly so) to the growth surface of the host trepostome colony. Muddy seafloors may have promoted this symbiosis between conulariids and bryozoans because the former required a hard substrate for attachment. It is possible that the numerous smaller specimens among endobiotic conulariids usually died as juveniles together with their bryozoan host, or alternatively, the smaller endobiotic conulariids may have been Lilliput forms of free-living conulariids that died at a mature age. Conulariid-trepostome associations were likely not a result of accidental intergrowth of two organisms. Additional protection against predators provided by the calcitic bryozoan skeleton may have been among the benefits for the conulariid symbionts. Usually trepostomes with conulariid symbionts do not contain other invertebrates, but in the Katian in some cases they also hosted Anoigmaichnus bioclaustrations. The exact type of symbiosis between trepostomes and conulariids remains unresolved, but most likely the associations were slightly parasitic or commensal. The available data suggest that bryozoans preferred cnidarians over the other invertebrates as symbionts.

Tetracapsuloides bryosalmonae abundance in river water.

Tetracapsuloides bryosalmonae is a myxozoan parasite of freshwater bryozoans and salmonids, causing proliferative kidney disease in the latter. To date, detection of the parasite has required collection of hosts and subsequent molecular or histological examination. The release of infectious spores from both hosts offers an opportunity to detect the parasite in water samples. We developed a novel SYBR® Green quantitative real-time PCR (qPCR) assay for T. bryosalmonae in water samples which provides an estimation of bryozoan malacospore numbers and tested the assay in 3 rivers in southern England (UK) over a period of 5 wk. The assay proved to be both highly sensitive and specific to the parasite, detecting low levels of spores throughout the study period. Larger-volume samples afforded greater detection likelihood, but did not increase the number of spores detected, possibly as a result of low and patchy spore distributions and lack of within-site replication of large-volume samples. Based on point-measurements, temperature was positively associated with the likelihood of detecting spores, possibly reflecting the temperature dependence of spore shedding from bryozoan hosts. The presence of T. bryosalmonae in water samples was predominantly influenced by spatial (sites within rivers, amongst rivers) and temporal (sampling dates) factors, while the latter also influenced quantification cycle (Cq) values and spore abundance. Environmental monitoring for infectious stages can complement traditional methods, providing faster and easier detection and avoiding potentially prolonged searching, collecting and destructive sampling of invertebrate and vertebrate hosts.

Conditional persistence and tolerance characterize endoparasite-colonial host interactions.

Colonial hosts offer unique opportunities for exploitation by endoparasites resulting from extensive clonal propagation, but these interactions are poorly understood. The freshwater bryozoan, Fredericella sultana, and the myxozoan, Tetracapsuloides bryosalmonae, present an appropriate model system for examining such interactions. F. sultana propagates mainly asexually, through colony fragmentation and dormant propagules (statoblasts). Our study examines how T. bryosalmonae exploits the multiple transmission routes offered by the propagation of F. sultana, evaluates the effects of such transmission on its bryozoan host, and tests the hypothesis that poor host condition provokes T. bryosalmonae to bail out of a resource that may soon be unsustainable, demonstrating terminal investment. We show that infections are present in substantial proportions of colony fragments and statoblasts over space and time and that moderate infection levels promote statoblast hatching and hence effective fecundity. We also found evidence for terminal investment, with host starvation inducing the development of transmission stages. Our results contribute to a growing picture that interactions of T. bryosalmonae and F. sultana are generally characterized by parasite persistence, facilitated by multiple transmission pathways and host condition-dependent developmental cycling, and host tolerance, promoted by effective fecundity effects and an inherent capacity for renewed growth and clonal replication.

Description and experimental transmission of Tetracapsuloides vermiformis n. sp. (Cnidaria: Myxozoa) and guidelines for describing malacosporean species including reinstatement of Buddenbrockia bryozoides n. comb. (syn. Tetracapsula bryozoides).

This paper provides the first detailed description of a Tetracapsuloides species, Tetracapsuloides vermiformis n. sp., with vermiform stages in the bryozoan host, Fredericella sultana, and its experimental transmission from F. sultana to Cyprinus carpio. The suitability of morphological, biological and 18S rDNA sequence data for discrimination between malacosporean species is reviewed and recommendations are given for future descriptions. Presently, malacosporean species cannot be differentiated morphologically due to their cryptic nature and the lack of differential characters of spores and spore-forming stages in both hosts. We examined biological, morphological and molecular characters for the present description and for revising malacosporean taxonomy in general. As a result, Buddenbrockia plumatellae was split into two species, with its sac-like stages being ascribed to Buddenbrockia bryozoides n. comb. In addition to ribosomal DNA sequences multiple biological features rather than morphological characters are considered essential tools to improve malacosporean taxonomy in the future according to our analysis of the limited traits presently available.

Tetracapsuloides bryosalmonae infection affects the expression of genes involved in cellular signal transduction and iron metabolism in the kidney of the brown trout Salmo trutta.

Tetracapsuloides bryosalmonae is an enigmatic endoparasite which causes proliferative kidney disease in various species of salmonids in Europe and North America. The life cycle of the European strain of T. bryosalmonae generally completes in an invertebrate host freshwater bryozoan and vertebrate host brown trout (Salmo trutta) Linnaeus, 1758. Little is known about the gene expression in the kidney of brown trout during the developmental stages of T. bryosalmonae. In the present study, quantitative real-time PCR was applied to quantify the target genes of interest in the kidney of brown trout at different time points of T. bryosalmonae development. PCR primers specific for target genes were designed and optimized, and their gene expression levels were quantified in the cDNA kidney samples using SYBR Green Supermix. Expression of Rab GDP dissociation inhibitor beta, integral membrane protein 2B, NADH dehydrogenase 1 beta subcomplex subunit 6, and 26S protease regulatory subunit S10B were upregulated significantly in infected brown trout, while the expression of the ferritin M middle subunit was downregulated significantly. These results suggest that host genes involved in cellular signal transduction, proteasomal activities, including membrane transporters and cellular iron storage, are differentially upregulated or downregulated in the kidney of brown trout during parasite development. The gene expression pattern of infected renal tissue may support the development of intraluminal sporogonic stages of T. bryosalmonae in the renal tubular lumen of brown trout which may facilitate the release of viable parasite spores to transmit to the invertebrate host bryozoan.

Diversification and repeated morphological transitions in endoparasitic cnidarians (Myxozoa: Malacosporea)

Malacosporeans are a poorly known myxozoan clade that uniquely demonstrates a tissue level of organisation. Thus, when exploiting their invertebrate hosts (freshwater bryozoans) they occur as non-motile sacs or vermiform stages capable of active swimming. We combine phylogenetic analyses of SSU and LSU rDNA with morphological observations to substantially enhance understanding of malacosporean diversification. The phylogenetic analyses incorporate the widest taxon sampling and geographic cover to date, reveal four novel malacosporean lineages and several putatively new species, one with a novel morphology of irregular, bulbous sacs and no musculature. This lineage currently forms the earliest branch of malacosporeans. Vermiform stages may have been lost or gained several times within the Malacosporea, even in cases where SSU sequence divergence is very low. Yet, sac and vermiform Buddenbrockia plumatellae appear to be separate species, an inference also supported by their utilisation of different bryozoan hosts. Cryptic speciation is also apparent with two novel, genetically divergent lineages (novel lineage 2 and Buddenbrockia sp. 4) being morphologically indistinguishable from known species. Finally, we provide evidence that fredericellid bryozoans are the main hosts for Tetracapsuloides bryosalmonae and are therefore most relevant for research on the ecology and management of Proliferative Kidney Disease of salmonid fish.

Vertical transmission ofTetracapsuloides bryosalmonae(Myxozoa), the causative agent of salmonid proliferative kidney disease

The freshwater bryozoan, Fredericella sultana, is the main primary host of the myxozoan endoparasite, Tetracapsuloides bryosalmonae which causes proliferative kidney disease (PKD) of salmonid fish. Because spores that develop in bryozoan colonies are infectious to fish, bryozoans represent the ultimate source of PKD. Bryozoans produce numerous seed-like dormant stages called statoblasts that enable persistence during unfavourable conditions and achieve long-distance dispersal. The possibility that T. bryosalmonae may undergo vertical transmission via infection of statoblasts has been the subject of much speculation since this is observed in close relatives. This study provides the first evidence that such vertical transmission of T. bryosalmonae is extensive by examining the proportions of infected statoblasts in populations of F. sultana on two different rivers systems and confirms its effectiveness by demonstrating transmission from material derived from infected statoblasts to fish hosts. Vertical transmission in statoblasts is likely to play an important role in the infection dynamics of both bryozoan and fish hosts and may substantially contribute to the widespread distribution of PKD.

Hydroid epifaunal communities in Arctic coastal waters (Svalbard): effects of substrate characteristics

The knowledge of cryptic epifaunal groups in the Arctic is far from complete mostly due to logistic difficulties. Only recently, advances in sample collection using SCUBA diving techniques have enabled to explore delicate hydroid fauna from shallow waters. This study is the first attempt to examine the relationship between substrate property (such as size of rock, morphological characteristics of algal or bryozoan host) and hydroid community composition and diversity in the Arctic. Samples of substrates for hydroid attachment including rocks, algae, bryozoans and other hydrozoans were collected around the Svalbard. Examination revealed no substrate-specific species. The substrate property did not have a strong influence on hydroid community. Both species composition and richness were not related to colonized rock surface area and to morphological characteristic of algal host. Therefore, results indicate the opportunistic nature of hydroid fauna in terms of substrate preference. However, the presence or absence of hydroids depended on the surface area of rocky substrate. Hydroids were more often present on rocks of larger surface area. Erect hydroids and bryozoans were important attachment surface for stolonal hydroids.

Castrating parasites and colonial hosts

Trajectories of life-history traits such as growth and reproduction generally level off with age and increasing size. However, colonial animals may exhibit indefinite, exponential growth via modular iteration thus providing a long-lived host source for parasite exploitation. In addition, modular iteration entails a lack of germ line sequestration. Castration of such hosts by parasites may therefore be impermanent or precluded, unlike the general case for unitary animal hosts. Despite these intriguing correlates of coloniality, patterns of colonial host exploitation have not been well studied. We examined these patterns by characterizing the responses of a myxozoan endoparasite, Tetracapsuloides bryosalmonae, and its colonial bryozoan host, Fredericella sultana, to 3 different resource levels. We show that (1) the development of infectious stages nearly always castrates colonies regardless of host condition, (2) castration reduces partial mortality and (3) development of transmission stages is resource-mediated. Unlike familiar castrator-host systems, this system appears to be characterized by periodic rather than permanent castration. Periodic castration may be permitted by 2 key life history traits: developmental cycling of the parasite between quiescent (covert infections) and virulent infectious stages (overt infections) and the absence of germ line sequestration which allows host reproduction in between bouts of castration.