Differential Propagation of the Metazoan Parasite Myxobolus Cerebralis by Limnodrilus Hoffmeisteri, Ilyodrilus Templetoni, and Genetically Distinct Strains of Tubifex Tubifex

Abstract

Whirling disease, caused by the parasite Myxobolus cerebralis, has infected rainbow trout (Oncorhynchus mykiss) and other salmonid fish in the western United States, often with devastating results to native populations but without a discernible spatial pattern. The parasite develops in a complex 2-host system in which the aquatic oligochaete Tubifex tubifex is an obligate host. Because substantial differences in whirling disease severity in different areas of North America did not seem explainable by environmental factors or features of the parasite or its fish host, we sought to determine whether ecological or genetic variation within oligochaete host populations may be responsible. We found large differences in compatibility between the parasite and various laboratory strains of T. tubifex that were established from geographic regions with different whirling disease histories. Moreover, 2 closely related species of tubificids, Limnodrilus hoffmeisteri and Ilyodrilus templetoni, which occur naturally in mixed species assemblages with T. tubifex, were incompatible with M. cerebralis. Virulence of the parasite was directly correlated with the numbers of triactinomyxon spores that developed within each strain of T. tubifex. Thus, the level of virulence was directly related to the compatibility between the host strain and the parasite. Genetic analyses revealed relationships that were in agreement with the level of parasite production. Differences in compatibilities between oligochaetes and M. cerebralis may contribute to the spatial variance in the severity of the disease among salmonid populations.

Accelerated deactivation of Myxobolus cerebralis myxospores by susceptible and non-susceptible Tubifex tubifex

“…In contrast, studies all across western North America have repeatedly demonstrated that T. tubifex oligochaetes belonging to Lineages IV, V and VI are refractory to M. cerebralis infection (DuBey & Caldwell 2004, DuBey et al 2005, Arsan et al 2007, Hallett et al 2009, Zielinski et al 2011, Nehring et al 2013. Likewise, Limnodrilus hoffmeisteri and Ilyodrilus templetoni are also refractory to the M. cerebralis parasite (Kerans et al 2004). These 2 species of tubificids are closely related to T. tubifex and often occur in sympatry with them in microhabitats laden with organically rich fine sediments in both lakes and streams.…”

“…Some investigators have suggested that tubificids that are not susceptible to infection by the M. cerebralis parasite might be capable of deactivating M. cerebralis myxospores in the aquatic environment (Kerans et al 2004, Beauchamp et al 2005, 2006, Nehring et al 2013. However, none of those studies were designed to directly address that possibility.…”

“…The Eagle River treatment group (Table 3) was a mixed culture of T. tubifex oligochaetes belonging to Lineages I, III, V and VI. Lineage I worms from the Gallatin River in Montana, did produce a few TAMs when the dosage was 1000 myxospores worm −1 (Kerans et al 2004). Likewise, 77% of Lineage I oligochaetes from Windy Gap Reservoir, Colorado, that were exposed to 6000 myxospores worm −1 did release some TAMs (Beauchamp et al 2002).…”

“…Deactivation of myxospores in the natural environment by these tubificids could reduce or eliminate M. cerebralis infections where they were the dominant oligochaete (Beauchamp et al 2002, 2006, Kerans et al 2004, Nehring et al 2013. The objective of our study was to answer that question.…”

Effect of cadmium on the susceptibility of Tubifex tubifex to Myxobolus cerebralis (Myxozoa), the causative agent of whirling disease

“…Infection in T. tubifex may persist for the duration of the worm's lifespan and release of TAMs can occur periodically over the span of at least a few years (Gilbert & Granath 2001). Infected worms suffer from suppressed feeding, reduced growth (Stevens et al 2001, Kerans et al 2004, Steinbach Elwell et al 2006, Rasmussen et al 2008) and inhibited reproductive development (Shirakashi & El-Matbouli 2009), though no obvious parasite effects on survival have been shown (Shirakashi & El-Matbouli 2009). Several studies have revealed the importance of environmental factors such as temperature and substrate (Kerans & Zale 2002) and water flow ) on the establishment and development of the parasite within T. tubifex.…”