Billie L. Kerans

Potamopyrgus antipodarum: distribution, density, and effects on native macroinvertebrate assemblages in the Greater Yellowstone Ecosystem

Abstract Invasive species can have large effects on freshwater communities and ecosystems. Potamopyrgus antipodarum, a snail indigenous to New Zealand, has recently colonized North America. We documented the distribution and density of P. antipodarum in the major tributaries of the Madison River in the Greater Yellowstone Ecosystem, examined associations between P. antipodarum and native macroinvertebrates, and experimentally examined how P. antipodarum affected colonization of substrates by other macroinvertebrates. In 1997 and 1998, we sampled benthic macroinvertebrates in the Madison, Firehole, and Gibbon Rivers and Nez Perce Creek in 3 seasons. In 1999, we examined colonization of P. antipodarum and other macroinvertebrates in a field experiment using slate tiles in the Madison River. In September 1997, we found P. antipodarum at 23 of 32 locations. Where they were present, P. antipodarum densities ranged from 22 to 299,000 ind./m2. Densities of P. antipodarum declined between September 1997 and March 1998 and increased between March and July 1998. The composition and structure of native macroinvertebrate assemblages covaried with P. antipodarum densities. Whether the differences in macroinvertebrate communities among sites were related to differences in physical characteristics of streams or to interactions with P. antipodarum was unclear. However, in the field experiment, high densities of P. antipodarum were associated with low colonization of other macroinvertebrates; thus, negative interactions between native macroinvertebrates and P. antipodarum may have the potential to influence the large-scale distribution of other macroinvertebrates.

DIFFERENTIAL PROPAGATION OF THE METAZOAN PARASITE MYXOBOLUS CEREBRALIS BY LIMNODRILUS HOFFMEISTERI, ILYODRILUS TEMPLETONI, AND GENETICALLY DISTINCT STRAINS OF TUBIFEX TUBIFEX

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.

THE EFFECTS OF MYXOBOLUS CEREBRALIS MYXOSPORE DOSE ON TRIACTINOMYXON PRODUCTION AND BIOLOGY OF TUBIFEX TUBIFEX FROM TWO GEOGRAPHIC REGIONS

The aquatic oligochaete Tubifex tubifex is an obligate host of Myxobolus cerebralis, the causative agent of salmonid whirling disease. Tubifex tubifex can become infected by ingesting myxospores of M. cerebralis that have been released into sediments upon death and decomposition of infected salmonids. Infected worms release triactinomyxons into the water column that then infect salmonids. How the dose of myxospores ingested by T. tubifex influences parasite proliferation and the worm host are not well understood. Using replicated laboratory experiments, we examined how differing doses of myxospores (50, 500, 1,000 per worm) influenced triactinomyxon production and biomass, abundance, and individual weight of 2 geographically distinct populations of T. tubifex. Worm populations produced differing numbers of triactinomyxons, but, within a population, the production did not differ among myxospore doses. At the lowest myxospore dose, 1 worm population produced 45 times more triactinomyxons than myxospores received, whereas the other produced only 6 times more triactinomyxons than myxospores. Moreover, total T. tubifex biomass, abundance, and individual weight were lower among worms receiving myxospores than in myxospore-free controls. Thus, T. tubifex populations differ in ability to support the replication of M. cerebralis, and infection has measurable consequences on fitness of the worm host. These results suggest that variability in whirling disease severity observed in wild salmonid populations may partially be attributed to differences in T. tubifex populations.

Myxobolus cerebralis in Native Cutthroat Trout of the Yellowstone Lake Ecosystem

Abstract The exotic parasite Myxobolus cerebralis was first detected in native adult Yellowstone cutthroat trout Oncorhynchus clarkii bouvierii from Yellowstone Lake in 1998, seriously threatening the ecological integrity of this pristine, naturally functioning ecosystem. We immediately began to assess the prevalence and spatial extent of M. cerebralis infection in Yellowstone cutthroat trout within Yellowstone Lake and to determine the infection risk of age-0 Yellowstone cutthroat trout, the relative abundance and actinospore production of tubificid worms, and the basic environmental characteristics of tributaries. During 1999–2001, juvenile and adult Yellowstone cutthroat trout were infected throughout Yellowstone Lake; the highest prevalence (15.3–16.4%) occurred in the northern and central regions. Exposure studies in 13 streams indicated that Pelican and Clear creeks and the Yellowstone River were positive for M. cerebralis; the highest prevalence (100%) and severity was found in Pelican Creek during...

Risk Of Myxobolus Cerebralis Infection To Rainbow Trout In The Madison River, Montana, USA

Myxobolus cerebralis, the parasite that causes salmonid whirling disease, has had detrimental effects on several salmonid populations in the Intermountain West, including the rainbow trout in the Madison River, Montana, USA. The goal of this study was to examine relationships among characteristics of the environment, Tubifex tubifex (the alternate host) populations, and rainbow trout whirling disease risk in the Madison River. Environmental characteristics were measured in side channels of the Madison River, and differences were described with a principal components analysis. The density of T. tubifex, the prevalence of infection in T. tubifex, and the density of infected T. tubifex were determined for the side channels using benthic core samples and examination of live tubificids for infection. The site-specific contribution to whirling disease risk in the side channels was determined using in situ exposures of sentinel rainbow trout. Regression analyses were used to determine correlations among these characteristics. Side channels differed in site-specific contribution to rainbow trout whirling disease risk, which was positively correlated to the density of infected T. tubifex. Side channels with fine sediments and lower water temperatures made greater site-specific contribution to whirling disease risk and had higher densities of infected T. tubifex than side channels with coarser sediments and higher temperatures. The ability to characterize areas of high whirling disease risk is essential for improving our understanding of the dynamics of M. cerebralis such that appropriate management strategies can be implemented. In addition, this study provides a model of how the disease ecology of complex aquatic parasites can be examined when the influential processes operate on different spatial scales.

Relation of Spawning and Rearing Life History of Rainbow Trout and Susceptibility to Myxobolus cerebralis Infection in the Madison River, Montana

Abstract The Madison River, Montana, is the site of a whirling disease epizootic among rainbow trout Oncorhynchus mykiss caused by the parasite Myxobolus cerebralis. We investigated how the timing and location of the spawning and rearing of rainbow trout influences the risk of exposure to the parasite. Sentinel fish exposures were used to assess the spatial and temporal variation in disease severity in 1998 and 1999. Redd counts, radiotelemetry of spawning rainbow trout, and electrofishing estimates of fry abundance indicated that during the critical 2–3-month posthatch period, when rainbow trout are most susceptible to whirling disease, the majority of fry in the Madison River population are concentrated within a relatively small portion of the upper drainage. Disease severity ranged from low to very high in this area of the river. Large temporal variation in disease severity was also evident: severity was significantly higher in the spring than in the fall and in 1999 than in 1998. These data indicate t...

Water Temperature Affects a Host–Parasite Interaction: Tubifex tubifex and Myxobolus cerebralis

Abstract The aquatic oligochaete worm Tubifex tubifex is an obligate host of Myxobolus cerebralis, the causative agent of salmonid whirling disease. Tubifex tubifex becomes infected by ingesting M. cerebralis myxospores and releases triactinomyxons (TAMs) into the water that then infect salmonids. In a laboratory experiment, we examined how water temperature influenced changes in oligochaete population size and biomass and the release of TAMs in three genetically identified strains of T. tubifex when exposed and not exposed to M. cerebralis myxospores. Increases in population size and biomass were greatest at 8.0°C for the Gallatin River strain, greatest at 15.0°C for the Madison River strain, and similar at both temperatures for the Mt. Whitney strain. After exposure to M. cerebralis myxospores, Mt. Whitney and Madison River T. tubifex both released TAMs at 15°C beginning on day 88 and at 8.0°C on day 169 (Mt. Whitney strain) and day 182 (Madison River strain); thus, between 1,320 and 1,456 degree-days w...

Predator effects on prey population dynamics in open systems

Animal population dynamics in open systems are affected not only by agents of mortality and the influence of species interactions on behavior and life histories, but also by dispersal and recruitment. We used an extensive data set to compare natural loss rates of two mayfly species that co-occur in high-elevation streams varying in predation risk, and experience different abiotic conditions during larval development. Our goals were to generate hypotheses relating predation to variation in prey population dynamics and to evaluate alternative mechanisms to explain such variation. While neither loss rates nor abundance of the species that develops during snowmelt (Baetis bicaudatus) varied systematically with fish, loss rates of the species that develops during baseflow (Baetis B) were higher in streams containing brook trout than streams without fish; and surprisingly, larvae of this species were most abundant in trout streams. This counter-intuitive pattern could not be explained by a trophic cascade, because densities of intermediate predators (stoneflies) did not differ between fish and fishless streams and predation by trout on stoneflies was negligible. A statistical model estimated that higher recruitment and accelerated development enables Baetis B to maintain larger populations in trout streams despite higher mortality from predation. Experimental estimates suggested that predation by trout potentially accounts for natural losses of Baetis B, but not Baetis bicaudatus. Predation by stoneflies on Baetis is negligible in fish streams, but could make an important contribution to observed losses of both species in fishless streams. Non-predatory sources of loss were higher for B. bicaudatus in trout streams, and for Baetis B in fishless streams. We conclude that predation alone cannot explain variation in population dynamics of either species; and the relative importance of predation is species- and environment-specific compared to non-predatory losses, such as other agents of mortality and non-consumptive effects of predators.

A Risk Assessment Based Approach for the Management of Whirling Disease

This article began as an exercise during the 9th Annual Whirling Disease Symposium, “Whirling Disease: Managing the Risk” held in Seattle, Washington, in 2003. The exercise was designed to address the needs of fishery managers to more accurately assess the various factors associated with the risks of the introduction and the establishment of the myxosporean parasite, Myxobolus cerebralis, and the development of whirling disease in salmonids. Here we introduce concepts used in risk assessment, review aspects of whirling disease relevant to risk assessment, present a working model for a whirling disease risk assessment, and work through examples of how this model might be used to estimate risks and identify actions to reduce these risks. While this approach was designed to address factors controlling the introduction and establishment of M. cerebralis and the development of whirling disease in salmonids, the concepts are highly relevant to the management of other infectious diseases of aquatic animals.

Variability in triactinomyxon production from Tubifex tubifex populations from the same mitochondrial DNA lineage infected with Myxobolus cerebralis, the causative agent of whirling disease in salmonids.

Myxobolus cerebralis, the causative agent of whirling disease, infects both salmonid fish and an aquatic oligochaete, Tubifex tubifex. Although M. cerebralis has been detected in river drainages throughout the United States, disease severity among wild fish populations has been highly variable. Tubifex tubifex populations have been genetically characterized using sequences from the 16S mitochondrial DNA (mtDNA) gene, the 18S ribosomal RNA gene, the internal transcribed spacer region 1 (ITS1), and randomly amplified polymorphic DNA (RAPD). Our earlier work indicated that large differences in compatibility between the parasite and populations of T. tubifex may play a substantial role in the distribution of whirling disease and resulting mortality in different watersheds. In the present study, we examined 4 laboratory populations of T. tubifex belonging to 16S mtDNA lineage III and 1 population belonging to 16S mtDNA lineage I for triactinomyxon (TAM) production after infection with M. cerebralis myxospores. All 4 16S mtDNA lineage III populations produced TAMs, but statistically significant differences in TAM production were observed. Most individuals in the 16S mtDNA lineage III-infected populations produced TAMs. The 16S mtDNA lineage I population produced few TAMs. Further genetic characterization of the 16S mtDNA lineage III populations with RAPD markers indicated that populations producing similar levels of TAMs had more genetic similarity.