Modeling Abiotic Influences on Disease Dynamics for the Complex Life Cycle of the Myxozoan ...

198 Pages·2013·2.82 MB·English

by  Ray, Robert

AN ABSTRACT OF THE DISSERTATION OF

Robert Adam Ray for the degree of Doctor of Philosophy in Fisheries Science presented
on September 26th, 2013.
Title: Modeling Abiotic Influences on Disease Dynamics for the Complex Life Cycle of
the Myxozoan Parasite Ceratomyxa shasta.

Abstract approved:
Jerri L. Bartholomew
Most parasites and their hosts live in a balance within their environment; however
a disease outbreak can occur when either the parasite, host, or environment, are
perturbed. Myxozoan parasites are associated with a wide variety of cultured and wild
fish populations. Most myxozoans are relatively benign to their vertebrate host; however
some cause dramatic population level effects on both cultured and wild fish populations.
These parasites have a complex life cycle involving a vertebrate host (fish), an
invertebrate host (annelid), and two spore stages (actinospore and myxospore).
Interactions between these parasites and their hosts can be strongly influenced by
environmental factors, most notably by water temperature and water velocity. Given the
complex life cycle of myxozoan parasites and the lack of any chemical treatments or
preventatives, controlling infections and disease caused by these parasites is challenging,
especially for wild populations.
The myxozoan Ceratomyxa shasta is endemic to many of the major rivers of the
Pacific Northwest and infects all species of Pacific salmon. In the Klamath River, CA,
USA, C. shasta infection is associated with decreased returns of adult Chinook salmon
(Oncorhynchus tshawytscha). The goals of this dissertation were to 1) quantify the effect
that elevated water temperature has on C. shasta-induced disease severity and mortality
rate for both Chinook and coho (O. kitsch) salmon, 2) identify transmission patterns and
quantify transmission rates of the actinospore stage to the salmon host, 3) develop an
epidemiological model of this host-parasite life cycle and assess the sensitivity of specific
parameters that may act as suitable management strategies, and 4) utilize a mixture cure
model, an alternative survival analysis method, to quantify the effects water temperature
and discharge on the total and rate of C. shasta-induced mortality of both Chinook and
coho salmon.
I found that, similar to disease progression naïve salmon species (i.e. from waters
where C. shasta is absent), elevated water temperature increases the rate and overall
mortality for salmon species from river systems where the parasite is endemic. Elevated
water temperatures also increase the transmission rate of the actinospore stage to the
salmon host. The transmission rate of the actinospore stage to the salmon host was
inversely related to water velocity, and I identified a potential velocity threshold of
~0.3m/sec, above which transmission was greatly reduced. From the epidemiological
model I sensitivity analyses and identified that reduction of the myxospore transmission
rate from the adult salmon to the polychaete host during the winter may be the most
effective management action to reduce C. shasta-related disease in the Klamath River.
This action could potentially be achieved by increasing discharge during the winter to
minimize contact between the polychaete host and myxospore stage. Lastly, I applied the
mixture cure models to quantify how the daily survival rates of Chinook and coho salmon
change over time after the fish become infected with C. shasta. Although varied in
approach, the output from both of the models presented in this dissertation can be used to
guide management and conservation actions for fish populations affected by myxozoan
parasites.
© Copyright by Robert Adam Ray
September 26, 2013
All Rights Reserved
Modeling Abiotic Influences on Disease Dynamics for the Complex Life Cycle of the
Myxozoan Parasite Ceratomyxa shasta.

by
Robert Adam Ray

A DISSERTATION
Submitted to
Oregon State University

In partial fulfillment of
the requirements for the
degree of

Doctor of Philosophy

Presented September 26, 2013
Commencement June 2014
Doctor of Philosophy dissertation of Robert Adam Ray presented on September 26, 2013.

APPROVED:

Major Professor, representing Fisheries Science

Head of the Department of Fisheries and Wildlife

Dean of the Graduate School

I understand that my dissertation will become part of the permanent collection of Oregon
State University libraries. My signature below authorizes release of my dissertation to
any reader upon request.

Robert Adam Ray, Author
ACKNOWLEDGEMENTS

I would like to thank my advisor Dr. Jerri Bartholomew for letting me work on this
engaging project and providing constant feedback, support, and encouragement. Thank
you to everyone in the Bartholomew lab for making the past 6 years an enjoyable and
memorable experience. I would also like to thank Dr. Rich Holt, Dr. Sascha Hallett, Dr.
Julie Alexander, and Gerri Buckles for allowing me to pester them with my questions and
taking the time to share their experiences and knowledge with me. Thank you to Dr.
Russell Perry and Dr. Nicholas Som for guiding and nurturing me in all things statistical.
Lastly, I would like to thank my parents and my family (Katie, Kaleb and Sydney) for
their support and companionship throughout.
CONTRIBUTION OF AUTHORS
Dr. Jerri Bartholomew served as the major advisor and was involved in all aspects of the
research presented in this dissertation. Dr. Richard A. Holt assisted with experimental
design, field and laboratory data collection, and provided editorial feedback of Chapter 2.
Dr. Nicholas A. Som and Dr. Russell W. Perry assisted with model development,
analysis, and writing of Chapter 5.
TABLE OF CONTENTS

Page
Chapter 1: Introduction.......................................................................................... 1
Disease ecology: parasites, hosts, and environment.................................. 1
Myxozoan parasites..................................................................................... 4
Environmental influences on myxozoan infection......................... 5
Ceratomyxa shasta..................................................................................... 8
Environmental influence on Ceratomyxa shasta infection............ 9
Epidemiological models............................................................................. 10
Survival analysis......................................................................................... 12
Research objectives.................................................................................... 14
References.................................................................................................. 17
Chapter 2: Relationship between temperature and C. shasta–induced mortality in
Klamath River salmonids......................................................................................... 24
Abstract........................................................................................................ 25
Introduction................................................................................................. 27
Methods and Materials................................................................................. 30
Results.......................................................................................................... 34
Discussion..................................................................................................... 38
Acknowledgements...................................................................................... 44
Literature cited.............................................................................................. 45
Chapter 3: Estimation of Transmission Dynamics of the Ceratomyxa shasta
Actinospore Stage to the Salmonid Host.................................................................. 54