AN ABSTRACT OF THE THESIS OF
Wataru Koketsu for the degree of Master of Science in Fisheries Science
Presented on April 19, 2004.
Title: Environmental Correlates of Parasitism in Introduced Threespine Stickleback
(Gasterosteus aculeatus) in the Upper Deschutes River Basin, Oregon
Redacted for Privacy
Abstract Approved:
W. Daniel Edge
The Pseudophyllidean tapeworm, Schistocephalus solidus, is a parasite that
requires both copepods and fish, mainly the threespine stickleback (Gasterosteus
aculeatus) as intermediate hosts, and birds as its final host to complete its life cycle. A
rapid increase in the abundance of both the non-native stickleback and the tapeworm in
the Upper and Middle Deschutes Basin began in the late 1990s. To determine
environmental factors that correlate with higher infection levels, fish and water quality
data were collected at 77 sites during the summer of 2003 using a stratified random
sampling design. The sites at which stickleback were infected with the parasite were
concentrated both in the Crane Prairie and Wickiup reservoirs area. Multiple
regression and logistic regression analyses showed mean size of stickleback, catch-perunit-effort, and water flow were significantly related to parasite prevalence (the
percentage of hosts that are infected with the parasite) and mean infection intensity
(mean number of parasite per fish). These occurrences were likely associated with
human-altered habitat. A differential equation model was developed to characterize
the parasite distribution among the host populations. This equation may serve to
quantify and compare the impact of the parasite in host populations among basins or
among different parasite species.
© Copyright by Wataru Koketsu
April 19, 2004
All Rights Reserved
Environmental Correlates of Parasitism in
Introduced Threespine Stickleback (Gasterosteus aculeatus)
in the Upper Deschutes River Basin, Oregon
By
Wataru Koketsu
A THESIS
Submitted to
Oregon State University
in partial fulfillment
of the requirements for the
degree of
Master of Science
Presented April 19, 2004
Commencement June 2004
Master of Science thesis of Wataru Koketsu presented on April 19, 2004.
APPROVED:
Redacted for Privacy
Major Professor, representin4'isheries Science
Redacted for Privacy
Head of the Department of Fisheri-and Wildlife
Redacted for Privacy
Dean oft
ate School
I understand that my thesis will become part of the permanent collection of Oregon
State University Libraries. My signature below authorizes release of my thesis to any
reader upon request.
Redacted for Privacy
Wataru Koketsu, Author
ACKNOWLEDGEMENTS
I wish to express sincere appreciation to W. Daniel Edge for his guidance and
assistance with the preparation of this manuscript. Without his unwavering help and
patience, I could not have completed this thesis. I would also like to thank Philippe A.
Rossignol who always encouraged and motivated me, Jerri L. Bartholomew who
provided me with plenty of concrete and practical input, and Ikuo Ninomiya who gave
me many solutions and wisdom regarding both my research and academic life. I
would like to thank Barbara Shields and William Liss for providing me with my study
design and the initial concept. I would like to thank Phil Larsen, David Peck and
Yonghai Li for their kindness and sharp methodology and analyses skills. I would like
to thank Jaya Lapham and Victoria Cronin for their great assist and encouragement
with my field work. In addition, I would like to thank Jay Bowerman for his
hospitality and cooperation throughout my entire field season. I would also like to
express deep appreciation to my family and relatives for their financial and mental
support, and I would like to thank all of my friends including Todd Miller, John Seigle,
Cory Overton, Troy Guy, Ted Hart, Luis Francisco, and Chichang Liu for their support.
Especially, I deeply appreciate Ichiro Misumi and Yusuke Koseki, both talented young
researchers, who provided overall support of my academic life. I would like to thank
Howard and Jeannine Horton, and Mary Concer who have been surrogate parents for
me here in the U.S. I sincerely appreciate the assistance of Soshichiro Nakagawa,
Robert E. Witters, Yasuaki Ninomiya, and Lori Emmons; my life in the U.S. could not
have begun without their initiative. I deeply appreciate Tsunehal Hibino for his 20
years of help and encouragement as my best friend. Whenever I faced difficulty, he
was the first person for me to talk to. Finally, I would like to announce that I fulfilled
my promise to Tsuya Hioki, my grandmother who went to heaven in May 2003, to
acquire a Masters degree in the United States of America.
TABLE OF CONTENTS
Page
GENERAL INTRODUCTION
Exotic Species
Stickleback Case Study
Stickleback
Tapeworm
Research Significance
4
6
INTRODUCTION
7
1
1
2
3
MATERIALS AND METHODS
Study Area
Fish Sampling and Measurement of Environmental Factors
Data Analyses
..10
10
13
..15
RESULTS
Fish and Parasite Distribution
Environmental Correlates of Parasitism
Distribution of Parasite in Host
Differential Equation Models
16
.
..16
24
... .29
31
DISCUSSION
33
REFERENCES
42
APPENDIX
49
LIST OF FIGURES
Figure
Page
Life cycle of the tapeworm, Schistocephalus solidus
5
Map of study area in the Upper Deschutes Basin, central Oregon. The
number in parenthesis indicates the elevation
11
Photos of study sites representing various habitat conditions in the
Upper Desehutes Basin, central Oregon, July - August 2003: a) Cultus
River, a tributary of Crane Prairie Reservoir; b) Crane Prairie Reservoir resort
area; c) connection between Crane Prairie reservoir and Wickiup Reservoir;
d) Sunriver residence area near golf course; e) Mainstem of Upper
Deschutes River, Little Lava Island area; f) Mirror Pond area in Bend.
Photos by Wataru Koketsu
. ..12
Plot layout used to collect fish samples and environmental data for study of
parasites in threespine stickleback in the Upper Deschutes Basin, central
Oregon, July August 2003
14
Study area indicating distribution of threespine stickleback and S. solidus
infections in the Upper Desehutes Basin, central Oregon, July - August
2003
Length distribution of (a) all stickleback (n 4,208), (b) infected stickleback
(n = 549), (c) stickleback at non-infected sites (n = 2,259) and (d) stickleback
at infected sites (n 1,949), Upper Deschutes Basin, central Oregon,
July - August 2003
. .20
Relationship between catch-per-unit-effort and mean fork length of fish
measured at 62 sites (a), and relationship between prevalence of infection
and mean intensity of S. solidus (b) measured at 27 sites, Upper Desehutes
Basin, central Oregon, July - August 2003 ..
22
Mean number of S. solidus per threespine stickleback (11 549) sorted by total
fork length of threespine stickleback, Upper Deschutes Basin, central Oregon,
July - August 2003
23
LIST OF FIGURES (continued)
Figure
Page
Relationship between mean parasite intensity of S. solidus in threespine
stickleback and environmental factors measured at 62 sites, Upper Deschutes
Basin, central Oregon, July - August 2003
25
Relationship between mean parasite intensity of S. solidus in threespine
stickleback and environmental factors measured at 62 sites, Upper Deschutes
Basin, central Oregon, July - August 2003
26
10. Distribution of S. solidus in three spine stickleback with normal scale (a) and
with log scale (b), Upper Deschutes Basin, central Oregon, July - August
2003
..30
LIST OF TABLES
Table
Summary of threespine stickleback, parasite and environmental parameters
collected at 62 sites, Upper Deschutes Basin, central Oregon, July - August
2003
Page
18
Ordinary least squares multiple regression statistics for independent variables
predicting mean parasite intensity in threespine stickleback, Upper Deschutes
Basin, central Oregon, July - August 2003
.26
Logistic regression statistics for independent variables predicting parasite
prevalence in threespine stickleback, Upper Deschutes Basin, central Oregon,
July - August 2003
28
Environmental Correlates of Parasitism in
Introduced Threespine Stickleback (Gasterosteus aculeatus)
in the Upper Deschutes River Basin, Oregon
GENERAL INTRODUCTION
Exotic Species
The infestation of exotic species because of human influences has been massive
(Li etal. 1999). According to the U.S. Congress (1993), within the last [00 years, over
4,500 exotic species have become established in the continental U.S. alone, and the
worldwide explosion of fish diseases has been unprecedented during this period.
The U.S. may have the largest number of fish introductions of any country in
the world. Nearly 200 native species and at least 70 fishes from other continents have
been introduced and become established in new ecosystems (Dextrase and Coscarelli
1999). At the same time, aquatic ecosystems in the world have been and are being
altered at an alarming speed (Dudgeon 1992). These changes are caused by various
interactive factors, but most ecosystems have experienced habitat alteration, overharvesting, and introductions of exotic species. Exotic species in particular may
significantly affect native species through competition, predation, hybridization, and
the introduction of new parasites and diseases (Harvey and Matthews 1999).
Unfortunately, ecologists and natural resource managers cannot predict the outcome of
the addition of exotic species to aquatic ecosystems (Lodge 1993).
Since European colonization of North America, most nonindigenous
introductions have been caused by human activities. These introductions include not
only species that arrived from outside of North America, but also species native to
North America introduced to waters outside their historical ranges. Coho salmon
2
(Oncorhynchus kisutch) is an example of the latter. Native of the Pacific Coast from
northern California to Alaska, this species was introduced into the Great Lakes as early
as the 1930s (Benson and Boydstun 1999). Moyle and Sato (1991 from Harvey and
Matthews 1999) noted that the establishment of exotic species often is associated with
past or ongoing habitat alterations. They also suggest the linear, interconnected nature
of streams, the mobility of many aquatic species, and the possibility of accidental or
illegal introductions make likely the infestation of exotic species even in the most
closely managed stream preserves (Moyle and Sato 1991 from Harvey and Matthews
1999, Moyle and Light I 996a, b).
By the time biologists become concerned about the presence of an alien species,
it is often well established in its new habitat, and its source and natural history are
either unknown or poorly understood (Li et al. 1999). The importance of studying
exotic organisms is in understanding their possible effects on native organisms and the
surrounding physical environment. In response, a large effort has been undertaken to
document the history and monitor the distribution of aquatic introductions in North
America (Benson and Boydstun 1999). Li et al. (1999: 431) point out that "the greatest
need is for a management framework to assess the following issues: (1) the potential
impact of the alien species upon the receiving community, (2) the ecological
interactions for which understanding is most critical, and (3) strategies that guide
management policy to minimize potential deleterious effects of ecological change."
Stickleback Case Study
In the Upper Deschutes River Basin, Oregon, the introduction of an exotic host
and parasitic disease has occurred and may be still proceeding today. The threespine
stickleback (Gasterosteus aculeatus) is believed to have been introduced from west of
the Cascade Range as bait for recreational fishing or as released pets within last two
decades, and has since spread to the Upper Deschutes River Basin. In addition, the
3
parasitic tapeworm, Schistocephalus solidus, has been observed in the body cavity of
stickleback at multiple sites in the Deschutes Basin in Oregon. This parasite requires
both copepods and fish, as intermediate hosts, and birds as its final host to complete its
life cycle (Hopkins and Smyth 1951, Arme and Owen 1967). The introduction of
stickleback into the Upper Deschutes River Basin has resulted in a rapid increase in the
abundance of both the stickleback and the tapeworm since middle 1990s.
In the case of parasites that require multiple intermediate hosts, the alteration of
community structure directly affects the broader ecosystems via food webs because the
amount of primary production, phyto/zooplankton community or mortality, and
population dynamics of host predators are all linked by the parasite (Anderson and May
1982, Kennedy et al. 1986, Kennedy and Fitch 1990, Huxham et al. 1996, Marcogliese
2002). The colonization of stickleback may affect the habitat or resource competition
with other species (e.g., juvenile salmonids, sculpins). Increases of parasitized
stickleback population may also affect the survival of fish-eating birds or other wildlife
(Hopkins and Smyth 1951, Arme and Owen 1967). These alterations of community
structure, triggered by an exotic host, may induce parasite outbreaks in host
populations if optimal environmental conditions occur.
Stickleback
The worldwide distribution of the threespine stickleback is in boreal and
temperate regions of the northern hemisphere where it inhabits coastal marine waters,
brackish water, and a wide array of freshwater habitats (Bell and Foster 1994). In the
Pacific Basin, their habitat ranges from Baja California, Mexico, northward along the
coast of North America, across the Bering Strait and southwest along the coast of
mainland Asia and Japan to the southwest coast of Korea (Wootton 1984a). Unlike
central Europe, populations in Asia and North America do not appear to penetrate
significantly into interior fresh waters.
4
The normal body size of the stickleback is about 5 cm from the tip of the snout
to the end of the vertebral column (Hubbs and Lagler 1970 from Bell and Foster 1994),
but length ranges up to 11 cm (Bell and Foster 1994). In the Upper Deschutes River
Basin in Oregon, the maximum size was approximately 7 cm and 4 g. Stickleback
have been observed in various lentic habitats over a range of sizes. For example, Bell
and Baumgartner (1984) reported a population from a 260-m2 spring pooi, and at the
other extreme, Hubbs and Lagler (1970 from Bell and Foster 1994) reported
stickleback from the 1,968-km2 Lake Ontario, North America. Similarly, stickleback
can use various lacustrine habitats and resources (Bell and Foster 1994).
When male sticklebacks become reproductive, their eyes and body typically
change to a blue tinge, and the ventral surface of the head and trunk becomes red
(Wootton 1 984b, Reimchen 1989). The color change of reproductive females is less
pronounced, but it is biologically significant (Rowland et al. 1991), and reproductive
females are distinguished by the distension of the pale abdomen containing a massive
brood of eggs (Bell and Foster 1994). The threespine stickleback is also well known
for a wide array of conspicuous, highly ritualized behaviors. Studies of stickleback
aggression, territoriality, courtship, and male parental behavior have contributed to our
understanding of basic is sues in animal behavior (Rowland et al. 1991).
Tapeworm
The life cycle of the S. solidus tapeworm was unknown until 1919, when
Nybelin experimentally infected a copepod (Cyclops spp.) with coracidia (Hopkins and
Smyth 1951). Hopkins and Smyth (1951) and Clarke (1954) summarized these
historical findings of multiple hosts and revealed the lifecycle of S. solidus in more
detail. A free-swimming larva, a coracidium, hatches out after development and is
eaten by a copepod. Development up to the procercoid stage occurs in the body cavity
of the crustacean, and when the crustacean is swallowed by a stickleback, growth and
5
development of procercoid continue in the body cavity of the fish to the plerocercoid
stage. Two species of sticklebacks, the threespine and the ninespine (Pungitius
pungitius), are the usual hosts at this stage. When the stickleback is eaten by a bird, the
worm sexually matures in the avian gut (adult stage) and produces eggs. An estimated
20,000 eggs could be expected from average-sized worms. The eggs pass out into the
water with the feces (Cooper 1918 from Clarke 1954, Hopkins and Smyth 1951, LoBue
and Bell 1993) (Fig. 1). Schistocephalus solidus appears to occur normally in species
Fish-eating bird
(adult stage)
Paratenic host
Eggs
(coracidium stage)
Threespine stickleback
(plerocercoid stage)
Copepod
(procercoid stage)
Figure 1. Life cycle of the tapeworm, Schistocephalus solidus.
6
of the stickleback family, and its occurrence in other secondary hosts is probably
accidental and rarely happens (Hopkins and S myth 1951). Five species of Cyclops and
40 species of birds have been reported as potential first and final host respectively
(Hopkins and Smyth 1951, Clarke 1954, Anne and Owen 1967). Infection of paratenic
host, which is an accidental host and rarely occurs, may include larger fish or mammals
which forage on stickleback.
Research Significance
In the Deschutes Basin, Oregon, stickleback have not been studied and are not
being managed because they are a nongarne species. Thus, little research has been
conducted dealing with both the stickleback and tapeworm from a viewpoint of
ecological impacts. Specifically, the distribution of parasitized stickleback is largely
unknown. One goal of this study was to determine the environmental conditions where
stickleback and tapeworms occur.
I started this research by gathering basic information about stickleback and
tapeworm occurrences and their associated habitat characteristics, such as water
quality, in the Upper Deschutes River system. My research question is whether there
are correlations between parasitism and environmental parameters. I collected fish and
environmental data at 77 sites along 90 km of streams, tributaries and lakes in the
summer of 2003. The goals of this research are to (1) determine the distribution of
stickleback and its parasite, (2) predict the sites that likely contain parasites, and (3)
seek an alternative indicator to evaluate the degree of parasite infection.
7
INTRODUCTION
Emergent parasitic pathogens, caused by the introduction of exotic species,
have triggered new and complicated ecological interactions in many ecosystems
(Sakanari and Moser 1990, Marcogliese and Cone 1997). Introduced hosts or parasites
can establish new associations in which the host-parasite interactions may lead to
increased host resistance and increased parasite virulence (Anderson and May 1982).
Parasites are known to have the capacity to regulate host populations, and may be
important determinants of community structure because they are typically considered
as top predators within food webs, although their host (and the parasites) may fall prey
to predators (Dubois et al. 1996, Marcogliese and Cone 1997). Introduction of exotic
hosts often cause changes in populations of native species, and the parasites of exotic
species may colonize the new region if they are capable. Transmission into another
species of hosts is also possible. Alterations of host's habitat or feeding behavior by a
parasite normally enhance further opportunity for transmission (Apanius and Schad
1994). For example, mate selection, reproductive success and host survival may each
be affected by parasitism (LoBue and Bell 1993, Reimchen and Nosil 2001, Hems and
Baker 2003). Especially in the case of parasites that require multiple intermediate
hosts, the alteration of host's behavior or population structure affects the broader
ecosystem via food webs (i.e., the amount of primary production, phyto/zooplankton
community, or mammal and bird survival and density) (Anderson and May 1982,
Kennedy et al. 1986, Kennedy and Fitch 1990, Huxham et al. 1996, Marcogliese 2002).
In addition to endogenous factors, exogenous factors such as environmental
conditions may induce parasitism and alter community structure because they play
important roles in susceptibility of hosts and for habitat selection of both host and
parasite (Whittier and Hughes 1998, Sandell et al. 2001, Malcogliese 2002). Water
pollution, as a result of pesticides, metal cations and paper mill effluents, may change
the population structure of zooplankton and effect humoral and cellular immune
8
functions with the consequent impairment of fish health and diseases resistance (Maule
et al. 1989, Kuris et al. 1991, Marcogliese et al. 1992, Dunier 1996). In addition, some
environmental factors, like conductivity or pH, may be associated with both parasite
and host abundance, or prevalence of parasite infection (Marcogliese 1995,
Marcogliese and Cone 1996, Sandell et al. 2001). Some researchers consider parasite
communities to be variable and those local factors, chance of colonization and
extinction events promote the distinctiveness of parasite communities (Kennedy et al.
1989; Kennedy and Fitch 1990; Dubois et al. 1996; Marcogliese etal. 1992;
Marcogliese 2001, 2002). Human mediated disturbance on local and landscape scales
have also been implicated for rapid increases in parasites (Barker et al. 1996,
Marcogliese 2001). Introduction of parasites can substantially alter basic food web
properties, including connectance, chain length and proportions of top and basal
species, and can allow the testing of specific hypotheses related to food-web dynamics.
Fish-parasite dynamics may also affect copepod communities (Marcogliese and Esch
1989, Mareogliese and Cone 1997).
The threespine stickleback, Gasterosteus aculeatus, was believed to have been
introduced to the Upper Deschutes River Basin from west of the Cascade Range as bait
for recreational fishing or as released pets in the 1 980s and has since spread to the
basin (Jay Bowerman, Sunriver Nature Center, personal communication). This species
is widely distributed in coastal ranges in North America, and are tolerant of a wide
range of temperatures but prefer cool temperatures (Bell and Foster 1994). The
Pseudophyllidean tapeworm, Schistocephalus solidus, is a parasite that requires both
copepods and fish, as intermediate hosts, and birds as its final host to complete its life
cycle (Hopkins and Smyth 1951, Arme and Owen 1967). Although the tapeworm
naturally occurs in rivers or lakes, the infection intensity for fish and birds is normally
low under equilibrium conditions (Clarke 1954). Prior to the introduction of the
threespine stickleback, the Upper Deschutes Basin might not have contained a suitable
intermediate host for the tapeworm, whereas the cyst of the tapeworm had already
9
been carried into the basin by birds. However, the introduction of stickleback into the
Upper Deschutes River Basin has resulted in a rapid increase in the abundance of both
the stickleback and the tapeworm since the middle 1 990s.
This study was designed to examine patterns of occurrence of S. solidus of
stickleback in freshwater habitats of the Upper Deschutes River and adjacent systems.
I sought to determine the distribution of stickleback and parasites throughout the region
and to establish if there were relationships between the prevalence and intensity of
infection of stickleback and environmental factors. Additionally, I attempted to
evaluate the impact of parasite burden on fish populations by building differential
equation models. During three weeks beginning the end of July 2003, I collected
information on the abundance of stickleback, tapeworm and on water quality variables
at 77 sites using a stratified random sampling program based on a modified
Environmental Monitoring Assessment Program (Peck et al. 2003).
10
MATERIALS AND METHODS
Study Area
The study area is located in central Oregon in the Upper and Middle Deschutes
Basin. Seventy-seven potential sampling sites were distributed from Little Lava Lake
(elevation
1,444 m) to Cline Falls (elevation
Deschutes near Redmond (elevation
865 m) located on the Middle
913 m), Oregon (Fig. 2). These sites were
selected based on land use, road access, and river conditions with enough gradients of
targeted environmental factors at sites which have various habitat characteristics (Fig.
3). I collected samples from 77 of these possible sites over 3 weeks starting 30 July
2003 when there was no snowmelt and little precipitation. All sampling sites were
selected using a stratified random sampling design based on the U.S. Environmental
Protection Agency's Environmental Monitoring Assessment Program (EMAP) (Peck et
al. 2003) and sampling order was determined by block-randomized sampling. The
limitations of the stratified random sample were that sites must be physically
accessible, on public land, and 20 minutes walk from the road. The EMAP is a
synoptic survey designed to answer questions about the numbers, spatial extent, and
ecological condition of surface water resources at a regional scale (Larsen and
Christine 1993). The sampled plots are representative of the range of conditions in all
but the inaccessible sites in the Upper Deschutes River because of the probabilitybased design used to select them (Larsen and Christine 1993, Whittier and Hughes
1998, Peck et al. 2003).
Oregon
Cline Falls
(865 m)
.
Redmond
(913 m)
Turn al 0
(970 m)
Tumalo Creek
Bend
(1,106 m)
Little Lava
Lake
(1,444 m)
Sunriver
(1,271 m)
Desch utes
River
Cultus Lake
(1,423 m)
Crane Prairie
Reservoir
(1,355 m)
Paulina Creek
. La Pine
Wickiup 1
Reservoir
(1,322 m)
(1,290 m)
Little
Deschutes
River
Paulina Lake
(1,930 m)
0
10km
Figure 2. Map of study area in the Upper Deschutes Basin, central
Oregon. The number in parenthesis indicates the elevation.
12
(d)
Figure 3. Photos of study sites representing various habitat conditions in the
Upper Deschutes Basin, central Oregon, July August 2003: a)
Cultus River, a tributary of Crane Prairie Reservoir; b) Crane Prairie
Reservoir resort area; c) connection between Crane Prairie reservoir
and Wickiup Reservoir; d) Sunriver residence area near golf course;
e) mainstern of Upper Deschutes River, Little Lava Island area; f)
Mirror Pond area in Bend. Photos by Wataru Koketsu.
13
Fish Sampling and Measurement of Environmental Factors
Fish were collected and environmental parameters were measured at each
sample site. At each site, a 15 m X 1 m plot was defined along the littoral and riparian
line. Fish were collected by dip nets to obtain a range of fish sizes using a fishing
effort of 30 minutes per site within the 15 m X 1 m plot. The field sampling objective
was to collect a representative sample of the fish assemblage at each plot. All
stickleback were packed in ice immediately after capture. Length and weight were
measured, and the body cavity of each fish was opened and plerocercoids were
removed, counted, and weighed. Plerocercoids were identified according to Hopkins
and Smyth (1951) and Clarke (1954). At each station, three replicates were taken for
all environmental data by dividing the plot into three 5 m X 1 m subplots (Fig. 4).
Except for fish collections, water flow and maximum water temperature, all
environmental parameters were measured at the center of each subplot. Maximum
water temperature in a day was measured by high-low thennal recorder. I measured
minimum temperature between 05:30 h and 08:30 h with a YSI 85 dissolved
oxygen/conductivity meter. Water flow was measured three times at the center of the
plot. I timed a porous plastic ball (diameter =4 cm) flowing 10 m and calculated the
flow velocity. For plots with very low flows, this distance was shortened to 5 m.
Dissolved oxygen, conductivity and water temperature were measured with a YSI 85
dissolved oxygen/conductivity meter. Water level was measured with a wooden ruler;
depths ?120 cm were recorded as 120 cm. Cover of submerged macrophytes and
substrate, i.e., mud and sand substrate ratio, were visually estimated according to Peck
et al. (2003).
14
Dissolved oxygen
Conductivity
Minimum temperature
Water depth
Vegetation
Substrate
/
/
Fish collection
Water flow
Maximum temperature
/
water
stream bank
Figure 4. Plot layout used to collect fish samples and environmental data for
study of parasites in threespine stickleback in the Upper Deschutes
Basin, central Oregon, July - August 2003.
15
Data Analyses
Because 2.2 cm sticklebacks were the smallest fish infected with plerocercoids,
I only used fish ?2.2 cm for my analysis. Prevalence and mean intensity were
calculated for each site. I defined "prevalence" as the percentage of hosts with parasite
infection (%) and "mean intensity" as the mean number of parasites per host.
Significant correlations of environmental variables with the prevalence and mean
intensity of infection of stickleback were identified by regression analysis. Ordinary
least squares (OLS) multiple regression was used to determine if any of the
environmental variables could account for variation in mean intensity. All multiple
regression models were analyzed for multi-collinearlity to ensure that the assumptions
of the OLS technique were met (Ramsey and Schafer 1997). For stepwise variable
selection, a significance level of 0.05 was used as the criterion for allowing a variable
to enter the model, and 0.05 was used as the criterion for retaining a variable in the
model. Variables were tested for normality and log transformed when required.
Significance was defined as P <0.01. To determine correlates of parasite prevalence,
logistic regression was used because the response variable is the probability of parasite
infection among host populations. I used chi-square for the rich model to test for lack-
of-fitness. Three observations were eliminated because they were outliers in residual
plots. A full model was constructed and model selection was conducted by drop in
deviance test (Ramsey and Schafer 1997). Statistical analyses were conducted using SPLUS (Statsci 2000) and SAS version 8.2 (SAS 2003).
In the past, many parameters have been created to evaluate parasite influence on
individual host or host populations (e.g., prevalence, mean intensity, Parasite Index
[Pennycuick 1971], and truncated negative binomial analysis [Brass 1958, Crofton
1971, Lanciani and Boyett 1980]). To evaluate parasite distribution in host population
among basins, differential equations were developed based on the host frequency parasite per host relationship using a log transform of the y-axis.
16
RESULTS
Fish and Parasite Distribution
Between 30 July and 17 August 2003, I collected fish and environmental data at
77 sites. Stickleback were observed and captured at 62 sites, resulting in a total capture
of 4,208 fish. A total at 549 fish from 27 sites were infected with S. solidus. My
research objectives were 1) to determine the distribution of both stickleback and
tapeworm throughout the study area, and 2) to characterize the variation of
environmental factors between sites.
I collected stickleback throughout most of the study area (Fig. 5). However,
stickleback habitat was patchy and locally distributed, resulting in 15 sites where
stickleback were absent. The 27 sites where infected fish were collected were mostly
concentrated upstream of Crane Prairie and Wickiup reservoirs, located near the origin
of Deschutes River (Fig. 5). Sites with infected fish were generally characterized as
lower elevations with pool habitats, submerged macrophytes and muddy substrates.
Most of the sites in mainstream of the Deschutes River did not have parasites except
for the Bend area. Other infected sites in mainstream of the Deschutes River were
detected sporadically. No fish with parasites were collected at either Paulina Lake or
Paulina Creek.
Prevalence and mean intensity varied throughout the study area (Table 1). I
collected a total of 1,463 fish at the 27 sites with infected fish; 549 of the fish had a
total of 1,464 worms. Among infected fish (n = 549), mean number of parasite per host
was 2.667 worms/fish (SD
fish (n
2.197). Among all fish captured at the sites with infected
1,463), mean number of parasite per host was 1.001 worms/fish (SD = 1.865).
Mean intensity per site was 0.620 worms/fish (SD
site was 22.4 % (SD = 37.6).
1.224) and mean prevalence per
17
Upper Deschutes
River
x stickleback with parasite
I
(27)
Redmond
stickleback without parasite (35)
0
stickleback absent
(15)
Tumalo Creek
Bend
Sunriver
Crane Prairie
Reservoir
Paulina
Lake
La Pine
Wickiup
Reservoir
10km
0
I
I
I
Figure 5. Study area indicating distribution of threespine stickleback and
S. solidus infections in the Upper Deschutes Basin, central
Oregon, July - August 2003.
18
Table 1. Summary of threespine stickleback, parasite and environmental
parameters collected at 62 sites, Upper Deschutes Basin, central
Oregon, July - August 2003.
Variable
Mean
Range
SD
CVa
Total fish captured at each site
67.9
1 -483
69.9
103.0
Number of fish 2.2 cm
48.7
39.5
81.1
Number of fish infected
Prevalence (%)
Mean intensity (mean # of worms/fish)
Mean fish size (fork length, cm)
Catch-per-unit-effort (fish/br)
Dissolved Oxygen (mg/I)
Conductivity (ps/cm)
Water flow (mis)
Water depth (cm)
Minimum temperature (°C)
Maximum temperature (°C)
Submerged macrophytes cover ratio (%) b
Substrate cover ratio (%) b
8.9
17.2
194.6
0.6
l -237
0- 72
0-100
0.0-5.7
3.26
1.90-5.00
0.82
25.3
173.5
2-966
190.9
110.0
7.063
2.51 - 10.73
1.477
20.9
82.4
28.2-530.0
117.6
142.7
0.222
0.000 - 0.859
0.203
91.7
42.9
1.8- 120.0
28.5
66.4
a
b
Coefficient of variation (SD/mean X 100).
Categorized according to Peck et al, (2003).
22.4
37.6
168.1
1.2
197.4
16.4
5.2- 24.3
4.0
24.5
20.0
10.0-35.6
4.8
23.8
56.4
0.0-87.5
0.0-87.5
32.9
58.3
28.8
39.8
72.4
19
The reservoir area encompasses various watershed characteristics (i.e., two
large reservoirs with large daily temperature fluctuations, many tributaries originating
from cold springs, lakes, dams, etc., resulting in large variations in environmental data),
whereas the Deschutes River mainstem had less variation because of its relatively
constant water environment. The highest and second highest dissolved oxygen levels
were recorded at Quinn River and Cultus River, respectively; both are tributaries of
Crane Prairie Reservoir. Conductivity was high at Paulina Lake, South Twin Lake and
Sunriver area. Water temperature was high in the reservoir and Sunriver areas.
Compared with the reservoir areas, the mainstream of the Deschutes River had
relatively higher dissolved oxygen levels, lower conductivity levels, lower water
temperature and higher water flows. Most of these parameters were stable and had less
variation than tributaries, reservoirs and lakes.
During dissections, I found that sexually mature female and male stickleback
and gravid females tended not to be infected with S. solidus, even in areas with high
infection prevalence.
The size structure of all stickleback collected suggested two age classes (Fig.
6a), with a high frequency of young-of-the-year stickleback. In contrast, most of the
infected fish were more than one year old (Fig. 6b). The length distribution at sites
without infected fish had a uni-model distribution (Fig. 6c), whereas the sites with
infected fish had a bi-model length distribution (Fig. 6d).
20
10
(a)
All fish (n = 4,208)
8
0
.0
1.5
2.0
2.5
3.0
3.5
4.0
4.5
5.0
5.5
6.0
6.5
7.0
Total fork length (cm)
10
(b)
All infected fish (n = 549)
U-
.jhØ5,0 !"&
0
;.
1.0
Total fork length (cm)
10
(c)
Fish at non-infected sites (n = 2,259)
IbihIllIhIl JLn
0
1.5
1.0
2.0
2.5
3.0
3.5
4.0
4.5
5.0
5.5
6.0
6.5
7.0
Total fork length (cm)
10
(d)
Fish at infected sites (n = 1,949)
0
1.0
1.5
2.0
2.5
3.0
3.5
4.0
4.5
5.0
5.5
6.0
6.5
7.0
Total fork length (cm)
Figure 6. Length distribution of(a) all stickleback (n 4,208), (b) infected
stickleback (n = 549), (c) stickleback at non-infected sites (n = 2,259)
and (d) stickleback at infected sites (n = 1,949), Upper Deschutes Basin,
central Oregon, July - August 2003.
21
The reservoir areas had relatively large mean fork length and CPUE, and
Deschutes River mainstem had relatively small mean fork length and CPUE except for
the Bend area. There was no significant linear relationship between mean fork length
and CPUE (partial r
0.270, P
0.034). The sites with larger mean fork length had
lower CPUE, whereas the sites with smaller mean fork length had a wide range of
CPUE (Fig. 7a). The sites with higher prevalence tended to have a higher level of
mean intensity. Prevalence and mean intensity were correlated (partial r
0.901, P <
0.001) and were highest at the sites in Crane Prairie Reservoir (Fig. 7b).
Mean number of parasite per host was plotted against fish fork length to
characterize the relationship between mean parasite intensity and host size, which
resulted in a curvelinear or exponential curve relationship (Fig. 8). Intensity appeared
to be most pronounced around 5.0-cm size fish, and either reached equilibrium or
gradually declined with larger fork length.
22
900 -
1000
S
(a)
800 -
S
700- n = 62
600- r20.073
500- P=0.034
D 400l:L
o 300-
S
S
S
-
200 100 0
0.0
1.0
.
S
5
2.0
0
4.0
3.0
6.0
5.0
Arage fork length (cm)
.
100
S
S
90
80
S
.
S
70
60
50
n= 27
40
30
20
0.812
P< 0.001
10
0
0.0
1.0
2.0
3.0
4.0
5.0
6.0
Mean intensity (worms/fish)
Figure 7.
Relationship between catch-per-unit-effort and mean fork
length of fish measured at 62 sites (a), and relationship
between prevalence of infection and mean intensity of S.
solidus (b) measured at 27 sites, Upper Deschutes Basin,
central Oregon, July - August 2003.
23
5.0
4.5
I.
4.0
-C
(1)
I
3.5
3.0
I.
S
2.5
I I
2.0
.
C
S
S
S
I
S
1.5
1.0 -
S 5.5.5. .5
I
0.5 0.0
2.0
2.5
3.0
3.5
4.0
4.5
5.0
5.5
6.0
6.5
7.0
Total fork length (cm)
Figure 8. Mean number of S. solidus per threespine stickleback (n 549)
sorted by total fork length of threespine stickleback, Upper
Deschutes Basin, central Oregon, July August 2003.
24
Environmental Correlates of Parasitism
My second objective was to determine environmental factors that are correlated
with parasitism. Firstly, I checked correlations between mean parasite intensity and
each single variable. There were no significant linear relationships between mean
parasite intensity and any single environmental parameter (partial r < 0.69, F> 0.001).
However, there may be an optimal range or threshold of parasitism for dissolved
oxygen level and water temperature (Fig. 9a, 9b). I used OLS multiple regression
analysis to determine variables that influenced mean intensity and used both-ward
stepwise model selection to build my models. Before analysis, water depth and
minimum water temperature were omitted from the full model because of interactions,
and mud/sand substrate cover ratio was omitted because it was highly skewed.
Mean fork length, CPUE, conductivity and water flow were significantly
correlated with mean parasite intensity (Table 2). Mean parasite intensity was
positively related to mean fish size and CPUE, and negatively correlated with
conductivity and water flow. Mean parasite intensity was not related to dissolved
oxygen level (partial r = 0.002, P
minimum (partial r 0.299, P
0.9896), water depth (partial r = 0.401, P = 0.0012),
0.0181) or maximum daily temperature (partial r
0.334, P = 0.008), submerged macrophytes cover ratio (partial r = 0.389, P = 0.0018)
or mud/sand substrate cover ratio (partial r = 0.229, P
0.074). The OLS multiple
regression model that best describes mean intensity of tapeworms in stickleback was
log e mean intensity -10.96 + 2.72 mean fork length (cm) + 0.520 log e CPUE
(fish/hr) - 1.54 loge conductivity (ts/cm) - 0.55 log e water flow (mis) (r2
0.0001).
0.6537, P <
25
6.0
6.0
5.0
r=0.477
4.0
P< 0.001
5.0
..
3.0
S
.
C
U)
I
.
0.020
P= 0.273
C
..
3.0
CU
(U
2.0
2.0
I.
I
1.0
0.0
(U
1.0
2.0
3.0
4.0
Fvan fork length (Cm)
5.0
6.0
6.0
6.0
5.0
5.0
500
600
0.061
P=0.053
4.0
(0
C
41)
(U
3.0
C
I
I
C
(U
41)
200
300
400
Conductivity (ps/cm)
100
0
C
'
S
0.0
00
4
I
1.0
I
(U
2.0
I
I
.
1.0
I
1.0
0.0
I
0.0
0
200
400
600
800
1000
0.0
0.2
0.4
CF'(JE (fish/hour)
6.0
6.0
5,0
,2
4.0
P= 0.990
0.000
0.8
1.0
.
2
5.0
(U
41)
(U
3.0
I
I I
3.0
.
C
(U
(U
I
IS
2.0
I
I.
1.0
0.161
P= 0.001
.
(U
C
2.0
0.6
Water flow (rn's)
1.0
0.0
00
0. 0I0 5-4
0.0
2.0
4.0
6.0
8.0
Dissolved oxygen (n/l)
10.0
12.0
0
20
40
111-4
60
80
100
Water depth (cm)
120
140
Figure 9a. Relationship between mean parasite intensity of S. solidus in threespine
stickleback and environmental factors measured at 62 sites, Upper
Deschutes Basin, central Oregon, July - August 2003.
26
6.0
5.0
-
6.0
.
0.090
P=0.018
.
r2 = 0.152
5.0
P= 0.002
.
C
a,
3.0
1
S
C
Ce
a,
S
2.0
S
1.0
.
I
5
10
S
1.0
I
.
0.0
.
2.0
.
15
:
0.0..
20
30
25
35
40
0.0
0.2
0.4
Mninumw ater teirçerature (°c)
6.0
5.0
-
0.8
6.0
= 0.052
P=0.008
S
P=0.074
5.0
p4.0
S
.
Ce
C
.
3.0
S
S
C
.
Ce
2.0
2.0
.
S
1.0
2
.
I
1.0
¶
0.0
0
5
10
. .....
15
25
30
35
40
Maxinijmw ater terrperature (cc)
..
!
0.0
20
1.0
Vegetation (%)
.
r=0.112
0.6
0.0
0.2
0.4
0.6
0.8
1.0
Fvtid/sand substrate (%)
Figure 9b. Relationship between mean parasite intensity of S. solidus in threespine
stickleback and environmental factors measured at 62 sites, Upper
Deschutes Basin, central Oregon, July - August 2003.
Table 2. Ordinary least squares multiple regression statistics for independent
variables predicting mean parasite intensity in threespine stickleback,
Upper Desehutes Basin, central Oregon, July - August 2003.
Variable
Mean fork length (cm)
Catch-per-unit-effort (fishlhr) b
Conductivity Qis/cm) b
Water flow (mis) b
Coefficient
Sum of Squares a
2.718
307.409
38.203
0.0000
0.520
-1.543
7.842
0.0011
-0.554
83.680
0.0000
P-value
a
0.0851
aSum of squares and probability for each variable when entered into the model after all other
variables.
bNatural log (loge) transformed.
27
Logistic regression analysis indicated that mean fork length, CPUE, dissolved
oxygen level, conductivity, water flow, maximum daily water temperature, and
mud/sand substrate cover ratio were significantly correlated with prevalence (Table 3).
The odds that a stickleback will be infected by a parasite decrease with mean fork
length and increase with CPUE, dissolved oxygen level and mud/sand substrate cover
ratio (Table 3). The odds of infection decrease by an estimated 99.9 % per centimeter
for the mean fork length, increase by an estimated 2.0 % per number of fish/h for the
CPIJE, 5.93 x io % per mgIL of dissolved oxygen, 1.63 X l0 % per rn/s for water
flow, 101.4 % per degree for maximum daily water temperature and 5.3 )< l0' % per
cover ratio of mud/sand substrate. The logistic regression model that best describes
prevalence of tapeworms in stickleback was logit (ir) = - 29.640 - 11.63 mean fork
length (cm) + 0.026 CPUE (number of fish / h) + 3.94 dissolved oxygen (mg / L) +
0.024 Conductivity (ps/cm) + 9.759 water flow (mi's) + 0.038 Water depth (cm) +
0.6701 highest water temperature in a day (°C) + 29.01 mud/sand substrate cover ratio
(%) + square terms (P < 0.00 1).
Although the results of both regression analyses were slightly different, two
endogenous factors, mean fork length and CPUE, and the one exogenous factor, water
flow, were common parameters for both analyses. Endogenous factors of fish size
(age) and abundance, rather than exogenous factors, appear to better explain mean
parasite intensity and prevalence of infection.
28
Table 3. Logistic regression statistics for independent variables predicting
parasite prevalence in threespine stickleback, Upper Deschutes
Basin, central Oregon, July - August 2003.
Variable
Coefficient
z-statistic
Intercept
-29.640
-11.630
-2.76 1
-3.116
0.0038
0.026
6.502
0
Meanforklength(cm)
Catch-per-unit-effort (fish/br)
Dissolved Oxygen (mg/i)
Conductivity (.ts/cm)
Water flow (mIs)
Water depth (cm)
Maximum temperature (°C)
Substrate cover ratio (%) b
Squared mean fork length
Squared Catch-per-unit-effort
Squared dissolved oxygen
Squared conductivity
Squared water flow
Squared Maximum temperature
Squared substrate cover ratio
P-value a
3.941
7.63 5
0
0.024
2.424
0,0099
9.759
2.795
0.0056
0.038
3.338
0.0003
0.670
3.319
0.0004
29.008
1.148
0.0031
2.679
4.849
0
-0.00002
-5.586
0
-0.287
-6.659
0
-0.00007
-2.468
0.0007
-50.945
-7.155
0
-0.013
-2.834
0.0027
-23.348
-1.3 18
0.0025
d.f.=43
Residual Deviance = 60.9
ap
- value was calculated by drop in deviance test except for intercept. Values less than
are indicated as zero.
10
bCategorized and measured according to Peck etal. (2003).
29
Distribution of Parasite in Host
To clarifr the distribution of S. solidus in the threespine stickleback population,
the frequency of the host population (n = 549) was plotted against the number of
parasites that hosts contain (Fig. 1 Oa). The maximum number of worms per fish was
15 and the mean number of worms per fish was 1.001 (SD = 1.865). Most of the host
population was aggregated at the one worm infection level and frequency declined
substantially after one or two worms; few hosts contained 210 worms. I fitted
observed data to a negative binomial distribution curve; the observed relationship
closely approximated a negative binomial distribution (2' 2 = 7.975, P < 0.01).
To characterize the bar graph, I plotted the number of parasites per host on the
x-axis, and the number of host on the y-axis (Fig. lob). The y-axis was log scaled and
O for parasite load was omitted to focus only on fish with parasites. If as the number of
parasites per host increases, the mortality of the host also increases, this relationship
can be modeled with an exponential function:
Nae
(1)
Where
N: the number of host
n : the number of parasite per host
a : constant number
b : constant number
I found a significant relationship between number of hosts (log scale) and the
number of parasites per host (N= 225.16 e
0393ui,
[r2= 0.9326, P <0.01]). The slope
of the line (b = 0.393) represents the degree of utility that the parasite could make of
the host population or the degree of the host capacity for containing parasites.
30
250
(a)
Host
200
:n=549
Parasite: n = 1,464
150
100
50
0
IIIII1I.l____l
1
2
3
4
5
6
7
8
9 10 11 12 13 14 15 16
Number of parasite per host
1000
C)
(b)
Y= 225.16 e°39
C.)
C,)
.2
r2=O.9326
100
U)
0
9-
0
10
C)
E
2
1
2
3
4
5
6
7
8
9
10 11 12 13 14 15 16
Number of parasite per host
Figure 10. Distribution of S. solidus in threespine stickleback with normal
scale (a) and with log scale (b), Upper Deschutes Basin, central
Oregon, July - August 2003.
31
Differential Equation Models
An alternative model was developed to express the characteristics of parasite
distribution in a basin-wide host population and to evaluate the potential of the parasite
to induce host mortality. Based on the host frequency - parasite per host relationship
and its trend line (Fig. 1 Oa, b), differential equations were built using log transform of
the y-axis to obtain an alternative model. This model can be used for comparison of
infection level of host population in a large scale habitat compared to evaluations from
a small scale habitat such as mean parasite intensity or prevalence of infection in local
populations. I transformed equation (1) into a differential equation,
N ae -
dn
b
bN
then divided both sides by time dt,
dt
dt
and the per capita rate of change is:
1 dN
-b
N di' and solved for b.
dn
di'
32
Ndt/
(5)
dt
The term "parasite intensity" is defined as the number of worms per host. The
term -
in equation (5) indicates the per capita host frequency reduction, and
is the per capita parasite intensity increment. The "per capita" concept is often
used for population growth models in population ecology (Gotelli 2001). Therefore,
equation (5) shows that the ratio of the per capita host frequency reduction to the per
capita parasite intensity increment is constant. Because the ratio of numerator to
denominator is constant, if
dt
increases,
dN
Ndt
decreases at a regular rate and vice
versa. For the Deschutes Basin in August 2003, this ratio was 0.393 (N= 225.16 e 0.393
?
0.9326, thus, b
0.393). We might be able to compare b among multiple
reaches or basins to evaluate the risk of the parasite to the host.
Furthermore, if I multiply both sides by n, equation (6) is available.
ldN //ldn
---=nb
Ndt/ ndt
This equation represents the ratio of
words, when n is large, the ratio of
ldN
ldn
- Ndt
-- to -ndt
ldN
- Ndt
-
regulation of the parasites intensity on both
(6)
.
is in proportion to n. In other
ldn
ndt
to -- also becomes large, i.e. the
- -Ndt
and
---
ndt
becomes stronger.
33
DISCUSSION
Threespine stickleback are distributed throughout the Upper Deschutes River
system, but the sites with parasites are concentrated at high-elevation reservoirs sites
and infection level was correlated primarily with endogenous factors of the host. Both
the mean parasite intensity and prevalence of tapeworm infection were related to mean
fork length of stickleback, catch-per-unit-effort, and water flow indicating the parasite
may have a preferred host size, host density, and physical enviromnent. An alternative
model may be used to express the characteristic of parasite distribution in basin-wide
host population whereas the mean parasite intensity and prevalence of infection are
'used to evaluate the degree of infection among local populations. In its native habitat,
the threespine stickleback does not tolerate high-gradient streams, and rarely occurs in
fluvial streams more than a few hundred meters above sea level (Bell 1982). However,
stickleback have successfiully colonized the Upper Deschutes River Basin and
acclimated to the systems elevation, water flow, and water temperatures. This
unexpected acclimation may be a key event for infestation of the exotic host and its
parasite population in the system.
I predicted that low dissolved oxygen level, high conductivity level, low water
flow, high water temperature, and larger abundance of submerged macrophytes and
mud/sand substrate at sites would result in a higher parasite prevalence or mean
intensity. As water temperature increases, the activity and metabolism of fish increases
and fish have greater appetites and digestion ability (Guderley 1 994 Moyle and Light
1 996a, 1 996b), which may increase consumption of copepods and increase the speed of
intestine wall penetration by the procercoid (Clarke 1954, LoBue and Bell 1993).
Lower dissolved oxygen is stressful for fishes and weakens their immune system
(Maule et al. 1989), which may make fish more susceptible to parasitism. When water
flow decreases, parasite prevalence and intensity should increase because coracidia,
copepods, and stickleback prefer slow or standing water (Clark 1954), facilitating the
34
consumption of coracidia by copepods and of copepods by stickleback. My prediction
for water flow was supported by my analyses, but my other predictions of
environmental correlates were not. In my study, parasitism in the threespine
stickleback was more related to the endogenous factors of fish size and CPUE rather
than exogenous parameters.
Catch-per-unit-effort is an index of population density. As population density
increases, the per capita fish size decreases because of decreasing food and resource
availability. In my results, this appeared to occur at approximately half of the sites (i.e.,
the larger the fish length, the lower the CPUB [Fig. 7aJ). However, some sites had both
smaller fish length and lower CPUE; most of these sites were located in the mainstem
of Deschutes River. Larger fish can use a wider range of flow conditions whereas
smaller fish live in only slow or zero-flow habitat.
Because many factors can alter water quality, it is unlikely that generalizing the
interaction between water quality and parasitism is possible (Marcogliese 1992, Khan
et al. 1994, Lafferty and Kuris 1999). Likewise, I found only indirect relationships
between parasitism and environmental factors. Other studies have also attempted to
identify relationships between parasite infection in fish and environmental factors.
Sandell et al. (2001) tried to identify environmental correlates for whirling disease in
salmonids caused by a myxozoan parasite. Of four water quality measurements, only
conductivity was correlated with infection prevalence (Sandell et al. 2001). Vincent
(2002) demonstrated that as water volume increases, the intensity of microparasitic
infection of trout decreases. He hypothesized that as water volume increases the
parasite becomes diluted, decreasing the chance of "hitting" and attaching to the host
(Vincent 2002). This conclusion may be applicable in my study because both
copepods and stickleback prefer lower water flow areas as their habitat (Bell and Foster
1994, Marcogliese 2001). In such habitats, the abundance of both copepods and
procercoid may be greater, and stickleback will have greater opportunity to forage on
copepods, resulting in higher infectious by S. solidus. As Vincent (1998, 2002)
35
suggested, a comparison study between in-situ and in-vitro experiments might provide
more conclusive results.
Lafferty and Kuris (1999) suggest that altered water quality may improve
conditions for parasites if host density increases. Eutrophication and thermal effluent
often raise rates of parasitism because the associated increased productivity can
increase the abundance of intermediate hosts (Lafferty and Kuris 1999). This may be
the case in the reservoir areas. The Upper Deschutes River Basin is highly developed
and altered, containing numerous reservoirs, dams, and agricultural diversions, often
resulting in large fluctuations of daily water temperatures or algal blooms. These
combined effects of high temperatures or high nutrient concentrations increase pH and
decrease dissolved oxygen levels via metabolic activity of algae, and can create
stressful conditions for fish (Giannico and Heider 2001). The sites in Crane Prairie
Reservoir, Sunriver residence, and Bend areas where most parasitism occurred were
typical of conditions containing these human modifications, resulting in substantially
higher water temperatures. In fact, of 11 sites having ?20 °C minimum daily water
temperature, 10 contained parasites with relatively higher prevalence and mean
intensity (Fig 9b). Likewise, of 9 sites with ?25 °C maximum daily water temperature,
8 contained parasites with relatively higher prevalence and mean intensity (Fig 9b).
These sites were all in either Crane Prairie Reservoir or the Sunriver residence area.
The procercoid stage of S. solidus and copepods both prefer human-altered areas with
higher primary production and standing water (Hopkins and S myth 1951, Arme and
Owen 1967, Marcogliese et al. 1992). Although stickleback are able to colonize these
habitats, they prefer cooler temperatures, and thus may be stressed to a certain extent
by unsuitable water quality and climate, making them more susceptible to parasitism
(Bell and Foster 1994, Guderley 1994). These three biological conditions, preferred
procercoid and copepod habitat, and stressed stickleback may have influenced parasite
occurrence.
36
Based on the relative importance of biotic and abiotic factors, a series of six
predictions regarding fish invasions in California streams and estuaries were developed
by Moyle and Light (1996b). Three of their predictions may applicable to the
introduction of stickleback in the Upper Deschutes River Basin (Moyle and Light
1996b: 1667, 1668, 1669): "In streams, the most successful invaders will be those
adapted to the local hydrologic regime"; "In aquatic systems with high level of human
disturbance, a much wider range of species can invade than in systems with low levels
of human disturbance"; and "Successful invasions in aquatic systems are most likely to
occur when native assemblages of organisms have been temporarily disrupted or
depleted". Their study also suggests that the match between introduced species and the
hydrologic regime is the most important factor for the success of colonization, and they
conclude that biotic interactions seem to play a smaller role than abiotic factors except
during the early stages of introduction. However, this is only partially consistent with
my results. The local hydrologic regime in the Upper Descbutes River Basin has
strong seasonal patterns; low flows in the rainless summer and higher flows in winter
and spring in response to higher precipitation and snow melt. In the reservoirs, large
fluctuations of water level occur because of diversions for irrigation. These hydrologic
regimes do not match with stickleback's favored habitat (Bell 1982, Bell and
Baumgartner 1984, Bell and Foster 1994). Wild runs of native salmonids in the
Deschutes River, kokanee (Oncorhynchus. nerka) and chinook (0. tshawytscha)
salmon, steelhead (anadromous rainbow trout, 0. mykiss), and bull trout (Salvelinus
confluentus), had been eliminated or their populations decreased because of the barriers
of hydroelectric projects or agricultural diversions (Sollid et al. 2002). The most
important factors for stickleback introduction in the Upper Deschutes River Basin may
be its high capacity for physiological acclimation and low biota resistance, especially
from native and wild salmonids.
Theoretical considerations of the evolution of host-parasite associations include
three models proposed by Holmes (1983 from Sakanari and Moser 1990): the mutual
37
aggression model, the prudent parasite model, and the incipient mutualism model. In
addition, Sakanari and Moser (1990) suggested an alternative model as 1-sided
evolution based on increased host resistance. The type of ho st-parasite relationship
depends on the nature of the system's equilibrium. Because I have no evidence to
support or to refute whether emergent parasitism in the Upper Deschutes has reached
equilibrium or not, I am not able to conclude which type of host-parasite associations
applies to my study. However, stickleback have a three-year lifespan, were introduced
more than 20 years ago, and were distributed throughout the Upper Deschutes. Also,
infection of S. solidus may not directly make stickleback's physiological condition
lehal (Pennycuick 1971). My study system may be less likely to represent mutual
aggression or incipient mutualism models and more likely to represent the prudent
parasite or 1-sided evolution models. My results represent a cross-sectional study in a
single river system and they should not be extrapolated outside of the study area or
time. To generalize my results, longitudinal studies in multiple river systems are
needed. Monitoring fish migration (daily, monthly, yearly) to determine the time and
specific location of parasite infection would be necessary for more accurate prediction
of prevalence and mean intensity, and to expand a risk assessment to other fish and
wildlife.
I collected healthy post spawning stickleback in the heaviest infection sites.
During dissection, I noticed that post-spawning females and male stickleback and
gravid females tend to not be infected with S. solidus, even in areas with extremely
high prevalence. For example, the Quinn River Campground site in Crane Prairie
Reservoir is one of the heaviest infected sites with 71 out of 79 fish infected.
Uninfectecl fish in this site were four post-spawning sticklebacks, ?5 .5 cm fork length,
and four juvenile sticklebacks, all 2.3 cm. I suggest two hypothetical reasons for this
tendency: (1) natural mortality of parasite -- fish were infected once, but parasite died
before the fish were captured; and (2) dominance against parasite infection -- dominant
fish were not infected by parasites and were not consumed by predators. In their
38
experimental study, Milinski and Bakker (1990) demonstrated that because the ciliate
parasite Ichthyophthirius multfihiis infects stickleback and causes less coloration,
female stickleback use male coloration in mate choice and therefore avoid parasitized
males. If this result is applicable for S. solidus, uninfected males would tend to have
higher reproductive success. Additionally, parasite infection generally alters host
behavior, making them more susceptible to predation by the next host, possibly
enhancing parasite transmission (Milinski 1984, Apanius and Schad 1994). Thus,
parasitized fish are more likely eaten by predators before a physiological condition
reaches a lethal stage (Pennycuick 1971). Stickleback mortality induced by S. solidus
may be primarily caused by predation, not physiological deterioration. These reports
may explain my observation that uninfected stickleback have higher mating success
and live longer. I did not identify gender of stickleback during dissection; a
comparison study of parasitism between genders may also increase understanding of
reproductive success influenced by parasite infection.
My study has a number of limitations. My study encompasses 19 days at a total
of 77 sites. The sampling period was short to reduce seasonal influences on data. Also,
although I standardized my daily schedule, time of fish collection and parameter
measurement varied among sites. Stickleback migration, behavior, and susceptibility
might vary with time of day. Additional field crews could conduct sampling within
shorter time periods in a day. Sample size of fish varied from 0 to 250 fishes per site.
Electro-fishing may have allowed me to increase sample sizes at each site and to
determine the population densities. Ordinary linear regression requires sufficient
variance for the explanatory variables (Ramsey and Schafer 1997). In my study, visual
estimates for submerged macrophytes and mud/sand substrate cover had low variance
and were skewed, inducing lack of fit and decreased statistical significance. To avoid
this problem, more detailed classification or quantitative measurement might be useful
for these two parameters. Because half of my sites contained no infected fish, it would
be useful to focus sampling on areas with parasite infection if the goal were to
39
maximize fish collected. Reservoirs areas, that seem to contain the source of parasite
populations, would be preferable sample sites for obtaining larger sample sizes of
infected fish. Also, OLS regression analysis assumes that sample
units are independent regardless of the size of the study area (Ramsey and Schafer
1997). Biological interactions among sites, such as stickleback migration, should be
eliminated to obtain low biased samples.
Biological parameters rather than environmental factors seemed to have
stronger relationships with parasitic infection. Survey for zooplankton community
structure or of stickleback predators (e.g., birds) would be helpful for future study
(Marcogliese et al. 1992). Although mating choice of parasitized males has been
researched (Milinski and Bakker 1990), clarifying the relationship between
susceptibility of pre-spawning stickleback and post-spawning stickleback, or the
relationship between parasitic infection and spawning ability would increase our
understanding of intermediate host - parasite dynamics. My study focused on a macro
perspective, the spatial distribution and host - parasite population. A micro perspective
of the infection, the physiological mechanism of stressor to the host and parasite and
how they compromised by each other, may also be an important topic.
Many parameters have been used to evaluate infection level of macro/micro
parasites, bacteria, virus or other diseases. However, estimating infectious degree (the
"force of infection") has been a problem that preoccupies researchers in most
epidemiological sub-disciplines (Smith 1994). Incidence, prevalence, and attack rate
are relatively easy and convenient parameters (Smith 1994), but they work only in
limited cases and require many assumptions, hence, are often poor indicators. Mean
intensity, parasite index, condition factor and truncated negative binomial analysis may
represent a more accurate characterization of infectious events in the host population
(Arnie and Owen 1967, Crofton 1971, Pennycuick 1971, Meakins 1974, May and
Anderson 1979). The negative binomial analysis is a useful tool for estimating host
mortality induced by a parasite. When parasites are more highly aggregated than free-
40
living organisms, their distribution can be estimated by the negative binomial
distribution (Crofton 1971). According to Burgett et al. (1990: 1424), "Briefly, the
negative binomial distribution belongs to a family of functions that
describe either aggregation (negative binomial), randomness (Poisson), or repulsion
(positive binomial)". In my study, the frequency distribution of stickleback can be
described statistically by the negative binomial distribution. Although S. solidusassociated mortality may be detected by truncation of the negative binomial (Crofton
1971, Lanciani and Boyett 1980), I could only test lack-of-fitness and did not compute
the truncated analysis because of the complexity and not being able to obtain the
program.
In this study, I compared the degree of parasitism among sites using prevalence
and mean intensity. The benefit of my alternative model is its parsimonious model
structure and the durability of the characteristics expressed. Because this model
explains the availability of tapeworm infection among stickleback populations within
this particular basin, I assume that the slope, b, would be similar regardless of when
and where the samples were collected from within Upper Deschutes Basin. Because of
the similarity of the curve, the slope may also be similar regardless of the sample size.
Only the y-intercept will be changed by sample size. Data from another river system
might have a different value for b because of a difference in ability of the parasite to
kill the host or the fish's physiological tolerance for parasitism. We need to be careful
when we compute mortality from this technique because fish behavior is changed by
parasitism, and mortality from predators (i.e., birds, mammals or other fish) also
increases (Pennycuick 1971, Apanius and Schad 1994, Medley 1994). Thus, the
computed degree of parasitism represents physiological impact of the parasite, parasite
load, and physical impact of predatory animals.
Parasites are important components of food webs and should no longer be
neglected. Parasites can regulate host populations and can be keystone species
41
(Marcogliese and Cone 1996, 1997). In this study, introduction of stickleback made
the ecosystem more complex and both stickleback and tapeworm may not have
reached equilibrium conditions yet. Thus, it remains uncertain whether the tapeworm
is regulating the stickleback population. I suggest that risk assessments with
longitudinal observations are needed to better define the risk to the ecosystem from this
introduced fish.
42
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49
APPENDIX
Dataset collected in the Upper Deschutes Basin, central Oregon from July - August 2003.
Number
ID
Site name
Fish
Captured
Mean Intensity
(paras eel
I
CP cow meadow a
54
1.333
2
3
CPresorta
4
5
6
CP resortc
CPdam a
CPdam b
44
77
15
7
CP dam gaging
8
9
Southtwinlakea
2.475
2.754
2.071
3.633
3.000
1.609
1.375
0.000
0.000
0.377
0.015
0.000
0.000
2.158
0.208
0.177
2.117
5.708
3.910
1.458
3.000
0.667
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.037
0.000
0.000
0.000
10
11
12
13
14
15
16
17
18
19
CP resort b
Bigrivercamp
Bigriverboatlaunch
SunriverLodge
Sunriveraspine lake
Sunriver humming bird
Sunrivermarina
CP cow meadow b
Cultus river
CP quinn a
CP quinn b
CP rock boat
20 CP rock camp
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
South twin lake b
Bull bend camp
Wyeth boat launch
Lapinebigtree
La pine dayuse camp
Paulina lake a
Paulina lake b
Paulina lake c
Paulina lake d
Burgess rd. south
Burgess rd. north
Recriatjon rd. south
Recriation rd. north
Threft shop south
Threft shop nouth
31
12
69
32
40
36
54
67
231
39
19
24
483
79
24
67
61
1
23
45
37
68
180
87
106
22
96
56
65
25
71
)
Prevalence
( o)
Mean
fork length
(an)
100.0
60.0
4.757
4.307
3.822
4.547
4.446
4.367
3.436
96.9
0.0
0.0
24.5
4.141
2.465
2.219
4.043
1.5
0.0
0.0
100.0
12.5
3.452
2.914
3.003
4,284
4.533
12.2
93.5
100.0
98.5
96.6
100.0
60.0
2.211
74.1
75.0
76.9
85.7
93.3
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
3.7
0.0
0.0
0.0
4.619
4.750
4.460
4.030
5.000
2.504
3.020
2.173
2.809
2.503
2.322
2.828
3.200
2.602
2.352
2.498
3.072
2.593
r)
(
810
88
231
60
124
36
276
64
141
154
108
134
462
78
38
48
966
158
48
134
122
2
46
90
74
204
540
174
212
44
192
112
130
50
213
Dissolved
Minimum
Maximum
Submerged
Oxygen Conductwty Water flow Water depth temperature temperature
macrophytos
(l.is rn)
s)
(cm)
(mg/I)
C)
(CC)
(%)
C
8.777
5.503
7.587
7.677
6.207
6.240
5.587
6.827
4.377
6.737
2.507
4.760
2.613
7,337
8.597
10.093
7.750
10.727
6.570
6.470
6.827
7.730
7.523
7.567
7.743
7.517
7.510
7.227
5.333
6.333
6.267
6.423
6.450
6.723
6.670
28.5
35.4
46.8
46.2
46.2
46.9
46.8
135.6
48.1
48.0
146.9
121.3
124.2
50.0
28.2
38.3
43.4
33.0
42.3
44.1
135.5
47.3
47.2
46.4
46.9
514.0
507.0
514.7
530.0
30.9
30.9
33.0
33.0
48.2
48.2
0.655
0.000
0.000
0.000
0.000
0.085
0.300
0.000
0.131
0.229
0.013
0.000
0.016
0.268
0.494
0.196
0.000
0.184
0.000
0.000
0.000
0.457
0.337
0.443
0.527
0.000
0.000
0.000
0.000
0.518
0.389
0.257
0.323
0.375
0.395
29.3
1.8
9.0
12.2
10.0
15.0
52.7
29.7
17.0
20.3
63.0
29.3
48.7
18.0
9.0
20.7
19.0
17.0
7.7
8.3
27.3
76.0
52.3
89.3
75.3
13.0
29.3
26.3
10.3
78.0
44.7
81.7
36.0
120.0
47.7
9.90
12.77
22.43
22.40
23.33
24.17
24.27
23.20
15.60
16.57
20.53
21.77
20.50
15.80
9.53
5.17
19.43
5.23
19.63
21.57
22.93
15.57
15.40
15.00
15.07
17.30
17.07
17.17
17.73
18.10
18.00
18.47
18.50
16.73
16.60
18.0
35.6
28.9
29.4
27.0
27.0
26.7
30.0
22.0
16.7
25.0
26.7
26.7
16.0
14.0
10.0
24.0
12.8
22.0
16.7
23.0
17.2
21.1
15.0
14.4
21.0
20.5
20.0
18.0
20.6
21.1
20.6
21.1
18.0
20.0
0.083
0.117
0.033
0.225
0.392
0.000
0.675
0.775
0.875
0.775
0.775
0.875
0.875
0.775
0.000
0.083
0.875
0.017
0.775
0.000
0.017
0.567
0.875
0.358
0.567
0.033
0.875
0.875
0.575
0.183
0.775
0.567
0.667
0.875
0.875
Mud/sand
substrate
(%)
0.575
0,875
0.875
0.875
0.875
0.875
0.575
0.875
0.875
0.875
0.875
0.875
0.875
0.875
0.875
0.875
0.875
0.875
0.875
0.875
0.875
0.875
0.875
0.875
0.575
0.000
0.875
0.875
0.575
0.575
0.875
0.875
0.667
0.875
0.875
Dataset collected in the Unner Deschutes Basin. central Oregon from July - August 2003. (continuecfl
Number
ID
36
37
site name
Tumalo a
Tumalo b
38 Tumalo
39
101
c
9
Tumalod
31
40 Tumalo e
41 Tumalof
18
42
43
Clinefallssouth
24
Mirror pond north
26
44
45
46
Mirrorpondsouth
59
64
47
Bend mall north
39
Old mill bidge north
Old mill bidge south
6
48 Bend mall south
49 Lava island north
139
150
103
38
50
Lava island middle
34
51
Lavaislandsouth
51
52
53
54
55
Dillon falls north
23
85
52
Dillonfallsn,
Dillonfallssouth
Benham falls north
56 Benham falls middle
57 Benhamfallssouth
63
61
North davis west
96
115
63
103
84
175
62
Northdaviseast
17
58 Cardinal land middle
59 Cardinal land south
60 Cardinal land extra
Mean
Maximum number
Prevalence
Mean
Dissolved
Conducteity Water flow Water depth
Cared
67.9
483
Minimumnumber
1
Standard Deviation
Coefficient Variance
69.919
103.018
0.000
0.000
0.000
0.000
0.000
0.000
0.042
0.000
0.123
0.083
0.000
0.034
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.056
0.000
0.000
0.013
0.000
0.022
0.000
0.620
5.708
0.000
1.224
197.384
0.0
0.0
0.0
0.0
0.0
0.0
4.2
0.0
12.3
6,7
0.0
1.1
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
5.6
0.0
0.0
1.3
0.0
2.2
0.0
22.39
100.000
0.000
37.643
168.120
3.382
2.654
3.756
3.629
4.128
3.850
3.579
3.712
3.446
3.822
2.366
2.429
2.629
3.305
3.232
3.167
3.122
2.651
3.340
3.070
2.205
2.142
2.556
2.603
2.327
2.688
1.894
3.258
5.000
1.894
0.824
25.283
78
202
18
62
36
12
48
52
118
128
278
600
412
76
68
102
46
170
104
126
192
230
126
206
168
700
34
173.5
966.000
2.000
190.896
110.047
7.833
7.543
7.783
7.893
7.907
8.007
7.647
8.003
7.437
7.703
8.240
7.513
7.773
7.873
7.950
8.000
7.997
8.063
8.100
7.760
7.617
7.587
7,533
6.773
7.240
3.560
3.800
7.063
10.727
2.507
1.477
20.915
49.1
48.7
48.8
47.9
47.8
47.8
51.6
50.4
50.3
50.4
50.4
49.5
49.8
49.3
49.4
49.3
48.9
48.9
48.6
49.0
48.9
48.7
48.1
48.2
48.1
34.2
34.2
82.41
530.000
28.200
117.598
142.693
0.273
0.025
0.546
0.172
0.400
0.462
0.181
0.442
0.038
0.411
0.275
0.341
0.362
0.337
0.859
0.378
0.289
0.269
0.330
0.195
0.000
0.254
0.022
0.146
0.147
0.000
0.000
0.222
0.859
0.000
0.203
91.723
26.0
65.7
23.7
37.7
39.3
16.0
50.7
29.7
85.3
80.7
60.3
46.3
30.7
54.7
56.3
88.7
120.0
85.3
28.0
75.0
70.7
53.3
15.0
28.3
31.7
47.7
67.7
42.89
120.000
1.800
28.502
66.448
Minimum
Medmum
Submerged
temperature temperature macrophytos
16.27
15.97
15.97
15.60
15.63
15.63
18.03
16.20
16.13
16.13
16.40
15.37
15.47
14.90
14.90
14.90
14.47
14.50
14.53
14.97
14.77
14.57
14.30
14.20
14.43
8.73
8.80
16.358
24.270
5.170
4.011
24.520
20.5
23.0
21.0
22.0
20.6
20.0
24.0
17.8
18.3
19.5
20.0
18.1
18.1
16.1
15.8
15.8
15.8
16.1
15.8
18.3
18.3
18.3
17.8
17,8
17.8
12.2
13.3
19.98
35.600
10.000
4.764
23.844
0.358
0.775
0.292
0.183
0.358
0.183
0.875
0.358
0.875
0.875
0.875
0.875
0.567
0.667
0.250
0.000
0.467
0.875
0.875
0.875
0.875
0.875
0.875
0.875
0.875
0.575
0.875
0.564
0.875
0.000
0.329
58.319
Mud/sand
substrate
0.050
0.875
0.000
0.117
0.117
0.050
0.875
0.000
0.875
0.875
0.875
0.875
0.775
0.250
0.050
0.575
0.875
0.875
0.875
0.875
0.875
0.875
0.875
0.875
0.875
0.875
0.875
0.724
0.875
0.000
0.288
39.777