Pelagic Trophic Interactions in Contrasting Basins of Lake Chelan
Erik R. Schoen
A thesis submitted in partial fulfillment of the requirements for the degree of
Master of Science
University of Washington
2007
Program Authorized to Offer Degree: School of Aquatic and Fishery Sciences
University of Washington Graduate School
This is to certify that I have examined this copy of a master’s thesis by
Erik R. Schoen
and have found that it is complete and satisfactory in all respects, and that any and all revisions required by the final
examining committee have been made.
Committee Members:
___________________________________ David A. Beauchamp
____________________________________ Timothy E. Essington
____________________________________ Daniel E. Schindler
Date: ____________________
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University of Washington
Abstract
Pelagic Trophic Interactions in Contrasting Basins of Lake Chelan
Erik R. Schoen
Chair of the Supervisory Committee: Associate Professor David A. Beauchamp School of Aquatic and Fishery Sciences
Introductions of Mysis relicta are associated with declines in planktivorous fish populations in many lakes throughout western North America. Mysis may negatively impact planktivorous fishes by consuming a shared prey resource (exploitative competition) or by enhancing the density and body size of shared predators (apparent competition). I evaluated evidence for these interactions between Mysis and kokanee (Oncorhynchus nerka) in Lake Chelan, WA. I compared food web patterns between two lake basins of contrasting depth to investigate the potentially mediating influence of this habitat characteristic. Zooplankton production was enhanced in the shallower lake basin but Mysis density was not enhanced, resulting in a greater food supply available to kokanee in that basin. Kokanee migrations between basins were not explained by seasonal food availability alone, suggesting that predation risk was also an important factor. Lake trout diets contained more Mysis in the shallower basin, and this was associated with a seven-fold greater catch per unit effort of lake trout compared to the deeper basin. This result was consistent with strong apparent competition in the shallower basin. However, bioenergetics model simulations predicted that lake trout consumption of kokanee was slightly greater in the deeper basin. This analysis likely underestimated the strength of apparent competition due to greater fishing mortality for lake trout in the shallower basin and other factors. I compare Lake Chelan to other oligotrophic lakes and propose that lake depth may mediate the relative importance of exploitative competition and apparent competition in Mysis interactions with planktivorous fishes. Understanding this change in ecology along a depth gradient may be crucial for managers who aim to conserve planktivorous fish populations.
i
TABLE OF CONTENTS
Page
List of Figures............................................................................................................... ii
List of Tables ...............................................................................................................iii
Chapter I: Does Lake Basin Depth Mediate Competition Between Mysis relicta and Kokanee in Lake Chelan? ......................................................................... 1
Introduction ..................................................................................................... 1
Study Area ....................................................................................................... 3
Methods ........................................................................................................... 5
Results ........................................................................................................... 12
Discussion ...................................................................................................... 15
Notes to Chapter I .......................................................................................... 31
Chapter II: Does Lake Basin Depth Mediate Lake Trout Predation on Mysis relicta in Lake Chelan? Implications for Kokanee ......................................... 37
Introduction ................................................................................................... 37
Study Area ..................................................................................................... 39
Methods ......................................................................................................... 41
Results ........................................................................................................... 44
Discussion ..................................................................................................... 47
Notes to Chapter II ........................................................................................ 61
References ................................................................................................................. 65
Appendix A: Additional Tables for Chapter II........................................................... 73
ii
LIST OF FIGURES
Figure Number Page
1. Map of Lake Chelan including sampling sites .............................................. 24
2. Longitudinal depth profile of Lake Chelan ................................................... 24
3. Density of principal zooplankton taxa ........................................................... 25
4. Density of Mysis relicta ................................................................................. 26
5. Growth trajectory of Mysis relicta ................................................................ 27
6. Kokanee density and seasonal migration patterns ......................................... 28
7. Vertical distribution of kokanee and Mysis at night during August 2005 ..... 29
8. Seasonal zooplankton production and planktivore consumption .................. 30
9. Piscivore catch per unit effort ........................................................................ 53
10. Annual lake trout diet composition ............................................................... 54
11. Density of Mysis relicta and contribution of Mysis to lake trout diets across a depth gradient ...................................................................................55 12. Annual northern pikeminnow diet composition ............................................ 56
13. Annual burbot diet composition .................................................................... 57
14. Age-frequency of lake trout captured in gill nets .......................................... 58
15. Annual consumption by simulated lake trout populations of 1000 fish ages 2-16 in each basin of Lake Chelan ........................................................ 59 16. Annual consumption of fish prey by simulated lake trout populations in each basin of Lake Chelan scaled to the relative density of lake trout in those basins .................................................................................................... 60
iii
LIST OF TABLES
Table Number Page
1. Limnological characteristics of Lake Chelan ................................................ 22
2. Inputs used in bioenergetics simulations for Mysis relicta ........................... 22
3. Thermal experience and prey energy density inputs used in bioenergetics simulations for kokanee ................................................................................. 23
4. Growth inputs used in bioenergetics simulations for kokanee ...................... 23
5. Ratios of planktivore consumption to zooplankton production .................... 23
6. Prey energy density inputs used in bioenergetics simulations for lake trout ................................................................................................................ 51 7. Thermal experience inputs used in bioenergetics simulations for lake trout ................................................................................................................ 51 8. Growth, proportion of maximum consumption, and population structure used in bioenergetics simulations for lake trout ............................................ 52 A1. Seasonal diet composition of lake trout........................................................ 74 A2. Seasonal diet composition of northern pikeminnow .................................... 75 A3. Seasonal diet composition of burbot ............................................................ 76
iv
ACKNOWLDEGEMENTS
This project was funded by the US Geological Survey, the UW School of
Aquatic and Fishery Sciences, and the Lake Chelan Sportsmen’s Association.
I would like to give special thanks to Nathanael Overman, Anna Buettner, and
Brittany Long, who contributed innumerable hours to this project. The work in this
thesis is in large part theirs as well as mine. Chris Sergeant, Martin Grassley, and Erin
Lowery made major contributions in the field with their bulging biceps, ingenuity, and
the steady stream of b.s. that kept us going when we were soaked, sleep deprived, and
getting snowed on. I am grateful to Jen McIntyre, Liz Duffy, Mike Mazur, Cara
Menard, Sophie Pierszalowski, Sarah McCarthy, Susan Wang, Hillary Limont, Hans
Berge, Jim and Rob Mattilla, Verna Blackhurst, Jenn Scheuerell, Angie Lind, Neala
Kendall, Jared Mitts, Neil Jones, and Evelyn Cheng, for their help and ideas.
The Lake Chelan Sportsmen’s Association provided biological samples,
logistical support, and most importantly, expert local knowledge. Special thanks to
Anton and Sandy Jones, Frank and Patricia Clark, Joe Heinlen, and Mark Lippincott
for their help and advice. Local facilities and logistical support were provided by the
Chelan Ranger District of the US Forest Service, the Lake Chelan Fish Hatchery,
Washington State Parks, North Cascades National Park, and the city of Manson.
Many thanks to the Lake Chelan Fishery Forum, especially Art Viola, Phil
Archibald, Jeff Osborn, Steve Hays, and Reed Glesne, for thoughtful comments and
encouragement that helped direct my focus to the issues most relevant to local
managers. My committee members, Daniel Schindler and Tim Essington, provided
valuable advice for preparing this work for publication.
My major advisor, Dave Beauchamp, gave me the right mix of guidance and
encouragement as I entered a new field of study, with increasing free rein as I
developed my own ideas. I am happy to have hit the jackpot with an advisor who is a
role model both as a professional and as a person.
Finally, I would like to thank my family and my fiancé Jenny for their love and
support over the last three years.
1Chapter I: Does Lake Basin Depth Mediate Competition between Mysis relicta and Kokanee in Lake Chelan? Introduction
In aquatic ecosystems, habitat characteristics often influence the strength of
biotic interactions (Dunson and Travis 1991; Wellborn et al. 1996; Jackson et al.
2001). Basin morphometry, degree of thermal stratification, and nutrient loading
structure pelagic communities through effects on primary and secondary production
(Brett and Goldman 1997; Shuter and Ing 1997), top-down control (Jeppesen et al.
2003; Aksnes et al. 2004), and connectivity between adjoining riparian, littoral, and
profundal habitats (Schindler and Scheuerell 2002; Vadeboncoeur et al. 2002). The
establishment success and subsequent impacts of non-native species depend in part on
traits of the recipient system (Lodge 1993; Mills et al. 1994). Thus, the study of non-
native species ecology in pelagic habitats should benefit from consideration of how
these physical structuring factors affect the outcomes of introduction events.
Introductions of the opossum shrimp Mysis relicta have altered lake
communities throughout western North America and Scandinavia (Lasenby et al.
1986; Nesler and Bergersen 1991). In many cases, planktivorous fishes declined in
body size or density, or disappeared altogether following Mysis introductions
(Lasenby et al. 1986). Competition between Mysis and planktivorous fish for high-
quality cladoceran prey may explain these declines (Morgan et al. 1978; Martinez and
Bergersen 1991; Spencer et al. 1999; Clarke and Bennett 2002), although apparent
competition mediated by shared predators has also been proposed as a mechanism
2(Bowles et al. 1991; Spencer et al. 1991; Vander Zanden et al. 2003). The severity of
responses by planktivorous fish populations to Mysis introductions have varied
considerably among recipient lake systems (Northcote 1991). Although over 100
lakes now contain introduced Mysis populations, these systems vary simultaneously in
many potentially mediating habitat variables, including lake size, basin morphometry,
productivity, climate, species composition, and invasion history. These confounding
variables complicate the task of identifying factors that mediate the impacts of Mysis
on lake food webs.
Lake depth may mediate competitive interactions between Mysis and kokanee
(Oncorhynchus nerka), an ecologically and economically important planktivorous fish
in the Western USA and Canada. Zooplankton production is generally expected to
increase with decreasing lake depth in oligotrophic lakes, due to warmer, deeper
epilimnia in shallower lakes (Wetzel 1983). Kokanee foraging and growth rates might
increase with enhanced zooplankton production along this gradient. Kokanee may
also benefit if warmer temperatures restrict Mysis from a greater proportion of
epilimnetic zooplankton production (Martinez and Bergersen 1991; Chipps and
Bennett 2000). Kokanee growth was negatively correlated with reservoir depth both
before and after establishment of Mysis in Lake Granby, CO (Martinez and Wiltzius
1995), in support of a hypothesis that shallower lakes provide greater food resources
for kokanee in the presence of Mysis. However, zooplankton standing biomass can be
strongly controlled by predation (Brett and Goldman 1997; Borer et al. 2006) and
Mysis can consume several times more zooplankton than kokanee at the population
level (Chipps and Bennett 2000). Thus, a competing hypothesis predicts that
3shallower, more productive lakes may not generally produce greater food supplies for
kokanee if enhanced zooplankton production in these lakes is consumed by enhanced
Mysis populations (Thompson 2000; Hyatt et al. 2005).
To investigate whether enhanced zooplankton production in shallower systems
is available to kokanee, I compared patterns of zooplankton production and
planktivore consumption between two contrasting basins of a large, ultraoligotrophic
lake. By comparing distinct basins within a single lake, I controlled for other
confounding variables in order to draw conclusions about the influence of basin depth
on competition between planktivores. I quantified zooplankton density and
production, planktivore density, and planktivore consumption : zooplankton
production ratios in a deeper and a shallower basin during four seasonal periods. If
planktivore densities were primarily limited by food supply, then the basin with
greater zooplankton production would be expected to support greater densities of
Mysis and kokanee. Because kokanee were able to migrate between lake basins via a
narrow channel, differences in kokanee density between basins could be interpreted as
seasonal measures of basin suitability, whereby suitability incorporated food supply as
well as other factors such as predation risk.
Study Area
Lake Chelan is a deep (maximum depth 453 m), glacially-formed lake located
in the Cascade Range in north-central Washington (48° N, 120° W; Fig. 1). The lake
is long and narrow (length 81 km, maximum width < 3 km), and is composed of two
4basins joined by a narrow channel. Lucerne Basin in the northwest is extremely deep
and steep-sided (mean depth 190 m), while Wapato Basin in the southeast is relatively
broad and moderately deep (mean depth 45 m; Fig. 2; Kendra and Singleton 1987).
The two lake basins also differ slightly in thermal regime, as expected given the
difference in depth and volume (Wetzel 1983); the deeper Lucerne Basin begins to
stratify approximately one month later and has cooler surface water during peak
stratification (approx. 17º vs. 19º C) than the shallower Wapato Basin (Pelletier et al.
1989). Both lake basins are ultraoligotrophic (total phosphorus averages 3.2 µg/L),
and Wapato Basin is slightly more productive than the Lucerne Basin (Table 1). Lake
Chelan is slightly less transparent than other lakes of similarly low productivity due to
small amounts of glacial flour in the water (annual mean Secchi depth 13 m; Pelletier
et al. 1989).
Native fish species in Lake Chelan include bridgelip sucker (Catostomus
columbianus), burbot (Lota lota), largescale sucker (Catostomus macrocheilus),
northern pikeminnow (Ptychocheilus oregonensis), peamouth (Mylocheilus caurinus),
slimy sculpin (Cottus cognatus), threespine stickleback (Gasterosteus aculeatus), and
westslope cutthroat trout (Oncorhynchus clarki lewisi). Many nonnative fish and
invertebrate species have been introduced to the lake, primarily to enhance sport
fisheries, including landlocked Chinook salmon (Oncorhynchus tshawytscha),
kokanee, lake trout, Mysis relicta, rainbow trout (Oncorhynchus mykiss), smallmouth
bass (Micropterus dolomeiu), and tench (Tinca tinca) (Brown 1984; Wydoski and
Whitney 2003). Of these species, kokanee and Mysis are assumed to be the only
5ecologically relevant planktivores, because of low abundances of other planktivorous
species (Brown 1984).
Kokanee is the major pelagic fish in Lake Chelan. Most Lake Chelan kokanee
spawn at age 4, with smaller numbers of spawners at ages 3 and 5 (Peven 1990). Over
90% of kokanee spawning takes place in the Stehekin River and its tributaries at the
north end of the lake, during September and October (Peven 1990; Schoolcraft and
Mosey 2006). Kokanee were introduced to the lake in 1917 and have been the target
of a major recreational fishery for most of the last century (Brown 1984; Hagen 1997;
DES 2000). Mysis were first introduced in 1967, and were established throughout the
lake by 1975. The kokanee population crashed during the late 1970s and early 1980s,
following the establishment of Mysis and the concurrent introduction of landlocked
Chinook salmon (Brown 1984). The kokanee population recovered following the
collapse of Chinook salmon in the early 1980s and is currently stable, supported by
natural reproduction and a hatchery supplementation program (DES 2000; Schoolcraft
and Mosey 2006).
Methods
I used empirical data, zooplankton production models, and bioenergetics
models to compare seasonal patterns of food supply and planktivory by Mysis and
kokanee in the two basins of Lake Chelan. I collected limnological data, biological
samples, and conducted hydroacoustic surveys on Lake Chelan from August 2004 to
6August 2006. Sampling was conducted each February, May, August, and November
during this period.
Field sampling
Temperature profiles, zooplankton hauls, and Mysis hauls were conducted at
five sites in the lake: two in Wapato Basin and three in Lucerne Basin (see Fig. 1).
Temperature profiles were collected with a Hydrolab Datasonde (Hach Environmental
Inc.). Zooplankton were sampled during daylight, using a conical 35-cm-diameter,
153-µm-mesh net, with vertical hauls from 80 m depth to the surface. Mysis were
sampled at night, using a conical 1-m-diameter, 1-mm-mesh net, with vertical hauls
from 80 m depth to the surface. Efficiency of zooplankton and Mysis hauls was
assumed to be 100% when calculating densities, and we considered zooplankton
density estimates to be conservative because net efficiency, while unknown, was likely
lower than 100%. Zooplankton and a subset of Mysis individuals were preserved in
95% ethanol. A subset of Mysis individuals was preserved by freezing.
Kokanee were sampled using mid-water gill nets and by angling. Kokanee
densities were generally extremely low, and samples were successfully collected only
during spring, when kokanee aggregated in the Wapato Basin, and during late summer
when adult pre-spawners staged at the mouth of the Stehekin River. Kokanee were
weighed and measured, scales were collected from the area of earliest scale formation
(DeVries and Frie 1996), and stomachs were collected and frozen for subsequent
analysis. Additional scale and stomach samples were contributed by fishery managers
and sport anglers. Two independent readers aged each fish from scales. Kokanee
7growth was characterized with a mass-at-age relationship. Kokanee stomach
contents were identified to the finest possible taxonomic level and characterized as
diet proportions by blotted wet weight.
Zooplankton biomass and production
Seasonal standing stock biomass and production were calculated for primary
crustacean zooplankton species using empirical data and an egg-ratio production
model. Crustacean zooplankton were identified to species, enumerated, and body
length (from the base of the helmet to the base of the tail spine or setae) was measured
for the first 15 individuals of each taxon using an ocular micrometer. Zooplankton
eggs attached to or contained within the carapace of adult females were enumerated by
species. Loose eggs were identified as cladoceran or copepod based on size and
assigned to taxa within those groups based on the proportion of adults of each taxon
present in the sample. Zooplankton body mass was estimated from body length using
taxa-specific length-weight relationships (Dumont et al. 1975). Egg development
times were calculated using empirical water temperature data and taxon-specific
relationships (Paloheimo 1974; Brett et al. 1992). Seasonal production rates were
calculated for the dominant cladoceran (Daphnia spp. and Bosmina longirostris) and
copepod (Diacyclops thomasi and Leptodiaptomus ashlandi) populations separately
for each lake basin using the egg-ratio method (Edmondson 1972; Paloheimo 1974;
Cooley et al. 1986). We grouped Daphnia thorata, D. galeata, and D. longiremis into
a single category for estimating production because the length-weight and egg
development time relationships did not distinguish among Daphnia species.
8Production for each taxon was calculated for the upper 80 m of the water column,
which likely resulted in conservative estimates of productivity during thermally
stratified periods (Kuns and Sprules 2000).
Planktivore density and growth
Body length (from the tip of the rostrum to the tip of the telson) and blotted
wet weight were measured for each Mysis sample. Mysis age classes were identified
from modes in length-frequency histograms and growth of each age class was
calculated as seasonal mean wet weight, stratified by lake basin. To determine
whether size-selective predation biased Mysis growth estimates during August in
Wapato Basin, when adult growth appeared to be negative, we compared the length
distribution of mysids collected in net tows to the length distribution of Mysis found in
lake trout and burbot stomachs during that period. Lake trout and burbot were the
major Mysis predators in Lake Chelan and were collected with gill nets (Chapter 2).
Body lengths of partially digested Mysis were reconstructed based on lengths of eye
stalks, which were usually intact in stomach samples (Gal et al. 2006). We derived a
linear regression relating body length (BL) to eye-stalk length (EL), both measured in
mm, using intact mysids collected by net (BL = 144.7 EL – 1.70, n = 90, r2 = 0.87, p <
0.001).
Kokanee abundance, density, migration patterns, and vertical distribution were
determined with hydroacoustic surveys. Surveys were conducted with a towed split-
beam, 200 kHz transducer, linked to a scientific echosounder (DE-6000, Biosonics
Inc.) on zig-zag transects at night. A quantitative survey was conducted on moonless
9nights in August 2005, during late-summer thermal stratification, to estimate density
and distribution of kokanee when schooling behavior was minimized (Luecke and
Wurtsbaugh 1993). Surveys were conducted during other sampling periods as well to
characterize seasonal kokanee migration patterns and vertical distribution. We
assumed that small (<310 mm fork length), pelagic fish targets were kokanee because
kokanee were the dominant pelagic fish in Lake Chelan, kokanee comprised 95% of
our mid-water gill net catch, and modal sizes of acoustic targets corresponded with the
size distribution of captured kokanee. Hydroacoustic data were analyzed using
standard echo-counting techniques with EchoView 4.2 software (SonarData Pty. Ltd.)
to estimate seasonal depth-specific density and distribution of kokanee, stratified by
size class (Love 1977) and lake basin. The target strength threshold for acoustic
surveys (-55 dB) excluded Mysis-sized targets, so we sampled additional, short
transects with a lower threshold (-70 dB) in conjunction with each Mysis netting event.
The vertical distribution of the Mysis scattering layer was determined by visual
inspection of echograms from these transects.
Planktivore consumption
Consumption by the Mysis and kokanee populations was estimated using
bioenergetics models (Hanson et al. 1997) parameterized for Mysis relicta (Rudstam
1989; Chipps and Bennett 2000) and sockeye salmon (Beauchamp et al. 1989). Model
inputs for each consumer species were stratified by age class and lake basin and
included growth (weight-at-age), thermal experience, diet composition, the energy
density of consumers and their prey, and consumer density.
10 Energy demand by Mysis population was modeled using empirical and
literature values as model inputs (Table 2). Individual growth and population density
were estimated from seasonal mass (g wet) and areal density (individuals • m-2)
values. Thermal experience was estimated as the mean temperature of the
hypolimnion, metalimnion, and the depth reached at the apex of the vertical migration,
weighted by time spent in each depth zone. Mysids were assumed to spend the
daylight and civil twilight period in the hypolimnion, one hour in the metalimnion
during each of the upward and downward migrations, and the remainder of the diel
period at the apex depth (seasonal diel period data for Chelan, WA from US Naval
Observatory, Astronomical Applications Department: <http://aa.usno.navy.mil>).
Energy densities averaged 3,135 J • g-1 wet weight for juvenile and 3,720 J • g-1 wet
weight for adult Mysis in Char Lake (Lasenby 1971). I used these energy densities
during May and August, and reduced the adult value by 20% during November and
February to account for diminished Mysis lipid reserves during winter (Adare and
Lasenby 1994). Juvenile Mysis (length < 8 mm) were assumed to be herbivorous
(Rybock 1978; Chipps 1997; Johannsson et al. 2001). Adult Mysis are omnivorous,
consuming predominantly zooplankton but also algae, detritus, and benthic prey
(Grossnickle 1982; Johannsson et al. 2001). Thus, I considered the total consumption
demand by adult Mysis to be an upper bound of zooplankton consumption. The
energy density of the adult Mysis diet was estimated based on published Mysis prey
preferences and seasonal patterns of cladoceran abundance. Mysis prefer cladoceran
prey, but consume copepods as well when cladoceran densities are low (Cooper and
Goldman 1980; Grossnickle 1982; Spencer et al. 1999). Dietary energy density was
11modeled as the energy density of cladocerans (2,039 J • g-1 wet weight) during
August, when Daphnia and Bosmina densities were high, and as the energy density of
copepods (2,721 J • g-1 wet weight) during all other periods (values from Cummins
and Wuycheck 1971).
Consumption by kokanee was modeled using annual growth (mean wet
weight) except from May to August for the age-3 cohort, when seasonal growth data
were available. Kokanee in Lake Chelan were treated as a single population moving
between Lucerne and Wapato Basins; thus, growth inputs were identical among basins
but density varied seasonally among basins. Seasonal kokanee density in each basin
was estimated by assuming that lake-wide kokanee density equaled the density during
the quantitative August hydroacoustic survey, and distributing this total population
between basins using seasonal proportions of targets within each basin, stratified by
age-class. Kokanee thermal experience was estimated as the mean temperature of the
metalimnion, or the mean temperature of the upper 50 m of the water column during
non-stratifed periods (Table 3). Diet composition inputs were compiled from the
current study and from a previous study in Lake Chelan (Brown 1984). Zooplankton
prey were treated as a single prey type in bioenergetics simulations because
zooplankton population dynamics can be highly variable among years (e.g. Romare et
al. 2005) and kokanee diet proportions from previous years might not reflect the
spatial-temporal availability of specific taxa during the current study period. I
interpreted consumption of “zooplankton prey” by assuming that kokanee preferred
cladocerans, especially Daphnia, when they were available, and consumed copepods
during the rest of the year (Beauchamp et al. 2004; Scheuerell et al. 2005). Kokanee
12energy density varied with body size as described by Beauchamp et al. (1989). Prey
energy density was compiled from literature values (Table 3). Energy density of
zooplankton prey was modeled as the energy density of cladocerans (3,800 J • g-1 wet
weight; Luecke and Brandt 1993) during August, when Daphnia and Bosmina
densities were high, and as the energy density of copepods (2,721 J • g-1 wet weight;
Cummins and Wuycheck 1971) during all other periods. Cladoceran energy densities
were greater than those used in the Mysis model because kokanee are known to
increase the energy density of cladoceran prey by squeezing water out of the carapace
(Stockwell et al. 1999), while this pattern has not been documented in Mysis.
Total seasonal, basin-specific consumption by the Mysis and kokanee
populations was compared to the production of cladoceran zooplankton alone and
cladocerans plus copepods. The ratio of planktivore consumption to zooplankton
production was calculated to indicate the proportion of zooplankton production
consumed by planktivore populations in each lake basin.
Results
Density and standing stock biomass of cladoceran zooplankton were greater in
the shallower Wapato Basin than in the deeper Lucerne Basin during all periods but
August (Fig. 3). Areal density of cladoceran zooplankton was greater in the shallower
Wapato Basin than in the deeper Lucerne Basin during all sampling periods except
August. Biomass of Daphnia was 2.3 – 30.2 times greater in Wapato Basin than in
Lucerne Basin during the February, May, and November sampling periods. Biomass
13of Bosmina was 4.0 – 11.4 times greater in Wapato Basin during those periods.
During August, Daphnia biomass was slightly greater in Lucerne Basin than in
Wapato Basin (1.8 vs. 1.7 g • m-2, respectively), but Bosmina biomass was 2.7 times
greater in Wapato Basin. Copepod standing biomass was greater than cladoceran
biomass in both basins, during all seasons. Diacyclops biomass was 1.3 and 2.7 times
greater in Wapato Basin than Lucerne Basin during February and May, respectively,
and was similar between basins during August and November.
Mysis density varied seasonally and was generally similar between Lucerne
Basin and Wapato Basin, except during summer when density was greater in Lucerne
Basin (Fig. 4). Mysis exhibited a 1.5-year life span, with juveniles released between
February and May and the parental generation disappearing by the following
November. Total Mysis growth from juvenile to adult was similar among lake basins,
but seasonal growth patterns differed (Fig. 5). Mysis grew at a relatively consistent
rate in Lucerne Basin, while Mysis in Wapato Basin achieved most growth between
spring and summer and less growth during the rest of the year. Body length of Mysis
collected in lake trout and burbot stomachs in the Wapato Basin during August did not
differ from Mysis collected in nets during that period (t-test, equal variances not
assumed: p > 0.2), providing no evidence of size-selective predation during that
period.
Kokanee made distinct seasonal migrations between lake basins, and densities
were greater in Lucerne Basin during most of the year (Fig. 6). During May, age-0
kokanee were evenly distributed between Lucerne Basin near the Stehekin River outlet
(likely naturally produced fry) and Wapato Basin (likely hatchery-origin fry). Age-0
14kokanee were most dense near the Stehekin River during August and November,
with lower densities in the rest of the lake. Age-1 and older kokanee were most dense
in Lucerne Basin during all periods except May (ages 1-3) and November (age 2-3).
Kokanee density was relatively low overall (mean summer density = 49.1 kokanee •
ha-1). Mean body mass of kokanee captured during May was 37.5, 165.8, and 225.2 g
wet (ages 1, 2, and 3, respectively). Mean body mass of age 3+ kokanee staging to
spawn during August was 262.1 g. May and June kokanee diets consisted
predominantly of Diacyclops (age 1) and chironomids, Daphnia, and Bosmina (ages 2
and 3). August diets of kokanee prespawners were dominated by Daphnia and
Bosmina.
During stratified periods, the apex of the Mysis vertical migration was in or
below the thermocline. Night kokanee distributions overlapped with those of Mysis,
but some kokanee were distributed in the epilimnion, with age-0 kokanee more likely
to be distributed near the surface than older age classes (Fig. 7). During non-stratified
periods, both Mysis and kokanee were distributed higher in the water column. These
patterns were consistent in both lake basins.
The deeper Lucerne Basin supported less zooplankton production than the
shallower Wapato Basin during all four seasons (Fig. 8). This pattern was consistent
when considering production of cladocerans alone or production of both cladocerans
and copepods. Consumption by the Mysis population in Lucerne Basin was similar or
greater than consumption in Wapato Basin, resulting in a lower ratio of production to
planktivore consumption in that basin during all seasons (Table 5). Kokanee
consumption ranged from 23-30% of maximum bioenergetic consumption rates.
15
Discussion
Lake basin differences in zooplankton supply and consumption demand
Density and production of zooplankton were generally greater in the shallower
Wapato Basin than in the deeper Lucerne Basin of Lake Chelan. Production rates of
Daphnia and Bosmina were greater in Wapato Basin during all four seasonal sampling
periods. However, densities of Mysis and kokanee did not mirror this pattern: Mysis
densities were similar or greater in Lucerne Basin, and kokanee densities were greater
in Lucerne Basin for most age classes, during most seasons.
Planktivores consistently consumed a smaller proportion of zooplankton
production in Wapato Basin than in Lucerne Basin. This pattern held when
considering production by cladoceran prey alone, or when including copepod
production as well. Cladoceran production alone was generally insufficient to explain
the observed growth of the planktivore populations, indicating that planktivores must
have consumed copepods or other prey in order to achieve the observed growth.
Production by cladocerans plus copepods was sufficient to meet planktivore
consumption demand during all periods except November-February in Lucerne Basin.
During that period, planktivores may have reduced copepod standing stocks or relied
heavily on alternative prey. Although non-zooplankton prey was not quantified in this
study, it is unlikely that between-basin differences in non-zooplankton prey
availability would qualitatively change the pattern of greater food availability in
Wapato Basin. The only significant non-zooplankton prey item found in kokanee
16diets was chironomid pupae. Chironomid production is likely greater in Wapato
Basin with its moderate depth and soft bottom than in Lucerne Basin with its extreme
depth and steep, rocky slopes. A previous study found chironomids in kokanee
stomachs only in Wapato Basin and near the Stehekin River (Brown 1984), supporting
the overall pattern of greater food availability in Wapato Basin. I considered my
estimates of zooplankton production to be conservative because of less than perfect
net efficiency and because I estimated production of the entire 80 m of the water
column rather than as the sum of multiple discrete depths (Kuns and Sprules 2000). I
expected these underestimates to be similar between basins; thus, true C : P ratios are
likely lower than reported here, but I considered between-basin comparisons to be
robust.
These results support the hypothesis that lake basins of decreasing depth
support increasing levels of zooplankton production that is available to kokanee even
in the presence of Mysis (Martinez and Wiltzius 1995). Further, they suggest that
planktivorous fish may be most strongly affected by resource competition from Mysis
in deeper lakes with less zooplankton production. The two basins of Lake Chelan
provided a distinct contrast along the axis of lake depth many of the confounding
variables that complicate among-lake comparisons (Olden et al. 2006). Nutrient
loading and primary productivity was slightly greater in Wapato Basin (Table 1), and
this likely also enhanced zooplankton production. Primary productivity is strongly
inversely correlated with lake depth (Wetzel 1983), so the differences that I described
between basins may be considered as a function of both decreasing depth and
increasing productivity, rather than as a function of depth alone. Both basins of Lake
17Chelan lie towards one end of this habitat gradient; even the Wapato Basin is
relatively deep and very low in productivity. Thus, the patterns I observed may
provide insights into competitive interactions between planktivores among relatively
deep, oligotrophic lakes, but may not be apply to smaller, more productive lakes.
Spatial mismatches between zooplankton production and planktivore density
The lack of correspondence between zooplankton production and Mysis
density suggests that other factors may limit the Mysis population in the relatively
zooplankton-rich Wapato Basin. First, warmer epilimnetic temperatures may have
restricted Mysis to a smaller proportion of summer cladoceran production in the
Wapato Basin than in the cooler Lucerne Basin. This would be consistent with the
difference in growth patterns between basins: while Mysis growth was relatively
consistent in Lucerne Basin, Mysis showed apparently negative growth from August to
November, when the epilimnion penetrated deepest. However, thermal segregation
from prey would not explain slow Mysis growth in Wapato Basin during the
destratified period. Second, predation by lake trout and burbot may have limited
Mysis densities in the Wapato Basin. Predation rates on Mysis were likely much
greater in the Wapato Basin than the Lucerne Basin because lake trout densities were
greater and Mysis made up a greater proportion of lake trout diets there (Chapter 2).
Size-selective predation on Mysis might also explain relatively slow growth in Wapato
Basin from August through May, although I found no evidence of size-selective
predation during August. Finally, Mysis may have actively avoided shallow areas of
Wapato Basin despite the greater zooplankton availability. Mysis areal density
18increased with depth among sampling sites in Okanagan Lake, BC, Canada (Whall
2000), Lake Ontario (Johannsson 1995), and Flathead Lake, MT (Wicklum 1999),
although it is not clear whether this pattern was caused by increased predation in
shallow areas, dispersal by Mysis, or another mechanism.
Trade-offs between food supply and predation risk (Eggers 1978; Werner and
Gilliam 1984; Houston et al. 1993) may explain the spatial mismatch between
zooplankton production and kokanee density. Increased predation risk can alter
planktivore foraging behavior and consequently reduce access to food resources
(Romare and Hansson 2003; Jensen et al. 2006). Conversely, when food is scarce,
slower growth and riskier foraging behavior may increase the susceptibility of
planktivores to predation (Houston et al. 1993; Biro et al. 2003). Although the
shallower Wapato Basin produced more zooplankton prey than the deeper Lucerne
Basin, it also contained seven-fold greater densities of lake trout, a major kokanee
predator (Chapter 2; Figure 1). Kokanee densities were greater in the depauperate but
potentially less risky Lucerne Basin except when kokanee migrated into the Wapato
Basin during May (age 1 and older) and November (age 2 and older). These
migrations into the Wapato Basin occurred during spring and autumn, when Mysis is
expected to limit kokanee food supply most strongly (Clarke et al. 2004) by truncating
of the duration of peak cladoceran production (Spencer et al. 1999; Clarke and Bennett
2003). During February and August, densities of all kokanee age classes were greater
in Lucerne Basin. Cladoceran production was relatively high in both basins during
August, and this may have obviated the need to risk increased predation in the Wapato
19Basin. During February, low water temperatures in both basins limited the potential
for growth, perhaps limiting the potential foraging benefits in Wapato Basin.
The optimal solution in the trade-off between foraging opportunity and
predation risk is expected to change with body size, and this may explain ontogentetic
changes in kokanee distribution with age. McGurk (1999) showed that mortality rate
was inversely related to length in 11 populations of juvenile kokanee and sockeye
salmon, and argued that this relationship likely holds for older kokanee as well. Total
energy requirements for positive growth, however, increase with body size
(Beauchamp et al. 1989; Rieman and Myers 1992) and larger kokanee may be less
able to satisfy these requirements without access to high quality prey. Bioenergetics
results suggested that kokanee became increasingly food-limited with age in Lake
Chelan: age 0-1 and age 1-2 kokanee fed at a greater proportion of their maximum
possible consumption rate (p = 0.29-0.30) than age 2-3 kokanee (p = 0.23-0.24). Age-
0 kokanee densities indicated the strongest preference for Lucerne Basin. Age 1
kokanee made one major migration into Wapato Basin during May, while age 2-3
kokanee migrated into Wapato Basin during May and November. This increasing use
of Wapato Basin with age may reflect both a decrease in predation risk and an increase
in energy requirements with size.
Comparisons with other oligotrophic lakes
Mean Mysis density in Lake Chelan (16-146 m-2) fell within the low end of the
range of other lakes where Mysis has been implicated for declines or extirpation of
kokanee populations. Mysis densities ranged from 20-90 m-2 in Flathead Lake, MT
20during 1988-1998 (Wicklum 1999), and were 137 m-2 in Priest Lake, ID during
1988 (Bowles et al. 1991). Densities were much greater in Okanagan Lake (150-500
m-2) during 1996-1998 (Whall 2000) and in Lake Pend Oreille, ID (200-1,250 m-2)
during 1995-1996 (Chipps and Bennett 2000). Consumption by the Mysis population
was an order of magnitude greater than population-level consumption by kokanee in
Lake Chelan. Similarly, Mysis consumed over four times as much zooplankton as did
kokanee in Lake Pend Oreille (Chipps and Bennett 2000). Because consumption by
Mysis far exceeds consumption by kokanee in these lakes, interspecific competition
with Mysis may limit kokanee growth in oligotrophic lakes more strongly than
intraspecific density-dependence (Rieman and Myers 1992). Thermal exclusion of
Mysis from epilimnetic cladoceran production may help to ameliorate competitive
interactions during the peak kokanee growing season.
Kokanee in Lake Chelan achieved moderate body size and consumption rates
compared to populations in other oligotrophic lakes, suggesting that the population
was not strongly limited by food supply during the period of study. Age-4 kokanee
achieved a mean body mass of 262.1 ± 39.1 (g wet ± SD) in Lake Chelan. In
comparison, age-4 kokanee achieved a mean weight of 154.0 g in Lake Pend Oreille
during 1995 and 1996, a period when kokanee were considered to be food limited
(Chipps and Bennett 2000). Mean kokanee density was 42 ha-1 in Lake Chelan and
227-329 ha-1 in Lake Pend Oreille during these periods. Lake Chelan kokanee
consumption ranged from 23-30% of maximum bioenergetic consumption rates
(Cmax). Kokanee consumption in Lake Pend Oreille ranged from 28-39% of Cmax
during 1995 and 1996 (except age-0 kokanee during late summer, which consumed
21prey at 60% of Cmax; Chipps and Bennett 2000). Rieman and Myers (1992)
compared kokanee length and density across 10 oligotrophic lakes and reservoirs in
Idaho. Compared to kokanee in these lakes, age-1 kokanee in Lake Chelan were
relatively large (mean total length 153 mm), given their density (10.5 ha-1), providing
further support that kokanee were not strongly limited by food given the low
productivity of the system.
Conclusions
I compared patterns of planktivory by Mysis relicta and kokanee between two
connected lake basins of different depths. The deeper lake basin supported less
zooplankton production than in the shallower lake basin during all four seasonal
sampling periods. Mysis density and consumption rate was similar between basins,
and planktivores consumed a smaller proportion of zooplankton production in the
shallower basin. These results support the hypothesis that food supply for
planktivorous fish is enhanced in a shallower lake basin, not merely consumed by
increased densities of Mysis. Kokanee densities did not reflect these between-basin
differences in food availability: densities were greater in the deeper basin for most age
classes during most seasons. Increased predation risk in the shallower basin may
explain this pattern. Kokanee use of the shallower basin increased with age,
suggesting ontogenetic changes in the trade-off between foraging success and
predation risk. Overall, kokanee in Lake Chelan achieved a moderate adult body size
but a low density relative to other oligotrophic lakes with Mysis relicta populations.
Kokanee did not appear to suffer from strong food limitation during the period of
22study, despite the low primary productivity and moderate density of Mysis in Lake
Chelan.
Table 1. Selected limnological characteristics of the two basins of Lake Chelan, Washington, April - September 1987 (Kendra and Singleton 1987; Pelletier et al. 1989). Values reported are annual (April – September) means ± 1 SE.
Lake basin
Sur-face area (ha)
Mean depth (m)
Secchi depth (m)
Total P (µg • L-1)
Chloro-phyll a
(µg • L-1) 14C productivity (mg C • m2 • d-1)
Lucerne 9,984 190 13.8 ± 0.7 3.0 ± 0.2 0.7 ± 0.0 104.4 ± 20.4 Wapato 3,502 45 13.4 ± 0.9 3.9 ± 0.2 0.7 ± 0.0 147.6 ± 26.4
Table 2. Inputs used in bioenergetics simulations for Mysis relicta in Lake Chelan. Simulation day 1 corresponds to May 15. Body mass and thermal experience inputs are reported separately for Lucerne and Wapato Basins. Prey energy density values (J • g-1 wet weight) indicated in parentheses.
Diet composition Body mass
(g wet) Thermal experience
(ºC) Algae Zoop-
lankton Age class
Simul- ation day Lucerne Wapato Lucerne Wapato
Mysis energy density (J • g-1) (2558)
(2,039-2,721)1
0 1 0.004 0.002 7.0 5.9 3135 1 0 0 91 0.013 0.019 8.4 6.8 3720 0 1 0 182 0.021 0.019 8.8 9.4 2976 0 1 0 273 0.031 0.024 6.3 5.4 2976 0 1 0 365 0.036 0.028 7.0 5.9 3720 0 1 1 1 0.036 0.028 7.0 5.9 3720 0 1 1 91 0.042 0.048 8.4 6.8 3720 0 1
1Zooplankton energy density varied seasonally (see Methods).
23Table 3. Thermal experience and prey energy density inputs used in bioenergetic simulations for kokanee in Lake Chelan. Simulation day 1 corresponds to May 15. Thermal experience inputs are reported separately for Lucerne and Wapato Basins.
Diet composition Thermal experience (ºC) Zooplankton ChironomidsSimulation
day Lucerne Wapato (2,260-3,800)1 (3400) 1 9.2 10.9 0.56 0.45 91 12.2 12.3 0.95 0.05
182 11.5 11.6 1.00 0.00 273 6.3 5.6 1.00 0.00 365 9.2 10.9 0.56 0.45
1Zooplankton energy density varied seasonally (see Methods). Table 4. Growth inputs used in bioenergetic simulations for kokanee in Lake Chelan. Simulation day 1 corresponds to May 15.
Age Simulation
day
Body mass
(g wet) 0 1 0.2 1 1 37.5 2 1 165.8 3 1 225.2 3 91 262.1
Table 5. Ratios of planktivore consumption to zooplankton production for Lucerne and Wapato Basins of Lake Chelan. Consumption : production ratios were consistently greater in the deeper Lucerne Basin than in the shallower Wapato Basin.
Cladocerans only Cladocerans +
Copepods Period Lucerne Wapato Lucerne Wapato
Feb-May >100 4.80 0.23 0.11 May-Aug 7.00 1.99 0.98 0.56 Aug-Nov 3.51 0.43 0.57 0.16 Nov-Feb >100 3.01 20.78 0.35
24
Figure 1. Map of Lake Chelan, showing the two lake basins and principal sampling sites (stars). The inset shows the location of the lake in north-central Washington, USA.
Figure 2. Longitudinal depth profile of Lake Chelan, showing pronounced depth differences among lake basins. Horizontal axis represents distance from lake outlet along the primary axis of the lake.
25
Figure 3. Areal density of principal cladoceran (Daphnia and Bosmina) and copepod (Diacyclops and Leptodiaptomus) taxa in two basins of Lake Chelan, from August 2004 to May 2006.
26
Figure 4. Density of Mysis relicta in two basins of Lake Chelan, Washington. Symbols represent mean ± 1 standard error. Mysis densities were generally similar among basins but varied temorally due to mortality and seasonal changes in the proportion of the population that migrated into the water column.
27
Figure 5. Growth trajectory of Mysis relicta in two basins of Lake Chelan, Washington. Symbols represent mean wet weight ± 1 standard error. Mysis had a 1.5-year lifespan in Lake Chelan, being released as juveniles between February and May, releasing their offspring one year later, and surviving until August.
28
Figure 6. Kokanee density in Lucerne and Wapato Basins of Lake Chelan, quantified with seasonal hydroacoustic surveys during 2005. Because of its roughly 3-fold greater area, Lucerne Basin contained large numbers of kokanee even when densities were greater in Wapato Basin. Estimates of lake-wide kokanee abundance varied seasonally due to changing vertical distributions and low detectability of targets located in surface waters. Conditions during the August survey were most favorable for a quantitative estimate of kokanee abundance.
29
Figure 7. Vertical distribution of kokanee and Mysis at night in Lucerne and Wapato Basins during August 2005. Kokanee and Mysis distributions were determined from hydroacoustic surveys. Dashed lines represent the uppermost and lowermost extent of the Mysis scattering layer on hydroacoustic echograms. Solid lines represent thermal profiles. Kokanee were able to access epilimnetic zooplankton production but Mysis were confined to the metalimnion and hypolimnion during summer stratification.
30
Figure 8. Seasonal production of major zooplankton taxa and seasonal consumption by Mysis and kokanee populations in the two basins of Lake Chelan. Production of preferred cladoceran prey (Daphnia and Bosmina) was greater in the shallower Wapato Basin than in the deeper Lucerne Basin year round. Population-level consumption by Mysis far exceeded consumption by kokanee. Planktivore consumption demand exceeded production by cladocerans during most periods, suggesting that Mysis and kokanee consumed less preferred copepod prey (Diacyclops and Leptodiaptomus) during those periods.
31Notes to Chapter I:
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Scheuerell, J.M., Schindler, D.E., Scheuerell, M.D., Fresh, K.L., Sibley, T.H., Litt, A.H., and Shepherd, J.H. 2005. Temporal dynamics in foraging behavior of a
35pelagic predator. Canadian Journal of Fisheries and Aquatic Sciences, 62(11): 2494-2501.
Schindler, D.E., and Scheuerell, M.D. 2002. Habitat coupling in lake ecosystems. Oikos, 98(2): 177-189.
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Spencer, C.N., Potter, D.S., Bukantis, R.T., and Stanford, J.A. 1999. Impact of predation by Mysis relicta on zooplankton in Flathead Lake, Montana, USA. Journal of Plankton Research, 21(1): 51-64.
Stockwell, J.D., Bonfantine, K.L., and Johnson, B.M. 1999. Kokanee foraging: A Daphnia in the stomach is worth two in the lake. Transactions of the American Fisheries Society, 128(1): 169-174.
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Wellborn, G.A., Skelly, D.K., and Werner, E.E. 1996. Mechanisms creating community structure across a freshwater habitat gradient. Annual Review of Ecology and Systematics, 27: 337-363.
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Wicklum, D. 1999. The Ecology of Mysis relicta in Flathead Lake, MT, Flathead Lake Biological Station, Polson, MT.
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37Chapter II: Does Lake Basin Depth Mediate Lake Trout Predation on Mysis relicta in Lake Chelan? Implications for Kokanee Introduction
Indirect interactions are responsible for far-reaching impacts on ecological
communities (Simberloff and Von Holle 1999; Courchamp et al. 2000; Crooks 2002),
but the nature of these interactions is often poorly understood (Chase et al. 2002;
White et al. 2006). While invasion ecologists have often focused on documenting the
consequences of species introductions, identifying the mechanisms by which exotic
species interact with recipient communities and the community traits that influence
these interactions are important steps towards effectively managing invaded systems
(Lodge 1993; Vander Zanden et al. 2004).
Introductions of the opossum shrimp Mysis relicta have altered freshwater
communities throughout the western United States and Canada, and in Scandinavia
(Nesler and Bergersen 1991). Outcomes vary across systems, but cladocerans and
planktivorous fish have often been reduced in body size or density, or extirpated
altogether, while profundal-feeding fish have often increased in body size or density
(Lasenby et al. 1986). Diel vertical migration behavior explains this general pattern:
Mysis forages in the water column at night and spends daylight hours in deep water or
in the sediments (Juday and Birge 1927; Levy 1991), where they are unavailable to
pelagic planktivores.
Two hypotheses have been proposed to explain the negative impacts of Mysis
on planktivorous fish via indirect trophic interactions. First, since Mysis are efficient
planktivores and share a preferred prey, cladocerans, with many planktivorous fishes,
38Mysis may deplete the shared food resource, leading to reduced growth and
population declines for planktivorous fish (Morgan et al. 1978; Spencer et al. 1991;
Chipps and Bennett 2000). Second, when Mysis and planktivorous fish share common
predators such as lake trout (Salvelinus namaycush), the introduction of Mysis may
benefit planktivorous fish in the short term by satiating predators, but longer-term
increases in predator growth or density may enhance predation mortality (Bowles et al.
1991; Vander Zanden et al. 2003). The first interaction represents exploitation
competition, while the second is an example of apparent competition (Holt 1977; Holt
and Lawton 1994; Noonburg and Byers 2005). The relative importance of each
mechanism in any particular lake may depend on system-specific mediating biotic and
abiotic factors. Existing empirical data are consistent with the resource competition
hypothesis in some systems (Beattie and Clancey 1991; e.g. Martinez and Bergersen
1991; Spencer et al. 1999; Clarke and Bennett 2002), but apparent competition has
received less empirical attention (Bowles et al. 1991).
Lake depth might influence the availability of Mysis prey to lake trout. Lake
trout have been observed feeding on Mysis in lake sediments during daylight (D. A.
Beauchamp, personal observation); if this is a primary feeding mode, then extremely
deep water might provide a refuge from predation by allowing Mysis to suspend in
open water in the absence of light rather than concentrating on the lake bottom.
Increasing basin depth might also reduce predation during nightly vertical migrations
if Mysis is able to disperse across a greater volume between the thermocline and lake
bottom, thus reducing the encounter rates of pelagic predators.
39I compared food web patterns in two lake basins of contrasting depth in
Lake Chelan, Washington, and asked:
1) Do lake trout consume greater proportions of Mysis at shallower sampling
sites? If so:
2) Are increases in Mysis consumption by lake trout associated with increases
in lake trout density or growth?
3) Is increased Mysis consumption by lake trout associated with net positive
(predation buffering) or negative (apparent competition) indirect effects on
salmonid prey?
Study Area
Lake Chelan is a deep (maximum depth 453 m), glacially-formed lake located
in the Cascade Range in north-central Washington (48° N, 120° W; see Chapter 1, Fig.
1). The lake is long and narrow (length 81 km, maximum width < 3 km), and is
composed of two basins joined by a narrow channel. Lucerne Basin in the northwest
is extremely deep and steep-sided (mean depth 190 m), while Wapato Basin in the
southeast is relatively broad and moderately deep (mean depth 45 m; Kendra and
Singleton 1987). The two lake basins also differ slightly in thermal regime, as
expected given the difference in depth and volume (Wetzel 1983); the deeper Lucerne
Basin begins to stratify approximately one month later and has cooler surface water
during peak stratification (approx. 17 vs. 19 º C) than the shallower Wapato Basin
(Pelletier et al. 1989). Both lake basins are ultraoligotrophic (total phosphorus
40averages 3.2 µg/L), and Wapato Basin is slightly more productive than the Lucerne
Basin. Lake Chelan is slightly less transparent than other lakes of similarly low
productivity due to small amounts of glacial flour in the water (annual mean Secchi
depth 13 m; Pelletier et al. 1989).
Native fish species in Lake Chelan include bridgelip sucker (Catostomus
columbianus), burbot (Lota lota), largescale sucker (Catostomus macrocheilus),
northern pikeminnow (Ptychocheilus oregonensis), peamouth (Mylocheilus caurinus),
slimy sculpin (Cottus cognatus), threespine stickleback (Gasterosteus aculeatus), and
westslope cutthroat trout (Oncorhynchus clarki lewisi). A variety of nonnative fish
and invertebrate species have been introduced to the lake, primarily to enhance sport
fisheries, including landlocked Chinook salmon (Oncorhynchus tshawytscha),
kokanee, lake trout, Mysis relicta, rainbow trout (Oncorhynchus mykiss), smallmouth
bass (Micropterus dolomeiu), and tench (Tinca tinca) (Brown 1984; Wydoski and
Whitney 2003). Kokanee were introduced to Lake Chelan in 1917 and has been the
target of a major recreational fishery for most of the last century (Brown 1984; DES
2000). The kokanee population is currently stable, supported by natural reproduction
and a hatchery supplementation program (Hagen 1997; Schoolcraft and Mosey 2006).
Mysis were first introduced in 1967, and were established throughout the lake by 1975
(Brown 1984). Lake trout were introduced in 1980 and stocked consistently during
the 1990s. Lake trout are no longer stocked and have established a self-sustaining
population in the lake, which is the target of a trophy fishery (DES 2000).
41Methods
Field sampling
I collected biological samples and limnological data at Lake Chelan between
August 2004 and May 2006. Sampling was conducted each February, May, August,
and November during this period. Lake trout, northern pikeminnow, and burbot were
captured with horizontal sinking gill nets at five fixed sites in the lake, two in Wapato
Basin and three in Lucerne Basin (see Chapter 1, Fig. 1). Gill nets were set in “gangs”
of eight nets. Nets were set at four depths per site: one each in the epilimnion and
metalimnion, and two in the hypolimnion. One small-mesh net (mesh sizes 2.5, 3.2,
3.8, 5.1, 6.4, and 7.6 cm stretched) and one large-mesh net (mesh sizes 8.9, 10.2, 11.4,
12.7, and 15.2 cm stretched) were set at each depth at each site, with net pairs
separated by at least 100 m. Additional horizontal sinking gill nets were deployed
opportunistically in other areas to target species and size classes underrepresented in
standardized gill net catches. Gill nets were set during daylight hours, left to soak
overnight, and retrieved during daylight the next day. Captured fish were measured,
weighed, and their sex was recorded in the field. Stomachs were collected from all
piscivores and frozen immediately. Opercles were collected from all lake trout.
Vertical thermal profiles were collected with a Hydrolab Datasonde (Hach
Environmental Inc.) at each sampling site concurrently with gill netting. Mysis relicta
samples were collected in deep water adjacent to each gill netting site at night. Mysis
were collected with vertical hauls from 80 m depth to the surface using a conical 1-m-
diameter, 1-mm-mesh net.
42Fish stomach contents were identified to fish species or invertebrate family
and life stage when possible. Roughly half of salmonid prey specimens were
identifiable as kokanee; the rest could be identified only as salmonids from vertebrae.
Unidentified salmonid prey was assumed to be predominantly composed of kokanee,
because kokanee were much more numerous than other salmonids in Lake Chelan.
The blotted wet weight of each prey type was recorded, and diet proportions were
calculated by weight, with each non-empty stomach serving as a sampling unit. Lake
trout were aged from opercles, which allow similar precision as otoliths, and are more
precise than scales for long-lived lake trout (Sharp and Bernard 1988). The age
frequency distribution for captured lake trout was corrected for gill net size selectivity
(Hansen et al. 1997) and for inequalities in effort among mesh sizes (Ruzycki et al.
2003). The lake trout instantaneous annual mortality rate (Z) was estimated by fitting
a simple linear regression model to the descending limb of the natural log of this
corrected age frequency distribution. A stable age distribution was determined for the
lake trout population using this estimate of Z.
Model simulations
Consumption by the lake trout population was estimated with a bioenergetics
model (Hanson et al. 1997) using lake trout physiological parameters from Stewart et
al. (1983). Simulations were stratified by age (from 2 to 16 yr) and lake basin
(Lucerne versus Wapato), and run using a daily time step starting on May 15th as day 1
of the simulation. Model inputs included annual growth (weight-at-age), diet
composition, thermal experience, and the energy densities of consumers and prey
43species. Growth inputs were determined by fitting a Von Bertalanffy growth model
to empirical length and age data from the subset of fish that were aged (n = 188), and
converting length to wet weight with a linear model fit to data from all fish captured (n
= 506). The length-weight model was chosen using backward model selection, by
iteratively dropping the least significant predictor based on t-tests of significance,
given all other predictors in the model, until all predictors met a significance criterion
of p < 0.05 (Kutner et al. 2005). The full model predicted Loge(weight) and included
season and lake basin as fixed factors, Loge(fork length) as a covariate, and all
possible interaction factors.
Lake trout were assigned to size classes based on ontogenetic shifts in diet.
Seasonal thermal experience for each lake trout size class was estimated as the mean
temperature of the top 80 m of the water column, weighted by the proportion of that
size class captured in each 10 m depth bin in gill nets. The energy density of lake
trout (Stewart et al. 1983) and prey species were taken from the literature (Table 1).
Invertebrate prey was assumed to be 10% indigestible (Stewart et al. 1983).
Terrestrial and aquatic invertebrates (other than Mysis) were accounted for separately
in the model because their energy densities were dissimilar. Consumption estimates of
these prey types were subsequently combined for presentation because they each made
up only a small proportion of lake trout diets. Energy losses to spawning were
simulated by reducing lake trout body mass by 6.8% on October 15th of each year
(Stewart et al. 1983) once they exceeded 390 mm fork length.
Consumption estimates for each lake trout age were modeled separately and
scaled up to a population unit of 1000 lake trout ages 2-16 using the stable age
44distribution determined above. The absolute abundance of lake trout in Lake
Chelan was unknown so I estimated the relative densities of each lake trout size class
between the two lake basins using gill net catch per unit effort data and assuming that
density was proportional to catch per unit effort. Population-level consumption by
lake trout was scaled relative to lake trout catch per unit effort in each basin, stratified
by size class, to allow comparisons of the impact of lake trout predation on an areal
basis between basins.
Statistical analyses were performed using R version 2.4.0 (Ihaka and
Gentleman 1996).
Results
Catch rates of piscivores
Catch per unit of gill net effort varied substantially between lake basins for
lake trout, but not for northern pikeminnow or burbot. Lake trout catch per unit effort
(CPUE) was 7.8 times greater in Wapato Basin than in Lucerne Basin (Fig. 1).
Northern pikeminnow CPUE was similar between basins. CPUE of small (<450 mm
total length) burbot was 4.8 times greater in Lucerne Basin than in Wapato Basin,
while CPUE of larger burbot was similar among basins.
Piscivore diets and Mysis availability
Lake trout diets varied markedly between lake basins (Fig. 2). Young lake
trout ate large proportions of Mysis relicta in Lucerne Basin, but then switched to a
45mostly piscivorous diet after growing larger than 390 mm fork length. Lake trout
diets contained greater proportions of Mysis in Wapato Basin, and the ontogenetic
transition to piscivory occurred more gradually, with even the largest (>600 mm fork
length) lake trout consuming Mysis. Lake trout diets contained larger proportions of
salmonid prey in Lucerne Basin than in Wapato Basin. Within lake trout size classes,
the diet proportion of Mysis was inversely related to lake depth among sampling sites
(Fig. 3). This pattern did not reflect Mysis areal densities, which tended to increase
with increasing depth among sampling sites (Fig. 3). Among-site differences in Mysis
density were not significant after taking seasonal differences into account (ANOVA,
F4,29 = 2.14, p > 0.1).
Northern pikeminnow consumed large proportions of invertebrate prey as well
as fish in both lake basins (Fig. 4). Salmonid prey composed 24% of the diet of large
(>400 mm fork length) northern pikeminnow in Wapato Basin. Salmonids contributed
only slightly to northern pikeminnow diets in Lucerne Basin.
Burbot diets were composed of fish, Mysis, and other invertebrates (Fig. 5).
Unlike lake trout, burbot consumed similar proportions of Mysis in both lake basins.
Salmonid prey composed only 7% of the diet of large (>450 mm total length) burbot
in Wapato Basin, and salmonids did not contribute to burbot diets in Lucerne Basin.
Lake trout age, growth, and survival
Length-at-age and weight-length relationships indicated that lake trout grew
more slowly at a young age but reached a larger maximum size in Lucerne Basin than
in Wapato Basin (Table 2). Von Bertalanffy growth parameters were ω = 103 mm •
46year-1 and L∞ = 894 mm for Lucerne Basin and ω = 121 mm • year-1 and L∞ = 682
mm for Wapato Basin. Lake trout weighed less at small lengths but gained weight
faster with increasing length in Lucerne Basin than in Wapato Basin, and these
differences were significant (ANCOVA; main effect of basin, F1, 493 = 46.2, p <
0.0001; basin • Loge(FL) interaction, F1, 493 = 4.47, p < 0.05). The length-weight
relationships were best described in Lucerne Basin as:
W = 3.60 x 10-6 FL 3.18 (1)
and in Wapato Basin as:
W = 1.18 x 10-5 FL 3.01 (2)
where W is wet mass (g) and FL is fork length (mm).
Instantaneous annual mortality rates (Z) for lake trout were estimated from the
descending limb of the age-frequency distributions (ages 7-12) for each basin,
corrected for gill net size selectivity. Mortality rates were Z = 0.40 (n = 86, r2 = 0.88)
in Wapato Basin, corresponding to an annual survival rate of 67%, and Z = 0.13 (n =
37, r2 = 0.07) in Lucerne Basin, corresponding to an annual survival rate of 88%. The
Wapato Basin survival rate was used for modeling both populations because survival
curves gave poor fits to the Lucerne Basin data and to data pooled from both basins (n
= 123, r2 = 0.48).
Lake trout consumption rates
Consumption rates were estimated for lake trout population units of 1000
individuals ages 2-16 in each lake basin (Fig. 7). Lake trout in Lucerne Basin
consumed 1,949 kg of prey annually per 1000 individuals, including 311 kg of
47salmonid prey and 500 kg of Mysis. A population of 1000 lake trout in Wapato
Basin consumed 2861 kg of prey annually, including 41 kg of salmonids and 2312 kg
of Mysis. Differences in total prey consumption were largely due to growth
differences among basins, with rapid growth of smaller lake trout in Wapato Basin
leading to high consumption of Mysis and large body size of adult lake trout in
Lucerne Basin leading to high consumption of fish.
Scaled according to CPUE, the prey consumption estimates for 1000 lake trout
in Wapato Basin were compared with consumption by 128 lake trout in Lucerne
Basin. Total annual consumption was 7.6 times greater in Wapato Basin; however
lake trout consumed 1.2 times more salmonid prey in Lucerne Basin despite the
relatively low population density in that basin (Fig. 8).
Discussion
Lake trout consumed greater proportions of Mysis relicta at shallower
sampling sites, and this difference was associated with substantial increases in lake
trout density but a net decrease in simulated predation on salmonids. Lake trout
utilization of Mysis prey was much greater in the shallower Wapato Basin than in the
deeper Lucerne Basin of Lake Chelan. This was associated with a seven-fold greater
catch per unit effort of lake trout in Wapato Basin, suggesting a much greater lake
trout density there than in the deeper basin. Further, predation on Mysis in the
shallower basin was associated with rapid growth rates of young lake trout and
reduced maximum body size (L∞) of adults relative to the deeper basin. These
48patterns mirrored changes seen in the other lake trout populations after the
introduction of Mysis (Johnson et al. 2002; Stafford et al. 2002). Although both
northern pikeminnow and burbot consumed some salmonid prey, I focused on lake
trout for the remainder of the study because only lake trout consumed significant
proportions of both Mysis and salmonids.
Increases in lake trout density and juvenile growth rates could have severe
consequences for kokanee if those changes result in greater predation rates. However,
a bioenergetics exercise incorporating empirical growth, diet, and density differences
between basins showed that the dense lake trout population in Wapato Basin
consumed slightly less salmonid prey than the sparser population in Lucerne Basin.
This was due to greater proportions of salmonids in the diets of lake trout from
Lucerne Basin and the larger body size of adult lake trout in that basin. These results
suggest that Mysis have both positive and negative effects on lake trout predation
rates, with potentially offsetting impacts on kokanee. These opposing effects
apparently counteracted each other in Wapato Basin at no net detriment to the kokanee
population. I interpreted this result with caution because my analysis may have
underestimated the potentially negative impact of apparent competition for several
reasons: First, because effort in a lake trout trophy fishery is focused almost
exclusively on the Wapato Basin, the full numerical response of lake trout to Mysis
availability in that basin may be masked by fishing mortality. Second, since the two
lake basins are joined by a narrow channel, increased recruitment of lake trout in
Wapato Basin may have been diluted by dispersal into the deeper basin. Finally, all
age classes of kokanee migrated seasonally between lake basins, with densities
49generally greater in Lucerne Basin (Chapter 1). The enhanced Wapato Basin lake
trout population may pose a greater predation risk to kokanee but the reduced rate of
predation may be due to seasonal avoidance of that basin by most of the kokanee
population.
Increasing lake depth was associated with reduced lake trout predation on
Mysis, and this pattern could not be explained by patterns in areal Mysis densities,
which were similar or slightly greater at deeper sampling sites. Aside from directly
inhibiting lake trout predation on Mysis, as discussed earlier, greater lake depth might
also weaken apparent competition between Mysis and kokanee by separating those
prey species spatially. Community ecology theory predicts that prey species with
shared predators will not negatively affect each other if they occupy different habitats
such that predators must move from one habitat to the other to switch between target
prey (Holt 1984). Lake trout may be less able to exploit both the profundal Mysis and
pelagic kokanee resources in a deeper basin than in a shallower basin. This prediction
is consistent with the general pattern of diminishing trophic linkages between pelagic
and benthic habitats with increasing lake size (Schindler and Scheuerell 2002;
Vadeboncoeur et al. 2002). However, the availability of Mysis would still be expected
to boost the number of kokanee predators when Mysis and kokanee are exploited by
the predator during different life stages (White et al. 2006), as is the case for lake
trout.
This study found that lake trout consumed more Mysis in a shallower lake
basin and that this increased utilization of an abundant prey source was associated
with substantial changes in predator density and juvenile growth, both of which are
50likely to increase predation rates on kokanee on the whole basin scale (although I
did not find evidence of a net increase in predation on kokanee here). In the previous
chapter I found that zooplankton production was lower in the deep Lucerne Basin and
Mysis density and consumption rates were similar between basins, suggesting that
kokanee were most likely to be food limited in the deeper basin. However, causation
cannot be inferred from a comparison of two systems; another unnoticed process
might explain these observations. Are these general patterns? Can some of the
variability in outcomes of Mysis introductions be attributed to a depth-mediated
tradeoff between exploitation competition and apparent competition? The
consequences of Mysis establishment in three better-studied lakes are at least
superficially consistent with this hypothesis. For example, when Mysis was
introduced into Flathead Lake, MT (mean depth = 50 m) and Priest Lake, ID (mean
depth = 38 m), lake trout populations increased dramatically (Stafford et al. 2002) and
kokanee crashed without a concurrent reduction in growth (Beattie and Clancey 1991;
Bowles et al. 1991; Spencer et al. 1991). By contrast, in Lake Pend Oreille, ID (mean
depth = 164.0 m), lake trout diets contain few Mysis (Clarke et al. 2005); kokanee
body size has declined, and reductions in kokanee abundance have been linked to a
limited cladoceran food supply (Chipps and Bennett 2000; Clarke and Bennett 2002;
Clarke and Bennett 2007). The introduction of Mysis into hundreds of lakes was a
classic resource management disaster, but those lakes now offer a well-replicated
experiment with the potential to test predictions of community ecology theory. Future
synthesis studies may offer an important opportunity for hypothesis testing and
development of general principles to aid in management decisions.
51Table 6. Prey energy density (J/g wet weight) inputs used in bioenergetics simulations for lake trout in Lucerne and Wapato Basins of Lake Chelan. Simulation day 1 corresponds to May 15. Simul-ation Day
Sal-monidsa
Cyp-rinidsa
Stickle-backa
Other fisha Mysidsb
Other aquatic invertsa
Terres-trial
invertsc
1 7745 7093 6949 4514 3720 3114 4705 91 7287 7093 6949 4267 3720 3114 4705 182 7129 7093 6949 4380 2976 3114 4705 273 5211 7093 6949 4178 2976 3114 4705 365 7745 7093 6949 4514 3720 3114 4705
a(Mazur 2004), b(Lasenby 1971), c(Cummins and Wuycheck 1971)
Table 7. Thermal experience inputs used in bioenergetics simulations for lake trout in Lucerne and Wapato Basins. Simulation day 1 corresponds to May 15.
Thermal experience (C)
Simulation day
Size class
Lucerne Basin
Wapato Basin
1 / 365 180-390 8.2 5.6 1 / 365 391-520 8.3 7.0 1 / 365 521-600 8.4 6.7 1 / 365 601-910 8.7 7.6
91 180-390 8.2 11.7 91 391-520 11.6 10.7 91 521-600 9.8 9.4 91 601-910 9.8 9.4 182 180-390 7.7 7.4 182 391-520 10.8 8.8 182 521-600 10.5 9.6 182 601-910 10.7 8.4 273 180-390 6.3 5.2 273 391-520 6.3 5.2 273 521-600 6.3 5.4 273 601-910 6.3 5.2
52Table 8. Growth inputs, proportion of maximum consumption (prop. Cmax) outputs, and simulated numbers at age for bioenergetics simulations of lake trout consumption in Lucerne and Wapato Basins of Lake Chelan. Weight inputs corresponded with simulation day 1 of each year (May 15th), the approximate onset of new opercle growth past the most recent annulus. Age 17 weights were used as inputs for age 16, simulation day 365. Numbers at age were for determined for a population unit of 1000 lake trout ages 2-16 in each lake basin based on empirical mortality rate estimate of Z = 0.40.
Weight (wet, g) Prop. Cmax
Age Lucerne Wapato Lucerne Wapato
Numbers: simulated population
2 58 103 0.71 0.82 332.8 3 178 273 0.72 0.81 222.3 4 374 510 0.67 0.75 148.5 5 643 791 0.40 0.68 99.2 6 975 1094 0.41 0.68 66.3 7 1355 1401 0.40 0.68 44.3 8 1770 1698 0.38 0.57 29.6 9 2206 1978 0.39 0.54 19.8
10 2652 2234 0.41 0.54 13.2 11 3098 2465 0.41 0.51 8.8 12 3537 2671 0.40 0.42 5.9 13 3962 2851 0.40 0.41 3.9 14 4369 3009 0.40 0.41 2.6 15 4755 3145 0.40 0.40 1.8 16 5117 3262 0.40 0.40 1.2 17 5456 3363
53
Figure 9. Catch per unit effort of lake trout, northern pikeminnow, and burbot in the two basins of Lake Chelan. One unit of effort was defined as one gang of gill nets (described in the methods) set once during each of four seasonal sampling periods. Lake trout catch was corrected for gill net size selectivity . Fish were assigned to size classes based on fork length (lake trout and northern pikeminnow) or total length (burbot).
54
Figure 10. Annual diet composition of four size classes of lake trout (calculated as proportion of diet by wet mass). Sample sizes for non-empty stomachs are given in parentheses.
55
Figure 11. Areal density of Mysis relicta and proportional contribution of Mysis to lake trout diets (by mass) across a depth gradient in Lake Chelan. Mysis density was sampled at night with vertical hauls of a mysid net. Lake trout were sampled with gill nets adjacent to Mysis sampling sites, with gill nets set at the same standardized depths at all sampling sites. The independent variable indicates the maximum depth of the shortest lake cross-section passing through the sampling site, such that greater values indicate deeper parts of the lake.
56
Figure 12. Annual diet composition of three size classes of northern pikeminnow (calculated as proportion of diet by wet mass). Sample sizes for non-empty stomachs are given in parentheses.
57
Figure 13. Annual diet composition of two size classes of burbot (calculated as proportion of diet by wet mass). Sample sizes for non-empty stomachs are given in parentheses.
58
Figure 14. Age-frequency distributions for lake trout captured in gill nets in the two basins of Lake Chelan, corrected for gill net size selectivity.
59
Figure 15. Annual consumption by a lake trout population unit of 1000 fish age 2-16 yr in each basin of Lake Chelan. Consumption estimates are based on bioenergetics modeling of individual consumption scaled up to the population level based on an empirically derived mortality rate.
60
Figure 16. Annual consumption of fish prey by lake trout in Wapato and Lucerne Basins, scaled to the relative density of lake trout in those basins. Wapato Basin values represent consumption by a population unit of 1000 fish ages 2-16 yr. Lucerne Basin values represent consumption by a population unit of 128 fish age 2-16 yr such that the numbers in each size class are in proportion to the catch per unit effort of that size class in Lucerne vs. Wapato Basin.
61Notes to Chapter II:
Beattie, W.D., and Clancey, P.T. 1991. Effects of Mysis relicta on the zooplankton community and kokanee population of Flathead Lake, Montana. American Fisheries Society Symposium, 9: 39-48.
Bowles, E.C., Rieman, B.E., Mauser, G.R., and Bennett, D.H. 1991. Effects of introductions of Mysis relicta on fisheries in northern Idaho. American Fisheries Society Symposium, 9: 65-74.
Brown, L.G. 1984. Lake Chelan Fishery Investigations. Chelan County Public Utility District No. 1 and Washington Dept. of Game.
Chase, J.M., Abrams, P.A., Grover, J.P., Diehl, S., Chesson, P., Holt, R.D., Richards, S.A., Nisbet, R.M., and Case, T.J. 2002. The interaction between predation and competition: a review and synthesis. Ecology Letters, 5(2): 302-315.
Chipps, S.R., and Bennett, D.H. 2000. Zooplanktivory and nutrient regeneration by invertebrate (Mysis relicta) and vertebrate (Oncorhynchus nerka) planktivores: Implications for trophic interactions in oligotrophic lakes. Transactions of the American Fisheries Society, 129(2): 569-583.
Clarke, L.R., and Bennett, D.H. 2002. A net-pen experiment to evaluate kokanee growth rates in autumn in an oligotrophic lake with Mysis relicta. Transactions of the American Fisheries Society, 131(6): 1061-1069.
Clarke, L.R., and Bennett, D.H. 2007. Zooplankton production and planktivore consumption in lake Pend Oreille, Idaho. Northwest Science, 81(3): 215-223.
Clarke, L.R., Vidergar, D.T., and Bennett, D.H. 2005. Stable isotopes and gut content show diet overlap among native and introduced piscivores in a large oligotrophic lake. Ecology of Freshwater Fish, 14(3): 267-277.
Courchamp, F., Langlais, M., and Sugihara, G. 2000. Rabbits killing birds: modelling the hyperpredation process. Journal of Animal Ecology, 69(1): 154-164.
Crooks, J.A. 2002. Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos, 97(2): 153-166.
Cummins, K.W., and Wuycheck, J.C. 1971. Caloric equivalents for investigations in ecological energetics. Mitteilungen internationale Vereinigung für theoretische und angewandte Limnologie, 18.
Duke Engineering and Services (DES) 2000. Lake Chelan Fisheries Investigation, Lake Chelan Hydroelectric Project No. 637., Prepared for Public Utility District No. 1 of Chelan County, Bellingham, WA.
Hagen, J.E. 1997. An Evaluation of a Trout Fishery Enhancement Program in Lake Chelan. Master's thesis, University of Washington, Seattle.
Hansen, M.J., Madenjian, C.P., Selgeby, J.H., and Helser, T.E. 1997. Gillnet selectivity for lake trout (Salvelinus namaycush) in Lake Superior. Canadian Journal of Fisheries and Aquatic Sciences, 54(11): 2483-2490.
Hanson, P.C., Johnson, T.B., Schindler, D.E., and Kitchell, J.F. 1997. Fish Bioenergetics 3.0. University of Wisconsin Sea Grant Inst., Madison, Wis.
Holt, R.D. 1977. Predation, apparent competition, and the structure of prey communities. Theoretical Population Biology, 12(2): 197-229.
62Holt, R.D. 1984. Spatial heterogeneity, indirect interactions, and the coexistence of
prey species. American Naturalist, 124(3): 377-406. Holt, R.D., and Lawton, J.H. 1994. The ecological consequences of shared natural
enemies. Annual Review of Ecology and Systematics, 25: 495-520. Ihaka, R., and Gentleman, R. 1996. R: A language for data analysis and graphics.
Journal of Computational and Graphical Statistics, 5(3): 299-314. Johnson, B.M., Martinez, P.J., and Stockwell, J.D. 2002. Tracking trophic interactions
in coldwater reservoirs using naturally occurring stable isotopes. Transactions of the American Fisheries Society, 131(1): 1-13.
Juday, C., and Birge, E.A. 1927. Pontoporeia and Mysis in Wisconsin lakes. Ecology, 8: 445-452.
Kendra, W., and Singleton, L.R. 1987. Morphometry of Lake Chelan. Water Quality Investigations Section, Washington State Dept. of Ecology.
Kutner, M.H., Nachtschiem, C.J., Neter, J., and Li, W. 2005. Applied Linear Statistical Models. McGraw-Hill Irwin, Boston.
Lasenby, D.C. 1971. The ecology of Mysis relicta in an arctic and a temperate lake. Doctoral dissertation, University of Toronto, Toronto.
Lasenby, D.C., Northcote, T.G., and Furst, M. 1986. Theory, practice, and effects of Mysis relicta introductions to North American and Scandinavian lakes. Canadian Journal of Fisheries and Aquatic Sciences, 43(6): 1277-1284.
Levy, D.A. 1991. Acoustic analysis of diel vertical migration behavior of Mysis relicta and kokanee (Oncorhynchus nerka) within Okanagan Lake, British Columbia. Canadian Journal of Fisheries and Aquatic Sciences, 48(1): 67-72.
Lodge, D.M. 1993. Biological invasions: Lessons for ecology. Trends in Ecology and Evolution, 8(4): 133-137.
Martinez, P.J., and Bergersen, E.P. 1991. Interactions of zooplankton, Mysis relicta, and kokanees in Lake Granby, Colorado. American Fisheries Society Symposium, 9: 49–64.
Mazur, M.M. 2004. Linking Visual Foraging with Temporal Prey Distributions to Model Trophic Interactions in Lake Washington. Doctoral dissertation, University of Washington, Seattle.
Morgan, M.D., Threlkeld, S.T., and Goldman, C.R. 1978. Impact of the introduction of kokanee (Oncorhynchus nerka) and opossum shrimp (Mysis relicta) on a subalpine lake. Journal of the Fisheries Research Board of Canada, 35(12): 1572-1579.
Nesler, T.P., and Bergersen, E.P. 1991. Mysids in fisheries: hard lessons from headlong introductions. American Fisheries Society Symposium.
Noonburg, E.G., and Byers, J.E. 2005. More harm than good: When invader vulnerability to predators enhances impact on native species. Ecology, 86(10): 2555-2560.
Pelletier, G., Patmont, C.R., Welch, E.B., Bandon, D., and Ebbesmeyer, C.C. 1989. Lake Chelan Water Quality Assessment, Washington Department of Ecology, Olympia, WA.
63Ruzycki, J.R., Beauchamp, D.A., and Yule, D.L. 2003. Effects of introduced lake
trout on native cutthroat trout in Yellowstone Lake. Ecological Applications, 13(1): 23-37.
Schindler, D.E., and Scheuerell, M.D. 2002. Habitat coupling in lake ecosystems. Oikos, 98(2): 177-189.
Schoolcraft, J.M., and Mosey, T.R. 2006. Lake Chelan kokanee spawning ground surveys 2005, Chelan County Public Utility District, Wenatchee, WA.
Sharp, D., and Bernard, D.R. 1988. Precision of estimated ages of lake trout from five calcified structures. North American Journal of Fisheries Management, 8: 367-372.
Simberloff, D., and Von Holle, B. 1999. Positive interactions of nonindigenous species: Invasional meltdown? Biological Invasions, 1(1): 21-32.
Spencer, C.N., McClelland, B.R., and Stanford, J.A. 1991. Shrimp stocking, salmon collapse, and eagle displacement. Bioscience, 41(1): 14-21.
Spencer, C.N., Potter, D.S., Bukantis, R.T., and Stanford, J.A. 1999. Impact of predation by Mysis relicta on zooplankton in Flathead Lake, Montana, USA. Journal of Plankton Research, 21(1): 51-64.
Stafford, C.P., Stanford, J.A., Hauer, F.R., and Brothers, E.B. 2002. Changes in lake trout growth associated with Mysis relicta establishment: A retrospective analysis using otoliths. Transactions of the American Fisheries Society, 131(5): 994-1003.
Stewart, D.J., Weininger, D., Rottiers, D.V., and Edsall, T.A. 1983. An energetics model for lake trout (Salvelinus namaycush): application to the Lake Michigan population. Canadian Journal of Fisheries and Aquatic Sciences, 40: 681-698.
Vadeboncoeur, Y., Vander Zanden, M.J., and Lodge, D.M. 2002. Putting the lake back together: Reintegrating benthic pathways into lake food web models. Bioscience, 52(1): 44-54.
Vander Zanden, M.J., Olden, J.D., Thorne, J.H., and Mandrak, N.E. 2004. Predicting occurrences and impacts of smallmouth bass introductions in north temperate lakes. Ecological Applications, 14(1): 132-148.
Vander Zanden, M.J., Chandra, S., Allen, B.C., Reuter, J.E., and Goldman, C.R. 2003. Historical food web structure and restoration of native aquatic communities in the Lake Tahoe (California-Nevada) Basin. Ecosystems, 6(3): 274-288.
Wetzel, R.G. 1983. Limnology. Saunders, Toronto, Ont. White, E.M., Wilson, J.C., and Clarke, A.R. 2006. Biotic indirect effects: a neglected
concept in invasion biology. Diversity and Distributions, 12(4): 443-455. Wydoski, R.S., and Whitney, R.R. 2003. Inland Fishes of Washington. University of
Washington Press.
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APPENDIX A: ADDITIONAL TABLES FOR CHAPTER II
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