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Dispersal and reproductive success of Chinook (Oncorhynchus tshawytscha)and coho (O. kisutch) salmon colonizing newly accessible habitat
Joseph H. Anderson
A dissertationsubmitted in partial fulfillment of the
requirements for the degree of
Doctor of Philosophy
University of Washington
2011
Program Authorized to Offer Degree:Aquatic and Fishery Sciences
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University of Washington
Graduate School
This is to certify that I have examined this copy of a doctoral dissertation by
Joseph H. Anderson
and have found that it is complete and satisfactory in all respects,
and that any and all revisions required by the finalexamining committee have been made.
Chair of the Supervisory Committee:
__________________________________________________
Thomas P. Quinn
Reading committee:
__________________________________________________
Thomas P. Quinn
__________________________________________________Kerry-Ann Naish
__________________________________________________
Julian D. Olden
Date:____________________________________
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In presenting this dissertation in partial fulfillment of the requirements
for the doctoral degree at the University of Washington, I agree that theLibrary shall make its copies freely available for inspection. I further
agree that extensive copying of the dissertation is allowable only for
scholarly purposes, consistent with fair use as prescribed in the U.S.Copyright Law. Requests for copying or reproduction of this dissertation
may be referred to ProQuest Information and Learning, 300 North Zeeb
Road, Ann Arbor, MI 48106-1346, 1-800-521-0600, to whom the authorhas granted the right to reproduce and sell (a) copies of the manuscript in
microform and/or (b) printed copies of the manuscript made from
microform.
Signature __________________________
Date ______________________________
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University of Washington
Abstract
Dispersal and reproductive success of Chinook (Oncorhynchus tshawytscha)and coho (O. kisutch) salmon colonizing newly accessible habitat
Joseph H. Anderson
Chair of the Supervisory Committee:
Professor Thomas P. QuinnSchool of Aquatic and Fishery Sciences
Although dam removal and fish passage projects offer extraordinary potential to
conserve threatened Pacific salmon (Oncorhynchusspp.) and other migratory fishes, only
rarely has the biological response to these restoration activities been evaluated. Modification
of Landsburg Diversion Dam on the Cedar River, WA, USA in fall 2003 provided a unique
opportunity to investigate the process of colonization as coho (O. kisutch) and Chinook (O.
tshawytscha) salmon were granted access to over 33 km of spawning and rearing habitat.
Adult salmon were sampled as they bypassed the dam, and total counts of both species
tended to increase from 2003 to 2009, although more rapidly for coho salmon. DNA-based
parentage identified salmon from the second generation of colonization as recruits if they
were produced above the dam or strays if they were produced elsewhere. In 2008 and
2009, coho salmon recruits vastly outnumbered the strays, but strays were more abundant
than recruits for Chinook salmon. Chinook salmon strays included a much larger proportion
of hatchery origin salmon than coho salmon, despite the absence of any hatchery on the
Cedar River for either species. Productivity, calculated as the ratio of recruits sampled at the
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dam to spawners, exceeded replacement in all four coho salmon cohorts but only one of three
Chinook salmon cohorts. Parentage analysis was also used to investigate individual
reproductive success and the traits of the most successful salmon. Reproductive success of
male hatchery Chinook salmon was 70 90 % that of natural origin fish across three cohorts,
but there was no consistent trend for the females. In both sexes of coho salmon, larger fish
produced more adult offspring for each of three cohorts, and early breeders produced more
offspring in 2003, but not in 2004 and 2005 when fish spawning during the middle of the
season were favored. In addition, there was evidence for widespread dispersal within the
new habitat by stream-rearing juvenile coho salmon, most notably immigration into a
tributary of the Cedar River. Overall, these results demonstrated that reconnecting
previously isolated habitats is an effective conservation strategy for Pacific salmon.
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i
Page
List of Figures ........................................................................................................................... iiList of Tables ........................................................................................................................... iii
General introduction ..................................................................................................................1Chapter 1: Dispersal and productivity of Chinook and coho salmon colonizing newly
accessible habitat .......................................................................................................................5Abstract ..................................................................................................................................5Introduction ............................................................................................................................6Methods ..................................................................................................................................9Results ..................................................................................................................................15Discussion ............................................................................................................................19Appendix ..............................................................................................................................37
Chapter 2: Demographic and genetic consequences of permitting captively bred Chinook
salmon to colonize following modification of an impassable dam ..........................................39
Abstract ................................................................................................................................39Introduction ..........................................................................................................................40Methods ................................................................................................................................42Results ..................................................................................................................................50Discussion ............................................................................................................................52
Chapter 3: Selection on breeding date and body size in colonizing coho salmon ...................69Abstract ................................................................................................................................69Introduction ..........................................................................................................................70Methods ................................................................................................................................73Results ..................................................................................................................................79Discussion ............................................................................................................................83
Chapter 4: Dispersal of colonizing juvenile coho salmon: tributary immigration and the
influence of emergence date and kin association ...................................................................100Abstract ..............................................................................................................................100Introduction ........................................................................................................................101Methods ..............................................................................................................................105Results ................................................................................................................................109Discussion ..........................................................................................................................114
Summary ................................................................................................................................132References ..............................................................................................................................136
TABLE OF CONTENTS
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LIST OF FIGURES
Page
1-1: Map of Cedar River and Lake Washington basin ............................................................321-3: Parentage LOD distributions ............................................................................................33
1-3: Origin of Chinook and coho salmon at the dam ...............................................................341-4: Strays and potential source populations ...........................................................................351-5: Chinook vs. coho hatchery straying .................................................................................362-1: Map of Cedar River and Lake Washington basin ............................................................662-2: Reproductive success histograms .....................................................................................672-3: Indices of genetic diversity ...............................................................................................683-1: Coho salmon reproductive success histograms ................................................................973-2: Coho salmon cubic splines ...............................................................................................983-3: Coho salmon maternal arrival date vs. juvenile offspring body size ...............................994-1: Map of Cedar River above Landsburg Diversion Dam ..................................................126 4-2: Spatial distribution of brood year 2003 maternal families .............................................127
4-3: Spatial distribution of brood year 2004 maternal families .............................................1284-4: Rock Creek duration of residence vs. immigration date ................................................1294-5: Relationship between juvenile coho dispersal and maternal migration date ..................1304-6: Juvenile coho salmon maternal migration date by Rock Creek capture reach ...............131
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LIST OF TABLES
Page
1-1: Counts of adult Chinook and coho salmon sampled at the dam.......................................29 1-2: Productivity of Chinook and coho salmon .......................................................................30
1-3: Origin of below dam Chinook salmon samples ...............................................................312-1: Chinook salmon microsatellite DNA markers .................................................................612-2: Counts of adult Chinook salmon ......................................................................................622-3: Chinook salmon reproductive success mean and variance ...............................................632-4: Genetic differentiaion and effective population size of Chinook salmon ........................642-5: Effective number of Chinook salmon breeders ................................................................653-1: Coho salmon microsatellite DNA markers.......................................................................90 3-2: Body size, breeding date and reproductive success of coho salmon ................................913-3: Adult coho salmon population genetics ...........................................................................923-4: Juvenile coho salmon population genetics .......................................................................943-5: Coho salmon parentage assignments ................................................................................95
3-6: Coho salmon selection gradients ......................................................................................964-1: Maternal families of juvenile coho salmon ....................................................................1224-2: Densities of juvenile coho salmon in Rock Creek..........................................................123 4-3: Movement into Rock Creek by juvneile coho salmon ...................................................1244-4: Juvenile coho salmon kin asssociation ...........................................................................125
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ACKNOWLEDGEMENTS
First and foremost, I would like to thank Paul Faulds and John McDowell from Seattle Public
Utilities for sampling all the adult Chinook and coho salmon at the dam. Their meticulous
attention to detail on many cold wet winter days made my dissertation possible. A number ofother folks at Seattle Public Utilities provided logistical and intellectual support: Karl Burton,
Dwayne Paige, David Chapin, Rand Little, Heidy Barnett, and Bruce Bachen. Their
thoughtful questions have helped me focus on the key conservation issues and present resultsthat are relevant and understandable to anybody interested in salmon.
I also received field help from many people in my pursuit of juvenile coho salmon in thestream. Andy Kingham and Dylan Galloway were always enthusiastic in chasing salmon
within the Cedar River, which sometimes included tough marches through overgrown
windfall. The NOAA watershed program, particularly Todd Bennett, Ranae Holland, RyanKlett, Thomas Buehrens, Jeremy Cram, Martin Liermann, and Kris Kloehn, sampled juvenile
coho from Rock Creek efficiently and were kind enough to clip many fins for me.
Countless long hours were spent in the laboratory over the course of my dissertation, and Icould not have processed the samples without the extensive help of Will Atlas and Melissa
Baird. Will spent two years pipetting and quickly demonstrated total independence. Melissa
and her predecessor as lab manager, Lyndsay Newton, kept the equipment running and thesupplies in stock despite the inevitable machine malfunction.
No research is possible without funding, and I received significant support from SeattlePublic Utilities, Washington Sea Grant, and the H. Mason Keeler Endowment.
I have been surrounded by top quality students during my time in graduate school, and their
critique improved the quality of my work immensely. In particular, Quinn lab meetings
provided insightful and friendly critique, so a big thank you goes to members of the Quinngroup, both past and present. Many former students, particularly Stephanie Carlson and Jon
Moore, were an inspiration and raised my expectations of what I could accomplish.
I would also like to thank my committee for their feedback on my work. Despite busyschedules, Kerry Naish, Julian Olden, Peter Kiffney and John Marzluff made themselves
available and provided succinct, erudite feedback on my work.
I am enormously indebted to two mentors I consider unofficial committee members. Todd
Seamons was always willing to sit down and talk in excruciating detail about genetic
analysis, and these discussions were absolutely crucial to my dissertation. Similarly, chatswith George Pess helped keep an ecological perspective on my work and its real world
relevance to salmon conservation. Thanks guys!
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I could not imagine having a better advisor than Tom Quinn. Toms contagious enthusiasm
for my research and salmon ecology in general has driven me to challenge myself. I workedhard because I wanted to earn his respect, and he provided intellectual and financial support
throughout my time in school. It is clear that Toms top priority is the professionally
development of his students, and I will use Toms approach to advising as a model in my
own future endeavors.
One of the biggest lessons I have learned over the past seven and half years is that balance in
life is crucial to my happiness. The friends I have made while at the University ofWashington provided relief from the stresses of school and have taught me life lessons
outside of academics. Whether it was fly fishing on the Queets, sailing in Puget Sound or
cross-country skiing through the Cascades, outdoor adventures with my friends helped mekeep my perspective on the big picture. Eric Ward and Kristin Marshall, Chris and Courtney
Kenaley, Keith and Lauren Denton, and Ross Peterson were always down to have a beer and
unwind from work life.
Quite simply, my family shaped the person I am today and so I want to thank my parents Philand Donna Anderson, and my sister Leslie Anderson. From an early age, I realized that I
liked learning and my family has given me every opportunity to succeed in school. Familyfishing and camping trips across the Rockies unquestionably provided the experiences that
inspired a career in fisheries science.
Finally, I want to thank my wife Jennie for her unwavering support and love. When the
dissertation started to overwhelm me in the final few months, Jennie would not let me get
discouraged and got my mind away from work. I finally did it, baby!
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General introduction
Habitat loss has attracted the attention of conservation biologists for decades because
it has numerous deleterious demographic, ecological and genetic consequences for plants and
animals. This problem is particularly acute for migratory animals that require intact corridors
for movements between breeding and feeding areas; interruption of such corridors causes
local extirpation. In aquatic systems, dams have become a widespread feature of the
hydrologic landscape over the last century, and dramatically reduced the habitat accessible to
migratory freshwater fish.
Dams have an enormous impact on the conservation status of Pacific salmon
(Oncorhynchus spp.) in the Pacific Northwest, where four of the five species of Pacific
salmon plus steelhead trout (O. mykiss) have population segments listed under the
Endangered Species Act. Although salmon face many threats, lost habitat due to stream
blockages is one of the most severe. As such, there is a growing movement to remove or
circumvent dams and enable salmon to reclaim access to spawning and rearing areas.
Indeed, the goal of enhancing depleted salmon runs has galvanized several major dam
removal projects on the Sandy (OR), Rogue (OR), and Elwha (WA) rivers. Despite the
tremendous potential afforded by dam removal and fish passage for restoring migratory
fishes in general and salmon in particular, the science of barrier removal is still in its infancy
because the biological response to such projects has rarely been monitored.
My dissertation takes advantage of a unique opportunity to investigate the process of
salmon colonization following restoration of habitat connectivity. In fall 2003, modification
of Landsburg Diversion Dam on the Cedar River, WA, USA granted coho (O. kisutch) and
Chinook (O. tshawytscha) salmon access to 33 km of spawning and rearing habitat from
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which they had been excluded for over a century. Salmon entered the new habitat if they
reached fish passage structures within the dam complex on their own volition; there was no
transplanting or artificial supplementation. The overall goal of my dissertation is to
understand the behavior and ecology of salmon recolonizing this newly accessible habitat,
and I have focused on two themes. First, I evaluated dispersal by colonizing salmon, in
terms of adult salmon entering the new habitat from some other source population and
movements by stream-rearing juvenile coho salmon within the new habitat. Second, I
measured the reproductive success of colonizing salmon, in terms of both the population
productivity of the initial colonists and the traits of the most successful individual salmon.
These themes of dispersal and reproductive success are addressed in four discrete chapters.
Chapter 1 tackles the most crucial conservation questions, namely dispersal into the
new habitat by adult salmon and the productivity of the initial colonists. Salmon are famous
for homing to their natal site during their return migration from the ocean, and strict
philopatry might preclude dispersal into newly accessible habitats. However, some salmon
do not return to their natal site, and it is these strays that permitted species-wide range
expansions following retreat of glaciers that covered much of current day salmon habitat in
Washington, British Columbia and southern Alaska. Chapter 1 quantifies the number of
salmon that dispersed into the habitat made accessible by the fish ladder on the Cedar River.
Furthermore, for successful colonization, any initial colonists must produce offspring that
return to the new habitat to spawn themselves. Thus the second objective of Chapter 1 was
to determine if the productivity of the initial colonists exceeded replacement such that the
colonizing populations were self-sustaining.
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Chapter 2 addresses role the captively bred salmon during recolonization, and this is
another important conservation question for management of recolonizing populations.
Hatcheries are pervasive throughout the Pacific Northwest, so managers planning
reintroductions will likely have access to artificial supplementation facilities. Although
hatchery salmon can provide an immediate demographic boost to recolonizing populations,
artificial propagation might reduce the fitness of salmon for life in the wild or decrease
genetic diversity. On the Cedar River, there was no direct transplanting or hatchery releases,
but hatchery-origin salmon were permitted to access the new habitat if they reached the dam
under their own volition. In order to evaluate the consequences of permitting the hatchery
Chinook salmon to colonize, we compared their reproductive success and genetic diversity to
natural origin salmon.
Chapter 3 focuses on the influence of two quantitative traits, body size and breeding
date, on individual reproductive success in coho salmon. In general, sexual selection tends to
favor traits in males that increase their access to receptive mates and traits in females that aid
in competition for breeding resources required for nest sites. All else being equal, larger
salmon tend to be more successful. Large males can dominate competitors in contests for
mates; large females tend to win competitions for nest sites and produce more numerous
offspring. The influence of breeding date is more difficult to predict, particularly in river
systems where extreme fluctuations in discharge and can affect breeding success and
offspring survival. Although early breeding salmon are often favored because their offspring
emerge early and gain growth advantages, early breeding may also increase the exposure of
embryos and juveniles to unfavorable environmental conditions and predators.
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In the fourth chapter, I evaluated the dispersal of stream-rearing juvenile coho
salmon. In Puget Sound, coho salmon typically rear for one year in freshwater prior to
seaward migration, and movements during this period can influence patterns of density
dependent survival, and hence, population dynamics. Breeding densities are typically low
during colonization, so there is likely to be ample scope for dispersal into unoccupied
habitats for mobile organisms. The analysis of dispersal evaluated the spatial distribution of
maternal families that emerged from the same nest, and patterns of immigration into a
tributary of the Cedar River where juveniles were common but adult spawning was rare. In
addition, Chapter 4 assessed the influence of emergence date and kinship on juvenile
dispersal.
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Chapter 1: Dispersal and productivity of Chinook (Oncorhynchus tshawytscha) and
coho (O. kisutch) salmon colonizing newly accessible habitat
Abstract
Although dam removal and fish passage projects offer extraordinary potential to
conserve threatened Pacific salmon (Oncorhynchusspp.) and other migratory fishes, only
rarely has the biological response to these restoration activities been evaluated. In this study,
we quantified two processes crucial to successful recolonization: the number of salmon
dispersing into the newly accessible habitat, and productivity of the initial colonists.
Research was conducted on the Cedar River, WA, USA, where modification of Landsburg
Diversion Dam (river km 35) in fall 2003, gave coho (O. kisutch) and Chinook (O.
tshawytscha) salmon access to over 33 km of spawning and rearing habitat from which they
had been excluded for over a century. We used DNA-based parentage analysis to identify
salmon from the second generation of colonization as recruits if they were produced above
the dam or strays dispersing into the new habitat if they were produced elsewhere. For
both species, strays were present in all years (mean SD; Chinook 114.4 82.6; coho: 97.1
54.2). Chinook salmon strays were more numerous in years of greater abundance below
the dam and included a much larger proportion of hatchery origin salmon (28 69 % vs. 2
11 %) than did coho salmon, despite the absence of any hatchery on the Cedar River.
Productivity, calculated as the ratio of recruits sampled at the dam to spawners, exceeded
replacement in all four coho salmon cohorts but only one of three Chinook salmon cohorts.
However, DNA samples from Chinook salmon that spawned in the Cedar River below the
dam indicated that some were produced by parents that spawned above the dam; extrapolated
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abundance estimates based on these samples increased productivity of all three the colonizing
Chinook salmon cohorts above replacement. Neither of these estimates accounted for
salmon that survived to maturity but were caught in fisheries, and inclusion of these fish
would have further increased the estimates of natural productivity. Overall, these results
demonstrated that reconnecting previously isolated habitats is an effective conservation
strategy for Pacific salmon.
Introduction
Habitat loss is a primary threat to biodiversity, as it can cause population extirpations
and species extinctions (Wilcove et al. 1998). Movement barriers that block access to areas
required for reproduction, rearing, or feeding often cause the loss of habitat that would
otherwise be suitable. Indeed, reconnection of previously isolated high quality habitats
offers a promising conservation strategy to reintroduce animals to areas from which they had
been extirpated. In such cases, the hope is that animals will colonize the new area and
establish a persistent population.
Simply increasing habitat connectivity does not guarantee success, however, and
resource managers could opt for an active or passive role in recolonization. Initially, the
densities of a reintroduced species are likely to be quite low, and successful colonization may
be hindered by Allee effects, defined as a positive relationship between population
abundance and growth rate. Under a strong Allee effect, a population must cross some
critical abundance threshold or it will fail to establish (Deredec and Courchamp 2007; Taylor
and Hastings 2005). Active translocation has become a primary means of conservation by
ensuring movement of a minimum number of colonists into unoccupied habitats, and success
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is typically defined as a having established a self-sustaining population (Griffith et al.
1989; Wolf et al. 1996). Alternatively, resource managers may opt for passive recolonization
(i.e., no translocation or transplanting) for mobile species, and this option has received less
attention in the reintroduction literature (Seddon et al. 2007).
A passive approach to recolonization following restoration of habitat connectivity
requires natural dispersal into the newly accessible habitat without human assistance.
Although passive approaches may therefore take longer for population establishment relative
to translocation, this strategy would not compromise key evolutionary processes such as
natural and sexual selection. However, for species such as Pacific salmon (Oncorhynchus
ssp.), strict philopatry might preclude natural dispersal into newly accessible habitats.
Indeed, Young (1999) advocated an active role for management in salmon recolonization,
suggesting that they should be translocated into suitable but unoccupied habitats to hasten
the recovery of Pacific salmon in an ecologically realistic way. However, even in species
famous for homing, a measurable proportion of the population does not return to the natal
site (salmon: Quinn 1993; passerine birds: Weatherhead and Forbes 1994). Thus populations
near the newly accessible habitat could provide a source of colonists. The number of
colonists (termed strays in salmon lexicon) entering a new habitat is likely to depend on
the demographics and proximity of the source population. In the first generation, a
colonizing population will be composed entirely of strays, but these initial colonists must
produce offspring that successfully return to the new habitat to spawn themselves for long
term sustainability.
Pacific salmon have suffered widespread extinctions and declines in abundance, and
many Evolutionary Significant Units are listed under the U.S. Endangered Species Act
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(Gustafson et al. 2007). Although salmon face many threats, the loss of spawning and
rearing habitat due to dams and other migration barriers is one of the most significant
(National Research Council 1996; Nehlsen et al. 1991). Barrier removal or circumvention
has become a primary means of restoring salmon and other anadromous fish populations
(Bryant et al. 1999; Burdick and Hightower 2006; Kiffney et al. 2009). Despite the
significant expense of these and other stream restoration actions, only rarely has the
biological response to such projects been evaluated (Bernhardt et al. 2005; Katz et al. 2007;
Roni et al. 2008).
In this paper, we used molecular genetics to measure the dispersal and productivity of
Chinook and coho salmon recolonizing spawning and rearing habitat above Landsburg
Diversion Dam on Cedar River, Washington (Fig. 1-1). Following construction of a fish
ladder, a passive recolonization strategy was adopted, and salmon were allowed volitional
access to the new habitat. Both species had pre-existing source populations below the dam
(located at river kilometer 35), and thus the colonization process is best described as the
expansion of an established population into a new area. DNA-based parentage analysis
identified salmon from the second generation of colonization as recruits if they were
produced above the dam or strays dispersing into the new habitat if they were produced
elsewhere. Our first objective was to assess dispersal by quantifying the total number of
strays and determine if their abundance was correlated with that of proximate potential
source populations. Our second objective was to estimate the productivity of the colonizing
populations to determine whether they are self-sustaining.
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Methods
Study site and sampling protocols
The Cedar River flows west from the Cascade mountain range into the south end of
Lake Washington, which is connected to Puget Sound via a man-made shipping canal
through Seattle, Washington, U.S.A. (Fig. 1-1). Landsburg Diversion Dam, located at river
kilometer 35.1, blocked fish migration from 1901 to 2003. In fall 2003, fish passage
structures added to the dam enabled salmon to recolonize approximately 33 km of habitat
above the dam on their own volition. There was no active transplantation or hatchery
supplementation but the modifications of the dam allowed us to sample the fish before they
entered the habitat above the dam.
Naturally spawning populations of both salmon species are found immediately below
the dam. Chinook salmon abundance below the dam was assessed by counts of spawning
nests (redds; K. Burton, Seattle Public Utilities, unpublished data) but no assessments were
made for coho salmon. Hatchery fish of both species are produced at two facilities in the
basin: a large hatchery run by the Washington Department of Fish and Wildlife at Issaquah
Creek, and a smaller hatchery run by the University of Washington at Portage Bay (Fig. 1-1).
The numbers of salmon returning to the Issaquah hatchery were obtained from Washington
Department of Fish and Wildlife Hatchery Escapement Reports (accessible
wdfw.wa.gov/hatcheries/escapement) and the numbers of UW hatchery salmon were
provided by the hatchery manager (J. Wittouck, personal communication). In the Cedar
River, hatchery origin fish routinely comprise a significant portion of the Chinook salmon
population spawning below the dam (K. Burton, Seattle Public Utilities, unpublished
manuscript).
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Adult Chinook and coho salmon were sampled as they ascended the fish ladder and
bypassed the dam. Each sampled fish was identified by species and sex, and we took a small
tissue sample for subsequent DNA analysis. Hatchery fish were identified by a missing
adipose fin. For the vast majority of the migration period, the fish ladder was configured
such that adult salmon could not bypass the dam without being handled by dam staff,
providing us with a nearly complete census of all colonists. A small number of salmon
migrated upriver unsampled before (Chinook salmon) or after (coho salmon) the ladder was
configured in this fashion. However, an automatic camera system (described by Shardlow
and Hyatt 2004) provided an estimate of the number of unsampled fish during these periods.
Digital photographs and infrared length measurements were used to distinguish salmon from
sympatric rainbow trout, cutthroat trout, and sockeye salmon. The camera records indicated
that > 98% of the Chinook salmon were sampled each year, and the sampling fractions for
coho salmon were: 100 % in 2003 and 2004, 96% in 2005, 92% in 2006, 95% in 2007, 85%
in 2008, and 98 % in 2009.
Samples were also collected from locations other than the dam. In 2006 2009, we
obtained scale and, in some cases, tissue samples from adult Chinook salmon carcasses in the
Cedar River below the dam from surveys conducted jointly by the Washington Department
of Fish and Wildlife, King County, and Seattle Public Utilities. Each of these adults was
aged via scale analysis, and we only genotyped individuals that could have been produced
above the dam (i.e., return year minus age 2003 and not hatchery marked). Tissues were
also collected from juvenile coho salmon produced by adults spawning 2003 2007 from
sites above the dam to test the accuracy of our parentage-based methods to classify adults as
either recruits or strays (see below for details).
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Identification of recruits and trays
Samples were genotyped at 10 microsatellite loci using previously described
protocols (Chapter 2, Chapter 3). We included all samples that had been genotyped at 7
loci and the vast majority of these were genotyped at nine or ten loci (Chinook = 93.0 %,
coho = 89.9 %). We were unable to genotype a small number of samples (N = 5 Chinook
and N = 11 coho salmon) collected at the dam, and these were excluded from further
analysis. Genotyping error rate had previously been assessed at 0.56 % for Chinook and 0.66
% for coho salmon (Chapter 2 and 3).
We used Cervus version 3.0.3 (Kalinowski et al. 2007; Marshall et al. 1998), which
assigns parentage based on a likelihood ratio (or LOD) score, for all parentage assignments.
The pool of potential offspring was based on well-known age at maturity patterns of each
species (Quinn 2005), with the constraint that 2009 was the final year of sampling offspring.
For each parental cohort in year x, potential offspring were all natural origin salmon sampled
in years x + 2 and x + 3 for coho salmon, and years x + 2, x + 3, x + 4, and x + 5 for Chinook
salmon. The LOD threshold for assigning parentage was readily apparent by inspection of
the LOD scores for the most likely parents for each potential offspring. Both species showed
a bimodal distribution of LOD scores for the most likely mother-father-offspring trio and the
most likely single parent (Figure 1-2). These histograms were used to establish the LOD
assignment thresholds: 20.0 for Chinook salmon mother-father-offspring trios, 10.5 for
Chinook salmon single parents, 15.5 for coho salmon mother-father-offspring trios, and 6.5
for coho salmon single parents. We did not assign any mother-father-offspring trios with 3
mis-matching loci even if they had LOD scores above the threshold.
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Parentage analysis was used to classify natural origin salmon according to the
location in which they were spawned. We use the term recruit for fish that were offspring
of parents who spawned above the dam. Conversely, we refer to individuals spawned from
the lower river (below the dam) or elsewhere as strays. First, all hatchery-produced salmon
(identified by missing adipose fin), and all natural origin salmon in 2003 2004 were
classified as strays. Natural origin individuals that returned in 2005 2009 were classified as
recruits if they assigned two parents that had bypassed the dam in a previous year. The
remaining fish from 2005 2009 were classified as strays if the LOD score for the most
likely single parent fell below the assignment threshold. There were also some salmon
assigned a single parent, and these were more difficult to classify. They might have been
strays if the assigned parent (i.e., a fish sampled at the dam) retreated below the dam to
spawn with a mate that never reached the dam. Alternatively, they might have been recruits
if both parents ascended the fish ladder but one did so without being sampled. All such fish,
with only one assigned parent, were classified as uncertain. All parentage assignments
were made based on an absolute LOD score, rather than LOD relative to next most likely
parent(s), to avoid mis-classifying individuals because of failure to discriminate between two
parents with similar genotypes.
We used two different approaches to assess the accuracy of the DNA-based parentage
methods for classifying fish as either recruits or strays. First, to evaluate how often we
misclassified true recruits as strays, we assigned parentage to 1719 juvenile coho salmon
sampled from sites above the dam that were produced by parents spawning in 2003 2007.
All of these juvenile coho salmon were known to be produced by adults that bypassed the
dam, and thus the number that correctly assigned as recruits reflected the strength of our
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sampling, genotyping and parentage methods. We were unable to collect any samples from
juvenile Chinook salmon because they move downriver shortly after they emerge from nests
in spring.
Second, for each parent in each assignment, we evaluated the probability that an
unsampled fish was the true parent rather than the observed parent. There were many
unsampled fish breeding below the dam, and of these, full siblings of the fish sampled at the
dam were most likely to have similar genotypes. Therefore, we calculated the probability
that an unsampled full sibling of each assigned parent could have a genotype equally
compatible with the assigned offspring; we denote this probability aspfs. For single parent
assignments at locus i, this probability waspi= 0.5 +f- 0.5f2wherefwas the cumulative
frequency of unique alleles in the assigned parent. For parents assigned as mother-father-
offspring trios at locus i, this probability waspi= 0.5 + 0.5fwherefwas the frequency of
the inherited allele. See Appendix for more details and derivation of both cases. The final
probability (pfs) was the product of probabilities across all loci that matched between parent
and offspring.
Estimation of productivity
We calculated the productivity of the initial colonizing cohorts (Chinook: 2003
2005; coho: 2003 2006) as the number of recruits divided by the number of spawners that
produced them. Because there was uncertainty over the number of recruits due to the one
parent assignments, productivity estimates are reported as ranges, where the numerator for
the lower bound includes recruits only and the numerator for the upper bound includes both
the recruit and uncertain categories. We also report two sets of productivity values: one
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based on females only because this best represents the reproductive capacity of the
population and one based on both males and females because this best represents the overall
abundance of the population. In our analysis, a lower productivity bound 1.0 would
indicate that the population replaced itself, and thus was considered self-sustaining.
The samples collected from Chinook salmon below the dam were identified as
originating from above the dam using the same criteria as that used for the samples collected
at the dam. For each cohort ifrom 2003 2005 spawning above the dam, we estimated the
number of offspring that returned to the Cedar River below the dam as the product of the
proportion of the sample from below the dam assigned to parents and the estimated number
of natural origin adult salmon from the correct cohort:
where ris the proportion of samples collected below the dam that were produced by parents
that ascended the fish ladder,Ajis the total abundance of Chinook salmon below the dam in
return yearj, njis the proportion of the lower river population that was natural origin for
return yearj, and cijis the proportion of return yearjproduced by cohort i. We obtained age
data, the proportion natural origin and the total number of Chinook salmon nests counted
during systematic surveys throughout the Cedar River below the dam (Karl Burton, Seattle
Public Utilities, unpublished data). To estimate abundance, we assumed two salmon per
observed nest because females virtually never make more than one nest (Murdoch et al.
2009). Estimates of female only recruits and productivity included an extra term within the
summation sign for the proportion of below dam fish that were female in each return yearj,
and these data were also obtained from K. Burton (unpublished data).
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Results
The counts of Chinook and coho salmon sampled as they bypassed the dam tended to
increase over time (Table 1-1). Chinook salmon had an exceptionally large return in 2007
but were less numerous than coho salmon in five of seven years, and had a much larger
proportion of hatchery origin fish in all years (Table 1-1). Both species tended to have a
male biased sex ratio, but Chinook salmon had a greater fraction of males in sex of seven
years (Table 1-1).
Among all natural origin adults sampled at the dam from 2005 2009, 174 Chinook
salmon and 874 coho salmon assigned two parents from a previous years run and were
classified as recruits produced above the dam. Seventy-nine Chinook and 129 coho did not
assign two parents, but had LOD scores above the threshold for single parents and were
classified as having an uncertain origin. The remaining salmon (405 Chinook and 489 coho),
for which the LOD of the most likely single parent fell below the threshold, were classified
as strays dispersing into the new habitat that were produced below the dam or elsewhere. For
salmon sampled at the dam, the number of loci genotyped was similar between salmon
classified as strays, recruits, and uncertain based on parentage (ANOVA; Chinook: F2,655=
0.32,p> 0.10; coho: F2,1489= 0.94,p> 0.10), indicating that assignment status was not
biased by the amount of genetic data collected for each sample.
Our assessment of the accuracy of parentage assignments indicated that few true
recruits were mis-classified as strays and vice versa. First, the vast majority of juvenile coho
samples collected from sites above the dam produced by parents spawning in 2003 2007 (N
= 329 in 2003, N = 572 in 2004, N = 195 in 2005, N = 316 in 2006, N = 307 in 2007) were
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correctly assigned as recruits (87.6 %). Samples that did not correctly assign as recruits were
predominantly classified as having an uncertain origin (9.8 %) and not mis-classified as
strays (2.6 %). Second, the probability that an unsampled full sibling of each assigned parent
could have a genotype equally compatible with the assigned offspring (pfs) was low for both
the two parent (Chinook: median = 0.0021, range = 0.0013 0.0066; coho: median = 0.0040,
range = 0.0017 0.041) and one parent assignments (Chinook: median = 0.074, range =
0.0042 0.040; coho: median = 0.036, range = 0.018 0.13), and this provided evidence that
we were unlikely to have misclassified true strays as recruits.
For the samples of adult salmon collected at the dam, the two species showed
different patterns of dispersal into the new habitat. Natural origin strays were more
numerous in coho salmon (mean sd = 89.6 49.1) compared to Chinook salmon (63.7
61.6) for all years except 2007 (Figure 1-3, paired t-testp> 0.10). However, hatchery origin
strays were more numerous in Chinook salmon (50.7 26.7 vs. 7.3 6.4, Figure 1-3), and
this difference was significant (paired t-test, p= 0.0075). The total number of strays
(hatchery and natural origin combined) were similar between the species (Chinook: 114.4
82.6; coho: 97.1 54.2, paired t-testp> 0.10), but a much larger proportion of the Chinook
salmon strays were from hatcheries (28 69 % vs. 2 11 %). Ordinary least squares (OLS)
regression indicated that there was no trend through time for the total number of strays in
either species (p> 0.10).
We also evaluated the relationship between the abundance of potential source
populations and the number of salmon strays bypassing the dam. Chinook salmon strays of
either hatchery or natural origin were more numerous in years when more redds were
observed below the dam (Figure 1-4A). There was some evidence for a threshold effect as
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the number of strays increased greatly above approximately 500 redds observed in the lower
river (Figure 1-4A) and a broken stick regression (p= 0.0012, r2= 0.95) fit substantially
better than a standard linear regression (p= 0.027, r2= 0.59). In neither species was the
number of hatchery origin strays related to the number of hatchery fish returning to the
Issaquah Creek hatchery, the UW hatchery, or their sum (Figure 1-4B and 1-4C, OLS,p>
0.10). Within each year 2003-2009, Chinook salmon comprised a greater proportion of the
hatchery salmon captured at the dam than salmon returning to Lake Washington basin
hatcheries (Fig. 1-5A). As a fraction of the total return to the Lake Washington basin
(hatchery returns plus upper Cedar River), a consistently larger percentage of Chinook than
coho salmon strayed into the newly accessible habitat above the dam (Fig. 1-5B).
The two species began to show differences in the composition of the colonizing
population in 2005, the first year in which recruits produced by salmon spawning above the
dam could be expected to return. Within each year 2005 2009, recruits were more
abundant in coho than Chinook salmon, both in terms of numerical count and as a proportion
of the entire run (Fig. 1-3). The number of recruits increased in each subsequent year for
coho salmon, but not for Chinook salmon (Figure 1-3). Finally, Chinook salmon strays
outnumbered recruits in all return years, whereas coho salmon recruits were more than twice
as abundant as strays in 2007 2009 (Figure 1-3). Chinook salmon recruits outnumbered
hatchery strays only in 2008 and 2009. As a proportion of all fish analyzed, the uncertain
category was greatest in 2006 for Chinook salmon (13.9 %) and in 2007 and 2008 for coho
salmon (2007: 14.2 %, 2008: 11.5 %), but < 10 % in all other years.
Estimates of productivity based on the samples collected at the dam showed different
patterns between species. There was strong evidence that coho salmon productivity
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exceeded replacement; for each of the first four cohorts, productivity calculated from females
had lower bounds > 1.0, and three of four estimates that included the males had lower bounds
> 1.0 (Table 1-2). Coho salmon spawning in 2003 and 2006 had estimates 2.0, indicating
that these cohorts doubled in abundance from one generation to the next (Table 1-2). The
minimum estimate of Chinook salmon productivity collected at the dam was > 1.0 in 2004
but not 2003 or 2005 (Table 1-2). In comparing the two species based on the samples
collected at the dam, coho salmon were more productive in 2003 and 2005. In 2004, the
Chinook salmon were more productive based on samples from both sexes, but ranges of the
female only values overlapped (Table 1-2).
A small proportion of the Chinook salmon tissue samples collected below the dam in
2006 2009 were assigned two parents (2.3 %, pooling all samples), and therefore originated
from spawning sites above the dam (Table 1-3). This was much lower assignment rate than
the samples collected at the dam in these years (20.3 %, Figure 1-3), and a binomial test of
proportions (sexes pooled) indicated that the below dam samples had a lower fraction
assigned two parents compared to the samples collected at the dam within each year 2007
2009 (2007:p= 0.0057; 2008:p< 0.0001; 2009:p< 0.0001) but not 2006 (p> 0.10). A
binomial generalized linear model failed to detect a difference between years in the
proportion of the below dam samples originating above the dam (females:p> 0.10, males
and females:p= 0.091), so samples were pooled across years to estimate the proportion of
fish spawning below the dam whose parents had spawned above it. Expansion of the number
of returning Chinook salmon that were produced above the dam using these samples
substantially increased the estimates of above-dam productivity (Table 1-2). Notably, the
lower productivity bound for the 2003 and 2005 female cohorts increased above the
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replacement value of 1.0 (Table 1-2). However, for these two cohorts, the above + below
dam productivity was < 1.0 for the values based on both sexes, likely because the sex ratio
was more heavily biased towards males in the spawners than the recruits (Table 1-2).
Discussion
Diadromous fishes, as a group, are in jeopardy in many areas around the globe
(Lassalle et al. 2008; Limburg and Waldman 2009), and improving habitat connectivity by
removing migration barriers is an increasingly common conservation strategy. Despite the
significant expense of river restoration, such projects are rarely followed by population
monitoring to evaluate their effectiveness in restoring the species of concern (Bernhardt et al.
2005; Katz et al. 2007; Roni et al. 2008). Our study, therefore, provides unique
documentation of the biological response following river restoration, and crucial information
that will help inform future management of recolonizing populations. An important but
unanswered question is whether active reintroduction strategies (i.e., transplanting or
hatchery supplementation) should follow barrier removal, or if fish should be allowed to
colonize on their own volition. Our study describes two critical ecological processes,
dispersal into the new habitat and productivity of initial colonizing cohorts, for coho and
Chinook salmon populations managed for natural recolonization.
In the Cedar River, coho and Chinook salmon dispersed into the newly accessible
habitat under a passive management policy of natural recolonization. Strays were present in
all years for both species and provided the basis for natural reproduction from the very first
generation. A key attribute of this study system was the naturally spawning populations of
both species immediately below the dam, and this seems the most likely source of the
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naturally-spawned strays. For Chinook salmon the number of strays was related to our
estimate of lower river abundance, and this is the only significant breeding population of this
species in the Cedar River watershed. Thus in situations where a migration barrier is
removed adjacent to a naturally reproducing, self-sustaining population of salmon,
transplanting or hatchery supplementation may not be necessary for population expansion. A
primary goal for future research should be to determine the distance from which source
populations can donate colonists through natural dispersal, and thus obviate the need for
active reintroduction. Furthermore, a significant number of salmon continued to disperse
into the new habitat from other source populations even during the second generation, when
a portion of the run was produced above the dam. This secondary colonization may alleviate
the deleterious consequences of inbreeding depression by supplying additional genetic
variation (Tallmon et al. 2004) in the initial stages of colonization when the population might
otherwise be subject to a founder effect. Management usually achieves this type of genetic
rescue of small isolated populations via active translocation of animals (Hedrick and
Fredrickson 2010), but in this case natural dispersal supplied a large number of population
immigrants or strays.
Although based on limited data, there was some evidence for a nonlinear response in
which the number of Chinook salmon strays increased markedly above approximately 500
redds in the lower river below the dam, and this suggests habitat saturation of the source
population above a threshold. In salmon management, surplus fish that are often targeted
for commercial harvest can have a disproportionately large value to alternative ecosystem
services (Moore et al. 2008). In this case, our results suggest that management should
consider the carrying capacity of potential source populations during future recolonization
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projects. If the source population is subject to harvest, and management wishes to prioritize
recolonization, reducing the fishing rate to permit breeding densities above habitat saturation
could enhance dispersal into the newly accessible habitat.
Another important conclusion was that a large proportion of the Chinook salmon
strays were hatchery origin despite the absence of a Chinook hatchery on the Cedar River.
Indeed, the proportion of hatchery origin Chinook sampled at the dam was consistently
higher than that observed in the lower river below the dam (K. Burton, Seattle Public
Utilities, unpublished manuscript). In our study, the higher proportion of hatchery origin
Chinook salmon compared to coho salmon was especially surprising because it did not
correspond to the numbers of fish of these two species produced by the basins two
hatcheries. There is no body of literature that indicates generally higher straying rates by
Chinook than coho salmon (Hendry et al. 2004; Quinn 1993). Furthermore, the lack of a
relationship between the number of hatchery salmon at the dam and returns to either Lake
Washington hatchery suggests that factors other than source population abundance
influenced the number of hatchery strays. One plausible mechanism that could account for
the discrepancy between the species is that some hatchery Chinook salmon reared as
juveniles in the Cedar River, and olfactory imprinting during this period may have caused
them to home to the Cedar River rather than the hatchery. Hatchery marked juvenile
Chinook salmon, but not hatchery coho salmon, were captured each year 2000 2009 in a
downstream migrant trap operated in the Cedar River roughly one km upstream from the
mouth during late spring (Washington Department of Fish and Wildlife, Evaluation of
downstream migrant salmon production from the Cedar River and Bear Creek report series,
accessible wdfw.wa.gov/publications/). Finally, Berge et al. (2006) recovered small numbers
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of adult Chinook salmon in the Cedar River that had been released from hatcheries outside
the Lake Washington basin, so some of the hatchery fish captured at the dam may have been
long distance dispersers.
A second crucial part of the colonization process is the reproductive success of the
initial colonists. Allee effects (i.e., depensatory population dynamics) are a primary concern
in reintroduction programs because initial abundances are often low, and if the effect is
strong, such processes could prevent successful population establishment (Deredec and
Courchamp 2007). We observed extremely low coho salmon densities at the onset of
colonization, and instantaneous densities were even lower than the season total counts
presented here because the coho salmon spawned over a protracted period from mid-October
through early February (Anderson and Quinn 2007). Despite these low densities, coho
salmon productivity exceeded replacement in all years, so mechanisms commonly cited for
depensatory processes did not preclude the success of the colonizing coho salmon
population. For example, reduced probability of fertilization success at low densities owing
to difficulty in finding a mate can cause depensation (Liermann and Hilborn 2001), but the
high mobility of males in this population (Anderson and Quinn 2007) might offset this issue.
Predation can also cause depensation if predators consume a larger proportion of the
population at lower densities (Liermann and Hilborn 2001). Much of the mortality of
juvenile salmon probably occurred during seaward migration (Pess et al. in press). During
this period, predators would encounter juveniles from other locations including the Cedar
River below the dam and other Lake Washington tributaries, so the rate of predation on the
colonizing juveniles may not have varied appreciably with the densities observed above the
dam. In general, salmon populations show high productivity at low densities because they
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are released from competition for breeding sites and, in the case of coho and Chinook
salmon, competition for rearing space in streams (Quinn 2005).
In contrast to coho salmon, the lower bounds of Chinook productivity estimates for
the samples collected at the dam from two of three cohorts (2003 and 2005) were
considerably below replacement. However, we cannot reject the hypothesis that these
cohorts replaced themselves in terms of salmon above the dam because the upper bound was
> 1.0, at least for the female only samples. In addition, coho salmon have a younger age at
maturity than Chinook salmon (age 2-3 vs. age 2-5), so more complete generations had
elapsed during the first seven years of colonization. Due to differences in productivity and
age at maturity, the two species appear to be on different trajectories. The coho salmon
population is dominated by recruits and increasing rapidly, whereas the Chinook salmon
population was composed primarily of strays in 2008 and 2009.
What factors might account for the lower productivity of Chinook salmon? We can
reject the hypothesis that Chinook salmon suffered from more severe mate-finding problems
because a larger proportion of female coho salmon failed to produce any returning adult
offspring (compare Figure 2-2 in Chapter 2 with Figure 3-1 in Chapter 3). We postulate that
two non-exclusive factors, one ecological and one evolutionary, may have played a role in
the lower productivity of the Chinook salmon relative to coho salmon. First, Chinook
salmon may have suffered greater early life mortality because they were exposed to a large
and diverse population of native and non-native predators in Lake Washington and Puget
Sound at a younger age, and hence a smaller size, than juvenile coho salmon. Juvenile coho
salmon typically spend > 1 year in freshwater prior to seaward migration, and upstream
reaches of the Cedar River above the dam had relatively low densities of piscivorous fish
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(cutthroat and rainbow trout) compared to similar systems in Western Washington (Kiffney
et al. 2009). In contrast, the ocean-type Chinook salmon in the Cedar River commonly
migrate downstream within months after emergence at age-0 into a Lake Washington habitat
with abundant predators, including non-native species such as smallmouth bass (Micropterus
dolomieui) and largemouth bass (M. salmoides), and may suffer greater mortality if predation
is size-selective. Furthermore, juvenile Chinook salmon can spend up to several months
rearing within Lake Washington (Tabor et al. 2004), whereas many coho salmon migrated
from headwater habitats to Puget Sound in < 1 month (Pess et al. in press).
It is also possible that the Chinook salmon were less adapted to the natural
environment due to the more substantial straying of hatchery fish onto the spawning grounds.
Domestication selection can reduce the fitness of populations for life in the wild (Ford 2002),
and the small degree of genetic differentiation between hatchery and natural origin Chinook
in this system suggests many of the unmarked wild fish had recent hatchery ancestry
(Chapter 2). Gene flow from the captive breeding environment into the wild, in both the past
and present, may have created a Chinook salmon source population below the dam that is
less fit for the natural conditions encountered above the dam than the coho salmon.
For Chinook salmon, a small proportion of the samples collected below the dam were
produced by salmon spawning above the dam, and this provided two important conclusions.
First, these data increased productivity estimates > 1.0 for the 2003 and 2005 female cohorts,
though this required a large expansion from a small subsample, and was thus subject to
various sources of inaccuracy. Regardless of the true productivity value, salmon that
spawned in the newly accessible habitat above the dam increased abundances below the dam,
and this recruitment spillover effect has been observed in other conservation contexts such
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as enhancement of fisheries adjacent to marine reserves (Gell and Roberts 2003). Second, in
2007 2009, the proportion of below dam samples that assigned two parents was
significantly lower than the samples collected at the dam. This provided evidence for reach-
scale homing precision, examples of which are relatively rare (but see Quinn et al. 2006;
Wagner 1969), such that salmon produced above the dam predominantly returned to the
upper reaches above the dam rather than anywhere within the Cedar River. Within a
colonization context, this result supported Curys (1994) assertion that imprinting permits
the fixation, in a single generation, of new possible reproductive locations found by strays.
The estimates of productivity are conservative because the salmon were sampled and
counted after commercial, tribal and recreational harvest. Lake Washington basin Chinook
salmon exploitation rate estimates for 2005 2008 were approximately 35 45 %, primarily
from northern fisheries in Alaska and British Columbia (Puget Sound Indian Tribes and
Washington Department of Fish and Wildlife 2010). Thus, true, biologically-based
productivity estimates for Chinook could be adjusted upwards by approximately 1.5X 1.8X
from the values presented in Table 1-4. In addition to a coastal troll fishery, coho salmon are
subject to recreational harvest in Puget Sound and a directed terminal tribal fishery in
Shilshole Bay, the ship canal, and Lake Union. Total harvest rates for 2006 2009 ranged
from 32.0 61.1 % (personal communication, Mara Zimmerman, WDFW Wild Salmon
Production Evaluation Unit, March 3, 2011), so biological productivity values would be
approximately 1.5X 2.6X greater than those presented here.
The sampling and genetic data provided a sound method of segregating salmon
produced above the dam (recruits) from those that were produced elsewhere (strays). Our
parentage approach to assigning location of origin relied on the virtually complete sampling
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of the potential parents that spawned above the dam in 2003 2007 because classification as
a recruit required sampling of both parents. This was successfully achieved, as the overall
sample proportions were very high (Chinook: 99 %, coho: 94 %). Furthermore, the
genotypes and LOD scores provided clear separation between salmon that matched parents
ascending the fish ladder in a previous year and those that did not (i.e., two distinct modes in
Figure 1-2). For both species, changing the assignment threshold by a few units in either
direction would have affected the assignment status of a relatively small proportion of
samples. Finally, the best evaluation of the quality of the genetic data came from our
control samples. In this chapter, juvenile coho salmon collected from sites above dam
revealed the rate at which we erroneously classified true recruits as strays (2.6 %). In
Chapter 2, we evaluated externally marked hatchery Chinook salmon, and these controlled
for the rate at which we mis-classified true strays as recruits (N = 267, recruits = 0.4 %,
uncertain = 2.2 %, strays = 97.4 %). In both cases, the proportion of mis-classified samples
was less than 5 %, indicating that our overall conclusions are robust.
Our approach was conservative because we avoided mis-classifying recruits as strays
and strays as recruits by we assigned salmon from 2005 2009 that assigned one parent as
having an uncertain origin. Given our high sampling proportion, the proportion of salmon
collected at the dam that matched only a single parent was surprisingly high, at least for the
Chinook salmon (Chinook: 31.2 %, coho: 12.9 %). The preceding evaluations of our
assignments suggest that it is unlikely that most of the missing parents were sampled but
failed to assign parentage. We suggest three alternative explanations. First, there was great
variation in reproductive success including some very productive parents (Chapter 2 and
Chapter 3), so it is possible that few unsampled parents produced many of the offspring
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assigned only a single parent. Second, it seems plausible that some salmon moved
downstream below the dam after they were sampled ascending the fish ladder, and any that
spawned successfully would have mated with an unsampled parent. Indeed, this behavior
was observed frequently in male coho salmon, and to a lesser extent, the females (Anderson
and Quinn 2007). Finally, any male Chinook salmon that matured as parr (without migrating
to sea) would not have been sampled, and this could account for some of the missing fathers.
Mature male parr are more common in interior populations of Chinook salmon with a stream-
type life-history (Healey 1991), but were occasionally observed in the Cedar River. Within
the Chinook salmon samples collected at the dam, we observed roughly equal numbers of
mother only (N = 42) and father only (N = 37) assignments, so it is difficult to evaluate the
relative contribution of each mechanism. Regardless of the explanation, the one parent
assignments introduced uncertainty into the point estimates of population productivity. We
therefore presented productivity as a range, and emphasize the lower bound because of our
high confidence that the recruits assigned two parents truly were produced above the dam.
In conclusion, we provide strong evidence that restoring connectivity to stream
habitats blocked by dams or other structures can immediately benefit Pacific salmon
populations. Both Chinook and coho salmon dispersed into the newly accessible habitat
from the very first year they were given access, and the expanding populations continued to
attract a significant number of strays originating from source populations below the dam or
elsewhere six years after restoration. Access to habitat above the dam was most beneficial to
coho salmon, as evidenced by their higher productivity than Chinook salmon. Even the
Chinook salmon population more than replaced itself when we considered individuals that
spawned in the lower as well as the upper Cedar River. Moreover, the populations of both
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species were subject to significant exploitation in distant and local fisheries; had these fish
also returned they would have revealed the populations to be growing rapidly. The
remarkable success of the colonizing coho salmon therefore underscores the importance of
access to high quality headwater habitats, which at least in this case, overshadowed a
degraded migratory corridor. The area above the dam is managed as a de factoreserve by the
City of Seattle, but during their lifetime both adults and juveniles must migrate through a
lower river below the dam dominated by suburban development, two heavily urbanized
lakes, and an industrial shipping lock system rather than a natural estuary. Thus even in
highly altered ecosystems, the removal of movement barriers can be an effective
conservation strategy for Pacific salmon.
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Table 1-1. Counts of adult Chinook and coho salmon sampled at Landsburg Diversion Dam
on the Cedar River, Washington, USA.
Chinook salmon Coho salmon
Year N Male (%) Hatchery (%) N Male (%) Hatchery (%)
2003 79 79.7 69.6 47 55.3 8.5
2004 51 56.9 66.7 99 65.7 2.0
2005 69 75.4 42.0 170 61.2 3.5
2006 182 82.4 45.0 190 57.9 4.7
2007 397 75.1 23.4 142 62.7 0.7
2008 146 65.8 17.1 366 49.5 2.5
2009 138 78.3 29.7 679 58.0 2.9
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Table1-2.ProductivityofChinookandcohosalmonfromintialcolonizingcohorts(Year).Forvaluesreportedasranges,the
lowerboundincludesonlyoffspringknowntoberecru
its;theupperboundalsoinclud
esoffspringofuncertainorigin.Fincludes
onlyfemalesandbestrepresentsreproductivecapacity
;M+Fincludesbothsexesandbestrepresentsabundance.
Numberofspawners
Numberofrecru
its
Productivity
Species
Year
F
M+F
Recruits
group
F
M+F
F
M+F
Chinook
2003
16
76
abovedam
918
2359
0.561.13
0.300.78
above+
belowdam
16.752.6
42.8134.1
1.043.29
0.561.76
2004
22
51
abovedam
2633
89113
1.181.50
1.752.22
above+
belowdam
42.9109.3
126.7256.2
1.954.97
2.485.02
2005
16
67
abovedam
1217
3553
0.751.06
0.520.79
above+
belowdam
16.537.3
45.592.7
1.032.33
0.681.38
Coho
2003
20
45
abovedam
4448
102111
2.202.40
2.272.47
2004
34
99
abovedam
3745
93109
1.091.32
0.941.10
2005
66
169
abovedam
128145
244289
1.942.20
1.441.71
2006
80
190
abovedam
185203
433484
2.312.54
2.282.55
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31
Table 1-3. Origin of Chinook salmon samples collected from the Cedar River below
Landsburg Diversion Dam. In comparison to the samples collected at the dam, above damis equivalent to recruits and elsewhere is equivalent to strays.
Females only Males and females
Returnyear
N Abovedam
Elsewhere Uncertain N Abovedam
Elsewhere Uncertain
2006 9 0 8 1 32 0 28 4
2007 32 1 30 1 53 1 51 1
2008 41 1 37 3 73 4 64 5
2009 26 0 24 2 55 0 51 4
total 108 2 99 7 213 5 194 14
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32
Figure 1-1. Map of the Cedar River and Lake Washington basin. The two hatcheries in the
area producing Chinook and coho salmon are denoted by stars.
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33
Figure 1-2. LOD distributions of the most likely parentage assignment for each naturalorigin salmon considered for parentage 2005 2009: (A) mother-father-offspring trios for
Chinook salmon, (B) mother-father-offspring trios for coho salmon, (C) single parents for
Chinook salmon, and (D) single parents for coho salmon for each. The arrows in each panelindicate the assignment threshold, and the gray bars in (C) and (D) represent the offspring
with LOD scores > than the threshold for mother-father-offspring trios in panels (A) and (B).
-20 0 20 40
0
10
20
3
0
40
Frequency
A
-20 0 20 40
0
20
40
60
80
100
B
-10 0 10 20
0
10
20
30
40
50
LOD score
Frequency
C
-10 0 10 20
0
50
100
150
LOD score
D
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34
Figure 1-3. Counts of (A) Chinook salmon and (B) coho salmon in each origin assignmentcategory during colonization of newly accessible habitat. Within each year, the left bar
represents hatchery (dark gray) and natural origin (black) strays, the middle (white) bar
represents recruits, and the right (light gray) bar represents fish of uncertain origin.
2003 2004 2005 2006 2007 2008 2009
0
50
100
150
200
250
Num
bero
fChinoo
ksa
lmon
A
2003 2004 2005 2006 2007 2008 2009
0
100
200
300
400
Num
bero
fcoh
osa
lmon
B
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35
Figure 1-4. Relationship between the number of strays and the abundance of potential source
populations. (A) Total Chinook salmon strays (both hatchery and natural origin) vs.abundance of spawning nests (redds) in the lower Cedar River below the dam (broken stick
regression:p= 0.0030, r2= 0.92; standard linear regression:p= 0.027, r2= 0.59). (B)Hatchery origin Chinook salmon vs. total Lake Washington basin hatchery returns (Issaquah
Creek plus UW Portage Bay). (C) Hatchery origin coho salmon vs. total Lake Washington
basin hatchery returns.
300 400 500 600 700 800
0
50
150
250
Number of Chinook redds below dam
To
talnum
bero
fChinoo
ks
trays
A
2003
20042005
2006
2007
20082009
4000 6000 8000 10000 12000 14000 16000
20
40
60
80
100
Total Lake Washington Chinook hatchery returns
Ha
tcheryorig
inChinoo
ks
trays
B
2003
2004
2005
2006
2007
2008
2009
5000 10000 15000 20000
0
5
10
15
20
Total Lake Washington coho hatchery returns
Ha
tcheryorig
inco
hos
trays C
2003
2004
2005
2006
2007
2008
2009
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36
Figure 1-5. Comparison of hatchery straying between Chinook and coho salmon. (A)Percentage Chinook salmon, as a fraction of the total number of salmon returning to Lake
Washington basin hatcheries (black) and as a fraction of the total number of hatchery originsalmon bypassing Landsburg Diversion Dam on the Cedar River (white). (B) Percentage of
hatchery fish straying into the upper Cedar River above the dam, as a fraction of the total
number of hatchery fish captured at the two hatcheries and the dam, for Chinook (black) andcoho (white) salmon. Asterisks indicatep-value of binomial test of proportions (***p 0.05), it demonstrated the potential for a genetic fitness cost with
little demographic benefit because it is unlikely that any females would have failed to spawn
had the hatchery males been excluded. Hatchery and natural origin salmon had similar
patterns of genetic diversity and effective population size, so there was no evidence that
inclusion of the hatchery fish reduced either parameter. We conclude that in the first
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40generation, the demographic benefits of the hatchery females certainly outweighed the
genetic consequences, but not for the males.
Introduction
The field of reintroduction biology aims to understand the ecological, demographic
and genetic factors that lead to establishment of self-sustaining populations in areas where
they had been extirpated (Seddon et al. 2007). In general, programs that release many
individuals and those that use primarily wild source populations tend to be more successful
(Fischer and Lindenmayer 2000; Wolf et al. 1996). The use of captively bred animals
therefore represents a difficult trade-off to resource managers. Captive breeding can increase
the initial abundance of colonists if wild animals are not available or difficult to transplant
but it also carries certain genetic risks that may affect long-term sustainability.
There are two primary genetic consequences of using captively bred animals in a
reintroduction program that could decrease the likelihood of population establishment and
persistence. First, animals may lose genetic diversity through captive breeding, increasing
the likelihood of inbreeding depression and reducing the amount of genetic material on
which selection might act to evolve traits in the new environment (Allendorf and Luikart
2007). Second, domestication selection in the captive environment often reduces the fitness
of animals for life in the wild (Ford 2002). This effect is generally more severe with
increasing numbers of generations in captivity, and can profoundly decrease the likelihood of
reintroduction success (Frankham 2008).
Whether or not to use captively bred animals in reintroduction programs is a pressing
issue for Pacific salmon (Oncorhynchusspp.) Hatcheries are pervasive throughout their
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41native ranges (reviewed by Fraser 2008; Kostow 2009; Naish et al. 2008), so managers
planning reintroductions would likely have access to artificial supplementation facilities.
Captively reared salmon can provide an immediate demographic boost to populations
targeted for reintroduction or conservation-oriented enhancement (Berejikian et al. 2008).
However, hatchery fish, especially those from non-local sources, tend to have lower
reproductive success than wild fish when both groups breed sympatrically in the wild
(reviewed by Araki et al. 2008) and such fitness declines have been observed after as little as
one or two generations in captivity (Araki et al. 2007a). Maximizing the effective population
size,Ne, has become a focus of recent hatchery reform efforts (Mobrand et al. 2005), but the
wide variety of hatchery goals, breeding protocols and program histories means that the
impact of hatchery production on genetic diversity varies substantially, thus making
generalization difficult (Fraser 2008; Naish et al. 2008).
Impassable dams and culverts prevent salmon from reaching historically accessible
spawning and rearing habitats in many rivers (National Research Council 1996), and
restoration of migratory corridors is an important conservation strategy. Despite their
homing ability (Quinn 2005), salmon naturally colonize new habitats (Anderson and Quinn
2007; Ciancio et al. 2005; Milner et al. 2000; Quinn et al. 2001). Such dispersal may obviate
the need for directed salmon transplantation or hatchery supplementation following the
removal of migration barriers, particularly if there is a nearby source population. Even if
supplementation is not necessary for successful colonization in the long term, some may
advocate using hatchery salmon to accelerate the rate of population expansion (Young 1999).
Agencies removing barriers are therefore confronted with difficult decisions in the
management of recolonizing salmon populations. Should hatchery fish be used to increase
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42the rate of recolonization? If so, how many and at which life stage (juvenile, adult, etc.)
should they be planted? If not, should hatchery fish that naturally stray into the new habitat
be allowed to spawn there or be culled?
In this paper, we address the role of captively bred animals during reintroduction in a
population of Chinook salmon, O. tshawytscha, in the Cedar River, WA, where modification
of Landsburg Diversion Dam in 2003 granted access to 33 km of spawning and rearing
habitat for the first time in over a century. Chinook salmon are listed as threatened in this
region under the Endangered Species Act, and thus are of particular conservation concern.
Hatchery fish were not actively transplanted above the dam but adults were allowed to
bypass the dam and spawn if they volitionally entered the fish passage facility. We sampled
these colonizing Chinook salmon in 2003 2009, and used molecular DNA markers to
evaluate the trade-off between the demographic benefit and genetic risk of permitting the
hatchery fish to spawn. Our analysis had three objectives. First, we quantified the number of
hatchery origin colonists and their numerical contribution to the next generation in order to
assess the demographic boost provided by the hatchery fish. Second, the potential for a
fitness cost associated with colonization by hatchery fish was evaluated by comparing per
capita reproductive success between hatchery and natural origin fish. Finally, we measured
the genetic diversity and estimated effective population size to determine if inclusion of
hatchery fish caused a reduction in either parameter.
Methods
Study site natural history and sampling
The Cedar River flows west from the Cascade mountain range into the south end of
Lake Washington, which is connected to Puget Sound via a man-made shipping canal
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43through Seattle, Washington, U.S.A. (Figure 2-1). Chinook salmon have a complicated
natural history in this basin owing to hydrologic changes and hatchery production.
Historically, the Cedar River was connected to Puget Sound via the Green and Black rivers,
although the extent to which the Cedar River Chinook were distinct from those in the Green
River is unclear (Ruckelshaus et al. 2006). In 1916, the Cedar River was diverted into Lake
Washington in conjunction with construction of the shipping canal and navigational locks.
Chinook salmon from a hatchery on the Green River founded the Issaquah Creek hatchery
population (Figure 2-1) in 1937 and continued to supply broodstock until 1992 (HSRG
2003). The Issaquah Creek hatchery is the primary production facility in the basin, spawning
approximately 2,500 of the 3,069 13,482 adult Chinook salmon trapped in 2003 2009
(Hatchery Escapement Reports, Washington Department of Fish