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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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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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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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iii

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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iv

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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1

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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14

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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21

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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23

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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24

(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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25

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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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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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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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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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

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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

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Number of Chinook redds below dam

To

talnum

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20042005

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20082009

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Total Lake Washington Chinook hatchery returns

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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

anderson j phd w 2011

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