Wintering and breeding distributions of

Black Oystercatchers (Haematopus bachmani):

Long-term trends and the influence of climate

by

Seth Gaborko Bennett

B.Sc., (Hons.), Memorial University of Newfoundland, 2013

Thesis Submitted in Partial Fulfillment of the

Requirements for the Degree of

Master of Science

in the

Department of Biological Sciences

Faculty of Science

© Seth G. Bennett 2018

SIMON FRASER UNIVERSITY

Summer 2018

Copyright in this work rests with the author. Please ensure that any reproduction or re-use is done in accordance with the relevant national copyright legislation.

ii

Approval

Name: Seth Gaborko Bennett

Degree: Master of Science

Title: Wintering and breeding distributions of Black Oystercatchers (Haematopus bachmani): Long-term trends and the influence of climate

Examining Committee: Chair: Jim Mattsson Associate Professor

David Green Senior Supervisor Professor

Mark Drever Supervisor Migratory Bird Biologist Canadian Wildlife Service

Daniel Esler Supervisor Research Wildlife Biologist United States Geological Survey

Ronald Ydenberg Supervisor Professor

Stephanie Hazlitt External Examiner Head, State of Environment Reporting Analysis, Reporting, and Knowledge Services Government of British Columbia

Date Defended/Approved: August 3, 2018

iii

Abstract

Black Oystercatchers (Haematopus bachmani) are argued to be at risk from global

climate change as rising sea levels could threaten their coastal habitat. However,

population estimates have doubled to ~15 000 since 1994. This has been attributed to

improvements in survey methods rather than to population trends, which remain

uncertain. I assessed trends and climatic influences on winter abundance (Christmas

Bird Counts, 1975/1976 – 2015/2016) and numbers of breeding pairs (British Columbia

breeding surveys, 1962 – 2014). Winter counts were stable or increasing across the

species' range. Numbers of breeding pairs were stable in British Columbia, but were

lower following the warm phase than the cool phase of the El Niño Southern Oscillation.

Although new challenges may arise as the climate continues to change, Black

Oystercatcher populations appear resilient to current environmental and anthropogenic

challenges.

Keywords: Aleutian low; bottom-up; carry-over effects; El Niño Southern Oscillation;

intertidal predator; partial migration

iv

Dedication

I dedicate this thesis to the birds.

v

Acknowledgements

First of all, my supervisor, David Green, guided, supported, and accommodated

me with seemingly endless patience. David provided so much valuable feedback on the

project, manuscript, and defence presentation, and helped me make sense of the model

outputs. The rest of my committee, Mark Drever, Dan Esler, and Ron Ydenberg, and my

examiner, Stephanie Hazlitt, provided valuable feedback, support, and encouragement.

They were also very accommodating particularly while trying to find a defence date that

worked for everybody at the end of the summer. Thanks also to Jim Mattsson, for taking

the time to act as chair for my defence.

Thanks to everyone in the Centre for Wildlife Ecology, particularly Sarah

Thompson, who extracted and prepared the temperature data used in Chapter 2. Philina

English helped me with R code for the AIC tables and graphs. Cailin Xu helped me with

the Christmas Bird Count data. David Hope, Richard Johnston, and Simon Valdez gave

me useful feedback on my defence presentation.

At the Canadian Wildlife Service, Mark Drever (again) supported me and helped

with the breeding data and R code used in Chapter 3. Holly Middleton compiled the

breeding data used in Chapter 3. Mark Hipfner supplied some updated data and useful

context for the oystercatcher surveys on Triangle Island.

At the United States Geological Survey, Dan Esler (again), Tim Bowman, Jon

Brown, Brian Uher-Koch, and Megan Willie (CWE) helped me get my hands on some

oystercatchers for the very first time in Prince William Sound. At the United States

National Park Service, Brian Robinson, Sam Stark, and Jordan Green gave me a first-

hand look at Black Oystercatcher parents and chicks on their breeding grounds in

beautiful Kenai Fjords. Thanks to the oystercatchers for being such darn cool birds.

At the Dean of Science office, Steve Obadia (IT support) saved my laptop and

the files within when it crashed and I feared all might be lost. At the SFU Counselling

Centre, Susan Brook and the rest of the Thesis Support Group provided support (as

support groups should) and shared their grad school experiences and struggles.

vi

Finally, my family: Maria Adey moved to BC with me and settled down with me

here. Her support, encouragement, and patience helped get me through. My family,

Mom, Dad, and Trevor, and Maria's family, Lin, Arnold, and Emily, were supportive and

patient and hardly ever asked me if I was getting close to finishing yet.

Funding for this project came from the CWE, CWS, Dean of Graduate Studies

(Graduate Fellowships), and the Green Lab.

vii

Table of Contents

Approval.............................................................................................................................iiAbstract............................................................................................................................. iiiDedication .........................................................................................................................ivAcknowledgements........................................................................................................... vTable of Contents.............................................................................................................viiList of Tables.....................................................................................................................ixList of Figures ................................................................................................................... xList of Acronyms ...............................................................................................................xi

Chapter 1. Introduction ............................................................................................... 1References........................................................................................................................ 3

Chapter 2. Temporal trends and climate effects on the winter numbers of a partially-migratory shorebird, the Black Oystercatcher (Haematopus bachmani), throughout its range......................................................................... 6

Introduction ....................................................................................................................... 6Methods ............................................................................................................................ 8

Study species ................................................................................................................ 8Winter distribution data.................................................................................................. 8Analyses........................................................................................................................ 9

Results ............................................................................................................................ 11Temporal trends in Black Oystercatcher winter numbers............................................ 11Relationships between climate variables .................................................................... 12Effects of winter conditions on Black Oystercatcher numbers in the following winter . 12Effects of pre-migration conditions on winter distributions of Black Oystercatchers ... 12

Discussion....................................................................................................................... 13References...................................................................................................................... 16Tables ............................................................................................................................. 20Figures ............................................................................................................................ 23

Chapter 3. The influence of the El Niño Southern Oscillation on Black Oystercatcher (Haematopus bachmani) breeding numbers in British Columbia.............................................................................................................. 25

Introduction ..................................................................................................................... 25Methods .......................................................................................................................... 27

Study species .............................................................................................................. 27Breeding surveys......................................................................................................... 27Climate indices and variables...................................................................................... 28

Southern Oscillation Index and Pacific Decadal Oscillation .................................... 29North Pacific Gyre Oscillation.................................................................................. 29Coastal Sea Surface Temperature .......................................................................... 30Upwelling ................................................................................................................. 30

viii

Analyses...................................................................................................................... 31Results ............................................................................................................................ 32

Temporal trends in numbers of Black Oystercatcher breeding pairs .......................... 33Relationships between selected climate variables ...................................................... 33Climate effects on numbers of Black Oystercatcher breeding pairs............................ 33

Discussion....................................................................................................................... 34References...................................................................................................................... 37Tables ............................................................................................................................. 42Figures ............................................................................................................................ 45

Chapter 4. Conclusions............................................................................................. 48References...................................................................................................................... 51

Appendix: Population estimates for Black Oystercatchers................................... 54

ix

List of Tables

Table 2.1 Summary of Christmas Bird Count data used for analyses of trends in Black Oystercatcher winter numbers and the effects of climate from 1975/1976 to 2015/2016. The second analysis, examining carry-over effects from winter climate conditions to numbers of oystercatchers in the following winter, used a slightly reduced data set due to gaps in the available climate data. Sample sizes for the data set used in the second analysis are shown in parentheses. ........................................................ 20

Table 2.2 AIC results from model sets examining (a) trends in winter counts of Black Oystercatchers across their range from 1975/1976 to 2015/2016, (b) counts of oystercatchers in response to conditions from the previous winter, and (c) counts of oystercatchers in response to temperatures across the species' Alaska range in the late summer (July & August) and fall (September & October). Regional trend model is bolded. All models included party distance + party distance2 as a measure of effort............ 21

Table 2.3 Parameter estimates for models examining (a) regional trends in winter counts of Black Oystercatchers and (b) trends with regional effects of Aleutian Low Pressure Index (ALPI) on counts in the following winter between 1975/1976 and 2015/2016........................................................ 22

Table 3.1 Sources and details of Black Oystercatcher breeding surveys in British Columbia, including areas surveyed, time of surveys, and survey methods. Preliminary surveys were performed from the boat except on Triangle Island, and sites were then searched more thoroughly by foot. 42

Table 3.2 AIC table for analysis of (a) Trends in numbers of breeding pairs of Black Oystercatchers and (b) climate effects on numbers of breeding pairs of Black Oystercatchers in British Columbia (n = 760 records at 193 sites). Null and subregional trend models are bolded. All models assumed a negative binomial distribution and included log-transformed shore length as an offset variable and site as a random variable. ............................... 43

Table 3.3 Parameter estimates for (a) null model showing no effect of trends in numbers of breeding pairs of of Black Oystercatchers and (b) effect of the mean April Southern Oscillation Index (SOI) on numbers of breeding pairs of Black Oystercatchers counted on surveys conducted across British Columbia between 1962 and 2014.......................................................... 44

x

List of Figures

Figure 2.1 Temporal trends in the observed numbers of Black Oystercatchers on Christmas Bird Counts conducted between 1975/1976 and 2015/2016 in five regions across their range. Lines show the predicted counts in each region and shading shows 95% confidence intervals based on the top model in Table 2.2a and Table 2.2c. Parameter estimates for this model are given in Table 2.3a. Rugging shows the distribution of data in each region, with positive partial residuals across the top and negative partial residuals across the bottom. ................................................................... 23

Figure 2.2 Relationship between Aleutian Low Pressure Index (ALPI) and observed numbers of Black Oystercatchers in Christmas Bird Counts the following year. Lines show the predicted counts in each region and shading shows the 95% confidence intervals based on the top model in Table 2.2b. Parameter estimates for this model are given in Table 2.3b. Rugging shows the distribution of data in each region, with positive partial residuals across the top and negative partial residuals across the bottom................................................................................................................. 24

Figure 3.1 Sites of lighthouses in British Columbia recording daily sea surface temperatures and salinity as of 2018. The year in parentheses next to the name of each site indicates the year in which data collection began. 7 lighthouses that no longer collect data are not shown. Source: http://www.pac.dfo-mpo.gc.ca/science/oceans/data-donnees/lightstations-phares/index-eng.html (accessed 21 August 2018) ................................ 45

Figure 3.2 Numbers of breeding pairs of Black Oystercatchers at breeding sites in British Columbia from 1962 to 2014. Subregions are denoted by colour (red = Haida Gwaii, blue = Strait of Georgia & Gulf Islands, and green = west coast of Vancouver Island). ............................................................ 46

Figure 3.3 Relationship between the Southern Oscillation Index (SOI) in April and numbers of breeding pairs of Black Oystercatchers at survey sites in British Columbia between 1962 and 2014. The line shows the relationship, and the shaded area shows the 95% confidence interval from the top model in Table 3.2b. Parameter estimates for the model are given in Table 3.3b. Rugging shows the distribution of data. .................. 47

xi

List of Acronyms

ADMB Automatic Differentiation Model Builder

AIC Akaike's Information Criterion

AK Alaska (United States of America)

ALPI Aleutian Low Pressure Index

BC British Columbia (Canada)

BCN Baja California (United Mexican States)

BCSOP British Columbia Shore Station Oceanographic Program

CA California (United States of America)

CBC Christmas Bird Count

CI Confidence Interval

DDT Dichlorodiphenyltrichloroethane

ENSO El Niño Southern Oscillation

GPS Global Positioning System

IQR Interquartile Range

NCEP National Centers for Environmental Prediction

NOI Northern Oscillation Index

NPGO North Pacific Gyre Oscillation

OR Oregon (United States of America)

PDO Pacific Decadal Oscillation

PFEL Pacific Fisheries Environmental Laboratory

SD Standard Deviation

SE Standard Error

SOI Southern Oscillation Index

SST Sea Surface Temperature

USA United States of America

WA Washington (United States of America)

1

Chapter 1. Introduction

Species occupying specialist niches tend to be more threatened by climate

change than generalist species, as they are less able to adapt to changes in their

environment (Clavel et al. 2010, Gilman et al. 2010, Stefanescu et al. 2011). This pattern

has been found to apply broadly across many taxa, such as birds (Julliard et al. 2004)

and butterflies (Stefanescu et al. 2011) in Europe. For the conservation of species

threatened by climate change, it is important to understand both the environmental

influences on these species as well as anthropogenic threats that could hinder recovery

and conservation efforts (Gilman et al. 2010, Stefanescu et al. 2011). For example, the

recovery of the Bald Eagle (Haliaeetus leucocephalus) following the 1972 ban of the

pesticide DDT was successful because the primary cause of decline was identified, and

the DDT ban was combined with other threat mitigation measures (e.g. a ban on killing;

Grier 1982).

Acquiring the data necessary to identify population trends and risks can require a

lot of time and resources, especially for data collected across broad spatial scales.

Citizen science, where volunteers from the public are enlisted to perform surveys and

record observations, can be an effective way to collect this data while also engaging the

public with the natural world (Bonny et al. 2009). Citizen science has been criticized

because differences in training, experience, and effort of participants may lead to

variation in the quality and reliability of data (e.g. Galloway et al. 2006). However, many

of these issues can be mitigated through thoughtful experimental design, volunteer

training, and data validation (Bonter & Cooper 2012). As a result, particularly effective

citizen science projects such as eBird have become invaluable sources of data (e.g.

presence/absence, counts) that are widely available to many researchers at different

institutions (Sullivan et al. 2014).

The Black Oystercatcher (Haematopus bachmani) is an important intertidal

predator and indicator species for evaluating the health of the Pacific rocky intertidal

shoreline (Wootton 1992, Bergman et al. 2013, Tessler et al. 2014). This species has

been classified as "Climate Endangered" by the Audubon Society, based on predictions

2

that the species' range could be reduced by more than 50 percent by 2050 (Langham et

al. 2015). This is largely because the species' habitat is limited to the rocky intertidal

coastline, which is expected to shrink as sea levels rise. Food availability may also be a

concern as Black Oystercatchers feed mainly on molluscs with calcified shells (Tessler

et al. 2014), which are themselves threatened by ocean acidification (Fabry et al. 2008).

Black Oystercatchers nest on beaches, and are sensitive to extreme high tides (Morse et

al. 2006). Anthropogenic factors are also of concern (Warheit et al. 1984, Spiegel 2008).

Immediately following the 1989 Exxon Valdez oil spill in Prince William Sound, Alaska,

oystercatchers in affected regions suffered reductions in population and breeding

success (Andres 1997, Murphy et al. 1997). Local populations recovered quickly,

however, and these effects were no longer observed by 1993, 4 years after the spill

(Andres 1999). Though they are one of North America's least abundant shorebirds

(fewer than 18 000 individuals globally; Appendix), populations are thought to be stable

or increasing (Hazlitt 2001, Tessler et al. 2014, Meehan et al. 2018).

Despite extensive study of the Black Oystercatcher's biology, there are still

significant gaps in our knowledge of the species' ecology. Long-term, broad-scale

population data are lacking (Tessler et al. 2014, Weinstein et al. 2014, Appendix).

Consequently, there are currently no peer-reviewed analyses of population trends in

Black Oystercatchers at a global scale. Little is known about migratory behaviour in

Black Oystercatchers, as well. The species is known to be partially migratory in the

northern part of their range (Andres 1994), and limited data have been collected on

migration timing, distances, and routes (Johnson et al. 2010). However, it is not known

to what extent migration varies from year to year in terms of distance, timing, and

proportion of migrants. Finally, there has been ample research into the species' breeding

biology and behaviour (e.g. Purdy & Miller 1988, Hazlitt et al. 2002, Hipfner et al. 2012),

and there is evidence that local climate, specifically sea surface temperature (SST),

influences breeding (Hipfner & Elner 2013). That said, it is unknown if this effect is

widespread across their range, or to what extent this species is influenced by

environmental factors other than SST.

In this thesis, I will examine long-term trends in oystercatcher numbers and

explore the influence of climate on wintering strategy and breeding numbers. In Chapter

2, I use Christmas Bird Count data to identify trends in the numbers of wintering

oystercatchers across the species' range. I then examine carry-over effects of winter

3

conditions on populations from one year to the next. Finally, I examine the influence of

summer and fall climate on winter distributions to determine the effect of environment on

wintering strategy (residency or migration) in a given year. In Chapter 3, I use summer

monitoring data from across British Columbia to determine long-term trends in the

numbers of breeding Black Oystercatchers in the province. I then examine a suite of

broad- and local-scale climate variables to determine how environmental conditions

influence breeding numbers from year to year. Together, these studies provide long-term

baseline information on population and breeding trends, which are invaluable for

contextualizing future monitoring efforts. These studies also provide insight into the

nature of environmental influences on the behavioural and breeding ecology of Black

Oystercatchers. This information could have important implications if this species

becomes a target for conservation efforts.

References

ANDRES B.A. (1994) Year-round residency in northern populations of the Black Oystercatcher. U.S. Fish and Wildlife Service, Anchorage, AK

ANDRES B.A. (1997) The Exxon Valdez oil spill disrupted the breeding of Black Oystercatchers. Journal of Wildlife Management 61(4): 1322–1328

ANDRES B.A. (1999) Effects of persistent shoreline oil on breeding success and chick growth in Black Oystercatchers. Auk 116(3): 640–650

BERGMAN C.M., PATTISON J., & PRICE E. (2013) The Black Oystercatcher as a sentinel species in the recovery of the Northern Abalone: Contemporary diet of Black Oystercatchers on Haida Gwaii includes an endangered prey species. Condor 115(4): 800–807

BONNY R., COOPER C.B., DICKINSON J., KELLING S., PHILLIPS T., ROSENBERG K.V., & SHIRK J. (2009) Citizen science: A developing tool for expanding science knowledge and scientific literacy. BioScience 59(11): 977–984

BONTER D.N. & COOPER C.B. (2012) Data validation in citizen science: A case study from Project FeederWatch. Frontiers in Ecology and the Environment 10(6): 305–307

CLAVEL J., JULLIARD R., & DEVICTOR V. (2010) Worldwide decline of specialist species: Toward a global functional homogenization? Frontiers in Ecology and the Environment 9(4): 222–228

4

FABRY V.J., SEIBEL B.A., FEELY R.A., & ORR J.C. (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. ICES Journal of Marine Science 65(3): 414–432

GALLOWAY A.W.E., TUDOR M.T., & VANDER HAEGEN W.M. (2006) The reliability of citizen science: A case study of Oregon White Oak stand surveys. Wildlife Society Bulletin 34(5): 1425–1429

GILMAN S.E., URBAN M.C., TEWKSBURY J., GILCHRIST G.W., & HOLT R.D. (2010) A framework for community interactions under climate change. Trends in Ecology and Evolution 25(6): 325–331

GRIER J.W. (1982) Ban of DDT and subsequent recovery of reproduction in Bald Eagles. Science 218(4578): 1232–1235

HAZLITT S.L. (2001) Black Oystercatcher population status and trends in British Columbia. Bird Trends 8: 34–36

HAZLITT S.L., YDENBERG R.C., & LANK D.B. (2002) Territory structure, parental provisioning, and chick growth in the American Black Oystercatcher. Ardea 90(2): 219–227

HIPFNER J.M. & ELNER R.W. (2013) Sea-surface temperature affects breeding density of an avian rocky intertidal predator, the Black Oystercatcher Haematopus bachmani. Journal of Experimental Marine Biology and Ecology 440: 29–34

HIPFNER J.M., MORRISON K.W., & KOUWENBERG A.-L. (2012) Biology of Black Oystercatchers breeding on Triangle Island, British Columbia, 2003–2011. Northwestern Naturalist 93: 145–153

JOHNSON M., CLARKSON P., GOLDSTEIN M.I., HAIG S.M., LANCTOT R.B., TESSLER D.F., & ZWEIFELHOFER D. (2010) Seasonal movements, winter range use, and migratory connectivity of the Black Oystercatcher. Condor 112(4): 731–743

JULLIARD R., JIGUET F., & COUVET D. (2004) Common birds facing global changes: What makes a species at risk? Global Change Biology 10(1): 148–254

LANGHAM G.M., SCHUETZ J.G., DISTLER T., SOYKAN C.U., & WILSEY C. (2015) Conservation status of North American birds in the face of future climate change. PLoS ONE 10(9): e0135350. https://doi.org/10.1371/journal.pone.0135350

MEEHAN T.D., HARVEY A.L., MICHEL N.L., LANGHAM G.M., & WEINSTEIN A. (2018) A population model exploring factors influencing Black Oystercatcher (Haematopus bachmani) population dynamics. Waterbirds 41(2): 115–221

5

MORSE J.A., POWELL A.N., & TETREAU M.D. (2006) Productivity of Black Oystercatchers: Effects of recreational disturbance in a national park. Condor 108: 623–633

MURPHY S.M., DAY R.H., WIENS J.A., & PARKER K.P. (1997) Effects of the Exxon Valdez oil spill on birds: Comparisons of pre- and post-spill surveys in Prince William Sound, Alaska. Condor 99: 299–313

PURDY M.A. & MILLER E.H. (1988) Time budget and parental behavior of breeding American Black Oystercatchers (Haematopus bachmani) in British Columbia. Canadian Journal of Zoology 66(8): 1742 – 1751

SPIEGEL C.S. (2008) Incubation patterns, parental roles, and nest survival of Black Oystercatchers (Haematopus bachmani): Influences of environmental processes and potential disturbance stimuli. MSc thesis, Oregon State University: 139p.

SULLIVAN B.L., AYCRIGG J.L., BARRY J.H., BONNY R.E., BRUNS N., COOPER C.B., DAMOULAS T., DHONDT A.A., DIETTERICH T., FARNSWORTH A., FINK D., FITZPATRICK J.W., FREDERICKS T., GERBRACHT J., GOMES C., HOCHACHKA W.M., ILIFF M.J., LAGOZE C., LA SORTE F.A., MERRIFIELD M., MORRIS W., PHILLIPS T.B., REYNOLDS M., RODEWALD A.D., ROSENBERG K.V., TRAUTMANN N.M., WIGGINS A., WINKLER D.W., WONG W.-K., WOOD C.L., YU J., & KELLING S. (2014) The eBird enterprise: An integrated approach to development and application of citizen science. Biological Conservation 169: 31–40

STEFANESCU C., CARNICER J., & PEÑUELAS J. (2011) Determinants of species richness in generalist and specialist Mediterranean butterflies: The negative synergistic forces of climate and habitat change. Ecography 34(3): 353–363

TESSLER D.F., JOHNSON J.A., ANDRES B.A., THOMAS S., & LANCTOT R.B. (2014) A global assessment of the conservation status of the Black Oystercatcher Haematopus bachmani. International Wader Studies 20: 83–96

WARHEIT K.I., LINDBERG D.R., BOEKELHEIDE R.J. (1984) Pinniped disturbance lowers reproductive success of black oystercatcher Haematopus bachmani (Aves). Marine Ecology Progress Series 17: 101–104

WEINSTEIN A., TROCKI L., LEVALLEY R., DOSTER R.H., DISTLER T., & KRIEGER K. (2014) A first population assessment of Black Oystercatcher Haematopus bachmani in California. Marine Ornithology 42: 49–56

WOOTTON T.J. (1992) Indirect effects, prey susceptibility, and habitat selection: Impacts of birds on limpets. Ecology 73(3): 981–991

6

Chapter 2. Temporal trends and climate effects on the winter numbers of a partially-migratory shorebird, the Black Oystercatcher (Haematopus bachmani), throughout its range

Introduction

Migration to high latitudes allows birds to take advantage of seasonally abundant

resources during the breeding season (Alerstam 1990, Newton 2007). Migrating

thousands of kilometres to breed is, however, energetically costly (Wikelski et al. 2003).

Birds that remain at high latitudes year-round do not incur this cost, and may benefit by

avoiding the high mortality associated with migration (Sillet & Homes 2002, Lank et al.

2003), having a competitive advantage when claiming or defending high quality breeding

territories (Kokko 2011), and being able to optimize their breeding phenology to spring

conditions in a given year (Helm et al. 2006). On the other hand, remaining at high

latitudes year-round can be risky as inclement weather may increase metabolic costs

and decrease food availability sufficiently to cause mortality (Robinson et al. 2007). In

some species, populations at higher latitudes may consist of both migratory and resident

individuals, indicating that the costs and benefits of migration and residency are finely

balanced.

The migratory strategy of an individual within a partially-migratory population may

be either genetically controlled (obligate) or condition dependent (facultative). Controlled

laboratory and field studies suggest that migration has a genetic basis (Partecke &

Gwinner 2007, Pulido 2011), and theoretical models tend to assume that migration is a

fixed genetic dimorphism that can persist if the two strategies have equal fitness

(Gauthreaux 1982, Lundberg 1987, 1988). Alternatively, migration may be conditional

with the optimal strategy for an individual being dependent on its phenotype (Swingland

& Lessells 1979). If this is the case migratory and non-migratory individuals need not

have equal fitness and the strategy of an individual may vary from year to year,

depending on individual condition, food availability, weather, or a combination of these

7

factors (Chapman et al. 2011, Pulido 2011). Empirical studies have shown that migratory

and sedentary individuals can differ in fitness (e.g. Andriaensen et al. 1993, Gillis et al.

2008), and that the proportion of migrants can vary with temperature and food availability

(Meller et al. 2016)

Oystercatchers are a group of shorebirds that display a variety of wintering

strategies: the three species that breed in the northern hemisphere all have partially

migratory populations (Eurasian Oystercatcher, Haematopus ostralegus: Ens et al. 1992;

American Oystercatcher, H. palliatus: Clay et al. 2010; and Black Oystercatcher, H.

bachmani, Andres et al. 1994). Eurasian Oystercatchers are known to be sensitive to

winter conditions that can influence both migration strategies and survival. Severe

winters can increase migration distances forcing northern populations to move further

south than usual, induce mass mortality, and increase summer mortality via carryover

effects (Camphyusen et al. 1996, Goss-Custard 1996, Duriez et al. 2012). A genetic

analysis by Van Treuren et al. (1999) found no genetic differences between migratory

and resident Eurasian Oystercatchers, suggesting that wintering strategy is most likely

facultative, not obligate, in this group.

The Black Oystercatcher of the North American Pacific coast exhibits both non-

breeding and breeding partial migration (sensu Chapman 2011). In Prince William

Sound, Alaska, residents and migrants share a breeding habitat, but approximately 75%

of the breeding population migrate south so they overwinter apart. Conversely, in British

Columbia, residents and migrants share a winter habitat but breed apart (Andres et al.

1994). Despite being a top predator of the rocky intertidal (Wootton 1992) and an

indicator species of the rocky intertidal (Clarkson & Zharikov 2007, Bergman et al. 2013,

Tessler et al. 2014), little is known about temporal trends in their numbers and winter

distributions. In this study, I used Christmas Bird Count data to (1) estimate long-term

trends in Black Oystercatcher populations across their winter range, (2) examine

whether winter conditions have a detectable impact on numbers in the following winter,

and (3) assess whether predicted winter conditions in Alaska influence the proportion of

migrants, and hence the winter distribution, of oystercatchers in the northern part of their

range.

8

Methods

Study species

The Black Oystercatcher is a long-lived shorebird that feeds mainly on molluscs

in the rocky intertidal zone. The species ranges from the Aleutian Islands in Alaska to

Baja California, Mexico. They are one of North America's least abundant shorebirds, with

estimated global numbers of roughly 12 500 – 17 500 (Appendix). Approximately 6750

are thought to breed in Alaska (Tessler et al. 2014). Some Alaskan populations are

partially migratory (Andres et al. 1994): migrants depart between mid-August and early

November and have been found to overwinter as far south as southern Vancouver

Island (Johnson et al. 2010).

Winter distribution data

Survey data were taken from the Christmas Bird Count (CBC), a citizen science

initiative coordinated by the Audubon Society (in the United States) and Bird Studies

Canada (in British Columbia). Volunteers conduct surveys in count circles with a 24 km

diameter, recording the total numbers of individuals of each bird species seen, the

number of volunteers in the party, the number of survey hours, and the distance covered

by each survey party. Counts within a circle are conducted during a 24 h period on a set

date in late December or early January. Counts are reported with party-hours and party-

distance (in either miles or km) as measures of search effort.

My analysis included circles that were surveyed on more than one occasion from

1975/1976 to 2015/2016 and had at least one recorded Black Oystercatcher sighting

during that time. I excluded surveys earlier than the winter of 1975/1976 as the number

and distribution of count circles along the Pacific Coast was relatively sparse before

then. Circles were grouped by region (province/state). Baja California (Mexico) only

contained one count circle, so it was combined with California into a single region. The

data set was reduced further when records were excluded due to a lack of available

environmental data for the circle for some years. Table 2.1 shows a summary of the data

sets used for each analysis.

9

Analyses

I created three candidate model sets to examine (1) temporal trends in the

number of wintering Black Oystercatchers counted in CBC surveys, (2) carry-over

effects from the climate in the previous winter, and (3) redistribution of oystercatchers

between regions from year to year. In each case I fitted generalised linear mixed models

including count circle as a random term. I determined the best-fitting distribution and

best measure of effort for each model set using Akaike’s Information Criteria (AIC).

Models fitted with a negative binomial distribution outperformed those with a zero-

inflated negative binomial distribution and a Poisson distribution (AICc weights: negative

binomial = 0.71, zero-inflated negative binomial = 0.29, Poisson < 0.01). Models with

quadratic distance travelled in kilometres (distance + distance2) outperformed models

with linear distance, party hours (quadratic and linear) as a measure of effort, and

models that did not include search effort (AICc weights: quadratic distance = 0.96, linear

distance = 0.02, quadratic hours = 0.01, linear hours & no effort < 0.01). Thus, all

candidate models in each of the three candidate sets assumed a negative binomial

distribution and used quadratic distance as a measure of effort.

The first candidate model set included models that examined temporal trends in

the number of wintering Black Oystercatchers counted in CBC surveys between

1975/1976 and 2015/2016. This candidate set included models with all combinations of

year (trend), region, the additive and interactive effects of these variables, and a null

model (n = 5 models).

The second candidate model set examined whether local or regional winter

conditions in one year influenced oystercatchers counted in CBC surveys in the

subsequent year. I used average mean daily temperatures during January and February

(the coldest months) in each count circle as a measure of local winter conditions. I used

the Aleutian Low Pressure Index (ALPI) as a measure of winter conditions for the whole

region. The ALPI is a measure of the intensity of winter conditions in the north Pacific

Ocean from December to March (Surrey & King 2015). This broad-scale climate pattern

is correlated with wind and storms in the northeastern Pacific (Surrey & King 2015). If

harsh winter conditions lead to increased winter mortality, or carryover effects that

influence summer mortality or productivity later in the year, I expected that harsher

winters (lower temperatures or positive ALPI values) would correspond with lower counts

10

in the following winter. This candidate model set included univariate models with either

winter temperature or ALPI alone, models that allowed the effects of ALPI or winter

temperature to vary by region, the top model from the first candidate set examining

regional differences or year trends, and versions of each of the temperature and ALPI

models that included the regional or year trends detected in the first candidate set (n = 9

models). Temperature data at each count circle were extracted from the National

Centers for Environmental Prediction (NCEP) data set (http://www.ncep.noaa.gov/,

accessed 25 June 2017) and ALPI data were retrieved from Fisheries and Oceans

Canada (http://www.pac.dfo-mpo.gc.ca/science/species-especes/climatology-ie/cori-

irco/indices/alpi_en.txt, accessed 16 September 2017).

The third candidate model set evaluated whether conditions prior to migration

influenced migration and thus the winter distribution of Black Oystercatchers across their

range. As broad-scale migration is only known to occur in the Alaskan breeding

population, I predicted that colder pre-migration temperatures in Alaska would lead to a

decrease in Black Oystercatchers counted in that region, mirrored by an increase in

oystercatchers counted in British Columbia, and possibly further south. This pattern

could occur if oystercatchers use temperatures in the late summer or fall as a cue to

predict winter temperatures or severity. Alternately, oystercatchers may migrate in

response to physiological cues, which could in turn be affected by pre-migration

temperatures. Most oystercatchers migrate between August and October (Johnson et al.

2010), so the decision to migrate or stay must be made before or during that period. I

used average mean daily temperatures in July and August to represent late summer

conditions, and in September and October to represent fall temperatures. This model set

included models with either late summer or fall temperature terms as interactions with

region in order to detect redistribution between regions across years. I also included the

top model from the first candidate set examining regional differences or year trends, and

versions of both temperature models that also included the regional or year trends

detected in the first candidate set (n = 5 models). Temperature data were extracted from

the NCEP data set (accessed 24 September 2017) on tiles that overlapped with the

Black Oystercatcher's Alaska range. The Alaska range shapefile was downloaded from

the Alaska Center for Conservation Science, University of Alaska, Anchorage

(http://akgap.uaa.alaska.edu/species-data/, accessed 24 September 2017).

11

I used Akaike's Information Criterion (AIC) to rank the models in the three

candidate model sets. All analyses were carried out in R version 2.15.1 (2012, The R

Foundation for Statistical Computing) using the glmmADMB (Fournier et al. 2012, Skaug

et al. 2015) and AICcmodavg (Mazerolle 2013) packages.

Results

There were clear differences in numbers of oystercatchers counted in CBC count

circles in Alaska and British Columbia compared to the other three regions (Table 2.1).

Alaska had the fewest count circles (7) and the lowest survey effort (median = 105.5 km,

IQR = 52.5 – 150.9 km), but the highest counts (median = 24, IQR range = 10 – 135).

Variation in counts was also much higher in Alaska than in other regions. The most

extreme variation was seen at the Kodiak count circle, where numbers ranged from 3

oystercatchers counted in 1980 to 902 counted in 2005 (median = 189, IQR 71.5 –

378.5, n = 40 records). British Columbia had a much higher number of count circles than

Alaska (34), but survey effort was fairly low (median = 171 km, IQR = 92 – 348 km).

Counts in British Columbia were high but varied less than counts in Alaska (median =

21, IQR = 6 – 45.5). Washington and Oregon were similar to each other in terms of

numbers of count circles (11 and 10), survey effort (Washington: median = 299 km, IQR

= 213 – 485.3 km; Oregon: median = 278 km, IQR = 217.8 – 378 km), and counts

(Washington: median = 10, IQR = 3 – 30; Oregon: median = 12, IQR = 6 – 22).

California & Baja California had the most count circles (40) and the highest survey effort

(median = 369 km, IQR = 233.5 – 482 km), with counts comparable to Washington and

Oregon (median = 12, IQR = 3.5 – 30).

Temporal trends in Black Oystercatcher winter numbers

The top model in the candidate set examining temporal trends in the numbers of

Black Oystercatchers counted on CBC surveys indicated that temporal trends varied by

region (AICc weight > 0.99; Table 2.2a & 2.3a). This model predicted increases in

oystercatchers counted in Alaska and British Columbia between 1975/1976 and

2015/2016. Counts in Washington, and California were stable or slightly increasing, and

counts in Oregon remained stable over this period (Figure 2.1).

12

Relationships between climate variables

Regional mean average daily temperatures (± SD) from January to February at

CBC count circles surveyed from 1975/1976 to 2015/2016 were as follows: Alaska =

1.45 ± 1.70 ºC, British Columbia = 2.18 ± 2.68 ºC, Washington = -0.02 ± 2.05 ºC, Oregon

= 4.58 ± 1.20 ºC, and California & Baja California = 9.60 ± 2.02 ºC. ALPI values ranged

from -3.96 to +6.69 between 1975/1976 and 2015/2016 with a mean value of +0.71 ±

2.16 SD. There was no annual trend in ALPI during that period (β = 0.01 ± 0.03 SE,

adjusted R2 = 0.02, F1,40 = 0.22, p = 0.64). Mean average daily temperatures across the

Black Oystercatcher's Alaska range were: late summer (July & August) = 9.66 ± 0.71 ºC,

fall (September & October) = 6.17 ± 0.72 ºC, winter (January & February) = -1.33 ± 1.17

ºC. Temperatures in the late summer and fall did not predict winter temperatures

(summer: β = 0.13 ± 0.27 SE, adjusted R2 = 0.02, F1,40 = 0.23, p = 0.64; fall: β = 0.25 ±

0.26, adjusted R2 = 0.003, F1,40 = 0.89, p = 0.35). Alaska temperatures in the late

summer and fall also failed to predict ALPI of the following winter (summer: adjusted R2

= 0.02, F1,39 = 0.26, p = 0.61; fall: adjusted R2 = 0.02, F1,39 = 0.02, p = 0.89).

Effects of winter conditions on Black Oystercatcher numbers in the following winter

I found some evidence to suggest that winter conditions in one year can affect

Black Oystercatcher winter numbers in the following year. The top model included both a

region × year interaction term, as well as a region × ALPI interaction term (AICc weight =

0.48; Table 2.2b, Table 2.3b), and received approximately 2.5× as much support as the

model with a region × year interaction only (AICc weight = 0.19; Table 2.2b). Counter to

expectations, counts in Alaska increased in years following deeper Aleutian Lows

(positive ALPI values) than years following milder Aleutian Lows (negative ALPI values).

ALPI showed little to no effect on counts in other regions (Fig. 2.2).

Effects of pre-migration conditions on winter distributions of Black Oystercatchers

I found no evidence that temperatures in Alaska prior to migration influenced the

distribution of Black Oystercatchers during the winter. The models that included either

the late summer or fall temperature × region interaction, which would indicate that

13

environmentally driven variation in migration influenced the subsequent distribution of

wintering Black Oystercatchers, received substantially less support than the simpler

model that only allowed temporal trends in the counts to vary by region (AICc weight =

0.89; Table 2.2c, Table 2.1a).

Discussion

My analysis of CBC counts conducted across the Black Oystercatcher's entire

range from Alaska to Mexico indicates that their global numbers are likely increasing.

The number of wintering oystercatchers counted in Alaska, British Columbia,

Washington, and California increased or remained stable over the last four decades,

while counts in Oregon remained stable. Estimates of the global population of Black

Oystercatchers as of 2014 (~15 000 individuals: Appendix) are higher than estimates in

1994 (7600 individuals) and 2001 (8900 individuals; Tessler et al. 2014), although these

increases are likely due to broader survey efforts (Tessler et al. 2014). The positive

temporal trends I found in Alaska and British Columbia are particularly welcome as these

regions are thought to contain more than half of the global breeding population. Andres

et al. (2012) estimated that 65% and 14% of the global breeding population are found in

Alaska and British Columbia, respectively. However, it should be noted that previous

estimates may have overestimated the relative importance of these two regions. The first

comprehensive surveys and assessment of oystercatcher populations in California by

Weinstein et al. (2014) increased the population estimate for that region by roughly six

times. The new estimate suggests that approximately 36% of the estimated global

breeding population is found in California (45% is found in Alaska and 10% is found in

British Columbia; Appendix).

Mass mortality of Eurasian Oystercatchers during severe cold spells has been

documented and attributed to increased metabolic costs combined with reduced prey

availability (Goss-Custard 1996). If Black Oystercatchers were sensitive to cold winters, I

expected to see lower counts in years following colder winters. However, I did not find

any evidence of temperature-related declines in Black Oystercatcher populations

between 1975/1976 and 2015/2016. Furthermore, beached bird surveys in the USA and

Canada also show no evidence for mass die-offs of Black Oystercatchers from 1986 to

2017 (13 dead Black Oystercatchers were found in surveys in the USA from 1998 to

2017: COASST 2017; only one dead oystercatcher was found in Canadian surveys from

14

1986 to 1997 and 2002 to 2017: Bird Studies Canada 2008). Differences in sensitivity of

Eurasian and Black Oystercatchers to winter temperatures may be due to the feeding

strategies of each species. Many Eurasian Oystercatchers inhabit mudflats and fields,

where they feed by probing the sand and soil for buried invertebrates. During prolonged

cold spells, the ground can freeze over, vastly reducing the food available to the birds.

By contrast, Black Oystercatchers feed mostly on molluscs that cling to rocks in the

rocky intertidal, where wave action usually prevents freezing over. Therefore,

oystercatchers may not experience the same drastic reductions in prey availability during

extreme cold spells.

Eurasian Oystercatchers also experience negative carry-over effects of severe

winters during the following summer (Duriez et al. 2012). If this were the case for Black

Oystercatchers, I expected to see lower counts in the years following colder

temperatures and deeper Aleutian Lows. Such decreases could signify that either (1)

mortality was higher in severe winters, which led to lower numbers in the following

winter, (2) oystercatcher recruitment decreased in years following harsh winters, or (3)

oystercatchers left the region (or, at least, the areas covered by count circles in the

region) following harsher winters. Curiously, I found the opposite relationship with ALPI

in Alaska, where deeper Aleutian Lows were followed by higher counts in the following

winter. This result could be spurious as there were only 7 count circles in Alaska and the

confidence intervals were very broad (Fig. 2.2). It is also possible that harsh winters

could drive oystercatchers to overwinter in more sheltered areas the following winter.

Small-scale redistributions within this region could bring more oystercatchers to areas

that are accessible to volunteer surveyors, making the birds more likely to be counted in

Christmas Bird Counts. It would be valuable to study whether winter conditions influence

future wintering strategies, and identify any mechanisms that drive this.

The relative fitness benefits of alternative migratory strategies likely depend on

environmental conditions that alter the costs and benefits of remaining at northern

latitudes year-round. I expected that the temperature in Alaska prior to migration could

predict the severity of winter conditions, leading to a change in migration rates.

Alternately, pre-migration conditions could influence the physiological state of

oystercatchers, affecting their ability to endure the average Alaska winter. In either of

these cases, I expected to find reduced numbers of oystercatchers counted on CBC

surveys in Alaska, and increased numbers in regions to the south, when pre-migration

15

temperatures were colder. However, I found no evidence that temperatures in Alaska in

the late summer and fall influenced the relative number of oystercatchers in Alaska and

in regions to the south. Temperatures in the late summer or fall prior to migration did not

predict temperatures the following winter, suggesting that temperature could not be used

by oystercatchers as a reliable cue to inform migratory strategies. There are also several

other plausible reasons that could explain the failure to detect temperature effects on the

winter distribution of Black Oystercatchers. First, migration may be a fixed rather than

facultative strategy in this species, although evidence from other bird species, including

other oystercatcher species (Van Treuren et al. 1999), suggests this is unlikely. Second,

increases in the proportion of migratory individuals in British Columbia or other regions

south of Alaska may not be detected if they occupy remote wintering grounds that are

not covered by CBC count circles. Weinstein et al. (2014) found that remote islands off

the coast of California are home to many more oystercatchers than was previously

thought, leading to a drastic increase in that state's estimated oystercatcher population.

These remote islands are inaccessible to most volunteer surveyors. Third, winter

temperature may not be the major selective force acting on partial migration in Black

Oystercatchers. Meller et al. (2016) found that fall temperatures explained temporal

variation in the proportion of residents in 9 partially migratory waterbird species in

Finland. By contrast, food availability best explained the proportion of residents in 18

partially migratory terrestrial songbirds. Meller et al. (2016) postulated that differences in

sensitivity of waterbirds and terrestrial birds to temperature could be related to the

greater dependence of waterbirds on non-frozen water for feeding. Black

Oystercatchers' foraging may not be constrained by temperature and freezing in the

same way, making food availability a more important selective force unrelated to

temperature. Further work linking climate, food availability and cues that could be used

to predict the migratory strategies of individuals and populations would be informative.

The results of my study indicate that Black Oystercatcher populations are

currently healthy, as it appears that populations are stable or increasing across their

range. In the northern extent of the species' range, more research is needed to identify

the triggers for migration and determine whether there is variation in proportions of

migrants and residents from year to year. Studies have found that both temperature and

wind speed impact survival in European Oystercatchers (Goss-Custard 1996), so it

would be worthwhile to test the effects of wind speed on Black Oystercatcher numbers

16

and migration. At the individual level, body condition may play a greater role than

environment in determining whether an individual will migrate or remain resident.

Therefore, it is also worth focussing on individual differences in future studies.

References

ALERSTAM T. (1990) Bird migration. Cambridge University Press, Cambridge, UK: 420p

ADRIAENSEN F., ULENAERS P., & DHONDT A.A. (1993) Ringing recoveries and the increase in numbers of European Great Crested Grebe Podiceps cristatus. Ardea 81: 59–70

ANDRES B.A. (1994) Year-round residency in northern populations of the Black Oystercatcher. U.S. Fish and Wildlife Service, Anchorage, AK

ANDRES B.A., SMITH P.A., MORRISON R.I.G., GRATTO-TREVOR C.L., BROWN S.C., & FRIIS C.A. (2012) Population estimates of North American shorebirds, 2012. Wader Study Group Bulletin 119: 178–194

BIRD STUDIES CANADA (2008) British Columbia beached bird survey. website: http//www.naturecounts.ca/ [accessed 29 June 2017]

BERGMAN C.M., PATTISON J., & PRICE E. (2013) The Black Oystercatcher as a sentinel species in the recovery of the Northern Abalone: Contemporary diet of Black Oystercatchers on Haida Gwaii includes an endangered prey species. Condor 115(4): 800–807

CAMPHUYSEN K.C.J., ENS B.J., HEG D., HULSCHER J.B., VAN DER MEER J., & SMIT C.J. (1996) Oystercatcher Haematopus ostralegus winter mortality in the Netherlands: The effect of severe weather and food supply. Ardea 84A: 469–492

CLARKSON P. & ZHARIKOV Y. (2007) Pacific Rim SoPR, Technical Compendium, EIMRP. Draft internal report, 9 p.

CHAPMAN B.B., BRÖNMARK C., NILSSON J.-A., & HANSSON L.-A. (2011) The ecology and evolution of partial migration. Oikos 120 (20): 1764–1775

CLAY R.P., LESTERHUIS A.J., SCHULTE S., BROWN S., REYNOLDS D., SIMONS T.R. (2010) Conservation plan for the American Oystercatcher (Haematopus palliatus) throughout the Western Hemisphere. Version 1.1. Manomet Center for Conservation Sciences, Manomet, MA. 53p

COASST: COASTAL OBSERVATION AND SEABIRD SURVEY TEAM (2017) website: https://depts.washington.edu/coasst/ [accessed 26 July 2017]

17

DURIEZ O., ENS B.J., CHOQUET R., PRADEL R., & KLAASSEN M. (2012) Comparing the seasonal survival of resident and migratory oystercatchers: carry-over effects of habitat quality and weather conditions. Oikos 121: 862–873

ENS B.J., KERSTEN M., BRENNINKMEIJER A., & HULSCHER J.B. (1992) Territory quality, parental effort, and reproductive success of oystercatchers (Haematopus ostralegus). Journal of Animal Ecology 61: 703–715

FOURNIER D.A., SKAUG H.J., ANCHETA J., IANELLI J., MAGNUSSON A., MAUNDER M., NIELSEN A., & SIBERT J. (2012) AD Model Builder: Using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optimization Methods & Software 27: 233-249

GAUTHREAUX S.A., Jr. (1982) The ecology and evolution of avian migration systems. In Avian Biology, Vol. 6 (DS Farner & SR King, eds.). Academic Press, New York & London, pp 93–167

GILLIS E.A., GREEN D.J., MIDDLETON H.A., & MORRISSEY C.A. (2008) Life history correlates of alternative migratory strategies in American Dippers. Ecology 89(6): 1687–1695

GOSS-CUSTARD J.D., ed. (1996) The oystercatcher: From individuals to populations. Oxford Ornithology Series, Oxford University Press.

HELM B., GWINNER E., & TROST L. (2006) Flexible seasonal timing and migratory behavior: Results from stonechat breeding programs. Annals of the New York Academy of Sciences. 1046(1): 216–227

JOHNSON M., CLARKSON P., GOLDSTEIN M.I., HAIG S.M., LANCTOT R.B., TESSLER D.F., & ZWEIFELHOFER D. (2010) Seasonal movements, winter range use, and migratory connectivity of the Black Oystercatcher. Condor 112(4): 731–743

LANK D.B., BUTLER R.W., IRELAND J., & YDENBERG R.C. (2003) Effects of predation danger on migration strategies of sandpipers. Oikos 103(2): 303–319

LUNDBERG P. (1987) Partial bird migration and evolutionary stable strategies. Journal of Theoretical Biology 125: 351–360

LUNDBERG P. (1988) The evolution of partial migration in birds. Trends in Ecology and Evolution 3: 172–175

KERSTEN M. & PIERSMA T. (1987) High levels of energy expenditure in shorebirds; metabolic adaptations to an energetically expensive way of life. Ardea 75: 175–187

18

KOKKO H. (2011) Directions in modelling partial migration: how adaptation can cause a population decline and why the rules of territory acquisition matter. Oikos 120: 1826–1837

MAZEROLLE M.J. (2013) AICcmodavg: Model selection and multimodel inference based on (Q)AIC(c). R package version 1.28. http://CRAN.R-project.org/package=AICcmodavg

MELLER K., VÄHÄTALO A.V., HOKKANEN T., RINTALA J., PIHA M., & LEHIKOINEN A. (2016) Interannual variation and long-term trends in proportions of resident individuals in partially migratory birds. Journal of Animal Ecology 85: 570–580

MORSE J.A., POWELL A.N., & TETREAU M.D. (2006) Productivity of Black Oystercatchers: Effects of recreational disturbance in a national park. Condor 108(3): 623–633

NEWTON I. (2010) The migration ecology of birds. Elsevier Academic Press, London, UK: 984p

PARTECKE J. & GWINNER E. (2007) Increased sedentariness in European Blackbirds following urbanization: a consequence of local adaptation? Ecology 88(4): 882–890

PULIDO F. (2011) Evolutionary genetics of partial migration – the threshold model of migration revis(it)ed. Oikos 120(23): 1776–1783

ROBINSON R.A., BAILLIE S.R., CRICK H.Q.P. (2007) Weather-dependent survival: implications of climate change for passerine population processes. Ibis 149: 357–364

SHAW A. (2016) Drivers of animal migrations and implications in changing environments. Evolutionary Ecology 30: 991, DOI: 10.1007/s10682-016-9860-5

SILLET T.S. & HOLMES R.T. (2002) Variation in survivorship of a migratory songbird throughout its annual cycle. Journal of Animal Ecology 71(2): 296–308

SKAUG H., FOURNIER D., BOLKER B., MAGNUSSON A., & NIELSEN A. (2015) Generalized Linear Mixed Models using 'AD Model Builder'. R package version 0.8.3.2

SPIEGEL C.S. (2008) Incubation patterns, parental roles, and nest survival of Black Oystercatchers (Haematopus bachmani): Influences of environmental processes and potential disturbance stimuli. Oregon State Univeristy, MSc thesis: 139 p

SURRY A.M. & KING J.R. (2015) A new method for calculating ALPI: the Aleutian Low Pressure Index. Canadian Technical Report of Fisheries and Aquatic Sciences 3135: v + 31p

19

SWINGLAND I.R. & LESSELLS C.M. (1979) The natural regulation of giant tortoise populations on Aldabra Atoll: movement polymorphism, reproductive success and mortality. Journal of Animal Ecology 48(2): 639–654

TESSLER D.F., JOHNSON J.A., ANDRES B.A., THOMAS S., & LANCTOT R.B. (2014) A global assessment of the conservation status of the Black Oystercatcher Haematopus bachmani. International Wader Studies 20: 83–96

VAN TREUREN R., BIJLSMA R., TINBERGEN J.M., HEG D., & VAN DE ZANDE L. (1999) Genetic analysis of the population structure of socially organized oystercatchers (Haematopus ostralegus) using microsatellites. Molecular Ecology 8: 181–197

WEINSTEIN A., TROCKI L., LEVALLEY R., DOSTER R.H., DISTLER T., & KRIEGER K. (2014) A first population assessment of Black Oystercatcher Haematopus bachmani in California. Marine Ornithology 42: 49–56

WIKELSKI M., TARLOW E.M., RAIM A., DIELHI R.H., LARKIN R.P., & VISSER G.H. (2003) Avian metabolism: Costs of migration in free-flying songbirds. Nature 423: 704

WOOTTON T.J. (1992) Indirect effects, prey susceptibility, and habitat selection: Impacts of birds on limpets. Ecology 73(3): 981–991

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Tables

Table 2.1 Summary of Christmas Bird Count data used for analyses of trends in Black Oystercatcher winter numbers and the effects of climate from 1975/1976 to 2015/2016. The second analysis, examining carry-over effects from winter climate conditions to numbers of oystercatchers in the following winter, used a slightly reduced data set due to gaps in the available climate data. Sample sizes for the data set used in the second analysis are shown in parentheses.

Region Median Count

± SE Median Survey Distance

± SE (km) # Count Circles # Records AK 24 ± 12.9 105.5 ± 6.35 7 (7) 140 (140) BC 21 ± 1.9 171 ± 10.09 34 (33) 595 (593) WA 10 ± 2.0 299 ± 13.52 11 (11) 185 (185) OR 12 ± 1.9 278 ± 7.70 10 (9) 193 (190) CA+BCN 12 ± 0.8 369 ± 6.07 40 (40) 771 (771) Total 15 ± 1.3 271.5 ± 4.62 102 (100) 1884 (1879)

21

Table 2.2 AIC results from model sets examining (a) trends in winter counts of Black Oystercatchers across their range from 1975/1976 to 2015/2016, (b) counts of oystercatchers in response to conditions from the previous winter, and (c) counts of oystercatchers in response to temperatures across the species' Alaska range in the late summer (July & August) and fall (September & October). Regional trend model is bolded. All models included party distance + party distance2 as a measure of effort.

(a) Model K AICc delta AICc weight Region × Year 14 14649.90 0.00 > 0.99 Region + Year 10 14673.98 24.07 < 0.01 Year 6 14681.40 31.50 < 0.01 Region 9 14782.98 133.07 < 0.01 Null 5 14793.17 143.27 < 0.01 (b) Model K AICc delta AICc weight Region × ALPIt-1 + Region × Year 19 14617.95 0.00 0.48 Region × Year 14 14619.79 1.84 0.19 Region × Winter Temperaturet-1 + Region × Year 19 14620.51 2.56 0.13 Winter Temperaturet-1 + Region × Year 15 14620.86 2.91 0.11 ALPIt-1 + Region × Year 15 14621.44 2.49 0.08 Region × Winter Temperaturet-1 14 14730.73 112.78 < 0.01 Region × ALPIt-1 14 14755.29 137.34 < 0.01 Winter Temperaturet-1 6 14757.50 139.56 < 0.01 ALPIt-1 6 14762.60 144.66 < 0.01 (c) Model K AICc delta AICc weight Region × Year 14 14649.90 0.00 0.89 Region × Fall TemperatureAK + Region × Year 19 14655.09 5.18 0.07 Region × Summer TemperatureAK + Region × Year 19 14655.73 5.82 0.05 Region × Fall TemperatureAK 14 14742.54 92.64 < 0.00 Region × Summer TemperatureAK 14 14775.04 125.14 < 0.00

22

Table 2.3 Parameter estimates for models examining (a) regional trends in winter counts of Black Oystercatchers and (b) trends with regional effects of Aleutian Low Pressure Index (ALPI) on counts in the following winter between 1975/1976 and 2015/2016.

(a) Count ~ Region × Year + Party Hours + Party Hours2, random effect = (1|Circle) Random term Var. S.D. Count Circle 1.19 1.09 n = 1884 records, 102 count circles Fixed terms Est. S.E. z p Intercept 2.65 0.45 5.92 < 0.01 Region AK BC -0.67 0.50 -1.35 0.18 WA -1.18 0.59 -2.00 0.05 OR -0.39 0.58 -0.66 0.51 CA + BCN -1.23 0.49 -2.50 0.01 Year 0.024 0.0070 3.49 < 0.01 Region × Year AK BC 0.0051 0.0078 0.65 0.52 WA -0.0044 0.0075 -0.59 0.55 OR -0.029 0.0084 -3.42 < 0.01 CA + BCN -0.0021 0.0093 -0.23 0.82 Party Hours (effort) 0.0020 0.00061 3.29 < 0.01 Party Hours2 (effort) -0.0000012 0.00000060 -2.09 0.04 (b) Count ~ Region × Year + Region × ALPI + Party Hours + Party Hours2, random = (1|Circle) Random term Var. S.D. Count Circle 1.22 1.10 n = 1879 records, 100 count circles Fixed terms Est. S.E. z p Intercept 2.44 0.46 5.31 < 0.01 Region AK BC -0.62 0.51 -1.22 0.22 WA -1.37 0.61 -2.27 0.02 OR -0.35 0.61 -0.58 0.56 CA + BCN -1.22 0.50 -2.43 0.02 Year 0.026 0.0071 3.66 < 0.01 Region × Year AK BC 0.0040 0.0080 0.50 0.62 WA 0.0014 0.0095 0.14 0.89 OR -0.031 0.0086 -3.58 < 0.01 CA + BCN -0.0037 0.0077 -0.48 0.63 ALPI 0.050 0.027 1.83 0.07 Region × ALPI AK BC -0.043 0.031 -1.38 0.17 WA 0.014 0.040 0.36 0.72 OR -0.093 0.036 -2.56 0.01 CA + BCN -0.055 0.030 -1.84 0.07 Party Hours (effort) -0.0019 0.00042 4.41 < 0.01 Party Hours2 (effort) 0.0000014 0.00000042 -3.30 < 0.01

23

Figures

Figure 2.1 Temporal trends in the observed numbers of Black Oystercatchers

on Christmas Bird Counts conducted between 1975/1976 and 2015/2016 in five regions across their range. Lines show the predicted counts in each region and shading shows 95% confidence intervals based on the top model in Table 2.2a and Table 2.2c. Parameter estimates for this model are given in Table 2.3a. Rugging shows the distribution of data in each region, with positive partial residuals across the top and negative partial residuals across the bottom.

Years since 1975/1976

Coun

t

0

100

200

300

10 20 30 40

AK BC

10 20 30 40

CA+BCN

OR

10 20 30 40

0

100

200

300

WA

24

Figure 2.2 Relationship between Aleutian Low Pressure Index (ALPI) and observed numbers of Black Oystercatchers in Christmas Bird Counts the following year. Lines show the predicted counts in each region and shading shows the 95% confidence intervals based on the top model in Table 2.2b. Parameter estimates for this model are given in Table 2.3b. Rugging shows the distribution of data in each region, with positive partial residuals across the top and negative partial residuals across the bottom.

Aleutian Low Pressure Index (t−1)

Coun

t

0

100

200

300

−4 −2 0 2 4 6

AK BC

−4 −2 0 2 4 6

CA+BCN

OR

−4 −2 0 2 4 6

0

100

200

300

WA

25

Chapter 3. The influence of the El Niño Southern Oscillation on Black Oystercatcher (Haematopus bachmani) breeding numbers in British Columbia

Introduction

Ocean climate has important and wide-ranging effects on marine ecosystems

(Doney et al. 2012). Top predators can experience these effects directly, or indirectly via

climate effects on the food web (e.g. Francis et al. 1998, Jaksic & Fariña 2010, Hazen et

al. 2013). Direct effects include climate-driven changes in metabolic rates and behaviour

that can influence survival and reproduction (Barber & Chavez 1983, Menge et al. 2009).

Indirect effects of climate are often mediated through bottom-up effects on primary

productivity (Guinet et al. 1998, Borstad et al. 2011). Some predators are influenced by

both direct and indirect climate effects. The Purple Sea Star (Pisaster ochraceus), a

keystone predator of the rocky intertidal, was found to drastically reduce feeding rates in

response to slight decreases in temperature within the species' thermal tolerance

(Sanford 1999). At the same time, climate effects on primary productivity influence these

same sea stars indirectly through bottom-up effects on recruitment and growth of their

mussel prey (Mytilus californianus; Menge et al. 2007, 2009).

Climate effects on predators may operate at both broad and local scales. Broad

scale oceanographic phenomena such as the El Niño Southern Oscillation (ENSO) can

have large impacts on primary productivity (Barber & Chavez 1983, Mellink 2003), the

phytoplankton community (Yoder & Kennelly 2003), and invertebrate recruitment and

settling (Menge et al. 2011). ENSO has consequently been shown to affect breeding and

foraging in marine avian predators along the North and South American Pacific coasts

(Mellink 2003, Jaksic 2004, Jaksic & Fariña 2010). Seabird species have generally been

found to suffer reduced breeding success during El Niño events (Surman & Nicholson

2009). However, the effects of El Niño were found to have a greater impact on specialist

piscivores than on more generalist feeders, as the specialists were less able to exploit

26

alternative food sources when their primary food sources became unavailable (Jaksic

2004, Jaksik & Fariña 2010).

On the other hand, local ocean conditions may have a more direct effect on

marine communities than broad-scale oceanographic phenomena. Phytoplankton

productivity and invertebrate recruitment frequently vary from site to site, and are often

only weakly or inconsistently correlated with global climate patterns (Navarrete et al.

2002, Menge et al. 2009, Borstad et al. 2011). Local conditions often better predict local

productivity and can influence species at higher trophic levels (Guinet et al. 1998, Wolf

et al. 2009, Borstad et al. 2011). For example, Wolf et al. (2009) found that local sea

surface height had a greater effect on the timing of breeding and breeding success in

Cassin's Auklets (Ptychoramphus aleuticus) than the Northern Oscillation Index (NOI), a

broad-scale composite climate index in the north Pacific.

The demography and population dynamics of predatory seabirds has been linked

to both broad (e.g. Velarde et al. 2002) and local (e.g. Borstad et al. 2011) climate. The

Black Oystercatcher (Haematopus bachmani) is a keystone species of the Pacific North

American coast that is known to influence the composition of the intertidal invertebrate

community (Wootton 1992). However, oystercatchers are also likely sensitive to changes

in the availability and quality of filter-feeding molluscs, which make up most of their diet

(Tessler et al. 2014). Hipfner & Elner (2013) found a negative correlation between local

spring sea surface temperatures and the number of breeding oystercatchers on Triangle

Island, British Columbia, which they attributed to changes in prey availability. In this

study I used long-term monitoring data from across British Columbia to (1) determine

long-term trends in numbers of breeding oystercatchers across British Columbia from

1962 to 2014, and (2) evaluate the nature and extent of broad- and local-scale climate

effects, including local sea surface temperature, on breeding numbers of oystercatchers

along the coast of British Columbia. This study sheds light on the influence of

environmental variables on the breeding biology of this species (Tessler et al. 2014).

27

Methods

Study species

The Black Oystercatcher is a long-lived shorebird that inhabits the rocky intertidal

zone from the Aleutian Islands in Alaska to Baja California, Mexico (Tessler et al. 2014).

They are one of North America's least abundant shorebirds, with an estimated global

population of approximately 12 500 – 17 500 (Appendix). Roughly 10% of the global

population (1000 – 2000 breeding individuals) is thought to breed in British Columbia

(Tessler et al. 2014, Appendix).

Breeding oystercatchers in British Columbia typically lay their initial clutch

between mid-May and early June (Hipfner et al. 2012). They can lay 1 – 2 replacement

clutches if the first clutch is lost (Tessler et al. 2014). On Triangle Island, replacement

clutches are laid as late as July 10 (Hipfner et al. 2012). Black Oystercatchers are

generally assumed to attempt to breed every year (Tessler et al. 2014). However,

Hipfner & Elner (2013) observed an individual that occupied a territory on Triangle Island

without breeding in 2010. This individual bred or attempted to breed at this site in every

other year from 2003 to 2012. Therefore, it is possible that Black Oystercatchers skip

breeding in some years (notably, Triangle Island experienced unfavourably warm April

sea surface temperatures in 2010; Hipfner & Elner 2013).

Breeding surveys

Oystercatcher breeding data were compiled from surveys performed by

numerous agencies in the spring and summer from 1962 to 2014. Survey dates ranged

from April 14 to August 25, with a median date of June 11. Surveys were typically

conducted by boat along suitable habitat, and beaches with suitable habitat were

searched on foot for evidence of breeding or territorial pairs of oystercatchers.

Exceptions to this were Triangle Island, where surveys were conducted only by foot, and

surveys from Vermeer et al. (1989), where beaches were searched by foot only if

oystercatchers were seen from the boat. Table 3.1 summarises the data sources and

specific survey methods used by the different agencies.

28

In addition to numbers of breeding pairs, observers typically recorded the number

of nests located but did not consistently record clutch sizes or other measures of

productivity. The number of pairs of oystercatchers observed in the final data set was

highly correlated with the number of nests located (r = 0.99, p < 0.0001), though 7.1% of

records had values for pairs but not nests. For my analyses, I examined variation in the

number of breeding pairs counted on surveys. Clutch sizes or numbers of chicks were

reported for 75.8% of nests in the final data set. Of those, 23.0% had no eggs or chicks.

It is possible that some pairs recorded held territories but did not attempt to breed, as

empty nest scrapes may remain on territories from previous years. However, it is likely

that some of these empty nests were surveyed before clutches were laid, or after eggs

or chicks were lost due to predation. After hatching, some chicks may not have been

detected on surveys as they are precocial and have effective camouflage. This could

further inflate the recorded numbers of pairs with empty nests. I assumed that all pairs

recorded had attempted to breed, as they were all observed displaying territorial or

breeding behaviour.

Survey sites were defined as either a single beach or a group of beaches in close

proximity that were always surveyed together. Each site was identified based on GPS

coordinates provided for each survey. ArcGIS was then used to measure shore lengths

for each site, and these shore lengths were used to approximate survey effort. I

excluded sites that were only surveyed in one year as I was interested in annual trends

in the numbers of breeding pairs. In the few cases where a site was surveyed more than

once in a given year, I used the record with the highest count. I subsequently grouped

sites into three broad subregions based on the similarities in latitude, geography, and

exposure to the open ocean: Haida Gwaii, the West Coast of Vancouver Island, and the

Strait of Georgia & Gulf Islands.

Climate indices and variables

I examined the impact of five broad- and local-scale climate variables on the

numbers of breeding pairs of Black Oystercatchers detected during surveys. I describe

these variables and their predicted effects on oystercatchers below.

29

Southern Oscillation Index and Pacific Decadal Oscillation

El Niño conditions are known to lower primary productivity and food availability

for marine predators (Mellink 2003). Spring productivity has, in turn, been linked to

breeding success of seabirds in British Columbia (Borstad et al. 2011). However, the

relationship between ENSO and the mollusc prey of oystercatchers is potentially

complex, since El Niño conditions can reduce food availability for molluscs (a negative

effect) while simultaneously increasing their metabolic rates and growth (a positive

effect; Menge et al. 2007). I used the Southern Oscillation Index (SOI), a measure of the

air pressure differential between Tahiti and Darwin, to describe variation in ENSO.

The Pacific Decadal Oscillation (PDO) is a longer-term pattern of warming and

cooling in the North Pacific Ocean that cycles over the course of decades. Warm PDO

events are thought to amplify El Niño effects, and counteract La Niña events. Likewise,

cool PDO events counteract El Niño and amplify La Niña (Gershunov & Barnett 1998). I

therefore predicted that the SOI effect would be stronger when coinciding with the

corresponding PDO phase, and weaker when coinciding with the opposing PDO phase.

SOI and PDO data were downloaded from the National Centers for

Environmental Information, National Oceanic and Atmospheric Administration (NOAA)

website (https://www.ncdc.noaa.gov/, accessed 7 January 2015).

North Pacific Gyre Oscillation

The North Pacific Gyre Oscillation (NPGO) is an index that describes changes in

intensity of the North Pacific Gyre, and is highly correlated with fluctuations in salinity,

nutrients, and chlorophyll (Di Lorenzo et al. 2008). NPGO has been identified as one of

the strongest correlates to mussel recruitment in the subtidal zone of the Pacific

Northwest Coast (Menge et al. 2009) as the stronger gyre brings more nutrients to the

coast, increasing primary productivity.

I predicted that a higher NPGO index during the time when mussels are

developing their gonads (January to April: Emmet et al. 1987) would have a positive

effect on the numbers of breeding pairs of oystercatchers the following year, as

increased gamete production could lead to higher larval recruitment and ultimately,

higher numbers of mussel prey for the oystercatchers to feed their young. I included

models with lagged effects of 1 – 3 years because oystercatchers preferentially target

30

older, larger mussels (Norton-Griffiths 1967, Wootton 1992). NPGO data were retrieved

from http://www.o3d.org/npgo/ (accessed 2 March 2016).

Coastal Sea Surface Temperature

Sea Surface Temperature (SST) influences productivity (Behrenfeld et al. 2006),

and by extension, the condition (Zwarts et al. 1991) and behaviour (Grenon & Walker

1981, Anestis et al. 2007) of intertidal invertebrates preyed on by oystercatchers. Warm

SST in the winter are associated with lower primary productivity, reducing food

availability while also increasing metabolic costs for marine invertebrates. As a result,

mussel mass is negatively correlated with winter sea surface temperatures (Zwarts et al.

1991). I therefore expected a negative relationship between SST (between November

and February) and the number of breeding oystercatchers in the following summer.

Warm water can also alter invertebrate behaviour, making them less vulnerable

to predators: mussels spend less time with their valves open (Anestis et al. 2007), and

limpets hold to rocks more strongly (Grenon & Walker 1981), in warmer waters. Hipfner

& Elner (2013) hypothesised that warmer waters in the spring could therefore create

unfavourable feeding conditions for Black Oystercatchers, explaining why there were

fewer oystercatcher nests on Triangle Island in warm years. I therefore expected a

negative relationship between April SST and the number of breeding pairs of

oystercatchers along the coast of British Columbia. SST data were taken from the British

Columbia Shore Station Oceanographic Program (BCSOP: http://www.pac.dfo-

mpo.gc.ca/ science/oceans/data-donnees/lighthouses-phares/index-eng.html, accessed

6 January 2015). I used monthly average SST data from 19 lighthouses (12 of which are

currently collecting data: Fig 3.1), averaging available data from all lighthouses within

each subregion.

Upwelling

Upwelling brings nutrient-rich water from the deep ocean to the surface,

increasing primary productivity. The increased productivity associated with upwelling

events may cause filter-feeding mussels and limpets to spend more time feeding

(Riisgård & Larsen 2015), making them more vulnerable to predation by oystercatchers.

Upwelling increases as SST drops and thus could explain the local SST effect on

variation in the number of breeding oystercatchers at Triangle Island in British Columbia

31

(Hipfner & Elner 2013). I therefore predicted that stronger upwelling in April would lead

to an increase in oystercatchers breeding in British Columbia in the summer.

Upwelling has also been linked to mussel recruitment. Menge et al. (2011) found

that upwelling was one of the best year-round predictors of mussel recruitment in the

subtidal zone. Furthermore, the year after an upwelling (and consequential mussel

recruitment event), they observed an increase in predatory sea stars and rock crabs. I

therefore predicted that average upwelling from January to April (Emmett et al. 1987)

would be related to the number of oystercatchers breeding 1, 2, or 3 years later, with

longer time lags being predicted by oystercatcher preferences for large mussels (see

North Pacific Gyre Oscillation section). Upwelling data were obtained from the Pacific

Fisheries Environmental Laboratory (PFEL: http://www.pfeg.noaa.gov/products/PFEL/

modeled/indices/upwelling/NA/data_download.html, accessed 2 February 2015).

Upwelling data are provided at a series of points that are off-coast at 3º latitude intervals.

There are three points with upwelling measurements along the coast of British Columbia:

48º N, 125º W; 51º N, 131º W; and 54º N, 134º W. I assigned the upwelling values of the

closest of these points to each breeding site. Because Vancouver Island creates a

geographical barrier between the Strait of Georgia & Gulf Islands and the points off the

coast at which upwelling was measured, I did not anticipate an upwelling effect in this

subregion. Thus, models examining the effect of upwelling included a subregion ×

upwelling interaction term.

Analyses

I created two candidate model sets to examine (1) temporal trends in the number

of breeding Black Oystercatcher pairs in British Columbia and (2) the influence of broad-

and local-scale climate variables on the number of pairs of oystercatchers detected in

breeding surveys across British Columbia. I fitted generalised linear mixed models with a

negative binomial distribution that included site as a random term and shore length as an

offset variable. Models fitted with a negative binomial distribution outperformed those

with a zero-inflated negative binomial or a Poisson distribution (AICc weights: negative

binomial = 0.74, zero-inflated negative binomial = 0.26, and Poisson = < 0.01).

The first candidate set included all univariate combinations of year (trend) and

subregion and a null model (n = 5 models). The second candidate set included 11

32

climate models with and without regionally-specific temporal effects, and the two

highest-ranked models from the first analysis (n = 23 models). I used Akaike's

Information Criterion (AIC) to rank the models in the two candidate model sets. All

analyses were carried out in R version 2.15.1 (2012, The R Foundation for Statistical

Computing) using the glmmADMB (Fournier et al. 2012, Skaug et al. 2015) and

AICcmodavg (Mazerolli 2013) packages.

Results

The data set included 190 sites monitored for 2 – 18 years (mean = 6.7 ± 5.2

SD). Haida Gwaii contained the most sites (n = 111 sites), followed by the Strait of

Georgia & Gulf Islands (n = 45 sites) and the West Coast of Vancouver Island (n = 34

sites). Survey dates ranged from 1971 – 2007 in Haida Gwaii, 1962 – 2014 on the West

Coast of Vancouver Island, and 1978 – 2011 in the Strait of Georgia & Gulf Islands.

Shore lengths were positively skewed, and varied significantly between subregions.

Haida Gwaii had the longest shore lengths (median length = 1058 m, IQR = 405 – 2211

m), followed by the West Coast of Vancouver Island (median length = 604 m, IQR = 244

– 136 m), and the Strait of Georgia & Gulf Islands (median length = 389 m, IQR = 215 –

647 m).

The numbers of, and variation in, pairs of Black Oystercatchers observed in

breeding surveys varied by subregion. The West Coast of Vancouver Island had the

most variation in breeding numbers, with a median count of 2 breeding pairs per site

(IQR = 1 – 6 pairs). Cleland Island and Triangle Island, the two sites with the consistently

highest breeding counts, were included in this subregion (Cleland Island: median count

= 39 breeding pairs, IQR = 35 – 45 breeding pairs; Triangle Island: median count = 14

breeding pairs, IQR = 11 – 15 breeding pairs). Haida Gwaii also had a median count of 2

breeding pairs per site, but variation was lower (IQR = 1 – 4 breeding pairs per site). The

Strait of Georgia & Gulf Islands had the lowest counts, with a median count of 1

breeding pair per site (IQR = 1 – 2 breeding pairs per site). The median count for the

overall data set was 2 breeding pairs per site (IQR = 1 – 4 breeding pairs per site).

33

Temporal trends in numbers of Black Oystercatcher breeding pairs

I found little to suggest that the number of breeding pairs of Black Oystercatchers

in British Columbia have changed significantly since the 1960s. The top model in the

candidate set examining temporal trends in the number of breeding pairs was the null

model (AICc weight = 0.33; Table 3.2a & 3.3a). This model received twice the support of

the 3rd-ranked model, which included year (AICc weight = 0.15; Table 3.2a). There was

some model uncertainty since the second-ranked model that included a subregion ×

year (trend) interaction received a similar level of support as the top model (AICc weight

= 0.28; Table 3.2a).

Relationships between selected climate variables

April SOI values ranged between -1.4 (mild El Niño conditions) and +1.9 (mild La

Niña conditions), and did not show a temporal trend between 1962 and 2014 (β = 0.0027

± 0.0075 SE, adjusted R2 = 0.016, F1,51 = 0.13, p = 0.72). SOI was negatively correlated

to PDO (β = -0.41 ± 0.10 SE, adjusted R2 = 0.22, F1,51 = 16.09, p = 0.00020), indicating

that warm phases of ENSO corresponded to warm phases of PDO, and cool phases of

ENSO coincided with cool phases of PDO (note that, unlike SOI, negative values

correspond to cool phases of the PDO while positive values correspond to warm phases

of the PDO). SST did not change significantly over the years when surveys were

conducted in British Columbia (Haida Gwaii: β = 0.0055 ± 0.0121 SE, adjusted R2 =

0.031, F1,25 = 0.21, p = 0.65; West Coast of Vancouver Island: β = 0.011 ± 0.006 SE,

adjusted R2 = 0.061, F1,30 = 3.02, p = 0.093; Strait of Georgia & Gulf Islands: β = -0.0094

± 0.0093 SE, adjusted R2 = 0.0019, F1,13 = 1.03, p = 0.33). SST was higher during the

warm phase of ENSO (Haida Gwaii: β = -0.43 ± 0.10 SE, adjusted R2 = 0.41, F1,25 =

19.40, p = 0.00017; West Coast of Vancouver Island: β = -0.32 ± 0.12 SE, adjusted R2 =

0.15, F1,30 = 6.65, p = 0.015; Strait of Georgia & Gulf Islands: β = -0.24 ± 0.11 SE,

adjusted R2 = 0.22, F1,13 = 5.00, p = 0.044).

Climate effects on numbers of Black Oystercatcher breeding pairs

I found evidence of ENSO effects on the numbers of breeding pairs of Black

Oystercatchers counted in surveys across British Columbia. The four top-ranked models

all included SOI as a fixed effect (Table 3.2b) and indicated that the number of breeding

34

pairs of Black Oystercatchers was related to the SOI (Table 3.3b, Fig 3.3). The top

ranked model included only the SOI term, and estimated a 30% increase in the number

of breeding oystercatcher pairs over an SOI range of -1.5 (indicative of mild El Niño

conditions) to +1.9 (mild La Niña conditions). This model received 1.7× the support of a

model that included SOI in addition to terms that allowed temporal trends in breeding

pairs to vary with subregion, 2.8× the support of a model that allowed SOI effects to be

moderated by the PDO, and 42× the support of the null model (Table 3.2b).

In contrast, I found no evidence that winter or spring sea surface temperature

influenced numbers of breeding pairs of black oystercatchers across British Columbia.

Models with the winter or April SST term alone or in combination with terms that allowed

temporal trends to vary subregionally received similar levels of support to the null model

(Table 3.2b). I also found no evidence to suggest that variation in the NPGO or upwelling

influenced the breeding propensity of oystercatchers. Models that included NPGO (with

a 1, 2, or 3 year lag) and upwelling (in April and in the winter with a 1, 2, or 3 year lag)

received less support than the null model (Table 3.2b).

Discussion

I found that the number of Black Oystercatcher pairs counted on breeding

surveys in British Columbia remained stable from 1962 to 2014. Numbers of breeding

pairs appeared to be sensitive to conditions in the spring related to the El Niño Southern

Oscillation (ENSO), with fewer pairs counted in years with El Niño conditions than in

years with La Niña conditions. Breeding in oystercatchers is limited by availability of

territories (Tessler et al. 2014), which creates an upper limit to the numbers of

oystercatchers that can breed per year in a given area. On the other hand, breeding

numbers are likely buffered on the lower end by a sizeable pool of nonbreeding birds

that fill vacated territories as they become available (as found in Eurasian

Oystercatchers: Heg et al. 2000). For these reasons, numbers of breeding pairs are

likely a better representation of the quality and availability of intertidal habitat than of

oystercatcher population size. Therefore, decreases in numbers of breeding

oystercatchers could indicate that either (1) available habitat is shrinking or becoming

unsuitable (Hazlitt 2001), (2) anthropogenic disturbance is increasing in severity

(Warheit et al. 1984, Spiegel 2008), or (3) climatic conditions are becoming unfavourable

to breeding (Hipfner & Elner 2013). I found no evidence that these threats impacted

35

breeding in Black Oystercatchers across British Columbia during the time period of the

study.

Climate conditions related to the El Niño Southern Oscillation (ENSO) have been

shown to influence foraging and breeding success in marine birds (Mellink 2003, Jacksic

& Fariña 2010). El Niño effects on seabirds are generally negative (Surman & Nicholson

2009). However, species that specialise on fish have few alternative feeding options

when their food source is impacted. As such, they tend to be more impacted by El Niño

conditions than bird species with more omnivorous diets (Jaksic 2004). Here, I show that

ENSO is associated with a modest but significant fluctuation in the numbers of breeding

Black Oystercatchers at survey sites across British Columbia. This study therefore

provides additional evidence for the effect of broad-scale climate phenomena

(specifically ENSO) on reproduction in marine birds. ENSO is modulated by the Pacific

Decadal Oscillation (PDO), as the effects of El Niño and La Niña have been found to be

more consistent when coinciding with the corresponding PDO phase (Gershunov &

Barnett 1998). Despite this, I did not find evidence that a SOI × PDO interaction had an

effect on the numbers of breeding oystercatchers in British Columbia (Table 3.2b). As

SOI and PDO were correlated in this data set (see results), the addition of a SOI × PDO

interaction term would have complicated the model without improving it enough to earn it

a higher AICc rank.

Local climate conditions act directly on populations, and therefore often have a

stronger effect on seabird biology than broad-scale climate indices (e.g. Wolf et al.

2009). Hipfner & Elner (2013) found a negative relationship between local spring SST

and breeding propensity in Black Oystercatchers at one site, which they suggested could

be due to climate effects on prey behaviour. Therefore, I expected numbers of Black

Oystercatcher breeding pairs to be higher when spring SST was cooler and upwelling

was stronger. However, I found no evidence that either SST or upwelling in the spring

influenced the number of breeding Black Oystercatchers at a broad scale across British

Columbia. ENSO is associated with warm local SST under El Niño conditions and cool

SST under La Niña conditions (Stenseth et al. 2002, and see results). However, ENSO

also influences other local climatic variables, such as precipitation (Ropelewski et al.

1986). The findings presented here suggest that oystercatchers breeding in British

Columbia are not influenced by April SST or upwelling alone, but perhaps by some

36

combination of local climate variables whose interactions are encapsulated to some

extent within ENSO (sensu Hallett et al. 2004).

Climate effects on recruitment of prey species may cause lagged effects on

predators that target mature prey (Menge et al. 2011). As oystercatchers preferentially

target larger prey (Norton-Griffiths 1967, Wootton 1992), I expected that climate

conditions favourable to mollusc recruitment would lead to an increase in prey

availability and oystercatcher breeding propensity in subsequent years. However, I found

no evidence for lagged effects of climate on oystercatcher breeding numbers. I may

have failed to detect lagged effects of NPGO and upwelling on oystercatcher breeding

for a few reasons. First, increases in prey recruitment due to climate may correspond to

reductions in prey size. Mussel populations are limited by available space, and

increased crowding due to recruitment of juvenile mussels can reduce mussel growth

(Petraitis 1995). Second, the climate effects on mollusc recruitment were found in the

subtidal zone (Menge et al. 2009), not the intertidal where oystercatchers feed.

Relationships between climate, mussel recruitment, and/or mussel growth may differ

between the two habitats (Rilov et al. 2008). While I found no overall effect of lagged

climate variables on breeding in Black Oystercatchers, there are several stages in the

life histories of molluscs and oystercatchers alike where the influence of climate may be

lagged. Future studies that examine more direct climate effects on oystercatchers or

their prey could help establish clearer relationships between environmental variables

and biological populations.

The stable wintering (Ch. 2) and breeding trends in Black Oystercatchers over

the last 40 – 50 years in British Columbia are encouraging for this species. However,

climate change is expected to introduce new threats such as sea level rise that could

greatly reduce the oystercatcher's habitat (Langham et al. 2015). The relationship

between ENSO and climate change are poorly understood (Collins et al. 2010), so it is

unclear how oystercatcher breeding will be affected in the future. It is therefore important

to continue monitoring oystercatcher populations so that changes can be detected if, and

when, they occur. The decades of survey data compiled and used in this study will

provide a valuable baseline for future monitoring efforts.

37

References

ANESTIS A., LAZOU A., PÖRTNER H.O., MICHAELIDIS B. (2007) Behavioral, metabolic, and molecular stress responses of marine bivalve Mytilus galloprovincialis during long-term acclimation at increasing ambient temperature. American Journal of Physiology. Regulatory, Comparative, and Comparative Physiology. 293(2): 911–921

BARBER R.T. & CHAVEZ F.P. (1983) Biological consequences of El Niño. Science 222: 1203–1210

BEHRENFELD M.J., O'MALLEY R.T., SIEGEL D.A., MCCLAIN C.R., SARMIENTO J.L., FELDMAN G.C., MILLIGAN A.J., FALKOWSKI P.G., LETELIER R.M., & BOSS E.S. (2006) Climate-driven trends in contemporary ocean productivity. Nature Letters 444: 752–755

BORSTAD G., CRAWFORD W., HIPFNER M.J., THOMSON R., & HYATT K. (2011) Environmental control of the breeding success of rhinoceros auklets at Triangle Island, British Columbia. Marine Ecology Progress Series 424: 285–302

COLLINS M., AN S.-I., CAI W., GANACHAUD A., GUILYARDI E., JIN F.-F., JOCHUM M., LENGAIGNE M., POWER S., TIMMERMANN A., VECCHI G., & WITTENBERG A. (2010) The impact of global warming on the tropical Pacific Ocean and El Niño. Nature Geoscience 3: 391–397

DI LORENZO E., SCHNEIDER N., COBB K.M., CHHAK K., FRANKS P.J.S., MILLER A.J., MCWILLIAMS J.C., BOGRAD S.J., ARANGO H., CURCHISTER E., POWELL T.M., & RIVERE P. (2008) North Pacific Gyre Oscillation links ocean climate and ecosystem change. Geophysical Research Letters 35: L08607, doi:10.1029/2007GL032838

DONEY S.C., RUCKELSHAUS M., DUFFY J.E., BARRY J.P., CHAN F., ENGLISH C.A., GALINDO H.M., GREBMEIER J.M., HOLLOWED A.B., KNOWLTON N., POLOVINA J., RABALAIS N.N., SYDEMAN W.J., & TALLEY L.D. (2012) Climate change impacts on marine ecosystems. Annual review of Marine Science 4: 11–37

EMMET B., Thompson K., & POPHAM J.D. (1987) The reproductive and energy storage cycles of two populations of Mytilus edulis (Linne) from British Columbia. Journal of Shellfish Research 6 (1): 29–26

FOURNIER D.A., SKAUG H.J., ANCHETA J., IANELLI J., MAGNUSSON A., MAUNDER M., NIELSEN A., & SIBERT J. (2012) AD Model Builder: Using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optimization Methods & Software 27: 233-249

38

FRANCIS R.C., HARE S.R., HOLLOWED A.B., & WOOSTER W.S. (1998) Effects of interdecadal climate variability on the oceanic ecosystems of the NE Pacific. Fisheries Oceanography 7: 1–21

GERSHUNOV A. & BARNETT T.P. (1998) Interdecadal modulation of ENSO teleconnections. Bulletin of the American Meteorological Society 79(12): 2715-2725

GRENON J.F. & WALKER G. (1981) The tenacity of the limpet, Patella vulgata L.: An experimental approach. Journal of Marine Biology and Ecology 54(3): 277–308

GUINET C., CHASTEL O., KOUDIL M., DURBEC J.P., & JOUVENTIN P. (1998) Effects of warm sea-surface temperature anomalies on the Blue Petrel at the Kerguelen Islands. Proceedings of the Royal Society of London B 265(1400): 1001–1006

HALLETT T.B., COULSON T., PILKINGTON J.G., CLUTTIN-BROCK T.H., PEMBERTON J.M., & GRENFELL B.T. (2004) Why large-scale climate indices seem to predict ecological processes better than local weather. Letters to Nature 430: 71–75

HAZEN E.L., JORGENSON S., RYKACZOUSKI R.R., BOGRAD S.J., FOLEY D.G., JONSEN I.D., SHAFFER S.A., DUNNE J.P., COSTA D.P., CROWDER L.B., & BLOCK B.A. (2013) Predicted habitat shifts of Pacific top predators in a changing climate. Nature Climate Change 3: 234–238

HAZLITT, S.L. (2001) Territory quality and reproductive success of Black Oystercatchers in British Columbia. The Wilson Bulletin 113 (4): 404–409

HAZLITT S.L. & BUTLER R.W. (2001) Site fidelity and reproductive success of Black Oystercatchers in British Columbia. Waterbirds 21 (2): 203–207

HEG D., ENS B.J., VAN DER JEUGD H.P., BRUINZEEL L.W. (2000) Local dominance and territorial settlement of nonbreeding oystercatchers. Behaviour 137:473 – 530

HIPFNER J.M. & ELNER R.W. (2013) Sea-surface temperature affects breeding density of an avian rocky intertidal predator, the Black Oystercatcher Haematopus bachmani. Journal of Experimental Marine Biology and Ecology 440: 29–34

HIPFNER J.M., MORRISON K.W., & KOUWENBERG A.-L. (2012) Biology of Black Oystercatchers breeding on Triangle Island, British Columbia, 2003–2011. Northwestern Naturalist 93: 145–153

JAKSIC F.M. (2004) El Niño effects on avian ecology: Lessons learned form the southeastern Pacific. Ornitologia Neotropical (Suppl.) 15: 61–72

39

JAKSIC F.M. & FARIÑA J.M. (2010) El Niño and the birds: A resource-based interpretation of climatic forcing in the Southeastern Pacific. Anales del Instituto de la Patagonia 38: 121–140

LANGHAM G.M., SCHUETZ J.G., DISTLER T., SOYKAN C.U., & WILSEY C. (2015) Conservation status of North American birds in the face of future climate change. PLoS ONE 10(9): e0135350. https://doi.org/10.1371/journal.pone.0135350

MAZEROLLE M.J. (2013) AICcmodavg: Model selection and multimodel inference based on (Q)AIC(c). R package version 1.28. http://CRAN.R-project.org/package=AICcmodavg

MELLINK E. (2003) Effects of the 1997–1998 El Niño and 1998–1999 La Niña on breeding waterbirds and sea lions in the upper Gulf of California, Mexico. Geofísica Internacional 42: 539–546

MENGE B.A., CHAN F., & LUBCHENCO J. (2007) Response of a rocky intertidal ecosystem engineer and community dominant to climate change. Ecology Letters 11(2): 151–162

MENGE B.A., CHAN F., NIELSEN K.J., DI LORENZO E., & LUBCHENCO J. (2009) Climatic variation alters supply-side ecology: impact of climate patterns on phytoplankton and mussel recruitment. Ecological Monographs 79(3): 379–395

MENGE B.A., GOUHIER T.C., FREIDENBURD T., & LUBCHENCO J. (2011) Linking long-term, large-scale climatic and environmental variability to patterns of marine invertebrate recruitment: Toward explaining "unexplained" variation. Journal of Marine Biology and Ecology 400: 236–249

NAVARRETE S.A., BROITMAN B., WIETERS E.A., FINKE G.R., VENEGAS R.M., & SOTOMAYOR A. (2002) Recruitment of intertidal invertebrates in the southeast Pacific: Interannual variability and the 1997–1998 El Niño. Limnology & Oceanography 47(3): 791–802

NORTON-GRIFFITHS M. (1967) Some ecological aspects of the feeding behaviour of the Oystercatcher Haematopus ostralegus on the edible mussel Mytilus edulus. Ibis 109: 412–424

PETRAITIS P.S. (1995) The role of growth in maintaining spatial dominance by mussels (Mytilus edulis). Ecology 76(4): 1337–1346

RIISGÅRD H.U. & LARSEN P.S. (2015) Physiologically regulated valve-closure makes mussels long-term starvation survivors: test of hypothesis. Journal of Molluscan Studies 81(2): 303–307

RILOV G., DUDAS S.E., MENGE B.A., GRANTHAM B.A., LUBCHENCO J., & SCHIEL D.R. (2008) The surf zone: a semi-permeable barrier to onshore recruitment of invertebrate larvae? Journal of Experimental Marine Biology and Ecology 361: 59–74

40

ROPELEWSKI C.F. & HALPERT M.S. (2002) North American precipitation and temperature patterns associated with the El Niño/Southern Oscillation (ENSO). Monthly Weather Review 114: 2352–2362

SANFORD E. (1999) Regulation of keystone predation by small changes in ocean temperature. Science 283(5410): 2095–2097

SKAUG H., FOURNIER D., BOLKER B., MAGNUSSON A., & NIELSEN A. (2015) Generalized Linear Mixed Models using 'AD Model Builder'. R package version 0.8.3.2

SPIEGEL C.S. (2008) Incubation patterns, parental roles, and nest survival of Black Oystercatchers (Haematopus bachmani): Influences of environmental processes and potential disturbance stimuli. Oregon State Univeristy, MSc thesis: 139pp

STENSETH N.C., MYSTERUD A., OTTERSEN G., HURRELL J.W., CHAN K.-S., & LIMA M. (2002) Ecological effects of climate fluctuations. Science 297: 1292–1296

SURMAN C.A. & NICHOLSON L.W. (2009) The good, the bad, and the ugly: ENSO-driven oceanographic variability and its influence on seabird diet and reproductive performance at the Houtman Abrolhos, eastern Indian Ocean. Marine Ornithology 37: 129–138

TESSLER D.F., JOHNSON J.A., ANDRES B.A., THOMAS S., & LANCTOT R.B. (2014) A global assessment of the conservation status of the Black Oystercatcher Haematopus bachmani. International Wader Studies 20: 83–96

VELARDE E., EZCURRA E., CISNEROS-NATA M.A., & LAVIN M.F. (2002) Seabird ecology, El Niño anomalies, and prediction of sardine fisheries in the Gulf of California. Ecological Applications 14: 607–615

VERMEER K., MORGAN K.H., SMITH G.E.J. (1989) Population and nesting habitat of American Black Oystercatchers in the Strait of Georgia. In: VERMEER K. & BUTLER R.W., eds. The ecology and status of marine and shoreline birds in the Strait of Georgia, British Columbia. Canadian Wildlife Service Occasional Paper 75: 118–122

WARHEIT K.I., LINDBERG D.R., BOEKELHEIDE R.J. (1984) Pinniped disturbance lowers reproductive success of black oystercatcher Haematopus bachmani (Aves). Marine Ecology Progress Series 17: 101–104

WOLF S.G., SYDEMAN W.J., HIPFNER J.M., ABRAHAM C.L., TERSHY B.R., & CROLL D.A. (2009) Range-wide reproductive consequences of ocean climate variability for the seabird Cassin's Auklet. Ecology 90(3): 742–753

WOOTTON T.J. (1992) Indirect effects, prey susceptibility, and habitat selection: Impacts of birds on limpets. Ecology 73(3): 981–991

41

YODER J.A. & KENNELLY M.A. (2003) Seasonal and ENSO variability in global ocean phytoplankton chlorophyll derived from 4 years of SeaWiFS measurements. Global Biogeochemical Cycles 17(4), DOI: 10.1029/2002GB001942

ZWARTS L. (1991) Seasonal variation in body weight of the bivalves Macoma balthica, Scrobicularia plana, Mya arenaria, and Cerastoderma edule in the Dutch Wadden Sea. Netherlands Journal of Sea Research 28(3): 231–245

42

Tables

Table 3.1 Sources and details of Black Oystercatcher breeding surveys in British Columbia, including areas surveyed, time of surveys, and survey methods. Preliminary surveys were performed from the boat except on Triangle Island, and sites were then searched more thoroughly by foot.

Study/Author Area Surveyed

What Was Surveyed

Survey Window Year(s)

When To Land

What Was Noted On Land

Vermeer et al. Nanaimo to Chain Islands, Northern GI, Race Rocks

all islands and islets

June, July

1987 if BLOY seen

presence or absence of young and nests; vegetation; nest site characteristics

Gulf Islands National Park

Nanaimo to Chain Islands, Northern GI, Race Rocks

islands and islets with suitable habitat

mid-June 2005 to 2012

always number of eggs, chicks, nests searched

Butler & Golumbia

Nanaimo to Chain Islands, Northern GI, Race Rocks

all islands and islets

mid-June 1997, 1999, 2005 to 2006

all except Vancouver to Cortes leg

number of eggs and chicks

Triangle Triangle Island

all beaches Mid-June to Aug

2003 to 2012

N/A shoreline search, nest monitoring for fate, egg count

Canadian Wildlife Service

North Coast, Haida Gwaii, Scott Islands

all beaches April to June

1980's always empty, egg, young, adult count, nest material

Gwaii Haanas National Park, Laskeek Bay

Lost Island to Alder Island, Cumshewa to Hassell

all suitable habitat

early June to July

1992 to 2012

always occupied, active, breeding evidence

Pacific Rim National Park

high density core area

all habitat in dense area

late May to early June

2000 to 2012

always nest contents, adult count

Hazlitt Nanaimo to Chain Islands, Northern GI, Race Rocks

all habitat three visits

1996 to 1998

always

RBCPM Pacific Rim Park

incidental varying 1962 to 1873

unknown nest contents, some adult behaviour

43

Table 3.2 AIC table for analysis of (a) Trends in numbers of breeding pairs of Black Oystercatchers and (b) climate effects on numbers of breeding pairs of Black Oystercatchers in British Columbia (n = 760 records at 193 sites). Null and subregional trend models are bolded. All models assumed a negative binomial distribution and included log-transformed shore length as an offset variable and site as a random variable.

(a) Model K AICc delta AICc weight Null 3 3080.01 0.00 0.33 Subregion × Year 8 3080.37 0.36 0.28 Subregion 5 3081.46 1.45 0.16 Year 4 3081.53 1.52 0.15 Subregion + Year 6 3082.89 2.88 0.08 (b) Model K AICc delta AICc weight SOIApril 4 3072.55 0.00 0.42 SOIApril + Subregion × Year 9 3073.60 1.05 0.25 SOIApril × PDOApril 6 3074.61 2.06 0.15 SOIApril × PDOApril + Subregion × Year 11 3076.57 4.02 0.06 SSTApril + Subregion × Year 9 3079.44 6.89 0.01 NPGOt-3 + Subregion × Year 9 3079.48 6.93 0.01 SSTNovember–February + Subregion × Year 9 3079.58 7.03 0.01 SSTApril 4 3079.99 7.44 0.01 Null 3 3080.01 7.46 0.01 Subregion × Year 8 3080.37 7.82 0.01 NPGOt-1 4 3080.77 8.22 0.01 NPGOt-3 4 3080.81 8.26 0.01 NPGOt-1 + Subregion × Year 9 3081.10 8.55 0.01 SSTNovember–February 4 3081.17 8.62 0.01 Subregion × Upwellingt-3 8 3081.67 9.12 <0.01 Subregion × Upwellingt-2 + Subregion × Year 11 3082.01 9.46 <0.01 NPGOt-2 4 3082.03 9.48 <0.01 Subregion × Upwellingt-3 + Subregion × Year 11 3082.09 9.54 <0.01 NPGOt-2 + Subregion × Year 9 3082.40 9.85 <0.01 Subregion × Upwellingt-2 8 3084.37 11.82 <0.01 Subregion × UpwellingApril + Subregion × Year 11 3085.85 13.30 <0.01 Subregion × Upwellingt-1 + Subregion × Year 11 3086.15 13.60 <0.01 Subregion × UpwellingApril 8 3086.35 13.80 <0.01 Subregion × Upwellingt-1 8 3086.91 14.36 <0.01

44

Table 3.3 Parameter estimates for (a) null model showing no effect of trends in numbers of breeding pairs of of Black Oystercatchers and (b) effect of the mean April Southern Oscillation Index (SOI) on numbers of breeding pairs of Black Oystercatchers counted on surveys conducted across British Columbia between 1962 and 2014.

(a) Pairs ~ 1 + offset(log(Shore Length)), random = (1|Site) Random term Var. S.D. Site 1.67 1.29 n = 760 records, 193 sites Fixed terms Est. S.E. z p Intercept -5.95 0.10 -59.10 < 0.01 (a) Pairs ~ SOI + offset(log(Shore Length)), rand. = (1|Site) Random term Var. S.D. Site 1.67 1.29 n = 760 records, 193 sites Fixed terms Est. S.E. z p Intercept -5.96 0.10 -59.30 < 0.01 SOI 0.079 0.025 3.12 < 0.01

45

Figures

Figure 3.1 Sites of lighthouses in British Columbia recording daily sea surface temperatures and salinity as of 2018. The year in parentheses next to the name of each site indicates the year in which data collection began. 7 lighthouses that no longer collect data are not shown. Source: http://www.pac.dfo-mpo.gc.ca/science/oceans/data-donnees/lightstations-phares/index-eng.html (accessed 21 August 2018)

46

Figure 3.2 Numbers of breeding pairs of Black Oystercatchers at breeding sites in British Columbia from 1962 to 2014. Subregions are denoted by colour (red = Haida Gwaii, blue = Strait of Georgia & Gulf Islands, and green = west coast of Vancouver Island).

47

Figure 3.3 Relationship between the Southern Oscillation Index (SOI) in April and numbers of breeding pairs of Black Oystercatchers at survey sites in British Columbia between 1962 and 2014. The line shows the relationship, and the shaded area shows the 95% confidence interval from the top model in Table 3.2b. Parameter estimates for the model are given in Table 3.3b. Rugging shows the distribution of data.

−1.5 −1.0 −0.5 0.0 0.5 1.0 1.5 2.0

1.0

1.2

1.4

1.6

1.8

2.0

2.2

Southern Oscillation Index

Bree

ding

Pai

r Cou

nts

48

Chapter 4. Conclusions

The Black Oystercatcher plays an important ecological role as a top intertidal

predator in some regions (Wootton 1992) and is considered an indicator species for the

rocky intertidal coast of the Pacific northwest (Clarkson & Zharikov 2007, Parks Canada

2012a, Parks Canada 2012b, Bergman et al. 2013). Given the threat that a changing

climate could pose to this species (Langham et al. 2015), it is important that populations

are monitored and the species' biology and ecology are studied to determine whether

conservation efforts are needed. In this thesis, I used Christmas Bird Count data from

1975/1976 to 2015/2016 and breeding survey data in British Columbia from 1962 to

2014 to examine long-term trends in wintering and breeding numbers of Black

Oystercatchers over time and with respect to several climate variables. In Chapter 2, I

found that numbers of wintering oystercatchers counted in Christmas Bird Count surveys

have generally increased between 1975/1976 and 2015/2016. I found some evidence

that winter conditions affect oystercatcher numbers counted in Christmas Bird Counts in

subsequent years. However, the relationship was counterintuitive: deeper Aleutian Lows

resulted in higher counts in Alaska. In Chapter 3, I found that the numbers of Black

Oystercatchers breeding in British Columbia remained generally stable from 1962 to

2014. Finally, I found that the El Niño Southern Oscillation (ENSO), a global climate

phenomenon, influenced oystercatcher breeding numbers in British Columbia during that

time. Breeding numbers increased in years with La Niña conditions (cool SST and

increased precipitation) in April and decreased in years with El Niño conditions (warm

SST, decreased precipitation; Ropelewski et al. 2002).

Black Oystercatchers are one of North America's least abundant shorebirds

(fewer than 18 000 birds; Appendix), and this small population makes it potentially

vulnerable to perturbation (Tessler et al. 2014). That said, the overall increase in Black

Oystercatchers counted in CBC surveys over time (Ch. 2) is consistent with suggestions

that populations are stable or slightly increasing (Hazlitt 2001a, Tessler et al. 2014,

Weinstein et al. 2014, Meehan et al. 2018). Improvements in survey data in California

resulted in an approximately six-fold increase in population estimates for that region

49

(Tessler et al. 2014, Weinstein et al. 2014, Appendix). Likewise, improved surveys

across the species' range could lead to further increases in population estimates in other

regions. Numbers of breeding oystercatcher pairs remained stable overall in British

Columbia between 1962 and 2014 (Ch. 3), but population trends in breeding and

nonbreeding birds are not known.

Broad-scale climate phenomena appear to influence oystercatcher winter

abundances, as well as breeding numbers. Winter numbers in Alaska and breeding

numbers in British Columbia were linked to the previous year's Aleutian Low (Ch. 2) and

April ENSO (Ch. 3), respectively. It is unclear why a deeper Aleutian Low had an

unexpected positive effect on counts in Alaska, and this may have been a spurious

result due to the small number of count circles in Alaska. It seems unlikely that breeding

would increase in Alaska in summers following deeper Aleutian Lows. Deeper Aleutian

Lows have been linked to El Niño conditions (Hoerling et al. 1997), and during the years

covered by the Christmas Bird Count data used in this study (1975/1976 to 2015/2016),

deeper Aleutian Lows (positive ALPI values; measured from December to March) tended

to be followed by warm phase ENSO conditions in the spring (negative SOI values;

April): ALPI was negatively related to mean April SOI (β = -0.16 ± 0.05 SE, adjusted R2 =

0.17, F1, 39 = 8.90, p = 0.005). Based on the relationship between ENSO and

oystercatcher breeding numbers in British Columbia (Ch. 3), I would expect fewer

breeding pairs and possibly fewer chicks in the years following winters with deeper

Aleutian Lows. This would be more likely to manifest as lower, not higher, CBC counts. I

also found no evidence of migration between regions in response to ALPI (Ch. 2), and it

seems unlikely that numbers of resident oystercatchers in Alaska would increase in the

year after a winter with a deeper Aleutian Low. If this result represents a real relationship

and not a spurious result, a more plausible explanation for this pattern is redistribution

within Alaska (see Ch. 2). Tracking and observing individual birds over multiple seasons

and years could help explain this phenomenon.

The cues for migration in Black Oystercatchers remain unclear. While I examined

a number of local and broad-scale climate variables using linear models, other variables

not examined here, such as wind speed, may influence oystercatcher feeding and

migration behaviour, as well (Goss-Custard 1996). Further studies should also examine

the effects of severe winters and extreme weather events on oystercatchers, as these

effects may not be linear. While this thesis examines the effects of environmental

50

variables on abundances and distributions of oystercatchers, physiological factors may

be equally important when it comes to migration (Camphuysen et al. 1996). Finally,

territory quality may play a role, as well. Black Oystercatchers breeding on high quality

territories have higher reproductive success (Hazlitt 2001b), and show high site fidelity

(Hazlitt & Butler 2001). Therefore, birds that control high quality territories may choose to

remain resident in order to maintain control of the site over the winter, while birds with

without territories or controlling low-quality territories may opt to migrate. Future studies

that track individual birds over multiple years would be invaluable for determining what

causes oystercatchers to migrate.

So far, Black Oystercatcher populations appear to be fairly resilient to their

environmental and anthropogenic challenges (Ch. 2, Ch. 3, Andres 1999, Morse et al.

2006). However, global climate change is expected to introduce new threats to the

species, such as sea level rise (Langham et al. 2015). Climate change is expected to

lead to deeper Aleutian Lows, resulting in more severe winters (Fyfe et al. 1999). How

this will affect Black Oystercatcher populations is uncertain. Further study is needed to

determine if ALPI-linked variables such as wind speed and frequency of storms (Surrey

& King 2015) will influence Black Oystercatcher numbers and distributions. The

relationship between climate change and ENSO is less clear (Collins et al. 2010).

Though Black Oystercatchers in British Columbia are more likely to breed in La Niña

conditions than in El Niño conditions (Ch. 3), it is unknown how this relationship could be

affected by global climate change in the future.

Given the potential impacts of a changing climate on Black Oystercatchers,

continued monitoring and further studies are needed to inform the species' conservation

needs. The Christmas Bird Count, a citizen science project, is the source of the most

widespread, long-term, and consistent survey data for Black Oystercatchers across their

range. Citizen science is invaluable for providing researchers with more data than they

would have the resources to collect otherwise. It also makes the data widely available for

analysis by many researchers around the world (Sullivan et al. 2014). The Black

Oystercatcher is a particularly suitable species for monitoring via CBC surveys, as their

distinctive appearance is virtually unmistakable, even to very novice birdwatchers.

Oystercatchers are found only on rocky beaches, which make up a small portion of most

CBC count circles. These few areas of oystercatcher habitat are likely visited fairly

consistently by CBC participants each year, so counts likely vary less with search effort

51

in Black Oystercatchers than in other species. That said, many oystercatchers are found

in remote locations that lie outside of CBC count circles or are inaccessible to CBC

volunteers (Weinstein et al. 2014). A large portion of the population is therefore not

included in the counts. The median number of Black Oystercatchers counted in

Christmas Bird Counts across the years used in this study was 1143 individuals (IQR:

944 – 1795), which only accounts for 7.6% of the estimated global population

(Appendix). Therefore, remote surveys targeted specifically at oystercatchers, such as

the census carried out in California by Weinstein et al. (2014), are important as well. The

data used in this thesis can serve as useful long-term baselines for future analyses. It is

important that monitoring efforts continue so that any future declines in Black

Oystercatchers can be recognized and mitigated.

References

ANDRES B.A. (1999) Effects of persistent shoreline oil on breeding success and chick growth in Black Oystercatchers. Auk 116(3): 640–650

BERGMAN C.M., PATTISON J., & PRICE E. (2013) The Black Oystercatcher as a sentinel species in the recovery of the Northern Abalone: Contemporary diet of Black Oystercatchers on Haida Gwaii includes an endangered prey species. Condor 115(4): 800–807

CAMPHUYSEN K.C.J., ENS B.J., HEG D., HULSCHER J.B., VAN DER MEER J., & SMIT C.J. (1996) Oystercatcher Haematopus ostralegus winter mortality in the Netherlands: The effect of severe weather and food supply. Ardea 84A: 469–492

CLARKSON P. & ZHARIKOV Y. (2007) Pacific Rim SoPR, Technical Compendium, EIMRP. Draft internal report, 9 p.

COLLINS M., AN S.-I., CAI W., GANACHAUD A., GUILYARDI E., JIN F.-F., JOCHUM M., LENGAIGNE M., POWER S., TIMMERMANN A., VECCHI G., & WITTENBERG A. (2010) The impact of global warming on the tropical Pacific Ocean and El Niño. Nature Geoscience 3: 391–397

FYFE J.C., BOER J.G., & FLATO G.M. (1999) The Arctic and Antarctic Oscillations and their projected changes under Global Warming. Geophysical Research Letters 26(11): 1601–1604

GOSS-CUSTARD J.D., ed. (1996) The oystercatcher: From individuals to populations. Oxford Ornithology Series, Oxford University Press.

HAZLITT S.L. (2001a) Black Oystercatcher population status and trends in British Columbia. Bird Trends 8: 34–36

52

HAZLITT S.L. (2001b) Territory quality and reproductive success of Black Oystercatchers in British Columbia. Wilson Bulletin 113(4): 404–409

HAZLITT S.L. & BUTLER R.W. (2001) Site fidelity and reproductive success of Black Oystercatchers in British Columbia. Waterbirds 24(2): 203–207

HOERLING M.P., KUMAR A., & ZHONG M. (1997) El Niño, La Niña, and the nonlinearity of the teleconnections. Journal of Climate 10: 1769 – 1786

LANGHAM G.M., SCHUETZ J.G., DISTLER T., SOYKAN C.U., & WILSEY C. (2015) Conservation status of North American birds in the face of future climate change. PLoS ONE 10(9): e0135350. https://doi.org/10.1371/journal.pone.0135350

MEEHAN T.D., HARVEY A.L., MICHEL N.L., LANGHAM G.M., & WEINSTEIN A. (2018) A population model exploring factors influencing Black Oystercatcher (Haematopus bachmani) population dynamics. Waterbirds 41(2): 115–221

MORSE J.A., POWELL A.N., & TETREAU M.D. (2006) Productivity of Black Oystercatchers: Effects of recreational disturbance in a national park. Condor 108: 623–633

PARKS CANADA (2012a) Black Oystercatcher monitoring program sampling protocol Gulf Island National Park Reserve. Gulf Islands National Park Reserve 31 p.

PARKS CANADA (2012b) 2012 Black Oystercatcher survey in Gwaii Haanas. Unpublished report. Gwaii Haanas archive, Skidegate, BC. 52 p.

ROPELEWSKI C.F. & HALPERT M.S. (2002) North American precipitation and temperature patterns associated with the El Niño/Southern Oscillation (ENSO). Monthly Weather Review 114: 2352–2362

SULLIVAN B.L., AYCRIGG J.L., BARRY J.H., BONNY R.E., BRUNS N., COOPER C.B., DAMOULAS T., DHONDT A.A., DIETTERICH T., FARNSWORTH A., FINK D., FITZPATRICK J.W., FREDERICKS T., GERBRACHT J., GOMES C., HOCHACHKA W.M., ILIFF M.J., LAGOZE C., LA SORTE F.A., MERRIFIELD M., MORRIS W., PHILLIPS T.B., REYNOLDS M., RODEWALD A.D., ROSENBERG K.V., TRAUTMANN N.M., WIGGINS A., WINKLER D.W., WONG W.-K., WOOD C.L., YU J., & KELLING S. (2014) The eBird enterprise: An integrated approach to development and application of citizen science. Biological Conservation 169: 31–40

SURRY A.M. & KING J.R. (2015) A new method for calculating ALPI: the Aleutian Low Pressure Index. Canadian Technical Report of Fisheries and Aquatic Sciences 3135: 31 + v p.

TESSLER D.F., JOHNSON J.A., ANDRES B.A., THOMAS S., & LANCTOT R.B. (2014) A global assessment of the conservation status of the Black Oystercatcher Haematopus bachmani. International Wader Studies 20: 83–96

53

WEINSTEIN A., TROCKI L., LEVALLEY R., DOSTER R.H., DISTLER T., & KRIEGER K. (2014) A first population assessment of Black Oystercatcher Haematopus bachmani in California. Marine Ornithology 42: 49–56

WOOTTON T.J. (1992) Indirect effects, prey susceptibility, and habitat selection: Impacts of birds on limpets. Ecology 73(3): 981–991

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Appendix: Population estimates for Black Oystercatchers

Global population estimates for Black Oystercatchers have increased from 7600

(Paige & Gill 1994) to 8900 (Morrison & Gill 2001) to 10 000 (Morrison et al. 2006,

Andres et al. 2012). However, Tessler et al. (2014) remarks that the increasing

population estimates are more likely due to more extensive survey efforts than to an

increasing population. Furthermore, the majority of the surveys that these estimates are

based on are not effective at counting oystercatchers specifically (Tessler et al. 2014).

Weinstein et al. (2014) used an improved survey design that detected far more

oystercatchers, increasing the population estimate in California by approximately 6

times. The study by Weinstein et al. (2014) reveals that California is a much more

important region to Black Oystercatchers than was previously thought. It is also likely

that better surveys across the species' range could lead to higher estimates in other

regions. Table A1 summarises the most recent regional population estimates, including

the estimate by Weinstein et al. (2014).

Table A1: Regional population estimates for Black Oystercatchers during the summer across their range. Regional estimates were compiled by Tessler et al. (2014). An updated estimate for California by Weinstein et al. (2014) and an adjusted total estimate are included in parentheses.

Region Est. range Est. midpoint Sources Southwest Alaska 2000 – 3000 2500 Andres & Falxa 1995 South-Central Alaska 2500 – 3000 2750 Andres & Falxa 1995, Gill et al. 2004 Southeast Alaska 1000 – 1500 1500 Andres & Falxa 1995 Alaska (total) 5500 – 8000 6750 Andres & Falxa 1995, Gill et al. 2004 British Columbia 1000 – 2000 1500 Jehl 1985, Campbell et al. 1990 Washington 470 – 720 595 Speich & Wahl 1989, Lyons et al. 2012 Oregon 560 – 660 610 Naughton et al. 2007, Lysons et al. 2012 California 700 – 1000

(4749 – 6067) 850

(5408) Sowls et al. 1980, (Weinstein et al. 2014)

Baja California 80 80 Palacios et al. 2009 Total (Adjusted total)

8310 – 12 460 (12 359 – 17 527)

10 385 (14 943)