ANTHROPOGENIC DEBRIS AND PATHOLOGY IN AQUATIC BIRDS

By

Erika R. Holland

B.Sc. (Hons.), Acadia University, 2015

Thesis submitted in partial fulfillment of the requirements for

the Degree of Master of Science (Biology)

Acadia University

October 2017

© by Erika Reigh Holland, 2017

ii

This thesis is accepted in its present form by the Division of Research and Graduate

Studies as satisfying the thesis requirements for the degree Master of Science (Biology).

.................................................

I, Erika R. Holland, grant permission to the University Librarian at Acadia University to

reproduce, loan or distribute copies of my thesis in microform, paper or electronic

formats on a non-profit basis. I, however, retain the copyright in my thesis.

Erika Holland

_ _

Dr. Mark Mallory

_

Dr. Dave Shutler

_ _________________

Date

iii

TABLE OF CONTENTS

TABLE OF CONTENTS ...................................................................................................................... iii LIST OF TABLES .............................................................................................................................................. iv LIST OF FIGURES .............................................................................................................................................. v ABSTRACT .......................................................................................................................................................... vi ACKNOWLEDGMENTS ............................................................................................................................... vii PREFACE .............................................................................................................................................................. ix

CHAPTER ONE: GENERAL INTRODUCTION TO ENVIRONMENTAL ANTHROPOGENIC DEBRIS ............................................................................................................. 1

Introduction ............................................................................................................................................................ 1 Plastics in Marine Environments ..................................................................................................................... 4 Plastics in Freshwater Environments ............................................................................................................. 7

Microbeads: A growing concern ................................................................................................................ 9 My Research ........................................................................................................................................................ 12

Structure of this thesis ................................................................................................................................. 13 CHAPTER TWO: PLASTICS AND OTHER ANTHROPOGENIC DEBRIS IN FRESHWATER BIRDS FROM CANADA ................................................................................. 15

Introduction .......................................................................................................................................................... 15 Material and Methods ....................................................................................................................................... 19

Sampling .......................................................................................................................................................... 19 Processing, separation, sorting and identifying .................................................................................. 19 Statistical analyses........................................................................................................................................ 21

Results .................................................................................................................................................................... 22 Discussion ............................................................................................................................................................. 24 Conclusions .......................................................................................................................................................... 27

CHAPTER THREE: ANTHROPOGENIC DEBRIS AND PATHOLOGY OF FULMARS AND SHEARWATERS BEACHED ON SABLE ISLAND, NOVA SCOTIA, CANADA ............................................................................................................................. 33

Introduction .......................................................................................................................................................... 33 Materials and Methods ..................................................................................................................................... 37

Sample collection and processing ............................................................................................................ 37 Statistical analyses........................................................................................................................................ 38

Results .................................................................................................................................................................... 39 Sooty Shearwater .......................................................................................................................................... 40 Great Shearwater .......................................................................................................................................... 40 Northern Fulmar ........................................................................................................................................... 41

Discussion ............................................................................................................................................................. 42 CHAPTER FOUR: GENERAL DISCUSSION AND FUTURE DIRECTIONS .............. 52

Future Actions ..................................................................................................................................................... 52 Appendices ........................................................................................................................................................... 86

iv

LIST OF TABLES

Table 1. Sample sizes, body mass, the frequency, and mean number of pieces for plastic,

metal, and any debris…………………………………………...………………………..30

Table 2. Amount and types of debris recovered from the nine species that ingested

debris.…………………………………………………………………………………….32

Table 3. Overview of the number and corresponding percentages of age, sex, and season

collected, for four species of Procellariiformes collected beached on Sable Island, Nova

Scotia, between 2000 and 2012.……………………………………...………………….47

Table 4. Pathology, ranked from most to least common, in 318 procellariids collected

beached on Sable Island, Nova Scotia, Canada, between 2000 and 2012……………….48

Table 5. Average body mass, and average mass of anthropogenic debris particles found

in the gizzards and proventriculi of four species of Procellariiformes collected beached on

Sable Island, Nova Scotia, between 2000 and 2012..………………………………........49

v

LIST OF FIGURES

Figure 1. Omnivore and piscivore digestive tracts showing physiological differences in

structure.…………...………………………………………………..……………………14

Figure 2. Sample sites used for this study...…………………………………..…………29

Figure 3. Monthly collection breakdown of procellariid carcasses found beached on

Sable Island, Nova Scotia, Canada, between 2000-2012...………………………………50

Figure 4. Plumage morphs of beached northern fulmars (Fulmarus glacialis) collected

from Sable Island, Nova Scotia, Canada, between 2000-2012 and associated ingested

masses of anthropogenic debris (g) removed from the gizzard and proventriculus of

birds………………………………………………………………………………………51

vi

ABSTRACT

Plastics in marine and freshwater environments are a global environmental issue.

Plastic ingestion is associated with a variety of deleterious health effects for wildlife, and

is a focus of much international research and monitoring. However, little research has

focused on the ramifications of plastic debris for freshwater organisms. In chapter 2 I

quantified plastic and other anthropogenic debris in 350 individuals of 17 freshwater and

one marine bird species collected across Canada. I determined prevalence of

anthropogenic debris in freshwater birds’ to be 11.4% across all species studied.

In chapter 3 I determined the prevalence of anthropogenic debris and their

consequences in seabirds, using four species of procellariid seabirds found beached on

Sable Island, Nova Scotia, Canada between 2000 and 2012. Pooling the four species, no

differences in prevalence of different pathologies was found relative to age or sex, with

birds having (in descending order of occurrence) emaciation, autolysis, parasite infection,

inflammation, trauma, bacterial infection, drowned, tumors, tissue necrosis, impaction,

myopathy, or pneumonia. Northern fulmars washed up dead of emaciation less frequently

(69/115; 60%) than sooty (36/48; 75%) or great (67/86; 78%) shearwaters. Pathology in

northern fulmars (Fulmarus glacialis), sooty (Ardenna grisea) and great shearwaters

(Ardenna gravis) appeared unrelated to mass of debris ingested or body mass, and

similarly body mass was not significantly related to mass of debris ingested.

This work established that anthropogenic debris is a genuine concern for

management of the health of freshwater and marine ecosystems, provided a baseline for

the prevalence of anthropogenic debris ingestion in freshwater birds in Canada, and

presented the first in-depth look at pathology of birds beached on Sable Island.

vii

ACKNOWLEDGMENTS

First and foremost, thank you to my advisors and co-authors Drs. Mark Mallory

and Dave Shutler, without whom this thesis would not have been possible. Thanks also to

Dr. Pierre-Yves Daoust and Zoe Lucas for providing data for chapter two. Thanks are

also due to my advisory committee, composed of Drs. Mark Mallory, Dave Shutler, and

Steve Mockford. A million thanks to Danielle Quinn, Trevor Avery, and the entire R-Bar

crew for your essential help with stats in R. I also thank my family and friends for their

continuous and unending support, patience, and humour.

A huge thank you to all the individuals who contributed digestive tracts to my

research: Leo and Maria Brink, Peggy Crawford, Matthew English, Mark Gloutney, John

Goas, Randy Goreham, Matt Gregoire, Jeff Krete, Julie Mallett, Regan Maloney, Nic

McLellan, Michael O'Brien, Kirsten Pearson, Eric Reed, Greg Robertson, Ken Tucker,

Becky Whittam, Paul Woodard, and most of all, Laurie Wilson. Thanks also to Brook

Beauliua, Ashton Baich, Robin Dornan, Laura McGinnis, Sarah Mitchell, Jackie Morris,

Alexandra Nesnidalova, Dione Rousseau, and Lindsay Trainor for their help in lab with

freshwater bird dissections. Special thanks to Matthew English for his assistance with

dissection methods, and to Stephanie White for her assistance finding local hunters and

lab assistants through the Annapolis Valley Ducks Unlimited Canada Chapter.

Financial support for this project was provided by a Natural Sciences and

Engineering Research Council of Canada Alexander Graham Bell Canada Graduate

Scholarship - Master’s Program (CGS M), The Nova Scotia Innovation & Research

Graduate Scholarship (Master's) in Ocean Science & Tech/Life Sciences, an Alden B.

viii

Dawson Scholarship, an Acadia Graduate Scholarship, a Ducks Unlimited

Canada/Acadia Research Partnership Grant, and the Natural Sciences and Engineering

Research Council of Canada (NSERC; Grant numbers 418551-2012 and 2015-05617).

Collection and possession of waterfowl were made under appropriate permits from the

Canadian Wildlife Service (Service Permit no. SS2802).

ix

PREFACE

Chapters 2 and 3 of this thesis were written with the intent of being published in

peer-reviewed journals along with co-authors. Thus, I have chosen to retain the more

inclusive pronouns “we” and “our” for those chapters.

Chapter 2 has previously been published in a peer-reviewed journal, although it

has been updated since this publication. The original publication may be referenced in

other works as:

Holland, E., Mallory, M.L., Shutler, D., 2016. Plastics and other anthropogenic debris in

freshwater birds from Canada. Science of the Total Environment 571, 251–258.

doi:http://dx.doi.org/10.1016/j.scitotenv.2016.07.158

1

CHAPTER ONE: GENERAL INTRODUCTION TO ENVIRONMENTAL

ANTHROPOGENIC DEBRIS

Introduction

Extending over three quarters of the Earth’s surface, aquatic ecosystems play a

critical role in planetary life support (Secretariat of the Convention on Biological

Diversity, 2012). Humans rely on aquatic systems for food, water, industry and

agriculture, and millions of jobs (Food and Agriculture Organization of the United

Nations, 2016; Millennium Ecosystem Assessment, 2005; Secretariat of the Convention

on Biological Diversity, 2012). However, human actions, specifically pollution by

anthropogenic debris such as plastics, constitute a major threat to aquatic environments,

the species therein, and the resources they provide (Derraik, 2002).

Humans have been releasing plastics into their environment since the early 1900s

(Bijker et al., 1987; Klar et al., 2014), and plastics in marine environments have been

identified as an emerging environmental issue at a global level, with concentrations

increasing rapidly (United Nations Environment Programme, 2014). Since commercial

production began in the 1950s, the plastics industry has grown by an average of 8.7% per

year, and in 2013, global production rose to 299 million tonnes (Plastics Europe, 2013,

2015).

Of all anthropogenic debris released into our waterways, plastic debris may

overall be the most problematic due to its negative effects on wildlife (Ashton et al.,

2010; Rios et al., 2010; Wright et al., 2013) and slow breakdown time (Derraik, 2002).

2

Plastic entanglement of marine organisms can lead to general debilitation, entanglement-

related injuries, impaired diving for feeding or surfacing for breath, starvation, and

eventual death (Mascarenhas et al., 2004; Gregory, 2009; Votier et al., 2011). Marine

plastic waste can mimic natural food, leading to debris ingestion by aquatic organisms

being more than proportional to their availability. However, plastics fail to provide

nutrition and once ingested can lead to weakness, false feelings of satiation, irritation of

the stomach lining, digestive tract blockage, internal bleeding, abrasion, ulcers, failure to

put on fat stores necessary for migration and reproduction, and death through starvation

(Moore, 2008; Wright et al., 2013). Plastic debris also vector heavy metal contaminants

and high concentrations of organochlorines such as polychlorinated biphenyls (PCBs),

dichlorodiphenyl trichloroethane (DDT) and polycyclic aromatic hydrocarbons (PAHs)

(Teuten et al., 2007; Ashton et al., 2010; Rios et al., 2010). Once plastics are discharged

into an aquatic environment they can persist for anywhere from three to 50 years prior to

complete disintegration, and complete mineralization may take hundreds or thousands of

years (Gregory, 1978; Derraik, 2002; Driedger et al., 2015).

Although plastic debris is the most prevalent and most researched form of aquatic

anthropogenic debris it is not the only material with reported deleterious effects (van

Franeker and Meijboom, 2002). Fragments of metals, rubber, cloth, glass, Styrofoam, and

other anthropogenic products often find their way into aquatic ecosystems, resulting in

seabird ingestion (Auman et al., 1997; Moser and Lee, 1992; Tourinho et al., 2009; van

Franeker and Meijboom, 2002). However, ingestion rates among a variety of species are

higher for plastic debris than other anthropogenic materials (van Franeker and Meijboom,

2002). This may be due to higher exposure, as plastics often make up the majority (80-

3

92%) of total anthropogenic material present in aquatic ecosystems and along shorelines

(Lucas, 1992; Driedger et al., 2015).

To date little research has focused on the ramifications of plastic and other

anthropogenic debris for freshwater organisms. Research on freshwater ecosystems is

needed to put into effect crucial laws and regulations governing debris release into

waterways. These regulations are needed to stop potentially harmful biomagnification up

the food chain, reducing future plastic and debris contaminant contact by humans through

their freshwater food sources.

This introduction reviews the current state of knowledge for marine

anthropogenic debris and research, including species harmed by plastic exposure, and

introduces the growing field of freshwater debris research, with a specific focus on the

rising issue of microbeads. I suggest future analyses on freshwater organisms are

important to maintaining healthy populations, and decreasing anthropogenic debris

contact. Research into freshwater plastic and other anthropogenic debris is significant

because little is currently known about anthropogenic debris exposure and ingestion in

freshwater organisms. More data are required to determine potentially negative effects on

humans through biomagnification from wild-caught avian foods. Research has shown

that for North Sea cod (Gadus morhua), plastic ingestion appears to be a pathway for

intestinal tract leaching, and subsequent cod exposure to nonylphenol (NP) and bisphenol

A (BPA), although concentrations acquired are negligible (Koelmans et al., 2014).

Research on short-tailed shearwaters (Puffinus tenuirostris) and great shearwaters

(Puffinus gravis) has shown that avian tissues can acquire polybrominated diphenyl ether

(PBDE) flame retardants and polychlorinated biphenyls (PCBs) from ingested plastic

4

debris (Ryan et al., 1988; Tanaka et al., 2013, 2015), which could put humans consuming

contaminated tissues at risk of bioaccumulation. Likewise, northern fulmar (Fulmarus

glacialis) eggs of the Faroe Islands contain high levels of brominated flame retardants

(BFRs) and PBDEs, and may be a source of lipid-soluble persistent pollutants to the

Faroese peoples (Karlsson et al., 2006). PBDEs ingested by humans can have adverse

health effects, including cancer, thyroid hormone disruption, anti-androgen action,

neurodevelopmental deficits, and developmental neurotoxicity (McDonald, 2002; Costa

et al., 2008; Talsness et al., 2009). Humans ingesting PCBs through animal fats may find

that the accumulation of these fat-soluble substances can initiate suppression of the

immune system, alter thyroid and reproductive function, increase risk of developing

cardiovascular and liver disease and diabetes, while pregnant women exposed to PCBs

are at risk of giving birth to infants of low birth weight (Cheek et al., 1999; Holladay and

Smialowicz, 2000; Carpenter, 2006). PCB exposure in infants may also reduce IQ and

alter behaviour (Carpenter, 2006).

Plastics in Marine Environments

Marine environments from the equator to the poles contain plastic debris from

their surface waters to their deep-sea sediments (Kanehiro et al., 1995; Derraik, 2002;

Van Cauwenberghe et al., 2013; Obbard et al., 2014; Woodall et al., 2014; Taylor et al.,

2016). Due to plastic’s initial buoyancy and eventual settlement, surface-feeding birds

and dabbling ducks may be particularly susceptible to plastic debris ingestion (Ng and

Obbard, 2006; Eriksen et al., 2014; Ivar do Sul and Costa, 2014). Research on plastics in

marine environments has identified plastic’s initial buoyancy (specific gravity of 0.9;

5

Snyder and Vakos, 1966) as detrimental, because this buoyancy often leads to dispersal

over long distances (Derraik, 2002; Eriksen et al., 2014) and increased availability to

surface-feeding species (Day et al., 1985; Moser and Lee, 1992). However, over time

plastic debris in aquatic environments undergoes fouling due to biofilms, hitchhiking

organisms, and absorption of pollutants, causing plastics to become negatively buoyant

and sink into sediment (Ye and Andrady, 1991; Barnes et al., 2009; Frias et al., 2010;

Driedger et al., 2015).

Entanglement and ingestion of marine anthropogenic debris negatively affects all

seven known species of sea turtle (100%), 45% of all species of marine mammals, and

56% of seabird species (Secretariat of the Convention on Biological Diversity, 2012; Gall

and Thompson, 2015). Studies on seabird plastic ingestion have been conducted since the

1960s, when Kenyon and Kridler (1969) found that Laysan albatross (Phoebastria

immutabilis) fledglings were consuming plastic. Estimates from the 1990s were that 35%

of the world's seabird species were negatively affected by marine plastics (Laist, 1997).

Recent studies predict that, unless effective waste management practices are put into

place, 99% of all seabird species will be ingesting plastics by 2050 (Wilcox et al., 2015).

Once consumed it can take a bird one month to a year to pass ingested plastics (Day,

1980; Ryan and Jackson, 1987; van Franeker and Law, 2015). Despite estimates of slow

plastic expulsion times, the majority of studies fail to find plastics in seabird digestive

tracts or feces (studies on albatross, fulmars, shearwaters, storm-petrels, gulls, auklets,

and puffins; Day, 1980; Pettit et al., 1981; Rothstein, 1973). This could in part be due to

adults of certain species feeding their chicks through regurgitation, and thus passing their

6

plastic load on to their offspring (Pettit et al., 1981; Laist, 1987). Due to this unloading,

young birds often suffer mortality due to plastic (Derraik, 2002).

Some seabirds consume specific plastic shapes and colours more frequently,

perhaps mistaking them for prey items (Day et al., 1985; Moser and Lee, 1992; Shaw and

Day, 1994). Pale particles are often overrepresented in fulmars, shearwaters, petrels,

phalaropes, gulls, kittiwakes, and terns (Rothstein, 1973; Day, 1980; Moser and Lee,

1992; Lavers and Bond, 2016), although this could be due to the higher availability of

light-colored plastic particles in the environment (Moser and Lee, 1992). Selective

ingestion also ties into foraging style, and availability of certain plastics in certain niches

(Ryan, 1987). For example, Moser and Lee (1992) reported aerial plunging birds had the

lowest percentage of plastic in their gizzard (2%), pursuit diving species were mid-range

(8%), and surface seizing (12%) and pattering seabirds (14%) had the highest. Similarly,

Day et al., (1985) found that aerial plunging birds contained no plastic, pattering (9%)

and surface seizing (16%) seabirds were midrange, and pursuit diving species were

highest (26%), indicating that surface-feeding species are among the most likely to have

plastics in their diets.

In the Maritimes, research into plastic pollution begin in 1983, when Gregory

(1983) reported small virgin plastic pellets and granules in litter on the shores of Nova

Scotia and Sable Island. In 1989, it was determined that 62% of persistent marine litter in

Halifax Harbor originated from recreation and land-based sources (Ross et al., 1991).

Most notable research done on microplastic pollution centers around the Gully Trough, a

marine protected area located 200 kilometers off Nova Scotia, on the edge of the Scotian

Shelf (GTA Consultants Inc., 1999; Government of Canada, 2010), and Sable Island, a

7

long, crescent-shaped, sandy island located 160 km off the coast of mainland Nova Scotia

and 53 km west of the Gully Trough (Lucas et al., 2012). Studies done on Sable Island

have assessed both coastal debris and seabird plastic ingestion.

Studies on seabird plastic ingestion often rely on culling live birds, or collecting

samples opportunistically from birds found dead on beaches. These beached birds offer

an opportunistic window into natural seabird mortality (although these individuals are

often emaciated; Barrett et al., 2007), and rates of anthropogenic debris ingestion (Pierce

et al., 2004).

Plastics in Freshwater Environments

Although most historic research focuses on plastics in marine environments,

increasing work is focusing on freshwater environmental plastic contamination.

Freshwater bodies may have comparable plastic concentrations to marine waters. The

most commonly detected plastics are < 5 mm fragments of polyethylene and

polypropylene polymers (Zbyszewski and Corcoran, 2011; Eriksen et al., 2013;

Zbyszewski et al., 2014; Corcoran et al., 2015). Corcoran et al. (2015) found up to nine

microplastic particles (0.5-3 mm in size) per 2 cm, to depths of 8 cm, in Lake Ontario

sediments, indicating deposition and accumulation over approximately the past 38 years.

Over 80% of anthropogenic litter found along the Great Lake shorelines is composed of

plastics (Driedger et al., 2015). Anthropogenic debris entering freshwater and marine

ecosystems can come from a variety of sources, the majority of which originate from

land-based activities and waterway use (Ocean Conservancy, 2010). Freshwater plastic

waste commonly includes microplastic beads (polyethylene and polypropylene

8

microspheres widely used in cosmetics as exfoliating agents; Eriksen et al., 2013) from

consumer products, pellets from the plastic manufacturing industry, and waste from

beach-goers, shipping activities, and fishing (Driedger et al., 2015). The distribution of

plastics in bottom sediments of the Great Lakes is essentially unknown, because the

majority of what is known about microplastic pollution in freshwater bodies focuses

primarily on surface waters (Castañeda et al., 2014; Driedger et al., 2015). However,

deep-sea sediments at 1100 to 5000 m contain microplastic pollution of up to an average

of one particle per 25 cm2 (Van Cauwenberghe et al., 2013) and in Tokyo Bay, Japan,

plastics made up 80-85% of seabed debris (Kanehiro et al., 1995). Sediments of the St.

Lawrence River have microbead pollution comparable in density to marine microplastic

concentrations (Castañeda et al., 2014).

Aside from environmental concentrations, data from freshwater organisms

suggest that plastic ingestion levels are also comparable to those in marine ecosystems

(Denuncio et al., 2011; Castañeda et al., 2014). Franciscana dolphins (Pontoporia

blainvillei) in estuarine habitats had higher levels of plastic ingestion (34.6%) than their

marine counterparts (19.2%; Denuncio et al., 2011), suggesting that plastic ingestion by

freshwater organisms could be a larger issue than previously thought. Likewise, up to

33% of estuarine catfish (Cathorops spixii, Cathorops agassizii and Sciades herzbergii)

from the southwestern Atlantic and 7.9% of estuarine drums (Stellifer brasiliensis and

Stellifer stellifer) of the Goiana Estuary in Brazil consumed plastics (Possatto et al., 2011;

Dantas et al., 2012). Studies focusing on freshwater ecosystems have found plastic debris

affected some green algae (Scenedesmus obliquus) and zooplankton (Daphnia magna)

(Besseling et al., 2014), as well as gudgeons (Gobio gobio; Sanchez et al., 2014), yellow

9

perch (Perca flavescens; Moseman, 2015), and could potentially also affect benthivorous

fishes [preliminary results on benthic round gobys’ (Neogobius melanostomus) digestive

tracts suggested the presence of microbeads] and macroinvertebrates (Castañeda et al.,

2014).

Red phalaropes (Phalaropus fulicarius) and red-necked phalaropes (P. lobatus),

which spend a portion of their life consuming freshwater zooplankton, also consume

plastic debris (Day et al., 1985; Moser and Lee, 1992; Bayly, 1993). English et al. (2015)

examined three waterfowl species wintering in Atlantic Canada: mallards (Anas

platyrhynchos), American black ducks (A. rubripes) and common eiders (Somateria

mollissima). They found a surprisingly high prevalence of plastics in ducks’ stomachs

[46.1% (6/13) of mallards, 6.9% (6/87) of black ducks, and 2.1% (1/48) of eiders

contained plastic]. However, it is unknown whether the birds acquired plastic debris in

freshwater or marine locations. Likewise Gil-Delgado et al. (2017) reported plastic in the

faeces of three species of waterfowl: shelduck (Tadorna tadorna), European coot (Fulica

atra), and mallard. Shelduck faeces had a 43.8% prevalence of plastic remnants,

European coots 60%, and mallards 45% (Gil-Delgado et al., 2017).

Microbeads: A growing concern

Studies on freshwater species potential acquisition of plastics are important,

especially in light of research on freshwater microbead concentrations. Microbeads have

gained popularity in recent years and their increased use has led to an unforeseen increase

of these plastics entering aquatic ecosystems (Castañeda et al., 2014; Doughty and

Eriksen, 2014). Their relatively small diameter (< 1 mm) means many wastewater

10

treatment plants cannot remove them, unless they employ fine- or micro-screens,

microfiltration, sand filtration, or mixed media filtration (Castañeda et al., 2014; Doughty

and Eriksen, 2014; Driedger et al., 2015). In New York State, USA, sampling showed

that not employing these filtration methods led to six out of seven wastewater treatment

plants discharging microbeads into rivers, lakes, and oceans (Schneiderman, 2014). An

example of the effectiveness of these methods can be seen when comparing Lake Huron,

USA’s 2,779 plastic particles km2 due to high plastic recycling rates, and high

wastewater treatment plant retention efficiencies, to Lake Hovsgol, Mongolia, which

lacking a modern waste management system has 20,264 plastic particles/km2 (Free et al.,

2014).

To date, relatively little research has been conducted on microbeads. However,

public outcry has meant that some major companies have banned, or are planning to ban,

microbeads, but lax regulations mean that loopholes still exist (Newman et al., 2013;

International Joint Commission Canada and United States, 2016). To combat this, the

Great Lakes and St. Lawrence Cities Initiative (GLSLCI), a binational coalition of

mayors and municipal officials, has adopted a resolution calling for industries to phase

out microbeads (Great Lakes and St. Lawrence Cities Initiative, 2014). GLSLCI further

calls for bans on developing new products containing microbeads, for companies to phase

out the use of all existing products containing microbeads, and for provincial, state, and

federal bans on microbead usage in consumer products (Great Lakes and St. Lawrence

Cities Initiative, 2014). In response, the United States recently passed the Microbead

Free Waters Act of 2015 (House Report No. 114-371, 2015) and the Canadian

government added microbeads to the Schedule 1 list of toxic substances under the

11

Canadian Environmental Protection Act (Environment and Climate Change Canada,

2010; Government of Canada, 2015). The proposed Microbeads in Toiletries Regulations

would prohibit the sale of products that contain microbeads by 2019 (Government of

Canada, 2016). The Belgian, Netherlands, Austrian and Swedish delegations to the

European Union, supported by the Luxembourg delegation, are pushing for a European

ban on microbeads (Council of the European Union, 2014) and the UK government is

preparing to ban the sale and manufacture of cosmetics and personal care products

containing microbeads (UK Government, 2016). In Australia, New South Wales and

South Australia are leading a phase-out of microbeads in their jurisdictions, to be

completed by 2018 (Australian Government, 2016). Legislation banning the use of

microbeads in consumer goods may be a huge and necessary step, because per capita

consumption of polyethylene microplastic beads in personal care products for the U.S.

population is approximately 2.4 mg per person each day, leading to the U.S. alone

discharging 263 tonnes per year of polyethylene microplastic (Gouin et al., 2011). Large

concentrations of these plastics are problematic because microbeads are expected to

persist for centuries before re-entering normal biogeochemical cycles (Leslie, 2014).

Although efforts are being made to clean ocean waters of plastics and help

mitigate increasing concentrations (Kershaw et al., 2011), lack of data, primarily through

the absence of work documenting the scale and scope of this problem, has meant that no

similar initiatives exist for freshwater bodies (Ryan et al., 2009). Inadequate initiatives

and legislation governing freshwater plastic debris could be due to the inadequacy of

standardized measures for quantifying plastic debris (Driedger et al., 2015).

Complications derived from different methods of reporting plastic debris concentrations

12

in freshwater and marine environments could also affect initiatives, because there is no

internationally agreed upon classification system for plastic debris (Driedger et al., 2015).

However, the following size classes, defined by mesh filter sizes, are often used:

microscopic plastic debris (0.45 μm to 333 μm), microplastics (> 333 μm to 5 mm), and

macroplastic (> 5 mm) (Arthur et al., 2008; Andrady, 2011; Driedger et al., 2015).

My Research

I researched anthropogenic debris ingestion in freshwater and marine birds, with a

specific focus on microplastics and other micro-debris. Although numerous similar

studies have been conducted on marine birds, little research has focused on the

ramifications of increasing debris concentrations to freshwater species. I also conducted

research into beached bird pathology, and the relationship of pathological findings to

ingested debris, among fulmars and shearwaters from Sable Island, Nova Scotia, Canada.

These studies were primarily dissection-based, with the gastrointestinal tract of

individuals sampled being dissected in a lab. The digestive tracts of birds are relatively

simple, consisting of an esophagus, an acid-proteolytic stomach (consisting of the

proventriculus and gizzard), a tubular small intestine, and a very short colon (Hilton et

al., 2000). For these studies only the proventriculus and gizzards were dissected.

Piscivorous birds, such as seabirds and loons, have a larger proventriculus than gizzard,

while omnivorous waterfowl have larger gizzards (Fig. 1).

13

Structure of this thesis

Chapter 2 presents data on anthropogenic debris in the diets of freshwater birds

collected from across Canada. Digestive tracts of freshwater ducks, geese, and loons were

acquired from hunters and government employees for subsequent in-lab dissections and

dietary analyses. All methods were consistent with van Franeker and Meijboom (2002)

and sampling was carried out in accordance with Environment Canada’s Canadian

Wildlife Service Migratory Birds Regulations. We quantified debris in 350 individuals of

17 freshwater and one marine bird species collected across Canada. Collaboration with

other studies and organizations (e.g. Ducks Unlimited Canada and Nova Scotia’s

Department of Natural Resources) ensured that sampled birds served many purposes.

Chapter 3 presents data on the pathology of four species of seabirds (Cory’s

shearwater, Calonectris borealis, sooty shearwater, Puffinus griseus, great shearwater,

Puffinus gravis, and northern fulmar, Fulmarus glacialis) collected beached on Sable

Island, Nova Scotia, Canada. Beached birds offer an opportunistic window into seabird

mortality, pathology, and anthropogenic interactions (Camphuysen and Heubeck, 2001;

Roletto et al., 2003; Balseiro et al., 2005; van Franeker et al., 2011), although individuals

collected in this manor are often emaciated (Barrett et al., 2007). Beached birds often

contain ingested anthropogenic debris, yet to date little is known of the interaction among

debris, pathology, body mass, age and sex. Chapter 3 evaluated these factors, and

analyzed pathological findings among the four species.

Chapter 4 concludes the thesis by summarizing the research and results, making

further recommendations for future research, and discussing possible management

implications for this work, with a specific focus on plastic debris.

14

Figure 1. Overhead image of omnivore (duck; left) and piscivore (loon; right) digestive

tracts showing anatomical differences in structure. Images taken by author.

15

CHAPTER TWO: PLASTICS AND OTHER ANTHROPOGENIC DEBRIS IN

FRESHWATER BIRDS FROM CANADA

Holland, E., Mallory, M.L., Shutler, D., 2016. Plastics and other anthropogenic debris in freshwater birds

from Canada. Science of the Total Environment 571, 251–258. doi:http://dx.doi.org/10.1016/j.scitotenv.2016.07.158

Introduction

Humans have been releasing plastic debris into the environment since the early

1900s (Bijker et al., 1987). Originally thought to be little more than an eyesore, we now

know that the very properties that make plastics ideal for human use (i.e., being

lightweight and strong, and having a durable physical configuration) also make plastics

serious environmental hazards (Laist, 1987; Derraik, 2002). The ubiquity of

anthropogenic debris in the environment, such as plastic and waste metal, raises concerns

regarding its ingestion by animals, and so has been particularly well studied for animals

living in aquatic habitats (Rochman et al., 2014). Anthropogenic debris is problematic

due to its negative effects on wildlife, including entanglement and ingestion (Derraik,

2002; Wright et al., 2013; Provencher et al., 2014). Plastic debris also has an affinity for

certain non-essential trace elements and persistent organic pollutants (POPs), such as

polychlorinated biphenyls (PCBs) and dichlorodiphenyltrichloroethane (DDT; Ashton et

al., 2010; Bakir et al., 2014). Once plastics are discharged into aquatic environments,

they can persist for up to 50 years, and their complete mineralization may take hundreds

or thousands of years (Gregory, 1978; Derraik, 2002; Driedger et al., 2015).

Entanglement and ingestion of marine anthropogenic debris negatively affects all seven

known species of sea turtle (100%), about half of all species of marine mammals (45%),

16

and one-fifth of all species of seabirds (21%); these numbers represent a 40% increase

(from 247 to 663 affected species) from 1997 (Secretariat of the Convention on

Biological Diversity, 2012). As of 2015, 56% of seabird species were affected by marine

anthropogenic debris (Gall and Thompson, 2015), with predictions that by 2050, 99% of

seabird species will be affected (Wilcox et al., 2015) and the mass of plastics in the

oceans will outweigh fish (Neufeld et al., 2016). Whereas much is known about effects of

plastic debris on marine birds, virtually no comparable data are available for freshwater

species.

Freshwater bodies can have comparable anthropogenic debris concentrations to

marine waters (Castañeda et al., 2014; Lechner et al., 2014; Driedger et al., 2015). In the

Great Lakes of North America, over 80% of anthropogenic shoreline debris is composed

of plastics (Castañeda et al., 2014; Driedger et al., 2015) and sediments of the St.

Lawrence River have microbead (polyethylene and polypropylene microspheres widely

used in cosmetics as exfoliating agents; Eriksen et al., 2013) pollution comparable in

magnitude to marine microplastic concentrations [Castañeda et al., 2014; microplastics

defined by Moore (2008) and Arthur et al. (2008) as plastic fragments < 5 mm].

Likewise, a multiyear study on the Danube River in Austria quantified discharges of

1,533 tonnes of plastics per year into the Black Sea (Lechner et al., 2014), although the

majority turned out to be industrial microplastics from a plastic-producing company

(Lechner and Ramler, 2015). A similar study in Mongolia found that Lake Hovsgol has

plastic particle concentrations reaching 20,264 particles/km2 (Free et al., 2014), and a

recent study on two lakes in central Italy (Lake Bolsena and Lake Chiusi) found 2.68 to

3.36 particles/m3 and 0.82 to 4.42 particles/m3, respectively, in surface waters (Fischer et

17

al., 2016). These studies suggest that not only are plastics a major problem in marine

settings, they are also an issue in freshwater ecosystems.

Studies focusing on organisms in freshwater ecosystems have found dietary

plastic debris in green algae (Scenedesmus obliquus) and zooplankton (Daphnia magna)

(Besseling et al., 2014), as well as planktivorous fish (Sanchez et al., 2014; Moseman,

2015). Plastics could also potentially affect benthivorous fishes and macroinvertebrates

[preliminary results on benthic round goby’s (Neogobius melanostomus) digestive tracts

suggest the presence of microbeads (Castañeda et al., 2014) while reports on benthic

gudgeon (Gobio gobio) found ingested polymer fibers and pellets (Sanchez et al., 2014)].

Migratory birds, such as red phalaropes (Phalaropus fulicarius) and red-necked

phalaropes (P. lobatus), which eat freshwater zooplankton, also consume plastic debris

(Day et al., 1985; Moser and Lee, 1992). English et al. (2015) examined mallard (Anas

platyrhynchos), American black duck (A. rubripes), and common eider (Somateria

mollissima) wintering in Atlantic Canada, and found an 11.5% prevalence of

anthropogenic debris in 140 birds. However, it was not known whether those birds

acquired debris in freshwater or marine locations due to the long residency time of

dietary plastics (from two months to a year; Connors and Smith, 1982; Ryan and Jackson,

1987) and known movement patterns of these ducks between marine and freshwater

ecosystems in this area (English, 2016).

Encounters between organisms and marine debris have been reported since the

1960s, with the first study on seabird plastic ingestion on Laysan albatross (Phoebastria

immutabilis) conducted in 1966 (Kenyon and Kridler, 1969; Gall and Thompson, 2015).

Between 1969-1977 and 1988-1990, a significant increase (up to 26.3%) was recorded in

18

the frequency of seabird plastic ingestion (Robards et al., 1995). If trends in freshwater

waterfowl ingestion of debris mirror seabird historical trends, we may see a similar

increase in waterfowl debris consumption over time. This is problematic due to the

negative consequences of consuming debris. Debris fails to provide nutrition proportional

to its mass or volume, and can lead to weakness, false feelings of satiation, irritation of

the stomach lining, digestive tract blockage, internal bleeding, abrasion, ulcers, failure to

put on fat stores necessary for migration and reproduction, absorption of toxins, and

potential death through starvation (Moore, 2008; Wright et al., 2013; Zhao et al., 2016).

Surface-feeding birds and dabbling ducks may be particularly susceptible to

plastic ingestion due to the initial buoyancy of plastic. Plastics eventually sink over time

from biofilm fouling and hitchhiking organisms (Barnes et al., 2009; Frias et al., 2010;

Driedger et al., 2015). However, after settling, they remain available to benthic

organisms, and those that feed on benthos, and thus can return to food webs (Wright et

al., 2013). Due to biomagnification through debris consumed by fish, piscivorous birds

may also be at risk (Day et al., 1985; Castañeda et al., 2014; Sanchez et al., 2014;

Moseman, 2015). Additionally, urban birds are at an increased risk of ingesting debris

because of a greater density of plastic near industrial centers (Zbyszewski et al., 2014).

We undertook this study to bridge a knowledge gap on anthropogenic debris

ingestion by freshwater birds. We asked the following questions: 1) What is the

prevalence of anthropogenic debris in freshwater birds? 2) Is there geographic variation

in prevalence? 3) Are there differences among species in prevalence and does this relate

to their foraging niches? 4) Is prevalence related to body mass? 5) What are the

characteristics of ingested particles (i.e., type, color and size)?

19

Material and Methods

Sampling

Ducks, geese, and loons occupying freshwater habitats were collected from across

Canada (Fig. 2); 40 common eiders (a marine sea duck) were also acquired as a

comparison group. All birds were from hunter kills, airport culls or collisions, and

predation, and were shipped frozen to Acadia University where dissections were

performed. We recorded species, date, location, and if available, sex, age, and body mass

(g). Birds were kept frozen at -22°C until dissection and analysis, and allowed to thaw for

one to two days prior to dissection.

Processing, separation, sorting and identifying

Methods followed the recommendations of van Franeker and Meijboom (2002)

and van Franeker (2004) for quantifying anthropogenic debris ingestion by seabirds. To

avoid contamination, work surfaces were thoroughly cleaned with a 1/3 to 2/3 bleach and

water mixture and all tools were cleaned under running tap water between each specimen.

Gloves, lab coats, and facemasks were worn throughout the study. Sample analysis was

standardized, with the primary author inspecting all samples. Thawed digestive tracts

were opened over their full length, and contents carefully flushed with cold tap water

above a 0.5-mm mesh sieve to ensure that no small particles were left behind on organ

20

walls (particles smaller than 0.5 mm were detected due to debris’ ability to adhere to

larger dietary particles). All material was rinsed under running tap water (van Franeker

and Meijboom, 2002). Proventriculus and gizzard tissues were examined for

inflammation, abrasion, or swelling from exposure to debris. Care was taken to note any

indications of damage from birdshot. Proventriculus and gizzard contents were

transferred to a Petri dish, and inspected under a dissecting microscope (AmScope SM-

2BZ) as follows:

a) Anthropogenic debris was identified (per Desforges et al., 2015 and Zhao et al.,

2016) if: i) no cellular or organic structures were visible; ii) fibers were

uniformly thick over their length and not tapered at the end, bendable, or soft; iii)

colored items were homogeneously colored and of hues not usually occurring in

food; iv) debris had unnatural edges of obvious anthropogenic origin. All

potential microscopic anthropogenic debris was re-examined with extra care and

under higher magnification (4.5× zoom objective). Once classified as artificial

material, particles were transferred into Petri dishes and ready for step b). If there

was an indication of birdshot damage to digestive organs, shot was assumed to

have been hunting-related, and not consumed, and was therefore not included in

analysis as contaminant debris.

b) Anthropogenic debris was classified following van Franeker and Meijboom

(2002): plastic (fragments and other), non-plastic rubbish (thread-like, foil, paint

chips, glass, and rubber), and metal (birdshot and metal fragments).

21

Anthropogenic debris was classified as either light (clear-white, yellow, light

green-blue, pink-tan) or dark (red-orange, dark green, dark blue-purple, brown-

black; Day et al., 1985; Moser and Lee, 1992). After sorting contents under a

dissection microscope, items were counted for each bird. Each particle was

measured (in mm) for length, width, and height or diameter (only for round

debris, and measured where widest). Debris was photographed for subsequent

analyses. Once confirmed, anthropogenic debris items were removed from a

sample, and remaining items were categorized as natural.

Statistical analyses

Previous studies using power analyses have generally found that a minimum of 18

to 40 or more individuals per species are required for reliable estimates of intraspecific

prevalence (van Franeker and Meijboom, 2002; Provencher et al., 2015), so we used a

minimum sample size of 18 individuals to include a species in interspecific comparisons.

We used Fisher exact tests for most comparisons because >20% of the cells had expected

counts of less than five (Cochran, 1954). We used logistic regression to test if debris

presence was related to interspecific and intraspecific variation in body mass. Statistical

analyses were performed in program R (version 3.2.2; R Core Team, 2015) using the

“dplyr” package (Wickham and Francois, 2015). Values are reported as mean ± SD

unless otherwise stated.

22

Results

We obtained data from 350 birds of 18 species, including three herbivorous geese,

eight omnivorous dabbling ducks, three omnivorous diving ducks, one carnivorous sea

duck, and three piscivorous loons (Table 1; all diving duck and loon species sampled are

partially marine species that breed on inland freshwater bodies. All individuals of these

species in this study were culled inland). Because we recovered no debris from the

proventriculus (nor have others, e.g., Day et al., 1985; Moser and Lee, 1992; Robards et

al., 1995), hereafter we focus only on the gizzard. We found 110 items of anthropogenic

debris, ranging in size from 50 μm to 5 mm (hence all plastic debris would be classified

as microplastics; Arthur et al., 2008; Moore, 2008; Ivar do Sul and Costa, 2014), in 10 of

18 (55%) species, and 40 of 350 (11.4%) birds, with an average of 0.31 (± 3.1) items per

bird. Sample sizes for the eight species that did not have ingested anthropogenic debris

were all < 15, so their anthropogenic debris prevalence of zero should be interpreted

cautiously. There was no difference in debris ingestion among foraging niches (Table 1;

Fisher exact test, p > 0.99).

Of the 10 species with ingested debris, five had the minimum recommended

samples of 18 (Table 1). These species had similar prevalences of anthropogenic debris

(Fisher exact test, p = 0.50). For species with the recommended minimum sample sizes

[we had mass data for < 12 Canada geese (Branta canadensis) and American wigeon

(Anas americana)], interspecific variation in body mass was not associated with

anthropogenic debris ingestion (logistic regression, t1, 99 = 0.5, p = 0.64) nor was

intraspecific variation in body mass associated with debris ingestion (three species, all N

23

for individuals with body mass > 24, all t < 0.34, all p > 0.60]. A more detailed

breakdown is presented in Table 2 (also see Appendix A), but is not amenable to

statistical analysis.

Plastic debris was present in eight species and 15 of 350 (4.3%) birds; prevalence

did not differ among species with sufficient samples (Fisher exact test, p = 0.85). Non-

plastic rubbish was present in six species, and ingested by 13 of 350 (3.7%) birds. Non-

plastic rubbish prevalence did differ among species with sufficient samples [Fisher exact

test, p = 0.01; Canada goose (7/43, 16.3%), American wigeon (1/32, 3.1%), mallard

(3/120, 2.5%), common eider (1/40, 2.5%), snow goose (Chen caerulescens; 1/47,

2.1%)]. Metal debris was present in six species, and ingested by 12 of 350 (3.4%) birds,

and prevalence did not differ among species with sufficient samples (Fisher exact test, p

= 0.48). All ingested birdshot was a non-toxic alternative to lead shot, such as steel, based

on uncrushed, rounded shapes of recovered pellets. One northern pintail (Anas acuta) had

17 lead birdshot pellets in its gizzard, but was presumably hunted with this shot. Pellet

composition was determined visually and with a simple crush test. Lead pellets tend to be

deformed and fragmented upon impact with soft tissues and bone, whereas steel shot

usually remains round (Wilson, 1999; Peitzman et al., 2012). The remaining metal

fragments were metalworking waste (swarf).

Prevalences of anthropogenic debris in British Columbia (23/145, 15.9%), Nova

Scotia (6/74, 8.1%), Northwest Territories (5/66, 7.6%), Newfoundland (3/29, 10.3%),

Ontario (1/19, 5.3%) and New Brunswick (0/13) (Fig. 2) were not statistically different

(Fisher exact test, p = 0.30). Of four common eiders without accompanying information

on origin, one had ingested debris.

24

Ingested particle coloration was classified for all debris except birdshot (7/39,

17.9%), because we assume birds encounter this by accident and it becomes retained as if

it were grit (a mixture of mineral, rock, and hardened food fragments retained to aid in

fibrous food digestion; Thomas et al., 1977). Light-colored anthropogenic debris was

more commonly ingested (27/32, 84.2%) than dark colored (5/32, 15.6%). Clear and

white debris were the most common colors ingested by all species (11/32, 34.4%). Gold

was the second most commonly ingested color (4/32, 12.5%), and black was the least

common (1/32, 3.1%). All other colors (light yellow, light green-blue, dark green, dark

blue-purple) were ingested with the same frequency (2/32, 6.3%).

Discussion

Prevalence of anthropogenic debris in freshwater birds and the marine common

eider comparison group presented in this study (11.4%) provides compelling evidence

that freshwater and marine organisms currently face similar threats from anthropogenic

debris ingestion. Although our sample was mostly limited to commonly hunted or culled

species, our results suggest that anthropogenic debris ingestion by freshwater birds is

likely to apply to a wider range of species, because anthropogenic debris ingestion was

found in some species for which we had small samples. We expect that sampling of other

waterfowl and freshwater bird species (such as herons and kingfishers) will likely reveal

ingestion of anthropogenic debris.

Seabird plastic ingestion is assumed to occur because plastics mimic natural food

items (Day et al., 1985; Moser and Lee, 1992). Although freshwater birds may mistake

plastic debris as food, the high prevalence of birdshot (which they encounter

25

opportunistically after it sinks into sediment, and does not appear to mimic any known

food items) suggests freshwater birds may be retaining birdshot as grit (Thomas et al.,

1977; Moore et al., 1998). They could also acquire small, broken pieces of plastic debris

in this manner. Some seabirds consume specific plastic shapes and colors more

frequently, and debris ingestion ties into foraging niche and availability of certain plastics

in particular habitats (Day, 1980; Day et al., 1985; Ryan, 1987; Moser and Lee, 1992).

Surface-feeding species are most likely to have plastics in their diets, perhaps due to

polyethylene’s specific gravity of 0.9, enabling plastics to float at the water’s surface

(Snyder and Vakos, 1966; Day et al., 1985; Moser and Lee, 1992). Although our study

supports previous evidence that birds preferentially ingest lighter colored debris

(Rothstein, 1973; Day, 1980; Moser and Lee, 1992; Lavers and Bond, 2016), we cannot

evaluate whether this reflects selective uptake without knowing availability in the

environment. However, we did not find evidence that debris ingestion was related to

foraging niche.

Anthropogenic debris ingestion by freshwater birds should also be an important

issue to waterfowl hunters. In 2013 alone, approximately 189,844 individuals across

Canada hunted approximately 2,286,951 waterfowl (Environment and Climate Change

Canada, 2016; Gendron and Smith, 2016). Given that debris can vector various

contaminants (Teuten et al., 2007; Ashton et al., 2010; Rios et al., 2010) this may put

hunters such as Aboriginal peoples, who rely most heavily on wild foods (Van Oostdam

et al., 1999; Johansen et al., 2001; El-Hayek, 2007), at risk of consuming contaminated

tissues. Quantifying plastic-associated toxins is crucial to understanding potentially

26

hidden effects of anthropogenic debris ingestion on Aboriginal peoples and other

vulnerable groups, and to developing future avian conservation plans.

In contrast to marine anthropogenic debris, microscopic anthropogenic debris in

freshwater ecosystems may be perceived as an environmental issue that is closer to home,

hopefully resulting in more scientific and public attention. One example of this is the

recent passing of the Microbead Free Waters Act of 2015 in the United States (House

Report No. 114-371, 2015). Microbead use has increased in recent years, and their

relatively small diameter (< 1 mm) means many wastewater treatment plants cannot

remove them, leading to an increase of these plastics entering aquatic ecosystems

(Castañeda et al., 2014; Doughty and Eriksen, 2014; Driedger et al., 2015). The resultant

increase in microbead concentrations in waterways led to public outcry, and shortly

thereafter many major companies banned microbeads (Newman et al., 2013). Although

care was taken in our study to find microbeads, none were recorded. This could be due to

the sieves used. Our finest was a 0.5 mm mesh, the same size used by (Castañeda et al.,

2014) to sieve microbeads from river sediment. However, despite our similar sieve size,

we found that running a microbead-containing product (Clean & Clear® morning burst®

facial scrub) through our sieve permitted passage of smaller beads, retaining only less

frequent larger beads. Similarly, larger beads could have been ground down over time in

gizzards, permitting their passage through our sieve. Therefore our microbead findings

should be interpreted cautiously, because waterfowl are likely ingesting them.

Our results on the prevalence of anthropogenic debris ingestion in waterfowl

indicate that it is occurring at similar rates to historic trends in in some marine birds

(Laist 1997) and current rates in some freshwater birds (English et al., 2015). Future

27

studies examining gut contents of freshwater birds should adopt a screening method for

anthropogenic debris similar to that of van Franeker and Meijboom (2002) and van

Franeker (2004), and collection points for examination of harvested bird digestive tracts

should be established. This could be essential in monitoring anthropogenic debris

ingestion over a number of years to reliably assess trends.

Conclusions

Our study adds to the limited but mounting evidence (Moser and Lee, 1992;

Denuncio et al., 2011; Besseling et al., 2014; Sanchez et al., 2014; English et al., 2015;

Moseman, 2015; Fischer et al., 2016) that anthropogenic debris may be a threat to aquatic

biota in freshwater environments. We found debris in 55% of species collected from

freshwater habitats in Canada, including from remote sites as far as 63ºN. However, there

was no suggestion of patterns in anthropogenic debris ingestion relative to body mass,

geographic location of capture, or foraging niche. This was surprising, because we

expected that birds collected near urban or industrial centers (where debris may occur at

higher densities; Zbyszewski et al., 2014) or those foraging as carnivores or omnivores

might be more likely to ingest anthropogenic debris. We did not acquire many samples

from the Great Lakes region, where research has shown significant pollution by plastic

(Eriksen et al., 2013; Castañeda et al., 2014; Driedger et al., 2015), and thus we expect

that greater sampling effort of birds wintering there will reveal higher prevalence of

ingested plastic and other debris. Consequently, we suggest that our data represent a

conservative baseline of anthropogenic debris ingestion in waterbirds in Canada and we

28

expect that additional studies will confirm debris ingestion in other species, as has been

shown in marine birds (Provencher et al., 2015).

Although there is evidence that anthropogenic debris is a threat to aquatic biota,

there is still a need for long term monitoring to provide input for conservation

management, to strengthen the basis for educational campaigns, and to provide scientists

with better evidence that could be used to increase efforts to mitigate the problem

(Derraik, 2002). Our baseline data provide insights suggesting that this may have to occur

sooner than expected to prevent waterfowl debris ingestion levels from reaching the

levels currently observed in seabirds.

29

Figure 2. Sample sites used for this study. Circles indicate collection locations. BC:

British Colombia, NT: Northwest Territories, ON: Ontario, NB: New Brunswick, NS:

Nova Scotia, NL: Newfoundland.

30

Table 1. Sample sizes, body mass ± SE (g), the frequency, and mean number of pieces ± SE for plastic, metal, and any debris. N =

number of specimens dissected. Means include birds without ingested debris. GWFG = greater white-fronted goose; SNGO = snow

goose; CAGO = Canada goose; GADW = gadwall; AMWI = American wigeon; ABDU = American black duck; MALL = mallard;

BWTE = blue-winged teal; NOSH = northern shoveler; NOPI = northern pintail; GWTE = green-winged teal; LESC = lesser scaup;

WWSC = white-winged scoter; LTDU = long-tailed duck; COEI = common eider; RTLO= red-throated loon; COLO = common loon;

YBLO = yellow-billed loon.

Mean body

mass ± SE (g)

Ingestion frequency (%) Mean pieces of debris/bird ± SE

Foraging niche Species N Plastic Rubbish Metal Plastic Rubbish Metal

Geese GWFG 2 1616 ± 203 0.0 0.0 50.0 0.00 ± 0.00 0.00 ± 0.00 0.50 ± 0.71

SNGO 47 2119 ± 423 2.1 2.0 2.1 0.02 ± 0.15 0.02 ± 0.15 0.02 ± 0.15

CAGO 43 3584 ± 241 4.7 14.0 0.0 0.05 ± 0.30 0.21 ± 0.51 0.00 ± 0.00

Dabbling Ducks GADW 2 836 ± N/A 0.0 0.0 0.0 0.00 ± 0.00 0.00 ± 0.00 0.00 ± 0.00

AMWI 32 738 ± 102 6.3 3.1 0.0 0.06 ± 0.25 0.03 ± 0.18 0.00 ± 0.00

ABDU 5 1242 ± N/A 0.0 0.0 20.0 0.00 ± 0.00 0.00 ± 0.00 0.25 ± 0.50

MALL 120 1185 ± 178 5.0 2.5 5.0 0.07 ± 0.34 0.52 ± 5.21 0.08 ± 0.37

BWTE 1 N/A 0.0 0.0 0.0 0.00 ± N/A 0.00 ± N/A 0.00 ± N/A

31

Mean body

mass ± SE (g)

Ingestion frequency (%) Mean pieces of debris/bird ± SE

Foraging niche Species N Plastic Rubbish Metal Plastic Rubbish Metal

NOSH 1 N/A 0.0 0.0 0.0 0.00 ± N/A 0.00 ± N/A 0.00 ± N/A

NOPI 10 762 ± 50 10.0 10.0 10.0 0.10 ± 0.32 0.00 ± 0.00 0.20 ± 0.63

GWTE 15 325 ± N/A 0.0 0.0 0.0 0.00 ± 0.00 0.00 ± 0.00 0.00 ± 0.00

Diving Ducks LESC 1 N/A 0.0 0.0 0.0 0.00 ± N/A 0.00 ± N/A 0.00 ± N/A

WWSC 16 N/A 6.3 0.0 0.0 0.06 ± 0.25 0.00 ± 0.00 0.00 ± 0.00

LTDU 4 N/A 0.0 0.0 0.0 0.00 ± 0.00 0.00 ± 0.00 0.00 ± 0.00

Sea Ducks COEI 40 1825 ± 126 2.5 2.5 5.0 0.02 ± 0.16 0.10 ± 0.63 0.05 ± 0.22

Loons RTLO 7 N/A 0.0 0.0 0.0 0.00 ± 0.00 0.00 ± 0.00 0.00 ± 0.00

COLO 1 N/A 0.0 0.0 0.0 0.00 ± N/A 0.00 ± N/A 0.00 ± N/A

YBLO 3 N/A 33.3 0.0 0.0 0.33 ± 0.58 0.00 ± 0.00 0.00 ± 0.00

32

Table 2. Amount and types of debris recovered from the ten species that ingested debris. N = number of anthropogenic debris

fragments recovered. GWFG = greater white-fronted goose; SNGO = snow goose; CAGO = Canada goose; AMWI = American

wigeon; ABDU = American black duck; MALL = mallard; NOPI = northern pintail; WWSC = white-winged scoter; COEI = common

eider; YBLO = yellow-billed loon.

Foraging niche

Species

Plastic (N) Rubbish (N) Metal (N)

Fragments Other Thread-like Foil Paint chips Glass Rubber Birdshot Metal

Geese GWFG 0 0 0 0 0 0 0 0 1

SNGO 1 0 1 0 0 0 0 0 1

CAGO 2 1 0 5 1 2 0 0 0

Dabbling Ducks AMWI 2 0 0 0 0 1 0 0 0

ABDU 0 0 0 0 0 0 0 1 0

MALL 8 0 0 4 0 1 57 8 1

NOPI 1 0 0 0 0 1 0 1 0

Diving Ducks WWSC 1 0 0 0 0 0 0 0 0

Sea Ducks COEI 1 0 0 4 0 0 0 1 1

Loons YBLO 1 0 0 0 0 0 0 0 0

33

CHAPTER THREE: ANTHROPOGENIC DEBRIS AND PATHOLOGY OF

FULMARS AND SHEARWATERS BEACHED ON SABLE ISLAND, NOVA

SCOTIA, CANADA

Introduction

Throughout the world seabirds are frequently found dead on beaches, with

recorded reports from Europe as early as the late 19th century (Gray, 1871; Stephen and

Burger, 1994; Furness and Camphuysen, 1997). These “beached bird” carcasses can

provide an opportunistic window into seabird diets and causes of death (Barrett et al.,

2007). However they may be biased, often revealing that beached birds are primarily

emaciated individuals which have likely starved to death (Barrett et al., 2007). Autopsies

of beached birds can provide information on causes of death, diet prior to death, and

other deleterious health conditions (Camphuysen and Heubeck, 2001; Roletto et al.,

2003; van Franeker et al., 2011). Likewise, beached bird surveys can record any large

species die offs or sudden influxes of dead oiled birds (Camphuysen and Heubeck, 2001;

Roletto et al., 2003; Balseiro et al., 2005). This information is important for monitoring

disease outbreaks and quantifying impacts of human activities (Camphuysen and

Heubeck, 2001; Balseiro et al., 2005).

Although the majority of seabird mortality is likely natural, and related to

biotoxins, infectious diseases, emaciation, trauma, and predation, anthropogenic causes of

mortality may also be responsible (Newman et al., 2007). One commonly recorded

anthropogenic cause of seabird death is entanglement in and ingestion of marine

34

anthropogenic debris (Moser and Lee, 1992; Newman et al., 2007). With respect to the

latter, debris, most commonly plastic, is problematic due to concerns about its toxicity,

digestive tract blockage, internal abrasion, and attendant starvation (Moore, 2008; Wright

et al., 2013). Written records of humans releasing anthropogenic debris into the

environment exist since the early 1900s (Klar et al., 2014), and studies on seabird debris

ingestion have been conducted since the 1960s (Kenyon and Kridler, 1969). Surface-

feeding seabirds, such as fulmars and shearwaters, may be particularly susceptible to

plastic ingestion because plastics can float at the water surface and appear to be food

(e.g., specific gravity of polyethylene is 0.9; Day et al., 1985; Snyder and Vakos, 1966).

Fulmar and shearwater species are long-lived (> 40 years; Michel et al., 2003),

philopatric (86% per annum rate of nest-site return; Macdonald, 1977), largely pelagic

seabirds, which only come to land only to breed (Powers, 1984). However, many pass by

islands on the Atlantic Coast during migration, and birds that die at sea occasionally wash

onto shores of islands (Bond et al., 2014). Sable Island is situated 160 km east of Halifax,

Nova Scotia (Canada; 43.9337° N, 59.9149° W). Sable Island is 45 km long, crescent-

shaped, and sandy with over 64 species of beached seabirds collected since the 1970s

(Lucas et al., 2012). Sable Island is a potentially highly valuable monitoring site because

large numbers of Procellariiformes are encountered dead regularly on the beaches (Lucas

et al. 2012). To date, no information exists on pathologies of birds beached on Sable

Island, because most published studies deal with anthropogenic causes of death, such as

oiling and anthropogenic debris ingestion (Bond et al., 2014; Lucas and MacGregor,

2006). Although beached bird surveys have been conducted on Sable Island since the

1970s, surveys to determine persistent coastal litter only started in the early 1980s

35

(Gregory, 1983; Lucas, 1992). These surveys found that the majority of total

anthropogenic material present on Sable Island’s beaches was plastic (Gregory, 1983;

Lucas, 1992). In fact, up to 93% of northern fulmars (Fulmarus glacialis) beached on

Sable Island have ingested plastic (Bond et al., 2014).

Across their broad range, high rates of plastic ingestion by northern fulmar are

well documented, so much so that these birds are used as an indicator species on the state

of the North Sea ecosystem (van Franeker, 2004). Current Ecological Quality Objective

targets have been established in the North Sea of no more than 10% of fulmars having >

0.1 g of ingested plastic (OSPAR Commission, 2010). However, relatively recent surveys

showed that 48–78% of fulmars exceed this goal (van Franeker et al., 2011).

Northern fulmars have variability in plumage coloration, and this coloration may

be related to their breeding success and life history (Hatch, 1991). A four color phase

system is used to classify fulmar plumage morphs: single light, double light, single dark,

and double dark (O’Reilly, 1818; Fisher, 1952; van Franeker and Wattel, 1982).

However, in practice the main distinction is made between the double light color phase

and the darker color phases (van Franeker, 2004; van Franeker and Luttik, 2008). Double

light individuals make up nearly 100% of southern subspecies in the temperate breeding

range, and a variable proportion (0-10%) of Arctic populations (van Franeker, 2004; van

Franeker and Luttik, 2008). Previous studies have found no statistical differences in

stomach plastic content between the different color morphs (Trevail et al., 2015).

However, these studies examined only individuals from the single light, single dark, and

double dark color phases (Trevail et al., 2015). The lightest fulmar morphs (double light)

have a more southerly distribution (Hatch, 1991); thus they are likely exposed to more

36

debris, and therefore may consume debris at a greater frequency (van Franeker and Law,

2015).

Although not as well studied as northern fulmars, plastic ingestion among

shearwater species has also been documented, with 83% of Cory’s shearwater

(Calonectris borealis), 72% of sooty shearwater (Ardenna grisea), and 88% of great

shearwater (Ardenna gravis) having ingested plastic (Rodríguez et al., 2012; Bond et al.,

2014). Comparisons to northern fulmar show that great shearwater did not differ in the

proportion of ingested debris, whereas sooty shearwaters had a lower frequency of debris

ingestion (Bond et al., 2014).

Beached birds of all four of the preceding seabird species were collected on Sable

Island, Nova Scotia, Canada. Sooty shearwaters, great shearwaters, and northern fulmars

are found beached regularly on Sable Island, whereas Cory’s shearwaters rarely range

into Canadian waters (Lucas et al., 2012). Between 1993 and 2009, only 14 of the latter

species were recorded beached on Sable Island (Lucas et al., 2012), and during our

collection period only three birds were collected. Due to this small sample size reliable

analyses could not be run on this species independently of the others.

The purpose of this study was to quantify pathological findings of beached birds

of these species, as well as to asses the time of year, gender, and relative age of birds

beaching on Sable Island, determine if pathology was associated with these variables, and

compare nutritional condition of these birds in relation to mass of anthropogenic debris

ingested.

37

Materials and Methods

Sample collection and processing

Intact procellariid carcasses were collected from the entire Sable Island shoreline

between July 2000 and January 2012. The majority of birds were collected during

beached bird surveys conducted every 25-45 days (weather and beach conditions

permitting), with the longest interval between surveys being 96-days (additional details in

Lucas et al., 2012). The remainder of birds were gathered opportunistically when

encountered on the beach (Lucas et al., 2012). Carcasses were frozen and stored on the

island prior to shipment to the Department of Pathology and Microbiology, Atlantic

Veterinary College, University of Prince Edward Island in Charlottetown, Prince Edward

Island, Canada. Carcasses were then dissected at the Atlantic Veterinary College, where

the upper gastrointestinal tract was removed, ingested anthropogenic material was

quantified, and pathology was determined (see Bond et al., 2014 for further detail).

Gender and age (immature or adult) were determined based on the criteria

described by van Franeker (2004). Carcasses were examined for external lesions, debris

entanglement, or other signs of trauma. Emaciation was characterized by severe atrophy

of the pectoral muscles, complete absence of subcutaneous and/or abdominal fat deposits,

and serious atrophy of the pericardial fat. Samples for histopathology were collected from

the brain, heart, lung, gizzard, liver, kidney, bursa, adrenal, ovary or testis, and skeletal

system. Liver, kidneys, lungs, intestine, and duodenum swabs were submitted for

38

bacteriological investigations to the Department of Pathology and Microbiology at the

Atlantic Veterinary College.

Statistical analyses

Previous studies using power analyses have generally found that a minimum of 18

to 40 or more individuals per species are required for reliable estimates of intraspecific

prevalence of debris ingestion (van Franeker and Meijboom, 2002; Provencher et al.,

2015). Chi-squared and Fisher exact tests (the latter when expected values were less than

5 for any cell) were used to test for relationships between the explanatory variables age

and gender and the response variable pathology, categorized as emaciated or ‘other’

(representing all pathology other than emaciation and pooled because of small samples

sizes) (Cochran, 1954; Larntz, 1978). Generalised Linear Models (GLM; Venables and

Ripley, 2002) were used to test for relationships between pathology (emaciated or

‘other’), individual mass (heavily scavenged or soiled carcasses were not included), and

mass of ingested debris, for all species and within species if sample sizes were sufficient.

We evaluated whether the mass of debris consumed was negatively associated

with body condition, through a principle components analysis (PCA). To do this we first

calculated a correlation matrix of structural measurements which was used to generate PC

scores of “size” (Wold et al., 1987) for northern fulmars on five structural variables:

culmen, bill depth, total head, tarsus, and wing (Mallory and Forbes, 2005). On the

remaining three species, metrics of structural measurements were not recorded. We used

PC1 scores for each fulmar as a measure of body size and regressed mass on PC1 to

39

determine body condition (Kirk and Gosler, 1994). This metric of condition was then

regressed against mass of debris ingested (Blanco et al., 1997).

Means are reported ± standard deviation unless noted otherwise. Statistical

analyses were performed in R (version 3.2.2; R Core Team, 2015) using the “dplyr” and

“broom” packages (Wickham and Francois, 2015; Robinson, 2016).

Results

We gathered data from 318 seabird carcasses (Table 3). The majority of birds

recovered were northern fulmars (55%) and great shearwaters (28%), and were primarily

immature birds of all species (222/318; 70%). Most birds were collected between March

and July when regular surveying due to stable beach conditions was possible (Fig. 3).

Winter conditions on Sable Island often result in narrow beach profiles, eroded peat,

irregular beach topography, decreased visibility, post-storm flooding, and an increased

prevalence of beach debris, all of which affect detectability of beached birds and

increased the intervals between surveys (Lucas et al., 2012)

Pathological symptoms (defined in Table 4) were found for 251 (79%) of the 318

collected individuals, with most birds displaying symptoms of emaciation (54%),

followed by autolysis (8%), parasite infection (3%), inflammation (3%), trauma (3%),

bacterial infection (2%), drowning (2%), tumors (1%), tissue necrosis (1%), egg and

rectal impaction (1%), myopathy (1%), or pneumonia (1%) (some additional pathological

and histological details are given in Appendix B). Northern fulmars washed up dead of

40

emaciation less frequently (69/115; 60%) than sooty (36/48; 75%) or great (67/86; 78%)

shearwaters (χ21 = 8.36, p = 0.02; Cory’s shearwater not tested due to small sample size).

Sooty Shearwater

Of 50 sooty shearwaters, pathological symptoms were found in for 48 (96%;

Table 4). Pathology was not related to sex (Fisher's exact test; p = 0.44) or age (p > 0.99).

Likewise, pathology was not related to the mass of debris (0.07 ± 0.17 g; Bond et al.,

2014) an individual had ingested (R2 = 0.01, F1, 45 = 0.50, p = 0.48), or body mass (R2 =

0.07, F1, 37 = 2.80, p = 0.10). Mass of debris ingested was also not related to body mass

(R2 < 0.01, F1, 38 = 0.1, p = 0.78; Table 5).

Great Shearwater

Pathology was found in 86 of 89 (97%) of great shearwaters (Table 4). Pathology

was not related to sex (χ21 < 0.1, p = 0.91) or age (p = 0.78). Likewise, pathology was not

related to the mass of debris (0.17 ± 0.33 g; Bond et al., 2014) an individual had ingested

(R2 < 0.01, F1, 78 = 0.37, p = 0.54), or individual mass (R2 = 0.02, F1, 75 = 1.19, p = 0.28).

Mass of debris ingested was also not related to mass of the individual (R2 < 0.01, F1, 71 =

0.3, p = 0.58; Table 5).

41

Northern Fulmar

Of 176 carcasses of northern fulmars, pathology was found in 115 (65%; Table

4). Pathology was not related to sex (χ21 = 0.2, p = 0.68) or age (χ2

1 < 0.1, p = 0.91).

Likewise, pathology was not related to the mass of debris (1.09 ± 1.93 g; Bond et al.,

2014) an individual had ingested (R2 < 0.01, F1, 113 = 0.02, p = 0.88), or individual mass

(R2 = 0.04, F1, 73 = 3.32, p = 0.07), and mass of debris ingested was not related to mass of

the individual (R2 < 0.01, F1, 113 = 0.1, p = 0.74; Table 5).

The first principal component (PC1) of the five morphometric variables had

loadings ranging from -0.51 to -0.35 (eigenvalue 2.83) and accounted for 57% of the total

original variance, more than expected by chance (Jackson, 1993). Residuals saved from

regressions on PC1 against body mass showed that body condition was not related to

mass of debris ingested (F1, 91 = 0.1, p = 0.80).

Fulmar plumage was grouped into two categories, double light and single dark,

because no single light birds were collected, and only one double dark individual was

collected. Double light birds made up the majority of beached birds (169/176; 96%).

There was no statistically significant difference in mass of debris ingested by fulmars of

these two morphs (Fig. 4; ANOVA F1, 174 = 1.5, p = 0.23).

42

Discussion

This is the first systematic pathological investigation of beached seabirds from

Sable Island, and builds on the detailed surveys on age and type of beached birds that

have previously been conducted (Lucas et al., 2012). The birds we analyzed had limited

physiological or tissue trauma, perhaps less than one might associate with high levels of

anthropogenic debris ingestion (Pierce et al., 2004). This suggests that post-mortem

dietary analyses of beached birds are a useful approach to monitoring ingestion amounts

and rates, but that ascertaining causes of mortality, or attributing them to debris, is more

difficult. This is especially true because most beached birds collected have likely died of

starvation.

The northern fulmar is an indicator species of the state of the North Sea

ecosystem within the current Ecological Quality Objectives (van Franeker, 2004; OSPAR

Commission, 2010), and thus it would be beneficial to know common causes of

mortality. Although three of the species studied (northern fulmar, Cory’s shearwater, and

great shearwater) are listed as Least Concern by the IUCN (BirdLife International, 2016a,

2016b, 2016c), the sooty shearwater is listed as Near Threatened, with a population trend

designated as decreasing (BirdLife International, 2016d). This designation should prompt

further studies into common causes of death in this species, both natural and

anthropogenic.

Northern fulmars were emaciated less often than sooty and great shearwaters. It’s

unlikely this is due to age, because 84% of sooty shearwaters were juvenile, a larger

proportion than northern fulmars (70%) and great shearwater (69%). A contributor to this

43

disparity may be species movements and home ranges, because northern fulmars are

transatlantic migrants, breeding in the Canadian Arctic and wintering in the northwest

Atlantic Ocean (Mallory et al., 2008), whereas both shearwater species are

transequatorial migrants that breed in the southern hemisphere (Huettmann and Diamond,

2000). As a group, the shearwater’s longer migratory pathways may be associated with

greater energetic stresses and more frequent emaciation. Fulmars could also encounter

conditions that lead them to die suddenly and not become emaciated. This may include

high organochloride tissue contamination. Fulmars have higher rates of plastic ingestion

than shearwaters, and fulmar muscle, fat, and eggs contain PCBs, DDTs,

hexachlorobenzene (HCB), and polybrominated diphenyl ethers (PBDEs) (Fängström et

al., 2005). Further research into the differences in rates of emaciation between these three

species is warranted.

For Sable Island, mortality rates and pathology of marine birds were not available

for comparison to our results. However, the main pathological findings, emaciation and

autolysis, were not unexpected in a sample composed of primarily immature beached

birds (Barrett et al., 2007). These findings attest to the challenges birds face surviving at

sea, especially weak, young, and inexperienced animals. Most parasitic and bacterial

infections in these birds had been recorded previously in these four species, as had many

cases of inflammation, trauma, and tumors (Appendix C). Avian influenza, a disease of

recent concern (Lang et al., 2016), was not found in any of the specimens that we

examined. Similarly, we did not detect avian cholera, despite recent outbreaks of this

disease in larids of this region (Wille et al., 2016).

44

Pathological symptoms we reported have been recorded in other seabird species.

Autolysis is often reported in beached birds, although in many cases it has likely occurred

post-mortem (Stephen and Burger, 1994; Harris et al., 2006). Capture myopathy has been

reported in many seabird species (Newman et al., 1997) but has not previously been

noted in beached birds. Multi-organ, including hepatic, necrosis has been recorded in

wedge-tailed shearwater (Puffinus pacificus), although we found no previous reports of

tissue necrosis for sooty shearwater, great shearwater, or northern fulmar (Work and

Rameyer, 1999). Likewise, there are no mentions of sarcocystosis in great shearwater and

northern fulmar in the literature; however, the protozoan Sarcocystis has been reported in

common murre (Uria aalge) (Muzaffar and Jones, 2004). Trematodes and pododermatitis

in northern fulmar have not previously been reported; however other seabird species have

had these symptoms (Haman et al., 2013; Bogstad et al., 2014). Septicemia has been

recorded in many seabird species previously, but always in relation to rehabilitation

(Lieske et al., 2002; Steele et al., 2005). Mycobacteriosis has not previously been

recorded in seabirds, but has been in dunlin (Calidris alpina) and oystercatchers

(Haematopus ostralegus) (Pennycott, 2016).

Some novel pathological findings we report may have been observed before (e.g.,

unpublished findings, or those outside of indexed peer-reviewed journals and

publications in languages other than English). Some of these pathologies may have been

difficult to detect because beached bird surveys often yield decaying and/or heavily

scavenged carcasses, making necropsies difficult (Stephen and Burger, 1994). Carcass

mass can also be difficult to accurately ascertain in cases where birds are wet, covered in

sand, or scavenged.

45

Data were clearly biased towards immature and emaciated individuals as well as

double light birds. The majority of birds were collected in spring and summer due to

decreased winter sampling, so reliable tests could not be run on these data. Due to our

sample sizes, ages, seasons and year were pooled, which could have obscured patterns.

For all three species with sufficient data, pathology was neither related to the

mass of debris ingested nor body mass, and mass of debris ingested was unrelated to

body mass. This was surprising because previous studies have found that heavier birds

were more likely to contain ingested plastics (Spear et al., 1995; Verlis et al., 2013).

Body condition could only be calculated for fulmars, and despite some prior studies

finding that birds with higher amounts of ingested plastic had reduced body condition

(e.g., Ryan, 1987), we found no support for this prediction. However, this is consistent

with Avery-Gomm et al. (2016) who found no connection between dovekie (Alle alle)

body condition and mass of plastic ingested. Our findings could be due to debris amounts

being below thresholds known to affect a bird, although data for these thresholds are hard

to determine. Current thresholds are only available in the literature for northern fulmars

and the Ecological Quality Objectives (OSPAR Commission, 2010; Bond and Lavers,

2013). These objectives are arbitrary, as no biologically meaningful level has yet been

established (OSPAR Commission, 2010).

Because anthropogenic debris is increasing in the world’s oceans, even species

with northern ranges or in seemingly remote locations are being exposed (Provencher et

al., 2015; Trevail et al., 2015; Amélineau et al., 2016). Recent reports of microplastics

have been confirmed in Arctic waters in concentrations comparable to those of other

oceans, and recent studies have documented plastic ingestion by Arctic birds (Provencher

46

et al., 2015; Trevail et al., 2015; Amélineau et al., 2016). Studies of beached bird

mortalities, pathology, and debris ingestion are important for tracking trends among

endangered and non-threatened species. Without these baseline studies, it is hard to

determine if threats facing wild populations are sustainable long term, or emerging and

deadly to long-term species survival. Because Sable Island is the only site in Atlantic

Canada where large numbers of Procellariiformes are encountered regularly (Lucas et al.,

2012), it could be an important monitoring site for marine anthropogenic debris, seabird

mortality, and pathology.

47

Table 3. Overview of the number and corresponding percentages of age, sex, and season collected, for four species of

Procellariiformes collected beached on Sable Island, Nova Scotia, between 2000 and 2012. Seasons delimited by seasonal equinoxes.

COSH = Cory’s shearwater; GRSH = great shearwater; N = Number collected; NOFU = northern fulmar; SOSH = sooty shearwater;

Unk. = Unknown.

N (%)

Immature Adult Age unknown Season

Species Male (%)

Female (%)

Unk. (%)

Male (%)

Female (%)

Male (%)

Female (%)

Unk. (%)

Spring (%)

Summer (%)

Fall (%)

Winter (%)

Unk. (%)

COSH 3 (1) - - - 1 (33) 2 (67) - - - 2 (67) - 1 (33) - - SOSH 50 (16) 24 (48) 16 (32) 2 (4) 3 (6) 2 (4) - - 3 (6) 32 (64) 18 (36) - - - GRSH 89 (28) 35 (39) 26 (29) 1 (1) 7 (8) 6 (7) 9 (10) - 5 (6) 12 (13) 75 (84) 1 (1) - 1 (1) NOFU 176 (55) 52 (30) 55 (31) 10 (6) 19 (11) 10 (6) 11 (6) 8 (5) 11 (6) 107 (61) 13 (7) 19 (11) 34 (19) 3 (2) Total 318 (100) 111 (35) 97 (31) 13 (4) 30 (9) 20 (6) 20 (6) 8 (3) 19 (6) 152 (48) 106 (33) 22 (7) 34 (11) 4 (1)

48

Table 4. Pathology, ranked from most to least common, in 318 procellariids collected

beached on Sable Island, Nova Scotia, Canada, between 2000 and 2012. Percentage of

total by species displayed in brackets. “-” indicates no symptoms were found.

PATHOLOGY

Cory’s Shearwater

(%)

Sooty Shearwater

(%)

Great Shearwater

(%)

Northern Fulmar

(%)

Total

(%) Starvation 1 (33) 36 (72) 67 (75) 69 (39) 173 (54) Unknown - 2 (4) 3 (3) 61 (35) 66 (21) Autolysis 2 (67) 7 (14) 5 (6) 12 (7) 26 (8) Parasite Infection - - 4 (4) 6 (3) 10 (3) Sarcocystosis - - 2 2 4 Intestinal cestodiasis - - - 2 2 Parasitic proventriculitis - - 2 - 2 Pulmonary nematodiasis - - - 1 1 Renal parasitism (trematodes) - - - 1 1 Inflammation - - 1 (1) 7 (4) 8 (3) Air sacculitis - - - 2 2 Myocarditis - - - 1 1 Oophoritis and peritonitis - - - 1 1 Periarterial abscesses - - - 1 1 Pericarditis and air sacculitis - - - 1 1 Podpdermatitis - - - 1 1 Proventriculitis and serositis - - 1 - 1 Trauma - - 3 (3) 5 (3) 8 (3) Bacterial Infection - 1 (2) 2 (2) 4 (2) 7 (2) Cellulitis - - 2 1 3 Chronic ventricular ulcer - 1 - - 1 Mycobacteriosis - - - 1 1 Orchitis and funiculitis - - - 1 1 Septicemia - - - 1 1 Drowned - 3 (6) 2 (2) - 5 (2) Tumour - - - 4 (2) 4 (1) Fibromas - - - 2 2 Fibrochodroma - - - 1 1 Neoplasia - - - 1 1 Tissue Necrosis - 1 (2) 1 (1) 1 (1) 3 (1) Fat necrosis - 1 - 1 2 Hepatic necrosis - - 1 - 1 Impaction - - - 3 (2) 3 (1) Egg impaction - - - 2 2 Rectal Impaction - - - 1 1 Myopathy - - 1 (1) 2 (1) 3 (1) Pneumonia - - - 2 (1) 2 (1)

49

Table 5. Average body mass, and average mass of anthropogenic debris particles found

in the gizzards and proventriculi of four species of Procellariiformes collected beached on

Sable Island, Nova Scotia, between 2000 and 2012.

Body mass (g) Mass of debris (g) Species x̅ ± SD x̅ ± SD

Cory’s shearwater Calonectris borealis

686.83 ± 257.03 0.00 ± 0.00

Sooty shearwater Ardenna grisea

513.23 ± 69.05 0.07 ± 0.17

Great shearwater Ardenna gravis

528.70 ± 92.64 0.17 ± 0.33

Northern fulmar Fulmarus glacialis

665.24 ± 133.41 1.09 ± 1.93

50

Figure 3. Monthly collection breakdown of procellariid carcasses found beached on

Sable Island, Nova Scotia, Canada, between 2000-2012. Years combined. GRSH = great

shearwater; NOFU = northern fulmar; SOSH = sooty shearwater. Made in R using the

“ggplot2” package (Wickham, 2009).

51

Figure 4. Plumage morphs of beached northern fulmars (Fulmarus glacialis) collected

from Sable Island, Nova Scotia, Canada, between 2000-2012 and associated ingested

masses of anthropogenic debris (g) removed from the gizzard and proventriculus of birds.

Masses on y-axis log (x + 1)-transformed.

52

CHAPTER FOUR: GENERAL DISCUSSION AND FUTURE DIRECTIONS

Future Actions

A better understanding of the prevalence and effect of anthropogenic debris on

freshwater organisms, such as waterfowl, may help justify stronger regulations

controlling the manufacture and use of microbeads and microplastics, and improve

legislation to prevent their release into our waterways. Although there is evidence that

anthropogenic debris is a threat to aquatic biota, there is still a need for long term

monitoring to provide input for conservation management, strengthen the basis for

educational campaigns, and provide scientists with better evidence that could be used to

increase efforts to mitigate the problem (Derraik, 2002).

Although much is known about marine plastic debris, future research needs to

focus on the effects of freshwater debris. Freshwater environments are as polluted as their

marine counterparts (Eerkes-Medrano et al., 2015), and human plastic contaminant

exposure from either habitat could lead to potential long-term negative human health

effects. Future analyses on freshwater organisms are crucial to limiting exposure, and

decreasing human contaminant contact, as little is currently known about plastic exposure

and ingestion in freshwater organisms, and potential subsequent biomagnification to

humans. A specific focus on freshwater birds would be timely due to recent studies

finding plastics in commonly consumed bird species (English et al., 2015; Holland et al.,

2016).

53

Due to the ability of aquatic microplastics to vector heavy metal contaminants and

pollutants, it is likely that through biomagnification and subsequent aquatic animal

consumption, human health will be affected (Teuten et al., 2007; Ashton et al., 2010;

Rios et al., 2010). In laboratory settings zooplankton consume microplastics (Cole et al.,

2013; Wright et al., 2013; Cole et al., 2014) and recently, microplastics have been found

in digestive tracts of mesopelagic and epipelagic planktivorous fishes and in demersal

estuarine fish species (Boerger et al., 2010; Possatto et al., 2011; Dantas et al., 2012). Of

fish sold in markets for human consumption in California, USA, and Makassar,

Indonesia, 25-28% had anthropogenic debris present in their digestive tracts (Rochman et

al., 2015). Microplastics have also been found in the soft tissues of marine bivalves

(Mytilus edulis and Crassostrea gigas) commercially cultured for human consumption,

and resultant human dietary exposure from these two species could amount to 11,000

microplastic pieces consumed per year (Van Cauwenberghe and Janssen, 2014).

In regards to determining secondary exposure to plastics through contaminated

food species tissues, necropsies and stable isotope analyses of waterfowl would be

beneficial. Waterfowl are among one of the most culturally and economically significant

groups of hunted wildlife in Canada with most being taken from freshwater sites. In 2015

alone, an estimated 186,201 individuals across Canada hunted waterfowl (numbers from

Migratory Game Bird Hunting Permit stubs returned to Environment and Climate Change

Canada, 2016) and collected 2,167,973 birds from across Canada (Gendron and Smith,

2016).

Due to the large number of waterfowl sustenance hunters and their heavy focus on

hunting in freshwater environments, mitigation efforts to control plastic and other

54

potentially harmfully anthropogenic materials into the environment should be enacted.

We now know plastics are consumed by freshwater birds (English et al., 2015; Holland et

al., 2016; Gil-Delgado et al., 2017). Although efforts are being made to clean ocean

waters of plastics and help mitigate increasing concentrations (Kershaw et al., 2011), lack

of standardized research has meant that no similar initiatives exist for freshwater bodies

(Ryan et al., 2009). Problematically, legislation regarding marine dumping is often

ignored or not enforced, leading to little decrease in plastic debris release in marine

waters (Derraik, 2002), and thus seabirds continue to be exposed to debris.

Although more is known about seabird plastic ingestion, research needs to be

done to determine potential connections between seabird mortality, pathology, and plastic

ingestion. To determine which mortalities are natural, thorough investigations into

common causes of seabird mortality need to be conducted. Beached bird surveys are a

potential opportunistic sampling method, although these surveys often yield a

disproportionate number of immature and emaciated individuals. Our research on Sable

Island provides a much-needed baseline on seabird pathology in Nova Scotian waters.

This research also shows that seabird plastic ingestion continues to be a very real threat,

and illustrates that one population’s relationship with plastic may not apply to another.

To decrease aquatic anthropogenic debris concentrations in general, and plastic in

particular, stricter enforcement of existing laws and increased efforts at education are

required. Previous research has shown that education starting at a young age is effective

in bringing about positive change (Orr, 2004; Upham et al., 2009). Awareness of issues

and participation in their mitigation at a young age can not only help change

environmentally destructive habits, it can also lead to shared awareness with families and

55

communities, working as a catalyst for change (Derraik, 2002; Checkoway and Gutierrez,

2006). However, the most effective method will likely be a combination of legislative

and education-based ecological and environmental consciousness (Derraik, 2002).

Although past initiatives have been lacking, stronger regulations, enforcement, and public

education could make a positive difference.

Given that there is evidence that plastic pollution is a threat to aquatic

biodiversity, there is still a need for long term monitoring to provide input for

conservation management, strengthen the basis for educational campaigns, and provide

scientists with better evidence that could be used to increase efforts to mitigate the

problem (Derraik, 2002). It is imperative that research commence immediately, because

due to the long life of plastics, even if production and disposal of plastics was stopped

today, existing debris would continue to cause harm for many decades (Derraik, 2002).

Complications derived from different methods of reporting plastic debris concentrations

in freshwater and marine environments could hamper initiatives, because there is no

internationally agreed upon classification system for plastic debris (Driedger et al., 2015).

A better understanding of the prevalence and effect of microplastics on freshwater

organisms, such as waterfowl, may help justify stronger regulations against the

manufacture and use of microbeads and microplastics, and improve legislation to prevent

their release into our waterways. Our baseline data provide insights that this may have to

occur sooner than expected to prevent freshwater waterfowl debris ingestion levels from

reaching the levels currently observed in seabirds.

Steps to control plastic in the environment have been made, with plastic product

bans (e.g. polystyrene, bottled water and plastic bags) sweeping the world, while public

56

awareness and involvement increases (Wabnitz and Nichols, 2010). Likewise, increases

in knowledge of the harm debris can cause has led to subsequent increases in research

and legislation. As research into the newly arising field of freshwater anthropogenic

debris continues, we hopefully will continue to see public outcry over plastic waste, and

see renewed interest in renewable and ecologically friendly options.

References

Amélineau, F., Bonnet, D., Heitz, O., Mortreux, V., Harding, A.M.A., Karnovsky, N.,

Walkusz, W., Fort, J., Grémillet, D., 2016. Microplastic pollution in the

Greenland Sea: Background levels and selective contamination of planktivorous

diving seabirds. Environmental Pollution 219, 1131–1139.

doi:10.1016/j.envpol.2016.09.017

Andrady, A.L., 2011. Microplastics in the marine environment. Marine Pollution Bulletin

62, 1596–1605. doi:10.1016/j.marpolbul.2011.05.030

Arthur, C., Baker, J., Bamford, H., 2008. Proceedings of the international research

workshop on the occurrence, effects, and fate of mircroplastic marine debris.

National Oceanic and Atmospheric Administration Technical Memorandum

NOS-OR&R-30, 1–49.

Ashton, K., Holmes, L., Turner, A., 2010. Association of metals with plastic production

pellets in the marine environment. Marine Pollution Bulletin 60, 2050–2055.

doi:10.1016/j.marpolbul.2010.07.014

57

Auman, H.J., Ludwig, J.P., Giesy, J.P., Colborn, T., 1997. Plastic ingestion by Laysan

albatross chicks on Sand Island, Midway Atoll, in 1994 and 1995. Albatross

Biology and Conservation, 239-244.

Australian Government, 2016. Federal Government strengthens efforts to tackle plastic

waste [Media Release] [WWW Document]. The Hon. Greg Hunt MP Minister for

the Environment. URL

https://www.environment.gov.au/minister/hunt/2016/pubs/mr20160229a.pdf

(accessed 3.17.17).

Avery-Gomm, S., Valliant, M., Schacter, C.R., Robbins, K.F., Liboiron, M., Daoust, P.-

Y., Rios, L.M., Jones, I.L., 2016. A study of wrecked dovekies (Alle alle) in the

western North Atlantic highlights the importance of using standardized methods

to quantify plastic ingestion. Marine Pollution Bulletin 113, 75–80.

doi:10.1016/j.marpolbul.2016.08.062

Bakir, A., Rowland, S.J., Thompson, R.C., 2014. Enhanced desorption of persistent

organic pollutants from microplastics under simulated physiological conditions.

Environmental Pollution 185, 16–23. doi:10.1016/j.envpol.2013.10.007

Balseiro, A., Espí, A., Márquez, I., Pérez, V., Ferreras, M.C., Marín, J.F.G., Prieto, J.M.,

2005. Pathological features in marine birds affected by the Prestige’s oil spill in

the north of Spain. Journal of Wildlife Diseases 41, 371–378. doi:10.7589/0090-

3558-41.2.371

Barnes, D.K.A., Galgani, F., Thompson, R.C., Barlaz, M., 2009. Accumulation and

fragmentation of plastic debris in global environments. Philosophical

58

Transactions of the Royal Society B: Biological Sciences 364, 1985–1998.

doi:10.1098/rstb.2008.0205

Barrett, R.T., Camphuysen, K.C.J., Anker-Nilssen, T., Chardine, J.W., Furness, R.W.,

Garthe, S., Hüppop, O., Leopold, M.F., Montevecchi, W.A., Veit, R.R., 2007.

Diet studies of seabirds: A review and recommendations. International Council

for the Exploration of the Sea Journal of Marine Science 64, 1675–1691.

doi:10.1093/icesjms/fsm152

Bayly, I.A.E., 1993. The fauna of athalassic saline waters in Australia and the Altiplano

of South America: Comparisons and historical perspectives, in: Hurlbert, S.H.

(Ed.), Saline Lakes V, Developments in Hydrobiology. Springer Netherlands,

Bohn Stafleu van Loghum, Houten, Netherlands, pp. 225–231. doi:10.1007/978-

94-011-2076-0_18

Bellizzi, M., Duerr, R.S., 2013. Northern fulmar (Fulmarus glacialis) rehabilitation

during “wrecks” in California, in: The 44th Annual International Association for

Aquatic Animal Medicine Conference. The Marine Mammal Center, Sausalito,

California.

Besseling, E., Wang, B., Lürling, M., Koelmans, A.A., 2014. Nanoplastic affects growth

of S. obliquus and reproduction of D. magna. Environmental Science &

Technology 48, 12336–12343. doi:10.1021/es503001d

Bijker, W.E., Hughes, T.P., Pinch, T. (Eds.), 1987. The social construction of Bakelite:

toward a theory of invention, in: The Social Construction of Technological

Systems: New Directions in the Sociology and History of Technology. MIT Press,

Cambridge, Massachusetts, USA, pp. 159–187.

59

BirdLife International, 2016a. Fulmarus glacialis: BirdLife International: The IUCN Red

List of Threatened Species 2016: e.T22697866A89663126 [WWW Document].

Fulmarus glacialis. doi:10.2305/IUCN.UK.2016-

3.RLTS.T22697866A89663126.en

BirdLife International, 2016b. Calonectris borealis. The IUCN Red List of Threatened

Species 2016: e.T22732244A86237651 [WWW Document]. Calonectris borealis.

doi:10.2305/IUCN.UK.2016-3.RLTS.T22732244A86237651.en

BirdLife International, 2016c. Ardenna gravis. The IUCN Red List of Threatened Species

2016: e.T22698201A93669258 [WWW Document]. Ardenna gravis.

doi:10.2305/IUCN.UK.2016-3.RLTS.T22698201A93669258.en

BirdLife International, 2016d. Ardenna grisea: BirdLife International: The IUCN Red

List of Threatened Species 2016: e.T22698209A95225016 [WWW Document].

Ardenna grisea. doi:10.2305/IUCN.UK.2016-3.RLTS.T22698209A95225016.en

Blanco, G., Tella, J.L., Potti, J., 1997. Feather mites on group-living red-billed choughs:

A non-parasitic interaction? Journal of Avian Biology 28, 197–206.

doi:10.2307/3676970

Boerger, C.M., Lattin, G.L., Moore, S.L., Moore, C.J., 2010. Plastic ingestion by

planktivorous fishes in the North Pacific Central Gyre. Marine Pollution Bulletin

60, 2275–2278. doi:10.1016/j.marpolbul.2010.08.007

Bogstad, B., Drevetnyak, K.V., Byrkjedal, I., Dolgov, A.V., Gjøsæter, H., Johannesen,

E., Mehl, S., Høines, Å., Shevelev, M.S., Smirnov, O.V., 2014. Infectious

organisms [WWW Document]. BarentsPortal: Barents Sea Environmental Status

(A Norwegian-Russian Collaboration). URL

60

http://barentsportal.com/barentsportal/index.php/en/more/general-description-of-

the-ecosystem/89-biotic-components/155- (accessed 3.22.17).

Bond, A.L., Lavers, J.L., 2013. Effectiveness of emetics to study plastic ingestion by

Leach’s storm-petrels (Oceanodroma leucorhoa). Marine Pollution Bulletin 70,

171–175. doi:10.1016/j.marpolbul.2013.02.030

Bond, A.L., Provencher, J.F., Daoust, P.Y., Lucas, Z.N., 2014. Plastic ingestion by

fulmars and shearwaters at Sable Island, Nova Scotia, Canada. Marine Pollution

Bulletin 87, 68–75. doi:10.1016/j.marpolbul.2014.08.010

Camphuysen, C.J., Heubeck, M., 2001. Marine oil pollution and beached bird surveys:

The development of a sensitive monitoring instrument. Environmental Pollution

112, 443–461.

Carpenter, D.O., 2006. Polychlorinated biphenyls (PCBs): Routes of exposure and effects

on human health. Reviews on Environmental Health 21, 1–24.

doi:10.1515/REVEH.2006.21.1.1

Castañeda, R.A., Avlijas, S., Simard, M.A., Ricciardi, A., Smith, R., 2014. Microplastic

pollution in St. Lawrence River sediments. Canadian Journal of Fisheries and

Aquatic Sciences 71, 1767–1771. doi:10.1139/cjfas-2014-0281

Checkoway, B.N., Gutierrez, L.M., 2006. Youth participation and community change:

An introduction. Journal of Community Practice 14, 1–9.

doi:10.1300/J125v14n01_01

Cheek, A.O., Kow, K., Chen, J., McLachlan, J.A., 1999. Potential mechanisms of thyroid

disruption in humans: Interaction of organochlorine compounds with thyroid

61

receptor, transthyretin, and thyroid-binding globulin. Environmental Health

Perspectives 107, 273–278.

Cochran, W.G., 1954. Some methods for strengthening the common χ2 tests. Biometrics

10, 417–451. doi:10.2307/3001616

Cole, M., Lindeque, P., Fileman, E., Halsband, C., Goodhead, R., Moger, J., Galloway,

T.S., 2013. Microplastic ingestion by zooplankton. Environmental Science &

Technology 47, 6646–6655. doi:10.1021/es400663f

Cole, M., Webb, H., Lindeque, P.K., Fileman, E.S., Halsband, C., Galloway, T.S., 2014.

Isolation of microplastics in biota-rich seawater samples and marine organisms.

Scientific Reports 4, 4528. doi:10.1038/srep04528

Connors, P.G., Smith, K.G., 1982. Oceanic plastic particle pollution: Suspected effect on

fat deposition in red phalaropes. Marine Pollution Bulletin 13, 18–20.

doi:10.1016/0025-326X(82)90490-8

Corcoran, P.L., Norris, T., Ceccanese, T., Walzak, M.J., Helm, P.A., Marvin, C.H., 2015.

Hidden plastics of Lake Ontario, Canada and their potential preservation in the

sediment record. Environmental Pollution 204, 17–25.

doi:10.1016/j.envpol.2015.04.009

Costa, L.G., Giordano, G., Tagliaferri, S., Caglieri, A., Mutti, A., 2008. Polybrominated

diphenyl ether (PBDE) flame retardants: Environmental contamination, human

body burden and potential adverse health effects. Acta Biomed 79, 172–183.

Council of the European Union, 2014. 3363rd Council meeting [Press Release] [WWW

Document]. Environment. URL

62

http://www.consilium.europa.eu/uedocs/cms_data/docs/pressdata/en/envir/146374

.pdf (accessed 3.29.17).

Dantas, D.V., Barletta, M., Costa, M.F. da, 2012. The seasonal and spatial patterns of

ingestion of polyfilament nylon fragments by estuarine drums (Sciaenidae).

Environmental Science and Pollution Research 2, 600–606. doi:10.1007/s11356-

011-0579-0

Day, R.H., 1980. The occurrence and characteristics of plastic pollution in Alaska’s

marine birds (MSc Thesis). University of Alaska, Fairbanks, Alaska, USA.

Day, R.H., Wehle, D.H.S., Coleman, F.C., 1985. Ingestion of plastic pollutants by marine

birds, in: Proceedings of the Workshop on the Fate and Impact of Marine Debris.

National Oceanic and Atmospheric Administration, Honolulu, Hawaii, USA, pp.

344–386.

Denuncio, P., Bastida, R., Dassis, M., Giardino, G., Gerpe, M., Rodríguez, D., 2011.

Plastic ingestion in Franciscana dolphins, Pontoporia blainvillei (Gervais and

d’Orbigny, 1844), from Argentina. Marine Pollution Bulletin 62, 1836–1841.

doi:10.1016/j.marpolbul.2011.05.003

Derraik, J.G., 2002. The pollution of the marine environment by plastic debris: A review.

Marine Pollution Bulletin 44, 842–852.

Desforges, J.P.W., Galbraith, M., Ross, P.S., 2015. Ingestion of microplastics by

zooplankton in the Northeast Pacific Ocean. Archives of Environmental

Contamination and Toxicology 69, 320–330. doi:10.1007/s00244-015-0172-5

Doughty, R., Eriksen, M., 2014. The case for a ban on microplastics in personal care

products. Tulane Environmental Law Journal 27, 277.

63

Driedger, A.G.J., Dürr, H.H., Mitchell, K., Van Cappellen, P., 2015. Plastic debris in the

Laurentian Great Lakes: A review. Journal of Great Lakes Research 41, 9–19.

doi:10.1016/j.jglr.2014.12.020

Eerkes-Medrano, D., Thompson, R.C., Aldridge, D.C., 2015. Microplastics in freshwater

systems: A review of the emerging threats, identification of knowledge gaps and

prioritisation of research needs. Water Research 75, 63–82.

doi:10.1016/j.watres.2015.02.012

El-Hayek, Y.H., 2007. Mercury contamination in Arctic Canada: Possible implications

for Aboriginal health. Journal on Developmental Disabilities 13, 67–89.

English, M.D., 2016. Diet and body condition of American black ducks (Anas rubripes)

overwintering in Atlantic Canada (MSc Thesis). Acadia University, Wolfville,

Nova Scotia.

English, M.D., Robertson, G.J., Avery-Gomm, S., Pirie-Hay, D., Roul, S., Ryan, P.C.,

Wilhelm, S.I., Mallory, M.L., 2015. Plastic and metal ingestion in three species of

coastal waterfowl wintering in Atlantic Canada. Marine Pollution Bulletin 98,

349–353. doi:10.1016/j.marpolbul.2015.05.063

Environment and Climate Change Canada, 2016. Permit Sales [WWW Document]. URL

https://www.ec.gc.ca/reom-mbs/default.asp?lang=en&n=C9046964 (accessed

3.19.17).

Environment and Climate Change Canada, 2010. Environment and Climate Change

Canada - Acts & Regulations - Toxic Substances List - Schedule 1 [WWW

Document]. URL http://www.ec.gc.ca/lcpe-

64

cepa/default.asp?lang=En&n=0DA2924D-1&wsdoc=4ABEFFC8-5BEC-B57A-

F4BF-11069545E434 (accessed 3.17.17).

Eriksen, M., Lebreton, L.C.M., Carson, H.S., Thiel, M., Moore, C.J., Borerro, J.C.,

Galgani, F., Ryan, P.G., Reisser, J., 2014. Plastic pollution in the world’s oceans:

More than 5 trillion plastic pieces weighing over 250,000 tons afloat at sea. PLoS

ONE 9, e111913. doi:10.1371/journal.pone.0111913

Eriksen, M., Mason, S., Wilson, S., Box, C., Zellers, A., Edwards, W., Farley, H., Amato,

S., 2013. Microplastic pollution in the surface waters of the Laurentian Great

Lakes. Marine Pollution Bulletin 77, 177–182.

doi:10.1016/j.marpolbul.2013.10.007

Fängström, B., Athanasiadou, M., Athanassiadis, I., Bignert, A., Grandjean, P., Weihe,

P., Bergman, Å., 2005. Polybrominated diphenyl ethers and traditional

organochlorine pollutants in fulmars (Fulmarus glacialis) from the Faroe Islands.

Chemosphere 60, 836–843. doi:10.1016/j.chemosphere.2005.01.065

Fischer, E.K., Paglialonga, L., Czech, E., Tamminga, M., 2016. Microplastic pollution in

lakes and lake shoreline sediments – A case study on Lake Bolsena and Lake

Chiusi (central Italy). Environmental Pollution 213, 648–657.

doi:10.1016/j.envpol.2016.03.012

Fisher, J., 1952. The colour-phases of the fulmar, in: The Fulmar, Collins New Naturalist.

Collins, London, England, pp. 266–288.

Food and Agriculture Organization of the United Nations, 2016. The state of world

fisheries and aquaculture: Contributing to food security and nutrition for all. Food

and Agriculture Organization of the United Nations, Rome, Italy.

65

Free, C.M., Jensen, O.P., Mason, S.A., Eriksen, M., Williamson, N.J., Boldgiv, B., 2014.

High-levels of microplastic pollution in a large, remote, mountain lake. Marine

Pollution Bulletin 85, 156–163. doi:10.1016/j.marpolbul.2014.06.001

Frias, J.P.G.L., Sobral, P., Ferreira, A.M., 2010. Organic pollutants in microplastics from

two beaches of the Portuguese coast. Marine Pollution Bulletin 60, 1988–1992.

doi:10.1016/j.marpolbul.2010.07.030

Furness, R.W., Camphuysen, K.C., 1997. Seabirds as monitors of the marine

environment. ICES Journal of Marine Science 54, 726–737.

Gall, S.C., Thompson, R.C., 2015. The impact of debris on marine life. Marine Pollution

Bulletin 92, 170–179. doi:10.1016/j.marpolbul.2014.12.041

Gaynor, A.M., Fish, S., Duerr, R.S., Cruz, F.N.D., Pesavento, P.A., 2015. Identification

of a novel papillomavirus in a northern fulmar (Fulmarus glacialis) with viral

production in cartilage. Veterinary Pathology 52, 553–561.

doi:10.1177/0300985814542812

Gendron, M.H., Smith, A.C., 2013. National Harvest Survey web site. Bird Populations

Monitoring, National Wildlife Research Centre, Canadian Wildlife Service,

Ottawa, Ontario [WWW Document]. National Harvest Survey. URL

http://www.ec.gc.ca/reom-mbs/enp-nhs/index.cfm?do=a&lang=e (accessed

3.19.17).

Gendron, M.H., Smith, A.C., 2016. National Harvest Survey web site. Bird Populations

Monitoring, National Wildlife Research Centre, Canadian Wildlife Service,

Ottawa, Ontario. [WWW Document]. National Harvest Survey. URL

66

http://www.ec.gc.ca/reom-mbs/enp-nhs/index.cfm?do=def&lang=e (accessed

3.19.17).

Gil-Delgado, J.A., Guijarro, D., Gosálvez, R.U., López-Iborra, G.M., Ponz, A., Velasco,

A., 2017. Presence of plastic particles in waterbirds faeces collected in Spanish

lakes. Environmental Pollution 220, 732–736. doi:10.1016/j.envpol.2016.09.054

Gouin, T., Roche, N., Lohmann, R., Hodges, G., 2011. A thermodynamic approach for

assessing the environmental exposure of chemicals absorbed to microplastic.

Environmental Science & Technology 45, 1466–1472. doi:10.1021/es1032025

Government of Canada, 2016. Canada Gazette – Microbeads in Toiletries Regulations

[WWW Document]. Microbeads in Toiletries Regulations. URL

http://www.gazette.gc.ca/rp-pr/p1/2016/2016-11-05/html/reg2-eng.php (accessed

3.17.17).

Government of Canada, 2015. Microbeads [WWW Document]. URL

http://www.chemicalsubstanceschimiques.gc.ca/plan/approach-approche/microb-

eng.php (accessed 3.17.17).

Government of Canada, F. and O.C., 2010. The Gully [WWW Document]. URL

http://www.inter.dfo-mpo.gc.ca/Maritimes/Oceans/OCMD/Gully/Gully-MPA

(accessed 3.17.17).

Grant, G.S., Trail, P.W., Clapp, R.B., 1994. First specimens of sooty shearwater,

Newell’s shearwater, and white-faced storm-petrel from American Samoa.

Notornis 41, 215–217.

Gray, R., 1871. The birds of the west of Scotland, including the Outer Hebrides. T.

Murray, Glasgow, Scotland.

67

Great Lakes and St. Lawrence Cities Initiative, 2014. Great Lakes and St. Lawrence

Cities Initiative Resolution 03-2014M [WWW Document]. Microbeads. URL

https://glslcities.org/wp-content/uploads/2015/05/2014_3_microbeads.pdf

(accessed 3.29.17).

Gregory, M.R., 1978. Accumulation and distribution of virgin plastic granules on New

Zealand beaches. New Zealand Journal of Marine and Freshwater Research 12,

399–414. doi:10.1080/00288330.1978.9515768

Gregory, M.R., 1983. Virgin plastic granules on some beaches of Eastern Canada and

Bermuda. Marine Environmental Research 10, 73–92. doi:10.1016/0141-

1136(83)90011-9

Gregory, M.R., 2009. Environmental implications of plastic debris in marine settings –

entanglement, ingestion, smothering, hangers-on, hitch-hiking and alien

invasions. Philosophical Transactions of the Royal Society B: Biological Sciences

364, 2013–2025. doi:10.1098/rstb.2008.0265

GTA Consultants Inc., 1999. Socio-economic profile of the Sable Gully. GTA

Consultants Inc., Halifax, Nova Scotia, Canada.

Haman, K.H., Norton, T.M., Ronconi, R.A., Nemeth, N.M., Thomas, A.C., Courchesne,

S.J., Segars, A., Keel, M.K., 2013. Great shearwater (Puffinus gravis) mortality

events along the eastern coast of the United States. Journal of Wildlife Diseases

49, 235–245. doi:10.7589/2012-04-119

Harris, R.J., Tseng, F.S., Pokras, M.A., Suedmeyer, B.A., Bogart, J.S.H., Prescott, R.L.,

Newman, S.H., 2006. Beached bird surveys in Massachusetts: The seabird

ecological assessment network (SEANET). Marine Ornithology 34, 115–122.

68

Harvey, J., Nevins, H.M., Hatch, S., Adams, J., Hill, J., Ames, J., Parkin, J., Newton, K.,

Roletto, J., Mortenson, J., Hall, J., Hass, T., 2004. An unusual mortality of

northern fulmar (Fulmarus glacialis), in: Sanctuary Currents Symposium.

Monterey Bay National Marine Sanctuary, Seaside, California, USA.

Hatch, S.A., 1991. Evidence for color phase effects on the breeding and life history of

northern fulmars. The Condor 93, 409–417. doi:10.2307/1368957

Hilton, G.M., Furness, R.W., Houston, D.C., 2000. A comparative study of digestion in

North Atlantic seabirds. Journal of Avian Biology 31, 36–46. doi:10.1034/j.1600-

048X.2000.310106.x

Holladay, S.D., Smialowicz, R.J., 2000. Development of the murine and human immune

system: Differential effects of immunotoxicants depend on time of exposure.

Environmental Health Perspectives 108, 463–473.

Holland, E., Mallory, M.L., Shutler, D., 2016. Plastics and other anthropogenic debris in

freshwater birds from Canada. Science of the Total Environment 571, 251–258.

doi:http://dx.doi.org/10.1016/j.scitotenv.2016.07.158

House Report No. 114-371, 2015. H. Rept. 114-371 - Microbead-free waters act of 2015

[WWW Document]. URL https://www.congress.gov/congressional-report/114th-

congress/house-report/371/1 (accessed 3.19.17).

Huettmann, F., Diamond, A.W., 2000. Seabird migration in the Canadian northwest

Atlantic Ocean: Moulting locations and movement patterns of immature birds.

Canadian Journal of Zoology 78, 624–647. doi:10.1139/cjz-78-4-624

69

Humphries, G.R.W., 2014. Using long term harvest records of sooty shearwaters (Tītī;

Puffinus griseus) to predict shifts in the Southern Oscillation (PhD Thesis).

University of Otago, University of Otago, Dunedin, New Zealand.

International Joint Commission Canada and United States, 2016. Microplastics in the

Great Lakes workshop report. International Joint Commission Canada and United

States Final Report, 1–31.

Ivar do Sul, J.A., Costa, M.F., 2014. The present and future of microplastic pollution in

the marine environment. Environmental Pollution 185, 352–364.

doi:10.1016/j.envpol.2013.10.036

Jackson, D.A., 1993. Stopping rules in principal components analysis: A comparison of

heuristical and statistical approaches. Ecology 74, 2204–2214.

doi:10.2307/1939574

Jessup, D.A., Miller, M.A., Ryan, J.P., Nevins, H.M., Kerkering, H.A., Mekebri, A.,

Crane, D.B., Johnson, T.A., Kudela, R.M., 2009. Mass stranding of marine birds

caused by a surfactant-producing red tide. PLoS ONE 4, e4550.

doi:10.1371/journal.pone.0004550

Johansen, P., Asmund, G., Riget, F., 2001. Lead contamination of seabirds harvested with

lead shot – implications to human diet in Greenland. Environmental Pollution

112, 501–504.

Kalmar, I.D., Dicxk, V., Dossche, L., Vanrompay, D., 2014. Zoonotic infection with

Chlamydia psittaci at an avian refuge centre. The Veterinary Journal 199, 300–

302. doi:10.1016/j.tvjl.2013.10.034

70

Kanehiro, H., Tokai, T., Matuda, K., 1995. Marine litter composition and distribution on

the sea-bed of Tokyo Bay [Japan]. Fisheries Engineering (Japan) 31, 195–199.

Karlsson, M., Ericson, I., van Bavel, B., Jensen, J.K., Dam, M., 2006. Levels of

brominated flame retardants in Northern Fulmar (Fulmarus glacialis) eggs from

the Faroe Islands. Science of The Total Environment 367, 840–846.

doi:10.1016/j.scitotenv.2006.02.050

Kenyon, K.W., Kridler, E., 1969. Laysan albatrosses swallow indigestible matter. The

Auk 86, 339–343. doi:10.2307/4083505

Kershaw, P., Katsuhiko, S., Lee, S., Samseth, J., Woodring, D., Smith, J., 2011. Plastic

debris in the ocean, UNEP Year Book. United Nations Environment Programme,

Nairobi, Kenya, Africa.

Kirk, D.A., Gosler, A.G., 1994. Body condition varies with migration and competition in

migrant and resident South American vultures. The Auk 111, 933–944.

doi:10.2307/4088825

Klar, M., Gunnarsson, D., Prevodnik, A., Hedfors, C., Dahl, U., 2014. Everything you

(don’t) want to know about plastics. Swedish Society for Nature Conservation 1–

197.

Koelmans, A.A., Besseling, E., Foekema, E.M., 2014. Leaching of plastic additives to

marine organisms. Environmental Pollution 187, 49–54.

doi:10.1016/j.envpol.2013.12.013

Laist, D.W., 1997. Impacts of marine debris: Entanglement of marine life in marine

debris including a comprehensive list of species with entanglement and ingestion

71

records, in: Coe, J.M., Rogers, D.B. (Eds.), Marine Debris. Springer New York,

New York, NY, pp. 99–139. doi:10.1007/978-1-4613-8486-1_10

Laist, D.W., 1987. Overview of the biological effects of lost and discarded plastic debris

in the marine environment. Marine Pollution Bulletin 18, 319–326.

doi:10.1016/S0025-326X(87)80019-X

Lang, A.S., Lebarbenchon, C., Ramey, A.M., Robertson, G.J., Waldenström, J., Wille,

M., 2016. Assessing the role of seabirds in the ecology of influenza A viruses.

Avian Diseases 60, 378–386. doi:10.1637/11135-050815-RegR

Larntz, K., 1978. Small-sample comparisons of exact levels for chi-squared goodness-of-

fit statistics. Journal of the American Statistical Association 73, 253–263.

doi:10.2307/2286650

Lavers, J.L., Bond, A.L., 2016. Selectivity of flesh-footed shearwaters for plastic colour:

Evidence for differential provisioning in adults and fledglings. Marine

Environmental Research 113, 1–6. doi:10.1016/j.marenvres.2015.10.011

Lechner, A., Keckeis, H., Lumesberger-Loisl, F., Zens, B., Krusch, R., Tritthart, M.,

Glas, M., Schludermann, E., 2014. The Danube so colourful: A potpourri of

plastic litter outnumbers fish larvae in Europe’s second largest river.

Environmental Pollution 188, 177–181. doi:10.1016/j.envpol.2014.02.006

Lechner, A., Ramler, D., 2015. The discharge of certain amounts of industrial

microplastic from a production plant into the River Danube is permitted by the

Austrian legislation. Environmental Pollution 200, 159–160.

doi:10.1016/j.envpol.2015.02.019

72

Leslie, H.A., 2014. Review of microplastics in cosmetics (No. Report R14/29). Institute

for Environmental Studies [IVM], Amsterdam, Netherlands.

Li, L., Pesavento, P.A., Gaynor, A.M., Duerr, R.S., Phan, T.G., Zhang, W., Deng, X.,

Delwart, E., 2015. A gyrovirus infecting a sea bird. Archives of Virology 160,

2105–2109. doi:10.1007/s00705-015-2468-1

Lieske, C.L., Ziccardi, M.H., Mazet, J.A., Newman, S.H., Gardner, I.A., 2002.

Evaluation of 4 handheld blood glucose monitors for use in seabird rehabilitation.

Journal of Avian Medicine and Surgery 16, 277–285.

Lucas, Z., 1992. Monitoring persistent litter in the marine environment on Sable Island,

Nova Scotia. Marine Pollution Bulletin 24, 192–199. doi:10.1016/0025-

326X(92)90529-F

Lucas, Z., Horn, A., Freedman, B., 2012. Beached bird surveys on Sable Island, Nova

Scotia, 1993–2009, show a decline in the incidence of oiling. Proceedings of the

Nova Scotian Institute of Science 47, 91–129.

Lucas, Z., MacGregor, C., 2006. Characterization and source of oil contamination on the

beaches and seabird corpses, Sable Island, Nova Scotia, 1996–2005. Marine

Pollution Bulletin 52, 778–789. doi:10.1016/j.marpolbul.2005.11.023

Macdonald, M.A., 1977. Adult mortality and fidelity to mate and nest-site in a group of

marked fulmars. Bird Study 24, 165-168.

doi:http://dx.doi.org/10.1080/00063657709476552

Mallory, M.L., Akearok, J.A., Edwards, D.B., O’Donovan, K., Gilbert, C.D., 2008.

Autumn migration and wintering of northern fulmars (Fulmarus glacialis) from

73

the Canadian high Arctic. Polar Biology 31, 745–750. doi:10.1007/s00300-008-

0417-0

Mallory, M.L., Forbes, M.R., 2005. Sex discrimination and measurement bias in northern

fulmars Fulmarus glacialis from the Canadian Arctic. Ardea 93, 25–36.

Mallory, M.L., Mclaughlin, J.D., Forbes, M.R., 2007. Breeding status, contaminant

burden and helminth parasites of northern fulmars Fulmarus glacialis from the

Canadian high Arctic. Ibis 149, 338–344. doi:10.1111/j.1474-919X.2006.00636.x

Mascarenhas, R., Santos, R., Zeppelini, D., 2004. Plastic debris ingestion by sea turtle in

Paraı́ba, Brazil. Marine Pollution Bulletin 49, 354–355.

doi:10.1016/j.marpolbul.2004.05.006

McDonald, T.A., 2002. A perspective on the potential health risks of PBDEs.

Chemosphere 46, 745–755.

Michel, P., Ollason, J.C., Grosbois, V., Thompson, P.M., 2003. The influence of body

size, breeding experience and environmental variability on egg size in the

northern fulmar (Fulmarus glacialis). Journal of Zoology 261, 427-432.

doi:10.1017/S0952836903004291

Millennium Ecosystem Assessment, 2005. Ecosystems and human well-being.

Moore, C.J., 2008. Synthetic polymers in the marine environment: A rapidly increasing,

long-term threat. Environmental Research 108, 131–139.

doi:10.1016/j.envres.2008.07.025

Moore, J.L., Hohman, W.L., Stark, T.M., Weisbrich, G.A., 1998. Shot prevalences and

diets of diving ducks five years after ban on use of lead shotshells at Catahoula

74

lake, Louisiana. The Journal of Wildlife Management 62, 564.

doi:10.2307/3802330

Moseman, E., 2015. Micro-plastic bioaccumulation in yellow perch (Perca flavescens) of

Lake Champlain, in: Center for Earth and Environmental Science Student Posters.

Center for Earth and Environmental Science, Plattsburgh, New York, USA.

Moser, M.L., Lee, D.S., 1992. A fourteen-year survey of plastic ingestion by western

north Atlantic seabirds. Colonial Waterbirds 15, 83. doi:10.2307/1521357

Mougin, J.L., Jouanin, C., Roux, F., Zino, F., 2000. Fledging weight and juvenile

survival of Cory’s shearwaters Calonectris diomedea on Selvagem Grande.

Ringing & Migration 20, 107–110. doi:10.1080/03078698.2000.9674231

Muzaffar, S.B., Jones, I.L., 2004. Parasites and diseases of the auks (Alcidae) of the

world and their ecology – a review. Marine Ornithology 32, 121–146.

Nemeth, N., Keel, K., Yabsley, M., 2011. Case W10-367, in: The 39th Annual South

Eastern Veterinary Pathology Conference (SEVPAC). The University of Georgia

Veterinary Diagnostic & Investigational Laboratory, Athens, Georgia.

Nemeth, N.M., Yabsley, M., Keel, M.K., 2012. Anisakiasis with proventricular

perforation in a greater shearwater (Puffinus gravis) off the coast of Georgia,

United States. Journal of Zoo and Wildlife Medicine 43, 412–415.

doi:10.1638/2011-0193.1

Neufeld, L., Stassen, F., Sheppard, R., Gilman, 2016. The new plastics economy:

Rethinking the future of plastics. World Economic Forum 1–36.

Newman, S., Chmura, A., Converse, K., Kilpatrick, A., Patel, N., Lammers, E., Daszak,

P., 2007. Aquatic bird disease and mortality as an indicator of changing

75

ecosystem health. Marine Ecology Progress Series 352, 299–309.

doi:10.3354/meps07076

Newman, S., Watkins, E., Farmer, A., 2013. How to improve EU legislation to tackle

marine litter. Institute for European Environmental Policy, London. 1–65.

Newman, S.H., Piatt, J.F., White, J., 1997. Hematological and plasma biochemical

reference ranges of Alaskan seabirds: their ecological significance and clinical

importance. Colonial Waterbirds 20, 492–504. doi:10.2307/1521600

Ng, K.L., Obbard, J.P., 2006. Prevalence of microplastics in Singapore’s coastal marine

environment. Marine Pollution Bulletin 52, 761–767.

doi:10.1016/j.marpolbul.2005.11.017

Obbard, R.W., Sadri, S., Wong, Y.Q., Khitun, A.A., Baker, I., Thompson, R.C., 2014.

Global warming releases microplastic legacy frozen in Arctic Sea ice. Earth’s

Future 2, 2014EF000240. doi:10.1002/2014EF000240

Ocean Conservancy, 2010. Trash travels: From our hands to the sea, around the glove,

and through time. [WWW Document]. International Coastal Cleanup. URL

http://act.oceanconservancy.org/site/DocServer/icc2010report_regional_Mex.pdf?

docID=6004 (accessed 3.29.17).

O’Reilly, B., 1818. Greenland, the adjacent seas, and the North-west Passage to the

Pacific Ocean, illustrated in a voyage to Davis’s strait, during the summer of

1817. London, Baldwin, Craddock and Joy, London, England.

Orr, D.W., 2004. Earth in Mind: On Education, Environment, and the Human Prospect.

Island Press, Washington, DC, USA.

76

OSPAR Commission, 2010. The OSPAR system of ecological quality objectives for the

North Sea, a contribution to OSPAR’s quality status report 2010. OSPAR

Commission, London, London, England.

Peitzman, A.B., Fabian, T.C., Rhodes, M., Yealy, D.M., Schwab, C.W., 2012. Chapter 3:

Patterns of penetrating injury, in: The Trauma Manual: Trauma and Acute Care

Surgery. Lippincott Williams & Wilkins, pp. 16–22.

Pennycott, T., 2016. Seabirds. Images of pathology (miscellaneous diseases 2) 1994-

2013. University of Edinburgh, Royal (Dick) School of Veterinary Studies,

Midlothian, Scotland.

Pettit, T.N., Grant, G.S., Whittow, G.C., 1981. Ingestion of plastics by Laysan albatross.

The Auk 98, 839–841.

Pierce, K.E., Harris, R.J., Larned, L.S., Pokras, M.A., 2004. Obstruction and starvation

associated with plastic ingestion in a northern gannet Morus bassanus and a

greater shearwater Puffinus gravis. Marine Ornithology 32, 187–189.

Plastics Europe, 2015. Plastics – the facts 2014/2015. An analysis of European plastics

production, demand and waste data. Plastics Europe, Brussels, Belgium.

Plastics Europe, 2013. Plastics – the facts 2013: An analysis of European latest plastics

production, demand, and waste data. Plastics Europe, Brussels, Belgium.

Pokras, M.A., 1988. Captive management of aquatic birds. Association of Avian

Veterinarians Today 2, 24. doi:10.2307/30134115

Possatto, F.E., Barletta, M., Costa, M.F., Ivar do Sul, J.A., Dantas, D.V., 2011. Plastic

debris ingestion by marine catfish: An unexpected fisheries impact. Marine

Pollution Bulletin 62, 1098–1102. doi:10.1016/j.marpolbul.2011.01.036

77

Powers, K.D., 1984. Pelagic distributions of marine birds off the northeastern United

States. US Department of Commerce, National Oceanic and Atmospheric

Administration, National Marine Fisheries Service, Northeast Fisheries Center,

Manomet, Massachusetts, USA.

Provencher, J.F., Bond, A.L., Hedd, A., Montevecchi, W.A., Muzaffar, S.B., Courchesne,

S.J., Gilchrist, H.G., Jamieson, S.E., Merkel, F.R., Falk, K., Durinck, J., Mallory,

M.L., 2014. Prevalence of marine debris in marine birds from the North Atlantic.

Marine Pollution Bulletin 84, 411–417. doi:10.1016/j.marpolbul.2014.04.044

Provencher, J.F., Bond, A.L., Mallory, M.L., 2015. Marine birds and plastic debris in

Canada: A national synthesis and a way forward. Environmental Reviews 23, 1–

13. doi:10.1139/er-2014-0039

R Core Team, 2015. R: A language and environment for statistical computing [WWW

Document]. The R Project for Statistical Computing. URL https://www.r-

project.org/ (accessed 3.19.17).

Reyes-Arriagada, R., Campos-Ellwanger, P., Schlatter, R.P., Baduini, C., 2007. Sooty

shearwater (Puffinus griseus) on Guafo Island: The largest seabird colony in the

world? Biodiversity and Conservation 16, 913–930. doi:10.1007/s10531-006-

9087-9

Rios, L.M., Jones, P.R., Moore, C., Narayan, U.V., 2010. Quantitation of persistent

organic pollutants adsorbed on plastic debris from the Northern Pacific Gyre’s

“eastern garbage patch.” Journal of Environmental Monitoring 12, 2226.

doi:10.1039/c0em00239a

78

Robards, M.D., Piatt, J.F., Wohl, K.D., 1995. Increasing frequency of plastic particles

ingested by seabirds in the subarctic North Pacific. Marine Pollution Bulletin 30,

151–157.

Robinson, D., 2016. broom: Convert statistical analysis objects into tidy data frames. R

package version 0.4.1.9000 [WWW Document]. GitHub. URL

https://github.com/tidyverse/broom (accessed 3.21.17).

Rochman, C.M., Hentschel, B.T., Teh, S.J., 2014. Long-term sorption of metals is similar

among plastic types: Implications for plastic debris in aquatic environments.

PLoS ONE 9, e85433. doi:10.1371/journal.pone.0085433

Rochman, C.M., Tahir, A., Williams, S.L., Baxa, D.V., Lam, R., Miller, J.T., Teh, F.-C.,

Werorilangi, S., Teh, S.J., 2015. Anthropogenic debris in seafood: Plastic debris

and fibers from textiles in fish and bivalves sold for human consumption.

Scientific Reports 5, 1–10. doi:10.1038/srep14340

Rodríguez, A., Rodríguez, B., Nazaret Carrasco, M., 2012. High prevalence of parental

delivery of plastic debris in Cory’s shearwaters (Calonectris diomedea). Marine

Pollution Bulletin 64, 2219–2223. doi:10.1016/j.marpolbul.2012.06.011

Roletto, J., Mortenson, J., Harrald, I., Hall, J., Grella, L., 2003. Beached bird surveys and

chronic oil pollution in central California. Marine Ornithology 31, 21–28.

Ross, J.B., Parker, R., Strickland, M., 1991. A survey of shoreline litter in Halifax

Harbour 1989. Marine Pollution Bulletin 22, 245–248. doi:10.1016/0025-

326X(91)90919-J

Rothstein, S.I., 1973. Plastic particle pollution of the surface of the Atlantic Ocean:

evidence from a seabird. Condor 75, 5.

79

Ryan, P.G., 1987. The effects of ingested plastic on seabirds: Correlations between

plastic load and body condition. Environmental Pollution 46, 119–125.

doi:10.1016/0269-7491(87)90197-7

Ryan, P.G., Connell, A.D., Gardner, B.D., 1988. Plastic ingestion and PCBs in seabirds:

Is there a relationship? Marine Pollution Bulletin 19, 174–176. doi:10.1016/0025-

326X(88)90674-1

Ryan, P.G., Jackson, S., 1987. The lifespan of ingested plastic particles in seabirds and

their effect on digestive efficiency. Marine Pollution Bulletin 18, 217–219.

doi:10.1016/0025-326X(87)90461-9

Ryan, P.G., Moore, C.J., van Franeker, J.A., Moloney, C.L., 2009. Monitoring the

abundance of plastic debris in the marine environment. Philosophical

Transactions of the Royal Society B: Biological Sciences 364, 1999–2012.

doi:10.1098/rstb.2008.0207

Sanchez, W., Bender, C., Porcher, J.M., 2014. Wild gudgeons (Gobio gobio) from French

rivers are contaminated by microplastics: Preliminary study and first evidence.

Environmental Research 128, 98–100. doi:10.1016/j.envres.2013.11.004

Schneiderman, E.T., 2014. Unseen threat: How microbeads harm New York waters,

wildlife, health and environment. New York State Attorney General, New York,

New York, USA.

Secretariat of the Convention on Biological Diversity, 2012. Impacts of marine debris on

biodiversity: Current status and potential solutions, CBD technical series.

Secretariat of the Convention on Biological Diversity, Montreal, Quebec, Canada.

80

Shaw, D.G., Day, R.H., 1994. Colour- and form-dependent loss of plastic micro-debris

from the North Pacific Ocean. Marine Pollution Bulletin 28, 39–43.

doi:10.1016/0025-326X(94)90184-8

Snyder, J.A., Vakos, H.C., 1966. High shear strength blends of high and low density

polyethylene. US3231636 A.

Spear, L.B., Ainley, D.G., Ribic, C.A., 1995. Incidence of plastic in seabirds from the

tropical pacific, 1984–1991: Relation with distribution of species, sex, age,

season, year and body weight. Marine Environmental Research 40, 123–146.

Steele, C.M., Brown, R.N., Botzler, R.G., 2005. Prevalences of zoonotic bacteria among

seabirds in rehabilitation centers along the Pacific Coast of California and

Washington, USA. Journal of Wildlife Diseases 41, 735–744.

Stephen, C., Burger, A.E., 1994. A comparison of two methods for surveying mortality of

beached birds in British Columbia. The Canadian Veterinary Journal 35, 631–

635.

Talsness, C.E., Andrade, A.J.M., Kuriyama, S.N., Taylor, J.A., vom Saal, F.S., 2009.

Components of plastic: Experimental studies in animals and relevance for human

health. Philosophical Transactions of the Royal Society B: Biological Sciences

364, 2079–2096. doi:10.1098/rstb.2008.0281

Tanaka, K., Takada, H., Yamashita, R., Mizukawa, K., Fukuwaka, M., Watanuki, Y.,

2015. Facilitated leaching of additive-derived PBDES from plastic by seabirds’

stomach oil and accumulation in tissues. Environmental Science & Technology

49, 11799–11807. doi:10.1021/acs.est.5b01376

81

Tanaka, K., Takada, H., Yamashita, R., Mizukawa, K., Fukuwaka, M., Watanuki, Y.,

2013. Accumulation of plastic-derived chemicals in tissues of seabirds ingesting

marine plastics. Marine Pollution Bulletin 69, 219–222.

doi:10.1016/j.marpolbul.2012.12.010

Taylor, M.L., Gwinnett, C., Robinson, L.F., Woodall, L.C., 2016. Plastic microfibre

ingestion by deep-sea organisms. Scientific Reports 6. doi:10.1038/srep33997

Teuten, E.L., Rowland, S.J., Galloway, T.S., Thompson, R.C., 2007. Potential for plastics

to transport hydrophobic contaminants. Environmental Science & Technology 41,

7759–7764. doi:10.1021/es071737s

Thomas, G.J., Owen, M., Richards, P., 1977. Grit in waterfowl at the Ouse Washes,

England. Wildfowl 28, 136–138.

Tourinho, P.S., Ivar do Sul, J.A., Fillmann, G., 2010. Is marine debris ingestion still a

problem for the coastal marine biota of southern Brazil? Marine Pollution Bulletin

60, 396-401. doi:https://doi.org/10.1016/j.marpolbul.2009.10.013

Trevail, A.M., Gabrielsen, G.W., Kühn, S., van Franeker, J.A., 2015. Elevated levels of

ingested plastic in a high Arctic seabird, the northern fulmar (Fulmarus glacialis).

Polar Biology 38, 975–981. doi:10.1007/s00300-015-1657-4

UK Government, 2016. Microbead ban announced to protect sealife [WWW Document].

URL https://www.gov.uk/government/news/microbead-ban-announced-to-

protect-sealife (accessed 3.17.17).

United Nations Environment Programme, 2014. UNEP Yearbook: Emerging Issues in

our global environment, UNEP Year Book. United Nations Environment

Programme, Nairobi, Kenya, Africa.

82

Upham, P., Whitmarsh, L., Poortinga, W., Purdam, K., Darnton, A., McLachlan, C.,

Devine-Wright, P., 2009. Public attitudes to environmental change: A selective

review of theory and practice (A research synthesis for the living with

environmental change research programme). Living With Environmental Change,

Cardiff, Manchester, UK.

Van Cauwenberghe, L., Janssen, C.R., 2014. Microplastics in bivalves cultured for

human consumption. Environmental Pollution 193, 65–70.

doi:10.1016/j.envpol.2014.06.010

Van Cauwenberghe, L., Vanreusel, A., Mees, J., Janssen, C.R., 2013. Microplastic

pollution in deep-sea sediments. Environmental Pollution 182, 495–499.

doi:10.1016/j.envpol.2013.08.013

van Franeker, J.A., 2004. Save the North Sea fulmar-Litter-EcoQO manual part 1:

Collection and dissection procedures. Alterra, Wageningen Alterra-rapport 672,

38.

van Franeker, J.A., Blaize, C., Danielsen, J., Fairclough, K., Gollan, J., Guse, N., Hansen,

P.-L., Heubeck, M., Jensen, J.K., Olsen, B., Olsen, K.-O., Pedersen, J., Stienen,

E.W.M., Turner, D.M., 2011. Monitoring plastic ingestion by the northern fulmar

Fulmarus glacialis in the North Sea. Environmental Pollution 159, 2609–2615.

doi:10.1016/j.envpol.2011.06.008

van Franeker, J.A., Law, K.L., 2015. Seabirds, gyres and global trends in plastic

pollution. Environmental Pollution 203, 89–96. doi:10.1016/j.envpol.2015.02.034

van Franeker, J.A., Luttik, R., 2008. Colour and size variation in the northern fulmar

Fulmarus glacialis on Bear Island, Svalbard. Circumpolar Studies 4, 39–58.

83

van Franeker, J.A., Meijboom, A., 2002. LITTER NSV, Marine litter monitoring by

northern fulmars (a pilot study). Wageningen, Alterra, Green World Research,

Alterra-rapport Alterra-rapport 401, 72.

van Franeker, J.A., Wattel, J., 1982. Geographical variation of the Fulmar Fulmarus

glacialis in the North Atlantic. Ardea 70, 31–44.

Van Oostdam, J., Gilman, A., Dewailly, E., Usher, P., Wheatley, B., Kuhnlein, H., Neve,

S., Walker, J., Tracy, B., Feeley, M., Jerome, V., Kwavnick, B., 1999. Human

health implications of environmental contaminants in Arctic Canada: A review.

Science of the Total Environment 230, 1–82.

Venables, W.N., Ripley, B.D., 2002. Random and mixed effects, in: Modern Applied

Statistics with S. Springer, pp. 271–300.

Verlis, K.M., Campbell, M.L., Wilson, S.P., 2013. Ingestion of marine debris plastic by

the wedge-tailed shearwater Ardenna pacifica in the Great Barrier Reef, Australia.

Marine Pollution Bulletin 72, 244–249. doi:10.1016/j.marpolbul.2013.03.017

Votier, S.C., Archibald, K., Morgan, G., Morgan, L., 2011. The use of plastic debris as

nesting material by a colonial seabird and associated entanglement mortality.

Marine Pollution Bulletin 62, 168–172. doi:10.1016/j.marpolbul.2010.11.009

Wabnitz, C., Nichols, W.J., 2010. Plastic pollution: An ocean emergency. Marine Turtle

Newsletter 129, 1–4.

Walther, I., Daoust, P.Y., Lucas, Z., 2008. Plastic ingestion in northern fulmars

(Fulmarus glacialis) in the western North Atlantic. Wildlife Health Centre

Newsletter 13, 5–6.

84

Wickham, H., 2009. ggplot2: Elegant graphics for data analysis, Use R! Springer

International Publishing, New York, New York, USA.

Wickham, H., Francois, R., 2015. dplyr: A grammar of data manipulation. R package

version 0.5.0 [WWW Document]. URL https://cran.r-

project.org/web/packages/dplyr/index.html (accessed 3.19.17).

Wilcox, C., Van Sebille, E., Hardesty, B.D., 2015. Threat of plastic pollution to seabirds

is global, pervasive, and increasing. Proceedings of the National Academy of

Sciences 112, 11899–11904. doi:10.1073/pnas.1502108112

Wille, M., McBurney, S., Robertson, G.J., Wilhelm, S.I., Blehert, D.S., Soos, C.,

Dunphy, R., Whitney, H., 2016. A pelagic outbreak of Avian Cholera in North

American gulls: Scavenging as a primary mechanism for transmission? Journal of

Wildlife Diseases 52, 793–802. doi:10.7589/2015-12-342

Wilson, A.J., 1999. Gunshot injuries: What does a radiologist need to know?

RadioGraphics 19, 1358–1368. doi:10.1148/radiographics.19.5.g99se171358

Wold, S., Esbensen, K., Geladi, P., 1987. Principal component analysis. Chemometrics

and Intelligent Laboratory Systems 2, 37–52. doi:10.1016/0169-7439(87)80084-9

Woodall, L.C., Sanchez-Vidal, A., Canals, M., Paterson, G.L.J., Coppock, R., Sleight, V.,

Calafat, A., Rogers, A.D., Narayanaswamy, B.E., Thompson, R.C., 2014. The

deep sea is a major sink for microplastic debris. Royal Society Open Science 1,

140317–140317. doi:10.1098/rsos.140317

Work, T.M., Rameyer, R.A., 1999. Mass stranding of wedge-tailed shearwater chicks in

Hawaii. Journal of Wildlife Diseases 35, 487–495. doi:10.7589/0090-3558-

35.3.487

85

Wright, S.L., Thompson, R.C., Galloway, T.S., 2013. The physical impacts of

microplastics on marine organisms: A review. Environmental Pollution 178, 483–

492. doi:10.1016/j.envpol.2013.02.031

Ye, S., Andrady, A.L., 1991. Fouling of floating plastic debris under Biscayne Bay

exposure conditions. Marine Pollution Bulletin 22, 608–613. doi:10.1016/0025-

326X(91)90249-R

Yorio, P., Caille, G., 1999. Seabird interactions with coastal fisheries in Northern

Patagonia: Use of discards and incidental captures in nets. Waterbirds 22, 207.

doi:10.2307/1522209

Zbyszewski, M., Corcoran, P.L., 2011. Distribution and degradation of fresh water plastic

particles along the beaches of Lake Huron, Canada. Water, Air & Soil Pollution

220, 365–372. doi:10.1007/s11270-011-0760-6

Zbyszewski, M., Corcoran, P.L., Hockin, A., 2014. Comparison of the distribution and

degradation of plastic debris along shorelines of the Great Lakes, North America.

Journal of Great Lakes Research 40, 288–299. doi:10.1016/j.jglr.2014.02.012

Zhao, S., Zhu, L., Li, D., 2016. Microscopic anthropogenic litter in terrestrial birds from

Shanghai, China: Not only plastics but also natural fibers. Science of The Total

Environment 550, 1110–1115. doi:10.1016/j.scitotenv.2016.01.112

86

Appendices

Appendix A. Details on each bird that ingested anthropogenic debris in this study. N = number of anthropogenic debris fragments

recovered per-bird. GWFG = greater white-fronted goose; SNGO = snow goose; CAGO = Canada goose; AMWI = American wigeon;

ABDU = American black duck; MALL = mallard; NOPI = northern pintail; WWSC = white-winged scoter; COEI = common eider;

YBLO = yellow-billed loon (data on all birds, including those that did not ingest plastic, are available from the authors).

Plastic (N) Rubbish (N) Metal (N) Foraging niche

Species Location Sex Age Fragments Other Thread-like

Foil Paint chips

Glass Rubber Birdshot Metal

Geese GWFG 49°11'41 N 123°10'48 W

M Juvenile 0 0 0 0 0 0 0 0 1

SNGO 49°11'41 N 123°11'02 W

M Juvenile 0 0 1 0 0 0 0 0 0

SNGO 49°11'41 N 123°10'48 W

N/A Juvenile 1 0 0 0 0 0 0 0 0

SNGO 49°04'34 N 123°09'37 W

F Juvenile 0 0 0 0 0 0 0 0 1

CAGO 44°50'29 N 65°17'22 W

N/A Unknown 0 0 0 0 1 0 0 0 0

CAGO 49°11'41 N 123°11'02 W

M Adult 0 0 0 2 0 0 0 0 0

CAGO 49°10'27 N 121°54'38 W

M Adult 0 0 0 2 0 0 0 0 0

CAGO 49°10'27 N 121°54'38 W

F Adult 0 0 0 1 0 0 0 0 0

CAGO 49°10'12 N 121°54'36 W

F Adult 0 0 0 0 0 1 0 0 0

CAGO 49°10'12 N 121°54'36 W

F Adult 0 0 0 0 0 1 0 0 0

87

Plastic (N) Rubbish (N) Metal (N) Foraging niche

Species Location Sex Age Fragments Other Thread-like

Foil Paint chips

Glass Rubber Birdshot Metal

CAGO 44°50'29 N 65°17'22 W

N/A Unknown 2 0 0 0 0 0 0 0 0

CAGO 44°50'29 N 65°17'22 W

N/A Unknown 0 1 0 0 0 0 0 0 0

Dabbling Ducks

AMWI 49°06'22 N 122°05'31 W

F Adult 1 0 0 0 0 0 0 0 0

AMWI 48°59'34 N 122°13'30 W

M Adult 0 0 0 0 0 1 0 0 0

AMWI 49°04'35 N 123°09'39 W

M Adult 1 0 0 0 0 0 0 0 0

ABDU 44°48'06 N 65°23'57 W

N/A Unknown 0 0 0 0 0 0 0 1 0

MALL 44°48'05 N 65°23'57 W

N/A Unknown 0 0 0 0 0 0 0 3 0

MALL 49°12'50 N 121°46'57 W

M Adult 3 0 0 0 0 0 0 0 0

MALL 49°12'50 N 121°46'57 W

M Adult 0 0 0 0 0 0 0 0 1

MALL 49°09'27 N 122°34'48 W

F Adult 0 0 0 4 0 0 0 0 0

MALL 49°12'50 N 121°46'58 W

M Adult 0 0 0 0 0 0 0 1 0

MALL 49°12'50 N 121°46'57 W

M Adult 0 0 0 0 0 0 0 1 0

MALL 49°06'41 N 123°04'53 W

F Adult 1 0 0 0 0 0 0 0 0

MALL 49°12'50 N 121°46'58 W

F Adult 0 0 0 0 0 0 57 0 0

MALL 49°12'50 N 121°46'58 W

M Adult 0 0 0 0 0 1 0 0 0

MALL 49°16'00 N 121°43'12 W

F Adult 1 0 0 0 0 0 0 0 0

MALL 49°12'50 N 121°46'58 W

N/A Unknown 0 0 0 0 0 0 0 2 0

88

Plastic (N) Rubbish (N) Metal (N) Foraging niche

Species Location Sex Age Fragments Other Thread-like

Foil Paint chips

Glass Rubber Birdshot Metal

MALL 62°44'06 N 115°42'35 W

N/A Unknown 1 0 0 0 0 0 0 0 0

MALL 62°44'06 N 115°42'35 W

N/A Unknown 0 0 0 0 0 0 0 1 0

MALL 62°44'06 N 115°42'35 W

N/A Unknown 1 0 0 0 0 0 0 0 0

MALL 45°06'26 N 64°39'19 W

F Adult 1 0 0 0 0 0 0 0 0

NOPI 49°04'44 N 123°02'43 W

M Adult 0 0 0 0 0 1 0 1 0

NOPI 49°06'41 N 123°04'48 W

F Adult 1 0 0 0 0 0 0 0 0

Diving Ducks

WWSC 43°19'31 N 79°47'56 W

N/A Unknown 1 0 0 0 0 0 0 0 0

Sea Ducks COEI 49°48'44 N 54°07'07 W

M Adult 1 0 0 0 0 0 0 0 0

COEI 49°48'44 N 54°07'07 W

F Adult 0 0 0 0 0 0 0 0 1

COEI 49°48'44 N 54°07'07 W

M Juvenile 0 0 0 0 0 0 0 1 0

COEI Unknown

F Adult 0 0 0 1 0 0 0 0 0

Loons YBLO 63°26'04 N 109°11'10 W

N/A Juvenile 1 0 0 0 0 0 0 0 0

89

Appendix B. Summary of pathology and microbiology findings of note from 39 procellariids collected beached on Sable Island, Nova

Scotia, Canada, between 2000 and 2012. GRSH = great shearwater; Imm. = Immature; NOFU = northern fulmar; NSF = No

significant findings; Sp. = Species; SOSH = sooty shearwater.

Sp. Date (D/M/Y) Age Sex Weight

(g) Gross lesions Histological lesions Debris (g)

SOSH 03/06/2008 Imm Female 524.2 Emaciation Chronic multifocal coelomic fat necrosis 0.0087

SOSH 04/07/2010 Imm. Male 441.5 Chronic ventricular ulcer; emaciation Intralesional nematodes 0.0000

GRSH 17/06/2005 Adult Female NA Emaciation Moderate muscular sarcocystosis 0.0000

GRSH 20/06/2006 Imm. Male 764.5 Chronic locally extensive cellulitis, esophageal perforation (fish bone); emaciation

NSF

0.0798

GRSH 23/06/2006 NA NA 492.1 Emaciation Mild muscular sarcocystosis 0.0781 GRSH 01/07/2006 Adult Female 506.4 Emaciation Focally extensive subacute myopathy 0.1327 GRSH 23/08/2006 NA Male 568.3 Emaciation Acute multifocal hepatic necrosis 0.0957

GRSH 29/06/2007 Imm. Female 736.8 Coelomic cavity infection Proventricular parasitic infection, transmural proventriculitis, fibrinous perihepatitis, fibrinous air sacculitis

0.1346

GRSH 01/09/2010 Imm Male NA Trauma, multifocal renal hemorrhages; emaciation NSF 0.1663

GRSH 07/07/2011 Imm. Male 528.4 Emaciation Focal chronic parasitic proventriculitis 0.0395

GRSH 07/07/2011 Imm. Males 471.9 Proventricula perforation; emaciation

Focal chronic transmural proventriculitis, chronic fibrinous serositis

0.0182

GRSH 14/09/2011 Imm Male 717.9 Trauma fibrinopurulent cellulitis 0.0000 GRSH NA Adult Male 511.7 Chronic focal cellulitis; emaciation NSF 0.9740 NOFU 01/05/2004 Adult Male 751.2 Emaciation Moderate muscular sarcocystosis 0.1780 NOFU 01/05/2004 Imm. Male 847.6 Emaciation Hepatic neoplasia 0.3370 NOFU 04/05/2004 Adult Female NA Egg impaction, autolysis; emaciation NSF 4.2050 NOFU 22/10/2004 NA Male 402.7 Emaciation Chronic pericarditis, air sacculitis 0.0590 NOFU 04/04/2005 Imm. Male NA NSF Chronic focal myocarditis 4.4720

NOFU 16/04/2005 Adult Male NA Multifocal subcutaneous fibromas; emaciation NSF 1.3760

NOFU 01/06/2005 NA Male 650.0 Focal subcutaneous fibroma Cartilaginous metaplasia 0.7040

90

Sp. Date (D/M/Y) Age Sex Weight

(g) Gross lesions Histological lesions Debris (g)

NOFU 21/12/2005 Adult Female 677.2 NSF Acute multifocal pectoral myopathy, mild (multi-) focal granulomatous hepatitis

0.0773

NOFU 22/12/2005 Imm. Male 659.6 Emaciation Moderate acute pectoral myopathy with mineralization.

0.0000

NOFU 13/04/2006 Imm Male NA NSF Chronic intracoelomic fat necrosis 3.6307

NOFU 04/05/2006 Imm. Female 604.7 NSF Mild renal parasitism (trematodes), mild muscular sarcocystosis, and mild subacute multifocal (pectoral) myositis

0.4839

NOFU 26/02/2007 Imm. Female 630.7 NSF acute septicemia 0.0096 NOFU 01/03/2007 Imm. NA 869.0 NSF Sarcosystis 0.0000 NOFU 13/06/2007 Imm. Male 567.3 Emaciation Severe intestinal cestodiasis 0.1583 NOFU 28/02/2007 NA Male 881.4 Subacute periarterial abscesses NSF 0.3080 NOFU 29/04/2007 Imm. Female NA Emaciation Focal mycotic air sacculitis. 0.0871

NOFU 04/01/2008 Imm Female NA Chronic focal traumatic proventriculitis (fish hook) NSF 0.9322

NOFU 30/05/2008 Imm. Female 604.6 Emaciation Chronic focal pyogranulomatous air sacculitis. 0.0000 NOFU 06/06/2008 Imm. Male 540.9 Intestinal cestodiasis NSF 0.0600 NOFU 07/04/2009 Imm. Male NA Emaciation Mild pulmonary nematodiasis 0.5993 NOFU 09/04/2009 Imm. NA NA Podpdermatitis, emaciation NSF 0.7583 NOFU 27/09/2010 Imm. Male NA Fibrochodroma; emaciation NSF 0.1042 NOFU 15/05/2011 Imm. NA 603.5 NSF Hepatic and splenic mycobacteriosis 2.5595

NOFU 05/06/2011 Adult Male 745.3 Severe unilateral chronic necrotizing orchitis and funiculitis; emaciation NSF 0.1817

NOFU 05/06/2011 Adult Female NA Chronic fibrinous oophoritis and peritonitis; emaciation NSF 0.3575

NOFU 20/01/2012 Imm. Male 557.2 Emaciation Chronic focal cellulitis 0.0222

91

Appendix C. Pathology of four procellariid species collected beached on Sable Island, Nova Scotia, Canada, between 2000-2012, and

comparisons to previous pathological descriptions in the literature. “This study” indicates pathological reports new to these species,

determined by a literature review searching species name and the pathological symptom. “-” indicates no symptoms were found.

Pathology Cory’s Shearwater

Sooty Shearwater

Great Shearwater

Northern Fulmar

Starvation Mougin et al., 2000

Grant et al., 1994 Pierce et al., 2004 Harvey et al., 2004

Autolysis This study Humphries, 2014 This study Harris et al., 2006 Parasite Infection Sarcocystosis - - This study This study Intestinal cestodiasis - - - Mallory et al., 2007 Parasitic proventriculitis - - Nemeth et al., 2011 - Pulmonary nematodiasis - - - Mallory et al. ,2007 Renal parasitism

(trematodes) - - - This study

Inflammation Air sacculitis - - - Jessup et al., 2009 Myocarditis - - - Kalmar et al., 2014 Oophoritis and peritonitis - - - This study Periarterial abscesses - - - This study Pericarditis and air

sacculitis - - - Jessup et al., 2009

Pododermatitis (bumblefoot)

- - - This study

Proventriculitis and serositis

- - Nemeth et al., 2012 -

Trauma - - Haman et al., 2013 van Franeker and Meijboom, 2002

92

Pathology Cory’s Shearwater

Sooty Shearwater

Great Shearwater

Northern Fulmar

Bacterial Infection Cellulitis - - This study Li et al., 2015 Chronic ventricular ulcer - This study - - Mycobacteriosis - - - This study Orchitis and funiculitis - - - This study Septicemia - - - This study Drowned - Reyes-Arriagada et al., 2007 Yorio and Caille, 1999 - Tumour Fibromas - - - Pokras, 1988 Fibrochodroma - - - Pokras, 1988 Neoplasia - - - Gaynor et al., 2015 Tissue Necrosis Fat necrosis - This study - This study Hepatic necrosis - - This study - Impaction Egg impaction - - - Walther et al., 2008 Rectal Impaction - - - van Franeker and

Meijboom, 2002 Myopathy - - This study This study Pneumonia - - - Bellizzi and Duerr, 2013