Abird's-eyeviewofairpollution

Theimpactsofhealth-damagingairpollutantsonavifaunaby

OliviaV.Sanderfoot

Athesissubmittedinpartialfulfillmentof

therequirementsforthedegreeof

MasterofScience

(EnvironmentandResources)

atthe

NelsonInstituteforEnvironmentalStudies

UNIVERSITYOFWISCONSIN–MADISON

2017

APPROVED Tracey Holloway Date Professor

i

Abstract

Despite the well-established links between air pollution and human health,

vegetation,andaquaticecosystems,lessattentionhasbeenpaidtothepotentialimpact

ofreactiveatmosphericgasesandaerosolsonavianspecies.Inthisthesis,Isynthesize

andanalyze findingspublished since1950 regardingavian responses to airpollution

anddiscussknowledgegapsthatcouldbeaddressedinfuturestudies.Ifindconsistent

evidenceforadversehealthimpactsonbirdsattributabletoexposuretogas-phaseand

particulate airpollutants, including carbonmonoxide (CO), ozone (O3), sulfurdioxide

(SO2),smoke,andheavymetals,aswellasmixturesofurbanandindustrialemissions.

Avian responses to air pollution include respiratory distress and illness, impaired

reproductive success, increased detoxification effort, elevated stress levels,

immunosuppression, and behavioral changes. Exposure to air pollution may

furthermorereducepopulationdensity,speciesdiversity,andspeciesrichness inbird

communities.ThisthesisconstitutesakeystepindeterminingifthesecondaryNational

Ambient Air Quality Standards (NAAQS) set by the United States Environmental

Protection Agency (EPA) to protect public welfare are sufficient in safeguarding

avifauna from the adverse health outcomes associated with air pollution. To my

knowledge, this is the firstmeta-analysis of studies examining the effects of reactive

gasesandaerosolsonnon-humanspecies.

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Acknowledgements

Support for this project was provided by the National Science Foundation Graduate

ResearchFellowshipProgramunderGrantNo.DGE-1256259,withadditionalsupport

from the National Aeronautics and Space Administration (NASA) Applied Sciences

Program through the Air Quality Applied Sciences Team (AQAST) initiative. Any

opinions,findings,andconclusionsorrecommendationsexpressedinthismaterialare

those of the author and do not necessarily reflect the views of the National Science

FoundationorNASA.

I would like to thank my advisor and committee chair, Dr. Tracey Holloway

(Department of Atmospheric & Oceanic Sciences and Nelson Institute Center for

SustainabilityandtheGlobalEnvironment),andmycommitteemembers,Dr.Benjamin

Zuckerberg(DepartmentofForestandWildlifeEcology)andDr.PaulRobbins(Nelson

Institute for Environmental Studies), for their mentorship and feedback during my

graduatestudiesat theUniversityofWisconsin–Madisonandthedevelopmentof this

researchthesis.

I would also like to thank my friends and colleagues, especially Dr. Alexandra

Karambelas (The Earth Institute, Columbia University), Dr. Daegan Miller (Nelson

Institute Center for Sustainability and the Global Environment, University of

Wisconsin–Madison), Nick Etzel (Department of Biostatistics, University of

Washington), LizWendt (MedicalCollegeofWisconsin), andBeckyReese (Wisconsin

InstituteforMedicalResearch,UniversityofWisconsin–Madison),fortakingthetimeto

providefeedbackonearlydraftsoftheliteraturereviewincludedinchaptertwo.

This thesis is dedicated to my sister, Ivy Leone Sanderfoot, whose tenacious spirit,

cleverlifehacks,andbeautifulsongmakehersoverybirdlike.

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Finally, I would like to thank the faculty and staff at the Nelson Institute for

EnvironmentalStudiesfortheirsupportduringmyundergraduateandgraduatestudies

at the University ofWisconsin–Madison, especially JimMiller, Becky Ryan, and Nick

Horan.Youcouldnot findamorededicated,motivated,andenthusiastic team.Thank

youforhelpingmegrowasastudent,scholar,andscientistoverthepastsevenyears.

BeingaNelsonitemeanstheworldtome.OnWisconsin!

TableofContents:

Abstract………………………………………………………………………...................................................i

Acknowledgements…………………………………………………………………………………………..ii

ChapterOne:Introduction………………………………………………………………………………..1

OurAtmosphere………………………………………………………………………………………..2

AirPollution&HumanHealth……………………………………………………………………3

AirQualityRegulation………………………………………………………………………………..4

TheCulturalSignificanceofBirds……………………………………………………………….6

AvianRespiration..…………………………………………………………………………………….8

AnOriginalMeta-analysis…………………………………………………………………..........10

ChapterTwo:Areviewofairpollutionimpactsonavianspecies………………………..12

Introduction……………………………………………………………………………………………12

Methods………………………………………………………………………………………………….15

KeyFindings……………………………………………………………………………………...........16Respiratorydistressandillness…………………………………………………………………..............................17

Impairedreproductivesuccess………………………………………………………………………………………..25

Increaseddetoxificationeffort,elevatedstresslevels,andimmunosuppression………………..29

Behavioralchanges…………………………………………………………………………………………………………35

Habitatdegradation………………………………………………………………………………………………………..36

Demographicresponses………………………………………………………………………………………………….38

Discussion……………………………………………………………………………………………….40

WorksCited…………………………………………………………………………………………….47

ChapterThree:Conclusion……………………………………………………………………………...56

ImplicationsforAirQualityPolicy……………………………………………………………56

AdditionalPolicyRecommendations…………………………………………………..........59

FutureStudies…………………………………………………………………………………………59

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I.Introduction

Birdsareavaluedcomponentofpublicwelfareformyriadreasons.Birdsplayan

integral role in ecosystems around theworld, acting as keystone predators, foragers,

and scavengers. There are over 10,000 species of birds; together they represent an

incredible reservoir of genetic diversity that supports nature’s grand resiliency.

Studyingbirdsprovidesscientistswiththeopportunitytolearnmoreaboutlifehistory

strategies,physiologicalmechanisms,andtheevolutionofflight.Themereexistenceof

birds is of benefit to mankind, as these animals are of great cultural significance to

societiesaroundtheworld,andtheircharismaisfrequentlyexploitedbyconservation

groupstocreatemoreengagingeducationalprogramming.

It is clear that birds are negatively impacted by many of the environmental

challenges we face today, including urbanization, habitat degradation, and climate

change. Air pollutionmay also impose undue stress on birds, resulting in long-term,

negativeeffectsonfitnessandpossiblyleadingtodemographicconsequences,suchas

reducedpopulationsizeordensityorshiftsincommunitycomposition.Unfortunately,

researchonthetopicofavianresponsestoairpollutionislimitedatbest.

Itispossiblethatdisciplinarydividesmaybeinhibitingtheresearchcommunity

from learningmore abouthowbirds are affectedby air quality. It becameevident in

developing this thesis that there has been little collaboration amongst atmospheric

chemists, ecologists, toxicologists, ornithologists, and veterinarians on characterizing

avianresponsestoairpollution.Tomyknowledge,thisthesisistheonlyworktodate

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with the goal of linking research on this topic from distinct fields. In this thesis, I

synthesizeandanalyzefindingsfromnumerousfieldsofstudyonavianresponsestoair

pollutiontosupport futureresearchonthis important topicand informpublicpolicy.

Toprovidecontextforthiswork,thischapterpresentskeybackgroundinformationon

air pollution, air quality regulation, avian respiration, and the cultural significance of

birds.

OurAtmosphere

This thesisexploresavianresponses toairpollution,so it isuseful tobeginby

considering the nature of air pollution as an environmental problem. Planet Earth is

encompassedbyablanketofgaseswerefertoasouratmosphere.Thoughthinrelative

to our planet’s radius, our atmosphere is essential in supporting life on Earth by

insulatingEarth’ssurfacefromthesun’sharmfulultravioletrays.Ouratmospherealso

playsakeyrole in thehydrologiccycleandthecyclingofnutrients, includingcarbon,

nitrogen, and phosphorus. Our atmosphere is made up almost entirely of nitrogen

(78%), oxygen (21%), and argon (0.9%) in proportions that do not vary spatially or

temporally. Trace gases and aerosols account for just one-tenth of the atmosphere’s

chemical composition, yet the concentrations of these compounds, constantly in flux,

dramaticallyaffectbothairqualityandthecapacityofouratmospheretoretainheat.

Bothhumanactivity andnaturalprocesses contribute to the concentrationsof

trace gases and aerosols in our atmosphere, sometimes referred to as pollutants.

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Primary air pollutants are gases and aerosols that are directly emitted to the

atmosphere. Secondary air pollutants are gases and aerosols that are formed in the

atmosphere due to complex chemical reactions. Though vastly outnumbered by the

mixing ratios of nitrogen, oxygen, and argon, the ambient concentrations of primary

andsecondaryairpollutants,whetherofnaturaloranthropogenicorigin,determinethe

qualityoftheairwebreatheandthedegreeofglobalwarmingthatoccurswithinour

atmosphere.

AirPollution&HumanHealth

There are thousands of different trace gases and aerosols found in the

atmosphere, each with a unique chemical composition and set of properties. While

some air pollutants are highly reactive, others are inert. The chemical lifetime of air

pollutants is therefore highly variable. For example, the characteristic oxidation time

for benzene (C6H6), a volatile organic compound, is 9.6 days,while the characteristic

oxidation time for methane (CH4), a greenhouse gas, is 4.1 years.1 Long-lived

greenhouse gases, includingmethane, carbon dioxide (CO2), and nitrous oxide (N2O),

contribute to global warming by trapping the heat of infrared radiation emitted by

Earth’s surface. Reactive gases and aerosols, including volatile organic compounds

(VOCs),nitrogendioxide(NO2),andozone(O3),arelessofaconcernwhenconsidering

1“AirPollutants&EffectsII.”ClassLecture.AirPollutionEffects,Measurement,andControls.UniversityofWisconsin–Madison.Dr.JamieSchauer.January24,2017.

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the capacity of the atmosphere to retain heat because these compounds are rapidly

consumedinchemicalreactionsordepositedtoEarth’ssurface.

However,reactivegasesandaerosolsareoftenassociatedwithadversehuman

health impacts. For example, exposure toO3 andparticulatematter (PM, referring to

any solid or liquid suspended in the air) has been linked to cardiovascular disease,

respiratorydisease,andprematuremortality.Infact,exposuretohealth-damagingair

pollutantssuchasPMandO3isaleadingcontributortotheglobalburdenofdiseaseand

leadstomillionsofprematuredeathseachyear,accordingtoresearchconductedbythe

InstituteforHealthMetricsandEvaluation(IHME).2IHMErankedexposuretoambient

PM as the 5th leading risk factor formortalityworldwide. Household air pollution is

ranked 10th and exposure to ambient O3 is ranked 33rd. Exposure to air pollution is

clearlydetrimentaltohumanhealth.

AirQualityRegulation

While there are natural sources of reactive gases and aerosols, high outdoor

concentrations of health-damaging air pollutants are primarily driven by human

activity.Environmentalregulationdesignedtocontrolbothemissionsofairpollutants

and ambient concentrations of specific compounds is effective in reducing human

exposure to health-damaging air pollutants. In the United States, the Environmental

Protection Agency (EPA) is granted the authority to regulate air quality to protect

2http://www.healthdata.org/sites/default/files/files/infographics/Infographic_AAAS_Air-pollution_2016.pdf

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publichealthandtheenvironmentundertheCleanAirAct.Accordingtoareportissued

by the Office of Management & Budget (OMB) in 2014, the estimated benefits of

regulations imposedbytheEPA’sOfficeofAir&Radiationamount to threetimesthe

costsof their implementation.3 In fact, theOMBestimatedthat98%to99%ofall the

benefitsofenvironmentalpolicysetby theEPAareassociatedwithrulesdesignedto

improveairquality.3Whileexpensive,airqualityregulation isevidentlyaworthwhile

investment.

TheNationalAmbientAirQualityStandards(NAAQS)setbytheEPAareakey

component of the regulatory framework established to reduce air pollution and

improveairqualityintheUnitedStates.PrimaryNAAQSaredesignedtoprotectpublic

healthby limitingambientconcentrationsofhealth-damagingairpollutants thathave

been linked tocardiovascularandrespiratorydisease.SecondaryNAAQS are intended

toprotectpublicwelfarebyimprovingvisibilityandreducingdamagetoinfrastructure,

vegetation, crops, and animals, including birds. Given the limited number of studies

regardingtheimpactsofairpollutiononwildlife,itisunclearifthesecondaryNAAQS

are sufficient to protect our nation’s rich biodiversity. Research does show that air

pollutionnegatively impactsecosystems.Ozonedamages the leaf tissueofplantsand

industrialandagriculturalemissionsleadtothedepositionofsulfuricandnitricacids

to lakes and rivers, commonly referred to as “acid rain.” This adversely impacts

fisheries and the wildlife dependent on freshwater habitat. Additional research is

needed to determine if current air quality regulation is sufficient to protect wildlife3https://obamawhitehouse.archives.gov/sites/default/files/omb/inforeg/2014_cb/draft_2014_cost_benefit_report-updated.pdf

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from elevated ambient concentrations of health-damaging air pollutants. Birds in

particulararelikelymoresusceptibletothenegativehealtheffectsassociatedwithair

pollution because they respire more efficiently than any other type of terrestrial

vertebrate. This thesis focuses on identifying known avian responses to air

pollutantsregulatedbytheEPAtodetermineifthesecondaryNAAQSsetbythe

EPA should be additionally stringent to protect the hundreds of bird species

living in the United States and provide additional policy recommendations to

protectbirdsasavitalcomponentofpublicwelfare.

TheCulturalSignificanceofBirds

There are well over 10,000 species of birds on Planet Earth. They persist on

every continent, occupy myriad habitats, and serve as living, breathing examples of

evolution in action, demonstrating the intimate tie between form and function that

drives natural selection. Humans have always been fascinated by these feathered

descendants of dinosaurs. Over thousands of years, birds have become an important

cultural symbol. In the U.S., for example, the American Robin is often considered a

harbingerofspringwhileinruralareasofsouthernAfricavulturesareoftensaidtobe

asignofimpendingdoom.

Acrossmanycultures,birdshavealsocometosymbolizehumanvulnerabilityto

environmentalchange.Intheearly1900s,coalminersbroughtcanariesdownintothe

minestohelpmonitorlevelsofnoxiousgases,leadingtotheuseofthecolloquialphrase

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“canaryinthecoalmine”torefertoanearly-warningsignalofsomefuturedanger.In

the1960s,RachelCarson’saward-winningbookSilentSpringbroughtattentiontothe

widespread impact of pesticide and insecticide applications on wildlife, especially

songbirds, amessage that struck a chordwith hundreds of thousands of people and

inspiredthemovementthatledtotheestablishmentoftheEPA.Today,birdshavebeen

assessed for their value in the biomonitoring of heavymetals and persistent organic

pollutants, and work by citizen scientists shows that birds are responding to the

warmertemperaturesbroughtaboutbyclimatechange.

Despite the demonstrated importance of birds to society, several knowledge

gapsremaininthescientificcommunity’sunderstandingofhowhumanactivityaffects

theseanimals.Researchclearly shows thatbirdsarenegatively impactedby landuse

change, urbanization, habitat fragmentation, and contamination of freshwater and

saltwater habitats, but substantially less is known about how air quality affectswild

avianpopulations.Thereisnodoubtthatrespiratoryexposuretohealth-damagingair

pollutantsposesarisktohumans,andbirdsrespiremoreefficientlythanwedo.This

likelyrendersbirdsmoresusceptibletotheadversehealthimpactsassociatedwithair

pollution.However,studiesonhowbirdsrespondtoairpollutionare few innumber,

anduntilnowhavenotbeencompiledinameaningfulway.Thishasmadeitdifficultto

pinpoint species-specific responses at the physiological and demographic level.

Ecologistsandatmosphericchemistsshouldworktogethertoextendthevastliterature

onairpollutionandhumanhealthtoconsiderhowairqualityaffectsbirds,animalsthat

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are not only vitally important to dozens of ecosystems but also have great cultural

significanceincommunitiesaroundtheworld.

AvianRespiration

Birds respire much more efficiently than mammals, thanks to the unique

structureoftheavianrespiratorysystem.Avianlungsdonotexpandandcontractlike

thoseofmammals. Instead, birdsutilize a series of air sacs— thin-walled structures

that act as bellows — to constantly push fresh air into their lungs. This strategy

supportsunidirectionalair flow,maximizingcontactof fresh,oxygenatedairwith the

gasexchangesurfacesofthelungs.Gasexchangeistheprimarypurposeofrespiration.

Therespiratorysystemsuppliesthebodywithoxygen(O2)andremovesCO2,awaste

productofmetabolicactivity.

Because avian lungsdonot expand and contract like those ofmammals, birds

manipulate their skeletal structure to alter the pressure in the respiratory systemas

neededtodrawandexpelair.Todoso,birdslowerthesternumininhalationandraise

thesternuminexhalation.Loweringthesternumduringinhalationexpandstheribcage,

openingupthechestcavityandextendingtheairsacs.Thisreducesthepressurewithin

the air sacs, which then pull in air. Raising the sternum contracts the ribcage,

compressingthechestcavityandtheairsacs.Thisincreasesthepressurewithintheair

sacs,which then expel air. Thesemovements are synchronizedwithwingbeatswhen

birdsareinflight.

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Avian respiration occurs in four steps, or two cycles of inspiration and

expiration,asdescribedbelow:

•Step#1(Inhalation):Airisinhaledthroughthenostrilsatthebaseofthebeakandpulled

downthetrachea,throughtheprimarybronchi,totheposteriorairsacs.

•Step#2(Exhalation):Airheldintheposteriorairsacsispushedthroughthesecondaryand

tertiarybronchitotinyaircapillariesinthelung.Theaircapillariescrisscrossbloodcapillaries,

allowinggasexchange tooccur.Thebloodcapillaries takeupO2as theaircapillaries takeup

CO2.

•Step#3(Inhalation):O2-depletedairispulledfromthelungintotheanteriorairsacs.

• Step#4 (Exhalation):O2-depletedairheld in the anterior air sacs ispushed through the

primarybronchi,upthetrachea,andoutofthenostrils.

Thesefourstepstrackhowairmovesthroughtheavianrespiratorysystem.In

reality,air flowisconstant,andthestepsthatoccurduringinhalation(#1and#3)or

exhalation (#2 and #4) transpire simultaneously. As the ribcage expands, inhalation

pullsairfromtheenvironmentintotherespiratorysystemtobeheldintheposterior

airsacswhileO2-depletedair ispulledfromthelungintotheanteriorairsacs.Asthe

ribcage contracts, air is expelled from the air sacs, causing O2-rich air held in the

posteriorairsacstoflowintothelungandCO2-richairheldintheanteriorairsacsto

exit thebody.Unlike inmammals, air enters the lungduringexpirationandexits the

lung during inspiration. The unidirectional flow of air replaces nearly all the air

contained in the lungs with each breath. This helps maximize the efficiency of gas

exchange. In addition to supporting unidirectional air flow, the air sacs also help to

reducetheheatgeneratedbybirdsinflightandprotecttheirinternalorgans.

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Anotherimportantcharacteristicoftheavianrespiratorysystemiscrosscurrent

gas exchange, a strategy that further improves the efficiency of avian respiration.

Crosscurrent gas exchange occurs when air capillaries and blood capillaries are

positionedatrightangles.ThisgreatlyincreasesthediffusionofO2fromtheairtothe

blood.

The unique structure of the avian respiratory system enables birds tomove a

greatervolumeofoxygenatedairthroughtheirlungswitheachbreathascomparedto

mammals,andcrosscurrentgasexchangebetweentheairandbloodcapillaries inthe

lungsprovidesforevenmoreefficientrespiration.Thisallowsbirdstosustainflightin

environmentsthatcouldbe life-threateningtomammals,suchasthehighaltitudesof

the Himalayan mountain range through which the Bar-headed Goose migrates each

year.Giventheefficiencyoftheavianrespiratorysystemandthehighventilationrates

required during flight, it is reasonable to expect that birds might also be more

susceptible to the negative health effects associated with respiratory exposure to

reactivegasesandaerosols.

AnOriginalMeta-analysis

Inthisthesis,Iconductameta-analysisofresearchfindingsonavianresponses

to air pollution spanning amultitude of disciplines. In chapter two, I synthesize and

analyze findings published since 1950 on avian responses to reactive gases and

aerosolsanddiscussknowledgegapsthatcouldbeaddressedinfuturestudies.Please

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note that this chapter constitutes work in review at Environmental Research Letters.

Environmental Research Letters is one of the leading interdisciplinary journals in the

environmental sciences, and review articles must follow a quantitative methodology

that draws from the medical review literature. According to the publisher,review

articles are “systematic, evidence-based reviews of important and topical

environmental issues…. The journal hopes to lead the way in publishing more

quantitative,meta-data based reviews of important environmental questions.” In the

final chapter of this thesis, I consider the implications of this meta-analysis for air

qualitypolicyandproposeseveral ideas for futurestudiesonthis importantresearch

topic.

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II.Areviewofairpollutionimpactsonavianspecies

OliviaV.Sanderfoot1andTraceyHolloway1,2

1.CenterforSustainabilityandtheGlobalEnvironment(SAGE),NelsonInstitutefor

EnvironmentalStudies,UniversityofWisconsin–Madison,Madison,WI53726

2.DepartmentofAtmosphericandOceanicSciences,UniversityofWisconsin–Madison,

Madison,WI53726

I.Introduction:

It is well established in the peer-reviewed literature that exposure to air

pollution causes adverse human health outcomes, including increased risk of

respiratorydisease,cardiovasculardisease,cancer,andmortality[Westetal.,2016,and

references therein]. Public health research dating back to the 1950s has established

linkagesbetweentheseadversehealthoutcomesandrespiratoryexposuretoambient

airpollutants, includingtroposphericozone(O3),aerosols(orparticulatematter,PM),

nitrogendioxide(NO2),sulfurdioxide(SO2),carbonmonoxide(CO),heavymetals(e.g.

lead, mercury), certain hydrocarbons, and other chemically and biologically active

speciespresent intheair.Beyondhumanhealth,researchsuggeststhatallecosystem

typesarevulnerabletotheeffectsofairpollution[Lovettetal.,2009],withmostwork

todatefocusedoncharacterizingtheimpactsofairpollutiononvegetationandaquatic

environments.Ozone, inparticular,hasbeenshowntoreduceratesofphotosynthesis

inplants[ReichandAmundson,1985],andtheacidificationoflakesresultingfromSO2

andNOx (NO2 + NO) emissions affects both species diversity and species richness in

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freshwatercommunities[BrönmarkandHansson,2002].

Todatefewstudieshaveexploredhowchemicalcharacteristicsoftheairaffect

non-human animal species, especially in wild populations. In fact, searching the

ThomsonReutersWebofScienceplatforminNovember2016(referredtohereafteras

WoS) for articles related to “‘air pollution’ and ‘humanhealth’” published since 1950

produced 2,388 results, while searching for articles related to “‘air pollution’ and

‘animals’” or “‘air pollution’ and ‘wild populations’” produced 658 and 3 results,

respectively.

Among non-human animal species, birds may be particularly vulnerable to

health-damaging air pollutants. The avian respiratory system, unlike themammalian

respiratorysystem,ischaracterizedbyunidirectionalairflow,athinblood-gasbarrier,

andcross-currentgasexchange,all featuresthatimprovetheefficiencyofrespiration.

Infact,birdsrespiremoreefficientlythananyothertypeofterrestrialvertebrate.Avian

species are thereforemore likely to be susceptible to high concentrations of reactive

gases and aerosols in the air than mammalian species, and so may serve as useful

indicators of air quality [Brown et al., 1997]. The literature on this topic is limited: a

WoS search for articles related to “‘air pollution’ and ‘birds’” and “‘air quality’ and

‘birds’”producedjust132and87results,respectively.Ofthearticlesfoundinthelatter

search,thetopthreewerefocusedontheeffectsofpoorairqualityonpoultry,noton

wildbirdpopulations.

Birdshavelongbeenrecognizedassentinelspeciesforenvironmentalchange.In

the early 20th century, caged canaries were brought down into coal mines to signal

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whencarbonmonoxideandmethaneconcentrationsintheminesreachedunsafelevels,

apracticewhichledtotheuseofthecolloquialphrase“canaryinthecoalmine”torefer

to early warning signs of future danger. Rachel Carson’s award-winning book Silent

Spring,publishedin1962,broughtattentiontothewidespreadimpactofpesticideand

insecticideapplicationsonsongbirds.Anumberofavianspecieshavebeenassessedfor

their value in the biomonitoring of heavy metals [Burger and Gochfeld, 1995, 1997;

Saldiva and Böhm, 1998; Dauwe et al., 2003; Manjula et al., 2015] as well as

polychlorinatedbiphenylsandotherorganiccontaminants[Arenaletal.,2004;Miniero

et al., 2008]. Chronic dietary exposure to heavy metals — including aluminum,

cadmium,mercury, and lead— has been shown to limit avian reproductive success

[Scheuhammer,1987],anddietaryexposuretodichlorodiphenyltrichloroethane(DDT)

—achemicalcommonlyusedinpesticidesandinsecticidesinthemid-20thcentury—

appears to affect calcium metabolism in avian species [Jefferies, 1969] and leads to

deathinsongbirds[Wursteretal.,1965;Hilletal.,1971].Ecologistshavealsoidentified

a number of responses to climate change in wild bird populations, including

phenologicalshiftsinthetimingofspringmigrationandalteredspeciescompositionof

overwintering bird communities [Jones et al., 2012; Princé and Zuckerberg, 2015]. A

WoSsearchforarticlesrelatedto“‘climatechange’and‘birds’”found3,507results,with

thetoppapercitednearly3,800times.

Birds could also serve as sentinel species for air quality, as they are found

globally, inbothurbanandruralareas,andmakeuseofmanydifferenthabitat types

[Brownetal.,1997;Baesseetal.,2015].Theirwideflightrangescouldbebeneficialin

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studyingandunderstandingthespatialdistributionofairpollutants[SaldivaandBöhm,

1998]. Here we present a summary of findings regarding avian responses to air

pollution, with an emphasis on inhalation exposure. Our focus on the respiratory

system ismotivated by the highmetabolic rates of birds and expansive literature on

humanhealthoutcomesassociatedwithinhalationexposuretoairpollutants.Belowwe

outlinestudymethods,discusskey findings,andhighlight theroleof futureresearch.

Key findings are divided into six sections: 1) respiratory distress and illness, 2)

impairedreproductivesuccess,3)increaseddetoxificationeffort,elevatedstresslevels,

and immunosuppression, 4) behavioral changes, 5) habitat degradation, and 6)

demographicresponses.Weaimtoprovidefoundationalknowledgeonavianresponses

to air pollution, and to support a broader research effort on air pollution impacts on

birds.

II.Methods:

An initial literature review was performed in January 2016 to gather peer-

reviewed studies on avian responses to reactive gases and aerosols. This literature

reviewwasperformedagain inNovember2016 to capturemore recentpublications.

Searches were conducted using Thomson ReutersWeb of Science platform, accessed

throughtheUniversityofWisconsinlibrarysystem.Keysearchtermsincluded:

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airpollution airquality ozone(O3)

smog particulatematter(PM) PM2.5

PM10 particulates aerosols

haze nitrogendioxide(NO2) nitricoxide(NO)

nitrogenoxides(NOx) sulfurdioxide(SO2) carbonmonoxide(CO)

smoke soot metals

lead DDT mercury

Each term was paired with the words “birds” and “avian” in various combinations,

utilizing both the “title” and “topic” fields in the basic search function. Over 200

searcheswereperformed.Searchresultswererefinedsothatonlyarticlesorreviews

publishedinEnglishsince1950wereincludedinthelistsofarticlesgeneratedbyWeb

ofScience.Additionalreferencescitedinthesestudiesorcitingthesestudieswerealso

considered.Studiesexaminingpoultry-keepingsystemswereexcluded,asthesestudies

did not provide insight into how exposure to outdoor air pollution may affect wild

birds. However, laboratory studies designed to investigate the effects of inhalation

exposure to ambient air pollutants in birds were included, although some of these

studiesdidusedomesticatedspecies,suchaschickens,asstudyspecimens.

III.KeyFindings:

To date, three general approaches have been used to characterize avian

responsestorespiratoryexposuretoairpollution.Researchershaveexposedbirdsto

17

gaseous mixtures or specific concentrations of gases or aerosols in laboratory

experiments,anapproachwhichwerefertoas“controlledexposure.”Birdshavealso

beenmonitoredinnaturalhabitatsorcaughtinthewildforfurtherstudy,capturingin

situ exposure. Finally, we include case studies relevant to avian sensitivity to air

pollution. We report key findings below and note which of these three general

approaches(controlledexposure,insituexposure,orcasestudy)wasusedtoelucidate

thesefindings.

III.1Respiratorydistressandillness

Studieshave shown thatboth controlledand in situ exposure to airpollutants

cause morphological and physiological changes in the avian respiratory system.

Exposuretoairpollutionclearlycausesrespiratorydistressinbirdsandincreasestheir

susceptibilitytorespiratoryinfection.

A.Controlledexposure

Birds, like other vertebrate species, are susceptible to carbon monoxide

poisoning. Carbon monoxide (CO) is a product resulting from the incomplete

combustion of fossil fuels and biomass. Exposure to CO results in the formation of

carboxyhemoglobin(HbCO),limitingthecapacityofhemoglobintotransportoxygento

tissues throughout the body [Baker and Tumasonis, 1972]. Treatment for carbon

monoxide poisoning in birds typically includes provision of supplemental oxygen,

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whichreducesthehalf-lifeofHbCO[VerstappenandDorrestein,2005;Simone-Freilicher,

2008].Theaviancarbonmonoxidepoisoningmechanismwasexploredina1974study

[Tschorn and Fedde, 1974], which suggested that CO may depress inhibitory

interneurons in the central nervous system, resulting in the abnormal breathing

associatedwithCOpoisoningobservedinthestudyspecimens.

Ozone(O3)alsoappearstoposeahealthrisktobirdsbycausingmorphological

andphysiologicalchangesintheavianrespiratorysystem[Romboutetal.,1991;Cuesta

et al., 2005]. Ozone in near-surface environments is chemically formed through

reactionsinvolvingnitrogenoxides(NOx)andvolatileorganiccompounds(VOCs)inthe

presence of sunlight. In a study byRombout et al. [1991], adult,male Japanese quail

(Coturnixcoturnix japonica)wereexposedtovaryingO3concentrations,andexposure

to0.50partspermillion(ppm)O3resulted inthereductionandshorteningofcilia in

the trachea and bronchi (Figure 1), hypertrophy in the secondary bronchi,

hemorrhaging and inflammation in the capillary network, necrosis of epithelial cells

liningtheaircapillaries,andsymptomsofpulmonaryedema.Quailexposedtohigher

concentrations of O3 (1.50 ppm) were more severely affected. Individuals in this

treatment group showed a dramatic reduction in the number of ciliated cells in the

trachea and bronchi. Hemorrhaging and changes in the structure of the atrial

epithelium resulted in the closing of the atrial space, reducing air flow and possibly

contributing to the labored breathing exhibited by this treatment group during the

experiment.Onlythebirdsinthistreatmentgrouppresentedastatisticallysignificant

increase in lung weight and lactate dehydrogenase (LDH) activity [Rombout et al.,

19

1991],oftenconsideredaresponsetoinjuryorstress.Cuestaetal.[2005]alsofounda

statistically significant increase inexpressionofadrenomedullin-likeproteinbetween

pigeons (Columba livia domestica) exposed to high levels of O3 and a control group,

whichappearstobetheonlystudytodateonairpollutionimpactsonadrenomedullin-

likeimmunoreactivityinbirds,asignofrespiratorydistress.

Exposure to sulfur dioxide (SO2) may impair the avian immune response to

inhaledantigens,makingbirdsmoresusceptibletodisease[Wakabayashietal.,1977].

Sulfurdioxide is a gas that is emitted from the combustionof sulfur-containing fuels,

such as coal or petroleumoil. Results froma 1977 study show that exposure to SO2,

even at concentrations as low as 1.4 ppm, compromises the effectiveness of the

mucocilliarysysteminWhiteLeghornchickens,whichplaysacrucialrole inreducing

Figure 1: Standard electron microscopy (2000x) of the epithelium of a secondarybronchusina)aJapanesequailexposedto0.0ppmO3andb)aJapanesequailexposedto0.50ppmO3.Notethereductionandshorteningofcilia inthe individualexposedtoO3.ImageryfromRomboutetal.,1991.

20

the incidence of respiratory disease by clearing contaminants, including infectious

agents,fromtheairway[Wakabayashietal.,1977].FeddeandKuhlmann[1979]found

thatWhite Leghorn chickens exposed tomuch higher concentrations of SO2 (>1,000

ppm)exhibitedsignsofrespiratorydistress,andthemajorityofthoseexposedtoSO2at

aconcentrationof5,000ppmdied.

Multiple studies have shown that birds are also likely affected by elevated

concentrationsofparticlepollution[Sterner,1993a,1993b;Telletal.,2006;Telletal.,

2012]. Particulate matter (PM) includes any liquid or solid suspended in the air,

typically classified by size such that PM2.5 represents PM less than 2.5 microns in

diameterandPM10representsPMlessthan10micronsindiameter.Health-relevantPM

can include directly emitted particles, such aswind-blown dust or smoke from fires,

and/or chemically formed particles, such as sulfate and nitrate aerosols. Tell et al.

[2006]examinedtheuseofanaerosolizedfluorescentmicrospheretechniqueoftheir

own design to study particle deposition in adult domestic pigeons. Their results

demonstrated that smaller particles (those less than threemicrons in diameter) are

more likely tobewelldispersed in theavian respiratory system than largerparticles

(those greater than sixmicrons in diameter),which aremore likely to remain in the

upperairway[Telletal.,2006].Telletal.[2012]confirmedthattheextentofdeposition

increases with exposure time [Tell et al., 2012]. Understanding how particles are

deposited in therespiratorysystemandcleared fromtheairwaywillbe important in

differentiatingresponsestoacuteandchronicexposuretoairpollution.

21

B.Insituexposure

A number of studies have usedmicroscopic imagery and chemical analysis to

comparethemorphologyandbiochemistryoflungtissuefrombirdscapturedinurban

andruralareasinordertodiscernphysiologicaldifferencesthatarelikelyattributable

tourbanairpollution[LorzandLópez,1997;Cuestaetal.,2005;Sicoloetal.,2009,Ejaz

etal.,2014;SteynandMaina,2015].Birdsexposedtourbanairpollutionmayexhibita

buildup of cellular andmineral debris leading to lung parenchymal consolidation or

alveolar consolidation, a characteristic condition of pneumonia [Ejaz et al., 2014].

Researchers inSpainhaveshowedthaturbanairpollutionmayalso impact theavian

pulmonarysurfactantsystem[LorzandLópez,1997;Cuestaetal.,2005].

Pulmonarysurfactant isa lipoproteincomplex,andthesecretionofpulmonary

surfactant helps reduce tension in the respiratory system, thus preventing the lungs

from collapsing during expiration [Lorz and López, 1997; Cuesta et al., 2005].

Pulmonary surfactant also plays an important role in the defensemechanisms of the

lung.Thelipidsandproteinsthatmakeupthesurfactantarestoredinlamellarbodies

— dense structures found in the cytoplasm of type II pneumocytes [Lorz and López,

1997].Ina1997study,pigeonswerecapturedandstudiedtodetermineifthenumber

of lamellar bodies in lung tissue differed between birds living in rural habitats

(collectedfromafarminthevillageofGuadalajara)andurbanhabitats(capturedinthe

cityofMadrid). Ifmorepulmonarysurfactant isexcretedbytypeIIpneumocytes, the

numberoflamellarbodieswouldbeexpectedtodecline.Theresearchersfounda33%

reductioninthequantityoflamellarbodiesinurbanbirdsascomparedtoruralbirds,

22

indicative of elevated secretion of pulmonary surfactant and, therefore, respiratory

distress[LorzandLópez,1997].

Phosphatidylcholine is an important component of pulmonary surfactant. In

mammals,secretionofphosphatidylcholineisstimulatedbyadrenomedullin,apeptide

hormone. Elevated concentrations of adrenomedullin have been documented in the

pathologies for several mammalian respiratory diseases, including asthma. A 2005

study demonstrated the presence of an adrenomedullin-like protein in the avian

respiratory system [Cuesta et al., 2005]. In this study, pigeons were captured and

observed to determine if expression of this adrenomedullin-like protein differed

betweenbirdslivinginruralandurbanhabitats.Resultsshowedthatexpressionofthe

adrenomedullin-likeproteinwashigherinbirdsexposedtochronicurbanairpollution,

evidenceofgreaterstimulationofphosphatidylcholinesecretionandelevatedlevelsof

pulmonarysurfactant.Thisfindingsuggeststhatpigeonsexposedtourbanairpollution

sufferfromrespiratorydistress[Cuestaetal.,2005].

In Johannesburg, South Africa, Steyn and Maina [2015] found that house

sparrows(Passerdomesticus),CapeGlossyStarlings(Lamprotornisnitens),andlaughing

doves(Streptopeliasenegalensis)exposedtourbanairpollutionhadagreaternumber

offreesurfacemacrophagesinthelungsthanthosefromruralareas.Macrophagesplay

an important role in immune response by destroying or sequestering foreign

particulates andaerosols.Thedoves exhibited thegreatestnumbersofmacrophages,

followed by the starlings,while the sparrows had the least [Steyn andMaina, 2015].

TheseresultsalignwithobservationsbyLorzandLópez[1997],whichdemonstrated

23

thatdomesticpigeonsfromurbanareashada

greaternumberofmacrophagesinlungtissue

thanthosefromruralsites(Figure2).

A series of studies conducted at the

UniversityofBarcelonainthe1990ssoughtto

study changes in the tracheal epithelium of

birds exposed to SO2, NOx, and particulate

emissions from coal-fired power plants in

northeasternSpain[Llacunaetal.,1993,1996;

Gorriz et al., 1994]. Goldfinches (Carduelis

carduelis)exposedtoemissionsfromapower

plant showed greater mucus production, a

shortening of the cilia in the epithelial cells

lining the trachea, and an increase in the

numberandsizeofsecretoryvesicles.Thesechanges to the trachealepitheliumwere

lesspronouncedinrockbuntings(Emberizacia)andcoaltits(Parusmajor),whichthe

authors suggest may be attributable to the study design which prevented the

goldfinches,trappedincages,frommovingawayfromthesourceofemissions[Llacuna

etal., 1993].A related study foundabnormalorientationof the cilia in rockbuntings

and great tits (Parus major) exposed to emissions from a power plant, possibly

resulting from increased production of mucus, but not in goldfinches or blackbirds

Figure 2: Images of atrial lung tissueharvested from A) rural pigeons and B)urban pigeons produced using lightmicroscopy (x240). Note the clustering ofmacrophages near the atrial space in thebirds exposed to higher levels of urbanpollution. Imagery from Lorz and López,1997.

24

(Turdusmerula).Normalorientationofciliahelpstoclearparticlesfromtheairwayand

supportairflow[Gorrizetal.,1994].

C.Casestudies

Smoke is known to cause both thermal and chemical damage to avian lung

tissue,aswellas increaseabird’ssusceptibility torespiratory infection [Morrisetal.,

1986; Verstappen and Dorrestein, 2005; Simone-Freilicher, 2008; Kinne et al., 2010].

Morris et al. [1986] linked exposure to smoke with an outbreak of the contagious

respiratory disease laryngotracheitis in a flock of chickens, as well as a short-term

increase in mortality and a short-term decline in egg production. Verstappen and

Dorrestein [2005] documented the effects of indoor smoke exposure in blue-fronted

Amazon parrots (Amazona aestiva aestiva) kept in an aviary.Within hours following

exposure, the parrots developed dyspnea, pulmonary edema, and minor damage to

theirlungtissue[VerstappenandDorrestein,2005].Afemalerubyblue-headedpionus

parrot (Pionus menstruus rubrigularis) showed similar symptoms, as well as weight

loss,secondaryrespiratoryinfections,anddecreasedactivityafterrepeatedincidences

of indoor smoke exposure [Simone-Freilicher, 2008]. Kinne et al. [2010] suggest that

carbon monoxide poisoning is usually the cause of death in birds following smoke

exposure,butthatmycoticairsacculitis,pneumonia,andadditionalresponsestoother

compoundspresentinsmokemaycontinuefordaysorweeks.

Smoke inhalation may also compromise the ability of birds to escape during

wildfire events. While the eggs and chicks of ground-nesting species and waterfowl

25

undergoing molt are thought to be most susceptible to fire events, monitoring of

wadingbird species in theEverglades showed thatevenadult, flightedbirdsmaydie

during wildfires. A fire in April of 1999 caused the death of 50 adult white ibises

(Eudocimusalbus)foundonacattailisland.Theibiseslikelybecametrappedduetothe

presenceofthicksmoke[Epanchinetal.,2002].

III.2Impairedreproductivesuccess

Inadditiontorespiratorydistressandillness,exposuretoairpollutantsisalso

correlatedwith impaired reproductive success. Reproductive success is ameasure of

how effective a parent generation is in passing their genes onto subsequent

generations, and as such is often assessed by determining not only the number of

offspringproducedbutalsothefitnessofthoseoffspring.

A.Controlledexposure

While previous studies had established that embryos do respond to their

gaseous environments, a 1972 study provided further insight into how carbon

monoxide (CO) diffusion through the eggshell and inner and outer shell membranes

mayaffectthegrowthanddevelopmentofbirdembryos.BakerandTumasonis[1972]

foundthatthehatchabilityandviabilityofWhiteLeghornchickeneggsdeclinedasCO

levels increased (Figure 3), and 425 ppm CO was determined to be the critical

concentrationfortheseparameters.Vasodilationofbloodvesselswasnotedinembryos

26

exposed to CO concentrations above 425 ppm. Lactate dehydrogenase (LDH)

concentrations in the blood serum also increased in embryos exposed to CO at the

criticallevel,acommonindicatorofinjuryorstress.Exposuretohigherconcentrations

ofCOalsoresulted in increasedmortality,andexposure to1,000ppmCOresulted in

100% mortality. Chicks that hatched following exposure to CO were smaller than

control chicks and showed physical abnormalities if exposed during the embryonic

stagetoCOconcentrationsabove425ppm[TschornandFedde,1974].Furthermore,the

resultsofthisstudyshowthatwhilethe

eggshellandinnerandoutermembranes

ofWhite Leghorn chicken eggs limit the

diffusionofCO,theabilityoftheselayers

to protect embryos from CO poisoning

appears to degrade with time. Both the

age of the egg and the shell condition

therefore affect the permeability of an

embryonated egg [Tschorn and Fedde,

1974]. If the eggshell and inner and outer membranes of eggs provide only limited

protectionagainstelevatedconcentrationsofCO,itisplausiblethatotheratmospheric

contaminantsmightalsobeabletodiffusethroughtheegg’slayeredsurfaceandaffect

birdembryos.

Figure 3: Plot fromTschorn and Fedde, 1974showing percent hatchability as a function ofcarbon monoxide concentration. As carbonmonoxide concentrations increase,hatchabilitydeclines.

27

B.Insituexposure

RecentstudiesinEasternEurope[EevaandLehikoinen,1995;Belskiietal.,2005]

have examined the reproductive successof birds livingwithin airpollutiongradients

resultingfromtheoperationofcoppersmelters,aswellasthefitnessoftheiroffspring.

In a study conducted in the 1990s, researchers observed pied flycatchers (Ficedula

hypoleuca), a migratory species, and great tits, a resident species, at nest boxes

constructed at 14 study sites located within an elliptical air pollution gradient

surroundingacopper-smeltercomplexinHarjavalta,Finland.Theresearchteamused

theheavymetal contentof thesoil at this industrial siteasaproxymeasurement for

total air pollution exposure associatedwith operation of the smelter, known to emit

sulfur dioxide (SO2) and heavy metals (copper, lead, and nickel). The heavy metal

content decreased exponentially with distance from the smelter. The researchers

wanted to determine whether or not the reproductive success of these birds was

impaired at study sites closer to the copper smelter due to the production of low-

quality eggs. This hypothesiswas based on previouswork showing that exposure to

heavymetals and acidifying compoundsmight impair avian reproductive success by

affecting calcium metabolism and reducing the availability of calcium in local food

resources, all ofwhich results in eggswith thinner shells [Scheuhammer, 1991;Eeva

andLehikoinen,1995].

Boththepiedflycatchersandthegreattitsoccupyingnestboxesatsitesclosest

to the smelter laid fewer eggs, but the pied flycatcher showed an overall greater

vulnerability to exposure to industrial air pollution than did the great tit. Hatching

28

successofpiedflycatcherswasalsodramaticallyreducedatsitesclosesttothecomplex

[Eeva and Lehikoinen, 1995]. Production of low-quality eggs did appear to drive the

impairment in reproductive success at this industrial site. The eggs of the pied

flycatcherswere8%smallerbyvolumewith17%thinnershellsatsitesclosesttothe

factory complex as compared to sites located 10 kilometers away, and microscopy

revealedthatthesurfaceoftheeggscollectedfromsitesnearestthefactoryweremore

rough and porous [Eeva and Lehikoinen, 1995]. The foraging strategy of the pied

flycatcherwas suggested to account for its greater sensitivity to industrial pollutants

[EevaandLehikoinen,1995].Laterworkbythisgroupalsofoundthatpiedflycatchers,

unlike great tits, exhibit stress responses suggestive of a direct toxic effect in the

vicinityofpointsourcesofindustrialairpollution[Eevaetal.,2000].

TheimpactsofheavymetalandSO2emissionsfromacopper-smeltingplanton

piedflycatcherswerealsostudiedinRussiabyBelskiietal.[2000,2005].Resultsfrom

thesestudies indicate thatreproductivesuccess is impairedatnestingsitesclosest to

point sources of industrial emissions [Belskii et al., 2000, 2005]. At nests at least 15

kilometers fromthecoppersmelter, clutchsize increasedbya factorof1.5,andboth

thenumberofhatchedchicksandthenumberoffledglingspernestdoubledcompared

tonestslocatedinthenearbyvicinityoftheplant.Atthosesitesclosesttotheplant,egg

mortalitywasalso3.5timesgreater[Belskiietal.,2005].Inaddition,theresultsofthis

studyshowedthattheproportionofnestlingsinfestedbyparasiticflylarvaeaswellas

the severity of infestation (as measured by the average number of fly larvae per

infested chick) increased with decreasing distance to the plant. Higher liver indices,

29

reducedhemoglobinconcentrations,andgreaterproportionsofimmatureerythrocytes

(redbloodcells)innestlingswerelinkedtoboththedirecttoxiceffectofairpollutants

and greater incidence and severity of parasitic infestation, leading the authors to

suggest that exposure to industrial air pollution leads to a general weakening in

nestlings, rendering them more susceptible to infestation and subsequent infection

[Belskiietal.,2005].

Fortunately, Eeva and Lehikoinen [2000, 2015] show that reducing industrial

emissionsfrompointsourcesimprovesthereproductivesuccessofbirdslivingnearby.

Asemissionsatthecopper-smelterinHarjavaltadeclined,boththeclutchsizeandthe

number of fledglings per nest increased [Eeva and Lehikoinen, 2000, 2015]. These

findingssupportpreviousworkinEasternEuropelinkingexposuretoairpollutionwith

impairedreproductivesuccessinbirds.

III.3Increaseddetoxificationeffort,elevatedstresslevels,andimmunosuppression

Laboratory and field studies have also determined that exposure to air

pollutantsresults in increaseddetoxificationeffortandelevatedstress levels inbirds,

providing further evidence of the negative health impacts of air pollution on avian

species. This research also shows that the avian immune responsemay be impaired

following acute or chronic exposure to air pollution, giving added weight to the

previous discussion of how birds exposed to health-damaging air pollutants may be

30

more susceptible to respiratory disease (see section III.1 Respiratory distress and

illness).

A.Controlledexposure

Inhalation exposure to air pollution may increase the stress response and

detoxificationeffortinbirds[Cruz-Martinezetal.,2015b].Sulfurdioxide(SO2),nitrogen

dioxide (NO2), and volatile organic compounds (VOCs) are the major air pollutants

associatedwithoilsandsoperations,an importantpointsourceofairpollution.VOCs

are a class of chemicals that contain carbon and hydrogen, many of which are

associatedwithdirecthumanhealthimpacts,especiallycancer.Tostudyhowemissions

fromoilsandsoperationsmayimpactavifauna,researchersexposedJapanesequailand

American kestrels (Falco sparverius) to gaseous mixtures of SO2, NO2, and VOCs in

whole-bodyinhalationchambersandmeasuredresultingcorticosterone(CORT)and7-

ethoxyresorufin-O-dealkylase(EROD)concentrationsinbloodsamples.CORTactivityis

anindicatorofstress,whileERODactivityisoftenusedtosignalthebody’s increased

detoxificationeffort,especiallyofpolycyclicaromatichydrocarbons.

Japanesequailwererandomlyassignedtothreegroups:control(hydrocarbon-

free air), low exposure (0.5 ppm SO2, 0.2 ppm NO2, 0.6 ppm benzene, and 1 ppm

toluene),andhighexposure(50ppmSO2,20ppmNO2,60ppmbenzene,and100ppm

toluene).Quailwereexposedtothesegaseousmixtures for1.5hourseachdayfor20

days. American kestrels were separated into a control and experimental group and

exposedtohydrocarbon-freeairand5.6ppmSO2,2ppmNO2,0.6ppmbenzene,and1

31

ppm toluene, respectively, for 1.4 hours each day for 18 days [Cruz-Martinez et al.,

2015b].

CORT activity increased and EROD activity doubled in the kestrels exposed to

experimental conditions compared to those exposed to hydrocarbon-free air, though

these resultswerenot statistically significant. CORTactivity increased in thequail in

the lowexposuregroupas compared to thecontrolandhighexposuregroups.These

resultsarecharacteristicofahormeticresponsetotoxins,inwhichlowdosesoftoxins

prompt a response that is inhibited at higher doses. There was no statistically

significantdifferenceinthedetoxificationeffortamongstquailinexposuretrials.Quail,

like other species in the Galliformes family, may bemore resistant than other avian

species to toxic gases [Cruz-Martinez et al., 2015b]. Though the results of this study

demonstrate a specific physiological response to elevated levels of common

atmosphericcontaminants, it isnotpossibleto isolatetheresponsetoanyof the four

distinct compounds the quail and kestrels were exposed to in these trials [Cruz-

Martinez et al., 2015b]. Fernie et. al [2016] also show that exposure to a gaseous

mixture of benzene, toluene, NO2, and SO2 might up regulate function of the

hypothalamus-pituitary-thyroid axis in kestrels, which could affect the hormonal

control of many key activities, including metabolism and reproduction. Additional

research is needed to further characterize the role of the thyroid gland in the stress

responseanddetoxificationeffortinbirdsfollowingexposuretoairpollution[Fernieet

al.,2016].

32

According to a study conducted in 2005 and 2006, exposure to VOCs may

compromisetheavianimmunesystem[Olsgardetal.,2008].In2005,Americankestrels

caught in the wild near Prince Albert, Saskatchewan, Alberta were divided into two

groups:control(breathinggradeair)andhighexposure(10ppmbenzeneand80ppm

toluene).Thekestrelswereexposedto thesegaseousmixtures foronehoureachday

for 28 days. In 2006, captive kestrels were assigned to one of three groups: control

(breathinggradeair),lowexposure(0.1ppmbenzeneand0.8ppmtoluene),andhigh

exposure(10ppmbenzeneand80ppmtoluene).Thekestrelswereexposedto these

gaseousmixturesfor1.5hourseachdayfor27days.Theresultsofthisstudyindicate

thatwhilethehumoralimmuneresponsemightnotbeimpactedbyinhalationexposure

to VOCs, the cell-mediated immune response is suppressed in kestrels exposed to

gaseousmixtures of benzene and toluene, at both the low dose and high dose levels

[Olsgardetal.,2008].Thesefindingssupportearlierstudiesindicatingthatexposureto

airpollutionmayincreasetheriskofrespiratoryinfectioninbirds.

B.Insituexposure

Exposuretoindustrialairpollutionhasbeenlinkedtogenotoxiceffectsinbirds

[Baesse et al., 2015], including higher rates of heritable geneticmutations [Yauk and

Quinn, 1996;Yauketal., 2000;Kingetal., 2014]. Industrial emissionshavealsobeen

associatedwith the bioaccumulation of heavymetals in the tissues of vital organs of

birdsthatoccupyhabitatsnearpointsourcesofairpollution[Llacunaetal.,1995;Hui,

2002;BurgerandGochfeld,2000;Lovettetal.,2009;Berglundetal.,2011].Theuptake

33

ofleadinparticularhasbeenshowntoaffectthebehavioraldevelopmentofchicksand

negatively impact their growth and survival rates [Burger and Gochfeld, 2000],while

avian exposure to mercury is correlated with neurological damage and impaired

reproductivesuccess[Scheuhammer,1991;Lovettetal.,2009].

A1996studyfocusedoncharacterizinghematologicalchangesingreattits,rock

buntings,andblackbirdsexposedtoemissionsfrompowerplants[Llacunaetal.,1996].

The study found that exposure to industrial emissions from a coal-fired power plant

decreased erythrocyte counts by 11.4% in great tits and by 16.2% in rock buntings.

Erythrocytes were also noticeably larger. This is likely due to the immune system’s

targeteddestructionofdefectiveerythrocytesandrapidproductionofnew, immature

erythrocytes,whicharebigger.Blackbirdsalso showedstatistically significantweight

lossandgreaterconcentrationsoftransaminases,asymptomindicativeofliverdisease.

Plasma samples from rock buntings captured near the power plant also showed a

decreaseinbeta-globulins,indicativeofinfection[Llacunaetal.,1996].

Industrial air pollution associated with oil sands activity may also negatively

affect the health of avifauna. A recent study by Cruz-Martinez et al. studied

detoxification effort and immune response in tree swallow nestlings (Tachycineta

bicolor)atsitesnearoilsandsoperations[2015a].Exposuretoelevatedconcentrations

of ambient air pollutants associated with oil sands activity was linked to increased

detoxification effort and suppression of cell-mediated immunity [Cruz-Martinez et al.,

2015a].

34

Exposure to high levels of urban air pollution was found to increase

concentrationsofelementaltoxinsinthetissuesofvitalorgansinwildbirds,including

starlings,owls,crows,andpigeons,capturedinLahore,Pakistan.Themagnitudeofthis

increase varied by tissue type and species. Researchers also noted symptoms of

degenerationandnecrosisoflivertissueincapturedbirds[Ejazetal.,2014].

Findings from a study of pigeons in the city of Milan, Italy indicate that

porphyrinconcentrationsinbirdexcrementandbloodmethemoglobinlevelsmayserve

as useful bioindicators of urban air pollution. Results from this study showed that

excreta collected from the pigeons exposed to urban air pollution had significantly

higher total porphyrin concentrations and greater proportions of protoporphyrins

compared to that collected from control pigeons. Methemoglobin levels were also

higherinbloodsamplescollectedfromtheurbanbirds.Thiswasoneofthefewstudies

we discuss in our review that includedmeasurements of ambient air quality, which

allowedtheresearcherstolinkincreasedprotoporphyrinconcentrationsinexcretato

elevated concentrations of polycyclic aromatic hydrocarbons and higher blood

methemoglobin levels to elevated concentrations of ozone and benzene [Sicolo et al.,

2009].

35

III.4Behavioralchanges

Few studies have assessed how exposure to air pollutants may alter bird

behavior, but existing research suggests that many different behaviors could be

affected,fromspontaneousactivitytohoming.

A.Controlledexposure

Avian exposure to phosphoric acids aerosolsmay result in changes in activity

andweight loss [Sterner, 1993a, 1993b]. A series of studies conducted by Sterner in

1993wasdesignedtodetermineifacuteexposuretophosphoricacidsaerosolsaffected

spontaneous activity such as walking and preening in rock doves (Columba livia).

Twenty-fourrockdoves(11malesand13females)wereexposedtophosphoricacids

aerosols at concentrations of 0.0, 1.0, and 4.0 mg/L for 80 min/day for two days.

Preening and ambulatory activitywere found to significantlydecline in the4.0mg/L

group following the firstexposure [Sterner,1993a].Sterner’s studiesalsodetermined

that rockdovesexposed toconcentrationsof1.0mg/Land4.0mg/Lexhibit reduced

water intake, food intake, and body weight as compared to control groups, with

recoverydependentonbothconcentrationandsex(Figure4)[Sterner,1993b].

36

B.Insituexposure

A recent study also established a connection between behavioral changes and

exposure to particulate pollution in cities. It is possible that high concentrations of

particulatematterresultinginthehazeseeninmetropolitancentersmaymotivatecity

pigeonstohomefaster.Furtherstudyisneededtodetermineifthischangeinbehavior

isseeninothercitiesorasaresultofexposuretodifferenttypesofairpollutants[Liet

al.,2016].

III.5Habitatdegradation

Industrial emissions often include nitrogen oxides (NOx), sulfur dioxide (SO2),

andheavymetals.EmittedNOxand/orSO2react intheatmospheretoformnitricand

sulfuricacid,whichwhendepositedinwetordryformcontributestoaciddeposition

(commonly referred toas “acid rain”) and soil acidification.Aciddepositionhasbeen

Figure 4: Plot showingmean food intake by rock doves in grams during the pre-exposure (2days), exposure (2days), andpost-exposure (6days)periods. The lines represent results fromdifferenttreatmentgroups(dotted line:0.0mg/L,dashed lined:1.0mg/L,solid line:4.0mg/L).Note that food intake declines in each treatment group, but drops most significantly in birdsexposed to thehighest levelofphosphoric acidsaerosols.Recovery in thepost-exposurephasedependsonconcentration[Sterner,1993b].

37

hypothesized to contribute to the bioaccumulation of heavy metals in birds

[Scheuhammer, 1991; Nybø et al., 1996], possibly by increasing the solubility of

elements such as aluminum [Scanes and McNabb, 2003]. Exposure to acid rain also

affects calcium and phosphorus metabolism, production of stress hormones, food

intake, growth rate, and reproductive success [Scanes and McNabb, 2003]. Acid

depositionandheavymetaluptakeofsoilsnearpointsourcesof industrialemissions

oftenaffectsthecompositionoftheplantandinvertebratecommunitiesonwhichbirds

dependfortheirfoodsupply[Eevaetal.,1998,2003;Costaetal.,2011].Changesinthe

chemicalenvironmentmaypromoteecologicalshiftsthatincreasefoodavailabilityfor

some species. For example, great titsmay have greater reproductive success at sites

near point sources of emissions associatedwith the pulp and paper industry due to

higher abundance of caterpillars— a key food resource for this species— in these

areas[Costaetal.,2011,2014].However,otheravianspeciesmaysufferifairpollution

reducesthequantityorqualityoffoodresources[Eevaetal.,2003].

Changes in food supply may also result in a decrease in the availability of

pigment-bearing foods, which in turn could indirectly affect reproductive success by

reducingthevibrancyofabird’splumage.Fadedplumageisadisadvantageformales,

as more vibrant, colorful plumage appears to be a sign of good physical condition,

rendering males more attractive to potential female mates [Eeva et al., 1998]. Food

intakemayalsobeaffectedbybehavioralchanges that limit foraging time.Birdsmay

spendlesstimeforagingiftreecanopiesthinasaresultofairpollution,makingbirds

moresusceptibletopredators[Brotonsetal.,1998].Changesinforeststructureorthe

38

compositionoflocalhabitatmayalsoaffecttheprevalenceofectoparasites,whichcould

affectthehealthofbothnestlingsandadultbirds[EevaandKlemola,2013].

III.6Demographicresponses

Researchsuggeststhatavianexposuretoindustrialairpollutionmayalsohave

demographic consequences. Several studies have linked declines in bird population

density [Flousek,1989;EevaandLehikoinen,1998;SahaandPadhy,2011;Eevaetal.,

2012;Belskii andBelskaya, 2013;Alaya-Ltifi andSelmi, 2014], speciesdiversity [Saha

and Padhy, 2011;Eeva et al., 2012;Belskii and Belskaya, 2013;Alaya-Ltifi and Selmi,

2014],andspeciesrichness[BelskiiandLyakhov,2003;BelskiiandBelskaya,2013] to

industrialairpollutiongradients(Figure5).Researcherspointoutthatchangesinthe

structure and composition of soils and vegetation resulting from air pollution may

affect a number of variables important to the life histories of the birds studied,

includingfoodsupplyandtheavailabilityofnestingsites.Noneofthesestudiescausally

linkedinhalationexposuretoindustrialairpollutantstochangesinpopulationdensity,

speciesdiversity,orspeciesrichness.Withinanairpollutiongradient, it isdifficult to

determine how much of the variation in these metrics is due to direct exposure to

airborne toxins and howmuch is due to other abiotic and biotic changes associated

with industrialpollution in the local environment [Belskii andBelskaya., 2013].Noise

pollutionmayalsobeaconfoundingvariableinassessingtheimpactsofindustrialair

pollutiononbirds,asnoisepollutionoftenincreaseswithproximitytoindustrialsites

[SahaandPadhy,2011].

39

Airpollutionmayalsoindirectly impactthecompositionofaviancommunities.

Damagecausedbyairpollutiontotreesaltersthestructureofforestecosystems.While

somebirdsmaybeable tocolonize thesehabitats,othersmaymakeuseofecological

niches thatareno longeravailablewithin that landscape.Over time, thismaychange

thecommunitycompositionofforestsexposedtoindustrialairpollution[Capek,1991;

Capek et al., 1998;Eeva et al., 2002;Belskii and Lyakhov, 2003;Belskii and Belskaya,

2013]. For example, point counts of bird observations in an air pollution gradient

resulting fromindustrialemissions fromtheKarabashCopperSmelter inChelyabinsk

Oblastshowedthattheproportionofcanopy-nestingandground-nestingspeciesinthe

area increased along the gradient while the proportion of hole-nesting species

decreased[BelskiiandBelskaya,2013].

Figure5:Aschematicofanindustrialairpollutiongradient.Thestarrepresentsanindustrialsite.The

concentriccirclessurroundingthestarareofincreasinglylightercolor,illustratinghowairpollutionand

uptakeofheavymetalsby soils andvegetationdecreaseswithdistance froman industrial site.Asone

movesalong thisgradient (in thedirection indicatedby thedottedarrow),populationdensity, species

diversity,andspeciesrichnessincrease.

40

IV.Discussion:

Thisreviewfindsclearevidencethatbirdsareaffectedbyexposuretoarangeof

reactivegasesandparticlesintheair,includingairpollutantswithestablishedadverse

impactsonhumanhealth.Avianresponsestoairpollutionincluderespiratorydistress

and illness, impaired reproductive success, increased detoxification effort, elevated

stress levels, immunosuppression, and behavioral changes. Key studies elucidating

these responsesare listed inTable1, andamapshowing locationsofwherebirds in

thesestudieswereexposedtoairpollutioninsituisincludedinFigure6.Airpollution

may also reduce population density, species diversity, and species richness in bird

communities. These demographic consequences are a result of both the direct, toxic

effectofexposuretoairpollutionaswellashabitatdegradationresultingfrompoorair

quality.Althoughavailable evidence consistently suggests airpollution impactsbirds,

thetotalnumberofstudiesislimited,andimportantgapsremain.

41

Figure6:Amapofthelocationswherebirdswereexposedtoairpollutioninsituinthestudieslistedin

Table1.

42

Table1:Thistableliststhe19studiesweidentifyaskeyincharacterizingindividualavianresponsesto

air pollution, including respiratory distress and illness, impaired reproductive success, increased

detoxification effort, elevated stress levels, immunosuppression, and behavioral changes. Entries are

categorizedbyboththetypeofresponseexploredandthetypeofexposure(controlledorinsitu)study

specimensweresubjectedto.Amapshowingthelocationswherebirdsinthesestudieswereexposedto

airpollutioninsituisincludedinFigure6.AdditionalpapersreferencedinsectionIII.KeyFindingswere

excluded from this table to focus on demonstrating the range of physiological and morphological

Baker and Tumasonis, 1972 White Leghorn chickens

Tschorn and Fedde, 1974 White Leghorn chickens

Wakabayashi et al. , 1977 White Leghorn chickens

Rombout et al. , 1991 Japanese quail

Cuesta et al. , 2005 pigeons

Llacuna et al., 1993 goldfinches, rock buntings, and coal tits

Gorriz et al., 1994 goldfinches, rock buntings, coal tits, and blackbirds

Lorz and López, 1997 pigeons

Cuesta et al. , 2005 pigeons

Ejaz et al., 2014 starlings, owls, crows, and pigeons

Steyn and Maina , 2015 house sparrows, Cape Glossy Starlings, and laughing doves

Baker and Tumasonis, 1972 White Leghorn chickens

Tschorn and Fedde, 1974 White Leghorn chickens

Eeva and Lehikoinen, 1995 great tits, pied flycatchers

Belskii et al., 2005 pied flycatchers

Olsgard et al., 2008 American kestrels and Japanese quail

Cruz-Martinez et al., 2015b American kestrels

Llacuna et al., 1996 great tits, rock buntings, and blackbirds

Sicolo et al., 2009 pigeons

Ejaz et al., 2014 starlings, owls, crows, and pigeons

Cruz-Martinez et al., 2015a tree swallows

Behavioral changes: Study Species

Sterner , 1993a rock doves

Sterner , 1993b rock doves

In situ exposure

Controlled exposure

Controlled exposure

SpeciesStudyIncreased detoxification effort,

elevated stress levels, and immunosuppression:

Controlled exposure

SpeciesStudyImpaired reproductive success:

In situ exposure

Controlled exposure

SpeciesStudyRespiratory distress and illness:

In situ exposure

43

responsesdocumented in thepeer-reviewedarticlesdownloaded inouroriginal literature review(see

sectionII.Methods).

Researchershavedocumentedavianresponsestobothindustrialandurbanair

pollution by studying birds in air pollution gradients and by comparing the

characteristics of birds captured from industrial and urban areas to those from less

polluted sites. While some studies do include information about atmospheric

contaminants at study sites, many do not quantify exposure or nearby ambient

concentrations of specific chemicals. Quantitative measures of pollutants are rarely

usedtocharacterizethesensitivityofaresponsetospecificcontaminants.Rather,most

studyresultsreflectacomparisonbetweenbirdsofthesamespeciesfrommoreorless

pollutedsites.While thestatistical significanceof thesecomparativestudies indicates

that air pollution is affecting birds, additional confounding variables such as habitat

degradation and changes in diet may also contribute to the responses observed.

Without exposure estimates for individual contaminants, there is insufficient data to

quantifyairpollutionrisktowildbirdpopulations.

Themainchallengeincharacterizingbirds’exposuretospecificairpollutantsis

theavailabilityofambientairpollutionmeasurementsforcomparisonwithecological

and biological outcomes. Epidemiological studies of human health risk from air

pollution often rely on centrally located ambient monitors as a proxy for individual

exposure (e.g. the network of surface air monitors run by the U.S. Environmental

ProtectionAgency).Thesesurfacemonitorscouldalsosupportanalysisofriskstobirds,

with sufficient information on species habitat and/or migration patterns. However,

44

mostareasof theworlddonothaveground-basedairpollutionmonitors, and short-

termmeasurements canbedifficult, expensive, andof limited relevance to long-term

exposure (depending on the duration of themeasurements and the variability of the

pollutant). Two additional data sources from the atmospheric chemistry community

could supplement in situ chemical measurements for the benefit of ornithologists:

chemical transportmodels(CTMs)andsatellitedata.MostwidelyusedCTMsprovide

calculatedconcentrationsofthegasandparticulatepollutantsdiscussedinthisreview,

andmodelshavebeenusedtoestimatehumanandvegetationexposureintheabsence

of in situ measurements. CTMs take information on natural and anthropogenic

emissions, with a global example shown in Figure 7, and calculate ambient

concentrations based on chemical reactions and meteorological transport. Satellite

retrievals also offer promise for health- and ecosystem-relevant pollutants, including

nitrogendioxide, carbonmonoxide, andparticulatematter,withavailable globaldata

on a near daily basis going back as far as 1999, depending on the instrument.

Laboratory-based risk factors, discussed above, and ambient air pollution

concentrationsfrommeasurements,models,and/orsatellitedatacouldbecombinedto

estimatebirdhealthriskonalocal,regional,orglobalbasis.

45

Figure7:Mapshowingtotalanthropogenicemissionsofnitrogenoxides(NOx) in2008;NOxisemitted

byallcombustionprocesses,andthusservesasan indicatorofemissions fromall fuel types.Thismap

doesnotshowtheambientconcentrationsofpollutantsbirdsareexposedto,butratherhighlightswhere

anthropogenic air pollution would be expected to pose the greatest risk to bird communities. Map

created using ECCAD (Emissions of atmospheric Compounds & Compilation of Ancillary Data),

maintained by the GEIA (the Global Emissions InitiAtive) based on data included in the Emission

DatabaseforGlobalAtmosphericResearch(EDGAR).

While potentially informative, such integration of laboratory exposure studies

and ambient pollution estimateswould have limitations. Rombout et al. [1991] point

out that results from laboratory studies must be interpreted with caution, as these

studies often use inhalation chamber techniques, which require that birds are

stationaryduringexposure.Inthewild,birdswouldhavehighermetabolicrates,which

wouldpotentiallymagnifythenegativeeffectsofairpollutionontherespiratorysystem

[Rombout et al., 1991; Gorriz et al., 1994]. Sterner [1993a, 1993b] discusses how

restrictingbirdstocagesmayresultinbehavioralchangesthatarenotactuallydueto

concentrations of reactive gases and aerosols. He refers to this as the “chamber

confinement effect.” Finally, Llacuna et al. [1993] also point out that the results of

46

laboratory studies examining avian responses to exposure to a single pollutant are

important, though not sufficient, in characterizing the impacts of air pollution on

avifauna innaturalsettings,where theyareexposedtoacombinationofatmospheric

contaminantsofvaryingconcentrations.Someofthesesamelimitationsalreadyaffect

the characterization of air pollution risk to humans, including the challenge of

extrapolating laboratory studies to realworld conditions (e.g. toxicological results of

ratsandothernon-humanspecies),andisolatingtheeffectsofasinglepollutanthealth

riskwhenexposureoccurssimultaneouslytomultiplepollutants.

While physiological responses to exposure to air pollutants may serve as

examples of phenotypic plasticity, this is not discussed in the studies cited in this

review. The capacity for both phenotypic plasticity and adaptation in response to

increased concentrations of near-surface reactive gases and aerosols could inform

whichspeciesmaybeatagreaterlong-termrisktopollutionexposure.

Asweimprovethecharacterizationofairpollutionrisktobirds,itisimportant

to consider interaction of the chemicals in the air with other aspects of global

environmental change, including shifts in land use and climate change [Lovett et al.,

2009]. For example, urbanization affects both land use and air quality, and warmer

temperaturesassociatedwithclimatechangeaffectairpollutionemissions(e.g.smoke

fromwildfires) and chemical reactions in the atmosphere (e.g. production of ozone)

[JacobandWinner,2009].

Oftheroughly10,000speciesofbirdsknownworldwide,onlyafewhavebeen

studied to characterize avian responses to air pollution, and the animals used in

47

laboratoryexperimentsmaynotberepresentativeofthewildbirdspeciesmostatrisk

toairpollution.Futurestudiesshouldworktoidentifywhichspeciesacrosstheglobe

maybemost sensitive toairpollution,aswellashowresponses toairpollutionmay

changewithageandsex.Futureresearchonavianresponsestoairpollution,especially

of endangered species, could inform bird conservation programs and improve

managementofwildbirdpopulations.

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III.Conclusion

ImplicationsforAirQualityPolicy

ThesecondaryNationalAmbientAirQualityStandards(NAAQS)establishedby

the Environmental Protection Agency (EPA) are designed to protect public welfare,

including“damagetoanimals,crops,vegetation,andbuildings.”4However,ananalysis

ofwhetherornot thesesecondarystandardsareadequate inprotectingwildlife from

any negative effects associated with exposure to health-damaging air pollutants

remains out of reach, given the limited research to date on the impacts of poor air

qualityonnon-humanspecies.Tosupportfutureworkonthisimportantresearchtopic,

this thesis summarizeswhat is currently known about how birds are affected by air

pollution. Birds respiremore efficiently than any other type of terrestrial vertebrate

and are therefore likely more vulnerable than mammals, reptiles, or amphibians to

atmosphericcompoundswithknownrespiratoryeffects,suchasthoseregulatedbythe

EPA.

Birds are undoubtedly negatively impacted by exposure to air pollution

associated with both urban and industrial activity (see II. A review of air pollution

impacts on avian species). However, most field studies designed to assess avian

responsestoairpollutionfailtomeasureinsituexposure.Itisthereforeimpossibleto

knowifthebirdsobservedinthesestudieswereexposedtoambientconcentrationsof

atmospheric contaminants that exceed the secondary NAAQS or fall below these4https://www.epa.gov/criteria-air-pollutants/naaqs-table

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standards.Whilecontrolledexposurestudiesarefewinnumber,theydoprovidesome

insightastowhatlevelsofairpollutionmightposearisktobirds.

Whilethereisnosecondarystandardsetforcarbonmonoxide(CO),theEPAhas

establishedtwoprimaryNAAQSforCO;concentrationsofCOarenottoexceeda)a1-

houraverageof35partspermillion(ppm)orb)an8-houraverageof9ppmmorethan

onceayear.Birds,likemammals,areclearlysusceptibletoCOpoisoning,andbecause

theyarelikelymoresensitivetorespiratoryexposuretoreactivegasesandaerosols,it

ispossible that toprotectadultbirds thesecondaryNAAQSshouldbemorestringent

than the primary NAAQS. However, the hatchability and viability of chicken eggs

appears todecline ifexposed toambientconcentrationsofCOgreater than425ppm,

several times higher than the maximum concentration allowed by the EPA. The

secondaryNAAQS for COmight therefore be adequate in protecting birds during the

embryonicstage.

Laboratory studies also show that pigeons exhibit morphological and

physiological changes in the respiratory system following exposure to ozone (O3) at

concentrationsof50ppm.TheprimaryandsecondaryNAAQSsetbytheEPArequire

that the annual fourth-highest daily maximum 8-hour ambient O3 concentration,

averagedover3years,mustnotexceed70partsperbillion.Thesecondarystandardfor

O3 is therefore far lower than the O3 concentrations birds have been exposed to in

laboratorysettings;therefore,availabledataisinsufficienttodeterminewhetherornot

thesecondaryO3standardissufficientinprotectingbirds.

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Studiesalsoshowthatexposuretosulfurdioxide(SO2)atconcentrationsaslow

as1.4ppmmightimpairtheavianimmuneresponse.ThesecondaryNAAQSforSO2isa

3-houraverageconcentrationof0.5ppm,nottobeexceededmorethanonceeachyear.

The secondary standard for SO2 is therefore lower than the SO2 concentrationsbirds

have been exposed to in laboratory settings, and available data is insufficient to

determinewhetherornot the secondary SO2 standard is sufficient to reduce risks to

avian species. Controlled exposure studies have also examined avian responses to

gaseous mixtures of SO2, nitrogen dioxide (NO2), and volatile organic compounds,

includingbenzeneandtoluene,butitisimpossibletoknowfromthesestudieswhichof

thesegasescausedtheobservedresponses.

Additional research is evidently needed to assess the sufficiency of the

secondary NAAQS in protecting birds as a valued component of public welfare.

Researchersshouldfocusonidentifyingresponsestobothacuteandchronicexposure

tothesixcriteriaairpollutantsregulatedbytheEPAthroughtheNAAQS,includingCO,

lead(Pb),O3,NO2,SO2,andfineandcoarseparticulatematter.Bothcontrolledexposure

studies and field studies would be useful in this endeavor, but it is essential that

researchers carefully measure in situ exposure to ambient air pollution when

conducting fieldstudies inorder tocompareconcentrationsofairpollutantswith the

primaryandsecondarystandardsandperformrigorousstatisticalanalysistopinpoint

whichpollutantiscausingtheobservedresponses.

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AdditionalPolicyRecommendations

Limited research on the topic of birds and air quality makes it impossible to

definitivelydeterminewhetherornotthesecondaryNAAQSaresufficientinprotecting

birds from the risks associated with exposure to health-damaging air pollutants.

However, it is clearly important to have secondary standards in place to safeguard

animals, especiallybirds, from theadversehealthoutcomes linked to exposure to air

pollution. The EPA must continue to carefully review the secondary standards as

required by the Clean Air Act, considering the results of new peer-reviewed science

from diverse disciplines, including atmospheric science, ecology, and veterinary

medicine.

It is also recommended that wildlife managers continue to address other

stressorsresultingfromanthropogenicactivitythataffectbirdsandmightincreasethe

vulnerability of avian species to air pollution, including urbanization, habitat

degradation, and climate change. By alleviating the impact of other environmental

stressors on birds, managers will reduce risks associated with exposure to health-

damagingairpollutantsandsupporttheoverallfitnessandsurvivalofavifauna.

FutureStudies

Futurestudiesonbirdsandairqualityshouldseektoaddresstheknowledgegaps

identified in chapter two of this thesis and inform air quality regulation. This

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interdisciplinaryresearchshouldutilizetoolsfromatmosphericchemistryandecology

tolinkchangesinthechemicalenvironmentwithavianoutcomes.

Ambient concentrationsof reactivegasesandaerosols aremeasuredusingboth

ground-based monitors and satellite data. Ground-based mass concentration and

speciationdataisavailablefromtheEPAAirQualitySystemDatabase.Measurementsof

air pollutants as observed from space, including aerosol optical depth (AOD) and

concentrationsofNO2,CO,andO3,areavailable frominstrumentsaboardtheorbiting

satellites that make up the National Aeronautics and Space Administration (NASA)

Earth Observing System. NASA has also developed interactive online tools to help

researchers visualize satellite data, includingWorldview and Giovanni. Both ground-

based data and satellite data are used to inform and improve air quality models,

anotherpowerfultoolforanalyzingairpollutiontrendsacrossbroadspatialscales.

Whenanalyzingisolatedairpollutionepisodes,atmosphericscientistsalsorelyon

archived meteorological data, mathematical models, and emissions inventories.

Researchers and air quality managers use the Hybrid Single Particle Lagrangian

Integrated Trajectory (HYSPLIT) Model, developed by the National Oceanic and

AtmosphericAdministration(NOAA),todeterminewhetherornotlong-rangetransport

may have contributed to a specific air pollution episode. This model computes both

backwardandforwardtrajectoriesofairparcels,allowingairqualityanalyststobetter

understandhowatmosphericpollutantsmayhavetraveledthroughagivenareabefore

and after an event. These simplified trajectories are computed using archived

meteorologicalobservations,suchasmeanwindfield,andrepresentthebestpossible

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estimateofanairparcel’sroutetoorfromaspecifiedsiteoveragivenperiodoftime.

To characterize pollution dispersion from point sources, such as smoke stacks,

atmosphericscientistsandengineersoftenusetheGaussianPlumeModel.Thismodel

is also informed by archived meteorological data. Climate models and climate data

visualization tools such as ClimateReanalyzer are useful to both to atmospheric

scientists andecologists in investigatinghowchanges in the atmospheremight affect

ecological processes, ecosystems, and public health. Emissions inventories and data

visualizationtoolssuchasECCAD:EmissionsofatmosphericCompounds&Compilation

ofAncillaryDataalsohelpairqualityscientiststoanalyzeairpollutionepisodes,build

understanding of spatial trends in air pollution, and make management

recommendations.

Ecologistsuseseveraldifferentsetsofcitizensciencedatatoassesstrendsinbird

populations,includingeBird,ProjectFeederWatch,theBreedingBirdSurvey,andMAPS

(MappingAvianProductivityandSurvivorship):

• eBirdwas launched in 2002by theCornell LabofOrnithology and theNational

AudubonSociety.Thisonlinereportingtoolfacilitatesthecollectionofmillions

of bird observations each year by aggregating checklists submitted by birders

aroundtheworld.Allcollecteddataarefilteredautomaticallytoflaganyunusual

observations,whicharethenreviewedbylocalexperts.Qualityassureddatais

made available to scientists and wildlife managers to use in research or the

strategicplanningofconservationefforts.

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• Project FeederWatch is run by the Cornell Lab of Ornithology and Bird Studies

Canada.Thisprogramsupportscitizens inmonitoring thebirds thatvisit their

feedersduring thewintermonthsandenables researchers to track changes in

thewinterdistributionofcommonbirdspecies.

• TheBreedingBirdSurvey(BBS)isorchestratedbythePatuxentWildlifeResearch

Centerand theCanadianWildlife Service.Thegoalof the survey is tomonitor

trends in the distribution of North American bird populations. Thousands of

birdersparticipateinBBSdatacollectioneachyear.Birderswhoparticipateare

assigned to a random roadside route and must follow a strict protocol when

makingobservations.Theirobservationsaresent toa teamofresearchersand

statisticians who analyze the data to assess the status of hundreds of bird

speciesinNorthAmerica.

• MAPS(MappingAvianProductivityandSurvivorship)isorganizedbytheInstitute

forBirdPopulations.Theinstituteengageslocalandstateagencies,non-profits,

and individuals in collecting demographic data to help explain trends in avian

populations. There are over 1,200 monitoring stations associated with MAPS

throughout the United States and Canada. By collecting information about the

vital rates of birds that visit these stations, researchers are able to assess the

underlyingcauseof the shifts inpopulations identified in theanalysisofother

datasets. Vital rates include several key demographic parameters, such as

survival,recruitment,residency,andproductivity.

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Integrating tools from atmospheric science and ecology will help bring

environmentalsciencetoanewfrontiertoaddressemergingconservationquestionsof

globalimportance.Therearemanypossibilitiesforfuturestudies.

Oneideathathasemergedfromthisthesisisexploringtheuseofbirdfeathersas

a biomarker for health-damaging air pollutants, such as aerosols or ozone. Isotopic

analysisoffeathersisalreadyusedtostudythemigratorybehavioranddietsofbirds,

and research has shown that feathers serve as useful biomarkers for elemental

pollution,5 persistent organic compounds,6 and agricultural activity.7 Atmospheric

scientists alsouse isotopic analysis in studiesdesigned todetermine theoriginof air

pollutants.Itthereforemightbepossibletodevelopanoninvasivesamplingtechnique

toassessavianexposuretoairpollutantsduringmoltbyanalyzingtheconcentrations

ofstableisotopesofcarbon,hydrogen,nitrogen,andsulfurfoundinbirdfeathers.

Asecond idea fora futurestudy is toconducta retrospectiveanalysisofoneor

moreof the fieldstudiescited inchapter twoof this thesis inorder toquantifyavian

exposure to health-damaging air pollutants using data from both ground-based

monitorsandsatelliteinstruments.Thiswouldallowresearcherstocomparetheactual

ambient concentrations of air pollutants birdswere exposed to in these studieswith

standardssetbytheEPA.

It might also be possible to compare bird observations or demographic data

5http://journals.plos.org/plosone/article?id=10.1371/journal.pone.01376226http://www.academia.edu/12826878/Evaluation_of_the_usefulness_of_bird_feathers_as_a_non-destructive_biomonitoring_tool_for_organic_pollutants_A_comparative_and_meta-analytical_approach7https://www.ncbi.nlm.nih.gov/pubmed/11563650

64

collected by citizen scientists in the years before, during, and after a serious air

pollutionepisode,suchasan intensewildfire, todetermine ifacuteexposurehadany

immediate or long-termeffects onpopulations. Thiswouldbe the first integration of

large-scale atmospheric chemistry and ecology datasets to address the impact of

reactivegasesandaerosolsonnon-humanspecies.Ideally,additionalresearchonbirds

and air quality will enable environmental scientists to determine which species are

mostsensitivetoairpollution.Thiscouldbeespeciallyimportantinensuringadditional

protectionsforendangeredspecies.

This thesis constitutes an important first step in linking research findings from

diversedisciplinestocharacterizeavianresponsestoairpollution.However,inorderto

determine whether or not current air quality regulation is sufficiently stringent to

protectbirdsfromtherisksassociatedwithexposuretohealth-damagingairpollutants,

additionalresearchmustseektoassesstheextentofbothacuteandchronicexposure

to reactivegasesandaerosolsamongstavifaunaand the impactsof saidexposureon

avianphysiologyanddemography.Thiswillrequirethatresearcherscollaboratewith

experts outside of their field and pull in tools from numerous scientific disciplines.

Researchonthistopicwillthereforeinformpolicyandwildlifemanagementaswellas

improve communication between fields of study, creating new opportunities in

interdisciplinaryenvironmentalscience.