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Abird's-eyeviewofairpollution
Theimpactsofhealth-damagingairpollutantsonavifaunaby
OliviaV.Sanderfoot
Athesissubmittedinpartialfulfillmentof
therequirementsforthedegreeof
MasterofScience
(EnvironmentandResources)
atthe
NelsonInstituteforEnvironmentalStudies
UNIVERSITYOFWISCONSIN–MADISON
2017
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.
ii
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.
iii
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
1
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
2
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.
3
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.
4
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
5
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
6
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
7
“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
8
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.
9
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.
10
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
11
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.
12
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
13
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
14
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
15
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:
16
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,
18
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.
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.