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J Appl Ecol. 2019;00:1–11. wileyonlinelibrary.com/journal/jpe
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© 2019 The Authors. Journal of Applied Ecology
© 2019 British Ecological Society
Received:25Novemb er2018
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Accepted:4May2019
DOI:10.1111/1365-2664.13449
RESEARCH ARTICLE
Large‐scale manipulation of the acoustic environment can alter
the abundance of breeding birds: Evidence from a phantom
natural gas field
Elizeth Cinto Mejia1 | Christopher J. W. McClure1,2 | Jesse R. Barber1
1Depar tmentofBiologi calSci ences,Boise
StateUniversit y,Boise,Idaho
2ThePeregrineFund,Boise,Idaho
Correspondence
ElizethCintoMejia
Email:elizethcinto@gmail.com
JesseR .Barber
Email:jessebarber@boisestate.edu
Funding information
Nationa lParkSe rvice,Grant/Award
Number :CESUPl3AC01172;Directorate
forBiologicalS cience s(NSF),Grant /Award
Number :CNH1414171
HandlingEditor :VitorPaiva
Abstract
1. Alteredanimaldistributionsareaconsequenceofhumanexpansionanddevelop-
ment.Anthropogenicnoisecanbeanimportantpredictorofabundancedeclines
nearhuman infrastructure, yet moreinformation is needed to understandnoise
impactsatthespatialandtemporalscalesnecessarytoalterpopulations.
2. Energydevelopment andassociated anthropogenic noiseareglobally pervasive,
and expand ing. For example, 60 0,000 n ew natural gas wells have be en drilled
acrosscentralNorthAmericainlessthan20years.
3. Weexperimentallybroadcastenergysector noise(recordingsofcompressoren-
gines)inSouthwest Idaho (USA).Weplaced arraysof speakerscreatinga‘phan-
tomnaturalgasfield’inalarge-scale experimentandtested theeffects ofnoise
alone on breeding songbird abundance.To examine variationin human-caused
noise, we broa dcast two ty pes of compressor n oise, one with a slightl y higher
soundintensityandgreaterbandwidththantheother.
4. Ourphantomnaturalgas fieldencompassedapproximately 100km2. We broad-
castnoiseoverthreecontinuousmonths,foreachoftwoseasons,andquantified
over20,000hrofbackgroundsoundlevels.
5. Brewer's sparrows (Spizella breweri) were affected byour narrowband playback,
declining30%,50mfromthespeakerarrays.Duringourbroadbandplayback,all
species combinedandBrewer'ssparrows decreased20%and33%,respectively,
atthescaleofoursites(~0.5km2;upto400mfromspeakerarrays).
6. Synthesis and applications.Ourresults show the importanceof incorporatingthe
acousticstructureofnoisewhenestimatingthecostofnoiseexposureforpopula-
tions.Wesuggestanurgentneedfornoisemitigation,suchasquietingcompres-
sorst at ions,inener gyextra ctionf ie ldsandothersourcesinnaturalareasbroadly.
KEY WORDS
anthropogenicnoise,noiseexposure,noisepollution,oilandgasdevelopment,populations,
sagebrushsteppe,sensoryecology,songbirdabundance
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1 | INTRODUCTION
From urban a reas (Barber, Croo ks, & Fristru p, 2010) to the deep-
estoceantrench(Dziaketal.,2015),anthropogenicnoiseisubiqui-
tous.Extensiveliteraturedocuments the negativeeffects ofnoise
on foragi ng efficie ncy, surviv al, distri bution and re product ive suc-
cessofwildlife(see reviews Francis&Barber,2013;Shannonetal.,
2016). Recent stu dies have exper imentall y broadca st noise to dis-
entangletheroleoftheacousticenvironmentfromothercovarying
factorsassociatedwithhumandisturbance(e.g.directdeaths, edge
effec ts, chemi cal pollut ion). For exampl e, playback of in termitten t
trafficnoiseandcontinuousdrillingnoisereducedmalesagegrouse
(Centrocercus urophasianus)lekattendanceby73%and29%respec-
tively (Blickley, Blackwood,& Patricelli, 2012).An experiment that
replicatedthesoundscapeofahighwaydemonstratedthatmoder-
ately inten se (~55dBA , 24 hr Leq at 50 m) acousti c environment s
can alter bird distributions (McClure, Ware, Carlisle, Kaltenecker,
& Barber, 2013), change the age structure of a bird community
(McClure,Ware, Carlisle, & Barber,2016)andthwartthe abilit y of
birds to gain weight during migratory stopover (Ware, McClure,
Carlisle,&Barber,2015).
Energyextractionisa globallydistributed, and rapidlyexpanding
source of noi se (Bentley, 200 2). For example , 50,00 0 new wells per
yearhavebeen drilledthroughoutcentral North America since 2000
(Allre d et al., 2015). Energ y extrac tion fields ca use habitat los s and
fragmentation,andbringroadsandotherpermanentinfrastructureto
thelandsca pe(McDonal d,Fargione,Kie secker,Miller,&Powell,2009).
Consequently,energ yex traction fields reduce songbird abundance,
alternestingsuccessandchangelargemammalspaceuseandbehaviour
(Northrup & Wittemyer,2013). Tounderstand theroleofenerg yex-
tractionnoiseinthesemultimodaleffects,previousstudieshavetaken
adv antageofvariatio ninsoundlevelscreat edb ydi ff erentty pe sofen-
ergyextractioninfrastructure:loudcompressorstations(enginesthat
maintainpressureinpipelines)andquieterwell pads.Comparingbird
communitiesnearthesetypesofinfrastructure,Bayneandcolleagues
(Bayne, Ha bib, & Boutin , 2008) s howed that den sity and occ upancy
ratesofseveralsongbirdspeciesdecreasednearloudcompressorsta-
tions in th e Canadian bo real forest . Francis and cowo rkers descri be
similar patterns in a naturalgasfield in New Mexico;they report de-
creasedsongbirdspeciesrichness nearloudgas compressorstations
(Francis, Ortega, & Cruz, 2009), which altered ecosystem services
suchas pollinationandseeddispersal(Francis,Kleist,Ortega,&Cruz,
2012). Furth er work in the s ame gas field h as documente d reduced
bat acti vity (Bunkl ey, McClur e, Kleist, Fran cis, & Barber, 2015), and
alteredarthropoddistributions(Bunkley,McClure,Kawahara,Francis,
&Barber,2017).Inthesenaturalexperiments,there were otherun-
measur edf ac torss uchasa irp ollut ion(Roy,Ada ms,&Ro binson,2 014),
andpresenceofadditionalpowerlinesatcompressorstations(Braun,
Oedekoven, & Aldridge, 20 02) that may have influenced the results.
Regardlessofc aveats,these studies strongly indicate that the causal
factorsbehindtheseecologicalimpactsarelikelynoisemediated.
Due to the importance of understanding the scale of noise
effects, and the significant and expanding footprint of energy
extraction noise globally, we aimed to experimentally test thein-
flu enceofcompres sorstat ionno iseonlar ge-sc al espac eus eduring
thebreedingseason ,acr iti caltimeforwildlife.Wecreateda‘phan-
tomnaturalgasfield’withspeakerarraysbroadcastingcompressor
noise on a spatial scalelarge enough(sites distributedacross 100
km2)andatemporalscalelongenough (anentirebreedingseason)
toalterpopul ations.Bec aus esoundp ropagationvarieswithtopog-
raphy and ove r time due to cha nging atmos pheric con ditions, we
were able tocreate a gradientofnoise exposure across sites and
time (see Figures 1d and 2). We conducted ourexperiment in the
sagebrushsteppe,anecosystemthathassufferedrapidalterations
du eto h uma n exp a nsi o nan d dis t u rba n ce( K nic k eta l .,2 0 0 3), inc l u d-
ingwidespreadenergyextraction(Northrup&Wittemyer,2013).
Based on economic incentives and resource properties, ex-
traction fields contain many types of compressor stations (U.S.
Energy Information Administration, 2007) that produce dif ferent
spectralbandwidths(therangeoffrequenciescontainedinasound
source) and associated sound levels (Francis, Paritsis, Ortega, &
Cruz, 2011). Give n this variatio n, we replicate d two distinc tly dif-
ferentnoiseprofiles,onemorebroadbandandhigherintensit ythan
theother(Figure1).Wepredictedthatplaybackofcompressorsta-
tionnoiseofbroaderbandwidthandintensitywouldhaveagreater
negativeimpactonbirdabundanceowingtoincreasedoverlapwith
thehearing rangesof birds and other trophicallyconnectedgroups
(Greenfield,2014).Totesttheeffectsofourplaybacks,weevaluated
noiseasacategoricalandcontinuousvariable.Toexaminenoiseas
acategoricalvariable,wecompared birdabundance atcontroland
noises ites.Totestt hecontinuousef fect sofno ise,weus edthevari-
ation in sound levelsat each site as a predictor of bird abundance
(Figure 1d).Studying therelationshipbetweensoundlevelandbird
abundancecanprovidemanagersinformationontheecologicalben-
efitsofquietinganthropogenicallyalteredecosystems.
2 | MATERIALS AND METHODS
2.1 | Phantom natural gas field
We played compressor station noise in the sagebrush steppe of
SouthwestIdaho (USA),inanarea used forrecreationandmilitary
training—theOrchardCombatTrainingCenter.Webroadcastnoise
from1Aprilto15 October in2014and 2015. Weselectedexperi-
mental si tes, and ran domly assign ed them to noise ve rsus control
treatments—sevencontrol and eightnoise sites in 2014, wherewe
broadc ast our narr owband playba ck, and six cont rol and six noi se
sites in 2015 (reu sing 10 sites from 2014, and e stablish ing 2 new
sites),wherewebroadcastour broadbandplayback(detailsbelow)
(See Figure 2 and Figure S1 in Supporting Information).At control
sites, we pl aced dummy 'spe akers' that wer e similar in shap e, size
andcolourtoourbroadcastspeakers.Siteswereatleast1kmapar t
and500mormorefromadirtroad.
All sites hadsimilar plantcommunities, dominated by bigsage-
brush (Artemesia tridentata). To quantify the percentage of sage-
brushcoverateachsiteweusedphotographicmethods(Booth,Cox,
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&Be rry man,200 6).Wemeasuredveg et at io na lo ng fi ve30 0 -m tr an-
sectsradiatingfromthe centreofeach site.Withacamera(Fujifilm
FinePix XP7016.4MegapixelCompactC amera)at tachedtoa2-m
pole(Sokkia724,290Economy2mAluminum2SectionGPSRover
Rod), we photographed 20 points along each transect that were
15mapart, obtaining a hundred pictures per site. We obtained 1-
m2photographsthatwereanalysedusingtheopensourcesoftware
Sample Point (version 1.58 ; Booth et al., 20 06). We identified th e
vegetationtypeof64individualpointsofeachphotographtoobtain
apercentcoverforsagebrush.
2.2 | Noise playback and acoustic monitoring
Webroadcasttwonoisestimuli,oneperyear(Figure1a–c).Foreach
stimul us type (nar rowband and b roadband ) we used one play back
filethatincombinationwithtwo differentspeakersystemscreated
the two di fferent nois e stimuli. Arr ays were mounted on s upport
structures 2 m above the ground. For the narrowband playback in
2014,we placedfour horn-loadedspeakers(Dayton RPH16; MCM
40 W; 4 0 0–3,0 0 0 Hz±5d BA) int hefou rcar din aldir e cti ons ,an dam -
plified themusingclassD amplifiers (PartsExpress,2W,4-ohm).In
2015,forthebroadbandplayback,weusedomni-directionalspeak-
ers(Octasound SP820A;35–20,000 Hz ±10dBA,)andsubwoofers
(Octasound OS2X12; 25–20,000 Hz ± 10dBA) driven by class T
amplifiers(LepaiLP-2020A20W,4-ohm). Amplifiers were powered
by solararr aysystems (Solarland SLP 15S-12 panels, Morningstar
PS-30M controllers and PowerSonic12Vbatteries). We delivered
soundfiles(WAV)totheamplifiersusingOlympusLS-7playersthat
werepoweredwith20-amphourLiFePO4(Batter yspace)batteries.
Weplayedsyntheticcompressornoise,createdinAudacit yver-
sion2.1.2.Becausecompressorstationstendtobeidiosyncratic,we
createdouraudiofilefromanaverageofthreecompressorstations
recordedintheSanJuanbasin,NewMexicoandGreenRiverBasin,
Wyoming. C ompressor st ations were recorde d with a Sennheise r
ME66 microp hone (40–20,000 Hz; ±2.5dBA) a nd Roland R-05 re-
corder (samplingrate48kHz)at40m. Wecreated a3-hrplayback
file that w as repeated 24 hr/day.It i s important to n ote that the
compressorstationswerecordedverylikelyproducedenergybelow
20Hz(Francisetal.,2011),outsideoftherecordingorplaybackca-
pabilitiesofourequipment.
To measure sound levels at each site through the season,
we placed acoustic recording units (ARUs; Roland R-05 audio
FIGURE 1 Broadcastfilesandequipment.(a)A5-minrecordingofournarrowbandplaybackdisplayedasaspectrogram
(frequency(kHz)×time(min)),andoscillogramshowingtheamplitude(voltage×time).(b)A5-minrecordingofourbroadbandplayback
displayedasaspectrogram(frequenc y×time),andoscillogramshowingtheamplitude(voltage×time).(c)Visualcomparisonofreal
compressorsandourplaybacks.Powerspectra(soundlevel×frequency)oft wogascompressorstationsinNewMexico(Compressor1)
andWyoming(Compressor2),andrecordingsofthetwofilesbroadcastinourexperiment(allfilesrecordedat40meters).Comparedto
thenarrowbandplayback,thebroadbandplaybackwas~6kHzhigherinbandwidthasmeasured55dBbelowpeakfrequency.Theaverage
songbirdhearingrange(asmeasured55dBabovethebesthearingthresholdfortheaveragebird)isdepictedbytheshadedgreybar
(Dooling,2011),showingstrongoverlapbetweenournoisebroadcastsandbirdspectralsensitivity.Whencomparingthenarrowbandand
broadbandplaybacks,notethegreaterspectraloverlapofthebroadbandtreatmentwithbirdhearingatbothlowandhighfrequencies.(d)
Meanvalues(±SE)ofsoundlevels(dBA)fromeachsiteatthe50and250mpointcountlocations.Circlesrepresent50-msitesandtriangles
represent250-msites.Yellowrepresentscontrolsitesandredrepresentsnoisesites.Thelargervariationofnoisesitesat250misdueto
changesinwinddirec tionandourplaybacknoisetravelling250mfromthespeakers
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recorders)thatwere calibrated followingMennitt&Fristrup,2012,
and mounted inside a protective wind screen at each bird point
countlocation(30 in2014and 24in 2015).WecamouflagedARUs
inshru bsandmo un tedth em 50cmaboveth eg ro undbylash in gs up-
portrodstovegetation.Usingcustomprograms(DamonJoyce,NPS,
AUDIO2NVSPL and Acoustic Monitoring Toolbox), we obtained
hourly sound levels from MP3 recordings (equivalent continuous
soundlevel;LEQindBA).
Acrossourstudy site, the gradientofbackgroundnoiseranged
fr om~2 2d BAt o6 3dB A(F igu re1d),a llo win gu sto co m par en oto nly
noiseandcontrol sitesbut alsoexamineagradient ofsound levels
due to the va riation bet ween sites with t he same treat ment, and
variationwithinthesamesite(decibelsat50mvs.250m).Foreach
site,weobtainedthemedianofthehourlyLEQ(dBA)permonth
(Lynch,Joyce,&Fristrup,2011)asapredictorofbirdabundance.In
2014,under the narrowband playback (Figure 1a),sound levels at
50mfromthespeakerarraysaveraged56.3±1.7dBA(mean±SE)
at noise site s and 37 ± 0.7 dBA at control s ites. At 250 m, noi se
sites avera ged 46 ± 1.5 dBA and c ontrol sites 35 ± 1. 59dB A. In
2015,underthebroader bandwidthandhigher intensityplayback
(Figure1b),soundlevelsat50maveraged58±1dBAatnoisesites
and 30.6± 1 dBA at control sites. At 250 m, noise sites averaged
39.8±1dBAandcontrolsitesaveraged33±0.9dBA.Itisimport-
anttonotesoundlevelsofourcontrolsiteswerehigherthanmany
natural environments (Bux ton et al., 2017) duetomilitary training
andrecreationalactivityinourstudyarea.Fur thermore,thesound
lev el sofourcon tr olsi te sweresimilart ocontr olsites(w el lpadsites)
usedinprevious'natural'ecologicalexperimentsinrealnaturalgas
fields (e.g.,Francis et al., 2009).Figures 1 and2show the hetero-
geneity and variability between sites due to atmospheric (wind)
conditionsandtopographyin2015.Seesupportinginformationfor
detailsaboutoursoundscapemapduringthenarrowbandplayback
in2014(FigureS1).
2.3 | Bird abundance
We counted bird s at each site seven to te n times from 8 A pril to
17June2014during the narrowband playback,and seven to eight
timesfrom5Aprilto15June2015duringthebroadbandplayback.
Ateachsite,weplacedtwopointcountlocations,oneat50mfrom
the spea ker array and the s econd at 250 m from t he array. Point
countlocationswereplacedinoppositedirectionsfromthespeaker
arraytomaximizetheindependenceofcountsites.Allcountswere
6mininlength,andconductedwithin4hraftersunrisebythesame
two obse rvers, duri ng both seasons. N o surveys were con ducted
understrongwindorheavyrain.Countingmethodologyfolloweda
modifiedprotocol oftheRockyMountain Bird Observatory (Hanni
etal.,2014).Foreachdetectedbird,werecordedspecies,direc tion
and dist ance (using laser r ange finders) of al l birds. We identif ied
species by call,song or sight.Becauseprobability of detection can
vary betweenobser vers (Alldredge, Simons,&Pollock, 2007;2015
&Barber,22015;Sauer,Peterjohn,&Link,1994),werandomizedthe
surveys thateachobservercompletedwithin site (50mvs.250m)
and between sites, making sure both observers visited all sites.
Excessivenoise can decrease the numberofbirds detected during
pointcounts(e.g.McClureetal.,2015;Simons,Alldredge,Pollock,&
Wettroth,2007;Pacifici,Simons,&Pollock,2008).However,Ortega
and Francis (2012) found that noise from natural gas compressors
didnotinterferewithdetectionratesforsoundlevelsunder45dBA.
Furthermore, Koper and colleaguesshowed that quiet tomoderate
FIGURE 2 Thephantomnaturalgas
field.Estimatedsoundlevels(dBA1hr
LEQ)ofnoisesitesagainstabackground
of28dBA,themedianL50forcontrol
sitesfromMaytoJuneduringbroadband
playback(2015).Soundlevelwas
modelledusingSPreAD-GIS(Reed,
Boggs,&Mann,2010);seesupporting
informationfordetails(AppendixS1).
Thismapisaheuristicofthebroadband
soundsc ape.Greencircles(control)and
triangles(noise)representthecentreof
thesite,speakersordummyspeakers.
Yellowcirclesrepresentthetwopoint
countlocations.Pulloutintheupperright
cornerrepresent ssoundlevelsfroman
exampleplaybacksite
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levelsofextractionnoisewereunlikelytointerferewithdetectionof
songbirds(Koper,Leston,Baker,Curry,&Rosa,2016).Nevertheless,
weturnedoffourspeakersduringpointcountssothatnoisewould
notinterferewithratesofdetection(McClureetal.,2013).Because
noise levels were between ~30 and 37 dBA undernoise-offcondi-
tions at control and noise sites,relative comparisonof bird counts
between the two site types are likely not biased by imperfect
detection.
2.4 | Statistical analysis
Weanalysed all data using R (R Core Team, 20 00 R language defi-
nition), version 3.2.1 and package lme4 (Barton, 2016; Bates,
Maechle r, Bolker, & Walker, 2014). We truncated dat a to include
detect ions only wit hin 150 m of point co unt locatio ns. Truncating
ourdetectionsto150mallowedustoincludeindividuals thatwere
400 m from the noi se source at the 250-m point count l ocation
(250m + 150m),therefore, our results only applywithin400 mof
ourspeakerarrays.
We were interes ted in the five song bird species that b reed
in our site and are associated with the sagebrush ecosystem—
Brewer's sparrow(Spizella breweri),hornedlark(Eremophila alpes‐
tris),western meadowlark(Sturnella neglecta),sagebrush sparrow
(Artemisiospiza nevadensis) and sage thrasher (Oreoscoptes monta‐
nus) (Baker, Eng, Gashwi ler,S chroeder, & Clait , 1976). We mod-
elle da bu ndanc eofourfi ve sp eciesofintere stco mbine d,andeach
species individually, using generalized linear mixedmo delswith
a Poisson dis tribution (B olker et al., 20 09). We only considere d
parame ters as informat ive if they had 95% confid ence interva ls
excluding zero (Arnold, 2010). To test the effec ts of dif ferent
playbacksindependently,we analysed each year separately.We
also z-transformed independent variables to improve model
convergence.
To test whether b ird abundance is re lated to the prese nce or
absence ofnoisewefirst createdamodel withthe variables 'treat-
ment'(indicatingnoisevs.controlsites),interactionoftreatmentand
pointcountlocation(50or250mfromthespeakers),combinations
oflinear and quadratic ef fectsofthe day of the census(to include
seasona l fluctuatio ns), and percent sag ebrush cover (be cause it is
an impor tant predictor of songbird settlement decisions; Chalfoun
&Martin, 2007). Totest therelationship between bird abundance
andsoundlevel,wecreatedanothermodelwithavariable'dBA'(in-
dicatingthemonthlymediansoundlevel(LEQindBA)ateachpoint
countlocation),combinationsoflinearandquadraticeffectsofday,
and perce nt sagebrush cove r. Note that dBA a nd treatment we re
never in the s ame model , thus avoiding m ulticollin earity. For bot h
models,weincludedsiteandpointcountlocationasrandomeffects.
During the analysis, wekeptthewhole modelandwe did not drop
anyparameterthatwasnotinformative.Duetovariousmethodsof
studyingsoundscapes,eventhoughourresultsdonotqualitatively
change,weincludeaseparateanalysisusingthemediansoundlevel
(L50;TableS2).
3 | RESULTS
3.1 | Treatment model
During the narrowband playback, parameters that explained
Brewer's sparrow abundance were treatment, interaction of
treatment and point count location, day and day2. Brewer 's
sparrow showedanegativeresponseto treatmentonly at the
50-mpointcountlocation,decreasing30%atnoisesites(aver-
agecount1.13±0.18atcontroland0.76±0.12atnoisesites).
Parametersthatexplainedtheabundanceofthesongbirdcom-
munityweredaya ndday2 ( Table1,Figure3).Duringthebroad-
bandplayback,theparametersthatexplainedBrewer'ssparrow
abundancewere treatment, interactionoftreatmentand point
countlo catio n, dayandday2.B rewer'ssparrow,showedanega-
tive response to treatment at both 50-m and 250-m count
locations,decreasing51.8%(averagecount2.31±0.32atcon-
trol and 1.11 ± 0.18 at noise si tes), and 13% (average count
2.06 ± 0.25atcontrol and1.79± 0.25 at noise sites),respec-
tively,inthepresenceofnoise.Parametersthatexplainedthe
abu ndanceofth esong birdcommun it yweretreat me nt ,dayand
day2,decreasing20%(averagecount1.12±0.06atcontroland
0.89±0.05a tnoises ites) atnoi sesites(50ma nd250mcounts
combined). The parameters that explained the abundance of
sagebrush sparrow were day and day2, only underthe broad-
band playback. The parameter thatex plainedthe abundance
ofsage thrasher with a positive relationshipunder both play-
backswassagebrushcover(Table1,Figure3).Allresponsesto
day and day2werepositivequadratics(Table1).Thisresponse
indicates that bird abundance increases with time as migrant
specie sar rivedatourst udysite,a ndl aterinthesummer,fewer
bir dsaredete ctedasaresultofth eendoft hebree dingseason.
Horned lark and western meadowlark showedno response to
anyparameters.
3.2 | Sound level model
During the narrowband playback, parameters that explained
Brewer's sparrow abundance were dBA, day and day2. Brewer's
sparrow showed a negative response to increased sound levels
with a decrease of 15%per 9 dBA . Parameters that explainedthe
abundanceofthe songbird community wereday,andday2. During
thebroadband playback,parametersthatexplained Brewer'sspar-
rowabundanceweredBA ,day,andday2.Brewer'ssparrowshowed
a negative r esponse to incr eased sound le vels with a decre ase of
17% per 9 dBA . During the bro adband playb ack, parame ters that
explained the abundance of the songbird community were dBA,
day and day2, with a decrease of 7.5%per 9 dBA . The parameters
thatexplainedthe abundanceofsagebrushsparrowonly underthe
broadband playback were day and day2. The parameter that ex-
plained the abundanceofsage thrasherwithapositiverelationship
under both playbackswaspercentageof sagebrushcover( Table1,
Figure 3). A ll responses to d ay and day2 were posit ive quadratic s
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CINTO MEJ IA ET Al .
TABLE 1 Scaledestimatevalues,standarderrors,pvaluesand95%confidenceintervalsofallparameterswith95%confidenceinter vals
excludingzero
Parameter Estimate Std. Error p95 C.I. 95 C.I.
Treatmentmodel
Allbirds ,narrowband Day2−1. 71 0.38 0.00 −0.96 −2 . 46
Day 1.69 0.38 0.00 2.43 0.95
Treatment −0.19 0.17 0.25 −0.53 0.15
Treatment×Point 0.00 0.21 0 .99 −0.47 0.4 4
Point −0.10 0.15 0 .51 −0.43 0.23
Sagebrushcover 0.02 0.06 0.76 −0.1 2 0.15
Allbirds ,broadband Day2−4.13 0.58 0.0 0 −2.99 −5 .26
Day 4.20 0.58 0.00 5.33 3.06
Treatment −0.29 0.10 0.00 −0 .10 −0.48
Treatment×Point 0.10 0 .13 0.44 − 0.16 0.37
Point 0.06 0.09 0.50 −0.11 0. 23
Sagebrushcover 0.06 0.03 0.05 0.00 0.13
Brewer'ssparrow,
narrowband
Day2−10 . 68 1.16 0.00 −8.40 −12 .97
Day 10.3 4 1.11 0.00 12.52 8.16
Treatment −0.51 0.25 0.04 −0.03 −1 . 01
Treatment×Point 0.50 0.25 0.04 1.13 0.16
Point −0 .14 0.17 0.43 −0.49 0.21
Sagebrushcover 0.05 0.10 0.60 −0.16 0.28
Brewer'ssparrow,broadband Day2−10. 79 1 .13 0.00 −8.57 −13 . 01
Day 10.85 1.12 0.00 13.05 8.65
Treatment −0.78 0.17 0.00 −0.44 −1 . 12
Treatment×Point 0.56 0.23 0.01 1.01 0. 11
Point −0.11 0.14 0.4 4 −0.38 0.16
Sagebrushcover 0.02 0.05 0.72 −0.09 0.13
Sagethrasher,narrowband Day22.19 2.09 0.29 −2.15 6 .14
Day −2. 5 7 2.05 0.21 −6 .51 1.62
Treatment 0.53 0.69 0.4 4 −0.80 2.08
Treatment×Point −0.23 0.84 0.78 −2.18 1 .42
Point 0. 61 0.65 0.35 −0.66 2.14
Sagebrush cover 0.66 0.26 0.01 1.16 0 .16
Sagethrasher,broadband Day2−2. 4 6 2.39 0.30 −7. 2 5 2.18
Day 2.78 2.42 0.25 −1.9 2 7. 6 0
Treatment −0.31 0.48 0.52 −1 . 3 0 0.82
Treatment×Point 0.31 0.61 0. 62 −0.88 1.53
Point 0.26 0.38 0.49 −0.48 1.03
Sagebrush cover 0.82 0.18 0.00 0 .47 1.50
Sagebrushsparrow,
broadband
Day2−4.95 1.35 0.00 −2 . 30 −7.60
Day 4.98 1.35 0.0 0 7. 62 2.34
Treatment −0.26 0.22 0.24 −0.71 0 .18
Treatment×Point −0.37 0.31 0. 24 −0 .99 0.25
Point 0.20 0.19 0.29 −0 .17 0. 59
Sagebrushcover 0.11 0.07 0.13 −0.06 0. 27
(Continues)
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CINTO MEJ IA ET Al .
(Table1).Hornedlarkandwesternmeadowlarkshowednoresponse
toanyparameters.
3.3 | Carryover effects
Becausewerandomized sites eachyear,andused someofthe same
sitesacross years,we testedforcarryovereffectson bird abundance
from the treatmentinthe previous year. Admit tedly, our lowsample
size sprovideonlyawea ktest.N odiffer encewaso bser vedinson gbird
abundancein2015when comparing controlsites that were exposed
tonoise in2014(N=2)tositesthatdidnotreceivenoiseexposure
ineither year (i.e. sites that werecontrolsboth years)(N=2),norto
controlsitesstudiedonlyin2015(N=2),indicatingcarryovereffects
wereun likel y(β=0.04,±0.0 8,p=0.62;Fig ureS2).Overtwoyears,we
recorded2,074detectionsoffivesongbirdspeciesthatnestedinour
studysite(TableS1).
4 | DISCUSSION
Ourlarge-scale,experimentalbroadcastofcompressorstationnoise
revealed a m arked effe ct on breed ing songbir d abundance . Under
playback of broadband noise,theabundanceof all birds combined,
and one individual species, decreased. In contrast, playback of
Parameter Estimate Std. Error p95 C.I. 95 C.I.
Soundlevel(dBA)model
Allbirds ,narrowband Day2−1. 71 0.38 0.00 −1. 0 0 −2 . 51
Day 1.71 0.38 0.00 2.46 0.97
dBA −0.02 0.05 0.71 −0 .12 0.09
Sagebrushcover 0.01 0.07 0.85 −0.13 0.15
Allbirds ,broadband Day2−4.10 0.58 0.00 −2 .97 −5.24
Day 4.17 0.58 0.00 5.31 3.04
dBA −0.10 0.03 0.00 −0.02 −0.17
Sagebrushcover 0.06 0.03 0.08 −0.01 0.13
Brewer'ssparrow,
narrowband
Day2−10 .78 1.17 0.00 −13. 15 −8.53
Day 10.43 1.12 0.00 8 .27 12.68
dBA −0.16 0.07 0.03 −0.31 −0.01
Sagebrushcover 0.06 0.10 0.53 −0 .15 0.28
Brewer'ssparrow,broadband Day2−10. 77 1.13 0.00 −1 3. 0 4 −8.60
Day 10.8 3 1.12 0.00 8.67 13.06
dBA −0. 24 0.07 0.00 −0. 37 −0 .11
Sagebrushcover 0.01 0.06 0.90 −0.13 0.14
Sagethrasher,narrowband Day22.26 2.08 0. 28 −2.0 7 6.21
Day −2. 65 2.05 0.20 −6.58 1.54
dBA 0.20 0.20 0.33 −0.20 0.62
Sagebrush cover 0.62 0.25 0.01 0.12 1.20
Sagethrasher,broadband Day2−2. 51 2.40 0.30 −7. 3 0 2.16
Day 2.83 2.43 0. 24 −1 . 89 7.67
dBA −0. 24 0.17 0 .15 − 0. 61 0.07
Sagebrush cover 0.80 0.19 0.00 0.43 1.39
Sagebrushsparrow,
broadband
Day2−4. 87 1.35 0.00 −7. 58 −2 . 26
Day 4.91 1.35 0.0 0 2.30 7. 5 4
dBA −0.06 0.11 0.60 −0.26 0 .17
Sagebrushcover 0.11 0.09 0.25 −0.10 0.33
Note: Inboldparametersthatpredictbirdabundance.Theparameter‘treatment ’representsnoisever suscontrolsites,‘sagebrushcover’represents
thepercentofsagebrushcoverateachsite,‘dBA’representssoundlevels,‘day’representsJuliandayand‘day2’represent sthequadraticeffectsof
day.
TABLE 1 (Continued)
8
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CINTO MEJ IA ET Al .
narrowbandnoise alteredthe abundance ofonly one species, sup-
port ing our predic tion that a high er bandwidth a nd level of noise
would resultinastrongernegativeeffecton bird populations. We
demonstratethatnoisealonecanrecreatesimilarpatternsofsong-
bird space u se found in natural g as extract ion fields. Gilb ert and
Chalfoun (2011)obtained comparable resultsinaWyoming natural
gasfieldwhereananalogous songbirdcommunityshowedchanges
inabundanceasdensityofextractioninfrastructureincreasednear
birdcount locations. Additionally,our workbroadly confirms other
studies performed in energy extraction fields (e.g. Bayne et al.,
2008;Francisetal., 2009)aimedatteasing apar tnoise from other
variables.
Underthenarrowbandbroadcast,Brewer'ssparrowabundance
decreased30% compared tocontrolsat the50m sur vey locations
only.Asimilarnarrowbandplaybackofroadwaytrafficnoiseduring
songbirdmigrationresultedinan~30%decreaseinabundance,with
significant declines in 12 migratory species (McClure et al., 2013).
Althoughthereis nooverlapinbirdspeciesexaminedbet weenour
current study and this previous work, our resultshighlightthe im-
portanceofexaminingwildlife responses to noise duringdivergent
lifestages(e.g.migrationvs.breedingseason).Atsitesthatreceived
our broad band noise play back, the ab undance of the ent ire sage-
brush songbird community, and Brewer's sparrowalone, declined
20%and33% respectively.Notethatthesepercentagedecreases
inbirdabundance,althoughderivedfromsmallreductionsinoverall
average coun ts, transl ate to signific ant declines w hen consideri ng
the amount of area pote ntially exposed to g as compressor nois e
acrosssagesteppehabitat(Allredetal.,2015).
Toprovide managers with an informativemetricto parameter-
izethe ecological effectsofquietinglandscapes,weexaminedthe
relationshipbetweensongbirdabundanceandsound level,specifi-
cally.Thisisparticularlyrelevantforexistingenergyextractionfields
where removal of noise sources is unlikely, yet quieting sources is
tract able. The overall songbird communit y declined 7.5% per 9
decibels under the broadband playback, although there was no
measurablechangeunderthenarrowbandplayback.Wefoundthat
Brewer's sparrowdecreased15% per 9decibelsunderthenarrow-
band playback and 17% per 9 decibels under the broadband play-
back. O ur noise sites did n ot recreate som e of the highest s ound
levelcompressorstationsthatexist inextractionfields (Bunkleyet
al.,2015;Mason,McClure,&Barber,2016).Wecan,therefore,pre-
dict that theseintense noise sources willhave a moredetrimental
effectonbirdpopulations.Ourfindingscouldhavebeeninfluenced
byayeareffect.However,thenumberofbirdencounterseachyear
wassimilar(TableS1),and ourexperimentwasdesignedtotestthe
relative,not absolute, differences bet ween noise and control sites
FIGURE 3 Birdabundanceresults.
(a–c)Songbirdabundanceresultsfrom
ourfirsttreatmentmodel.Smallgreydots
representthenumberofbirddetections
inadayateachsite,redsquaresrepresent
meanvalues(±SE)atnoisesitesand
yellowsquaresrepresentmeanvalues
(±SE)atcontrolsites.(d–f)Songbird
abundanceresult sfromoursecond
dBAmodel.Smallgreydotsrepresent
birddetec tionspersoundlevel(dBA),
indicatinganegativerelationshipbetween
birdabundanceandincreasedsound
levels
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9
Journal of Applied Ecology
CINTO MEJ IA ET Al .
between treatments. In addition, based on plumage, 70% of the
Brewer'ssparrowmalesinoursystemt hatwerebandedforthepur-
posesofadifferentstudyinourarea,werefirsttimebreeders,aged
assecondyearindividuals(birdsknowntohavehatchedinthecalen-
daryearprecedingthebandingyear)duringbothyears.
Alt ho ughwedonotknowtheme chanismbehin dthedecrea se
insongbirdabundanceweobserved,ourplaybackscouldhavein-
creased visualvigilancebehaviourowingtolost auditory aware-
ness,andthusreducedforagingrates—forcingbirdstoleave(Ware
et al., 2015). A lternativel y,for aging behavio ur might have been
alteredbyreduced acoustic detectability of prey (Montgomerie
& Weatherhead, 1997), indirectly by altering arthropod distri-
butions (Bunkley etal., 2017), or perhaps byalteringfood webs
(Francisetal.,2009).Infact,arecentstudyindicatesthatarthro-
podschangespaceuseinanaturalgas fieldinresponseto noise
(Bunkleyetal.,2017).
Songbirdspecies thatproduce lowerfrequency songsexhibit a
strongeravoidanceresponsetoanthropogenicnoise(Francis,2015).
In our sagebrush songbird community, most species have simi-
larsong bandwidth andpeakfrequency(seeTableS3), apart from
hornedlarksthathaveaslightlybroaderbandwidthoffrequenciesin
theirsong.However,sagethrashers,aspecieswiththelowestpeak
frequencysonginourcommunity,showednoresponsetonoiseex-
posure. It s eems song cha racteri stics, al though showi ng intriguin g
trends with birdresponses, arenota predictorofthedistributional
shifts we quantified. Thus, the underlying mechanisms driving the
distributionalshiftsweobser vedremainunclear.
Alteredconspecificinteractions,perhapsdrivenbyvocalization-
mediated processes, such as interactions bet ween males (Kleist,
Guralnick,Cruz, &Francis, 2016)andmates(Halfwerket al.,2011),
might also underpinsome results from our study. It is conceivable
thatalteredabundancesofspeciesinthebirdcommunitymighthave
changedheterospecificinteractions,suchasalarmcallingnet works
(Grade&Sieving,2016),withcascadingconsequences.Furthermore,
noise could have altered stress hormones of individuals, either di-
rectly or indirectly, thus driving birds to abandon breeding sites
(Kleist ,Guralnick,Cruz,Lowry,&Francis,2018).Futureresearchinto
causes ofaltereddistributionsand thepotentialofsomespecies to
habituatetonoiseexposureisessentialtoprovidebetterpredictive
modelsoftraitsthatincreaseriskforwildlifeexposedtochronican-
thropogenicnoise.
The data we present here are important for management de-
cisions regarding where future noise-producing infrastructure is
placed andthecurrentimplementationofmitigationstrategies in
high-valu e habitats expo sed to noise. Energ y extract ion compa-
nies can d esign and build co mpressor eng ines to be quieter a nd
lower bandwidth(Motruik, 20 00) and placecompressor stations
where they will create the lowest noise footprint (Keyel et al.,
2018).Building noise-attenuating wallsaround existing compres-
sorstationswill reduceboththesound level(Francis et al., 2011)
and potent ially the bandwid th of noise that intru des onto adja-
cent wildli fe habitat (Hidak a, Beranek, & O kano, 1995). In some
areas, wa lls have alread y been built ar ound compre ssor stati ons,
decreas ing sound leve ls by 10 decibels (dB C) at 30 m (Francis e t
al.,2011).Ene rgydevelopmentandit sassociatedchronicnoiseex-
posure comes with anecological cost, and the current efforts by
theUS governmentto open drillingin protectedareas(The White
House,2017)willdegradethehabitatqualityofthesecriticaleco-
logical preser ves. One clear route to protec ting ecosystems is to
include noiseexposurethresholds in leasesofpublic landstoen-
ergy extractioncompanies.Ourstudyaddsto mounting evidence
indicating significant ecological effects of anthropogenic noise
exposurefor breedingbirdsandsupportstheassertionthatnoise
mitigationshouldbeimplementedinenergyextractionfieldspost
haste(Bayneetal.,2008;Blickleyetal.,2012;Francisetal.,20 09).
Thes ou ndsca pemus tb econsid er edifwe aretoh olist ica ll yp rotec t
ecologicalsystems.
ACKNOWLEDGEMENTS
Wethank Alexander Keyel for soundscapemodelling; the Idaho
ArmyNationalGuardforaccess tooursites;Krystie Miner,Brian
LeavellandHeidiWare forprojectinput;MichaelBrownlee,Nate
Azaved o, Leo Ohyama, Cydney Mid dleton, Annie Ba xter, Bailee
Riesberg, Kaisha Young, Jillian Greene, Carlie Levenhagen and
Patrick N iedermeyer for f ield assist ance; Keith Reinhar dt, Maria
Pacioret ty, Peggy Ma rtinez, Ma rie-Anne de Gr aaff, Clint Franci s
and Juliette Rubin for their intellectual and physical contribu-
tions; Damon Joyce for cus tom code; and Mitchell Levenhagen
for ever ything. We tha nk all the reviewe rs that help ed with the
editing process. We thank the American Philosophical Society
(Franklin Research Grant to CJWM), the National Park Ser vice
Natural S ounds and Night Sk ies Division (CESU Pl 3AC01172 to
JRB)andtheNationalScienceFoundation(CNH1414171to JRB)
forfunding.
AUTHORS’ CONTRIBUTIONS
E.C.M.,J.R.B. and C.J.W.M. designed the experiment and method-
ology;E.C.M.collected the data; E.C.M., J.R.B.,and C. J.W.M.ana-
lysed the data; E.C .M. and J.R .B. led the writingofthemanuscript.
Allauthorscontributedcriticallytomanuscriptdraftsandgavefinal
approvalforpublication.
DATA AVA ILAB ILITY STATE MEN T
Data available via the Dryad Digital Repository https://doi.
org/10.5061/dryad.7d069p5(CintoMejia,McClure,&Barber,2019).
ORCID
Elizeth Cinto Mejia https://orcid.org/0000-0002-1418-5494
Christopher J. W. McClure https://orcid.
org/0000-0003-1216-7425
Jesse R. Barber https://orcid.org/0000-0003-3084-2973
10
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CINTO MEJ IA ET Al .
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How to cite this article:CintoMejiaE,McClureCJW,Barber
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altertheabundanceofbreedingbirds:Evidencefroma
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