Urbanization, Biodiversity, and Conservation

Author(s): Michael L. McKinney

Source: BioScience, Vol. 52, No. 10 (Oct., 2002), pp. 883-890
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Articles

Urbanization,
Biodiversit
and

Conservation

MICHAEL
L. McKINNEY

mong the manyhumanactivities that cause

abitat loss (Czech et al. 2000), urban development

producessome of the greatestlocal extinctionratesand frequentlyeliminatesthe largemajorityof nativespecies (Vale
and Vale 1976,Luniak1994,Kowarik1995,Marzluff2001).
Also, urbanizationis often more lastingthan other types of
habitatloss. Throughoutmuch of New England,for example, ecologicalsuccessionis restoringforesthabitatlost from
farmingand logging,whereasmost urbanizedareasin that
regionnot only persistbut continueto expandand threaten
otherlocal ecosystems(Steinet al. 2000).
Anothergreatconservationchallengeof urbangrowthis
that it replacesthe native species that are lost with widespread"weedy"nonnativespecies.This replacementconstitutes the processof biotic homogenizationthat threatensto
reducethe biologicaluniquenessof local ecosystems(Blair
2001). Urban-gradientstudiesshow that,for manytaxa,for
example,plants (Kowarik1995) and birds and butterflies
(BlairandLauner1997),the numberof nonnativespeciesincreasestowardcentersof urbanization,while the numberof
nativespeciesdecreases.
Thefinalconservationchallengeof sprawlis its currentand
growinggeographicalextent (Benfieldet al. 1999).A review
by Czechand colleagues(2000) finds that urbanizationendangersmore speciesand is more geographicallyubiquitous
in the mainlandUnited Statesthan any other human activity.Speciesthreatenedby urbanizationalsotend to be threatenedby agriculture,
recreation,roads,andmanyotherhuman
the uniquely far-reachingtransforemphasizing
impacts,
mationsthat accompanyurbansprawl.
About 50% of the US population lives in the suburbs,
with another30%living in cities (USCB2001). Over5% of
the totalsurfaceareaof the UnitedStatesis coveredby urban
andotherbuilt-upareas(USCB2001).Thisis morelandthan
is coveredby the combinedtotal of nationaland stateparks
and areaspreservedby the NatureConservancy.More ominously, the growth rate of urban land use is accelerating
fasterthan land preservedas parksor conservationareasby
the Conservancy(figure1). Muchof this growthis fromthe

THE IMPACTSOF URBANIZATION

ON
NATIVESPECIES
AREPOORLYSTUDIED,
BUT EDUCATING
A HIGHLYURBANIZED
HUMANPOPULATION
ABOUTTHESE
IMPACTSCAN GREATLY
IMPROVESPECIES
CONSERVATION
IN ALLECOSYSTEMS

spread of suburbanhousing. It is estimated,for example,

that residentialyards occupy 135,000 acres in the state of
Missouri(MDC 2002).This residentiallandscaperepresents
nearly1%of the totalareaof Missouriandis nearlythreetimes
the areaoccupiedby Missouristateparks.
HereI reviewthe growingliteraturethat documentshow
urban (and suburban)expansionharmsnativeecosystems.
This knowledgecan aid conservationeffortsin two major
ways.One is throughthe use of ecologicalprinciples-such
aspreservingremnantnaturalhabitatand restoringmodified
habitatsto promotenativespeciesconservation-to reduce
the impactsof urbanizationon nativeecosystems.Rareand
endangeredspeciessometimes occur in urbanizedhabitats
(Kendleand Forbes1997,Godefroid2001) andthus couldbe
conservedthere.Managingthelargeamountof residential
vegetation(1%of the statearea,asnotedabove)in waysthatpromote nativeplantsand animalscould alsomakea significant
contributionto conservation.

is a professor
MichaelL.McKinney(e-mail:mmckinney@utk.edu)
ofgeological
StudiesProgramat theDepartment
sciencesanddirectorof theEnvironmental
Knoxville,TN
of GeologicalSciences,Universityof Tennessee-Knoxville,
37996.His currentresearchinterestsfocuson theimpactsof urbanizationon
at theuniversity,he
In additionto hisprofessorialresponsibilities
biodiversity.
strivesto educatethegeneralpublicaboutconservationin all ecosystems.?
2002 AmericanInstituteof BiologicalSciences.

October2002 / Vol.52 No. 10 * BioScience 883

Articles 4
120

developed land
0
100

roundingnativeecosystemsas urban sprawlexpands.Generalpatternsthatemergefromthesestudies aredescribedbelow.

0
80-

nationalparks

Physical gradients. Physical

changes along the gradient

stronglyinfluenceavailablehabitat fornativespecies.A numberof
60
reviews(SukoppandWerner1982,
Medley et al. 1995, Pickettet al.
0
0
2001) show increases in these
O
40
0
physicalchanges,as one movestowardthe urbancore,in suchmet20
ricsas humanpopulationdensity,
state parks
A
road density, air and soil polluA
A
A
A
A
A
0
a0
tion,
averageambient temperam
Conservancy
ture
island"effect), aver("heat
2000
1995
1975
1985
1990
1980
1970
o1965
annual
rainfall, soil
age
Year
soil
compaction,
alkalinity,and
other
indicators
of
anthropogenic
Figure1. Amount of land coveredin the lower48 states, by category.Source:All data are
disturbance. The percentage of
of
the
Statistical
Abstract
United
States
the
Nature
Confrom
for
years shown, exceptfor
area that is impervious surface
servancydata, which isfrom Stein and colleagues(2000).
(pavement, asphalt, buildings)
rangesfrom well over 50%at the
A secondwayin whichthe studyof urbanecologycanserve
urbancoreto less than 20%at the fringeof urbanexpansion
conservationis by helping to develop a more ecologically
(figure2). In addition,the amount of subsidizedenergyand
informedpublic.Providinga well-informedpubliccouldbe
matterimported for use by humans and availableto other
the most importantapplicationof urbanecology,as a means
speciesincreasestowardthe urbancenter(Collinset al.2000,
Pickettet al. 2001).
of promotingeffectiveconservationof nativespecies(Kendle
and Forbes1997).Because80%of the Americanpubliclives
Habitat-loss gradient. Thesephysicalchangesproduce
in or nearurbanareas,therearemanyopportunitiesfor crea gradientof naturalhabitatloss that steepensfromruralaratingan informedpublicthatcanwieldenormouseconomic
eas towardthe urbancenter.As habitatis lost, it becomesinandpoliticalpressureto promoteconservationpolicies.Peocreasingly fragmented into more numerous but smaller
ple who live in urban environmentsoften have a greatapremnantpatches(Medleyet al. 1995,Collinset al.2000).The
preciationof manyurbanspecies,such as birds(Clergeauet
lost naturalhabitatis then replacedby four types of altered
al.2001).Indeed,residentsof suburbanand urbanareastend
habitatthatbecomeprogressivelymore common towardthe
to place a much highervalue on species conservationthan
urbancore.The four types of replacementhabitatarelisted
those living in ruralareas(Kellert1996).This is reflectedin
below, in order of increasing habitabilityto most native
voting behavior:Legislatorsfrom highly urbanizedstates
and districtstend to be more supportiveof strengtheningthe
species and decreasingproportion of coveragetowardthe
urban core. The latter three types are based on Whitney
EndangeredSpeciesAct (Mehmoodand Zhang2001).
(1985).
Unfortunately,these conservationopportunitiesarehinderedby the verypoor ecologicalknowledgeof typicalAmer1. Builthabitat:buildingsand sealedsurfaces,suchas
icanurbanites.A surveyof Texashigh schoolstudents,for exroads
the
misidentified
the
students
of
that
showed
60%
ample,
huof
and
that
as
a
rodent
ecologicalunderstanding
opossum
2. Managedvegetation:residential,commercial,and other
man effectson biotawasevenpoorer;only2%of the students
knew that raccoonstend to benefit from many human acregularlymaintainedgreenspaces
tivities (Adamset al. 1987).
3. Ruderalvegetation:emptylots, abandonedfarmland,
and othergreenspacethatis clearedbut not managed
The urban-rural gradient:

Generalpatterns

Urban-to-rural
gradientstudiesexaminechangesin plantsand
animalsalonga transectfromthe innercity to surrounding,
less-alteredecosystems;theyalso showwhathappensto sur884 BioScience a October2002 / Vol.52 No. 10

4. Naturalremnantvegetation:remainingislandsof original vegetation(usuallysubjectto substantialnonnative

plantinvasion)

oArticles
Diversity changes
along the
urban-rural
gradient

It is probablyintuitiveto even
the most casualobserverthat
the increasingfragmentation
of naturalhabitatby human
disturbancesin the direction
toward urban centers will
tend to reduce species richness (number of species) in
thatdirection.Thereare,however,manyvariablesthat can
affectthe rateandconsistency
of speciesloss along the gradient,so empiricalstudiesare
crucial in measuring urban
impacts.

Urban core, low diver-

Conservation
strategies
Restoremanagedandruderalhabitats
Acquireremnanthabitats

Species
richness

Rural
Surfacearea
Urban biotas
Examples

Urbanfringe
< 20%impervious

Suburbia
20%-50%impervious

Avoiders

Adapters

Forestinteriorspecies

Edgespecies

Urbancore
> 50%impervious
Exploiters
Commensals

gradient.Thisis a verygeneralizedandsimplifieddepictionof changes

Figure2. Urban-rural

sity. Manystudiesdocument in surfacearea,speciesrichness,andcomposition,

as compiledfroma numberof sourcesdisthat the lowestspeciesdivercussedin thetext.Twobasicconservation
strategieswithrespectto urbansprawlareshownat
sities along the urban-rural
thetop.
gradientoccur in the intensively"built"environmentsof
the urbancore.This has been shown for manytaxa,including, and other common landscapingpracticesfurther rethe volume of the remainingvegetation(Gilbert1989,
duce
and
butterflies
birds
(Blair2001),
ing plants(Kowarik1995),
Adams
and
Schmidt
insects
1994).
1998, McIntyre2000),
(Denys
many
and mammals (Mackin-Rogalskaet al. 1988). In all these
Suburbandiversity:Peakorplunge?Somestudiesintaxa,the numberof speciesat the urbancoreis reducedto less
dicate
that speciesrichnesstends to be higher in areaswith
at
the
natural
areas
in
more
the
of
that
found
half
than
rural,
to
moderatelevelsof human development(such as outlow
end
of
the
gradient(figure2).
opposite
suburban
bird
7
resident
found
summer
for
Blair(2001), example,
developments)thanin morenaturalruralarlying
just
as
eas
such
Califorof
Palo
Alto,
preserves.This suburbanpeakin speciesnumbers
speciesin the centralbusinessdistrict
in
evident
is
area
a
natural
nia, comparedwith 21 speciesthat inhabited
manytaxa,such as mammals(Raceyand Euler
butterflies(Blair2001),bumblebees(Pawliand
birds
1982),
(preserve)outside the city limits. Similarreductionswere
Pokorniecka
and
kowski
1990),ants(NuhnandWright1979),
found for birds and butterfliesin other cities, as shown by
and
lizards(Germaine Wakeling2000), and plants(Kowarik
Blair's(2001), and especiallyby Marzluff's(2001), comprehensivecompilationof studieson urbanizationimpactson
1995).
An explanationoften suggestedfor this suburbanpeak
birds.
Much of the reductionin richnessis obviouslycausedby
(e.g., Blairand Launer1997,Germaineand Wakeling2000,
Blair2001) is the intermediatedisturbancehypothesis.The
the loss of vegetation.The numberof speciesof animaltaxa,
initial human impacts of suburbansprawlare sometimes
such as birds (Shugartet al. 1975) and insects (Majer1997),
tendsto correlatewith the numberof plantsin an area.Also,
relativelymild, with only a few housing subdivisionsin a
habitat.Thispromotes
matrixof largelynaturalor agricultural
area covered by vegetation is a good predictor of species
environmentalheterogeneity,becausedifferenthabitatsocnumbers for birds (Goldsteinet al. 1986); mammals,amcur alongsideone another.Suchhabitatdiversityis enhanced
phibians,and reptiles(Dickman1987);andinsects(McIntyre
the factthat individualhomeownersoften makeindividby
2000).
ualisticchoicesin the plantsthat they cultivate(Henderson
As over80%of most centralurbanareasis coveredby paveet al. 1998).
ment and buildings (Sukopp and Werner 1982, Blair and
In addition to providingspatialheterogeneity,these anLauner1997),less than 20%,therefore,remainsas vegetated
area. Furthermore,the remainingvegetatedhabitat often
thropogenichabitatsaretypicallyveryproductive(Falk1976),
containslow plantdiversityas a resultof erosion,trampling,
being highly subsidized in scarce resources,ranging from
waterto nutrients(e.g.,fertilizers).Cultivatedplantsinclude
pollution,invasionor cultivationof a few nonnativespecies,
and many other human disturbances.Also, mowing, prunmanyornamentalsthatoftenbearfruitsandseedsthatareutiOctober2002 / Vol.52 No. 10 * BioScience 885

Articles
lized by animals,especiallybirdsand bats (Munyenyembeet
al. 1989,Adams1994).Some animalshaveadaptedto the directconsumptionof humanresources(Adams1994)thatare
providedaccidentally(garbage)or intentionally(birdfood).
In contrastto the above,otherstudiesshowthatsuburban
areashavereducedspeciesdiversitycomparedto less-altered
ruralhabitats(figure2). Forexample,Marzluff's(2001)compilationof 51 birdstudiesfound that31 of the studies(61%)
showedlower speciesrichness in suburbanand other areas
of human settlement,comparedwith more naturalruralareas. The remaining20 studiesreportedeitheran increaseor
no change in diversitywith increasinghuman settlement.
The 51 studiescovereda wide rangeof geographicand natural settings,so it is difficultto identifywhich variablesdeterminewhethera riseor fallof speciesrichness occurswith
increasingsettlementand suburbandevelopment.
Teasingapartthesevariables,suchasthe roleof the natural
setting,is clearlya priorityfor furtherwork on urban-rural
gradients.Bell (1986), for example,has suggestedthat urbanizationin a tropicalrainforestmayhavedifferenteffects
on local speciesrichnessthan urbanizationin other natural
settings,becauserainforestbirdshaveexceptionaldifficulty
adaptingto human settlements.

Local extinctions during housing development.

Areasof activedevelopmenttendto havelow biodiversitybecauseof the devastatingimpacton nativespeciesof most residentialand commercialdevelopmentmethods.Beforeconstructionof most residentialand commercialbuildings,it is
common for developersto removemost vegetationand even
topsoil (Sharpeet al. 1986).This reducesconstructioncosts
by allowingequipmentreadyaccessto the constructionsite.
A studyof the fateof naturalvegetationduringurbandevelopmentin Wisconsinfound that only aboutone-thirdof
the originalvegetationwasnot destroyed(Sharpeet al. 1986).
The loss of nativevegetation(and totalvegetatedarea)has a
negativeimpacton nativeanimaldiversity.Birdspeciesrichness declineddramaticallyin the earlystagesof housingconstruction(comparedto preconstruction
diversity)in California
(Valeand Vale 1976) and Poland(Luniak1994).
Once constructionis finished,some of the areais paved,
which removes it as habitat for nearly all species. In Palo
Alto, California,for example,25% of the areaof residential
communitiesis coveredby pavement(BlairandLauner1997);
another20%of the areais coveredwith housing.Of the remainingnonpavedportions,much is replantedwith (usually
nonnative) grasses,shrubs, and trees (Wasowskiand Wasowski2000).
Conservation strategies. Habitatconservationcan utilize preservationand restoration(figure2). The most effective (and cheapestin the long term) strategyis to preserveas
much remnantnaturalhabitatas possible.Manystudiesdescribehow native species richnessin a remnanthabitatincreaseswiththe areaof thathabitat.Thisis trueformanytaxa,
886 BioScience * October2002 / Vol.52 No. 10

includingbirds(Tilghman1987),mammals(Dickman1987),
and plants (Dawe 1995).
One wayto preserveremnantsin housingdevelopmentsis
to retain predevelopmentvegetation.A number of recent
Revolution
books,suchas TheLandscaping
(WasowskiandWasowski2000), havepointed out the benefitsof retainingpreexistingvegetationwhen buildingnew homes.Unfortunately
for conservationgoals,this type of constructionis rarelyundertakenby most residentialrealestatedevelopers.Although
ostensiblyrelatedto cheapercosts of mass construction,retainingmore predevelopmentvegetationis less expensivein
the long term (Dorneyet al. 1986) and is preferredby many
homeowners(Wasowskiand Wasowski2000).
A majorinfluenceon naturalremnantsis the matrix,or the
type of habitat,thatsurroundsthem.Remnantsareoftenembeddedin a highlydisturbedmatrixthat also servesas a continuous source of nonnative species.A major challengeis
that remnanthabitatsareopen to colonizationby nonnative
speciesof invasiveplants(Luken1997)andpredatoryanimals
such as housecatsand dogs (Marzluff2001). These nonnative invadersand predatorscan greatlyreducethe abilityof
the remnant habitat to support native species, especially
birds.In the languageof populationbiology,theseremnants
become population"sinks"that are unableto support selfsustainingpopulationsof the nativespecies.

Restorationstrategies:Successionand cultivation.

Conservation strategy can also focus on restoring native

speciesin managedand ruderalhabitats.In naturalecosystems,bioticsuccessionincreasesthe numberof plantand animal speciesaftera disturbance(Gibsonet al. 2000). This is
alsotrueof ruderaland managedhabitatsthatremainundisturbedlong enough for successionto occur.Variousstudies
havedocumentedhow successionincreasesspeciesdiversity
in ruderalandmanagedcommunities,forexample,increased
plantdiversityin urbanlots (Crowe1979),increasedarthropod diversityin restoredcommunities(Majer1997),and increasedbirdspeciesrichnessin residentialcommunities(Vale
andVale1976,Munyenyembeet al. 1989,Luniak1994).As a
consequence,olderresidentialareas(usuallynearerthe urban
core)tend to havehigherspeciesrichnessthanyoungerones
(e.g., Munyenyembeet al. 1989).
The studiescitedaboveshowthatthe accumulationrateof
new speciesduringsuccessionis initiallyveryrapidandis substantiallyslowerafterthe first few yearsand especiallyafter
the first decades.Aside from increasingtotal diversity,ecological succession also often reducesthe diversityof nonnativespeciesin an area(Gibsonet al.2000), manyof which
relyon disturbanceto sustaintheirpopulations(Luken1997).
Anotherrestorationstrategyto increasenativebiodiversity
in managedhabitatsis to cultivatea varietyof plantspecies.
Cultivationwith nativeplantspeciesmaybenefitnot only nativeplantpopulationsbut alsonativeanimalpopulations.For
example, native bird species richness in Australia(Munyenyembeet al. 1989)andNorthAmerica(SearsandAnderson
1991)tendsto positivelycorrelatewiththe volumeandspecies

Articles
diversityof native vegetation. Similarly,the percentageof
nativeinsectspeciesin a faunahasbeenfoundto correlatewith
the percentageof native plant species (Crisp et al. 1998).
Landscapinggolf courseswith nativeplantscanbenefitmany
local nativebird species (Terman1997).

Compositionalchangesalong
the urban-ruralgradient

Speciesvaryin theirabilityto adaptto the oftendrasticphysical changesalong the urban-ruralgradient(Gilbert1989,

Adams 1994). Although there are probablymany ways to
categorizethese changesin speciescomposition,manybird
(e.g.,Goldsteinet al. 1986,Maedaand Maruyama1991,Blair
2001) and mammal(e.g.,Nilon andVanDruff1987) studies
haveconcludedthat speciesalongthe gradientcan be classified,for convenience,into threedistinctcategoriesreflecting
theirreactionto humanactivities.UsingBlair's(2001) terms,
these categoriesare"urbanavoiders,""urban
adapters,"and
"urban exploiters" (figure 2). While birds are the beststudiedtaxafor work on urban-ruralgradients,these three
categorieshavealso been used for work on butterflies(Blair
andLauner1997)andlizards(GermaineandWakeling2000).
Thesecategoriesshow that,even in highlymodifiedenvironments,speciesarenonrandomlyassembledin waysthat
approximatecommunityassemblyprocessesin nature.Each
of these assemblageshas a distinctiveset of ecologicalcharacteristicsthat reflectthe impactsof urbansprawlon native
species.One of the most importanttraitsthat separatesthe
three categoriesis the extent to which species depend on
human-subsidizedresourcesto exist in an area (Johnston
2001). As subsidizedresourcesincreasetoward the urban
core, there is a concurrent increase in species that utilize
them.Urbanexploitersaregenerallycommensalsthatarealmostentirelydependenton humansubsidies(i.e.,obligateparasites).Urbanadaptersareableto utilizesubsidiesbut arefacultativein that they also widely use natural(wild-growing)
resources.Urban avoiderstend to rely only on naturalresources(Johnston2001).

Characteristics
of urbanavoiders,adapters,and

exploiters. Becausebirds,mammals,and,to a lesserextent,

plantsarethe best-studiedtaxaalongurban-ruralgradients,
they will be the majorfocus here. Urbanavoidersarespecies
thatareverysensitiveto humanpersecutionand habitatdisturbances.The firstspeciesto disappearin the proximityof
humansareusuallylargemammals,especiallypredators,becausetheyareactivelypersecuted,relativelyrare,andhavelow
reproductiverates.Thus,cougars,bison,and elkwereamong
the first to disappear after European settlement began
(Matthiaeand Stearns1981).Avianurbanavoidersinclude
speciesadaptedto the interiorof large,old forests,suchastreeneotropicalmigrants,andmanygroundforaginginsectivores,
are
that
birds
verysensitiveto the presenceof humans
nesting
and pets (Whitcomb et al. 1981, Beissingerand Osborne
1982,Searsand Anderson 1991,Adams 1994).Plantspecies
thatareverysensitiveto humanactivitieswouldincludelate-

successional(old-growth) and wetland plants (Stein et al.

to our tendencyto clear
2000),the lossof whichis attributable
forests and drain wetlandsfor agriculturaland settlement
goals.
Urbanadapters
areoftenfoundin the matrixof humanland
usesthat occurin suburbanlandscapes.Forplants,earlysuccessionalspeciesarecommon in managedsuburbanhabitats,
such as residentialyardsand commercialas well as unmanagedruderalhabitats(e.g.,undevelopedlots).Theseearlysuccessionalplantsincludeboth cultivatedspeciesfavoredby humans (e.g., turfgrass,fast-growingornamentalshrubs,and
trees), as well as weedy species that are common in both
managedandunmanagedsuburbanhabitats.The most common weedy species are wind-dispersed lawn weeds (e.g.,
dandelions,crabgrass)and bird-dispersedinvasiveshrubs
(e.g.,privet,pokeweed)that commonlygrowon cleared,unsuburbanlandtendedlandscapes(Crowe1979).Botanically,
scapesareoften characterizedas structurallyapproximating
sparselyforestedsavannaor grasslandcommunities(Dorney
et al. 1984).Thisis apparentlyan aestheticallypreferredlandscapefor most suburbanites(Hendersonet al. 1998).
Among animals,urban adapterstypicallyinclude many
speciesoften referredto as "edgespecies,"which areadapted
to forestedgesand surroundingopen areas(Whitcombet al.
1981,Adams 1994). These animalsexploit many foods, infoods,suchascultivatedplantsand
cludinghuman-subsidized
of suchsubsidizedfoods is one
The
abundance
garbage. great
reasonwhytheseanimalurbanadaptersoftenattainan abundance and biomass that is much greaterthan in natural
areas(Adams1994,Marzluff2001).Anotherreasonis thatnaturalpredatorsof theseanimalsareusuallyeliminatedby human activities(Geringand Blair1999).
For birds, urban adaptersinclude a high proportion of
certainfeedingguilds.Theseincludeomnivoresand ground
foragers, such as the American robin and many corvids
(crows,jays);seedeaterssuch as finches;and aerialsweepers
such as swifts (Whitcomb et al. 1981, Beissingerand Osborne 1982,SearsandAnderson1991,Adams1994,Johnston
2001). Eachof these threeguilds seems to be respondingto
differentaspectsof humanimpacts.Thehighlyproductive(i.e.,
fertilized)lawn and ornamentalplant ecosystemprovidesa
rich source of invertebrateand plant foods (Falk 1976) for
groundgleaners,while seedeatersfavorbirdfeedingstations
and many ornamentalplants that produce seeds (Adams
1994).Aerialsweeperstakeadvantageof the manyopen areas, including pavement, over suburbanhabitats and the
high abundanceof manyflyinginsects,especiallythose that
areattractedto artificiallights.Tree,shrub,and cavitynesters
arealso common among urbanadapters(Johnston2001).
As most mammalslackthe highmobilityof flightpossessed
by birds,life in suburbanenvironmentsposes differentchallenges.Nevertheless,mammalianurbanadaptersareableto
find shelterfrom intensivehuman activityas well as exploit
rich sources of food provided by humans (Matthiae and
Stearns 1981, VanDruffand Rowse 1986, Nilon and VanDruff 1987).One groupof mammalianadaptersfindsrefuge
2002/ Vol.52 No. 10 * BioScience887
October

Articles
throughtheirburrowinghabits.Groundhogs,cottontailrabbits,moles,and skunksareexamplesof successfuladaptation
to human proximityin suburbia.Trophically,these animals
derivemuch food fromthe richsubsidiesof suburbanlawns,
includingrapidlygrowinggrasses,ornamentalplants,andinvertebrates(Falk1976).
Anothergroupof mammaladaptersincludesspeciesthat
require adjacentforest fragments (e.g., in cemeteriesand
parks)forshelter(Dickman1987).Thesespeciestypicallyforage for human-subsidized food supplies in surrounding
areas.Some are medium-sized omnivores (especiallyraccoons and opossums) that foragein garbage,vegetablegardens, and other resourcesprovidedby humans. Othersare
medium-sized carnivores,such as foxes and coyotes, that
consumea wide varietyof prey.As with birds,eliminationof
largepredators(in additionto subsidizedresources)leadsto
very high population densities of urban adaptermammal
species (Crooksand Soule 1999).
Urbanexploiters,often calledsynanthropes(e.g., Sukopp
and Werner 1982, Mackin-Rogalskaet al. 1988, Johnston
2001),arevery(oftentotally)dependenton humanresources.
The abundanceof urbanexploitersis usuallynot dependent
upon the amountor typesof vegetation(Lancasterand Rees
et al. 1988,
1979,Nilon andVanDruff1987,Mackin-Rogalska
Johnston2001).The combinationof predatorrelease(predator removal,suchasthe exterminationof wolvesand cougars)
with abundantfood subsidiesallowsthemto attainenormous
populationdensities(LancasterandRees1979,Adams1994).
Urbanexploitersprobablyrepresentthe mosthomogenized
of the world'sbiotas (Blair 2001). Unlike urban adapters,
which are largely composed of early successional species
fromnearbyecosystems,urbanexploitersarecomposedof a
very small subset of the world'sspecies;these exploitersare
welladaptedto intenselymodifiedurbanenvironmentswhereverhumansconstructthem acrossthe planet(Adams1994,.
Johnston2001, Marzluff2001).
Urbanenvironmentstypicallyhavemorein commonwith
other cities than with adjacentnaturalecosystems(Sukopp
andWerner1982),so urbanexploitersareoftennot nativeto
a region (Adams 1994,Kowarik1995,Blair2001), but tend
to leapfrogfromcityto city.Thus,rockdoves,starlings,house
sparrows,Norwayrats,and the house mouse arefound in all
cities in Europe (Mackin-Rogalskaet al. 1988) and North
America (Adams 1994). This is also true for urban plants
(Whitney 1985).
Among plants,urbanexploiterstend to be ruderalspecies
thatcan toleratehigh levelsof disturbance,especiallygrasses
and annuals(see reviewsin SukoppandWerner1982,Whitney 1985,Kowarik1995).Examplesincludewind-dispersed
weeds that colonize abandonedindustrialand commercial
propertiesand plants that can grow in and around pavement. Adaptivetraits that are typical of urban-exploiting
plantsincludetoleranceto high levelsof airpollution (especially smog and acidic fog); trampling;and alkaline,compacted,and nitrogenoussoils.
2002/ Vol.52 No. 10
888 BioScience- October

Avian urban exploiters are often species evolutionarily

adaptedto cliff-likerockyareasand thereforearepreadapted
to the devegetatedconcreteedificesof very urbanizedareas
(Lancasterand Rees 1979,Adams1994).Common examples
include the rockdove and peregrinefalcon.Another group
of avianexploitersconsistsof cavity-nestingspeciesthatare
ableto inhabithumandwellings.Examplesincludethehouse
sparrow,house finch, and Europeanstarling.Trophically,
avianurbanexploiterstend to be ground-foragingseedeaters
or omnivores(Lancasterand Rees 1979,Adams 1994).
Mammalian urban exploiters find shelter in human
dwellingsand exploitthe rich food sourcesin or nearthem.
Trophically,they areusuallyomnivorous(Adams1994)and
include such familiarspecies as the house mouse, black or
brown rat, and insects, including a variety of cockroach
species.

Increasingnonnativespeciestowardthe city.Many
studies have found that the number (and proportion) of
nonnativespeciestendsto increasealongthe urban-ruralgradient, moving towardthe urbancenter.In general,the proportion of speciesthatis nonnativegoes fromlessthan a few
percentin ruralareasto over 50% at the urban core.These
changingproportionsapply to plants in the United States
(Whitney1985)andEurope(Kowarik1995)andbirdsin the
United States(Blair2001). The population densityof nonet al. 1988)
nativespecies--bothmammals(Mackin-Rogalska
andbirds(Marzluff2001)-also tendsto increasethe nearer
they areto the urbancore.
The increasein nonnativespeciestowardthe urbancore
reflectsa numberof humancauses.One is thathigherhuman
populationdensitiesnearerthe urbancoreproduceincreasing importation("propagulepressure")of nonnativespecies,
for example,the cultivationof nonnative plants (MackinRogalskaet al. 1988,Kowarik1995).Anothercauseis the increasingamount of "disturbed"habitat toward the urban
core,which providesopportunitiesfor nonnativespeciesof
plants (Kowarik1995, Luken 1997) and animals (Adams
1994,Marzluff2001) that can utilizethe new resources.
Conservation implications of compositional

Kendle
changes. In theirbook UrbanNatureConservation,
andForbes(1997)notethat,ashighlyurbanizedareasaregenerallyoccupiedby speciesthat thrivein the presenceof humans, therewill be relativelyfew rarenativespeciesof conservationconcernin areasof high humanpopulationdensity.
They reviewsome examples,Jlowever,of rarespeciesof insects and plants found in highly urbanized areas;habitat
conservationand restorationcould be plannedfor sitesthat
most rarespeciesin urharborsuchspecies.Not surprisingly,
banizedareasarefound sitesthathaveescapedhigh-intensity
development(Godefroid2001).Siteswhererarespeciesmost
commonly occur include city parks, cemeteries, railroad
trackways,vegetated areas under transmission lines, and
other publicrights-of-waythat areprotectedfrom development (Gilbert1989,Kendleand Forbes1997).

oArticles
Asidefromthe conservationof rarenativespecies,knowledge of the speciescompositionof urbanbiodiversitycan be
veryusefulas an educationaltool to betterunderstandthe naturalworld.An enhancedappreciationof natureby the 80%
of the Americanpublic that lives in this environmentcould
promote more effectivepoliticaland economic action. Examplesof suchknowledgeincludebettereducationof thepublic in the naturalhistoryof local speciesand problemswith
nonnativespecies (Kendleand Forbes1997).

Conclusions
Urbanizationis a rapidlygrowing cause of many environmental problems (Benfieldet al. 1999). The impact of urbanizationis documentedin the growingliteratureon the
urban-ruralgradient.Thesestudiesshow consistentchanges
in speciesrichnessand speciescompositionalongthe gradient.
Species richness of many taxa often declines along the
gradient,with the lowest richnessto be found in the urban
core.Urbanplannersshould find waysto preservebiodiversity as cities expandoutwardand subsequentlymodify naturalhabitat.Sucheffortswouldmostlikelyfocuson preserving
as much remnantnaturalhabitatas possible,as opposed to
most currentland developmenttechniques,which remove
most naturalvegetationduringconstruction.
Whereintensiveland developmenthas alreadyoccurred,
native animalbiodiversitycan be increasedby revegetation
with a diversityof nativeplantspecies.Protectingthis revegetatedhabitatfromdisturbanceto allowecologicalsuccession
will not only enhance plant and animal diversitybut also
tend to reducethe diversityof nonnativespecies.Unfortunately,most current landscapingtends to revegetatewith
nonnative plant species in unnaturalspatial distributions
(Hendersonet al. 1998,Wasowskiand Wasowski2000) and
arrestssuccessionthroughthe managementof those ecosystems (at greatfinancialcost;Kendleand Forbes1997).
Speciescompositionalsoshowspronouncedchangesalong
the urban-ruralgradient.Most notable is that nonnative
morecommontowardthe urspeciesbecomeproportionately
ban core.Urbanavoidersincludenativespeciessuchas large
predatorsand forest-interior(especiallyinsectivorous)birds
that disappearquicklyin the initial stagesof suburbanencroachment,unlessspecialeffortis madeto retainlargetracts
of nativehabitatand reducehuman persecutionof species.
Urban adapters, mammals and birds that are mainly
adaptedto forestedgesand open areas,flourishin suburban
habitats,especiallyolder subdivisionswhereecologicalsucUrcessionhasadvancedandproducedextensiverevegetation.
for
are
ban adapters very important biodiversityeducation,
becausehalf of the Americanpubliclivesin a suburbanenvironment(USCB2001).Publicbiodiversityeducationwould
be most effectiveif we drawon thesefamiliarsuburbancommunity assemblagesand speciesto promotean understanding of conceptssuch as ecologicalsuccessionand the role of
nativeplantsin promotingnativeanimaldiversity.Because
of its enormous size,wealth,and politicalinfluence,a more

ecologically informed suburbanpopulation could greatly

improvethe socialsupportfor conservationof nativespecies
in all ecosystems.

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