Download Effects of Habitat Fragmentation on Biodiversity

Effects of Habitat Fragmentation on Biodiversity
Author(s): Lenore Fahrig
Source: Annual Review of Ecology, Evolution, and Systematics, Vol. 34 (2003), pp. 487-515
Published by: Annual Reviews
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Annu. Rev. Ecol. Evol. Syst. 2003. 34:487-515
doi: 10.1146/132419
Copyright@ 2003 by AnnualReviews. All rights reserved
First publishedonline as a Review in Advance on August 14, 2003
FRAGMENTATION
ON
OFHABITAT
EFFECTS
BIODIVERSITY
LenoreFahrig
Instituteof Biology,CarletonUniversity,
Ottawa-Carleton
Ottawa,Ontario,
@carleton.ca
CanadaK1S5B6;email:LenorelFahrig
Key Words habitatloss, landscapescale,habitatconfiguration,
patchsize, patch
isolation,extinctionthreshold,landscapecomplementation
0 Abstract The literatureon effects of habitatfragmentationon biodiversityis
in difhuge. It is also very diverse,with differentauthorsmeasuringfragmentation
ferentways and,as a consequence,drawingdifferentconclusionsregardingboththe
is usuallydefinedas a
magnitudeand directionof its effects. Habitatfragmentation
landscape-scaleprocessinvolvingboth habitatloss and the breakingapartof habitat. Resultsof empiricalstudiesof habitatfragmentationare often difficultto interat the patchscale, not the
pretbecause(a) manyresearchersmeasurefragmentation
scale
and
most
researchers
measure
in ways thatdo not
(b)
landscape
fragmentation
distinguishbetweenhabitatloss and habitatfragmentation
per se, i.e., the breaking
apartof habitataftercontrollingfor habitatloss. Empiricalstudiesto date suggest
thathabitatloss has large,consistentlynegativeeffects on biodiversity.Habitatfragmentationper se has muchweakereffects on biodiversitythat are at least as likely
to be positive as negative.Therefore,to correctlyinterpretthe influenceof habitat
on biodiversity,the effects of these two componentsof fragmentation
fragmentation
mustbe measuredindependently.More studiesof the independenteffects of habitat
loss andfragmentation
per se areneededto determinethe factorsthatlead to positive
versus negativeeffects of fragmentationper se. I suggest that the term "fragmentation"shouldbe reservedfor the breakingapartof habitat,independentof habitat
loss.
INTRODUCTION
A recentsearchof the CambridgeScientificAbstractsdatabaserevealedover 1600
articlescontainingthe phrase"habitatfragmentation."The task of reviewingthis
literatureis dauntingnot only because of its size but also because differentauthors
use differentdefinitionsof habitatfragmentation,andthey measurefragmentation
in differentways and at differentspatialscales.
This diversity of definitions of habitatfragmentationcan be readily seen in
the titles of some articles. For example, "Impactsof habitatfragmentationand
1543-592X/03/1215-0487$14.00
487
488
FAHRIG
patchsize..." (Collingham& Huntly2000) suggeststhat habitatfragmentationandpatchsize aretwo differentthings.However,otherauthorsactuallyuse
patchsize to measurehabitatfragmentation
(e.g.,Golden& Crist2000,Hovel&
"The
effects
of
forest
and isolation..." (GoodLipicus2001).
fragmentation
man& Rakotodravony
that
forest
andisolationare
2000)suggests
fragmentation
in
contrast
to
authors
who
use
forest
isolation
as
a
measureof fordifferent,
est fragmentation
Mossman
&
Waser
Rukke
2001,
2000). "Effectof land
(e.g.,
cover,habitatfragmentation,and.. ." (Laakkonenet al. 2001) contrastswith many
authorswho equatelandscapefragmentation
with landcover(e.g., Carlson&
Hartman2001; Fuller2001; Gibbs 1998, 2001; Golden& Crist2000; Hargis
& Crist2001;Virg6s2001)."The
et al. 1999;Robinsonet al. 1995;Summerville
influenceof forestfragmentation
andlandscapepattern..."(Hargiset al. 1999)
as an aspectof landscape
contrastswith researchers
who definefragmentation
Wolff
et
al.
Trzcinski
et
al.
As
a finalexample,"Effects
1997,
1999).
pattern(e.g.,
habitatfragmentation
andconnectivity..."(Ims& Andreassen
of experimental
andconnectivitycanbe examinedin1999)suggeststhathabitatfragmentation
as "a diswhereas
some
researchers
actuallydefinefragmentation
dependently,
et
see
also
in
al.
1997;
(With
Young& Jarvis
ruption landscapeconnectivity"
2001).
availableon the effects
My goal in this reviewis to discussthe information
TomeetthisobjectiveI firstneedto exof habitatfragmentation
on biodiversity.
is conceptualized
and
aminethe differentways in whichhabitatfragmentation
measured.Of course,the conceptof biodiversityis probablyat least as wideHowever,I do not deal with
rangingas the conceptof habitatfragmentation.
the conceptof biodiversity.
the issues surrounding
Instead,I includeany ecological responsevariablethatis or can be relatedto biologicaldiversity(see
Table1).
I conducted
To determinecurrentusage of the termhabitatfragmentation,
a searchof the CambridgeScientificAbstracts(BiologicalSciences)database
"forest
on 11 April2002 for paperscontainingeither"habitatfragmentation,"
the
I
reviewed
in
the
title
of
or
paper.
fragmentation"
fragmentation,""landscape
of thejournalin which
in detailthemostrecent100resultingpapers,irrespective
in the
I
limited
this
search
to
paperscontaining"fragmentation"
theyappeared.
titleto ensurethatmy sampleincludedonlypapersthataredirectlyon thesubject
in Table1.
Theresultsaresummarized
of habitatfragmentation.
I then surveyedthe broaderecologicalliteratureto ask the following:How
andaretheeffects
on biodiversity,
strongaretheeffectsof habitatfragmentation
is generallythoughtto havea large,
negativeor positive?Habitatfragmentation
andis therefore
widelyviewedasanaspectof habitat
negativeeffectonbiodiversity
(Haila2002).However,as I show,thisconclusionis generallyvalid
degradation
fromhabitatloss.
thatareinseparable
of fragmentation
onlyforconceptualizations
Otherways of conceptualizinghabitatfragmentationlead to otherconclusions. I
end the paperwith recommendations.
EFFECTSOF HABITATFRAGMENTATION
the
in
(3) 3
Population
growth
1
0
1
1
1
0
0
1
1
1
1
patches
all
across
(4) 3
Movement/
dispersal
2
1
0
0
1
0
0
0
1
3
0
(5) 3
habitat
Individual
3
0
2
1
0
2
0
3
2
2
1
(averaged
(8) 3
turnover
Extinction/
5
0
1
3
1
0
0
1
0
8
(10) 7 5
interactions
Species
(response)
3
4
2
2
0
1
0
4
3
3
(15) 11 9
measures
Fitness
may
variable.
study
(biodiversity)
because
100
response
to
andadd
not
scale
or do
landscape
rows
variable
and
the
at
or
Columns
patch)
(12) 3 8
variability
Genetic
Biodiversity
Numbers
contain
scale
0
variables
more
each
summed
or
use
in
6
0
0
0
2
0
4
7
3
2
each
for
2
2
2
2
1
0
10 6
4
5
(fragmentation)
variable.
that
predictor
of
using
landscape.
patch.
100)
(individually
(of variable.
combination
single
single
scale
a
a
1 1 2 7
16 4 6
(26) 20 13 11 3 0
absence
Presence/
papers
given
patch
from of
from
the
the
biodiversity
studies.
1 1 2 1 9
fragmentation
one
7
5
7
6
number
17
14
(28) 21
Richness/
diversity
either
studied
at
information
information
than
thattotal
corridor
recent
the more
and
papers
areand
100
measured
represents
2 3 3 0 13 17 7 10
represents
of
(35) 26 21 14 11
density
Abundance/
of
be
studies
names
can
(8)
analysis variable
analysis
numbers
(60)
that
(10)
the the
(37)
in in thevariable
(28)
Summary(predictor)
(35)
(7)
connectivityare
(4)
only(42)scaled
1
(63)
patches
point after
point
variables
connectivityb
landscape
both
fragmentation
loss/amountof
(21)
quality
(22)
datadataentries
sizea isolationa
shapea scalec and
one
scales
Qualitative
TABLE Fragmentation
variables
Patch
Habitat
Patch
Patch
Patch
Patch aPredictor
landscape).
Structural
Edgea
Number
Matrix
than
Landscape
bIncludes
cEach
*Table
parentheses
dEach
studies*
489
490
FAHRIG
AND MEASUREMENT
CONCEPTUALIZATION
OF
HABITATFRAGMENTATION
Fragmentationas Process
Habitat
is oftendefined
asaprocessduring
which"alargeexpanse
fragmentation
of habitat
is transformed
intoa number
of smaller
totalarea,
patchesof smaller
isolated
fromeachotherbyamatrix
ofhabitats
unliketheoriginal"
etal.
(Wilcove
a landscape
canbe qualitatively
1986)(Figure1).By thisdefinition,
categorized
as eithercontinuous
continuous
or fragmented,
wherethe
habitat)
(containing
the
of
the
of
fragmented
landscape
endpoint
represents
process fragmentation.
on biodiversity
conform
Manystudiesof theeffectof habitat
fragmentation
to thisdefinition
some
of
at
"reference"
sites
bycomparing aspect(s) biodiversity
of
at
sites
within
withina continuous
to
the
same
landscape
aspect(s) biodiversity
a fragmented
et al.2002,Diaz
landscape
(e.g.,Bowers&Dooley1999,Cascante
et al.2001,MacNally&Brown2001,
et al.2001,Laurance
et al.2000,Groppe
& Waser2001,Renjifo1999,
Mahan& Yahner
1999,Morato2001,Mossman
et al. 1999).Frommysampleof 100recentstudies,
28%conducted
such
Walters
of continuous
versusfragmented
(Table1).Inthesestudlandscapes
comparisons
a landscape
beforefragmentation
ies, thecontinuous
(time
landscape
represents
a landscape
1 in Figure1) andthefragmented
following
landscape
represents
(time2 ortime3 inFigure1).
fragmentation
offragmentation
asaprocess,
tothedefinition
thisapproach
conforms
Although
it has two inherentweaknesses.First,becausehabitatfragmentationis a landscapescale process (McGarigal& Cushman2002), the sample size in such studies, for
questions about the effects of habitatfragmentationon biodiversity,is typically
1
2
3
time
where"alargeexpanseof habitatis
Figure 1 The processof habitatfragmentation,
totalarea,isolatedfromeach
of
smaller
a
number
of
smaller
transformed
into
patches
otherby a matrixof habitatsunlikethe original"(Wilcoveet al. 1986). Black areas
representhabitatandwhiteareasrepresentmatrix.
EFFECTS
OFHABITAT
FRAGMENTATION 491
andonefragmented
Withsucha
landscape
landscape.
onlytwo,i.e.,onecontinuous
inferences
about
the
effects
of
are
weak.
effectsof
fragmentation
Apparent
design,
could
be
due
to
other
differences
between
the
For
landscapes.
fragmentation easily
et
al.
found
consistent
Mac
differences
between
(2000)
vegetation
example, Nally
andreferencesitesandconcludedthatapparent
effectsof fragmentation
fragments
habitatdifferences
betweenthetwolandscapes.
onbirdscouldbeduetopreexisting
of habitatfragmentation
is strictlyqualitative,
Second,thischaracterization
i.e.,
eachlandscapecanbe in only one of two states,continuousor fragmented.
This
betweenthedegreeof habitat
designdoesnotpermitoneto studytherelationship
andthe magnitudeof the biodiversityresponse.Quantifyingthe
fragmentation
degreeof fragmentation
requiresmeasuringthe patternof habitaton the landin the fragmentation
literaturearisesmainly
scape.The diversityof approaches
fromdifferencesamongresearchers
in how theyquantifyhabitatfragmentation.
Thesedifferenceshavesignificantimplicationsfor conclusionsaboutthe effects
of fragmentation
on biodiversity.
Fragmentationas Pattern:QuantitativeConceptualizations
Thedefinitionof habitatfragmentation
aboveimpliesfoureffectsof theprocessof
on habitatpattern:(a) reductionin habitatamount,(b) increasein
fragmentation
numberof habitatpatches,(c) decreasein sizesof habitatpatches,and(d)increase
in isolationof patches.These foureffects formthe basis of most quantitative
measuresof habitatfragmentation.
measuresvarywidely;
However,fragmentation
someincludeonlyoneeffect(e.g.,reducedhabitatamountorreducedpatchsizes),
whereasothersincludetwoorthreeeffectsbutnotall four.
Does it matterwhichfragmentation
measurea researcher
uses?The answer
on
whether
the
different
effects
of
the
of
onhabitat
depends
process fragmentation
have
the
same
effects
on
If
we
can
draw
pattern
biodiversity. they do,
general
conclusionsaboutthe effectsof fragmentation
on biodiversityeven thoughthe
differentstudiesmakingup the fragmentation
literaturemeasurefragmentation
in differentways.As I showin Effectsof HabitatFragmentation
on Biodiversity,
thedifferenteffectsof theprocessof fragmentation
onhabitatpatterndonotaffect
in thesameway.Thishasledto apparently
conclusions
biodiversity
contradictory
abouttheeffectsof fragmentation
on biodiversity.
Inthissection,I reviewquantitativeconceptualizations
of habitatfragmentation.
Thisis animportant
steptoward
results.
reconcilingtheseapparently
contradictory
FRAGMENTATION
AS HABITAT
LOSS The most obvious effect of the process of
is theremovalof habitat(Figure1). Thishasled manyresearchers
fragmentation
to measurethe degreeof habitatfragmentation
as simplythe amountof habitat
on
the
Carlson
&
Hartman
2001,Fuller2001, Golden
remaining
landscape(e.g.,
& Crist2000,Hargiset al. 1999,Robinsonet al. 1995,Summerville
& Crist2001,
Virg6s 2001). If we can measurethe level of fragmentationas the amountof habitat, why do we call it "fragmentation"?
Why not simply call it habitatloss? The
492
FAHRIG
thewordinvokesmorethan
reasonis thatwhenecologiststhinkof fragmentation,
... not only causesloss of the amountof habihabitatremoval:"fragmentation
tat,butby creatingsmall,isolatedpatchesit also changesthe propertiesof the
habitat"
(vandenBerget al. 2001).
remaining
Habitatcanbe removedfroma landscapein manydifferentways,resultingin
manydifferentspatialpatterns(Figure2). Do somepatternsrepresenta higher
thanothers,anddoes this haveimplicationsfor biodidegreeof fragmentation
to
eitherof thesequestionsis "no,"thenthe conceptof
If
the
answer
versity?
is redundant
withhabitatloss. Theassertionthathabitatfragmenfragmentation
tationmeanssomethingmorethanhabitatloss dependson theexistenceof effects
to changesin the pattern
of fragmentation
on biodiversitythatcanbe attributed
define
of habitatthatareindependent
of habitatloss.Therefore,
manyresearchers
habitatfragmentation
as anaspectof habitatconfiguration.
AS A CHANGE IN HABITATCONFIGURATION In addition to loss
FRAGMENTATION
resultsin threeothereffects:inof habitat,the processof habitatfragmentation
creasein numberof patches,decreasein patchsizes, andincreasein isolation
thatgo beyondsimplyhabitatamountare
of patches.Measuresof fragmentation
generallyderivedfromtheseor otherstronglyrelatedmeasures(e.g., amountof
(McGarigalet al.
edge). Thereare at least 40 suchmeasuresof fragmentation
withtheamountof habi2002),manyof whichtypicallyhavestrongrelationships
tat as well as witheachother(Belisleet al. 2001, Boulinieret al. 2001, Drolet
& Chopping1996,Hargiset al. 1998,
et al. 1999,Gustafson1998,Haines-Young
et al. 1999)
et al. 1999,Wickham
Robinsonet al. 1995,Schumaker
1996,Trzcinski
(Figure3).
arenotwidelyrecogTheinterrelationships
amongmeasuresof fragmentation
do notseparatethe
Mostresearchers
literature.
nizedin thecurrentfragmentation
Thisleads
effectsof fragmentation.
effectsof habitatloss fromtheconfigurational
on bioto ambiguousconclusionsregardingthe effectsof habitatconfiguration
It
&
Franklin
Swenson
&
Crist
Summerville
2001,
2000). is also
diversity(e.g.,
studiesto reportindividualeffectsof fragmentation
commonfor fragmentation
therelationships
measureswithoutreporting
amongthem,whichagainmakesthe
resultsdifficultto interpret.
PROBLEM Similarproblemsarise when fragmentationis meaTHEPATCH-SCALE
is
suredat thepatchscaleratherthanthelandscapescale.Becausefragmentation
are
measurements correctly
a landscape-scale
process(Figure1), fragmentation
madeat the landscapescale (McGarigal& Cushman2002). As pointedout by
Delin & Andr6n(1999),whena studyis at the patchscale,the samplesize at
inferenceis
the landscapescale is only one, whichmeansthatlandscape-scale
not possible(Figure4; see Brennanet al. 2002, Tischendorf& Fahrig2000).
However,in approximately42% of recent fragmentationstudies, individualdata
points representmeasurementson individualpatches, not landscapes (Table 1).
Similarly,using a differentsampleof the literature,McGarigal& Cushman(2002)
EFFECTS
FRAGMENTATION 493
OFHABITAT
numberof patches
mean patchsize
mean isolation
A
numberof patches
mean patchsize
mean isolation
B
C
numberof patches
mean patchsize
mean isolation
D
numberof patches
mean patchsize
mean isolation
E
numberof patches
mean patchsize
mean isolation
Figure 2 Illustrationof habitatloss resultingin some,butnot all, of the otherthree
expectedeffects of habitatfragmentationon landscapepattern.Expectedeffects are
(a) an increasein the numberof patches,(b) a decreasein mean patch size, and
(c) anincreasein meanpatchisolation(nearestneighbordistance).Actualchangesare
indicatedby arrows.
494
FAHRIG
A
B
Size
Patches
of
Patch
Number
0
Mean
HabitatAmount(%)
100
0
C
HabitatAmount(%)
100
D
Distance
Edge
Neighbor
Nearest
0
Total
HabitatAmount(%)
100
0
HabitatAmount(%)
100
Mean
E
Patch
Largest
of
Size
0
HabitatAmount(%)
100
Figure 3 Illustrationof the typicalrelationshipsbetweenhabitatamountandvariousmeaIndividualdatapointscorrespondto individuallandscapes.Basedon
suresof fragmentation.
relationshipsin B61isleet al. (2001), Boulinieret al. (2001), Droletet al. (1999), Gustafson
(1998), Haines-Young& Chopping(1996), Hargiset al. (1998), Robinsonet al. (1995),
Schumaker(1996), Trzcinskiet al. (1999), andWickhamet al. (1999).
OFHABITAT
FRAGMENTATION 495
EFFECTS
Landscape-Scale
Study
Patch-ScaleStudy
Density
Patch
Population
in
in
PatchSize
Density
Population
Landscape
Habitat
AmountinLandscape
Figure 4 (A)Patch-scalestudy.Eachobservationrepresentsthe informationfroma single
patch.Only one landscapeis studied,so samplesize for landscape-scaleinferencesis one.
(B) Landscape-scalestudy.Eachobservationrepresentsthe informationfroma singlelandscape. Multiplelandscapes,with differentstructures,are studied.Here, sample size for
landscape-scaleinferencesis four.
estimatedthat more than 57% of all fragmentationstudies are at the patch scale.
Some researcherseven refer to patch-scalemeasuresas landscapefeatures(e.g.,
Fernandez-Juricic2000, Schweiger et al. 2000).
Patch size: an ambiguousmeasureof fragmentation The relationshipbetween
patch size and fragmentationis ambiguousbecause both habitatloss and habitat
fragmentationper se (i.e., the breaking apartof habitat,controlling for changes
in habitat amount) result in smaller patches (Figure 5). Using patch size as a
measureof habitatfragmentationper se implicitly assumesthatpatch size is independentof habitatamountat the landscapescale (e.g., Niemelai2001). However,
regions where patches are large often correspondto regions where there is more
habitat(Fernandez-Juricic2000, McCoy & Mushinsky 1999) (Figure 6). Ignoring potential relationshipsbetween a patch-scale measure (e.g., patch size) and
landscape-scalehabitatamountdoes not control for this relationship;it can lead
to misinterpretationof results.
496
FAHRIG
Habitat
loss
Habitat
fragmentation
perse
per se (independentof habitat
Figure 5 Bothhabitatloss andhabitatfragmentation
loss) resultin smallerpatches.Therefore,patch size itself is ambiguousas a measureof eitherhabitatamountor habitatfragmentation
per se. Note also thathabitat
se
to
isolation.
leads
reduced
patch
fragmentation
per
Patch isolation: a measure of habitat amount In the fragmentationliterature,
patch isolation is almost universallyinterpretedas a measureof habitatconfiguration. However, patch isolation is more accuratelyviewed as a measure of the
lack of habitatin the landscapesurroundingthe patch. The more isolated a patch
is, generally speaking, the less habitatthere is in the landscape that surrounds
it (Figure 7). Therefore,when translatedto the landscape scale, isolation of a
patch is a measure of habitatamountin the landscape,not configurationof the
landscape.
Bender et al. (2003) reviewed measures of patch isolation. All measures are
stronglynegatively related to habitatamountin the surroundinglandscape.The
most common measureof patchisolationis the distanceto the next-nearestpatch,
EFFECTS
OFHABITAT
FRAGMENTATION 497
B
A
1km
Figure 6 Landscapein southernOntario(fromTischendorf2001) showingthatregions
whereforestpatches(blackareas)are smalltypicallycorrespondto regionswherethereis
little forest.Compare(A) and (B), where(A) has smallpatchesandless than5%forestand
50%forest.
(B) has largerpatchesandapproximately
or "nearest-neighbor
distance"(e.g., Delin & Andr6n1999, Haig et al. 2000, Hargis
et al. 1999). Patcheswith small nearest-neighbordistancesaretypicallysituatedin
landscapescontainingmore habitatthan are patches with large nearest-neighbor
distances (Figure 7), so in most situationsthis measureof isolation is relatedto
habitatamountin the landscape.Anothercommon measureof patch isolation is
the inverseof the amountof habitatwithin some distanceof the patchin question
(e.g., Kinnunenet al. 1996, Maguraet al. 2001, Miyashitaet al. 1998). In other
words, patch isolation is measuredas habitatamountat the landscapescale. All
othermeasuresof patch isolation are a combinationof distancesto otherpatches
and sizes of those patches (or the populationsthey contain) in the surrounding
landscape(reviewedin Bender et al. 2003). As such they are all measuresof the
amountof habitatin the surroundinglandscape.
498
FAHRIG
N
I
jlN
I
I
I
N
N
1 km
Figure 7 Illustrationof the relationshipbetweenpatchisolationandamountof habitatin
the landscapeimmediatelysurroundingthe patch.Grayareasare forest.Isolatedpatches
(blackpatcheslabeled"I")aresituatedin landscapes(circles)containingless forestthanare
less isolatedpatches(blackpatcheslabeled "N").
MEASURING
HABITAT
FRAGMENTATION
PERSE How can we measurehabitatfragmentation independentof habitat amount? Some researchershave constructed
landscapes in which they experimentallycontrolledhabitatamountwhile varying habitatfragmentationper se (e.g., Caley et al. 2001, Collins & Barrett1997).
Researchersstudyingreal landscapeshave used statisticalmethodsto controlfor
habitatamount.For example,McGarigalandMcComb (1995) measured25 landscape indices for each of 30 landscapes.They statisticallycorrectedeach index
for its relationshipto habitat amount and then entered the corrected variables
into a PCA. Each axis of the resultingPCA representeda differentcomponentof
OFHABITAT
EFFECTS
FRAGMENTATION 499
landscapeconfiguration.In a similarapproach,Villardet al. (1999) measuredthe
numberof forest patches, total length of edge, mean nearest-neighbordistance,
and percent of forest cover on each of 33 landscapes.They used the residualsof
the statistical models relating each of the first three variables to forest amount
as measuresof fragmentationthat have been controlledfor their relationshipsto
habitatamount.
EFFECTSOF HABITATFRAGMENTATION
ON BIODIVERSITY
InthissectionI reviewtheempiricalevidenceforeffectsof habitatfragmentation
on biodiversity.This review is not limited to the 100 paperssummarizedin Table
1. The fragmentationliteraturecan be distilled into two majoreffects: the generally strong negative effect of habitatloss on biodiversity,and the much weaker,
positive or negative effect of fragmentationper se on biodiversity.Because the
effect of fragmentationper se is weakerthanthe effect of habitatloss, to detectthe
effect of fragmentationper se, the effect of habitatloss must be experimentallyor
statisticallycontrolled.
Effectsof HabitatLoss on Biodiversity
Habitatloss haslarge,consistentlynegativeeffectson biodiversity,
so researchers
who conceptualize
andmeasurefragmentation
as equivalentto habitatloss typhas largenegativeeffects.The negativeefically concludethatfragmentation
fects of habitatloss applynot only to directmeasuresof biodiversitysuch as
species richness(Findlay& Houlahan1997, Gurdet al. 2001, Schmiegelow
& Minkktinen2002, Steffan-Dewenter
et al. 2002, Wettstein& Schmid1999),
and
abundance
distribution
et al. 2001, Gibbs1998, Guthery
(Best
population
et al. 2001, Hanski et al. 1996, Hargis et al. 1999, Hinsley et al. 1995, Lande
& Calvo1999,Venier& Fahrig1996)andgeneticdiversity
1987,Sainchez-Zapata
(Gibbs2001),butalso to indirectmeasuresof biodiversityandfactorsaffecting
biodiversity.A model by Bascompte et al. (2002) predicts a negative effect of
habitatloss on populationgrowthrate. This is supportedby Donovan & Flather
are
(2002),whofoundthatspeciesshowingdecliningtrendsin globalabundance
morelikelyto occurin areaswithhighhabitatloss thanarespecieswithincreasing or stable trends.Habitatloss has been shown to reduce trophicchain length
(Komonen et al. 2000), to alter species interactions(Taylor & Merriam 1995),
and to reduce the numberof specialist, large-bodiedspecies (Gibbs & Stanton
2001). Habitatloss also negativelyaffectsbreedingsuccess(Kurkiet al. 2000),
dispersalsuccess(B61isleet al. 2001, Pither& Taylor1998,With& Crist1995,
With & King 1999), predationrate (Bergin et al. 2000, Hartley& Hunter 1998),
andaspectsof animalbehaviorthataffectforagingsuccessrate(Mahan& Yahner
1999).
500
FAHRIG
INDIRECT EVIDENCEOF EFFECTSOF HABITATLOSS Negative effects of habitat
loss on biodiversity are also evident from studies that measure habitatamount
indirectly,using measuresthat are highly correlatedwith habitatamount.For example, Robinson et al. (1995) found that reproductivesuccess of forest nesting
bird species was positively correlatedwith percentageof forest cover, percentage
of forest interior,and average patch size in a landscape.Because the latter two
variableswere highly correlatedwith percentageof forest cover, these all represent positive effects of habitatamounton reproductivesuccess. Boulinier et al.
(2001) found effects of mean patch size on species richness,local extinctionrate,
and turnoverrateof forestbirdsin 214 landscapes.Because meanpatchsize had a
0.94 correlationwith forestamountin theirstudy,this resultmost likely represents
an effect of habitatamount.
Patch isolation effects Patch isolation is a measureof the lack of habitatin the
landscapesurroundingthe patch(Figure7). Therefore,the many studiesthathave
shown negativeeffects of patchisolation on species richnessor presence/absence
representfurtherevidence for the strongnegativeeffect of landscape-scalehabitat
loss on biodiversity(e.g., McCoy & Mushinsky1999, Rukke2000, Virg6s 2001).
Benderet al. (2003) andTischendorfet al. (2003) conductedsimulationanalyses
to determinewhichpatchisolationmeasuresaremost stronglyrelatedto movement
of animalsbetween patches. They found that the "buffer"measures,i.e., amount
of habitatwithin a given bufferaroundthe patch,were best. This suggests a strong
effect of habitat amount on interpatchmovement. It also suggests, again, that
effects of patch isolation and landscape-scalehabitatamountare equivalent.
Patchsize effects Individualspecies have minimumpatchsize requirements(e.g.,
Diaz et al. 2000). Therefore,smallerpatchesgenerallycontainfewer species than
largerpatches (Debinski & Holt 2000), and the set of species on smallerpatches
is often a more-or-lesspredictablesubset of the species on largerpatches (e.g.,
Ganzhorn& EisenbeiB2001, Kolozsvary& Swihart1999, Vallan2000). Similarly,
the amountof habitaton a landscaperequiredfor species occurrencetherediffers
among species (Gibbs 1998, Vance et al. 2003), so landscapeswith less habitat
should containa subset of the species found in landscapeswith more habitat.
Despite this apparentcorrespondencebetween patch- and landscape-scaleeffects, the landscape-scaleinterpretationof patch size effects dependson the landscape context of the patch. For example, Donovan et al. (1995) found that forest
birds had lower reproductiverates in small patchesthanin large patches.If small
patches occur in areas with less forest, the reducedreproductiverate may not be
the result of patch size, but may result from largerpopulationsof nest predators
and brood parasitesthat occur in landscapeswith more open habitat(Hartley&
Hunter1998, Robinsonet al. 1995, Schmiegelow & Monkkinen 2002).
The numberof individualsof any species that a landbe
can
should
a positivefunctionof the amountof habitatavailableto
support
scape
EXTINCTIONTHRESHOLD
EFFECTS
OFHABITAT
FRAGMENTATION501
area
Proportional
hypothesis
size
Extinction
threshold
hypothesis
Population
0
HabitatAmount
of the extinctionthreshold
in comparison
to the
Figure8 Illustration
hypothesis
area
proportional hypothesis.
thatspeciesin thelandscape.However,severaltheoretical
studiessuggestthatthe
is notproportional;
habitatlevelbelowwhich
relationship
theypredicta threshold
the populationcannotsustainitself,termedthe extinctionthreshold(Bascompte
& Sole 1996,Boswellet al. 1998,Fahrig2001, Flather& Bevers2002, Hill &
Caswell1999,Lande1987,With& King1999;Figure8). Therehavebeenvery
few directempiricaltestsof the extinctionthresholdhypothesis(butsee Jansson
& Angelstam1999).
Notethatthepredictedoccurrence
of theextinctionthreshold
resultsfromhabitatloss, nothabitatfragmentation
studiessuggestthathabitat
perse. Theoretical
fragmentation
perse canaffectwheretheextinctionthresholdoccurson thehabitatamountaxis.Also, the effectsof habitatfragmentation
perse arepredictedto
increasebelow some level of habitatloss (see The 20-30%Threshold,below).
However,the occurrenceof the extinctionthresholdis a responseto habitatloss,
notfragmentation
in interpretation
of empirperse. Thishasledto someambiguity
ical literature.
Forexample,Virg6s(2001)foundthatpatchisolationaffectsbadger densityonlyforpatchesin landscapeswith<20%forestcover.As explained
above,patchisolationis typicallyanindexof habitatamountatthelandscapescale.
thisresultprobablysuggestsa thresholdeffectof forestloss on badger
Therefore,
the
density.Thisconclusionis differentfromthatof the author,who interpreted
isolationeffectas aneffectof habitatconfiguration.
Theinterpretation
is ambiguous becausetherelationship
betweenhabitatamountandpatchisolationwasnot
controlledin thisstudy.Similarly,Andr6n(1994)reviewedpatchsize
statistically
andpatchisolationeffectson population
densityandconcludedthattheseeffects
502
FAHRIG
increasebelow a thresholdamountof habitatin the landscape.Because patchsize
and isolation can be indicatorsof habitatamountat a landscapescale (see Patch
size: An Ambiguous Measureof Fragmentationand Patch Isolation:A Measure
of HabitatAmount, above), this result could be interpretedas an intensification
of the effects of habitatloss at low habitatlevels, i.e., it supportsthe extinction
thresholdhypothesis (Figure8). This resulthas also been viewed as evidence for
configurationeffects below a thresholdhabitatlevel (e.g., Flather& Bevers 2002,
Villardet al. 1999). Again, the interpretationis ambiguousbecause the relationships between patch size and isolation and amountof habitatsurroundingeach
patchwere not controlledfor.
Effectsof HabitatFragmentationper se on Biodiversity
In this section I reviewthe empiricalevidence for fragmentationeffects per se, i.e.,
for effects of "breakingapart"of habitaton biodiversity,thatareindependentof or
in additionto the effects of habitatloss. The 17 studiesin Table2 representall of the
empiricalstudies of fragmentationper se of which I am aware.Some theoretical
studiessuggest thatthe effect of habitatfragmentationper se is weak relativeto the
effect of habitatloss (Collingham& Huntley2000, Fahrig1997, Flather& Bevers
2002, Henein et al. 1998), althoughother modeling studies predict much larger
effects of fragmentationper se (Boswell et al. 1998, Burkey 1999, Hill & Caswell
1999, Urban& Keitt2001, With& King 1999;reviewedin Fahrig2002). All these
recent models predictnegativeeffects of habitatfragmentationper se, in contrast
with some earliertheoreticalwork (see Reasonsfor PositiveEffects of Fragmentation, below). The empiricalevidence to date suggests thatthe effects of fragmentationper se are generallymuch weakerthanthe effects of habitatloss. Unlike the
effects of habitatloss, and in contrastto currenttheory,empiricalstudies suggest
thatthe effects of fragmentationperse areatleast as likely to be positiveas negative.
The 17 empiricalstudieson the effects of habitatfragmentationper se (Table2)
range from small-scale experimentalstudies to continental-scaleanalyses. They
cover a range of response variables, including abundance,density, distribution,
reproduction,movement, and species richness. About half of the studies are on
forest birds; other taxa include insects, small mammals,plants, aquaticinvertebrates, and a virus, and other habitatsinclude grasslands,cropland,a coral reef,
and an estuary.
The 17 studies used a variety of approachesfor estimatingthe effect of fragmentationper se. In five of them, experimentallandscapeswere constructedto
independentlycontrolthe levels of habitatamountand fragmentationper se. Four
of these variedboth habitatamountand fragmentationper se, and one variedonly
fragmentation,holding the amountof habitatconstant.Threeof the 12 studies in
real landscapescomparedthe response variablein one large patch versus several
smallpatches(i.e., holdinghabitatamountconstant).In the remainingnine studies
in real landscapes,the effect of fragmentationper se was estimatedby statistically
controllingfor the effect of habitatamount.
EFFECTSOF HABITATFRAGMENTATION
503
of on
se
habitat
per
of
effect(s)
of
effects
for
negative
1
effect
effect
positive,
Direction
6
fragmentation
biodiversity
No
No
negative
4
negative
2
(Continued)
effect
negative positive,
positive,
2
2
No
Positive
Positive
4
controlling
i.e.,
se,
per
versus
lossse
per
habitat
of
fragmentation
effects
fragmentation
habitat
of
fragmentation
fragmentation
fragmentation
fragmentation
fragmentation
fragmentation
fragmentation
fragmentation
>
>
>
>
>
>
>
-
habitat n.a.a Amount
Relative
Amount Amount Amount
Amount
Amount
Amount
Amount
effects
the
homing
bird
success
and
owl:
(various):
presence/
species:
species:
species:
reproduction
forest
incidence
species:
responsetaxa
species
homing
abundance
spotted
bird bird bird
bird
andvirus:
and
forest
late-seral
forest
forest
forest
Tanager
forest
absence
presence/absence,
persistence,
111distribution
15 species:
14 presence/absence
15 presence/absence
Taxa
Northern
6 populations:
31 presence/absence
3 timeHanta
variable(s)
examined
that
studies
empirical
of
Summary
biodiversity
2 on
McComb
Merriam
landscapes
1998
&
&
al.
real
et
in
1983 1995
Middleton
McGarigal
Meyer
Studies
TABLE
amount Study
1999
al.
et
1999
2001
1999 1999 2001 al.
al.
et
al.
al.
al.
et
et
et
et
Rosenberg
Trzcinski
Drolet VillardBdlisleLanglois
504
FAHRIG
of on
se
per
effect(s)
of
(adult
(juvenile (total
richness)
endangered
effect
negative
positive
positive
1 density)
andspecies
1 survival),
2
No
biodiversity
fragmentation
Direction
positive
1
n.a.b
Positive Positive
Positive
versus
lossse
per
habitat
of
amount
>
fragmentation
fragmentation
fragmentation
>
>>
>
effects
fragmentation
stated
n.a.a
habitat
Relative
n.a.a
Amount
Not Amount
Fragmentation
Amountn.a.a
aggregation
species
abundance,
abundance,
spatial
varied.
density
abundance
speciesabundance
vole:
was
species
insects: and
juvenile
response
vole: reproductive
richness
commensals:
insects: insects.
(predator)
birds:
and crab:
the
of
coral
species
richness
density,
recruitment
endangered
adult
fragmentation
Clover
8
Grassland
Gray-tailed
Forest Meadow
Butterflies:
Taxa Blue
richness
variable(s)
survival,
richness,
density
rate,
only
2001
(Continued)
2
Lipcius
&
Hovel
TABLE Study
2002
al.
et
landscapes:
1997
1999
1997
Barrett
al.
& al.
et experimental
et
in
Wolff
Flather Collins
Tscharntke
Studies
distribution
1998
constant;
spatial
held
was
2002 was
2001
Forman
&
al.
al.
et
et
variable
amount
Caley With
Collinge
aHabitat
bResponse
EFFECTSOF HABITATFRAGMENTATION
505
The overall result from these studies is that habitat loss has a much larger
effect thanhabitatfragmentationper se on biodiversitymeasures(Table2). When
fragmentationper se did have an effect, it was at least as likely to be positive
as negative (Table2). Given the relatively small numberof studies and the large
variationin conditions among studies, it is not possible to tease apartthe factors
that lead to positive versus negative effects of fragmentationper se. However,
the positive effects of fragmentationcan not be explained as merely responses
by "weedy,"habitat generalist species. For example, the results reportedfrom
McGarigal& McComb (1995) are specificallylimited to late-seralforest species,
and Tscharntkeet al. (2002) found a positive effect of fragmentationper se on
butterfly species richness, even when they only included endangeredbutterfly
species.
THE 20-30% THRESHOLD Some theoretical studies suggest that the effects of frag-
mentationper se should become apparentonly at low levels of habitatamount,
below approximately20-30% habitaton the landscape (Fahrig 1998, Flather&
Bevers2002). Todate,thereis no convincingempiricalevidencefor thisprediction.
If the thresholddoes occur, it should result in a statisticalinteractioneffect between habitatamountand habitatfragmentationper se; such an interactionwould
indicate that the effect of fragmentationper se depends on the amountof habitat
in the landscape.Trzcinskiet al. (1999) tested for this interactioneffect but found
no evidence for it. The hypothesis that fragmentationeffects increase below a
thresholdof habitatamounthas not yet been adequatelytested.
REASONSFOR NEGATIVEEFFECTSOF FRAGMENTATION
PER SE
Negative
effects
of fragmentationare likely due to two main causes. First, fragmentationper se
implies a largernumberof smaller patches. At some point, each patch of habitat will be too small to sustain a local populationor perhapseven an individual
territory.Species that are unable to cross the nonhabitatportionof the landscape
(the "matrix")will be confinedto a large numberof too-small patches,ultimately
reducingthe overallpopulationsize and probabilityof persistence.
The second main cause of negative effects of fragmentationper se is negative
edge effects; more fragmentedlandscapescontainmore edge for a given amount
of habitat.This can increasethe probabilityof individualsleaving the habitatand
enteringthe matrix.Overallthe amountof time spent in the matrixwill be larger
in a more fragmentedlandscape,which may increase overall mortalityrate and
reduceoverallreproductiverateof the population(Fahrig2002). In addition,there
arenegativeedge effects due to species interactions.Probablythe most extensively
studied of these is increasedpredationon forest birds at forest edges (Chalfoun
et al. 2002).
REASONSFOR POSITIVEEFFECTSOF FRAGMENTATION
PER SE
More than half of
the effects of fragmentationperse thathavebeen documentedarepositive(Table2).
Some readerswill findthis surprising,probablybecausehabitatloss is inextricably
506
FAHRIG
includedwithin theirconceptualizationof habitatfragmentation.In this case even
if fragmentationper se has a positive effect on biodiversity,this effect will be
maskedby the large negativeeffect of habitatloss.
Haila (2002) describeshow the currentconcept of habitatfragmentationemerged fromthe theoryof islandbiogeography(MacArthur& Wilson 1967). The two
predictorvariablesin this theory are island size and island isolation, or distance
of the island from the mainland.When this theory was conceptually extended
from island archipelagosto terrestrialsystems of habitat patches, the concept
of isolation changed; isolation was now the result of habitatloss, and it representedthe distancefrom a patchto its neighbor(s),not the distanceto a mainland.
Because of its roots in island biogeography,isolation was viewed as representing habitat subdivision even though it was inextricably linked to habitat
loss.
However,a parallelresearchstream,which arose independentlyof the theory
of island biogeography,suggested thathabitatfragmentationcould have positive
effects on biodiversity.Huffaker's(1958) experimentsuggestedthatsubdivisionof
the sameamountof habitatinto manysmallerpieces can enhancethepersistenceof
a predator-preysystem. He hypothesizedthathabitatsubdivisionprovidestemporaryrefugiafor the prey species, where they can increasein numbersand disperse
elsewherebeforethepredatororparasitefindsthem.Theplausibilityof thismechanism was supportedby earlytheoreticalstudies(Hastings1977,Vandermeer1973).
Early theoreticalstudies also suggested that habitatfragmentationenhances the
stabilityof two-species competition(Levin 1974, Shmida& Ellner 1984, Slatkin
1974), and in an empiricalstudy,Atkinson& Shorrocks(1981) foundthatcoexistenceof two competingspecies couldbe extendedby dividingthehabitatintomore,
smallerpatches.Enhancedcoexistenceresultedfroma trade-offbetweendispersal
rateand competitiveability.This trade-off,along with asynchronousdisturbances
thatlocally removedthe superiorcompetitor,allowed the inferiorcompetitor(but
superiordisperser)to colonize the emptypatchesfirst,beforebeing laterdisplaced
by the superiorcompetitor(Chesson 1985). Otherresearcherssuggestedthathabitat subdivisioncould even stabilizesingle-speciespopulationdynamicswhen local
disturbancesareasynchronousby reducingthe probabilityof simultaneousextinction of the whole population(den Boer 1981; Reddingius& den Boer 1970; Roff
1974a,b).
Why has this earlywork,suggestingpositiveeffects of habitatfragmentationper
se, been largely ignored in the more recent habitatfragmentationliterature?One
reason is that later theoreticaland empirical studies (reviewedin Kareiva 1990)
demonstratedthat the predictedpositive effects of fragmentationper se depend
stronglyon particularassumptionsaboutthe relativemovementrates of predator
versusprey (or host versusparasite),the trade-offbetween competitiveabilityand
movementrate,andthe asynchronyof disturbances.It seems thatthe sensitivityto
these assumptions,alongwith the misrepresentationof patchisolationas a measure
of habitatsubdivision,led researchersto ignore the possibility thatfragmentation
per se could have a positive effect on biodiversity.
EFFECTS
OFHABITAT
FRAGMENTATION507
Thereareatleastfouradditional
possiblereasonsforpositiveeffectsof habitat
First,Bowmanet al. (2002)arguedthat,for
fragmentation
perse on biodiversity.
rateis a functionof the lineardimensionof a habitat
manyspecies,immigration
rate
patchratherthantheareaof thepatch.Forthesespecies,overallimmigration
shouldbe higherwhenthe landscapeis comprisedof a largernumberof smaller
patches(higherfragmentation
perse) thanwhenit is comprisedof a smallernumberof largerpatches.In situationswhereimmigration
is animportant
determinant
of population
this
could
result
in
a
effect
of
density,
positive
fragmentation
perse
on density.
Second,if habitatamountis held constant,increasingfragmentation
per se
smaller
distances
between
a
actuallyimplies
patches(Figure5).Therefore,positive
effectof fragmentation
perse couldbe dueto a reductionin patchisolation.
Third,manyspeciesrequiremorethanone kindof habitat(Law& Dickman
insectsandamphibians
oftenusedifferenthabitats
1998).Forexample,immature
thanthosetheyuse as adults.A successfullife cyclerequiresthatthe adultscan
moveawayfromthehabitatwheretheywererearedto theiradulthabitatsandthen
backto theimmature
habitatto layeggs.Theproximityof differentrequired
habitattypeswill determinethe ease withwhichindividualscanmoveamongthem.
Forexample,Popeet al. (2000)showedthatthe proximityof feedinghabitatto
of leopardfrogpopulations.
Pedlaret al.
breedingpondsaffectedthe abundance
washighestin landscapeswithintermediate
(1997)foundthatraccoonabundance
amountsof forest.Theysuggestedthatthislevel of forestmaximizedthe accessibilityto the raccoonsof bothfeedingareas(grainfields)anddenningsites in
forest.
Thedegreeto whichlandscapestructure
facilitatesmovementamongdifferent
habitat
was
labeled
required
types
"landscape
complementation"
byDunninget al.
For
the
same
amount
of
a
more
(1992).
habitat,
fragmentedlandscape(more,
smallerpatches,and moreedge) will have a higherlevel of interdigitation
of
differenthabitattypes.This shouldincreaselandscapecomplementation,
which
hasapositiveeffectonbiodiversity
et al.2002).
(Law&Dickman1998,Tscharntke
Finally,it seemslikely thatpositiveedge effectsare a factor.Some species
do showpositiveedge effects(Carlson& Hartman2001, Kremsater
& Bunnell
et al. 2001).Fora givenamountof habitat,morefragmented
land1999,Laurance
scapescontainmoreedge.Therefore,positiveedge effectscouldbe responsible
forpositiveeffectsof fragmentation
or distribution
of some
perse on abundance
species.
CONCLUSIONSAND FUTUREDIRECTIONS
Habitat Loss Versus Fragmentation
Mostresearchers
viewhabitatfragmentation
asa processinvolvingboththelossof
habitatandthebreakingapartof habitat.Thefactthatmostfragmentation
research
does not differentiatebetween these two effects has led to severalproblems.First,
508
FAHRIG
the apparentinconsistencyin the effects of a single process (fragmentation)gives
the impressionthat fragmentationeffects are difficultto generalize.In fact, generalizationis possible, but only for the separatecomponentsof fragmentation,not
for the combinedconceptof loss andbreakingapartof habitat.Empiricalevidence
to date suggests thatthe loss of habitathas large negative effects on biodiversity.
On the otherhand,the breakingapartof habitat,independentof habitatloss, has
ratherweak effects on biodiversity,which are as likely to be positive as negative.
Second, the merging of these two aspects of fragmentationhas obscuredthe
fact thatthe effects of habitatloss outweighthe effects of habitatfragmentationper
se. In fact, the effects of fragmentationper se areabsentor too small to be detected
in most empiricaltests to date.This is in contrastto severaltheoreticalpredictions
(Burkey1999, Hill & Caswell 1999, Urban& Keitt2001, With & King 1999) and
has importantimplicationsfor conservation.It suggests that conservationefforts
shouldfocus on habitatpreservationandrestoration.It also suggests thatresearch
in supportof particularconservationproblems should focus on determiningthe
amount of habitatrequiredfor conservationof the species of concern. The fact
that effects of fragmentationper se are usually small and at least as likely to be
positive as negative suggests that conservationactions that attemptto minimize
fragmentation(for a given habitatamount)may often be ineffectual.
Note, however,thatthis conclusion is preliminarybecause thereare still only a
small numberof relevantempiricalstudies.To my knowledgethereare,to date,no
studiesin tropicalregions of the effects of forestfragmentationper se (controlling
for habitatloss). Lauranceet al. (2002) concludedthatin Braziliantropicalforest
there are strong negative effects of forest edge on several taxa. These effects
are apparentlymuch strongerthan negative edge effects in temperatesystems
(Kremsater& Bunnell 1999). Negative edge effects could translateinto a negative
effect of fragmentationper se at the landscape scale because fragmentationper
se increases the amountof edge on the landscape.This suggests that effects of
fragmentationper se may be greaterin tropicalsystemsthanin temperatesystems.
This predictionremainsto be tested.
Third,ambiguousempiricalresultscould lead to errorsin modelingstudies.For
example,Donovan& Lamberson(2001) constructeda model to look at the effects
of habitatfragmentationon populationgrowthrate. They held amountof habitat
constantandvariedmeanpatchsize. Forinputparameterstheyused empiricalwork
suggestingthatreproductivesuccess increaseswithincreasingpatchsize. However,
as they point out, in these empiricalstudiespatch size was highly correlatedwith
habitatamountin the surroundinglandscape.It is not knownwhetherreproductive
success increaseswith increasingpatchsize when habitatamountin the landscape
is held constant.It could be that reproductivesuccess increases with amountof
habitaton the landscape,independentof habitatfragmentationper se. If this is
true,the resultsof the simulationmay be misleading.
These conclusions are based on the relatively small, but growing, numberof
empiricalstudiesthatseparatethe effects of habitatloss andfragmentationper se.
So far these studieshave been conductedon a limited set of taxa primarilywithin
EFFECTS
OFHABITAT
FRAGMENTATION509
NorthAmerica.Moreresearchis neededto determine
howgeneraltheconclusions
are(Harrison
& Bruna1999).
IS "FRAGMENTATION"
A USEFUL
TERM?The term"fragmentation"
is quickly los-
ing its usefulnessas moreandmoreeffectsof humanactivitiesareincorporated
intothissingleterm.Someauthorshaveevensuggestedthatsomespeciesare"indicatorsof fragmentation"
that
(e.g.,Hager1998,Niemeli2001).Theimplication
canbe indicatedby the declineof somespeciesor speciesgroup
fragmentation
habitatchanges
suggeststhatthe termis becominga catchallfor human-caused
thathavenegativeeffectson biodiversity.
As questionedby Haila(2002),"Isa
termfruitfulas a generic
conceptuallyambiguousandempiricallymultifaceted
of humaneffectson landscapes?"
description
I suggestthattheterm"fragmentation"
shouldbe limitedto thebreakingapart
of habitat.Habitatloss shouldbe calledhabitatloss; it has important
effectson
that
are
of
effects
of
habitat
biodiversity
independent any
fragmentation
per se.
Habitatfragmentation
shouldbe reservedforchangesin habitatconfiguration
that
resultfromthebreakingapartof habitat,independent
of habitatloss.
Implications for Biodiversity Conservation
Does ourknowledgeaboutfragmentation
effectshavegeneralimplicationsfor
conservation
of biodiversity,
simultaneous
conservation
of multiple
particularly
literatureprovidesstrongevidencethathabitatloss
species?The fragmentation
haslarge,consistentlynegativeeffectson biodiversity.
Thisimpliesthatthemost
is probably"Howmuchhabitat
important
questionforbiodiversityconservation
is enough?"Differentspeciesuse differentkindsof habitat,anddifferentspecies
of
requiredifferentamountsof habitatfor persistence.Therefore,conservation
all speciesin a givenregionrequiresidentifyingwhichspeciesin thatregionare
mostvulnerableto habitatloss (Fahrig2001,With& King1999)andestimating
the minimumhabitatrequiredfor persistenceof each of thesemostvulnerable
species.Thisdeterminesthe minimumhabitatamountsfor eachkindof habitat
in the region.In addition,manyspeciesrequiremorethanone kindof habitat
withina life cycle.Therefore,
thatmaintaintherequired
habitat
landscapepatterns
the differenthabitattypesas muchas possible,should
amounts,butintersperse
producethelargestpositivebiodiversity
response(Law& Dickman1998).
ACKNOWLEDGMENTS
I thankJeffBowman,JulieBrennan,
DanBert,Tormod
Burkey,NeilCharbonneau,
Jeff
Jochen
KathrynFreemark,
AudreyGrez, Houlahan,
Jaeger,MaximLarriv6e,
LutzTischendorf,
RebeccaTittler,PaulZorn,andmembersof theLandscape
Ecolat
Carleton
for
comments
on
an
earlier
version
of thismanuscript.
ogy Laboratory
Thisworkwas supported
by a grantfromthe NaturalSciencesandEngineering
ResearchCouncil of Canada.
510
FAHRIG
The AnnualReviewof Ecology,Evolution,and Systematicsis online at
http://ecolsys.annualreviews.org
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Andr6nH. 1994.Effectsof habitatfragmen- hierarchical
studyof habitatfragmentation:
tationon birdsandmammalsin landscapes responsesat theindividual,
patch,andlandof suitablehabitat: scapescale.Landsc.Ecol. 14:381-89
withdifferent
proportions
BowmanJ, CappuccinoN, FahrigL. 2002.
a review.Oikos71:355-66
B. 1981.Competition Patchsize andpopulation
AtkinsonWD,Shorrocks
density:theeffect
Ecol.6:9.
behavior.Conserv.
of immigration
resource:a simon a dividedandephemeral
ulationmodel. J. Anim.Ecol. 50:461-71
http://www.consecol.org/vol6/issl/art9
TA,Fahrig
BascompteJ, Sol6 RV. 1996. Habitatfrag- BrennanJM,BenderDJ,Contreras
L. 2002. Focalpatchlandscapestudiesfor
mentationandextinctionthresholdsin spawildlifemanagement:
optimizingsampling
tially explicit models.J. Anim.Ecol. 65:465effort across scales. In Integrating Land73
J.
scape Ecology into Natural ResourceManBascompteJ, PossinghamH, Roughgarden
in stochasticenvi2002.Patchypopulations
agement,ed. J Liu, WW Taylor,pp. 68Univ.Press.
MA:Cambridge
91.Cambridge,
criticalnumberof patchesforperronments:
480 pp.
sistence.Am. Nat. 159:128-37
A, FortinM-J.2001.In- BurkeyTV. 1999. Extinctionin fragmented
M, Desrochers
B61lisle
birth-death
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