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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 Stable URL: http://www.jstor.org/stable/30033784 Accessed: 20/09/2009 20:38 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. 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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 LITERATURE CITED 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. 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