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Copyright1973.Allrightsreserved

ECOLOGI
CAL
R SYSTEM
S
O
CS.Holling
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Instituteof
ResourceEcology,
Universityof
British
Columbia,Vancou
ver,Canada

INTRODUCTIO
N
Individualsdi
e,
populationsdi
sappear,and
species
becomeextinc
t.Thatisone
viewofthe
world.But
anotherview
ofthe
worldconcent
ratesnotso
muchon
presenceor
absenceas
uponthe
numbersof
organismsand
thedegreeof
constancyof
their
numbers.The
searetwo
ver s analytic
y y approachde
diff f velopedin
ere o one area
nt O becauseit
wa u was useful
yso and then
f transferred
vie to another
win whereit
gth maynotbe.
e Ourtraditional
beh viewofnatural
avi systems,therefor
oro e,mightwellbe
f lessa
sys meaningful
tem reality than
san aperceptual
d convenienc
the e.There can
use in
ful someyears
nes be
sof moreowls
the and fewer
vie miceand in
w others, the
dep reverse.
end Fish
sve populations
ry waxand
mu waneas a
cho natural
n condition,
the and insect
pro populations
per can range
ties over
extremestha
of
t only
the
logarithmic
1
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ne
2 HOLLING

transformationscaneasily
illustrate. Moreow:r,over
distinctareas,duringlong
or short periods of time,
species can completely
disappear and then
reappear. Different and
useful insight might be
obtained, therefore, by
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viewingthe behavior of
ecological systems in
termsoftheprobabilityof
extinction of their
elements,andbyshifting
emphasis from the
equilibrium states to the
conditions for
persistence.
Anequilibriumcentered
viewisessentiallystatic
andprovideslittleinsight
intothetransientbehavior
ofsystemsthatarenot
neartheequilibrium.
Natural,undisturbed
systemsarelikelytobe
continuallyinatransient
state;theywillbeequally
soundertheinfluenceof
man.Asman'snumbers
andeconomic
demandsincrease,hisuse
ofresourcesshifts
equilibriumstatesand
movespopulationsaway
fromequilibria.The
presentconcernsfor
pollutionandendangered
speciesarespecificsignals
thatthewellbeingofthe
worldisnota~dequately
describedbyconcentrating
onequilibriaand
conditio mightparadoxically
nsnear increasethechancefor
them. extinctions.
Moreov The purpose of this
er, reviewistoexploreboth
strategie ecologicaltheoryandthe
sbased behavior of natural
upon systemsto seeif different
these perspectives of their
two behavior can yield
differen different insights useful
t for both theory and
viewsof practice.
the
worldmi SomeTheory
ghtwell
be Letusfirstconsiderthe
antagon behavioroftwo
istic.It interactingpopulations:a
isat predatoranditsprey,a
least herbivoreanditsresource,
conceiv ortwocompetitors.Ifthe
ablethat interrelationsareatall
the regulatedwemightexpect
effectiv adisturbanceofoneor
eand bothpopulationsina
responsi constantenvironmentto
ble befollowedby
effortto fluctuationsthatgradually
provide decreaseinamplitude.
a Theymightberepresented
maximu asinFigure1,wherethe
msustai fluctuationsofeach
ned populationovertimeare
yield shownasthesidesofa
froma box.Inthisexamplethe
fish twopopulationsin
populati somesenseareregulating
onora eachother,butthelagsin
nonfluct theresponsegeneratea
uating seriesofoscillations
supply whoseamplitudegradually
ofwater reducestoaconstantand
froma sustainedvalueforeach
watersh population.Butifweare
ed(both alsoconcernedwith
equilibri persistencewewouldlike
toknownotjusthowthe
um
populationsbehaw:from
centered
oneparticularpairof
views)
starting difficultontimeplotsto
values, showthefullvarietyofre
but sponsespossible,andit
fromall provesconvenienttoplot
possible atrajectoryinaphase
pairs plane.Thisisshownbythe
since endoftheboxinFigure1
there wherethetwoaxes
mightw representthedensityof
ellbe thetwopopulations.
combin
ationsof Thetrajectoryshownon
starting thatplanerepresentsthe
populati sequentialchangeofthe
onsfor twopopulationsat
constanttimeintervals.
which
Eachpointrepresentsthe
ultimate uniquedensityof
lythe
each population at a
fateo["
particular point in time
oneor and the arrows indicate
otherof the direction of change
the over time. If oscillations
populati aredamped,asinthecase
onsis shown,thenthetrajectory
extincti isrepresentedasaclosed
on.It spiral that eventually
become reaches a stable equilib
svery rium.
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RESILIENCEANDSTABILITYOFECOLOGICALSYSTEMS 3
systemsimilartothatofFigure1,in
whichallpossibletrajectoriesinthe
phaseplanespiralintoan
equilibrium.Thesethree
examplesarerelativelysimpleand,
howeverrelevantforclassical
stabilityanalysis,maywellbe
theoreticalcuriositiesin
ecology.Figures2d2fadd
somecomplexities.Inasense
Figure2drepresentsacombinationof
aandc,witharegioninthecenterof
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I, thephaseplanewithinwhichall
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possibletrajectoriesspiralinwardsto
equilibrium.Thoseoutsidethis
regionspiraloutwardsandlead
eventuallytoextinctionofoneorthe
otherpopulations.Thisisan
exampleoflocalstabilityincontrast
totheglobalstabilityofFigure2c.I
designatethe
regionwithinwhichstabilityoccursas
thedomainofattraction,andtheline
thatcontainsthisdomainasthe
F boundary
i
oftheattractiondomain.
W ThetrajectoriesinFigure2e
e behaveinjustthe
F oppositeway.Thereisaninternal
i regionwithinwhichthetrajectories
spiralouttoastablelimitcycleand
beyond
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4 HOLLING
node,oreven
neutrallystable
orbits.AlthoughI
havepresumeda
constantworld
throughout,inlhe
presenceof
random
fluctuationsof
parametersorof
drivingvariables
E (Waiters39),any
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onetrajectory

I/ couldwanderwith
onlyitsgeneral
formapproaching
theshapeofthe
trajectoryshown.
X POPULATION
Theseadded
F complicationsare
i( exploredlater
e whenweconsider
w realsystems.For
h the
moment,however,l
etusreview
theoretical
treatmentsinthe
lightofthe
possibilities
suggestedin
Figure2.

The present
status of
ecological
stabilitytheoryis
very well
summarizedin a
numberof
analyses of
classical models,
particularly
May's(2325)
insightf 2 funclionaland
ul 4 numerical
analy responses,asin
ses of Holling(11)].
the Variousforms
Lotka havebeengiven
Volterr totheseterms;the
a familiarLotka
modela Volterramodel
nd its includesthe
exp~tns simplestandleast
ions, reaiistic,inwhich
the deathofpreyis
graphic causedonlyby
al predation,
stability predationisa
analyse
linearfunctionof
s of
theproductof
Rosenz
preyand
weig
(33,
34),
and the
method
ological
review
of
Lewont
in(20).
May(
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RESILIENCE ANDSTABILITYOFECOLOGICAL
SYSTEMS
p gnizesthebasicallydiscontinuous
r featuresofecologicalsystemsand
n incorporatesexplicitlags.
o NicholsonandBaileyinitiatedthis
T traditionwhentheydevelopeda
h modelusingtheoutputofattacksand
t survivalswithinonegenerationas
o theinputforthenext(29).The
T introductionthisexplicitlag
h generatesoscillationsthatincreasein
e amplitudeuntiloneorotherofthe
r speciesbecomesextinct(Figure2a).
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Theirassumptionsareas
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e
is unrealisticallysimpleasLotka'sand
a Volterra's;theinstabilityresults
n becausethenumberofattacking
o predatorsatanymomentissomucha
t consequenceofeventsinthe
h previousgenerationthatthereare
e "toomany"whenpreyaredeclining
r and"toofew"whenpreyare
tr increasing.Ifalagisintroducedinto
a theLotkaVolterraformulation
d (Wangersky&Cunningham40)the
it sameinstabilityresults.
i Thesenseonegains,then,ofthe
o behaviorofthetraditionalmodelsis
n thattheyareeithergloballyunstable
o or globally stable, that neutral
f
stability is very unlikely, and that
m
whenthe models are stable a limit
o
cycleisalikelyconsequence.
d
e Many,butnotall,ofthesimp!
ls ifyingassumptionshavebeenrelaxed
t insimulationmodels,andthereisone
h example(Holling&Ewing14)that
a joinsthetwotraditionsinitiatedby
t LotkaVolterraandNicholsonand
r Baileyand,further,includesmore
e realismintheoperationofthe
c stabilizinganddestabilizingforces.
o Thesemodificationsaredescribedin
moredetaillater;theimportantfeatures
accountingforthedifferenceinbehavior
resultfromtheintroductionofexplicit
lags,afunctionalresponseofpredators
thatrisesmonotonicallytoaplateau,a
nonrandom(orcontagious)attackby
predators,andaminimumpreydensity
belowwhichreproductiondoesnot
occur.Withthesechangesavery
differentpatternemergesthatconforms
mostcloselytoFigure2d.Thatis,there
existsadomainofattractionwithinwhich
thereisastableequilibrium;beyondthat
domainthepreypopulationbecomes
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6 HOLLING

extinct.UnliketheNicholsonandBaileymodel,thestabilitybecomes
possible,althoughinalimitedregion,becauseofcontagiousattack.
[Contagiousattackimpliesthatforonereasonoranothersomepreyhavea
greaterprobabilityofbeingattackedthanothers,aconditionthatis
cornmoninnature(Griffiths&Holling9).]Theinfluenceofcontagious
attackbecomessignificantwheneverpredatorsbecomeabundantin
relationtotheprey,forthenthesusceptiblepreyreceivetheburdenof
attention,allowingmorepreytoescapethanwouldbeexpectedby
randomcontact.This"inefficiency"ofthepredatorallowsthesystemto
counteractthedestabilizingeffectsofthelag.
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Ifthisweretheonlydifferencethesystemwouldbegloballystable,
muchasFigure2c.Theinabilityofthepreytoreproduceatlowdensities,
however,allows
someofthetrajectoriestocutthisreproductionthreshold,andtheprey
becomeextinct.Thisintroducesalowerpreydensityboundarytothe
attractiondomainand,atthesametime,ahigherpreydensityboundary
abovewhichtheamplitudesoftheoscillationsinevitablycarrythe
populationbelowthereproductionthreshold.Theothermodificationsin
themodel,someofwlhichhavebeentouchedonabove,alterthispicture
indegreeonly.Theessentialpointisthatamorerealisticrepresentation
ofthebehaviorofinteractingpopulationsindicatestheexistenceofat
leastonedomainofattraction.Itisquitepossible,withinthisdomain,to
imaginestableequilibriumpoints,stablenodes,orstablelimitcycles.
Whateverthedetailedconfiguration,theexistenceofdiscretedomainsof
attractionimmediatelysuggestsimportantconsequencesforthe
persistenceofthesystemandtheprobabilityofitsextinction.

Suchmodels,howevercomplex,arestillsosimplethattheyshouldnot
beviewed
inadefinitiveandquantitativeway.Theyaremorepowerfullyusedasa
startingpointtoorganizeandguideunderstanding.Itbecomesvaluable,
therefore,toask
whatthemodelsleaveoutandwhethersuchomissionsmakeisolated
domainsofattractionmoreorlesslikely.
Theoreticalmodelsgenerallyhavenotdonewellinsimultaneously
incorporatingrealisticbehavioroftheprocessesinvolved,
randomness,spatialheterogeneity,andanadequatenumberof
dimensionsorstatev~triables.Thissituationischangingveryrapidlyas
theoryandempiricalstudiesdevelopaclosertechnicalpartnership.In
whatfollowsIrefertorealworldexamplestodeterminehowthefour
elementsth~.ttendtobeleftoutmightfurtheraffectthebehaviorof
ecolo EXAMPLES
gical
syste SelfContained Ecosystems
ms. Inthebroadestsense,theclosestapproximationwecouldmakeofareal
worldexamplethatdidnotgrosslydepartfromtheassumptionsofthe
SOM theoreticalmodelswouldbeaselfcontainedsystemthatwasfairly
E homogenousandinwhichclimaticfluctuationswerereasonablysmall.If
REA suchsystemscouldbediscoveredtheywouldrevealhowthemorerealistic
L interactionofrealworldprocessescouldmodifythepatternsofsystems
WOR behaviordescribedabove.Verycloseapproximationstoanyofthese
LD conditionsarenotlikelytobefound,butifanyexist,theyareapttobe
fresh
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RESILIENCEANDSTABILITYOFECOLOGICALSYSTEMS7
w acceleratedandlimnologistshave
a recordedsomeoftheresponsesto
T thesechanges.Themostdramatic
h changeconsists
M ofbloomsofalgaeinsurfacewaters,
o anextraordinarygrowthtriggered,in
mostinstances,bynutrientadditions
fromagriculturalanddomestic
sources.
Whilesuchinstancesofnutrient
additionprovidesomeofthefew
examplesavailableofperturbation
effectsinnature,therearenocontrols
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andtheperturbationsareexceedingly
di~culttodocument.Nevertheless,the
qualitativepatternseemsconsistent,
particularlyinthoselakes
(Edmundson4,Hasler10)towhich
sewagehasbeenaddedforatimeand
thendivertedelsewhere.Thispulseof
disturbancecharacteristicallytriggers
periodicalgalblooms,low
oxygenconditions,thesudden
disappearanceofsomeplankton
species,andappearanceofothers.As
onlyoneexample,the,nutrient
changesinLakeMichigan(Beeton2)
havebeenaccompaniedbythe
replacementofthecladoceran
BosminacoregonibyB.Longirost~s,
Diaptomusoregonensishasbecome
animportantcopepodspecies,anda
brackishwatercopepodEuryternora
af~nisisanewadditiontothe
zooplankton.
In Lake Erie, whichhas been
particularly affected because of its
shallowness andintensity ofuse, the
mayfly Hexagenia, which originally
dominatedthebenthiccommunity,has
been almost totally replaced by
oligochetes.Therehavebeenblooms
of the diatom Mlosira binderana,
which had never been reported from
the
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8 HOLLING

United States until 1961 but nowcomprises as muchas 99%of the total
phytoplanktonaroundcertainislands.Inthosecaseswheresewagehasbeen
subsequentlydivertedthereisagradualreturntolessextremeconditions,the
slownessofthereturnrelatedtotheaccumulationofnutrientsinsediments.
Theoverallpatternemergingfromtheseexamplesisthesuddenappearance
or disappearance of populations, a wide amplitude of fluctuations, and the
establishmentofnewdomainsofattraction.
ThehistoryoftheGreatLakesprovidesnotonlysomeparticularlygood
informationonresponsestomanmadeenrichment,butalsoonresponses
offishpopulations
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tofishingpressure. Theeutrophicationexperiencetouchedonabovecanbe
viewedasanexampleofsystemschangesindrivingvariablesandparameters,
whereasthefishingexampleismoreanexperimentinchangingstatevariables.
The fisheries of the Great Lakes have always selectively concentrated on
abundantspeciesthatareinhighdemand.Priorto1930,beforeeutrophication
complicatedthestory,thelakesturgeoni'nalltheGreatLakes,thelakeherring
in Lake Erie, andthelakewhitefishinLakeHuronwereintensivelyfished
(Smith37).Ineachcasethepatternwassimilar:aperiodofintenseexploitation
duringwhichtherewasaprolongedhigh
'levelharvest,followedbyasuddenandprecipitousdropinpopulations.Most
significantly,eventhoughfishingpressurewasthenrelaxed,noneofthese
populationsshowedanysignofreturningtotheirpreviouslevelsofabundance.
Thisisnotunexpectedforsturgeonbecauseoftheirslowgrowthandlate
maturity,butitisunexpectedforherringandwhitefish.Themaintenanceof
theselowpopulationsinrecenttimesmightbeattributedtotheincreas:ingly
unfavorablechemicalorbiologicalenvironment,butinthecaseoftheherring,
atleast,thedeclinestookplaceintheearly1920sbeforethemajordeterioration
inenvironmentoccurred.Itisasifthepopulationhadbeenshiftedbyfishing
pressurefromadomainwithahighequilibriumtoonewithalowerone.Thisiis
clearlynotaconditionofneutralstabilityassuggestedinFigure2bsinceonce
thepopulationswereloweredtoacertainpointthedeclinecontinuedeven
thoughfishingpressurewasrelaxed.Itcanbebetterinterpretedasavariantof
Figure2dwherepopulationshavebeenmovedfromonedomainofattractionto
another.

Since1940therehasbeenaseriesofsimilarcatastrophicchangesinthe
GreatLakesthathasledtomajorchangesinthefi.,;hstocks.Beeton(2)
providesgraphssummarizingthecatchstatisticsinthelakesformanyspecies
since1900.Laketrout,whitefish,herring,walleye,sauger,andbluepikehave
experiencedprecipitousdeclinesofpopulationstoverylowvaluesin~tllofthe
lakes.Thechangesgenerallyconformtothesamepattern.Aftersustainedbut
 fluct peddramaticallyinaspanofaveryfewyears,coveringarangeoffromoneto
uatin fourordersofmagnitude.Inanumberofexamplesparticularlyhighcatches
g wereobtainedjustbeforethedrop.Althoughcatchstatisticsinevitably
level exaggeratethesteplikecharacterofthepattern,populationsmusthave
sof generallybehavedinthewaydescribed.
harve Theexplanationsforthesechangeshavebeenexploredinpart,andinvolve
stthe variouscombinationsofintensefishingpressure,changesinthephysicaland
catch chemicalenvironment,andtheappearanceofaforeignpredator(thesea
drop lamprey)and
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RESILIENCEANDSTABILITYOF
ECOLOGICALSYSTEMS9

foreigncompetitors(thealewifeandcarp).Forourpurposethespecificcauseis
lessinterestthantheinferencesthatcanbedrawnconcerningtheresilienceof
these~ystemsandtheirstabilitybehavior.TheeventsinLakeMichiganprovide
atypicalexampleofthepatterninotherlakes(Smith37).Thecatchoflake
troutwashigh,butfluctuatedataroundsixmillionpoundsannuallyfrom1898
to1940.Forfouryearscatchesincreasednoticeablyandthensuddenly
collapsedtonearextinctionbythe1950sduetoacompletefailureofnatural
reproduction.Lakeherringandwhitefishfollowedasimilarpattern(Beeton2:
Figure7).Smith(37)arguesthattriggerforthelaketroutcollapsewasthe
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appearanceofthesealampreythathadspreadthroughtheGreatLakesafterthe
constructionoftheWellandCanal.Althoughlampreypopulationswere
extremelysmallatthetimeofthecollapse,Smitharguesthatevenasmall
mortality,addedtoacommercialharvestthatwasprobablyatthemaximumfor
sustainedyield,wassufficienttocausethecollapse.Moreover,Ricker(31)has
shownthatfishingpressureshiftstheagestructureoffishpopulationstowards
youngerages.Hedemonstratesthatapointcancomewhereonlyslight
increasesinmortalitycantriggeracollapseofthekindnotedforlaketrout.In
addition,thelaketroutwascoupledinanetworkofcompetitiveandpredatory
interconnectionswithotherspecies,andpressuresonthesemighthave
contributedaswell.

Whateverthespecificcauses,itisclearthatthepreconditionforthecollapse
wassetbytheharvestingoffish,eventhoughduringalongperiodtherewere
noobvioussignsofproblems.Thefishingactivity,however,progressively
reducedtheresilienceofthesystemsotliatwhentheinevitableunexpectedevent
occurred,thepopulationscollapsed.Ifithadnotbeenthelamprey,itwould
havebeensomethingelse:achangeinclimateaspartofthenormalpatternof
fluctuation,achangeinthechemicalorphysicalenvironment,orachangein
competitorsorpredators.Theseexamplesagainsuggestdistinctdomainsof
attractioninwhichthepopulationsforcedclosetotheboundaryofthe
domaincanthenflipoverit.
Theaboveexamplesarenotisolatedones.In1939anexperimentalfishery
wasstartedinLakeWindermeretoimprovestocksofsalmonidsbyreducing
 the ationswereparticularlyaffectedbytrappingandthepopulationsfell
abun drasticallyinthefirstthreeyears.Mostsignificantly,althoughnoperchhave
danc beenremovedfromtheNorthBasinsince1947,populationshavestillnot
eof shownanytendencytoreturntotheirpreviouslevel(LeCrenetal19).
perch Thesamepatternshaveevenbeensuggestedforterrestrialsystems.Manyof
(a thearidcattlegrazinglandsofthewesternUnitedStateshavegradually
comp becomeinvadedanddominatedbyshrubsandtreeslikemesquiteandeholla.In
etitor someinstancesgrazingandthereducedincidenceoffirethroughfireprevention
)and programsallowedinvasionandestablishmentofshrubsandtreesattheexpense
pike ofgrass.Nevertheless,Glendening(8)hasdemonstrated,fromdatacollectedin
(a a17yearexperimentinwhichintensityofgrazingwasmanipulated,thatonce
preda thetreeshavegainedsufficientsizeanddensitytocompletelyutilizeor
tor). materiallyreducethemoisturesupply,eliminationofgrazingwillnotresultin
Perch thegrasslandreestablishingitself.Inshort,thereisalevelofthestatevariable
popul "trees"that,onceachieved,moves
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A ionofthetreesandshrubs.
nn Theseexamplespointtooneormoredistinctdomainsofattractioninwhich
ua theimportantpointisnotsomuchhowstabletheyarewithinthedomain,but
l howlikelyitisforthesystemtomovefromonedomainintoanotherandso
Re persistin
vi 1 changedconfiguration.
ew Thissamplingofexamplesisinevitablybiased.Therearefeweaseswell
s docu
mentedoveralongperiodoftime,andcertainlysomesystemsthathavebeen
w greatlydisturbedhavefullyrecoveredtheiroriginalstateoncethedisturbance
w wasremoved.Buttherecoveryinmostinstancesi.sinopensystemsinwhich
w.
an reinvasionisthekeyingredient.Thesecasesarediscussedbelowinconnection
nu with the effects of spatial heterogeneity. For the momentI conclude that
alr
ev distinctdomainsofattractionarenotuncommonwithinclosedsystems.Ifsuch
ie isthecase,thenfurther
ws
.or confirmationshouldbefoundfromempiricalevidenceofthewayprocesses
g/
ar whichlinkorganismsoperate,foritistheseprocessesthatarethecauseofthe
on behavior
lin
e observed.

10 Process Analysis
HOL
LING One way to represent the combinedeffects of processes like fecundity,
predation,andcompetitionisbyusingRicker's(30)reproductioncurves.These
simply represent the population in one generation as a function of the
the
populationinthepreviousgeneration,andexamplesareshowninFigures3a,c,
syste
and e. In the simplest form, and the one most used in practical fisheries
m
management(Figure 3a), the reproduction curve is domeshaped.Whenit
from
crosses a line with slope 1 (the straight line in the figures) an equilibrium
one
conditionispossible,foratsuchcrossoversthepopula
domai
nof POPULATIONIN GENERATIONt
attract
ionto
g,not
her.
Retur
nto
the
origin
al EQ ES EQ
domai
ncan
only
be
made
byan
explic
it
POPULATIONDENSITY
reduct
Figure3Examplesofvariousreproduction thecontributionsoffecundityand
curves(a,c,ande)andtheirderivationfrom mortality(b,d,andf).
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RESILIENCEANDSTABILITYOFECOLOGICALSYSTEMS11
t resultingcontributiontomortalityfrom
i theseresponsescantherefore
M showrangesofpreydensityinwhich
o thereisdirectdensity
o dependence(negativefeedbackfrom
r thepositivelyacceleratedportionsof
thetype3response),density
independence(thestraightlineriseof
type1),andinversedependence(the
positivefeedbackfromthenegatively
acceleratedandplateauportionsofthe
curves).Thereare,inaddition,various
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numericalresponsesgeneratedby
changesinthenumberofpredatorsas
thedensityoftheirpreyincreases.
Evenforthosepredators
whosepopulationsrespondby
increasing,thereoftenwillbealimitto
theincreasesetbyotherconditionsin
theenvironment.When
populationsareincreasingtheytend
toaugmentthenegativefeedback
features(althoughwithadelay),but
whenpopulationsareconstant,despite
increasingpreydensity,thepercent
mortalitywillinevitablydeclinesince
individualattackeventuallysaturates
atcompletesatiation(theplateauxof
allthreefunctionalresponses).In
Figures3dand3fthemortalitycurves
shownsummarizeacommontype.
Therisingordirectdensitydependent
limbofthecurveisinducedby
increasingpredatorpopulationsand
bythereducedintensityofattackat
lowdensities,shownbytheinitial
positivelyacceleratedportionofthe
Sshapedtype3response.Sucha
conditioniscommonforpredators
withalternateprey,bothvertebrates
(Holling14)andatleastsome
invertebrates(Steele38).The
declininginversedensitydependent
limbisinducedbysatiationofthe
predatorandanumericalresponse
 thathasbeenreducedorstopped. w designatedastheescapethreshold(ES
Fecunditycurvesthatdeclineregularly i inFigure3).Effectsofrandomchanges
overaverywiderangeofincreasing
populationdensities(asinFigure3d)are
commonandhavebeenreferredto
Drosophilatypecurves(Fujita6).This
declineinfecundityiscausedbyincreased
competitionforovipositionsites,interference
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12 HOLLING

populationsorparameterscouldreadilyshiftdensitiesfromaroundthelower
equilibrium to above this escape threshold, and in these circumstances
populationswouldinevitablyincreasetothehigherequilibrium.
Thefecunditycurvesarelikelytobemorecomplex,however,sinceit~seems
inevitablethatatsomeverylowdensitiesfecunditywilldeclinebecauseof
difficultiesinfindingmatesandthereducedeffectofavarietyofsocial
facilitationbehaviors.Wemightevenlogicallyconcludethatformanyspecies
thereisaminimumdensitybelowWhichfecundityiszero.Afecunditycurveof
thisAlicetype(Fujita6)hasbeenempiricallydemonstratedforanumberof
insects(Watt42)andisshownFigure3f.Itsinteractionwiththedomeshaped
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mortalitycurvecanaddanothertransientequilibrium,theextinctionthreshold.
(EXinFigure3f).Withthisadditionthereisalowerdensitysuchthatif
populationsslipbelowittheywillproceedinexorablytoextinction.The
extinctionthresholdisparticularlylikelysinceithasbeenshownmathematically
thateachofthethreefunctionalresponsecurveswillintersectwiththeordinate
ofpercentpredationatavalueabovezero(Holling13).
Empiricalevidence,therefore,suggeststhal;realisticformstofecundityand
mortalitycurveswillgeneratesinuousreproductioncurveslikethoseinFigures
3cand3ewiththepossibilityofanumberofequilibriumstates,sometransient
andsomestable.Thesearepreciselytheconditionsthatwillgeneratedomainsof
attraction,witheachdomainseparatedfromothersbytheextinctionandescape
thresholds.Thisanalysisofprocesshenceaddssupporttothefieldobservations
discussedearlier.

Thebehaviorofsystemsinphasespacecannotbecompletelyunderstoodby
thegraphicalrepresentationspresentedabove.Thesegraphsareappropriateonly
wheneffectsareimmediate;inthefaceofthelagsthatgeneratecyclicbehavior
thereproductioncurveshouldreallyproducetwovaluesforthepopulationin
generationt+Iforeachvalueofthepopulationingenerationt.Thegraphical
treatmentofRosenzweig&MacArthur(33)toadegreecanaccommodatethese
lagsandcyclicbehavior.Intheirtreatmenttheydividepha:seplanesofthekind
showninFigure2intovariousregionsofincreasinganddecreasingxandy
populations.Theregionsareseparatedbytwolines,onerepresentingthe
collectionofpointsatwhichthepreypopulationdoesnotchangeindensity
(dx/dt=0,thepreyisocline)andone
inwhichthepredatorpopulationdoesnotsochange(dy/dt=0,thepredator
 isocli domeshapedformuchthesamereasonasdescribedforthefecunditycurvesof
ne). Figure3f.Thepredatorisocline,inthesimplestcondition,ispresumedtobe
They vertical,assumingthatonlyonefixedlevelofpreyisnecessarytojustmaintain
dedu thepredatorpopulationatazeroinstantaneousrateofchange.
ce Intersectionofthetwoisoclinesindicatesapointwherebothpopulationsare
that atequilibrium.Usingtraditionallinearstabilit:analysisonecaninferwhether
the theseequilibriumstatesarestable(Figure2c)ornot(Figure2a).
prey Considerableimportanceisattachedtowhetherthepredatorisoclineintersects
isocli therisingorfallingportionofthepreyisocline.Asmentionedearlierthe'~e
ne techniquesareonlyappropriatenearequilibrium(May24),andthe
will presumedunstableconditionsinfactgeneratestablelimitcycles(Figure2e).
be Moreover,itisunlikelythatthepredatorisoclineis
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A withtheattackprocessthatalargernumberofpreywouldberequiredforstable
nn predatorpopulations.Itispreciselythisconditionthatwasdemonstratedby
ua Griffiths&Holling(9)whentheyshowedthatalargenumberofspeciesof
l parasitesdistributetheirattackscontagiously.Theresultisa"squabbling
Re predatorbehavior"(Rosenzweig34,35)thatdecreasestheefficiencyofpreda
vi tionathighpredator/preyratios.Thisconvertsanunstablesystem(Figure2a)
ew a stable one(Figure 2c); it is likely that stability is the rule, rather than the
s exception,irrespectiveofwherethetwoisoclinescross.
The empirical evidence described above showsthat realistic fecundity and
mortality (particularly predation) processes will generate forms that the
w
w theoristsmighttendtoidentifyasspecialsubsetsofmoregeneralconditions.
w. Butitisjustthesespecialsubsetsthatseparatetherealworldfromallpossible
an
nu ones, and these more realistic forms will modifythe general conclusions of
alr simplertheory.Theascending
ev
ie limboftheAlleetypefecunditycurvewillestablish,throughinteractionwith
ws
.or mortality,aminimumdensitybelowwhichpreywillbecomeextinct.Thiscanat
g/ the same time establish an upper prey density above whichprey will
ar
on becomeextinctbecausetheamplitudeofpreyfluctuationswilleventuallycarry
lin thepopulationovertheextinctionthreshold,asshownintheoutertrajectoryof
e
Figure 2d. These conditions alone are sufficient to establish a domainof
RESILIENCEANDSTABILI
attraction,althoughtheboundariesofthisdomainneednotbeclosed.Within
TYOF
thedomainthecontagiousattackbypredatorscanproduceastableequilibrium
ECOLOGICALSYSTEMS
13 orastablenode.Otherbehaviorsofthemortalityagents,however,couldresult
instablelimitcycles.
Morerealisticformsoffunctionalresponsechangethispatternindegreeonly.
verti
Forexample,anegativelyacceleratedtypeoffunctionalresponsewouldtendto
cal
makethedomainofattractionsomewhatsmaller,andanSshapedonelarger.
one
Limitationsinthepredator'snumericalresponseandthresholdsforreproduction
inthe
ofpredators,similartothoseforprey,couldfurtherchangetheformofthe
real
domain.Moreover,thebehaviorsthatproducethesinuousreproductioncurves
worl
ofFigures3cand3ecanaddadditionaldomains.Theessentialpoint,
d,
however,isthatthesesystemsarenotgloballystablebutcanhavedistinct
since
domainsofattraction.Solongasthepopulationsremainwithinonedomainthey
comp
haveaconsistentandregularformofbehavior.Ifpopulationspassaboundary
etitio
tothedomainbychanceorthroughinterventionofman,thenthebehavior
n
suddenlychangesinmuchthewaysuggestedfromthefieldexamplesdiscussed
betw
earlier.
een
preda
The RandomWorld
tors
at Tothispoint,Ihavearguedasiftheworldwerecompletelydeterministic.In
high fact,thebehaviorofecologicalsystemsisprofoundlyaffectedbyrandomevents.
preda Itisimportant,therefore,toaddanotherlevelofrealismatthispointto
tor determinehowtheaboveargumentsmaybemodified.Again,itisapplied
densi ecologythattendstosupplythebestinformationfromfieldstudiessinceitisonly
ties insuchsituationsthatdatahavebeencollectedinasufficientlyintensiveand
woul extensivemanner.Asoneexample,for28yearstherehasbeenamajorand
dso intensivestudyofthesprucebudwormanditsinteractionwiththesprucefir
interf forestsofeasternCanada(Morris
ere
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14 HOLLING

27).Therehavebeensixoutbreaksofthesprucebudwormsincetheearly1700s
(Baskerville1)andbetweentheseoutbreaksthebudwormhasbeenan
exceedinglyrarespecies.Whentheoutbreaksoccurthereismajordestructionof
balsamfirinallthematureforests,leavingonlythelesssusceptiblespruce,the
nonsusceptiblewhitebirch,andadenseregenerationoffirandspruce.The
moreimmaturestandssufferlessdamageandmorefirsurvives.
Betweenoutbreakstheyoungb~ilsamgrow,togetherwithspruceandbirch,to
formdensestandsinwhichthespruceandbirch,inparticular,sufferfrom
crowding.Thisprocessevolvestoproducestandsofmatureandovermature
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Thisisanecessary,butnotsufficient,conditionfortheappearanceofan
outbreak;outbreaksoccuronlywhenthereisalsoasequenceofunusuallydry
years(Wellington43).Untilthissequenceoccurs,itisargued(Morris27)that
variousnaturalenemieswithlimitednumericalresponsesmaintainthe
budwormpopulationsaroundalowequilibrium.Ifasequenceofdryyears
occurswhentherearematurestandoffir,thebudwormpopulationsrapidly
increaseandescapethecontrolbypredatorsandparasites.Theircontinued
increaseeventuallycausesenoughtreemortalitytoforceacollapseofthe
populationsandthereinstatementofcontrolaroundthelowerequilibrium.The
reproductioncurvesthereforewouldbesimilartothoseinFigures3cor3e.
Inbrief,betweenoutbreaksthefirtendstobefavoredinitscompetitionwith
spruceandbirch,whereasduringanoutbreakspruceandbircharefavored
becausetheyarelesssusceptibletobudwormattack.Thisinterplaywiththe
budwormthusmaintainsthespruceandbirchwhichotherwisewouldbe
excludedthroughcompetition.Thefirpersistsbecauseofitsregenerative
powersandtheinterplayofforestgrowthratesandclimaticconditionsthat
determinethetimingofbudwormoutbreaks.

Thisbehaviorcouldbeviewedasastablelimitcyclewithlargeamplitude,
butitcanbemoreaccuratelyrepresentedbyadistinctdomainofattraction
determinedbytheinteractionbetweenbudwormanditsassociatednatural
enemies,whichisperiodicallyexceededthroughthechanceconsequenceof
climaticconditions.Ifweviewthebudwormonlyinrelationtoitsassoc!~ated
predatorsandparasiteswemight
arguethatitishighlyunstableinthesensethatpopulationsfluctuatewidely.
Buttheseveryfluctuationsareessentialfeaturesthatmaintainpersistenceofthe
budworm,together,withitsnaturalenemiesanditshostandassociatedtrees.
By so fluctuating, successive generations of forests are replaced, assuring a
continuedfoodsupplyforfuturegenerationsofbudwormandthepersistenceof
thesystem.
UntilnowIhaveavoidedformalidentificationofdifferentkindsofbehavior
ofecologicalsystems.Themorerealisticsituat:ionslikebudworm,however,
makeitnecessarytobegintogivemoreformaldefinitiontotheirbehavior.Itis
usefu kindsofbehavior.Onecanbetermedstability,whichrepresentstheabilityofa
lto systemtoreturn'toanequilibriumstateafteratemporarydisturbance;themore
disti rapidlyitreturnsandthelessitfluctuates,themorestableitwouldbe.Butthere
nguis isanotherproperty,termedresilience,thatisameasureofthepersistenceof
h systemsandoftheirabilitytoabsorbchangeanddisturbanceandstillmaintain
two thesamerelationshipsbetweenpopulationsorstatevariables.Inthissense,the
AnnualReviews
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RESILIENCE ANDSTABILITYOFECOLOGICALSYSTEMS
15
b nsofattractionisfound
u inaquaticsystemsaswell.For
T example,pinksalmonpopulationscan
h becomestabilizedforseveralyearsat
e verydifferentlevels,thenewlevels
i beingreachedbysuddenstepsrather
n thanbygradualtransition(Neave28).
f Theexplanationisverymuchthesame
l asthatproposedforthe
u
budworm,involvinganinterrelation
e
betweennegativeandpositive
n
c feedbackmortalityofthekinds
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e describedinFigures3dand3f,and
o randomeffectsunrelatedtodensity.
f Thesamepatternhasbeendescribed
r byLarkin(18)inhissimulationmodel
a oftheAdamsRiversockeyesalmon.
n Thisparticularrunofsalmonhasbeen
d characterizedbyaregularfouryear
o periodicitysince1922,withonelarge
m ordominantyear,onesmallor
e subdominant,andtwoyearswithvery
v smallpopulations.Thesame
e explanationasdescribedabovehas
n
beenproposedwiththeaddedreality
t
ofalag.Essentially,duringthe
s
o dominantyearlimitednumerical
n responsesproduceaninversedensity
s dependentresponseasinthe
y descendinglimbofthemortality
s curvesofFigure3dand3f.The
t abundanceofthepreyinthatyearis
e neverthelesssu~cienttoestablish
m populationsofpredatorsthathavea
s majorimpactonthethreesucceeding
w lowyears.Bufferingofpredationby
it thesmoltsofthedominantyear
h accountsforthelargersizeofthe
d subdominant.
o
m These effects have been simulated
a (Larkin 18), and when random
i influences are imposedin order to
simulateclimaticvariationsthesystemhasa d resultcanbeproducedthanis
distinctprobabilityofflippingintoanother o expected.
stable configuration that is actually I
reproducedinnaturebysockeyesalmonruns n
in other rivers. Whensubdominant
escapementreachesacriticallevelthereis
aboutanequalchancethatitmaybecomethe
samesizeasthedominantoneorshriveltoa
verysmallsize.
Randomevents, of course, are not
exclusivelyclimatic.Theimpactoffireson
terrestrial ecosystemsis particularly
illuminating(Cooper3)andtheperiodicap
pearanceoffireshasplayedadecisiverole
in the persistence of grasslands as well as
certainforestcommunities.Asanexample,
therandomperturbationcausedbyfiresin
Wisconsinforests(Loucks2i)hasresultedin
asequenceoftransientchanges
that move forest communities from one
AnnualReviews
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16 HOLLING
T which
h introduced
T heterogeneity
o overtime.
Thefinalstepis
nowtorecognize
thatthenatural
worldisnotvery
homogeneousover
space,aswell,but
consistsofa
mosaico["spatial
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elementswith
distinctbiologi
cal,physical,and
chemical
characteristicsthat
arelinkedby
mechanismsof
biologi
calandphysicaltransport.Theroleofspatialheterogeneity hasnotbeenwell
exploredinecologybecauseoftheenormouslogisticditficulties. Itsimportance,
however,was
revealedina
classic
experimentthat
involvedthe
interaction
betweena
predatorymite,its
phytophagousmite
prey,andthe
prey'sfoodsource
(Huffakeretal
15).Briefly,in
therelatively
smallenclosures
used,whenthere
wasunimpeded
movementthrough
outthe
experimental
univers n previouslycould
e,the notsupporttent
system f caterpillarsnow
was i can,and
unstabl T populationsare
eand h established
oscillati throughinvasion
r
ons e bythevigorous
increase dispersersfrom
d otherlocales.In
din
e thesenewareas
amplitu
de. theytendto
Whenb produceanother
arriers generationwitha
were highproportion
introdu ofvigorous
cedto behavioraltypes.
impede Becauseoftheir
dis highdispersal
persal behaviorandthe
betwee smallareaofthe
nparts localein:relation
ofthe toitsperiphery,
univers theythentendto
e, leaveingreater
howeve numbersthanthey
r:,the arrive,.Theresult
interacti isagradual
on increaseinthe
persiste proportionof
d.Thus moresluggish
popu typestothepoint
lations wherethelocal
inone population
small collapses.But,
locale althoughits
that fluctuationsare
suffer considerable,
chance evenunderthe
extincti mostunfavorable
ons conditionsthere
could arealways
be enclavessuitable
reestabl fortheinsect.It
ished isanexampleofa
populationwith
by
highfluctuations
invasio
thatcantake
advant
ageof
transie
nt
periods
of
favorab
le
conditi
onsand
that
has,
becaus
eof
this
variabil
ity,a
high
degree
of
resilien
ceand
capacit
yto
persist.
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A
BI
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O
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C
O
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O
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IC
A
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S
Y
S
T
E
M
S
'1
7

Afurther
embellishmenthasbeen
addedinastudyof
naturalinsect
populationsbyGilbert
&Hughes(7).
Theycombinedan
insightf ion.Theyfoundthat
ulfield specificfeaturesofthe
study parasitehostinterac
ofthe tionallowedtheparasite
interact tomakefulluseofits
ion aphidresourcesjust
betwee shortofdrivingthehost
naphids toextinction.Itis
and particularlyintriguingth
their attheparasiteandits
parasite hostwere
switha introducedinto
simulat Australia
ion fromEuropeandinthe
model, shortperiodthatthe
concent parasitehasbeen
ratingu presentinAustralia
pona therehavebeen
specific dramaticchangesinits
locale developmentalrateand
andthe fecundity.Theother
events majordifference
within betweenconditionsin
it EuropeandAustraliais
underdi thattheimmigrationrate
fferent ofthehostinEnglandis
conditi considerablyhigherthan
onsof inAustralia.Ifthe
immigr immigrationratein
ation Australiaincreasedto
from theEnglishlevel,then,
other accordingtothe
locales. modeltheparasite
Againt shouldincreaseits
he fecundityfromthe
importa Australianleveltothe
nt Englishtomakethe
focus mostofits
was opportunityshortof
uponpe extinction.Thisstudy
rsistenc provides,therefore,a
erather remarkableexampleofa
than parasiteanditshost
degreeo evolvingtogetherto
f permitpersistence,and
fluctuat furtherconfirmsthe
importa oassumedefinitionsthat
nceof relatetoconditionsvery
systems nearequilibriumpoints.
resilien Thisisa
ceas simpleconveniencedicta
distinct tedbytheenormous
fromsy analyticaldifficultiesof
stemsst treatingthebehaviorof
ability. nonlinearsystemsat
somedistancefrom
SYNT equilibrium.Onthe
HESIS otherhand,moregeneral
treatmentshavetouched
Some onquestionsof
Del~ni persistenceandthe
tions probabilityof
Traditi extinction,defining
onally, thesemeasuresas
discussi aspectsofstabilityas
onanda well.Toavoidthis
nalyses confusionIproposethat
of thebehaviorof
stabilit ecologicalsystemscould
y wellbedefinedby
haveess twodistinctproperties:
entially resilienceandstability.
equated Resilience
stabilit determinesthe
yto persistence of
systems relationships within a
behavio systemand is a
r.In measureof the ability
ecology of these systemsto
,at absorbchangesof state
least, variables, driving
thishas variables,
causedc andparameters,andstill
onfusio persist. In this
nsince, definitionresilienceis
in the property of the
mathe systemandpersistenceo
matical r probabilityof
extinctionis theresult.
analyse
Stability, onthe other
s,stabili
hand,istheabilityofa
tyhas
systemto return to an
tendedt
equilibriumstate after
 a ity is the propertyof
tempor the systemandthe
arydist degreeof fluctuation
urbance aroundspecific states
.Themo theresult.
rerapidl
y it Resilienceversus
returns, Stability
andwit Withthese definitions
h the inmindasystemcanbe
least veryresilientandstill
fluctuat fluctuate greatly, i.e.
ion, have lowstability. I
~.hemo have touchedaboveon
restable exampleslike the
itis.In spruce budwormforest
this communit~.in_~vhicht
definiti he very fact of
onstabil lowstability seemsto
intro
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fromarjournals.annualreviews.org
A latedones,asWatt(41)
n hasshownhisanalysis
n ofthirtyyearsofdata
u collectedforeverymajor
a forestinsectthroughout
l CanadabytheInsect
Surveyprogramofthe
R CanadaDepartmentof
e theEnvironment.This
statisticalanalysis
v
showsthatinthoseareas
i
subjectedto
e
extremeclimatic
w
conditionsthe
s
populationsfluctuate
widelybuthaveahigh
w capabilityofabsorbing
w
w periodicextremesof
. fluctuation.Theyare,
a
n therefore,unstable
n
u .usingtherestricted
a definitionabove,but
l
r highlyresilient.In
e mor,~benign,less
v
i variableclimaticregions
e thepopulationsare
w
s muchlessabletoabsorb
.
o chanceclimatic
r extremeseventhough
g
/ thepopulationstendto
a bemoreconstant.These
r
o situationsshowahigh
n
l degreeofstabilityanda
i lowerresilience.
n
e Thebalanceb~.~tweenres
18 ilienceandstabilityis
clearlyaproductofthe
HOLLIN evolutionaryhistoryof
G thesesystemsintheface
oftherangeofrandom
fluctuationstheyhave
duce
experienced.
high
resilienc InSlobodkin'sterms
e.Nor (36)evolutionislikea
aresuch game,butadistinctive
cases.iso oneinwhichtheonly
payoffistostayinthe
game. restoreitsabilityto
Therefo respondtosubsequent
re,a unpredictable
major environmentalchanges.
strategy Vari.abilityoverspace
selected andtimeresultsin
isnot variabilityinnumbers,
one andwiththisvariability
maximi thepopulationcan
zing simultaneouslyretain
either geneticandbehavioral
efficien typesthatcanmaintain
cyora theirexistenceinlow
particul populationstogether
ar withothersthatcan
reward, capitalizeonchance
butone opportunitiesfor
which dramaticincrease.The
allows morehomogeneousthe
persiste environmentinspace
nceby andtime,themorelikely
maintai isthesystemtohavelow
ning fluctuationsantilow
flexibilit resilience.Itisnot
yabove surprising,therefore,
allelse. thatthe
A commericalfishery
populati systernsoftheGreat
on Lakeshaveprovideda
respond vividexampleofthe
stoany sensitivityofecological
environ systemstodisruptionby
mental man,fortheyrepresent
change climaticallybuffered,
bythe fairlyhomog~neousand
initiatio selfcontainedsystems
nofa withrelativelylow
seriesof variabilityandhence
physiolo highstabilityandlow
gical, resilience.Moreover,the
behavio goalofproducinga
ral, maximumsustainedyield
ecologic mayresultinamore
al,and stablesystemofreduced
genetic resilience.
changes
that Nor is it surprising
that ehaveahighresilience.
howeve Similarly, some Arctic
r ecosystemsthoughtofas
readily fragile maybe highly
fish resilient, although
stocks unstable.
in.lakes Certainlythisisnottrue
can be for somesubsysterns in
driven the Arctic, such as
to Arctic frozen soil, self
extincti contained Arctic lakes,
on, it and cohesive social
has populationslikecaribou,
but these might be
been
exceptions to a general
extreme
rule.
ly
Thenotionofan
difficult
interplaybetween
to do resilienceandstabilty
the mightalsoresolvethe
same to conflictingviewsofthe
insect roleofdiversityand
pests of stabilityofecological
man's communities.Elton(5)
crops. andMacArthur(22)have
Pest arguedcogentlyfrom
systems empiricalandtheoretical
are pointsofviewthat
highly stabilityisroughly
variable proportionaltothe
inspace numberoflinksbetween
and speciesinatroph!cweb.
time; as Inessence,iftherearea
Opensy variety of trophic links
stems thesameflowofenergy
theyare and nutrients will be
muchaff maintained through
ected alternate links when a
by species becomesrare.
However, May's(23)
dispersa
recent mathematical
l and analysesofmodels
therefor
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R
E
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A
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D
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A
BI
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19

ofalargenumberof
interactingpopulations
showsthatthisrelation
betweenincreased
diversityandstabilityis
notamathematical
truism.Heshowsthat
ran
domlYa definitionofstability
ssemb.l used,however,isthe
ed equilibriumcentered
comple one.WhatMayhas
xsystem shownisthat
sarein complexsystemsmight
general fluctuatemorethanless
less complexones.Butif
stable, thereismorethanone
and domainofattraction,
never thentheincreased
more variabilitycouldsimply
stable, movethesystemfrom
than onedomaintoanother.
less Also,themorespecies
comple thereare,the
xones. moreequilibriatheremay
He beand,although
points numbersmaythereby
outthat fluctuateconsiderably,
ecologi theoverallpersistence
cal mightbeenhanced.It
systems wouldbeusefulto
are explorethepossibility
likelyto thatinstabilityin
have numberscanresultin
evolved morediversityofspecies
toa andinspatialpatchiness,
very andhenceinincreased
small resilience.
subset
ofall Measurement
possible Ifthereisa
setsand worthwhiledistinction
that betweenresilienceand
MacArt stabilityitisimportant
hur'scon thatbothbemeasurable.
clusions Inatheoreticalworld
, suchmeasurementscould
therefor bedevelopedfromthe
e, behaviorofmodel
mightsti systemsinphasespace.
llapply Justasitwasusefulto
inthe disaggregatethe
real reproductioncurvesinto
world. theirconstituent
The componentsofmortality
and ethetwoweneedto
fecundit imaginefirstthe
y,soit appearanceofaphase
is spaceinwhichthereare
useful nosuchforcesoperating.
to Thiswouldproducea
disaggr referenttrajectory
egate containingonlythecyclic
the propertiesofthesystem.
informa Iftheforceswere
tionina operating,departurefrom
phase thisreferenttrajectory
plane. wouldbeameasureofthe
There intensityofthe~forces.
aretwo Thereferenttrajectories
compon thatwouldseemtobe
entsthat mostusefulwouldbethe
are neutrallystableorbitsof
importa Figure2b,forwecan
nt:one arbitrarilyimaginethese
that trajectoriesasmovingona
concern flatplane.Atleastfor
sthe morerealistic
cyclic
modelsparametervalues
behavio
canbediscoveredthatdo
rand
generateneutrallystable
its orbits.Inthe
frequen
complexpredatorprey
cyand
amplitu modelofHolling(14),ifa
de,and rangeofparametersis
onethat chosentoexplorethe
concern effectsdifferentdegrees
sthe ofcontagionofattack,the
configu interactionisunstable
ration
whenattackisrandomand
of
forces stablewhenitis
caused contagious.Wehave
bythe recentlyshownthatthere
positive isacriticallevelof
and contagionbetweenthese
negativ extremesthatgenerates
e neutrallystableorbits.
feedbac
k Theseorbits,then,havea
relation certainfrequencyand
s. amplitudeandthe
departureofmorerealistic
separat trajectoriesfromthese
 referent withpeaksandvalleys.If
ones thewholepotentialfield
should wereashallowbowlthe
allow systemwouldbeglobally
the stableandalltrajectories
comput wouldspiraltothebottom
ationof ofthebowl,the
the equilibriumpoint.Butif,
vector ataminimum,therewere
of alowerextinction
forces. thresholdforpreythen,in
Ifthese effect,thebowlwould
were haveaslicetakenoutof
integrat oneside,assuggestedin
eda Figure4.Trajectoriesthat
potenti initiatedfarupontheside
alfield ofthebowlwouldhave
wouldb amplitudethatwouldcarry
e thetrajectoryoverthe
represe slicecutoutofit.
nted Onlythose
byWIB6151DeutscheForschungsgemeinschaft
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fromarjournals.annualreviews.org
A
n
n
u X POP
a
l 1 Figure 4
Diagramatic
representation
showingthe feedback
R forcesasapotentialfield
uponwhichtrajectories
e move.Theshaded portion
v is the domainof
attraction.
i
e trajectoriesthatjust
w avoidedthelowestpoint
s ofthegapformedbythe
slicewouldspiralinto
w thebowl'sbottom.Ifwe
w termedthebowlthe
w
. basinofattraction
a (Lewontin20)thenthe
n
n domainofattraction
u wouldbedeterminedby
a
l boththecyclicbehavior
r
e andtheconfigurationof
v forces.Itwouldbe
i
e confinedtoas~naller
w portion
s
. ofthebottomofthe
o bowl,andoneedge
r
g wouldtouchthe
/ bottomportionofthe
a
r slicetakenoutofthe
o basin.
n
l Thisapproach,then,
i suggestswaysto
n measurerelative
e
amountsofresilience
20 andstability.Thereare
tworesilience
HOLLIN measures:Since
resilienceisconcerned
G
with
probabilitiesof
extinction,firstly,the
overalllareaofthe
domainofattractionwill
inpartdetermine
whetherchanceshiftsin
statevariableswill
movetraj stabilitywouldbe
ectories designedinjustthe
outside oppositewayfrom
the thosethatmeasure
resilience.Theywould
domain.
becenteredonthe
Secondl equilibriumratherthan
y,the on
height theboundaryofthe
ofthe domain,andcouldbe
lowest representedbya
pointof frequencydistribution
the oftheslopesofthe
basinof potentialfieldandby
attractio thevelocityofthe
n(e.g. neutralorbitsaround
the theequilibrium.
bottom Butsuchmeasures
ofthe requireanimmeanse
slice amountofknowledgeof
describe asystemanditis
dabove) unlikelythatwewill
above oftenhaveallthatis
equilibri necessary.
umwill Hughes&Gilbert(16),
bea however,have
measure suggestedapromising
of approachtomeasuring
howmuc probabilitiesofextinc
hthe tionandhenceof
forces resilience.Theywere
haveto abletoshowina
be stochasticmodelthat
changed thedistributionof
before survivingpopulation
all sizesatanygiventime
trajector doesnotdiffersignifi
ies cantlyfromanegative
moveto binomial.Thisofcourse
extinctio isjustadescription,but
nofone itdoesprovideawayto
or estimatetheverysmall
moreof probabilityofzero,i.e.
thestate ofextinction,fromthe
variable observedmeanand
s. variance.The
confilgurationofthe
measure potentialfieldandthe
sof cyclicbehaviorwill
determi domainsofattraction,
nethe andthesewillinturn
number affecttheparameter
~nd valuesofthenegative
formof binomialorofany
the
AnnualReviews
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RESILIENCEANDSTABILITYOFECOLOGICALSYSTEMS 21
o aslittle fluctuation aspossible.The
t
resilience viewemphasizesdomainsof
d
attractionandtheneedforpersistence.
i
But
t
e extinctionisnotpurelyarandomevent;it
resultsfromtheinteractionofrandom
b eventswiththosedeterministicforcesthat
e definetheshape,size,andcharacteristics
t
ofthedomainofattraction. Thevery
h
approach,therefore, thatassuresa
b
stable
e
DeutscheForschungsgemeinschaft on10/19/08.Forpersonaluseonly.
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maximumsustained yieldofa
a
renewableresourcemightsochange
p
thesedeterminis
r
e tic conditionsthattheresilience
islostorreducedsothatachanceand
A rareevent
P
that previouslycouldbeabsorbed
T cantriggerasuddendramaticchange
h andloss
y ofstructuralintegrityofthesystem.
i Amanagementapproachbasedon
v resilience, ontheotherhand,
e wouldemphasize
theneedtokeepoptionsopen,theneed
tovieweventsinaregionalrather
thana
local context,andtheneedto
emphasizeheterogeneity. Flowing
fromthiswould
benotthepresumptionofsufficient
knowledge,buttherecognitionofour
ignorance;
nottheassumptionthatfutureeventsare
expected,butthattheywillbe
unexpected.
Theresilienceframeworkcan
accommodatethisshiftofperspective,
foritdoesnot
requireaprecisecapacitytopredictthe
future,butonlyaqualitativecapacityto
devisesystemsthatcanabsorband
accommodatefutureeventsinwhatever
unex
p es,Consequences, nt. ,H.1954.
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