Vol. 108, No. 964
The AmericanNaturalist
1974
November-December
MULTIPLE STABLE POINTS IN NATURAL COMMUNITIES
JOHN P. SUTHERLAND
Duke University Marine Laboratory, Beaufort, North Carolina 28516
Lewontin (1969) distinguishedtwo opposingways of accountingfor the
observedstructureof communities." The firststatesthat historyis relevant
to the presentstate of populations,species,and communities,
and that their
presentstate cannot be adequately explained withoutreferenceto specific
historicalevents.This is equivalentto sayingthat multiplestable points ...
[stable communitieswithdifferent
structures]exist and that the interesting
problemis why the systemis at a particular stable point. . . . The second
mode of explanationattemptsto explain the presentstate of natural populations or communitieswithoutany historicalinformation,but as a result
of certainfixedforces." The latterapproach has as a basic assumptionthat
only one stable point exists. In Lewontin's terminology,
this assumptionis
one of "global stability,"while if multiplestable pointsexist,each is stable
only in the immediate"neighborhood" or "locality" of the point in question.
If multiple stable points exist, application of currenttheoryis complicated (Horn and MacArthur 1972; Levins and Culver 1971; MacArthur
1972), and developmentof systemsmodels (Patten 1971, 1972) becomes
intractable;a separate model must be built for each stable point and these
submodels joined with an appropriate superstructure.Recognizing this
problem,MacArthur (1972, p. 187) charges us to look "for patterns in
relativelyhomogeneoushabitatsof size just large enoughto hold an adequate
sample of species.In [habitats] of thissize we have reason to hope the traces
of historywill have been erased." However,my own researchand that of
otherslead me to believe that it is oftenimpossibleto pick study areas of
this appropriatesize. I believe that historyoftenhas an importanteffecton
the observedstructureof many communities.In these communities,therefore, multiple stable points are an undeniable reality,both in space and
time.
In this discussionI shall make use of the conceptualdistinctionbetween
habitat and niche proposedby Whittakeret al. (1973): thus,"the m variables of physical and chemicalenvironmentthat formspatial gradientsin
a landscape or area define as axes a habitat hyperspace.
. .
. The n variables
by whichspecies in a given communityare adaptivelyrelated defineas axes
a niche hyperspace." The question posed here is whetheror not the niche
hyperspaceis such that stable communitiesof different
structurecan occur
in the same habitat hyperspace-that is, can species interactionsproduce
multiplestable points in the same physical locality.
859
860
THE AMERICAN NATURALIST
Identifyingmultiple stable points depends on attributingto them some
degreeof stability.We mustdistinguishbetweenwhat Margalef (1969) has
called "adjustment stability" and "persistence stability." Ideally, we
should consider only the community'sresponse to perturbations-adjustment stability-and considerit stable only if it returnsto the same point
after being perturbed.However, these experimentsare rarely done, and
thereis some questionabout the kind and intensityof perturbationsappropriate for such a test.Measured more oftenis the persistenceof a community throughtime. Persistencestabilityimplies nothingnecessarilyabout
adjustmentstability,exceptthat natural communitiesmustusually contend
withunknownenvironmental
perturbations.Thus, persistencethroughtime
can mean thatthe communitypossessessome degreeof adjustmentstability,
althoughwe are not sure to what degreeand to what perturbationsit is resistant.We can strengthen
our argumentabout stabilitybased on persistence
data by identifyingforceswhichhave the potentialof alteringcommunity
structure,but which do not. In the general absence of data on adjustment
stability,I identifymultiple stable points by their persistencefor some
period of timein a given physicallocality,in spite of forceswith the potential of alteringtheir structure.We must use our "naturalist's judgment"
to decide on appropriatescales of space and time.Since thesevary with the
system,I deferspecificconsiderationsto the appropriateplace below.
EVIDENCE FROM THE FOULING COMMUNITY AT BEAUFORT,
NORTH CAROLINA
The foulingcommunityat Beaufort,North Carolina, is a complexassemblage of hydroids,tunicates, bryozoans,sponges, and associated species
(Maturo 1959; McDougall 1943; Sutherlandand Karlson 1973; Wells et al.
1964). For several years I have followedcommunitydevelopmentbeneath
theDuke Marine Laboratorydock,on unglazed ceramictile plates (232 cm2)
suspended horizontallyabout .3 m below low water. Percentage cover for
each species that settledand grew on the lower surfacewas estimatedperiodicallyby a point-sampling
technique,using 75 pointsrandomlypositioned
over the plate area. This numbergave repeatable estimatesof percentage
cover to within ?5%. The technique was also nondestructive,allowing
plates to be resubmergedaftersampling.Only the basal area of attachment
was countedas beingoccupiedby a species,and greaterthan 100% coverage
for all species was possible because of epizooic overgrowth.
Plates in the same series,submergedat the same time,were not sampled
simultaneously.Thus, data froma given plate oftenapplied to a different
time intervalfromthat of other plates in the same series. Data within a
series were pooled by a methoddescribedelsewhere (Sutherland 1970). I
assumed the eventson each plate occurreduniformlythroughouta sample
interval.For example,if the percentcover of a species changedby 30%oin
30 days, the rate of changewas assumed to be 1%/day during each day of
thatinterval.In a computermemory,an arraywas set aside for each species
MULTIPLE
STABLE
POINTS
861
on each plate and numberedfor each day aftersubmergence.The appropriate rate of change (+) for each species was placed in the elementsof the
array representinga day in a given sample interval,e.g., from day 70 to
day 100 after submergence.When this was done for all species on a given
plate, the percentagecoverof each species was estimatedat arbitraryintervals (e.g., day 30, 60, 90, etc.) by summingthe rate of change fromday 1
(day of submergence).Data were transformedusing the angular transformation,and foreach seriesa mean and 95%oconfidenceinterval (Sokal and
Rohlf1969) were thencalculated for each speciesat each arbitraryinterval.
During 1971, seriesof threeplates were submergedeach monthfromMay
throughNovember.In 1972 (and 1973), the numberof plates in a series
was increased to four, and new series were submergedeach month from
April throughNovember.Only a few of these series will be discussed here.
Additionally in 1972 (and 1973), competitor-removal
and fish-predatorexclusionexperimentswere conductedin April, July,and Octoberto evaluate the importance of competitionand fish predation on community
development.The experimentalunit was a rack containing20 plates. Within
each rack,four plates were controls(= no removals), and therewere four
treatments(= removalby hand of a potentiallydominantsessile species or
species group), each of which was carried out on four plates. Treatments
and controlswere assigned at random within the rack. Each experiment
(e.g., in April, July,or October) consistedof two racks of 20 plates each,
one of whichwas enclosedin a nylonfishnet (l/4-inchmesh size). Identical
treatmentswere conductedbothinside and outsidethesefish-exclosure
nets.
Only data fromthe experimentbegun in April 1972 are consideredhere.
Developmentin this communitywas extremelyvariable. Associated with
seasonal temperaturefluctuations(of about 250C) there were distinctly
seasonal patterns of species recruitment(Sutherland and Karlson 1973;
see also McDougall 1943). In addition,there were dramatic differences
in
recruitmentfromyear to year (Sutherland and Karlson 1973). Seasonal
and year-to-year
variationsin abundance were also seen in the community
of adult organisms,althoughthese were not as dramatic as the variability
in recruitment(Sutherland and Karlson 1973). Commonhydroids were
Tubulariacrocea,Eudendriumcarneum,and Pennariatiarella; common
wereStyelaplicata,Ascidiainterrupt,andMolgulamanhattensis;
tunicates
commonbryozoanswere Bugula neritinaand Schizoporellaunicornis; com-
monspongeswereMicrociona
prolifera,
Haliclonasp.,Halichondriabowerbanki, and Mycale cecilia. Also commonwere several species of barnacles
(Balanus) and a serpulid polychaete (Jydroides dianthus). Below, I restrict attentionto species which, at some time during the time interval
consideredhere,occupied at least 10%oof the area of a series.
The seriesof threeplates submergedin May 1971 was initiallydominated
by Tubularia and to a lesser extentby B. neritina (fig.1). Bugula neritina
has a small zone of attachmentand is underestimatedby our samplingtechnique. These two species produced a dense canopy some 180 mm in depth.
In June, Stycta (and Ascidia) settled beneath this canopy; during July,
THE AMERICAN
862
NATURALIST
100.
0
25-
w
0-
M
J
J
A
S O
N
D
J
F
M
A
M
1971
J
J A
S O
N
D
1972
FIG. 1.-Series submerged
May 6, 1971 (N = 3). Estimatedmeanpercentage
actual day of
and 95% confidence
intervalat arbitraryintervalapproximating
census. Tubularia 0; Pennaria A; EudendriumX; Styela *; Bugula *;
SchizoporellaA; Balanus V; HydroidesV.
theseriesbecameessentially
a monoculture
ofStyela,a condition
whichpersisteduntiltheend of October(fig.1). I viewthisStyelamonoculture
as
a locallystablepointbecauseit persistedforsomeperiodof time(about4
months)in spiteof forcespotentially
In
capableof alteringits structure.
thiscase,these"forces" wererepresented
by potentiallarval recruitsof
otherspecies.Thus,newsubstrate
in Junebecamedominated
submerged
by
Ascidia (whichkeptsettlingafterStyelct
stopped)and Pennarica(Sutherland and Karlson1973). Similarly,the Julyseriesbecamedominatedby
Balanussp. (Sutherlandand Karlson1973), and theAugustseriesbecame
dominated
bySchizoporella(fig.2). Noneof thesespecieswas recruited
to
theMay seriesat thesametime;thisindicatesthattheirlarvaewere"filteredout" in somewaybyStyela.
100
w
75)
7
Z
50-
w
0
M
J
J
A
S
197 1
0
N
D
J
F tM
A
M
J
J
A
S
0
N
D
1972
FIG. 2.-Series submerged
August2, 1971 (N = 3). For symbolssee fig.1.
863
MULTIPLE STABLE POINTS
Toward the end of Octoberand in November,many Styela died, rendering thetightlygrown-together
mat of Styela unstable.As a result,essentially
all Styela sloughed off,leaving considerablefree space, which was again
dominatedby Tubularia (fig.1). Tubularia persistedthroughoutthe winter
(a time of minimallarval recruitment)but was again invaded by Styela
in the spring of 1972 (fig. 1). In contrastto the behavior in spring of
1971, Styela did not form a monocultureduring 1972. As a result,other
species were able to invade the series (e.g., Pennaria, Eudendrium,Balanues
sp., and Schizoporella) (fig. 1).
The seriesof threeplates submergedin August 1971 became dominatedby
Schizoporella (fig.2). I view this as anotherlocally stable point because it
persisted (for at least a year) in spite of potentialchange. The most dramatic evidence for this resistanceto change was the general absence of
Styela in thisseriesduringthe springof 1972,whenat the same timeStyela
was invading the May 1971 series (i.e., Tubularia) very successfully(figs.
1 and 2). Indeed, except for the August series,Styela invaded all of the
1971 series (May-November) during the spring of 1972 (Sutherland and
Karlson 1973).
Experimentsconductedin April 1972 shed additional light on the productionof thesetwo (Styela and Schizoporella) stable points. Controlsoutside the fish-exclosure
net are comparableto the May 1971 series, except
thattheywere submergedin April. However,the May 1972 series developed
in essentiallythe same way as the April 1972 series (Sutherland and Karlson 1973). In contrastto the events of spring of 1971, Tubularia did not
settleheavily during 1972 and did not produce an extensivecanopy (figs.
3 and 4; Sutherlandand Karlson 1973). The controlsoutsidethe net became
dominatedby Schizoporella, which persisted throughDecember (fig. 3),
again in spite of the presenceof potentiallarval recruits.In dramaticcontrast, controlsinside the fish-exclosure
net, submergedat the same time,
100-
0
0T
s75-
a-
a]25./
A
M
J
J
A
S
0
N
D
4
1972
net submergedApril 9, 1972
FiG. 3.-Control series outside fish-exelosure
(N = 4). For symbolssee fig.1.
864
THE AMERICAN NATURALIST
}1
75
e=
Z
w
50:
W
25-
0
0
00
A
M
J
J
A
S
0
N
D
J
1972
FIG. 4.-Control series inside fish-exclosure
net submergedApril 9, 1972
(N =4). For symbolssee fig. 1.
became dominatedby Styela (fig.4). Styela formeda monoculture,as was
formedon the May 1971 series, and this monoculturepersistedfor about
the same lengthof time (figs.1 and 4). AfterStyela sloughedoff,the area
was takenoverby Schizoporellain 1972 (fig.4), as opposed to the regrowth
of Tubularia in 1971 (fig.1). Styela removalsinsidethe net were dominated
by Schizoporella,indicatingthat the nets themselveshad no adverse effects
on recruitmentand survival of Schizoporella.
I interpretthese resultsto mean that fishpredation is a potentiallyimportant source of mortalityto young Styela. If the foragingefficiency
of
thefishis reducedat the timeof Styela recruitment,
thenmanymoreStyela
survive.Thus, Styela survivedwell in the absence of nets duringthe spring
of 1971 because Tubularia had formedan extensivecanopy (fig.1). In 1972,
Styela survivedonly inside the fish-exclosure
nets (fig. 4) and on the 1971
series (except the one submergedin August) whereotherorganisms,including Tubularia, provided some degree of protection(fig. 1; Sutherland and
Karlson 1973).
I should point out that I have been unable to duplicate these results in
subsequent experiments.There was no significantrecruitmentof Styela
during the July and October experimentsin 1972. Schizoporella was the
most abundant colonizer,and initial recruitmentand growthwere equal
both inside and outside the enclosurenets. Probably Schizoporella is not a
preferredfood for fishbecause of its encrustinggrowthform and heavy
calcification.Thus, thereis no reason to expect an increasein survivalwhen
Schizoporeltais protectedfromfishpredation.During the April 1973 experiment,Styela did not settleheavilyinside the enclosurenet. The net inadvertentlybecamefouledwithStyela,whichprobablypreventedadditional
larvae fromreachingthe enclosedplates. Thus, no test of the fisheffectwas
MULTIPLE STABLE POINTS
865
possible.In July 1973,Schizoporella
was again the mostabundantcolonizer,
and there is no necessaryreason to expect a fisheffect.
I conclude that the productionof these two stable points depends on a
complex and potentiallyhierarchical pattern of switches involving both
larval recruitmentand, occasionally,fishpredation. Thus, a Schizoporelladominatedsystemcan be produced directlyby larval recruitmentin the
absence of Styela,as in the fall of 1971 (fig. 2), or it can be produced in
the presenceof Styelarecruitmentif fishare able to forage effectively
on
the substrate (fig. 3). A Styela-dominatedsystemcan result if previously
recruitedspecies (or a net) affordprotectionfromfishpredationand Styela
is able to invade the area occupied by thesespecies. Tubulariasatisfiesthese
criteria; Schizoporella
does not. Additionally,Styelalarvae must be available in the plankton.Initial developmentinto one stable point or anotheris
thus a highlystochasticprocesswith the order of eventsjust as important
as theirnature. As a result,the historyof developmentmust be knownto
explain communitystructureat any given time.
Maintenanceof thesetwo stable pointsappears largely determinedby the
abilityof eitherStyela (in monoculture)or Schizoporella
to exclude potential larval recruits,the "migration competition" of Levins and Culver
(1971). Each point has a differentdegree of neighborhoodstability,perreasons.
sistingfor a different
period of timeand disappearingfor different
Thus, Styelasloughsoffwhen the mat is destabilizedby the death of some
individuals. However,Schizoporella
not only persistslonger,but its dominance also appears to be brokenup more slowly.With increasingage, the
mat becomesmore and more convoluted,and
surface of the Schizoporella
this occurrenceseemsto reduce the efficiency
with whichit excludes potential recruits.For example, Styelafinallyinvaded the August 1971 series
during the fall of 1972 (fig. 2).
The major providersof free space on our local pilings are sea urchins
(Arbaciapunctultata).My experimentalsystemgenerallyexcludes urchins
fromthe tile surfaces,althoughI am duplicatingtheireffectby periodically
submergingnew tiles. In the absence of urchin predation,there is some
indicationof successionto a somewhatoscillatory"climax" (although not
necessarilya global one) consistingof a mixture of hydroids,tunicates,
bryozoans,and sponges (Sutherland and Karlson 1973). However, as we
have seen, the approach to this "climax" is not continuous,but rather is
marked by "stops along the way" as one of several potentiallydominant
species exerts control over the space on the plates. I view these various
"stops" as multiple stable points. Their importancelies in the fact that
withsomedegreeof disturbance,such as is normallyprovidedby sea urchin
predation,the systemmay neverreach the "climax" point. The time course
of eventsmay be such that the traces of historyare never erased from a
givenlocality.
I have discussed only the few stable points in this systemfor which I
presentlyhave some data. Casual observationsindicate that several differ-
866
THE AMERICAN
NATURALIST
ent species of spongesare also capable of monopolizinglocal areas for considerableperiods of time.In addition,species in the systemmay be capable
of attainingspace monopolieswhich "never" revertto the "climax" describedabove. For example,anotherhydroid,Hydractinia echinata,appears
able to exclude mostpotentiallarval recruitsand is resistantto urchinpredation as well (R. H. Karlson, personal communication).Thus, the larger
basin of attractionaround the "climax" discussed above may not be a
"global" basin; theremay be more than one stable point with all species
present.
My interpretationof these data restson a belief that it is appropriateto
view large areas (e.g., pilings) as composedof many smaller patches and
that these patches,more or less the size of my tile plates, are the local situations of interest.I take this view because the organismsI study are sessile
and because sea urchinsare relativelynonmobile.However,similarprocesses
can certainlyoccur over large areas (e.g., when a new piling is submerged),
and the appropriatepatch size is conceivablya directfunctionof predation
intensityby urchins.
EVIDENCE PROM OTHER COMMUNITIES
Marine rocky intertidal.-In the lower rocky intertidal of the Pacific
Northwest,Paine (1966) has shownhow a given local area can be switched
betweenstable pointsby the removal (or addition) of the starfish,Pisaster
ochraceus.In the presenceof Pisaster, the characteristicassemblageof organismspersistedin spite of potentiallydisruptingspace competitionfrom
the mussel,Mytiluscalifornianus.In the absence of Pisaster,Mytilusdominated the lower intertidal.Given enough time to grow,these musselsmay
even persistin spite of the presenceof Pisaster, as theybecometoo large to
be eaten (Paine 1974). Removalof starfishfrommusselbeds in New Zealand
(Paine 1971) has yielded similarresults.
At somewhathigher intertidalheights,Dayton (1971) has shown how
various levels of disturbance(bulldozing by limpets,predationby Pisaster
and several species of the gastropod genus Thais, and logs strikingthe
rocks) normallypreventedmonopolizationof space by the competitively
superior barnacle, Balanus cariosus. In these disturbed areas, two other
barnacleswerefound in additionto B. cariosus.In areas whereone or more
of the disturbanceswere absent, e.g., above the foragingzone of Pisaster
or in an area wherelogs struckless frequently,B. cariosus did indeed monopolizespace to the exclusionof the otherbarnacle species (Dayton 1971).
The normal balance of disturbancescould be upset in time as well as in
space. For example, in the San Juan islands above the foragingzone of
Pisaster, Thais populationswere normallyadequate to preventmonopolization of space by B. cariosus (in the presenceof log damage). However,after
a cold spell that killed many Thais, these areas became dominatedby B.
cariosus (Dayton 1971). As withthePisaster-Mytilus
interaction,B. cariosus
MULTIPLE STABLE POINTS
867
can becometoo large to be eaten by Thais (Dayton 1971) and after some
timemay persisteven in the presenceof Thais.
Paine and Vadas (1969) have experimentedwiththe structureof benthic
algal populationsin intertidaltide pools. Pools grazed by sea urchinswere
characterizedby a "mixture of [encrusting] calcareous and small fleshy
algae" (Paine and Vadas 1969). Upon removalof urchins,tide pools eventually became dominatedby the large, competitivelydominantalga, ledophyllum sessile. During the same period, control pools with urchins
maintainedtheir characteristicappearance. Although the experimentwas
not done,presumablyadding urchinsto the experimentalpools would return
the systemto the original state,dominatedby encrustingcalcareous forms.
In each of these studies,one locally stable point was maintainedby the
activitiesof a specificconsumerin spite of potentiallydisruptivecompetitive
interactions.Upon removal of the consumer,the ensuing competitionproduced a communityof differentstructurein the same physical locality.
Abioticfactors(e.g., logs and cold spells) were importantto the extentthat
they disturbedthe local balance of competitionand predation.
A knowledgeof historywas necessaryto interpretthe observeddifferences
in structureof theselocal communities.The observerhad to knowthat starfishand urchinshad been experimentallyremovedor that Thais were absent because of a cold spell the previouswinter.
This interpretationof communityprocessesdepends upon the perception
of large areas (e.g., several miles of coast line) as composedof small local
patches about the size of a single large rock or a given tide pool. I believe
this can again be justifiedin view of the limitedmobilityof most of the
dominantorganisms.Stable points cannot be identifiedin this systemfor
and relativelyslow
at least a year or so because of the seasonal recruitment
growthof the organismsinvolved.
Coral reefs.-Stephensonand Searles (1960) demonstrated
experimentally
that browsingof fishwas the main factorresponsiblefor the paucity of organismson intertidalbeach rocksat Heron Island in the Great Barrier reef.
When thesefishwere excluded by means of wire cages, algal standingcrop
and diversityboth increased. Even thoughmost of the fishwere classified
as algal feeders,the authorssuggestedthey also removedjuvenile animals
while browsing.Thus, the considerablymore abundant floraand fauna on
the mainlandof Australia at similarlatitudesmay be related to the absence
of fish(Stephensonand Searles 1960), whichare found only on coral reefs.
Similarly,Randall (1965) and Earle (1972) implicated grazing fish as
primarilyresponsiblefor the absence of benthicvegetationon a coral reef
in the Virgin Islands. Not only was vegetationlacking fromthe reef itself,
but also froma band averagingabout 10 m in widtharound the reef (Randall 1965). This band was maintainedby the intensegrazingof herbivorous
fish,which apparentlystayed close to the reef for protectionfromlarger,
predaceous fish.Beyond this band, vegetationwas abundant. When cages
that excludedfishwere placed withinthe band, therewas an increasein the
868
THE AMERICAN NATURALIST
growthof vegetationwithinthe cages in 6 weeks (Earle 1972). When artificial reefs of concretebuilding blocks were built out into the surrounding
beds of vegetation,a new zone of bare sand developed around these blocks
in about 8 months (Randall 1965).
In a morerecentstudy,Ogden et al. (1973) showedthat in someinstances
thesebare zones may be produced by sea urchingrazing instead of by fish.
When urchins,Diadema antitlarum,were removedfroma patch reef, the
existinghalo disappeared in 8 months.
All studies indicate that the characteristicabsence of vegetationon the
reef and immediatesurroundingswas produced by grazing activities of
somekind in spite of considerablepotentialfor plant growth.The alternate
absent but could
communitydominatedby vegetationwas characteristically
be expectedin any local situationwherebrowserswere eliminated.In view
of reportedrates for developmentand destructionof the halo (8 months),
alternate stable points cannot be identifieduntil about a year's time has
passed.
Phytotelmata.-In a recentreview,Maguire (1971) pointed out the importanteffectof biologicalinteractionsin the processesof colonizationand
extinctionin small aquatic systems.He divided the organismsin this community into four major groups: protozoans,algae, inefficientmetazoan
predators,and efficient
metazoanpredators.In temperateareas where desiccation is a major deterrentto dispersal,the relative colonizingability of
thesegroupsvaried greatly.Protozoansand algae were the mosthighlydispersed groups, with inefficient
metazoan predatorsabout half as well dismetazoan predators only about one-thirtiethas well
persed and efficient
dispersed (Maguire 1971). In the wet tropics, dispersal was much more
efficientfor all groups. Specific combinationsof these groups produced
differentspecies equilibria. Thus, the average number of species at equilibriumin Heliconia bracts in the presenceof ostracods (inefficient
predators) and absence of mosquitos (efficientpredators) was significantly
greater than in bracts where mosquitos were present in the absence of
ostracods (Maguire 1971).
In this systemcommunitiescan apparentlybe switchedfrom one equilibriumto anotherwith the immigrationof specificpredatortypes; species
interactionscan produce communitiesof differentstructurein the same
physical locality. History becomesmore importantat higher latitudes bein dispersal of the various animal groups are greater.For
cause differences
in
example, temperateareas some local communitiesmay never be invaded
by the poorly dispersed, efficientpredators.
In communitiesas small and disjunct as these,the scale of studyin space
is rathereasily definedas the individual bodies of water. Apparently,3-4
monthsis an appropriatetimescale withinwhichto view the persistenceof
alternatecommunities,
adequate to allow for the levelingoffof most colonization curves (Maguire 1971).
1
Freshwater lakes.-Brooks (1968), Brooks and Dodson (1965), Dodson
(1970), Galbraith (1967), Hall et al (1970), and Sprules (1972) have all
MULTIPLE STABLE POINTS
869
providedevidencefor the opposingeffectsof competitionand predationon
the structureof freshwaterzooplanktoncommunities.Larger zooplankters
are apparently more efficient
collectorsof a wider variety of particulate
foods and in the absence of predation exclude the competitivelyinferior,
smaller forms.However, vertebratepredators prey preferentiallyon the
larger forms,and when predation is intense,the small zooplanktersthat
escape predation become the dominants.Thus, in a series of Connecticut
lakes, those with and withoutplanktivorousfishwere dominatedby small
and large zooplankton,respectively;in one, smaller formsreplaced larger
ones after the invasion of fish (Brooks and Dodson 1965). Similarly,in
some small subalpine ponds in Colorado, communitiescomposed of large
zooplanktonformswere foundto be inverselyrelatedto the presenceof the
predatorysalamander,Ambystomatigrinum(Dodson 1970; Sprules 1972).
Finally, Galbraith (1967) and Hall et al. (1970) have experimentallyalteredzooplanktoncommunitiesin a similarfashionby adding and subtracting fishpredators.
In thesesystemstherewere generallytwo stable points for the zooplankton communities,one produced and maintained by competitionand the
otherby predation.Switchingbetweenthese two communitiesdepended on
historicalfactors,whichaffecteddispersaland survivalof specificpredators.
Mattersof scale in space are easily resolvedin these disjunct communities
as long as the bodies of waterremainsmall relativeto the locomotorabilities
of predators.In lakes of larger size, these argumentsapply only to appropriately sized patches, and differences
in communitystructurewill probably be less pronounced (e.g., Brooks and Dodson 1965). Since these are
temperatelakes withmarkedseasonal changesin theirbiology,a year or so
seems an appropriatescale in timewithinwhich to view the persistenceof
locally stable points.
Terrestrialplant communities.-Harper (1969) presentedseveral kinds
of evidencedemonstrating
that herbivorescan controlthe structureof terrestrialplant communities.For example,high populationsof rabbitsregulated vegetationaldiversityin many parts of Britain duringthe latterhalf
of the nineteenthand early twentiethcentury.Upon removal of rabbits,
eitherby exclosuresor the virus disease myxomatosis,
vegetationaldiversity
changed radically. Afteran immediateincreasein the numberof recognizable species,diversitydeclined as a few grassesdominated,and after 5 or 6
years woodyvegetationbegan to appear (Harper 1969). Thus, a characteristic type of vegetationwas maintainedby rabbitsfor 50-75 years in spite
of considerablepotential for change.
The appropriate scale in space for studyingthe effectsof rabbitswould
depend on the factorsaffectingtheirpresenceor absence. A small area inside a rabbit exclosure (compared to an outside control) or islands differentiallyaffectedby myxomatosis(Harper 1969) would suffice.Certainlya
50-75-year period seems adequate for attributingsome stability to the
communityproduced by rabbit browsing.
870
THE AMERICAN NATURALIST
DISOCUSION
Lewontin (1969) points out that "if the systemof equations governing
the species compositionof the communityis linear, then only one stable
compositionis possiblewithall the species represented.However,theremay
be otherstable pointswithsome of the species missing.. . . If the systemof
equationsdescribingthe transformation
of state is nonlinear. . . theremay
be multiplestablepointswithall speciespresent." Thus, we mustbe careful
to definethe taxonomicuniverse of interestwhen we ask whetheror not
multiplestable points exist. Our exampleshere are all of stable points with
some species missing,called "boundary points" by Lewontin. Conceptually
thereare as manyof thesepointsas thereare species in the community,
but
manyare probablytrivial. That is, removalof some species may have little
effecton the abundances of those that remain. However, in examples presentedhere thesepointswere nontrivial;for example,when the addition or
subtractionof an importantconsumerproduced dramaticchanges in abundance of remainingspecies.With consumerspresent,the existingcommunity
persistedforsomeperiodin spite of potentiallydisruptivecompetitiveinteractions,i.e., the exclusionof species by the competitivedominant(s). With
consumersabsent,the communitypersistedbecause potential invasions of
competitivelyinferior species were prevented by the competitivedominant(s). There was never any obvious environmentalexplanation for observed differencesin structure,since these events took place in the same
physicallocality.To explain whythe systemwas at a particularstable point,
it was necessaryto refer to specifichistoricalevents that determinedthe
presenceor absence of the consumer.
The existenceof stable boundarypoints does not rule out the possibility
that there may still be only one stable point with all species present,a
globally stable point. However, some of the above studies suggested the
presence of nonlinearities,multiple stable points with all species present.
For example, if Mytilus escaped being eaten by Pisaster when small, it
could becometoo large to be eaten and could persistin the presence of its
major predator (Paine 1974). The same was true for the Thais-Balanus
cariosus interactionabove the foraging zone of Pisaster (Dayton 1971).
Finally, it seemsunlikelythat rabbitscould eliminatethe woodyvegetation
which appeared in their absence (Harper 1969). As a result, the plant
communitywould probably not revert to its original state if rabbits returned.In these systemsthereare no globally stable points,and reference
to historicaleventsis again necessaryto explain why a systemis at a particular point. Holling (1973) reached an identical conclusion in a more
general treatmentof this same subject.
The stabilityof the various points can be visualized with respect to a
topographicsurface with valleys and craters correspondingto the basins
of attractionof stable points (Lewontin1969; Holling 1973). Depending on
the configuration
of a local basin, the stable point may be resistantto per-
MULTIPLE
STABLE
POINTS
871
turbationsin some directions,but not in others.Thus, we have seen that
some locally stable points are resistantto the invasion of some species, inferiorcompetitors,but can still be invaded by others,particular kinds of
consumers.The shape of a global basin can only be determinedby drastic
perturbationssuch as removingall speciesfromthe community(submerging
new plates) and followingcommunitydevelopment.One stable point in the
foulingcommunityat Beaufortappeared to have a large basin of attraction
withsmallervalleysand cratersinset into the sides,althoughtherewas still
some questionwhetherthis was a global basin or not.
In orderto constructa systemsmodel,"both the orientationand the class
of admissiblestimulimustbe explicitlyspecifiedbeforea state space is constructed" (Caswell et al. 1972). Most systemsmodelsassume global stability
and are descriptivestudies of energyor material transfersbetween compartments(Patten 1971, 1972; Van Dyne 1969); "destabilizing" experimentsof the kind describedhere are usually not done. Thus, all appropriate
stimulimay not be identifiedand the model may have limited use in describingnatural systemswithoutthe assumed constraints.Since a major
goal of ecologicalmodelingis thepowerof prediction,it seemsthata different
approach towardcommunity
modelingis required,at least forsomesystems.
Dayton (1972) suggesteda tactic based on the recognitionof "foundation
species," "the groupof criticalspecieswhichdefinemuchof the structureof
a community" (Dayton 1972). In the fouling communitythese would be
species such as Tubularia, Schizoporella, Styela, and Arbacia. Research
would consistof the experimentalanalysis of the interactionsbetweenthese
species, rather than being descriptiveand correlative.Once these interactionswere known,we could estimatethe numberof stable points and determinethe mechanismsinvolved in the production and maintenanceof
each. Effectsof perturbationson the communitycould thenbe predictedon
a knowledgeof whethertheywould alter the relationshipsbetweenfoundation species and produce communitiesof differentstructure.Of course,
changes in communitystructurewould also be expected if perturbations
alter the habitathyperspace.
SUMMARY
Evidence is presentedwhichindicatesthe importanceof historicalevents
in determiningthe structureof a variety of natural communities.In the
foulingcommunityat Beaufort,NorthCarolina,the orderof larval recruitmentdeterminedwhichspecies monopolizedthe available space during initial communitydevelopment.In othersystems,communitystructurecould
be explained only by referringto the specifichistoricaleventswhich determined the presence or absence of importantconsumers.Since historywas
relevantto the observedcommunitystructure,multiplestable points are an
undeniable reality in space and time in these systems.
872
THE AMERICAN
NATURALIST
ACKNOWLEDGMENTS
These ideas weregreatlyclarifiedthroughdiscussionswithJ. A. Commito,
S. P. Hubbell, R. H. Karlson, R. T. Paine, and D. I. Rubenstein.Financial
supportwas providedby the Officeof Naval Research (Contractno. N0001467-A-0251-0006).
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