Society for Conservation Biology
The Ecology of Extinctions in Kelp Forest Communities
Author(s): James A. Estes, David O. Duggins and Galen B. Rathbun
Reviewed work(s):
Source: Conservation Biology, Vol. 3, No. 3 (Sep., 1989), pp. 252-264
Published by: Wiley-Blackwell for Society for Conservation Biology
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TheEcologyofExtinctions
in
Kelp ForestCommunities
JAMESA. ESTES
U.S. Fish and WildlifeService
Instituteof MarineSciences
University
of California
SantaCruz,CA 95064, U.S.A.
DAVID 0. DUGGINS
FridayHarborLaboratories
University
of Washington
FridayHarbor,WA 98250, U.S.A.
GALEN B. RATHBUN
U.S. Fish and WildlifeService
P.O. Box 70
San Simeon,CA 93452, U.S.A.
Abstract: We recognizethreelevels of extinction-global,
local, and ecological -and provide examples of each. The
protectionand recoveryof sea otters(Enhydralutris) has
providedabundant evidenceof theconsequencesof theirlocal extinctionfrom kelp forestcommunitiesin the North
Pacific Ocean. Theseconsequencesinclude release of benthic
invertebrate
populations from limitationbypredation; deforestationof kelp beds due to increasedgrazing by herbivorous sea urchins,one of theotter'smain prey;and various
cascading effectsresultingfrom thebiological and physical
importanceof kelp in coastal ecosystems.Theseinteractions
probably wereimportantagents of selectionfor certainspecies.
Two otherexamples are discussed:Steller'ssea cow (Hydrodamalisgigas),a case ofglobal extinction,and spinylobsters,a possible case of ecological extinction.We speculate
thatgrazing by sea cows was an importantdisturbanceto
surface-canopy-forming
kelps and otheralgae in thelittoral
zones, but also point out thatany such interactionsprobably acted in concert withphysical disturbancesby ocean
waves. The ecological and evolutionaryimportanceof sea
cow grazingprobably will remain a matterof speculation
and conjecturebecause thespecies is globally extinct
Predation byspiny lobsterslimitsa varietyof littoraland
sublittoralinvertebrate
populations, particularlymollusks.
In one remarkableexample, the reductionor local extinction of spiny lobstersenabled predatorywhelks to increase
in size and abundance, ultimatelyresultingin a predatorpreyrole reversal.From theseand othercase studieswe con252
ConservationBiology
Volume 3, No. 3, September1989
Resumen: Reconocemos tres niveles de extinci6n: global,
local y ecol6gica y proporcionamos elemplos de cada una
La protecciony recuperaci6nde nutriasmarinas (Enhydra
lutris) ha proveido evidencia abundante sobre las consecuencias de su extinci6n local en comunidades de algas
marinas - bosques de kelp - en el norte del Oceano
Pacifico.
Estas consecuencias incluyenla liberaci6ndepoblaciones
de invertebrados(bent6nicos) de su limitaci6npor la caza
porparte de la nutria marina; la deforestaci6nde areas con
kelp debido al aumento delpastoreopor lospepinos de mar
herbivoros,una de las principales presas de la nutria marina; y varios efectosen "cascada " Estas interaccioneshan
sido,probablemente,agentes importantesde selecci6npara
ciertasespecies.
Discutimos dos ejemplos mais:la vaca marina de Steller
(Hydrodamalisgigas), que representaun caso de extincion
global, y la langosta espinoza, queposiblemente representa
un caso de extinci6necol6gica
Especulamos que el pastoreo de las vacas marinas ha perturbado de manera importanteal dosel superficial de los
bosques de kelp y a otras algas en las areas litorales,pero
asimismo senialamosque tales interaccionesactuaronprobablemente en conjunto a disturbiosfisicos causados por el
oleaje marino.
La importancia ecol6gica y evolutiva del pastoreo de las
vacas marinas seguira siendo,probablemente,un tema deespeculaci6ny conjetura,dado que dicha especieestdextinta
a nivel global.
Esteset al.
in KelpForestCommunities 253
Extinctions
clude that(1) theextinctionof consumersmay have broad,
and sometimesunexpected influenceson kelpforestecosystems; (2) direct or indirectinteractionswith now-extinct
speciesprobably exertedimportantselective influenceson
many extantforms; (3) such ecological and evolutionary
influencesare best understoodwherelocal or ecological extinctions,
followed byrecoveries,
haveprovidedcomparisons
in space or time;and (4) because of various ecological and
behavioral barriers,local extinctionsand theirecological
consequences may not be simply reversedbyprotectingor
reintroducingdepletedor locally extinctspecies.
La predaci6n de langostas espinozas limita a una variedad de poblaciones de invertebrados,litoralesy sublitorales,particularmentea moluscos.
En un ejemplo admirable, la reducci6n o extinci6n local
de langostas ha permitidoa las conchas univalvas espirales
(whelks) incrementarsu tamanioy abundancia dando por
resultadoa una inversi6ndel rol predador-presa
En base a estosy otros estudios,podemos concluir que
(1) La extinci6n de consumidorespuede tenervastas y,
algunas veces, inesperadas influencias en ecosistemas de
bosques de algas marinas (kelp).
(2) Probablemente, interacciones directas o indirectas
con especiesboy en dia extintasejercieroninfluenciasselectivas sobre muchasformas existentes.
(3) Estas influenciasecol6gicas y evolutivasse entienden
mejoren aquellos casos donde extincioneslocales o ecol6gicas,seguidas de una recuperaci6n,ban proporcionado comparaciones en tiempo o en espacio.
(4) Debido a numerosas barrerasecologicas y conductuales, las extincioneslocales y sus consecuencias ecol6gicas
no pueden ser invertidas simplementeprotegiendo o reintroduciendoespeciesdisminuidas o extintas localmente.
Introduction
cies maycause substantialadjustmentsin theabundance
and populationstructureof other species in the community,includingfurtherextinctions.
We recognizethreeclasses of extinctionsin thispaper: (1) global extinction-the ubiquitous disappearance of a species; (2) local extinction-the disappearance of a species frompartof its naturalrange;and (3)
ecological extinction-the reduction of a species to
such low abundance that,althoughit is stillpresentin
the community,
it no longerinteractssignificantly
with
otherspecies.
We discuss the ecological consequences of extinctionsin kelpforestecosystemsby describingthreecase
studies.The firstand best knownof these is thatof the
sea otter(Enhydra lutris). We summarizethe known
directand indirectinfluencesof sea otterpredationin
NorthPacifickelp forestecosystems,speculate on possible evolutionaryeffectsof these interactions,and
show how local extinctionsand recoveries served as
naturalfieldexperimentsthatled to these discoveries.
Next,we discuss two othercases in less detail- those
of the spinylobster(Panuluris interruptusin the eastern North Pacific and Jasus lalandii in the eastern
South Atlantic)and Steller'ssea cow (Hydrodamalis
gigas in the North Pacific). We conclude with some
generalcommentson the ecological and evolutionary
importanceofextinctionsin kelpforestsystems;withan
examinationof the circumstancesunderwhich the importanceof extinctionsis likelyto be understood;and
bypointingout whylocal extinctionsmaynot be easily
reversiblethroughreintroductionsor other conserva-
Ecologists have traditionallyinterpretedpatternsobservedin naturalpopulationsor communitiesbased on
extant physical and biological processes. Historical
events also can have importantinfluenceson natural
to assess
communities,althoughtheymay be difficult
unlesstheyrecurand are observed,or unlesstheyleave
otherclues in the historicalrecord.Extinctionsare historiceventsthathave occurredat varyingratesthrough
geological time (Berggren& VanCouvering1984; Valentine1985). Pleistoceneand Recenthuman-causedextinctionsalso are known or suspected (Martin 1973;
Martin& Klein 1984), and althoughspecies are being
ratesbecause of humanexploitalost at ever-increasing
tion or habitatdestruction,the consequences of these
losses are understoodpoorly,ifat all.
Justas all species varyin theirimportanceto the organizationof theirextantcommunities,so must it be
that extinctionshave been of varyingimportancein
shapingextant communities.By definition(Lewontin
1969), the loss of a species sets its communityat another "boundarypoint." However,unless thatspecies
withotherspecies in the commuinteractssignificantly
nity(e.g., it is an importantpredator,competitor,symbiont,mutualist,or prey),its loss mayresultin littleor
no adjustmentto the abundance and populationstructureof otherspecies. At the otherextremeare species
in communitieswithstrongly
thatinteractsignificantly
linkedfood webs (Paine 1980); the loss of such a spe-
ConservationBiology
Volume 3, No. 3, September1989
254
Extinctions
in KelpForestCommunites
tion measuresbecause of various behavioraland ecological barriers.
Case StudiesofExtinctions
Sea Otter-
Local Extinction
Sea otters once ranged across the Pacific rim from
northernJapan to central Baja California (Kenyon
was huntedto extinction
1969). The species apparently
in small areas by aboriginalpeople (Simenstadet al.
1978), but the Pacificfurtrade,whichbeganwithVitus
Bering'sexpeditionto NorthAmericaand the Aleutian
Islandsin 1741, markedthebeginningoflarge-scaleexBythebeginningofthetwentiethcenturysea
tirpations.
ottershad been eliminatedfrommost of theirnatural
range. Small remnantcolonies survivedat 13 known
locations,some of which later dwindledto extinction
(Kenyon 1969). Afterprotectionwas imposed in 1911
treaty,severalof theseremnantcolby an international
onies began to increase. By the late 1930s or 1940s
largepopulationsagainoccurredat severalislandsin the
western and centralAleutianarchipelago,and by the
early1970s sea otterswere at or near equilibriumdensityat numerousislandsin theAleutianand Kurilarchipelagos. Other isolated island groups,and most of the
shorelineofcontinentalNorthAmerica,remaineduninhabited.Some oftheseareas are now beingrecolonized.
The ecologicalconsequencesoflocal sea otterextinctionsare knownfromspatialcomparisonsof areaswith
and withoutsea otters,or fromtemporalchanges that
have followedthe species' recolonization.
DIRECT EFCTS
species
Sea ottersfeedon a hostofbenthicinvertebrate
(Kenyon 1969; Estes et al. 1981). The directeffectof
otterextinctionswas thatpopulationsofmanyofthese
were released fromlimitationby predainvertebrates
tion,whichchangedtheirabundanceand size structure.
There is evidence fromnumerousstudiesthatthe extinctionof sea otterscaused populationincreasesin a
wide varietyof invertebrates,
includingechinoids,gastropods,bivalves,and decapods (reviewed by Estes &
VanBlaricom1985; VanBlaricom& Estes 1988). Several
recentexamplesare Lauret al.'s ( 1988) findingthatthe
frandensitiesof red sea urchins(Strongylocentrotus
ciscanus) and purple sea urchins(S. purpuratus) declined to nearlyzero afterthe arrivalof sea ottersnear
PointSan Luis,California;the findingby Wendell et al.
(1986) that the recreational catch of Pismo clams
(Tivela stultorum)declined to zero afterthe arrivalof
sea ottersat Pismo Beach, California;and the reportby
Garsheliset al. (1986) thatthe commercialfisheryfor
Dungenesscrab (Cancer magister)collapsed following
thearrivalofsea ottersin easternPrinceWilliamSound,
Alaska.Estes& Palmisano( 1974) and Esteset al. (1978)
ConservationBiology
Volume 3, No. 3, September1989
Esteset al.
argued thatthe extinctionof sea ottersinfluencedthe
size distribution
of populationsof the green sea urchin
(Strongylocentrotuspolyacanthus) in the western
AleutianIslands by pointingout thaturchinswith test
diametersgreaterthan about 35 mm are almost never
foundat islandswith sea otters,whereas urchinswith
testdiametersfromabout 50-85 mm compose mostof
the biomass at islands lackingsea otters.Selection by
ottersof the largestsea urchinsis the mechanismmost
likelyresponsiblefor these differences(J.A. Estes &
D. 0. Duggins,in preparation).
INDIRECTEFFECTS
Most of the knownor suspectedindirectconsequences
of the extinctionof sea ottersare those resultingfrom
the release frompredation,and thus population increases, of herbivorousechinoids. Stronginteractions
(sensu Paine 1980) seem to occur between manyelementsof the food web in kelp forestecosystems.Because sea otterslimitedsea urchinsand sea urchinscan
limitpopulationsof fleshymacroalgae(see reviewsby
Lawrence 1975 and Harrold & Pearse 1987), and because kelp beds influencenearshorecommunitiesin a
ways (Mann 1982; Duggins 1988),
varietyof important
thelocal extinctionofsea ottershad cascadingeffectsof
broad influencein kelp forestecosystems.The primary
indirectconsequence of the local extinctionof sea otterswas thereductionofkelp and otherfleshymacroalgae due to increased grazingintensityby sea urchins.
Althoughother factors,such as physical disturbance,
can directlyaffectalgalpopulations(Dayton et al. 1984;
Foster& Schiel 1988), evidence froma wide range of
locations along the northeasternPacific leaves little
doubt about the importanceof sea ottersin structuring
kelp-dominatedcommunities (VanBlaricom & Estes
1988). For example,samplestakenin 1987 froma large
numberofrandomlyselectedlocations(128 sites,2,377
quadrats) in the western and centralAleutianIslands
showed thatkelp beds or deforestedhabitatswere respectivelycorrelated (with > 95 percent certainty)
withthepresence or absence ofsea otters(J.A. Estes &
D. 0. Duggins,in preparation).Similarsamplingprogramsrecentlycompleted or under way in southeast
Alaska(J.A. Estes & D. 0. Duggins,in preparation;J.A.
Estes, G. R. VanBlaricom,& D. Carney, unpublished
data) and BritishColumbia (J.Watson & J.A. Estes,unpublisheddata) are revealingsimilarpatterns.We (Estes
and Duggins) recentlyresampled five study sites in
Torch Bay,Alaska,which in the late 1970s, beforethe
arrivalofsea otters,were extensivelydeforestedby red,
purple,and green(S. drobachiensis) sea urchins(Duggins 1980). Several hundred sea otters recolonized
Torch Bay in 1986-87. By 1988 kelp beds had come to
dominatethese sites (and all otherswe sampled), and
locatingany livingsea urchins.
we had difficulty
Esteset al.
Reductionsin the abundanceof kelp and othermacroalgaethataccompaniedlocal extinctionsofsea otters
are knownto influenceor are suspectedof influencing
otherspecies of consumersin Pacifickelp forests.Various fishesare linked to kelp beds (Quast 1971a, b;
Ebeling & Laur 1988; Bodkin 1988). The largernearshore fishes,most notablyrock greenling(Hexagrammos lagocephalus) in the AleutianIslands,are one to
two orders of magnitudemore common where kelp
beds were presentthanwhere theywere absent(C. A.
Simenstad,
J.A. Estes,& R. K Cowen,unpublisheddata).
in turn,seems to influencetheforaging
Thisinteraction,
economics of other species. For example, Glaucouswinged Gulls (Larus glaucescens) fed largelyon interat AttuIsland (sea otterssparce or
tidal invertebrates
absent), whereas theyfed mainlyon fishat Amchitka
Island,wheresea ottersare abundant(Irons et al. 1986).
sea ottersfed almostexclusivelyon inverteSimilarly,
bratesat AttuIslandand extensivelyon fishat Amchitka
foragingeffort
Island (Estes et al. 1981). Furthermore,
uniformly
throughtheday
by sea otterswas distributed
at AttuIsland but peaked near dawn and dusk at AmchitkaIsland- patternsconsistentwith temporalvariofthedifferent
ationin availability
preygroups(Estes et
al. 1982).
We (D. 0. Duggins,C. A. Simenstad,and J.A. Estes)
have begun to look at the importanceof kelp production in coastal ecosystemsin the centraland western
AleutianIslands where most of the productioncomes
froma marinesystemin which fleshymacroalgaeand
are the two mainprimary
producers.For
phytoplankton
reasonsnot yetfullyunderstood,theseplantgroupsfix
the stable isotopes of carbon,12C and 13C,in different
ratios.By comparingthe ratio of these isotopes in a
varietyof consumerspecies between islandswith and
withoutsea otters,we foundthat,on average,75 percent (range 20-80 percent) of the organiccarbon is
derivedfromkelp productionat islandswithabundant
sea otterpopulations,whereasat islandslackingsea ottersthe relativeimportanceof kelp versusphytoplankton is reversed (Duggins et al., 1989). These results
indicatethatlocal extinctionsof sea otterssignificantly
affectedprimaryproductionand food web structurein
at least some coastal communities.
EFFECTS
EVOLUTIONARY
The evolutionaryeffectsof sea otter predation are
largelyunknown.Yet it is likely,ifnot inevitable,thata
species involvedwith such strongand broad-ranging
had selectiveinfluenceson otherspecies in
interactions
the community.
Estes & Steinberg(1988) argued thatpredationon
herbivoresby sea otters,theirancestors,and perhaps
marinemammals,influotherspecies ofbenthic-feeding
enced the evolution of kelps (order Laminariales)by
Extinctions
in KelpForestCommunities 255
creatingan environmentin which the intensityof herbivorywas low. The kelps probably radiated in the
NorthPacificlate in the Cenozoic because (1) the diversityof extant taxa is greatestthere,and (2) only
since the late Tertiaryhave water temperaturesin the
NorthPacificbeen low enoughto allow theexistenceof
any extantkelp species. These conditionsshould have
selected for species that were good competitorsbut
poorlydefendedagainstherbivores,an idea supported
by Steinberg's(1989) findingthatboth the varietyand
amountof knowndefensivesecondarycompounds are
low in North Pacific kelps, compared with kelps and
rockweeds(order Fucales) fromthe cool southwestern
PacificOcean where sea ottersor theiranalogues are
absent.If thisscenario is true,the evolutionaryhistory
of kelp communitiesfiguresprominently
in explaining
the extensivedeforestation
of kelp beds thatoccurs in
manyparts of the cool temperateto subarcticNorth
PacificOcean. Thus,followingthelarge-scaleextinction
of sea otters, the kelps (and perhaps other marine
plants) were subjected to intensitiesof herbivorythat
farexceeded those thathad occurred duringtheirlate
Tertiaryevolutionin the NorthPacificOcean
RECOVERYAND CONSERVATION
OF SEA OTfERS AND THE
NEAR-SHORE
COMMUNITY
Conservationists
and wildlifemanagershave been endeavoringto reestablishsea ottersin various parts of
theirnow unoccupiednaturalrange.Because ofthelimited capacityof thisspecies fornaturaldispersal,reestablishmenthas sometimes required reintroductions.
We nextreviewsome ofwhathas been learnedin these
relocationefforts,
and in studiesofsea otterpopulations
and near-shorecommunitiesduringthe process of recovery.
Most of the sea otter'shistoricalrange appears suitable for recovery of the species, despite pollution,
shooting,and entanglementin fishinggear. Most of the
coastalhabitatfromPrinceWilliamSound,Alaska,westward to Kamchatkaand the Kuril Islands has been recolonized,and populationsare probablyat or nearequilibriumdensityin much of thisarea. Besides occasional
surveysor anecdotal reports(summarizedby Kenyon
[1969]), littleis known about the rate at which these
populationsrecovered,thepatternsofrangeexpansion,
or the temporalpatternsof change in benthiccommunitiesthataccompanied these recoveries.More useful
information
is availablefromrecentnaturalrecolonizations(AttuIsland) or fromreintroductions
to southeast
Alaska,BritishColumbia,WashingtonState,Oregon,and
San Nicolas Islandin the southernCaliforniaBight.Populationchangeshave been documentedat each location
by periodic or occasional surveys.The methods and
data are fromJamesonet al. (1982, 1986), Brownell&
Rathbun(1988), Estes (manuscript),and unpublished
recordsof the U.S. Fish and WildlifeService.
ConservationBiology
Volume 3, No. 3, September1989
in KelpForestCommunities
Extinctions
256
Esteset al.
Two patternsare seen in these data (Fig. 1). First,
once established,the rate of increaseforeach population has been 17-20 percentper year. This rate,estimated fromthe least squares best fitof In population
countsversustime,probablyrepresentsthe maximum
rate of increase
2500-
OREGON SAN NICOLAS
ATTUISLAND, SOUTHEAST BRITISH WASHINGTON
ALASKA
ISLANO,
ALASKA
COLUMBIA STATE
CALIFORNIA
0
a) 1000-
N
(,
0
W 250 -
0
1001
F-
0~
25
0
00
~" 500-
Number
Released
sensu Caughley [1977]) for the
(rm.,
species in its naturalenvironment.Such high rates of
supportto theargumentthatmost
increaselend further
of the unoccupied rangeof the sea otteris highlysuitable forthespecies' recovery.Second,as notedbyJameson et al. (1982), the reintroducedcolonies declined
substantiallyafterthe animalswere released into the
Althoughthe numberof animalsrenew environments.
is known,theexact patterns
leased in each translocation
to ascertainbecause follow-up
of decline are difficult
surveyswere not done forseveralyears,except in Oregon and at San Nicolas Island.The Oregon population
and at San
was surveyedone year afterreintroduction,
Nicolas Island therehas been an intensiveand almost
continualmonitoringeffort.We have estimatedpostrelease populationdeclinesforsoutheastAlaska,British
the growth
Columbia,and Washingtonby extrapolating
regressionsback in timeto one yearaftereach reintrowere done overseveral
duction(where reintroductions
years,we have estimatedpopulationsize one yearafter
most of the animalswere moved- see Jamesonet al.
[1982]). These data and analysesindicatethatat best
oftheanimalsremainedin therelocated
aboutone-third
colony afterone year(Table 1). Declines were considerablygreater(to about 7-23 percentof the initialcol-
5000
Table 1. Declinesin reintroduced
sea otterpopulations.N, =
numbers
ofanimalsrelocated;N,+1= observedor estimated
one
yearlater.
0e
0
0
000
~~~~~~~~~0
0
100
Co0o
8
0
5-
00
TIME (years)
Figure 1. Population trendsin six recentlyreestablishedsea otterpopulations. TheAttupopulation is
a natural recolonization;all otherswerereestablished by relocations.Open circlesare countsfrom
population surveys.Darkened circlesrepresentnumbers of animals relocated.Note thatcounts at San
Nicolas Island were done at one-monthintervals
whereasone year or longerintervalsseparate counts
from the otherfive locations.
ConservationBiology
Volume 3, No. 3, September1989
SoutheastAlaska
BritishColumbia
WashingtonState
Oregon
San Nicolas
Island
412
89
59
93
47
Estimatedor
observednumber
1 year later
150t
28t
4t
21*
7*(10
Nt+1/Nt
.364
.315
.068
.226
mths)
.149
Observed
tEstimatedfrompopulation growthcurves
*
ony) in Washington,
Oregon,and at San Nicolas Island.
The rateofdecline at San Nicolas Islandappearsto have
been roughlyconstantduringthe first10 monthsafter
release (Fig. 1).
A preliminary
analysisof the resultsfromstudies at
San Nicolas Island has shown that the decline of sea
ottersat thissite is at least partlyand perhapslargelya
result of animals leaving the island. Since all the sea
ottersreleased at San Nicolas Island were individually
marked with unique flipper-tagcombinations, we
knownwhich ones stayed,which ones left,and the fate
ofsome ofthosethatdispersed.Of thefirst50 sea otters
takento San Nicolas Island duringAugustand September 1987, 3 are known to have died of stress at the
islandsoon afterrelease. There has been a distincttendencyforthe largeranimalsto leave. Of the remaining
47, 18 (38 percent) weighed 40 lbs. or more. Of the 8
animalsknownto have stayedat theIslandthroughJune
1988 (9 months),only 1 (14 percent) weighed 40 lbs.
or more at the timeof capture.By August1988, 10 of
the 14 animalsknownto have leftSan Nicolas Islandhad
been resightedback withinthe mainlandrange of sea
ottersin centralCalifornia.Others,as yet unidentified,
no doubt have returnedas well. Of the 10 known returnees,5 were resightedwithinabout 1 mile of the
pointofinitialcapture;4 ofthese 5 animalsweighed 40
lbs. or more when initiallycaptured.
We had presumedthat,because of the isolated locationofSan Nicolas Islandand the abundantinvertebrate
food, most of the relocated sea otterswould remain
there,even ifnot all survived.Thiswas clearlyan incorrect presumption.It is now known thatsea ottersare
capable of crossingthe 25 miles or more of open sea
separatingSan Nicolas Island fromthe nearestotherisland (SantaBarbaraIsland),or thenearly70 milesto the
mainlandcoast, and then navigatingthe ca. 200 miles
along the coast to theircapturelocationsin centralCalifornia.These observationsindicatethatsea otters,for
that
whateverreasons,have a stronghome rangefidelity
createsa behavioralbarrierto theirreestablishment
by
reintroductions.
The barrieris strengthened
by theeven
strongertendencyto dispersein subadultsand sexually
Esteset al.
matureadultsthanin juveniles,thuspreventingthe imof a translocatedpopulation
mediate reestablishment
withanyreproductivepotential.Homingbehavioris not
unique to sea otters;it has been foundto be a problem
in establishingreintroducedpopulationsof manyother
mammals,includingtheblackbear (Ursusamericanus),
wolf(Canis lupis), and pronghorn(Antilocapraamericana), to mentiononly a few (Boyer & Brown 1988,
Rogers 1988).
We now shiftto a briefdiscussion of community
and
changesthathave accompaniedthereestablishment
growthof sea otterpopulations.These data are being
analyzed and are to be discussed in more detail elsewhere(Estes & Duggins,in preparation).Here we compare temporalchangesin echinoidand macroalgalpopof sea ottersat two
ulationsafterthe reestablishment
sitesinAlaska:AttuIsland,westernmostoftheAleutians,
and the outercoast ofsoutheastAlaskanear Cape Spencer.
We have been workingat AttuIsland since the early
1970s and have data on kelp abundanceand thedensity
and size distribution
of sea urchinsfromsitesthathave
been occupied by otterssince thattime,as well as from
sites that were occupied more recently.In most inof sea otterswas followed
stances,the reestablishment
withina year or so by the loss of virtuallyall largesea
urchinsfromthepopulation(Fig. 2). However,thedensityof sea urchinsincreased,perhapsas a resultof recompetition.Anddespitethereducduced intraspecific
tion of large sea urchins,deforestedhabitatsremainin
mostareas;in contrastwithour expectations,kelpsand
othermacroalgaehave not recovered.Two ofthe study
sitesat Attuhave been withinthe otter'srangeand have
for at least 15 years.It
persistedin this configuration
appearsthatthe behaviorof thissystemis drivenby at
least two importantinfluences:the frequent,predictable, and heavyrecruitmentof sea urchins;and selection by sea ottersof the largerurchins.Evidence for
(i.e., large numbersof
heavyand frequentrecruitment
animals< 15 mm testdiameter)has been foundat virtuallyall areas and timesthatwe have sampled in the
westernand centralAleutianarchipelago(Estes & Duggins,in preparation).Dependingon thepresenceor abare typsence ofsea otters,sea urchinsize distributions
ically as shown in Fig. 2. We have estimatedthe size
ofurchinseatenbyottersfromtheremains
distributions
of urchindemipyramidsin otterscats. The method is
similarto thatused by Simenstadet al. (1978). These
dataindicatea preferencebyottersat AttuIslandforsea
urchins> about 30 mm testdiameter(Fig. 3). Apparentlyas sea otterpopulationsgrowtowardequilibrium
levels,as indicatedby thedata fromAmchitkaand Adak
islands(Fig. 3), smallerurchinsare eaten,althoughthe
otterscontinueto preferanimals> about 20 mmdiamand growthof sea
eter.Thus,with the reestablishment
otterpopulations,the systemin the westernAleutian
in KelpForestConununities 257
Extinctions
SOUTHEASTERN ALASKA
10l
s drobachiensis
s pupuats
WESTERN ALEUTIAN
ISLANDS
s franciscanuss
polyacanthus
4
E
2 x=E1m
x
3 4me
x=
9/
4m
c
>-
14
Z
12
D
Cl
10-
rr
B
ABSENT IN
SAMPLES
x=
10
x
14/m2
50
10
50
90
10
x
01 6/m2
50
90
130
10
134/M2
50
90
SEA URCHIN TEST DIAMETER (mm)
Figure2. Size frequencydistributionsof sea urchins
before(top panels) and after(bottompanels) they
were exploited by sea otters.The southeastAlaska
data are fromfive sites in TorchBay, surveyedin the
late 1970s (beforethearrival of sea otters)and
again in 1988 (two years afterthearrival of sea
otters).The westernAleutian Islands data contrasts
Alaid, Shemya,and Nizki Islands (ottersabsent)
withnearbyAttuIsland (otterspresentfor about 20
years). Shaded, hatched,and open sections offrequency distributionsin the upperpanels respectivelyrepresent(1) > modal size eaten by sea otters;
(2) < modal size eaten by sea otters;and (3) <
minimumsize eaten by sea otters(see Fig. 3).
Islands apparentlybehaves in the followingway: The
largestsea urchinsare removedsoon afterarrivalofthe
otters.However,heavy and predictablesea urchinrecruitment,
coupled withtheotter'spreferenceforlarger
sea urchins,providessmallerurchinswitha refugefrom
predation.High densitiesof smallurchins,sufficient
to
preventreestablishmentof fleshymacroalgae,persist
despitethe otter'spresence.Althoughwe have not yet
followedthesystemfromotterreestablishment
to equilibriumdensity,we suspect thatit remainsdeforested
by sea urchingrazinguntilthe ottersbecome limitedby
competitionforfood. Judgingby data fromAmchitka
and Adak islands,ottersbegin at thispoint to feed on
smallersea urchins,the densityand biomass of sea urchinsare reduced and the intensity
ofherbivoryis consequentlyreduced, and kelp beds eventuallyrecover
(Fig. 4). This process may require severaldecades.
The systemin southeastAlaska behaves verydifferently.Althoughhigh densitiesof three urchinspecies
persistin the absence of sea otters(Fig. 2), individuals
< 15 mmdiameterare rareor absentfrompopulations
ofeach species,thusindicatingthatrecruitment
is light
or infrequent,
compared with thatin the westernand
centralAleutians.Presumablysea ottersselect similarly
sized sea urchinsin southeastAlaska and the western
ConservationBiology
Volume 3, No. 3, September1989
258
Extinctions
in KelpForestCommunities
ATTU ISLAND
16
14
12E
10-
_
*
o
E
0
0,0
C
o.
z
>_
WJ
Esteset al.
MAX
Q NATURAL POPULATION
El CONSUMED BY SEA OTTERS
SOUTHEAST
w
o
z
8-
<
L
z
/KELP
6 -
m
4-
WU
0
2-
ALASKA
SEA URCHINS
?
MAX-
-----WESTERN ALEUTIAN ISLANDS
0
Cl)
0-
AMCHITKA AND ADAK
18-
~~ISLANDS
___________________________ ____ _____
p__
16-
0
0%14X
LiL
,-----------------------------------------
MAXIMUM
SEA OTTER ABUNDANCE
12-
Figure 4. Schematicrepresentationof community
changes on therockybenthosin the westernAleutian Islands and southeastAlaska with the reestablishmentof sea ottersand theirpopulation growth
to an eventual equilibrium density.
10864206
terns.Frequentsea urchin recruitment,
coupled with
size-selectivepredationbysea otters,appearsto provide
a temporaryecological barrierto recoveryof the kelp
forestcommunity.
Althoughmore speculativethanthe interactionsjust
described,thereis evidence thatsea otterpopulations
in some areas exist at multipleequilibriumdensities.
Thispossibilityis suggestedbythepatternofpopulation
recoveryat AmchitkaIsland (Fig. 5). Althougha remnantpopulationsurvivedat Amchitka,
it containedonly
a fewanimalsat the startof thiscentury.Fromobservations made at otherAleutianIslands where ottersare
rareor absent,we presumethatthe rockybenthossurroundingAmchitkaIslandwas largelydeforestedby sea
urchingrazingat thattime (anecdotally supportedby
observationsof Aleutswho lived at Amchitkaearlyin
10 2'0 30 40 5'0 6'0
SEA URCHINTEST
DIAMETER (mm)
Figure3. Size frequencydistributionsof sea urchins
in natural populations (open histograms)and eaten
by sea otters(hatched histograms)at AttuIsland
(sea otterpopulation below equilibrium density)
and Amchitkaand Adak islands (sea otterpopulations at or near equilibrium density).Sizes of urchins eaten by ottersweredeterminedby measuring
the lengthof demipyramidsin otterscats collected
fromAttu,Amchitka,and Adak islands. Urchintest
diameterswere estimatedfrom demipyramidlength
by Y = - 5.9484 + 5.7132 x (from Simenstad et al.
1978) whereY = urchintestdiameter(mm) and X
= demipyramidlength(mm).
Aleutians,althoughthere are no data fromsoutheast
Alaska.Withthe reestablishment
of sea otters,changes
in sea urchinpopulationshave been immediateand profound.Purpleurchinswere effectively
drivento extinction,and thedensitiesofred and greensea urchinswere
reduced to 0.25 percentand 2.33 percent,respectively,
of the numbertherebeforethe otter'sarrival(in contrast,numbersincreased 42.5 percent at AttuIsland).
Echinoid herbivoryin southeastAlaskawas effectively
ofkelpbeds
eliminated,allowingtherapidproliferation
(Fig. 4). Thus,temporalpatternsof communitychange
in response to the reestablishment
and growthof sea
otter populations differfundamentallybetween the
AleutianIslands and southeastAlaska,perhaps largely
because the herbivoreshave different
recruitment
pat-
ConservationBiology
Volume 3, No. 3, September1989
8000(
Q)
7000-
-
6000-
?
5000-
o
4000-
(D
-Q
3000-
E
Z
20001000-
0
1910 1920 1930 1940 1950 1960 1970 1980 1990
Year
Figure5. Long-termpopulation trendsof thesea ottersat AmchitkaIsland, Alaska Data are population
counts;solid line drawn by eye.
Esteset al.
this century-Kenyon [1969]). This situationmay,in
fact,have persistedfora centuryor moreifsea ottersat
were huntedto low levels earlyduringthefur
Amchitka
trade.In any case, it seems likelythatthe ottersthat
survivedthereinto thiscenturyfed in an environment
were plentifuland kelp
in which benthicinvertebrates
bed fisheswere rare.ObservationsfromAttu(J. Estes,
unpublisheddata) suggestthatas theotterpopulationat
AmchitkaIsland began to increase,the rockybenthos
remainedlargelydeforestedby sea urchingrazing.The
otterpopulationat Amchitkapeaked in the early1940s
(about 3,500 were counted,fromwhich about 4,500
dewere estimated- Kenyon [1969]), and thereafter
thisnumber.The
clinedto perhapsone-halfto one-third
population subsequentlyincreased again, and by the
early 1970s had reached 5,000-8,000, where it now
remains(Estes, manuscript).Inasmuchas manyotters
starved(Kenyon 1969), presumablytherewas intense
competitionforfood when the populationpeaked and
declined in the 1940s. The sizes ofsea urchinsselected
by ottersprobablyshiftedto includesmallerindividuals
duringthistime(as suggestedin Fig. 3), thusreducing
sea urchindensityand increasingkelp beds and associatedpopulationsofkelpbed fishes.Sea ottersapparently
did notfeedextensivelyon fishuntilsometimeafterthe
population declined in the early 1940s (Estes et al.
1978,1982). Thus,theinclusionoffishin thesea otter's
dietmayresettheequilibriumpopulationsize to a level
well above that attainableon a diet of invertebrates
alone.
It is intriguingto furtherspeculate that perhaps
learned behavioralskillsrequired forforagingon fish
were lost to local populationswhen the species was
reduced to a fewremnantcolonies at the end ofthefur
huntingera. Because benthic invertebratesprobably
were common comparedwithfishwhen otterpopulationswere low, the economicsofpreychoice mayhave
excluded fishfromthe otter'sdiet underthosecircumstances.Studiesofpreychoice in Californiashow highly
individualistic
diets(Lyons 1989), whichmaybe matrilineallyinherited(by learning)frommotherto pup (M.
Riedman,unpublisheddata). If similarlyindividualistic
diets occur in Alaska (they probablydo; Estes et al.
1981), and ifpiscivoryby sea ottersrequiressearchand
different
fromthoserequired
captureskillssubstantially
the behavioralinforfeedingon benthicinvertebrates,
novationsnecessaryforpiscivorymayrecuronlyrarely
in populationsthathave lost thisbehavior.Under cir(i.e.,
cumstanceswhere this behavior is cost-effective
benthicinvertebrates
when a populationis food-limited,
are rare, and fishare common), such an innovation,
once discovered,mightconveya largeadvantageto the
individualsthatadoptedit.Sincepreypreferencesin sea
ottersmay be learned duringthe extended period of
pup dependence (M. Riedman,unpublisheddata), piscivorycould easilyspread throughthe population.Al-
Extinctions
in KelpForestCommunities 259
thoughwe have no directevidence to supportthisidea,
it would explain the timecourse of populationchange
at AmchitkaIsland(Estes 1981), as well as the comparativelysmallsea otterpopulationat MednyIslandin the
CommanderIslands (i.e., about 1,000 animalsat an island about the size of Amchitka),which appears to be
food-limitedbut where ottersdo not feed on fish(A.
Zorin,personalcommunication).
There are numerouswell-documentedaccounts of
behavioralinnovationbeing spread througha population by imitativelearning(Bonner 1980). Two commonlycited examples,which involve optimalforaging
tactics, are the opening of milk bottles by blue tits
(Parus caeruleus) in England(Hinde & Fisher 1951)
and potato and wheat washing by Japanese macaques
(Macaca fuscata) in Japan (reviewed by Wilson
1975:170). Both of these examples involveindividuals
inventingor discoveringinnovativebehaviorsthat allowed themto takeadvantageofa new foodresourcevery similarto what we suggest may have occurred
with sea otters and fish.If this idea is true (and we
reiteratethatit is speculative),it would explain the rein sea otterdensitybetween popmarkabledifferences
ulationsthatdo notfeedon fish(e.g., centralCalifornia,
Prince WilliamSound, AttuIsland,and Medny Island)
and those thatdo (e.g., Amchitkaand Adak islands).
Steller'sSea Cow- GlobalExtinction
Steller'ssea cow, a dugongidsirenianthatlived in north
Pacifickelpforestcommunities,
was a strictly
algivorous
herbivore(Domning 1978). It was the lastspecies in an
old and reasonablywell known lineage. The hydrodafromthetropical
malinesapparently
radiatednorthward
Pacificwithpolar cooling late in the Cenozoic. Presumably the earliertropicaldugongidsfed extensivelyon
marineangiosperms(Domning 1978), as does the extant dugong,Dugong-dugon (Marsh 1982). The late
Cenozoic decline in marineangiospermsand radiation
of the kelps in the NorthPacificOcean (Estes & Steinberg 1988) was accompanied by a progressivereductionin thedentitionofadulthydromalines
(Takahashiet
al. 1986) and an increasedtendencyforsea cows to feed
on macroalgae(which do not containthe abrasivecompoundsfoundin marineangiosperms).Steller'ssea cow
was abundantacross the Pacificrimintothe
apparently
late Pleistocene,but probablydeclined abruptlyover
mostofitsrangewiththe "discoveryofAmerica"(Martin 1973) and the developmentof aboriginalmaritime
huntingcultures(Domning 1972). The most compellingevidence forthisidea is that(1) Steller'ssea cows
were abundantin the CommanderIslands when Vitus
Bering landed there in 1742, but were extinct elsewhere, and (2) the CommanderIslands are the only
location withinthe sea cow's range that never were
inhabitedby aboriginalpeople. Steller'ssea cows were
ConservationBiology
Volume 3, No. 3, September1989
260
in KelpForestCommunities
Extinctions
so numerousin the CommanderIslands thatthe early
furhuntersmade a special point of stoppingthere to
to the east;howtakeon freshmeatduringtripsfurther
ever,the species apparentlywas so vulnerableto hunters, and so highlysought after,that this last remnant
populationwas drivento extinctionby 1768, 26 years
afterits discovery.
Because Steller'ssea cow is globallyextinct,it is possible only to speculate on its ecological importancein
kelp forestcommunities.If the species was unable to
dive, as suggestedby Steller'sdirectobservations(Stejeneger 1887) and Domning's(1978) morphological
evidence,whateverinfluenceit had as a grazerin kelp
forestcommunitiesmusthave been limitedto the surfacecanopyand littoralzones.Atbest,theanimalsprobablycould feed no more thanseveralmetersbelow the
surface.There are four main surfacecanopy-forming
kelps in the NorthPacific:Macrocystispyriferaand M
integrifolia (giant kelps) range from about Prince
William Sound to central Baja California;Nereocystis
leutkeana (bull kelp) ranges fromUmnak Island to
northof PointConception;and Alaria fistulosa ranges
fromnear Kamchatkato the Queen CharloetteIslands
(Druehl 1969). AlthoughSteller'ssea cow mayhave fed
extensivelyon these species, disturbanceby sea cow
grazingon the surfacecanopy musthave acted in concertwithphysicaldisturbancesfromocean waves. Thus
to attributelifehistorycharacteristicsof
it is difficult
anyofthesespecies as adaptationsto sea cow grazing.If
cost to anyof
sea cow grazingconstituteda significant
the surface canopy-formingkelps (beyond that incurredfromphysicaldamageby ocean waves) and ifsea
urchinpopulationswere so small as to be an insignificant selective factoron kelps, one mightexpect the
surfacecanopy kelps to be defendedbetterthan the
epibenthickelps againstherbivores.But this does not
appear to be true. Althoughsome of the epibenthic
ofsecondary
concentrations
kelpssynthesizesignificant
chemicals(phlorotannins)thatare knownto deter invertebrategrazers,all of the surfacecanopykelps containlow concentrationsofthesecompounds(Steinberg
bothAlaria fistulosa and Nereo1985). Furthermore,
cystisleutkeana are competitivelysubordinateto the
epibenthickelps (Dayton 1975a; Duggins 1980). Thus
it seems unlikelythatsea cow grazingmediatedcompetitionbetweensurfacecanopyand subcanopykelp species, at least in boreal and subarcticregions.
The same may not have been true for kelp forests
dominatedbyMacrocystispyriferain the temperateto
and Baja California.
watersofCalifornia
warm-temperate
lightHere thisperennialspecies oftenhas an important
limitinginfluenceon the epibenthiccanopy (Reed &
Foster1984; Daytonet al. 1984). Macrocystisforestsin
centraland southernCaliforniaoftenare largelydevoid
of an epibenthicalgal assemblage,the rockybenthos
instead being covered with sessile suspension-feeding
ConservationBiology
Volume 3, No. 3, September1989
Esteset al.
invertebrates.
One can easilyimaginethatsea cow grazing opened the Marcrocystissurfacecanopy,allowing
morelightto penetrateto thesea floor.Thisinteraction,
whichmayhave been especiallyprevalentduringspring
and summer when kelp growth is high and stormgeneratedwave disturbanceis low, mighthave driven
Macrocystis-dominated
communitiestowardincreased
abundance of epibenthickelps and other macroalgae,
and decreased the abundances of benthic suspension
feeders.Similarargumentsabout the possible influence
of sea cows can be made forepibenthicalgae livingin
the littoralzones and at the sublittoralfringe(which,
fromthe morphologicaland behavioralevidence,was
perhapsthe sea cow's mainfeedinghabitat).These species are subjected to strongdisturbancesfromocean
waves (Dayton 1973, 1975b; Paine 1979; Sousa 1979),
effectsthatmayhave been largelycomplementary
to sea
cow grazingunless sea cows were selective foragers.
Furthermore,
disturbancesfromsea cow grazingmay
have been importantthroughoutthe year, whereas
ocean wave disturbancesare most importantafterautumnand winterstorms.It is also intriguing
to note that
two surface-canopy
kelps (Macrocystisspp. and Alaria
fistulosa) bear their sporophylls near the bottom,
whereas most of the epibenthickelps distributetheir
reproductivetissuesover thelengthoftheirblades. The
sad factis thatthe global extinctionof Steller'ssea cow
tookwithit anypossibilityof obtainingdirectevidence
about its herbivorousrole in kelp forestcommunities,
or as a selectivefactorshapingkelp evolution.
- Ecological
Extinction
SpinyLobsters
The Californiaspiny lobster ranges fromabout Point
Conception to centralBaja California.This species is
known to prey on various bivalves, gastropods,and
echinoids as well as on animal detritus.The size and
abundanceof spinylobstershave been greatlyreduced
throughoutthe rangeof the species by commercialand
recreationalfisheries(Duffy1973). Tegner & Dayton
(1981) and Tegner& Levin(1983) suggestedthatlobstersare importantpredatorson sea urchinsin subtidal
communities,and Robles (1987) demonstratedexperimentallythatintertidal
populationsof mussels(Mytilus
edulis andM. californianus) are limitedby lobsterpredation in an area closed to fishingat Santa CatalinaIsland, California.These findingssuggestthatspinylobsters may have been importantpredators in warmtemperate kelp forest communities before their
populationswere reduced by the fishery.
Alternatively,
iflobsterpopulationswere reduced by sea otterpredation (our recent studies at San Nicolas Island have
shown that sea otterseat lobsters), lobster predation
mayhave been relativelyunimportant
when sea otters
were stillabundantsouth of Point Conception.
The South Africanspinylobsterhas been shown by
Esteset al.
Barkai& McQuaid (1988) to be an extremelyimportant
predatorin kelpforestcommunities.In theirstudy,subtidalcommunitieswere comparedbetweentwo nearby
islands,one where lobsterswere absent and another
where lobsterswere abundant.Caged lobsterssurvived
indefinitelyat both islands, thus demonstratingthe
physicalsuitabilityof both islands for lobsters.Anecdotal evidence provided by local fishermenindicated
that both islands supportedabundantlobsterpopulationsuntilthe early1970s, but forreasonsstillunclear
(local oxygendepletionwas speculated),lobstersat one
of the islandsdeclined to extinction.Both islandswere
laterclosed to fishing.
Barkai& McQuaid (1988) found
thatthe rockybenthosat the islandwith lobsterssupported a lush kelp forest,and that lobstersmade up
about 70 percentof the macroinvertebrate
biomass.In
contrast,therockybenthosat theislandlackinglobsters
was dominated by a dense subtidal mussel bed and
abundantpopulationsof several species of predatory
whelks.Laboratory
and fieldexperimentssuggestedthat
lobsterpredationon musselsand whelkswas probably
responsibleforthe observeddifferences
betweenthese
communities.In an effort
to testthishypothesis,
Barkai
& McQuiad (1988) translocated1000 lobstersto the
islandwhere theyhad become extinct.Remarkably,
the
predatorywhelksattackedand consumedall ofthe lobsters. This study demonstrateda wholly unexpected
role switchingbetweenpredatorandpreyafterthelocal
extinctionor reductionoflobsters.Presumablythe loss
or reductionoflobstersdrovethesystemto an alternate
stable state (sensu Lewontin1969; Sutherland1974),
fromwhich thereis no obvious means or likelihoodof
recovery,evenwhen lobstersare reestablishedand protectedfromfishing.
Conclusions
It is probablytruethatfew marinespecies are globally
extinctbecause ofhumanactivities,althougha number
have come close. On the otherhand,thereare numerous examples of human-causedlocal extinctions,and
due largelyto commercialand recreationalfisheries,
thereprobablyare few marinesystemsin which some
species have not been reduced to such low levels that
their ecological importanceis either insignificant
or
drasticallyaltered.Unfortunately,
althoughpopulations
of numerouspotentiallyimportantspecies have been
recentlyreduced in kelp forestcommunities,usually
little or nothingis known of the ecological consequences of these reductions.A few otherexamples include giant sea bass (Stereolepsis gigas), California
sheephead (Semicossyphuspulcher), lingcod (Ophiodon elongatus), and rock crabs (Cancer spp.) in the
North Pacific,Americanlobsters(Homarus americanus) in the NorthAtlantic,and loco (Concholepis con-
Extinctions
in KelpForestConununities 261
cholepis) in the South Pacific.The ecological importance of these species is almost entirelyunknown,
exceptfortheCaliforniasheephead(e.g., Tegner& Dayton 1981; Cowen 1983), the Americanlobster(Mann
1973; Breen & Mann 1976; but see Pringleet al. 1982;
Miller 1985), and the loco (Castilla & Duran 1985;
Castilla& Paine 1987; Duran et al. 1987; Moreno et al.
1986).
Fromwhatis knownin severalspecificcases,we offer
the followingconclusionsabout the ecology of extinctionsin kelp forestecosystems:
(1) Some consumershave broad influencein kelp
forestecosystems:Extinctionof these species,whether
global, local, or ecological, may have had profound,
complex,and unexpected consequences.
(2) In some instancesthese interactionsmay have
been importantover evolutionarytime in shapingthe
lifehistoriesof associated species. We have speculated,
in one such possible example,thatpredatorson herbivorous macroinvertebrates
influencedthe evolution of
defensestrategiesin thekelps.Evolutionary
interactions
ofthissortno doubthave affectedboththe characterof
extant communitiesand the consequences of extinctions.
(3) These ecological and evolutionaryeffects,and
theirmechanisms,are best understoodwhere local extinctionshave occurred.In particular,such understanding has been derivedby comparingareas where populationsare extinctwiththosewhere theyare not,or by
watchingareas recoverfromlocal extinction.The consequences ofglobal extinctionsprobablywill alwaysremain poorlyunderstood.Steller'ssea cow is an exemplary case: although these animals probably were
abundantin NorthPacifickelp forestcommunities,and
thusprobablyate largequantitiesofkelp and othermacroalgae,the ecological and evolutionaryconsequences
of thisinteraction,thoughpossiblyveryimportant,
are
largelya matterof speculation.Similarly,
littleis known
about the consequences of mostecological extinctions.
One difficulty
is that most population reductionsoccurredbeforescuba permittedextensiveobservationor
data acquisitionfromunderwatercommunities,and at
presentthereare no obvious comparisonsin space or
time fromwhich the effectsof population reductions
mightbe evaluated.However,in some instancesthereis
hope of betterunderstandingecological extinctionsif
changesthatoccur afterthe cessationof humanexploitationare carefullydocumented.The sea otter in the
easternNorthPacificand the loco in the easternSouth
Pacificprovidegood examples of the power of thisapproach.
(4) Because ofbehavioralor ecological barriers,local
extinctionsand theirecological consequences maynot
be simplyreversiblethroughprotectionor species reintroductions.
We have foundwith sea ottersthateven
thoughhabitatmay be suitable for reestablishingthe
ConservationBiology
Volume 3, No. 3, September1989
262
in KelpForestCommunities
Extinctions
species,reintroductions
are difficult
because of individuals' fidelityfor an establishedhome range.With the
SouthAfricanspinylobster,role reversalbetweenpredator and prey seems to have renderedthe community
lobstersonce they
whollyunsuitableforreestablishing
were absent froman area long enough for theirprey
In instanceswhere
populationsto increasesubstantially.
recoveryof a locally or ecologicallyextinctspecies is
possible,theremaybe ecological barriersto reestablishmentof the naturalcommunity.
Kelp forestecosystems
in thewesternAleutianIslandsprovideone such example. Because of frequentsea urchin recruitmentand
preyselectionby sea ottersof the largerurchins,habitatsdeforestedofkelpbeds by urchingrazingpersistfor
and growthof
longperiods,despitethereestablishment
sea otterpopulations.Kelp populationseventuallybecome reestablished,but this may require decades. In
eventsare
otherregions,where sea urchinrecruitment
rare, kelp beds recover almost immediatelyafterthe
reestablishment
of sea otters.Finally,theremaybe beof
havioralor ecological barriersto thereestablishment
an originalor naturalpopulation equilibriumdensity.
Indicationsofsuch subtleand complex processes again
come fromstudies of sea otters.We have speculated
thatpiscivoryin thisspecies maybe necessaryto support the high-density
populationsthatoccur at certain
islandsin the centraland westernAleutianarchipelago.
Conceivably,piscivorousforagingtactics,which may
have been lost to sea ottersduringan extendedperiod
were commonand fishrare,need to
when invertebrates
be rediscoveredbeforehighequilibriumdensitypopulationscan be reattained.
Althoughsome of our suggestionsare admittedly
speculative,they indicate that conservationstrategies
more complexprocessesthan
mayinvolvesubstantially
thoseimaginedin thetypicallysimpleconstructsofnatural resourcemanagement.
Acknowledgments
We are grateful
to themanypeople who have assistedus
throughthe years with fieldworkin the AleutianIslands, southeastAlaska,and California.We thankthe
AlaskaMaritimeNationalWildlifeRefugeforfieldsupport in the AleutianIslands; the U.S. Coast Guard for
transporting
personneland equipmentto remotesites
in the NorthPacific;the NationalParkServiceforsupportand shiptimein southeastAlaska;and theU.S.Navy
foraccess to San Nicolas Island.Fundingwas provided
by the U.S. Fish and WildlifeServiceand by NSF Grant
No DfPP 84? I6.?
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