Intertidal Community Structure: Space

Transcription

Intertidal Community Structure: Space-Time Interactions in the Northern Gulf of California
Author(s): Curtis M. Lively, Peter T. Raimondi and Lynda F. Delph
Source: Ecology, Vol. 74, No. 1 (Jan., 1993), pp. 162-173
Published by: Ecological Society of America
Stable URL: http://www.jstor.org/stable/1939511
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Ecology, 74(1), 1993. pp. 162-173
(C 1993 by the Ecological Society of America
INTERTIDAL COMMUNITY STRUCTURE: SPACE-TIME
INTERACTIONS IN THE NORTHERN
GULF OF CALIFORNIA'
CURTIS
M.
LIVELY
Bloomington,Indiana 47405 USA
Biology Department,Indiana University,
PETER
T.
RAIMONDI2
Parkville,Victoria,Australia 3052
Zoology Department,Melbourne University,
LYNDA
F.
DELPH
Bloomington,Indiana 47405 USA
Biology Department,Indiana University,
Abstract. Long-termstudiesare requiredforan understandingof how temporalvariation and space-timeinteractionsaffectthe structureof communities.Here we reporton
a long-termstudyof the independenteffectsof, and the interactionsamong, two sources
oftemporalvariation(seasonal and annual) and two sourcesof spatial variationfora rocky
intertidalcommunityin the northernGulf of California.The sources of spatial variation
were: (1) microspatialeffectsdue to the foragingpatternsof a common predatorysnail
due to differences
among sites.The results
(Acanthinaangelica) and (2) macrospatialeffects
from semiannual samples of 100-cm2 quadrats showed highlysignificanttemporal and
spatial effectsforall membersof the sessile community(barnacles,mussels,algae) and for
limpets over the 8-yr study period. There were also highlysignificantseason x space
interactionsforall sessile membersof the community,whichprobablyresultedfromseasonal settlementby thesessile membersofthecommunity,and aestivationby thepredator.
Finally,we observed highlysignificantyear x space effectsas well as year x season x
formostspecies.These latterinteractionscan be understoodas an amplification
space effects
of seasonal and spatial effectsdue to the largelyunpredictabledifferences
among years.
An analysisofthevariance componentsshowedthatmost ofthevariationin percentage
while most
cover of barnaclesand a brownencrustingalga was due to microspatialeffects,
of the variation in mussels, limpets,and a greenalga was due to year and season effects.
This combination of results suggeststhat competitionand predation by Acanthina are
relativelymoreimportantin controllingthedistributionsand local abundances ofbarnacles
and encrustingalgae, and thatunpredictabledifferences
among yearsin settlementare more
importantin controllingthe local population densities of mussels and limpets. The imof short-termexare discussed in relationto interpretation
portanceof these differences
perimentalstudies in population and communitystudies.
Key words: algae; barnacles; communitystructure;Gulf of California; limpets; long-termfield
spatial heterogeneity;
temporal
study;mussels;predation;rockyintertidalcommunity;seasonal effects;
heterogeneity.
Underwood 1981, 1984, Underwood et al. 1983, Sousa
Experimentson rockyintertidalshoreshave provid- 1984, Menge and Sutherland1987, Menge and Farrell
ed much of theempiricalfoundationformoderncom- 1989). Otherrecentstudieshave been concernedwith
munityecology.The earlyexperimentson competition the indirecteffectsbetween consumers of competing
(Connell 1961a), predation (Connell 1961b, Paine adult prey (e.g., Lubchenco 1978, Menge 1978a, b,
1966a), and disturbance(Dayton 1971, Sousa 1979) Underwood et al. 1983, Jernakoffand Fairweather
led to excitingideas concerningthe general mecha- 1985, Dungan 1986, 1987, Livelyand Raimondi 1987,
nisms underlyingthe zonation of sessile species, and Petraitis1990), and therehas been a growingawareness
the mosaic of species withinthesezones (Menge 1976, of the importanceof larval settlementin structuring
Denley and Underwood 1979, Paine and Levin 1981, thesecommunities(e.g., Grosberg1982, Shanks 1983,
Caffey1985, Connell 1985, Gaines et al. 1985, Raimondi 1988a, b, 1990, 1991). The resultsoftheselatter
I Manuscriptreceived27 June1991; revised13 March 1992;
studieshave generallyshown thatsettlementis patchy
accepted 16 March 1992.
2 Presentaddress: Marine Science Institute,Universityof in both space and time.
Given theexistenceofspatialand temporalvariation
California,Santa Barbara, California93106 USA.
INTRODUCTION
January1993
INTERTIDAL
COMMUNITY
we shouldexpectto findthattheintensity
in settlement,
and importanceof predation and competitionvaries
in space and time. For example, intraspecificcompetitionamong sessileplanktotrophicspecies should vary
among yearsifthe numberof recruitinglarvae is variable and sometimesless than thatrequiredto saturate
the available resources. Similarly,the importanceof
competitionvaries withsettlementdifferinterspecific
ences among years (Connell 1985), and these differences maypromotespeciescoexistencein thelongterm,
especially when they are driven by "storage effects"
(Chesson 1985, 1986). Finally,predationand herbivoryby the mobile membersof intertidalcommunities
are also known to vary in both space and time, especiallyin tropicaland subtropicalareas (e.g., Garrity
and Levings 1981, Fairweather et al. 1984, Lively
1986a, Fairweather1988a). Hence, a completeunderstandingof the structureof intertidalcommunitiesrequires an evaluation of the importance of temporal
ofspace and time
variationand thenon-additiveeffects
over multiplespatial scales (Underwood 1984, Dayton
and Tegner 1984, Butlerand Chesson 1990). Such an
evaluation requires long-termstudies. Herein, we report the results of a long-termstudy of spatial and
temporal variation in a rocky intertidalzone in the
northernGulf of California.We found markeddifference among species in the relativeimportanceof temporal variation,and highlysignificantspace-time interactionsformost species studied.
STUDY
SITE AND SPECIES
The northernGulf of Californiais a highlyseasonal
regiondue to theinfluenceofthe surroundingSonoran
Desert. Sea surfacetemperaturesrangefrom90C in the
winterto 320C in the summer,and intertidalsubstratum temperaturesrange from <00C in the winterto
>500C in the summer (Thomson and Lehner 1976,
Raimondi 1988a). In addition, waves are generally
small, and sometimes absent, so there is little moderationby splash of the atmosphericextremesduring
low tide. For example, Lively and Raimondi (1987)
estimatedthatwave actionwettedtheirsitesan average
of only 6 min before the incoming tide would have
wettedthem on waveless days. In spite of these extremes,or perhapsbecause of them,the northernGulf
has a highdiversityof species, and a high proportion
of endemic species (Brusca 1980).
The exposed rockyintertidalshore near Puerto Penasco, Sonora, Mexico, is the most extensivelystudied
in the northernGulf of California.The tidal rangein
thisregionis > 7 m duringspringlow tides,whichoccur
in the morningsand evenings(Thomson 1980-1988).
Experimentalstudies therehave focused on barnacles
(Chthamalus anisopoma and Tetraclita stalactifera),
mussels(Brachidontessemilaevis),algae (especiallyUOva
sp. and Ralfsia sp.), carnivoroussnails (Acanthinaangelica and Morulaferruginosa),and limpets(Collisella
strongianaand C. acutapex)(Dungan 1985, 1986, 1987,
STRUCTURE
163
Lively 1986a, b, Malusa 1986, Lively and Raimondi
1987, Raimondi 1988a, b, 1990, 1991).
The carnivoroussnail Acanthina appears to be especially important in structuringthis community
(Lively 1986a, Dungan 1987). It makes use of a single
spine on the marginof its shell to penetratethe opercularplatesofundefendedbarnacleprey(Yensen 1979,
Malusa 1985), and it is responsible for inducingjuvenile Chthamalus to develop as a discrete ("bent")
morph that is more resistantto specialized attack of
thiskind,but less fecundand slowergrowingthan the
undefended("conic") morph (Lively 1986a, b). Predation by Acanthina is spatially variable as a direct
resultof its foragingbehavior. When exposed by low
tides the snails emergefromcracksand crevicesin the
reefand attack barnacles duringthe entireperiod of
tidal exposure. As the incomingtide reaches the foragingindividuals,theyreturnto crevicesand aggregate
there,possiblyto escape predationby fishes.Exclosure
experimentsshowed that this back-and-forthmovementby the snails createsa discretearea of highbarnacle predation near to crevices,while slightlymore
remote areas receive little or no predation (Lively
1986a). It is in theseregionsofhighpredationintensity
that the bent formof Chthamalus is most commonly
observed. In addition to this spatial variation in predation intensity,there is also temporal variation in
predationdue to aestivation by Acanthina. Foraging,
which is most intense duringthe winter,declines to
virtually zero during the summer months (Lively
1986a). This summertimelull in predationby Acanthinacorrespondsto a peak in recruitment
by the barnacle Chthamalus (Dungan 1986, Malusa 1986, Raimondi 1990).
The barnacle Chthamalus and the mussel Brachidontescompete forprimaryrock space. Settlementby
Brachidontes(a small"seed" mussel,< 10 mmin length)
is facilitatedby the presenceof Chthamalus (basal diameterup to 7 mm), whichcan become overgrownby
themussel (Dungan 1986, Livelyand Raimondi 1987).
This interactionis mediated by the carnivoroussnail
Morula, which foragesduring periods of tidal inundation throughoutthe year and specializes on mussel
prey(Lively and Raimondi 1987). Algae also compete
withbarnaclesforprimaryrockspace, and theoutcome
of theseinteractionsis affectedby the presenceof limpets. Dungan (1986, 1987) has shown that limpetsof
the genus Collisella have a positive effecton barnacles
in this regionby removingthe encrustingbrownalga,
Ralfsia, and therebycreatingprimaryrock space for
barnacle settlement.This positive directeffectof limpets on barnacles translatesinto an indirectpositive
effecton Acanthina(Dungan 1987). Conversely,Acanthina has an indirectpositive effecton limpetsby removing barnacles, so this predatorysnail and its coexistinglimpetsmay be regardedas indirectmutualists
in the sense of Vandermeer(1980) (Dungan 1987).
The goal of the presentstudy was to estimate the
Ecology,Vol. 74, No. 1
CURTIS M. LIVELY ET AL.
164
interactionsbetweenseasonalityand yearon two scales
of spatial variation: (1) differencesamong adjacent
withinsitesdue to the
similarsites,and (2) differences
presenceof local refugiaforAcanthina,the "barnacle
specialist" (Paine 1966b). This informationis theninterpretedin the lightof the informationgained by the
directexperimentalstudies outlined above to suggest
hypothesesconcerningthe relative impacts of competition,predation,and recruitmenton the different
species in this community.
METHODS
AND MATERIALS
In January1980, eightsites(1-2 m above mean low
water) were selected withina 300-M2 area at Pelican
Point,a graniticoutcropnearthetownofPuertoPenasco, Sonora, Mexico (31020' N, 113?40' W). These sites
were all ; 1 m2 in total area, and were bordered by
crevices of the typenormallyused foraggregationby
Acanthinaduringperiods oftidal inundation.All eight
siteshad a minimumdiameterof 80 cm ofrocksurface
thatwas unbrokenby crevices.Two 15 x 15 cm quadrats were established near to crevices (within20 cm)
and, similarly,two quadrats of the same size were establishedfarfromcrevices(>40 cm) at all eightsites;
the resulting32 quadrats werethencleared of attached
species and "sterilized" using a propane torch. The
quadratsweresampled at leastonce duringthesummer
(Julyor August) and winter (December or January)
from 1980 through1988 for barnacle cover, mussel
cover,and algal cover. These samples consistedof percentagecover estimates,gained by placing a 10 x 10
cm plexiglass plate in the center of a quadrat, and
countingthe numberof randomlyplaced dots directly
over each of the sessile species. Limpets (primarily
Collisella strongiana,with some C. acutapex) within
the marginsofthe 10 x 10 cm area weresimplycounted.
ofproximityto crevTo decouple thephysicaleffects
predation by
ices (e.g., wave wash) fromdifferential
Acanthina,fencesweremaintainedat one nearand one
far quadrat at all eight sites for the firstyear of the
experiment(along with unfencedcontrols;see Lively
1986a for details). The fence treatmentshowed that
predationby thiscarnivoroussnail is severenear crevices, but rare or absent far fromcrevices. Moreover,
the communitiesnear to and far fromcrevices were
similarin theAcanthinaenclosures,whichsuggeststhat
ifphysicalfactorsvaried as a functionof distancefrom
crevices, they did not affectthe communitysignificantly (Lively 1986a). Direct counts of the predator
showed in additionthatpredationby Acanthinais seasonal, with highdensitiesof the snails foragingin the
autumnthroughspring.The presentstudyis concerned
with those data collected from these same quadrats
fromsummer 1981 throughwinter1988. This period
followsthe removal of fencesand the convergenceof
fencedand unfencedquadrats withrespectto barnacle
cover (see Lively 1986a: Fig. 4); hence the previously
fencedquadrats wereused as replicatesofthe near and
far"treatments"at each site,to give two replicatesper
cell.
The resultswere analyzed by a repeated-measures
analysis of variance, using both univariateand multivariateprocedures(SAS 1982). MultivariateP values
are consideredto be morereliablethanthosegenerated
fromunivariate repeated-measuresmodels (Tabachnick and Fiddell 1983), but the univariateresultswere
needed for the estimation of variance components.
Variance componentswerecalculated followingWiner
(1971), and were used to calculate the percentageof
variationdue to each ofthespatialand temporalfactors
forall species. These componentsare extremelysensitive to experimentaldesign (P. S. Petraitis,personal
communication),so we have restrictedour discussion
to qualitativecomparisonsamong species in the same
experiment.
The two independentvariables "season" (summer
vs. winter)and "distance" fromcrevices(near vs. far)
were analyzed as fixed effects(see Sokal and Rohlf
1981). "Year" was also analyzed as a fixedeffect,because we cannot be sure that the period of studyis a
valid representationof the more generalsituation.For
example there may be interdecadal variation of the
kind reportedby Dayton (1989) in an Antarcticcommunity;our studyfolloweda dramatic decline in the
once-abundanttop predator,Heliaster kubiniji(Dungan et al. 1982). Finally,"site" was analyzed as a random effect(see Sokal and Rohlf 1981); however,generalizationsshould be restrictedto the upper part the
Chthamalus zone where Acanthina are reasonably
abundant.
RESULTS
For the conic morph of the barnacle Chthamalus,
all of the main effectsand most of the interactions
among main effectswere highlysignificant(Table 1).
However, most of the variation(24%) was due to distance from predator refuges(Fig. 1). The season x
distance interactionaccounted for - 10% of the variation (suggestingthat a seasonal effectoccurrednear,
but not farfrom,crevices),and differences
among sites
accounted for _5% of the variation. The least influential factorswere year and season, which each accounted for <3% of the variation, and the year x
season interaction,which accounted for <2% of the
variation. Hence, for our experimentaldesign, it appears that spatial factorswere more influentialthan
temporalfactorsin determiningthe occupation of primaryrock space by the conic morph of Chthamalus.
Similar resultswere observed forthe bent morphof
the barnacle (Fig. 2). Distance fromrefugeswas the
accountingfor21% ofthe
most importantsingleeffect,
variation (Table 2). However, the season x distance
effectwas less influentialthan observedforconics,and
the year x distance and the year x season x distance
effects
wererelativelymoreinfluential(compareTables
January1993
INTERTIDAL
COMMUNITY
STRUCTURE
BentmorphofChthamalus
Conic morphof Chthamalus
80 -
Cc
10|
10
60
0
as40 f refugit
(T
so
yT
Near
|
I
~~Far
8-
0 4
< 61
ToI
20
--~
-
0
~-~~
z
lT
60-
165
Near
-Far
0
S81 W82S82 W83S83 W84S84 W85S85 W86S86 W87S87 W88
;>
S81 W82S82 W83S83 W84S84 W85S85 W86S86 W87S87 W88
TIME
1. Percentageof primaryrock space covered by the
FIG. 2. Percentage
ofprimary
rockspacecoveredbythe
conic morph of the acorn barnacle Chthama/usanisopoma bentmorphoftheacornbarnacleChthamalus
anisopomaas
as a functionof season, year, and distance from predator a function
ofseason,year,anddistancefrompredator
refugia
and symbolsare as in Fig. 1
refugia(means ? 1 SE). Data are means of 100-cm2 quadrats (means? 1 SE). Abbreviations
nearcrevices,combinedwith
withinsites averaged over eightsites in the upper midinter- legend.Note the seasonality
of thestatistical
tidal in the northernGulf of California.Summer samples are largedifferences
amongyears.A summary
indicatedby S, and wintersamples are indicated by W (e.g., analysisofthesedata is givenin Table 2.
TIME
FIG.
S81 = summer 198 1). Dashed lines representsamples taken
fromquadrats near to (within20 cm of) rock crevices used
as refugiaby thepredatorsnailAcanthinaangelica; solid lines
representsamples taken far (>40 cm) from such crevices.
Note the strongseasonalitynear crevices,which reflectsthe
aestivation of the predator and summer settlementof the
barnacle. A summaryof the statisticalanalysis of these data
is given in Table 1.
1 and 2). The temporalmain effects(year and season)
and the year x season interactionaccounted for <4%
of the variation,as was observed forthe conic formof
the barnacle. Hence, forboth morphsof the barnacle,
1. Results of repeated-measuresANOVA forpercentageof cover by the conic morph of the barnacle Chthamnalus
anisopoma at eightsites in the intertidalin the northernGulf of California. Data were arcsine transformedprior to the
analysis. Uni P and Multi P referto univariateand multivariateprobabilityvalues, respectively.Pillai's tracevalues were
used forthe multivariateprobabilityestimates,and were calculated using the generallinear models program(GLM) from
SAS (SAS 1982).
TABLE
Source of variation
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
df
MS
Distance (Dist)
Site
Dist x Site
Subj. withingroups
Between subjects
1
13.567
7
0.723
7
0.307
16
0.048
Year (Y)
Y x Dist
Y x Site
Y x Dist x Site
Y x Subj. withingroups
Season (S)
S x Dist
S x Site
S x Dist x Site
S x Subj. withingroups
Year x Season (Y x S)
Y x S x Dist
Y x S x Site
Y x S x Dist x Site
Y x S x Subj. withingroups
6
6
42
42
96
1
1
7
7
16
6
6
42
42
96
Withinsubjects
0.218
0.306
0.083
0.044
0.012
1.441
2.274
0.124
0.084
0.019
0.123
0.058
0.034
0.026
0.010
Uni P
Multi P
<.00 1
<.001
.001
variance
accounted
for
24.2
4.9
3.8
<.001
<.001
<.001
<.001
<.001
.012
<.001
.001
1.3
3.3
3.6
3.3
<.001
.013
.002
.007
<.001
.013
.001
.007
2.6
9.6
1.5
2.1
<.001
.057
<.001
<.001
.004
.204
<.001
.003
...
1.4
0.8
2.5
3.3
...
166
2. Results of repeated-measuresANOVA for percentageof cover by the bent morph of the barnacle Chthamalus
anisopoma, at eightsites in the intertidalin the northernGulf of California. Data were arcsine transformedpriorto the
analysis. Abbreviationsare as definedin Table 1.
TABLE
df
Source
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
Distance (Dist)
Site
Dist x Site
Subj. withingroups
1
7
7
16
Between subjects
2.223
0.045
0.037
0.012
Year (Y)
Y x Dist
Y x Site
T x Dist x Site
T x Subj. withingroups
Season (S)
S x Dist
S x Site
S x Dist x Site
Y x S x Dist
Y x S x Site
Y x S x Dist x Site
6
6
42
42
96
1
1
7
7
16
6
6
42
42
96
Withinsubjects
0.122
0.089
0.011
0.013
0.003
0.175
0.127
0.011
0.011
0.002
0.013
0.009
0.007
0.008
0.003
the proximityof predatorrefugiawas more influential
than seasonal or annual differences.
by temporal
Mussels,bycontrast,weremoreaffected
effectsthanwereeithermorphof the barnacle (Fig. 3).
Distance (13.6%), year ( 11.7%), season (10.66%),and
theyear x season interaction(9.5%) all explainedabout
the same proportionof the total variation (Table 3).
Site effects(< 1%) and the distance x site interaction
--
0
30-
Multi P
% variance
accounted for
20.8
5.1
1.9
<.001
.015
.031
<.001
<.001
<.001
<.001
<.001
.004
<.001
<.001
4.0
5.1
2.1
5.3
<.001
.011
.007
.007
<.001
.011
.007
.005
1.6
2.2
0.7
1.4
<.001
.303
<.001
<.001
.002
.458
.002
.004
0.7
0.1
2.1
5.3
...
...
...
(2%) were the least influentialfactors.Hence, relative
to barnacles,temporaleffectsseemed to be more importantin controllingthe distributionand abundance
of mussels,but therewas nonethelessa strongindirect
effectarisingfromthe presenceof predatorrefugia.
accounted formostofthevariation
Temporal effects
in limpetdensities(Fig. 4). Year (10.4%) and the year
x season interaction(13.9%) werethe most influential
factors,followedby site (6.8%) and the year x season
Mussels
40 -
LU
Uni P
MS
a:
Limpets
10
--Near
Far
--
--Near
Far
LU
z
<20-
LU
Z
10
-6
I
uJo
S81 W82S82 W83S83 W84S84 W85S85 W86S86 W87S87 W88
TIME
rockspacecoveredbymusofprimary
FIG. 3. Percentage
sels (Brachidontessemilaevis) as a functionof season, year,
(means? 1 SE). Abbrerefugia
and distancefrompredator
viationsand symbolsare as describedin Fig. 1. Note the
combinedwithlargediffarfromcrevices,
seasonality
strong
analysis
ofthestatistical
ferences
amongyears.A summary
ofthesedata is givenin Table 3.
I~~~~TM
0
S81 W82S82 W83S83 W84584 W85S85 W86S8'6 W87S87 W'88
TIME
FIG. 4.
Number of limpets (Collisella acutapex and C.
of season,year,and distancefrom
as a function
strongiana)
and symbols
(means? 1 SE). Abbreviations
refugia
predator
analysis
ofthestatistical
inFig.1.A summary
areas described
ofthesedata is givenin Table 4.
January1993
INTERTIDAL
COMMUNITY
STRUCTURE
167
3. Results of repeated-measuresANOVA forpercentageof cover by mussels (Brachidontessemilaevis). Data were
arcsine transformedpriorto the analysis. Abbreviationsare as definedin Table 1.
TABLE
Source
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
df
MS
Distance (Dist)
Site
Dist x Site
Subj. withingroups
1
7
7
16
Between subjects
2.464
0.040
0.063
0.017
Year (Y)
Y x Dist
Y x Site
Y x Dist x Site
Season (S)
S x Dist
S x Site
S x Dist x Site
Y x S x Dist
Y x S x Site
Y x S x Dist x Site
6
6
42
42
96
1
1
7
7
16
6
6
42
42
96
Withinsubjects
0.598
0.124
0.012
0.013
0.005
1.888
0.384
0.015
0.005
0.004
0.254
0.022
0.008
0.011
0.005
Uni P
Multi P
% variance
accounted for
13.6
0.5
2.1
<.001
.072
.013
<.001
<.001
<.001
<.001
<.001
.063
<.001
.076
11.7
4.4
1.1
2.5
<.001
<.001
<.001
.357
<.001
<.001
.010
.357
10.6
4.3
0.5
0.1
<.001
.099
.009
<.001
<.001
.468
.012
.019
9.5
0.9
0.9
3.8
...
...
x site interaction(6.2%) (Table 4). Distance (0%) and main algal species in the vicinityof our studysite. The
the season x distance interaction(0%) were the least greenalga U/vawas most sensitiveto season (26.0%)
importantfactors,which is directlyopposite to the and to the season x site interaction(15.9%) (Table 5);
resultobserved for the conic morph of Chthamalus. the regularseasonality exhibited by U/va is evident
Hence, compared to barnacles,limpetsappear to have from Fig. 5. The least influentialfactorswere those
been controlledmore by differences
among years and involvingthe distance effect:distance (0%), season x
less by differences
associated withthe crevice effect. distance(0%), year x distance(1.2%), and year x seaMarked differenceswere evident between the two son x distance (1.9%). Hence Ulva is highly sea4. Results of repeated-measuresANOVA for number of limpets(Collisella). Data were log (base 10) transformed
priorto the analysis. Abbreviationsare as definedin Table 1.
TABLE
Source
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
df
MS
Distance (Dist)
Site
Dist x Site
Subj. withingroups
Between subjects
1
3.101
7
8.678
7
3.208
16
0.405
Year (Y)
Y x Dist
Y x Site
Y x Dist x Site
Season (S)
S x Dist
S x Site
S x Dist x Site
Year x Season (Yx S)
Y x S x Dist
Y x S x Site
Y x S x Dist x Site
6
6
42
42
96
1
1
7
7
16
6
6
42
42
96
Withinsubjects
14.561
2.018
0.704
0.461
0.230
12.789
0.184
0.589
0.361
0.271
9.832
0.732
0.766
0.416
0.228
Uni P
Multi P
variance
accounted
for
0.0
6.8
4.6
.358
<.001
<.001
<.001
.002
<.001
.003
<.001
.259
.038
.025
...
10.4
2.2
2.7
2.7
<.001
.498
.095
.298
<.001
.498
.095
.297
...
2.6
0.0
0.5
0.3
...
<.001
.131
<.001
.008
..
<.001
.306
.004
.163
...
13.9
0.9
6.2
4.3
...
168
Ulva
40 -
Near
Far
0
LU030
o
< 20 _-1
Ecology, Vol. 74, No. 1
brownalga Ralfsia is less seasonal, and appeared to be
more affectedby indirecteffectsarisingfromthe presence of predatorrefugia.Finally,note that a large increase in Ralfsia was observed betweensummer 1981
and thefollowingwinter(from14 to 50% cover). Raifsia thengraduallydecreased fromwinter1984 to winter 1988 (Fig. 6).
A
LU
DISCUSSION
Short-term
fieldexperimentsare irreplaceableforthe
determinationof direct and indirecteffectsresulting
20
fromthe interactionsamong coexistingspecies. The
enthusiasmforthese kinds of studies and the recent
focus on experimentalrigorhave led to a greatlyenhanced understandingof marine,freshwater,
and terS81 W82S82 W83S83 W84Ss4 W8'5Sss W8'6S86 W87S87 W~8 restrialcommunities,
and may be regardedas one of
TIME
the major successes of modern ecology (e.g., Dayton
rockspacecoveredbythe 1975, Peterson 1982, Morin 1983, McAuliffe 1984,
ofprimary
FIG. 5. Percentage
ofseason,year,anddistance Brown et al. 1986). These studies, nonetheless,gengreenalga Olva sp. as a function
frompredatorrefugia(means ? I SE). Abbreviationsand sym- erally accord only a "snapshot" in time. Long-term
bols are as describedin Fig. 1. Note the strongseasonalityat observationsin concertwith short-term
experimental
both near and farsites. A summaryof the statisticalanalysis
manipulations
provide
a
powerful
way
of
placing the
of these data is given in Table 5.
results of short-termexperimentsin context (Fairweather 1988b, Brown and Heske 1990), and may allow foran understandingof the dynamics as well as
sonal, and minimally affectedby indirect effectsarising
themechanismsunderlying
from the presence of predator refugia.
communitystructure.
They
may also allow fora determinationof the relativeefThe brown encrusting alga Raffisia by contrast, was
fectsof spatial and temporal sources of variation,as
much more sensitive to distance from refuges (21.8%)
and site (8.8%) (Table 6). The least influential factors well as the importanceof space-timeinteractions.The
purposeofthepresentstudywas to integratetheresults
involved season: season x distance (0%), year x season x distance (0%), and season x distance x site of an 8-yrsurveywiththe resultsof several short-term
(1.5%), although there was a strong year x season in- experimentsconducted on intertidal shores in the
teraction (8 .3%). Nonetheless, relative to Olva, the northernGulf of California,and to determinethe rel5. Resultsofrepeated-measuresANOVA forpercentageofcover by thegreenalga U/va.Data werearcsinetransformed
priorto the analysis. Abbreviationsare as definedin Table 1.
TABLE
Source
df
MS
Uni P
Multi P
% variance
accounted for
1.
2.
3.
4.
Distance (Dist)
Site
Dist x Site
Subj. withingroups
1
7
7
16
Between subjects
0.037
0.444
0.118
0.011
.591
<.001
<.001
5.
6.
7.
8.
9.
Year (Y)
Y x Dist
Y x Site
Y x Dist x Site
6
6
42
42
96
Withinsubjects
0.168
0.064
0.031
0.019
0.009
<.001
.010
<.001
<.001
<.001
.183
.002
.015
2.0
1.2
2.3
2.0
<.00 1
.628
<.001
<.001
<.001
<0.001
0.628
<0.001
<0.001
26.0
0.0
15.9
3.9
<.001
.012
<.001
<.001
<.001
.275
<.001
.002
2.7
1.9
4.5
4.1
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
Season (S)
S x Dist
S x Site
S x Dist x Site
Year x Season(Y x S)
Y x S x Dist
Y x S x Site
Y x S x Dist x Site
1
1
7
7
16
6
6
42
42
96
7.104
0.020
0.554
0.076
0.010
0.115
0.056
0.030
0.018
0.008
..
..
..
0.0
6.3
3.1
...
...
January1993
INTERTIDAL
COMMUNITY
STRUCTURE
169
activeimportanceof space, time, and space-time in60
Ralfsia
teractionsformembersof this community.
~ ~ ~ ~ ~ ~~
~Near
The resultsshowed strongdifferences
among species
-Far
in theirsensitivitiesto spatial and temporalvariation. E 50
!
For example,most of the variationwe observed in the
/1
o40
percentageof cover by the conic formof the barnacle
A
was due to distance from refugesfor the predatory
snail, Acanthina. This distance or "crevice" effectis < o30
explicable in terms of previous experimentalresults, z
which showed thatbarnacle densitiesare significantly
depressedbyAcanthina(Lively 1986a, Dungan 1987).
O 20
These snails forageout fromcrevices duringperiods
of tidal exposure,and therebycreate areas of intense
10
predationnearcrevices(Lively 1986a). Similarcrevice
effectshave been reportedby Menge (1 978a) forNew
S81 W82S82 W83S83 W84S84 W85S85 W86S86 W87S87 W88
England, Garrity and Levings (1981) for Panama,
TIME
Sutherlandand Ortega(1986) forCosta Rica, and Moran (1985) and Fairweather(1988a) foreasternAusrockspacecoveredbythe
ofprimary
FIG. 6. Percentage
ofseason,year,
algaRalfsiasp.as a function
tralia.The resultsof the presentstudyindicatefurther brownencrusting
(means? 1 SE). Abbrerefugia
thatthe creviceeffectis stable over relativelylong pe- and distancefrompredator
viationsand symbolsare as describedin Fig. 1. Note the
riods at the same sites in the northernGulf of Cali- strong
analA summary
ofthestatistical
siteandyeareffects.
fornia. In addition, distance from crevices also ex- ysisofthesedata is givenin Table 6.
plained mostofthevariationin thepercentageofcover
by the bent formof the barnacle. However, whereas
theconic morphwas more common farfromcrevices, season x distanceinteraction(Table 1). In otherwords,
the bent morph was most common near to crevices therewas a strongseasonal effectnear to, but not far
(compare Figs. 1 and 2). This result stems fromthe from,crevices (Fig. 1). This resultmay be explained
factthatthebentphenotypeis inducedby thepresence as follows.Barnacle settlementis maximal duringthe
of Acanthina,and thattheyare more resistantto spe- summer (Malusa 1986, Raimondi 1990), and occurs
cialized attackby this predator(Lively 1986a).
during a period of aestivation by Acanthina (Lively
A relativelylarge portion of the variation for the 1986a, Dungan 1987); because the cue inducingthe
conic morphof the barnacle was also explained by the bent formof the barnacle (i.e., Acanthina) is absent,
J
6. Results of repeated-measuresANOVA for percentageof cover by the brown alga Ralfsia. Data were arcsine
transformedpriorto the analysis. Abbreviationsare as definedin Table 1.
TABLE
Source
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
df
MS
Distance (Dist)
Site
Dist x Site
Subj. withingroups
Between subjects
1
11.304
7
1.137
7
0.363
16
0.030
Year (Y)
Y x Dist
Y x Site
Y x Dist x Site
Subj. withingroups
Season (S)
S x Dist
S x Site
S x Dist x Site
Subj. withingroups
Y x S x Dist
Y x S x Site
Y x S x Dist x Site
6
6
42
42
96
1
1
7
7
16
6
6
42
42
96
Withinsubjects
0.658
0.281
0.126
0.048
0.019
0.229
0.047
0.227
0.057
0.010
0.604
0.012
0.036
0.031
0.010
Uni P
Multi P
<.001
<.001
<.001
variance
accounted
for
21.8
8.8
5.3
<.001
<.001
<.001
<.001
<.001
.052
.001
.019
<.001
.397
<.001
.002
<.001
.397
<.001
.002
4.5
3.3
6.0
3.2
0.4
0.0
3.5
1.5
<.001
.876
<.001
<.001
<.001
.287
.001
.002
8.3
0.0
2.9
4.7
170
mostofthesesummersettlerswilldevelop as thefaster- of settlementvariation among years, short-termexgrowingconic form(Lively 1986a). Followingrenewed perimentscan be misleading.In thecase ofthemusselactivityby Acanthina in the autumn, many of these barnacleinteraction,theaveragemagnitudeofthenegrecruits are eaten near crevices, producing a pro- ative effectof mussels on barnacles may have been
nounced seasonal effectfor the conic form in these underestimated.Similarly,the average positive effect
areas; theeffectis less extremefarfromcreviceswhere of barnacles on mussels may have also been underespredationis low (Fig. 1), which resultsin a highlysig- timated.In 1981, whichwas one of thebetteryearsfor
mussel recruitment(Fig. 3), Dungan (1986) found a
nificantseason x distance interaction(Table 1).
As an aside, it is worthnotingthat the absence of strongpositive effectof barnacles on mussels in a barAcanthinaduringpeak barnacle settlementmakes the nacle-removalexperiment.
Limpets, like barnacles and mussels, were variable
inducingcue forthebentmorphpoorlycorrelatedwith
the risk of futurepredationnear crevices. In general, in both space and time(strongsite,year x season, and
poor cues will select for canalized over conditional year x season x site effects),but showed proportionstrategies(Lloyd 1984), but it may be importantto atelygreaterannual effectsthan eitherof these species
separatethe cues foreach of the separate patches and (Table 4). Unlike barnaclesand mussels,however,the
which at firstseems
to considerthefrequenciesofthepatches(Lively 1986c). crevice effectwas not significant,
While the cue forthe high-predationpatch (the pres- to run counterto expectationsbased on experimental
ence of Acanthina) seems poorly correlatedwith pre- studies in the area (Dungan 1986, 1987). Dungan
dation risk in the presentstudy,the cue forthe low- showed in manipulativeexperimentsthatlimpetdenpredationpatch (the absence of Acanthina) seems to sities were negativelyaffectedby barnacles through
be highlycorrelated,as the bent morph is extremely competitionfor primaryrock space, and that Acanrare far fromcrevices (Fig. 2). In other words, some thina and limpets are indirectmutualists(Acanthina
barnacles seem to be making the "wrong" choice in removes barnacles, which aids limpets, and limpets
the near-to-crevicepatch,but most barnacles seem to removealgae, whichfacilitatesbarnaclesettlementand
be makingthe "right" choice in the far-from-crevicetherebyaids Acanthina). The positive effectof Acanthina on limpetsshould have been manifestedin the
patch.
To summarizetheresultsforbarnacles,distancefrom presentstudyas a significantcrevice effect(i.e., more
creviceswas the most influentialmain effectforboth limpets near to crevices where Acanthina dispropormorphs. The season x distance interactionwas also tionatelyremove barnacles). In contrast,therewas no
importantfor the conic form.Neither morph of the obvious relationshipbetweenlimpetdensityand barbarnacle was stronglyaffectedby the temporal main nacle cover (compare Figs. 1 and 4), and the crevice
effects,year and season, or by the year x season in- effectwas not significant(Table 4). There were,howteraction,althoughthese effectswere statisticallysig- ever, highlysignificantsite effectsand a strongsite x
nificant.Hence, we do not mean to suggestthat tem- distance interaction(Table 4). This latterresult sugporal differencesin barnacle settlementdo not exist. gests that the occurrenceand strengthof the indirect
The results,however,do suggestthat adult densityat mutualismbetween limpets and Acanthina is simply
our siteswas controlledmore by competitionand pre- site dependent.In otherwords,sites withfewlimpets
while siteswherelimpets
dation than by temporal variation in larval recruit- showed weak creviceeffects,
werecommon showed strongcreviceeffects,
givingthe
ment.
In contrastto barnacles,theabundance ofadult mus- site x distance interaction.This particularset of findamong years in ings also demonstrateshow controlledmanipulative
sels was more sensitiveto differences
recruitment.In good years,when mussels did recruit, experiments,by ensuringthe presence or absence of
they tended to do so in the summer (Fig. 3). This species in factorial combinations, elucidate mechamost likelyaccounts forthe nisms and determinethe possible, while longerterm
seasonalityin recruitment
highlysignificantseason and season x year interac- studies help to determinethe actual.
The greenalga, UOva,was the most seasonal of the
tions we observed. Distance (from refuges)was also
presumablydue to the tendencyfor investigatedspecies. Over the course of the study it
highlysignificant,
mussels to settleon barnacles (Dungan 1986, Lively always was more abundant in the winterthan in sumand Raimondi 1987) and the greaterconcentrationof mer,whenit usuallydisappearedfromthecommunity.
This patternwas true for sites both near to and far
barnacles away fromcrevices.
One ramificationof the large annual variation in fromcrevices.Two explanationscould account forthis
musselsis theimplicationforexperimentalstudies.For pattern:(1) the species is unable to survivethe heat or
example, Lively and Raimondi (1987) found a mar- desiccation associated with summertimetidal expoginally significantnegative effectof mussels on bar- sure, or (2) it does not recruitin the summer.Expernacles in a mussel-removalexperimentconducted in imentalstudies supportthe second of the two hypoth1982. We now know that 1982 was a relativelypoor eses (but do not rule out a combination).As part of a
yearformussel recruitment(Fig. 3). The implications factorialexperimentconducted duringthe summerof
are clear:forspecies likemusselsshowinga largedegree 1982, some sites were kept damp duringdaytimelow
January1993
INTERTIDAL
COMMUNITY
tidesto examine theeffectsof desiccationon the entire
community(Lively and Raimondi 1987). Contraryto
expectation,therewas no effectof this treatmenton
the percentageof cover by Ulva, or any otherspecies.
Specifically,the cover of Ulva was never > 1%, suggestingthatit does not recruitduringthe summer,and
that the seasonality evident in Fig. 5 of the present
study is due to the timingof settlementratherthan
post-settlement
mortality.
The brown alga Ralfsia, by contrast,showed large
spatial effects,but only minor seasonality, and this
seasonalitywas only observed farfromcrevices (Fig.
6). In addition,Ralfsia was consistentlymorecommon
near crevices,wherebarnacle cover is low due to predation by Acanthina. This result is consistentwith
Dungan's (1 987) findingthatAcanthinahas an indirect
on Ralfsiaby removingbarnacles,which
positiveeffect
preemptspace for settlementand growthby Ralfsia.
The second major trendin the cover by Ralfsia was a
gradual decline in the near-to-crevicesites afterthe
winterof 1984 (from - 50% to - 10%). This trendis
harderto explain usingexperimentally
confirmedpostsettlementmechanisms. Barnacle cover did not increase significantly
duringthe decline of Ra/fsia,and
limpetdensitiesfollowedratherthan precededthe decline in Ralfsia. The Ralfsia decline thereforeremains
unexplained.
Taken overall, the resultsshowed highlysignificant
effectsof both space and time forall membersof this
relativelysimple rocky intertidalcommunityin the
northernGulf of California. Spatial effects,resulting
fromdistancefrompredatorrefuges,were much more
influentialthan temporaleffectsforbarnacles and the
brown alga Ralisia, suggestingthat these two species
are controlledmore by the directand indirecteffects
of predation,respectively,than by seasonal or annual
in recruitment.
differences
For mussels,seasonalityand
unpredictablerecruitmentamong years appear to be
of about the same order of importanceas the occurrence of predator refugia,and for limpets year and
season are of much greaterimportthan such refugia.
For these two species, then,recruitmentphenomena
would appear to be moreinfluentialthanforbarnacles.
These latterresultssuggestthatshort-term
experimental studies,althoughessentialto determinequalitative
effects(both directand indirect),can be misleadingif
taken to be indicative of average quantitativeeffects
over time.
There were also highlysignificantseason x space
interactionsforall sessile membersof the community.
These interactionsare probablybest understoodas resultingfromthe seasonal amplificationofexistingspatial differences
due to seasonal settlementof the sessile
members of the communityand aestivation by the
as well
predator.Highlysignificant
year x space effects
as year x season x space effectswere also observed
formost species. These complex interactionsmay be
understoodas an amplificationof seasonal and spatial
STRUCTURE
171
effects due to the largely unpredictable differences
among years. The existence of such strong space-time
interactions in this relatively simple and stable community demonstrates the value of long-term observations in association with short-term experimental
manipulations.
ACKNOWLEDGMENTS
We thankMelissa Hart and Katrina Mangin forhelp in the
field,and MargaritaTurk and Rick Boyer (of the Centerfor
the StudyforDeserts and Oceans) forlogisticalsupportand
friendship.The manuscriptbenefittedfromcritiquesby Joe
Connell,Paul Dayton,Mike Dungan, PeterFairweather,Mick
Keough, Andy Peters,PeterPetraitis,and Tony Underwood.
Gracias tambien por nuestro amigos en Puerto Penasco y
Bahia Cholla, Sonora, Mexico. Fundingduringtheeightyears
of this project was gratefullyreceived fromSigma Xi, The
Lerner-GrayFund forMarine Research,Regentsof the Universityof California,the Graduate College of the University
of Arizona, and the NSF (Pre-doctoral Fellowship to Raimondi). The finalreportwas compiled duringa period supportedby theNSF (BSR-9008848 to Livelyand BSR-9010556
to Delph), NIH (BRSG grantRR 7031-25 to Lively),and by
a Universityof Melbourne Research Fellowshipand an AustralianResearch council grantto Raimondi.
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Intertidal Community Structure: Space

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