Download CONSUMERS - Lubchenco/Menge Lab

J. Exp. Mar. Biof. &of., 1986, Vol. 100, pp. 225-269
225
Elsevier
JEM 726
EXPERIME~AL
SEPARATION OF EFFECTS OF CONSUMERS ON
SESSILE PREY IN THE LOW ZONE OF A ROCKY SHORE IN THE BAY
OF PANAMA: DIRECT AND INDIRECT CONSEQUENCES OF FOOD WEB
COMPLEXITY
BRUCEA. MENGE’, JANE LUBCHENCO, LINDA R. ASHKENAS*
Department
ofZoology. Oregon State University, Cowallis. OR 97331, U.S.A.
and
FRED RAMSEY
Department of Statistics, Oregon State University, Corvallis, OR 97331, U.S.A.
(Received 20 September 1985; revision received 14 April 1986; accepted 25 April 1986)
Abstract: The effects of predation by a diverse assemblage of consumers on community structure of sessile
prey was evaluated in the low rocky intertidal zone at Taboguilla Island in the Bay of Panama. Four
mnctional groups of consumers were defined: (I) large fishes, (2) small fishes and crabs, (3) herbivorous
molluscs, and (4) predaceous gastropods. (1) and (2) included fast-moving consumers and (3) and (4)
included slow-moving consumers. Experimental treatments were: no consumers deleted (all groups
present), most combinations of deletions of single groups (i.e., one group absent, three present), pairs of
groups deleted (two absent, two present), trios of groups deleted (three absent, one present), and the entire
consumer assemblage deleted (all groups absent). Changes in abundance (percent cover) of crustose algae,
solitary sessile invertebrates, foliose algae, and colonial sessile invertebrates were quantified periodically
in 2-4 plots of each treatment from February 1977 to January 1980 after the initiation of the experiment
in January 1977.
Space on this shore is normally dominated by crustose algae; foliose algae, solitary sessile invertebrates,
and colonial sessile invertebrates are all rare. After deletion of all consumers, ephemeral green algae
increased from 0 to nearly 70% cover. Thereafter, a succession of spatial dominants occurred, with peak
abundances as follows: the foliose coralline alga Junia spp. by July 1977, the barnacle Balanus inexpectutus
by April 1978, and the rock oyster Chama echinata by January 1980. Although no longer occupying primary
rock space, Jania persisted as a dominant or co-dominant turf species (with the brown alga Giffordia
mitchelliae and/or the hydrozoan Abietinariu sp.) by colonizing shells of sessile animals as they became
abundant instead of the rock surface.
Multivariate analysis variance (MANOVA) indicated that the effect of each group was as follows.
Molluscan herbivores grazed foliose algae down to the crier-resistant,
but com~titively inferior algal
crusts, altered the relative abundances of the crusts, and inhibited recruitment of sessile invertebrates.
Predaceous gastropods reduced the abundance of sohtary sessile animals. SmaJl fishes and crabs, and large
fishes reduced the cover of solitary and colonial sessile animals and foliose algae, although they were
incapable of grazing the foliose algae down to the rock surface. Many of the effects of each consumer group
on prey groups or species were indirect; some effects were positive and some were negative. The variety
of these indirect effects was due to both consumer-prey interactions among the consumers, and competitive
or commensalistic interactions among the sessile prey. Comparison of the sum of the effects of each of the
’ To whom reprint requests should be addressed.
* Present address: Department of Fisheries and Wildlife, Oregon State University, Corvalhs, OR 9733 1,
U.S.A.
226
BRUCEA. MENGEH-AL.
single consumer groups (i.e., the sum of the effect observed in treatments
with one group absent, three
present) with the total effects of all consumers (i.e., the effect observed in the treatment with all groups
absent) indicates that a “keystone” consumer was not present in this community. Rather, the impacts of
the consumer groups were similar but, due to dietary overlap and compensatory
changes among the
consumers, not readily detected in deletions of single consumer groups. The normally observed dominance
of space by crustose algae is thus maintained by persistent, intense predation by a diverse assemblage of
consumers
on potentially dominant sessile animals and foliose algae. The large difference in structure
between this and temperate intertidal communities seems due to differences in degree, not kind of ecological
processes which produce the structure.
Key words: community
structure
and organization;
competition;
herbivorous
mollusc; indirect effect; keystone consumer;
Panama;
intertidal; tropics
consumer;
crab; fish; gastropod;
predation;
pseudoreplication;
rocky
Investigations of community dynamics have traditionally followed one of two
avenues. These are (1) study of the influence of biotic interactions on the structure of
the community (here termed “community regulation”), and (2) study of energy flow and
nutrient cycling of the community (here termed “community or ecosystem function”).
Studies of community regulation typically focus on the roles of species, and an ultimate
goal is to understand how species interact with each other and the physical en~onment
to produce patterns of community structure (i.e., distribution, relative abundances,
species richness, size structure). Studies of ecosystem function typically focus on the
roles of entire trophic levels in the flow of energy and nutrients through food chains,
and an ultimate goal is to understand patterns and efficiencies of transfer between levels.
Both approaches have limitations on the insight they provide into community
dynamics (Paine, 1980; Dayton, 1984). Most importantly, experimental, communitylevel (as used here, co~unity
= all macroscopic species at all trophic levels in a
particular habitat) studies which focus on the roles of individual species rapidly become
impractical as diversity increases. Only in very simple communities can we realistically
investigate nearly all of the important species and thereby understand the regulation of
the entire community (e.g., Menge, 1976; Lubchenco & Menge, 1978; Lubchenco, 1980,
1983, 1986). Since most communities are complex, community studies usually evaluate
the regulation of subunits (e.g., guilds, subwebs; Root, 1973) rather than entire
communities, and our present underst~d~g of community regulation is based mosdy
on studies which have ignored portions of the community. In contrast, studies
concerning the function of ecosystems sacrifice the insight obtained from species manipulations for the knowledge of rates of transfer among components of the entire
community, and thus complexity and diversity are typically not major foci of study.
Instead, species are lumped into trophic groupings with “functional groups” (Cummins,
1974) typically representing the finest level of subdivision investigated.
If complex co~~ities
are so d~cult to study, why not simply ignore them in favor
of rigorous study of entire simple co~~ities?
First, communities sufficiently simple
ORGANIZATIONOFATROPICALINTERTIDALCOMMUNI~
221
to permit manipulations with no lumping seem to be the exception rather than the rule.
Second, at least some aspects of the organization of complex communities are likely to
be different from those of simple communities. For example, dete~ination
of the
regulation of complex communities is necessary if we are to determine how the relative
importance of different structuring agents (e.g., predation, competition, mutualism,
physical factors) varies in time and space (Connell, 1975; 1983; Menge & Sutherland,
1976; Schoener, 1983; Lubchenco, 1986; Sih etal., 1985).
This paper presents an effort to investigate the regulation of an entire complex
community in a tropical rocky intertidal habitat. The study drew on features used in both
approaches to study community dynamics described above. In so doing, we chose to
grapple with problems of experimental design, complexity, analysis, and interpretation
heretofore avoided in most investigations of community regulation. Our goals are: (1)
to report (in the main body of the text) the results of experiments done to detente
the
organization of an entire complex community, which is, to our knowledge, the first of
its kind, and (2) to evaluate (mostly in the Appendix) the pros and cons of the hybrid
approach employed in this investigation. Some aspects of the study were less than ideal:
(1)the experimental design included pseudoreplication (sensu Hurlburt, 1984), (2) the
effects of individual consumer species were blurred by the necessity of lumping species
into trop~c~ly and/or pra~ati~~ly defined groups, and (3) the separate effects of one
of the consumer groups (small fishes & crabs) could not be experimentally isolated (i.e.,
the design was non-orthogonal). However, these or similar flaws appear unavoidable
in such studies since biological constraints and pragmatic limitations in funding,
techniques, and personnel can greatly compromise the ideal experimental design and
execution. Despite these problems, the experimental results provide ecologically
important insights into the regulation of a complex community.
STUDY SITE
The main study site has been described elsewhere (Menge & Lu~hen~o, 1981;
Lubchenko et al., 1984). Briefly, studies were established along a 0.5 km stretch of the
southern shore of Taboguilla Island in the Gulf of Panama (15 km south of the Pacific
entrance of the Panama Canal; Fig. 1). Supplementary information on community
structure was taken at several other sites including Chitre Island, Tortola Island, and
Punta Bruja (Gulf of Panama), and Uva Island (Gulf of Chiriqui; Fig. 1). Tidal
amplitude is 7.2 m (Z 21 feet), and five zones occur on this basaltic rocky shore
( = splash, high, mid, low, very low; Lubchenco et al., 1984). The emphasis here is on
the low zone, which ranges from + 0.6 to + 2.4 m above MLW. The climate is tropical
(about 9”N latitude), with dry (mid December-April) and wet (May-mid December)
seasons.
228
BRUCE A. MENGE ETRL.
4
CARIBBEAN
PACIFIC
\
PERLAS
ARCHIPELAGO
5km
,
I
Fig. 1. MapshowingPanamastudy~eas:TA
= TaboguiIla,themain study site; supplement~obse~ations
were made at CH = Chitre Island (Perlas Archipelago), TT = Tortoia Island, and PB = Punta Bruja
(all in the Bay of Panama), and U = Uva Island (Gulf of Chiriqui); other islands labelled include:
TB = Taboga, UR = Urava, NA = Naos, PE = Perrico, CU = Culebra, and FL = Flamenco; PC =
Panama Canal.
COMMUNITY
STRUCTURE
Our previous reports about this community focused on the total impact of predation
on prey abundance (e.g., Menge & Lubchenco, 198 1; Lubchenco et al., 1984; Menge
etal., 1986) or quantitative variation in predator abundance (Menge et al., 1986).
Prelimin~y qu~itative differences among consumers were considered in some cases,
but onfy with respect to how they affected the differential use of refuges by prey species
(e.g., Menge & Lubchenco, 1981; Menge et al., 1983). The present paper focuses on
qualitative differences among the consumers in this community.
The structure of this system has been described in detail (Lubchenco et al., 1984).
Briefly, the shores of Ta~guilla Island (and all nei~bo~ng islands; authors’ pers. obs.)
appear barren, particularly in comparison to temperate rocky shores. Closer inspection
reveals that most space in the low (and mid) zone(s) is covered by algal crusts. Sessile
ORGANIZATION
OF A TROPICAL
INTERTIDAL
COMMUNITY
229
invertebrates and foliose algae, so abundant in most temperate regions, are scarce,
although most of the higher taxa of invertebrates typical of many temperate shores (e.g.,
barnacles, bivalves, gastropods, &tons, crabs, sea urchins, seastars) do occur in the
Bay of Panama. Fishes are abundant and forage extensively both on mobile and sessile
organisms throughout the rocky intertidal. Taxonomic authorities and references used
to identify the species in this community are given in Lubchenco et al. (1984).
COMPOSITION
OF CONSUMER
GROUPS
Compared to well-known temperate rocky intertidal communities, the food web at
Taboguilla is particularly complex (Lubchenco et al., 1984; Menge et al., 1986). Animal
(but not plant) species richness is high (> 100 species occur in the low zone) and trophic
links are numerous, occurring both between trophic levels and among species of similar
trophic status. Consumers include both slow-moving and fast-moving, benthic
invertebrates and fishes (Menge & Lubchenco, 198 l), with up to 29 species of four types
of predator, up to five species of two types of omnivore, and up to 13 species of six types
of herbivore (“type” = major taxonomic groups like crabs, neogastropods, sea urchins,
fishes, etc. ; see Lubchenco et al., 1984).
Since simultaneous determination of the separate and combined effects of each
species of consumer in this food web was deemed impossible, we focused on groups
of consumers which were species foraging in similar ways (“functional groups”)
(Cummins, 1974). Functional groups are distinct from “guilds” (= groups of species
using similar resources; Root, 1967) in that the focus is on the method of foraging, not
on the resource.
To evaluate the single and combined effects of four groups of consumers on the
abundance of sessile organisms, we removed one, most combinations of two and three,
and all four groups of consumers. We were particularly interested in identifying “strong”
interactions; i.e., those in which the consumer had a large effect on the abundance of
prey species (see Paine, 1980). Although interactions among the species within the
consumer groups could conceivably cancel out the predatory effects of some species,
observations of behavioral interactions, data on diets, and evidence from experiments
(Menge et al., 1986) suggest that such effects are probably minor.
The four consumer groups were: (1) slow-moving invertebrate predators (hereafter
termed “slow-moving predators” or, in some cases, abbreviated as “P”), which
consisted primarily of predaceous gastropods; (2) slow-moving invertebrate herbivores
(“slow-moving herbivores”, or “H”), primarily limpets; (3) small fishes and crabs
(“SF,,‘), blennies and fast-moving herbivorous crabs; and (4) large fishes (“LF”),
large-bodied, fast-moving fishes.
Although each group includes several species (Table I; see Lubchenco et al., 1984 for
a complete species list by group), much of the effect of each group on sessile organisms
is probably attributable to one or a few abundant species. This is because most
consumer species in each group are either rare or restricted to microhabitats. Herewith
is a brief description of the dominant species in each of the four functional groups.
BRUCE
230
A. MENGE
TABLE
ETAL.
I
Consumer species in each group: species occurring only in the low zone are included; abundance expressed
as absolute number per m2 and percent of total at minimum and maximum densities recorded (as reported
in Lubchenco er al., 1984); numerical dominants, defined as comprising > 20% of the total abundance of
the group are indicated with an asterisk.
7’ Total
Consumer
group
Composition
Slow-moving
predators (P)
Slow-moving
herbivores
(H)
Small fishes,
crabs (SFC)
Large fishes (LF)
Unmanipulated
Acanthina brevidentata*
(gastropod)
Thais melones*
(gastropod)
others (12 gastropods,
1 seastar)
Fissureha virescens*
(keyhole limpet)
F. longzzssa
(keyhole limpet)
Siphonaria maura*
(pulmonate limpet)
S. palmata*
(pulmonate limpet)
Acanthochitona
hirudiniformis (chiton)
Ceratozona angusla
(chiton)
Chiton stokesi
(chiton)
Echinometra vanbrunti
(sea urchin)
others (2 limpets, 1 pulmonate limpet, 2 chitons)
Ophiobliennius
sreindachner? (blenny)
Grapsus grapsus* (crab)
Herbivores
Eupomacentrus acapulcoensti (damselfish)*
Kyphosus elegans
(chub)
Scarus perrico
(parrotfish)
others (4 species, including 3 damselfishes, 1 surgeonfish)
Predators (P)
Bodianus diplotaenia
(wrasse)*
Holacanthus passer
(angelfish)*
others (6 species, including 2 puffers, 1
porcupine fish, 2 triggertishes, 1 angelfish
Pachygrapsus transversus
(grapsid crab)
Abundance”
(range of X no./m2)
Minimum
Maximum
0.7 to 6.5
19.4
43.3
2.4 to 6.4
66.7
42.7
0.5
13.9
14.0
73.8
25.0
5.6
to 2.1
12.4 to 24.0
0.8
to 5.4
4.8
0
to 31.0
0
32.4
0
to 23.5
0
24.5
0
to 1.5
4.8
1.6
0
to 2.5
0
2.6
0.8 to 2.0
4.8
2.1
1.1 to 3.2
6.6
3.3
0.9 to 2.7
5.4
2.8
0.011 to 0.024
47.8
15.6
0.012 to 0.13
52.3
84.4
0.29
87.9
71.9
0.013 to 0.046
3.9
9.4
0.006 to 0.035
1.8
7.2
0.008 to 0.026
2.4
5.3
to 0.35
0.008 to 0.017
0.003 to 0.005
0.002 to 0.008
2.4
(61.5% of P)
0.9
(23.1% of P)
0.6
(15.4% of P)
3.5
(56.7% of P)
1.0
(16.7% to P)
1.6
(26.7% of P)
2.3 to 4.8
a P and H values = ranges of four neighboring sites; small fishes, LF = ranges of three neighboring sites;
Grapsus = range of six neighboring sites; from Lubchenco et al., 1984 and authors’ unpublished
data.
ORGANIZATION
OF A TROPICAL
INTERTIDAL
COMMUNITY
231
The effect of the slow-mo~ng predators (Z 15 species) was probably due mostly to
Thais melones and Acunth~n~brevidentfftu, whelks with broad, overlapp~g diets (Menge
et al., 1986; Table I). The effect of slow-moving herbivores appeared largely due to four
of 13 species (the limpets Fissurella virescens, F. longifissa, Siphonaria maura, and S.
pafmata; Table I). Neither sea urchins (Echinometra vanbrunti) nor chitons were very
abundant in this zone (Table I). We assume that their effect was small or restricted to
holes (Menge et al., 1983). The effect of small fishes and crabs was probably attributable
primarily to the bienny Uphiob~ennius steindachneri and the crab Grapsus grapsus
(Table I)_ Grffpsus use their claws to scrape org~isms off the rock (Hawkins &
Hartnoll, 19X3), and to crush small solitary invertebrates. They cannot crop algae as
close to the rock as can the slow-moving grazers. Juveniles of larger species of fish,
although generally scarce, were also included in this group.
The effect of large fishes appeared due mostly to five species, including the territorial
damselfish Eupomacentrus acapulcoensis, the chub Kyphosus elegans, the parrottish
Scarus perrico, the wrasse ~odiffnus diplotaenia, and the porcupinefish Diodon hystrix.
All reside in the shallow subtidal zone and frequently forage in intertidal zone at high
tide. All use jaws to scrape food from the substratum or crush hard-shelled prey, have
broad diets, and, although they are often categorized as either herbivores or carnivores,
are actually omnivorous consumers of both mobile and sessile benthic animals and algae
(Wellington, 1982; Menge et al., 1986). Although numerically scarce, Diodon is potentially important due to its large size, large foraging ambit, and voracious consumption
of limpets, predaceous gastropods, barnacles, bivalves, and crabs (Table I in Menge
eta/., 1986; see also Palmer, 1979; Bertness eta/., 1981; Bertness, 1981; Garrity &
Levings, 1981; 1983; Gaines, 1983; 1985). Field observations indicate that the damselfish defend loosely-defined subtidal territories against all other fishes, but will move
well into the low zone to forage at high tide. The wrasses defend dens under boulders
or in deep crevices in the shallow subtidal. Aggression and chasing seemed infrequent
or absent when both these species and the other fishes foraged intertidally. Our observations suggest that the different fish species are quite similar to one another in their
effects. We thus assume that the large fishes constitute generalized, non-specific sources
of mortality for most sessile prey. This assumption is strengthened by field observations
of foraging, in which both individuals and schools of fishes would graze intensely in
“lawnmower” fashion over rock surfaces, and by the uniform spread of the characteristic
graze marks left by the fishes on the substratum. Although there is some species-specific
predation, the above-described generalized foraging is our justification for lumping these
fishes together into a single functional group.
One fish and one crab species were too small to be excluded in our fish and crab
exclosures. Both the herbivorous crab ~achygrupsus trffnsvers~ and the wrasse
Thalassoma lucasanum could pass through the 1 cm2 holes in the mesh of the cages, and
thus had access to both caged and uncaged plots. Since we never observed any
differential use of any treatment by either of these species, we assumed that their effects
were similar across treatments. Later experiments focusing on the specific effect of
232
BRUCE
A. MENGE ETAL.
P~c~~g~~~~s indicated that this crab reduces the abundance of filamentous algae and
colonial invertebrates such as bryozoans, ascidians, and hydrozoans in holes and
crevices (Menge et af., 1983).
METHODS
CONSUMER
MANIPULATIONS
Expe~ments were initiated between January and March 1977 (Menge & Lubchenco,
1981; see Table II for the experimental design and the Appendix for an evaluation of
constraints and potential artifacts), and run through August 1980. The experiments were
maintained at least once, and usually twice per month. Conservatively, z 11,410
person-hours were devoted to establishing and maintaining this particular study.
Briefly, biologically and physically similar semi-isolated sections of shoreline 200 to
600 m2 in area were selected as sites for manipulation of slow-moving consumers.
Although random placement of the plots along the shore would have produced *‘true”
replicates, removal of the mobile invertebrates from some plots would have influenced
their abundances in neighboring, non-removal plots, thereby introducing a diflicultto-control experimental artifact. Given the constraints in funding and personnel, this
biological constraint thus imposed a pseudoreplicated design (Hurlbert, 1984) on the
study. We removed slow-moving predators from Site 1, both slow-moving predators
and herbivores from Site 2, slow-moving herbivores from Site 4, and left all slowmoving consumers on Site 6.
At each site, large fishes, which forage with their bodies pe~endicul~ to the substratum (e.g., Menge & Lubchenco, 198 1; Choat & Kingett, 1982), were excluded with
stainless-steel mesh roofs ( = two-sided cages). The 5 to 10 cm gap between the roof and
rock was too narrow for large fishes to enter and forage on the protected surface. Both
large fishes and small fishes and crabs were excluded with cages (= complete, or
four-sided cages), each of which covered 0.25 m2. Blennies and crabs forage with their
bodies parallel to the surface, and field observations indicated that both fed without
hindr~ce under roofs but were too large to penetrate the 1 cm* mesh openings of the
cages. Comparison of these exclosures with marked, uncaged plots at each site
permitted us to evaluate the effects of the fast-moving consumers. Abundance (percent
cover and/or density) of sessile organisms in experimental plots were monitored from
March, 1977 to February, 1980 using standard methods (Menge & Lubchenco, 1981;
Lubchenco et al., 1984) at intervals ranging from 1 to 6 months (see the Appendix for
further details).
STATISTICAL
ANALYSIS
Analyses employed primarily multivariate analysis of variance (MANOVA), because
more than one variate (i.e., sessile species) changed in response to the consumer
manipulations (Morrison, 1976; Morin, 1983). Statistical interactions between con-
ORGANIZATION
OF A TROPICAL
INTERTIDAL
COMMUNITY
233
sumer groups were evaluated using a MANOVA model developed by F. Ramsey. We
generated linear regressions for changes in abundance of each sessile species (Y) vs. time
in months since initiation (X) for each plot. Before analysis, percent covers were
transformed with the arcsin transformation, and densities were transformed with the
TABLE II
Design of consumer
deletion
experiments:
number
presence and absence
of plots of each treatment
of the consumer groups.
Treatments
Slow-moving
consumer
manipulations
(removals)
Fast-moving
consumer
manipulations
(exclusions)
No manipulation
(Site 6)
No exclusion
Code
in parentheses;
Presence
or absence
Slowmoving
predators
(=P)
Slowmoving
herbivores
(=H)
of consumer
Large
fishes
(=LF)
+H+P+LF+SFC
+
+
+
+H+P-LF+SFC
+
+
_.
+H+P-LF-SFC
+
+
_
+H-P+LF+SFC
-
+
+
+H-P-LF+SFC
_
+
-
+H-P-LF-SFC
_
+
_
-H+P+LF+SFC
+
-t
-H+P-LF+SFC
+
_
-H+P-LF-SFC
+
-H-P+LF+SFC
_
+
-H-P-LF+SFC
_
+
-H-P-LF-SFC
-
(4)
2-sided cage
(2)
Complete
cage
(2)
Predator removal
(Site 1)
No exclusion
(4)
2-sided cage
(2)
Complete
cage
(2)
Herbivore removal
(Site 4)
No exclusion
(4)
2-sided cage
(2)
Complete
cage
(2)
Predator and
herbivore
removal
(Site 2)
No exclusion
(4)
2-sided
cage
(2)
Complete
(2)
cage
+ and
- ,
group
Small
fishes
large
crabs
(= SFC)
234
BRUCEAMENGEETAL.
square root transformation (Sokal & Rohlf, 198 1). Although we consider the experimental plots to be as spatially independent as allowed by biological constraints (see above
and Appendix), results are not independent with respect to time within plots. To achieve
greater independence of treatments and replicates, we removed time as a variable by
using regression coefftcients as indices of short-term and long-term change, and by
deriving an index of seasonal change for each species in each plot (Appendix).
The Y-intercept was presumed to index short-term change because it should reflect
whether or not rapid changes in abundance occurred in experimental vs. control plots
after initiation of the experiments. Similarly, the slope of the regression was presumed
to index long-term change because it should reflect more gradual divergences in
abundance over the 3-yr period of the experiment. Finally, we derived an index of
seasonal change (see Appendix) because fluctuations in abundance of sessile organisms
from the dry (December-April) to the wet (May-November)
seasons (Glynn &
Stewart, 1973) were possible (although virtually no biologically significant seasonal
changes in abundance occurred in unmanipulated plots; Lubchenco et al., 1984). The
MANOVAs were performed on each of these indices of change in abundance of sessile
organisms.
RESULTS
NATURAL
CHANGES
IN SPACE
OCCUPATION
Patterns of space use in unmanipulated plots in the low zone changed little, either
seasonally or annually (Lubchenco et al., 1984) although cover of Ralfia sp. gradually
increased (Fig. 2; Spearman rank correlation coefftcient = 0.65, P < 0.01). From 1977
to 1980, 80 to 95% of primary space was covered by algal crusts and the remaining
5 to 20% of the space was covered by dead coralline crust, the rock oyster Chama
echinata, shells of dead bivalves and barnacles, and traces of other sessile organisms
(Fig. 2). Ranked from most to least abundant, algal crusts included the brown Ralfsia
sp., the blue-green Schizothrix calcicofa, a multi-specific (but difftcult-to-identify-in-thefield) pavement of coralline crusts, and the red Hildenbrandia sp. (Fig. 2; Lubchenco
et al., 1984). Foliose algae were virtually absent throughout this period, except for trace
amounts located in holes and crevices (Menge & Lubchenco, 198 1; Menge et al., 1983 ;
1985). The most noticeable seasonal fluctuations at Taboguilla were small changes in
cover of coralline crust (increased during wet season and decreased during dry season)
and ephemeral green algae (increased during dry season and decreased during wet
season ; Lubchenco et al., 1984).
Together, these data and qualitative observations at Taboguilla beginning in January,
1973 and ending in February, 1983 suggest a pattern of near constancy in community
structure. Large seasonal and annual fluctuations like those usually observed in
temperate regions were not observed at Taboguilla. Observations at other sites in the
Bay of Panama suggest that near constancy in community structure is widespread in
this region.
ORGANIZATION
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235
OF A TROPICAL INTERTIDAL COMMUNITY
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19
XXI
80
C*
Fig. 2. Changes in patterns of abundance of quantitatively dominant occupants of primary space in control
plots (n = 4) in the low zone from February, 1977 to January, 1980: RALF. = Ru&u, SC = Schizothrix
calcicolu, cc = coralline crusts, HILD. = Hildenbrandiu (all algal crusts), and Ce = Chama echinata; the
remainder of the primary space was covered by other sessile organisms, bare space, dead shells of solitary
invertebrates, and dead coralline crust.
EXPERIMENTALLY-INDUCED
CHANGES IN COMMUNITY STRUCTURE
Community development in the absence of all consumers
In strong contrast to the persistent patterns of space utilization in unmanipulated
plots, community structure changed dramatically in the absence of consumers (Fig. 3).
Immediately after consumer deletion, foliose algae increased in abundance from 0 to
nearly 80% cover. This bloom was dominated by ephemeral greens for 3-4 months
(Fig. 3C). At this time (July 1977), cover of Jania spp. and, to a lesser extent, Gelidium
pusilIum and the hydrozoan Abie~nu~a sp. increased, and cover of crustose algae
decreased sharply (Fig. 3B, C). The decline of crustose algae (including the near
elimination of Schizothrix calcicola and Hildenbrandia sp.) was due primarily to overgrowth by Japria spp., whose holdfasts form a dense turf. Jania was the lone turf
dominant until November 1977, when successive blooms of Giffordia mitchelliae (peak
in November) and the filamentous greens (peak in March 1978) were temporarily
co-dominant foliose algae (Fig. 3C). Barnacles (primarily Balunus inexpectatus)
appeared in late 1977, and co-dominated primary space with crustose algae (still
dwindling in cover), Jania holdfasts, and, in late 1978, the rock oyster Chama echi~ata
(Fig. 3B). Thereafter, Chama increased, while Jania holdfasts, crustose algae, and
eventually, barnacles, decreased in abundance until January 1980, when the experiment
was terminated. Note that despite a decrease in the primary space its holdfasts covered,
BRUCE A. MENGE ETAL.
236
the upright portions of Junia remained abundant (compare Fig. 3B and C). This was
due to the increase in cover of sessile animals, which decreased the availability of
primary space, forcing Jade to shift to an epibiotic mode on the shells of barnacles and
oysters. Thus, in the absence of all consumers, crustose algae are slowly eliminated by
a sequence of increasingly effective competitors for space (Fig. 3).
A.
CRUSTS
Ralfsia
Schizo.
COR.
CR.
Hilden.
me,
C.
SECONDARY
SPACE
FII..
1977
1978
1979
GRNS.
=
Gelidium
=
GifforUia
=
Jsnia
=
Abiet.
=
1980
Fig. 3. Changes in abundance of qu~titatively dominant sessile animals and plants in the low zone after
deletion of all consumers, February, 1977 to January, 1980: Schizo. = Schizothrix, COR. CR. = coralline
crust, Hilden. = Hildenbrundiu, CRUSTS = summed cover of the four algal crusts shown in A., Jania
HF = primary space covered by the holdfasts of J&a, DD SES = primary space covered by shells of
dead barnacles and bivalves, FKL. GRNS. = filamentous greens, Abiet. = Abietinariu; other names are
self-evident.
ORGANIZATION
OF A TROPICAL
INTERTIDAL
COMMUNITY
231
Comparison among treatments
Although initial patterns of space occupancy among the 12 treatments were similar
(Appendix), final patterns varied (Fig. 4). For example, algal crusts still covered > 70%
of the surface in all treatments from which single groups of consumers had been deleted,
and covered 2 50% of the surface in all but three of the rest of the treatments (Fig. 4).
-++--++--+:::+-+LF +
+
+
SFC+++++++--+=IN rem. 0
I I
-++---
_+_+_-
122223334
Fig. 4. Comparison
of final community structure (mean percent cover of prey species or groups) in each
experimental treatment (experimental
code and number of consumer groups removed is listed below each
bar): codes in boxes are listed in the same order in which they are given on the histograms;
abbreviations
are as given in previous figures, except: PERENN. = perennial foliose algae, EPHEM. = ephemeral foliose
algae, dd. sol. ses. = remains of dead solitary sessile animals (e.g., barnacle tests, oyster shells), dd.
crusts = bleached
and presumably
dead encrusting
coralline
algae, other biv. = other bivalves, or.
sponge = unidentified encrusting orange sponge, Schizo. = Schizorhrix culcicola.
Chama, which covered l-2% of the surface in unmanipulated plots, covered 2 10% of
the surface in four treatments, most strikingly in total deletions, where it covered z 50%
of the surface. Solitary sessile animals such as barnacles and bivalves tended to cover
more space in nearly all consumer deletion treatments, as did total abundance of species
of ephemeral and perennial algae and arborescent colonial animals (Fig. 4).
The magnitude of changes in abundance during the 3 yr of the experiment were
equally variable, with even the controls demonstrating modest changes in cover of algal
crust species (Fig. 5). Although the largest changes occurred in treatments from which
either slow-moving herbivores, large fishes, or both were deleted, in general, the greater
the number of consumer groups that were deleted, the greater the total change in
abundance of sessile species (Fig. 5).
BRUCE A. MENGE ETAL.
238
n
1
R
INCREASE
II=
20
A = Ablebinaicr
P =PERENNIALS
E =EPHEMERALS
IO
08 qOTHER BIVALVES
0; ‘ORA’RA: SPONGE
E
C = Cbama echinata
M 5 hfesospom
H = Mdenbrandia
CC = COR. CRUST
S = Schizatkix
R = Raifsia
= DECREASE
0
H+-++--++--+p++-+-+-+-+-Sk;
N Rem
$2
0
=
I
I
T
;
_t
+
1
T
I-
-
122223334
Fig. 5. Mean total change in percent cover of secondary and primary space-occupying sessile species or
groups from initiation to conclusion of experiment: codes in box are listed in the same order in which they
are given on the histograms; height of each bar represents the total sum of increases (shaded bars) and
decreases (open bars) in abundance; each bar is broken down into the magnitude of change for each prey
species or group contributing to the total; percent covers are untransformed for ease in interpretation; no
statistics were performed on these data; secondary cover species are separated from primary cover species
by a space; treatment code and number of consumer groups removed is listed below each bar.
Separate effects of consumer groups
What was the contribution of each of the groups of consumers in this assemblage to
the overall effects shown above? The MANOVA analysis suggests that each consumer
group had statistically and ecologically significant effects on community structure
(Table III). However, as indicated by the rates and sequences of changes in prey
abundance, these effects varied both seasonally and between years (Table III; Figs. 6,
7). Moreover, some consumer groups had effects on some prey which were independent
of other groups (see below), while some had effects which depended on the presence
or absence of other consumer groups (as suggested by the significant statistical interaction terms; see next section).
Independent effects of removing slow-moving herbivores included: (1) over the short
term (0 to 6 months), ephemeral and perennial foliose algae (the green Ulva-Enteromorpha, and the reds Gelidium and Jania) increased, and two of the crusts (the red
Hildenbrandia sp. and the blue-green Schizothrix calcicola) decreased in abundance
(Fig. 6A1, II, III, row 1). (2) Seasonal fluctuations were induced in covers of perennial
foliose algae Gelidium and Jania), Ulva-Enteromorpha, and the algal crust Ralfsia sp.
(Fig. 6B1, II, III, row 1). (3) Over the long term (6 months to 3 yr), cover of algal crusts
as a prey group decreased and cover of solitary sessile animals as a prey group increased
(Fig. 71). The only prey species effected over the long term, however, were Hildenbrandia
ORGANIZATION
A.
SHORT-TERM
B.
SEASONAL
I.
OF A TROPICAL
GROUPS:
lo
& 2O
INTERTIDAL
II.
239
COMMUNITY
SPECIES:
lo
III.
SPECIES:
2’
CHANGE
CONSUMER
GROUP
= PRESENT
= ABSENT
N=
I
I
= ABSENT*
Fig. 6. Impacts of consumers on: A, short-term (top two rows of panels), and B, seasonal changes (bottom
two rows of panels) of: I, prey groups (occupants of both primary = 1’) and secondary = 2” space); II, prey
species occupying 1’ space; III, prey species occupying 2” space; left and right bars of each pair are values
with consumers
present and absent, respectively;
significant effects of deletion of a consumer group
independent
of the composition
of the remaining consumer assemblage are indicated by solid right bars;
significant effects of a consumer group which are dependent on other consumer groups (i.e., interactions)
are shown in Figs. 8 (short-term effects) and 10 (seasonal effects); - H = slow-moving herbivores removed;
- P = slow-moving predators
removed;
- LF = large fishes excluded;
- SFC = small fishes and crabs
excluded; CRUSTS = algal crusts; SOL SES = solitary sessile invertebrates;
ENC COL = encrusting
colonial invertebrates;
ARB COL = arborescent
colonial animals; other code names are as given earlier
or are self-evident. NS = not significant; * P < 0.05 or less.
sp., which decreased less, and Ulva-Enteromorpha, which increased greatly in the
absence of slow-moving herbivores (Fig. 711, III).
The only independent direct effects of removing slow-moving predators were a
short-term increase in the barnacle Balunus sp. (Fig. 6AI1, row 2) and a long-term
increase in all solitary sessile animals (Fig. 71, row 2). Other independent effects of
slow-moving predators (i.e., those on plants) were indirect, however, because the
predaceous gastropods were strictly carnivorous. These will be considered in a later
section.
240
BRUCE
A. MENGE
ETAL.
Jania
UlvalEnteromorpha
Giffordia
Gelidium
Jania
filamentous
greens
Abietinaria
Species all (secondary)
Balanus
Chama
crustose
corallines
Ra&a
Schizothrix
Hildenbrandia
Groups all
Encrusting
Colonial
Animals
Perennials
Species all (primary)
***
**
**
**
***
loo***
**
**
**
**
**
**
**
41***
***
***
45.1***
**
NS
126
I,26
1,26
1,26
I ,26
1,22
1,22
1,22
6,21
1,26
I,22
I,22
1,22
1.21
I,27
6,17
I,24
6,22
I,24
1,24
I,24
1,24
**
f
**
5,20
22/I***
(none)
(none)
(none)
(none)
P x H x SFC
P x SFC
(none)
P x LF
P x H x SFC
(none)
(none)
(none)
P x H, P x LF,
P x SFC, H x SFC,
PxHxLF
(none)
(none)
(none)
(none)
(none)
P x LF, P x SFC,
H x LF
(none)
(none)
P x LF, P x SFC,
H x LF, P x LF
P x LF
:Ytal)
H
P
LF
(Total)
(Total)
kotal)
(Total)
LF
H
(Total)
H, LF, SFC
P
H
P, H, SFC
il Raw data were percent covers taken on 18 sample dates from February or March 1977 to January 1980. Statistics were performed on transformed data
(arcsin transformation; Sokal & Rohlf, 1981). “(none)” under Interactions indicates that no interactions between consumer groups were significant for that
particular prey category. “(Total)” under Main effects means that the significant effect indicated in the Total effect column was due to the entire assemblage
of consumers, not to a single group of consumers. No consumer groups are listed in the Main effects column when they are included in an interaction because
the interaction supercedes the main effect in such cases. F-values are listed only for the overall MANOVA for each analysis; significance levels and degrees
of freedom (d.f.) are listed for all prey categories. *** P i 0.001; ** P < 0.01; * P < 0.05; NS = P > 0.05.
C. Induction of
seasonal fluctuation
(R = seasonal index)
Ulva/Enteromorpha
G@ordia
~lamcntous
greens
Abietinaria
Species all (secondary)
BRUCE A. MENGE ETAL.
242
The independent effects of removing the remaining two consumer groups were fewer.
Small fishes and crabs had a single short-term effect (ephemeral algae increased in their
absence; Fig. 6A1, row 2), no effect on seasonal fluctuations, and two long-term effects
(ephemerals decreased and the rock oyster Chama increased in their absence; Fig. 71,
I. GROUPS:
0.5
i”&
2’
II.
SPECIES1
III.SPECIES:
2’
0.4
0.2
0
0
0
-0.5
0.4
-0.1
0.5
0.2
0
Y
0
0.2
^r
0
;:
0.5
0
-0.5
Fig. 7. Impacts of consumers on long-term changes of: I, prey groups (occupants of both 1’ and 2” space);
II, prey species occupying 1” space; III, prey species occupying 2” space; significant long-term effects of
a consumer group which are dependent on other consumer groups are shown in Fig. 9; see caption for Fig. 6
for further explanation of codes.
II, row 4). Large fishes had no short-term effects, induced a single seasonal fluctuation
(encrusting colonial animals, a relatively scarce prey group, fluctuated more in their
absence), and had direct long-term effects on solitary sessile animals as a prey group,
although Balanus sp. was the only species affected independently (Fig. 71, II, row 3).
Non-additive effects of consumer groups
Statistical interactions among consumer groups are indicated when a significant
amount of the variation in the abundance of a prey is explained by combinations of two
or more consumer groups (i.e., the effect of one group depends on whether or not one
ORGANIZATION
OF A TROPICAL
INTERTIDAL
COMMUNITY
243
or more groups is present; Table III). In such cases, the statistical interaction supersedes
any significant effect of a single consumer group, unless, of course, the single group was
not included in the interaction. To interpret the statistical interactions, celI means of
each of the significant interactions (out of five possible two-way interactions and two
possible three-way interactions) were plotted (Figs. 8-10). Statistical interactions are
indicated whenever the lines joining cell means are not parallel. A brief scan of Figs.
8, 9, and 10 indicate that there were many statistical interactions among the consumer
groups in this experiment.
A.
P
x
;:jy=j
H
6.
PxHxSFC
;;Ei
+
H
+
-
+
-
H
Fig. 8. Short-term changes of sessile prey: analysis of significant statistical interactions
between consumer
groups. A, interaction
between slow-moving
predators
(P) and herbivores
(H) with respect to their
short-term (i.e., shortly after the experiment began) effects on tilamentous green algae (FIL. GRNS.). B,
interaction
between slow-moving predators (P), herbivores (H), and small fishes and crabs (SFC) with
respect to their effects on the brown tilamentous alga, Giffordiu mitchelliae. In this figure, and Figs. 9 and
10, dots indicate the average Y-intercept when the consumer group is present ( + ), triangles indicate the
average Y-intercept when the consumer group is absent ( - ).
Interpreting the biological significance of statistical interactions is difficult even in
simple systems, so it is not surprising that interpretations are not always self-evident
in this complex food web. Among the factors that need to be considered are the
following. (1) There were four consumer groups, each dominated by one to four species
(Table I). (2) Trophic links occur among the consumer groups, as well as between
consumers and sessile organisms (Menge et al., 1986). (3) The sessile organisms interact
(e.g., compete for space, provide substratum or microhabitats for each other, etc.; see
above). (4) The richness of sessile organisms is high (Lubchenco et al., 1984; Menge
et al., 1985), which by itself increases the chances for complexity in species interactions.
For these reasons and to save space, we do not attempt a detailed examination of
the ecological meaning of all significant statistical interactions. Instead, we discuss two
examples for the sake of illustration, and then use these analyses to emphasize three
results. (1) All consumer groups have major effects on the abundance of one or more
prey, either independently or through interactions. (2) Some changes in prey abundance
noted earlier (decline in crust cover due to increases in solitary invertebrates and foliose
algae) were at least partly due to rather complex, and still unexplored, interactions
among many mobile and sessile species. (3) Many significant statistical interactions are
due to indirect effects of consumers on prey they do not directly eat (see below).
244
BRUCE A. MENGE ETAL.
An example of an interaction of uncertain meaning is shown in Fig. 8A. Here, removal
of slow-moving herbivores (for brevity, we here use H) led to a short-term decrease in
the cover of tilamentous algae when slow-moving predators (P) were present (dots and
solid line in Fig. 8A) but to an increase when P were absent (right triangle in Fig. 8A).
Although P eat H, P shun algae, and their effect in this case must be either spurious
or indirect. A spurious effect could be due to patchy blooms of filamentous greens
A.
l-
-
PREY
ClUBTO
:
-+
LF
GROUPS
1l OI.
f
A”.
SLB
f
COL
pi’-+
-
0.5--
LCHLY
LF
---f--l--
-
+
,L”l!”
LF-
+LF_
:+
O/
- : p
-:
:
t
f-
+-
+SFC
+-
+-
fLF
+-
+-
+-
+
+-
+-
-
t
+-
-
H
Fig. 9. Long-term changes of sessile prey: analysis of significant statistical interactions between consumer
groups. A, interaction between slow-moving predators (P), herbivores (H), and large fishes (LF) with respect
to five prey groups; CRUSTS = crustose algae; SOL SES = solitary sessile invertebrates; ARB
COL = arborescent colonial animals; EPHEM = ephemeral fohose algae; and PEREN = perennial foliose
algae. B, interactions between P and H, P and LF, P and SFC, H and LF, and P, H, and SFC with respect
to various prey species (except SOL SES in the first panel of B: see the caption to Fig. 6 for further
explanation and codes of prey groups or species.
ORGANIZATION OF A TROPICAL INTERTIDAL COMMUNITY
245
unrelated to experimental manipulations. However, the blooms we observed occurred
uniformly along the shore and were usually barely perceptible, while dense growths
occurred in consumer exclusion experiments. Alternatively, P may indirectly affect
filamentous green algae through predation both on H, which graze filamentous algae,
PxHxSFC
B.
PxSFC
A.
9
JaniaSFc
+
+
5
11*.
-
J
C.
nr.-
A>+
..A-
I
+-
+-
H
SFC
lo-
i
:’
p
-
+
;
HxSFC
l
e
“1
cc
I*
en
SFC
D.
PxHxLF
Fig. 10. Seasonal changes of sessile prey: analysis of significant statistical interactions
between consumer
groups. A, interaction between slow-moving predators (P) and small fishes and crabs (SFC) with respect
to seasonal changes in crustose coralline algae (COR CR). B, interaction between slow-moving predators,
slow-moving herbivores (H), and small fishes and crabs with respect to seasonal changes in the foliose
coralline alga,Junia. C, interaction between slow-moving herbivores and small fishes and crabs with respect
to seasonal changes in Rufjikz (RA), Schimhrix (SC), ~ffde~bra~djff (HI), coralline crusts (CC), Balanus
(BA), and Chuma (CH). D, interaction between slow-moving predators, herbivores, and large fishes (LF)
with respect to the same prey categories as in C. See caption and text for Fig. 8 for further explanation.
246
BRUCE
A. MENGE
ETA.
or on sessile solitary invertebrates (e.g., barnacles, bivalves). The latter might shelter
small grazers, foster settlement of lilamentous greens (and other foliose algae), and filter
algal spores from the water. We do not presently know enough of the natural history
of this system to discern among these possibilities.
A more readily interpreted example is shown in Fig. 9A. Here, the effect of P on cover
of solitary sessile animals depends on the presence or absence of H and large fishes
(LF). Removal of P (or H) alone produces no long-term change. Removals of LF only,
H and P, H and LF, or P and LF all produce long-term increases in cover of solitary
sessile animals of similar magnitude, while removal of all three consumer groups
produces the largest effect. All these effects are most likely direct; P and LF consume
metamorphosed juveniles and adults of most sessile animals, while H probably bulldoze
recently settled juveniles.
Thus, each consumer group has effects on sessile prey, some independent of, and
some dependent on, the composition of the remainder of the consumer assemblage.
Many interdependent effects are quite complicated. For example, in Fig. lOD, seasonal
changes in abundance of six sessile species depend on interactions between P, H, and
LF. Further, as considered below, many statistically significant effects of consumers on
prey are indirect; i.e., they are due not to trophic interactions, but to interactions
between a prey and a non-prey organism (e.g., Bender et al., 1984; Holt, 1984).
Direct vs. indirect eflects
The above analyses, coupled with knowledge of the links in the food web of this
system (Menge et al., 1986), permitted us to distinguish between direct and indirect
interactions (Table IV}. Most direct effects were obvious and were noted above. Indirect
effects, although clearly indicated by significance in the statistical analyses, are more
difficult to characterize without detailed field investigation. Thus, some of the interpretations offered in Table IV are tentative, although all are based on our field observations and most have been documented in other, usually simpler systems.
Our interpretations fall into four categories. (1) Indirect beneficial effects of
consumers on one species or group of sessile organisms by removing competitively
superior sessile organisms. For example, H, P, and LF benefit the bier-resist~t
algal
crusts by removing solitary sessile animals or foliose algae or both gable IV).
(2) Indirect negative effects on foliose algae by removing sessile prey, whose irregularlyshaped shells serve as partial havens from consumers which graze most effectively on
smoother surfaces. For example, LF consume barnacles and oysters, whose shells
evidently provided somewhat better conditions for perennial foliose algae than did
smoother rock surfaces. The probable advantage of settling on irregular surfaces like
shells of invertebrates is that limpets and chitons, which crop foliose algae completely
from smoother substratum, are less eficient on more rugose surfaces. In contrast, the
beaks or jaws of fishes and the claws of crabs are less effective than are the radulae of
the molluscs and neither fishes nor crabs can graze foliose algae closely, regardless of
ORGANIZATION
substratum
rugosity.
OF A TROPICAL
(This interpretation
algal turfs only on smooth surfaces
accessible to fishes and crabs.).
is suggested
lacking
TABLE
Direct and indirect
INTERTIDAL
by the occurrence
shelter
for grazing
effects of consumer
H
groups
community
I Jnmanipulated
Ralfsia sp.
Schizothrix calcicola
encrusting corallines
Hildenbrandia sp.
Manipulated
community
Chama echinata
Balanus inexpectatus
Abietinaria sp.
Jania spp.
Gelidium pusillum
Giffordia mitchelliae
tilamentous greens
Ulva-Enteromorpha
molluscs
_
f
Dir.
but still
group
LF
SFC
+
+
+
+
I
I
1;
I
_-,+
+ -_ +
_
-1
_
_
+
_
Ind.
of
on sessile organisms.
P
Dir.
of patches
IV
Consumer
Dominant space
occupiers
247
COMMUNITY
Ind.
Dir.
Ind.
Dir.
Ind.
+
+
+
f
:
_
-1
_
_
_
_
_
_
_
+
+
+_
+ = positive effect; - = negative effect; . = no effect on abundance;
brackets indicate that the consumer
effect is exerted on a prey group rather than on individual species, e.g., consumers
affect algal crusts
positively,
not individual
crust species;
H = slow-moving
herbivores;
P = slow-moving
predators;
LF = large fishes; SFC = small fishes and crabs; Dir. = the effect of the consumer group is direct; Ind. = the
effect of the consumer group is indirect.
(3) By eliminating
foliose algae, H inhibit
recruitment
of Chama, which seems to
recruit best to algal turfs (possibly because of the cooler, moister microhabitat
found
among the holdfasts of the turf; authors’ personal observations).
In contrast, grazing
of foliose algae by H may enhance recruitment of Balanus, since these barnacles virtually
never recruited
to turfs (and our observations
in New England
indicate that
Semibalanus balanoides is inhibited by thick mats of the filamentous greens, Ulothrix and
Urospora). However, this latter effect is likely to be balanced by the direct bulldozing/grazing
of barnacle recruits by slow-moving grazers.
Finally, (4) H, which are directly preyed upon by P, may thus indirectly enhance
abundance of larger barnacles and oysters by diverting some of the predation pressure
exerted by P on these prey. This possibility is suggested by the PxH and PxHxSFC
interactions for solitary sessile prey, Balanus and Chama in Fig. 9B, where Balanus, for
instance, declined in the absence of H and presence of P but increased in the absence
of both consumers.
248
BRUCE A. MENGE ITAL.
We emphasize that our interpretations have not been subjected to field testing and
must remain hypothetical at present. However, the main point, that numerous indirect
interactions occur in this community, is robust. We further note that, with the exception
of the indirect effect of consumers in maintaining the dominance of the algal crusts (by
consuming foliose algae and solitary sessile invertebrates), most effects occurred under
experimental conditions. Thus, interaction complexity among sessile organisms in this
system may not normally be as high since most sessile species are rare and interspecific
encounters among these organisms are infrequent. High interaction complexity may
thus be a transient phenomenon, occurring under unusual conditions of temporarily
reduced consumer pressure.
An implication of the statistical interactions which revealed these indirect effects is
that interactions among consumers can have important effects on prey community
structure. One important theoretical question concerning the structure of consumer
assemblages is the extent to which generalized consumers have equivalent effects on
their prey. Previously, we have suggested (Menge & Lubchenco, 1981) that there is no
true “keystone” predator (sensu Paine, 1969) at Taboguilla. That is, no consumer has
effects which are overwhelmingly greater than those of any other consumer. We consider
this possibility below.
Impact of consumer groups: individual vs. combined effects
To evaluate how interactions between consumer groups influence their individual vs.
combined impact on major prey groups, we performed the following analysis. To
determine the effect of a consumer group (slow-moving herbivores, for example) on
abundance of sessile prey, we subtracted the mean cover of each prey group in controls
from that in slow-moving herbivore deletions on each sample date. This was done for
each single-consumer group deletion (with the exception of small fishes and crabs) and
for the total consumer deletion treatments for each of five prey groups (crustose algae,
solitary sessile animals, holdfasts of foliose algae, upright portions of foliose algae, and
arborescent colonial animals). The effect of small fishes and crabs was estimated as the
average prey cover in large fish plus small fish and crab deletions minus that in large
fish deletions. Statistical analysis of the resulting trends over the 1977-80 time period
was done using analysis of covariance.
This analysis permitted us to consider three questions. First, do the consumers
remaining after deletion of a given consumer group compensate for the absence of the
deleted group? Second, is the sum of the effect of the consumers in the single-consumer
group deletions equivalent to their effect in the total consumer deletions? Third, is there
a keystone consumer (or consumer group), and if so, which is it?
The evidence suggests that the consumers remaining after the deletion of a singleconsumer group can partially compensate for the absence of that group. Since cover
of sessile organisms is inversely related to cover of crustose algae (Figs. 2-3, we used
cover of crustose algae after consumer deletion as an inverse index of increase in total
ORGANIZATION
OF A TROPICAL
INTERTIDAL
COMMUNITY
249
cover of sessile organisms (Fig. 11). The results indicate that deletions of single
consumer groups (i.e., H, P, LF, or SFC) eventually lead to slight decreases in cover
of crustose algae, while deletion of the entire consumer assemblage (TOTAL deletion)
CRUSTOSE
-*cm!
1
,
,
,
,
,
s
8
7
.
1
1977
I
I
1978
ALGAE
,
,
1
7
,
10
,
11
,
I
,
I
1979
,
7
9
1980
Fig. 11. Effects of consumers on space availability as estimated by the difference between abundance of
crustose algae in consumer-deletion
treatments
and controls: TOTAL is the total effect of consumers as
estimated by the difference between y0 cover of crusts in total consumer deletions and controls (i.e.,
TOTALS - CO); SUMMED is the total effect of consumers as estimated by the sum of the effects of each
of the four consumer groups as separately estimated by the differences between y0 cover of crusts in
deletions of single consumer groups and controls (i.e., [H - CO] + [P - CO] + [LF - CO] + [SFC LF] = SUMMED effect); - H, - P, - LF, and - SFC indicate the separate effects of the single consumer
groups which when added yield the SUMMED line in the figure; the negative initial values (i.e., for 2/77)
indicate that the average abundance of crusts in treatments was initially slightly less than that in controls;
we regard this as within the range of normal variation.
leads to near-elimination of crustose algae (Fig. 11). If the consumers did not compensate, then the sum of the separate effects (i.e., SUMMED in Fig. 11) of each group
would equal the effect of the TOTAL deletion, which is not the case (Fig. 11, Table V).
Since there were three major groups of prey which increased in response to consumer
deletions (solitary sessile animals, both upright and holdfast portions of foliose algae,
and arborescent colonial animals), the answer to questions 2 (are the effects of the
consumer groups additive or not) and 3 (is there a keystone consumer group) are best
approached by considering each prey group separately. As indicated in Fig. 12, the
answer to these questions depends on which group is considered. The separate effects
of each consumer group on solitary sessile animals was small (Fig. 12A, dashed
lines), and the sum of these separate effects was significantly less than their effect in
TOTAL deletion plots (Table V).
In contrast, the sum of the separate effects of consumers on foliose algae and upright
colonial animals did not always differ from the effects in total exclusions (Table V).
Further, the effect of a single group on these prey (H on foliose algae, SFC on colonial
BRUCE A. MENGE ETAL.
250
animals) is similar to the effect in total exclusions, suggesting a keystone effect (Fig. 12B,
C, D). Specifically, the effect of H on the holdfasts of the foliose algae was not
si~i~c~tly different from either the sum of the separate effects (ANCOVA; P = 0.32),
TABLE V
Analysis of covariance comparing regressions on effects of the four consumer groups estimated either by
summing the effects of removing single groups in four separate treatments or by the effect observed in
removals of all groups simultaneously in a single treatment.
Ho
Sessile group
Algal crusts
Solitary
sessile animals
Algal holdfasts
Foliose algae
Arborescent
colonial
animals
Treatment
Sum of single
group effects
Total effect
Sum of single
group effects
Total effect
Sum of single
group effects
Total effect
Sum of single
group effects
Total effect
Sum of single
group effects
Total effect
Y-intercept
Slope
_ 24.9
- 0.205
- 16.8
Slopes
equal
Slopes
=0
Regressions
equal
- 1.997
0.459
***
***
***
- 13.3
19.6
2.13
- 0.437
***
***
***
31.6
60. I
- 0.768
0.512
NS
*
NS
66.1
-0.622
0.381
*
NS
*
0.497
NS
**
*
- 1.90
10.5
2.68
Degrees of freedom (slopes equal) = 1, 22; d.f. (slopes = 0, regressions equal) = 1,23. *** P < 0.001;
**P< 0.01;
*P< 0.05;
NS = P> 0.05.
or the effect in total exclusions (ANCOVA; P = 0.07). Similarly, the analysis suggests
that small fishes and crabs have a keystone effect on arborescent colonial animals
(Fig. 12D, Table V; ANCOVA; SFC regression is not different from that for either the
sum of the separate effects [P = 0.068] or the total effect [P = 0.8431).
The keystone effect of slow-moving herbivores on the thalli of foliose algae was
similar, although it appears a bit more complex in Fig. 12C. The long-term effect of H
on the thalli of the foliose algae was not different from the effect in total exclusions
(ANCOVA; P = O.OSS),
~thou~ a difference (P = 0.011) between the slopes of the
regressions for the H and total effects suggests an initial. difference in these effects
(Fig. 12C). The effect of H on thalli was parallel to (ANCOVA; slopes are equal,
P = 0.943), but less than the sum of the separate effects (ANCOVA; P < 0.0004),
suggesting that other consumers (mostly SFC) also had an effect on the abundance of
foliose thalli.
Unexpectedly, the total effect was also less than the sum of the separate effects
(Fig. 12C, Table V; regressions were not equal, P = 0.02). This implies that the effect
ORGANIZATION
251
OF A TROPICAL INTERTIDAL COMMUNITY
of a given consumer group was less when excluded with all other consumers than when
removed separately, or, in other words, that the effect of some consumers was enhanced
by the presence of others. However, this apparent “super-keystone” effect seems best
explained as an artifact of an indirect effect. Since solitary sessile animals covered more
A.SOL
50
SES
B. ALGAL
ANIMALS
HOLDFASTS
I
0
0
3
5
7
9
13
4
C. FOLIOSE
7102
4
7
1
ALGAE
3
5
7
9
D.ARB
1‘3
4
CO1
7102
4
7
ANIMALS
10
5
4---T
,
,
3
7
9
5
TOTAL=
*
I
13
I
74
I__...
7102’4
SUMMED=
7
l
1
-H=m
3
:
5
7
-p=+
9
13
-LF=&
4
7102
:
4
-SF&
7
A
Fig. 12. Effects ofconsumers on each of four major prey groups: A = solitary sessile animals; B = holdfasts
of foliose algae; C = secondary cover of foliose algae; D = secondary cover of arborescent colonial animals;
symbols coded as in Fig. 11; the third lines in B and C ( - H line) and D ( - SFC line) are connected by
solid lines because ANCOVA analysis indicates that they are statistically indistinguishable from the TOTAL
and/or SUMMED LINES; see text for details of the analysis.
space in total exclusions than in single group exclusions (e.g., Fig. 12A), less space was
available for the turfy foliose algae in total exclusions. That is, the lower cover of foliose
algae in total exclusions is probably due to competition for space with solitary sessile
invertebrates, and not to some dependence of some consumers on the presence of
others.
Thus, this analysis suggests that the roles played by the consumer groups depends,
in part, on the prey group considered. Since the impact of consumers on solitary sessile
252
BRUCE A, MENGE ETAL.
prey is revealed only when all are s~ult~~usly
removed (Fig. 12A), their effects on
these prey are ~terdependent but not additive. In contrast, the elects of consumers on
foliose algae (mostly the perennials Gelidium and Janiu) and arborescent colonial
animals (mostly the hydrozoan Abielinatiu sp., but also bryozoans) are attributable
mostly to slow-moving herbivores and small fishes and crabs, respectively
(Fig. 12B-D).
DISCUSSION
COMMUNITY
DYNAMICS AT TABOGUILLA
Normally, space in this low zone habitat is dominated by four algal crusts (Lubchenco
et al., 1984; Fig. 2). This pattern is both temporally and spatially persistent: quantitative
transects taken at 11 sites in the Bay of Panama and the Gulf of Chiriqui were
dominated by algal crusts (Menge & Lubchenco, 198 1; Lubchenco et a/., 1984; Menge,
unpubl. data), and obse~ations and transects at Tanaka
from 1973 to 1983 indicate
that these patterns vary little over time (Lubchenco eta& 1984; B. Menge and J.
Lubchenco, pers. obs.).
What are the causes of this apparent stability? Physically, this habitat is harsh,
especially during the dry season when waters are often calm and one of the two daily
low tides occurs in midday (Garrity, 1984; Lubchenco et al., 1984). In the high and mid
zones, evidence indicates that heat and desiccation stresses reduce the activity and
cause mo~~ity of mobile ~ve~ebrates (Garrity, 1984), and may suppress abundances
of sessile organisms (Lubchenco et al., 1984; B. Menge 62J, Lubchenco, unpubl. data).
With one exception, our results suggest that physical stress has a small effect in the low
zone. This exception is a slight seasonal fluctuation in the upper limit of crustose
coralline algae (Lubchenco et al., 1984), with a lower upper limit occurring during the
dry season. We have not investigated longer-term, sublethal effects of heat or desiccation
stress on community structure.
Consumers and interspecific competi~on are two major dete~n~ts
of community
structure in the low zone at Taboguilla. Prey groups most strongly affected were foliose
algae, arborescent colonial invertebrates, solitary sessile invertebrates, and, indirectly,
crustose algae. Each of these groups is discussed in turn. First, the total abundance of
foliose algae was suppressed by both grazing invertebrates and browsing fishes and
crabs (see summary in Table IV). Thus, reduction in the abundance of grazing molluscs
produced a rapid increase in foliose algae, with ephemerals, and then perennials
exhibiting large increases in abundance (e.g., Fig. 3). Although slow-moving herbivores
evidently had the largest short-term effect, large and small fishes and crabs also reduced
the abundance of foliose algae, especially over the long term. While grazing molluscs
also had longer-term effects, these were dependent on interactions with other consumer
groups (e.g., Figs. 6-10).
Important qualitative differences may exist in the ways in which these groups
ORGANIZATION
OF A TROPICAL INTERTIDAL COMMUNITY
253
influenced the abundance of foliose algae. On a local spatial scale, grazing molluscs
appeared to crop foliose algae closer to the surface than did fishes and crabs. However,
at larger spatial scales, molluscan grazers appeared relatively inefficient in controlling
macroalgal abundance, presumably due to their sluggish nature and limited perception
of their surrounding environment, and local patches of algae may occasionally be found
which have evidently escaped the molluscan grazers. In comparison, fishes and crabs
have a small short-term effect on fohose algae, probably because they cannot crop it
close to the surface; hence, short algal turfs may be essentially unavailable to these
consumers. However, fishes and crabs are large, fast-moving, have wide perceptual
fields, and powerful feeding apparatuses, all of which presumably combine to allow
rapid detection of, movement to, and consumption of concentrations of food. Since the
effects of fishes and crabs are greatest on prey taking longer to become large or abundant
(several months for foliose algae, a year or more for sessile invertebrates; Figs. 7,9),
the effects of grazing molluscs and of fishes and crabs on foliose ma~ro~gae at
Taboguilla appear complementary. Indeed, were it not for substratum heterogeneity,
which provides temporary microrefuges from these consumers (Menge & Lubchenco,
1981; Menge et al., 1983), foliose algae would probably virtually disappear from these
shores.
Second, the abundance of arborescent, colonial invertebrates, primarily the
hydrozoan Abietinaria sp., was controlled by large fishes. This hydrozoan is normally
ubiquitous, but scarce, on Taboguilla. Deletion of large fishes led to significant increases
in its abundance (Fig. 9B, Table IV), although it never truly dominated any pIot. This
species achieved its greatest prominence as an epibiont on shells of sessile invertebrates
(e.g., Fig. 3). It did not appear to be an effective competitor for space.
Finally, the abundance of solitary sessile invertebrates was strongly affected by all
consumer groups, usually in combinations of two or more groups. Recruitment of the
dominant sessile invertebrates, Balunus and Chama, was evidently inhibited by slowmoving grazers, and possibly, small fishes and crabs, and larger individuals were preyed
upon by large fishes and predaceous snails. Like the foliose algae, these animal prey are
normally scarce on the shore, and Chama, but, interestingly, not Balanus, are usually
found primarily in holes and crevices in the rock.
Expl~ations for the occurrence of palace on surfaces exposed to fishes and crabs
are (1) that they grow exceptionally fast, and/or (2) that fast-moving consumers do not
consider barnacles to be attractive prey. Regarding the first hypothesis, we have
observed growth of recently settled individuals (i.e., within the past week) to “adult”
size within a month or less. Thus, B&anus may simply escape fishes over the short-term
by rapid growth, but eventually be discovered and consumed. Regarding the second
hypothesis, adult barnacles seem to live only a matter of weeks before they are preyed
upon by predaceous snails, primarily Thaiv melones. However, their empty shells may
persist on the shore for months, thus, dead barnacles typically outnumber living ones.
Hence, unless an empty barnacle shell displays outward signs of attractiveness as food
(e.g., it is used as a shelter by a small crab or other potential prey, or is festooned with
254
BRUCE A. MENGE
ETAL.
foliose algae), crabs and fishes may ignore all barnacles, because in their experience,
most are empty and not worth the effort.
As we have discussed elsewhere (Menge & Lubchenco, 1981; Menge et al., 1985),
bivalves (Chama, and possibly the mussel Modiolus cupax and the giant oyster Ostrea
iridescens) are likely to eventually replace the crustose algal monopoly with a bivalve
monopoly. This is, however, a result observed in experiments, and it is pertinent to ask
whether or not bivalve-dominated shores wouid ever occur naturally in this region. We
have observed sites in the Bay of Panama (ChamC Island) and the Gulf of Chiriqui (Uva
Island) where abundances of C~~~~ are higher than that seen anywhere on Ta~guilla
or neighboring islands. In all instances, high cover of Chama is correlated with either
alterations in the consumer assemblage, or factors that might alter the effectiveness of
consumers, or both. Thus, oysters are often more abundant on shores with severe water
turbulence; that is, sites where all consumers are likely to be less efficient foragers (e.g.,
Menge, 1978a, b, 1983). Also, oysters are generally more abundant at sites with
persistent high turbidity, which may influence fish presence and foraging ability. Despite
these examples, however, we never observed a non-expedite
rocky surface in the
>
80%
covered)
by
bivalves. Combined
Gulf of Panama which was truly dominated ( =
with the intensive maintenance required by our consumer deletions and the diversity of
the consumers in this community, our observations suggest that such sites will generally
be rare in this region.
Thus, we suggest that the spatial and temporal uniformity of dominance of low
intertidal rock surfaces by algal crusts at Taboguilla is due to uniformly intense
predation by a complex assemblage of consumers. Each consumer group has a distinct
effect on sessile prey: molluscan grazers virtually eliminate foliose macroalgae and alter
the relative abundances of algal crusts; all consumers interact to keep solitary sessile
invertebrates scarce; and fishes and crabs browse both foliose macroalgae temporarily
escaping the control of molluscan grazers, and arborescent colonial invertebrates,
COMPLEX
FOOD
WEBS AND
COMMUNITY
THEORY
The results presented above bear on several general issues, including the concept of
“keystone” species (Paine, 1969), diffuse competition (MacArthur, 1972), indirect vs.
direct effects (e.g., Bender et al. 1984), and whether or not observed spatial variation
in community structure indicates differences in underlying causes.
Our experiments suggest that a keystone species is lacking in this community.
Although slow-moving herbivores have by far the largest effect on foliose algae, and
small fishes and crabs have the greatest effect on abundance of arborescent colonial
animals, neither of these prey groups includes a strong competitor for space. The
dominant competitor for space is evidently Chama echinata, and our analyses suggest
that this species is collectively controlled by all consumer groups. Although no
single-group removal had a dramatic effect on the dominant space-occupants, one might
ORGANIZATION
OF A TROPICAL
INTERTIDAL
COMMUNITY
255
argue that large fishes, especially Bodiunus and Diodon, play a keystone role by virtue
of their ability to control prey that escape from the intermediate trophic level consumers.
Our experiments and observations are not consistent with this interpretation, primarily
because prey do not appear to escape from the abundant, trophically intermediate
predaceous gastropods. Thais melones, for example, can successfully attack and
consume the largest sessile invertebrate prey we have seen on the shore (Menge et al.,
1986). Also, in the absence of large fishes and presence of other consumers, sessile
invertebrates did not become abundant even after more than 3 yr. Hence, at present,
the evidence suggests that a keystone species is lacking in this community.
The absence of a keystone species may be related to a number of characteristics of
the community, including the high species richness at upper trophic levels and the fact
that the intertidal zone represents only part of the foraging range of the top predators.
Virtually all fishes at Taboguilla reside in the subtidal region, and although many forage
intertidally at high tide, feeding time in that region is limited by both the tidal cycle and
wave action during high tide. Furthermore, since few of the intertidal prey species occur
in the subtidal region, the fishes forage on different prey in the intertidal and subtidal
zones (authors’ unpublished data). Hence, fishes may not form the strong
predator-prey relationships with potentially dominant intertidal prey that are known
for communities with keystone species (e.g., Paine, 1974, 1980; Menge, 1982a).
The existence of diffuse competition (sensu MacArthur, 1972) among many of the
predaceous species and among many of the herbivorous species in the community is
suggested by both the exceptionally broad diets of most species and the compensatory
changes expressed when single consumer species were removed. This idea warrants
testing in this community.
Recent theoretical work has emphasized the potential importance of indirect (vs.
direct) species interactions (Holt, 1977, 1984; Abrams, 1984; Bender et al., 1984). As
summarized above (Table IV), statistically significant indirect effects are common in
this complex community. For example, the occasional formation of patches of foliose
algal turf on smooth rock surfaces seems dependent on localized reduction of limpet
densities by fishes. Further, the dominance of space by algal crusts depends on the
normal elimination of foliose algae by grazers. Since indirect effects are also important
in certain simple communities (e.g., Lubchenco & Menge, 1978; Brown et al., 1986;
Dungan, unpubl. data), it seems unlikely that indirect effects are uniquely associated
with tropical or complex communities. Although we can predict that indirect interactions will be prominent features of the dynamics of all communities, we know too little
about the details of interactions between most types of organisms to predict with much
accuracy where and when they will occur, let alone their importance in community
regulation. The existence of indirect interactions serves to underline the complexities of
the dynamics of communities, and emphasizes the necessity of knowing natural history.
Despite much progress, we still know far too little about even reasonably well-studied
systems.
The structural differences between this and temperate communities (i.e., dominance
BRUCE A. MENGE ETAL.
256
by encrusting algae vs. dominance by sessile invertebrates and large erect algae) are not
due to uniquely different causal agents, but to variation in the intensities of the same
set of causal agents. The structure of this community depends on the same processes
stressed in studies of other communities, but the rates and intensities of these processes
appear different at Taboguilla. Specifically, predation appears more intense, competition for space and physical disturbance seem much less intense, and recruitment rates
are much lower than in most cool temperate rocky intertidal communities. As we argue
elsewhere (Menge & Lubchenco, 198 l), some of these differences probably derive from
such physical features as (e.g.) relatively high and little seasonal variation in water
temperatures. Presumably, this permits consistently high metabolic rates, and yeararound activity of consumers (see Discussion in Gaines & Lubchenco, 1982).
Combined with other factors, near-continuous consumption of prey would seem to be
a key factor in producing high levels of predation.
Despite the many environmental and biological differences between Taboguilla and
certain temperate communities, experimental deletions of consumers usually lead to
dominance by sessile invertebrates, particularly bivalves (e.g., Paine, 1966, 1971, 1974,
1984; Dayton, 1971; Menge, 1976; Lubchenco & Menge, 1978; Peterson, 1979; Menge
& Lubchenco, 1981; Fairweather et al., 1984; this paper). This not only supports our
argument that such communities are organized by different intensities of similar forces,
it is also consistent with models of community organization which stress such
commonality in the dynamic processes which underlie divergent patterns of community
structure (e.g., Paine, 1966; Connell, 1975; Menge & Sutherland, 1976), counter
arguments notwithstanding (Underwood & Denley, 1984). Although these models are
not without flaws, they have also enjoyed modest success in predicting community
organization in a variety of other habitats (e.g., Morin, 1983; McNaughton, 1983;
Peckarsky, 1983). As empirical knowledge increases, revision of these partially successful theories should lead to continued progress in the development of a conceptual
framework in community ecology.
TRADE-OFFS
IN ALTERNATIVE
EXPERIMENTAL
APPROACHES
TO COMMUNITY
REGULATION
There are a number of different experimental approaches that could be used to
understand the dynamics of communities. They include: (1) a simultaneous investigation of the role of all major species in the system, (2) sequential studies of different
ecological processes (competition, predation, etc.) focussed at the species level, (3) a
simultaneous evaluation of different. ecological processes focussed at the level of
functional groups, or (4) some combination of these three approaches. Each approach
has advantages and disadvantages. Although approach (1) has been successfully
employed in some communities (Lubchenco & Menge, 1978) and provides the most
comprehensive analysis of community dynamics, it is impossible to use in complex
communities. There are simply too many species, for example, in the low zone at
Taboguilla for separate, simultaneous manipulations of even only the major ones.
ORGANIZATIONOFATROPICALINTERTIDALCOMMUNITY
251
Approach (2) has long been the dominant method of choice in co~unity
ecology,
and it offers the advantage of detail and precision in ident~~g the ecological processes
at play in the community. However, as recently noted by numerous authors (e.g.,
Connell, 1983; Schoener, 1983; Bender et al., 1984; Lubchenco, 1986), this approach
does not reveal the relative impact of each process and is subject to problems in
interpretation due to the necessity of having to ignore some species. Although sequential
or separate investigations may show that physical disturbance, competition, and grazing
all have significant effects in a community, determination of the relative importance of
each is impossible unless all factors were studied in the same experiment. Moreover,
if some species are ignored, as they must be using this approach, especially in complex
communities, then experiments may produce misleading results (Bender et al., 1984).
For example, a species may be regarded as having no effect, when in fact its effect was
masked by an unmanipulated species.
In approach (3), the complexity demanded by simultaneous investigation of different
processes is offset by the simplification provided by a focus on functional groups. This
was the appro~mate method used in the experiment reported in the present paper, and
it offers the advantages of revealing the overall organization of the community,
suggesting the relative importance of different processes and reducing problems of
interpretation caused by ignoring species. However, it lacks precision, loses detail, and
introduces problems of interpretation caused by lumping. For example, in the present
paper, consumer species were lumped together (reducing precision in manipulations and
blurring detail in the responses to manipulations). Nonetheless, this type of experiment
produces a broad understanding of the org~ization of a community, and has the
potential to provide sufficient detail to identify fruitful avenues of further research.
Approach (4), a combination of (2) and (3), offers probably the best solution for a
complex community. We found that using approach (3) first, then approach (2) provided
a very reasonable way to attack the dynamics of a complex system. The initial studies
described above and in Menge & Lubchenco (1981), Menge et aZ. (1985, 1986) and
Lubchenco et al. (1984) all used approach (3), using manipulations of functional groups
to elucidate the overall dynamics of the system. These studies laid the ~oundwork for
and have been supplemented by more in-depth investigations of individual species, i.e.,
approach (2) (Garrity & Levings, 198 1, 1983 ; Levings & Garrity, 1983 ; Menge et al.,
1983, in prep.; Garrity, 1984; Gaines, 1983). Together these studies have shown a
feasible way of approaching the dynamics of a complex community.
ACKNOWLEDGEMENTS
We thank S. Gaines, C. Marsh, W. Rice, J. Sutherland, T. Turner, A. Brown, T.
Farrell, A. Olson, L. West, R. Paine, and an anonymous reviewer. Many others assisted
in this study, most notably R. Emlet, S. Garrity, P. Lubchenco, J. Lucas, A. Matson,
L. Olds, S. Sargent, S. Strauss, J. Valenter, and P. Williams. The Republic of Panama
BRUCE
258
A. MENGE
ETAL.
and the Smithsonian Tropical Research Institute provided field access, laboratory
space, and logistical support. I. Rubinoff, V. Vergel, J. Budria, E. Lombardo, R. Ely,
and L. van Valkenhoef of STRI were particularly helpful. The research was supported
by NSF grants OCE76-22251, OCE78-17899, and OCE80-19020 to B. Menge and
J. Lubchenco, and writing was supported by NSF grant OCE-8415609 to B. Menge.
APPENDIX
EVALUATION
OF EXPERIMENTAL
DESIGN,
EXECUTION,
AND
ANALYSIS
OF RESULTS
“Proper statistical methods should be used, but the biologically defined objective should dominate
use the statistics, rather than the reverse” (Green, 1979, p. 6).
Below, we describe the design, execution, and analysis of this study, and evaluate problems therein
Hurlbert,
1984). In particular,
we consider the independence
of the experimental
plots, since
assumption of independence
of errors is the only one in most statistical methods for which violation is
serious and impossible to cure after the data have been collected” (Green, 1979).
EXPERIMENTAL
and
(e.g.,
“the
both
DESIGN
Premanipulation similarity among sites
Some physical and biological variation among sites (and plots) is inevitable in experimental field studies;
the best we can manage is to make initial conditions in sites or plots as similar as possible (see, e.g., Connell,
1974). Since our experiences
in temperate
rocky intertidal habitats accustomed
us to observing large
between-site differences in community structure, we were initially struck by the apparent homogeneity
of
the community on the shores of Taboguilla (and neighboring islands). More detailed sampling supported
these impressions (Fig. A-l).
Physically, all sites are: southerly in aspect, intermediate
in wave exposure, and probably virtually
identical in desiccation stress, water and air temperature,
insolation, and water turbidity (Lubchenco et al.,
1984). All have a heterogeneous
basaltic substratum,
but Sites 4 and 6 are somewhat less heterogeneous
than Sites I and 2 (Fig. A-l). Tidal levels of the plots were similar, but varied somewhat (Table A-l) due
to our use of “biological indicators”, rather than absolute tidal height when selecting plot locations. That
is, because the vertical locations of the biota vary with local variation in wave exposure, aspect, etc. (Lewis,
1964), local patterns of species composition and abundance are better indicators of a particular “realized”
tidal height than is absolute height with respect to a fixed reference point (e.g., mean low water). When the
entire range of physical conditions in rocky intertidal habitats in this region is considered, most differences
between sites are ecologically insignificant.
Biologically, the sites also differed little prior to the experiment (Fig. A-IB,C). Premanipulation
percent
cover ofthe eight most abundant occupants ofprimary space did not differ among sites (MANOVA, F = I .80;
P = 0.13; 8, 2 I d.f.). However, premanipulation
cover of the eight most abundant occupants of secondary
space did differ (MANOVA, F = 2.66; P = 0.03; 8,2l d.f.), as indicated by a significant slow-moving predator
( = P) x slow-movingherbivore
( = H)statistical
interaction. Graphic analysis indicates that this effect is due
largely to relatively high abundance of several foliose species on Site 4 (average percent cover ranges from
0. I to 8.4%) compared to the normal 0 to I % ; Fig. A-2). However, no single prey species differs significantly
in abundance among sites (multiple comparisons tests = one-way ANOVA with critical value adjusted with
theBonferronimethod;P
> 0.05inallcases).Therefore,thesignificantMANOVAmustbeduetothecollective
effect ofhigher abundances offoliose algaeon Site 4. The premanipulation
difference attributable to P-removal
sites (as indicated by the P x H interaction) is evidently due to slightly higher abundance of the hydrozoan
Abietinaria sp. at site 1 than at the other sites (Fig. A-2).
Since ecological systems commonly exhibit considerable
variation,
and differences in percent cover
< 10% are difficult to detect without extensive replication, we consider the premanipulation
difference in
foliose algae among sites to be ecologically trivial. However, correlated with this slightly higher abundance
ORGANIZATION
OF A TROPICAL INTERTIDAL COMMUNITY
259
of algae is the absence from site 4 of the herbivorous crab Grupsus grupsus (Fig. A-l). Although this crab
is one of the most abundant members of the small fish and crab ( = SFC) consumer group, and its absence
from Site 4 could have led to a partial escape by the algae from consumers, other members of this consumer
group (e.g., Ophioblennius, juvenile fishes, the crab Ertphides hispida) were present at this site. We conclude
that the study sites were initially similar in physical and biological characteristics, and that the exceptions
were unimportant relative to the questions being asked in this study.
A. PHYSICAL
ENVIRONMENT
EXP.
8. SESSILE
5
b
40
BAR
Biv
ORGANISMS
COL.
SES.
m.
COR.
CR.
FOL.
ALG.
T
C. MOBILE
ORGANISMS
Fig. A-i. Physical environmental characteristics (A) and community structure (B and C) prior to
experiment initiation at Taboguilla (summarized from Lubchenco et nl., 1984): bars are 95% confidence
ranges at each site; mean and 95 % confidence intervals are given For temperature, windspeed, and visibility;
data were not transformed before plotting to make interpretation easier; abscissa labels: 1,2,4, and 6 refer
to experimental site numbers; D and W refer to dry and wet seasons. A, MSD = mean substratum depth,
an index of substratum heterogeneity; EXP. TO FMC = percent of the substratum exposed to fast-moving
consumers (large fishes and large crabs), ASPECT = arrows indicate direction each site faces;
TEMP. = temperature (open symbols = air, and solid symbols = surface sea-water temperatures);
WIND = windspeed (open symbols); VISIB. = lateral visibility in the water column (solid symbols). B,
BAR. = barnacles; BIV. = bivalves; COL. SES. = encrusting colonial animals (all sessile animals);
Hild = Hi~denbrandia spp., COR. CR. = encrusting coralline algae; Rulf: = Ra(fsiu sp., S.C. = Schizothrix
calcicola (all encrusting algae); FOL. ALG. = foliose algae. C, SMC = slow-moving consumers;
F.v. = ~~s~re~~a virescens (keyhole limpet); LIMP. = tota limpets; CHIT. = chitons; E.v. = Ech~ometra
vanbrunti (sea urchin); P.t. = Pachygrapsus tramversus (crab); PRED. GAST. = total predatory gastropods;
FMC = fast-moving consumers; G.g. = Grupsus grapsus (crab); E.a. = Eupomacentrus acapulcoensis (damself&h); K.e. = Kyphosus eiegans (chub); 3.d. = Bodianus diplotaenia (wrasse).
of treatment
plots)
+H-P-LF+SFC
Predator removal and
large fish exclusion
tH+P-I.F-SFC
tH+P-LFtSFC
+H+PtLFtSFC
Code
+H-PtLFtSFC
(roof)
A-I
(+6.3)
(+ 6.5)
(t6.1)
(+ 5.3)
t 0.8 (t 2.6)
+0.6 (t2.1)
+ 0.7 ( + 2.4)
+ 0.7 ( t 2.2)
+ 0.7 ( t 2.2)
+ 0.7 ( + 2.4)
1
2
tl.6
(+5.2)
+ 1.8 (t 5.8)
t 1.8 (t 5.8)
ND
+I.6 (+5.2)
t 1.6 (t 5.3)
t 1.8 (t 5.8)
ND
t 1.9
+ 2.0
+I.9
+ 1.6
m (ft)
Tide height
1
2
3
4
2
3
4
I
1
2
3
4
1
2
3
4
Plot
NO.
5.9
5.9
3.9
3.5
4.8 c 0.6
2.8
5.5
4.1
3.7
4.0 + 0.6
2.9
3.2
3.4
4.3
3.5 f. 0.3
7.0
7.7
5.1
4.7
6.1 k 0.7
7.8
8.4
8.1 k 0.3
M&III
Substratum
60.4
15.2
92.5
72.0
75.0 * 6.6
63.5
52.6
47.4
67.6
57.8 r 4.7
96.9
66.2
54.6
62.5
70.0 + 9.3
77.1
78.8
106.4
63.1
81.4 * 9.1
59.9
62.9
61.4 k 1.5
Coefficient
of variation
heterogeneity”
4.4
3.5
2.8
2.1
*
k
i
i
8.0
4.2
5.6
5.6
& 2.8
+ 3.6
* 7.3
+ 7.6
& 3.2
+ 2.4
+ 4.6
f 6.4
+
t
k
f.
1 SE
5-5 1
17-84
5-96
12-61
17-94
12-91
O-38
19-65
17-87
17-95
20-59
10-39
26-64
17-79
18-75
18-54
11-44
12-33
Range
Herbivores
25.5 + 3.6
43.2 + 5.4
50.9
33.6
46.4
47.2
12.5
38.8
39.3
36.2
39.5
23.8
45.9
37.4
45.8
36.1
24.7
21.2
i*
depending
date.
on the treatment,
16
16
16
16
16
16
16
16
IO
10
16
15
9
10
15
15
16
14
N
i
f
f
f
( 1.6
( 1.8
(2.2
( 1.1
0.6
0.4
0.5
0.3
1.6
1.4
1.3
5.6
1.2
1.2
1.9
2.2
(5.1 + 1.4
( 5 3 * 0.9
k
i_
i_
t
*
*
k
i
? 0.9
& 0.4
+ 0.8
+ 0.7
7.4
9.8
5.4
19.7
4.1
7.7
6.2
6.7
4.9
1.9
4.1
4.1
O-20
o-12
O-8
O-6
o-7
o-4
O-18
3-24
o-14
o-47
o-17
o-14
O-18
O-23
o-12
O-6
o-11
O-8
Range
Predators
No. slow-moving consumers
present or entering
(in parentheses) each plotb
plot tide heights (datum = MLW) and substratum
heterogeneities
and number of slow-consumers:
latter data are mean number present per sample date or mean number removed per sample
Predator removal
(marked plots)
(cage)
Large, small fish and
crab exclusion
(roofI
Large fish exclusion
(marked
Control
Treatment
Summary
TABLE
16)
16)
16)
16)
16)
16)
16
16
10
10
16
15
9
10
15
15
16
14
the
-H-P-LF-SFC
Herbivore and predator
removal, large, small
fish exclusion (cage)
il See Lubchenco
et al. (1984) for methods
N = number
of dates monitored.
-H-P-LFtSFC
-H-P-LF+SFC
-H+P-LF-SFC
-HtP-LF+SFC
-H+P+LFtSFC
+H-P-LF-SFC
Herbivore and predator
removal, large fish
exclusion (roof)
(roof)
Herbivore removal and
large, small fish and
crab exclusion (cage)
Herbivore and predator
removal (marked
plots)
Herbivore removal and
large fish exclusion
(cage)
Herbivore removal
(marked plots)
Predator removal and
large, small fish and
crab exclusion
used
+ 1.1
t 1.1
I
I
+
+
t
+
in obtaining
2
3
4
I
2
3
4
+
+
+
+
0.8
0.8
0.8
0.8
1.1
1.0
0.7
0.8
data.
2.7)
2.6)
2.6)
2.6)
3.5)
3.4)
2.3)
2.6)
these
t
+
t
+
t
+
+
t
t 1.0(+ 3.3)
t 1.0 (+ 3.2)
+ 0.7 t 2.3)
+ 0.9 + 2.8)
I
2
3
4
+1.1 (+3.6)
+l.O (t3.2)
+ 3.5)
t 3.6)
+ 3.7)
+ 3.4)
13.1)
+ 2.9)
2.5)
+ 2.5)
t
1
2
2
2
3
4
+
+
t
+
1.1
1.0
0.9
0.9
t 0.8
t 0.8
I
1
2
’ Data
(and
66.6
44.8
66.0
55.7
58.3 f 5.1
115.6
87.2
101.4 k 14.2
68.4
57.6
63.0 k 5.4
71.3
62.1
69.4
72.6
68.8 + 2.3
66.6
76.0
93.1
58.2
73.5 * 7.5
58.9
64.0
120.5
66.4
77.4 * 14.4
66.5
65.2
65.8 f 0.6
are mean
4.1
4.5
2.5
6.8
4.5 * 0.9
4.3
2.2
3.2 + 1.0
2.2
3.5
2.8 f 0.7
8.0
4.6
6.0
4.9
5.9 + 0.8
6.3
7.1
3.8
3.8
5.2 f 0.8
5.3
5.4
4.2
3.4
4.6 ?r 0.5
4.6
3.5
4.0 + 0.5
*
+
k
+
1.4
0.3
1.5
2.3
+
*
+
k
+
t
f
k
1.4
1.2
1.6
4.5
4.0
5.0
2.7
4.4
& 3.6
+ 3.0
+ 7.0
f 2.8
1 SE) and range
(7.8
(5.4
(8.9
(29.8
(22.3
(22.6
(17.9
(28.7
(21.1
(20.9
(12.7
(14.4
(5.5 + 1.7
(16.6 + 2.5
(8.1 f 1.9
(5.7 f 1.1
(5.5
(1.2
(6.9
(13.9
39.9 + 4.5
37.3 + 5.3
of number
O-25
o-19
2-17
IO-61
O-62
3-80
4-27
4-47
o-47
o-35
1-31
2-35
O-24
5-33
l-22
1-14
O-20
o-4
O-16
3-31
lo-65
lo-78
per plot.
18)
18)
10)
10)
18)
18)
10)
10)
18)
18)
18)
16)
13)
14)
13)
13)
13)
13)
14)
14)
16
16
i
*
f
-f
0.4
0.7
0.4
0.4
+
*
*
*
+
+
?
*
f
+
f
+
1.8
0.9
1.4
2.1
0.9
1.4
0.5
0.9
0.3
0.4
0.5
0.3
18)
18)
10)
10)
18)
18)
10)
10)
18)
18)
18)
16)
13
14
13
13
13
13
14
14
16)
16)
available;
O-29
o-12
O-13
o-2 1
o-17
O-18
O-16
O-8
O-6
O-6
O-6
o-5
o-5 1
1-33
2-9
l-31
o-5
o-7
o-5
o-5
o-43
o-13
ND = no data
(7.2
(4.0
(3.7
(7.7
(2.7
(5.2
(1.8
(2.6
(1.7
(1.1
(1.8
(0.6
15.2 + 3.9
10.6 + 2.6
5.6 + 0.7
10.6 f 2.6
0.8
2.2
1.1
3.1
(6.2 & 2.6
(4.4 f 1.0
BRUCE A. MENGE ETAL.
262
‘0
F. GRN.
Ab.
-I
G. m.
&!-I!5
O-P
*tP
!s
Y
%
‘“7
G.p.
+H
Jani0
-H
rH
F. RED
4
+H
-H
TURF
+H
-H
Fig. A-2. Analysis of significant statistical interactions between study sites in MANOVA done on
abundance of secondary space occupants prior to initiation of experiments: percent covers were transformed before analysis; ordinate labels were back-transformed to percent cover for easier interpretation;
means indicate untransformed percent cover ofeach species or group on Site 4 = - H + P; Site 1 = + H-P,
Site 2 = -H-P,
Site 6 = + H + P; Ab. = Abietinariu sp. (arborescent hydrozoan); F. GRN. = green
filamentous algae; U.-E. = Vlva-Enteromorpha (green foliose algae); G.m. = Gt@rdiu mitchelliae (brown
foliose alga); G.p. = Gelidium pusilium; Jania = Jania spp.: F. RED = red filamentous algae;
TURF = multispecific turf of foiiose algae.
Constraints
Our experimental design departed from the ideal dictated by purely statistical considerations. Most
departures were imposed by biological characteristics of the system and were thus, we believe, largely
unavoidable, at least in the context of studying the dynamics of the entire community.
Because benthic consumers were highly mobile and more frequent monitoring (e.g. every 2-5 days) was
simply unfeasible (tidal patterns prevented low tide monitoring for periods of 1 to 3 wk per month), we
selected sites with natural barriers (e.g., surge channels, deep crevices, boulder fields) to hinder lateral
reinvasion by slow-mo~ng consumers. P were removed from Site 1, H were removed from Site 4, both P
and H were removed from Site 2, and neither was removed from Site 6. Thus, with respect to slow-moving
consumer manipulations, the plots were not intermingled among sites but were clustered within sites.
Because P, H, and PH removals were each done at one site only, the plots were “pseudoreplicates”
(Hurlbert, 1984). To conform to Hurlbert’s “replicates”, each plot of each treatment should have been
assigned randomly along the shore, and manipulations should have been focused on plots, not sites.
However, manipulations at the level ofthe plot may also have artifacts associated with them, such as dilution
of consumers from nearby controls (Underwood, 1981; Hawkins & Hartnoll, 1983). In fact, this is the
biological constraint that prevented us from scattering plots and treatments at random along the shore.
Mark-recapture studies confirmed that P in particular have large, wandering ambits. Had a P-removal plot
been randomly located near a P-present plot, our removals would have eventually had a strong effect on
non-removals, introducing uncontrolled variation into the design.
Alternatively, replication of the slow-moving consumer treatments could have been done by locating four
additional semi-isolated sites and performing another set of P, H, PH, and control manipulations.
Unfortunately, funding, and thus personnel, limitations eliminated this option. As it was, monitoring the
design we used kept two to four investigators more than fully occupied, and over 11000 person-hours were
devoted to its maintenance.
ORGANIZATION
OF A TROPICAL INTERTIDAL COMMUNITY
263
However, after the initial removals ofslow-moving consumers from the sites, we concentrated subsequent
removals on, and around, each plot. Hence, non-adjacent plots were at least partially independent with
respect to slow-mov~g consumer m~ipulations. Roofs and cages excluding fast-moving cons~ers (SFC,
LF) were placed over locations which were amenable to attachment within each tidal zone; otherwise, these
plots were intermingled within sites.
The experimental design was not orthogonal (Table II), because we could not separate the effects of SFC
from those of LF. Although roofs exclude LF alone, and cages exclude both groups, we could not devise
a practical method of excluding SFC alone. However, subsequent statistical comparisons between
treatments differing only in the presence or absence of SFC gave an indication of the effects of this group
(see Table III).
As in many experimental field studies, relatively few plots per treatment (two to four) were used. Plot
number per treatment was a compromise between the statistical ideal of high replication and several
constraints ofthe system. For example, preliminary studies (in 1974) indicated that photographic monitoring
of the plots would not permit accurate taxonomic identification. We therefore resorted to monitoring plots
directly in tbe field, which was time-consuming, and often hazardous (due to wave surge). Limitations of
personnel availability, and the broad scope of the study also set limits on plot number. Despite these
problems, we have confidence in our results because similar results were obtained in a separate experiment
of similar design (in prep.).
Execution of the experiment
Experiment initiation included (1) identifying surfaces similar in heterogeneity and species composition,
and, for exclosures, amenable to attachment of roofs or cages; (2) quantification ofpre-manipulation species
abundances in each plot; and (3) removal or exclusion of consumers. We did not denude the substratum
prior to initiation of the experiments because open rock surfaces were virtually devoid of sessile organisms
except for algal crusts (Menge 62 Lubchenco, 1981; Lubchenco et al., 1984; Fig. A-l). The effect of aIga1
crusts on colonization was minor as indicated in a later set of experiments of similar design (authors’ unpubl.
data).
Abundances were quantified using flexible vinyl quadrats (0.25 m’) with 100 randomly-plotted dots to
estimate percent cover of sessile organisms, and aluminum frame quadrats to estimate numbers of mobile
and solitary sessile invertebrates. Two categories of space use were distinguished. Primary space occupants
used space on the rock surface, while secondary space occupants were attached to, but grew away from
the surface to a height of 1-3 cm (see Connell, 1970; Dayton, 1971; Menge, 1976; Lubchenco & Menge,
1978; Menge & Lubchenco, 1981 for further details).
Large, rather than more manageable smaller (e.g., 0.1 x 0.1 or 0.2 x 0.2 m) plots were used both because
substratum heterogeneity was high, and abundance of sessile organisms was low (e.g., Lubchenco et al.,
1984) relative to intertidal habitats we had studied elsewhere. We judged that 0.25 m2 plots were the best
compromise between the opposing constraints of including a large surface area, and the practical problems
of attaching, monito~ng, and majnt~ning large exclosures.
Statistical ana(ysis
Hurlbert (1984) recommends against using inferential statistics when the assumption of independence of
sample plots is not met, although this recommendation can be disputed (S. Overton, pers. comm.). Even
when “replication” is “pseudo”, parametric statistics may be used to determine whether or not plots differ,
but cannot be used to infer that the difference is due to the treatments. Moreover, temporal synchrony of
replicates may not be required either, and repetition of an experiment at some other point in time can serve
as a replicate (S. Overton, pers. comm.).
The goals of this study were basically (I) to determine whether or not different consumer groups had an
effect on the structure of the sessile organisms, (2) if so, how large the effect was, and (3) whether or not
the consumers exerted their effects independently of each other. Although inspection and comparison of
the results ofeach treatment without using statistics should provide a partial answer to both of these goals,
detection of interactions (in the statistical sense) among consumer groups using this method would be
exceedingly difftcult. We thus used a combination ofinferential statistics (see below) as a means ofdetecting
such interactions, and graphical examination of results as a guide in interpreting our data. However, we
stress that our conclusions, particularly regarding the interactions among groups, must be regarded as
tentative.
BRUCE
264
A. MENGE
ETAL
As noted in the text, changes in abundances
of prey species (i.e. the dependent variables, Yi) constitute
a multivariate response to variation in consumer deletions (i.e. the independent variables, Xi ). To eliminate
time as a variable (sampling was done at intervals from 1977-80), a regression equation for percent cover
ofeach species (i.e., the response variables,y[abm])
at time t(in months from the beginning oftbe experiment)
was calculated using multiple linear regression:
where y (abm) x t = the percent cover of a species m at time t in plot n (n = 2 or 4) of treatment b (n = 12);
BO = the Y-intercept of the response vector; B 1 = the slope of the response vector; E x t = the error term,
and the remaining terms are used to generate the seasonal (R) and phase (PHI) statistics. Thus, BO and
5 1 are taken directly from the regression equations, while R, the index of seasonal variation in the response
vectors, = ,/(B2’ + B3*), and PHI, the index of change in phase in the response vector, = tan-l (B3/82).
Each index quantifies a distinct aspect of changes in abundance
of sessile prey over time. Differences
among: (1) Y-intercepts (= BO) reflect the magnitude
of short-term
(0 to 6 months) changes in prey
abundance,
(2) slopes (Bl) reflect long-term (6 months to 3.5 yr) changes in prey abundance, (3) seasonal
indices (R) indicate the magnitude of differences in seasonal pattern of abundance,
and (4) phase indices
A.
Y-INTERCEPT
SLOPE
1
ANALYSIS
&
B.
C.
SEASONAL
PHASE
m
0
ANALYSIS
ANALYSIS
-CONSUMERS
-CONSUMERS
i
TIME
i
il
(YR)
CONTROL=
-A-
Fig. A-3. Illustration of hypothetical
sessile organism response vectors. A, Y-intercept and slope analysis:
for species 1, the Y-intercept (EO) would be different from controls but the slope (Bl) would not; for
species 2, both Y-intercept and slope would be different; for species 3, the Y-intercept would not be different,
but the slope would. B, seasonal analysis: the prey species exhibits more strongly seasonal patterns in
experiments (the line labelled - CONSUMERS)
than in controls. C, phase analysis: peak abundance of
seasonally variable species shifts (e.g., from wet to dry season) in the absence of consumers.
(PHI) indicate differences in the phase of seasonal pattern. Examples of the types of prey response
are diagrammed
in Fig. A-3. The general form of the MANOVA model is:
Yi = pi + CtiXi+ /?kXk + dmXm f E
vectors
,
where Yi = the coefficients (BO, B 1, R, or PHI) estimated from the prey response vectors for each plot of
each treatment for each of species i (i = 1 to n); pi = constant, estimated by the overall mean of the Yi;
Xj = the effects of the consumer groups j (j = 1 to 4) with coefficients uj; Xk = the two-way interactions
k (k = 1 to 5) among the consumer groups with coefficients fik; Xm = the three-way interactions
m (m = 1
to 2) among the consumer groups with coefficients 6m; and E = the error term.
ORGANIZATION
For example, the MANOVA
Table III) was:
OF A TROPICAL
equation
INTERTIDAL
for the BO (Y-intercept)
analysis
COMMUNITY
on primary
space occupants
265
(see
Ra,Hi,Sc,CC,Ba,Ch
= CONSTANT + P + H + LF + SFC + P x H + P x LF
+PxSFC+HxLF+HxSFC+PxHxLF+PxHxSFC,
where Ra, Hi, etc. signify the coefftcients (i.e., BO values) for each of the most abundant occupants of primary
space (Ralfsia, Hildenbrandia, Schizothrix, Coralline Crust, Balanus, and Chama), and P, H, LF, etc. indicate
the effects of the consumer groups (main effects, two-way, and three-way interactions).
The CONSTANT and
the coefficients of the consumer groups (i.e., the x and /I values, etc.) are estimated by the MANOVA
analysis. The effects of each consumer group (i.e., the Xi values) and the interactions
(i.e., the Xk, and Xm
values) are incorporated
using indicator variables. That is, + I in the data file indicates that a group was
present, and - 1 indicates that it was absent.
Thus, only four MANOVAs (one each for Y-intercepts, slopes, seasonal patterns, and phase patterns),
rather than 14 (one for each abundant prey species) were necessary. Further, we were able to evaluate five
two-way interactions
and two three-way interactions,
as well as the “main” effects (the four consumer
groups; see above).
Interpretations of results
Interpretations
of the effects of each consumer group were based on both inspection of the average
coefficients (i.e., the BO, Bl, and R values; no phase changes were significant) and the MANOVA analyses.
Prey were included in an analysis only if they were common (i.e., occupied z 5% cover) in all plots in all
treatments.
If MANOVAs
on Y-intercept, slope, or both indicated differences between plots, both the
changes over time and the coefficients (i.e., BO, B I, R, and PHI) were graphed and inspected to determine
what changes had occurred (Fig. A-3). Differences in Y-intercepts indicated that the sessile organism had
increased or decreased in abundance almost immediately after the experiment began. Differences in slope
indicated that the sessile organism had increased or decreased in abundance more gradually. Differences
in the index of seasonal change indicated that the sessile organism had exhibited seasonal fluctuations.
Finally, combinations
of difference in more than one index were also possible.
If the analyses indicated that differences were due to statistical interactions (i.e. the effect depended on
the combination of consumers removed), subsequent analyses were performed to identify which prey groups
or species had changed. Unless the statistical interactions
were significant at P < 0.01 or less, and could
be detected by graphic analysis (Figs. 6-9) they were ignored.
POSSlBlF AR-,ItAC,'SDUE TO EXPERIMENTAL
DEVICES
Potential artifacts of exclosures included direct effects of the devices and indirect effects through
alteration of either the physical environment or the biology of the organisms. Direct effects included either
detrimental or beneficial influences ofthe device on survival. A potential detrimental effect, use ofgalvanized
mesh exclosures for the first 6 months (after which we switched to stainless steel mesh), was done to reduce
the expense of cage loss while attachment
techniques were perfected. Fortunately,
no detrimental effects
of the galvanized cages were observed in low zone experiments.
Potential indirect effects ofexclosures included: enhanced survival ofcolonists due to reduced desiccation
or ultraviolet radiation, positive or negative effects due to sediment accumulation or alteration ofwater flow,
and heightened effects of small consumers due to use of exclosures as shelter from large consumers (e.g.,
Menge, 1976; Menge & Lubchenco, 1981; Dayton & Oliver, 1980; Hulberg & Oliver, 1980; Virnstein, 1978;
Peterson,
1979; Edwards et al., 1982). However, relatively few artifacts of artificial devices have been
detected in studies on rocky shores, particularly in lower zones (e.g., Connell, 1961a,b, 1970; Dayton, 1971;
Menge, 1976; Lubchenco & Menge, 1978; Menge & Lubchenco,
1981; Menge, 1982b).
Because ofthe complexity ofthe food web and the rapid recruitment of mobile invertebrates
in this system
(see below), the usual controls for exclosure effects were ineffective, or were themselves exclosures for some
consumers (see above). We thus used alternative methods of evaluating potential experimental
artifacts.
Merhods
To determine the effects of shade by the mesh in the low zone, we performed shade (SHADE; described
in Menge & Lubchenco,
1981). water evaporation
(EVAPORATION), and exclosure removal/replacement
266
BRUCE A. MENGE ETAL.
(DESICCATION)
experiments. In the SHADEexperiments, colonization of prey under roofs of differing mesh
size was examined. In the EVAPORATION
experiments, we compared water loss rates with and without shade
from the mesh. Preweighed, water-filled vials were placed under roofs and in nearby marked plots (10 vials
per treatment) at Site 2 from 1030to 133531 January, 1979, a typically clear, cloud-free, hot day. The vials
were capped at the conclusion of the experiment and taken to the laboratory where they were reweighed.
In the DESICCATION
experiments, we used plots that were due for termination after being roofed or caged
for 4 yr. We removed cages and roofs for the entire day-time low tide for 5 days during a series of spring
tides. Cages and roofs were replaced just before they were covered by the advancing tide each day. We
compared changes in abundance of sessile organisms in the presence or absence of shade from the mesh
during low tide. Four exclosures in which prey abundances were still high were selected as experimentals
and four as controls (two roofs and two cages each) at Site 2 z 1 yr after intensive monitoring of the
experiments had stopped. Prey covers were estimated 21 January (premanipulation) and 25 January
(postmanipulation), 1981. Sunny, hot, and dry conditions prevailed during this period, and desiccation and
heat stress were presumably high.
Experimental artifacts from roofs and cages appear minimal. First, over an 11 month period in the SHADE
experiments, changes in abundance of sessile organisms under mesh roofs with 2.5 x 2.5 cm (“large”)
openings were not different from those with 1 x 1 cm (“standard”) openings (for details, see Menge &
Lubchenco, 1981). Second, in the EVAPORATIONstudy, the rate of water evaporation under mesh
(X f. 1 SE = 3.6 + 0.2%; initial volume = 26 ml/vial) was lower than the rate away from mesh (5.1 rl: l.O%),
but the difference was not significant (one-way ANOVA; F= 1.97, 1,18 d.f., P > 0.1). Third, in the
DESICCATIONstudy, cover of the major space-occupying groups (coralline crust, fleshy crust, foliose
corallines, fohose fleshy algae, hydroids, sponges, barnacles, oysters, mussels, dead coralline crust, and dead
foliose coralline algae) did not differ in control and experimental plots (one-way ANOVAs with Bonferroni
correction, P > 0.05). These results thus suggest that mesh-induced artifacts are minor; however, with the
exception of the SHADEexperiment, these short-term experiments are unlikely to detect sublethal effects.
Further investigation of the ecological effects of physical stress in this habitat would be rewarding (see, e.g.,
Garrity, 1984).
As in most such studies, experimental removals and exclusions of consumers resulted in major reductions,
but not total elimination of the organisms (e.g.. Table A-l). Substantial numbers of recruits of P and H were
often found in exclosure plots (Table A-l). However, since most invaders were small (< 1.0 cm in width),
and since the plots and sites were intensively maintained, the impact of these consumers was minimized.
Although very small crabs and fishes were able to enter cages, we were not focusing on the effect of
microconsumers, but rather on those of macroconsumers.
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