varied carnivore effects and the prevalence of intertidal algal turfs

.I. E,YI~. MUV. Viol. Kcol., 166 (1993) 65-91 0 1993 Elscvier Science Publishers BV. All rights reserved 0022498 1~93/$06.00

JEMBE 01894

Varied carnivore effects and the prevalence of intertidal algal turfs

Carlos Robles and Jack Robb

(Received 6 January 1992; revision received 11 August 1992: accepted 3 I August 1992)

Abstract: A red algal turf covers mid-shore levels of much of the California Channel Islands. Our expcrimenta at Santa Catalina Island show that carnivores maintain the turf by consumingjuvenile mussels ,W~~tihr.c

spp. and associated invertebrates. Exclusion of spiny lobsters Punulirza inrerruptuy (Randall) from compar-

atively wave-cxposcd sites caused the complete and persistent replacement of the turf by the mussel asscm- blagc. On sites protected from wave action, the lobsters were joined by carnivorous fishes, i.c., Hrdichorw

.\emi.sinctu.c (Ayrcs). Ox~$dis crrhfbrnica (Gunther) and Srmico.r.~~phu.v pulcher (Ayrcs), and whelks, i.e..

Ccrcrro.rr~ma nr~tftrlli (Conrad) and MuxwrNiu ~emmrr (Sowcrby). Compensatory foraging shifts by the whelks prevented significant increases of mussels in lobster and fish cxclosures. Exclusion of all predators at the protected site caused a moderate but statistically significant increase. Thus. experiments at different sites indicated either “kcystonc” or “diffuse” effects of predators.

Experimental clumps of large Mj~tilir.~ ccrlifkwionus (Conrad) persisted longer after rc-exposure to predation in the post-experimental periods than did clumps of smaller M. c&vrkurus or M. rdu/i.v L. Transplants of matched cohorts indicated that the size differences of mussels in the exclosure experiments wcrc caused

by diffcrcnccs in shell growth rates correlated with wave exposure. We speculate that changing growth rates may inHuencc the outcome of size-limited predation, accounting for some of the variation in the rclattvc abundance of turf and mussels over the wave exposure gradient.

Key words: Algal turf; Corallim~; Growth; Haemurop~r.~; Indirect effect; Intertidal zone; Kcystonc predator:

Labrid; ~Mrril~rs; Panulirus: Sire-limited predation: Whelk

After > 3 decades of field experiments (reviews in Sih et al., 1985; Menge & Far-

rell, 1989) it is clear that predation often molds the structure of benthic communities.

Yet, for many benthic communities, the effects of specific predators remain obscure.

Below, we examine two contrasting depictions of predator effects, the “keystone” and

“diffuse” predation hypotheses, in a rocky intertidal community.

We recognize a keystone predator by a consequence of its removal: marked shifts

in relative abundance at lower trophic levels, including the replacement of dominant

species (Paine, 1966, 1969, 1974, 1980). For example, urchin barrens apparently rc-

Correspondence address: C. Robles, Department of Biology. California State University. Los Angclcs, CA 90032, USA.

Contribution 143 to the publications of the University of Southern California Catalina Marine Science Ccntcr.

66 C. ROBLES AND J. ROBB

placed kelp beds following otter removals from shallow subtidal communities (c.g.,

Estes & Palmisano, 1974; Dayton, 1975; Simenstad et al., 1978; Duggins, 1980).

Mussel beds replaced perennial algae following sea star removals from rocky shores

(e.g., Paine, 1966, 1974). Both the original dominant species and their replacements

may harbor diverse “associated species” (e.g., Suchanek, 1979; Tsuchiya & Nishihira,

1986; Dean & Connell, 1987). The patterns of species interactions differ between the

pre- and postremoval assemblages because: (1) some species exist in only one assem-

blage; and (2) species shared by the assemblages may play different roles within each.

Thus, a transformation of community structure attends the change of dominants, even

though the alternative assemblages may share some species.

The concerted effects of several predator species, which we term “diffuse” predation,

is revealed by a different experimental design and outcome. The field experiments arc

compound removals, in which the different members of the predator fauna are removed

both separately and in combination (e.g., Peterson, 1979; Menge & Lubchenco, 198 1;

Lubchenco et al., 1984; Menge et al., 1986). Predator effects may show no interaction

between different treatments or they may interact. In the former, the probability of the

prey falling to one predator species does not depend on the presence or absence of a

second. With interaction, the probability of the prey falling to one predator species does

depend on whether others are removed (see Wilbur & Fauth, 1990, for the statistical

treatment of interaction among predator effects). Menge and Lubchenco (1981) present

an apparent case of interaction wherein significant increases in prey required the re-

moval of all or nearly all predator species. One explanation for such effects is the

compensatory foraging shifts hypothesis: after removal of one, the remaining predators

respond numerically (sensu Helling, 1959) and drive the prey’s densities towards

premanipulation levels. An increase in the proportion of that prey species in the diets

of the remaining predators also might be observed. However, no data exist confirm-

ing aggregation or diet shifts of unmanipulated predators.

Whether interactive or not, diffuse predation differs from keystone predation because

the removal of any one predator produces comparatively small changes in the abun-

dance of dominant prey and associated species (e.g., Menge & Lubchenco, 1981).

WC investigated predation on the M. cnlifornhnus assemblage in a community set-

ting very different from the original account of keystone predation (Paine. 1966, 1974).

The alternative to the mussel bed assemblage is a red algal turf that forms an unbro-

ken sward across much of the mid-shore levels of the California Channel Islands. The

turf was thought to owe its prevalence to tolerance of physical stresses and weak bi-

otic interactions, i.e., moderate browsing by fishes (Littler & Littler, 1980; Hay, 1981;

Stewart, 1982). Indirect effects of predators (sensu Kerfoot, 1987) had not been stud-

ied.

The predators included spiny lobster Punulirus interruptus (Randall) labrid fishes, i.e.,

Hnlichoeres semisinctus (Ayrcs), O.xyjulis calcjbrnica (Gunther), and Semicossyphus pul-

cher (Ayres), and whelks, i.e., Cerutostoma nuttalli (Conrad), and Maxwelliu gemnul

(Sowerby). Depending on differences in the abundance of predators among sites,

https://www.researchgate.net/publication/230693484_iThe_Odonata_of_Canada_and_Alaska_Volume_Two_by_Edmund_M_Walker_Professor_Emeritus_of_Zoology_University_of_Toronto_Honorary_Curator_of_Zoology_Royal_Ontario_Museum_of_Zoology_and_Palaeontology_xi_318?el=1_x_8&enrichId=rgreq-6fa1a265-8f7c-482f-9254-ff3cc1010c91&enrichSource=Y292ZXJQYWdlOzIyMjQ2MzY5NDtBUzoxMDMxNDkyMDEyNjQ2NTVAMTQwMTYwNDA5NTAzMA==

CARNIVORE EFFECTS 67

lobster exclusion alone or compound removal experiments were done. For the latter,

we collected data on compensatory foraging shifts and diffuse effects.

Earlier, C. Robles (1987; Robles et al., 1990) demonstrated that the lobster’s rapid

movement and short prey handling times denied mussels an upper intertidal spatial

refuge, such as that described for the sea star-mussel interaction (Paine, 1966, 1974).

Lobster exclusion increased the relative abundances of Mytilus spp. in the understory

of high intertidal beds of fucoid algae (Robles, 1987). Among the results we now re-

port is the complete and persistent replacement of a major vegetal formation, the algal

turf, in lobster exclosures below the zone of the fucoid algae.

METHODS

NATURAL HISTORY

We studied rocky shores near the Catalina Marine Science Center, Santa Catalina

Island (33’ 25’ N, 118’ 30’ W). Mean monthly surface temperatures varied from 14 ‘C

in January to 20.5 “C in September. The tidal excursion ranged from -0.7 to + 2.2 m

mean lower low water (MLLW).

In our initial Catalina observations and prior studies of temperate zone littoral

mussel predators (e.g., Menge, 1976, 1983; Peterson, 1979; Robles et al., 1989) rela-

tive abundances varied markedly across gradients of wave exposure. Therefore, we

chose three sites to span the range of wave exposures over which the algal turf occurred.

The protected site was a horizontal bench 0.5 m above MLLW on the southern side

of Big Fisherman’s Cove (Fig. 1). This site was protected from wave action by the walls

of the cove, a submerged reef, and a rocky islet (Bird Rock) ~0.75 km to the wind-

ward. The semiprotected and exposed sites were near the leeward and windward ends

of the islet. The semiprotected site was a horizontal bench 0.7 m above MLLW rc-

ceiving swells that refracted around the island. The exposed site was a similar platform

0.9 m above MLLW that received the full force of prevailing northwesterly swells.

The turf covers mid-shore levels (= 0.1 to + 1.0 m MLLW) of the islands from

sheltered covers to all but the most wave-exposed promontories (Emerson & Zelder.

1978; Murray & Littler, 1978; Murray et al., 1980; Thorn & Widdowson, 1980; Stewart,

1982). Only 1-3 cm thick, the turf consists of the branching thalli of the anchor spe-

cies, principally Corullina ojficinalis L., entwined with epiphytes, predominantly Gigrrr-

tinu canaliculrrtn (Harvey), Laurencia pacifica (Kylan), and Gelidium coulteri (Harvey).

The relative abundance of species in the turf varies seasonally, the epiphytes increas-

ing in summer (Murray & Littler, 1978; Stewart, 1982).

Invertebrates were present underneath or in gaps in the turf. These included barna-

cles, Tetruclitcr squamosa var. rubescens (Darwin); jewel box oysters Pseudochnma e.x--

og)wz (Conrad); and sessile tubiculous gastropods, Aletes squumigerus (Carpenter).

Three species of mussels occurred in the turf: Mytilus californianus, M. edulis and

Brcrchidontes czdumsianus (Dunker). [MacDonald & Koehn (1988) provide electro-

6X C. ROBLES AND J. ROBB

Exposed Site

Semi Protected Site

ISTHMUS REEF

Fig. 1. Location of study sites. Contour lines for 2 and 5 m below MLLkV.

phorctic data suggesting that the southern California form ofM. edulis is in fact ~4, ,$-

Ioprowk’ulis (Lamarck).] The M_~jtilus spp. recruit in densities sometimes exceeding

10000 m-‘, but few survive to reproductive sizes (2-3 cm long; Suchanek, 198.5; C.

Robles, pers. obs.). ~rae~~d~nte.~ is a small mussel (adults t3 cm long at Catalina).

Though numerous, it habitually nestles in crevices and does not form mussel beds

(Robles, 1987).

The predators included both resident predators, which remain within the intertidal

zone at all times, and transient predators, whose presence in the intertidal zone depends

on tidal, daylight, or migratory cycles. The resident predators were whelks, Cerf~rff.~~#r~~ff


~~utt~lli and ~a,~~el~ia gemmu. The transient predators were diurnal fishes in the La-

bridae, Haiichoeres sernisimtus, O.x_@dis culjbrniea, and Semicus.yvphus p&her; a bird,

the black oystercatcher, Haematopus bathmani Audubon, and P. interruptus. The vulnerability of mussels to different predators depends on their species and size.

Whelks, crabs, and lobsters prefer M. edulis to M. cal$mkwus @Larger, 1967. 1972;

C. Robles, pet-s. obs.). In laboratory feeding trials (Robles et al., 1990; C. Rob&

unpubl. data), the largest M. edulis occurring on Catalina (7 cm) were readily eaten by

all lobsters, even small subadults; whereas M. cal~fkziunus > 6 cm were invutnerable

to lobsters < 9.5 cm carapace length, z 80”; of those foraging intertidally. Gape limits

of the labrid fishes restrict their feeding to mussels <4 cm. H. b~~h~~~~zj, the black

oystercatcher. eat both ~~~j/M.~ spp, and can kill M. ~~l~i~~~?~~~~?u~ > 9 cm (Hartwick,

1976; this study).

OBSERVATIONAL METHODS

The apparent differences in wave action were confirmed by divers, who estimated

bottom velocities during high tide surveys of lobster abundance (see below). They timed

the oscillatory drift of neutrally buoyant spheres (perforated ping pong balls) or flot-

sam over grids painted on the sLlbstratun1. A grid was located on the protected site,

the s~miprotected site, and z 30 IX to the lee of the exposed site. The latter placement

and our un~~illingness to sample high wave action (8 m was the largest horizontal

displacement endured in the dive surveys) provided an underestimate of mean bottom

velocity of the exposed site. The velocities lo-40 cm above the substratum were esti-

mated on 21 nights in spring-summer 1986. The divers also noted horizontal displace-

ment (no period was estimated) in the middle of the cove and islet transects in all

seasons 1982-87.

Predator nbur~dunce and diet

Densities of whelks at the protected site were estimated by counting their numbers

in 50 9#0-cm’ square quadrats running c~~ntiguously along the mid-level of the turf

zone. Similar censuses were not done on the islet because years of close scrutiny of

the turf had failed to reveal a single whelk.

Divers using either snorkel or scuba estimated the densities of the labrid fishes, i.e.

S. pulr’her, H. .semisinctus, and 0. calijk-r&a, by swimming along permanently marked

20-m belt transects on the midline of the turf zone. Surveys were made on tides cov-

ering the turf by at least 1 m and falling between sunrise and sunset; the latter restriction

w’as imposed because the fishes are diurnal (Hobson et al., 198 1). The transects at the

protected site spanned the experimental area. On the islet, the 60 m of transects fell

midway between the semiprotected and the exposed site, with either end of the transect

line 30-40 m away from the two experimental areas. Lobster densities were estimated


by swimming transects during nocturnal high tides (within 1 h of predicted tides

> + 1.3 m MLLW, at least 1 h after sunset and 1 h before sunrise). Details of whelk,

fish, and lobster surveys appeared in Robles (1987).

Avian mussel predators (Marsh, 1986) were never observed at the protected site.

However, a pair of black oystercatchers used the islet as a nest site from April to August

each year. We estimated the foraging effort devoted to the turf zone by making repeated

spot checks of the birds’ location and activity. At all times of day and phases of the

tides, we motored along the shore of the islet in a small skiff. Once the birds were

sighted, their behavior and position relative to the turf zone were recorded. We used

this spotting method because the birds changed position and activity when people were

on the islet. z 100 surveys were made from 1985 to 1990. Here, we report data taken

when the turf zone was accessible to the birds (water level < + 0.6 m MLLW).

The apparent diets of whelks, fishes, and lobsters at the protected site were reported

previously (Robles, 1987). For comparison, we made additional collections of lobsters

from the turf zone of the islet. We also directly observed oystercatcher kills during some

of the spotting surveys, collecting the shells to measure sizes and confirm initial iden-

tifications.

EXPERIMENTAL METHODS

Experiments at the protected site

The predator abundance and diet surveys indicated that whelks, fishes, and lobsters

killed mussels at the protected site. Here, we excluded transient predators (lobsters and

fishes), either separately, or in combination with the whelks, in two successive exper-

iments.

The first experiment tested whether the transient predators limited the survival of

mussel recruits over a broad stretch of turf while predation by whelks was greatly re-

duced (Table I). Fishes and lobsters were excluded from plots with large mesh cages.

Hardware cloth with square openings of 2.5 cm (89”; open area) was bent into dome-

shaped cages ~20 cm high and 35 cm long, coated with a saltwater-resistant epoxy,

and nailed to the sandstone substratum. To control for possible artifacts caused by the

wire mesh, each cage exclosure was matched with a similarly prepared open-ended

cage, which admitted lobsters and fishes (Robles, 1987) and an open plot, with no mesh

(Fig. 2). The locations of treatments and control plots of three replicates were assigned

randomly along a 30-m strip of turf. Since the whelks could pass through the large

mesh, we removed them from the site by hand at monthly or shorter intervals. Initial

removals yielded hundreds of whelks, but after 10 months, near the end of the exper-

iment, 1 h of searching the site (E 100 m2) yielded only four.

The second experiment at the protected site tested whether the whelks could limit

the survival of mussel recruits in the absence of the transient predators, and if so,

whether this regulation could be explained by compensatory foraging shifts, i.e., the


TABLE I

Summary of experimental design

Experiment Date (month/year) Manipulation Predators cxcludcd

First protected

Second protected

12182 to 1 l/83

04186 to 12i86

Manual removals of cc helks

from bench Open plots Large mesh arch

Large mesh cage

Open plots Large mesh arch

Large mesh cage Small mesh arch Small mesh cage

Semiprotected 04186 to 02/87 Open plots None Large mesh arch None Large mesh cage Lobsters

Exposed OS/S5 to 03:‘86 Open plots Large mesh arch Large mesh cage

None None Lobsters

Whelks

Whelks Whelks, lobsters and fishes

None None Lobsters and fishes Lobsters and fishes

Lobsters, fishes and whelks

Ftp. 2. A replicate in the large mesh exclosure experiments. From left to right: arch control, open plot control. and cage treatment.

I? C. ROBLES AND J. ROBB

whelks aggregating in the transient predator exclosures. To do this, we used large and

small mesh cages to exclude transient predators either separately or in combination

with the whelks. Five different treatments were randomly assigned to turf plots and

replicated six times. The treatments were: (I) a small mesh cage, excluding both whelks

and the transient predators: (2) a small mesh arch, excluding only the transient prcd-

ators; (3) a large mesh cage, again excluding only the transient predators; (4) a large

mesh arch. accessible to all predators; and (5) an open plot, also accessible to ail

predators (Table I).

The small mesh exclosures were A-frame cages, 20 cm high, 25 cm wide at the base,

fashioned from hardware cloth of 1.2-cm” openings, and supported by a 0.5cm steel

rod running up the center of either end and along the peak. The ends of the rod were

set in concrete in l-cm diameter holes drilled in the rock. The stnall mesh arches were

similar in every way, except that a strip of the wire cloth was removed from the base

of the end panels to provide 2 cm clearance for the whelks. The small mesh cages were

not perfect cxclosures; occasionally a few whelks, small enough to fit through the mesh,

cntcrcd and consumed mussels. They were removed at regular intervals with long

forceps. Thus, the small mesh cages were most similar to the large mesh treatment in

the whelk manual removal experiment, testing the effect of transient predators when

whelk predation was reduced, but not eliminated.

The experiment used the entire turf zone of the protected site. The six replicates wcrc

arranged in two groups, three replicates along the shoreline of the first (whelk manual

removal) experiment, and three along the shore not subject to removals.

To test for compensatory foraging shifts, biweekly records of the experimental whelk

densities were analyzed using a multivariate general linear model of repeated measures

ANOVA (software: SYSTRT, Evanston, Illinois). The model contained two main,

between-subject, effects: treatment group (cage assignment) and location (previous

whelk manual removal or nonremoval shorelines). The variation among census dates

was partitioned as the within-subject effect, i.e., the repeated measure. Post hoc con-

trasts were used to determine which treatment groups differed significantly on specific

survey dates. If the whelks did respond numerically to increases in mussel abundances

resulting from the removal of lobsters and fishes, then their densities would increase

significantly in the large cage and small arch plots, but not in the large mesh arch plots

or open plots. Significant increases in the per cent cover of mussels would occur only

in the small cage treatment (excluding all predators). The comparisons between large

arch and open plots, and between small arch and large cage, tested for artifacts of wire

mesh, because the effects on predators were equivalent, but the cover of wire differed

within each pair.

E.qwriments at semiprotected and exposed sites

The predator abundance and diet surveys showed that lobsters were the primary

mussel predator on the isfet sites (see Results). Therefore, large mesh cages were


sufficient to stop predation. Three replicates were arranged on the turf of the semipro-

tccted site. The exclosures remained in place from 4 April 1986 until 28 February 1987.

when winter storms removed one of the exclosures (Table I).

From 1983-84, turf completely covered the most wave-exposed site. In May 198.5,

this site showed a heavy set of Myrilus spp.. Mussels covered 67”~” of the turf, reach-

ing maximum lengths of 3 cm. We installed three replicates of each treatment of the

large mesh exclosure experiment on 23 June 1985 and left them in place for 4 wk. On

22 July 1985, we detached the cages, recorded the results, and then reattached the cages

(Table I).

All experiments were concluded by removing the cages and visually estimating the

per cent covers of algae and invertebrates. We verified the accuracy of our visual per

cent cover estimates by comparing them with a conventional technique employing point

sampling of color transparencies (e.g., Cubit, 1984). Estimates of mean per cent cov-

ers differed between the two methods by < 5 “/, . For the first protected site and the

exposed site experiments we also scraped up and preserved for microscopic examina-

tion the cover of a 230-cm’ quadrat from the center of each experimental plot. These

samples provided densities and shell lengths for the mussels and herbivorous mollusks.

The scraping destroyed less than half of the substratum under the cages, allowing the

intact portion to be observed after the conclusion of an experiment. Notes were kept

on the cover and sizes of experimental mussels in the post experimental period. i.e..

after cages were removed, re-exposing the plots to predators.

The variances of per cent cover estimates were found to be “0” for some experimental

groups, and thus, heteroscedasticity and the differences among the means could not

be tested using F ratios. Kruskal-Wallis tests were applied to mean mussel covers of

all the groups in an experiment, and when these proved significant, Mann-Whitney C’

tests were used to compare covers on open plots with each of the other experimental

groups (Sokal & Rohlf, 1981). For the second protected site experiment (Table I),

which required four of the latter tests, a procedure-wise error rate of 5’:” was main-

tained using Bonferroni’s procedure (Sokal & Rohlf, 1981).

With one exception, original or square root-transformed densities were homosce-

dastic. The differences in means were tested with ANOVA, and statistically similar

means were grouped using Tukey’s HSD tests (Sokal & Rohlf, 1981). The exception

was sample variances of mussels > 1 cm, which on control plots often were at or near

zero, requiring Kruskal-Wallis tests.

RESULTS

WATERMOTION

The mean velocity estimates differed more than three-fold between protected and

exposed sites (Fig. 3). Significant swell heights increased in the vicinity of Santa Cat-

C. ROBLES AND J. ROBB

35 I

30 -

0 protected site semi-protected exposed site

Fig. 3. Mean bottom velocities and 1 SE near experimental sites. Each site was observed withm I h of the predicted high tide on 21 nights in spring-summer 1986.

alina Island from spring-summer to fall-winter (Seymore, 1984-87). In the cove, mean

horizontal displacement increased 11 Y/l> between seasons. and at the islet a minimum

of 56”,.

PREDATOR ABUNDANCE AND DIET

Predator abundances differed markedly between the protected cove and the islet. In

the former, avian mussel predators were absent, but whelks, fishes, and lobsters for-

aged on the turf year-round (Table II). Peak abundances of lobsters occurred in

spring-summer (Table II). This pattern probably arose from seasonal shifts in the die1

phasing of the tides. Extreme high tides occur during daylight hours in fall-winter, but

change to the night in spring-summer, thus favouring spring-summer foraging by the

nocturnal lobsters. The changes in lobster abundance were also possibly affected by

seasonal bathymetric migrations undertaken by a portion of the population (Mitchell

et al., 1969).

Whelks and labrid fishes were absent or rare on the islet (Table II). The pair of black

oystercatchers, though sometimes present, seldom foraged on the islet during late fall

through winter. They devoted most of their foraging to the mussel beds on the wind-

ward and leeward extremities of the islet (Table II, Fig. 4). ~20”~ of the sightings of

foraging occurred on the turf, even though turf covered >80”, of the horizontal

substratum at midshore levels. Lobster abundances varied seasonally. They occurred

in 82’i,, of the spring-summer nocturnal high tide surveys vs. 141; of the fall-winter

surveys. The few lobsters occurring in the latter period were seen only in October-


TABLE II

Densities of mussel predators in the turf zone of the cove (protected) and the islet (semi-exposed and ex-

posed). Mean number f 1 SD,m ~’ are tabulated by location and season (s/s, spring-summer; f/w, fall-

winter). Number of surveys (N) and number of samples.survey. ’ (n) between parentheses.

Cerurostoma

cove b,‘S 2.1 f 4.7 (2!50) 2.3 i 4.1 (2/50) 0.046 2 0.330 (25.6) $‘\v 4.4 * 7. I (2!‘50) 1.3 k 2.5 (2.‘50) 0.028 + 0.360 (I 5 6)

lslct S/S 0.040 + 0.044 ( 19.6) 1.; w 0.001 t 0.003 (14’6)

cow $5 0.010+0.021 (17:3) 0.047 f 0.061 (7:3) 0.025 k 0.045 (7.3) S’\h 0.010 0.020 2 (23,/3) 0.053 f 0.077 (7/3) 0.000 t 0.000 (7:3)

Islet GS 0.000 2 0.000 (5;3) 0.002 + 0.005 (3:‘3) 0.006 &0.012(3.3) r;vv 0.001 0.003 + (20,‘3) 0.008 i 0.014 (7:3) 0.000 k 0.000 (7 3)

COW Islet \‘b s,‘s 4.8 x 10 J+9.8x 10 1 (23:‘l) I“\\ s’u 1.3 x 10 ‘i4.l x IO 1 (22,‘l)

70 i

b 30 -

5 20-

2 a lo

:

Mussel beds Surf Grass Turf

m Spring/summer m Fall/winter

Fig. 4. Frequency of black oystercatcher foraging on different intertidal substrates of the islet. Percent of total sightings of foraging birds are graphed by season and substratum type.

16 C. ROBLES .AND J. ROBB

November. Nevertheless, lobsters were by far the most abundant large predator on the

islet. reaching mean densities on the turf transects of 0.17.m-’ on single evenings in

spring-summer. Taking into consideration the frequency of feeding individuals within

total densities (100 vs. 7856, respectively, for lobsters and the black oystercatchers),

foraging lobsters were at least 100-fold more abundant than foraging birds on the turf

in spring-summer.

,411 predators ate A4~~ilus spp., and all but the whelks ate the associated herbivores:

limpets, chitons, and grapsid crabs (Robles, 1987; this study; see U’inget, 1968, for

discussion of lobster diets). Mussel shell fragments in the gut were found more frc-

qucntly and in greater volume in the lobsters than the labrid fishes from the protected

site (Roblcs, 1987). Of 25 lobsters collected on six occasions from the turf of the islet,

100°O contained Mytilus spp., 489, Bmchidontes. Afvtilus spp. also constituted by far

the largest proportion of recognizable fragments in the cardiac stomachs, though shells

of herbivorous gastropods were also found.

Of 57 kills observed during 18 black oystercatcher spotting surveys, 35”,, were

M. cal~j~wr~imus, 9’1, M. rdulis, 34”,, limpets, and 22O, coiled gastropods (A.Ptrcreu sp.,

Norrisiu sp., and Tegukz spp.). The birds killed M. cnlifbrnimus l-9 cm (mean length

5.2 cm). Small (< 3 cm) M. cul$minnus constituted < 5 “<, of the total mussel kills.

24.

Mean No. Mytilus per 100 cm2

Fig. 5. Proportion of mussels in the apparent diet of whelks. Dietary records were selected for periods within I month of one of four dates of mussel density surveys. The later were chosen to show the extreme temporal variation in MJ~U.T spp. abundance. Graphs are arranged by increasing density of musscls. Solid bar, .M. rdulis; fine hatch, M. cul$mianu.v; diag. hatch, Brcrchidonres sp.; clear, the barnacle, Trtruclircr sp.; and

coarse hatch, other prey.


To determine whether the whelks’ diet changed with the abundance of Mytilus spp.,

as expected under the compensatory foraging shifts hypothesis, we compared the

proportions of Myrilus spp. in the apparent diets at times of different mussel abun-

dances in the turf. The abundances of small mussels had been estimated by micro-

scopically examining samples of turf (details in Robles, 1987). When Mytilus spp.

abundances were high, they comprised the largest proportion in the diet; when low,

barnacles were the greatest proportion (Fig. 5).

EXPERIMENTS AT THE PROTECTED SITE

In the first experiment at the protected site (whelk manual removal, Table I), mean

total densities of M. edulis were significantly greater for the exclosures than the arch

controls (Table III). Total densities for the open controls were intermediate and did

not differ significantly from either the arch or exclosure means. Bruchidontes showed

similar, but nonsignificant, trends (Table III). The nonsignificant tendency for total

densities to be lower in the arch than open controls suggests that the wire mesh de-

pressed the numbers of small mussels, possibly by interfering with settlement. If so, then

the test for effects of predation would be conservative, because mussel recruitment

should be similarly depressed in the exclosures. Whelk aggregation under the mesh to

avoid desiccation stress would not have been a factor because after the initial removals

whelks were only found at the periphery of the site. Total densities of M. cal~fortzimus

increased slightly, though significantly, in exclosures relative to both the arch and open

controls.

Densities of mussels > 1 cm were uniformly low in both open and arch plots, and

significantly higher in the exclosures (Table III). The differences were significant for

TABLE III

Mean numbers f 1 SD of mussels.230-cm’ sample- ’ in the first protected site experiment (whelk manual removals) are tabulated with respect to experimental conditions and shell length. P values of ANOVA fo- low 4 values. The df values in the ANOVAs were 2 and 6, respectively. for effects of treatment and error. Tukey’s HSD tests (Sokal& Rohlf, 1981) were used to distinguish significant from nonsignificant differcncea

(underlined). Comparisons with SD values of 0 were tested with Kruskal-Wallis tests, and Y values were not grouped. The df values for these tests were 2.

Species Open Arch Cage P value

M. rduh

Total density Density > I cm

31.00~4.58 17.00 t 10.82 83.33 k 40.77* 0.028 0.00 & 0.00 0.00 + 0.00 33.33 i 6.69 0.022

.M. cul~fimiarzus

Total density Density > 1 cm

Bruchidontes

Total density Dcnsitj > 1 cm

0.33 + 0.58 0.33 & 0.58 4.67 + 1.53 0.003 0.00 i_ 0.00 0.00 & 0.00 2.00 f 2.00 0.105

256.00 f 46.03 178.67 + 82.72 447.672 157.91 0.05 1 5.33 & 1.53 8.00 2 1.73 52.00 5 3.61 i 0.000

* P value for Tukey’s HSD comparison of 7 values of open and caged plots = 0.1 I.


M. edulis and Bruchidontes, but not for M. californianus. Mussels begin to protrude

above the surface of the turf as they grow to 2 1 cm, presumably exposing themselves

to greater predation.

The Mjltilus spp. in exclosures overgrew the turf, causing moderate, but statistically

significant increases in their per cent cover (Fig. 6A). The arch and open controls

maintained unbroken covers of turf. These results demonstrate that the lobsters and

fishes were capable of extirpating mussel recruitment over a broad area (100 m’) even

while whelk predation was greatly reduced.

MYTILUS

FLESHY CORALLINE

MY-rlLUS

FLESHY CORALLINE

WfrlLUS

FLESHY CORALLINE

FLESHY CORALLINE

OPEN 0 LARGE CAGE 0 SMALL CAGE 0

LARGE ARCH A SMALL ARCH a

Fig. 6. Triangular coordinate plots of the relative proportions of the cover of coralline algal matrix. flesh! cpiphytes, and the M~~filus assemblage. Together these categories comprised > 90”,, of the mean total coc- crs of all experimental plots, with the exception of the second protected site experiment. as explained in Results. Positlon of the symbols within the triangles represents the mean relative proportions of the three types of cover. Thus, symbols falling on the base line of the triangle have no mussel cover. but differing

proportions of epiphytes to coralline algal matrix. Symbols at the center of the ficld represent approximate11 cqual mean amounts of all three covers. Symbols near the apex of the triangle represent covers approach- ing IOO”,, M,ri/us assemblage. Different symbol shapes represent different treatment groups. as indicated. Shading distinguishes means of experimental groups that differed significantly from those of the open control plots in the Mann-Whitney U tests. Diagrams A-D are results for first protected site, second protected

site, semiprotected site, and exposed site experiments, respectively.


0 50 100 150 200

Days

Fig. 7. Plot of the mean abundances of whelks in different treatment plots of the second protected site CK-

periment. T, mean of data pooled from small arch and large cage trcatmcnts; C, mean of data pooled from large arch and open controls. Asterisks denote dates that the mean of treatments (T) differs signiticantl! from

the mean of controls (C; x= 0.05). 93”, of the whelks observed were C. rnmalli.

In the second experiment at the protected site (small and large mesh cages; Table

I), densities of whelks in the absence of transient predators (large mesh cage or small

mesh arch) were higher than in the control plots (large mesh arch or open plots, Fig. 7).

Repeated measures ANOVA yielded significant treatment effects (Table IV). In post

hoc contrasts of adjacent curves for single treatments in Fig. 7, only the large mesh

cage,‘large mesh arch comparison differed significantly. Since the differences among the

curves are transitive, transient predator exclosure curves (small mesh arch and large

mesh cage) do not differ significantly from one another, nor do the control curves (large

mesh arch and open). Pooled whelk densities for transient predator removals (means

of small mesh arch and large cage, the T curve in Fig. 7) and controls (means of large

TABLE IV

Repeated measures ANOVA of whelk densities in the second protected site experiment (small and large mesh cages). The upper table presents results for the effect of treatments, location (area previously used for the whelk removals or a nonremoval arca) and the interaction of treatment and location. The lower table prc-

sents results for the effect of time (repeated measures) and its interaction with the previous variables.

Source Sum of squares df Mean Square F ratio 1’ value

Trcatmcnt 52.50 3 17.50 4.47 Location 60.00 I 60.00 15.32 Interaction 12.23 3 4.08 1.04 Error 62.61 16 3.92

Time 21.25 9 3.03 1.70 Time x Treatment 45.92 21 1.70 0.95 Time x Location 12.75 9 1.42 0.80 Time x Treatment x Location 56.02 27 2.08 1.16 Error 256.67 144 1.78

0.0 I8

0.001 0.4OI

0.091

0.535

0.622 0.279


TABLEV

Mean per cent covers _t 1 SD of bare rock, undcrstorey invertebrates exposed with the decline of turf oovcr, and the turf in the second protected site experiment. P values for ANOVA of the differences in means among

treatment groups are also tabulated.

Treatment Bare rock Invertebrates TurS

Small cage Small arch

tar&x cage Large arch Open

P \altlc

19.50j 14.24 30.50+21.74 37.50 i_ 12.97 33.67 + 16.53 16.17 + 17.36 ah.33 _i 27.44

19.17i_5.81 11.50~21.69 52.SO + 12.07 20.00 + 8.65 16.17+22.19 63.33 + 77. IJ 30.50 & 13.25 IX.83 & 16.53 SO.67 * 10.75

0.140 0.437 0.313

mesh arch and open plots, the C curve in Fig. 7) differed signi~cantIy on five occasions.

Thus, whether grouping by the cage designs (single treatment curves) or by their effect

on transient predators (T and C curves) the results confirm that the whelks aggregated

in the transient predator exclosures.

The repeated measures ANOVA also revealed a significant location effect (Table IV).

Whelk densities were lower in the area used in the previous experiment for the whelk

manual removal, which would be expected if the whelk population had not fully re-

covered. Variation associated with sampling date followed a nonsignificant trend (Table

IV, P = 0.09).

Unlike the other experiments, in which the rock surfaces were never uncovered, the

thickness and cover of the turf assemblage declined in all plots, exposing either bare

rock or invertebrates, principally ~r~c~i~o~te~, barnacles (Tetr~clit~), and jewel box

oysters (Pseudoch~ma; Table V). Cage effects are not implicated because open and wire

covered plots were similarly affected (ANOVA; Table V). The turf is naturally thinner

at this site, and gaps in the turf appeared in other years.

The mussel assemblage increased according to the number of predators removed.

The percent cover of mussels in the large arch and open controls remained nil; small

arches and large cages, the transient predator removals, showed a nonsignificant in-

crease; and the small cage treatment, removing all but a few of the smaller whelks,

showed a statistically significant increase (Fig. 6B). Predation by whelks surely ac-

counted for most of the loss of mussels in plots protected from the transient preda-

tors. 93”; of a total of 69 empty &#.rtilus spp. shells retrieved from cage covered plots

bore whelk drill holes.

EXPERIMENTS AT THE SEMIPROTECTED AND EXPOSED SITES

Lobster exclosures at the semiprotected site (large mesh cages; Table I) produced

marked increases of the Mytilus assemblage. Mussels dominated the treatment plots,

while the turf remained unbroken on the controls (Fig. 6C). The cover of mussels in


f’lg. 8. ~‘h(~~~)~r~ph of an cxclosurc plot at the conclusion of lhc exposed site expwimenl. The crclt~trc cage has been I-cmovcd, but its outline on the turf is clearI) delineated by the cover of muss&. The rule IS

I5 cm long.

individual treatment plots was 45-93 OO. hf. calfjimiarzus comprised = 20”; of the total

cover of mussels. During nocturnal high tides, divers watched some lobsters foraging

on open and arch-covered control plots, while other lobsters pushed their foretegs

through the mesh of the cages, trying unsuccessfully to grasp the M~jtilus spp. protruding

from the turf.

Still greater increases in the Mq’tilus spp. assemblage were produced by lobster

exclosures on the exposed site (large mesh, Table I). At the start of the experiment, a

heavy set of juvenile mussels attached to the turf over the entire exposed site. During

the following 4 wk we observed the margin of the cover of mussels recede from its

seaward extremity shoreward across the bench until the turf was again the only sig-

nificant cover outside of the exclosures. inspection of the copious shell litter at the

receding margin revealed broken shells that bore sculptured fractures produced

by the lobsters (Robles et al., 1990; black oystercatchers make little or no mark

opening the shell). Mussels were cleared from control plots, but in the exclosurcs they

continued to grow rapidly, completely displacing the turf in two of the three ex-

closures (Fig. 8). The mean percent cover of mussels on exclosure plots exceeded

909, (Fig. 6D). Densities of ~~tjlu.~ spp. differed significantly between treattnents and

controfs (Table VI).

x2 C. ROBLES AND J. ROBB

TABLE VI

Mean numbers f 1 SD of mussels and herbivorous mollusks.230-cm’ sample- ’ in the experiment at the exposed site tabulated with respect to experimental conditions and shell length. Statistical analysis as in

Table III.

Species value Open Arch Cage P

M. edulis Total density 9.61 k 3.22 2.00 f 1.73

Density > 1 cm 1.33 2 1.58 1.67? 1.16

,M. culifbrnimus Total density Densit) > I cm

0.33 * 0.58 6.67 i 8.15 72.00 2 4.58 0.00 * 0.00 4.67 k 4.73 68.00* 5.57

Bmchidoniev Total density Density > 1 cm

Chitons > 0.5 cm Limpets > 0.5 cm Herbivorous mollusks

Total > 0.5 cm

16.00 f 10.54 6.22 i 3.06 1.00 + 1.73 0.67 i 0.58

3.33 +_ 2.08 0.33 +_ 0.58 3.00 k 4.36 3.00 + 1.00

6.33 k 5.51 3.33 k 1.16

8O.OOi30.12 i 0.000 7l.OO_t30.51 i 0.000

44.00 k 6.08 2.00* 1.73

7.33 +_ 2.3 1 14.33 + 8.74

21.675X.51

i 0.000 0.024

0.002 0.540

0.0 IO

0.079

0.018

MUSSEL SIZE AND PERSISTENCE

We observed a correspondence between prey size and persistence in the postexper-

imental periods. At the protected site, M. californianus comprised < 5 Oh of the total

mussel cover at the conclusion of the experiments. The mean length of the three largest

individuals of this species in each of the treatment plots was 1.3 & 0.7 cm, the longest

2.5 cm. All mussels disappeared in the first few weeks of the postexperimental periods

at this site.

Storms removed one cage from the semiprotected site in February 1987, just prior

to the spring resumption of lobster predation. z 15 y0 of the cover was large (4-5 cm)

M. calijxnianus, which persisted through spring and summer while a 701, cover of

M. edulis was lost. All experimental clumps and portions of the turf disappeared dur-

ing a stormy period late fall of 1987.

In the experiment on the exposed site, some M. californianus attained 4-5 cm lengths

as early as the July 1985 sampling (Fig. 9). By winter, when cages were removed, the

largest M. calijornianus had reached > 5 cm length (Fig. 9) and the cover of this spe-

cies was 40 YO. The experimentally induced clumps persisted until at least the winter

of 1991-92. increasing only slightly in area, but comprising > SOu/, M. ca/$wnimus.

DISCUSSION

DIFFUSE VS. KEYSTONE EFFECTS

Experimental results from the protected site support the hypothesis of diffuse pre-

dation through compensatory foraging shifts. Lobster and fish removals produced

CARNIVORE EFFECTS x3

5 -

o- - 0.0 0.0 1.0 1.6 20 1.6 ruI t.S 4.0 48 6.0 6.6 6.0

LENQTH CM

Fig. 9. Length-frequency distributions of M. cul~jhiunus in turf samples made on three different dates of the exposed site cxpcriment: the beginning, (23/06!85) conclusion (22/07iS5) and following winter (7;03,‘86).

Latter two samples are from the treatment plots.

significant changes only in combination with whelk removals. The whelks did aggrc-

gate in the transient predator exclosures. Mussel shell collections confirm that the

whelks caused most of the mortality in transient predator exclosures, and the chang-

ing proportions of Mjtihs spp. in the apparent whelk diets (Fig. 5) suggest that the

whelks might play a compensatory role in nature.

Predation on the wave-exposed site fits the keystone hypothesis: exclusion of lobsters

caused the persistent replacement of the turf by mussels. Considering the abundance

x4 C. ROBLES AND J. ROBB

and dietary information, contributory effects of the other predators are unlikely. Al-

though a single pair ofblack oystercatchers was sometimes present, the birds consumed

few M. cul(fornianus < 3 cm (Hart-wick, 1976; this study), the size range removed in the

experimental period. Furthermore, the experimental clumps of M. cnl$wnicrrm sur-

vived re-exposure to the lobsters and birds at lengths (> 5 cm) that were resistant to

the lobsters, but within the range killed by black oystercatchers in the natural mussel

beds.

The prior examples of keystone and the diffuse predation were separated from each

other by geographic region and species composition. The Catalina results suggest that

keystone and diffuse predation can operate in the same community, and in this case.

they may represent extremes of a continuum of the increasing effect of one prcdatot

relative to the others. We did not investigate the factors favoring the emergence of a

keystone predator. Although differences in the relative abundances of predators among

the sites coincide with the gradient of wave exposure, the cause of the differences rc-

mains unknown.

However, we caution that compound removal experiments have technical limita-

tions, and consequently, the diffuse effects at the protected site may be, at least in part.

an artifact. Out of practical necessity, compound removals couple the type of preda-

tor targeted with the scale of the manipulation (e.g., Menge & Lubchenco, 198 1). The

first experiment on the protected site (Table I) demonstrated that the transient pred-

ators were capable of limiting muss& over much of the available habitat (Z 100 m2

whelk removal bench). But in the second experiment (Table I), the whelks limited the

mussels only in the small areas of the transient predator exclosures ( < lo,, of the turf

zone) in which they congregated from the entire shore. The trend towards increased

mussel covers in large cage and small arch plots (Fig. 6B) shows that even with ag-

gregation, mussel removal by the whelks was incomplete. Therefore, the whelks might

not control the mussel assemblage over the entire turf zone, if large scale removals of

lobsters and fishes were feasible. Problems with experimental scale may exaggerate the

effects of compensatory foraging shifts.

Simultaneous removal of several predators does not measure the proportion of the

prey population falling to a specific predator. Apparent diets provide an indication, but

these may be biased by handling times (see Fairweather & Underwood, 1983. for

discussion). Consumption of mussels by large decapods and fishes is several orders of

magnitude faster than by gastropod predators (e.g., Chao, 1973; Brett, 1979; Edwards

et al., 1982; Menge, 1983). Thus, an arthropod, vertebrate, or other large consumer

within a diverse predator fauna may be the principal control of a dominant prey, yet

it remains unrecognized as a keystone under the limitations of our techniques.

KEYSTONE EFFECTS OF AN ARTHROPOD

Whether by natural constraints or the limitations of our assessments, strong effects

of single predator species are reported less frequently for: (1) terrestrial than aquatic


environments; (2) carnivores than herbivores; and (3) arthropods and mammals than

other taxa (Sih et al., 1985; but see Risch & Carroll, 1982; Lock, 1972; for marked

effects of insects and hippopotamus in terrestrial communities). Concurring with the

hypothesis that strong effects are rare at higher trophic levels (Menge & Sutherland,

1976) Sih et al. (1985) attribute the paucity of arthropod examples, especially in the

marine environment, to their characteristically high trophic status.

Heretofore, putative examples of marine arthropod keystones were supported pri-

marily by observations (e.g., Mann & Breen, 1972; Breen & Mann, 1976: see Elner &

Vadas. 1990, for discussion). Previous experimental studies of predation by marine

arthropods propose diffuse effects (eg., Menge & Lubchenco, 1981; Menge ct al.. 1986;

Hines ct al., 1990). Peterson (1979) describes a case in which observations suggested

a keystone effect of swimming crabs, but whelks and other predators prevented the

survival of mussels in crab exclosures. To our knowledge, the Catalina study provides

the first experimental demonstration of keystone effects of a marine arthropod.

CHANGING COMMUNITY INTERACTIONS

Removing predators cause more than the replacement of dominants. We illustrate

potential changes in community interactions with herbivorous mollusks. These are

among the most abundant of the > 200 invertebrate spp. found in mussel clumps

(Suchanek. 1979; Tsuchiya & Nishihira, 1986). In replicated turf samples (Robles,

1987; pers. obs.), combined densities of juvenile limpets and chitons ranged from 60

to 1050.11~’ However, large adults were very rare. The mollusks were found in the

lobster guts (Robles, 1987; this study) and the abundances of individuals >0.5 cm

increased significantly in lobster exclosures (Table VI), suggesting that they too are

limited by predation. Although the juvenile herbivorous mollusks do not clear the turf

from the rock, the adult populations associated with the mussel beds may prevent the

overgrowth of mature M. ccd~fivnirrnus by algae and other spatial competitors

(Suchanek, 1979; Paine & Suchanek, 1983). This overgrowth might otherwise lovvcr

mussel survivorship and reproduction (Witman & Suchanek, 1984; Dittman & Rob-

les, 1991). The results suggest a change in community interactions, even though the

assemblages share many species. [See Suchanek (1979) Tsuchiya & Nishihira (I 986),

and Dean & Connell (1987) for associated fauna of turf and mussel beds. Witman

(1985) describes community relationships of species associated with subtidal tnusscl

beds.]

SIZE RELATIONS AND PERSISTENCE OF EXPERIMENTAL CHANGES

The abilities of M. calijimGums to hold space and to resist predators accrue to large

body size (Paine, 1966, 1974, 1976; Dayton, 197 1; Harger, 1972; Roblcs et al., 1990).

The persistence of downward extensions of mussel zones following sea star removals

apparently depends on the mussels’ size range relative to that of the returning stars


(Paine et al., 1985). Farrell (1988) proposes a similar relationship for the persistence

of barnacles following a limpet removal. Therefore, size-limited predation probably

caused the longer persistence of relatively large M. californianus in the postexperimental

periods.

Differences in mussel growth rates among the sites apparently determined much of

the size differences of experimental mussels. Records of mussels lengths in the exclo-

sure plots indicated that M. califovniun~s grew out of the turf roughly twice as fast at

the exposed site than at the protected site. We tested for possible site-specific differ-

cnces in mussel growth rates by transplanting matched cohorts of small (2-4 cm)

M. calijbrniutzus simultaneously to the same shore level of each site and recording the

shell growth increment. The groups were covered with 1.2-cm’ opening wire mesh to

protect them from predators. Successive runs of the experiment were begun fall and

winter of 1990-91. The mussels did grow significantly faster at the wave-exposed sites

(Fig. 10).

Perennial beds of Mytilus spp. cover many wave-beaten shores of North America and

Europe. Wave stress in these areas favors higher mussel abundances by hampering

predator foraging (e.g., Menge, 1978a,b). M. californianus beds replace the turf on the

most wave-washed ends of the islet, and predator foraging ceased at these locations

in the season of highest wave action. Our transplant experiments, studies of natural

mussel populations in different wave exposures (Robles & Sherwood-Stephens; C.

Robles, unpubl. data) and indirect estimates (turnover of biomass; Leigh et al., 1987)

show a positive relationship between wave exposure and growth rate. We speculate that

81

protected site semi-protected exposed site

m Fall Run k?%@ Winter Run

Fig. 10. Mean increment and 1 SE of shell growth in two transplants of M. culijbrniunur to the three sites. The “fall” transplant ran from 15 September 1989 to 23 February 1990; the “winter” transplant from 4 March 1990 to 8 June 1990. For the latter, mussels were not transplanted to the semiprotected site. P values of

ANOVA of growth increments were 0.04 and 0.01. respectively, for fall and winter runs.


shifts in the relative abundance of turf and mussels over the wave exposure gradient

reflect changing relative levels of production and predation. Prey gaining resistance to

predators with size i.e., M. califovniunus, should display greater persistence on wave-

washed shores.

PHYSICAL STRESS, INDIRECT EFFECTS, AND PREVALENCE OF THE TURF

Prior explanations for the prevalence of the turf emphasized its tolerance to physi-

cal and biotic stresses (Littler & Littler, 1980; Hay, 1981). The mat’s ability to trap

water and sediments imparts resistance to desiccation (Hay, 1981). Desiccation stress

appears to be greatest in fall, when prolonged low tides coincide with strong sun and

dry winds (Seapy & Littler, 1982). If sun, storm waves, or other disturbances damage

the cover, vegetative propagation from intact thalli and sprouting from crusts quickly

close the gaps (Sousa et al.. 1981).

The turf resists some biotic challenges. The entrapped sediments may deprive some

spatial competitors of firm substrata for attachment (Seapy & Littler, 1982; Stewart,

1982, 1989). Seapy & Littler (1982) propose that fall desiccation frees space for the turf

by removing adult sedentary invertebrates. Rapid closure of gaps by vegetative prop-

agation may preclude other macroalgal species that colonize only by spores (Sousa

ct al., 198 1). Finally, the turfs tough tissues, low profile, and ability to increase branch-

ing when terminal portions are clipped evidently allows it to withstand moderate

browsing by fishes (Littler & Littler, 1980; Hay, 1981).

Although the mussels may be less tolerant of physical stress than the turf, the

replacement of turf by mussels in exclosures cannot be attributed to cage artifacts, i.e.,

reduced desiccation stress (Dayton & Oliver, 1980). Seapy & Littler (1982) cite algal

bleaching as evidence for desiccation stress. We compared per cent of total algal cover

bleached among open, arch, and cage plots during an episode of marked bleaching (fall

of 1982). Mean percentages of bleaching were 32.3, 28.7, and 26.7”, respectively, for

open, arch, and cage plots (ANOVA: F = 0.408; df = 2,6; P = 0.682). In all experiments,

50-loo’:, of the differences in mussel abundances between treatments and controls

developed in spring-summer, when physical stress are thought to be minimal, but

intertidal predators were most abundant. The hypothetical effects of desiccation would

have been preempted by predation. At the wave-exposed site (Table I), the mussels

survived the prolonged daytime emergence of the fall-winter after cages were removed.

In the second experiment on the protected site (Table I), we can not discount the

possibility that some of the treatment effect was an artifact, because there lvas no strict

small mesh control, i.e., a small mesh arch that excluded no predators. However, mean

mussel covers for small mesh arches and large mesh cages appeared more similar to

one another than to mean covers of either the large mesh arches or small mesh cages,

an outcome that would be expected if predation, rather than differing mesh sizes,

caused the differences among treatment groups (Fig. 6B).

While imparting resistance to some biotic and physical stresses, the turfs morphol-

xs ~.ROBLESA~DJ.ROBB

ogy may render it vulnerable to the mussels. Filamentous algae attract the settling stages

of the mussels (e.g., Seed, 1969a,b, 1976; Paine, 1974; Petraitis, 1979; Peterson, 1984).

and we found much higher densities of mussel plantigrades (recently settled individ-

uals < 1 cm) in the turfs than on bare rock (C. Robles, pers. obs.). On the islet, the

rapid growth of plantigrades quickly overtopped the low profile of the turf.

Resistance to desiccation, invasion of sporelings, and moderate browsing may well

explain the success of the turf relative to other algal assemblages, however. the prev-

alence of the turf also depends on the indirect effects of carnivores.

R. Desharnais, D. Levitan, R. Paine, P. Petraitis, IS. Pfister, S. Prescott, T. Raw-

lings, R. Sherwood-Stephens, and W. Sousa provided valuable criticism of preliminary

drafts. M. Alvarado, E. Carriazo, D. Dittman, C. Gramlich, G. Jung, K. Petit, H.

Ramos, D. Sweetnam, M. Vcla, and F. Villeda assisted the field work. The work was

supported by NSF Grants OCE8200474, R118505428, and RII8804679.

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