Ecology, 79(8), 1998, pp.

27592770
q 1998 by the Ecological Society of America

ROLES OF DISTURBANCE, SEDIMENT STRESS, AND SUBSTRATUM

RETENTION ON SPATIAL DOMINANCE IN ALGAL TURF
LAURA AIROLDI1
Dipartimento di Scienze dellUomo e dellAmbiente, Universita di Pisa, Via A. Volta 6, I-56126 Pisa, Italy

Abstract. A common assumption of ecological theories addressing the causes of spatial

dominance and stability in natural communities is that organisms have trade-offs between
resistance to disturbance, environmental tolerance, and competitive abilities, i.e., that dif-
ferent species or groups of species dominate under different regimes of disturbance and
stress. A multifactorial field experiment was conducted from June 1994 to October 1995
in a turf-dominated macroalgal assemblage on a rocky subtidal shore south of Livorno
(western Mediterranean, Italy) to test the hypothesis that variable patterns of disturbance
and stress influence the differential success of species, and to identify functional charac-
teristics resulting in persistent monopolization of space. The experiment, which included
manipulation of the depositional environment, was designed specifically to test whether
patterns of recovery following abrasion or removal of the biota differed among patches of
different sizes, produced at different times of the year and at different locations and un-
dergoing different rates of sediment deposition.
Variable size, intensity, timing and location of disturbance, and variable stress induced
by deposition of sediment significantly influenced the success of erect algae that persist by
sexual reproduction but did not affect spatial dominance by the filamentous algal turf. The
turf regained space very quickly by vegetative reproduction and persisted as the dominant
species in all the experimental plots, independent of the disturbance and stress regimes
imposed. The impressive rate of vegetative propagation was identified as a major deter-
minant of the structure of the assemblage and the probable basis for the capability of the
turf to compete for space and resist disturbance. Patterns of growth may be as crucial as
the disturbance regime in determining community structure, and packaging of compet-
itive and resistance abilities into a single species or group of species could be more common
than generally thought.
Key words: disturbance intensity; macroalgae; Mediterranean; patch size; Polysiphonia setacea;
recovery; rocky shore; sediment stress; spatial dominance; subtidal; turf, algal; vegetative propagation.

INTRODUCTION adaptive, competitive, and reproductive characteristics

In densely colonized environments, such as rocky
intertidal and subtidal shores, salt marshes, old fields,
and tropical rain forests, much of the community or-
ganization and dynamics are functions of factors in-
volved in the provision, procurement, and subsequent
utilization of space by sessile species (Dayton 1971,
Sousa 1979a, Dethier 1984, Brokaw 1985, Bertness and
Ellison 1987, Holt et al. 1995). In these habitats, dis-
turbance associated with partial or total loss of biomass
has been recognized as a primary mechanism that cre-
ates open space, allowing the expansion of vegetative
growth forms and the opportunity for recruitment of
sexual species (Sousa 1984a, Pickett and White 1985).
The subsequent sequence of replacement of species is
a complex process, depending on disturbance, envi-
ronmental stress, availability of resources, and the
Manuscript received 7 July 1997; revised 2 December
1997; accepted 4 December 1997; final version received 8
January 1998.
1 Present address: Centre for Research on Ecological Im-
pacts of Coastal Cities, Marine Ecology Laboratories A11,
University of Sydney, NSW 2006, Australia.
2759
of the important space occupiers (Connell and Slatyer
1977, Bazzaz 1979, Sousa 1984b, Menge and Suther-
land 1987, Wilson and Tilman 1991). Variable patterns
of disturbance and recovery may lead to coexistence
of diverse assemblages of organisms or, alternatively,
to extensive dominance by a few species that tend to
define the structure of the community (Sutherland
1974, Knowlton 1992). In some cases, monopolization
of space may be remarkably persistent. Examples range
from forest trees (Woods and Whittaker 1981) to sub-
tidal kelps (Dayton et al. 1992), emphasizing the im-
portance of understanding the general mechanisms re-
sponsible for dominance and stability in natural com-
munities (Dayton et al. 1984).
Prior explanations of spatial dominance pointed to
the roles of disturbance, of environmental stresses lim-
iting the productivity of the system and of competitive
exclusion (Connell 1978, Lubchenco 1978, Huston
1979, Sousa 1979b, Taylor and Littler 1982, Hawkins
1983). Regardless of differences arising because of dif-
ferent spatial and temporal scales of observation (Pe-
traitis et al. 1989, Jackson 1991), most of these models
2760 LAURA AIROLDI
predict that monopolization of space occurs because
the environmental conditions are too harsh, allowing
persistence of only those species that are resistant or
resilient to disruption or tolerant to stress that lowers
productivity. Alternatively, space may be monopolized
by species that are especially vigorous at interference
competition or at pre-empting open space made avail-
able by the death of previous occupants and which can
hold space against later invasion. This perspective as-
sumes that organisms have trade-offs between resis-
tance, tolerance, and competitive abilities (Petraitis et
al. 1989, Tilman 1990), i.e., that species or groups of
species with different morphology, physiology, or be-
havior dominate under different regimes of disturbance
and stress (Jackson 1979, Steneck and Dethier 1994).
In New England salt marshes, for example, trade-offs
in plant-specific abilities either to withstand wrack
burial or to resist invasion by potential competitors
have been related to patterns of spatial dominance
across gradients of physical disturbance (Bertness and
Ellison 1987). Further, trade-offs in species-specific re-
productive and growth abilities often have been in-
voked to explain differential patterns of recovery fol-
lowing disturbances creating patches of different sizes
(Barden 1981, Sousa 1984b, Pickett and White 1985,
Farrell 1989, Shumway and Bertness 1994). Most ex-
perimental work on processes affecting the dynamics
of space release and occupancy has, however, been con-
fined to a few habitats, and the relevance and generality
of the above paradigm remains to be demonstrated for
most natural communities.
Algal turfs are the dominant flora on many tropical
and temperate intertidal and subtidal shores (Hay 1981,
Stewart 1982, Adey and Goertmiller 1988, Kendrick
1991, Underwood et al. 1991) and, in recent years,
there seems to have been a trend of increasing abun-
dance of these growth forms (Thom and Widdowson
1978, Seapy and Littler 1982, Airoldi et al. 1995a). In
spite of the extension of turf-dominated assemblages,
few studies have examined in the field the factors po-
tentially involved with procurement and utilization of
space by turfs. These studies have suggested different
possible explanations accounting for the dominance of
turfs, including the ability to withstand invasion by
other spatial competitors (Sousa et al. 1981, Airoldi
and Cinelli 1997) in addition to the tolerance of phys-
ical and biotic stresses (Littler and Littler 1980, Hay
1981, Airoldi et al. 1995a) and the resistance to and
quick recovery from disturbance (Sousa 1980, Stewart
1989). This would suggest that turfs may dominate
space under a wide range of disturbance and stress
regimes.
In this study, I tested the hypothesis that variable
patterns of stress and disturbance influence the differ-
ential success of macroalgal species in a turf-dominated
assemblage on a rocky subtidal shore (Ligurian Sea,
Italy) and attempt to identify functional characteristics
associated with persistent monopolization of space. By
Ecology, Vol. 79, No. 8
stress, I mean external constraints that preclude or limit
the productivity and growth of the assemblage, while
disturbance refers to mechanisms causing the partial or
total removal of organisms (Grime 1977). Previous in-
vestigations (see Methods: Study system) have indi-
cated that disturbance in the study area is mainly related
to wave action and scouring by sediment, which may
completely or partially remove the turf from patches
of rock. Moreover, small-scale variations in sediment
deposition may locally influence the rate of growth of
the turf (Airoldi and Cinelli 1997). Events of distur-
bance that are small relative to the area of the habitat
or to the sizes of the individuals are common, and their
variability in time, space, and intensity has been shown
to exert an effect on the structure of some marine and
terrestrial communities by influencing the differential
success of species in neighboring patches with different
sizes and availability of resources (Werner 1977, Sousa
1979b, 1984b, Barden 1981, Palumbi and Jackson
1982, Smith and Brumsickle 1989, Benedetti-Cecchi
and Cinelli 1996, Burke and Grime 1996). A multi-
factorial field experiment, including manipulation of
the depositional environment, was designed specifi-
cally to test whether patterns of recovery following
abrasion or removal of the biota differed among patches
of different size, produced at different times of the year
and at different locations, and undergoing different
rates of deposition of sediment. The interaction among
these factors was also investigated by using a full fac-
torial design. The effects of the experimental treat-
ments on patterns of recovery of turf-forming and erect
species were assessed for .1 yr. Encrusting corallines
may also be present below the turf, but, due to diffi-
culties of quantifying these forms with nondestructive
sampling, they were not considered in this study. Spe-
cific experiments on these components of the assem-
blage will be reported in a subsequent paper.
METHODS
Study system
Turf-dominated algal assemblages colonizing sub-
tidal habitats on the exposed rocky shore south of Li-
vorno (latitude 438309 N, longitude 108209 E) have re-
ceived some attention in recent years (Airoldi et al.
1995a, Airoldi and Cinelli 1997). Here the bottom con-
sists of a wide sandstone platform that extends $300
m seaward to a depth of ;40 m. From 5 m downward,
the platform has eroded to form outcrops that support
a dense turf mostly consisting of Polysiphonia setacea
Hollenberg. This species has become widely distrib-
uted on subtidal shores in various areas of the Medi-
terranean basin (Airoldi et al. 1995b). It occurs on rocks
and as an epiphyte on encrusting forms and develops
dense mats of upright filaments #1 cm high from pros-
trate branches firmly attached to the substratum by rhi-
zoids.
The area is characterized by moderately large sedi-
December 1998 DETERMINANTS OF SPATIAL DOMINANCE
ment loads, compared to other shallow coastal regions
(Airoldi et al. 1996). During the present research, rates
of sedimentation fluctuated between 2.1 and 177.9
gm22d21, with an average of 32.5 gm22d21 (Airoldi
and Virgilio 1998). Contrary to other habitats, where
algae may be subjected to complete burial by sedi-
ments, the algal turf of this study is never totally buried.
Local patterns of deposition of sediment largely vary
on a scale of meters (Airoldi and Virgilio 1998). The
abundance of grazers is small at the study site during
most of the year, and disturbance is mainly related to
wave action and scouring by sediment. The intensity
of these factors varies greatly through time (Airoldi et
al. 1996); maximal disturbance generally occurs in the
autumn, when the turf may be removed from the sub-
stratum exposing the underlying encrusting algae and
bare rock. Generally, however, disturbance by sediment
is neither frequent nor intense enough to completely
remove prostrate basal axes of Polysiphonia setacea
from the substratum. Patches of bare rock, ranging from
5 cm2 up to ;500 cm2, are produced by violent episodic
perturbations, such as storms or, to a lesser extent, an-
choring boats, which may also cause the outcrops to
break apart due to the action of boring animals riddling
the sandstone.
The experiment was done, from June 1994 to Oc-
tober 1995, in a gently sloping (;308) field of outcrops
extending 200 m parallel to the shoreline at a depth
between 13 and 17 m. Two stations, 500 m2 each, were
selected at random among four arbitrarily established
in the study site. A total of 48 outcrops for each station
were selected at random among those which had hor-
izontal top surfaces larger than 35 3 40 cm; these were
used in the experiment described below. The minimum
distance between outcrops was 1.5 m.
Experimental study
A 5 3 5 factorial experiment was used to examine
the independent and interactive effects of sediment de-
position, size, and location of areas on patterns of re-
covery of the algal assemblage following abrasion or
removal of the biota at different times of the year. Two
sizes of patches, within the opposite ends of the range
of disturbances in the study area, were used. In June
1994, 24 experimental plots consisting of 12 large (20
3 20 cm) and 12 small (12 3 12 cm) quadrats were
established at each of the two stations on the horizontal
top surface of as many boulders and permanently
marked at their edges with epoxy putty (Subcoat S.,
Veneziani). The abrasion of the biota was obtained in
six plots of each size by rubbing with a cotton cloth
for 1 min. This treatment thinned the algal turf, while
affecting to a lesser extent the other algae. The re-
maining plots were scraped completely clean of resi-
dent organisms by using hammer and chisel, in order
to mimic the effect of disturbance induced by intense
perturbations. The heterogeneity of the substratum, rich
in crevices, made scraping rather difficult; prostrate
2761
axes of specimens in the deepest crevices probably
were not completely removed.
The effect of variable sediment stress on algal re-
covery was assessed by adding known amounts of sed-
iment dry mass (10 or 28 g on 12 3 12 and 20 3 20
cm plots, respectively) to half of the plots in each com-
bination of treatments. The sediment was taken from
a nearby shore, passed through a 200-mm mesh sieve,
and dried to constant mass (at 608C). The fine texture
of the sediment used should have limited abrasion, thus
allowing separation of the effects of sediment smoth-
ering. Sediment generally was applied once every 7 d
(except for a few occasions when bad weather made
diving unsafe for longer periods) which increased sed-
imentation rates by 100 gm22d21. Chronic rates of
sedimentation .100 gm22d21 have been considered
highly stressful for other habitats (Rogers 1990), but
little quantitative information is available for rocky
shore assemblages.
A second series of disturbed areas was produced in
December 1994. Since the time at which recovery was
initiated was not replicated within season, any differ-
ences among plots produced in different times may
reflect chance temporal variation rather than predict-
able seasonal trends. Every combination of treatments
had three randomly assigned replicates. The entire de-
sign, therefore, consisted of two sizes of plots, with
one of two disturbance treatments (abrasion or removal
of algae) and two sediment treatments (natural or add-
ed). The eight combinations were each replicated three
times in each of two locations and the experiment was
done twice. Three additional plots (20 3 20 cm) were
marked in each location to monitor temporal variations
of the algal assemblage in unmanipulated plots during
the experiment. The reproductive phenology of the
dominant alga Polysiphonia setacea was also studied
throughout the research by samples taken once every
two weeks, in order to assess its reproductive status.
Sampling and analysis of data
The percent cover of turf-forming and erect species
was visually estimated at intervals of 13 mo until
October 1995, when the extensive cover of the turf
made it difficult to relocate some experimental plots.
A surface of 100 cm2 was sampled in the middle of
large and small plots by means of the visual estimation
method (Dethier et al. 1993). A Plexiglas sheet divided
into 25 small quadrats was used: a score from 0 to 4%
was given to each species in each small quadrat, while
organisms filling less then 1/4 square (percent cover
,1%) were given an arbitrary value of 0.5%.
The experimental data were analyzed using a five-
way mixed model analysis of variance (ANOVA) with
Disturbance (abrasion vs. removal), Patch size (12 3
12 vs. 20 3 20 cm), and Sediment deposition (natural
vs. experimentally accreted) as fixed factors, and Lo-
cation (two stations) and Time of formation (June vs.
December 1994) as random factors (Underwood 1997).
2762 LAURA AIROLDI
FIG. 1. Percent covers of most abundant algae in unmanipulated plots near Livorno (Italy) during the course of the study.
Data are means 61 SE pooled across two stations (n 5 6 replicates [three reps. from each of two stations]).
Patterns of recruitment of some algae were highly sea-
sonal: date-by-date comparisons of treatments initiated
at different times of the year would have confounded
differences due to the timing of disturbance with either
seasonal trends or different ages of patches. Inspection
of graphs showed that differences between treatments
were generally consistent over time. Analyses were,
therefore, run by using as the dependent variable the
percent cover values of each species in each plot av-
eraged over sampling dates. This procedure allowed
me to estimate the overall effects of treatments on the
recruitment success of species over the study period,
independently of seasonal periodicities. Before running
the analyses, the assumption of homogeneity of vari-
ances was examined using Cochrans C test. Data were
opportunely transformed only when necessary to sta-
bilize variances. In the case of algal turf, variances
remained slightly heterogeneous (0.01 , P , 0.05)
even after transformation, and the analysis was run at
a 5 0.01 for significance test. When possible, pooling
procedures were applied to increase the power of tests
(Underwood 1997). Students t tests were used to com-
pare average percent covers of algae over sampling
dates in unmanipulated plots from the two stations.
RESULTS
Filamentous turf dominated the unmanipulated algal
assemblage throughout the course of the study. A sea-
Ecology, Vol. 79, No. 8
sonal trend was evident, with lower abundance in au-
tumn and winter, but mean percent covers of the turf
were generally .70% (Fig. 1). Erect algae did not form
a canopy, and the calcareous alga Halimeda tuna (Ellis
et Solander) Lamouroux represented the most abundant
erect species during the study. Peaks in abundance oc-
curred in the summer for H. tuna and the seasonal algae
Dictyota dichotoma (Hudson) Lamouroux and Padina
pavonica (Linnaeus) Lamouroux. Conversely Aceta-
bularia acetabulum (Linnaeus) P. C. Silva and Flabellia
petiolata (Turra) Nizamuddin were rare (Fig. 1), the
latter species being more common on sloping surfaces.
The observed patterns were consistent at both stations
(Students t tests, df 5 10, P . 0.05 for all species).
In spite of the frequent sampling, Polysiphonia se-
tacea was never seen in a reproductive state, and col-
onization of cleared space by the turf likely proceeded
by vegetative propagation (see Discussion). At both
stations, time of formation of the patches significantly
influenced patterns of recovery of the algal turf fol-
lowing removal of the biota (Fig. 2 and Table 1). Re-
covery proceeded more rapidly in quadrats scraped in
June than in those scraped in December. In the former,
the turf reached average percent covers .60% just after
4 mo from the beginning of the experiment. As indi-
cated by the significant interaction Time 3 Disturbance
(Table 1), this temporal pattern was not evident in quad-
rats treated by abrasion, where the turf quickly recov-
December 1998 DETERMINANTS OF SPATIAL DOMINANCE
FIG. 2. Effects of sediment deposition and patch size on patterns of recovery of the algal turf following abrasion or
removal of the biota in plots in June and December 1994. Data are mean percent covers (61 SE) pooled across two stations
(n 5 6 replicates as in Fig. 1).
ered to control covers 1 or 2 mo after the start of the
experiment. The other factors (Location, Patch size,
and Sediment) did not affect the cover of the turf in
either abrasion or removal plots.
Halimeda tuna and Flabellia petiolata were probably
the algae most resistant to abrasion, which negligibly
affected the initial covers of these species. Overall,
patterns of recovery of H. tuna were very complex,
varying as a function of the interaction of all the factors
considered in the experiment (Fig. 3 and Table 2). Dif-
ferences between treatments were, however, rather
small. The only noticeable pattern was that H. tuna
sparsely recruited in the removal plots started in De-
cember while it densely colonized the plots scraped in
June, where it reached percent covers comparable to
those in control and abrasion plots. Patterns of recovery
of F. petiolata were similar, but this species recovered
little in removal plots. Its abundance slightly increased
in abrasion plots as a function of deposition of sediment
and size of the quadrat, the effects of which varied
significantly depending on the timing of rubbing and
location (Table 2).
Patterns of abundance of Dictyota dichotoma in the
experimental plots were seasonal. In fact, colonization
2763
of this species peaked during the summer in both years
(Fig. 4). Covers were affected by all the factors (Table
2). D. dichotoma was more abundant in removal plots
cleared in June, but its percent cover varied in patches
of different size depending on the station (significant
Time 3 Location 3 Disturbance 3 Patch size inter-
action). A significant Sediment 3 Disturbance inter-
action was also detected, indicating that D. dichotoma
was slightly more abundant in total removal plots sub-
jected to natural rates of sedimentation.
Recovery of Padina pavonica was significantly in-
fluenced by the intensity and timing of disturbance as
main factors (Table 2). This seasonal species was more
abundant in removal plots independent of any other
treatment. Its recruitment was generally higher in all
the quadrats produced in December. These trends were
even more evident for Acetabularia acetabulum (Fig.
5). This species colonized removal plots started in De-
cember; maximal percent covers were sustained by
large quadrats subjected to enhanced deposition of sed-
iment. This resulted in a significant interaction Time
3 Sediment 3 Disturbance 3 Patch size (Table 2). A
significant Location 3 Disturbance interaction was also
2764 LAURA AIROLDI Ecology, Vol. 79, No. 8

TABLE 1. Results of the ANOVA on the effects of five experimental manipulations of a subtidal
environment on the west coast of Italy on patterns of recovery of the filamentous algal turf.

Denominator MS of
Source of variation df MS F P F ratio
Time 5 T 1 1.2465 8.324 0.212 T3L
Location 5 L 1 0.0417 0.278 0.691 T3L
Sediment 5 S 1 0.0129 0.078 0.827 T3S
Disturbance 5 D 1 6.0872 4.085 0.292 T3D
Patch size 5 P 1 0.0228 2.920 0.337 T3P
T3L 1 0.1497 1.348 0.249 Residual
T3S 1 0.1659 1.772 0.410 T3L3S
L3S 1 0.0502 0.536 0.597 T3L3S
T3D 1 1.4900 13.58 0.0004 Pooled term
L3D 1 0.0279 1.237 0.466 T3L3D
S3D 1 0.0171 0.038 0.876 L3S3D
T3P 1 0.0078 0.655 0.566 T3L3P
L3P 1 0.0083 0.119 0.699 T3L3P
S3P 1 0.0092 4.068 0.293 L3S3P
D3P 1 0.0104 0.054 0.855 L3D3P
T3L3S 1 0.0936 0.843 0.362 Residual
T3L3D 1 0.0226 0.203 0.653 Residual
T3S3D 1 0.0001 0.001 0.980 T3L3S3D
L3S3D 1 0.4419 3.195 0.325 T3L3S3D
T3L3P 1 0.0119 0.107 0.744 Residual
T3S3P 1 0.0259 0.800 0.535 T3L3S3P
L3S3P 1 0.0023 0.069 0.835 T3L3S3P
T3D3P 1 0.0000 0.019 0.913 T3L3D3P
L3D3P 1 0.1933 107.7 0.061 T3L3D3P
S3D3P 1 0.0517 0.431 0.630 L3S3D3P
T3L3S3D 1 0.1383 1.245 0.269 Residual
T3L3S3P 1 0.0323 0.291 0.591 Residual
T3L3D3P 1 0.0018 0.016 0.899 Residual
T3S3D3P 1 0.0051 0.017 0.918 T3L3S3D3P
L3S3D3P 1 0.1199 0.395 0.643 T3L3S3D3P
T3L3S3D3P 1 0.3032 2.729 0.103 Residual
Residual 64 0.1111
Pooled term 65 0.1097
Notes: The treatments Sediment deposition (natural vs. experimentally accreted), Disturbance
(abrasion vs. removal), and Patch size (12 3 12 vs. 20 3 20 cm) are fixed, while Time of
formation (June vs. December 1994) and Location (two stations) are random. The analysis was
run using as the dependent variable the percent cover values in each plot averaged over sampling
dates. The P values of significant terms (P , 0.01) are shown in boldface type. The pooled
term 5 (T 3 L 3 D) 1 Residual. Data were log-transformed prior to analysis. Cochrans C
test: C 5 0.226, 0.01 , P , 0.05.

detected, indicating differences between stations in pat-
terns of colonization of removal plots.
DISCUSSION
On exposed rocky habitats like those in this study,
localized wave disturbance is often combined with
scouring and smothering by sediment (Airoldi et al.
1996). Scouring may remove whole organisms or their
parts, while smothering involves reduced availability
of light, oxygen, nutrients, and firm substratum for set-
tlement and recruitment (Daly and Mathieson 1977,
Devinny and Volse 1978). The strength of water motion
and the degree and duration of shear determine the
intensity of the perturbation, ranging from frequent
moderate damage by abrasion to unpredictable severe
disturbance of patches within the pre-existing back-
ground assemblage of organisms. Spatial and temporal
patchiness of deposition of sediments contribute to cre-
ate a mosaic of asynchronous patches that differ in
terms of disturbance damage, size, and availability of
resources. The results of this study indicate that all
these factors potentially influence the structure of the
assemblage. Colonization of the experimentally dis-
turbed areas depended significantly on timing, intensity
and size of disturbances, and on variable stress induced
by local deposition of sediment. The effects of these
factors were highly interactive and varied in proximate
locations of the shore, emphasizing the importance of
multiple causation in the regulation of subtidal com-
munity structure. The observed differences were, how-
ever, quantitative rather than qualitative, and the over-
all composition of the assemblage was similar across
different areas. The algal turf regained space very
quickly and persisted as the dominant species in all the
experimental plots, independent of the treatments ap-
plied. The ability of this growth form to monopolize
space under a wide range of environmental conditions
appeared to be the major determinant of the structure
of the assemblage.
The algal turf retained space and persisted during
December 1998 DETERMINANTS OF SPATIAL DOMINANCE 2765

FIG. 3. Effects of sediment deposition and patch size on patterns of recovery of the erect alga Halimeda tuna following
abrasion or removal of the biota in plots in June and December 1994. Data are mean percent covers (61 SE) pooled across
two stations (n 5 6 replicates as in Fig. 1).

the entire year without serious damage by abrasion or
wave disturbance. Major fluctuations in its abundance
were related to thickness rather than cover and, when
disturbed, its rate of recovery was rapid, despite po-
tential differences related to the timing of disturbance.
The phenological data suggest that colonization of
Polysiphonia setacea proceeded by vegetative repro-
duction, which, at the moment, is the only form of
reproduction that has been observed both in the field
and in culture for specimens of this species from var-
ious areas of the Mediterranean (Airoldi et al. 1995 a
and references therein; F. Rindi, personal communi-
cation). Visual inspection of the plots suggested that
the turf secures space by encroachment of prostrate
axes from the periphery and regrowth of surviving
prostrate axes. This latter mechanism probably is en-
hanced in this habitat by the heterogeneity of substra-
tum texture, where cracks and crevices provide refuge
from disturbance. The capacity of P. setacea to regen-
erate under culture (F. Rindi, personal communication)
suggests that drifting fragments produced by hydro-
dynamic drag and breakage could also contribute to the
fast recovery of the turf. Further, culture observations
suggest that new plants can be quickly regenerated by
single living cells even in decaying filaments (F. Rindi,
personal communication). More research in the field is
needed to investigate mechanisms of vegetative prop-
agation by P. setacea. Whatever the mechanism, the
turf can continuously spread physically resistant, basal
filaments across cleared areas.
When vegetative growth is the major mechanism of
colonization, small clearings should exhibit faster rates
of recovery than do large ones because of their close-
ness to undisturbed thalli and their greater perimeter/
area ratio. Different rates of recovery in patches of
varying sizes generated naturally or experimentally
have been observed in a variety of marine and terres-
trial habitats and over a wide range of spatial scales
(Barden 1981, Kay and Keough 1981, Paine and Levin
1981, Palumbi and Jackson 1982, Brokaw 1985, Farrell
1989, Shumway and Bertness 1994). In this study, the
size of the disturbed area did not affect the rate of
recovery of the turf in either the abrasion or the removal
treatments. Logistic limitations did not allow replica-
tion of the experiment over a larger range of patch
sizes, but results of subsequent experiments in the same
area with clearings of 7.5 3 7.5 cm and 15 3 15 cm
(L. Airoldi, unpublished data) confirm that prostrate
axes secure space independently of the size of patches,
at least within some possible threshold sizes (Paine and
2766 LAURA AIROLDI Ecology, Vol. 79, No. 8

TABLE 2. Results of ANOVA on the effects of five experimental manipulations of a subtidal environment on the west coast
of Italy on patterns of recovery of the erect algae Halimeda tuna, Flabellia petiolata, Dictyota dichotoma, Padina pavonica,
and Acetabularia acetabulum.

Halimeda tuna Flabellia petiolata

Source of variation df MS F P MS F P
T 1
D 1 0.114 13.3 0.035
L3D 1
S3D 1
T3S3P 1 0.001 208 0.044
L3S3P 1 0.013 2740 0.012
T3L3D3P 1
T3S3D3P 1
T3L3S3D3P 1 46.34 5.78 0.019
Residual 64 8.015 0.008
Pooled term 65 0.007

Transformation None Angular

Cochrans C test C 5 0.17, P . 0.05 C 5 0.13, P . 0.05
Notes: Treatments are as in Table 1. The analyses were run using the percent cover values of each species in each plot
averaged over sampling dates as the dependent variable. Tests of terms involved in significant higher order interactions are
not shown, because there are no hypotheses related to them (Underwood 1997). Only significant terms (P , 0.05) are shown.
Denominator mean square of F ratio 5 ([T 3 D] 1 [L 3 D] 1 [T 3 L 3 D]).
Denominator mean square of F ratio 5 ([T 3 L] 1 Residual).
\ Denominator mean square of F ratio 5 ([T 3 L 3 D] 1 Residual).
Denominator mean square of F ratio 5 ([T 3 L 3 S 3 D 3 P] 1 Residual).

Levin 1981). Restoration of a dense mat takes longer,
and thickness rather than cover of the turf appears to
be affected more by the intensity of disturbance and
smothering by sediment (Airoldi and Virgilio 1998).
Severe disturbance of the assemblage allowed the
invasion of some erect annual species which, other-
wise, were scattered or rare at the study site. These
species, which occur commonly in other Mediterranean
subtidal habitats and are more abundant higher on the
shore at the study site, where the filamentous algae do
not form an extensive mat, appeared to exploit oppor-
tunistically bare gaps in the turf. Their colonization
was dependent highly on the timing of disturbance,
probably reflecting different reproductive periodicities.
Dictyota dichotoma, which attains reproductive ma-
turity shortly after it first appears, recruited more abun-
dantly in plots cleared in June. In contrast, Padina
pavonica and Acetabularia acetabulum, which release
reproductive structures shortly before they become se-
nescent, colonized plots cleared in December. The dif-
ficulty of following the experimental plots for .1 yr
prevented determination of whether these species per-
sisted over time. Nevertheless, inspection of the plots
that could be relocated in summer 1996 and observa-
tions gathered in the area over several years indicate
that these annual species can colonize and grow to
adulthood in disturbed areas, but usually are unable to
replace themselves locally.
Patterns of recovery of the erect algae suggest that
the turf pre-empts space and inhibits the invasion of
species that recruit only from the seasonal germination
of propagules, relegating them to the status of fugitive
species. Analogous conclusions were obtained by Sou-
sa et al. (1981) for turf-forming red algae in the low
intertidal zone of southern California. These authors
suggested that, in areas where grazing by urchins is
low, large brown algae do not form a persistent canopy
because disturbances are neither frequent nor intense
enough to generate the space required to ensure the
persistence of local populations. Possible mechanisms
by which algal turfs interfere with the recruitment of
sexual algae have already been discussed by these au-
thors and probably include the ability of the turf to
entrap large amounts of sediment (Scoffin 1970, Ken-
drick 1991). Such ability could also limit grazing by
urchins or other herbivores, which have been suggested
to be deterred by the presence of sediment in the habitat
(DAntonio 1986, McGuinness 1987). No experimental
data actually support these hypotheses, and further in-
vestigation is necessary to elucidate the mechanisms
of interaction between algal turfs and erect algae.
The results of this study suggest that the success
of Polysiphonia setacea turf in becoming established
over rocky surfaces and in persisting from year to
year as the dominant algal form depends on its ability
to retain and regain substratum over a large range of
environmental conditions and to prevent invasion by
potential competitors. This conclusion is somewhat
at odds with the general paradigm that a species can
be good at resisting either invasion or disturbance.
The assumption of this trade-off in species-specific
abilities is central to both equilibrium and nonequi-
librium models predicting a greatest number of spe-
cies at intermediate levels of disturbance (Petraitis
et al. 1989, Tilman 1990). According to these mod-
els, disturbance should ensure the global persistence
of species that go extinct locally and prevent dom-
ination by competitively superior and/or long-lived
December 1998 DETERMINANTS OF SPATIAL DOMINANCE 2767

TABLE 2. Extended.

Dictyota dichotoma Padina pavonica Acetabularia acetabulum

MS F P MS F P MS F P
11.52 4.46 0.038
6.095 3116 0.011
0.565\ 4.24 0.044
0.003 366 0.033

0.025 4.67 0.034

1.448 10.8 0.001

0.005 2.620 0.133

2.581 0.133

Angular None Cubic-root

C 5 0.11, P . 0.05 C 5 0.17, P . 0.05 C 5 0.13, P . 0.05

species (Dayton 1971, Connell 1978, Lubchenco
1978, Sousa 1979 b , Paine and Levin 1981, Dethier
1984). The spatiotemporal heterogeneity in resource
availability generated in marine and terrestrial hab-
itats by localized disturbances should, therefore, af-
fect the composition of neighboring patches depend-
ing on the size and intensity of disturbance to which
each was subjected (Sousa 1984 b ). In this study,
variable size and intensity of disturbance and vari-
able amounts of sediment influenced the success of
sexual annual algae but did not affect spatial dom-
inance by the turf, which retained substratum in all

FIG. 4. Effects of sediment deposition and patch size on patterns of recovery of the erect alga Dictyota dichotoma following
abrasion or removal of the biota in plots in June and December 1994. Data are mean percent covers (61 SE) pooled across
two stations (n 5 6 replicates as in Fig. 1).
2768 LAURA AIROLDI Ecology, Vol. 79, No. 8

FIG. 5. Effects of sediment deposition and patch size on patterns of recovery of the erect alga Acetabularia acetabulum
following abrasion or removal of the biota in plots in June and December 1994. Data are mean percent covers (61 SE) pooled
across two stations (n 5 6 replicates as in Fig. 1).

the plots, independently of the disturbance and stress
regimes imposed.
The importance of life histories in mediating spatial
dominance is beginning to be appreciated in terrestrial
and marine systems (Jackson 1977, Lovett Doust 1981,
Sousa et al. 1981, Schmid and Harper 1985, Bertness
and Ellison 1987) and patterns of growth have been
suggested to be as crucial as the disturbance regime in
determining community structure (Huston 1979). The
results of this study clearly indicate the importance of
vegetative propagation as a structuring factor in this
turf-dominated assemblage. The rapid mode of growth
of this turf is probably at the basis of its capability
either to compete for space and recover from distur-
bance. Packaging of abilities to compete and to re-
sist disturbance has been also observed in some chei-
lostome bryozoans with zooidal budding (Hughes and
Jackson 1992) and could be more common than gen-
erally thought. This would have important implications
for the development of predictive models of patch and
community dynamics. According to Petraitis et al.
(1989), when a species or group of species is moder-
ately resistant to both disturbance and invasion, diver-
sity patterns should be opposite to those predicted by
the intermediate disturbance hypothesis, and domi-
nance should be maximal at intermediate levels of dis-
turbance.
In the last 20 yr, there appears to have been a world-
wide trend of increasing abundance of algal turfs (Air-
oldi et al. 1995a and references therein) that has been
related by many authors to enhanced levels of distur-
bance (e.g., by sediment loads) in coastal areas (Thom
and Widdowson 1978, Seapy and Littler 1982, Airoldi
et al. 1995a). Geographical differences in the regimes
of physical and biological disturbance also used to ac-
count for latitudinal variation in patterns of spatial
dominance by turfs and canopy algae (Lubchenco
1980, Sousa et al. 1981). The potential role of changes
of the regimes of disturbance has been dramatically
shown for Caribbean coral reefs, where expanding fish-
ing pressure together with hurricane damage and mass
mortality of urchins has resulted in a phase shift be-
tween communities dominated by corals to commu-
nities dominated by macroalgae (Knowlton 1992,
Hughes 1994). The prediction of threshold levels of
disturbance is pressing to environmental management
(Underwood 1996). This field experiment could cover
only a small range of sizes compared to all possible
December 1998 DETERMINANTS OF SPATIAL DOMINANCE
scales of disturbance and did not include temporal vari-
ation in the frequency of disturbance. Nevertheless, in
the light of the present results, the idea that the prev-
alence of space-monopolizing structures, such as fila-
mentous algal turfs, relates to their ability to withstand
physical and biotic challenges seems to be a realistic
model. Thus, these turfs should be favored by inter-
mediate levels of disturbance. Verification of this sce-
nario will require further experimental research, which
should include large-scale temporal and geographic
comparisons among systems with different regimes of
disturbance and stress.
ACKNOWLEDGMENTS
This work was supported by a Postdoctoral Fellowship of
the Universita di Pisa. I wish to thank L. Benedetti-Cecchi,
J. B. C. Jackson, G. A. Kendrick, A. J. Underwood, and two
anonymous reviewers for stimulating comments on the manu-
script. J. B. C. Jackson gave substantial inputs to the work
and helped clarifying the ideas and presentation of the data.
A. J. Underwood gave important advice on the statistical
analyses. F. Rindi kindly updated me on the results of his
experiments on patterns of growth of P. setacea. F. Cinelli
provided space and facilities at the Dipartimento di Scienze
dellUomo e dellAmbiente of the Universita di Pisa. A very
special thank goes to M. Abbiati, for his patience and his
continuous support in ideas, energy, and field work during
all these years. I am grateful to all.
LITERATURE CITED
Adey, W. H., and T. Goertemiller. 1988. Coral reef algal turfs:
master producers in nutrient poor seas. Phycologia 26:374
386.
Airoldi, L., and F. Cinelli. 1997. Effect of sedimentation on
subtidal macroalgal assemblages: an experimental study
from a Mediterranean rocky shore. Journal of Experimental
Marine Biology and Ecology 215:271290.
Airoldi, L., and M. Virgilio. 1998. Responses of turf-forming
algae to spatial variations in the deposition of sediments.
Marine Ecology Progress Series 165:271282.
Airoldi, L., M. Fabiano, and F. Cinelli. 1996. Sediment de-
position and movement over a turf assemblage in a shallow
rocky coastal area of the Ligurian Sea. Marine Ecology
Progress Series 133:241251.
Airoldi, L., F. Rindi, and F. Cinelli. 1995a. Structure, sea-
sonal dynamics and reproductive phenology of a filamen-
tous turf assemblage on a sediment influenced, rocky sub-
tidal shore. Botanica Marina 38:227237.
Airoldi, L., F. Rindi, L. Piazzi, and F. Cinelli. 1995b. Dis-
tribuzione di Polysiphonia setacea (Rhodomelaceae: Rho-
dophyta) Hollenberg in Mediterraneo e possibili modalita
di diffusione. Biologia Marina Mediterranea 2:343344.
Barden, L. S. 1981. Forest development in canopy gaps of
a diverse hardwood forest in the southern Appalachian
Mountains. Oikos 37:205209.
Bazzaz, F. A. 1979. The physiological ecology of plant suc-
cession. Annual Review of Ecology and Systematics 10:
351371.
Benedetti-Cecchi, L., and F. Cinelli. 1996. Patterns of dis-
turbance and recovery in littoral rock pools: nonhierarch-
ical competition and spatial variability in secondary suc-
cession. Marine Ecology Progress Series 135:145161.
Bertness, M. D., and A. M. Ellison. 1987. Determinants of
patterns in a New England salt marsh plant community.
Ecological Monographs 57:129147.
Brokaw, N. V. L. 1985. Gap phase regeneration in a tropical
forest. Ecology 66:682687.
Burke, M. J. W., and J. P. Grime. 1996. An experimental
2769
study of plant community invasibility. Ecology 77:776
790.
Connell, J. H. 1978. Diversity in tropical rain forest and
coral reefs. Science 199:13021310.
Connell, J. H., and R. O. Slatyer. 1977. Mechanisms of suc-
cession in natural communities and their role in community
stability and organization. American Naturalist 111:1119
1144.
Daly, M. A., and A. C. Mathieson. 1977. The effect of sand
movement on intertidal seaweeds and selected invertebrates
at Bound Rock, New Hampshire, USA. Marine Biology 43:
4555.
DAntonio, C. M. 1986. Role of sand in the domination of
hard substrata by the intertidal alga Rhodomela larix. Ma-
rine Ecology Progress Series 27:263275.
Dayton, P. K. 1971. Competition, disturbance, and com-
munity organization: the provision and subsequent utili-
zation of space in a rocky intertidal community. Ecological
Monographs 45:137159.
Dayton, P. K., V. Currie, T. Gerrodette, B. D. Keller, R. Ro-
senthal, and D. V. Tresca. 1984. Patch dynamics and sta-
bility of some California kelp communities. Ecological
Monographs 54:253289.
Dayton, P. K., M. J. Tegner, P. E. Parnell, and P. B. Edwards.
1992. Temporal and spatial patterns of disturbance and
recovery in a kelp forest community. Ecological Mono-
graphs 62:421445.
Dethier, M. N. 1984. Disturbance and recovery in intertidal
pools: maintenance of mosaic patterns. Ecological Mono-
graphs 54:99118.
Dethier, M. N., E. S. Graham, S. Cohen, and L. M. Tear.
1993. Visual versus random-point percent cover estima-
tions: objective is not always better. Marine Ecology
Progress Series 110:918.
Devinny, J. S., and L. A. Volse. 1978. The effect of sediments
on the development of Macrocystis pyrifera gametophytes.
Marine Biology 48:343348.
Farrell, T. M. 1989. Succession in a rocky intertidal com-
munity: the importance of disturbance size and position
within a disturbed patch. Journal of Experimental Marine
Biology and Ecology 128:5773.
Grime, J. P. 1977. Evidence for the existence of three primary
strategies in plants and its relevance to ecological and evo-
lutionary theory. American Naturalist 111:11691194.
Hawkins, S. J. 1983. Interactions of Patella and macroalgae
with settling Semibalanus balanoides (L.). Journal of Ex-
perimental Marine Biology and Ecology 71:5572.
Hay, M. E. 1981. The functional morphology of turf forming
seaweeds: persistence in stressful marine habitats. Ecology
62:739750.
Holt, R. D., G. R. Robinson, and M. S. Gaines. 1995. Veg-
etation dynamics in an experimentally fragmented land-
scape. Ecology 76:16101624.
Hughes, T. P. 1994. Catastrophes, phase shifts, and large-
scale degradation of a Caribbean coral reef. Science 265:
15471551.
Hughes, T. P., and J. B. C. Jackson. 1992. Distribution and
abundance of cheilostome bryozoans on the Caribbean
reefs of Central Panama. Bulletin of Marine Science 51:
443465.
Huston, M. 1979. A general hypothesis of species diversity.
American Naturalist 113:81101.
Jackson, J. B. C. 1977. Competition on marine hard sub-
strata: the adaptive significance of solitary and colonial
strategies. American Naturalist 111:743767.
. 1979. Morphological strategies of sessile animals.
Pages 499555 in G. P. Larwood and B. R. Rosen, editors.
Biology and systematics of colonial organisms. Academic
Press, New York.
2770 LAURA AIROLDI
. 1991. Adaptation and diversity of reef corals.
BioScience 41:475482.
Kay, A. M., and M. J. Keough. 1981. Occupation of patches
in the epifaunal communities on pier pilings and the bivalve
Pinna bicolor at Edithburg, South Australia. Oecologia 48:
123130.
Kendrick, G. A. 1991. Recruitment of coralline crusts and
filamentous turf algae in the Galapagos archipelago: effect
of simulated scour, erosion and accretion. Journal of Ex-
perimental Marine Biology and Ecology 147:4763.
Knowlton, N. 1992. Thresholds and multiple stable states in
coral reef community dynamics. American Zoologist 32:
674682.
Littler, M. M., and D. S. Littler. 1980. The evolution of
thallus form and survival strategies in benthic marine mac-
roalgae: field and laboratory tests of a functional form mod-
el. American Naturalist 116:2544.
Lovett Doust, L. 1981. Population dynamics and local spe-
cialization in a clonal perennial (Ranunculus repens). I. The
dynamics of ramets in contrasting habitats. Journal of Ecol-
ogy 69:743755.
Lubchenco, J. 1978. Plant species diversity in a marine in-
tertidal community: importance of herbivore food prefer-
ence and algal competitive abilities. American Naturalist
112:2339.
. 1980. Algal zonation in the New England rocky
intertidal community: an experimental analysis. Ecology
61:333344.
McGuinness, K. A. 1987. Disturbance and organisms on
boulders. I. Patterns in the environment and community.
Oecologia 71:409419.
Menge, B. A., and J. P. Sutherland. 1987. Community reg-
ulation: variation in disturbance, competition, and preda-
tion in relation to environmental stress and recruitment.
American Naturalist 130:730757.
Paine, R. T., and S. A. Levin. 1981. Intertidal landscapes:
disturbance and the dynamics of pattern. Ecological Mono-
graphs 51:145178.
Palumbi, S. R., and J. B. C. Jackson. 1982. Ecology of cryp-
tic coral reef communities. II. Recovery from small dis-
turbance events by encrusting bryozoa: the influence of
host species and lesion size. Journal of Experimental
Marine Biology and Ecology 64:103115.
Petraitis, P. S., R. E. Latham, and R. A. Niesenbaum. 1989.
The maintenance of species diversity by disturbance. Quar-
terly Review of Biology 64:393418.
Pickett, S. T. A., and P. S. White, editors. 1985. The ecology
of natural disturbance and patch dynamics. Academic
Press, London, UK.
Rogers, C. S. 1990. Responses of coral and reef organisms
to sedimentation. Marine Ecology Progress Series 62:185
202.
Schmid, B., and J. L. Harper. 1985. Clonal growth in grass-
land perennials. I. Density and pattern-dependent compe-
tition between plants with different growth forms. Journal
of Ecology 73:793808.
Scoffin, T. P. 1970. The trapping and binding of subtidal
carbonate sediments by marine vegetation in Bimini la-
goon, Bahamas. Journal of Sedimentary Petrology 40:249
273.
Seapy, R. P., and M. M. Littler. 1982. Population and species
diversity fluctuations in a rocky intertidal community rel-
ative to severe aerial exposure and sediment burial. Marine
Biology 71:8796.
Shumway, S. W., and M. D. Bertness. 1994. Patch size effects
on marsh plant secondary succession mechanisms. Ecology
75:564568.
Ecology, Vol. 79, No. 8
Smith, C. R., and S. J. Brumsickle. 1989. The effect of patch
size and substrate isolation on colonization modes and rate
in an intertidal sediment. Limnology and Oceanography 34:
12631277.
Sousa, W. P. 1979a. Experimental investigations of distur-
bance and ecological succession in a rocky intertidal algal
community. Ecological Monographs 49:227254.
. 1979b. Disturbance in marine intertidal boulder
fields: the nonequilibrium maintenance of species diversity.
Ecology 60:12251239.
. 1980. The responses of a community to disturbance:
the importance of successional age and species life histo-
ries. Oecologia 45:7281.
. 1984a. The role of disturbance in natural commu-
nities. Annual Review of Ecology and Systematics 15:363
391.
. 1984b. Intertidal mosaics: patch size, propagule
availability, and spatially variable patterns of succession.
Ecology 65:19181935.
Sousa, W. P., S. C. Schroeter, and S. D. Gaines. 1981. Lat-
itudinal variation in intertidal community structure: the in-
fluence of grazing and vegetative propagation. Oecologia
48:297307.
Steneck, R. S., and M. N. Dethier. 1994. A functional group
approach to the structure of algal-dominated communities.
Oikos 69:476498.
Stewart, J. G. 1982. Anchor species and epiphytes in inter-
tidal algal turf. Pacific Science 36:4559.
. 1989. Establishment, persistence and dominance of
Corallina (Rhodophyta) in algal turf. Journal of Phycology
25:436446.
Sutherland, J. P. 1974. Multiple stable points in natural com-
munities. American Naturalist 108:859873.
Taylor, P. R., and M. M. Littler. 1982. The roles of com-
pensatory mortality, physical disturbance, and substrate re-
tention in the development and organization of a sand-
influenced, rocky-intertidal community. Ecology 63:135
146.
Thom, R. M., and T. B. Widdowson. 1978. A resurvey of a
Yale Dawsons 42 intertidal transects on the southern Cal-
ifornia mainland after 15 years. Bulletin of the South Cal-
ifornia Academy of Science 77:113.
Tilman, D. 1990. Constraints and trade-offs: toward a pre-
dictive theory of competition and succession. Oikos 58:3
15.
Underwood, A. J. 1996. Detection, interpretation, prediction
and management of environmental disturbances: some roles
for experimental marine ecology. Journal of Experimental
Marine Biology and Ecology 200:127.
. 1997. Experiments in ecology. Their logical design
and interpretation using analysis of variance. Cambridge
University Press, Cambridge, UK.
Underwood, A. J., M. J. Kingsford, and N. L. Andrew. 1991.
Patterns in shallow subtidal marine assemblages along the
coast of New South Wales. Australian Journal of Ecology
6:231249.
Werner, P. A. 1977. Colonization success of a biennial
plant species: experimental field studies of species cohab-
itation and replacement. Ecology 58:840849.
Wilson, S. D., and D. Tilman. 1991. Interactive effects of
fertilization and disturbance on community structure and
resource availability in an old-field plant community. Oec-
ologia 88:6171.
Woods, K. D., and R. H. Whittaker. 1981. Canopyunder-
story interaction and the internal dynamics of mature hard-
wood and hemlockhardwood forests. Pages 305323 in
D. C. West, H. H. Shugart, and D. B. Botkin, editors. Forest
succession. Springer-Verlag, New York, New York, USA.