AMER. ZOOL., 34:463^*75 (1994)
Spatial and Temporal Patterns in Assemblages of
Temperate Reef Fish1
SALLY J. HOLBROOK
Department of Biological Sciences, University of California, Santa Barbara, California 93106
MICHAEL J. KINGSFORD
School of Biological Sciences, University of Sydney, Sydney, Australia
RUSSELL J. SCHMITT
Coastal Research Center, Marine Science Institute, University of California,
Santa Barbara, California 93106
AND
J O H N S. STEPHENS, J R .
Department of Biology, Occidental College, Los Angeles, California 90041
For reef fish in temperate marine regions, such components
of local assemblage diversity (i.e., within a reef) as species richness, total
fish density, and rank order of abundance can remain relatively constant
through time. Long-term data (17 years) for assemblages on 2 reefs in
Southern California revealed that, despite high turnover in rare species,
overall species richness was affected only moderately by major oceanographic disturbances. This resilience of the assemblage is in marked contrast to high temporal variation in densities exhibited by many local
populations of individual species, and it suggests that measurements of
diversity to indicate status of an assemblage should be used with caution.
Here we consider various processes and factors, together with the spatial
and temporal scales over which they operate, that can influence local
diversity (and its estimation) of reef fishes. Mechanisms that can "buffer"
local diversity of reef fishes include dispersal of young that inter-connects
subpopulations, high "inertia" in relative abundance and population
structures (especially for long-lived species), and broad ecological requirements of many species. These considerations suggest that the effect of
disturbances on local diversity of reef fishes will depend in part on the
magnitude, duration, frequency and spatial scale of the perturbation. While
long-term data are few, available information suggests that, due to life
history characteristics of the fish and the spatial and temporal scales at
which disturbances are likely to occur, assemblages of temperate marine
reef fish might be relatively resilient to environmental perturbations.
SYNOPSIS.
propagules (Sale, 1991a). A plethora of
investigations has explored mechanisms that
influence dynamics of local populations of
reeffishes.These have revealed that marked
temporal variation in abundance of local
populations can arise from the recruitment
process (see reviews by Doherty, 1991;
• From the Symposium The Contribution of Long- Doherty and Williams, 1988), as well as from
INTRODUCTION
A current perspective is that the structure
of local assemblages of marine reef fish varies substantially through time as a result of
highly variable recruitment of planktonic
%£^££ZZfi£&«&Zl££
temporal variation in local habitats and
Society of Zoologists, 26-30 December 1992, at Van- Other reef attributes (Holbrook et at., 1990a,
couver, British Columbia, Canada.
b). Based on these findings, it might be
463
464
S. J. HOLBROOK ETAL.
expected that local assemblages of such fish
also vary greatly in time. There have, however, been few long-term studies of diversity
of reef fish. Evidence presented here suggests that local assemblages of temperate
reef fish often do not exhibit especially great
temporal variability in species richness or
in overall number of individuals present,
despite substantial variation in abundances
of individual species. This raises the issue
of what factors affect species richness of reef
fishes, as well as what mechanisms may
buffer temporal variation in these assemblages.
Assemblages of temperate zone reef fish
are composed of a great variety of species
representing a range of body sizes, life history attributes, trophic relations and other
ecological characteristics. Many of the species live in close association with the structure of the reef itself, but others spend substantial periods in the water column above
the reef. They also vary greatly in fidelity
to the reef; some inhabit a reef for just a
portion of their lives, or only for a part of
each day or year. The multitude of ecological characteristics of thefishes,together with
(potentially changing) heterogeneity in reef
attributes, pose a daunting challenge to the
collection of adequate data on local diversity of reef fish assemblages.
Here we explore temporal patterns of
diversity for a local assemblage of temperate
reef fish, and consider sources of spatial and
temporal variation in abundance of reef
fishes from temperate North America and
Australia. We then discuss possible mechanisms that ameliorate the effects of environmental perturbations on local diversity.
Finally, since species richness is considered
an important ecological indicator (Solbrig,
1992), the utility of measures of diversity
for detecting anthropogenic disturbances is
discussed.
METHODS AND STUDY SITES
Field work was conducted on rocky reefs
<20 m water depth at several locations in
California, USA [Santa Cruz Island (34°5'N,
119°45'W; see Schmitt and Holbrook,
1990a, b) and the mainland coast at Palos
Verdes Point and King Harbor (33°50'N,
118°20'W; see Stephens and Zerba, 1981;
Stephens et ai, 1984)] and in New South
Wales, Australia [Cape Banks, near the Botany Bay entrance (34°S, 151°13'E; see
Underwood et ai, 1991)]. Reefs in each
location were covered primarily with turf (a
low growing mixture of small plants, colonial animals, and debris) and various foliose
macroalgae including kelps (Macrocystis
pyrifera in California; Ecklonia radiata in
Australia). Localized areas of barrens, sampled on the Australian reefs, were devoid of
macroalgae and were covered with encrusting coralline algae. The pool of coastal reefdwelling fish in each area is approximately
100-200 species.
Estimates of species occurrences and densities were made using visual counts by
divers along isobathic transects, ranging
from 3 to 20 m bottom depth. Multiple
counts were made per year (at Palos Verdes,
King Harbor, and Australia) or annually (at
Santa Cruz Island). Detailed sampling
methodologies are presented elsewhere (e.g.,
Holbrook et ai, 1990a, b; Schmitt and Holbrook, 1990a, b; Stephens, 1983; Stephens
and Zerba, 1981; Stephens et ai, 1984).
Species richness reported for reefs at Palos
Verdes and King Harbor cover the 17 year
period of 1974-1990.
Bottom cover on the reefs at Santa Cruz
Island was characterized using a random
point contact method at the time fish were
counted (see Schmitt and Holbrook, 1986),
providing estimates of percent cover of turf
and various species of common understory
macroalgae. When present, abundance of
giant kelp was estimated in band transects
(Schmitt and Holbrook, 1990a; Holbrook
etai, 1990a, b).
The relationships between temporal variation in biological cover on a reef and in
densities of 2 species of fish (black surfperch, Embiotocajacksoni, and striped surfperch, E. lateralis) were explored. Coefficients of variation, based on annual
estimates of cover and densities taken
between 1982-1990 at 11 reefs on Santa
Cruz Island were calculated and regressions
performed between CVs for biological cover
and for density of each fish (see Holbrook
etai, 1993).
465
TEMPERATE FISH ASSEMBLAGES
TABLE 1. Spatial scales of variation in assemblages offish.
Scale
Mechanism(s)
Examples
Among habitats
Variation in resources
Attributes of physical environment
Behrents, 1987
Bodkin, 1988
Carr, 1989, 1991a, b
Choat and Ayling, 1987
Connell and Jones, 1991
DeMartini and Roberts, 1990
Holbrookand Schmitt, 1984
Holbrook et al, 1990a, b
Jones, 1984a, b, c
Leum and Choat, 1980
Moran and Sale, 1977
Moreno and Jara, 1984
Norman and Jones, 1984
Among depths
Variation in resources
Attributes of physical environment
Among reefs
Variation in resources
Attributes of physical environment
Diversity of habitats
Oceanographic influences
Hixon, 1980
Holbrook and Schmitt, 1986, 1989
Kingsford et al., 1989
Larson and DeMartini, 1984
Leum and Choat, 1980
McCormick, 1989
Terry and Stephens, 1976
Choat and Ayling, 1987
Choat etal, 1988
Cowen, 1985
Cowen and Bodkin, 1993
Holbrook et al., 1990a, b
Jessee<?Z al., 1985
Kingsford, 1989
Kingsford and Choat, 1989
Leum and Choat, 1980
McCormick, 1989
RESULTS AND DISCUSSION
Factors affecting the estimation of
local diversity of reef fish assemblages
The local occurrence and density of individual species of reef fish are subject to substantial spatial and temporal variation (e.g.,
Jones, 1988; Kingsford, 1988; Choat et al.,
1988; examples in Tables 1, 2). Understanding the sources of this variation is critical to interpretation of patterns of local
diversity, and is necessary for mechanistic
insight and for addressing issues of scaledependence. With respect to temporal patterns of diversity, or comparisons among
assemblages, it is especially important to
minimize artifacts introduced from sampling design. Below is a summary of some
of the known causes of variation (together
with their scale) in reef fish populations that
should be considered in the design of programs that estimate local diversity. Our
intent is not to review the large literature
on this topic, but to provide illustrations of
the sources and scales of variation that need
to be considered.
With respect to variation in space, substantial differences in occurrence and density of fishes can occur at relatively small
spatial scales, such as among habitats or
depths within a reef (e.g., Choat and Ayling,
1987; Holbrook et al., 1990a). For instance,
the territorial herbivore Parma microlepis
exhibits marked variation among habitats
on Australian reefs; it is abundant in urchin
barren grounds, but uncommon in adjacent
patches of kelp forest over the same depth
range (Fig. 1). Such variation among local
habitats is typical of many species on temperate reefs, and often results from spatial
variation in critical resources or in physical
attributes of the reefs (Table 1).
Many examples of larger-scale spatial
variability infishassemblages also have been
466
S. J. HOLBROOK ET AL.
TABLE 2. Temporal scales of variation in assemblages offish.
Scales
Examples
Mechanism(s)
Within day
Time of day
Tide
Bray, 1981
Hobson, 1965
Hobson and Chess, 1976
Jones, 1983
Kingsford and MacDiarmid, 1988
Within month
Lunar cycle
Within year
Seasons
Habitat alteration
Among years
Environmental disturbances
Habitat alteration
Oceanographic events
Ochi, 1989
Thresher et ai, 1989
Carr, 1991a, b
Matthews, 1990
Schmitt and Holbrook, 1986
Terry and Stephens, 1976
Cowen, 1985
Cowen and Bodkin, 1993
Ebelinge/a/., 1980
Ebeling «tf a/., 1985
Ebelingand Laur, 1988
Love etal, 1991
Schmitt and Holbrook, 1990a, b
Stephens et al., 1984
Stephens and Zerba, 1981
> 10 years
Long-term environmental change
Oceanographic events
documented, arising in part from oceanographic processes (Cowen, 1985; Kingsford,
1989; Table 1). Along the coast of Northland, New Zealand, oceanographic conditions vary considerably both along and
across the shelf. Cool water upwellings and
warm water intrusions to the northern region
generally move southward. Different water
masses therefore are likely to differ in composition and abundance of zooplankton,
Choat etal., 1988
Ebeling et ai, 1990
Stephens et al, 1986
thereby influencing the food available for
larval and adult planktivorous fishes among
reefs (Kingsford, 1989).
Temporal variation in abundance of local
populations of reef fish is found on scales
ranging from within a day to periods greater
than ten years. This variation can be attributed to a wide variety of causes (Table 2),
including dynamics in characteristics of a
reef and the fish themselves. Such features
as urchin barrens or presence of a kelp bed
URCHIN BARRENS
KELP FOREST
1967
1968
YEAR
FIG. 1. Density of Parma microlepis (Pomacentridae)
from May 1987 in two reef habitats near Cape Banks,
Botany Bay, Australia. Given are means (± 1 SE), n =
6 25 x 5 m transects.
1969
1990
1991
1992
YEAR
FIG. 2. Density of Hypoplectrodes maccullochi (Serranidae) in barrens habitat near Cape Banks, Botany
Bay, Australia. Given are means (± 1 SE), n = 6 25 x
5 m transects.
467
TEMPERATE FISH ASSEMBLAGES
CO
CO
LU
Z
g
rr
CO
LLJ
1988
1990
1991
1992
YEAR
5 -
o111
Q.
CO
FIG. 3. Density of Parupeneus signatus (Mullidae) in
barrens habitat near Cape Banks, Botany Bay, Australia. No fish were observed in kelp habitat. Given are
means (± 1 SE), n = 6 25 x 5 m transects.
SUMMER
WINTER
SUMMER
can remain constant for long periods, or
show a relatively rapid transition to a new
20
state (Holbrook et ai, 1990a, b). With
respect to characteristics of fish, some LU
mechanisms operate over very short time O
15
frames, such as within a day or a few weeks,
and typically are related to behavior of indi8
viduals {e.g., feeding migrations); others
occur over much longer time frames and
typically arise from demographic processes.
Invariably, component species in any given <
5
assemblage will differ greatly in these
responses, and thus in the degree of temporal variation in abundance exhibited.
Consequently, some species have relatively
constant population sizes, such as the terSUMMER WINTER SUMMER
ritorial pomacentrid Parma microlepis
which varied little over 5 years (Fig. 1). Other
SEASON
species undergo regular seasonal movements of adults on and off reefs, such as the FIG. 4. Seasonal patterns of species richness (top graph)
piscivore Hypoplectrodes maccullochi at and density (bottom) of tropical species in the shallows
Cape Banks that shows regular peak adult of a temperate reef near Cape Banks, Botany Bay, Ausabundances during the Austral autumn (Fig. tralia, from November, 1991.
2). The regular fluctuation in Hypoplectrodes may result from seasonal aggregation from strong recruitment events, which do
to this barrens habitat because its p r e y recruits of other fishes—are abundant in not occur each year.
Because many species of reef fishes have
summer and autumn, and/or because adults
a
planktonic
larval stage, wide-scale oceanmove to deep reef for spawning in spring
ographic
events
can alter the character of
(Webb and Kingsford, 1992). Finally, pulses
an
assemblage.
For instance, during the
of recruitment of young that may vary
summer
the
warm
East Australian current
annually in intensity can produce irregular
sweeps
down
the
coast
of Australia from the
patterns of abundance of a species on a reef.
Parupeneus signatus typifies this pattern tropics, bringing with it the larvae of a num(Fig. 3); occasional peaks in abundance result ber of tropical species (including Pomacentridae: Abudefdufvaigiensis, A. sexfasciatus.
S
468
z
i
o
a.
S. J. HOLBROOK ET AL.
be most useful if they are backed up by
information on shorter scale variability
coupled with mechanistic studies. Longterm data sets will be particularly difficult
to interpret correctly if sampling is too infrequent and knowledge of the major sources
of variability too little.
Observed temporal patterns of
local diversity in a
temperate reef assemblage
197S
1980
1982
19B4
Unlike variation over spatial and short
YEAR
temporal scales, little information exists on
FIG. 5. Species richness of teleost fishes at King Har- long-term dynamics of reef fish assembor (triangles) and Palos Verdes Point (circles), Cali- blages. Two 17 year data sets for fish assemfornia, USA. Arrows indicate periods of major envi- blages at King Harbor and Palos Verdes
ronmental disturbances.
Point, CA represent some of the best longterm information available on temperate
Pomacentrus coelestis, P. bankanensis; reeffishes.Identical sampling methods were
Labridae: Thalassoma lunare, T. amblyce- used, which facilitates comparison of
phalum, Halichoeres nebulosus, Stethojulis assemblage structures. Further, the 2 sites
interrupta; Acanthuridae: Acanthurus trios- are separated by only about 10 km, and
tegus). In this case, there is a regular annual hence "sample" the same pool of species.
input of tropical species to the temperate Nonetheless, species richness was consisreef communities at Cape Banks, followed tently higher at King Harbor (Fig. 5), reflectby subsequent dieoff during the following ing a greater range in types of local habitats
months (Fig. 4). These tropical species can and environmental conditions compared
account for up to 20% of the species richness with the Palos Verdes reef (Stephens and
of noncryptic fish in shallow water on local Zerba, 1981; Stephens et ai, 1984, 1993).
reefs.
With respect to temporal patterns, neither
Finally, species in any given assemblage assemblage displayed wild fluctuations in
typically represent a wide range in longevity species richness through time (Fig. 5). The
of individuals. Some species are relatively greatest declines in species richness (about
short-lived, such as surfperches (Embioto- 25 and 33%) occurred simultaneously at
cidae) in California which typically live for both sites in 1977; thereafter richness
< 5 years, whereas others, such as rockfishes remained relatively constant. Additional,
(Scorpaenidae), are capable of surviving for smaller declines can be discerned in 1983
several decades. This results in differences and in 1987 for King Harbor; in both of
among species in population inertia or resis- these cases, the assemblage appeared to
tance to change (Warner and Hughes, 1988; return rapidly to its more recent richness
so called "storage effects"). A sampling pro- (Fig. 5; also see Stephens et ai, 1993).
gram of a given length estimates change for
During this 17 year period, 3 major envidifferent numbers of generations of the ronmental disturbances occurred in the
component species.
Southern California Bight, and likely caused
Clearly, estimates of species richness or the observed depressions in species richness
diversity for reef fish assemblages will vary (Stephens and Zerba, 1981; Stephens et ai,
within and among reefs depending on the 1984, 1988, 1993). The 3 declines in richtemporal or spatial scale considered. Vari- ness coincided with periods of broad scale
ability arising from periodic or gradually oceanographic disturbances (Fig. 5): the first
changing oceanographic features will require 2 (1977, 1983) were El Nino-Southern
long-term data sets to both describe the pat- Oscillation (ENSO) phenomena, which in
terns of variability and suggest underlying the Southern California Bight result in above
mechanisms. Even so, long-term data will average ocean temperatures and an increase
469
TEMPERATE FISH ASSEMBLAGES
0.30
KING HARBOR
0.20
<n
n
a 5
Q
Q_
CO
1974
197B
1976
I960
1962
1984
YEAR
FIG. 6. Total density of adult teleost fishes at King
Harbor, California, USA. Arrows indicate periods of
major environmental disturbances.
n
Ifln
1 2 3 4 5 6 7 8
J3
o
•V
O
9 1 0 1 1 1 2 13 14 1 5 1 6 1 7
O
O
-n
LJJ
CO
CO
TJ
PALOS VERDES
Q
m
w
0.20
in the frequency and intensity of winter
storms. These in turn can alter greatly reef
structures and resources {e.g., destruction of
kelp forest; Tegner and Dayton, 1987; Dayton et ai, 1992). The third disturbance was
a series of especially severe storms during
the fall/winter period of 1987-1988,
including a once-in-a-100-year magnitude
storm that extensively damaged reef structures at the study sites (Stephens et al, 1993).
The effect of each physical disturbance on
species richness varied with the length of
the interval between disturbances. Prior to
the El Nino event in 1977, the previous El
Nino that severely affected the Southern
California Bight occurred almost twenty
years earlier. The 1977 El Nino had the
greatest effect on species richness (Fig. 5).
Full recovery may not have occurred before
the second El Nino occurred just 6 years
later (1983); the latter disturbance was
accompanied by a comparatively smaller
decline in richness (Fig. 5). The major storm
activity 4 years after the second El Nino also
had a relatively small effect on richness.
Thus, while major oceanographic events
may adversely affect local species richness,
the magnitude of the effect may depend in
part on the length of time between disturbances.
It appears that different types of species
were affected adversely by the various disturbances. Like species richness, the total
abundance of adult fish (species combined)
at King Harbor was depressed after each of
Infinni Snr-.nrinr-.r-.nn
1 2 3 4 5 6 7 8 9 10 1112 13 14 15 16 17
NUMBER OF YEARS OBSERVED
FIG. 7. Frequency distribution of number of years
species of teleost fish were observed during 17 years at
King Harbor and Palos Verdes Point, California, USA.
Given are total number of species, and proportion of
the total number of species observed at each location,
that was present for 1-17 years.
the 3 major disturbances (Fig. 6). However,
the 1977 El Nino, which had the largest
effect on species richness, had the smallest
relative effect on overall fish abundance (Fig.
6). By contrast, the storms of 1987-1988
had the greatest effect on total number of
fish present (Fig. 6), but a comparatively
smaller impact on richness. This indicates
that the first El Nino disproportionately
affected rarer species (although some common species also were greatly affected), but
the hundred year storm had a relatively
greater effect on abundant species.
Despite the moderate constancy in richness of the assemblages at King Harbor and
Palos Verdes, there was a substantial degree
of turnover in the species present (Fig. 7).
For example, >25% of all species observed
at a site were seen in 2 or fewer of the 17
years. However, the 2 assemblages differed
470
S. J. HOLBROOK. ETAL.
with respect to the proportions of permanent "resident" species (seen every year) and
extreme "transient" species (observed in <2
years). A greater number of species was
observed in all 17 years at King Harbor (25
spp) than at Palos Verdes (11 spp) (Fig. 7).
By contrast, about the same number of species was seen in 2 or fewer years at King
Harbor (21) and Palos Verdes (22) (Fig. 7).
As a fraction of all species observed at a
site, King Harbor had a greater proportion
of "residents" (30% vs. 18%) and a lower
proportion of extreme "transients" (25% vs.
36%). However, at both sites the "residents" accounted for > 80% of all individuals observed during the study period.
Finally, the "open" nature of reef fish
assemblages is evidenced by the continual
accumulation of previously unseen species
through time. The cumulative species richness at both King Harbor and Palos Verdes
increased linearly after a steeper rise in the
initial 2 years (regressions of new species by
year for the last 15 years; for both assemblages: r2 > 0.96; P < 0.001). After the
initial 2 years, an average of 1.08 new species was observed per year at each site. There
was no indication of an asymptote in cumulative richness at either site. Over the 17
years, a total of 83 and 61 species of teleost
fishes were observed at King Harbor and
Palos Verdes respectively, which represents
on the order of 50-70% of the total recorded
in Southern California (Gotshall, 1981;
Eschmeyer et ai, 1983).
Mechanisms maintaining local diversity of
reef fish assemblages
Species richness of the King Harbor and
Palos Verdes assemblages was moderately
constant through time, and appeared to be
affected only by major oceanographic perturbations. Even so, the effect of these events
appeared small relative to the intensity of
the disturbances. This suggests that attributes of temperate reef fishes facilitate local
persistence in the face of environmental
perturbations. Several features have been
identified that contribute to persistence of
species on a reef, including a high degree of
"connectedness" among local populations,
"inertia" in relative abundances, and broad
ecological requirements of reef-dwelling life
stages.
Most reef fishes have a bipartite life cycle,
which includes a young life stage that disperses in the plankton, and older life stages
that are much more sedentary on reefs (Sale,
1991 b). Consequently, their populations are
spatially divided in a patchy environment
(i.e., different reefs), with an individual reef
representing a local subpopulation (Mapstone and Fowler, 1988; Sale, 1991ft). Subpopulations are connected by the exchange
of propagules, and sometimes movements
of adults; recruits to a given reef are unlikely
to have been produced by the adults that
reside there. It is this decoupling between
local production and local recruitment,
combined with variability in planktonic
dispersal, that is thought to be centrally
important in governing dynamics of subpopulations (Doherty and Williams, 1988;
Doherty, 1991). While planktonic dispersal
can result in great fluctuations in the number of individuals of a given species on a
given reef, it also minimizes the probability
of local extinction by providing a supply of
young produced by other subpopulations
(Chesson, 1985; Chesson and Warner,
1981). Thus, dynamics of reef fishes with a
dispersing life stage perhaps are best
described in a metapopulation context (see
Roughgarden and Iwasa, 1986). Metapopulation dynamics can buffer variation in
overall abundance of a population (i.e., the
collection of connected subpopulations),
which results in a more constant "pool" of
reproductive output. Dispersal of that output provides the means to supply a local
reef with new individuals, regardless of the
presence or absence of locally reproducing
adults.
Rare species, of course, have a greater
probability of going extinct on a reef from
stochastic variation than those that locally
are more common. The long-term data on
assemblages at King Harbor and Palos Verdes indicate that rare species continually
appear and disappear. However, such turnover in rare species likely has little effect on
assemblage structure. Ebeling et al. (1990)
used randomization models to demonstrate
that substantial stochastic fluctuations in the
sizes of local populations had little effect on
the rank order of fish abundance on a reef.
Some reef fishes consistently are common,
whereas others remain rare; because of the
471
TEMPERATE FISH ASSEMBLAGES
disparity in mean abundances among species of reef fishes, especially large changes
in common species are necessary to alter
greatly the pattern of relative abundances.
Clearly, fluctuations in a subpopulation
can reflect both the supply of propagules and
events that transpire on the reef. Survival
and growth to older life stages will depend
in part on the local existence of appropriate
habitats and/or resources, and the abundance of such resources also can influence
the local density. On temperate reefs, macroalgae tend to be important in this context
by providing fish with sources of food (the
algae itself or associated animals), foraging
microhabitats, refuge from predators, and/
or by altering other aspects of the local environment (Jones, 1984a, b, c, 1988; Choat
and Ayling, 1987; DeMartini and Roberts,
1990; Holbrook et al, 1990a, b; Schmitt
and Holbrook, 1990a, b). Cover of macroalgae on a temperate reef can vary greatly
through time (Dayton, 1985; Dayton et al,
1984, 1992; Ebeling et al, 1985; Schiel and
Foster, 1986; Nisbet and Bence, 1989;
Underwood et al., 1991). Although little
long-term data exist on rates of change in
biotic cover on temperate reefs, the limited
information for Southern California indicates that the particular macroalgal assemblage on a reef can persist for a number of
years, but can rapidly change to a different
state (Holbrook et al., 1990a, b).
Surfperches on reefs in Southern California provide an excellent illustration of the
potential influence of temporally varying
resources on the local abundance of older
life stages on a reef. Unlike most reef fishes,
surfperch are viviparous and give birth to
large, non-dispersing juveniles; thus a population of surfperch is not spatially divided
among (widely spaced) reefs. This life history attribute removes variation due to the
supply of planktonically dispersed young,
which potentially obscures detection of a
relationship between availability of local
resources and density of older life stages.
Black surfperch (Embiotoca jacksoni) harvest crustacean food from algal turf, and
striped surfperch (E. lateralis) obtain prey
from foliose red algae on reefs. For each of
these surfperches, there was a strong, positive relationship between the degree of
temporal variation in the density of older
LLJ
Al
W
0
10
20
30
40
TEMPORAL VARIABILITY TURF (CV)
55
1
i
o
0.
0
20
40
60
TEMPORAL VARIABILITY GEUDIUM (CV)
FIG. 8. The relationship between temporal variability
in benthic cover (turf, Gelidium) and in densities of
the black surfperch (Embiotocidae), Embiotoca jacksoni (top; r2 = 0.73, P < 0.01) and striped surfperch
(Embiotocidae), Embiotoca lateralis (bottom; r2 = 0.47,
P < 0.05), at Santa Cruz Island, California, USA. Each
point represents a single reef over a 9 year period.
life stages on a reef and in the cover of its
primary foraging habitat—turf or red algae
(Fig. 8). Densities of adults were more variable on reefs where foraging habitat was
highly variable; reefs where these critical
habitats were temporally constant had
remarkably constant populations of surfperch.
While the abundance and variability of
reef resources can influence the abundance
and dynamics of a local fish population, it
should be noted that neither species of surfperch even approached local extinction on
any of the 11 reefs studied over the 9 year
period. Further, it is unlikely that fluctuations in surfperch populations were sufficiently great to alter their rank order of
abundance in the assemblage. Because surfperch lack a planktonically dispersed life
stage, this mechanism was not involved in
472
S. J. HOLBROOK. ET AL.
the persistence of these populations. This
suggests that, in general, local extinction of
a reef fish is likely only when a disturbance
eliminates all alternate reef resources needed
by the species; changes in rank order of
abundance require substantial alteration in
resources required by common species.
Anthropogenic impacts on diversity:
Issues of scale
Analyses of long-term data sets suggest
that the effect of an anthropogenic disturbance on local diversity of an assemblage
of reef fish will depend in part on the magnitude, spatial extent, and duration of the
perturbation. Because a population of a
demersal fish can be spatially divided among
reefs, important aspects determining the
effect of a disturbance will be its spatial
dimension relative to the area occupied and
number of component subpopulations
(reefs). The area occupied by a population
depends on the life history attributes of a
species, which determine the distance that
subpopulations effectively are interconnected by dispersal. For example, some
temperate reeffishesare viviparous and lack
a planktonic dispersal stage (e.g., surfperches). Thus, an entire population of these
species potentially can be affected by a highly
localized disturbance such as an ocean waste
water outfall. By contrast, a disturbance
must be more extensive in space (e.g., catastrophic pollution spill, intense over-fishing, winter storms, El Nino events) to affect
an entire population of species with planktonic dispersal. Even so, there likely is considerable variation in the areal extent of such
populations as the duration of the planktonic stage varies among reef fishes from
roughly 10 days to > 4 months (Brothers
et al, 1983; Victor, 1991). This and larval
behavior influence the dispersal distance of
propagules, and therefore the distance over
which subpopulations are connected. Even
relatively broadscale disturbances are
unlikely to result in regional extinction; for
example, most species in the King Harbor
and Palos Verdes assemblage occur along
> 1,500 km of coastline (Eschmeyer et al,
1983).
atively short-lived (e.g., El Nino event, pollution spill) or chronic (e.g., global ocean
warming). A given "pulse" or transitory disturbance is likely to affect species differently
depending on such characteristics as longevity and age structure. Populations of longlived individuals tend to be composed of
several age-classes; this "storage effect" can
buffer against fluctuations from perturbations of short duration (Warner and Chesson, 1985). Short-lived species have lower
population inertia, and therefore are more
likely to be affected by a disturbance of a
given duration.
Finally, attributes of marine reef fish
assemblages pose a serious challenge to the
detection of anthropogenic impacts on their
diversity. Hence, the utility of estimates of
diversity as a measure of the status of a reef
is suspect, and it will be important to develop
an understanding of the explicit relationship
between assemblage structure and function
(Caswell, 1976; for a recent review see Carney, 1994). Various sources of stochastic
variation, and indeed the processes and features that can buffer populations from disturbances, make it difficult to distinguish
natural variation from that imposed by
human activities. Detection of systematic
changes in relative abundances also will
require long-term data sets. Unfortunately,
such basic information is extremely rare for
reef fishes. The task of detecting impacts
probably will be more straightforward for
short-lived species with localized populations (e.g., viviparous surfperch), or those
which require specialized resources that are
at risk from human activities. However,
features that ease detection of effects may
hinder extrapolation to the assemblage as a
whole.
ACKNOWLEDGMENTS
We thank the many divers who assisted
underwater, especially D. Canestro, B. Williamson for technical assistance, and J.
Palmer (of SCE) for support. M. Steele provided helpful comments on the manuscript.
Financial support was provided by the US
National Science Foundation (OCE9102191 and earlier awards to SJH and RJS),
The potential effect on diversity also will and the University of Sydney Special Prodepend on whether the disturbance is rel- jects Grant (to MJK), and Southern Cali-
TEMPERATE FISH ASSEMBLAGES
fornia Edison Research and Development
(to JSS).
473
Islands, pp. 463-474. Santa Barbara Museum of
Natural History, Santa Barbara, California.
Dayton, P. K. 1985. Ecology of kelp communities.
Ann. Rev. Ecol. Syst. 16:215-245.
REFERENCES
Dayton, P. K., V. Currie, T. Gerrodette, B. Keller, R.
Rosenthal, and D. Van Tresca. 1984. Patch
Behrents, K. C. 1987. The influence of shelter availdynamics and stability of some southern Califorability on recruitment and early juvenile survinia kelp communities. Ecol. Monogr. 54:253-289.
vorship of Lythrypnus dalli Gilbert (Pisces: Gobiidae). J. Exp. Mar. Biol. Ecol. 107:45-59.
Dayton, P. K., M. J. Tegner, P. E. Parnell, and P. B.
Edwards. 1992. Temporal and spatial patterns
Bodkin, J. L. 1988. Effects of kelp forest removal on
of disturbance and recovery in a kelp forest comassociated fish assemblages in central California,
munity. Ecol. Monogr. 62:421-445.
J. Exp. Mar. Biol. Ecol. 117:227-238.
Bray, R. N. 1981. Influence of water currents and DeMartini, E. E. and D. A. Roberts. 1990. Effects of
giant kelp (Macrocystis) on the density and abunzooplankton densities on daily foraging movedance offishesin a cobble-bottom kelp forest. Bull.
ments of blacksmith, Chromis punctipinnis, a
Mar. Sci. 46:289-300.
planktivorous reef fish. Fish. Bull. U.S. 78:829Doherty, P. J. 1991. Spatial and temporal patterns
841.
in recruitment. In P. F. Sale (ed.), The ecology of
Brothers, E. B., D. McB. Williams, and P. F. Sale.
fishes on coral reefs, pp. 261 -293. Academic Press,
1983. Length of larval life in twelve families of
San Diego.
fishes at "One Tree Lagoon," Great Barrier Reef,
Doherty, P. J. and D. McB. Williams. 1988. The
Australia. Mar. Biol. 76:319-324.
replenishment of coral reef fish populations.
Carney, R. S. 1994. Marine benthic ecology in enviOceanogr. Mar. Biol. Ann. Rev. 26:487-551.
ronmental impact statements. In R. J. Schmitt and
C. W. Osenberg (eds.), Ecological impact assess- Ebeling, A. W., S. J. Holbrook, and R. J. Schmitt.
1990. Temporally concordant structure of a fish
ment: Conceptual issues and application in coastal
marine habitats. Univ. California Press, Los Angeassemblage: Bound or determined? Amer. Natur.
les.
135:63-73.
Carr, M. H. 1989. Effects of macroalgal assemblages Ebeling, A. W., R. J. Larson, W. S. Alevizon, and R.
N. Bray. 1980. Annual variability of reef-fish
on the recruitment of temperate zone reef fishes.
assemblages in kelp forests off Santa Barbara, CalJ. Exp. Mar. Biol. Ecol. 126:59-76.
ifornia. Fish. Bull. U.S. 78:361-377.
Carr, M. H. 1991a. Patterns, mechanisms, and consequences of recruitment of a temperate marine Ebeling, A. W. and D. R. Laur. 1988. Fish populations in kelp forests without sea otters: Effects of
reef fish. Ph.D. Diss., University of California,
severe storm damage and destructive sea urchin
Santa Barbara, California.
grazing. In G. VanBlaricom and J. Estes (eds.),
Carr, M. H. 1991 b. Habitat selection and recruitment
Community ecology of sea otters, pp. 169-191.
of an assemblage of temperate zone reef fishes. J.
Springer-Verlag, Berlin.
Exp. Mar. Biol. Ecol. 146:113-137.
Caswell, H. 1976. Community structure: A neutral Ebeling, A. W., D. R. Laur, and R. J. Rowley. 1985.
Severe storm disturbances and reversal of commodel analysis. Ecol. Monogr. 46:327-354.
munity structure in a southern California kelp forChesson, P. L. 1985. Coexistence of competitors in
est. Mar. Biol. 84:287-294.
spatially and temporally varying environments: A
look at the combined effects of different sorts of Eschmeyer, W. N., E. S. Herald, and H. Hammann.
1983. Afieldguide to Pacific Coastfishesof North
variability. Theor. Popul. Biol. 28:263-287.
America. Houghton Mifflin Company, Boston.
Chesson, P. L. and R. R. Warner. 1981. Environmental variability promotes coexistence in lottery Gotshall, D. W. 1981. Pacific coast inshorefishes.Sea
Challengers, Los Osos, California.
competitive systems. Amer. Natur. 117:923-943.
Choat,J.H.andA.M.Ayling. 1987. The relationship Hixon, M. A. 1980. Competitive interactions between
California reeffishesof the genus Embiotoca. Ecolbetween habitat structure and fish faunas on New
ogy 61:918-931.
Zealand reefs. J. Exp. Mar. Biol. Ecol. 110:257284.
Hobson, E. S. 1965. Diurnal-nocturnal activity of
some inshorefishesin the Gulf ofCalifornia. Copeia
Choat, J. H., A. M. Ayling, and D. R. Schiel. 1988.
1965:291-302.
Temporal and spatial variation in an island fish
fauna. J. Exp. Mar. Biol. Ecol. 121:91-111.
Hobson, E. S., Jr. and J. R. Chess. 1976. Trophic
interactions among fishes and zooplankters near
Connell, S. D. and G. P. Jones. 1991. The influence
shore at Santa Catalina Island, California. Fish.
of habitat complexity on postrecruitment proBull. U.S. 74:567-598.
cesses in a temperate reef fish population. J. Exp.
Mar. Biol. Ecol. 151:271-294.
Holbrook, S. J. and R. J. Schmitt. 1984. Experimental analyses of patch selection by foraging black
Cowen, R. K. 1985. Large scale patterns of recruitsurfperch (Embiotoca jacksoni Agazzi). J. Exp. Mar.
ment by the labrid, Semicossyphuspulcher. Causes
Biol. Ecol. 79:39-64.
and implications. J. Mar. Res. 43:719-742.
Cowen, R. K. and J. L. Bodkin. 1993. Annual and Holbrook, S. J. and R. J. Schmitt. 1986. Food acquisition by competing surfperch on a patchy enviSpatial Variation of the Kelp Forest Fish Assemronmental gradient. Envir. Biol. Fishes 16:135blage at San Nicolas Island, California. In D. M.
146.
Power (ed.), Third California Islands symposium:
Recent advances in research on the California Holbrook, S. J. and R. J. Schmitt. 1989. Resource
474
S. J. HOLBROOK ET AL.
overlap, prey dynamics, and the strength of competition. Ecology 70:1943-1953.
Holbrook, S. J., M. H. Carr, R. J. Schmitt, and J. A.
Coyer. 1990a. Effect of giant kelp on local abundance of reeffishes:The importance of ontogenetic
resource requirements. Bull. Mar. Sci. 47:104-114.
Holbrook, S. J., R. J. Schmitt, and R. F. Ambrose.
1990b. Biogenic habitat structure and characteristics of temperate reef fish assemblages. Aust. J.
Ecol. 15:489-503.
Holbrook, S. J., S. L. Swarbrick, R. J. Schmitt, and R.
F. Ambrose. 1993. Reef architecture and reef
fish: Correlations of population densities with
attributes of subtidal rocky environments. In C.
N. Battershill et al. (eds.), Proceedings of the Second International Temperate Reef Symposium, pp.
99-106. NIWA Marine, Wellington, NZ.
Jessee, W. N., A. L. Carpenter, and J. W. Carter. 1985.
Distribution patterns and density estimates of fishes
on a southern California artificial reef with comparisons to natural kelp-reef habitats. Bull. Mar.
Sci. 37:214-226.
Jones, G. P. 1983. Relationship between density and
Leum, L. and J. H. Choat. 1980. Density and distribution patterns of the temperate marine fish
Cheilodactylus spectabilis (Cheilodactylidae) in a
reef environment. Mar. Biol. 57:327-337.
Love, M. S., M. H. Carr, and L. J. Haldorson. 1991.
The ecology of substrate-associated juveniles of
the genus Sebastes. Envir. Biol. Fishes 30:225243.
Mapstone, B. D. and A. J. Fowler. 1988. Recruitment
and the structure of assemblages of fish on coral
reefs. Trends Ecol. Evol. 3:72-77.
Matthews, K. R. 1990. An experimental study of the
habitat preferences and movement patterns of
copper, quillback and brown rockfishes (Sebastes
spp.). Envir. Biol. Fishes 29:161-178.
McCormick, M. I. 1989. Spatio-temporal patterns in
the abundance and population structure of a large
temperate reef fish. Mar. Ecol. Prog. Ser. 53:215225.
Moran, M. J. and P. F. Sale. 1977. Seasonal variation
in territorial response, and other aspects of the
ecology of the Australian temperate pomacentrid
fish Parma microlepis. Mar. Biol. 39:121-128.
behaviour in juvenile Pseudolabrus celidotus Moreno, C. A. and H. F. Jara. 1984. Ecological studies on fish fauna associated with Macrocystis pyr(Pisces: Labridae). Anim. Behav. 31:729-735.
ifera belts in the Fueguian Islands, Chile. Mar.
Jones, G. P. 1984a. Population ecology of the temEcol. Prog. Ser. 15:99-107.
perate reef fish Pseudolabrus celidotus Bloch &
Schneider (Pisces: Labridae) I. Factors influencing Nisbet, R. M. and J. R. Bence. 1989. Alternative
recruitment. J. Exp. Mar. Biol. Ecol. 75:275-276.
dynamic regimens for canopy-forming kelp: A
variant on density-vague regulation. Amer. Natur.
Jones, G. P. 19846. Population ecology of a temper133:377^108.
ate reef fish Pseudolabrus celidotus Bloch &
Schneider (Pisces: Labridae): II. Factors influenc- Norman, M. D. and G. P. Jones. 1984. Determinants
ing adult density. J. Exp. Mar. Biol. Ecol. 75:277of territory size in the pomacentrid reeffish,Parma
303.
victoriae. Oecologia 61:60-69.
Jones, G. P. 1984c. The influence of habitat and Ochi, H. 1989. Mating behaviour and sex change of
the anemonefish, Amphiprion clarkii, in the tembehavioural interactions on the local distribution
perate waters of southern Japan. Envir. Biol. Fishes
of the wrasse, Pseudolabrus celidotus. Envir. Biol.
26:257-275.
Fishes 10:43-58.
Jones, G. P. 1988. Ecology of rocky reeffishof north- Roughgarden, J. and Y. Iwasa. 1986. Dynamics of a
metapopulation with space-limited subpopula. eastern New Zealand. N.Z. J. Mar. Freshwat. Res.
tions. Theor. Popul. Biol. 29:235-261.
22:445^162.
Kingsford, M. J. 1988. The early life history of fish Sale, P. F. 1991a. Reef fish communities: open nonequilibrial systems. In P. F. Sale (ed.), The ecology
in coastal waters of northern New Zealand: A
of fishes on coral reefs, pp. 564-600. Academic
review. N.Z. J. Mar. Freshwat. Res. 22:463-479.
Press, New York.
Kingsford, M. J. 1989. Distribution patterns of
planktivorous reef fish along the coast of north- Sale, P. F. 19916. The ecology offisheson coral reefs.
eastern New Zealand. Mar. Ecol. Prog. Ser. 54:13Academic Press, Inc., New York.
24.
Schiel, D. R. and M. S. Foster. 1986. The structure
of subtidal algal stands in temperate waters. Ann.
Kingsford, M. J. and A. B. MacDiarmid. 1988. InterRev. Oceanogr. Mar. Biol. 24:265-307.
relations between planktivorous reef fish and zooplankton in temperate waters. Mar. Ecol. Prog. Schmitt, R. J. and S. J. Holbrook. 1986. Seasonally
fluctuating resources and temporal variability of
Ser. 48:103-117.
interspecific competition. Oecologia 69:1-11.
Kingsford, M. J. and J. H. Choat. 1989. Horizontal
distribution patterns of presettlement reeffish:Are Schmitt, R.J. and S.J. Holbrook. 1990a. Contrasting
effects ofgiant kelp on dynamics of surfperch popthey influenced by the proximity of reefs? Mar.
ulations. Oecologia 84:419-429.
Biol. 100:285-297.
Kingsford, M. J., D. R. Schiel, and C. N. Battershill. Schmitt, R. J. and S. J. Holbrook. 19906. Population
responses of surfperch released from competition.
1989. Distribution and abundance of fish in a
Ecology 71(5):1653-1665.
rocky reef environment at the subantarctic Auckland Islands, New Zealand. Polar Biol. 9:179-186. Solbrig, O. T. 1992. The IUBS-SCOPE-UNESCO
program of research in biodiversity. Ecol. AppliLarson, R. J. and E. E. DeMartini. 1984. Abundance
cations 2:131-138.
and vertical distribution of fishes in a cobble-bottom kelp forest off San Onofre, California. Fish. Stephens, J. S., Jr. 1983. The fishes of King Harbor
Bull. U.S. 82:37-53.
A nine year study offishesoccupying the receiving
TEMPERATE FISH ASSEMBLAGES
waters of a coastal steam electric generating station. Research and Development Series 83-RD-1.
Occidental College, Los Angeles, California.
Stephens, J. S. Jr., J. E. Hose, and M. S. Love. 1988.
Fish assemblages as indicators of environmental
change in nearshore environments. In D. F. Soule
and G. S. Kleppel (eds.), Marine organisms as
indicators, pp. 91-105. Springer-Verlag, New York.
Stephens, J. S. Jr., G. A. Jordan, P. A. Morris, M. M.
Singer, and G. E. McGowen. 1986. Can we relate
larval fish abundance to recruitment or population
stability? A preliminary analysis of recruitment to
a temperate rocky reef. Cal COFI Rep. 27:65;-83.
Stephens, J. S. Jr., P. A. Morris, D. J. Pondella, T. A.
Koonce, and G. A. Jordan. 1994. Overview of
the dynamics of an urban artificial reef fish assemblage at King Harbor, California, USA, 1974-1991:
A recruitment driven system. Bull. Mar. Sci. (In
press)
Stephens, J. S. Jr., P. A. Morris, K. Zerba, and M.
Love. 1984. Factors affecting fish diversity on a
temperate reef: The fish assemblage of Palos Verdes Point, 1974-1981. Envir. Biol. Fishes 11:259275.
Stephens, J. S. Jr. and K. E. Zerba. 1981. Factors
affecting fish diversity on a temperate reef. Envir.
Biol. Fishes 6:111-121.
Tegner, M. and P. K. Dayton. 1987. El Nino effects
on southern California kelp forest communities.
Adv. Ecol. Res. 47:243-279.
475
Terry, C. B. and J. S. J. Stephens. 1976. A study of
the orientation of selected embiotocid fishes to
depth and shifting seasonal vertical temperature
gradients. Bull. South. Calif. Academy Sci. 75:170183.
Thresher, R. E., G. P. Harris, J. S. Gunn, and L. A.
Clementson. 1989. Phytoplankton production
pulses and episodic settlement of a temperate
marine fish. Nature 341:641-643.
Underwood, A. J., M. J. Kingsford, and N. L. Andrew.
1991. Patterns in shallow subtidal marine assemblages along the coast of New South Wales. Aust.
J. Ecol. 6:231-249.
Victor, B. J. 1991. Settlement strategies and biogeography of reef fishes. In P. F. Sale (ed.), The ecology offisheson coral reefs, pp. 231 -260. Academic
Press, New York.
Warner, R. R. and P. L. Chesson. 1985. Coexistence
mediated by recruitment fluctuations: afieldguide
to the storage effect. Amer. Natur. 125:769-787.
Warner, R. R. and T. P. Hughes. 1988. The population dynamics of reeffishes.Proc. 6th. Int. Coral
ReefSymp. 1:149-155.
Webb, R. O. and M. J. Kingsford. 1992. Protogynous
hermaphroditism in the half-banded sea perch,
Hypoplectrodes maccullochi (Serranidae). J. Fish.
Biology 40:951-961.