Download Community organization in streams: the importance of species

Oecologia (1992) 91:220-228
Oecologia
9 Springer-Verlag 1992
Community organization in streams:
the importance of species interactions, physical factors, and chance
David D. Hart
Academyof Natural Sciences, 1900 Ben Franklin Parkway, Philadelphia,PA 19103, USA
Received February3, 1992 / Accepted in revisedform March 30, 1992
Summary. Experimental studies were used to examine
the mechanisms governing the distribution and abundance of two major patch types in unshaded reaches
of Augusta Creek, Michigan (USA). One patch type is
dominated by Cladophora glornerata, a macroalga potentially able to monopolize space, whereas the other
type is comprised of a low-growing, epilithic microalgal
lawn inhabited by several species of sessile grazers
(especially the caddisflies Leucotrichia pictipes and Psychomyia flavida). Cladophora patches are absent from
mid-channel sites characterized by current velocities
_< ca. 50 cm s- 1; caging experiments indicate that their
absence is due to grazing by crayfish (Orconectespropinquus). Cladophora's presence in sites with velocities
> 50 cm s-1 apparently results in part because crayfish
foraging activity is impaired in high flow regimes. The
presence of Cladophora strongly affects various other
invertebrates due to its alteration of abiotic and biotic
characteristics of the microhabitat. For example, the
abundance of sessile grazers (e.g. Leucotrichia and Psychomyia) that inhabit microalgal patches is negatively
correlated to the abundance of Cladophora, whereas the
abundance of several other invertebrates (e.g. Stenonema
mayflies and Taeniopteryx stoneflies) is positively correlated to Cladophora's abundance. Therefore, in some
portions of this system, crayfish act as keystone predators because of their ability to regulate the abundance
of Cladophora, which in turn has strong positive and
negative effects on other components of the community.
Cladophora does not always monopolize space at high
velocities in the absence of crayfish, however. If sessile
grazers arrive at such sites before Cladophora, they can
prevent its establishment. Thus, where crayfish are absent, the likelihood that a site will be dominated by either
Cladophora patches or sessile grazer microalgal lawn
patches depends on two sets of stochastic processes: (1)
those that create bare space (e.g. disturbance and grazer
emergence); and (2) those controlling the timing of recruitment by Cladophora or grazers at these bare sites.
These priority effects (i.e. the ability of grazers and Cladophora to inhibit each other's establishment) contribute
to the marked spatial heterogeneity of these two patch
types. Collectively, these results demonstrate how interactions between competition, predation, and physical
factors can generate a complex mixture of community
patterns.
Key words: Indirect effects Keystone predators- Plantherbivore interactions - Predator refuges - Priority effects
Ecologists continue to seek a unified body of theory
that can account for observed variations in the organization of natural communities. In the past, debates often
centered on the explanatory power of opposing unitary
hypotheses, such as the degree to which communities
were regulated by abiotic vs. biotic factors, and the importance of competition vs. predation. There appears
to be a subtle but substantive shift occurring in the kinds
of questions being asked about ecological communities.
For example, more recent approaches explicitly focus
on interactions between a variety of ecological factors
that can regulate patterns of distribution and abundance
within and among communities (e.g. Dunson and Travis
1991). Attempts to ordinate communities with respect
to various ecological axes (Schoener 1986; Giller and
Gee 1987; Menge and Sutherland 1987) represent a particularly ambitious version of this trend. Thus, there is
a growing consensus that pluralistic models are needed
to explain how the relative importance of diverse ecological factors governing community organization varies at
different spatial and temporal scales.
Recently, stream ecologists have also begun to develop and test multifactorial models that can account for
patterns of distribution and abundance (e.g. Peckarsky
1983; McAuliffe 1984; Hart 1985a; Power et al. 1985;
Schlosser and Ebel 1989; Peckarsky et al. 1990; Power
1990a; Hansen et al. 1991). My study examines how an
interplay between physical factors and species interactions controls the organization of a benthic stream community. Specifically, I investigate the complex set of in-
221
teractions controlling the distribution and abundance of
two important patch types (one dominated by an arborescent macroalga, the other by a low-growing microalgal
lawn) by addressing the following questions: (1) How
does macroalgal abundance vary along a gradient in current velocity? (2) Can grazing by crayfish account for
the absence of this macroalga from sites with low velocities? (3) Does crayfish grazing, via its effect on macroalgal abundance, have either positive or negative indirect
effects on other invertebrates? (4) In the absence of crayfish, what role do sessile grazers play in preventing the
macroalga from monopolizing space at high velocities?
Taken together, these studies reveal an intricate web of
strong interactions that caution against simplistic views
of community organization.
Methods
The study system
These studies were carried out in a third order section of Augusta
Creek (Michigan, USA), a hard water stream whose flow regime
exhibits low variability (Poff and Ward 1989; Hart and Robinson
1990). Previous field experiments in this stream have demonstrated
that interactions between epilithic microalgae and grazing insects
are tightly coupled, resulting in strong competition among grazers
for limited algal resources (Hart 1985b, 1987; Hart and Robinson
1990). Two visually conspicuous and distinctly different patch types
often predominate in Augusta Creek's unshaded riffles and runs
from spring to fall (Fig. 1). The first is dominated by arborescent
growths (several-to-many mm thick) of the filamentous chlorophyte Cladophoraglomerata, along with associated epiphytes and
a variety of invertebrates. The second patch type is a low growing
( < < 1 mm thick) epilithic microalgal lawn composed primarily of
diatoms and cyanobacteria (Hart 1985 a), along with various sessile
and mobile grazers that harvest this microbial resource. Initial observations suggested that the pattern of occurrence of these two
patch types was unpredictable, because they were interspersed in
a complex mosaic on the stream bottom. Subsequent study, however, indicated that Cladophora patches were absent from midchannel sites that are characterized by low current velocities (see
below). I used a combination of experimental and descriptive field
studies to examine some of the factors governing the relative abundance of these two patch types during the summer and fall of
1981 and 1982. Stream discharge during the study ranged between
0.9-2.4 m ~ s -1 in 1981 and between 0.8-1.2 m 3 s -1 in 1982.
Relationship between Cladophora abundance
and current velocity
I made visual assessments of Cladophoracover in November, 1981
to determine how its abundance varied with current velocity. Measurements of cover have been shown to be a reliable means of
quantifying the abundance of a wide array of marine and freshwater macroalgae (e.g., Lubchenco and Menge 1978; Dudley et al.
1986). Cladophoracover was estimated in a 50 m long stream reach
that had an average width and depth of about 6 m and 0.4 m,
respectively. Cover was quantified using a 161 cmz hardware cloth
frame that was subdivided into twenty-five 6.5 cm 2 grids. The
frame was haphazardly tossed from the stream bank into the center
of the channel, and an underwater census of cover was made at
each of 31 sites where the frame came to rest. Cover was defined
as the percentage of grids in which Cladophorafilaments overlaid
> 2 5 % of the substrate area enclosed by a grid. This cover criterion, although less standard than techniques based on point estimates, was applied uniformly throughout the study and yielded
a high level of precision. The current velocity associated with each
cover sample was measured using an Issacs-Kidd flowmeter (propeller diameter = 5 cm) placed immediately above the substrate.
Effect of crayfish on Cladophora abundance
I assessed the ability of the crayfish Orconectespropinquusto reduce
the abundance of Cladophorain a field experiment. In July, 1981,
unglazed quarry tiles (upper surface area=2.25 dm 2) were placed
on wooden platforms where the current velocity measured over
a five minute interval averaged 68 cm s-1. These platforms were
elevated about 10-15 cm above the stream bottom to reduce the
accessibility of the tiles to crayfish. The tiles were covered with
substantial growths of Cladophoraby the time the experiment began two months later.
Tiles were randomly assigned to one of three caging treatments
(i.e. crayfish enclosures, crayfish exclosures, or open-sided cages),
with five replicates per treatment. The cages were 15 cm on a side
by 8 cm in height, and were constructed of 0.6 cm mesh hardware
cloth. This mesh size made the cages semipermeable (sensu Munger
and Brown 1981), since it was fine enough to prevent the passage
of all but the smallest crayfish, but large enough to permit passage
of all the other common macroinvertebrates in Augusta Creek.
Fig. 1. Tile substrates colonized by the two
patch types investigated in this study: the filamentous macroalga Cladophora (left); and the
microalgal lawn, encrusted with the cases of
Psychomyia and Leucotrichia, two sessile, grazing caddisflies (right). Pocket knife shown for
scale
222
Enclosure and exclosure cages were constructed with four side
walls. In contrast, open-sided cages had side walls on the upstream
and downstream faces of the cage, but lacked side walls on cage's
two lateral faces, thus permitting crayfish to move in and out of
the cages. It is unlikely that crayfish would be differentially attracted to these open-sided cages solely as a source of cover, since
natural crayfish shelters are abundant on the cobble bed of Augusta
Creek.
Cladophora cover on each tile was censused along three crosstile strip transects immediately after the tiles were placed within
the cages. Each transect consisted of twenty-four 0.4 cm 2 grids,
within which Cladophora was scored as present when its filaments
overlaid > 25% of the grid area. Each transect was censused twice,
and repeated counts of the number of grids in which Cladophora
was present never differed by more than one. The same person
measured cover on all tiles to increase the precision of these estimates. Five large crayfish (probably 1 or 2 years old; 2 + 1 S.E.
carapace length=28.3 +0.6 mm) were collected from a site about
150 m upstream; one crayfish was added to each of the enclosure
cages. One of these enclosure cages was deleted from subsequent
analyses because the crayfish within it died midway through the
experiment.
The cages were haphazardly arranged in an unshaded run where
crayfish densities averaged about 5 individuals m -2 (Hart, unpublished). The stream bed in this region was composed primarily
of gravel-cobble substrates, and the stream depth was about 30 cm.
Current velocity within 5 cm of the stream bed was measured midway through the experiment with an Issacs-Kidd flowmeter immediately upstream from five of the cages; the velocity (2_+1 S.E.)
was 53.0 __.2.8 cm s-1. After the experiment was completed, I used
a bucket wheel-type Pygmy flowmeter (Buchanan and Somers
1969) to compare velocities inside cages with velocities measured
immediately upstream from cages. The current velocity inside a
cage was determined by inserting the flowmeter through a hole
cut in the cage's roof and measuring the velocity within 2 - 3 cm
of the tile surface. This internal velocity (2_+1 S.E.), expressed
as a percentage of the external velocity, was 84.0 + 1.0 %, suggesting
that the velocity within the experimental cages was about 45 cm
s-1. Each day during the experiment, any leaves or other material
that accumulated on the cages was removed to reduce alterations
of flow and light. The experiment was ended after seven days,
at which time Cladophora cover was remeasured.
Effect of sessile grazers on Cladophora establishment
The purpose of these field experiments was to determine whether
sessile grazers could inhibit the establishment of Cladophora. Two
of the most abundant sessile grazers occurring in Augusta Creek's
unshaded riffles and runs are the larval stages of the caddisflies
Leucotrichia pictipes (Hydroptilidae) and Psychomyiaflavida (Psychomyiidae). The abundance of these two species can be readily
quantified in situ with minimal disturbance because their larvae
usually live in fixed silken shelters (see Hart 1985b; Hart and Robinson 1990).
Effect of Leucotrichia. In August, 1982, I manipulated the abundance of Leucotrichia on a series of bricks that had been placed
in Augusta Creek about three months earlier. These substrates were
initially placed in a shallow riffle where the average current velocity
measured with a Pygmy flowmeter exceeded 50 cm s- 1 (Hart, unpublished). At the outset of the experiment, the top of each brick
(surface area = 0.97 dm 2) had been colonized by high densities of
Leucotrichia and Psychomyia larvae, whereas no Cladophora filaments were visible. I censused the initial number of these two sessile
grazers on sixteen bricks. Half of these bricks were then randomly
assigned to a treatment in which all Leucotrichia larvae were removed from the upper surface of the brick. The remaining bricks
served as controls, in which Leucotrichia larvae were left on the
upper surface of the brick. The abundance of Psychomyia larvae
was not manipulated in either treatment. Immediately following
the establishment of these treatments, the bricks were systematically interspersed on wooden platforms elevated about 10 cm above
the stream bottom and exposed to velocities between 5 0 - 6 0 cm
s-1 (Hart, unpublished). Previous observations indicated that substrates placed on these platforms were inaccessible to crayfish.
About every 10-12 days during the course of the experiment,
fine-tipped forceps were used to remove any Leueotriehia larvae
that had colonized the bricks assigned to the removal treatment,
whereas Leucotriehia were not removed from bricks assigned to
the control group. The experiment was terminated after seven
weeks, at which time a final census of Leucotrichia and Psychomyia
densities and Cladophora cover was made. Cladophora cover on
each brick was estimated along seven cross-brick transects according to the method described previously. In addition, five algal biomass samples per brick were collected from haphazardly selected
locations on the upper surface of five removal and five control
bricks using a 1-cm 3 periphyton syrine sampler (modified from
Loeb 1981) that enclosed an area of about 17 mm 2. The algae
in each sample were collected onto a precombusted Whatman
G F / F filter at a vacuum of < 50 kPa, acid fumed for 15 minutes
to remove inorganic carbon (Wetzel 1965), dried at 60~ and
stored in a desiccator. Within 2 months the samples were cornbusted in a Carlo-Erba C H N analyzer (model number 1106, Carlo
Erba Strumentazione, Milan, Italy) to determine the particulate
carbon content of each sample (Stainton et al. 1977).
Effect of Psyehomyia. In August, 1982, I selected a set of ten unglazed quarry tiles (upper surface area = 2.25 dm 2) that had been
placed in a shallow riffle in Augusta Creek about two months
earlier. Psychomyia was the numerically dominant grazer on these
tiles, in contrast to the previous experiment using brick substrates,
on which Leucotriehia was the most abundant grazer. After performing an initial census of Psychomyia and Leueotrichia densities,
all insects were removed from one half of each tile while the other
half served as a control. In addition, forceps were used to remove
Cladophora filaments from the surface of each tile, after which
I scraped off the basal tissue. Each tile was then placed into a
crayfish exclosure cage (see above). The current velocity (i_+ 1 S.E.)
in the vicinity of these cages, as measured with a Pygmy flowmeter,
was 39.0+1.6cm s -1. Cages were cleaned daily, and the grazer
removal treatment was repeated at 1-2 week intervals. The experiment was terminated after about two months, at which point I
used the previously described methods to estimate Cladophora
cover on both halves of each tile, as well as the number of Psychomyia, Leucotrichia, and tube-dwelling chironomids.
Indirect effects of crayfish on other invertebrates
This field experiment was undertaken to quantify the potential
indirect effects of crayfish on other invertebrates due to alterations
in Cladophora cover caused by crayfish grazing. Specifically, I examined how variations in Cladophora cover affected the colonization of a diverse assemblage of invertebrates in the absence of
crayfish. Varying amounts of Cladophora were present on a group
of nine unglazed quarry tiles that had been incubated in August
Creek for about two months. In August, 1982, all macroinvertebrates were carefully removed from these tiles using forceps, whereas Cladophora filaments were disturbed as little as possible. Each
tile was then placed in an exclosure cage to prohibit access by
crayfish. These cages were haphazardly arranged in an unshaded
riffle, and the current velocity (2+ 1 S.E.) in the vicinity of these
cages, as measured with a Pygmy flowmeter, was 46.2+2.7 em
s-i. Cladophora cover was censused visually at about two week
intervals during the course of the experiment, using the method
described previously.
After two months, each cage was removed from the stream
bottom while a dip net was positioned immediately downstream
to minimize the loss of mobile animals during removal. In the
laboratory, all macroinvertebrates that were visible under 7x magnification were removed from the tile and stored in 75% ethanol,
after which they were enumerated and identified.
223
100
Statistical analyses
I
The relationship between Cladophoraabundance and current velocity was measured using Spearman's rank correlation coefficient.
One-way ANOVA was used to test for significant treatment effects
in the following experiments: (1) the effect of crayfish on Cladophora abundance; (2) the effect of Leueotrichia on Cladophoraestablishment; (3) the effect of Psychomyia on Cladophoraestablishment. Cladophoracover was arcsine-transformed prior to analysis
(Sokal and Rohlf 1981). When multiple measures of Cladophora
cover or biomass were available for a single experimental unit,
ANOVA was performed on the average of these measures to avoid
pseudoreplication. Pairwise comparisons among group means were
made using the Tukey Studentized Range test. When the assumption of variance homogeneity was rejected using Levene's test, I
assessed the treatment effect with Welch's test, in which variances
are not assumed to be equal (Dixon 1988).
Potential indirect effects of crayfish on other invertebrates were
assessed by determining the sign and magnitude of Spearman's
rank correlation coefficient between the abundance of various invertebrate taxa and the cover of Cladophorawithin the crayfish
exclosure cages. Rare taxa (i.e., those whose average abundance
per tile was < one individual) were not included in these analyses.
Results
Relationship between Cladophora abundance and current
velocity
There was a significant positive correlation between the
abundance of Cladophora and current velocity (rs = 0.83,
N = 3 1 , P < 0 . 0 0 1 ) (Fig. 2). Cladophora cover was zero
for samples with velocities less than 50 cm s-2. Even
when the analysis was restricted to those samples with
velocities greater than 50 cm s - 1 Cladophora cover increased significantly with velocity (rs = 0.69, N = 23, P <
0.001), although this relationship exhibited considerable
scatter. For example, at a velocity of about 80 cm s-1,
there was a three-fold range in Cladophora cover.
Effect of crayfish on Cladophora abundance
After seven days, Cladophora was virtually eliminated
from the enclosure cages, and cover was reduced by
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Velocity
(cm
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70
80
Initial
Final
80
Z_
60
2_
40
20
Exclosure
Open
Enclosure
Caging Treatment
Fig. 3. Initial and final Cladophoracover on tites randomly assigned
to three different caging treatments. Error bat's represent + one
standarderror
nearly 70% in the open-sided cages (Fig. 3). In contrast,
average cover increased by more than 50% in the exclosure cages. Changes in Cladophora cover between the
beginning and end of the experiment differed significantly a m o n g the three treatments (F 2.12 = 9 I. 2, P < 0.000 l).
For example, the decline in Cladophora cover within enclosure cages was significantly different f r o m the change
in cover within the other two caging treatments ( P <
0.01, Tukey test). The high effective density of crayfish
in enclosure cages (ca. 44 ind m -z) m a y overestimate
the natural effect of crayfish on Cladophora, however,
making it especially important to compare changes in
Cladophora cover between the exclosure and open-sided
treatments. Cladophora cover in open-sided cages also
declined significantly c o m p a r e d to the exclosure cages
( P < 0 . 0 1 , Tukey test). Because the major difference between these two treatments is accessibility by crayfish
(see Discussion), this strongly suggests that crayfish at
natural densities reduce Cladophora's abundance.
Effect of sessile grazers on Cladophora establishment
Effect of Leucotrichia. Before the experiment began, the
density (s _+ 1 S.E. larvae d m - 2 ) of Leucotrichia on control bricks (63.9+_4.5) and Leucotrichia removal bricks
{
50
I
90
s-')
Fig. 2. Relationship between Cladophoracover and current velocity
(56.7 +_3.2) did not differ significantly (F1,14= 1.70,P=
0.21). There was also no significant difference between
Psychomyia's density (2 4-1 S.E. larvae din-2) on control
bricks (44.4_+3.7) and Leucotrichia removal bricks
(41.1+3.5) (F2n~=0.43, P = 0 . 5 2 ) . By the end of the
experiment, the average density of Leucotrichia larvae
was significantly lower on removal bricks than on control bricks (Ft,:4 =439.1, P < 0.0001) (Fig. 4), thus confirming the success of the density manipulation. In contrast, there was no significant difference between the
average density of Psychomyia larvae on removal and
control bricks (FI,t4 = 0.03, P = 0.87).
The average percent cover of Cladophora on removal
bricks at the end of this experiment was more than 20fold greater than on Leucotrichia control bricks (F1,14 =
224
Table 1. Relationship between the abundance of common invertebrate taxa (i.e., those averaging > 1 individual per tile) and Cladophora cover on tiles within exclosure cages. For each taxon, the
value of Spearman's rank correlation coefficient is given
48
7
I00
40
32
Taxon
Correlation with
Cladophora cover
Leucotrichia
Psychomyia
Antocha
-0.93"***
8
40
24
s
16
o
2O
Oligochaetes
Hydropsyche
Baetis
Larval Chironomidae
0
Psychomyio
Leucotrichia
C[adophora
Fig. 4. Final insect density and Cladophora cover on control bricks
(hatched bars) and on Leucotrichia removal bricks (open bars). Error bars represent + one standard error
7
Pupa| Chironomidae
* 0.05<P<0.1, ** P<0.05, *** P<0.01, **** P<0.005, NS=not
significant
1~f
5_
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60
45
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40
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~z
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t~
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g
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c
Cheumatopsyche
Isoperla
Stenonema
Taeniopteryx
-0.86****
- 0.66'*
- 0 . 3 8 NS
- 0 . 1 5 NS
0.18 NS
0.42 NS
0.50*
0.58**
0.68**
0.80***
0.86****
20
15
Leucotrlchi~
Psychomyio
Chironomids
of the grazing effect on Cladophora (see below) can be
attributed to Psychomyia. In contrast to both Psychomyia and Leucotrichia, chironomid densities were significantly greater on tile halves from which grazers (including midges) were removed than on control halves
(F1,18 =25.47, P=0.0001).
The percent cover of Cladophora on tile halves from
which grazers were removed was nearly 20-fold greater
than on control halves (FL18=416.4, P < 0 . 0 0 0 1 )
(Fig. 5).
Clado ~hora
Fig. 5. Final insect density and Cladophora cover on control halves
of tiles (hatched bat's) and on grazer removal halves of tiles (open
bars). Error bars represent • one standard error
139.4, P < 0 . 0 0 0 1 ) (Fig. 4). Algal biomass (2___1 S.E. lag
C r a m - 2 ) on the upper surface of Leucotrichia removal
bricks (19.9_+1.1) was nearly four times greater than
on control bricks (5.6 ___0.4) (F1,7 = 132.9, P < 0.0001).
Effect of Psychomyia. The initial density (2_+ 1 S.E. larvae dm -z) of Psychomyia on control halves (58.1 _+4.8)
and on grazer removal halves (50.7+4.9) of the tiles
did not differ significantly (F1.18=1.19, P=0.2887).
There was also no significant difference between the initial density of Leucotrichia on control tiles (5.3_+ 1.6)
and grazer removal tiles (10.8_+2.8) (Fl,~S=2.55, P =
0.1277). At the end of the experiment, the density of
Psychomyia larvae on the control halves was about twice
as large as on grazer removal halves (F~,18=67.4, P <
0.0001) (Fig. 5). The density of Leucotrichia larvae on
grazer removal and control sections also differed significantly (Fl,18=14.63, P=0.0012), but Leucotrichia's
density in this experiment was 1-2 orders of magnitude
lower than that of Psychomyia. Because Psychomyia and
Leucotrichia larvae are very similar in body mass (Hart
and Robinson 1990), this marked difference in population density between the two species suggests that most
Indirect effects of crayfish on other invertebrates
A total of 22 invertebrate taxa colonized the tiles used
in these experiments, but only 12 of these taxa were
abundant enough to include in the correlation analyses.
Two-thirds of these taxa exhibited statistically significant
positive or negative correlations with Cladophora cover
(Table 1). For example, the abundances of Psychomyia,
Leucotrichia, and the tube-dwelling tipulid Antocha were
negatively correlated to Cladophora cover, whereas the
abundances of the mayfly Stenonema, the stoneflies
Taeniopteryx and Isoperla, and chironomid pupae were
positively correlated to Cladophora cover. There was
also a marginally significant positive correlation between
Cladophora and net-spinning caddisfly Cheumatopsyche.
Discussion
Cladophora's absence from sites with velocities
<50 cm s -1
At least three hypotheses can potentially explain the observed absence of Cladophora from mid-channel microhabitats with current velocities _< ca. 50 cm s - l : (1)
failure to disperse to these sites; (2) physiological unsuitability of the sites; (3) biological interactions that either
225
prevent Cladophora from establishing at the sites or that
eliminate it after establishment. Because bare substrates
protected from crayfish and sessile grazers are readily
colonized by Cladophora, however, its absence is not
the result of dispersal limitations. Moreover, Cladophora
cover on tiles transplanted to the crayfish exclosure
cages (in which the internal velocity averaged 45 cm s- 1)
increased by more than 50%, demonstrating that these
sites are favorable for growth. Thus, although the
growth of Cladophora may be strongly limited where
flow is very low or absent (e.g. Dodds 1991), the current
velocity at which the caging experiment was conducted
was more than adequate to support Cladophora's
growth.
The results from the enclosure cages clearly demonstrate that crayfish are able to control the abundance
of Cladophora, but they do not ensure that the observed
reduction of Cladophora in the open-sided cages is necessarily caused by crayfish. Two considerations strongly
support the conclusion that Cladophora's decline was
due to crayfish, however. First, other than crayfish, the
only common animal at the study site that was too large
to pass through the 0.6 cm mesh cages was the mottled
sculpin (Cottus bairdi). Underwater observations in both
the day and night confirmed that crayfish entered the
open-sided cages and fed upon Cladophora, whereas
sculpin were never observed in these cages. Second, a
preliminary analysis of the summer diets of these two
species indicated that 86% of the crayfish (N=7) contained an abundance of Cladophora fragments in their
guts, whereas Cladophora fragments were never found
in the guts of the sculpin ( N = 3). These results, although
based on small sample sizes, are consistent with other
data indicating that Cladophora commonly occurs in the
guts of O. propinquus (e.g. Capelli 1980) whereas sculpin
rarely ingest plant material (e.g. Koster 1937; Dineen
1951).
Flow-mediated refuges
The caging experiment demonstrates that crayfish can
eliminate Cladophora from sites with velocities < ca.
50 cm s- 1, and the descriptive data indicate that Cladophora is often abundant in sites whose velocities are faster than this. Collectively, these results strongly suggest
that the ability of crayfish to control Cladophora is constrained by flow. Maude and Williams (1983) quantified
the relationship between current velocity and the activity
of eight crayfish species in a laboratory flume. The average velocity at which these crayfish were dislodged from
the Plexiglas flume bed ranged between 26 and 50 em
s -1, and the 95% confidence interval bracketing this
average '~slip speed" for O. propinquus ranged between
31 and 38 cm s-1. Similarly, Howard and Nunny (1983)
demonstrated that juvenile lobsters (Homarus gammarus), whose size range bracketed the crayfish sizes used
in my study, were dislodged from semi-natural substrates in lab flumes at velocities of about 40-50 cm
s-1. They concluded that lobsters in the field are restricted to microhabitats in which velocities are lower
than this. My underwater field observations have confirmed that high flows can dislodge O. propinquus from
the stream bed. For example, I have observed crayfish
easily climb up the downstream (and therefore sheltered), vertical face of a large boulder, only to be "blown
off" the boulder once they reach the top, where they
encounter the full force of the current. The probable
role of flow in constraining the ability of crayfish to
control Cladophora is but one example of a growing
body of work indicating that flow can mediate the intensity of predator-prey interactions in a variety of freshwater and marine environments (e.g. Menge 1978; Palmer
1988; Peckarsky etal. 1990; Richardson and Brown
1990; DeNicola and McIntire 1991 ; Hansen et al. 1991).
The results of Maude and Williams (1983) clearly
demonstrate that flow can constrain the foraging activity
of crayfish, yet the velocity threshold suggested by their
slip speed estimate for O. propinquus is somewhat lower
than that implied by the observed relationship between
Ctadophora cover and current velocity (Fig. 2). Their lab
study might be expected to underestimate this velocity
threshold, however, since the ability of crayfish to resist
dislodgement is probably lower on the relatively smooth
Plexiglas flume bed used by Maude and Williams (1983)
than on the topographically complex stream bed where
my study was conducted.
Recent studies have shown that Cladophora's abundance in Augusta Creek sometimes exhibits a negative
correlation with depth as well as a positive correlation
with current velocity (Creed 1990). One possible explanation for the negative correlation between Cladophora
cover and depth is that crayfish avoid shallow sites
where they may experience greater predation risk (see
Power, 1987 for a similar pattern involving grazing
stream fish). Further experiments are required to assess
the relative importance of constraints involving depthrelated predation risk vs. flow in controlling the effects
of crayfish on Cladophora, especially because stream
depth and current velocity often exhibit a strong negative correlation.
Cladophora monopolies, sessile grazers, priority effects,
and chance
If crayfish were always excluded from sites with velocities > 50 cm s - 1 and if crayfish herbivory was the only
factor limiting Cladophora's abundance, then Cladophora should be able to monopolize space in these sites.
Cladophora cover in sites with velocities > 50 cm s-1
was highly variable, however, and rarely exceeded 50%.
Two factors may prevent Cladophora from monopolizing
these sites. First, some sites with velocities > 50 cm s-1
are presumably accessible to crayfish. For example, there
is probably no single velocity threshold at which crayfish
foraging becomes impossible. Rather, it seems likely that
there is a broad velocity zone over which the probability
of crayfish grazing varies as a function of numerous
factors, including crayfish size and posture (Maude and
Williams 1983), bed topography, and near-bed velocity
gradients.
226
Second, even in the absence of crayfish, it is clear
that both Leucotrichia and Psychornyia can prevent Cladophora from monopolizing sites where these sessile
grazers have established prior residence. Similarly, grazing insects have been observed to inhibit the establishment of Cladophora in a California stream (Dudley and
D'Antonio 1991). A reciprocal interaction also occurs
in Augusta Creek, since Cladophora patches can inhibit
the establishment of sessile grazers. Although such priority effects have been observed in a variety of marine
and terrestrial settings (see references in Connell and
Slatyer 1977; Yodzis 1986), they have rarely been documented in streams (Downes 1990; but see McAuliffe
1984). Further studies are needed to determine whether
priority effects influence species interactions in a broader
array of benthic stream communities.
Priority effects can generate considerable spatial and
temporal heterogeneity in natural communities as a result of two sets of stochastic processes influencing the
colonization history of sites. One set of processes controls the creation of bare space at a site. In Augusta
Creek, space becomes available when stones are overturned during spates, when sessile grazers pupate and
emerge following the completion of their larval feeding
stage, and when Cladophora sloughs from stone surfaces
as a result of either winter senescence or high drag during
floods. The second class of processes controlling patterns
of patchiness is linked to the factors governing the arrival of propagules at a site. For example, differences between sessile grazers and Cladophora in the phenology
of propagule dispersal will necessarily cause their establishment probabilities to differ in space and time. Therefore, interactions between species-specific life history
characteristics and factors controlling the availability of
bare space can cause microhabitats that are abiotically
similar to become dominated by very different species
assemblages (see also Sousa 1985). The manifestation
of priority effects in ecological communities will often
involve a large element of chance, which may contribute
directly to the complex spatial mosaic of these two patch
types in Augusta Creek. This strong but stochastic interaction also serves as a potent reminder that the observation of patchiness per se provides little information
about the degree to which a community is organized
by abiotic vs. biotic factors, since either set of factors
has the potential to generate marked heterogeneity.
Indirect effects of crayfish
The direct effect of crayfish grazing on Cladophora is
transmitted to other species via Cladophora's modification of the benthic environment. For example, the recruitment of species such as Leucotrichia and Psychomyia is inversely related to the abundance of Cladophora.
Several mechanisms probably account for these negative
effects. The tendency of Cladophora to form a thick mat
(hence its popular name, "blanket-weed"; Whitton
1970) significantly modifies the abiotic environment experienced by organisms living on the stone surface underneath the mat. For example, Dudley et al. (1986)
showed that current velocities beneath a Cladophoraglornerata mat were reduced by more than 40% compared
to velocities in the absence of the mat. Cladophora mats
also intercept light that would otherwise reach the epilithic microalgal lawn, and field experiments have indicated that shading reduces the standing crop of this lawn
(Hart, unpublished; see also Feminella and Resh 1991).
As a consequence, shading by Cladophora will negatively
affect various species that feed upon microalgae, because
many of these grazers are food-limited in Augusta Creek
(Hart 1987; Hart and Robinson 1990). Although the
biomass of the Cladophora mat is usually much greater
than the microalgal lawn (Hart et al. 1991), Cladophora
is not an acceptable alternative food source for these
grazers. Once the Cladophora mat becomes established
at a site, these grazers are apparently unable or unwilling
to consume it, probably because of various chemical and
physical properties that deter herbivores (LaLonde et al.
1979; Patrick et al. 1983). In contrast, Cladophora may
lack such defenses during its initial growth phase at a
site, which could explain why grazers are able to control
it at this time. Similar size-related changes in vulnerability to grazers have been documented in marine plantherbivore interactions (Lubchenco and Gaines 1981).
The abundances of several other insect taxa (i.e.,
Stenonema, Taeniopteryx, Isoperla, chironomid pupae,
and Cheumatopsyche) are positively related to Cladophora cover. A variety of mechanisms appear to underlie
these patterns, including: (1) enhancement of epiphytic
food resources on Cladophora filaments; (2) accumulation of fine particulate organic matter beneath the Cladophora mat; (3) the use of Cladophora filaments as
structural support for filtering nets; and (4) the role of
Cladophora mats in providing shelter from high current
velocities or potential predators. Similar explanations
were advanced by Dudley et al. (1986) to account for
positive associations between various invertebrate taxa
and the abundance of Cladophora.
Crayfish can have negative effects on the abundances
of invertebrates via at least two paths. First, as described
above, taxa whose abundances are positively correlated
to Cladophora cover will experience a negative indirect
effect as the result of Cladophora consumption by crayfish. Second, crayfish may directly feed upon various
invertebrates. Estimating the direct consumption of invertebrates by crayfish was not a primary focus of my
study. Nonetheless, preliminary dietary analyses and
laboratory experiments suggest that relatively few of the
invertebrate taxa described above are heavily preyed
upon by O. propinquus in Augusta Creek (Hart, unpublished data; see also Capelli 1980).
Because crayfish reduce the abundance of Cladophora, which in turn can have a strong negative effect
on the sessile grazer-microalgal lawn patch type, crayfish
therefore act as keystone predators (Paine 1966) in this
community. The general importance of keystone predation and other strong interactions (sensu MacArthur
1972) in stream communities remains poorly understood
(Hildrew 1992), but these interactions are obviously
more widespread than previously recognized (McAuliffe
1984; Hart 1985a; Power et al. 1985). Because crayfish
227
a n d / o r Cladophora o c c u r in a w i d e v a r i e t y o f s t r e a m
c o m m u n i t i e s , a n d b e c a u s e each species has been s h o w n
to i n t e r a c t s t r o n g l y in v a r i o u s settings w h e r e t h e y h a v e
been s t u d i e d (e.g. see D u d l e y et al. 1986; P o w e r 1990a,
1990b r e g a r d i n g Cladophora glomerata; see L o d g e a n d
L o r m a n 1987; W e b e r a n d L o d g e 1990; C r o w l a n d
Schnell 1990 r e g a r d i n g crayfish), s t r o n g i n t e r a c t i o n s m a y
be i m p o r t a n t in m a n y s t r e a m c o m m u n i t i e s w h e r e either
o r b o t h o f these species occur. M o r e generally, there
is a pressing n e e d for m o d e l s t h a t c a n p r e d i c t the k i n d s
o f e c o l o g i c a l a t t r i b u t e s a n d e n v i r o n m e n t a l settings t h a t
l e a d to s t r o n g i n t e r a c t i o n s a m o n g species (see also F a u t h
a n d R e s e t a r i t s 1991).
In c o n c l u s i o n , the c o m p l e x set o f i n t e r a c t i o n s d o c u m e n t e d in this s t u d y c a n n o t be easily r e c o n c i l e d with
v a r i o u s d i c h o t o m o u s r e p r e s e n t a t i o n s o f c o m m u n i t y org a n i z a t i o n (e.g. c o n t r o l b y a b i o t i c vs. b i o t i c factors, c o m p e t i t i o n vs. p r e d a t i o n , o r s t o c h a s t i c vs. d e t e r m i n i s t i c p r o cesses). I f ecologists wish to a c c o u n t fully for the p r o cesses c o n t r o l l i n g c o m m u n i t y p a t t e r n s , t h e n they will
need to d e v e l o p m o r e d e t a i l e d m o d e l s t h a t explicitly ack n o w l e d g e the m u l t i f a c t o r i a l o r g a n i z a t i o n o f c o m m u n i ties, a n d to design r e s e a r c h p r o g r a m s t h a t c a n identify
h o w the relative c o n t r i b u t i o n s o f these factors v a r y in
space a n d time.
Acknowledgements. I am very grateful to Earl Werner and Don
Hall for their support and friendship while I worked at the Kellogg
Biological Station. The Snyder family kindly provided access to
the study site. Steve Latta, Chris Robinson, Jean Marek, and Deb
Wohl assisted with the field and lab work, and Deb Wohl helped
analyze the data and prepare figures. Bob Wetzel and especially
Mike Klug generously provided equipment that permitted the
CHN analyses to be performed, and Greg Walker helped run the
CHN analyzer. I thank Joaquin Feliciano, Steve Kohler, Mark
Leighton, Pete Peterson, Peter Petraitis, LeRoy Poff, Deb Wohl
and an anonymous reviewer for their detailed and constructive
criticisms of earlier drafts of the manuscript. This work was supported by NSF grants DEB-8111305, BSR-8312629, and BSR8918608. KBS Publication No. 730.
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