Supply-side ecology, barnacle recruitment, and rocky intertidal

Transcription

Journal of Experimental Marine Biology and Ecology 392 (2010) 160–175
Contents lists available at ScienceDirect
Journal of Experimental Marine Biology and Ecology
j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / j e m b e
Supply-side ecology, barnacle recruitment, and rocky intertidal community
dynamics: Do settlement surface and limpet disturbance matter?
Bruce A. Menge ⁎, Melissa M. Foley 1, Jacque Pamplin, Gayle Murphy, Camryn Pennington
Department of Zoology, Oregon State University, Corvallis, OR 97331-2914, United States
a r t i c l e
Keywords:
Artificial collectors
Balanus glandula
Bulldozing
Chthamalus dalli
Cyprids
Limpets
Oregon
Recruitment
Rocky intertidal
Safety-walk plates
Settlement
i n f o
a b s t r a c t
The supply of new recruits can be a critical determinant of community structure, but estimating recruitment
density can be challenging due to variation in larval supply, settlement, substratum, species interactions and
physical stresses. We evaluated the effect of surface type and limpet “bulldozing” on settlement and
recruitment of barnacles, using replicated field experiments sampled monthly at each of four sites along the
central Oregon coast in 2001, 2003, and 2008. A particular goal was to evaluate the efficacy of Saf-T-Walk, a
widely used textured surface, in quantifying actual patterns and levels of recruitment. In 2001 and 2003
experiments, surfaces were bare rock (ROCK) and Saf-T-Walk (STW). In 2008 experiments, to further
evaluate the influence of surface rugosity, we added two additional artificial substratum types — smooth PVC
plates (no texture) and travertine plates (TRAV, low texture). Limpet activity was manipulated using barriers
of anti-fouling paint. Results indicated the overwhelming importance of surface texture. Recruitment density
was highest in 2001, lower in 2003, and lowest in 2008. Recruitment on STW, the most textured surface,
ranged up to 87 times greater than on ROCK, and the rank order of surfaces for recruitment density was
STW N ROCK N TRAV N PVC which matches that for texture. Settlement differences were even greater, with up
to 1180-fold higher settlement on STW than ROCK. Limpets usually had a negative effect on recruitment of
Balanus glandula on ROCK, likely due to bulldozing and direct consumption, but had a positive effect on STW.
These impacts were reduced or negated when recruitment density was higher (e.g., 2001) or lower than
average (e.g., 2008). Limpets had no consistent effect on Chthamalus dalli. Abundances of settlers and recruits
on the different surfaces were positively correlated (explaining up to 71% of the variance), and correlations
between STW and other surfaces generally were stronger in the absence of limpets. Although compared to
bare rock, recruitment to STW overestimates absolute rates of recruitment, use of STW settlement plates
provides an effective and relatively efficient means of determining spatial and temporal patterns of
recruitment at local to geographic scales.
© 2010 Elsevier B.V. All rights reserved.
1. Introduction
After decades of research focused at local scales, ecology has
undergone a dramatic shift in recent years towards investigation of
how patterns and dynamics of species interactions vary across
multiple spatial and temporal scales (Levin, 1992; Brown, 1995;
Holyoak et al., 2005). Investigations now routinely incorporate
multiple study sites often over vast spatial scales into their design
(Jenkins et al., 2000; Sagarin and Gaines, 2002; Menge et al., 2004;
O'Riordan et al., 2004, Navarrete et al., 2005; Coleman et al., 2006).
Such studies are challenging because of variation among coinvestigators, the biota, and physical conditions. For example,
⁎ Corresponding author.
E-mail address: [email protected] (B.A. Menge).
1
Current address: Department of Ecology and Evolutionary Biology, University of
California, Santa Cruz, CA 95064, United States.
0022-0981/$ – see front matter © 2010 Elsevier B.V. All rights reserved.
doi:10.1016/j.jembe.2010.04.032
incorporation of spatial scale requires standardization to ensure that
differences observed are independent of method.
In marine ecosystems, several recent large-scale studies exemplify
this approach and its challenges (Jenkins et al., 2000; Menge et al.,
2003; O'Riordan et al., 2004; Coleman et al., 2006). These studies are
typically carried out by a consortium of institutions and a number of
investigators at each institution. For example, the PISCO (Partnership
for Interdisciplinary Studies of Coastal Oceans) consortium is focused
on the linkages between coastal ocean environments and benthic
communities, and how these vary through time and across space
(Menge et al., 2004; Schoch et al., 2006).
A key potential determinant of community structure and an
important link between the coastal ocean and benthic habitats is the
supply of new recruits (Connell, 1985; Gaines and Roughgarden,
1985; Connolly and Roughgarden, 1999). PISCO has focused much
effort on the investigation of recruitment patterns of sessile
invertebrates to rocky intertidal regions and fish to kelp bed habitats
along the coasts adjacent to the California current (Amman, 2004;
B.A. Menge et al. / Journal of Experimental Marine Biology and Ecology 392 (2010) 160–175
Broitman et al., 2008). In these large-scale investigations, an
important tool has been the adoption of standardized units to
quantify recruitment that are inexpensive, uniform in size and
composition, and readily deployed, retrieved and processed. These
devices include plastic mesh ovoids used to quantify mussel
recruitment (Menge, 1992), and, our focus in this paper, settlement
plates covered with a textured surface to quantify barnacle recruitment (Farrell et al., 1991).
Barnacles are ubiquitous in marine habitats, and in rocky intertidal
systems are usually dominant components of ecological communities
(Lewis, 1964; Stephenson and Stephenson, 1972; Morton, 2004). As
expressed in many influential studies, they are central to the
dynamics of populations and communities around the world, serving
as competitors, facilitators, and prey in a wide variety of settings (e.g.,
Connell, 1961; Dayton, 1971; Menge, 1976 and many others).
Barnacles are particularly prominent in studies of recruitment
because larvae, settlers and recruits are identifiable, abundant, and
readily studied in the field (e.g., Hawkins and Hartnoll, 1982; Wethey,
1984; Connell, 1985; Caley et al., 1996).
In field investigations, two approaches have been taken to quantify
settlement and/or recruitment of barnacles. Some have investigated
recruitment to natural rock substrata (e.g., Hawkins and Hartnoll,
1982; Raimondi, 1988; Menge, 1991; Jenkins et al., 2000, 2008;
Bertness et al., 2006) or to human-fabricated rock surfaces (Noda,
2004), while others have used artificial settlement surfaces (e.g.,
Pomerat and Weiss, 1946; Sutherland, 1974; Menge et al., 1999;
Menge, 2000a). With artificial surfaces or collectors, a variety of
materials have been used including plexiglass plates with pits
(Raimondi, 1990), unglazed ceramic plates (Broitman et al., 2005),
and fiberglass, plexiglass, or PVC plates coated with a textured surface
(Farrell et al., 1991; Pineda, 1994; Menge, 2000a) among many others.
The multiplicity of surfaces used in studies of recruitment raises
questions of comparability among studies using different methods
and the extent to which artificial surfaces reflect patterns that occur
on natural rock surface (Raimondi, 1990). Further, rock surface
variation such as differences in rock type or texture may also cause
variation in settlement on natural surfaces (Pomerat and Weiss, 1946;
Barnes, 1956; Crisp, 1961; Raimondi, 1988). In addition, species
interactions can influence estimates of recruitment (Dayton, 1971,
Hawkins, 1983). For example, Dayton (1971) showed that barnacle
abundances were reduced by limpet “bulldozing,” defined as
dislodgement of barnacle cyprids and recent metamorphs by the
leading edge of the limpet shell as it grazes over the rock. Thus, if
bulldozing by limpets varies with their size, abundance, and species
composition, patterns of variation in recruitment of barnacles may be
influenced by limpet abundance.
Here we address these issues using results from factorial experiments to evaluate the importance of substratum (natural rock or
artificial settlement plates) and limpet bulldozing (present or absent)
in determining barnacle recruitment density. Following earlier
research (Connell, 1985; Raimondi, 1990), we define settlement as
the number of larvae attaching and surviving 24 h and recruitment as
the number of settlers surviving for up to one month. We addressed
six hypotheses:
161
H5. Because of texturing that can provide refuges for new recruits,
limpet bulldozing will have smaller effects on recruits on artificial
surfaces than on natural rock.
H6. recruitment of the coexisting acorn barnacle species Balanus
glandula and Chthamalus dalli will be affected in similar ways by
substratum and limpets.
2. Methods
2.1. Study sites
This study was carried out at five sites along the central Oregon coast
(Fig. 1), with subsets of four sites used in each of 2001, 2003, and 2008.
Replicate sites were located in regions of contrasting oceanographic
conditions, which are associated with variation in the width of the
continental shelf (Menge et al., 1997; Barth and Wheeler, 2005; Kosro,
2005). In all years the two northern sites were located in the narrow
continental shelf region (Fogarty Creek [both years] and Boiler Bay [both
years], 44°51′ N and 44°50′ N, respectively) while the southern sites
were located in the wider continental shelf region (Yachats Beach [2003,
2008], Strawberry Hill [all years] and Tokatee Klootchman= Gull Haven
[2001], southern sites; 44°17′N, 44°15′N, and 44°13′N, respectively). At
the intertidal areas at Fogarty Creek and Boiler Bay (hereafter, FC and
BB), abundance of macrophytes was relatively high, while abundances
of filter-feeders, predators, and macroherbivores were relatively low
(Menge et al., 1994, 1997; Allison, 2004). In contrast, at Yachats Beach,
Strawberry Hill, and Tokatee Klootchman (hereafter YB, SH, and TK) the
abundance of macrophytes was relatively low and abundances of filterfeeders, predators, and macroherbivores were relatively high (Menge
H1. Recruitment of barnacles on natural rock surfaces will be
positively correlated with recruitment on artificial surfaces.
H2. With increasing texture on artificial surfaces, settlement and
recruitment densities will increase.
H3. Recruitment of barnacles will be lower and more spatially
variable on natural rock surfaces than on artificial surfaces because
natural rock has lower and more spatially variable surface texture.
H4. Because of the negative effects of bulldozing, recruitment of
barnacles will be lower in the presence of limpets than in their absence.
Fig. 1. Study sites along the Oregon coast. Cape Blanco and the Columbia River are
shown for reference. Site codes are FC = Fogarty Creek, BB = Boiler Bay, YB = Yachats
Beach, SH = Strawberry Hill, and TK = Tokatee Klootchman.
162
et al., 1994, 1997, 2004). Differences in community structure were
reflected in differences in key dynamic processes. Rates of predation,
mussel recruitment, and grazing were all higher at southern sites than at
northern sites (Menge et al. 1994, 2004; Freidenburg et al., 2007).
Barnacle recruitment, however, did not vary consistently among the five
sites (Barth et al., 2007). These community and process differences have
persisted since at least the early 1980s to present (Menge et al., 2004,
Menge, B. A., pers. obs.).
2.2. Study design
To evaluate the simultaneous effects of limpet grazing and
settlement surface on the density of barnacle settlement (attached
cyprids) and recruitment (B. glandula and C. dalli), we established
experiments at wave-exposed locations at each site. All plots were
positioned at the lower edge of the mid zone, just below the mussel
bed. In 2001, five replicates of five treatments were set up in waveexposed areas at FC, BB, SH, and TK (Table 1). In 2003, we substituted
YB for TK to make wave action more consistent across all sites. Six
treatments were assigned randomly within each of five replicate
blocks (Table 1). In 2008, we included two additional settlement
surfaces to the two used in the 2001 and 2003 designs to evaluate the
influence of varying texture in addition to the effects of limpet
grazing. Eight treatments (four substrata × two grazing) in five blocks
were included in the 2008 experiment (Table 1).
Although several barnacle species settled in these experiments
(the above two plus Balanus crenatus, Balanus nubilis, and Pollicipes
polymerus), recruitment of the latter three was sporadic and usually
very low except for occasional annual pulses of the gooseneck
barnacle Pollicipes. Thus we focused our analyses on B. glandula and
Chthamalus. Cyprids of these species are identifiable, but our method
of monitoring bare rock plots lacked sufficient resolution to separate
these species so we combined all cyprid counts for analysis.
Earlier sampling of daily plates indicated that cyprid metamorphosis occurs within hours of settlement. We tested this assumption,
and also evaluated the rate at which metamorphosis to juvenile
barnacles occurred by carrying out daily sampling for two four-day
periods in July 2002 at the FC site. Three replicate settlement plates
were placed in the mid exposed zone on 09 July 2002 and collected
daily through 14 July. This process was repeated 22–26 July. Based on
this study (see Results), we define cyprids attached to the rock as
settlers and assume they reflect settlement over the past 24 h.
Table 1
Design of experiments testing the effects of substratum and limpets on recruitment of
barnacles.
Year
Surface
Treatment code
Treatment description
2001
ROCK
− limpets
+ limpets
− limpets
− limpets
+ limpets
− limpets
+ limpets
+ limpets
− limpets
+ limpets
+ limpets
− limpets
+ limpets
− limpets
+ limpets
− limpets
+ limpets
− limpets
+ limpets
− limpets
+ limpets
Paint barrier
Marked plot
Painted plate
Painted z-spar barrier
Unpainted plate
Paint barrier
Marked plot
Paint control
Painted plate
Unpainted plate
Paint control (partial paint barrier)
Painted z-spar ramp (YB only)
Unpainted z-spar ramp (YB only)
Paint barrier
Marked plot
Painted plate
Unpainted plate
Painted plate
unpainted plate
Painted plate
Unpainted plate
STW
2003
ROCK
STW
2003
STW
2008
ROCK
STW
TRAV
PVC
2.2.1. Substratum effect
Many types of artificial surfaces have been tried (see Introduction),
and over the years we have tested unglazed ceramic tiles, a building
material called “Hardiflex,” plastic plates coated with latex paint with
neoprene microspheres mixed in, Saf-T-Walk (see below), travertine and
polyvinyl chloride plate. Although each offers relative homogeneity in
surface texture, all have shortcomings. For example, tile undersides were
smooth except for a square of grooves. Barnacles settled primarily along
these grooves, leaving most of the surface unoccupied (Gaines, S. D., pers.
comm.; Blanchette, C. A., pers. comm.). Hardiflex and neoprene
microsphere surfaces also proved similarly inadequate; we often
observed recruits on the rock nearby but almost none on Hardiflex plates.
In this study, we used four different types of settlement surface. In the
2001 and 2003 experiments, to evaluate the effect of settlement surface,
we used 10 × 10 cm bare rock plots and 10 × 10 cm polyvinyl chloride
(PVC) plates covered with Saf-T-Walk® tape (3M Company, St. Paul,
Minnesota, USA)(Farrell et al., 1991; Menge, 2000a; Shkedy and
Roughgarden, 1997). Saf-T-Walk tape (hereafter STW) is a rubbery
textured surface that, since barnacles prefer to settle into pits and
rugosities (e.g., Barnes, 1956, Crisp, 1961), provides barnacle cyprids
with nearly ideal settlement surfaces and ensures substratum uniformity
(Farrell et al., 1991; see Fig. 2). The rock surface at all sites was basaltic, a
considerably less rugose surface than STW. Bare rock (hereafter ROCK)
plots were chosen to be representative of the texture of the rock at the
site (Fig. 2), but we avoided surfaces with crevices, pits, holes, grooves,
and similar heterogeneities to make these as comparable to the artificial
collectors as possible. This treatment allowed us to determine if plates
covered by STW reflected the patterns of recruitment that occur on
natural substrata. We note that this design does not specifically test the
effects of rock texture or substratum type since neither of these was
varied systematically in the design. Because of the differences in degree
of texturing on ROCK vs. STW, we expected to observe lower recruitment
densities on rock, but predicted that ROCK densities would be a
consistent fraction of the density on STW (Hypothesis H1).
In 2008, to evaluate the effects of surface texture, we added two
additional surfaces to the design. The smooth surface of PVC plates with
no STW (hereafter PVC) provided artificial surfaces with no texture and
travertine plates (hereafter TRAV) provided artificial surfaces with low
to moderate texture (Fig. 2). Ranked by texture, the surface order is thus
no texture (PVC), low texture (TRAV), moderate texture (ROCK) and
high texture (STW)(Fig. 2). All artificial plates were soaked in seawater
for at least a week to condition them before use in the field.
2.2.2. Limpet effect
To determine the effects of limpets on barnacle recruitment, we
established treatments with and without limpets (+limpet and
−limpet, respectively). To exclude limpets from ROCK and STW plots,
we surrounded one ROCK plot and one STW plate (2001 only) in each
replicate with a 3 cm wide band of marine epoxy, z-spar™ (Kop-Coat
Inc., Los Angeles, California), which was then painted with a copperbased anti-fouling paint (hereafter termed z-spar + paint barriers).
Copper paint barriers have been shown to impede limpets and chitons,
in most cases with no artifacts due to the presence of the paint (Cubit,
1984; Paine, 1992; Menge, 2000b; Freidenburg et al., 2007; Guerry,
2008; Guerry et al., 2009; see Benedetti-Cecchi and Cinelli, 1997 for
critique). Since past experiments indicated that the z-spar + paint
barrier had to be repaired often, we also tested the effectiveness of
copper paint in deterring grazers when coated on the sides and bottom
of the artificial plates (all years). Because differences between the
painted plate and plates with z-spar+ paint barriers were minimal (see
Results) we deployed only painted plates in the 2003 and 2008 studies.
2.2.3. Control experiment
The z-spar + paint barriers were relatively flat, so plate edges
protruded above the surrounding substratum by about 5 mm. This
abrupt edge could possibly create differences in flow over plates vs.
163
Fig. 2. Close-up photographs of the artificial surfaces used in the experiments, and of the range of rugosity observed in the rock settlement plots. The holes in the plates are 8 mm in
diameter. The area in the rock photos is scaled similarly to the area shown on the artificial plates. PVC = polyvinyl chloride plates, TRAV = travertine plates and STW = safety-walk
plates. The differences in surface texture and relative homogeneity of the artificial plates is evident in the photos, as is the heterogeneity in natural rock surfaces.
ROCK plots, or even deter limpets from +limpet treatments, and
could also have affected barnacle recruitment. In 2003, we tested this
potential artifact at YB by deploying additional treatments that
included z-spar “ramps” around the plates to minimize eddies over
the plate edges. The two treatments were ramps with (−limpet) and
without (+limpet) paint. All treatments are summarized in Table 1.
2.3. Monitoring procedures
The experiment was monitored monthly from June to September in
2001 and 2003, and biweekly in July and August in 2008. Plates were
replaced at all sites during the same tide series, usually on consecutive
days. Limpets on plates (bottom and top) were counted in the field.
Because small limpets are difficult to identify to species in the field, we
identified them to genus (Lottia) only. The species most likely to be
included in this group are Lottia digitalis, L. pelta, L. strigatella, and an
unidentified Lottia species. After collection, barnacle settlers (cyprids)
and recruits (juveniles) on plates were counted and identified to species
in the laboratory under dissecting microscopes. ROCK plots were also
monitored during the same tide series. All limpets in ROCK plots were
counted and in −limpet plots, removed. Barnacle recruits to the ROCK
plots were counted and identified to species in the field using a field
microscope (2001, 2003) or hand lens (2008). Field microscopes have
greater acuity than hand lenses but sampling the entire surface was
impractical with microscopes so we sampled five haphazard fields of
view (0.1 cm in diameter) in each plot. Subsequent analysis suggested
that subsampling introduced much variability, especially at lower
densities. Thus, in 2008 we switched to hand lenses and counted the
entire plot. Recruit densities were standardized to an area of 100 cm2 for
analysis. In the field, cyprids could not be resolved to species with
microscopes, so in 2001 and 2003 we lumped all taxa into a single count
of “cyprids.” Hand lenses have lower acuity than microscopes, so in 2008
field counts of cyprids were unreliable and cyprid counts were only
available from STW plates, which unlike other surfaces, were switched
out and processed in the laboratory.
ROCK plots were scrubbed clean using a stainless steel wire brush
after counts and rechecked to make sure all individuals were removed.
On all surfaces filamentous algal blooms occurred at times, especially in
the absence of grazers. To help counting accuracy, we used bleach to
remove the algae, either in the field (ROCK and TRAV) or in the lab
(PVC). Counts in areas where recruits were visible prior to bleaching
indicated that only algae was removed, not settlers or recruits, allowing
unobstructed counts of settlers and recruits prior to their removal. Prior
to removal, percent cover of algae was recorded in all plots to allow
testing for potential interactions between ephemeral algae and recruits.
2.4. Data analysis
All analyses were done using JMP v. 8 (SAS, 2008). Establishment of
experimental replicates takes 1–2 days, so it would be impractical to
redo experimental setup each month to vary the location of each. Hence,
ROCK plot locations were fixed in space as was the location of the plates,
although the latter were replaced monthly. Because plot and replicate
locations were fixed, we used repeated measures analysis of variance to
164
Fig. 3. Overall responses within each year of limpets, barnacles and algae in + limpet and − limpet treatments on STW and ROCK surfaces, arranged by cape from north (FC, BB) to
south (TK/YB, SH). TK is actually south of SH, but is grouped with YB, the site used in 2003 and 2008. Note that scales for limpets are arithmetic, for barnacles are ln, and for algae are
percent cover.
test the effects of limpet bulldozing, site, region, and substratum on
barnacle recruitment. Linear contrasts were used to test differences
among specific combinations of treatments. We used ordinary least
squares regression to test the magnitude and direction of the
relationship among settlement, recruitment, algal cover, and limpet
density. In most cases, raw data were not normally distributed but
normality was generally achieved using log-transformations.
3. Results
3.1. Effectiveness of treatments: limpet exclusion
Overall, as has been demonstrated before (Cubit, 1984; Paine,
1992; Menge, 2000b; Freidenburg et al., 2007), copper-based paint
barriers were effective in excluding limpets in all years (Fig. 3A–H,
Table S1a). Average densities of limpets in +limpet vs. − limpet
treatments were 8.6 ± 0.9 (mean ± 1SE) vs. 1.0 ± 0.2 in 2001 (n = 120
vs. 120), 13.0 ± 1.2 vs. 1.0 ± 0.3 in 2003 (n = 311 vs. 158), and 4.6 ±
0.6 vs. 0.3 ± 0.07 in 2008 (n = 302 vs. 296), or differences of ∼ 9- to
∼ 15-fold. The limpet exclusion treatment accounted for the majority
of the variance (Table S1a). However, the limpet response also varied
through time by year, site and substratum type (Fig. 3A–H, S1, S2,
Table S1a, S2). In 2001, these effects were expressed in the withinsubjects effects of the month × site × surface interaction and the
month × surface × limpet interaction (Table S2, p = 0.0004 and
p = 0.03, respectively). In 2003, the four-way within-subjects effect
of month × site × surface × limpet indicated a highly context-dependent effect of all factors in combination (Table S2, p = 0.01). In 2008,
variable limpet response appeared in both month × site × limpets and
month × surface × limpet interactions (Table S2, p b 0.0001).
Despite these statistical interactions, limpet densities were higher
in + limpet than in − limpet ROCK treatments in all years (Figs. S1,
S2). The same general pattern held on STW (Figs. S1, S2), although in
2001 and 2008 the differences occurred at only two of the four sites
(BB and SH in 2001, FC and YB in 2008; Figs. S1, S2). In 2003, limpet
densities did not differ between the two + limpet treatments (marked
plot without paint and paint control) except for SH (Fig. S1).
Limpet density in +limpet treatments averaged over all times within
each year was greater in ROCK plots than on STW plates at FC and SH but
not different between these surfaces at BB, TK and YB. Limpet density in
+limpet treatments differed by year at BB (2001 = 2003 N 2008 on both
STW and ROCK), TK/YB (01b 03N 08 on STW, 01 b 03 = 08 on ROCK) and
SH (01 = 03 N 08 on STW) but otherwise was similar among years
(Fig. 3A–H, Table S1a, linear contrasts in 4-way ANOVA, p b 0.05). Overall
densities across sites were greater on ROCK than STW in 2001 (11.1 ± 1.2
vs. 6.2 ± 1.2, n = 60 each), but in 2003 limpet densities on ROCK were
similar to those on STW (11.4 ± 0.9 vs. 14.7 ± 2.2; n = 159, 152). In 2008,
densities in + limpet treatments varied with surface (ROCK: 7.3 ±1.2,
n = 149; STW: 1.3 ± 0.25, n = 157; TRAV 0.8 ±0.19; n = 138; and PVC
0.4 ± 0.13, n =154).
The variation among the artificial surfaces (STW= TRAV N PVC;
linear contrasts, p b 0.05) indicates that surface texture influenced
grazer abundance. Among years, the most striking differences were the
near absence of limpets at BB in 2008, a site that had high densities in
2001 and 2003 and the large among-year differences at the southern
sites (TK, YB and SH). Similar annual variation has been observed
previously (Freidenburg et al., 2007). At the southern sites in particular,
the limpets involved in these large among-year differences are mostly
small individuals (b5 mm), which are likely new recruits, suggesting
among-year differences in recruitment can be substantial. The
165
Fig. 4. Settlement of cyprids to STW coated PVC plates and to bare rock plots (ROCK) in the presence (+L, open symbols) and absence (− L, closed symbols) of limpets at four sites in
2001 and 2003. Sites were Fogarty Creek (FC), Boiler Bay (BB), Tokatee Klootchman (TK) and Strawberry Hill in 2001, and the same sites except for Yachats Beach (YB) rather than TK
in 2003. Differences among sites by surface type (in left panels for each year; SW = safety walk, BR = bare rock) were calculated using linear contrasts.
increasing densities observed through the summer (Figs. S1, S2)
indicate that limpet recruitment pulses tend to occur from July to
September.
3.2. Potential artifacts
3.2.1. Paint barrier vs. paint control
As noted in Methods, we tested artifactual effects of paint in 2003
by adding a paint control treatment (partial paint barrier on bare rock
or partially painted underside of STW plates). Testing the overall
effect of paint (partial barrier vs. unpainted control) revealed no effect
on recruitment of Chthamalus (1-way ANOVA; p = 0.27), Balanus
(p = 0.10), cyprids (p = 0.54), total recruit density (p = 0.23), and
limpets (p = 0.14). Algal cover, however was greater in paint controls
(9.6 ± 1.5%) than in unpainted plots (4.1 ± 1.5%; p = 0.001), suggesting a weak effect of the paint on limpet access to the plot during
submergence.
3.2.2. Test of z-spar ramp vs. no ramp
In 2003 at YB we also tested the effect of the presence or absence of
a z-spar ramp. Abundances of Chthamalus, Balanus, cyprids, and cover
of algae did not differ in the presence or absence of the ramp
(p = 0.30, 0.75, 0.96 and 0.87, respectively). Limpets tended to be
more abundant on plates without a z-spar ramp (p = 0.052) but this
was opposite of the expected effect. The absence of a z-spar ramp
evidently had little effect on our tests of the effects of limpets and
substratum on recruitment of barnacles.
3.3. Settlement responses
3.3.1. Overall effects
Surface had by far the strongest effect on settlement of cyprids
(Table S3, Fig. 4). Settlement was always much higher on STW than on
ROCK (Fig. 4; Table S3). The effect of surface varied among sites in
both 2001 and 2003 (Table S3). In 2001, settlement was somewhat
higher at the southern sites, TK and SH, while in 2003, among-site
variation was more idiosyncratic with the site of lowest settlement on
ROCK, BB, differing from the southern sites, and the site of next lowest
settlement, FC, differing only from the site of highest settlement, SH
(Fig. 4). As noted above, in 2008, settlers were not counted in the field.
Limpet effects on cyprids were relatively weak. In 2001, limpet
effects on cyprids varied through time (Table S3, within-subjects,
month × limpet interaction) but overall (Table S3, between-subjects)
limpets had no influence either as a main effect or through
interactions. In 2003, the limpet effect was stronger, but varied with
surface (Table S3, between-subjects, surface × limpet interaction),
with positive effects on STW and negative effects on ROCK (Fig. 4). The
lack of an effect in 2001 may have been due to the limpets being
swamped by the much higher numbers of cyprids and to the less
effective exclusion of limpets in 2001 compared to 2003 (Table 3).
3.4. Recruitment responses
3.4.1. Overall effects
For both species, recruitment varied among years, sites, surfaces
and between limpet treatments (Figs. 3I–Y and 5). Surface had the
largest effects on recruitment of both barnacle species which was
always higher on STW than on ROCK (Figs. 3I–Y and 5; Tables S1b, c).
Further, recruitment was progressively lower on increasingly smooth
surfaces, with a rank order of densities for both barnacle species of
STW N ROCK N TRAV N PVC (Fig. 5).
In addition to surface type, site and limpets also had strong effects,
but these varied among years and by species, surface and site
(Figs. 3I–Y and 5; Tables S1b, S4–S9). Among years for Balanus,
recruitment on STW was higher in 2001 and 2003 than in 2008 except
at TK/YB (Fig. 3I–L; linear contrasts, p b 0.05) while on ROCK no
interannual differences were observed (Fig. 3M–P, linear contrasts,
p N 0.05). For Chthamalus, recruitment on both STW and ROCK was
higher in 2001 and 2003 than in 2008, again excepting TK/YB
(Fig. 3Q–Y, linear contrasts, p b 0.05). For Balanus, recruitment varied
among years by site and the surface effect varied by year and presence
of limpets (Table S1B; two-way interactions). Recruitment on STW
was higher at the northern sites (FC and BB) than at the southern sites
(TK and SH) in 2001, did not differ in 2003 and was reversed in 2008
(Figs. 3 and 5; linear contrasts). Recruitment on ROCK varied
idiosyncratically among sites but revealed no regional trend across
years (Figs. 3 and 5). Rank orders of Balanus recruitment were similar
on the other two surfaces (TRAV and PVC), and recruitment densities
were lowest at FC (Fig. 5).
Limpet effects on Balanus recruitment averaged across sites varied
by year and surface (Fig. 3). On ROCK, negative effects were observed
in 2001 and 2003 but limpets had no effect in 2008. On STW, limpets
had no effect in any year (Fig. 3).
For Chthamalus, average responses across months varied among
years, both by site and by surface but limpets had no impact (Fig. 3
and 5, Table S1C). On STW, recruitment was strikingly lower in 2008
166
Fig. 5. Recruitment of Balanus glandula and Chthamalus dalli on STW, ROCK, TRAV and PVC in + limpet and − limpet treatments at four sites in 2008. Rank order of recruitment
density for each surface type across sites is shown in the left panels.
than in 2001 and 2003 while on ROCK, recruitment was lower in 2001
and 2008 than in 2003 (Fig. 3, linear contrasts, p b 0.01 or less). By site,
recruitment of Chthamalus was generally similar among sites except
in 2008 when it was higher at YB than the other sites (Fig. 3, linear
contrasts, p = 0.03 or less). In 2008, no differences occurred among
sites on TRAV or PVC, which had very low recruitment (Fig. 5, linear
contrasts, p N 0.05).
3.4.2. Temporal changes
Analyses incorporating temporal variation within year modifies
some of the above conclusions, likely due to seasonal progressions in
recruitment intensity, limpet abundance and algal cover. Changes
through time for both Balanus and Chthamalus were highly context
dependent, varying with all factors tested (Figs. 6–8; Tables S4–S9; fourway interactions in 2001 for both species, in 2003 for Chthamalus, all
Fig. 6. Recruitment of C. dalli and B. glandula to STW in + limpet and − limpet treatments at four sites by month in 2001 and 2003. Overall differences (between subjects analysis) in
effects of limpets through time were analyzed using linear contrasts. ns = not significantly different at a significance level of p = 0.05.
three-way interactions in 2003 for Balanus, and two of three three-way
interactions for both species in 2008). In 2001, temporal patterns varied
by month, site and species as well as surface. Recruitment of both
barnacles tended to increase over the summer at the northern sites (FC
and BB) on STW but on ROCK recruitment peaks of the two species were
inversely related, with Balanus peaking in August and Chthamalus
tending to peak in July and September (Figs. 6A, B, E, F and 7A, B, E, F).
Temporal trends differed at the southern sites (TK and SH) and again,
patterns varied with species and surface (Figs. 6C, D, G. H and 8C, D, G,
H). In contrast to weak overall limpet effects reported above, limpet
impacts on ROCK tended to be positive for Chthamalus and negative for
Balanus, but effects on STW were weak compared to ROCK (Figs. 6A–H
and 8A–H). Contrarily, the only significant effect seen on plates was a
positive effect of limpets on Balanus, the one instance showing the
reverse of the usual negative effect on this species (Fig. 6E).
In 2003, similar patterns were observed. Recruitment of the two
species varied through time similarly on STW, with peaks later in
summer, while patterns on ROCK were less similar (Figs. 6I–P and 7I–P).
North–south differences were less pronounced, except for Balanus,
which recruited more heavily at southern than at northern sites
(Figs. 6M–P and 7M–P). The effects of limpet bulldozing were again
contrasting, with negative effects on Balanus and positive effects on
Chthamalus on bare rock and similar, but non-significant trends on STW
(Figs. 6I–P and 7I–P).
In 2008, patterns of recruitment of Balanus were similar across all
surfaces, but Chthamalus was more variable in temporal recruitment
pattern by surface and site and tended to recruit proportionally more in
July (sample periods 1 and 2) than Balanus (Fig. 8). Although Balanus
always recruited more densely than Chthamalus in 2001 and 2003
(roughly a ten-fold difference), in 2008 this difference was vastly
167
greater, ranging from a ∼20-fold to ∼900-fold difference (Fig. 8). As
indicated by the necessity of plotting the data using different ranges in
2008 to be able to see the results clearly, among-site differences were
also greater in 2008 than in 2001 and 2003 (Figs. 6–8). Recruitment was
highest at YB and generally higher at the southern sites (YB and SH) than
at the northern sites (FC and BB). Strikingly, the site rank of recruitment
densities was generally consistent across surfaces, especially for Balanus,
with YBN SH N BB= FC. For the northern sites, Balanus recruitment was
similar on STW (Fig. 8E, F), higher at FC on ROCK (Fig. 8M, N), and higher
at BB on TRAV and PVC (Fig. 8U, V, DD, EE). Overall, recruitment rate was
predicted by texture, with rank order STWN ROCKN TRAV N PVC. Finally,
limpet effects on recruitment appeared less consistent in 2008, but were
generally positive for both species on STW and weak otherwise on the
other surfaces.
3.5. Algal response in experiments
In all years, algal abundance varied with all factors (Figs. 3, 9, 10,
Table S1D, S10; interactions among month, site, surface, and limpets).
In 2001, limpet grazing was the stronger effect but all factors but
month contributed substantially to algal variation. In 2001 at the
northern sites (BB and FC), algal cover was higher on ROCK and lower
on STW. Southern sites (SH and TK) showed the opposite trend. In
2003, limpet effects were clearly the strongest influence and among
site or region differences were not observed; cover on ROCK did not
differ by site and cover on STW was variable in each region. In 2008,
each factor had strong effects (Table S10), and regional differences
again seemed important with higher algal abundance at the northern
sites (Figs. 3 and 10).
Fig. 7. Recruitment of C. dalli and B. glandula to ROCK in + limpet and − limpet treatments at four sites by month in 2001 and 2003. See Fig. 6 caption for further details.
168
Fig. 8. Recruitment of C. dalli and B. glandula to STW, ROCK, TRAV and PVC in + limpet and − limpet treatments at four sites by sample period (1 = early July, 2 = late July, 3 = early
August, 4 = late August) in 2008. Note that because of large differences in range of settlement, scales are different by species and site.
3.6. Recruitment correlations
Although settlers and recruits were more abundant on STW than
on ROCK, across all sites abundances on these two surfaces generally
were correlated (Table S11). In 2001/2003, with the exception of
Balanus in +limpet plots (p = 0.49), abundances of Chthamalus,
Balanus, and settlers (cyprids) on ROCK increased with increasing
numbers on adjacent STW (Table S11, p = 0.0004 or less, R2 from 0.16
to 0.68). These relationships were strongest for cyprids (R2 = 0.68 in
+limpet plots, 0.51 in −limpet plots) and lowest for Chthamalus
(R2 = 0.19 and 0.16) (Table S11).
In 2008, similar relationships were observed for Balanus (pb 0.0001,
R2 =0.24 in +limpet plots, 0.35 in − limpet plots) but not for Chthamalus
(p=0.83, 0.74), likely due to the very low recruitment of this species in
this year (Table S11). For Balanus, strong positive correlations were
observed between recruitment on all surfaces tested (STW, ROCK, TRAV
and PVC), explaining between 17% and 71% of the variance (Table S11).
Limpet grazing appears to have affected the strength of these
correlations, but differently in 2001/2003 vs. 2008. In 2001/2003, more
variance was explained in +limpet than in −limpet plots for Chthamalus
and cyprids, while in 2008, in all seven comparisons, less variance was
explained in +limpet than in −limpet plots (Table S11).
169
Fig. 9. Algal cover in +limpet and −limpet treatments on STW and ROCK at four sites by month in 2001 and 2003. Significance levels for differences between limpet treatments are shown
for each panel. In 2003, data are shown for both +L treatments (marked plot and paint control; see code in panel N), so upper significance level in each panel is for the −L to +L (marked
plot) comparison and lower significance level is for the −L to +L (PC) comparison. ns= no difference.
3.7. Potential interactions
The relationships among the cover of algae, the density of limpets,
and the abundance of recruits varied between STW and ROCK (Table
S12). Algal cover was inversely related to limpet density on ROCK in
all three years, explaining 14%–47% of the variance but on STW this
relationship was weak to nonexistent, explaining 0% to 7% of the
variance (Table S12).
Limpet-recruit regressions varied by year and surface but the two
species responded similarly (Table S12). Both Chthamalus and Balanus
recruit density was positively related to limpet density on STW and
ROCK, but this relationship was relatively strong only on STW in 2003
and 2008 with a weak effect on ROCK in 2003. Recruit-algal
regressions also varied by taxon, year and surface (Table S12).
Chthamalus abundance increased with algal cover on STW in 2001, but
was negatively affected on ROCK in 2003 and 2008 and on STW in
2008. Balanus abundance also increased with algal cover on STW in
2001 and on both surfaces in 2003, but was negatively affected on
STW in 2008. Barnacles were neutral to algal cover in other cases
(Table S12).
3.8. Daily samples
The two bouts of daily sampling of recruitment indicated that
inputs of larvae were much higher in early July than in later July,
especially during the first three days of this period (Fig. 11, Table 3).
They also showed that proportionately more Chthamalus had
metamorphosed after 1 day (0.71 ± 0.04) than Balanus (0.20 ± 0.04)
(Table 3; life stage × species interaction), suggesting that the former
metamorphoses more quickly than the latter. The daily patterns
suggest that a settlement episode was underway the first few days of
the first period in July 2002, and that low but relatively steady
numbers were settling beyond that time, perhaps lasting through the
second episode (Fig. 11).
4. Discussion
Our results suggest that, as expected, recruitment densities were
higher on STW than on ROCK. Densities on STW collectors were
always higher and often much higher, ranging by year, site and taxon
from 2.2 to 87 times higher, than on bare rock surfaces. As suggested
by the 2008 experiments, which incorporated two additional types of
artificial collector with successively smoother surfaces, this difference
seems most likely due to differences in texture. In contrast, limpet
effects on settlement and recruitment, although statistically significant, were much weaker. Our interpretation of these results is that
settlement surface was the most important factor in determining
settlement and recruitment density in our study. We suggest that
artificial collectors are best viewed as providing estimates of relative
recruitment or settlement as opposed to estimates of the actual
number of new individuals entering populations at rocky intertidal
sites. Below, we examine our results in some detail and further discuss
170
Fig. 10. Algal cover in + limpet and − limpet treatments on STW, ROCK, TRAV and PVC at four sites by month in 2008. Average rank of algal cover by site is shown in the third column
of panels. Significance levels for differences between limpet treatments are as in caption to Fig. 9.
their likely significance for studies of recruitment dynamics of rocky
intertidal communities.
4.1. Effects of surface type
In using tools such as artificial settling surfaces in ecological
research, it is important to know what the surfaces are actually
quantifying. As predicted by hypothesis H3 (see Introduction), this
experiment revealed that settlement and recruitment were both
substantially greater on STW surfaces than on bare ROCK surfaces. For
example, average abundances of Chthamalus and Balanus on STW
ranged from ∼ 2.2 to 87 times and from ∼ 1.45 to 86 times than on
ROCK, respectively (Table 2). These differences were sensitive to
interannual variation in recruitment. In 2008, recruitment of both taxa
on STW was lower than in earlier years (overall, STW, Balanus: 2.3 to
4.2-fold difference, Chthamalus: 22.3- to 29.3-fold difference).
Between-year differences were much less on ROCK and in fact,
Balanus recruitment on ROCK was actually 2–3 times higher in 2008
than in 2001 and 2003. Settlement (cyprids) differed between STW
and ROCK even more, ranging up to 1179 times greater on STW than
Fig. 11. Daily settlement (cyprids) and recruitment (metamorphs) over two blocks of time for Balanus and Chthamalus at Fogarty Creek.
171
Table 2
Average (+ 1SE) abundances of recruits, settlers, limpets and percent algal cover on STW plates vs. ROCK plots in + limpet and − limpet treatments, averaged across the four sites in
2001, 2003, and 2008. 2003 data combined limpet (+ limpets − paint) and paint controls (+ limpets + paint) abundances. Coefficients of variation (CV) are based on ln-transformed
data. STW N ROCK indicates the magnitude of the difference between the density of the taxon on STW plates vs. ROCK plots.
− limpet
+ limpet
Year
Taxon
Mean abundance
STW
Mean abundance
ROCK
CV
STW N ROCK
Mean abundance
STW
Mean abundance
ROCK
CV
STW N ROCK
2001
C. dalli
7.7 ± 1.7
(60)
32.3 ± 9.0
(60)
7.2 ± 1.1
(60)
20.3 ± 5.3
(55)
15.96 ± 1.61
(160)
15.26 ± 2.14
(160)
11.4 ± 0.88
(159)
0.94 ± 0.63
(159)
2.7 ± 0.7
SW = 42.7
RO = 105.2
SW = 22.0
RO = 85.6
86.1
4.8 ± 1.4
(60)
88.0 ± 11.3
(60)
5.7 ± 1.1
(60)
28.5 ± 6.0
(55)
9.2 ± 1.8
(80)
143.8 ± 24.7
(80)
1.7 ± 0.5
(80)
74.9 ± 3.5
(80)
3.3 ± 0.8
SW = 31.8
RO = 154.2
SW = 20.3
RO = 41.5
86.1
C. dalli
662.7 ± 150.3
(59)
1120.2 ± 211.6
(59)
6.2 ± 1.18
(60)
6.88 ± 2.4
(59)
419.1 ± 42.2
(152)
1323 ± 134.4
(152)
14.72 ± 2.21
(152)
12.9 ± 1.9
(158)
18.1 ± 4.8
B. glandula
(80)
634.0 ± 127.1
(80)
119.5 ± 43.2
(80)
2.6 ± 0.5
(80)
37.4 ± 4.5
(80)
(80)
13.5 ± 2.1
(80)
4.5 ± 2.2
(75)
B. glandula
Limpets
Algal cover
2003
C. dalli
B. glandula
Limpets
Algal cover
2008
Limpets
Algal cover
SW = 76.2
RO=115.3
6.7
413.1 ± 66.4
(57)
3542.5 ± 1843.3
(57)
0.3 ± 0.1
(60)
19.6 ± 4.7
(57)
401.8 ± 60.0
(78)
1675.2 ± 220.6
(78)
0.4 ± 0.1
(78)
32.0 ± 4.1
(80)
4.8 ± 1.2
SW = 49.5
RO = 53.2
5.3
(80)
500.7 ± 104.6
(80)
227.0 ± 55.3
(80)
0.35 ± 0.14
(80)
59.2 ± 4.9
(80)
(80)
0.6 ± 0.2
(80)
43.4 ± 5.0
(74)
34.7
0.86
0.34
SW = 23.1
RO = 66.1
SW = 20.0
RO = 78.2
26.3
86.7
1.3
13.7
on ROCK (Table 2). H1 also accurately predicted that variability of
settlement and recruitment was greater on ROCK than on STW
(Table 2). With the single exception of Balanus in − limpet plots in
2008, in every STW-ROCK comparison coefficients of variation (CV)
were higher on ROCK than on plates, with the highest values for
cyprids (Table 2).
The basis for this difference is most likely the difference in texture.
STW®, a plastic rubbery substance designed as an anti-skid surface for
boat decks, swimming pools and other slippery areas, has a uniformly
and highly textured surface with pits ranging in size up to 0.3 mm
(e.g., Fig. 2). ROCK surfaces at our sites, in contrast, are far less
textured varying from smooth to moderately rough and heterogeneous. Consistent with this interpretation, in the 2008 experiment,
recruitment on the additional artificial surfaces, TRAV (with low
surface texture; Fig. 2) and PVC (negligible texture; Fig. 2) was
successively lower than on ROCK. Cyprids prefer pitted or textured
surfaces over smoother surfaces (Barnes, 1956; Crisp, 1961; Connell,
1985; Sanford and Menge, 2001; Leslie, 2005), and range in average
length from ∼ 0.087 to 0.107 mm (Menge, B. A. unpubl. data). The
difference in settlement and recruitment can be easily understood in
terms of not only rugosity but the size and density of the pits on STW
vs. ROCK, TRAV and PVC.
If settlement and recruitment densities are so different between
rock surfaces and the artificial collectors, why use collectors at all? Or
why not use collectors that do a better job of reflecting actual rock
surface texture? As noted earlier, previous workers have used a
variety of surfaces, from natural rock to various types of artificial
surfaces (see Introduction). When we initiated our long-term studies
of recruitment in the late 1980s and early 1990s, we conducted a
number of preliminary investigations to evaluate the different options
available. Our primary research goal was to gain insight into relative
differences in recruitment rates in space and time. In this context, we
rejected sampling on natural rock surfaces because field observations
indicated that along the Oregon coast, surface texture and composition could vary dramatically at all conceivable spatial scales, from mm
0.19
8.3
40.3
0.05
0.69
SW = 25.7
RO = 108.2
SW=20.3
RO = 55.7
43.7
11.5
0.24
0.43
SW = 114.6
RO = 128.7
1.45
SW = 60.3
RO = 54.0
2.21
0.58
1.36
to thousands of km. As has been repeatedly demonstrated, surface
texture is a major cue for cyprid settlement (e.g., Barnes, 1956; Crisp,
1961 and many others), and thus one goal was to reduce among-plot
variance in recruitment invariably introduced by the naturally
heterogeneous surfaces of intertidal rocks (e.g., Fig. 2).
Another characteristic of intertidal rocks is variation in composition and hardness (e.g., rocks can consist of mudstone, sandstone,
basaltic, granite, etc.), both of which qualitatively have been observed
to be related to variation in density of recruits and adults of barnacles
(Menge, B. A., pers. obs.). For example, barnacle recruitment is
extremely low on sandstone and mudstone, and as a probable
consequence adult densities are also low, even when densities are
high on adjacent harder surfaces. Sandstone and mudstone erode at a
high rate (Menge, B. A., pers. obs.), so barnacles settling on these
surfaces face a very short lifespan (days to weeks). The low adult
densities on such surfaces is not due to a lack of supply; STW plates
attached to these substrata accumulate recruits at rates comparable to
those attached to harder surfaces (Menge, B. A., pers. obs.). These
considerations thus led to the conclusion that artificial collectors that
controlled for texture, hardness and composition were the best choice
for our purposes.
We have observed that under conditions of exceptionally dense
settlement, the smooth surfaces usually shunned by cyprids can be
settled on after the rugosities in the substratum, whether natural or
artificial, are filled (authors' pers. obs.). These massive settlement
events on smooth surfaces rarely result in similarly high densities of
juvenile barnacles, however, suggesting high mortality and thus that
such settlement is a poor choice and an act of “desperation” on the
part of the cyprids. Under more typical conditions, the vast majority of
settlement and recruitment occurs on rugose substratum.
This raises yet another issue; are STW plates “magnets” for
cyprids? That is, do the plates deplete the larval supply sufficiently
that settlement densities on nearby rock are lower than those that
would occur in the absence of the plate? We have no real way to
address this issue without further research. However, given the
172
turbulence of intertidal habitats and our observation that cyprids will
settle on rock within cm of the collector plates, it seems unlikely that
this possible behavior is the primary cause of the higher densities on
STW plates and lower densities on rock.
Shanks (2009) recently criticized the use of STW plates, citing
results of his research at a site on the southern Oregon that suggested
that STW plates heated rapidly in the sun, killing settled cyprids
within hours. In his studies, he found much higher recruitment on
ceramic floor tiles than on STW plates. His studies were carried out in
2007 from late May to the end of July.
Our results are inconsistent with Shanks' (2009) results. For
example, we find much lower recruitment on artificial tiles (both
TRAV and PVC) than on STW. One difference that could account for
our different results is that Shanks' studies were carried out in May
through July while ours were carried out from June/July through
August/September. The significance of this difference is that on the
Oregon coast, timing of low tides gradually falls earlier in the day in
each successive tide series through the summer. Thus, exposure of
settlers and recruits to warmer mid-day temperatures gradually
lessens as the summer progresses, presumably meaning lower
exposure to thermal stress. This could explain why numbers of
recruits on STW earlier in summer were generally lower in our
experiments than they were later in summer (e.g., Figs. 6–8).
However, numbers of recruits on other surfaces (TRAV, PVC and
ROCK) were usually also lower earlier in summer (Figs. 6–8). If
mortality explains the lower numbers on STW, and STW (and PVC)
plates get hotter than ROCK or TRAV, then it seems likely that
consistently higher numbers would be seen on the latter than on the
former surfaces. Further, we have also measured plate vs. rock
temperatures (B. Menge et al., unpublished data), and like Shanks
found that STW plates often reached temperatures in the 40 °C range.
It is possible that the differences between Shanks' (2009) results
and ours may be influenced by other differences in spatial or temporal
coverage. Shanks' study was done in one summer at one site while
ours spanned three separate years at four sites per summer. Further,
examination of our long-term data set spanning six sites along the
central and southern Oregon coast (including Cape Arago, which is a
few km south of Shanks' Bastendorff Beach site) and 20 years (1989–
2008) suggests other time/space differences that could be important
(B. Menge et al., unpublished data). Average recruitment of Balanus
was relatively high from March through November, with some sites
having peaks of recruitment in August or September and others
having relatively uniform recruitment through this 9-month period.
Importantly, variance among successive months could be very large,
especially at Cape Arago. Thus, it is possible that a repeat of Shanks'
(2009) study would have a different outcome. Without further
investigation, it is impossible to determine the causes for the different
results obtained by Shanks (2009) and the present paper.
What other alternatives to STW might we consider? Our sense is
that the best form of standard collector would be one that mimicked
Table 3
Three way analysis of variance of variation in numbers of settlers by period (early vs.
late July 2002), life history stage (cyprid vs. metamorph) and species (Chthamalus vs.
Balanus). Analysis was on ln-transformed data. R2 = 0.48. Boldface values are significant
at p = 0.05.
Analysis of variance
Source
SS
df
MS
F
p
Period
Life stage
Species
Period ⁎ life stage
Period ⁎ species
Life stage ⁎ species
Period ⁎ life stage ⁎ species
Error
40.70672
5.51549
5.91069
3.94577
1.08498
58.15874
5.70853
138.29542
1
1
1
1
1
1
1
100
40.70672
5.51549
5.91069
3.94577
1.08498
58.15874
5.70853
1.38295
29.43461
3.98819
4.27396
2.85314
0.78453
42.05399
4.12778
b 0.0001
0.049
0.04
0.09
0.38
b 0.0001
0.045
natural rock surface texture of moderate rugosity. After our initial
trials, we explored the possibility of having unglazed ceramic tiles
with appropriate surface texture manufactured for us, but high cost
made this option unfeasible. We felt such tiles should be used only
once since the porous nature of the tile could lead to accumulation of
biofilm residues that might not be removable and might influence
settlement in later uses (see Bourget, 1988; Keough and Raimondi,
1995; Thompson et al., 1998). (In contrast, STW plates are reusable;
the STW can be removed and a new layer applied to the non-porous
PVC plastic plate.) Similar restrictions applied to other surfaces
considered such as travertine, slate, granite, and other types of natural
rock. Nonetheless, given the extensive use of STW plates around the
globe, the apparent success (contra Shanks, 2009) of these collectors
in providing relative measures of recruitment in space and time, and
the lengthy time series that have been accumulated in PISCO and
other programs (Broitman et al., 2008; Navarrete et al., 2008), we are
hesitant to recommend switching to new surfaces at this point. If the
goals are to estimate absolute rates of input of recruits or the study is
short-term, more local-scale, and not aimed at making comparisons
with other investigations, however, then using natural rock surfaces
or molds of natural rock surfaces would be a good choice.
4.2. Effects of limpets
The results of the limpet manipulations suggest that their effects
are more complicated than the simple, uniformly negative effects
predicted by H4 (see Table 2). Overall, limpet activity had strong
effects on settlement and recruitment of Balanus (2-way ANOVA with
limpets and surface as factors, p = 0.008) but no effects on Chthamalus
(2-way ANOVA, p = 0.25). Further, the effect on Balanus varied among
years and surface type. Balanus recruitment densities were lower in
+limpet than in −limpet plots in 2001 and 2003 (suggesting a
negative effect of limpets), but in 2008 recruit density differences
suggested a positive effect on STW and a negative effect on ROCK
(Tables 2, S1B; surface × limpet interaction).
Our results suggest that limpet effects were contingent on density
of settlers or recruits. For example, on ROCK limpets negatively
affected settlement of cyprids strongly in 2003 (p = 0.005) and
weakly in 2001 (p = 0.049; linear contrasts in 3-way ANOVA),
possibly due to swamping by much higher cyprid densities in 2001
(Table 2). On STW, limpets had no effect on cyprids in 2001, again,
possibly due to swamping, but in 2003 had a positive effect (Table 3).
As predicted by H5, this positive effect may be a consequence of
the influence of rugosity on limpet crawling and grazing. Limpets,
which range in length from about 2 to 15 mm, with most in the 5–
10 mm range, are too large to fit in the pits and thus skim over the pits
on STW as they crawl. While the radula (tongue-like feeding
apparatus) of a 5 to 10 mm limpet is likely to be ∼0.12 to 0.25 mm
in width (Kitting, 1980; assuming proportional scaling using a limpet
24.2 mm with a radula 0.6 mm wide), and thus could fit into the larger
pits, it seems unlikely to be able to affect most cyprids that settle into
pits. In contrast, due to growth and change in morphology,
metamorphs extend further out of the pits in STW and may be
more vulnerable to bulldozing than are cyprids, at least during the
first several days after metamorphosis. A direct effect of limpets on
microalgae may also influence survival of cyprids by removing a
potential barrier to settlement. Finally, a weaker effect of bulldozing
on cyprids than on metamorphs may also reflect a shorter period of
vulnerability of cyprids (≤24 h) than metamorphs (several days)
coupled with spatial and temporal variability in limpet grazing. Thus,
the positive effect of limpets on STW may result from the removal of
microalgae from the ridges of the pits and a reduction in the ability of
the limpets to bulldoze cyprids in pits. Conversely, the negative effect
on ROCK seems likely due to the greater vulnerability of cyprids
because of the much smoother texture of the rock surface and thus
relative lack of settlement micro-refuges. Further investigation of the
interaction between grazing activity, substratum and life history stage
of barnacles seems warranted.
Effects of limpets similar to those on cyprids were also observed with
recruits, but counter to H6, which predicts similar effects of substratum
and bulldozing on both species, the taxonomic resolution reveals yet
another difference in how species responded to limpet bulldozing. With
the exception of STW in 2008, when grazing had a positive effect (Fig. 3,
3-way ANOVA on site, surface, and limpets, surface× limpets interaction, p b 0.0001), limpets had either no or weakly positive effects on
Chthamalus and negative effects on Balanus (Figs. 3 and 5; Tables S4–S9).
These effects varied in space (among sites) and time, likely as a
consequence of spatio-temporal variation in recruitment density,
abundance of limpets and algal cover (Figs. 3, 6–10).
The mechanism underlying the relative resistance of Chthamalus to
bulldozing compared to Balanus is unclear. Chthamalus recruits are
similar in size to those of Balanus (0.932 ± 0.01 vs. 0.95 ± 0.05 mm,
means of means of 9 measurements per species across 8 sample dates
in 2002), suggesting resistance is not based on size. However
Chthamalus do appear to metamorphose faster than Balanus. Two
sets of daily samples taken in July 2002 indicate that after one day, the
majority of Chthamalus were metamorphs while the majority of
Balanus were still cyprids (Fig. 11). Thus a possible mechanism
underlying resistance is that Chthamalus can quickly metamorphose
and thus attach more firmly faster than can Balanus. We conclude that
the effects of limpet bulldozing on settlement and recruitment are
context-dependent, varying with the density of settlers and recruits
(as indicated by the differences between 2001 and 2003 for cyprids
and 2001, 2003 and 2008 for metamorphs), surface rugosity, and
differences in the abilities of settlers or recruits to resist limpet
disturbance. Hence, the prediction of H5, that barnacle recruitment
will be similarly affected by surface and limpet grazing is not
supported. Bulldozing reduced the density of Balanus but had little
effect on the density of Chthamalus (excepting a positive effect in 2008
on STW), most likely due to more rapid metamorphosis and thus
firmer attachment of the latter.
4.3. Relationship between densities on different surfaces
Hypothesis H1 predicts that even though magnitudes of
settlement to different surfaces may differ, settlement and
recruitment on STW will be correlated to that on ROCK. Our
analyses support this prediction. For both settlers (cyprids) and
recruits (abundances of Chthamalus and Balanus), numbers on STW
were usually positively related to numbers on ROCK, the exceptions being Balanus in + limpet plots in 2001/2003 and Chthamalus
in 2008 (Table S11). These positive relationships explained
between 16% and 68% of the variance. In 2008, correlations
among the four different surfaces were also relatively strong
(explaining 17% to 71% of the variance; Table S11).
These relationships seem to be relatively insensitive to counting
method or location. In 2001 and 2003, counts on ROCK were made in
five fields of view of known area using field microscopes and then
adjusting numbers to 100 cm2. In 2008, we used hand lenses to count
recruits in the whole area of ROCK, TRAV and PVC plates, and counted
recruits on STW in the lab using both a hand lens and a dissecting
microscope (the method also used in 2001/2003). Despite this
variation in method, the amount of variance explained between
2001/2003 and 2008 on STW vs. ROCK tended to be similar for Balanus
(again excepting the 2001/2003 +limpet plots)(Table S11). Further,
STW counts using hand lenses and lab microscopes were strongly
correlated (62% to 86% of the variance explained for Balanus;
estimates for Chthamalus were compromised by very low recruitment
of this species in 2008). On the other hand, hand lenses did not
provide the resolution needed to detect and identify cyprids, which is
why these were not counted in 2008.
173
4.4. Spatial variation
Most analyses revealed strong differences among sites in recruitment, limpet densities, and algal cover (e.g., Fig. 3). The most
consistent spatial trend, however, was the regional difference
between the two northern sites on Cape Foulweather and the three
southern sites on Cape Perpetua (see also Menge et al., 1997, 2004;
Leslie et al., 2005; Barth et al., 2007; Freidenburg et al., 2007). Patterns
at FC and BB were consistent for barnacle recruitment, algal
abundance and limpet density. Similarly, patterns at SH tended to
be the same as those at TK and YB despite the switch from TK to YB
between 2001 and 2003, and, overall, different from FC and BB, at least
in the three years covered by this study. For barnacles, however,
longer-term data suggest that the regional differences observed
during these experiments is not consistent. Examination of longer
term (1989–2008) data indicated that in some years one cape had
higher recruitment, in others, the other cape had higher recruitment
and in still other years, the capes did not differ (e.g., Leslie et al., 2005;
Barth et al., 2007; Broitman et al., 2008).
5. Conclusions
We conclude that surface texture has the greatest effect on
settlement and recruitment of these two barnacles, an observation
that is consistent with classic studies in the United Kingdom and
elsewhere (e.g., Barnes, 1956; Crisp, 1961; Chabot and Bourget, 1988).
In addition, limpet grazing activity can influence settlement and
recruitment, but this effect is variable through time, with the density
of settlement and recruitment, with the specific barnacle taxa involved,
and with surface rugosity. Important variation can also occur in space,
both at the local site scale, and at the regional (cape) scale.
A primary goal in this study was to evaluate the extent to which
settlement on artificial surfaces provided relatively comparable
estimates across space and time that were independent of variation
in surface texture, and reflected actual recruitment rates to rock
surfaces in the intertidal. Our conclusions are that recruitment on
STW plates does provide a method for allowing comparisons of
potential recruitment across multiple spatial and temporal scales, but
that, not surprisingly, recruitment densities on STW substantially
overestimate actual recruitment to rock. The tradeoff between two of
the goals in a recruitment sampling program remains: STW plates
provide the ability to sample many sites across large spatial scales
over long time periods but overestimate recruitment densities, while
bare rock counts provide more direct estimates of actual recruit
densities but, due to much longer “handling times” in the field, are
more limiting in spatio-temporal coverage. It is possible that with a
correction factor, recruitment on STW potentially could provide an
approximation of actual recruitment to bare rock surfaces and thereby
allow for both precision in estimates and comparisons at multiple
spatial and temporal scales. However, the fractions of recruits on
ROCK compared to STW varied by species and year (e.g., for 2001,
2003, and 2008, respectively: Chthamalus, 1.1, 2.9, and 11.0% and
Balanus, 2.3, 5.4, and 26.8%), suggesting the need to maintain parallel
sampling schemes of both types of surface, at least at a few locations.
Acknowledgements
We thank the legions of undergraduate interns for their assistance
in fabricating collectors, and deploying, replacing, and processing the
many samples analyzed here. A. Iles, J. Tyburczy, S. Dudas, F. Chan, and
G. Rilov and anonymous reviewers provided constructive criticism on
the manuscript. The research was funded by an endowment from the
Wayne and Gladys Valley Foundation, and grants from the A. W.
Mellon Foundation, the David and Lucile Packard Foundation, and the
Gordon and Betty Moore Foundation. This is publication # 291 from
PISCO, the Partnership for Interdisciplinary Studies of the Coastal
174
Ocean, a Large-Scale and Long-Term Ecological Consortium, funded
principally by the David and Lucile Packard and Gordon and Betty
Moore Foundations. [SS]
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in
the online version, at doi:10.1016/j.jembe.2010.04.032.
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Supply-side ecology, barnacle recruitment, and rocky intertidal

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