Abstract:
Traditional ecological models developed in rocky intertidal systems state that
species ranges are determined primarily by physical stress in upper tidal zones and biotic
interactions in lower tidal zones. Studies of the barnacles Balanus and Chthamalus show
that smaller chthamaloids are able to persist in a larger range of habitats than balanoids
because of their greater tolerance to physical stress and lower susceptibility to predation.
Ttested this model on the barnacles Balanus glandula and Chthamalus spp. at two sites in
Monterey Bay which differed in wave exposure and abundance of the common predatory
snail, Nucella emarginata. I ran lab experiments to determine prey preferences of N.
emarginata, and measured densities of both species of barnacles and of the whelk along
transects in the field. B. glandula and Chthamalus spp. distributions were positively
correlated, indicating that competition between the two species did not play an important
role in determining distribution. Nested ANOVA's of barnacle densities revealed
significant differences between sites and among replicate transects within each site for
both species. Although whelks were abundant in the exposed site, they did not play a
major role in determining barnacle abundance. Lab experiments showed that Nucella
emarginata had a strong preference for B. glandula over Chthamalus spp. As this
difference did not manifest itself in differential distributions in the field, I conclude that
factors other than whelk predation alone regulate the distribution of these species. A
strong recruitment event in spring 2001 of B. glandula enabled me to compare
distributions of B. glandula adults and recruits. No strong difference was detected. The
very high variance in barnacle density in both sites may indicate that barnacle
distributions in Monterey Bay are regulated by multiple complex factors. Further
research is needed to understand these interactions.
Introduction:
The concept of distribution is fundamental to ecology. One of the first questions
we ask when we are attempting to understand a new species is, where can we find it?
Although exact ranges are difficult to determine, it is fundamental to our understanding
of écology that we can consistently expect to see certain species in certain habitats in
certain regions.
The factors that determine species' ranges are complex. However, certain systems
lend themselves to the study of ranges. The rocky intertidal is an excellent model system
for studying the factors that determine a species' range because biotic and abiotic
conditions vary greatly over a very small spatial scale. Species' vertical distributions are
determined over a narrow band of coastline where conditions vary from the permanently
submerged subtidal to the almost permanently emerged spray zone. Many classic
ecological studies have used the rocky intertidal as a model community for studies of the
determination of species' range.
The work of Connell (1961a, 1961b, 1970) on rocky shores in Scotland and Puget
Sound has been hugely influential in intertidal ecology and community ecology in
general (i.e. Menge & Branch, 2001). Successive long term studies of the dynamics of
barnacle populations established a model for the determination of species range.
Barnacles of the genus Balanus were observed to be competitively dominant over
barnacles of the genus Chthamalus. In Scotland, where both barnacles were present.
Chthamalus was overgrown by Balanus , which is a faster growing barnacle genus
(Sanford, 2001). Chthamalus populations persisted due to their increased tolerance to
physical stress - which enabled them to live higher on the shore than Balanus. (Connell
1961b) Predation by whelks of the genus Nucella (formerly Thais) had a strong effect on
populations of Balanus in Puget Sound. Whereas most mortality of Balanus in Scotland
were due to overcrowding, most mortality of Balanus in Puget Sound was due to
predation. As a result of this predation, Balanus was limited to areas above the zone in
which Nucella was able to persist, thus much like the Scottish chthamaloids, Pacific
Northwest balanoids persisted largely in a refuge zone (Connell 1970.) The effects
observed on barnacles in these and other studies were largely responsible for the creation
of a central paradigm in intertidal community ecology, which has been widely applied:
upper limits of species' ranges are determined by physical stresses (i.e. heat, dessication).
while lower limits are determined by biotic factors (i.e. competition, predation).
Preliminary observations made in April 2001 at Hopkins Marine Station in
Monterey Bay caused me to question the applicability of Connell’s observations about
Balanus, Chthamalus, and Nucella to the local ecosystem. I set out to test whether
predation by Nucella emarginata might be limiting the distribution of Balanus glandula,
and in turn, whether competition with Balanus glandula was limiting the distribution of
Chthamalus spp.
Methods & Materials:
Data were gathered at two sites in Monterey Bay, California. The first site was on
China Point, a part of the Hopkins Marine Life Reserve at Hopkins Marine Station of
Stanford University. China Point is the location of long term research on intertidal
ecology and ecophysiology, but is off limits to non-researchers, and is therefore relatively
undisturbed. The part of the point sampled is an area of protected outer coast (Ricketts et
al. 1985). The second site was in Monterey harbor, just south of the Coast Guard
Breakwater. This area is very protected from waves and storms, and is in an area of high
human activity. However, the section of rocky intertidal used was relatively inaccesible
to foot traffic, and appeared to have little direct human disturbance.
Sites were chosen to provide a contrast of whelk abundances. Preliminary
observations indicated that whelks (mostly Nucella emarginata, but also limited number
of other species) were abundant at China Point, but were completely absent in the harbor.
In order to determine relative abundances of different species, I sampled transects
perpendicular to the shoreline that ran from the lowest barnacle I could find to the highest
barnacle. At China Point, it was not always possible to reach the lowest barnacle due to
strong waves action and treacherous rocks. I never found a barnacle growing below the
highest feather boa kelp (Egregia menziesii), and thus used this species as a proxy for
lowest barnacle in these highly exposed areas. I also ran a horizontal transect through an
area of high whelk abundance in order to expand sample sizes. On China Point, I divided
sampling equally between high barnacles (growing above the highest clumps of the alga
Endocladia), mid zone (growing in the Endocladia zone), and low zone (below the
highest barnacle of species Tetraclita). Within zones, I sampled randomly. In the harbor,
the distance between highest and lowest barnacles was less, and no clear community
zonation was evident, so 1 simply sampled randomly along the transect line, from the
lowest point where barnacles were found to the highest.
I sampled whelks in a .25 m’ quadrat. I chose one .01 m’ quadrat randomly from
within the .25 m’ quadrat to count barnacles. All barnacles of species Balanus glandula
and Chthamalus spp. were counted. No attempt was made to differentiate between C.
dalli and C. fissus, as they are ecologically similar and impossible to differentiate in the
field (Sagarin 1999). Barnacles greater than 4mm in diameter were classified as large.
while barnacles less than Imm in diameter were considered to be recent recruits. This
size classification was based on preliminary observations of whelk feeding preferences.
After sampling, the height of each .01 m’ quadrat was measured relative to bolts placed at
known heights above Mean Lower Low Water in the intertidal,
1 conducted lab experiments to elucidate whelk prey preferences. Barnacle-
covered rocks were taken from the harbor area. I found rocks in the harbor with a
mixture of Balanus and Chthamalus of a variety of sizes. I then mapped all of the rocks.
and placed them in flow-through tanks. Each tank contained two rocks, with the goal of
giving each tank approximately the same surface area of rock and cover of barnacles. In
all, the six rocks used had 1869 barnacles attached to them. Each tank contained five
whelks collected from China Point. Whelks were all similar in size, and sizes ranges
were similar in all tanks. The tanks were covered, and the whelks were left to feed for a
week on the barnacles. I checked the tanks twice a day to monitor the feeding progress
and to make sure that whelks were not escaping. When whelks were found on the outer
edges of the flow-through tanks, they were returned to the bottom, to encourage them to
climb around on the rocks. The experiment was terminated when approximately half of
the large Balanus glandula were eaten.
After the termination of the experiment, I tallied the number of barnacles on each
rock that were dead. I used a small dentist's tool to poke the opercular plates. If
opercular plates were missing or fell out when poked, the barnacle was counted as having
been eaten. In order to estimate surface area covered by barnacles, I measured basal
diameters of a subsample of barnacles, and multiplied by the number of barnacles present
in that tank.
Data from field and lab experiments were analyzed in Microsoft Excel 98 and in
Systat 8.0. In most tests, all barnacles larger than Imm in diameter were grouped
together as adults. Except where explicitly examined (i.e. when looking at recruitment).
barnacles less than Imm in diameter were excluded from analysis, as they were assumed
to be recent recruits.
Results:
In the lab experiment the whelk Nucella emarginata had a strong preference for
Balanus glandula over Chthamalus spp. Percent cover was used as a measure of
availability, assuming that cover would be proportional to the frequency of encounter by
à randomly-foraging whelk. The availability of both species of barnacle was close to
equal in all tanks (Fig. 1). The mean diameter of Chthamalus spp. was 2.23 mm, while
the mean diameter of B. glandula was 5.20. There were six times as many individuals of
Chthamalus spp. as B. glandula, but many of the Chthamalus were very small. Forty
two percent of the individual B. glandula were consumed, compared to only 2.3% of the
Chthamalus spp. Pooling all 3 tanks, the whelk's diet was 75.5% B. glandula (Fig. 1).
Nucella ate significantly more B. glandula than expected, based on percent cover as a
measure of availability (Chi-square = 14.1, P«.001).
Analysis of field data revealed a positive correlation between densities of N.
emarginata and B. glandula (r = .377, P«.001) (Fig. 2). A stronger positive correlation
existed between densities of N. emarginata andChthamalus spp. (r= .511, P5,001)
(Fig. 3) N. emarginata was entirely absent at Breakwater Cove, so correlations could not
be calculated for that site.
The vertical ranges of B. glandula and Chthamalus spp. show little difference.
(Figs. 4, 5) Plots of densities vs. intertidal height indicate that both species are found at
the same maximum and minimum heights in both regions (although these maximum and
minumum values are highly variable between the two sites.) A strong positive
correlation was found between the densities of B. glandula and Chthamalus spp. (r -
630, P«.001, Fig. 6)
Barnacle distributions were highly patchy in all sites. Abundances per .01 m2
quadrat varied from 0 to over 250. Mean abundance within different transects at each site
were highly variable (Figs. 7, 8). Nested ANOVA showed significant differences in
mean abundances between sites and between transects within sites (Table 1). Overall
numbers were higher in Breakwater Cove than on China Pt., and there was significantly
higher variance in numbers of Chthamalus in Breakwater Cove than on China Pt. (F test.
P2.05). (Fig. 9) Recruitment of Balanus glandula was unusually high during the
spring of 2001 (J. Watanabe, pers comm). Recruitment occurred throughout the vertical
range of B. glandula (Figs. 10 & 1 1), but was highly patchy throughought, with recruits
uncommon in most quadrats, and highly abundant in a small number of quadrats (Fig.
12). Although there was a significant positive correlation between numbers of adults and
recruits (r==.207, P «.05), the tightness of this trend was low because of the high
patchiness.
Discussion:
Results trom the laboratory experiment clearly show that Nucella emarginata
préfers to prey on Balanus glandula rather Chthamalus spp. This confirms work by West
(1986) on China Pt., which showed that whelks in the field had a diet consisting primarily
of B. glandula. Based on this result, and the previous work by Connell (1961a, 1961b.
1970), 1 would expect that areas with high whelk abundance would correlate with areas
of decreased B. glandula abundance. With less competition, and a relatively small threat
from predation, I would expect Chthamalus spp. to increase in abundance. As discussed
below, this differs from what I found in the field.
All possible combinations of the three species showed significant positive
correlations. While this does not prove that there is no effect of competition or predation.
it does show that this effect is fairly weak. If predation interactions were strong, B.
glandula densities might be expected to correlate negatively with N. emarginata densities
(Connell, 1970), as whelks would eat all barnacles below a certain tidal height.
Furthermore, if predation by N. emarginata was the major factor determining abundance
of B. glandula, I would expect to see recruitment in areas of high whelk abundance where
B. glandula adults were absent. B. glandula recruits were not seen recruiting to any areas
where B. glandula adults were absent. On the other hand, as B. glandula is a sessile
species, and it is to be expected that its predators will be found in areas where it is
present. Although 1 did not see the very strong interactions reported by Connell in Puget
Sound (1970), it is probable that whelks play some role in regulating the abundance of B.
glandula.
Space competition between B. glandula and Chthamalus spp. did not appear to be
strong. The tightest correlation between pairs of species was that between B. glandula
and Chthamalus spp., indicating that where one species was abundant, the other was also
abundant. This is most likely not due to positive interactions between the two species.
but rather is due to the fact that where suitable habitat was present for one species, it was
also present for the other. Areas occupied by macroalgae, cleared by limpets, covered in
mussels, or in sandy gaps in the granite outcrops are all examples of types of habitat
frequently encountered in sites where barnacles were mostly or completely absent. Those
areas where barnacles were present were rarely completely covered. Free space was
nearly always present (although it was not specifically studied in this experiment.) Only
one out of the 155 quadrats I examined appeared to fit the description of Connell (1961b
of Balanus growing so densely as to cover all available space and outcompete
Chthamalus. Even in this one exceptional quadrat, numerous Chthamalus were found
growing among the Balanus. Thus, I conclude that interspecific competition between
these two species is not an important factor governing their distributions in southern
Monterey Bay.
The clear preference shown by Nucella emarginata for Balanus glandula is not
surprising. Paine (1981) proposed that the chthamaloid barnacles have taken an overall
evolutionary strategy of remaining too small to be eaten. I did not examine the size
preference of N. emarginata, but I did measure all barnacles in the field that were being
actively drilled by whelks. I was unable to find any that were less than 4 mm in basal
diameter. This size is larger than one standard deviation from the mean diameter of
Chthamalus spp., but is nearly one standard deviation smaller than the mean for B.
glandula. Thus, it seems probable that by staying small, Chthamalus avoids becoming
prey of Nucella. It is also possible that Chthamalus that grow to a size approaching 4
mm in basal diameter are rapidly eaten by whelks. If this were the case, I would expect
Chthamalus from Breakwater Cove, where whelks are absent, to be larger than
Chthamalus from Hopkins. I did not test this hypothesis, but the rocks on which a mean
basal diameter of 2.23 mm was measured came from Breakwater Cove. This appears to
lend support to Paine’s hypothesis.
The high degree of variability in population densities seen between the two sites.
and between transects within each site indicates that neither of these species are
competitevly dominant, but rather are part of a larger and more complex system. It is
likely that population densities are regulated by a variety of factors, rather than simple
competition and predation between the three species I studied. Recruitment patterns,
predation by other species, parasitsm (Lopez, 2001), physical stresses, and competition
with a variety of other space occupiers (macroalgae, limpets, and the mussel Mytilus
californianus) are all major space occupiers in Monterey Bay) probably play important
roles in determining space occupancy in the rocky intertidal. While I cannot completely
rule out predation effects by N. emarginata and competition between B. glandula and
Chthamalus spp. as determinators of distribution, it appears that neither plays an
overwhelming role compared to factors that have not yet been elucidated. The rocky
intertidal has proven a fertile ground for understanding the distribution of species.
Fürther investigation of the factors that determine the distribution of these species in
Monterey Bay may contribute to our understanding of distribution in many habitats.
12
Acknowledgements:
This paper would not exist without the patient support of Jim Watanabe. I cannot
thank him enough for his advice and the large amount of time he devoted to this project.
Many other professors and grad students were helpful along the way. Fiorenza Micheli,
Eric Sanford and Rafe Sagarin contributed both ideas and papers from their libraries.
Joanna Nelson and Luke Hunt aided in surveying tidal heights. The other students in the
spring class helped create a positive learning environment. Daniel Serres and Galen
Weston kept me entertained and excited through dawn tides, dark nights of labor on
computers, and bright nights of friendship and the cheapest, tastiest vegan food known to
Monterey Bay.
Literature Cited:
Connell, J. H. 1961a. Effects of competition, predation by Thais lapillus, and other
factors on natural populations of the barnacle Balanus balanoides. Ecol. Monogr. 31: 61-
104.
Connell, J.H. 1961b. The influence of interspecific competition and other factors on the
distribution of the barnacle Chthamalus stellatus. Ecology 42: 710-723.
Connell, J.H. 1970. A predator-prey system in the marine intertidal region. Balanus
glandula and several predatory species of Thais. Ecol. Monogr. 40: 49-76.
Lopez, J. 2001. Spatial Distribution, physiological tolerances, and respiration rates of
larvae of the intertidal fly, Oedoparena glauca. Final Papers Biology 175H, Stanford
University, Miller Marine Biology Library.
Menge, B.A. and G.M. Branch. 2001. Rocky intertidal communties, in Marine
community ecology, M.D. Bertness, S.D. Gaines, M.E. Hay eds. Sinauer Associates,
Sunderland Ma.
Paine, R.T. 1980. The forgotten roles of disturbance and predation. Paleobiology. 7:
553-560.
Ricketts, E.F., J. Calvin, J.W. Hedgepeth, and D.W. Phillips, 1985. Between Pacific
Tidesw, 5“ ed. Stanford University Press, Stanford, Ca.
Sagarin, R.D., J.P. Barry, S.E. Gilman, C.H. Baxter, 1999. Climate-Related Change in an
intertidal community over short and long time scales. Ecol. Monogr. 69: 465-490.
Sanford, E. and B.A. Menge, 2001. Spatial and temporal variation in barnacle growth in
à coastal upwelling system. Mar. Ecol. Prog. Ser. 209: 143-157.
West, L. 1986. Interindividual variation in prey selection by the snail Nucella
emarginata. Ecology. 67: 798-809.
Table 1.
ANÖVA table for Nested Anova comparison of means between sites and
between transects within sites. Data were square root transformed prior to
analysis ((x+0.5))
Source
Sum-of-Squares df Mean-Square F-ratio F
Between Sites
607.992 1 607.992
13.540 0.006
Between Transects
359.220 8 44.903 2.847 0.006
Error
1892.626 120 15.772
Figure Legends
Fig. 1. Predation on Balanus glandula and Chthamalus spp. by Nucella emarginata in
laboratory experiment. Bars on left are the percent of the rock surface covered by each
barnacle species. Bars on right are measurements of the percent of the whelk's diet
belonging to each barnacle species. (n = 3 tubs, 1869 barnacles).
Fig. 2. Relationship between abundance of Balanus glandula and Nucella emarginata on
China Pt. N. emarginata were sampled in 25 m’ quadrats, and a .01 m’ quadrat was
chosen randomly within the .25 m’ quadrat to sample barnacle abundance. (n = 95
quadrats)
Fig. 3. Relationship between abundance of Chthamalus spp. and Nucella emarginata on
China Pt. N. emarginata were sampled in 25 m’ quadrats, and a .01 m2 quadrat was
chosen randomly within the .25 m’ quadrat to sample barnacle abundance. (n= 95
quadrats)
Fig. 4. Vertical distributions of Balanus glandula and Chthamalus spp. in the intertidal
zone at China Pt. Densities based on counts in .01 m2 quadrats. (n= 95 quadrats)
Fig. 5. Vertical distributions of Balanus glandula and Chthamalus spp. in the intertidal
zone at Breakwater Cove. Densities based on counts in .01 m’ quadrats. (n= 55
quadrats)
Fig. 6. Relationship between abundance of Balanus glandula and of Chthamalus spp. in
quadrats. Data from Breakwater Cove and China Pt. are combined. (n= 150 quadrats)
g. 7. Variation in mean abundances of barnacles between vertical transects on China
2t. Transects were placed perpendicular to shore, from the highest barnacle to the lowest
barnacle, spaced unevenly over an area with a total spread of 20 meters. Means are based
of 15 quadrats per transect.
Fig. 8. Variation in mean abundances of barnacles between vertical transects in
Breakwater Cove. Transects were placed perpendicular to shore, from the highest
barnacle to the lowest barnacle, spaced unevenly over an area with a total spread of 20
meters. Means are based on 10 quadrats per transect. Transect four (with much lower
abundances of both species) ran through an area of smaller cobbles which had lower
abundances of barnacles.
g. 9. Variation in mean abundance of barnacles between Breakwater Cove and China
Pt. These two sites are approximately 2 km apart. China Pt. is considered protected open
coast, while Breakwater Cove is within Monterey Harbor, and thus highly protected. (n-
75 at Hopkins and 55 at Breakwater Cove)
Fig. 10. Vertical distribution of Balanus glandula recruits and adults on China Pt.
Densities based on counts in .01 m’ quadrats. (n = 95 quadrats)
Fig. 11. Vertical distribution of Balanus glandula recruits and adults on China Pt.
Densities based on counts in .01 m’ quadrats. (n = 55 quadrats)
Fig. 12. Relationship between numbers of recruits and adults of Balanus glandula in
quadrats. (n = 150 quadrats)
Fig. 1
0.9
0.8
5 04
Fig. 2
Predation by Nucella in Lab
» Balanus
a Chthamalus
% of barnacle % of barnacles
surface area that were eaten
Number of Balanus vs. Number of Nucella
200
150
100
50

10
Number of Nucella per .25 m2 quadrat
Fig. 3
Number of Chthamalus vs. Number of Nucella
150
2 100
111.
Number of Nucella per .25 m2 quadrat
Fig. 4
Balanus and Chthamalus distributions in Breakwater Cove
2.5
2.0
1.5

S



1.0

S
S



-

SPECIES

Balanus
Chthamalu
0.0
100
200
300
Number of Bamacles per .O1 m2 quadrat
Fig 5
Fig 6
Balanus and Chthamalus distributions on China Pt.
3






32 15.12.2 14 1.2 :: : - -..




.... ....... ....... ....... . ..... . .
..-
—
100
200
300
Humber of Baracles perO1 me quadrat
Numbers of Balanus vs. Numbers of Chthamalus
300

5 200

£ 1004-
b.
200
300
100
Numbers of Balanus per .01 m2 quadrat
SPECIES
Balanus
Chthamalu
Fig. 7
05
Fig. 8
Variation Among Transects on
China Point
Variation Among Transects at
Breakwater Cove
Balanus
Chthamalus
E Balanus
EChthamalus
Fig. 9
16
Fig. 10
Variation between Breakwater
and China Pt.
EBalanus
HChthamalus
Breakwate
Hopkins
Balanus Recruitment on China Pt.



SIZE
Adults
Recruits


300
Number of barnacles per .O1 m2 quadrat