Abstract
This study examined behavioral patterns of three intertidal whelks in response to
tidal variation. Nucella emarginata, Ocenebra circumtexta, Acanthanucella punctulata
have widely overlapping habitat but significantly different resource utilization strategies.
All three species were found in the primary study site, a 6m by 9m region of rocky
intertidal shore with a vertical range of 0 to +2.5m above MLLW. Individuals were
marked and observed at low tide for a two week period to discern basic patterns of
movement and aggregation. Following this, surveys of microhabitat and activity were
taken of the same area at daily high and low low tides for another two weeks.
Acanthanucella were highly responsive to tidal patterns with 76% feeding at high tide
and only 27% feeding at low. They also fed significantly more on sun-exposed patches of
barnacles, often horizontal surfaces, during high tide (66% feeding in sun) than during
low tide (21% feeding in sun). Ocenebra show a slight but significant tendency to feed
less in the sun at low tide (27%) than at high tide (46%). However, the frequency of
feeding in shaded areas does not vary significantly with the tide, possibly because these
whelks are unique in utilizing undercut habitat. Nucella appear to have the most
conservative behavior, feeding the least at high tide (61%) and showing non-significant
responses to sun exposure and the timing of the low tide.
Introduction
Marine organisms that inhabit intertidal ecosystems must be capable of coping
with an extreme range of environments. Most notably, they must be able to withstand
exposure during low tide and the accompanying increase in temperature and desiccation
rates (Somero, 2002). Because marine organisms are primarily adapted to an aquatic
environment, the period spent exposed during low tide often requires dramatic responses
and alterations in behavior. These pressures have produced a wide range of behavioral
strategies in intertidal organisms. While some strategies are clearly different, such as
between crabs and mussels, many more involve subtle differences in use of habitat. Even
organisms with similar physiology have developed markedly different ways of surviving
in the intertidal.
This study examines the behavioral strategies of three intertidal whelks, Nucella
emarginata, Ocenebra circumtexta, and Acanthanucella punctulata. Nucella is found in
variable wave conditions from mid to high intertidal height and feed predominantly on
Mytilus mussels and Balanus barnacles. Acanthanucella is typically found high in the
intertidal in moderate wave conditions and feed on Balanus and Chthamalus barnacles as
well as Littorina snails. Ocenebra is found commonly in heavy surf in the mid to low
intertidal and feed predominantly on Chthamalus and Tetraclita barnacles. Despite these
differences, these three species frequently occupy the same habitat. By observing these
whelks when they are found together, this study was able to distinguish unique behavioral
strategies that each species use to survive in the intertidal.
Materials and Methods
This study was carried out in the Hopkins Marine Life Refuge in Pacific Grove,
California (36°37N, 121°54'W). The principal study site was a 6 by 9 meter region of
rocky intertidal shore inhabited by Nucella emarginata, Ocenebra circumtexta,
Acanthanucella punctulata and a small number of Acanthanucella spirata. The latter
species was not included in this study due to its low abundance. The other three species
are found in patchy abundance along the shores of the Refuge, but this site was ideal
because it 1) was a place where all three species were found together in abundance, and
2) was easily accessible during high and low tides. To augment the data from this site,
two isolated granite boulders with abundant Acanthanucella, one within 10m of the
primary site and the other approximately 100 meters away, were also examined. All three
of these sites had healthy stocks of Chthamalus spp. and Balanus glandula which are the
principal prey for all three whelk species. The primary site also had a substantial
population of Tetraclita rubescens and a limited population of the mussel Mytilus
californianus.
Initially, all the individual whelks within a subsection of the primary site were
marked with enamel paint and observed at the daily low tide for 2 weeks. Twenty four
Nucella, 19 Acanthanucella, and 21 Ocenebra were individually marked. In addition, two
aggregations of 25 Acanthanucella were marked as groups, as was one Nucella
aggregation of 8. During each observational period I noted the location of each marked
whelk found within the study site.
I also performed site-wide surveys of feeding activity and microhabitat
conditions at the primary site and the two secondary sites. I conducted these surveys for
two weeks at daily low low and high low. The microhabitat data were categorized
according to the following factors: rock orientation (vertical, horizontal, overhang),
presence of protective cover (red algal growth or sea anemones versus bare rock), crevice
or open rock face, barnacle cover (none, sparse, medium, dense), and whether the
location was sun-exposed or shaded.
The results of microhabitat usage were statistically analyzed using chi-square tests
of goodness-of-fit, which compared the observed frequencies against the null hypothesis
that all species utilize each habitat category in the same proportion. A 3-factor analysis of
variance (ANÖVA) was used to compare feeding data, with species, tide height, and sun
exposure as orthogonal fixed factors. Subsequent post-hoc comparisons were conducted
using Student-Newman-Kuels tests (Underwood, 1997). The feeding frequency at high or
low tide was compared against time of day using simple linear regression.
Results
Daily Observation of Marked Individuals
Acanthanucella was the most active species. The two non-mating aggregates,
which had been relatively stable for at least 2 days before marking, quickly disbanded.
One aggregate fell to 7 Acanthanucella after one day and 1 after two, while the other
dropped to 9 then 3 in the same time. These marked individuals were observed in the area
for a few days but many were not seen again. Neither of these areas, which were
barnacle-free undercuts, was ever repopulated. An unmarked mating aggregate within the
study site remained relatively stable at approximately 20 individuals.
The individually marked Acanthanucella were similarly mobile. Äfter two weeks,
only 3 of the 19 (16%) were found on the rock were they were tagged initially. Those that
had moved often had to travel through extensive barnacle-free rubble to reach their new
location. On average, 33% of all marked individuals were found during daily observation.
Acanthanucella frequently foraged in groups, typically of 4 to 10 individuals that
emerged from shelter and traveled together into sun-exposed barnacle-covered areas.
Ocenebra, like Acanthanucella, was highly mobile with an average recovery of
only 23%. Äfter two weeks, only 2 of the original 21 (10%) were found on the same rock.
These whelks were never found in aggregations, though they often occurred in pairs in
what was possibly mating behavior. Ocenebra also traveled through rubble to reach new
rocks.
Nucella was less mobile than either Ocenebra or Acanthanucella. On average,
50% of all marked individuals were found each day and, unlike the other species, they
were likely to be found on the same rock on successive days. Ten of the 24 (42%)
remained on the same rock for the entire two weeks. Those that did travel remained on
near-continuous barnacle cover. There was some aggregation behavior in Nucella but it
was not as obvious or consistent as Acanthanucella. Several Nucella laid eggs, but these
individuals were always solitary or with no more than 4 other conspecifics. Of the 8
individuals marked as a group, 6 dispersed individually and 2 remained at the original
location. It was common for individual whelks to forage continuously for days or to
remain in a barnacle-free crevice for weeks.
The study site and the surrounding area were examined for marked snails after 1
month. Of the 24 Nucella originally marked, 11 were found within the site, 6 of which
had not moved in two weeks. Four individually marked Acanthanucella were found
within the site though all had moved to new rocks. One of the aggregations had relatively
high returns: 4 of the 25 were found in a mating aggregation and 5 were moving as part
of a foraging group. Only a single individual was found from the other aggregation. Two
of the 21 marked Ocenebra were observed after a month and only one was inside the
study site.
Feeding and Microhabitat
Relatively low proportions of Acanthanucella fed during low tide, but the percent
feeding increased dramatically at high tide (Fig.1). These proportions varied significantly
depending on the time of day when low tide or high tide occurred: there was a significant
increase in the percent feeding at high tide as the tide progressed from sunrise to noon
and a significant decrease in the percent feeding at low tide in the same progression (Fig.
2). The proportion feeding in shaded habitat remained low at high and low tides, but the
proportion feeding in sun-exposed habitat increased significantly between low and high
tide (Fig. 1, Table 1). When Acanthanucella are feeding at low tide, they were
predominantly found on vertical surfaces, with a low percentage feeding on horizontal or
undercut substrate (Fig. 3). At high tide, they fed in nearly equal proportions on vertical
and horizontal surfaces and few were found feeding on undercuts (Fig. 3). They fed in
similar proportions on low and medium density barnacle cover and slightly higher
proportions on high density barnacle cover (Fig. 4).
When not feeding, Acanthanucella were found in similar abundance on horizontal
and undercut substrate and slightly less on vertical (Fig. 5). In these three orientations
they were found in equal proportions in crevices and on rock faces (Fig. 6). However,
there was a greater percentage found in protective cover (i.e. red algal cover or at bases of
anemones) than on rock (Fig. 7).
Roughly half of observed Nucella were feeding at either low or high tide (Fig.1).
These feeding proportions did not change significantly as the high and low tides
progressed into the day (Fig. 8). Nucella did not feed in significantly different
proportions in sun-exposed or shaded habitat at either high or low tide. They fed
predominantly on vertical surfaces at both tides (Fig. 3) and were most often on medium
density barnacle cover, though this percentage was highly variable from day to day (Fig.
When not feeding, Nucella were found in roughly equal proportions on horizontal
and vertical substrate but did not make use of undercuts (Fig. 5). Nucella were much
more likely to be found in crevices than open rock faces when not feeding (Fig. 6) and
were rarely found nestled in protective cover (e.g. red algae or the bases of anemones).
Ocenebra fed in high proportions at both high and low tide (Fig. 1). The percent
feeding at high tide did not vary depending on the timing of that tide, but the percent
feeding at low tide decreased significantly as the low tide progressed into the day (Fig.
9). At high tide they fed in roughly equal proportions on sun-exposed and shaded habitat,
but at low tide percent feeding in the sun was significantly less (Table 1). Ocenebra fed
on undercut surfaces in approximately the same proportions as vertical at low tide and
slightly less at high tide (Fig.3). They made little use of horizontal substrate at either tide
(Fig.3). Ocenebra were characteristically found in higher proportions on high density
barnacle cover than low or medium density (Fig. 4).
Ocenebra were found predominantly on vertical surfaces when not feeding, but
the proportion found on each orientation was highly variable from day to day (Fig. 5).
Their use of crevices and protective cover was also highly variable and showed no clear
trends (Fig. 7, Fig. 8).
Discussion
Acanthanucella are highly mobile predators and very responsive to changes in
water level. As the tide rises, these whelks move into horizontal and sun-exposed habitat.
As the tide recedes and these areas become increasingly stressful, they move back into
protective cover (Morris et al, 1980). Acanthanucella also show dramatic variation in
feeding frequency depending on the timing of the tide. Similar behavior can also be
found in an Australian whelk, Thias orbita (Fairweather, 1988). In addition to this
pattern of local movement, Acanthanucella show high dispersal rates and may travel
across extensive rubble to reach new food sources. When foraging in this manner, they
tend to travel in groups. Acanthanucella are also commonly found in aggregations when
not foraging.
The extent to which Acanthanucella form aggregates and travel in groups may
depend on the time of year. This study was done during the peak of the Acanthanucella
mating season (May-June) and they are known to mate in tight aggregations (Morris et al,
1980). One such aggregation was observed in the primary study site. However, other
aggregations were loose and quickly dispersed. In addition, many foraging
Acanthanucella traveled in groups without apparent mating activity. This likely indicates
that coordinated behavior is characteristic of Acanthanucella and not entirely limited to
the mating season. The influence of mating season on aggregation behavior warrants
further investigation.
Nucella display more conservative behavior. When they do move, which is less
often than the other species, they rarely leave barnacle cover or face prolonged sun
exposure. In addition, they feed the least at high tide and show no significance response
to changes in the daily timing of the tides. When not feeding they typically seek
protection in crevices, which may decrease stress due to emersion. A few Nucella were
observed laying eggs, which supports the conclusion from the literature that they mate
sporadically throughout the year (Morris et al, 1980). However, because this was limited
to a few individual whelks, it is unlikely that mating had a large influence on the
observed behavior of the entire population.
The activity of Nucella varied dramatically within the population. This
observation is supported by a previous survey of 128 Nucella emarginata (West, 1986).
During a four month period of low tide observations, 19% of the marked individuals
where not observed to feed while 40% made five or more sequential feeding attacks. This
raises the question of whether individuals display uniformly different foraging behavior
or cycle between periods of high and low activity. This question could be addressed by
detailed long-term observation of individual whelks throughout the tide cycle.
Ocenebra is unique in feeding heavily in both sun-exposed and shaded habitat,
though they feed significantly less in the sun at low tide. Like Acanthanucella, the
proportion feeding at low tide varies significantly depending on the time of day.
Ocenebra do not, however, show any variation with the timing of the high tide, likely
because nearly the entire population feeds when submerged. Ocenebra is also unique in
utilizing undercut habitat for feeding as well as protection.
Previous studies of Ocenebra found interindividual variation in preferred prey
species (Dusek, 1999). If the species composition of barnacle cover is significantly
influenced by substrate orientation or sun-exposure, this variation may produce different
foraging strategies within an Ocenebra population whose individuals specialize on
different barnacle species. For example, individuals that feed preferentially on barnacles
found on sun exposed habitat may adopt a strategy similar to Acanthanucella and move
with the tide. Conversely, Ocenebra that feed on barnacles found on undercuts or
protected habitat may feed continually.
Although this study did not analyze barnacle distribution by microhabitat within
the study site, there is some evidence for such a hypothesis. Ocenebra feed
predominantly on Tetraclita and Chthamalus barnacles. (Morris et al, 1980). Of the three
barnacle species, Tetraclita occurs lowest on the shore and may therefore grow best in
undercuts and similarly protected habitat at higher levels (Morris et al, 1980). If this is
the case, then Ocenebra may be drawn towards undercuts out of food preference as well
as for protection from physical stress. In contrast, Burrow (2003) found that Chthamalus
is the dominant barnacle on sun-exposed rocks. As a result of these dispersal patterns,
Ocenebra with different food preferences may be forced to adopt different behavioral
strategies. Direct tests of the effect of individual food preferences on foraging strategies
of Ocenebra would be of interest.
A few general assumptions may require further investigation. When looking for
marked whelks, I had to assume that the enamel paint would be sufficiently permanent
for the duration of my study. I also took it for granted that applying the paint did not alter
the whelks' behavior. However, as many marked whelks were not recovered and both
Acanthanucella aggregations dispersed soon after being marked, these assumption may
be unwarranted. In addition, I assumed that the behavior of each species was not
dramatically influenced by the presence of the others. Although Acanthanucella have
been known to occasionally prey on Nucella, this was never observed in my site (Morris
et al, 1980).
Previous studies have found that behavioral patterns of individual species vary
depending on site conditions, local topography, and community structure. (Burrows and
Hughes, 1989; Dahlhoff et al, 2001; Fairweather, 1988). An obvious extension of this
comparative survey would be to examine behavior of these three whelks when they are
found together in different habitat.
In conclusion, this study has shown that Nucella emarginata, Ocenebra
circumtexta, and Acanthanucella punctulata exhibit different resource utilization
strategies when occupying the same habitat. Further information is needed from
additional sites to determine if these patterns are general or if they vary in space and time.
Regardless, my results suggest that further investigations to identify the ecological,
behavioral, and physiological selection pressures that produce divergence among such
ecologically similar, closely related sympatric species would be fruitful.
Acknowledgements
1 would like to sincerely thank Jim Watanabe who helped me extensively
throughout the entire process of this study. I would also like to thank Mark Denny for
supplying equipment to study physical processes in the intertidal.
Literature Cited
Burrow, T. 2003. Field observations of Nucella emarginata: effects of temperature on
feeding. Unpublished student paper, Hopkins Marine Station library, Stanford
University.
Burrows, M.T. and Hughes, R.N. 1989. Natural foraging of the dogwhelk, Nucella
lapillus (Linnaeus); the weather and whether to feed. Journal of Molluscan
Studies 55, 285-295.
Dahlhoff, E., Bradley, B. and, Menge, B., 2001. Physiology of the rocky intertidal
predator Nucella ostrina along an environmental stress gradient. Ecology 82(10),
2816-2829.
Dusek, E. 1999. Ocenebra circumtexta in the intertidal: stratification and prey selection
of a predatory gastropod. Unpublished student paper, Hopkins Marine Station
library, Stanford University.
Fairweather, P.G. 1988. Movement of intertidal whelks (Morula marginalba and Thais
orbita) in relation to availability of prey and shelter. Marine Biology 100, 63-68.
Morris, R.H., Abbott, D.P., and Haderlie, E.C., 1980. Intertidal invertebrates of
California. Stanford University Press, Stanford, CA. 277-283, 515-521
Somero, G. 2002. Thermal physiology and vertical zonation of intertidal animals: optima,
limits, and costs of living. Integrative and Comparative Biology 42, 780-789
Underwood, A.J. 1997. Experiments in ecology: their logical design and interpretation
using analysis of variance. Cambridge Univ. Press., New York, NY.
West, L., 1986. Interindividual variation in prey selection by the snail Nucella
emarginata. Ecology 67, 798-809.
Table 1:
Results of 3-way ANÖVA of daily percent feeding with tide height, sun exposure, and
whelk species. Tide height was high' or low', sun exposure was 'sun-exposed' or
'shaded'. Cochran's Test for homogeneity of variances was not significant (s'max - Esi
0.156); for Student-Newman-Keuls tests, means that are underlined are not significantly
different (P2.05).
Analysis of Variance
Source
Sum-of-Squares
Mean-Square
F-ratio
Species
6312.055
3156.027
17.188
5047.147
Tide
5047.147
27.487
62.995
62.995
Sun Exposure
0.343
Species x Tide
609.409
3.319
1218.818
Species x Sun
7209.064
14418.128
39.261
Tide x Sun
2873.009
2873.009
15.647
1156.295
2312.590
Species x Tide x Sun
6.297
183.619
Within
17627.392
Student-Newman-Keuls tests:
Acanthanucella:
HighSun LowSun
HighShade LowShade
Nucella:
HighShade Low Shade
HighSun LowSun
Ocenebra:
LowShade HighShade HighSun LowSun
5.001
.001
559
040
5.001
.001
003
Figure Legends
Figure 1: Percent feeding by whelk species, tide height, sun exposure. Percents are daily
average proportion of snails feeding at each tide in each sun exposure category.
Figure 2: Percent of Acanthanucella punctulata feeding versus time of day when high
tide (open circles) or low tide (closed triangles) occurred. Vertical lines
indicate time of sunrise and noon. High Tide: P «.001; r* =.92; Low Tide: P
-.001, r’=.80
Figure 3: Percent of feeding individuals of each species found on horizontal, vertical,
and undercut substrate at high and low tide. Error bars are + 1 standard
deviation. Chi-square = 142.64 (df = 4, PS.001)
Figure 4: Percent of feeding individuals of each species found on low, medium, and
high-density barnacle cover (all tide levels combined). Error bars are + 1
standard deviation. Chi-square = 27.88 (df = 4, Pk.001)
Figure 5: Percent of non-feeding individuals of each species found on horizontal, vertical
and undercut substrate at high and low tide. Error bars are + 1 standard
deviation. Chi-square = 152.20 (df = 4, PS.001)
Figure 6: Percent of non-feeding individuals of each species found in crevices vs. open
rock faces (all tide levels combined). Error bars are + 1 standard deviation.
Chi-square = 84.57 (df = 2, PS.001)
Figure 7: Percent of non-feeding individuals of each species found in protective cover
(red algal cover or at bases of anemones) vs. -bare open rock. Error bars are +
1 standard deviation. Chi-square = 105.91 (df = 2, PS.001)
Figure 8: Percent of Nucella emarginata feeding versus time of day when high tide
(open circles) or low tide (closed triangles) occurred. Vertical lines indicate
time of sunrise and noon. High Tide: P =.76, r’ =.02, Low Tide: P =.86, r
.004
Figure 9: Percent of Ocenebra circumtexta feeding versus time of day when high tide
(open circles) or low tide (closed triangles) occurred. Vertical lines indicate
time of sunrise and noon. High Tide: P = .35, r’ =.14, Low Tide: P =.03,r
48
Figure 1:
100
D Sun
□ Shade
80
60-
40
+ 20

0 +
Low High
Acanthanucella


Low High
Nucella

Low High
Ocenebra
O
Figure 2:
100-
80
High Tide
4 Low Tide
60
2
40
A
20
X

O
0 2 4 6 8 10 12 14 16 18 20 22 24
Time of Da
Figure 3:
100-
80-
60 -
40-
20
0 +
Orientation - Feeding
□ Horizontal
Undercut
Vertical
H
I I
Low
High
Low High
Nucella
Ocenebra

Low High
Acanthanucella
100
80
60
40-
20-
Figure 4:
Low
□ Medium
High
Acanthanucella
Barnacle Density
Nucella
Ocenebra
Figure 5:
100-
□ Horizontal
Undercut
80
Vertical
60
40
20-
0 +
Low High
Acanthanucella
Orientation - Not Feeding


Low High
Low High
Nucella
Ocenebra
100-
80-
60-
40
20-
0-
Figure 6:
Crevice usage when not feeding
D On Face
□ In Crevice

Acanthanucella
Nucella
Ocenebra
Figure 7:
Cover
g 100
Face
80-
60-
40-
2 20
Low High
Acanthanucella
Use of protective cover

Low High
Low High
Nucella
Ocenebra
LL
O
Figure 8:
0 High Tide
100
4 Low Tide
80

60

4
—-+4——

40
20
—

O-
O 2 4 6 8 10 12 14 16 18 20 22 24
Time of Day
S.
O
Figure 9:
100
80
60
40
20
O
a

High Tide
4 Low Tide


aa
0 2 4 6 8 10 12 14 16 18 20 22 24
Time of Day