Zonation of Tegula
Shi Jane Liaw
ABSTRACT
Two intertidal species of Tegula, T. brunnea and T. funebralis, display distinct
vertical zonation. T. brunnea inhabit the lower intertidal to shallow subtidal zone,
while T. funebralis are found in the upper-mid intertidal zone. Reciprocal
transplants of each species to the habitat of the other revealed that T. brunnea
returns to its typical height on the shore significantly more quickly than does T.
funebralis. Transplanted T. brunnea and transplanted T. funebralis move
significantly further and in a more consistent direction than do control animals
placed back in their respective natural habitats. Although no statistical differences
were observed between transplants done in high and low tides, a consistent trend of
less movement by T. brunnea during low tides was observed. Microhabitat
utilization during simulated low and high tides in the laboratory showed that T.
brunnea remains submerged and on horizontal surfaces significantly more than T.
funebralis, which tend to occupy vertical surfaces both above and below the
waterline. Night and daytime behavior are similar for T. funebralis and differ for T.
brunnea in the laboratory.
Zonation of Tegula
Shi Jane Liaw
INTRODUCTION
In order to understand the dynamics of a biological community, one must
first understand the behaviors of its component organisms, including the reasons
for their habitat choices. The rocky intertidal is an ideal community to study
because of the ease of access to intertidal areas, the gradient of abiotic stresses to
organisms caused by fluctuations in tidal height, and the abundance of many species
(Connell, 1974). Two such species are Tegula funebralis and Tegula brunnea.
Tegula funebralis is a gastropod abundant in the upper- to mid-intertidal
zone between one and five feet above Mean Lower Low Water
(Wara and Wright 1963, Abbott and Haderlie 1980) with a population center at about
+3 feet. Tegula brunnea is found in the low intertidal to shallow subtidal zone,
between 0 and 18 feet below MLLW (Abbott and Haderlie 1980, Watanabe 1984).
These two common turban snails share many characteristics, including shell shape,
size, diet and behavior. However, despite similar physiological characteristics, they
are clearly vertically zoned.
Because they are vertically zoned, abundant and move at a rate that is
relatively easy to track, T. funebralis and T. brunnea are useful organisms in which
to study habitat selection. While there has been substantial research on the
zonation and migration behavior of T. funebralis (Wara and Wright 1963, Frank
1975, Markowitz 1980, Byers and Mitton 1981, Byers 1983, Fawcett 1984), little
research has been done on T. brunnea zonation and migration. Thus, special
interest in T. brunnea behavior motivated this study. In this study, a reciprocal
transplant experiment and a laboratory experiment were conducted to examine the
reasons for the ecological separation of the two species.
Zonation of Tegula
Shi Jane Liaw
MATERIALS AND METHODS
Vertical Zonation
Two transects were sampled perpendicular to the shoreline at Hopkins
Marine Station, Pacific Grove, CA, and one transect was sampled at Point Pinos,
Pacific Grove, CA. Each transect was divided into four zones and all Tegula species
in five 0.25m2 quadrats were counted within each zone. The positions of the
quadrats along each transect were located using a list of random numbers. Heights
at Point Pinos were measured relative to water level at the predicted time of low
tide using a surveyor’s transit and stadia rod. Heights at Hopkins Marine Station
were determined from a detailed topographic map of the intertidal zone.
Laboratory Experiment
Fifty snails of each species were placed in a 3 x 3m outdoor tank with running
seawater. High and low tides were simulated during both day and night. To
simulate high tides, a stand-pipe was placed in the drain which maintained a water
depth of 10.1 inches in the tank. Observations were made every half-hour for at
least an hour; during high tides the number of each species above the waterline,
below the waterline and on the bottom of the tank were recorded. During low tides,
the stand-pipe was removed and the water allowed to drain out of the tank. Counts
were taken of snails on the walls and on the bottom surface of the tank every half-
hour for at least an hour.
Both day and nighttime sets of high and low tide experiments were replicated
three times, with three different groups of snails. Analysis of Variance and Tukey
Zonation of Tegula
Shi Jane Liaw
HSD tests were used to analyze differences in microhabitat utilization by T.
funebralis and T. brunnea during high tides and low tides.
Reciprocal Transplant Experiment, T. brunnea
T. brunnea were transferred to the typical shore height of T. funebralis, up to
heights between 2 and 4 feet above MLLW. Each set of high and low tide T. brunnea
transplants were done at two locations, three times at one location and one time at
the other. One of these sets of transplants was done during nighttime high and low
tides. One hundred snails were scrubbed to remove algae from their shells and were
then painted with flourescent enamel paints. During low tide transplants, snails
were placed on air-exposed surfaces about 0.5 m away from the water edge. During
high tide transplants, snails were placed under water at a depth of 0.3m to 0.5m.
Transplants were checked 1.5 hours, 3 hours and approximately 24 hours after
initiation of the experiment. Positions of snails found were recorded to the nearest
meter from the release site; negative values were given to snails moving upshore
and positive values were given to snails moving downshore. The average
displacement of all snails found at each time point was calculated.
Two controls were performed at high tide in which 100 T. brunnea were
painted in a similar fashion to transplanted snails but were placed back to their
typical height on the shore at about 4 feet below Mean Lower Low Water level.
Measurements were taken after 24 hours, and average displacement was calculated
as with transplanted T. brunnea.
Two-tailed t-tests assuming unequal variances, with adjusted a-level 0.013,
were performed between 24-hour displacement values of transplanted and control
T. brunnea, between transplanted T. brunnea at high and low tides after 1.5 hours,
Zonation of Tegula
Shi Jane Liaw
between transplanted T. brunnea at high and low tides after 3 hours and between
transplanted T. funebralis and T. brunnea at high and low tides after 24 hours. This
adjusted a-value was used because of lack of independence of the individual tests
and was obtained using the Dunn-Sidak equation (Sokal and Rohlf 1995). A
comparison between displacement values of transplanted T. brunnea at high and
low tides after 24 hours was not made because after 24 hours, the snails had already
experienced at least one high tide. A two-factor ANOVA test could not be used in
place of the t-tests because data sets were incomplete; control T. brunnea were not
counted at 1.5 hours and 3 hours.
Reciprocal Transplant Experiment, T. funebralis
T. funebralis were transplanted down to between 3 to 4 feet below MLLW, the
highest point at which T. brunnea could be found in abundance. Two transplants
were done at high tide, two transplants at low tide. Two sets of controls in which T.
funebralis were placed back to their natural habitat at upper-mid intertidal were
performed at high and low tides. Measurements of average displacement were
calculated as for T. brunnea.
A two-factor ANÖVA was performed with transplant-control as one factor
and high tide-low tide as the second factor, in order to determine significance of
differences within each factor and between each factor, and to determine significance
of interactions between the two factors.
Two-sample t-tests assuming unequal variances were also performed between
T. funebralis and T. brunnea at high and low tides to determine significance of
differences between displacements at these two tide heights. An ANÖVA test could
Zonation of Tegula
Shi Jane Liaw
not be used in place of these t-tests because data sets were incomplete; T. brunnea
controls were not performed at low tides.
RESULTS
Vertical Zonation
Abundance of T. funebralis was greatest between 2 and 4 feet above MLLW
and decreased with decreasing height on the shore. No T. brunnea were found at
heights above MLLW (Fig. 1). The zone of maximum T. brunnea abundance was
between 2 and 4 feet below MLLW. Densities of both species in the zones of overlap,
at 0 to 4 feet below MLLW, were low (less than 25 T. funebralis, less than 10 T.
brunnea per 0.25 m2 quadrat) compared to maximum T. funebralis densities (almost
75 T. funebralis per 0.25 m2 quadrat).
Laboratory Experiment
In all three replicates of experiments, T. brunnea tended to stay on the
horizontal bottom of the tank significantly more than did T. funebralis (Tables 1 and
2). No T. brunnea were ever found above the waterline during high tides, while T.
funebralis were regularly found above the waterline.
When low tides were simulated by removal of the standing-pipe, T. brunnea
visibly followed the receding waterline; often, in less than 10 minutes, all T.
brunnea had moved down to the bottom of the tank. During nighttime low tides,
more T. brunnea were found on the walls, with an average of 3% on the walls. For
Zonation of Tegula
Shi Jane Liaw
daytime low tides, the average percentage of T. brunnea on the walls was less than
1%.
T.brunnea were much more likely to climb and stay on the walls during high
tides than during low tides. Twenty percent of T. brunnea were found on the walls
during daytime high tides, below the waterline, while less than 1% were found on
the walls during daytime low tides.
T. funebralis did not avoid air exposure as much as T. brunnea, and did not
follow the waterline as it receded during low tides. Numbers of T. funebralis on the
wall were fairly consistent throughout day and nighttime, high- and low-tide
transplants. T. funebralis on walls and on the bottom surface did not exhibit any
movement when water was drained for low tides.
Reciprocal Transplant Experiment, T. brunnea
T. brunnea transplanted to heights between 2 and 4 feet above MLLW
migrated significantly (t = 9.55, p««0.01) more after 24 hours than control T. brunnea
placed at their typical shore height (Fig. 2). Transplants done during high and low
tides (Fig. 3) did not display significant differences (t = 3.15, p » 0.05) in migration
rate after 3 hours. Transplants done during high and low tides after 1.5 hours also
did not display significant differences and trends were similar to that of transplants
after 3 hours and thus, results were not graphed.
Reciprocal Transplant Experiment, T. funebralis
T. funebralis transplanted to heights between 3 and 4 feet below MLLW
migrated significantly more (ANOVA, p « 0.05) than control T. funebralis placed at
their typical shore height (Fig. 4). Transplants done during high and low tides
Zonation of Tegula
Shi Jane Liaw
(Table 3) did not display any significant differences (ANOVA, p » 0.05) in migration
rate.
Comparison of T. funebralis and T. brunnea movements
T. brunnea and T. funebralis migrated to their typical heights on the shore at
significantly different rates both at high tides (t =-10.78, p ««0.001) and at low tides (t
= -8.76, p «20.001). T. brunnea moved much faster downshore after both high tide
and low tide transplants (Fig. 5).
DISCUSSION
From this study, it appears that Tegula funebralis tolerate exposure to air
more than Tegula brunnea. T. brunnea generally avoids movement when exposed,
while T. funebralis exhibits a climbing behavior and prefers vertical faces to
horizontal surfaces, even when exposed.
Although differences in displacement of transplanted T. brunnea at high and
low tides were not significant,T. brunnea moved much faster downshore when they
were transplanted under water during high tides than when they were transplanted
at low tides and exposed to air. In three of the low-tide transplants, no snails moved
for the first three hours, and in the fourth and last transplant, only three snails
moved less than 1 meter away from the release site.
Transplanted T. brunnea moved not only further than controls, but also in a
more consistent direction. The majority of transplanted T. brunnea moved
downshore, whereas movement of control animals placed back into their natural
low shore habitat was more scattered in both directions.
Zonation of Tegula
Shi Jane Liaw
Transplanted T. funebralis could not be counted consistently at 1.5 hours and
3 hours because of rough water conditions and so a comparison of high and low tide
displacements at 3 hours could not be made. However, field observations indicate
that T. funebralis are more mobile than T. brunnea when exposed to air and tend to
move until they find a suitable area to cluster with other T. funebralis.
In the laboratory experiment, when water was drained out for the low tide,
T. brunnea followed the waterline to the bottom of the tank within an average of
approximately five minutes. In contrast, T. funebralis did not move from their
positions in clusters above the waterline. While T. brunnea preferred the bottom of
the tank during both day and night low tides, at least two and up to six T. brunnea
stayed on the walls during low tide at night. In contrast, only one T. brunnea was
ever on the wall at once during daytime. In contrast, there were no significant
changes in behavior of T. funebralis during different times and tides.
The migration behavior of the two species indicates that the upper limit of
the T. brunnea zone may be caused by an inability to tolerate heat and desiccation,
while the lower limit of the T. funebralis zone may be caused by an innate climbing
behavior. T. brunnea were never found above the waterline in the laboratory
experiment, they followed the waterline down at low tide and at lower temperatures
during the night, they were slightly more likely to stay on the walls during low tide.
In addition, T. brunnea did not move during low-tide transplants and instead
retracted into their shells until the water level rose to cover them.
A previous study also reveals that a combination of heat stress and water loss
probably determines how long T. brunnea can survive out of water (Rocca 1995).
Rocca (1995) found that when subjected to similar heat and desiccation treatments,
T. funebralis had a much higher survival rate than T. brunnea. It has been further
10
Zonation of Tegula
Shi Jane Liaw
demonstrated that, in comparison with organisms living lower, higher intertidal
animals tend to have higher desiccation tolerances and lower desiccation rates
(Wolcott 1973).
Climbing behavior of T. funebralis could be responsible for the lower limit of
their distributions. Both T. funebralis in the field and in the laboratory exhibited
this behavior. The reason for this is unknown, but it is possible that it was once an
attempt to avoid predators (Paine 1969) that has since evolved into behavior. T.
funebralis may have evolved this behavior while T. brunnea did not because a
major predator of the two species, Cancer antenarius, finds it easier to crack the
shells of T. funebralis than T. brunnea (Abbott and Haderlie 1980). Thus, T.
funebralis have a disadvantage in encounters with the predator Cancer.
While Rocca (1995) showed that physiological tolerance rather than behavior
allows T. funebralis to live in the high intertidal, this study indicates that both
factors play a part in their habitat selection. T. funebralis are better able to tolerate
heat and desiccation stress than T. brunnea and they have also developed a climbing
behavior that may allow them to escape predators which do not feed above the
waterline, such as Cancer antenarius and Pisaster ochraceus. Research has been
done that demonstrates T. funebralis exhibit climbing behavior in the presence of
predators (Fawcett 1984, Markowitz 1980, Paine 1969). In the laboratory component
of this study, T. funebralis climbing behavior is shown to occur even when no
predators are present.
Öther factors may also be responsible for T. funebralis and T. brunnea
zonation, including larval dispersal. Larval recruitment is an important cause of
the spatial segregation of the three subtidal Tegula species (Watanabe 1984) and it is
known that T. funebralis larvae settle high in the intertidal zone (Paine 1969) and T.
11
Zonation of Tegula
Shi Jane Liaw
brunnea larvae settle in the low intertidal to shallow subtidal zone (Watanabe 1984).
Larval recruitment may therefore play a part in the segregation of these two species
as well. However, this theory cannot fully explain why the snails would migrate
towards their typical shore habitat after being transplanted.
Microhabitat preferences may also be partially responsible for the zonation of
T. funebralis and T. brunnea. Byers and Mitton (1981) found that after translocation
T. funebralis return to their natural habitats through a recognition of ecological
characteristics of the habitats. T. brunnea are found most often in areas of dense
algal cover (Watanabe 1984) while T. funebralis avoids dense algal cover (Wara and
Wright 1963). It is thus possible that in the reciprocal transplants of this study, T.
funebralis and T. brunnea were migrating to areas of preferred microhabitat. Even
so, other factors must be considered in combination, for microhabitat preference
alone cannot explain how snails are able to discern their location when
transplanted, and move in the correct direction towards their natural habitats.
Interspecific competition does not appear to influence zonation patterns
between T. funebralis and T. brunnea, since intraspecific densities of T. funebralis
are much greater (about 75 T. funebralis per 0.25m2 quadrat) than interspecific
densities where the two species overlap (less than 25 snails per 0.25m2 quadrat).
Furthermore, Watanabe (1984) has shown that interspecific competition is not
higher than intraspecific competition between T. brunnea and the two other
subtidal Tegula species, T. montereyi and T. pulligo. This may also the case between
T. brunnea and T. funebralis.
While Wara and Wright (1963) demonstrated that T. funebralis movement
was light-dependent, with snails moving up to rock tops during night high tides
and not day high tides, this study found no significant differences between the
12
Zonation of Tegula
Shi Jane Liaw
number of snails at higher latitude in the tank during day and night. However,
further investigation would be of value.
The differences in displacements of transplanted T. funebralis and T.
brunnea, with T. brunnea moving significantly longer distances than T. funebralis,
show that the factors limiting T. brunnea are probably more direct than those
limiting T. funebralis. This is in keeping with previous studies (Dayton 1971, Paine
1974) that show that upper limits of intertidal organism range tend to be caused by
abiotic factors, while lower limits tend to be caused by biotic interactions. It is also in
keeping with the theory that heat and desiccation may be the cause of T. brunnea
zonation and an evolved climbing behavior may be the cause of T. funebralis
zonation.
ACKNOWLEDGEMENTS
I would like to thank my advisor, Jim Watanabe, for his guidance, dedication
and boundless knowledge of snails and other intertidal creatures. I would also like
to thank my "snorkel buddies", especially Josh Rapport, without whom I could
never have found and counted that many tiny fluorescent snails.
Zonation of Tegula
Shi Jane Liaw
LITERATURE CITED
Abbott, D. P. and E. C. Haderlie. 1980. Prosobranchia: Marine snails.
Pages 252-254. R. H. Morris, D. D. Abbott and E. C. Haderlie, ed.
Intertidal Invertebrates of California. Stanford University Press,
Stanford, CA.
Byers, B. A. 1982. Enzyme polymorphism associated with habitat choice in
the intertidal snail Tegula funebralis. Behavior Genetics 13: 65-75.
Byers and Mitton, 1981. Habitat choice in the intertidal snail Tegula
funebralis. Marine Biology 65: 149-154.
Connell, J. H. Effects of competition, predation by Thais labillus. Ecological
Monographs 31 (1): 83-104.
Dayton, P. K. 1971. Competition, disturbance, and community organization:
the provision and subsequent utilization of space in a rocky intertidal
community. Ecological Monographs 41: 351-389.
Fawcett, M. H. 1984. Local and latitudinal variation in predation on an
herbivorous Marine Snail. Ecology 65 (4): 1214-1230.
Frank, P. W. 1975. Latitudinal Variation in the life history features of the
black turban snail Tegula funebralis (Prosobranchia: Trochidae).
Marine Biology 31: 181-192.
Markowitz, D. V. 1980. Predator influence on shore-level size gradients in
Tegula funebralis. Journal of Experimental Marine Biology and
Ecology 45: 1-13.
Paine, R. T. 1969. The Pisaster-Tegula interaction: prey patches, predator
food preference, and intertidal community structure. Ecology 50 (6):
950-961.
Paine, R. T. 1974. Intertidal community structure: experimental studies
on the relationship between a dominant competitor and its principal
predator. Oecologica 15: 93-120.
14
Zonation of Tegula
Shi Jane Liaw
Underwood, A. J. 1979. The ecology of intertidal gastropods. Advanced
Marine Biology 16: 111-210.
Wara, W. M. and B. B. Wright. 1963. The distribution and movement
of Tegula funebralis in the intertidal region of Monterey Bay,
California. Veliger 6 supplement: 30-37.
Watanabe, J. M. 1984. The influence of recruitment, competition, and
benthic predation on spatial distributions of three species of kelp
forest gastropods (Trochidae: Tegula). Ecology 65 (3): 920-936.
Wolcott, T. G. 1973. Physiological ecology and intertidal zonation in
limpets (Acmaea): a critical look at "limiting factors. Biological
Bulletin 145: 389-422.
Zonation of Tegula
Shi Jane Liaw
FIGURE LEGENDS
Vertical Distribution of Tegula funebralis and T. brunnea at Hopkins
Figure 1.
Marine Station and Point Pinos. Error bars show 95% confidence
intervals.
Figure 2.
Average Displacements of Transplanted and Control T. brunnea put
out during high tide, at 24 hours (t = 9.55, p «« 0.001). Error bars show
95% confidence intervals.
Figure 3.
Average Displacements of Transplanted T. brunnea at high and low
tides after 3 hours (t = 3.15, p» 0.05). Error bars show 95% confidence
intervals.
Figure 4.
Average Displacements of Transplanted and Control T. funebralis
(ANÖVA, p « 0.05) after 24 hours. Error bars show 95% confidence
intervals.
Average Displacements of T. funebralis and T. brunnea at high tide (t =
Figure 5.
-10.78,p «« 0.001) and low tide (t =-8.76, p «« 0.001) after 24 hours.
Error bars show 95% confidence intervals.
Zonation of Tegula
Shi Jane Liaw
Figure 1.


204

.
to2.

E T. funebralis
E T. brunnea
210 0
410 2

2
50 75
25
100
Average number of snails per 0.25m22 quadrat
Zonation of Tegula
Shi Jane Liaw
transplant

control
Figure 2.
S T. brunnea
Zonation of Tegula
Figure 3.
1.5
0.5

O-
High
Low
tide height when snails released
Shi Jane Liaw
ET. brunnea
Zonation of Tegula
Figure 4.
0.5

.
.
-0.5-
high
low
tide height when snails released
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E transplants
controls
Zonation of Tegula
Figure 5.


.
high
low
tide height when snails released
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E T. funebralis
ET. brunnea
5
+


1+
20
u

55
+
4.
Shi Jane Liaw
Zonation of Tegula
P-value
F-Ratio
degrees of
Mean-
Sum of
Source of
freedom
Square
Squares
Variation
24.49
5.72
5.72
Species
41.69
9.73
Location
9.73
148.13
34.56
34.56
Interaction
0.23
20
467
Error
TWO-FACTOR ANOVA WITH SPECIES (T. FUNEBRALIS-T.
TABLE 2a.
AS ONE FACTOR AND LOCATION (ON WALL-ON BOTTOM) AS
BRUNNEA
OTHER FACTOR, FOR SIMULATED LOW TIDE IN TANK EXPERIMENT.
1.000
1.000
1.000
1.000
0.714
0.003
4
TABLE 2b. TUKEY HSD MULTIPLE COMPARISONS. MATRIX OF PAIRWISE
COMPARISON PROBABILITIES.
1—T. brunnea on bottom of tank.
2—-T. brunnea on wall of tank.
3—-T. funebralis on bottom of tank.
4—T. funebralis on wall of tank.
Shi Jane Liaw
Zonation of Tegula
P-Value
Mean-
F-Ratio
degrees of
Sum of
Source of
Squares
freedom
Square
Variation
25.38
Species
6.81
6.81
57.03
30.59
15.30
Location
15.04
56.06
Interaction
30.07
0.268
Error
8.05
30
—
TABLE 2c. TWO-FACTOR ANOVA WITH SPECIES (T. FUNEBRALIS-T.
BRUNNEA) AS ONE FACTOR AND LOCATION (ABOVE THE WATERLINE¬
BELOW THE WATERLINE-ON BOTTOM) AS OTHER FACTOR, FOR SIMULATED
HIGH TIDE IN TANK EXPERIMENT.
1.000
1.000
0.007
1.000
1.000
1.000
0.017
0.658
1.000
0.458
0.371
0.997
0.369
1.000
0.005

TABLE 2d. TUKEY HSD MULTIPLE COMPARISONS. MATRIX OF PAIRWISE
COMPARISON PROBABILITIES.
1—T. brunnea above waterline.
2—T. brunnea below waterline.
3—T. brunnea on bottom of tank.
4—T. funebralis above waterline.
5—T. funebralis below waterline.
6—T. funebralis on bottom of tank.
Zonation of Tegula
Shi Jane Liaw
F-critical
F-value
P-value
Mean-
Source of
degrees of
SS
value
Variation
Square
freedom
0.199
2.36
7.71
0.198
High tide¬
0.198
Low tide
119
7.71
1.006
0.026
1.006
Transplant
-Control
0.838
7.71
0.004
0.004
004
Interaction
Within
0.083
0.336
Total
1545
TABLE 3. TWO-FACTOR ANOVA WITH HIGH TIDE-LOW TIDE AS ONE
FACTOR AND TRANSPLANT-CONTROL AS THE OTHER FACTOR, FOR
TEGULA FUNEBRALIS AT 24 HOURS.