Abstract
An ecological survey noted nine species of limpets on Tegula funebralis.
The only adult limpet found on this host was Lottia asmi which is the most
abundant of any epizoic gastropod in three different habitats at Pacific Grove,
California. Other juvenile, commensal limpets may temporarily use the
microhabitat of T.funebralis as protection against desiccation until their shell
size is big enough to withstand the stress on rock surfaces. T.funebralis also
offers small limpets some protection against heavy wave action. L.asmi was
observed to be significantly larger in the wave exposed habitat. Possibly fewer
predators of L.asmi allow for a greater survivability in this area or the increased
amount of food on T.funebralis' shell permits faster growth. L.asmi did occur
on Pagurus, although not as frequently as on Tegula. The lack of correlation
found in this study between commensal and host size suggests that transfers
occur before food limitation. Laboratory observations of the movement of
L.asmi revealed that the mean number of days this limpet remains on a snail
or hermit crab is less than one. Transfers between substrates by L.asmi occured
most often during high tide and the number of transfers during the day was
higher than at night.
Introduction
Many studies have addressed the commensal relationship between L. asmi and T.
funebralis (ohnson et al, 1927; Test, F., 1945; Test, A., 1946; Radford, 1959; Eikenberry
& Wickizer, 1964; Alleman, 1968). L.asmi is a small, tall limpet with a dark
brown/black shell. A fairly large specimen would measure about 11 mm. long, 8
mm. high. This limpet forages on algal epiphytes that grow on T.funebralis shells
(McLean, 1966; Ricketts, Calvin, & Hedgpeth, 1985). T.funebralis is an abundant
intertidal snail in central California, found from the mean lower low water (MLLW)
to 1.5 m. above MLLW (Hines et al, 1981). L.asmi is the only true limpet to grow
from juvenile to adult size on T.funebralis, but it is not the only epizoic limpet on
this host. Juvenile limpets found on T.funebralis in California are: Lottia digitalis,
Lottia limatula, Lottia pelta, Lottia strigatella, MacClintockia scabra, and Tectura
scutum (Brewer, 1975; Ricketts, Calvin, & Hedgpeth, 1985). T.funebralis is also often
found with Crepidula adunca, the hooked slipper snail, aboard its shell (Ricketts,
Calvin, & Hedgpeth, 1985). Test (1945) reported that L.asmi was most frequently
found on the body whorl of T.funebralis and rarely seen on hermit crab shells.
McLean (1966) reported that juvenile L.strigatella occured as frequently on
T.funebralis as L.asmi in the same habitat at Pacific Grove, California.
My field study examines the abundance of limpet species and Cadunça on
T.funebralis in three different habitats at Hopkins Marine Station, Pacific Grove,
California. The sizes of L.asmi and its gastropod hosts were recorded. The position
of L.asmi on T.funebralis was noted and the frequency of L.asmi on hermit crabs in
T.funebralis shells was also studied.
L.asmi is known to transfer from host to host, yet the timing and frequency of this
movement is disputed in the literature (Test, F., 1945; Radford, 1959; Eikenberry &
Wickizer, 1964; Lindberg, 1990). There are no studies relating the tidal cycle to L.asmi
movement. Studies of other species of intertidal limpets have shown them to be
mostly active under the turbulence of tidal wash (Rogers, 1968; Wells, 1980).
A fixed period diurnal tide was simulated in aquaria to examine the effect of tidal
exposure on L.asmi movement. The size of T.funebralis and the total number of
days it carried limpets was investigated for any correlation. The transfer rate was
studied in a mixed population of snails and hermit crabs. The number of transfers
made during the day was compared to the number of transfers made at night.
Materials and Methods
Field Studies: Epizoic limpets on Tegula funebralis were studied at Hopkins Marine
Station, Pacific Grove, California. The study lasted from April 22 through May 25,
1991. Three different habitats around the station were chosen as study sites (Figure
1). Area 1 is a protected, low relief, rocky intertidal habitat in front of Bird Rocks,
area 2 is a sandy beach habitat with emergent rocks between Monterey Boat Works
and Fisher Laboratory, and area 3 is a steep, rocky, wave exposed habitat in front of
the Miller Library.
T.funebralis were collected from each study site on about four to five different
days during low tide. These snails were then brought into the lab and counted. The
T.funebralis with limpets and/or Crepidula adunca on their shells were separated
out from those without commensals. The epizoic limpets were then identified to
species. The position of L.asmi on T.funebralis was noted. The length, width, and
height of each L.asmi was measured along with the width and height of their
gastropod hosts. All measurements were made using a caliper with 0.Imm accuracy
A two-tailed t-test was performed on the mean measurements of L.asmi in the three
different habitats. Both the limpets and snails were returned to their natural
habitats once counting, identification, and analysis were complete.
Identification of juvenile limpet species was done after extensive observations
through a dissecting scope and with the aid of several books (Carlton & Roth, 1974;
McLean, 1978; Lindberg, 1986). Various sized limpets were found and collected out
in the field and from these, growth series were created. The juvenile limpets were
then related to their adult species by following through size series.
One collection of T.funebralis and Pagurus living in Tfunebralis shells was done
from fide pools in area 1. All commensal gastropods were counted and the epizoic
limpets were identified to species.
The surface area of the T.funebralis shells was calculated by using the equation
described by Lindberg (1990) with a slight modification. The surface area of the shell
base was included in the calculations of this study because this region was found to
be the area of the shell that was most frequently used by the L.asmi. The lateral
surface area of T.funebralis shells was estimated by a cone:
lateral surface area = ars
where r = the radius of the shell base and s = the slant height of the shell. Values
was found by solving the following equation for the hypotenuse of a right triangle
52-12452
where b = shell height. The surface area of the base was estimated by a circle, so the
total surface area of T.funebralis shells was estimated by the following equation:
total surface area = mr+ + ars.
Laboratory Studies: Thirty T.funebralis, twenty L.asmi, ten Pagurus in T.funebralis
shells and two algae covered rocks were collected at Hopkins Marine Station, Pacific
Grove, California on April 29, 1991. Each of the organisms was carefully marked
with a numbered square of waterproof paper (about 2 mm x 2 mm) glued to the apex
of their shells. The snail and limpet shells were measured as in the field study.
These limpets were then randomly placed on T.funebralis shells. Fifteen
T.funebralis, ten L.asmi, five Pagurus, and one rock were each placed in two indoor
aquaria. These aquaria were set up to have running, filtered, and aerated seawater
pass through them at all times. Tank#l was set up to have a low tide situation
during the day (LTD) and a high tide situation during the night and tankt2 had the
opposite cycle (HTD). Standpipes of different heights were manually replaced to
manipulate water level and low tide had 10 mm depth of water. The room was set
on a fourteen hour light, ten hour dark cycle; where the lights go out at 10 PM. The
snails were periodically fed the soft, fleshy algae (i.e. Mastocarpus and Macrocystis)
that they prefer eating (Ricketts, Calvin, & Hedgpeth, 1985). While krill was fed to
the hermit crabs from time to time.
Position of the limpets was noted three times daily after a few days of checking
their position about every two hours to figure out when the best times were to
record it. The limpets were looked at once in the mid morning, once in the late
afternoon, and once after 10 PM with a red light. Limpet position in tankstl and #2
was followed for a period of 30 days (from May 2 to May 31, 1991). The water level
was changed once after the morning recordings of position and then again after the
afternoon recordings of postion. Halfway through the experiment (on May 17, 1991),
the tidal level was changed after the evening recordings of position instead of the
afternoon recordings. This was maintained until the end of the experiment in order
to allow about twelve hours of each tidal situation to occur in each tank. A replicate
of each tank, tankst3 (HTD) and #4 (LTD), was set up eight days later. A few of the
limpets, crabs, and snails were found dead or eaten over the course of the
experiment. Each of these were immediately replaced with a similar sized organism.
The raw data collected was analyzed first by creating two matrices for each tank,
following the analysis techniques used by Lindberg (1990). The first set of matrices
(Figures 2-5) show the number of times a marked limpet was found on each type of
substrate (i.e. snail, crab, rock, and/or glass). The second group of matrices (Figures
6-9) reports the total number of days a numbered limpet spent on each different
substrate. These matrices were then used to further quantify and graph the data. To
calculate the mean number of days a particular limpet and substrate were associated.
each cell from the first set of matrices was divided by its corresponding cell in the
second set of matrices. The difference between certain moves were tested for
statistical significance using a two-tailed t-test.
The surface area of the T.funebralis shells was computed using the same formula
as in the field studies:
total surface area = m + rs.
Results
Field Studies: The percent T.funebralis with limpets and/or Cadunca appears to
vary from habitat to habitat in this study (Figure 10). At first glance, it looks like the
frequency of limpets and/or C.adunca is highest in the sandy beach habitat (area 2),
yet when these bars are broken down into the percent T.funebralis with just
Cadunca and the percent T.funebralis with just limpets, it is clear that the sandy
beach habitat has a higher percentage of T.funebralis with C.adunca. When the
percentage T.funebralis with limpets in various habitats is compared, it looks quite
similar in all three, although there does seem to be a slightly smaller percentage of
T.funebralis with limpets in area 1.
A closer look at the various species of limpets found on T.funebralis reveals some
more patterns (Figure 11). Nine different species of epizoic limpets were found to
reside on T.funebralis in the three habitats studied. The various limpets found
were: L.asmi, L.digitalis, L.gigantea, L.limatula, L.pelta, L.strigatella, L.triangularis
MacClintockia scabra, and Tectura scutum. L.asmi was found to be the most
abundant limpet on T.funebralis in all three habitats. The abundance of L.asmi is
highest in area 1 and this is the only time area 1 has the highest abundance of a
particular commensal gastropod. Area 2 has the highest abundance of C.adunca and
L.strigatella. Area 3 has the biggest diversity of limpets and the highest abundance of
the seven other species of limpets. L.pelta was only found in areas 2 and 3.
T.scutum and L.triangularis were only found in area 3. L.asmi was the only limpet
of adult size seen on T.funebralis. All the other species of limpets on T.funebralis
were juveniles. The smallest limpets of these species were seen on T.funebralis
shells, while the larger adults were often found on the rock substrate around the
T.funebralis.
The mean Lasmi measurements showed that the length of L.asmi in area 2 was
about 30% smaller than the length of those in areas 1 and 3 (P«0.001; Figure 12). The
length of L.asmi in area 3 was even a little longer than those in area 1 (P«0.05). The
height of L.asmi was about 40% smaller in area 2 than those in areas 1 and 3
(P20.001). The mean height of L.asmi in area 3 is slightly larger than those in area 1
(P«O.1).
L.asmi occurs most frequently on the base of T.funebralis in all three habitats
(Figure 13). The next most frequent position this limpet occupies on the snail shell
is the body whorl. L.asmi can be found further up the Tfunebralis shell (closer to
the apex), but these positions on the host's shell are rather infrequent when
compared to the number of times the limpet is found on the base and the body
whorl. The base of the snail tends to be the most common position of L.asmi on
T.funebralis, especially in area 3. The percent L.asmi on the body whorl of
Tfunebralis is greatest for area 2. Casual field observations have resulted in seeing
L.asmi anywhere from on the apex of T.funebralis to on its operculum. A L.asmi
has even been found on top of another L.asmi which was attached to a T.funebralis.
A linear regression of the length of L.asmi shell against the surface area of its
host's shell (n = 45) showed no correlation between these two variables (r2 = 0.047
Figure 14).
After collecting snails (n =213) and hermit crabs (n = 252) from the tide pools in
the rocky intertidal area, it was found that 11.3% of the T.funebralis had limpets
and/ or C.adunca on their shells, while 7.1% of the Pagurus had limpets and/or
Cadunca on their T.funebralis shells. 7.5% of the snails had L.asmi aboard and 2.0%
of the hermit crabs had L.asmi aboard. Of the total T.funebralis collected in area 1
(rocky intertidal habitat), 6.2% had a L.asmi on their shells. Three other species of
limpets (L.strigatella, L.limatula, and L.gigantea) and C.adunca were also found on
the hermit crabs' shells.
Laboratory Studies: From using the first set of matrices (Figures 2-5) for tanks #1-44,
it is clear that the mean number of different limpets is highest on each snail (8.3),
whereas the mean number of different limpets on each crab was 6 and the mean
number on rock and glass was 2.4. The mean number of times snails had limpets
aboard was 17.2, for crabs it was 9.7 and for the rock and glass it was 4.3. The mean
number of total different snails ridden by each limpet was 12.5 (83%) and the mean
number of total different crabs ridden by each limpet was 3 (60%). The mean total
number of transfers between snails by each limpet was 28.6 (for 30 day study) and 22.9
(for 20 day study). The mean total number of transfers between crabs by each limpet
was 5.8 (for 30 day study) and 3.9 (for 20 day study). The mean total number of
transfers between all substrates was 35.5 (for 30 day study) and 27.3 (for 20 day study).
The second set of matrices (Figures 6-9) allow for some more calculations to be
obtained for tanks f1-44. The mean total "limpet days" for each snail was 17 out of
30 (57%) and 11.5 out of 20 (58%). Therefore about 43% of the snails had no limpets
on them at any given time. The mean total "limpet days" for each crab was 7.2 out
of 30 (24%). and 4.8 out of 20 (24%). The mean total "limpet days" for each rock and
glass is 4.6 out of 30 (15%) and 2.1 out of 20 (11%).
A linear regression of total number of days each T.funebralis had limpets aboard
and each T.funebralis' surface area showed practically no correlation between the
variables (r2 = 0.166, Figure 15).
10
The mean number of days L.asmi spent on any one snail tended to be less than a
day (Figure 16). Approximately 70% of the total snails that were ridden had limpets
on them for less than a day. The longest amount of time a L.asmi spent on any one
snail was between 10 and 11 days. The tanks that were set up as HTD had slightly
higher transfer rates than those that were LTD.
The mean number of days L.asmi spent on any one hermit crab, also tended to be
less than one day (Figure 17). The transfer rate from the hermit crabs tended to occur
à little more frequently than from the snails. The longest amount of time a L.asmi
spent on any one crab was only between 4 and 5 days. With the crabs, once again the
HTD setup had slightly higher transfer rates than those that were LTD.
When comparing the mean number of transfers occuring in the tanks of different
tidal levels during the day (Figures 18-19), the mean for HTD was 8.2 and 5.1 for LTD.
The difference between the means was shown to be statistically significant by a
2-tailed t-test (P«0.001). More transfers are occuring during the high tide level in the
day.
At night the mean number of transfers occuring in the tanks of various intertidal
heights (Figures 20-21), is 6.5 for LTD and 4.6 for HTD. Again the difference between
the means is significant (P«0.001). Hence more transfers are also occuring during the
high tide level in the night.
Finally the mean number of transfers between T.funebralis by L.asmi during the
day was compared to those during the night (Figure 22). The mean number of
transfers during the day was 6.7 and the mean during the night was 5.6. These
means differ significantly (P,0.05). The average transfer rate was about 12.3 transfers
per day with approximately 123% of the population of limpets transferring between
substrates daily. The percentage is larger than 100% because a limpet may transfer
11
more than once in a day. Clearly from Figure 22, after the altercation in time of tide
changes (on the 15th day), the mean number of transfers during the day begins to
rise as the mean during the night begins to fall. Therefore the extra four hours of a
particular tidal level during the day is enough to significantly increase the mean
number of transfers during the day to a point where they are higher than during the
night.
Behavioral Observations in Aquaria: On the few occasions when L.asmi was
observed to transfer shells, the transfer always occured when the limpet and snails
were submerged. The sequence of events usually started with two snails making
contact with their shells. The limpet on one would lift up its shell and touch the
other snail with its tentacles. Then it would slowly move its body over to the other
snail as long as that snail remained relatively stationary. One time a limpet was
seen to begin to transfer shells when its host suddenly started to move away from
the other snail. So the limpet quickly pulled back its body onto its host and clamped
down on this shell. Once a successful transfer has occured, then the limpet will
usually move around its new host for a little while. Transfers are not always
successful. During the course of this study, some limpets were found lying on their
backs on the bottom of the tanks. These limpets remained on the glass for about 24
hours before they were eaten by a hermit crab. A limpet was even found to transfer
onto an empty shell which was in the tank after one of the hermit crabs had died. A
couple times during the study, a L.asmi was found on top of another L.asmi on a
T.funebralis. The limpet moved around on the other limpet and eventually moved
off onto the base of the snail. L.asmi on the rock substrata were noted to move about
15 cm. in 12 hours.
12
Discussion
The percentage of T.funebralis with just limpets on their shells was quite similar
in the various habitats, but the percentage of T.funebralis with just Cadunça on
their shells was definitely larger in the protected sandy beach area with rock outcrops
(Figure 10). This result is to be expected following the study done by Yokoe (1980),
who indicated that juvenile Cadunca are most abundant in sandy, shell-fragmented
areas. These young C.adunca attach themselves to juvenile T.funebralis, living in
sandy, lower habitats. These young hosts provide some protection against the strong
water currents and also protection against desiccation since they are almost
constantly submerged.
The abundance and diversity of various species of limpets in different areas was
not similar (Figure 11). Nine different species of limpets were found to inhabit the
shell of T.funebralis. Seven of these species had been observed previously on
T.funebralis (Brewer, 1975). The two new species, found for the first time on
T.funebralis, were: L.gigantea and L.triangularis.
Area 1, the protected rocky intertidal, had the highest frequency of L.asmi
occuring on T.funebralis, but L.asmi is the only species of limpet that occured most
frequently in this habitat. Actually L.asmi was the limpet which occured most often
on T.funebralis in all three habitats, contrary to what Brewer (1975) found in her
study. There may be some sort of interspecific competition which controls the
distribution and abundance of limpets on T.funebralis. It would be interesting to
remove L.asmi from the T.funebralis shells in area 1 to see if the frequency of
various species of limpets changed at all. At the present, it appears that L.asmi tends
13
to dominate on T.funebralis which would be expected since it is the only adult
limpet to reside on this host. The color of L.asmi is such that it is well camouflaged
when on T.funebralis. This may give L.asmi an added advantage over other species
of limpets whose shell coloring makes them more easily visible to predators. An
experiment testing this hypothesis might be to study the differential rates of
survivability of various limpets on T.funebralis in an area with a great abundance of
potential visual predators.
In the sandy beach habitat, area 2, C.adunca and L.strigatella were most commonly
noted on T.funebralis. Although this habitat was the one with the highest frequency
of L.strigatella (20.9%), it still did not come close to that of L.asmi (38.6%). McLean's
(1966) observations in Pacific Grove did not match my numerical data as he thought
that L.strigatella occured as abundantly as L.asmi on T.funebralis in the same habitat.
Overall the habitats, L.asmi represents 44% of the gastropod commensals on Tegula,
while L.strigatella represents 15%.
Area 3, the wave exposed, steep, and rocky habitat, had the greatest diversity of
limpets on its T.funebralis inhabitants. This area's T.funebralis carried every species
of limpet found in the study and C.adunca. It also had the highest frequency of
every type of limpet except L.asmi and L.strigatella. Limpets in this highly stressful
habitat probably seek out the protection offered to them by their host. T.funebralis
are thought to act as shock absorbers for the limpets against incoming waves (Test,
A., 1946). During times of heavy surge, this snail has been observed to move down
rocks to protected areas, a habit which would also shield epizoic limpets from
crashing water (Daniel, 1978). T.funebralis offers these small limpets much
protection in an otherwise perilous habitat.
In this study, T.funebralis was once again seen to serve as a microhabitat for
14
juvenile limpets (Brewer, 1975). It is probable that any species of juvenile limpet
living in the vicinity of T.funebralis could be found on this intertidal gastropod at
some point. The smallest limpets of each species, except L.asmi (the only adult
limpet found on T.funebralis), were noted on T.funebralis shells in the field, while
the adults of these same species were noticed on the rock substrate. It is known that
small limpets lose water proportionally faster than large individuals (Branch, 1986).
Hence since tiny limpets are highly susceptible to desiccation, their association with
T.funebralis plays a big part in their survivability. T.funebralis in the field were
frequently found clustered around sea anemones at low tide. This position in the
intertidal appeared to keep their shells continually moist.
It is only possible for an animal with a small aperture to maintain a tight fit on
T.funebralis' curved shell (Ricketts, Calvin, & Hedgpeth, 1985). Therefore, there
must come a point when the association between a juvenile limpet and its host is no
longer advantageous to the limpet. The food available to the growing limpet may be
a limiting factor and the increasing shell size of the limpet makes it harder to clamp
down tightly on the T.funebralis shell. L.asmi have shell characteristics and feeding
habits which are perfectly suited to obtaining maturity on this microhabitat.
The length and height of L.asmi in area 2 was found to be smaller than those in
areas 1 and 3 (P«0.001, Figure 12). L.asmi also tends to occur in the lowest density at
the sandy beach habitat. It is possible that the limpet has differential survival in this
area or a slower rate of growth.
L.asmi in area 3 were found to be larger in length (P«0.05) and height (P«0.1) than
those collected from area 1. This habitat, washed by heavy surge, was also heavily
covered with algae. Larger snails were found in areas with heavy agal covering as
noted previously by Wara & Wright (1964). Therefore the larger L.asmi in area 3
15
may be an adaption to their bigger hosts. It may also be possible that those L.asmi
which survive in this rough habitat are the larger ones because it has generally been
noted that the number of L.asmi is inversely proportional to the wave action
received by an area (Eikenberry & Wickizer, 1964). Eikenberry & Wickizer observed
that the shell length of L.asmi was bigger where wave battering was heavier. There
may be more food available to the limpets in such a habitat so that they tend to grow
faster. There may be fewer predators in this wave exposed area, so that the limpets
have a greater survivorship and therefore more old limpets are found. The
increased length of L.asmi in this habitat gives the limpet a larger pedal area which
may allow for stronger power of attachment. It could be interesting to see if there is
any correlation between pedal area of L.asmi and the limpet's ability to withstand
wave action.
L.asmi has been observed to occur most frequently on the base of T.funebralis in
all three habitats (Figure 13). The base of the snail's shell is probably a good position
for the limpet because this area can offer the most protection from wind and wave
action, dessication, direct sunlight, and predation. L.asmi was found on the base of
T.funebralis most frequently in area 3 which would be expected if that part of the
host's shell offers protection to the small limpet. The next most favored position on
the snail's shell is the body whorl. The base and body whorl tend to be the two areas
of the T.funebralis' shell where L.asmi can make the tightest fit. Yet L.asmi is
certainly not limited to any one area on T.funebralis' shell. Although other
researchers rarely found L.asmi above the body whorl of T.funebralis, the limpet can
be found on the upper whorls of the snail (Test, F., 1945; Radford, 1959). Actually
field observations revealed that L.asmi can be found anywhere from the apex of
T.funebralis to its operculum.
16
After collecting T.funebralis and Pagurus in T.funebralis shells in tide pools, it
was clear that L.asmi, C.adunca, and three other species of limpets do occur on
hermit crab shells in the field. The literature would suggest that L.asmi are only
rarely seen on T.funebralis shells occupied by hermit crabs (Test, F., 1945; Eikenberry
& Wickizer, 1964). Yet 2.0% of the hermit crabs collected from the tidepools in the
rocky intertidal had L.asmi on their shells. This is lower than the abundance of
L.asmi on Tegula in the pool habitat(7.5%), but it is still not such a rare occurence to
see L.asmi on Pagurus. L.asmi may transfer to hermit crabs in the field when they
are found amongst T.funebralis aggregations during low tide.
The linear regression of the length of L.asmi against the surface area of its host's
shell showed no correlation between the variables (r2 = 0.047 ,Figure 14). Again no
correlation was found between the total number of days each T.funebralis had
limpets aboard and the T.funebralis' surface area (r2 = 0.166, Figure 15). Hence both
studies in the field and in the laboratory indicated that L.asmi do not show shell size
correlation and this does not interact with the residence time on T.funebralis. It
might be expected that the larger T.funebralis have limpets aboard their shells more
frequently, but this is not what the study revealed. It appears that L.asmi will
transfer between T.funebralis at a frequency where food limitation is not a factor.
The first and second set of matrices produced for each tank clearly showed that
L.asmi prefer T.funebralis as their hosts, although they can also be found on hermit
crabs, the rock substrate, and the glass of the aquaria (in descending order of
preference even though area available for occupancy increases from Pagurus to rock
to glass, Figures 2-9). About 43% of the snails in my study had no limpets on them at
any given time. This figure is very similar to Lindberg's (1990) findings in his study,
although he reported the movement of 16 limpets on 17 snails and I looked at 10
17
limpets on 15 snails in each of my four tanks. Therefore the snails in my study
tended to have more limpets on them at any given time, while Lindberg's limpets
spent more time on the rock substrate.
The mean number of days L.asmi spent on any snail tended to be less than a day
(Flgure 16). About 70% of the total snails ridden had limpets on them for less than a
day. The limpets in Lindberg's (1990) study tended to remain on any one snail for
two to three mean number of days. Most of the limpets in my study moved more
frequently than the four that Radford (1959) observed. She saw no movement by the
limpets from their original hosts after one week. The longest time a limpet in my
study stayed on a snail was between 10 and 11 days, but the majority of limpets
followed Test's (1945) observed patterns where he never noted a limpet remaining
on the same T.funebralis for more than 24 hours. The highest transfer rates were
seen in the HTD tanks.
No one really knows why these organisms transfer so often, especially since each
transfer could potentially lead the limpet to death if it is not accomplished
successfully (like the limpets that fell onto the glass of the aquaria which were then
later eaten by hermit crabs). The amount of microscopic algae on a host's shell may
be a very important factor in determining the transfer rate of L.asmi. An interesting
study would be to look at epiphytic algal biomass as a function of occupancy by
L.asmi and to examine how algal biomass relates to transfer frequency; although the
lack of correlation found in this study with commensal size indicates that transfers
probably occur before food limitation.
The mean number of days L.asmi spent on any hermit crab was also usually less
than one day (Figure 17). The transfer rate from the hermit crabs was actually a little
more frequent than that from the snails. The longest time any limpet spent on a
18
crab was only between 4 to 5 days. In fact, it is surprising to find L.asmi on the shells
of Pagurus at all, for the hermit crab is a predator of these limpets. Maybe limpets
transfer onto crabs accidentally and then later realize their mistake when their host
moves around quite quickly and keeps fighting with other crabs for bigger shells.
Transfer onto or from hermit crab shells must be quite precarious for a limpet, as
this host is not often found to be stationary long enough for a limpet to successfully
transfer.
L.asmi was observed to transfer substrates more frequently at high tide both
during the day and at night (Figures 18-21). This activity pattern is similar to those
described for other limpets, such as T.scutum, L.limatula, and Mac.scabra (Rogers,
1968; Wells, 1980). These three species of limpets are most active while awash by the
tide. Such an activity pattern is expected for L.asmi because the limpet tends to hold
its shell about half a millimeter above the substrate when it is moving (Test, 1945).
Since the limpet shell is usually lifted to cool the body by evaporation when the
surrounding temperature rises too high, this habit could potentially cause L.asmi to
dry out in the air (Branch, 1986). Therefore transfering substrates while submerged
and pulling down its shell against the T.funebralis when emerged, appear to be
L.asmi's strategies against desiccation. Behavioral observations of L.asmi correspond
well with this hypothesis. Hence T.funebralis is a good host for L.asmi since it is
usually found in protected areas of the rocky intertidal zone where it is wetted at
least once daily (Glynn, 1965). There are many alternative hypotheses to why L.asmi
transfers more fregeuntly at high tide. The transfer may be easier at this tidal level
since the limpets may weigh less, the submerged snails may move more slowly,
more chemical cues may be available to the limpets, and/or the limpets may be
subject to less predation. Further research may test the validity of these hypotheses.
19
The mean number of transfers made by L.asmi was higher during the day than at
night (P«0.05, Figure 22). This result was quite different from what Lindberg (1990)
discovered in his study. He saw about 40% of the limpets transfer from one snail to
another between the late afternoon recordings of position and the next set in the
early morning. No transfers were observed to take place between his morning and
afternoon recordings. By contrast, the limpets in my experimental setup transferred
in the day, late afternoon, and evening. About 123% of the L.asmi transferred
between substrates daily, a much higher transfer rate than the limpets in Lindberg's
experiment. My transfer rates are similar to those found by Eikenberry & Wickizer
(1964) who studied limpets in a tank for an evening. Eikenberry & Wickizer's setup
would come close to a continual high tide situation, while Lindberg kept his limpets
at a constant low tide, although the substrate was damp. These different tidal
conditions in themselves could explain the discrepancy in their results.
Yet Lindberg still found more transfers at night while I observed more during the
day. Our definitions of night and day overlap from the late afternoon until 10 PM.
Therefore it is my hypothesis that the highest number of transfers occur somewhere
between 6 PM and 1OPM. After my experiment was changed on the 15th day, the
mean number of transfers in all tanks began to rise during the day and fall at night.
Four extra hours of a particular tidal level during the period between 6PM and 1OPM
appears to be enough to increase the mean number of transfers during the day to a
point where they are higher than the transfers at night.
Further research should be done on L.asmi to determine the validity of such a
hypothesis. A careful study of the activity patterns of L.asmi in the field could clarify
matters greatly. Wara & Wright (1964) noted that T.funebralis moves to the top of
rocks during night high tides, but not during daylight high tides. Therefore it would
20
seem logical that the ideal time for L.asmi to transfer substrates is during the
daylight high tides which was what I found through my laboratory studies.
Acknowledgements
Twould like to thank my advisor, Chuck Baxter, who first gave me an
appreciation of limpets and who always had another good question to ask. I
especially want to thank him for all the help he offered in the identification of
juvenile limpet species and for the many beautiful slides he took for my final
presentation. Thanks to all those at Hopkins Marine Station who lent invaluable
equipment to me, gave good advice, and offered much encouragement. Of course. I
thank the entire spring class 1991 of 175H for an awesome quarter in Pacific Grove. I
also thank my two dear roommates who probably learned more about tiny limpets
than they ever wished to know. Above all I thank God who is my strength and my
redeemer.
Literature Cited
Alleman, L.L. 1968. Factors affecting the attraction of Acmaea asmi to Tegula
funebralis. The Veliger 11(Suppl.): 61-63.
Branch, G. M. 1986. Limpets: their role in littoral and sublittoral community
dynamics. The Ecology of Rocky Coasts, ch.7:97-116.
Brewer, B. A. 1975. Epizoic limpets on the black turban snail, Tegula funebralis
(A. Adams, 1855). The Veliger 17:307-310.
Carlton, J. T. & B. Roth. 1975. Phylum Mollusca: shelled gastropods. Pp.
467-514. In: R. I. Smith & J. T. Carlton (eds.), Light's manual: intertidal
invertebrates of the central California Coast. University California
Press: Berkeley, California.
Daniel, Matthew N. 1978. Rhythmic Movement of the Marine Snail Tegula
funebralis (Prosobranchia: Trochacea) on Intertidal Rocks in Relation to
Tidal and Diel Cycles. Unpub. student report, on file at HMS Lib.
Eikenberry, A. B. & D. E. Wickizer. 1964. Studies on the commensal limpet
Acmaea asmi in relation to its host, Tegula funebralis. The Veliger
6(Suppl.):46-50.
Glynn, Peter W. 1965. Community composition, structure, and
interrelationships in the marine intertidal Endocladia
muricata-Balanus glandula association in Monterey Bay, California.
Beaufortia, vol. 12. 198 pp.
Johnson, Myrtle E. & H. J. Snook. 1927. Seashore animals of the Pacific Coast.
Macmillan, New York. 659 pp.
Lindberg, D. R. 1986. Name Changes in the "Acmaeidae". The Veliger
29(2):142-148.
Lindberg, D. R. 1990. Movement Patterns of the Limpet Lottia asmi
(Middendorff): Networking in California Rocky Intertidal
Communities. The Veliger 33(4):375-383.
McLean, J. H. 1966. West American prosobranch Gastropoda: superfamilies
Patellacea, Pleurotomariacea, Fissurellacea. Doctoral Dissertation,
Biology, Stanford University, Stanford, California. 255 pp.
McLean, J. H. 1978. Marine shells of southern California. Natural History
Museum Los Angeles County, Science Series 24, Revised Edition:1-104.
Radford, Ruth. 1959. A study on Acmaea asmi. Unpubl. Standford Univ.
honors paper.
Reidman, M. L., A. H. Hines, & J. S. Pearse. 1981. Spatial segregation of four
23
species of turban snails (Gastropoda: Tegula) in Central California.
Veliger 24:97-102.
Ricketts, E. F., J. Calvin, J. W. Hedgpeth & D. W. Phillips. 1985. Between Pacific
tides. 5th ed. Stanford University Press: Stanford, California. 652 pp.
Rogers, Don A. 1968. The Effects of Light and Tide on Movements of the
Limpet Acmaea scutum. The Veliger 11(Suppl.):20-24.
Test, A. R. G. 1945. Speciation in limpets of the genus Acmaea. Contributions
from the Laboratory of Vertebrate Biology, University Michigan 31:1-24.
Test, F. H. 1945. Substrate and movements of the marine gastropod Acmaea
asmi. American Midland Naturalist 33:791-793.
Wara, W. M. & B. B. Wright. 1964. The distribution and movement of Tegula
funebralis in the intertidal region of Monterey Bay, California. The
Veliger 6(Suppl.):30-37.
Wells, R. A. 1980. Activity Pattern as a Mechanism of Predation Avoidance in
Two Species of Acmaeid Limpet. J. Exp. Mar. Biol. Ecol. 48:151-168.
Yokoe, D. S. 1980. The Young of the Commensal Gastropod Crepidula adunca:
Feeding, Behavior and Habitat. (Unpublished MS. on file at Hopkins
Marine Station Library).
24
Figure Legends
Fig.1: The three areas at Hopkins Marine Station where the field studies were
done. Area 1 is a protected, rocky intertidal habitat, area 2 is a protected, sandy
beach habitat with rock outcrops, and area 3 is a steep, wave exposed, rocky habitat.
Figs.2-5: Matrices produced from the data collected from tankst1-44. The value in
each cell of the large matrix is the number of times a numbered limpet (1-10 or
11-20) was found on each numbered snail (1-15 or 16-30), each numbered crab
(31-35 or 36-40), the rock, or the glass substrate. The numbers in column A are the
total number of different snails ridden by each limpet and those in column Bare
the total number of different crabs ridden by each limpet. While the entries in
column Care the total number of transfers between snails by each limpet and
those in column Dare the total number of transfers between crabs by each limpet.
Column E gives the total number of transfers between all substrates (snails, crabs
rock, and glass). The means and ranges for each column is given right below it.
Row A lists the number of different limpets found on each substrate and row B
lists the total number of times a substrate had a limpet aboard. The means and
ranges for each row are provided as are the means and ranges just for the limpets
on snails and just for the limpets on crabs.
Figs.6-9: Another set of matrices created from the raw data from tankst1-44. The
value in each cell of the large matrix is the total number of days a numbered
limpet spent on a particular snail, crab, rock, or glass substrate. Row C gives the
total "limpet days" for each type of substrate and each individual organism. The
mean and range of row Cis provided as are the means and ranges just for the total
"limpet days" on all snails and just for the total "limpet days" on all crabs.
Fig. 19: The frequency of limpets and /or C adunca on T.funebralis collected from
three different habitats. The percent T.funebralis with only Cadunca are given
These values do tend to fluctuate from habitat to habitat whereas the percent
T.funebralis with limpets is almost the same in all three habitats.
Fig. 11: The frequency of various species of limpets and/or C.adunça in three
different habitats. L.asmi occurs most frequently in all three habitats, yet more
frequently in the rocky intertidal than in the others. Nine different species were
found along with Cadunca. The variety and abundance of epizoic limpets and/or
C.adunca varies from habitat to habitat.
Fig.12: Mean L.asmi measurements of shell height and shell length in three
different habitats. The difference in the means from the various habitats were
tested for statistical significance using a two-tailed t-test. It was found that the
difference in the mean lengths between areas 1 and 2 and between areas 3 and 2 are
statistically significant (P«0.001). Even the difference between areas 1 and 3 are
significant (P«0.05), although not as significant. The differences in the mean
heights between areas 1 and 2 and between areas 3 and 2 are again statistically
significant (P«0.001). The differences between the mean heights in areas 1 and 3
are not as strongly significant (P«O.1).
25
Fig.13: The position of L.asmi on its T.funebralis host in three different habitats.
The body whorl of the T.funebralis shell is denoted as b.w., just as 2nd w. = second
whorl, and 3rd w. = third whorl. When the limpet was found on more than one
part of the T.funebralis shell, all these parts were noted, e.g. b.w./2nd/3rd w. means
that the limpet was on the body whorl, second, and third whorl of its host's shell.
Fig.14: A linear regression of the length of L.asmi shell against the surface area of
its host's shell (n = 45). There appears to be no correlation between these two
variables (r2 = 0.047).
Fig. 15: A linear regression of the total number of days each T.funebralis had
limpets aboard against the surface area of each T.funebralis shell (n = 60). Again
there appears to be no correlation between these two variables (r2 = 0.166).
Fig.16: The transfer rate of L.asmi on T.funebralis. Most of the different snails
ridden over the entire time of the laboratory study had limpets aboard for a mean
number of less than one day. One limpet did remain om a snail for between ten to
eleven days. LTD = low tide day, HTD -high tide day, LTN = low tide night, and
HTN = high tide night.
Fig.17: The transfer rate of L.asmi on hermit crabs. Again most of the different
crabs ridden over the entire time of the laboratory study had limpets aboard for a
mean number of less than one day. One limpet did remain on a hermit crab for
between 4 to 5 days.
Fig.18: The number of transfers between T.funebralis by L.asmi during low tide
day (LTD) for tanksfl and f4. The mean number of transfers per low tide day is
5.1 out of 10 limpets.
Fig.19: The number of transfers between T.funebralis by L.asmi during high tide
day (HTD) for tanks#2 and 13. The mean number of transfers per high tide day is
8.2 out of 10 limpets.
Fig.20: The number of transfers between T.funebralis by L.asmi during low tide
night (LTN) for tanks#2 and 13. The mean number of transfers per low tide night
is 4.6 out of 10 limpets.
Fig.21: The number of transfers between T.funebralis by L.asmi during high tide
night (HTN) for tankst1 and #4. The mean number of transfers per high tide
night is 6.5 out of 10 limpets.
Fig.22: The mean number of transfers between T.funebralis by L.asmi during the
day and during the night. The mean number of transfers per night is 5.6, while the
mean number of transfers per day is 6.7 out of 10 limpets.
26
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