ABSTRACT
The hermit crabs Pagurus samuelis and Pagurus
granosimanis live in close association with the sea
anemones Anthopleura xanthogrammica and Anthopleura
elegantissima in the intertidal region at Hopkins
Marine Station. The crabs are often observed walking
on the columns and tentacles of the anemone without
any response from the nematocysts. This appears
similar in many ways to the relationship established
between the tropical anemone fish and their hosts.
The hermit crabs go through a sequence of be¬
havior in which they acquire a coating of mucus from
contact with the anemone. The mucus is acquired
through a series of behavioral steps exhibited by the
crabs: poking, brushing, and stroking the anemone.
Once acclimated, the crab freely walks among the
tentacles feeding off of small food particles stuck
to the Anthopleura and even removing food from the gut
of its host. The protective mucus coat gradually loses
its effectiveness if the hermit crab is isolated from
anemones. This is a symbiotic relationship benefiting
the crabs by providing a source of food and protection
from a potential predator.
INTRODUCTION
There are many studies on the symbiotic relationship
between sea anemones and fish (Lubbock, 1980) (Schlicter, 1976)
(Mariscal, 1966) (Davenport and Norris, 1958), anemones and
shrimp (Dales, 1966), and anemones and hermit crabs (Hand,
1975) (Ross, 1974). Closely related to these is the curious
behavior of the hermit crabs Pagurus samuelis (Stimpson, 1857)
and Pagurus granosimanis (Stimpson, 1859) in association with
the sea anemones Anthopleura xanthogrammica (Brandt, 1835)
and Anthopleura elegantissima (Brandt, 1835). In the inter-
tidal of Hopkins Marine Station, Pagurus were observed crawling
on the columns, tentacles, and oral discs of the anemones with
apparent immunity to their nematocysts. This behavior differs
considerably from the hermit crab-anemone association studied
by Ross (1974) where the anemone is carried attached to the
shell of the hermit crab.
These studies were carried out to investigate the nature
of the symbiosis chiefly through observing and recording the
crabs' behavior during the acclimation process, looking for
possible advantages in the relationship and studying the
behavior and cooccurrence of the involved species in the field.
My studies indicate the hermit crabs acclimate to anemones,
perhaps by picking up a coating of anemone mucus. The pagurids
may freely crawl over the anemones and take food from the
tentacles or even from the gut cavity. The findings presented
here indicate a somewhat labile symbiosis between these inter¬
tidal hermit crabs and anemones.
MATERIALS AND METHODS
Anthopleura xanthogrammica, Anthopleura elegantissima,
samuelis, and Pagurus granosimanis were all collected at Hopkins
Marine Station on Cabrillo Point, in Pacific Grove, California.
All experiments were conducted either in the field or in tanks
and aquaria with running seawater. One 40 gallon tank and two
10 gallon aquaria were used for all lab experiments. The 40
gallon tank was located outside, exposed to direct sunlight for
approximately 5 hours a day.
The aquaria were located in the
lab with no direct sunlight.
Each tank and aquarium was
decorated to simulate a rocky, sandy tide pool. The anemones
and crabs were fed a diet of Mytilus, barnacles, and a variety
of limpets. All observations at night were conducted with a
red light.
Hopkins intertidal area evidently offers a very suitable
habitat for A. xanthogrammica and A. elegantissima to grow and
multiply as there is an abundance of both species. Also present
in the same area are Pagurus samuelis and Pagurus granosimanis
in great abundance. The research was limited to these two
species of hermit crabs and their association with Anthopleura
of the size range 5 cm. to 11 cm.
Once transferred to the aquaria, the anemones took approxi¬
mately 3 to 5 days to attach and show normal behavior. One
noticeable change in behavior was that within a week the stick
iness of the tentacles decreased (Mariscal, 1966). For this
reason fresh anemones were brought in each week. The hermit
crabs taken from the same tidepools in field showed no apparent
changes of behavior in lab whereas those taken from separate
tidepools exhibited fighting for five days. The crabs from both
tidepools were equally as active at night as during the day.
Association
For a study on the duration of the relation between hermit
crabs and anemones, in the field eight tidepools were used,
four with anemones and four without. As much care as possible
was taken to select tidepools which were similar in exposure,
height, and location. In each tidepool shells of crabs were
marked with red fingernail polish. For a week, records were
kept as to the number of marked crabs remaining in each tidepool.
Distribution and Density
To determine the distribution and cooccurrence of crabs
and anemones in the study area, six transects, 10m x 5m, were
established as marked on the map of figure 2. Anemones in
the b to 11 cm size range were counted in these transects and
hermit crabs were sampled by haphazardly placing .25m
quadrats along each transect. This was done for both regions
sampled.
Acclimation
To quantify the shell acclimation of the hermit crabs, I
measured the force of adhesion of the tentacles to acclimated
and non-acclimated shells using a portable torsion balance
that measured up to 24 gms. Tegula were attached by nylon
thread and slowly lowered onto the tentacles of A. xanthogrammica
and the force required to free the shell was recorded.
To test for persistence of the acclimated state 50 empty
Tegula shells were acclimated by wiping them on the tentacles
of anemones. These were held in an aquarium with running sea
water along with 50 unacclimated Tegula shells. Tests were
made for the adhesion to anemone tentacles for samples of 5 of
each category for the first day at 1 hour intervals after
acclimation for 3 hours and then daily for 7 days (refer to
Table 1).
Haphazard samples of 40 crabs in 3 separate tidepools in
the field were tested for acclimation. A simulated tidepool
was set up by placing 40 unacclimated crabs into an aquarium
with two A. xanthogrammica and after 5½ weeks the number of
crabs which were acclimated was recorded.
Mucus and Nematocyst Verification
In the final experiment to verify mucus accumulation 5
acclimated and 5 non-acclimated shells were placed in flasks
with suspended carbon particles. The flasks sat for 24 hours
to allow normal settling. Observations were made under a
dissecting microscope to detect the presence of mucus.
For a verification of nematocyst discharge following crab
contact with the anemone, observations were made before and
after actual contact with the anemone. Nematocysts were
stained using methylene blue dye after scrapings were trans¬
ferred from the chelipeds and shell to cover slips.
RESULTS
Distribution and Density
A comparison of anemone density, hermit crab density, and
their association in the study area is shown in Figure 1.
West Beach had an average density of 2.7 anemones/m whereas
Bird Rock Beach showed 6.2 anemones/m2. These were significantly
different by the student t-test (p..05). In the sparsely
populated West Beach area 733 of the anemones were A. xantho¬
grammica and only 188 A. xanthogrammica along Bird Rock Beach.
The remaining percentages were A. elegantissima. In contrast,
the proportion of crabs grazing on the tentacles and columns
along West Beach was .25 crabs/anemone as compared to Bird
This shows a
Rock Beach where there was .5 crabs/anemone.
significant difference p..025 (Rx C contingency test).
Acclimation
Upon first encounter with the sea anemone, the hermit crabs
exhibited a behavior I call "poking and retreating." The crabs
approached an extended anemone and with their antennae and
chelipeds poked at the tips of the anemone's tentacles. Imme¬
diately after each poke they jumped back and retreated a
distance. In between pokes the crabs often explored or fed
on the immediate area of the rock. This continued for 5 to
30 pokes.
Once this behavior was completed, the crabs began a period
of brushing their shells on the tentacles of the anemone. Most
often the crabs faced away from the anemone, held on to the
substrate and placed their shells in contact with the tentacles,
They often sat in one spot and moved their shell back and forth
through the tentacles. On other occasions crabs would walk
back and forth brushing the tentacles. The tentacles often
retracted but did not appear to stick to the shell. They
displayed this behavior between 5 and 20 minutes.
When the brushing was discontinued, the crabs began sweeping
and stroking the tentacles with their antennae. The sweeping
motion extended along the entire length of the tentacles. An
occasional stroke of the antennae would be across the bodies
of the crabs. This behavior continued for 5 to 25 minutes,
The crabs were then observed freely walking among the tentacles,
Not all of the crabs which engaged in some of the steps
engaged in them all. However, those that actually walked on
the tentacles and therefore were considered completely acclimated
did display each step sequentially. Many pagurids completed
one or two steps and then left the vicinity of the anemone.
The anemone's response to these actions varied. Normally
only those tentacles being contacted while being brushed or
poked responded with retraction. Within a couple of minutes
these tentacles were again fully extended. However, 1 out of
10 anemones responded by slowly and completely closing. It took
from 20 minutes to 45 minutes for the anemone to relax and re¬
open. Once acclimation occurred, the only response was an
occasional retraction of a tentacle as it was contacted. As
the crab walked among the tentacles, it stroked each tentacle
in its path with its antennae. Again, as when acclimating, the
antennae would occasionally be brought to the body.
Some crabs were feeding off of the small particles stuck
to the tentacles. On three different occasions, I noticed a
crab aggressively entering through the tentacles of an
A. xanthogrammica and inserting its chelipeds into the gastric
cavity, withdrawing chunks of food and eating. One final ob¬
servation was the crab dislodging detritus which accumulated
on the tentacles.
Adhesion Tests
As seen in Table 1, the acclimated Tegula shells had very
little, if any, adhesion to the tentacles. This lasted for
several days but adhesion did increase from 1.5 gms. to 7.5
gms. within the week. The unacclimated shells registered an
average of 20 gms. or greater with each trial.
The results on the number of acclimated crabs after 2 months
in the aquarium with anemones showed 32 out of 40 or 803
acclimation as compared to 47 out of 120 or 398 for those sampled
in the field.
Discharged nematocysts were found on 5 out of 6 of the
acclimated crabs. The nematocysts were visible under the
compound microscope at 40x power and could be positively
identified at 100x magnification. Methylene blue dye colored
each nematocyst a bright purple.
It was obvious with the dissecting microscope that carbon
particles had settled in denser patches on the acclimated
shells. The particles appeared supported on a mucus layer
that held them above the shell as seen with 45x magnification
of the dissecting microscope. The unacclimated shells also
accumulated some carbon particles but not nearly as much.
All five acclimated shells were easily differentiated by eye
inspection from the unacclimated, once the particles had
settled.
It was also noticed throughout the study that a crab
acclimated to A. elegantissima was acclimated to both A. elegan¬
tissima and A. xanthogrammica. However, those acclimated to
A. xanthogrammica were not acclimated to A. elegantissima.
DISCUSSION
These studies indicate intertidal hermit crabs can become
acclimated to the large carnivorous anemones that share their
habitat. The association is in many ways similar to the many
observations that have been made on the clownfish and their
host anemones. There are however a significant number of
differences. They are similar in that a sequence of behavioral
steps is performed in which the symbiote acquires a coating of
anemone mucus which is necessary to gain immunity from the
host's nematocysts (Mariscal, 1966) (Davenport and Norris, 1958)
A recent investigation by (Lubbock, 1980) claims that the
immunity is attributable to special properties of the endo¬
genously produced mucus of anemone fish. It differs from the
mucus of other fish in being much thicker and contains neutral
polysaccharide rather than acidic ones. Hermit crabs produce
no external mucus and only lose their stickiness to anemone
tentacles after exposure to anemone mucus.
The two differ in specificity of association between
symbiote and host. The fish establishes onehost and will
return in preference to another anemone. The hermit crabs
are not closely tied to one anemone and are acclimated to and
visit a number of anemones in their range. While the clown¬
fish receives protection from the anemone's tentacles, the crab
benefits by feeding from the tentacles and actually with¬
drawing food from the anemone's gut. The crab-anemone asso¬
ciation is essentially a commensal symbiotic relationship
benefiting the crab whereas the anemone also benefits from the
fish categorizing it as mutualistic symbiosis (Mariscal, 1966).
The exposed, steeply graded, rocky West Beach area has a
lower density of sea anemones than the protected Bird Rock
region and they are primarily A. xanthogrammica. Despite all
of these differences this study revealed a remarkable similarity
in the pattern of association between the hermit crabs and
their host anemones. It is possible that the advantages to
the crabs in associating with the anemones compensate for the
many environmental differences. This is further supported by
the observation of marked stability of residency of crabs in
pools with anemones compared to pools without.
Another intriguing observation involved the percentage
of the hermit crab population in the Bird Rock transect areas
which were acclimated to anemones. In an area with an abundance
of anemones many clonal ones in addition to the large solitary
forms, only 408 of the crabs were acclimated. In the aquarium
where the hermit crabs were left in contact with the anemones
for over 5 weeks there were still 208 unacclimated. This may
result from some intraspecific differences in behavior,
social exclusion, stage of life cycle, or simple differences
in opportunity. It is certainly an aspect of the study that
requires more work.
The acclimation behavior pattern of the hermit crabs has
some interesting parallels with the acclimation behavior
described for the tropical anemone fish. The initial poking
and retreating behavior resembles the nibbling of the fish at
the base of the column and tentacles. The fish behavior of
diving into the tentacles and wriggling through them seems to
correspond to the crab's behavior of rubbing the shell on the
column and tentacles of the anemone. This probably indicates
the most effective behavioral sequence for acclimation to the
anemones is strongly conditioned by general properties of the
responses of anthozoan cnidoblasts and nerve net. If the
initial approach is too abrupt the anemone will be stimulated
into either feeding or protective withdrawal behavior and thus
terminate the encounter.
The poking and retreating initiates contact with the
tentacles and may orient the crab to the responses of the
anemone and begins habituation of the anemone to the crab,
This step probably accumulates mucus on the cheliped surfaces
and antennae. The brushing maneuver exposes the shell to
the mucus and brings it closer to the entire crab acclimation.
Shell acclimation is crucial to the crab for movement through
the tentacles without sticking and causing a contraction.
Hours of observations suggest that the small appendages and
upper abdomen obtain a mucus via the antennae.
The observation that unacclimated crabs, if large enough,
when placed on the oral disc can escape even after being
swallowed by the anemone indicates the crab is well adapted
to establish its symbiotic relationship. However, the escape
takes quite a bit of time in which the crab could be doing
other things. Also when the crabs are too small to free them¬
selves they will be eaten. The acclimation process permits the
pagurids to freely exploit their environment, gain another
source of food, and perhaps other unrecognized advantages.
Where encounters are frequent, as in crowded tide pools, this
has obvious advantages for both in simple saving of time.
Because of their similarity in times of activity, habitat
and population abundance, it seems evolutionarily and eco¬
logically fitting that their daily routines should involve
each other. Association may have evolved commensally as the
hermit crab acquired a series of behavioral acts to obtain a
food source. Benefits if proven for the anemone would give it
a more mutualistic definition.
ACKNOWLEDGEMENT
I would like to thank Dr. D. P. Abbott, Dr. I. A. Abbott,
Robin Burnett and Charles Baxter for instruction and counsel
during this study. Special thanks goes to Charles Baxter for
advice, encouragement, and the editing of this paper. I would
also like to thank my mother for coming all the way from
Oklahoma to type this paper.
LITERATURE CITED
Dales, R.P. 1966. Symbiosis in marine organisms. In Henry,
Mark S. (Ed.), Symbiosis, Vol. I. Academic Press, New
York. p. 478.
Davenport, D. 1955. Specificity and behavior in symbiosis.
The Quarterly Review of Bio., 30, 29-46.
Davenport, D., Norris, K. S. 1958. Observations on the symbiosis
of the sea anemone Stoichactis and the pomacentrid fish,
Amphiprion percula. Biol. Bull. mar. biol. Lab Woods Hole,
115(3), 397-410.
Hand, Cadet 1975. Behavior of some New Zealand sea anemones and
their molluscan and Crustacean Hosts. N.Z.J. Mar. Fresh-
water Res., 9(4), 509-527.
Hazlett, B. 1970. Tactile stimuli in the social behavior of
Pagurus bernhardus. Behavior, 36, 20-48.
Lubbock, R. 1980. Why are clownfishes not stung by sea anemones?
Proc. R. Soc. London, B207, 35-61.
Mariscal, R.N. 1966. A field and experimental study of the
symbiotic association of fishes and sea anemones. Doctoral
Dissertation, Univ. of Cal., Berkeley.
Ross, D. M. 1974. Behavior Patterns. In L. Muscatine and H.M.
Lenhoff (Ed.), Coelenterate Biology, Academic Press, New
York. pp. 281-309.
Winston, M. and Jacobsen, S. 1978. Aggressive interactions
among hermit crabs. Animal Behavior, 26(1), 184-191.
TABLE LEGEND
Table 1: Adhesion force exerted by the tentacles of Anthopleus
xanthogrammica on empty Tegula shells. Measurements which
exceeded 24 gms. maximum are recorded as 24+.
FIGURE LEGEND
Figure 1: Distribution map and graph showing the densities
of Anthopleura xanthogrammica and Anthopleura
elegantissima, the densities of hermit crabs and
the numbers of crabs associated with anemones for
6 transects around Cabrillo Point at Hopkins
Marine Station. Transect 1 and 2 are considered
West Beach transects. 3, 4, 5, and 6 are con¬
sidered Bird Rock Beach transects.
Figure 2:
Residency of marked crabs in pools with and pools
without anemones.
Table 1
hour
.5
1.5
2.5
day
Adhesive force
grams
Acclimated
Non-acclimated
range
mean
range
mean
10.0-244
22.04
0-4.0
7.5-24+
13.04
1.5
0-2.0
20.0-24+
1.0
24.0+
0-3.0
2.0
18.0-24+
20.0+
1.0-6.0
4.0
20.0-24+
22.0+
0-3.0
21.0+
1.0
12.0-24+
24+
0-3.5
24+
1.5
4.0
24+
24+
0-5.0
24+
24+
4.0
0-6.0
24 +
1.0-4.0
24+
2.0
24 +
24 +
2.0-9.5
7.5
24 +
2.0-10.0
24 +
6.5
1.0-12.0 7.5
24 +
24 +
16
9

28





25
u
5
E+
2
0-
9



58

EOE


10
18
18
Figure 2
50
40
30
20
10
F 50)
40
30
20
10
WITH ANEMONES

Number of Days
WITHOUT ANEMONES
O
-8=
Number of Days
-0
O
-—
5
9-
18