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I. INTRODUCTION
The hermit crab Pagurus samuelis (Stimpson, 1857) was observed
on the column, tentacles and oral disc of the sea anemones Anthopleura
elegantissima (Brandt, 1835) and Anthopleura xanthogrammica (Brandt,
1835). The crab was apparently not stung by the anemone's nematocysts.
Symbiotic relationships have been described between anemones
and fish (Mariscal, 1966), anemones and shrimp (Dales, 1966), and
anemones and crabs (Davenport, 1966; Dales, 1966) in which the fish
or crustacean is able to move among the anemone's tentacles without
being stung by nematocysts.
This investigation examines the behavior of Pagurus samuelis on
Anthopleura elegantissima and A. xanthogrammica, the crab's behavior in
becoming protected against nematocyst discharge, and possible mechanisms
of protection from nematocyst discharge.
II. GENERAL MATERIALS AND METHODS
All field and lab observations were carried out at Hopkins
Marine Station, Pacific Grove, California. A. elegantissima and
A. xanthogrammica were collected from the Marine Station reserve
and from Pescadero Point on the Monterey Peninsula. Pagurus samuelis,
which live between the 0.0 and 1.5 foot tide level in crevices and
pools, were collected from the Marine Station reserve. Crabs described
as "isolated" were collected from an isolated intertidal pool which
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has no anemones within 5 meters of it. Crabs described as "protected"
did not stick to anemone tentacles and did not jerk back upon contact
with tentacles. A crab was tested for protection by holding its shell
near anemone tentacles and observing the reaction when the crab came
out of its shell and encountered the tentacles. Crabs were always
handled with blunt forceps. Anemones and crabs were kept in the lab in
clear plastic tubs with running sea water. The animals were not fed but
remained active and responsive during the course of the study. All
night observations were conducted with red light.
III. BEHAVIORS OF HERMIT CRABS ASSOCIATED WITH ANEMONES
A. Observations
Each of the following types of behavior was observed both
in the field and in the lab and both during the day and at night.
The crab's interaction with the anemone was found to consist of distinct
behavioral units which are described below.
1. Nestling.
A study was made of the distribution of the crab-anemone
relationship during the day in thirteen one meter square quadrats
at the 0.5 to 1.5 foot tide level when covered by 1 to 2 feet of quiet
water. Of the 262 hermit crabs observed, 17% were sitting quiescently
nestled against anemones. Of the 58 solitary A. elegantissima and
A. xanthogrammica under water in the quadrats, nine anemones (15.5%)
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had crabs nestled against their columns. Of these nine, six anemones
had one crab against them, and the three other anemones had 2, 11 and
12 crabs nestled against their columns. Of the 28 solitary anemones
observed out of water, none had crabs nestled against their columns.
Of approximately 430 clonal A. elegantissima individuals observed,
four hermit crabs were seen nestled against individuals. Fourteen
anemone-crab relationships were set up in the lab: five tanks with
clonal A. elegantissima, two with a solitary A, elegantissima and
seven each with an A. xanthogrammica. Crabs were observed during both
the day and night nestling against the clonal A. elegantissima and the
solitary A. elegantissima and three of the seven crabs with A. xantho-
grammica were observed nestling.
2. Walking on the column.
Crabs were observed walking onto the column of anemones and
exploring it with their antennae and appendages. Using its chelipeds.
a crab often picked up detritus from the column and brought the detritus
to its mouth. Crabs sat quiescently on columns only occasionally. In
the previously described distribution study, 14.4% of the 262 hermit
crabs observed were found walking on the columns of anemones. Of the
58 solitary anemones under water, 8 had at least one crab walking on
their column: two anemones had one crab, two had three crabs, and the
remaining four anemones had 2, 4, 7 and 8 crabs on their column. Of
the 28 anemones observed which were out of water, one anemone had a
hermit crab walking on its column; this was the only hermit crab
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observed interacting with an anemone above water in the quadrats,
Of the fourteen lab relationships, all crabs but two, one with an
A. xanthogrammica and one with an A. elegantissima, were observed
walking on the columns of their anemones. All hermit crabs, including
the 17 isolated crabs observed in initial interactions with anemones,
were able to walk on the columns without being stung, and the anemones
made no response to the presence of crabs on their columns,
3. Poking tentacles.
Crabs were observed poking at tentacles with the tips of their
chelipeds and walking legs for periods of between 5 and 30 seconds.
The tentacles made no response, just as they made no response to the
gentle pokes of a straight pin.
4. Sweeping across tentacles.
In encountering tentacles, the crab would first poke the
tentacles as previously described and secondly sweep its antennae
then several appendages, both chelipeds and walking legs, over the
tentacles. In 5 out of 23 observations made of this behavior, the
crab went directly to the sweeping behavior without first poking the
tentacles. In response to the sweeps, the tentacles would move in
towards the mouth slightly such that the tentacles were no longer
drooping onto the column or substrate. Within thirty seconds, however,
the tentacles would droop back into their original position unless the
crab again swept its appendages over the tentacles. With small anemones,
continued sweeping resulted in the anemone closing completely. The
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crab would then walk onto the anemone and turn all the way around
the anemone, removing detritus from the column, or would shove its
cheliped into the gastric cavity as will be described later.
5. Stroking tentacles.
Crabs were observed using their chelipeds to stroke tentacles
from the base to the tip. The crab would move rapidly from one
tentacle to a neighboring tentacle. In response, the tentacle would
not contract but would move to where the crab pushed it and then spring
back to its original position.
6. Shoving cheliped into gastric cavity.
Crabs were observed walking onto the column and tentacles of
an anemone less than 5 cm. in diameter, sweeping their appendages
across the tentacles until the anemone was closed and then shoving
their chelipeds into the gastric cavity of the anemone. The crab
would usually bring its cheliped to its mouth upon withdrawing it
from the gastric cavity. Upon withdrawal of the cheliped the anemone
would begin to open up but would again close if the crab re-inserted
its cheliped. This activity was observed to continue for periods of
between  and 10 minutes. Crabs were observed climbing into the
opening of the anemone, almost disappearing from sight, only to climb
out within several seconds. Crabs were seen climbing into the mouth
opening of already-closed large anemones in only five cases of the
over 100 crab-anemone interactions observed in the field. In the
twelve lab set-ups with crabs and large anemones this behavior was
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never observed. In the field Mytilus califorianus tissue was fed to
a 15 cm. diameter solitary A. elegantissima which was almost closed,
and within five seconds three Pagurus samuelis on the column of the
anemone ran to the edge of the mouth opening, shoved their chelipeds
into the mouth opening, and removed and ate the Mytilus tissue.
7. Eating anemone tissue.
In the lab, two hermit crabs from the isolated tidepool and
three crabs found in the field on the column of A. xanthogrammica ate
excised tentacle, column and pedal disc tissue of both A. xanthogrammica
and A, elegantissima. A lab P. samuelis ate a tentacle excised from the
lab A. xanthogrammica which it often nestled against and sometimes
stroked the tentacles of. The stomach, intestine and feces of isolated.
field associated and lab associated crabs were examined three and one-half
hours after the crabs were given anemone tissue. Zooxanthellae (algae
symbiotic in anemone tissue and mucus) and three to ten undischarged
nematocysts were found in each digestive system component,
In lab and field observations, chelipeds were never observed
to "snip off" tentacles and damaged tentacles were never seen.
However, in the lab crabs were observed using their chelipeds to pull
at damaged pedal disc tissue of clonal A. elegantissima and damaged
column tissue of an A. xanthogrammica. Large chunks of tissue were
never seen in the chelipeds but the crabs did bring their chelipeds
to their mouths. In the lab and in the field crabs sitting on small
closed anemones were observed placing their chelipeds against the base
of the anemone and rocking backwards, thereby releasing a small part
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of the pedal disc from the substrate. The crab would then shove its
cheliped under the pedal disc and bring the cheliped to its mouth,
It was difficult to observe what the crab was holding in its chelipeds,
however.
The stomach, intestine and feces of a P. samuelis were examined
one and one-half hours after it was found stroking the tentacles and
climbing into the mouth area of a 5 cm. A. elegantissima. Zooxanthellae,
undischarged nematocysts and undischarged spirocysts were found in the
crab's intestine. Up to ten nematocysts/spirocysts and 50 zooxanthellae
were found in one 450x power microscopic field of the intestinal
material. It should be noted here that nematocysts and zooxanthellae
are found in both anemone tissue and mucus.
8. Protection from threat.
Threatened crabs on anemones remained on their anemone, backing
up around the anemone in the lab and wedging themselves between the
anemone and a rock in the field. In ten lab tanks with an anemone
and crab in each tank, the crab was removed from the tank to test for
protection against nematocysts and then replaced in the tank after a
few minutes. In six of the ten tanks the crab immediately ran to sit
beside the anemone or on the base of the anemone's column. In five of
these six tanks the crab had not been observed near the anemone for
several days previous to this encounter.
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B. Discussion
The interaction between hermit crabs and sea anemones may
provide several benefits to both parties. By nestling, crabs may
be protected against dessication and predators. Anemones may also
receive some protection from dessication by having shells against
their columns. Crabs are probably obtaining nutrition from anemones
in the form of detritus from the column and tentacles, other animal
tissue from the gastric cavity and either anemone mucus or tissue.
It is still not clear whether hermit crabs remove tissue from whole
anemones. Besides the other observations already presented, crabs
move among tentacles such that their mouth parts would be in a position
to bite off tips of tentacles, but it is very difficult to see just
what the mouth parts are doing. The anemone may benefit from the
crab's behavior by having excess mucus and detritus removed, but,
of course, the removal of tissue and/or food would be deleterious.
When the removed crabs ran to their anemones after being replaced in
their tanks, they could have been seeking protection or going to the
anemone after being "reminded" of its presence by contact with anemones
in the test for protection.
With large anemones the crab engages in sweeping behavior
when encountering tentacles while walking along the column of the
anemone. The tentacles move so that the crab is able to walk freely
along the column area formerly under the drooped tentacles. By
sweeping the tentacles of small anemones the whole anemone closes
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so the crab is free to walk on the anemone, pick up detritus, shove
its cheliped into the gastric cavity and walk into the mouth opening
of the anemone.
It is not clear why the crab strokes tentacles; the chelipeds
were seldom brought to the mouth during this behavior so the crab is
probably not eating. This behavior would fit, however, as would the
other crab behaviors, into the theory which will be discussed later
of anemone mucus as the crab's protection.
IV. INITIATION OF CRABS TO ANEMONES
A. Observations
One isolated Pagurus samuelis was placed in each of seven tanks,
each of which had one or more already-settled anemones. Five tanks had
one A, xanthogrammica, one tank had one solitary A. elegantissima and
one tank had twelve clonal A. elegantissima 1 to 2 cm. in diameter.
One crab was never seen encountering its A. xanthogrammica even after
two and one-half weeks in the tank, and so will not be included in the
initiation behavior data. The initiation behavior leading to protection
was observed to consist of the following sequential steps:
1. Exploring.
The crabs spent between 17 seconds and 10 minutes exploring the
tank, eating detritus and trying to climb the walls, before encountering
an anemone.
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2. Retreating.
During the exploring behavior the five crabs with A. xanthogrammica
each came within a few cms, of their anemone and then quickly walked
backwards away from the anemone. The crab which eventually had the
greatest number of interactions with its anemone did this three times,
The two crabs which had an intermediate number of interactions each
retreated from their anemone twice, and the two crabs which had the
fewest interactions did this once each.
3. Contacting the column.
With the four A. xanthogrammica the first encounter consisted
of touching the column with antennae and appendages. The crab was not
stung and the anemone did not react.
4. Contacting the tentacles.
Three of the four crabs associated with A, xanthogrammica were
seen to contact A, xanthogrammica tentacles with their appendages and
antennae. In this first contact with tentacles, the antenna or appen-
dage stuck to the tentacle, released and then was placed back on the
tentacle. This was repeated two to ten times. For crabs with A. ele-
gantissima, their first encounter with anemones was to touch their
antennae to the tentacles, which was repeated up to twenty times.
After this encounter the appendage or antenna stuck fewer times for
shorter, less severe contacts—the crab did not jerk back as much as
in previous encounters.
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5. Sweeping across tentacles.
The crab with the clonal A. elegantissima immediately began
to sweep its antennae across tentacles after its antennae were
protected. Three other crabs, the one with the solitary A. elegan-
tissima and two with A, xanthogrammica, were observed sweeping tentacles
while walking on the columns of their anemones several days after their
initial encounter.
6. Nestling
Nestling was observed with clonal A. elegantissima, solitary
A, elegantissima and two A. xanthogrammica the day after the initial
encounters.
Three weeks after their initial encounters the crabs were held
against the tentacles of their own anemones to test for protection.
Of the five total crabs with A. xanthogrammica, the crab with the most
tentacle contact during the three weeks was protected against nematocysts,
the crab with less tentacle contact was protected after one encounter
with the tentacles, and the three crabs with one or no encounters
during the three weeks were not protected. The crab with the solitary
A. elegantissima was stung upon contact with the tentacles four weeks
after the initial encounter, but the crab had not been observed near
the anemone for the previous eight days. The crab with the clonal
A. elegantissima was protected.
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B. Discussion
The behavior of an isolated crab with clonal A. elegantissima
was similar to the behavior, previously described, of crabs on clonal
A. elegantissima in the field. The only difference in behavior was
the initial encounter with the anemone in which the antennae of the
isolated crab stuck to the tentacles. The fact that at the end of
one month the crab with the solitary A. elegantissima was not protected
even though it had been at one point indicates that the protection
against nematocysts can be lost. This will be discussed further in the
next two sections. From the initiation set-ups with A. xanthogrammica
the following pattern of sequential steps leading to full protection
against nematocyst discharge can be elucidated: the crab retreats
from the anemone, later pokes at the column, walks on the column.
touches the tentacles and sticks several times, touches the tentacles
and sticks fewer times, and finally is able to touch, sweep and stroke
the tentacles without being stung. The retreating behavior indicates
that perhaps in the initial stages the crab perceives the anemone as
something to be avoided, but then changes this perception. However,
the fact that one crab was never seen to interact with its anemone,
and another crab was seen interacting only three times in four weeks
suggests that perhaps not all crabs seek to or are able to initiate
relationships with anemones.
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V. DEGREES OF PROTECTION
A. Observations
A crab found on the column of an anemone may or may not be
protected against nematocyst discharge by the same individual
anemone; of 15 Pagurus samuelis found on A. xanthogrammica columns,
8 were protected against nematocyst discharge. Of 14 isolated crabs
tested, none were found to be protected against the tentacles of
either A. xanthogrammica or A, elegantissima.
A crab found on the column of A. xanthogrammica was not
protected against the tentacles of solitary A. elegantissima in all
nine cases tested and was not protected against clonal A, elegantissima
in 8 out of 11 cases tested. However, all seven test crabs found on
the column or tentacles of solitary A. elegantissima were protected
against A, xanthogrammica. In seven cases tested, five crabs found
on the tentacles of clonal A. elegantissima were protected against
solitary A, elegantissima and A. xanthogrammica.
Hermit crabs have not been observed on anemones other than
A. elegantissima and A, xanthogrammica, but various anemone species
were tested in the lab for response to crabs. Tealia lofotensis and
Tealia crassicornis tentacles stuck very strongly to both isolated
crabs and crabs associated with A. xanthogrammica. Corynactis
californica tentacles stuck to the appendages of an isolated crab but
did not stick to crabs associated with A. xanthogrammica. Metridium
senile tentacles did not stick to either isolated crabs, associated
crabs or my finger.
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Hermit crabs found associated with anemones were isolated
from their anemones for various lengths of time and then their
protection against nematocysts was tested. The protection was found to
last from 45 minutes to three days.
B. Discussion
Apparently there are different degrees of protection against
nematocyst discharge, as evidenced by the varied times which crabs
remain protected and the fact that not all crabs found associated
with anemones are protected. In addition, there are species differences
between the protection acquired from an A, elegantissima and an A.
xanthogrammica. Possible explanations for these phenomena will be
discussed in the next section.
VI. POSSIBLE MECHANISMS OF PROTECTION AGAINST NEMATOCYST DISCHARGE
A. Observations
Two isolated crabs which were stung by A. xanthogrammica were
allowed to walk on the column for two minutes. The crabs were then
stung in only 4 and 6 out of 8 encounters with tentacles of the anemone
and the stings were apparently less severe since the crab was able to
touch the tentacle for a few seconds before jerking back and the crab
did not jerk back as far as before.
After rubbing my finger along the column of an anemone 15 to
20 times, the finger no longer stuck to the tentacles of the anemone
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but a control finger did stick. A finger protected against A. xantho-
grammica was also protected against other A. xanthogrammica, but not
against A. elegantissima. A finger protected against A. elegantissima
was also protected against other A. elegantissima and slightly protected
against A. xanthogrammica (the stings felt less severe than the stings
on the control finger).
Paint brush bristles stuck to the tentacles of a lab A. xantho-
grammica, and still stuck after being brushed in the detritus on the
floor of the tank around the anemone. However, after being brushed
along the column ten times the bristles stuck in only five out of ten
and then in one out of ten encounters with the tentacles.
B. Discussion
These observations and those of initial interactions indicate
that protection is acquired by contact with the anemone. There is
no direct evidence that anemone mucus is the factor which provides
protection to the crab, but mucus is a likely substance to be trans¬
ferred from the sea anemone to a crab, finger, or paint brush. Perhaps
these items are protected in only a fraction of the same group of
encounters because of incomplete coating with mucus. The idea of a
mucus protection also fits the observations of different degrees of
protection: crabs may have acquired different amounts of mucus and
therefore be protected to different degrees. Also, the protection
could be lost by a loss of mucus, and the more mucus a crab had and/or
the less active a crab was, the longer the protection would last. The
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species differences in protection against different species could
be explained by species-specific mucus: A. elegantissima is still
stimulated despite the presence of A. xanthogrammica mucus but
A. xanthogrammica is stimulated less in the presence of A. elegan-
tissima mucus.
The initiation of hermit crabs to anemones is similar to the
initiation of anemone-fish to anemones as described by Mariscal
(1966): the fish is stung upon contact with the anemone but continues
to touch tentacles and eventually is not stung. Schlichter (1972)
has shown that the anemone-fish becomes protected from nematocyst
discharge by acquiring anemone mucus. He proposes that this mucus
contains substances which de-sensitize the anemone's sensory inputs
so that the anemone does not sting itself or nearby objects with which
the tentacles have continuous contact. The acquisition of mucus may
also play a significant role in the acclimation of Pagurus samuelis to
Anthopleura elegantissima and A. xanthogrammica. Since an inanimate
object is able to become acclimated to an anemone, it is clear that a
theory explaining the crab's protection need not include a "crab
factor": we need not further examine the hypothesis that the crab
raises the threshold for nematocyst discharge by anesthetic or
recognition by the anemone. The development of immunity to nematocysts
after ingestion of anemone tissue would require a longer acclimation
period than has been observed; also, three crabs fed anemone tissue
for one week were still stung by tentacles,
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If the protection is strictly a matter of anemone mucus we
may ask why more animals are not associated with anemones in order
to reap the benefits of protection from predators and a ready food
source. In order to obtain anemone mucus without being captured by
the anemone, an animal must be able to jerk itself quickly and force-
fully from the tentacles when it is initially stung. Hermit crabs
and fish are capable of this. Because hermit crabs are scavengers,
they are able to exploit detritus on the anemone and partially digested
food in the anemone as food sources. Pagurus samuelis lives in crevices
and pools of the 0.0 to 1.5 foot tide level, a habitat which the
habitats of Anthopleura elegantissima and A. xanthogrammica include.
P. samuelis is therefore more likely to encounter these anemones than
P. granosimanus and P. hirsutiusculus which occur lower in the intertidal,
or shore crabs which occur higher. Occasionally these two other pagurid
species were observed interacting with A, elegantissima and A. xantho-
grammica and appeared to behave like P. samuelis. The main factor
preventing them from more abundant occurrence with anemones is probably
habitat exclusion.
VII. CRABS AS AN ANEMONE FOOD SOURCE
A. Observations
P. samuelis were placed on the tentacles of sixteen solitary
A. elegantissima to test the response of the anemones to hermit crabs
as food. The A. elegantissima ate two isolated crabs, two crabs found
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on A, xanthogrammica, two crabs found on clonal A. elegantissima and a
crab which was climbing on the column and sweeping the tentacles of a
solitary A. elegantissima several days previous to the experiment.
An isolated crab was in the gastric cavity of an A. elegantissima for
20 minutes then escaped or was released, covered with mucus and missing
one antenna. The solitary A. elegantissima did not eat two crabs
found on clonal A. elegantissima, three crabs found near solitary
A, elegantissima and three crabs found on the tentacles of solitary
A, elegantissima. Seven A. xanthogrammica were tested for their
response to hermit crabs as food. One crab found on the column of
A. xanthogrammica but isolated 45 minutes was not dropped on the tentacles
but was captured as it began to interact with a lab A. xanthogrammica,
and was eaten. A crab from the isolated tidepool was taken into the
gastric cavity of an A. xanthogrammica 15 minutes then released. A
crab found on the tentacles of a solitary A. elegantissima and a crab
from clonal A. elegantissima were both eaten by A. xanthogrammica. Two
crabs found on the column and one crab from the oral disc of A. xantho¬
grammica were not eaten. The remains of a Pagurus granosimanus were
found in the gastric cavity of a Tealia lofotensis in the lab. The
crab and anemone had been in the same tank for a week prior to the
crab being eaten.
B. Discussion
Generally, solitary A. elegantissima will eat isolated crabs and
crabs associated with A, xanthogrammica but not crabs associated with
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solitary A. elegantissima. Crabs found on clonal A. elegantissima
may or may not be eaten. A. xanthogrammica generally will not eat
crabs found associated with other A. xanthogrammica. This agrees
with the other observations of species-specific protection and
varying degrees of protection.
The one occasion in the lab in which a crab was captured when
the crab approached the anemone to interact with it indicates that
anemones are able to catch hermit crabs as food.
VIII. SUMMARY
The hermit crab Pagurus samuelis is able to develop a relation-
ship with the sea anemones Anthopleura elegantissima and A. xanthogrammica
such that the crab is able to interact with the column, tentacles and
oral disc of the anemone without being stung by the nematocysts. The
crab steals the anemone's food from its gastric cavity, picks up detritus
from the column and tentacles, and eats either anemone tissue or mucus,
The protection against nematocysts is probably due to the acquisition
of anemone mucus on the crab's appendages so that the anemone responds
to the crab as it would respond to its own tissue.
ACKNOWLEDGEMENTS
I wish to express my thanks and appreciation to Chuck Baxter,
D. P. Abbott, I. A. Abbott and F. A. Fuhrman for their aid and
encouragement in the pursuit of elucidation of the anemone-hermit
crab relationship.
e
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LITERATURE CITED
Dales, R. P. 1966. Symbiosis in marine organisms, p. 299-326.
In Henry, Mark S. (ed.), Symbiosis. Vol. I. Academic Press,
New York. 478 p.
Davenport, D. 1966. Anlysis of behavior in symbioses, p. 381-429.
In Henry, Mark S. (ed.), Symbiosis. Vol. I. Academic Press,
New York. 478 p.
Mariscal, R. N. 1966. A field and experimental study of the symbiotic
association of fishes and sea anemones. Doctoral Dissertation.
University of California, Berkeley.
Mariscal, R. N. 1972. Behavior of symbiotic fishes and sea anemones,
p. 327-360. In Winn, H. E. and B. L. Olla (eds.), Behavior of
Marine Animals. Vol. 2: Vertebrates. Plenum Press, New York,
503 p.
Schlichter, D. 1972. Chemische tarnung: die stoffliche grundlage
der anpassung von Anemonenfischen an Riffanemonen. Mar. Biol.
(Berl.). 12(2): 137-150.