Effects of Predation Pressure On the Mutualistic Interaction Between the Hermit Crab, Pagurus Pollicaris Say, 1817, and the Sea Anemone, Calliactis Tricolor (Lesueur, 1817)-bach1980

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104
- We thank Dr.
Raymond B. Manning for confirming
Acknowledgements.
the identification of the specimens and for reviewing the manuscript; Drs. E. C.
Raney and R. L. Wigley for their comments on the manuscript; R. D. Brodeur
for technical assistance; and T. C. Ellis for drawing the figure.
REFERENCES
R. P., 1894. Report on the Crustacea of the order Stomatopoda collected by the steamer
BIGELOW,
Albatross between 1885 and 1891, and on other specimens in the U.S. National Museum. Proc.
U.S. natn. Mus., 17: 489-550, pls. 20-22, text-figs. 1-28.
R. B., 1962. Seven new species of stomatopod crustaceansfrom the northwestern Atlantic.
MANNING,
Proc. biol. Soc. Washington, 75: 215-222.
1967. Preliminary account of a new genus and a new family of Stomatopoda. Crustaceana,
-,
13 (2): 238-239.
1969. Stomatopod Crustacea of the western Atlantic. Stud. trop. Oceanogr. Miami, 8:
-,
i-viii + 1-380.
1974. Marine flora and fauna of the northeastern United States. Crustacea: Stomatopoda.
-,
NOAA tech. Rep. NMFS Circ.-387.
SMITH,S. I., 1881. Preliminary notice of the Crustacea dredged, in 64 to 325 fathoms, off the south
coast of New England, by the U.S. Fish Commissionin 1880. Proc. U.S. natn. Mus., 3: 413-452.
OF PREDATION
PRESSURE ON THE MUTUALISTIC
THE
HERMIT CRAB, PAGURUS POLLICARIS
BETWEEN
CALLIACTIS TRICOLOR
SAY, 1817, AND THE SEA ANEMONE,
EFFECTS
INTERACTION
(LESUEUR,
1817)
BY
CATHERINE E. BACH
Division of Biological Sciences,University of Michigan, Ann Arbor, Michigan 48109, U.S.A.
and
WILLIAM F. HERRNKIND
Department of Biological Science, Florida State University, Tallahassee, Florida 32306, U.S.A.
Introduction. - Mutualistic interactions between organisms are widespread in
the marine environment
(see reviews by Dales, 1966, and Fricke, 1975). There
has been much speculation as to the benefits to each organism, but there is a marked
lack of data supporting these speculations. A commonly hypothesized benefit of a
mutualistic interaction is protection from predation (e.g. anemone-fish, Mariscal,
1970; scallop-sponge,
Bloom, 1975; fish-shrimp,
Fricke, 1975; and zoanthidIn
the
case
of
it should be possible
mutualisms,
West,
sponge,
1976).
obligate
to determine the degree to which the mutualistic interaction provides predator
protection by removing the mutualistic partner and observing a decline in survivor.
ship of the other organism. However, if the mutualism is facultative, one could
105
between the frequency of the mutualism and the
also look for a relationship
would be especially true if the formation of the
This
of
intensity
predation.
association occurred by active behaviors of the interacting organisms. If one
mutualistic partner is benefiting from predator protection, a greater frequency of
the mutualistic interaction is predicted in areas with greater predation pressure.
This study tests this hypothesis for a mutualism between a hermit crab, Pagurus
pollicari.r Say, and a sea anemone, Calliacti.r tricolor (Lesue.ur) . It has been suggested for such associations that the sea anemone protects the hermit crab from
predation (Ross, 1967; 1971). In some associations both the crab and the anemone
initiate the interaction (Ross & Sutton, 1961). Laboratory experiments document
that P. pol/¡caris is indeed protected from predators such as the oxystomatid crab,
and the octopus, Octopus joubini Adam, by having
Calappa f lammea (Herbst),
the anemone on its shell (McLean & Mariscal, 1973). In addition, another hermit
crab species, Dardanu.r arrOJor (Herbst), increases its behavior of acquiring anemones after octopus predators are introduced in laboratory conditions after a long
absence (Balasch & Mengual, 1974). It has been suggested that C. tricolor benefits
from the interaction by having a hard substrate on which to attach, allowing anemones to inhabit regions without suitable substrates for attachment, and by the
interception of food particles while crabs feed (Ross, 1967). Some species of
anemones even show preference for motile crabs over other substrates (Ross, 1974)
and some species of hermit crabs actually feed their sea anemones (Fox, 1965).
whether predictions arising from the results of
In this study, we determined
of
McLean's
and Mariscal's are upheld in the field, i.e.
laboratory experiments
is there a greater frequency of P. pollicarz.r carrying anemones in areas of greater
predation pressure?
Materials and methods. - Surveys were conducted during June, 1978, at five
shallow-water sites near the Florida State University Marine Laboratory, Sopchoppy,
Florida (A: Bay Mouth Bar, B and C: Dog Island Shoals, D and E: Turkey Point
Shoal). At each site, all individuals of P. pollicaris found while searching for
were collected and the following data were
four person-hours
approximately
recorded for each crab: (1) species of gastropod shell occupied, (2) presence or
absence of recent aperture damage to the gastropod shell, and (3) presence or
absence of anemone ( s ) on the gastropod shell.
Relative intensity of predation pressure was measured by the frequency of
gastropod shells inhabited by hermit crabs which showed evidence of recent damage
by predators. The box crab, Calap pa f lammea, a common predator on P. pollicari.r,
diurnally lives buried in the sand (thus making density estimates very difficult),
but leaves characteristic damage marks on shells (Shoup, 1968) by breaking them
open with a modified cheliped. Since measures of current, not past predation
pressure, were desired, only recent shell damage attributable to C. f lammea was
recorded (i.e., no epibiota on broken portion of shell).
Results. - There is a significant positive linear relationship between predation
pressure, as measured by the percentage of recently damaged shells, and the
106
frequency of hermit crabs carrying anemones (fig. 1). The particular gastropod
shell species present could affect the probability of a shell becoming damaged
or the probability of a hermit crab inhabiting that shell carrying an anemone. We
compared the frequency of shells with anemones to the overall frequency of the
various shell species and found no effect of shell species on the probability of
= 8.8,
= 9,
df
p> .25 ) . Similarly,
finding an anemone on a shell (chi-squared
the distribution of damaged shells also is not different from that predicted by
chance alone, based on the total number of shells of each species (chi-squared =
=
13.2, df
9, p > . i o ) . Thus, the distribution of shell species in the five sites cannot
explain the differences in the frequencies of damage or anemones between sites.
Discussion. - It appears that the higher the intensity of predation by shelldamaging predators at a particular site, the higher the frequency of the mutualistic
interaction between P. pollicariJ and C. tricolor. This relationship is not simply a
function of different shell assemblages at the five sites, nor is it likely to be a
function of different availabilities of anemones, since all sites were similar in
depth, substrate, and salinity patterns. In fact, the difference in anemone frequency
is much greater between different locations on the same sand bars than between
certain sites on different sand bars; e.g., site C on the offshore Dog Island Shoal
and site E on the inshore Turkey Point Shoal. Although the number of sites is not
as large as would be desirable, the large amount of variance explained by the
linear regression is indicative of a biologically realistic relationship.
Obviously a more direct way to test whether the presence of an anemone on a
Fig. 1. Relationship between predation pressure and percentage of Pagttrus pollicari.r Say carrying
anemones. Predation pressure is measured by the percentage of crabs in shells recently damaged by
Calappa flammea (Herbst). The equation for the regression line is y = .84 x + 2.61 (r2 = .83,
p<.05). Sample sizes of the collections at the five sites were: A (N = 75), B (16), C (29),
D (80), and E (27). Standard errors of estimates of the percentagesare indicated.
107
shell protects its hermit crab inhabitant, would be to analyze the relationship between predation pressure and anemone frequency for individual crabs (i.e., do
those crabs which are carrying anemone(s)
have a lower frequency of damaged
this
kind
of
is
because hermit
analysis
shells?). However,
clearly inappropriate
crabs are continually changing shells and also can transfer their anemones to their
new shells (Hazlett, 1972).
It must be pointed out that frequency of shell damage is only a relative estimate
of predation pressure. In addition to the characteristic damage to shell apertures,
C. f lammea may also break spires and render shells unfit for habitation by hermit
crabs. Other species may also damage some shells while removing epibiota. Finally,
other hermit crab predators, such as Octopus joubini, which do not damage shells,
may contribute to the phenomenon of increased incidence of anemones.
Despite these limitations, our data support the hypothesis that the anemone,
C. tricolor, may indeed provide protection for P. pollicaris. The predictions derived
from laboratory experiments seem to be supported in the field. However, a more
complete test of this hypothesis would involve studying survivorship of marked
crabs both with and without anemones and obtaining accurate density information
on predators.
- We thank the Florida State
Acknowledgements.
University Marine Laboratory
and the Psychobiology Program for support of this research. Also we thank Brian
Hazlett and William Lindberg for assistance in data collection, and Diane Deand David Wethey for
Steven, Pat Dillon, Brian Hazlett, John Vandermeer,
comments on the manuscript.
LITERATURECITED
1974. The behavior of Dardanus arrosor in association with Calliactis
J. & V. MENGUAL,
BALASCH,
parasitica in artificial habitat. Mar. Beh. Phys., 2: 251-260.
BLOOM,S. A., 1975. The motile escape response of a sessile prey: sponge-scallopmutualism. Journ.
exp. mar. Biol., 78: 311-328.
DALES,R. P., 1966. Symbiosisin marine organisms. In: S. M. HENRY,ed., Symbiosis,1 (Academic
Press, New York).
Fox, H. M., 1965. Confirmation of old observations on the behavior of a hermit crab and its commensal sea anemone. Ann. Mag. nat. Hist., (13) 8: 173.
FRICKE,H. W., 1975. The role of behavior in marine symbiotic animals. Soc. expl. Biol. Symp.,
29: 581-594.
HAZLETT,B. A., 1972. Ritualization in marine Crustacea. In: H. E. WINN & B. L. OLLA,eds.,
Behavior of Marine Animals, 1: 97-125. (Plenum Press, New York).
1973. Protection of a hermit crab by its symbiotic sea anemone
MCLEAN,R. B. & R. N. MARISCAL,
Calliactis tricolor. Experientia, 29: 128-130.
R. N., 1970. The nature of the symbiosisbetween Indo-Pacific anemone fishes and sea
MARISCAL,
anemones.Mar. Biol., 6: 58-65.
Ross, D. M., 1967. Behavioral and ecologicalrelationships between sea anemones and other invertebrates. Ann. Rev. Oceanogr. mar. Biol., 5: 291-316.
1971. Protection of hermit crabs (Dardanus spp.) from Octopus by commensalsea anemones
-,
(Calliactis spp.). Nature (London), 230: 401-402.
1974. Evolutionary aspects of associationsbetween crabs and sea anemones. In: W. B. VERN--,
BERG,ed., Symbiosisin the Sea. (Univ. South Carolina Press, Columbia, South Carolina).
Ross, D. M. & L. SUTTON,1961. The associationbetween the hermit crab Dardanus arrosor (Herbst)
and the sea anemone Calliactis parasitica (Couch). Proc. roy. Soc. London, 155: 282-291.
.
108
SHOUP,J. B., 1968. Shell opening by crabs of the genus Calappa. Science,New York, 160: 887-888.
WEST,D. A., 1976. Aposematic coloration and mutualism in sponge-dwellingtropical zoanthids. In:
G. O. MACKIE,ed., Coelenterate Ecology and Behavior: 443-452. (Plenum Press, New York).
AN INDIAN
OCEAN RECORD FOR SADAYDSHIA
BABA (DECAPODA,
ANOMURA)
ACROPORAE
BY
NASIMA M. TIRMIZI
Invertebrate Reference Museum, University of Karachi, Karachi, Pakistan
The genus Sadayoshia Baba, 1969 of the family Galatheidae contains five species,
all Indo-Pacific. Only one, S. edwardsi (Miers), was previously recorded from the
Indian Ocean. Three male specimens, obtained by the International
Indian Ocean
a
new
Indian
Ocean record for Sadayoshia
Expedition (IIOE) 1963-1964, provide
acropora.e Baba known only from the type locality: Ryukyu Islands (Baba, 1972:
43 ). The specimens at hand agree well with the holotype except in some details
which are noted in the following account.
Sadayoshia
acroporae
Baba, 1972
Sta. AB 29, Anton Bruun Cruise 1; 11°23'N 93°31'E, 80 m, 28 March 1963; 1
Sta. 363 P, Anton Bruun Cruise 7; 23°17'S 43°33'E, 1225 m, 6 August 1964 2 a a
mutilated and therefore not included in the detailed study).
(one badly
Measurements (in mm; of the male from Sta. AB 29 and the least damaged male
from Sta. 363 P, respectively). - Carapace length (including rostrum, but extreme
tip broken), 10, 9; carapace breadth, 6, 5.5; length of cheliped, 20 (left), 19
(right), -, (broken in the second specimen but at least 12 mm long).
The material will be deposited in the National Museum of Natural History,
Smithsonian Institution, Washington, D.C.
The rostrum and the supraorbital spines are without scales in the larger specimen from Sta. AB 29 (fig. 1); with a few scattered ones in the smaller specimen
from Sta. 363 P (fig. 2). The outer orbital angle is rather acute. The carapace,
excluding the rostrum, is either as long as or slightly longer than wide.
A small additional stria (fig. 1, s) is present behind the second stria of the
carapace, in the larger specimen. In the smaller specimen the number of striae m
front of the cervical groove is reduced. There are only three striae behind the
additional stria. Only one or two coarse setae are present on the dorsal surface of
the carapace. In the larger specimen there is an additional marginal tooth on the
right side, as illustrated.
The third maxilliped has the inner terminal tooth of the ischium poorly devel-
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