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Symbiosis of Sea Anemones and Hermit Crabs in Temperate Seas

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Abstract

Symbiosis, according to its initial meaning, refers to the biological interaction between two organisms living in close association. However, this definition is rather controversial, with the term being often used generically, since the outcome can vary across a continuum from negative to positive interactions. Symbiosis is a widespread phenomenon in temperate marine communities, and the association between sea anemones and hermit crabs belongs to the most common cases, being a familiar example of mutualism. In these latter specific cases of interactions gastropod shells are involved as prerequisite, since they provide both refuge for hermit crabs and substratum for the settlement of sea anemones; thus, shell resource availability is crucial for the establishment of this particular type of symbiosis. Within this context the present study aims to integrate the results of various studies to provide a general review about the symbiotic interactions of sea anemones and hermit crabs in temperate seas, addressing the following issues: (1) clarify the relevant terminology, which is differently interpreted by various authors; (2) provide a general description of the sea anemone - hermit crab association, as most studies examine separately the species involved and not the symbiosis as a whole; (3) assess the diversity and distribution of sea anemone - hermit crab associations in temperate seas, also incorporating gastropod shells and their availability, which although crucial, has been only little investigated; (4) address the behavioural patterns of both symbionts for the establishment of the symbiosis, including as well the behavioural plasticity of hermit crab related to shell resource utilization, and (5) report relevant information about co-evolution of the participant species, referring to the existing hypotheses on the evolution of the symbiosis, underlining its importance.
In: Symbiosis: Evolution, Biology and Ecological Effects ISBN:978-1-62257-211-3
Editors: A. F. Camisão and C. C. Pedroso © 2013 NOVA Science Publishers, Inc
Chapter 4
SYMBIOSIS OF SEA ANEMONES AND HERMIT CRABS IN
TEMPERATE SEAS
Chryssanthi Antoniadou
, Anna-Maria Vafeiadou
and Chariton Chintiroglou
School of Biology, Department of Zoology,
Aristotle University, Thessaloniki
ABSTRACT
Symbiosis, according to its initial meaning, refers to the biological interaction between two
organisms living in close association. However, this definition is rather controversial, with the
term being often used generically, since the outcome can vary across a continuum from
negative to positive interactions. Symbiosis is a widespread phenomenon in temperate marine
communities, and the association between sea anemones and hermit crabs belongs to the most
common cases, being a familiar example of mutualism. In these latter specific cases of
interactions gastropod shells are involved as prerequisite, since they provide both refuge for
hermit crabs and substratum for the settlement of sea anemones; thus, shell resource
availability is crucial for the establishment of this particular type of symbiosis. Within this
context the present study aims to integrate the results of various studies to provide a general
review about the symbiotic interactions of sea anemones and hermit crabs in temperate seas,
addressing the following issues: (1) clarify the relevant terminology, which is differently
interpreted by various authors; (2) provide a general description of the sea anemone - hermit
crab association, as most studies examine separately the species involved and not the
symbiosis as a whole; (3) assess the diversity and distribution of sea anemone - hermit crab
associations in temperate seas, also incorporating gastropod shells and their availability, which
although crucial, has been only little investigated; (4) address the behavioural patterns of both
symbionts for the establishment of the symbiosis, including as well the behavioural plasticity
of hermit crab related to shell resource utilization, and (5) report relevant information about
co-evolution of the participant species, referring to the existing hypotheses on the evolution of
the symbiosis, underlining its importance.
Email address: antonch@bio.auth.gr, Tel. +302310998901, Fax. +302310998269, Address: Chryssanthi Antoniadou
Aristotle University, School of Biology, Department of Zoology, Thessaloniki, Greece, Gr - 54124,
(Corresponding Author)
96 Chryssanthi Antoniadou, Anna-Maria Vafeiadou and Chariton Chintiroglou
Symbiosis: Meaning and Relevant Terminology Considering
the Specific Case of Sea Anemones - Hermit Crabs
In nature very few species, if any, live separated; almost all species depend on other to
gain vital resources, such as habitat, food and protection. This dependency among species has
been very early recognized from biologists under the concepts of biotic interactions and
symbiosis. The term symbiosis was coined originally by Anton de Bary in 1879 in his study
about lichens, to mean any association between different species, with the implication that the
organisms are in persistent contact, but that the relationship does not need to be advantageous
to all participants (see Douglas, 2010). Thus, according to its initial meaning, symbiosis refers
to the biotic interaction between two organisms living in close association; the latter phrase
differentiates symbionts from simply interacting species. However, this definition is rather
controversial, since the outcome of interactions can vary across a continuum from negative to
positive results, and among participant species. Moreover, the term has often been used
generically and its meaning has frequently been deviated from the original definition. The
subsequent proposition of additional definitions and the lack of agreement for a specific one
within the scientific community have further complicated the strength of this term; similar
problems can be found for many other, widely applicable, terms in the field of marine
ecology (see Dauvin et al., 2008).
After the first definition of symbiosis, very little awareness about the term, as defined
subject, existed between biologists and up to 1950s; the phenomenon has been encountered as
scattered among organisms and very little research was in progress, almost exclusively
covering terrestrial associations (see Smith, 2001 for a thorough review of symbiosis research
trends over the last century). Thereafter, and especially after 1970s, symbiosis research
advanced incorporating many topics and including major marine taxa, such as sponges, corals
and sea anemones. Symbiotic procedures are thought to be less diverse and widespread in
aquatic domain (Smith, 2001), despite the recognition of their prominent role in particular
marine ecosystems, such as coral reefs in tropics, and shallow benthic communities in
temperate seas (Grutter and Irving, 2007).
Considering all the above the first task of this study is to thoroughly revise and clarify the
relevant terminology, which is differently interpreted by various authors, focusing on the
marine domain and the specific case of interactions between closely associated sea anemones
and hermit crabs.
As Smith (2001) clearly pointed “there is still no clear and universally agreed definition
of symbiosis, even though it is 130 years after de Bary devised the term”. Currently symbiosis
is used under a wide range (Martin and Britayev, 1998) referring to all cases in which two
species live in close association (Henry, 1966), although many researchers attempted to
restrict the term to associations where partners mutually benefit (Rhode, 1981) or
alternatively and more sophisticated defined, symbiosis refers to intimate mutualism
involving direct supply of nutrients or other resources between physiologically integrated
species (Grutter and Irving, 2007). Proving benefit existence is highly problematic since, at
least in some associations, the partner’s cost surpasses any hypothetical benefit. Douglas
(1994) rejected mutual gains and suggested the acquisition of a novel metabolic capability
from one partner as the basis of symbiosis. However, this concept is complex as the gain is
strictly connected with metabolism, although practically applicable to some specific cases of
Symbiosis of Sea Anemones and Hermit Crabs in Temperate Seas 97
interactions between bacteria and plants or metazoans (e.g. symbiotic zooxanthellae and
corals or sea anemones). This fact, together with the largely unknown nature of species
interactions, hinders the general acceptance of the latter idea and enhances the generic sense
of the term.
As mentioned earlier, symbiosis constitutes a rather loose term up to date, which includes
a wide range of interactions that cover the specific cases of: (i) parasitism, i.e. when the
symbiosis is advantageous to one partner at the expense of the other, (ii) commensalism, i.e.
when the symbiosis is advantageous to one partner without harming the other, and (iii)
mutualism, i.e. when the symbiosis is reciprocally advantageous to both partners; these cases
are symbolized as follows +/-, +/0, +/+, respectively (Martin and Britayev, 1998; Bruno et al.,
2003; Patzner, 2004). Apart from parasitism which is interpreted as a negative interaction (at
least for one partnership) symbiosis is also described under the terms of facilitative or positive
interactions (Stachowicz, 2001). The latter terms are becoming of increasing applicability in
the scientific audience as they give a more precise description about the nature of species
interactions and thus, a trend to replace the more generically defined symbiosis is evolving
(Stachowicz, 2001; Grutter and Irving, 2007). A clear distinction, however, among the above
cases of symbiosis is not always evident, because many factors define the nature of these
interactions, such as the degree of association between the species and their specialization, its
necessity for the species survival, the temporal pattern, and the life stage at which interaction
occurs (Martin and Britayev, 1998). Considering all the above it seems rather reasonable to
adopt the latter authors’ opinion suggesting the use of the term symbiosis as “stepping stone
in helping to understand the real relationships in any particular association”.
Symbiosis appears to be more common in tropical marine communities (Grutter and
Irving, 2007); nevertheless, the phenomenon is widespread also in temperate seas with the
association between sea anemones and hermit crabs belonging to the most common and
widely acknowledged cases of mutualism (Williams and McDermott, 2004; Vafeiadou et al.,
2011). More specifically, each case of symbiosis, including mutualism, can be categorized as:
(i) obligate or facultative, in the first case partners may survive only in association and in the
second, while benefiting from the presence of each other, they may also survive in absence of
their partner (Boucher et al., 1982), (ii) direct or indirect, in the first case partners interact
physically and in the second they benefit from the each other’s presence without direct contact
(Boucher et al., 1982), (iii) permanent or temporary, in the first case partners are living
together during their whole life and in the second only in some phase of their life cycle
(Martin and Britayev, 1998), and (iv) monoxenic, oligoxenic or polyxenic, in the first case the
symbiont is associated with only one host, whereas in the other two cases few or several
different host species are involved, respectively (Lom, 2001); the latter category is used only
for parasitism.
Considering the particular case of symbiosis between sea anemones and hermit crabs, its
development requires the involvement of a third part, i.e. gastropod shells, which provide
both refuge for hermit crabs and substratum for the settlement of sea anemones. These
tripartite associations were assigned as ecological triangles by Ross and Sutton (1963).
Nevertheless, the term has been expanded and is currently used in the broad fields of ecology
and environmental biology to describe interactions among three biotic or abiotic parameters
(Styron, 1977; Kareiva, 1982; Xu et al., 2006). Taking into account its original description,
the limited implementation from other authors (Chintiroglou, et al. 1992; Christidis et al.,
1997), or even from the ones who suggested it (Ross 1974a, 1974b, 1979), and the doubt
98 Chryssanthi Antoniadou, Anna-Maria Vafeiadou and Chariton Chintiroglou
concerning its validity, since gastropods do not actively participate in the association although
their shells are vital for the development of the sea anemones - hermit crabs symbiosis
(Vafeiadou et al., 2011), the term ecological triangle is abandoned at the present review.
Sea Anemones - Hermit Crabs Symbiosis: A General Description
The interaction of sea anemones and hermit crabs is one of the most familiar examples of
symbiosis in temperate seas, interpreted as a typical case of mutualism. Considering
symbiosis terminology (see above), this specific case can further be described as a clear
paradigm of indirect, permanent, facultative, in most cases, mutualism. If we can expand the
use of the terms monoxenic/oligoxenic/polyxenic which so far is used for parasitism, we
assume most sea anemones as polyxenous symbionts, as they can be hosted by several
different hermit crab species; however, this term is rather species-specific (see for example the
case of the sea anemone Adamsia obvolva which associates only with the hermit crab
Sympagurus pictus as a monoxenous symbionts).
Nevertheless, much discussion around this aspect has followed due to confusion through
terms and suggestions by several authors; although sea anemone - hermit crab symbiosis had
been considered as mutualism from early studies (Roughgarden, 1975; Hazlett, 1981; Ross,
1984; Brooks, 1989), it has only recently been characterized as facultative mutualism
(Patzner, 2004; Williams and McDermott, 2004; Vafeiadou et al., 2011). With older studies
using contradictory terminology, given that an exact description of the symbiotic relationship
was missing, the kind of interaction should be re-examined, at least for some particular
species. The interaction between the sea anemone Adamsia palliata and the hermit crab
Pagurus prideaux for example had long been interpreted as a case of obligate commensalism,
before the anemone species was proved first to live alone, without any association with
hermit crabs, and second to live in association with other hermit crab species too (Ates,
1995). Even further, hermit crabs of some species may prey on their symbiotic sea anemones
under starvation, or under increased sea anemone densities (Imafuku et al., 2000). Williams
and McDermott (2004) in their review study on hermit crab symbiosis stress the difficulties
of such categorization. There are some examples of species among cnidarians in association
with hermit crabs that happen to feed on the eggs of hosts but the relationship had been
previously described as commensalism, or other cases of temporal changes in the symbiotic
nature of the relationship, i.e. switching from commensalism to mutualism or parasitism,
depending on different environmental and biological factors.
In this aspect, a general description of the sea anemone - hermit crab symbiosis is
presented below, encompassing all the relevant information included in the literature, as such
to underline the importance of symbiosis for both participant species, and for marine
ecosystems, respectively.
In the particular case of sea anemones - hermit crabs symbiosis, though, the presence of a
third, indirect participant is required: gastropod shells. They constitute the linking part of the
symbiosis, providing refuges for hermit crabs (to protect their abdomen part) and suitable
substratum for the settlement of sea anemones (Conover, 1978; Brooks, 1989). Thus, shell
availability is a crucial factor for the establishment of the symbiosis.
The development of the symbiotic interaction initiates by the detachment of sea
anemones from the substratum and their placement on gastropod shells inhabited by hermit
Symbiosis of Sea Anemones and Hermit Crabs in Temperate Seas 99
crabs. A cooperation of both symbionts is necessary for the well-establishment of the
symbiosis; however, some cases where symbiosis initiates by only one of the symbionts have
also been reported.As such, hermit crabs detach sea anemones, using tactile stimulation, and
actively transfer them on their shells (Brunelli, 1910; Cowles, 1919; Ross, 1970); in some
cases with the cooperation of the sea anemones, which loosen their connection with the
substratum to enhance their transfer (Ross, 1974a, 1974b; Lawn, 1976; McFarlane, 1976).
In particular, sea anemones are the only symbionts among cnidarians associated with
hermit crabs which are actively hosted by them and not haphazardly fixed on the shells during
larval settlement (Gusmão and Daly, 2010). In other cases, sea anemones do also transfer
themselves on shells inhabited by hermit crabs, without aid of the latter, to establish a
symbiotic relationship with them (Davenport et al., 1961; Ross, 1959, 1965; Ross and Sutton,
1961; see also section 4 for details in behavioural patterns).
The importance of symbiosis for both partners is diverse (Table 1). The hermit crab
enforces its defence to predators, gaining protection via the sea anemone nematocysts
(Brooks, 1989). As known, the main predators of hermit crabs are cephalopod molluscs (e.g.
octopus) which are not resistant to the toxins excreted by the nematocysts of cnidarians (Ross,
1967, 1971; Brooks, 1991). As a result, hermit crabs actively host sea anemones on the
gastropod shells they inhabit (Gusmão and Daly, 2010), evolving a whole behaviour towards
the establishment of the symbiosis, including gathering increased number of anemones under
predator pressure, or stealing anemones from other crabs (Ross and Boletzky, 1979; see also
section 4 for details in behavioural patterns).
Table 1. Overview of the advantages and disadvantages of symbiosis for sea anemones
and hermit crabs
Hermit crabs Sea anemones
Advantages
Protection from predators
Protection from predators
Increased shell strength
Substratum availability
Decreased energetic costs of
changing/searching for shells
Increased feeding capacity
(increased food resource
exploitation)
Prey on symbionts in case of
starvation (only some species)
Increased dispersal
Direct feeding by their host
Disadvantages
Increased energetic costs of carrying
heavier shells
Predation by the host
(only in specific cases)
Increased intra- and inter-specific
competition
Additional benefits for the hermit crab may also derive from expansion of the anemone
over the shell, forming a so called “living cloak” inhabited by the hermit crab, strengthening
the shell in this way and thus, the crab’s structural defence (Faurot, 1910; Doumenc, 1975;
Ross, 1984).Furthermore, sea anemones of the genus Adamsia form a chitin shell-like
structure, known as carcinoecium, which probably gives further protection to the hermit crab
while it grows, without the need of switching shells (Dunn et al., 1980; Gusmão and Daly
100 Chryssanthi Antoniadou, Anna-Maria Vafeiadou and Chariton Chintiroglou
2010), as it has also been reported for the genus Stylobates in tropical seas (Dunn and
Liberman, 1983; Fautin, 1987, 1992).
Protection against predators is a benefit for the sea anemones too, since symbiosis with
hermit crabs ensures their mobility, in addition with their active defence by hermit crabs
against animals which endeavour to prey on their symbiotic sea anemones (Brooks and
Gwaltney, 1993). Moreover, sea anemones increase their dispersal capability via hermit crab
mobility (Balss, 1924), gaining suitable substrata for their settlement (Nyblade, 1966;
Riemann-Zürneck, 1994).
Increased exploitation of food sources by sea anemones has also been reported as a
consequence of hermit crab mobility. For example, the sea anemones of the species Calliactis
parasitica when settled on stable substrata (e.g. rocky) are able to exploit food supplies from
only a limited area (ca. 0.5 m2/day), whereas they are able to move up to 20 m2/day due to
symbiosis, thus, increasing their feeding potential (Stachowitsch 1979, 1980). Increased food
supplies for the sea anemones can also derive from the food residuals of hermit crabs (Ross,
1960; Stachowitsch, 1979, 1980; Chintiroglou and Koukouras, 1991; Fautin, 1992). The exact
position the sea anemones are placed on the shell has also proved to be important, as the
closer they are to the shell aperture, and thus to the hermit crab, the more they benefit during
its feeding (Balasch et al., 1977; Brooks, 1989); however, the sea anemone is often placed on
the top of the shell, which may potentially increase their accessibility to suspended particulate
organic matter from the water column. The anemones are usually oriented with their mouth
below the shell aperture, to increase protection and allow their host to avoid changing shells
when it grows (Ross, 1974b). Direct feeding of the sea anemones by their associated hermit
crabs has also been mentioned in the literature (e.g. Wortley, 1863; Fox, 1965), being though
a rather controversial possibility (Ross, 1974a).
Apart from the positive outcomes for both hermit crabs and sea anemones, the symbiosis
has a great importance for biodiversity in marine benthic ecosystems, too. It is broadly known
that gastropod shells that are inhabited by hermit crabs host also a variety of other organisms
(epibiotic and endolithic), thus, formatting small biotic communities (Conover, 1979;
Stachowitsch, 1980; Hazlett, 1984; McClintock, 1985; Caruso et al., 2003; Turra, 2003;
Williams and McDermott, 2004).
Although gastropod abundance and distribution are important for the establishment of
such micro-communities (McLean, 1983), hermit crabs have also a key-role. They prolong
the presence of empty gastropod shells on the sea bottom by occupying them, avoiding their
burial in soft sediments in the opposite situation (Conover, 1975, 1979), and thus, the shells
can be available as substrata and colonized by a great diversity of organisms (McLean, 1983;
Williams and McDermott, 2004). As a result, the abundance and distribution of hermit crabs,
and the selection of shells, affect the abundance and distribution of a variety of organisms,
which use the shells as micro-habitats. With respect to this function of hermit crabs, they had
been characterized as allogenic ecosystem engineers, which are defined as these organisms
able to transform biotic or abiotic substances from one physical situation to another (Jones et
al., 1997; Gutiérrez et al., 2003; Jones and Gutiérrez, 2007).
Symbiosis of Sea Anemones and Hermit Crabs in Temperate Seas 101
Sea Anemones - Hermit Crabs Symbiosis: Diversity and
Distribution Patterns
In the comprehensive review of hermit crab associated species, Williams and Mc
Dermott (2004) reported 37 species of sea anemones living as symbionts with hermit crabs,
whereas Gusmão (2010) reduced the number of associate sea anemone species to 32.
According to our revision a total of 35 valid sea anemone species belonging to 14 genera
(Adamsia, Aiptasia, Antholoba, Calliactis, Carcinactis, Gonactinia, Hormathia, Neoaiptasia,
Paracalliactis, Paranthus, Sagartiogeton, Sagartiomorphe, Stylobates, Verrillactis) and
seven families (Actiniidae, Actinostolidae, Aiptasiidae, Gonactiniidae, Hormathiidae,
Sagartiidae, Sagartiomorphidae) have been reported as hermit crab symbionts (see Table 2).
The vast majority of those species belong to Hormathiidae family (22 valid species), whereas
other three sea anemone species are under uncertain taxonomic status (i.e. Paracalliactis
mediterranea, P. japonica and Verrillactis guttata). Hermit crabs of 41 species hosted sea
anemones (Table 2); those species belong to 15 genera (Anapagurus, Catapaguroides,
Catapagurus, Clibanarius, Dardanus, Diacanthurus, Diogenes, Lophopagurus,
Micropagurus, Oncopagurus, Paguristes, Pagurus, Parapagurus, Petrochirus, Sympagurus)
and three families (Diogenidae, Paguridae, Parapaguridae).
Overall, 68 different types of sea anemones - hermit crabs symbiosis, have been reported
in the literature up to date. The hermit crab Dardanus arrosor appeared to host the larger
diversity of sea anemones, i.e. seven species, followed by Pagurus alatus, P. bernhardus, P.
cuanensis and Paguristes eremita that were found in symbiosis, each, with three different
anemone species. The sea anemone Calliactis polypus is involved in symbiosis with eight
hermit crab species, followed by C. parasitica that has been found on the shells of seven
hermit crabs; C. tricolor and Adamsia palliata are associated with six hermit crabs, and
Verrillactis paguri with five. The rest hermit crab and sea anemone species appeared to be
more specialized as they have been reported associated with one or two different species.
Considering diversity of shell utilization, whether hermit crabs prefer the shells of
specific gastropod species remains unknown (see also Ates et al., 2007), and in most cases the
abundance of shells seems to be the major factor influencing shell utilization (Kellogg, 1976;
Barnes, 1999). Vafeiadou et al. (2011) studying shell resource utilization of hermit crab
species in symbiosis with Calliactis parasitica in the Mediterranean, reported that 53
different shells are occupied by the four hermit crabs: Dardanus arrosor, D. calidus, Pagurus
excavatus and Paguristes eremita, associated with C. parasitica (Figure 1). All crabs utilized
a large variety of discarded shells, although a preference for specific gastropods has also been
suggested, at least for some species.For example Pagurus excavatus inhabits 17 different
species, but in most cases it was found in Bolinus brandaris and Galeodea echinophora
shells, while Paguristes eremita most frequently occupied Hexaplex trunculus and B.
brandaris shells, although it is occasionally found in the shells of other 33 gastropod species
(Vafeiadou et al., 2011). A selective behaviour of hermit crabs towards the size of shells has
been suggested (Childress, 1972; Chintiroglou et al., 1992; Wada et al., 1997; Côté et al.,
1998; Caruso et al., 2003); nevertheless, selectivity to shells of certain gastropod species
remains doubtful and further research is necessary to elucidate relevant patterns.
102 Chryssanthi Antoniadou, Anna-Maria Vafeiadou and Chariton Chintiroglou
Table 2. Taxonomic list and temperate zone distribution of sea anemone and hermit
crab species reported to live in symbiosis; ? Refers to species under uncertain taxonomic
status (participant species data based on Williams and Mc Dermott, 2004; taxonomic
status checked with World Register of Marine Species; distribution data based on
Fautin, 2008 and Ocean Biogeographic Information System)
Sea anemone species Temperate zone distribution
Actiniidae
Stylobates aeneus Dall, 1903
Stylobates cancrisocia (Carlgren, 1928)
Indian
Stylobates loisetteae Fautin, 1987
Actinostolidae
Antholoba achates (Drayton in Dana, 1846)
SW Atlantic, SE SW Pacific
Paranthus rapiformis (Le Sueur, 1817)
NW SW Atlantic
Aiptasiidae
Aiptasia sp.
Neoaiptasia commensali Parulekar, 1969
Gonactiniidae
Gonactinia prolifera (Sars, 1835)
NE NW Atlantic, SE Pacific
Hormathiidae
Adamsia obvolva Dally et al., 2004
NW Atlantic
Adamsia palliata (Muller 1776)
NE Atlantic, Mediterranean
Adamsia sociabilis Verrill, 1882
NW Atlantic
Calliactis algoaensis Carlgren 1938
Indian
Calliactis argentacolorata Pei, 1996
Calliactis conchiola Parry 1952
SW Pacific
Calliactis japonica Carlgren, 1928
NW Pacific
Calliactis parasitica (Couch, 1842)
NE Atlantic, Mediterranean
Calliactis polypores Pei, 1996
NW Pacific
Calliactis polypus (Forskal, 1775)
NW Atlantic, NW SW NE SE Pacific,
Indian
Calliactis reticulata Stephenson, 1918
SW Atlantic
Calliactis tricolor (Le Sueur 1817)
NW SW Atlantic
Calliactis variegata Verrill, 1869
SE Pacific
Calliactis xishaensis Pei, 1996
Hormathia coronata (Gosse, 1858)
NE Atlantic, Mediterranean, Indian
Paracalliactis consors (Verrill, 1882)
N Atlantic
Paracalliactis lacazei Dechance and Dufaure, 1959
Mediterranean
Paracalliactis mediterranea Ross and Zamponi,
1982?
Mediterranean
Paracalliactis michaelsarsi Carlgren 1928
NE NW Atlantic
Paracalliactis japonica Carlgren 1928 ?
NW Pacific
Paracalliactis rosea Hand 1976
SW Pacific
Paracalliactis sinica Pei, 1982
NW Pacific
Paracalliactis stephensoni Carlgren 1928
NE Atlantic
Paracalliactis valdiviae Carlgren 1928
Indian
Symbiosis of Sea Anemones and Hermit Crabs in Temperate Seas 103
Sea anemone species
Temperate zone distribution
Sagartiidae
Carcinactis dolosa Riemann-Zurneck, 1975
SW Atlantic
Carcinactis ichikawai Uchida, 1960
NW Pacific
Sagartiogeton undatus (Muller, 1788)
NE Atlantic, Mediterranean
Verrillactis guttata (Agassiz in Verrill, 1864)?
N Atlantic
Verrillactis paguri (Verrill, 1869)
NW SE Pacific, Indian
Sagartiomorphidae
Sagartiomorphe carlgreni Kwietniewski, 1898
SW NW Pacific
Hermit crab species
Diogenidae
Clibanarius erythropus (Latreillei, 1818)
NE Atlantic, Mediterranean
Clibanarius padavensis De Mann, 1888
Clibanarius vittatus (Bosc, 1802)
NW SW Atlantic
Dardanus arrosor Herbst, 1796
NE SE Atlantic, Indian, Mediterranean,
NW SW Pacific
Dardanus calidus (Risso, 1827)
NE Atlantic, Mediterranean
Dardanus deformis (H. Milne Edwards, 1836)
SE SW Pacific, Indian
Dardanus impressus (De Haan, 1849)
NW Atlantic
Dardanus lagopodes (Forskal, 1775)
Dardanus pedunculatus (Herbst, 1804)
NW SW SE Pacific, Indian
Dardanus tinctor (Forskal, 1775)
Dardanus venosus (H. Milne Edwards, 1848)
NW SW Atlantic
Diogenes custos (Fabricius, 1798)
Diogenes edwardsii (De Haan, 1849)
NW Pacific
Diogenes sp.
Paguristes eremita (Linnaeus, 1767)
Mediterranean
Paguristes subpilosus (Henderson, 1888)
SW Pacific
Petrochirus diogenes (Linnaeus, 1767)
NW SW Atlantic
Paguridae
Anapagurus chiroacanthus (Lilljeborg, 1856)
NE Atlantic, Mediterranean
Anapagurus laevis (Bell, 1846)
NE Atlantic, Mediterranean
Catapaguroides fragilis (Melin, 1939)
Catapagurus sharreri A. Milne Edwards, 1880
NW Atlantic
Diacanthurus rubricatus (Henderson, 1888)
SW Pacific
Lophopagurus lacertosus (Henderson, 1888)
SE SW Pacific
Micropagurus polynesiensis (Nobili, 1906)
Pagurus alatus Fabricius, 1775
NE Atlantic, Mediterranean
Pagurus bernhardus (Linnaeus, 1758)
NW NE SW SE Atlantic
Pagurus cuanensis Bell, 1846
NW NE Atlantic, Mediterranean
Pagurus excavatus (Herbst, 1791)
Mediterranean
Pagurus forbesi Bell, 1846
NE Atlantic, Mediterranean
Pagurus impressus (Benedict, 1892)
NW Atlantic
104 Chryssanthi Antoniadou, Anna-Maria Vafeiadou and Chariton Chintiroglou
Hermit crab species
Temperate zone distribution
Pagurus longicarpus Say, 1817
NW Atlantic
Pagurus pollicaris Say, 1817
NW Atlantic
NE Atlantic, Mediterranean Indian
(A. Milne Edwards, 1880)
NW NE Atlantic
NE SE NW Atlantic, Mediterranean, Indian, NE NW
Pacific
Indian
SW SE Atlantic, Indian, SE SW Pacific
SE SW Pacific
NW Atlantic
SE SW Pacific, Indian
Figure 1. Sea anemone hermit crab symbiosis: specimens of the sea anemone Calliactis parasitica in
symbiosis with the hermit crab Pagurus excavatus, in Thermaikos Gulf (north Aegean Sea) using a
Bolinus brandaris shell (above) and with Dardanus calidus, in Sifnos Island (Cyclades plateau, South
Aegean Sea) using a Phalium granulatum shell (below).
Symbiosis of Sea Anemones and Hermit Crabs in Temperate Seas 105
N
S
E
W
Mediterranean
N
S
East Pacific
W
Indi an
stress val ue: 0
Atlantic
Pacific
Figure 2. Temperate zone distribution of sea anemone - hermit crab symbiosis types as visualized by
applying multi-dimensional scaling ordination via Bray-Curtis distances on presence absence data
(N = north, S = south, E = east, W = west).
Out of the 68 different types of sea anemones - hermit crabs symbiosis, 53 are distributed
in temperate zones. Their biogeographic distribution, as visualized applying non-metric
multidimensional scaling ordination via Bray-Curtis distances on presence absence data
(Figure 2), revealed the increased affinity in symbiotic types’ composition between: (i) the
Mediterranean and the Atlantic and (ii) within the Pacific Ocean with the exception of its
eastern part, where very few such associations have been reported. The symbiotic types
reported from the Indian Ocean (data from tropical zone excluded from the analysis) showed
increased similarity with the Pacific group, although to a smaller degree (Figure 2).
These results conform to the findings of Ross (1974a) which documented that sea
anemone - hermit crab symbiosis types cover mainly the circumtropical zone, extending also
to some warm-temperate areas such as the Mediterranean Sea, and differ in their qualitative
structure according to the geographic region in a global scale; accordingly the author claimed
the existence of different zoogeographic zones. An analogous pattern has been revealed in a
much smaller spatial scale, i.e. over the Aegean Sea (Vafeiadou et al., 2011). According to
the latter authors, the symbiotic types, even when only one sea anemone species has been
considered, followed a consistent pattern of spatial distribution according to the geographic
areas studied. After considering the diversity of shell utilisation as well, a similar pattern
emerged, concurring to the recently proposed latitudinal cline of shell resource utilisation by
hermit crabs (Barnes, 2003). Therefore, this trend in the distribution of sea anemones - hermit
crabs symbiosis types may be useful in biogeography studies.
106 Chryssanthi Antoniadou, Anna-Maria Vafeiadou and Chariton Chintiroglou
Sea Anemones - Hermit Crabs Symbiosis: Manifested
Behavioural Patterns
How beneficial symbiosis is for both sea anemones and hermit crabs has been already
discussed (see section 2, general description of the symbiosis); nevertheless, specific
behavioural patterns promoting their association exhibited by both symbionts, and verify once
again its importance. Since the development of a symbiotic relationship depends on specific
actions driven by particular behaviours of the participant species, behavioural patterns
exhibited by sea anemones and hermit crabs (summarized in Table 3) are reported in this part,
giving also examples of specific cases.
As aforementioned, the establishment of the sea anemones - hermit crabs symbiotic
interaction is primarily based on hermit crabs for they detach sea anemones from their
substrata, using tactile stimulation, and place them on the gastropod shells they inhabit
(Brunelli, 1910; Cowles, 1919; Ross, 1970). Hermit crabs of the species Dardanus arrosor,
known to host sea anemones of the species Calliactis parasitica in temperate seas, move the
anemones by manipulating their base little by little, a behaviour performed, though, only by
female individuals (Ross, 1967). Prior species recognition and selectivity by hermit crabs
towards particular sea anemone species has been mentioned in the literature (Ross, 1974b;
Brooks and Mariscal, 1986); however, such behaviour has not so far been confirmed by
experimental results. On the other extreme, the hermit crab species Pagurus alatus does not
facilitate the anemone transfer and settlement on the shell (Ross and Zamponi, 1982).
Table 3. Synopsis of the main behavioural patterns manifested by sea anemones and
hermit crabs to enhance symbiosis; (?) refers to uncertain behaviours
Hermit crabs
Sea anemones
Detachment / transfer of sea anemones (using tactile
stimulation)
Facilitation of its detachment by
the hermit crab
Preference towards particular sea anemone species (?)
Active transfer on the shell without
the participation of the host
Placement of increased number of sea anemones on the
shell under predator presence
Preference towards shells with increased number of sea
anemones under predation stress
Arrangement of sea anemones on the shell (balance,
predation stress)
Symmetric placement of sea anemones on the shell (?)
Intra- and inter-specific competition for sea anemones
Plasticity on shell selectivity patterns (depending on
various factors and previous experience)
Intra- and inter-specific competition for gastropod
shells
Active participation of the sea anemones during their detachment from the substratum by
the hermit crabs is one of the most interesting behaviours in the symbiosis (Balasch and
Mengual, 1974; Ross and Boletzky, 1979; Bach and Herrnkind, 1980). It has been reported
Symbiosis of Sea Anemones and Hermit Crabs in Temperate Seas 107
that sea anemones are loosening their connection with the substratum during their
manipulation by hermit crabs to enhance their transfer on the shells (Ross, 1974b; Lawn,
1976; McFarlane, 1976). According to Ross (1979), although sea anemones move themselves
from rocky substrata to attach on gastropod shells, they do not seem to actively change their
shell substratum for another, but only when getting transferred by their host crab.
Nevertheless, experiments revealed that they may transfer themselves by tentacle adhesion
(followed by pedal disc attachment) to a shell inhabited by a hermit crab without the active
participation of it under conditions of high predation risk for the latter, e.g. upon perception
of mollusc presence (Davenport et al., 1961; Ross, 1959, 1965; Ross and Sutton, 1961). This
particular behaviour has been observed in four species of the genera Calliactis and
Paracalliactis (Gusmão and Daly, 2010) and has been characterized as one of the most
complex behaviours of cnidarians (Ross, 1974b).
The perception of predator presence has as a result the active behaviour of hermit crabs
too (Balasch and Mengual, 1974; Ross and Boletzky, 1979), which prefer to inhabit shells
with more sea anemones, and/or place more sea anemones on their shell under increased
density of predators, in comparison with predator absence circumstances (Balasch and
Mengual, 1974; Ross and Boletzky, 1979; Brooks and Mariscal, 1986; Brooks, 1989). The
placement of sea anemones on the shell is also influenced by predation stress, with anemones
being typically placed close to the aperture of the shell, a key-position for better protection
(Cutress and Ross, 1969; Brooks, 1988, 1991); though, the balance of the crab is first and
foremost considered, with anemones being arranged in accordance with the center of gravity
of the shells (Balasch et al., 1977; Brooks, 1989; Caruso et al., 2003).
Preference towards a symmetric placement of the sea anemones by hermit crabs has also
been assumed, in particular for the species Dardanus pedunculatus living in symbiosis with
Calliactis tricolor in reef ecosystems (Giraud, 2011). The author mentioned a consistent
pattern, probably related to the balance of the shell, although this specific study does not use
anemone weight distribution data. Additionally, this behaviour of non-random but
symmetrical anemone placement by the hermit crab could be related to shell cover with sea
anemones in a way to maximize protection, without necessarily needing a large number of
them (Giraud, 2011) and thus, reducing the energy costs of the crab by carrying a heavier
shell. Another remarkable behavioural pattern manifested by hermit crabs is their strategy for
gathering more sea anemones, including intra- and inter-specific competition. Accordingly,
they steal sea anemones from the shells of other hermit crabs (Mainardi and Rossi, 1969;
Ross, 1974b, 1979), which sometimes might even be of the same species (Giraud, 2011). As
an example, the hermit crab species Dardanus arrosor appears to dominate over Pagurus
excavatus or Paguristes eremita when they occur at the same habitat, stealing their symbiotic
anemones as a result of antagonism (Ross, 1979). The size of both the hermit crab (and in
particular the size of its cheliped) and its shell are considered as the main factors for its
competitive dominance (Giraud, 2011; Yasuda, 2011; Yoshino, 2011), giving the advantage to
larger individuals and/or species.
In spite of its indirect benefit, gastropod shell selectivity by hermit crabs is a very
important aspect for the well-establishment of the symbiosis, and should not be neglected
from the behavioural patterns manifested by hermit crabs. Numerous studies have focused on
shell selection behaviours of hermit crabs (e.g. Reese, 1962; Balasch and Cuadras, 1976;
Fotheringham, 1976; Hazlett, 1978, 1984, 1992; Abrams, 1982; Dowds and Elwood, 1983,
1985; McClintock, 1985; Liszka and Underwood, 1990; Wada et al., 1997; Côté et al., 1998;
Hahn, 1998; Osorno et al., 1998). Experimental studies suggest gastropod mass, weight, total
size (McClintock, 1985) and protective ability (see Reese, 1962), as the main factors that
influence the selection by hermit crabs (Buckley and Ebersole, 1994). Intrinsic shell
properties (e.g. shape, spines, center of gravity, shell axis) are other important features in
shell selection by hermit crabs (Reese, 1963; Caruso and Chemello, 2009), influencing also
the placement of sea anemones on the shell (Ross and Boletzky, 1979; Brooks, 1989).
According to Wada et al. (1997), the preferential shell size for a hermit crab depends on
the growth rate of the latter. The same authors showed that hermit crabs tend to occupy larger
shells in proportion with their size in the following cases: (i) when shell resource availability
is restricted, (ii) when they are going to change their exoskeleton, and (iii) when the growth of
their body size after the next moulting phase is expected to be large. On the contrary, the size
of the gastropod shell may influence the rate of the hermit crab growth (Wada et al., 1997), a
fact which illustrates the complexity of these associations. For instance, by selecting an
oversized shell in proportion to its size, the hermit crab may on the one hand delay its
searching for a larger shell during its growth, as to assure its further growth and reproduction
(Childress, 1972; Wada et al., 1997; Côté et al., 1998), and on the other hand gain some
advantage over antagonists; however, the energy cost is much higher. Occupying a shell that
is too large could negatively affect growth and fecundity of the crab and its ability to protect
itself from predators (Vance, 1972; Bertness, 1981; Elwood et al., 1995). Hermit crabs seem
to select suitable shells not only with respect to their size but also regarding the
environmental conditions, as for instance the strength of marine currents, showing a
preference towards stronger/heavier shells under strong current conditions (Hahn, 1998),
balancing the energetic constraints of carrying a heavier shell by increasing their protection.
Among the most important factors affecting the choice of an adequate shell by hermit
crabs should also be considered their previous experience on shell selection, beginning from
the early stage of their life (Gilchrist, 1985; Hazlett, 1992; Hahn, 1998; Gherardi, 2006). The
preference hermit crabs show towards shells of specific gastropod species has been also
discussed to be related to such previous experience (Reese, 1963; Elwood et al., 1979;
Borjesson and Szelistowski, 1989). According to Hazlett (1992), individual hermit crabs can
also adjust their preferences on shell size/type depending on recent shell availability
experience. In spite of the importance of species-specific selectivity, whether such behaviours
are typical, or exhibited only by some hermit crab species, or even only in particular cases
related with shell availability, is very hard to be explicitly demonstrated, and thus remain
uncertain.
An exceptional behaviour of hermit crabs, under conditions of limited shell resources,
includes their fighting for a more suitable (better-fitting) gastropod shell than they already
have (Abrams, 1982; Dowds and Elwood, 1983, 1985; Gherardi, 2006). These fights seem to
either benefit both antagonists, as at the end they both gain a better shell than what they
initially had, or only the stronger crab (Hazlett, 1978; Abrams, 1982). As a result of these
competitions, or possibly of the lack of previous experience in shell selection, smaller hermit
crabs usually end up carrying less suitable shells. The ability of larger crabs to obtain more
suitable shells creates a pressure over smaller individuals to inhabit the remaining ones,
without the possibility of selection; this behaviour is considered indicative of the crabs’ ”high
social status”, according to Balasch and Cuadras (1976).
Analogous behaviours have been confirmed by examining the biometric relationships
between hermit crab weight and shell weight or total sea anemone biomass, for the species D.
Symbiosis of Sea Anemones and Hermit Crabs in Temperate Seas 109
calidus, D. arrosor and P. excavatus in symbiosis with C. parasitica in the Aegean Sea, SE
Mediterranean (Vafeiadou et al., 2011). The results of this study revealed that smaller hermit
crabs carry heavier shells and increased anemone biomass in proportion to their weight.
Analogous observations have been previously reported by two other studies (Balasch and
Cuadras, 1976; Chintiroglou et al., 1992) which examined the biometric relationships
between the shell and the symbionts, referred as biometric indicators (e.g. shell weight / crab
weight, shell and anemone weight / crab weight). Such biometric relationships are used to
describe the ability of the crab to carry its shell and the latter’s protective capacity, and their
application, at the very end, can give an approximation of the functionality of the symbiosis.
Sea Anemones - Hermit Crabs Symbiosis: Co-Evolution
of the Participant Species
Reciprocal altruism is among the first theories proposed to explain the evolution of
mutualism; such an interaction can be develop and maintained when individuals interact by
providing benefit to another in the expectation of future reciprocation, as in the case of marine
cleaning behaviour (Trivers, 1971). Reciprocal altruism has been formalized in the iterated
Prisoner’s Dilemma game (two individuals that can defect or cooperate, receive a high payoff
from defection independently of partner’s behaviour but receive higher payoff if they
cooperate than if both defect). Thereafter, other approaches also emerged, including by-
product mutualism (partners act selfishly but a benefit results from their behaviour),
pseudoreciprocity (at least one partner invests to cooperation), and biological market theory
(partners exchange goods or commodities but differ in the degree of controlling theme); for
details on above concepts see Grutter and Irving (2007).
Sea anemones - hermit crabs mutualistic symbiosis is characterized by increased
complexity being affected by a great variety of factors (e.g. shell resource availability,
predation, behavioural patterns), as thoroughly discussed in previous sections. The
development of the symbiosis depends on both members, as aforementioned (see previous
section), with both sea anemones and hermit crabs exhibiting behavioural patterns enhancing
their symbiosis. Therefore, their interaction constitutes a model case to examine species co-
evolution under symbiosis, and in particular under mutualism.
Evolutionary aspects of hermit crab symbiotic interactions have been thoroughly
investigated by Williams and Dermott (2004). According to the latter authors, and despite the
poor representation of hermit crab exoskeletons in the fossil records, hermit crabs seem to
have provided a new niche for epibiotic organisms in marine ecosystem during the middle
Jurassic (Walker, 1992). Shell resource utilization by hermit crabs has been hypothesized to
develop initially for refuge and protection of their abdomen which became decalcified when
posterior pereopods and uropods were modified to fit the animal in shells and pleopods were
placed on one side to maximize utilization of gastropod lumen during reproduction
(McLaughlin, 1983).
The knowledge on the shared evolutionary history of sea anemones and hermit crabs
remains limited and it is mostly based on behavioural patterns followed by the symbionts.
Ross (1974a, 1983) in his pioneer work of sea anemone - hermit crab symbiosis
110 Chryssanthi Antoniadou, Anna-Maria Vafeiadou and Chariton Chintiroglou
comprehensively studied evolutionary aspects, tried to elucidate possible drivers and
hypothesized that the symbiosis evolved independently multiple times.
This latter hypothesis has been recently supported by molecular data presented by
Gusmão and Daly (2010) who provided strong evidences of at least two independent origins
of the sea anemones - hermit crab symbiosis, by constructing a phylogenetic tree of the sea
anemone family Hormathiidae (a family that includes the vast majority of sea anemone
genera having symbiotic interactions with hermit crabs).
Moreover, the widely accepted idea of close evolutionary relation among sea anemone
genera symbiotic with hermit crabs, which has been assumed on the basis of common
morphological and behavioral patterns, has been currently rejected on the basis of
phylogenetic data; monophyly in the origin of the three symbiotic with hermit crabs sea
anemone genera examined, i.e. Calliactis, Adamsia and Paracalliactis, has not been
supported but evidences of paraphyly emerged (Gusmão and Daly, 2010). Accordingly, the
reported similarities in morphology and behaviour of some sea anemone genera forming
symbiotic interactions with hermit crabs is not due to shared evolutionary history but due to
the necessary ways for the development and maintenance of symbiosis, as explicitly stated by
Gusmão and Daly (2010).
Two main hypotheses have been suggested by Ross (1974a) to explain possible leading
factors to the development of the sea anemones - hermit crabs symbiosis: (i) the “crab-driven”
and (ii) the “shell-response” hypotheses which are driven by the behaviour of hermit crab and
sea anemone, respectively, and have been subsequently adopted and analysed by other
authors (Williams and Dermott, 2004; Gusmão and Daly, 2010).
According to the first hypothesis the initial establishment of the symbiosis is founded on
hermit crabs behaviour of placing sea anemones on their residence shells to be protected, i.e.
hidden from predators by camouflage, which, however, evolved afterwards to an actual
mechanism of defence. Under this hypothesis a clear benefit emerges for the hermit crab
increasing its fitness (Gusmão and Daly, 2010). According to the second hypothesis the
development of the symbiosis is based on the sea anemone behaviour of shell mounting. In
this case sea anemones firstly settled on living gastropod shells and later started also to utilize
shells occupied by hermit crabs as the settlement of the anemone is stimulated by a shell
factor stronger on alive than on discarded gastropod shells. Sea anemones, besides gaining
novel habitat, benefit by transportation; thus settlement behaviour reinforced toward shells
occupied by hermit crabs, since they are much more mobile than gastropods.
The most important evidence supporting the first hypothesis is that in most cases the
symbiosis of sea anemones with a hermit crab is initiated under the activity of the crab, while
sea anemones are more frequently found on shells occupied by crabs than on living
gastropods, even in areas with dense gastropod populations. In favor of the second hypothesis
is the exclusive presence of some anemones on living gastropods, such as the species
Allantactis parasitica and Hormanthia digitata, the ability of some other anemones to
actively move on gastropod shells, and the equal presence of some other species, e.g.
Calliactis conchiola, on both living gastropods and shells occupied by hermit crabs (Hand,
1975). Whatever was the initial behavioural pattern stimulating the establishment of sea
anemones - hermit crabs symbiosis, both patterns positively responded. Hermit crabs, after
having their residence shells being occupied by sea anemones, started to benefit under their
protection against predators, and evolved a specialized behaviour of actively enhancing
anemone colonization of their shells. Sea anemones, after being picked up by the hermit crab,
Symbiosis of Sea Anemones and Hermit Crabs in Temperate Seas 111
started to benefit from transportation, and evolved a positive respond to their stimulation by
the crab, as Ross (1974b) showed with manipulative laboratory experiments (i.e. only those
anemones that were previously symbiotic with hermit crabs responded to tactile stimulation
by the latter). Overall, the limited number of sea anemones living on gastropods or inactive
crabs (Gusmão and Daly, 2010) and the very strong pattern manifested by several hermit
crabs of stealing sea anemones from other ones (Ross, 1979), argue against the “shell-
response” hypothesis, which however, has been preferred to some extent by Ross (1974a).
Sea Anemones - Hermit Crabs Symbiosis: Summarized
Conclusive Remarks
The sea anemones - hermit crabs symbiosis represents a clear example of mutualism, as it
has reciprocal advantages for both symbionts. The partners’ interaction is characterized by
increased complexity as the establishment of the symbiosis depends on a large variety of
factors such as shell resource availability, predation pressure and environmental constraints,
and involves the cooperation of both participants in most cases. Well-developed behavioural
patterns exhibited by both symbionts, including from the sea anemones’ active transfer on
shells inhabited by hermit crabs to the behavioural plasticity of crabs in view of shell
utilization and gathering of sea anemones, determine the development of the symbiosis and
confirm its importance for both participants, making them excellent models to examine
species co-evolution under a mutual symbiotic context. Several species of sea anemones and
hermit crabs frequently form symbiotic interactions in temperate marine environments
providing benefits, not only to the directly involved partners, but also to other organisms,
which colonize this complex biotic formation. Thus, through the intermingle processes of
epibiosis and ecosystem engineering, sea anemones - hermit crabs symbiosis contribute to the
diversity of marine benthic ecosystems by supporting diverse micro-communities.
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Reviewed by: Dimitris Vafidis, Department of Ichthyology and Aquatic Environment,
School of Agricultural Sciences, University of Thessaly, Nea Ionia, Magnesia, Greece.
... Many species of hermit crabs are known to carry symbiotic sea anemones on the external surfaces of the shells they inhabit or on their chelipeds (at least 41 species, 15 genera, 3 families of hermit crabs; at least 35 species, 14 genera, 7 families of sea anemones; Williams & MacDermott, 2004;Antoniadou et al., 2013). The benefits for host hermit crabs include protection from predators, such as cephalopods and fish, by the nematocysts of sea anemones (Ross, 1971;Balasch & Mengual, 1973;Ross & Boletzky, 1979;McLean, 1983) and use of the sea anemones as emergency food (Imafuku et al., 2000). ...
... The symbiotic sea anemones also benefit from their association with hermit crabs in the form of access to food resources (Stachowitsch, 1979(Stachowitsch, , 1980, ensured substratum availability (Conover, 1979;Brooks, 1989), protection from predators, and increased dispersal (Balss, 1924;Jonsson et al., 2001;McLean & Mariscal, 1973). These reciprocal benefits have identified these relationships as mutualism (Antoniadou et al., 2013). ...
... Another important finding in this study is the high recognition ability of the hermit crabs. Other symbiotic sea anemone species are attached to the dorsal surface of the gastropod shell, the aperture of the shell, or the lateral surface of the major cheliped of hermit crabs (Antoniadou et al., 2013). However, the present study has clearly shown that the hermit crab recognized the site at which the sea anemone Verrillactis sp. ...
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