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Sea Anemones and Anemonefish: A Match Made in Heaven

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Sea anemones are amongst the most venomous organisms on earth and yet there are species of fish and crustacea that are known to tolerate anemone venoms and live in association with them in a mutually beneficial relationship. One of natures most compelling displays of symbiotic behavior is found in the relationship between anemonefish and their sea anemone host. This relationship was first described more than a century ago and despite it being widely studied since, our understanding of the evolution of the relationship and the mechanisms and behaviors involved remains shrouded in mystery. Anemonefish (Family: Pomacentridae) comprise of a distinct group of 28 species that are able to live within sea anemones. Despite the large diversity of anemones in the tropics, only ten species are suitable as hosts for anemonefish. Within these species, only certain pairs of anemone and anemonefish are compatible and found in the wild together. This relationship is obligatory for the fish and in some cases for the anemone, meaning that the symbionts are entirely or heavily dependent on each other for survival. Symbioses between the two groups provide the following benefits: mutual protection from predators, an exchange of nutrients, improved reproductive and lifetime fitness. While past studies have explored the different patterns of host species that fish use and multiple authors have examined the mechanisms involved in protecting fish from anemone venom, how fish acquire immunity from the anemone’s stinging tentacles and why only certain anemone species are found associated with some anemonefish more often than others still remains uncertain.
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425© Springer International Publishing Switzerland 2016
S. Goffredo, Z. Dubinsky (eds.), The Cnidaria, Past, Present and Future, DOI 10.1007/978-3-319-31305-4_27
Sea Anemones and Anemonefish:
A Match Made in Heaven
Karen Burke da Silva and Anita Nedosyko
Abstract
Sea anemones are amongst the most venomous organisms on earth and yet there are species
of fi sh and crustacea that are known to tolerate anemone venoms and live in association
with them in a mutually benefi cial relationship. One of natures most compelling displays of
symbiotic behavior is found in the relationship between anemonefi sh and their sea anemone
host. This relationship was fi rst described more than a century ago and despite it being
widely studied since, our understanding of the evolution of the relationship and the mecha-
nisms and behaviors involved remains shrouded in mystery. Anemonefi sh (Family:
Pomacentridae) comprise of a distinct group of 28 species that are able to live within sea
anemones. Despite the large diversity of anemones in the tropics, only ten species are suit-
able as hosts for anemonefi sh. Within these species, only certain pairs of anemone and
anemonefi sh are compatible and found in the wild together. This relationship is obligatory
for the fi sh and in some cases for the anemone, meaning that the symbionts are entirely or
heavily dependent on each other for survival. Symbioses between the two groups provide
the following benefi ts: mutual protection from predators, an exchange of nutrients, improved
reproductive and lifetime fi tness. While past studies have explored the different patterns of
host species that fi sh use and multiple authors have examined the mechanisms involved in
protecting fi sh from anemone venom, how fi sh acquire immunity from the anemone’s sting-
ing tentacles and why only certain anemone species are found associated with some anem-
onefi sh more often than others still remains uncertain.
Keywords
Anemonefi sh Clownfi sh Anemone Symbiosis Mutualism
27.1 Patterns of Association
Between Anemones and Anemonefi sh
The association between sea anemones and anemonefi sh is a
classic textbook example of a mutualistic interaction where
both symbionts appear to benefi t from living with each other,
but the relationship is complex. Since its discovery by
Collingwood in 1868, biologists and aquarists alike continue
to observe these endearing little fi sh that form close bonds
with anemones on coral reefs in order to understand how
they live unharmed in the toxic environment of their host.
For apart from only a few other fi sh and crustacean species,
the venom contained in the nematocysts of anemones is toxic
enough to kill other fi sh that make contact with their tenta-
cles. What has been discovered is that out of the approximate
1,200 species of sea anemones (Actinaria) (Dalay et al.
2008 ) only ten form symbiotic relationships with anemone-
sh in the wild (Fautin and Allen
1997 ; Hobbs et al. 2013 ).
These ten ‘host’ anemone species are phylogenetically
diverse arising from three different families (Actiniidae,
K. B. da Silva (*) A. Nedosyko
School of Biological Sciences , Flinders University of South
Australia , 2100 , Adelaide 5001 , Australia
e-mail: karen.burkedasilva@fl inders.edu.au;
anita.nedosyko@fl inders.edu.au
27
426
Stichodactylidae and Thalassianthidae) and fi ve genera
( Entacmaea , Macrodactyla , Stichodactyla , Heteractis and
Cryptodendrum ) (Astakhov
2002 ). Some of these species are
more closely related than others, with three species in the
Stichodactyla genus and four species within the Heteractis
genus.
In comparison to anemones, their symbiotic anemonefi sh
are phylogenetically similar. There are currently 28 defi ned
species of anemonefi sh that have historically been divided
into two sister genera, Amphiprion and Premnas , belonging
to the subfamily Amphiprioninae (Perciformes:
Pomacentridae) (Allen 1991 ; Jang-Liaw et al. 2002 ; Hobbs
et al. 2013 ). Recent studies of nuclear and mitochondrial
DNA analysis show a monophyletic origin of anemonefi sh,
indicating the two-genus partition is incorrect (Santini and
Polacco 2006 ) and all anemonefi sh fall within the Amphiprion
genus. Although Premnas biaculeatus is morphologically
distinct with cheek spines and large body size, we agree that
it warrants re-classifi cation as an Amphiprion species (Elliott
et al. 1999 ). In addition, two known hybrids exist ( Amphiprion
leucokranos and Amphiprion thielli ) that are no longer rec-
ognized as distinct species but do hybridize naturally in the
wild (Ollerton et al. 2007 ) as well as two recently identifi ed
anemonefi sh species (A mphiprion barberi and Amphiprion
pacifi cus ) (Allen et al. 2008 , 2010 ).
Host anemones and anemonefi sh can be found throughout
the Indian Ocean and across the western Pacifi c Ocean (Fig.
27.1 ). In these locations, anemones and anemonefi shes usu-
ally occur in relatively shallow waters (<40 m) on or near
coral reefs and associated sandy bottoms (Mariscal 1970;
Dunn 1981 ; Fautin 1991 ; Fautin and Allen 1997 ) but some
host species such as Entacmaea quadricolor and Heteractis
crispa have also recently been discovered at depths of
50–65 m (Bridge et al. 2012 ). Throughout their distribution,
only certain symbiotic pairings are observed. Some host
anemones have a large number of anemonefi sh species that
they form symbiotic relationships with, whereas other host
anemone species have only a single anemonefi sh symbiont .
For example, E. quadricolor has the highest number of fi sh
associates (16 species), whereas Heteractis malu and
Cryptodendrum adhaesivum both have only a single known
anemonefi sh symbiont, Amphiprion clarkii (Fautin and
Allen 1997 ; Ollerton et al. 2007 ). Host anemones may also
vary in the number of individual sh symbionts that they
have at any given time, with some having a single resident
breeding pair and others having a breeding pair plus multiple
non-reproductive individuals . Fautin and Allen ( 1997 ) and
Ollerton et al. ( 2007 ) suggest that the variable numbers of
sh that form associations with anemones are due to differ-
ences in host quality because geographical distribution alone
does not suffi ciently explain these patterns. These different
patterns of association vary so understanding how each sym-
biont supports the other in the relationship is worth
investigation.
27.1.1 Benefi ts of This Symbiotic Relationship
Whilst the exact benefi ts of the symbiotic partnership for
both anemonefi sh and anemones continues to be explored, it
is generally agreed that the relationship for the fi sh is obli-
gate, as they are never found in the wild without a sea anem-
one host . Suggested benefi ts for the fi sh include protection
from predators (Fautin 1991 ; Wilkerson 1998 ; Buston 2003 ),
removal of external parasites (Allen 1972), nourishment
from the anemone tentacles (Allen 1972) and reproductive
benefi ts gained through the protection of eggs (Saenz-
Agudelo et al. 2011 ).
Fig. 27.1 Geographical distribution of anemone and anemonefi shes and locations where host anemone bleaching has been documented (Fautin
and Allen
1997 ; Hobbs et al. 2013 ; K. Burke da Silva unpublished data)
K.B. da Silva and A. Nedosyko
427
Host anemones benefi t by being fi ercely defended by
their anemonefi sh associates, particularly against predators
such as butterfl yfi sh (Family: Chaetodontidae) (Godwin and
Fautin 1992 ). It has also been shown that having one or two
anemonefi sh in attendance can enhance survivorship, foster
faster growth and increase asexual reproduction of host
anemones (Holbrook and Schmitt
2005 ). Holbrook and
Schmitt ( 2005 ) also found that host anemones without anem-
onefi sh suffered greater mortality than those with fi sh in
attendance. Another advantage to an anemone living with an
anemonefi sh is that fi sh oxygenate their host at night
(Szczebak et al. 2013 ) and metabolize much more rapidly
than anemones resulting in large quantities of metabolic
waste, in the form of dissolved ammonia readily available
and assimilated by their host (Roopin et al. 2008 ). Thus
anemonefi sh are a major contributor to the tness of their
cnidarian host (which also harbour photosynthetic zooxan-
thellae that use the fi sh’s ammonia to produce food that is
then taken up by the anemone) through the use of their meta-
bolic wastes (Roopin et al. 2008 ).
The specifi c fi tness advantages of living symbiotically
with another organism (e.g. increased longevity and fecun-
dity ) are diffi cult to measure and would require long term
studies which currently have yet to be undertaken. Scientists
have been unable to accurately age sea anemones with cur-
rent technology, although there are records of very long-lived
individuals living within aquaria. While Holbrook and
Schmitt ( 2005 ) found a link to increased asexual reproduc-
tion in anemones that host anemonefi sh, lifetime reproduc-
tive success has not been ascertained. Anemonefi sh also live
surprisingly long lives with predicted lifespans of more than
30 years, which is twice as long as any other damselfi sh and
up to six times longer than marine fi sh of comparable size
that live only between 5 and 10 years (Buston and Garcia
2007 ). Clearly the protection provided to anemonefi sh
through their association with host anemones and the
decreased predation risk that follows represents a life history
strategy that is highly advantageous . How the association
evolved is a question that needs to be asked next.
27.1.2 Evolution of This Unique Association
It is estimated that this partnership has likely been in exis-
tence for at least 10 million years, with the fi rst anemonefi sh
diversifying in the Central Indo-Pacifi c area (Litsios et al.
2014 ). How the relationship was established is based mostly
on speculation. The closest relative of anemonefi sh are the
damselfi sh ( Dascyllus spp ) that also associates with the same
species of host anemones . However, they tend to be outcom-
peted by anemonefi sh (Holbrook and Schmitt 2004 ) and
only form mutualistic partnerships with anemones as
juveniles . Randall and Fautin ( 2002 ) describe a number of
reef fi sh that form loose associations with anemones whereby
they spend considerable amounts of time in close proximity
of the anemone but they avoid making contact with the ten-
tacles. A move from close association followed by full con-
tact and immersion into the tentacles may have been the
evolutionary pathway that anemonefi sh undertook which
eventually gave them protection against the stinging nemato-
cysts of host anemones .
Anemonefi sh have diversifi ed through an adaptive radia-
tion process that has been driven by the symbiotic associa-
tion with anemones (Timm et al.
2008 ; Litsios et al. 2013)
and the availability of different ecological niches may have
contributed to speciation and geographic spread. As anem-
onefi sh diversifi ed and spread geographically, it is likely that
more potential host anemone species would have been
encountered and new combinations of anemone- anemonefi sh
relationships would have evolved. Over time, a larger num-
ber of different associations formed and these varying com-
binations may have shaped the evolution of anemonefi sh
(Timm et al. 2008 ; Litsios et al. 2014 ) through adaptation
that enabled them to use different species of anemones living
in different ecological niches.
The degree of specifi city in a symbiotic relationship
depends on the number of host species that an organism will
live and interact with in nature (Miyagawa 1989 ). It was
originally proposed that ancestral anemonefi sh were host
generalists, living in multiple species of host anemones
(Allen 1972; Futuyma and Moreno 1998 ). However, an anal-
ysis using molecular phylogenetics by Elliott et al. ( 1999 )
supports the hypothesis that ancestral anemonefi sh probably
lived with a very limited number of anemones and were
likely host specialists. As they spread further geographically
increasing the numbers of associations with anemones, this
would have given rise to generalists and other specialist fi sh
species with the associated morphological characteristics
and behaviours that enabled successful speciation .
An optimal host anemone toxicity range may be biologi-
cally signifi cant for the establishment of anemonefi sh and
anemone associations as the potency of anemone venom dif-
fers (Nedosyko et al. 2014 ). This may be the limiting factor
in anemonefi sh niche expansion but as shown in at least one
anemonefi sh species , A. clarkii , utilization of an anemone
species with moderately higher toxicity, as found in C.
adhaesivum , may be an adaptation that will allow this unique
symbiotic relationship to continue expanding to use more
anemone species in the wild. Hence, the mechanism by
which anemonefi sh use that enables them to live within the
toxic environment of host anemones may be the limiting fac-
tor in the number of different associations found. An under-
standing of this mechanism may help understand the
evolution and establishment of the association.
27 Sea Anemones and Anemonefi sh: A Match Made in Heaven
428
27.1.3 Mechanisms for Living Within a Toxic
Environment
Probably the most intriguing aspect of this symbiosis is that
anemonefi sh are unharmed by the otherwise lethal sting of
anemone nematocysts . Although sea anemones harbor pow-
erful venom that is composed of haemolytic activity (Lanioa
et al.
2001 ; Uechi et al. 2005 ; Nedosyko et al. 2014 ), immu-
nomodulating activities (Tytgat and Bosmans 2007 ; Pento
et al. 2011 ), neurotoxic properties (Gondran et al. 2002 ;
Nedosyko et al. 2014 ), and cardiotoxic properties (Bruhn
et al. 2011 ) that are capable of killing prey and keeping preda-
tory fi sh at bay, anemonefi sh manage to settle and live within
anemones without negative effect. Numerous studies have
sought to understand the mechanisms underlying the protec-
tive elements that allows anemonefi sh to remain unharmed
from the stinging nematocysts of the host anemones (e.g.
Caspers 1939 ; Davenport and Norris 1958 ; Mariscal 1969 ;
Mariscal 1970a , b , 1971 ; Schlichter 1975 , 1976 ; Lubbock
1980 , 1981 ; Miyagawa 1989 ; Mebs 1994 ; Elliott et al. 1994 ;
Elliott and Mariscal 1996 ). Most research has come to a gen-
eral conclusion indicating that a protective mucus coat acting
as camoufl age or as a molecular mimic prevents anemones
from recognizing anemonefi sh as being different from self
and may be responsible for not eliciting nematocyst discharge
when in contact. Interestingly, immunity from anemone tox-
icity is not necessarily innate for the fi sh. A specifi c acclima-
tion procedure is performed by anemonefi sh when making
contact with a host anemone for the fi rst time (Mariscal
1970b ). In addition, when anemonefi sh are removed from
their host and reintroduced after a given period of time they
lose their resistance and will be stung (Mariscal 1970b , pers.
obs ). They must slowly re-acclimate to the toxic environment
before reestablishing the partnership.
Not all anemonefi sh species seem to require time to re-
acclimate as Lubbock ( 1980 , 1981 ) found with A. clarkii that
were able to settle into Stichodactyla haddoni immediately.
He assumed this was due to the fi sh producing it’s own
mucus that differs signifi cantly from other non-symbiotic
shes which elicit nematocyst discharge without A. clarkiis
“special” mucus . Follow up studies by Miyagawa and Hidaka
( 1980 ) and Miyagawa ( 1989 ) also support this fi nding and
suggest that A. clarkii has an innate protection produced in
their mucus coat. However, we have observed that after a
period of 2 months without a sea anemone host A. clarkii can
be stung by a host anemone species as indicated by white
sting marks on their black skin . Elliott et al. ( 1994 ) found
that within the mucus coat, A. clarkii held anemone antigens
that were not found in individuals that were not living in
association with a host anemone , moving the argument more
toward an acquired resistance than innate. Mebs ( 1994 ) also
found that anemonefi sh can acquire resistance to a host
anemone when exposed to low concentrations of mucus
from that particular anemone species in the water. It is still
unresolved how different species of anemonefi sh manage to
live within the toxic environment of their host anemone but
it is clear that compounds within the mucus of the fi sh are
inhibiting nematocyst discharge and thus preventing the fi sh
from being harmed. The ability of an anemonefi sh to locate
and recognize a host anemone is hard to imagine and will be
discussed next.
27.1.4 Recognizing and Locating a Host
Upon hatching from the egg, anemonefi sh larvae disperse
and have a brief pelagic stage before juveniles return back to
the benthic habitat in search of a host anemone. Juvenile
anemonefi sh have an incredible ability to recognize and
locate the same host anemone species that they were born
near. The ability to recognize a natal host provides an evolu-
tionary advantage for vulnerable juveniles by enabling them
to locate a safe refuge quickly and effi ciently.
Past research has focused on the question of how newly
settling juveniles detect their host anemone (Fricke 1974 ;
Miyagawa and Hidaka 1980 ; Murata et al. 1986 ; Miyagawa
1989 ; Konno et al. 1990 ; Elliott et al. 1995 ; Arvedlund and
Nielsen 1996 ; Arvedlund et al. 1999 ; Miyagawa-Kohshima
et al. 2014 ). Their ndings indicate that smell rather than
sight enables host anemone recognition during their fi rst
encounter however, visual cues may be important to fi nd
anemones later in life (Fricke 1974 ). Anemones release
chemical cues secreted in the mucus on the tentacles and the
oral disc (Murata et al. 1986 ; Konno et al. 1990 ) which
anemonefi sh are strongly attracted to (Miyagawa 1989 ;
Miyagawa and Hidaka 1980 ; Elliott et al. 1994 ). The attrac-
tion intensifi es in the later stages of larval development ,
which refl ects the period when larvae settle into the benthic
habitat (Dixson et al. 2011 ).
Host anemone choice experiments manipulating the breed-
ing environments of anemonefi sh larvae in association with
or without an anemone indicate that innate preference
(genetic) plays a role in identifying their symbiotic host
anemone, a preference that is enhanced by imprinting
(learned) (Arvedlund and Nielsen 1996 ; Arvedlund et al.
1999 , 2000 ; Dixson et al. 2011 ; Miyagawa-Kohshima et al.
2014 ). This infl uences where females choose to lay their
eggs, preferring sites that encourage the greatest amount of
chemical release from the anemones to carry over and imprint
upon the developing embryos (Miyagawa 1989 ; Mitchell
2003 ; Arvedlund et al. 2000 ). When given a choice, larvae
show a clear innate preference for the smell of their natal
anemone species and recognize the chemical quicker if
hatched normally next to their host anemone (Miyagawa-
Kohshima et al. 2014 ). Some anemonefi sh such as A. ocellaris
can be imprinted to live within anemones that they do not
K.B. da Silva and A. Nedosyko
429
commonly associate with in the wild through early exposure
to these anemone species in a hatching aquarium. It is not
possible however to imprint Amphiprion melanopus larvae to
their non-host anemone species H . malu (Arvedlund et al.
2000 ) which suggests that anemonefi sh imprinting on host
anemones may be rather restricted.
The ecological relevance of anemone host recognition in
the laboratory however, differs when compared to anemone
host choice by anemonefi sh larvae in their natural environ-
ment. Elliott et al. ( 1995 ) found that in eld experiments
where juveniles were released near other potential host
anemone species , the following anemonefi sh species , A.
polymnus , A. perideraion , A. sandarcinos and A. crysop-
terus , were all attracted to ‘unnatural’ host anemone species.
Similarly, genetic parentage analysis relating larval recruits
to parents of a population of A. percula at Kimbe Bay, Papua
New Guinea, indicate that recruits do not preferentially
return to their natal host anemone species (Dixson et al.
2011 ). An explanation for this could be that in areas where
anemone choice is limited, larvae may settle in less preferred
host anemones when encountered or when required.
However, the distinct specialization behavior that certain
anemonefi sh species such as P. biaculeatus display suggests
that anemone host choice is more complex than just random
selection. The authors of these confl icting data suggest that
the mechanisms for host recognition may be species specifi c
and larvae may be responding to a hierarchy of innate and
imprinted cues that relate to different components of the
environment that might infl uence settlement habitat selec-
tion in the wild. Choice and acquisition of high quality host
anemones could have signifi cant effects on anemonefi sh
behavior, reproductive success and lifetime survival .
Understanding what makes a host anemone more preferred
by anemonefi sh is clearly important.
27.1.5 Host Choice and Acquisition of High
Quality Anemones
The number of anemonefi sh species that are found inhabit-
ing particular species of anemones can be found in Table
27.1 . Observed patterns of anemone usage by anemonefi sh
in the wild indicate that some anemone species are used
more often as hosts than others. More popular host anemo-
nes have been found to host up to 16 species of anemonefi sh
compared to less popular host anemones that may only have
a single anemonefi sh species symbiont . Fautin ( 1986 )
inferred from this pattern that host anemones with the high-
est number of sh symbionts such as E . quadricolor must be
more desirable and preferred over others.
Hypotheses explaining the different patterns of relation-
ships between anemonefi sh and host anemone species have
been proposed by Fautin (
1985 , 1986 ) and Murata et al.
( 1986 ) and include olfaction and innate preference (by fi sh),
competitive exclusion (between sh), and environmental
requirements of the symbionts (both fi sh and anemone).
Authors have argued that anemone use by different anem-
onefi sh species can be largely explained by innate preference
and environmental requirements (Elliott et al. 1995 ; Fautin
and Allen
1997 ; Ollerton et al. 2007 ) however there must be
other contributing factors involved as some anemonefi sh are
known to move from one anemone species as juveniles to a
different anemone species as adults (Moyer and Bell 1976 ;
Dunn 1981 ; Chadwick and Arvedlund 2005 ; Huebner et al.
2012 ). The fact that some anemone species are used as nurs-
eries (as they only have immature anemonefi sh using them in
some locations) (Moyer 1976 ; Dunn 1981 ; Chadwick and
Arvedlund 2005 ; Huebner et al. 2012 ) from which an anem-
onefi sh must move if it is to reproduce, provides evidence
that choice of anemone can infl uence fi sh tness . What qual-
ities anemonefi sh deem as desirable however remains some-
what unclear.
Considering that anemonefi sh benefi t primarily from the
protection that a host anemone provides, Huebner et al.
( 2012 ) suggests that anemone morphology may play a role.
Specifi cally, the shelter that the tentacles provide could be an
indicator of host quality. Anemone morphology does vary
amongst the ten host anemone species , primarily in body
size and in tentacle length (Table 27.2 ). Some species have
long tentacles whereas others have very short tentacles such
as in the carpet anemones (Fig. 27.2 ). The most preferred
anemone, E . quadricolor has long tentacles that form bub-
bles on the tips and anemonefi sh can immerse their whole
bodies within the tentacles when hiding or sleeping thus
avoiding predators . The carpet anemone Stichodactyla
gigantea also has a large number of sh symbionts and
whilst anemonefi sh are not able to immerse themselves com-
pletely within their short tentacles, they can be found con-
cealed within the sizeable folds of the protective anemone
blanket. This indicates that tentacle length alone is not the
only indicative measure of host anemone quality. Huebner
et al. ( 2012 ) suggests that because adult A. bicinctus are
competitively excluding conspecifi c juveniles from living
within the highly desired host anemone E. quadricolor , this
species of anemone must be preferred over H . crispa , which
is used only by juveniles at their study area in the Gulf of
Aqaba, northern Red Sea .
An anemone characteristic that has not had much consid-
eration, but would clearly infl uence anemone quality is tox-
icity . A large variance in toxicity exists amongst host
anemone species and anemones with high haemolytic char-
acteristics typically have high neurotoxic characteristics as
well (Nedosyko et al.
2014 ). The study by Nedosyko et al.
(
2014 ) proposes that anemonefi sh may be forming associa-
tions with host anemones based on the potency of toxins,
and that this could be a critical factor in determining the
27 Sea Anemones and Anemonefi sh: A Match Made in Heaven
430
Table 27.1 Combinations of host anemone and anemonefi sh associations (Updated from Fautin and Allen 1997 )
Anemone species
Anemonefi sh
species
Entac-
maea
quadri-
color
Heteractis
crispa
Sticho-dactyla
mertensii
Heteractis
magnifi ca
Heteractis
aurora
Sticho-
dactyla
haddoni
Sticho-
dactyla
gigantea
Macro-
dactyla
doreensis
Hete-
ractis
malu
Crypto-
dendrum
adhaesivum
Total
anemone
associates
Premnas biaculeatus X 1
Amphiprion
akallopisos
X X 2
Amphiprion
akindynos
X X X X X X X 7
Amphiprion allardi X X X 3
Amphiprion bicinctus X X X X X X 6
Amphiprion barberi X a X a 2
Amphiprion
chagosensis
X 1
Amphiprion
chrysogaster
X X X X X 5
Amphiprion
chrysopterus
X X X X X X 6
Amphiprion clarkii X X X X X X X X X X 10
Amphiprion
ephippium
X X 2
Amphiprion frenatus X 1
Amphiprion
fuscocaudatus
X 1
Amphiprion
latezonatus
X b X 2
Amphiprion
latifasciatus
X 1
Amphiprion
mccullochi
X 1
Amphiprion
melanopus
X X X 3
Amphiprion nigripes X 1
Amphiprion ocellaris X X X 3
Amphiprion
omanensis
X X X 2
Amphiprion pacifi cus ?
Amphiprion percula X X X 3
Amphiprion
perideraion
X X X X 4
Amphiprion polymnus X X X 3
Amphiprion
rubrocinctus
X X 2
Amphiprion
sandaracinos
X X 2
Amphiprion sebae X 1
Amphiprion tricinctus X X X X X c 5
Total sh associates 16 14 12 11 7 8 7 4 1 1
a Described in Allen et al. ( 2008 )
b Described in Rushworth et al. ( 2011 )
c Described in Hobbs et al. ( 2014 )
K.B. da Silva and A. Nedosyko
431
quality of host anemones for anemonefi sh survival . This
study demonstrated that the most preferred host anemones,
in terms of the number of anemonefi sh symbionts , have a
venom toxicity value that falls within the mid range of
potency, suggesting that moderate toxicity may be optimal
for anemonefi sh survival and reproduction . Considering that
most anemonefi sh are not innately protected from anemone
venom but have to acquire protection through a process of
acclimation (Mariscal 1970b , pers. ob .), it is possible that an
upper toxicity threshold exists for anemonefi sh species to
establish tolerance to venom without being harmed. Low
anemone toxicity levels are also unlikely to be optimal for
anemonefi sh survival as anemonefi sh will not be able to
obtain the protective benefi ts from the association. Little
research has been done to ascertain whether higher quality
anemones afford their symbionts greater tness benefi ts .
This may be the true indicator of anemone quality and
would require an extensive fi eld-based project to determine
the outcome.
Among the preferred hosts such as E . quadricolor , com-
petition amongst sh dictates who lives where, as demon-
strated in two localities by Fautin ( 1986 , 1992 ) but who gets
the best anemone is the question to be asked next.
27.1.6 Competitive Exclusion : Who Gets
the Best Anemone?
Anemonefi sh species may look alike but when examined
closely not only do they vary in color and shape but a big
difference exists in size as well. The largest anemonefi sh
species P. biaculeatus is 160 mm in length compared to the
smallest species, A. percula , at only half the size, 80 mm in
length (Fautin and Allen 1997 ). With most competitive spe-
cies, size plays a major role in determining dominance and
resource holding potential. Studies on anemonefi sh competi-
tion have found that a hierarchy exists amongst anemonefi sh
species (Fautin 1986 ; Hirose 1995 ) with body size being a
major contributor to competitively dominant species
(Srinivasan et al.
1999 ; Hattori 2002 ). But what are
anemonefi sh competing for? Clearly, the most important ele-
ment for their survival and reproduction is their host anem-
one and as indicated above host anemones vary in their
morphology and likely quality. Therefore competition should
exist amongst anemonefi sh for the highest quality anemones;
indeed this is the case as reported by Fautin (
1986 ), Huebner
et al. ( 2012 ), and Srinivasan et al. ( 1999 ). Some anemonefi sh
species are known to be competitively superior to others and
therefore would be predicted to access and hold the most
valuable host anemone resource. Fautin ( 1986 ) demonstrated
in aquaria that interspecifi c competition between P. biacu-
leatus and A. akindynos , would require the latter species to
be 175 % larger in body length to outcompete P. biaculeatus
for an anemone host . Hirose ( 1995 ) also observed larger A.
frenatus displacing smaller individuals after a typhoon event.
Body size in these cases was the predictor for resource hold-
ing success of these species.
Anemonefi sh are classifi ed as either generalist or special-
ist based on the frequency of interactions fi sh species have
with host anemone species (Miyagawa 1989 ). In the case of
the extreme anemone specialists such as P. biaculeatus that
only uses E. quadricolor , there is probably strong selection
for individuals to out-compete those of other anemonefi sh
species for the single host anemone species with which it
lives. Indeed P. biaculeatus in particular has also evolved
enhanced morphological characteristics such as large cheek
spines that we propose increase its competitive advantage for
occupying the most preferred host anemone . Large specialist
anemonefi sh such as P. biaculeatus can always monopolise
their host anemonefi sh species to such an extent that they are
almost always found as a single breeding pair occupying a
large solitary E . quadricolor while smaller species are not
only pushed into the less desirable anemones but also often
forced to form size hierarchies within their host anemones
where individuals form queues of up to nine individuals for
a reproductive position within their anemone (Fricke 1979 ).
Aggressive behavior in the form of chasing, biting and con-
tinual harassment can limit anemonefi sh size and prevent
smaller individuals from challenging the position of
individuals above them in the queue (Buston
2003 ). However,
Table 27.2 Morphological
characteristics of host
anemone species (Fautin
and Allen
1997 )
Anemone species Tentacle length (mm) Oral disc diameter (mm)
Entacmaea quadricolor 100 50
Heteractis aurora 50 250
H. magnifi ca 75 1,000
H. crispa 100 500
H. malu 40 200
Macrodactyla doreensis 175 500
Stichodactyla gigantea 10 500
S. haddoni 10 800
S. mertensii 20 1,000
Cryptodendrum adhaesivum 5 300
27 Sea Anemones and Anemonefi sh: A Match Made in Heaven
432
perhaps increasing group size might be an evolutionary strat-
egy to maintain acquisition of host anemone resource against
larger congeners.
Limitation or reduction in the availability of host anemo-
nes can increase competition and affect community struc-
ture. Competition is expected to increase as coral reef
habitats come under threat from anthropogenic disturbances.
In areas where multiple anemonefi sh species coexist, species
that have greater resource-holding potential, such as those
gained from large body size, will be favored, thus driving
natural selection of competitively dominant morphology and
behavior . Monitoring changes in anemonefi sh population
structure in threatened areas will be important to elucidate
which species are most vulnerable to extinction .
Fig. 27.2 Host anemones with ( a ) long tentacles Heteractis magnifi ca
( b ) short tentacles Heteractis Aurora ( c ), a bleached Entacmaea quad-
ricolor (Lizards Island, Australia ) ( d ) and E. quadricolor with a shrimp
( Periclimenes brevicarpalis ) (Photograph credits: A. Rocconi ( a , b , d ),
C. Burke da Silva ( c ) )
K.B. da Silva and A. Nedosyko
433
27.2 Conservation Issues: Threats
to the Anemone Symbiosis and Hope
for the Future
Organisms that are dependent on anemones are diminishing
in numbers on reefs impacted by disturbances largely due to
anemone bleaching , but also from coastal process such as
run-off from fl ooding. There is now evidence that ocean
acidifi cation , as a result of increased atmospheric carbon
dioxide, could also threaten the survival of some anemone-
sh species by affecting their ability to locate a host anem-
one during a critical life history stage. As popular target
species for commercial aquarium collectors, anemonefi sh
are also at risk due to the compounding effects of unsustain-
able harvesting for trade. Anemonefi sh and their host anem-
ones have several life-history characteristics that make them
vulnerable to localized population decline (1) anemones are
long-lived, slow growing and have relatively low reproduc-
tive rates (i.e. they spawn infrequently, have low spawning
success, and have short larval lifespan) (2) anemonefi shes
have limited dispersal capabilities, are habitat specialists and
have long life spans (e.g. 30 years, Buston 2007) and (3) both
groups of organisms are mutually dependent on each other
for survival (Fautin and Allen 1997 ; Wilkerson 1998 ; Jones
et al. 2008 ; Shuman et al. 2005 ; Almany et al. 2007 ). Here
we explain these threats further and discuss why there is
hope for the conservation of anemones and their symbiotic
partners with the establishment of marine protected areas ,
aquaculture initiatives and reintroduction programs .
27.2.1 Anemone Bleaching
Similar to corals, anemones are susceptible to bleaching
(Fig. 27.2 ), due to the sensitivity of their symbiotic zooxan-
thellae to environmental stressors such as increased tempera-
ture of the ocean and high irradiance . These stressors cause
anemones to bleach by expelling their algal symbionts result-
ing initially in shrinking and often followed by death due to
lack of nutrition (Jones et al. 2008 ; Saenz-Agudelo et al.
2011 ). The occurrence of host anemone bleaching has now
been documented at twelve different reef locations (Fig.
27.1 ) and is expected to increase in frequency and extent.
Examining the thermal tolerance of a common host anemone
species , E . quadricolor , at Solitary Island, Hill and Scott
( 2012 ) found that at temperatures even 1 °C above the sum-
mer average of 27 °C will cause these anemones to expel
their symbiotic algae . The same study found that at tempera-
tures 3 °C above the summer average, anemones experience
severe bleaching that can lead to mortality . The effect of
anemone bleaching on host anemones and their associated
anemonefi sh has only recently been discussed in the litera-
ture and very little is known about the impacts to other
symbiotic species that associate with anemones. We know
that host anemone bleaching can severely degrade habitat
quality for anemonefi sh and can also affect recruitment of
juveniles and decrease reproductive tness (Saenz-Agudelo
et al. 2011 ) and survival (Lönnstedt and Frisch 2014 ). As a
result of decreased anemone abundance and reduced size of
bleached anemones, anemonefi shes are decreasing in num-
bers due to their dependence on host anemones for habitat
and protection (Hattori 2005 ; Jones et al. 2008 ; Frisch and
Hobbs 2009 ; Saenz-Agudelo et al. 2011 ; Hill and Scott
2012 ; Hobbs et al. 2013 ).
Anemonefi sh have been observed abandoning a bleached
host anemone in search of another suitable anemone (Hattori
2005 ) but other studies have shown that fi sh will stay associ-
ated with a bleached host anemone and that anemones can
regain full color within a year after a bleaching event (Saenz-
Agudelo et al.
2011 ; Hobbs et al. 2013 ). Abandoning a host
anemone is risky for an anemonefi sh due to exposure to
predators during relocation however we now know that stay-
ing associated with a bleached anemone has tness costs.
Saenz-Agudelo et al. (
2011 ) demonstrated that egg produc-
tion of female A. polymnus living in a bleached anemone was
reduced by 38 % during a bleaching event. A behavioural
study by Lönnstedt and Frisch ( 2014 ) demonstrated that A.
akindynos living in bleached anemones also display altered
avoidance behaviors (e.g. they uncharacteristically continue
feeding and don’t seek refuge within the tentacles of their
anemone) in the presence of a common predator and suggest
being eaten as a possible explanation for the observed reduc-
tion in anemonefi sh numbers on bleached anemones com-
pared to those living in healthy unbleached ones in the
southern Great Barrier Reef, Australia . We found that when
anemonefi sh are given a choice in a captive situation of a
bleached and unbleached anemone, they always chose to
associate with the unbleached anemone (K. Burke da Silva,
unpublished data ). The choices fi sh make in response to this
habitat disturbance may be dependent on the severity of the
bleaching event, mobility of the fi sh species and availability
of vacant non-bleached host anemones in the area.
Considering further temperature increases of 2.8–3.6 °C pre-
dicted in waters around coral reefs this century (Brainard
et al. 2011 ) the frequency of anemone bleaching is expected
to increase, which will have adverse impacts on both anemo-
nes and their resident anemonefi sh.
27.2.2 Ocean Acidifi cation
Ocean acidifi cation is the process of the ocean’s pH decreas-
ing as carbon dioxide is absorbed from the atmosphere into
the water (Munday et al. 2009 ). One of the major impacts of
acidifi cation is the inability for marine organisms like corals
to calcify their skeletons, shells and coccoliths because
27 Sea Anemones and Anemonefi sh: A Match Made in Heaven
434
minerals, calcite and aragonite become less available (Fabry
et al.
2008 ). This threatens the coral reef habitat of anemones
and their symbionts by diminishing coral abundance and
reef-building capabilities (Hoegh-Guldberg et al.
2007 ) and
making them more vulnerable to degradation by erosion,
storms, predation and other disturbances. In addition to caus-
ing habitat loss, the adverse effect of acidifi cation directly
threatens the survival of anemonefi sh as a result of distur-
bances to behavior and other biological functions. Recent
laboratory studies have found that ocean acidifi cation at lev-
els predicted mid to later this century (~pH 7.8–7.6) disrupts
the sensory capacity and behavior of anemonefi sh during a
critical life history stage (Munday et al.
2009 , 2010 ; Dixson
et al. 2010 ; Simpson et al. 2011 ; Nilsson et al. 2012 ; Nowicki
et al. 2012 ). These studies indicate that extended exposure to
lower pH levels of seawater affects the olfactory and audi-
tory system of larval anemonefi sh, which is likely to have
negative effects on their ability to locate settlement sites and
avoid predators . Munday et al. ( 2009 ) also found that when
A. percula larvae are reared in seawater at pH levels expected
to occur at the end of this century, they completely lose their
ability to discriminate the smell of their host anemone . While
it appears that some sea anemone species are predicted to
grow larger and much more abundant in a higher CO
2 envi-
ronment due to an increase in the energy output of their sym-
biotic algae (Suggett et al. 2012 ), without anemonefi sh to
protect them, it is unlikely that obligate anemone hosts will
survive. Disruption to these processes as a result of acidifi ca-
tion will have signifi cant consequences to larval settlement ,
population replenishment and likely population-level and
species decline of both host anemones and anemonefi shes as
early as mid-century.
27.2.3 Collection for the Aquarium Trade
Anemones and anemonefi sh are particularly vulnerable to
collection for the marine aquarium trade compared to other
targeted species because they are constantly in demand and
dealers can virtually guarantee a sale (Edwards and Shepherd
1992 ; Wood 2001 ; Wabnitz et al. 2003 ). In general, the fam-
ily Pomacentridae, consistently dominate the global marine
aquarium market and account for 43 % of all marine fi sh
traded (Zajicek et al. 2009 ). With the release of the Disney
lm ‘Finding Nemo’ in 2003, the global demand and trade of
anemonefi sh increased dramatically, particularly for the
orange clownfi sh A. percula and sister species A. ocellaris
that resemble the star character (Prosek 2010 ). Commercial
shers also harvest anemones but the extent of collection is
not well documented. Several international studies indicate
that anemones and anemonefi sh are threatened due to over-
exploitation from wild harvesting . In the Philippines, which
is the largest supplier of marine ornamental species and
accounts for ~55 % of global exports (Bruckner
2005 ; Rhyne
et al.
2012 ), anemonefi sh and anemones in this region have
been diminishing in numbers due to aquarium shing activi-
ties (Shuman et al.
2005 ). On the Great Barrier Reef,
Australia where habitat loss has been compounded by ther-
mal stress and low salinity from coastal run-off, there is evi-
dence that anemone and anemonefi sh populations in areas
subject to harvesting have also declined in numbers and
failed to recover (Jones et al.
2008 ; Frisch and Hobbs 2009 ).
Fisher’s logbooks can be a useful tool to determine catch
records, however, Jones et al. ( 2008 ) reported that the global
marine aquarium industry is almost entirely self-regulating
and collectors are reticent to reveal collection numbers and
location data due to competition . This is combated by weak
governance capacity in major source countries such as the
Philippines and Indonesia and high international demand
that offers few incentives to strengthen trade policies or man-
agement practices. Even in some of the best-managed reef
areas of the world, such as the Great Barrier Reef, where
quota restrictions, voluntary stewardship agreements and no-
take zones are implemented, populations of both anemone
and anemonefi shes are still declining in some areas (Jones
et al. 2008 ; Frisch and Hobbs 2009 ; Scott and Baird 2014 ).
It is common for collectors to remove a breeding pair of
adults or sub-adults, leaving at least one anemonefi sh behind
(Jones et al. 2008 ). Contrary to sustainable principles, col-
lectors are removing breeding adults on the assumption that
this will foster faster growth of sub-adults. Hattori ( 1991 )
however, found that it could take 1.5 years for the next fi sh in
line to mature to a breeding position. Even though a study
has indicated that post-larval anemonefi sh may rapidly settle
onto an unoccupied anemone (~30 days) after the removal of
adult fi sh residents (Fautin 1992 ), Sale et al. ( 1986 ) found
that removal of fi sh can cause a total cessation of recruitment
in some areas. It is apparent that long-term monitoring needs
to occur in areas where anemonefi sh are being collected to
inform a sustainable management approach.
27.2.4 Hope for the Future
We are faced with a real challenge to fundamentally change
the way we are living to reduce the synergistic impacts of
both ocean acidifi cation and global warming to protect reef
habitats. Growing evidence suggests that if we continue to
emit CO
2 into the atmosphere at the same rate as we are now,
reefs are predicted to experience rapid and terminal declines
worldwide before mid-century (Hoegh-Guldberg et al. 2007 ;
Wilkinson 2008 ). However, with technological progress into
the use of renewable energy resources, investment in aqua-
culture and better conservation management approaches,
including more targeted restrictions and in some cases
complete cessation of the harvest of anemones and
K.B. da Silva and A. Nedosyko
435
anemonefi shes, there is hope to safeguard species in threat-
ened coral reef habitats (Jones et al.
2008 ; Frisch and Hobbs
2009 ; Scott et al. 2011 ). Recent studies reveal the positive
impacts of implementing protective measures. For example,
no-take zones around north solitary island, far north
Queensland and Keppel Islands off the coast of Australia
(Jones et al. 2008 ; Scott et al. 2011 ) and also in the Maldives
where a cap on exports for all allowable coral reef species
has been implemented (Edwards and Shepherd 1992 ), which
has increased the abundance of different species of both
anemones and anemonefi shes in these areas. Larger body
size of host anemones is another observed benefi t in areas
closed to fi shing compared to open areas (Frisch and Hobbs
2009 ). With considered planning, protected areas may also
be vital for sustained larval recruitment of anemonefi sh
(Jones et al. 2009 ). In consideration of future ecological sce-
narios, we agree with the recommendation of a suspension of
commercial harvest in some areas to relieve the additional
pressure that over-collecting has placed on these species
(Jones et al. 2008 ).
Captive breeding is the most viable option to meet the
increasing demand for aquarium species particularly for
anemonefi sh but also of anemones. Currently, there are
records of successful asexual propagation of host anemones
in captivity such as E . quadricolor by cutting healthy speci-
mens longitudinally in half and quarters and attaching them
to a suitable substrate (Scott et al. 2014 ). Recent studies have
also advanced our understanding of the sexual reproductive
cycle of two highly collected anemones for marine aquari-
ums ( E. quadricolor and H. cripa ) (Scott and Harrison
2007a , b , 2008 , 2009 ). This information may one day enable
the supply of captive-bred anemones for the aquarium trade.
Captive breeding programs of several anemonefi sh species
are already well established in different parts of the world
(Le et al. 2011 ; Dhaneesh et al. 2012a , b ; Ghosh et al. 2012 ;
Kumar et al. 2012 ). The ‘Saving Nemo’ project based at
Flinders University in Adelaide, South Australia, aims to
reduce the harvest of anemonefi sh from the Great Barrier
Reef through a captive breeding and education outreach pro-
gram (The Saving Nemo Organisation 2015 ). Captive breed-
ing is most likely the only sustainable means to replenish the
already depleted natural source (Dhaneesh et al. 2012a ). In
some areas where overexploitation has occurred, captive
breeding can serve as a mechanism for the reintroduction of
captive bred species back into the wild thus supporting coral
reef biodiversity conservation. In 2002, a program guided by
Dr. Thon Thamrong-nawasawat was established to begin a
reintroduction of captive bred false anemonefi sh A. ocellaris
into its natural environment at Mu Koh Ha Yai in Krabi
Province, Thailand. The fi rst few years of the project had low
success rates with the majority of introduced anemonefi sh
eaten by predators . However, sh survival rates increased
during subsequent years after host anemones were protected
with mesh wire cages. This enabled released anemonefi sh to
swim freely in and out of the anemone but inhibited larger
predatory fi sh. This is the fi rst program of its kind to investi-
gate and establish suitable methods to increase survival rate
of reintroduced anemonefi sh.
27.3 Shrimps, Crabs and Other Fish
Symbionts
While no other fi sh lives as closely with an anemone as an
anemonefi sh , other sh form facultative associations with
sea anemones such as damselfi shes (Pomacentridae), cardi-
nalfi shes (Apogonidae), wrasses (Labridae), hawkfi shes
(Cirrhitidae), butterfl yfi shes (Chaetodontidae), blennies
(Clinidae and Blenniidae), parrotfi shes (Scaridae), gobies
(Gobiidae) and greenlings (Hexagrammidae) amongst others
(Fautin and Allen 1997 ; Randall and Fautin 2002 ; Arvedlund
et al. 2006 ). Arvedlund et al. ( 2006 ) provides a review of 51
species of shes that are assumed to be facultative symbionts
of sea anemones, mainly in tropical waters. These fi sh often
dwell within the area of the tentacles of sea anemones,
mostly as juveniles and appear to avoid the tentacles with
only few making contact. The damselfi sh Dascyllus spp and
the painted greenling Oxylebius pictus have been observed
living within the anemones tentacles as juveniles for protec-
tion (Elliott 1992 ; Fautin and Allen 1997 ). For example,
juvenile painted greenlings sleep amongst the tentacles of
the same individual anemone Urticina lofotensis each night
but leave during the daytime until they are mature enough to
live independently (Elliott 1992 ). These sh often associate
with an anemone on their own but damselfi sh will sometimes
share a host anemone with an anemonefi sh (Fautin and Allen
1997 ). The relationship of these fi sh to anemones is consid-
ered facultative because while the benefi ts to the fi sh are
obvious the complete behavioral and physiological facets of
these relationships remain to be studied.
Several shrimp and crab species such as Periclimenes (Fig.
27.2 ), Stenorhynchus , Mithraculus , Neopetrolisthes ,
Allopetrolisthes spp., are also associated with different sea
anemone species . For symbiotic crustaceans , sea anemone
hosts act as their reproductive habitat (Baeza et al. 2001 ),
food source (Viviani 1969 ) and a refuge against predators
such as fi shes and birds (Va’squez 1993 ). Laboratory experi-
ments suggest that the mechanisms that enable crustaceans to
live unharmed amongst the sea anemone are similar to those
of the anemonefi sh–anemone mutualism (Giese et al. 1996 ).
For example the crustacean species, Mithraculus sculptus ,
requires acclimation to a new host to acquire a protective
mucus coating from the anemone otherwise it will be imme-
diately stung and ingested (Mebs 2009 ). Similar to anemone-
shes , crustaceans are also found with only some of the
anemone species within their distribution (Nizinski
1989 ;
27 Sea Anemones and Anemonefi sh: A Match Made in Heaven
436
Gwaltney and Brooks 1994 ). It is understood that at least for
some species, crustaceans are able to distinguish and locate
potential hosts primarily by olfactory cues but it is likely that
more than one sensory modality is involved (Guo et al. 1996 ) .
References
Allen GR (1991) Damselfi shes of the world. Mergus, Melle
Allen GR, Kaufman L, Drew JA (2008) Amphiprion barberi, a new spe-
cies of anemonefi sh (Pomacentridae) from Fiji, Tonga, and Samoa.
Aqua, Int J Ichthyol 14(3):105–114
Allen GR, Drew J, Fenner D (2010) Amphiprion pacifi cus, a new spe-
cies of anemonefi sh (Pomacentridae) from Fiji, Tonga, Samoa, and
Wallis Island. Aqua, Int J of Ichthyol 16(3):129–139
Almany GR, Berumen ML, Thorrold SR, Planes S, Jones GP (2007)
Local replenishment of coral reef fi sh populations in a marine
reserve. Science 316:742–744
Arvedlund M, Nielsen LE (1996) Do the anemonefi sh Amphiprion
ocellaris (Pisces: Pomacentridae) imprint themselves to their host
sea anemone Heteractis magnifi ca (Anthozoa: Actinidae)? Ethology
102(2):197–211
Arvedlund M, McCormick MI, Fautin DG, Bildsøe M (1999) Host rec-
ognition and possible imprinting in the anemonefi sh Amphiprion
melanopus (Pisces: Pomacentridae). Mar Ecol Prog Ser
188:207–218
Arvedlund M, Bundgaard I, Nielsen LE (2000) Host imprinting in
anemonefi shes (Pisces: Pomacentridae): does it dictate spawning
site preferences? Envir Biol Fishes 58(2):203–213
Arvedlund M, Iwao K, Brolund TM, Takemura A (2006) Juvenile
Thalassoma amblycephalum Bleeker (Labridae, Teleostei) dwelling
among the tentacles of sea anemones: a cleanerfi sh with an unusual
client? J Exper Mar Biol Ecol 329(2):161–173
Astakhov DA (2002) Species composition of anemonefi shes
(Perciformes, Pomacentridae) and their host sea anemones
(Cnidaria, Actiniaria) in the Khanhhoa Province (South Vietnam).
J Ichthyol 42(1):37–50
Baeza JA, Stotz W, Thiel M (2001) Life history of Allopetrolisthes spi-
nifrons, a crab associate of the sea anemone Phymactis clematis.
J Mar Biol Assoc UK 81:69–76
Brainard RE, Birkeland C, Eakin CM, McElhany P, Miller MW,
Patterson M, Piniak GA (2011) Status review report of 82 candidate
coral species petitioned under the US Endangered Species Act. US
Department of Commerce, NOAA Technical Memorandum, NMFS-
PIFSC-27, Pacifi c Islands Fisheries Science Center, Honolulu, HI
Bridge T, Scott A, Steinberg D (2012) Abundance and diversity of
anemonefi shes and their host sea anemones at two mesophotic sites
on the Great Barrier Reef, Australia. Coral Reefs 31(4):1057–1062
Bruckner AW (2005) The importance of the marine ornamental reef fi sh
trade in the wider Caribbean. Rev Biol Trop 53:127–137
Bruhn T, Schaller C, Schulze C, Sanchez-Rodriguez J, Dannmeier C,
Ravens U et al (2011) Isolation and characterisation of fi ve neuro-
toxic and cardiotoxic polypeptides from the sea anemone
Anthopleura elegantissima. Toxicon 93:693–702
Buston PM (2003) Size and growth modifi cation in clownfi sh. Nature
424:145–146
Buston PM, García MB (2007) An extraordinary life span estimate for
the clown anemonefi sh Amphiprion percula. J Fish Biol
70(6):1710–1719
Caspers H (1939) Histologische Untersuchungen über die Symbiose
zwischen Aktinien und Korallenfi schen. Zool Anz 126:245–253
Chadwick NE, Arvedlund M (2005) Abundance of giant sea anemones
and patterns of association with anemonefi sh in the northern Red
Sea. J Mar Biol Assoc UK 85(5):1287–1292
Dalay M, Mercer R, Brugler MR et al (2008) The phylum Cnidaria: a
review of phylogenetic patterns and diversity 300 years after
Linnaeus. Zootaxa 1668:127–182
Davenport D, Norris KS (1958) Observations on the symbiosis of the
sea anemone Stoichactis and the pomacentrid fi sh, Amphiprion per-
cula . Biol Bull 115:397–410
Dhaneesh KV, Devi KN, Kumar TTA et al (2012a) Breeding, embry-
onic development and salinity tolerance of Skunk clownfi sh
Amphiprion akallopisos . J King Saud Univ Sci 24(3):201–209
Dhaneesh KV, Kumar TTA, Swagat G et al (2012b) Breeding and mass
scale rearing of clownfi sh Amphiprion percula : feeding and rearing
in brackishwater. Chi J Ocean Limnol 30(4):528–534
Dixson DL, Munday PL, Jones GP (2010) Ocean acidifi cation disrupts
the innate ability of fi sh to detect predator olfactory cues. Ecol Lett
13(1):68–75
Dixson DL, Munday PL, Pratchett M et al (2011) Ontogenetic changes
in responses to settlement cues by anemonefi sh. Coral Reefs
30(4):903–910
Dunn DF (1981) The clownfi sh sea anemones: Stichodactylidae
(Coelenterata: Actiniaria) and other sea anemones symbiotic with
pomacentrid fi shes. Trans Am Philos Soc 71:1–115
Edwards AJ, Shepherd AD (1992) Environmental implications of
aquarium-fi sh collection in the Maldives, with proposals for regula-
tion. Environ Conserv 19:61–72
Elliott J (1992) The role of sea anemones as refuges and feeding habi-
tats for the temperate fi sh Oxylebius pictus . Environ Biol Fish
35(4):381–400
Elliott JK, Mariscal RN (1996) Ontogenetic and interspecifi c variation
in the protection of anemonefi shes from sea anemones. J Exp Mar
Biol Ecol 208:57–72
Elliott JK, Mariscal RN, Roux KH (1994) Do anemonefi shes use
molecular mimicry to avoid being stung by host anemones? J Exp
Mar Biol Ecol 179(1):99–113
Elliott JK, Mariscal RN, Roux KH (1995) Do anemonefi shes use
molecular mimicry to avoid being stung by host anemones? J Exp
Mar Biol Ecol 179:99–113
Elliott JK, Lougheed SC, Bateman B et al (1999) Molecular phyloge-
netic evidence for the evolution of specialization in anemone fi shes.
Proc R Soc Lond B 266:677–685
Fabry VJ, Seibel BA, Feely RA et al (2008) Impacts of ocean acidifi ca-
tion on marine fauna and ecosystem processes. ICES J Mar Sci
65:414–432
Fautin DG (1985) Competition by anemone fi shes for host actinians.
Proc 5th Int Coral Reef Congr Tahiti 1:373–377
Fautin DG (1986) Why do anemonefi shes inhabit only some host actin-
ians? Environ Biol Fish 15(3):171–180
Fautin DG (1991) The anemonefi sh symbiosis: what is known and what
is not. Symbiosis 10:23–46
Fautin DG (1992) Anemonefi sh recruitment: the roles of order and
chance. Symbiosis 14:143–160
Fautin DG, Allen GR (1997) Anemonefi shes and their host sea anemo-
nes. Western Australian Museum, Perth
Fricke HW (1979) Mating system, resource defence and sex change in
the anemonefi sh Amphiprion akallopisos. Z Tierpsychol
50(3):313–326
Fricke HW (1974) Oko-Ethologie des monogamen Anemonenfi sches
Amphriprion bicinctus (Freiwasseruntersuchung aus dem Roten
Meer). Z Tierpsychol 36:429–512
Frisch AJ, Hobbs JP (2009) Rapid assessment of anemone and anem-
onefi sh populations at the Keppel Islands a report to the Great
Barrier Reef Marine Park Authority. Great Barrier Reef Marine
Park Authority. GBRMPA.
http://www.gbrmpa.gov.au/__data/
assets/pdf_fi le/0005/5594/gbrmpa_RP94_Rapid_Assessment_Of_
Anemone_2009.pdf . Accessed 20 Jul 2015
Futuyma DJ, Moreno G (1988) The evolution of ecological specializa-
tion. Ann Rev Ecol Syst 19:207–233
K.B. da Silva and A. Nedosyko
437
Godwin J, Fautin DG (1992) Defense of host actinians by anemone-
shes. Copeia 3:902–908
Ghosh S, Kumar TTA, Nanthinidevi K et al (2012) Reef fi sh breeding
and hatchery production using brackishwater, a sustainable technol-
ogy with special reference to Clark’s clownfi sh, Amphiprion Clarkii
(Bennett, 1830). Int J Environ Sci Dev 3(1):56–60
Giese C, Mebs D, Werding B (1996) Resistance and vulnerability of
crustaceans to cytolytic sea anemone toxins. Toxicon 34:955–958
Gondran M, Eckeli AL, Migues PV et al (2002) The crude extract from
the sea anemone, Bunodosoma caissarum elicits convulsions in
mice: possible involvement of the glutamatergic system. Toxicon
40:1667–1674
Guo CC, Hwang JS, Fautin DG (1996) Host selection by shrimps sym-
biotic with sea anemones: a fi eld survey and experimental labora-
tory analysis. J Exp Mar Biol Ecol 202(2):165–176
Gwaltney CL, Brooks W (1994) Host specifi city of the anemoneshrimp
Periclimenes pedersoni and P. yucatanicus in the Florida Keys.
Symbiosis 16(1):83–93
Hattori A (1991) Socially controlled growth and size-dependent sex
change in the anemonefi sh Amphiprion frenatus in Okinawa, Japan.
Jpn J Ichthyol 38:165–177
Hattori A (2002) Small and large anemonefi shes can coexist using the
same patchy resources on a coral reef, before habitat destruction.
J Anim Ecol 71(5):824–831
Hattori A (2005) High mobility of the protandrous anemonefi sh
Amphiprion frenatus : nonrandom pair formation in limited shelter
space. Ichthyol Res 52(1):57–63
Hill R, Scott A (2012) The infl uence of irradiance on the severity of
thermal bleaching in sea anemones that host anemonefi sh. Coral
Reefs 31(1):273–284
Hirose Y (1995) Patterns of pair formation in protandrous anem-
onefishes, Amphiprion clarkii , A. frenatus and A. perideraion ,
on coral reefs of Okinawa, Japan. Environ Biol Fish
43(2):153–161
Hobbs JP, Frisch AJ, Ford BM et al (2013) Taxonomic, spatial and tem-
poral patterns of bleaching in anemones inhabited by anemone-
shes. PLoS ONE 8(8):1–3
Hobbs JP, Beger M, De Brauwer M et al (2014) North-eastern range
extension of the anemone Stichodactyla haddoni to the Marshall
Islands represents a new record of host use by the endemic anem-
onefi sh Amphiprion tricinctus . Mar Biodivers Rec 7:e106
Hoegh-Guldberg O, Mumby PJ, Hooten AJ et al (2007) Coral reefs
under rapid climate change and ocean acidifi cation. Science
318:1737–1742
Holbrook SJ, Schmitt RJ (2004) Population dynamics of a damselfi sh:
effects of a competitor that also is an indirect mutualist. Ecology
85:979–985
Holbrook SJ, Schmitt RJ (2005) Growth, reproduction and survival of a
tropical sea anemone (Actiniaria): benefi ts of hosting anemonefi sh.
Coral Reefs 24:67–73
Huebner LK, Dailey B, Titus BM et al (2012) Host preference and habi-
tat segregation among Red Sea anemonefi sh: effects of sea anemone
traits and fi sh life stages. Mar Ecol Prog Ser 464:1–15
Jang-Liaw NH, Tang KL, Hui CF et al (2002) Molecular phylogeny of
48 species of damselfi shes (Perciformes: Pomacentridae) using 12S
mtDNA sequences. Mol Phyl Evol 25:445–454
Jones AM, Gardner S, Sinclair W (2008) Losing ‘Nemo’: bleaching and
collection appear to reduce inshore populations of anemonefi shes.
J Fish Biol 73(3):753–761
Jones GP, Almany GR, Russ GR et al (2009) Larval retention and con-
nectivity among populations of corals and reef fi shes: history,
advances and challenges. Coral Reefs 28(2):307–325
Konno K, Qin G, Nakanishi K (1990) Synthesis of amphikuemin and
analogs: a synomone that mediates partner-recognition between
anemonefi sh and sea anemones. Heterocycles 30:247–251
Kumar TTA, Gopi M, Dhaneesh KV et al (2012) Hatchery production
of the clownfi sh Amphiprion nigripes at Agatti Island, Lakshadweep,
India. J Environ Biol 33:623–628
Lanioa M, Morerab V, Alvareza C et al (2001) Purifi cation and charac-
terization of two hemolysins from Stichodactyla helianthus .
Toxicon 39:187–194
Le Y, Sheng-Yun Y, Xiao-Ming Z et al (2011) Effects of temperature on
survival, development, growth and feeding of larvae of yellowtail
clownfi sh Amphiprion clarkii (Pisces: Perciformes). Acta Ecol Sin
31:241–245
Litsios G, Pearman PB, Lanterbecq D et al (2014) The radiation of the
clownfi shes has two geographical replicates. J Biogeogr
41:2140–2149
Lönnstedt OM, Frisch AJ (2014) Habitat bleaching disrupts threat
responses and persistence in anemonefi sh. Mar Ecol Prog Ser
517:265–270
Lubbock R (1980) Why are clownfi shes not stung by sea anemones?
Proc R Soc Lond 207:35–61
Lubbock R (1981) The clownfi sh/anemone symbiosis: a problem of
cellular recognition. Parasitology 82:159–173
Mariscal RN (1969) The protection of the anemonefi sh, Amphiprion
xanthurus , from the sea anemone, Stoichactis kenti . Experientia
25:1114
Mariscal RN (1970a) The nature of the symbiosis between Indo-Pacifi c
anemone fi shes and sea anemones. Mar Biol 6:58–65
Mariscal RN (1970b) An experimental analysis of the protection of
Amphiprion xanthurus Cuvier and Valenciennes, and some other
anemone fi shes from sea anemones. J Exp Mar Biol Ecol
4:134–149
Mariscal RN (1971) Experimental studies on the protection of anemone
shes from sea anemones. In: Cheng TC (ed) Aspects of the biology
of symbiosis. University Press, Baltimore, pp 283–315
Mebs D (1994) Anemonefi sh symbiosis: vulnerability and resistance of
sh to the toxin of the sea anemone. Toxicon 32:1059–1068
Mebs D (2009) Chemical biology of the mutualistic relationships of sea
anemones with fi sh and crustaceans. Toxicon 54(8):1071–1074
Mitchell JS (2003) Mobility of Stichodactyla gigantea sea anemones
and implications for resident false clown anemonefi sh, Amphiprion
ocellaris . Environ Biol Fish 66(1):85–90
Miyagawa K (1989) Experimental analysis of the symbiosis between
anemonefi sh and sea anemones. Ethology 80:19–46
Miyagawa K, Hidaka T (1980) Amphiprion clarkii juvenile: innate pro-
tection against and chemical attraction by symbiotic sea anemones.
Proc Jpn Acad 56:356–361
Miyagawa-Kohshima K, Miyahara H, Uchida S (2014) Embryonic
learning of chemical cues via the parents’ host in anemonefi sh
( Amphiprion ocellaris ). J Exp Mar Biol Ecol 457:160–172
Moyer JT (1976) Geographical variation and social dominance in
Japanese populations of the anemonefi sh Amphiprion clarkii.
J Icthyol 23(1):12–22
Moyer JT, Bell LJ (1976) Reproductive behavior of the anemonefi sh
Amphiprion clarkii at Miyake-Jima, Japan. Jpn J Ichthyol
23(1):23–32
Munday PL, Dixson DL, Donelson JM et al (2009) Ocean acidifi cation
impairs olfactory discrimination and homing ability of a marine
sh. Proc Natl Acad Sci U S A 106(6):1848–1852
Munday PL, Dixson DL, McCormick MI et al (2010) Replenishment of
sh populations is threatened by ocean acidifi cation. Proc Natl Acad
Sci U S A 107(29):12930–12934
Murata M, Miyagawa-Kohshima K, Nakanishi et al (1986)
Characterization of compounds that induce symbiosis between sea
anemone and anemonefi sh. Science 234:585–587
Nedosyko AM, Young JE, Edwards JW et al (2014) Searching for a
toxic key to unlock the mystery of anemonefi sh and anemone sym-
biosis. PLoS ONE 9(5):1–8
27 Sea Anemones and Anemonefi sh: A Match Made in Heaven
438
Nilsson GE, Dixson DI, Domenici P et al (2012) Near-future carbon
dioxide levels alter fi sh behaviour by interfering with neurotrans-
mitter function. Nat Clim Chang 2:201–204
Nizinski MS (1989) Ecological distribution, demography and behav-
ioral observations on Periclimenes anthophilus , an atypical symbi-
otic cleaner shrimp. Bull Mar Sci 45(1):174–188
Nowicki JP, Miller GM, Munday PL (2012) Interactive effects of ele-
vated temperature and CO
2 on foraging behaviour of juvenile coral
reef fi sh. J Exp Mar Biol Ecol 412:46–51
Ollerton J, McCollin D, Fautin DG et al (2007) Finding NEMO: nested-
ness engendered by mutualistic organization in anemonefi sh and
their hosts. Proc R Soc B 274:591–598
Pento D, Pe’rez-Barzaga V, Dı’az I et al (2011) Validation of a mutant
of the pore-forming toxin sticholysin-I for the construction of
proteinase- activated immunotoxins. Protein Eng Des Sel
24:485–493
Prosek J (2010) Beautiful friendship. Natl Geogr Mag.
http://ngm.
nationalgeographic.com/print/2010/01/clownfish/prosek-text .
Accessed 4 May 2015
Randall JE, Fautin DG (2002) Fishes other than anemonefi shes that
associate with sea anemones. Coral Reefs 21:188–190
Rhyne AL, Tlusty MF, Schofi eld PJ (2012) Revealing the appetite of the
marine aquarium fi sh trade: the volume and biodiversity of fi sh
imported into the United States. PLoS ONE 7(5):e35808
Roopin M, Henry RP, Chadwick NE (2008) Nutrient transfer in a
marine mutualism: patterns of ammonia excretion by anemonefi sh
and uptake by giant sea anemones. Mar Biol 154(3):547–556
Rushworth KJ, Smith SD, Cowden KL et al (2011) Optimal tempera-
ture for growth and condition of an endemic subtropical anemone-
sh. Aquaculture 318(3):479–482
Saenz-Agudelo P, Jones GP, Thorrold SR et al (2011) Detrimental
effects of host anemone bleaching on anemonefi sh populations.
Coral Reefs 30:497–506
Sale PF, Eckert GJ, Ferrell DJ et al (1986) Aspects of the demography
of seven species of coral reef fi shes. Great Barrier Reef Marine Park
Authority, Townsville
Santini S, Polacco G (2006) Finding Nemo: molecular phylogeny and
evolution of the unusual life style of anemonefi sh. Gene 385:19–27
Schlichter D (1975) Produktion und Übernahme von Schutzstoffen als
Ursache des Nesselschutzes von Anemonenfi schen? J Exp Mar Biol
Ecol 20:137–150
Schlichter D (1976) Macromolecular mimicry: substances released by
sea anemones and their role in the protection of anemone fi shes. In:
Mackie GO (ed) Coelenterate ecology and behavior. Plenum Press,
New York, pp 433–441
Scott A, Baird AH (2014) Trying to nd Nemo: low abundance of sea
anemones and anemonefi shes on central and southern mid-shelf
reefs in the Great Barrier Reef. Mar Biodivers 2014:1–5
Scott A, Harrison PL (2007a) Broadcast spawning of two species of sea
anemone that host anemonefi sh, Entacmaea quadricolor and
Heteractis crispa . Invertebr Reprod Dev 50:163–171
Scott A, Harrison PL (2007b) Embryonic and larval development of the
host sea anemones Entacmaea quadricolor and Heteractis crispa .
Biol Bull 213(2):110–121
Scott A, Harrison PL (2008) Larval settlement and juvenile develop-
ment of sea anemones that provide habitat for anemonefi sh. Mar
Biol 154(5):833–839
Scott A, Harrison PL (2009) Gametogenic and reproductive cycles of the
sea anemone, Entacmaea quadricolor . Mar Biol 156(8):1659–1671
Scott A, Malcolm HA, Damiano C (2011) Long-term increases in abun-
dance of anemonefi sh and their host sea anemones in an Australian
marine protected area. Mar Freshwater Res 62(2):187–196
Scott A, Hardefeldt JM, Hall KC (2014) A sexual propagation of sea
anemones that host anemonefi shes: implications for the marine
ornamental aquarium trade and restocking programs. PLoS ONE
9(10):1–8
Shuman CS, Hodgson G, Ambrose RF (2005) Population impacts of
collecting sea anemones and anemonefi sh for the marine aquarium
trade in the Philippines. Coral Reefs 24(4):564–573
Simpson SD, Munday PL, Wittenrich ML et al (2011) Ocean acidifi ca-
tion erodes crucial auditory behaviour in a marine fi sh. Biol Lett
7(6):917–920
Srinivasan M, Jones GP, Caley MJ (1999) Experimental evaluation of
the roles of habitat selection and interspecifi c competition in deter-
mining patterns of host use by two anemonefi shes. Mar Ecol Prog
Ser 186:283–292
Suggett DJ, Hall-Spencer JM, Rodolfo-Metalpa R et al (2012) Sea
anemones may thrive in a high CO
2 world. Glob Chang Biol
18(10):3015–3025
Szczebak JT, Henry RP, Al-Horani FA et al (2013) Anemonefi sh oxy-
genate their anemone hosts at night. J Exp Biol 216(6):970–976
The Saving Nemo Organisation (2015) Homepage. The Saving Nemo
Organisation.
http://www.savingnemo.org . Accessed 20 Jul 2015
Timm J, Figiel M, Kochzius M (2008) Contrasting patterns in species
boundaries and evolution of anemonefi shes (Amphiprioninae,
Pomacentridae) in the centre of marine biodiversity. Mol Phylogenet
Evol 49:268–276
Tytgat J, Bosmans F (2007) Sea anemone venom as a source of insecti-
cidal peptides acting on voltage-gated Na+ channels. Toxicon
49:550–560
Uechi G, Toma H, Arakawa T et al (2005) Molecular cloning and func-
tional expression of hemolysin from the sea anemone Actineria vil-
losa . Protein Expr Purif 40:379–384
Va’squez JA (1993) Abundance, distributional patterns and diets of
main herbivorous and carnivorous species associated to Lessonia
trabeculata kelp beds in northern Chile. Ser Ocas Fac Cienc Mar
Univ Cato’ l, Norte (Chile) 2:213–229
Viviani CA (1969) Los Porcellanidae (Crustacea, Anomura) Chilenos.
Beitr Neotrop Fauna 6:1–14
Wabnitz C, Taylor M, Green E, Razak T (2003) From ocean to aquar-
ium: the global trade in marine ornamental species. UNEP-WCMC,
Cambridge
Wilkerson JD (1998) Clownfi shes: a guide to their captive care, breed-
ing and natural history. TFH Publications, Neptune City
Wilkinson C (2008) Status of coral reefs of the world: 2008 global coral
reef monitoring network and reef and rainforest research center.
Townsville, Australia, 296 pp
Wood EM (2001) Collection of coral reef fi sh for aquaria: global trade,
conservation issues and management strategies. Mar Conservation
Society UK, p 80. CiteSeerX.
http://citeseerx.ist.psu.edu/viewdoc/
download?doi=10.1.1.467.6465&rep=rep1&type=pdf . Accessed 3
Feb 2015
Zajicek P, Hardin S, Watson C (2009) A Florida marine ornamental
pathway risk analysis. Rev Fish Sci 17(2):156–169
K.B. da Silva and A. Nedosyko
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... Our anemonefish phylogeny comprised 27 out of the 28 currently defined anemonefish species (Ollerton et al. 2007;Allen et al. 2010;Burke and Nedosyko 2016). The extremely rare species Amphiprion fuscocaudatus was not included since its sequence was not available in GenBank. ...
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Five species of anemonefishes—Ampltiprion clarkii, A. frenatus, A. polymnus, A. perideraion, and A. sandaracinos and nine species of host sea anemones— Cryptodendrum adhaesivum, Entacmaea quadri-color, Macrodactyla doreensis, Heteractis aurora, H.crispa, H. magnifica, H malu, Stichodactyla haddoni, and S. mertensii are found off Khanhhoa Province. It is shown, that A. clarkii is associated with all above-mentioned species of sea anemones; A. polymnus, with sea anemones S. haddoni, H. crispa, M. doreensis, and Entacmaea quadricolor (one record); A. frenatus, with E. quadricolor; A.perideraion, with H. magnifica; and A. sandara-cinos, with S. meiiensii. Distribution of anemonefishes and their host sea anemones in various zones of the coral reef and the near-reef platform, over sandy-silt bottoms and basalt slopes is reviewed and the depth of occur­ rence is given for all species. Some biological aspects of anemonefishes and their host sea anemones are described. The broad distribution of A. polymnus on sandy-silt bottoms in predominant association with S. had­ doni and more rarely with H. crispa and M. doreensis is recorded. Our current knowledge of systematics of anemone­ fishes is based on Allen's revision composed in the early 1970s (1972) and more recent works of the same author (Allen, 1975a, 1975b, 1980, 1991). Information on taxonomic composition of anemonefishes of Viet­ nam is quite scattered and until recently was restricted to only few works. Chevey (1932) described Atnphip-rion macrostoma and A. bifasciatum annatnensis off the Vietnamese coast, which were subsequently recog­ nized by Allen (1972) as junior synonyms of A. frenatus and A. polymnus, respectively. The same author (Allen, 1972), based on investigations of museum mate­ rials, noted the presence of A. frenatus in the collec­ tions from south Vietnam (Nhatrang Bay) and A. clarkii off the coast of Vietnam (the exact location is not known). Later (Allen, 1980; Allen in Fautin and Allen, 1992), this author automatically expanded the distribu­ tion range of yet another two species—A. ocellaris and A. perideraion—to coastal waters of Vietnam, which were documented to the north and to the south off Viet­ nam (Allen, 1972), and in the more recent work (Allen in Fautin and Allen, 1992), expanded the distribution range (without reference to material) of Premnas bia-culeatus to the northwest up to central Vietnam. In the most recent paper, Allen (Allen in Randall and Lim, 2000) reconsidered this point of view and removed P. biaculeatus from the list of species of Pomacentridae of the South China Sea.
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Chapter
To provide a background for the investigations dealt with in this paper, it is necessary to summarize some fundamental experiments on the protection of anemone fishes.