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FOREWORD
Anemonefishes and their invertebrate hosts have delighted the
western world since 1881 when the first captive specimens were
kept in a tub of seawater. However, it was not until the mid-20th
century that the intimate relationship of these tropical animals
began to be known worldwide. With the advent of SCUBA diving and
the establishment of commercial air routes to equatorial destinations
in the Indian and Pacific Oceans, pristine coral reefs became
accessible to an increasing audience. Skin-diving tourists, sport
divers, naturalists, and marine scientists have all helped contributed
to underwater discoveries, among them the fascinating natural
history of anemonefishes. Virtually all large public aquaria have
at least one anemonefish display, and these animals have been
at or near the top in aquarium fish sales for the past three decades,
attesting to their tremendous popularity.
In view of this unprecedented public exposure to the fascinating
relationship between sea anemones and fishes, we have written
a book with needs at all levels, from teen-age aquarist to research
scientist, in mind. Because of confusion in sea anemone taxonomy,
previous works on this subject often used incorrect or outdated
names. This book permits quick and accurate identification of
the invertebrate hosts, as well as the fishes, through well-illustrated,
easy-to-use keys and underwater photographs. It is the first publication
on these animals designed as a field guide. We hope that it will
add even greater pleasure to your fish-watching endeavours and
provide new insights into the symbiotic relationship of fishes
and sea anemones.
We are grateful to the Christensen Research Institute for making
our long-held dream of writing this book come true.
Daphne G. Fautin
Gerald R. Allen
INTRODUCTION
While standing in the water, breast high, admiring this splendid
zoophyte [sea anemone], I noticed a very pretty little fish which
hovered in the water close by, and nearly over the anemone. This
fish was six inches long, the head bright orange, and the body
vertically banded with broad rings of opaque white and orange
alternatively, three bands of each . . . . I made several attempts
to catch it; but it always eluded my efforts -- not darting away,
however, as might be expected, but always returning presently
to the same spot. Wandering about in search of shells and animals,
I visited from time to time the place where the anemone was fixed,
and each time, in spite of all my disturbance of it, I found the
little fish there also.
Dr. Cuthbert Collingwood: Rambles of a Naturalist on the Shores
and Waters of the China Sea (John Murray, London, 1868, page
151)
That was how the first person to record the remarkable living
arrangement of anemonefishes (or clownfishes) and some sea anemones
described his discovery on Fiery Cross Reef, off the shores of
Borneo. He was captivated by what continues to fascinate anyone
who has had the good fortune to see these animals "at home,"
in the shallow tropical waters of Indian and Pacific Oceans. It
is their beauty, and it is their intimate symbiosis. (Symbiosis,
a word that literally means "living together," is used
by scientists to describe the relationship between unrelated species
of plants and/or animals that live in close association.)
The symbiosis between clownfishes and sea anemones fascinates
diver and biologist alike for many of the same reasons. The sea
anemones that play host to the fishes are, like most of their
kin, virtually immovably fixed. Each anemone constitutes the territory
of its fish, which therefore seldom venture far from it, retreating
into its tentacles when feeling threatened. This sedentariness,
which so intrigued Dr. Collingwood, allows biologists to do long-term
studies, revisiting the same animals repeatedly. Underwater enthusiasts,
having once found them, can be assured of relocating fish and
anemones on future dives. The fish can be approached very
closely, and both partners are extremely beautiful, making them
a prime subject of photographers.
GEOGRAPHICAL AND ECOLOGICAL DISTRIBUTION
Sea anemones live throughout the world's oceans, from poles to
equator, and from the deepest trenches to the shores, as do fishes.
But no one kind of either lives in all places. Of nearly 1000
species of sea anemones, only 10 are host to anemonefishes. They
live in the parts of the Indian and Pacific Oceans that lie within
the tropics or where warm, tropical waters are carried by currents,
such as the east coast of Japan (as far north as the latitude
of Tokyo!). Because the 28 species of clownfishes live only with
these 10 species of sea anemones, they are found in the same places.
The richest part of the world for these animals is around New
Guinea: we have found eight species of fishes and anemones in
the d'Entrecasteaux Islands off the east coast of that island,
and all 10 host anemones with nine fishes around Madang, on the
north coast of Papua New Guinea. The numbers of both diminish
outward from there. Typically, a central Indo-West Pacific locality
such as Guam, or Lizard Island on the Great Barrier Reef, has
up to five different species of fishes and about an equal number
of anemone species. Numbers are even smaller at the peripheries
of their range. For example, one kind of fish and three of host
anemones are known from the Comoro Islands, and no clownfishes
but one host sea anemone species occurs in Hawaii.
These anemones, and their anemonefishes, exist only in shallow
water, no deeper than SCUBA-diving depths. That is because within
the cells of an anemone's tentacles and oral disc live microscopic,
single-celled, golden-brown algae (dinoflagellates) called zooxanthellae.
Like all plants, they require sunlight for photosynthesis, a process
in which solar energy is used to make sugars from carbon and water.
Some of these sugars fuel the algae's metabolism, but most of
them "leak" to the anemone, providing energy to it.
Therefore, the anemones that are host to clownfishes must live
in sunny places. The amount of light in the sea diminishes rapidly
with depth because water filters out sunlight. Turbidity also
diminishes light penetration. So these anemones live at depths
of no more than about 50 m, generally in clear water. (Reef-forming
corals also contain algae, and coral reefs occur only in shallow,
mostly clear water for the identical reason.)
Anemonefishes live in habitats other than reefs, but are usually
thought of as reef dwellers because that is where most tropical
diving occurs. Other habitats may be less colourful and diverse
than reefs, but they can be equally fascinating. About as many
species of host actinians (= sea anemones) live on sand-flats
surrounding coral reefs, or even at some distance from reefs,
as live on reefs themselves. Individuals of some species can survive
in muddy areas, but they generally lack fish symbionts. Even on
reefs, most species of host actinians are inconspicuous, unlike
their partner fish. Spotting the fish first, then frightening
it so that it takes refuge in its anemone, or (preferably) waiting
patiently for its periodic bathe among the tentacles, is often
the best way to locate an actinian.
HOW IS THIS RELATIONSHIP POSSIBLE?
At the time of Collingwood's discovery, some species of fishes
and anemones involved in this relationship had been known to science
for a century already. Why had nobody reported their living arrangement
before? We can only speculate. Perhaps poisons had been used to
collect the fish, which causes them to float to the surface, so
nobody could know where they had come from. Perhaps collectors
saw fish living in anemones but did not appreciate its significance.
Or quite possibly it was seen and simply not believed, so unlikely
is an anemone as home to a fish.
Lovely, accessible -- and a most unlikely partnership. Sea anemones
are related to corals and more distantly to jellyfishes. Common
to all of these animals are nematocysts, the harpoon-like stinging
capsules that give jellyfish their sting, fire coral their burn,
and the tentacles of some sea anemones their stickiness. The microscopic
nematocysts, which are manufactured inside cells (but are not
themselves cells), are particularly dense in tentacles and internal
structures. Those of the tentacles function in defence and prey
capture; internal nematocysts are essential to digestion. Within
each capsule is coiled a fine tubule many times the capsule's
length. When the capsule is stimulated to fire (a combination
of chemical and mechanical stimuli is necessary to trigger most
kinds; there are over 30 in all), the tube shoots out, everting
like the sleeve of a coat turned inside out, to penetrate or wrap
around the target. Many types of nematocysts, although probably
not all, contain toxins, which are delivered to predator and prey
by or through the everting tubule.
The existence and function of nematocysts were known before the
anemonefish symbiosis was described. And so, when Collingwood
first reported "the discovery of some Actiniae of enormous
size, and of habits no less novel than striking," his prime
concern was with how the fish managed to survive in an environment
that is deadly to most fishes, even some much larger than anemonefishes.
Over the years, many biologists have suggested ways in which it
might be possible for the fish to survive in its hostile environment.
Among the hypotheses [and reasons for discarding them] were the
following. 1) Tentacles of these particular anemones do not contain
nematocysts. [Not only are there nematocysts, but those of all
10 species of host actinians are typical in kind and quantity
to those occurring in the majority of sea anemones.] 2) The fish
do not actually touch the tentacles. [While this is certainly
true of some Caribbean fish that seek protection behind and under
sea anemones, genuine anemonefishes swim among tentacles, and
sleep on the oral disc at night.] 3) The skin of anemonefishes
is thicker than normal so nematocysts cannot penetrate it. [It
differs little from that of other damselfishes, and may even be
slightly thinner. Indeed, an unprotected anemonefish can be killed
by its host's sting.] 4) While a fish is present, the anemone
will not fire its nematocysts. [Although a sea anemone can exert
some control over firing, this cannot be the solution to the riddle,
because an actinian can sting and capture prey while harbouring
clownfish.]
Anemonefishes are easily kept in aquaria, many of which are as
large as the fish's normal territory. Both fishes and sea anemones
survive -- apparently quite well -- when separated from one another.
However, if the separation lasts more than a few days or weeks,
depending on the species involved, when the partners are reunited
and the fish swims into the host's tentacles, it withdraws rapidly,
appearing (sometimes very obviously, sometimes less so) to have
been stung. Thus the protection of the fish is elicited or acquired,
and can disappear. A fish that had been living alone will be stung
by an anemone in which another clownfish is being harboured, so
the fish, rather than the actinian, is responsible for the protection.
But a stung anemonefish returns to its host repeatedly, going
through an elaborate, stereotyped swimming dance, gingerly touching
tentacles first to its ventral fins only, then to its entire belly.
Finally, after a few minutes to several hours of such "acclimation"
behaviour, it is able to dive right in.
Some anemonefishes nibble at their host's tentacles, which it
had been speculated might immunize them against the sting. But
the fish are not immune to being stung, as is sometimes stated.
Immunity is a physiological response that extends throughout an
animal's body. Experiments by Davenport and Norris conclusively
proved that the protective agent resides in the mucus coating
that anemonefishes, like all fishes, have on their surface. But
what is the source of this protective mucus?
One theory is that it comes from the host actinian. Supporters
of this theory (Schlichter foremost among them) believe that during
its elaborate "acclimation" swimming when contact is
initially made with its host, the fish smears mucus from the anemone
all over itself. Just as the sea anemone does not sting itself,
it does not sting a fish, or any other object, covered in its
mucus. The fish is thereby chemically camouflaged: it is, essentially,
a fish in anemone's clothing. The fish's normal behaviour of returning
to its anemone at least once a minute can be interpreted as serving
to maintain its protective layer of mucus. According to this theory,
what allows clownfishes to live in this peculiar habitat is their
unusual behaviour.
Finding anemone mucus on many objects with which the animal regularly
comes in contact, such as the rocks and algae around it, other
scientists (Lubbock foremost among them) believe that its presence
on a fish is the result of the fish's being protected rather
than its cause. The fish's own mucus has evolved to lack
components that stimulate nematocyst discharge, according to this
theory, and "acclimation" behaviour may be an artifact
of artificially separating animals that normally never are parted.
The secret to clownfishes' peculiar habitat, according to this
interpretation, is their unusual biochemistry.
As in so much of science, there is probably truth on both sides.
Although all anemonefishes are closely related and share an unusual
habitat, they vary in some aspects of their biology, including
how far they venture from their home, how many fish occupy a single
anemone, and which hosts and how many host species they occupy
(Table I). Similarly, they may not all adapt to an actinian in
the identical manner, as is generally assumed, with behaviour
and biochemistry probably both playing roles to varying degrees.
We believe that for fish that live with many types of hosts (such
as Amphiprion clarkii, which is the least host-specific),
behaviour is likely to be more important to adaptation, whereas
for host-specific fish (such as Premnas biaculeatus), biochemistry
is probably the more significant factor. An experiment by Brooks
and Mariscal provided evidence that both fish and anemone may
be active in forming the symbiosis for at least one combination
of fish and anemone species. The average acclimation time following
prolonged separation of A. clarkii from the host anemone
Macrodactyla doreensis was two and a half hours, but a
fish kept in an aquarium with a surrogate sea anemone made of
rubber bands glued to a Petri dish required an average of only
20 minutes to acclimate to a real anemone. Thus it would appear
that the fish does produce an especially protective mucus when
living in what it perceives to be a sea anemone, but since it
must still undergo a period of acclimation, that alone does not
suffice. Presumably, the anemone alters what is there, or adds
to it.
OTHER SYMBIONTS
Some host actinians harbour small mostly black damselfish of the
genus Dascyllus . However, this fish is not considered
to be a true anemonefish, as are the members of genera Amphiprion
and Premnas, because their lives are not dependent on the
anemone host. Rather, when small, they may live with actinians;
as they grow, they become independent. Sometimes Dascyllus
is the only fish in an anemone; sometimes it shares its host with
true anemonefish. In addition, other fishes, particularly young
wrasses, are sometimes seen in close proximity to sea anemones,
although only members of Thalassoma make infrequent contact
with the tentacles. Organisms that may, but need not, live with
those of another, unrelated species are termed "facultative
symbionts." Those that must, such as clownfishes, are "obligate
symbionts."
In addition to having algal symbionts and fish symbionts, some
species of these sea anemones harbour shrimps and crabs. Because
of their small size, and because they cannot easily be tagged
or recognized individually and they scurry under the overhang
of the anemone's oral disc when disturbed, they have hardly been
studied. Therefore, in contrast to anemonefishes, we do not know
how closely their lives are tied to the anemones, and whether
they are obligately or facultatively symbiotic.
Some sea anemones outside the tropical Indo-West Pacific have
facultative fish associates. No fewer than 30 species of Caribbean
fishes may occur in or near anemones. Some, like Dascyllus,
engage in this association only when small. Most never actually
come into contact with the anemone's tentacles, but merely hover
around them. Presumably, even proximity to an anemone confers
some benefit. In the cold waters of British Columbia, Canada,
some small individuals of the convict fish, Oxylebias pictus,
sleep lying in the tentacles of the sea anemone Urticina lofotensis.
They leave during the day, but return to the same anemone each
night. As the fish grows, it returns less regularly, until it
outgrows its "security blanket" altogether.
SCIENTIFIC NAMES AND WHAT THEY MEAN
In this book, we use both common and scientific names for fishes
and anemones. The common names are in English; a Japanese translation
of our book would use an entirely different set of Japanese common
names. But a scientific name is always in Latin. This began in
the era when Latin was the language of learning, and assures that
reader and writer, or speaker and listener need not share a language:
regardless of what languages they speak, both mean the same kind
of animal when they use a particular name.
A Latin, or scientific, name consists of two parts -- a genus
(always capitalised; its plural is genera) and a species (never
capitalized; its plural is also species). It is italicized (in
print) or underlined (in typing or hand-writing) to identify it
as being in Latin. Similar species are placed in the same genus.
Two species in the same genus are more alike, and are considered
more closely related evolutionarily, than are two species in different
genera. The first time a generic name is used in a piece of writing,
it must be spelled out, but subsequently it may be abbreviated
in a way that will not cause confusion. In this book, for example,
A. stands for Amphiprion. A generic name may be
used by itself, without a species name, but the reverse is not
allowed. That is because the same species name may be used for
species that belong to different genera -- but each combination
of the two is unique.
The generic and/or specific name of an organism often alludes
to some conspicuous feature of it, or to where it lives. For example,
Stichodactyla gigantea is among the largest sea anemones,
and Amphiprion chagosensis lives only in the Chagos Archipelago
of the Indian Ocean. It may also honor someone important in its
discovery, such as S. haddoni, which memorializes Alfred
C. Haddon, one of those 19th century all-round naturalists, who
did anthropological research in northern Australia, but collected
sea anemones on the side.
We provide the most accurate, current name for each species of
fish and actinian, as well as some of the other names (synonyms)
by which it has been known. Although each species has only one
valid scientific name, it may have been given other names during
the past. This is frequently the case for highly variable animals,
such as Amphiprion clarkii, to which more than 10 names
have been applied! In our studies of hundreds of animals from
many localities, we were unable to find consistent, significant
differences in those that have been called by different names,
and so concluded that the name A. clarkii is appropriate
for all of them. There is another reason for multiple names. Several
species of host sea anemones were first found in the Red Sea.
Animals of the same species subsequently collected from the East
Indies or Australia were commonly given new names. This may have
been partly because communications were poor in those days --
scientists were unaware that a particular species had already
been described. But more likely, early biologists probably did
not imagine that animals collected thousands of kilometers apart
might belong to the same species. So which of the many names should
be used? Usually, it is the oldest one. This gives the first person
to have named it credit for the discovery. For example, although
Radianthus ritteri is a name that has commonly been used
for one species of sea anemone, the valid name for that species
is the earlier described Heteractis magnifica; the former
dates from 1898, and the latter from 1830.
Each binomial scientific name uniquely applies to only one species,
but the following example illustrates how multiple uses for the
same name may arise. Stichodactyla gigantea was named by
Europeans to whom anemones of this species, first seen in the
Red Sea, was indeed gigantic, in comparison with most temperate
anemones. We now know that the name S. gigantea does not
belong to the largest sea anemone, although that is a logical
assumption, leading some people to apply that name to the largest,
which is actually S. mertensii. It is especially important
in symbioses to identify the partners accurately because the relationships
between different partners are not necessarily the same.
The name(s) of the person(s) who described the species, and the
year in which the description was published, are part of the formal
scientific name, but are not always appended to it. If a particular
name has been used more than once, this allows the reader to know
in which sense it is being used and to determine when the name
was proposed. If the name of the author is in parentheses, the
species has been transferred from the genus in which it was originally
described. For example, Heteractis magnifica was originally
named Actinia magnifica by Quoy and Gaimard in 1830, when
nearly all sea anemones were placed in the genus Actinia.
As more species were discovered, and we learned which are closely
and which distantly related, additional generic names were created,
each referring to a group of closely related species.
The names Stichodactyla and Heteractis are used
for anemones that were, in general, previously referred to as
Stoichactis and Radianthus, respectively, in the
technical literature, and still are in some popular writing. The
names we use were selected not only because they are senior, but
more importantly because the old names were used inconsistently.
Both names, for example, had been used to refer to species in
both genera. Species of other genera had also been referred to
them, and species that belong in Stichodactyla and Heteractis
had been called by other generic names. We hope that this book
will set a standard so that divers, hobbyists, aquarists, and
scientists alike will use the same name in the same way, avoiding
such confusion in future.
HOW TO USE THIS GUIDE
In the following two chapters, we explain how to identify the
10 species of host sea anemones and the 28 species of anemonefishes,
and characterise each. We describe the morphological features
of an animal most important to its identification in the field,
as well as geographical range and typical habitat.
The most important aspect of a fish's habitat is obviously its
host; the anemone's habitat specificity will govern where fish
associated with it are found. Species of partner may or may not
be an important clue in identification. For example, if you find
a fish you can identify as P. biaculeatus, you have also
identified the anemone with which it is living, for it is known
only from Entacmaea quadricolor. However, identifying an
anemone as E. quadricolor is not much help in identifying
a fish occupying it; 12 species of clownfishes other than P.
biaculeatus are symbiotic with it. Conversely, finding Amphiprion
clarkii in an anemone is no help, because it occurs with all
10 host actinians. But the fish in Cryptodendrum adhaesivum
is certainly A. clarkii, the only fish known to live with
it. Using a symbiont to identify its partner is valid only in
the field. In captivity, many fish can adapt to living with almost
any host actinian, in addition to numerous exotic ones (that is,
anemones from elsewhere, with which anemonefishes are not naturally
found).
Usually fish of only one species occur with an individual actinian,
but occasionally fish of two species may share a host (usually
a large one, which they divide into exclusive territories, so
in a sense they are not actually sharing the space). It is possible
that rarely three may coexist. But these instances are sufficiently
uncommon that they bear close scrutiny. The species summaries
in Chapter 3 describe variations in colouring with age, or variations
in striping with size, for example, that may lead to misidentifications.
In the later chapters, we discuss biology of the actinians, biology
of the fishes, and how the two influence one another. We conclude
with a chapter on keeping these lovely animals in aquaria.
