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 Because of confusion in sea anemone taxonomy, previous works on this subject often used incorrect or outdated names.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
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.
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.
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.
