BIOLOGY OF SEA ANEMONES
Sea anemones that are host to clownfishes, like many tropical actinians and some temperate ones, harbour unicellular algae within the cells of their tentacles and oral disc (see Introduction). A portion of the sugars produced by these plants through photosynthesis are "leaked" to their host. This may be the anemone's major source of energy. The widely flared oral disc of many host actinians serves not only to accommodate fish, but its large surface area is well adapted for intercepting sunlight.
However, actinians, like all coelenterates, capture and digest animal prey with their nematocysts. We have found small fish, sea urchins, and a variety of crustaceans (shrimps and crabs) in the coelenteron of host anemones. They also appear to feed on planktonic items conveyed by the currents. Although the energy they derive from photosynthesis may be sufficient to live, the anemones need sulfur, nitrogen, and other elements in order to grow and reproduce. These animals are not voracious predators: their prey probably consists of animals that bump into them (e.g. a fish fleeing a more active predator) or stumble over them (e.g. a sea urchin, which has no eyes). Therefore, the supply is probably small and irregular. A more predictable source of these nutrients may be from wastes of their symbiotic fish. This issue deserves to be studied scientifically. Anemones of some species are capable of absorbing nutrients directly from seawater through their thin tissues, and that may be another source of nutrition for these animals as well.
It is impossible to determine age of a sea anemone, except for one that has been raised in an aquarium or tracked continuously in the wild from first settlement. A small one is not necessarily young, for coelenterates grow only if well fed and shrink if starved. Individuals of species that harbour anemonefishes have been monitored for several years with no apparent change in size (although that is difficult to measure, due to the absence of a skeleton). However, studies on other species, in field and laboratory, have led to estimated ages on the order of many decades and even several centuries. There are scattered records of temperate anemones surviving many decades in commercial aquaria, and the life-span of a small sea anemone in New Zealand has been calculated, based on actuarial tables, to be over 300 years! From such data, it is likely that most individuals of the "gigantic" sea anemones we have encountered during our field work exceed a century in age. This is also consistent with the generalization that large animals of all kinds typically are long-lived.
Coelenterates are protected quite well by their nematocysts, but some predators have developed means of evading their effect. Small tropical anemones may be eaten by butterflyfishes (see chapter 5), but large ones appear to have few enemies, and we do not know what might ultimately kill them.
All coelenterates reproduce sexually. An individual of some species may produce both eggs and sperm; host anemones appear to have separate sexes, with an individual being either male or female its entire life. The typical coelenterate pattern is that of most marine animals, one that is fraught with dangers and uncertainty -- release of eggs and sperm into the sea, where fertilisation occurs and a larva (a tiny animal looking nothing like its parent that drifts in the sea) develops for several days or weeks before settling in an appropriate habitat. Many species spawn in response to an environmental cue such as a full moon or low tide so that eggs and sperm are in the same place at the same time. Typically, marine animals produce millions of tiny larvae, but the world is not overrun with them, proving that very few survive -- usually just enough to maintain a stable population. The rest of the larvae serve as food for a sea full of potential predators. Finally, the surviving larvae must find an appropriate habitat (how anemonefishes might do this is discussed in chapter 4).
We do not know if host actinians follow this pattern. There is a bit of evidence that in at least some species, the eggs are not released, but are fertilised inside the mother (this is not especially rare in corals and anemones; sperm enter the mother with water that is constantly being pumped in and out, and which carries food and oxygen also), where they grow to be released as tiny sea anemones. What is certain is that we seldom see small individuals of most host actinians in nature. However, it is not unusual to find large ones with ripe eggs and sperm. Therefore, we believe that successful recruitment must be rare. Very few eggs may be fertilised, or few larvae may survive, or larval settlement may be difficult, or young anemones may have high mortality (perhaps especially when they are too small to harbour fish). The apparent rarity of successful reproduction is also biologically consistent with long life.
In addition to sexual reproduction, some coelenterates undergo asexual reproduction. Entacmaea quadricolor is one of these. A polyp can divide longitudinally, resulting in two, somewhat smaller individuals, probably within the space of a few days. Each then grows to an appropriate size, divides, and so on. All descendants of the original anemone (the result of sexual reproduction) form a clone, a group of genetically identical individuals. In this species, each polyp is relatively small, but clonemates remain next to one another so their tentacles are confluent, and the associated anemonefish apparently regard them as a single large anemone.
This is so mainly for shallow-water individuals; those in deeper water grow large, and do not divide (see chapter 1). Several other species of actinians also have two different reproductive modes: small animals that clone and large ones that do not. This appears true of Heteractis magnifica, too. In the center of its range (i.e. in eastern Indonesia, on the Great Barrier Reef, in New Guinea), it occurs as single, large individuals. To the east and west (i.e. in western Indonesia and Malaysia, and in Tahiti), several to very many small individuals of identical colouration are typically clustered together, appearing to be a single large (or huge!) anemone. Based on their shared colour and their proximity, we infer that they are clonemates.
Once they settle from the plankton, most anemones seldom move from place to place. Although they are usually damaged when people try to collect them, actinians do have the ability to detach from the substratum, partly or entirely. Small, temperate anemones can do this in response to predators or unfavorable physical factors. Indeed, those of a few species can "swim," awkwardly launching themselves into the water briefly, a motion that often puts them beyond reach of the predator that provoked the activity. More typically, an individual glides on its pedal disc, covering a few millimeters in a day, or it may detach entirely, and roll or be carried quite a distance. That this is not terribly rare is attested by large animals suddenly appearing in well studied areas.
Sea anemones are very similar to corals. One of the solitary mushroom corals, Heliofungia actiniformis, extends its tentacles by day (most do so only at night) and looks very much like an actinian (hence its specific name). Could it not harbour clownfish? In an aquarium lacking an anemone, we did have a clownfish take up residence among a mushroom coral's tentacles. But it does not happen in nature. However, a small, snow-white pipefish, Siokunichthys nigrolineatus, lives among the tentacles, much like an anemonefish.
Corals and sea anemones differ not only in the respective presence and absence of a skeleton, but also in the types of nematocysts they possess and in their anatomy. Intermediate between them are corallimorpharians, skeletonless polyps having coral-like nematocysts and anatomy. In fact, some coelenterate experts regard corallimorpharians simply as corals without skeletons.
The corallimorpharian Amplexidiscus fenestrafer, the largest species known, resembles some host anemones. Bill Hamner first documented their feeding behaviour, in which prey is rapidly enveloped by the oral disc that closes like a draw-string purse. The mouth is then opened, the prey being swallowed and killed within the polyp. On several occasions he kept corallimorpharians in the same aquarium with anemonefishes, only to discover the following day that a fish was missing. He found that at night a fish settled onto the corallimorpharian's oral disc, just as it would with a host anemone, thereby provoking the draw-string response and subsequent ingestion. Their superficial similarity to some host anemones, and their living in areas of the reef where plankton accumulates, led us to speculate that these corallimorpharians might "lure" naive anemonefish larvae to attempt to settle in them. Of course, the possible mimicry of a host anemone, and the resultant predation on naive fry, requires that at least some anemonefish larvae recognize hosts at least in part visually (see chapter 4).
LIFE HISTORY OF ANEMONEFISHES
The life history of many pomacentrids, and particularly Amphiprion, is well studied. Most research on anemonefishes has focused on A. bicinctus, A. chrysopterus, A. clarkii, A. melanopus, A. ocellaris, A. perideraion, and A. tricinctus, which are all similar in courtship and spawning, and in subsequent development of eggs, larvae, and young.
COURTSHIP, SPAWNING, AND INCUBATION
Within the tropics, spawning occurs throughout most of the year, although there may be seasonal peaks of activity. In subtropical or warm temperate seas (for example, in southern Japan), reproductive activity is generally restricted to spring and summer, when water temperatures are highest. At Enewetak Atoll (about 11oN in the central Pacific), spawning is strongly correlated with the lunar cycle: most nesting occurs when the moon is full or nearly so. Moonlight may serve to maintain a high level of alertness in the male, which assumes most of the nest guarding duties. Moreover, because newly hatched larvae are attracted to light, moonlight may draw them towards the surface, thereby facilitating their subsequent dispersal by waves and currents.
Amphiprion and Premnas are unique among damselfishes in forming permanent pair bonds that sometimes last for years. In other damsels, one male may mate with several females during a single spawning episode, and different sets of females are often involved in subsequent spawnings. However, pair-bonding in most species of clownfishes is very strong and is correlated by the small size of their territories (centered on actinians) which is, in turn, correlated with the unusual social hierarchy that exists in each "family" group. Details of this social structure will be given later.
Courtship in anemonefishes, as in all pomacentrids, is generally stereotyped and ritualised. Several days prior to spawning, there is increased social interaction, as expressed by chasing, fin-erection, and nest preparation. Another activity, which occurs in many damselfishes, is "signal jumping": the male swims rapidly up and down, as though on a roller-coaster. In anemonefishes, the male becomes particularly bold and aggressive, chasing and nipping his mate. He also displays by fully extending his dorsal, anal, and pelvic fins, while remaining stationary in front of or beside her. During the nuptial period, he selects a nest site, usually on bare rock adjacent to the anemone. Initially the male spends considerable time clearing algae and debris from the site with his mouth; he is eventually joined in these activities by his mate.
Spawning, which occurs most often during morning hours, generally lasts from about 30 minutes to more than two hours. Once it commences, the tiny, conical ovipositor of the female is clearly visible. A number of eggs are extruded through this structure on each spawning pass, when the female swims slowly and deliberately in a zig-zag path with her belly just brushing the nest surface. She is followed closely by her mate, who fertilises the eggs as they are laid. Numerous passes occur during each spawning session. The number of eggs deposited ranges from about 100 to over 1000, depending on the size of the fish and on previous experience. In general, older, more experienced pairs produce more eggs than do recently formed pairs.
Amphiprion and Premnas eggs are elliptical or capsule-shaped, are about 3-4 mm in length, and adhere to the nest surface by a tuft of short filaments. They incubate six to seven days. Just prior to hatching, the embryo, which has undergone rapid development, is clearly visible through the transparent egg membrane: the most noticeable features are the large eyes with their silvery pupils, and the red-orange yolk sac that is responsible for the general colour of the entire egg mass when viewed from a short distance. Throughout incubation, the nest is meticulously guarded and cared for by the male. He aggressively chases other fishes from its vicinity, especially potential egg-eaters such as wrasses. He frequently visits the nest to fan the eggs with his pectoral fins and to remove dead eggs and debris with his mouth. The female is mainly occupied with feeding during this time, but occasionally assists the male with his duties.
LARVAL LIFE AND SETTLEMENT
Hatching generally occurs during the evening, shortly after dark on the sixth or seventh day after the eggs are laid. In an aquarium, the freshly hatched fish first sink to the bottom, but within a few minutes, swim to the upper part of the tank. The larvae are about 3-4 mm total length and transparent except for a few scattered pigmented spots, the eye, and the yolk sac. Recent studies of larval duration in damselfishes have greatly improved knowledge of early life history stages. By counting the daily growth rings in the ear bones (otoliths) with an electron microscope, scientists can determine the time between hatching and transformation to the juvenile stage. There is much variation between species of damselfishes, with the longest larval stages about 6-8 weeks. Clownfishes have the shortest larval period of damsels, ranging from about 8 to 12 days. It is assumed that during this time they are planktonic -- living in the surface waters of the ocean, where they are passively transported by currents. The short larval stage of anemonefishes is no doubt responsible for the localised distribution of many species.
The larval stage terminates when a young fish settles to the sea bottom and begins to assume the juvenile colour pattern. Aquarium observations indicate this metamorphosis is a rapid process, occurring within a day or so. At this stage it is vital for the young Amphiprion or Premnas to find a suitable anemone host or it will surely be consumed by one of its many predators. There is evidence that fish of some species can actively search and follow a trail of chemicals released by a host anemone, but others seem not to do that, and may locate a suitable host by sight, or simply encounter one by chance. For fish of some species, it takes several hours to become fully acclimated to the anemone once it is located; this is achieved by a series of progressively longer contacts with the tentacles, like the elaborate "acclimation behaviour" seen when an adult fish is artificially removed from its host. Other fishes seem capable of swimming right in without harm, according to Miyagawa (see chapter 5). Although she denied they go through "acclimation behaviour", she described swimming that resembles such behaviour. With 10 species of host actinians and 28 species of fish, there are probably many variations on how hosts are located and adapted to.
We assume that metamorphosis requires the presence of an anemone, since the fishes seem defenceless without one. We and others have done experiments proving that even adult anemonefishes cannot survive for long without the protection of a host actinian. What is obvious is that there are far fewer open slots available in appropriate anemones than there are fish to fill them. So there must be tremendous mortality among fry and larvae.
Even if it successfully locates an anemone, the immediate survival of the fish is not guaranteed. If the host is already occupied by anemonefish, the unusual social structure of the inhabitants makes life difficult for a newcomer. The number of fish that occupy a single anemone depends on species of fish, size of host, and sometimes size of the fish as well, but typically there is an adult pair and two to four smaller fish. As will be explained more fully below, the largest fish is usually the female and the next largest individual is her mate. A hierarchy, or "peck-order", exists in which the female is the dominant individual. There is generally an amicable relationship between the adult pair, and aggressiveness by the female is largely channeled into ritualised, non-harmful displays. Aggression is more overt farther down the hierarchy. The male spends considerable time chasing and "bullying" the next largest individual, which in turn vents its aggression on the smaller fish. Therefore, a new arrival becomes the immediate target for the resident fish. Attacks may be so severe as to drive away the newcomer, who must find another anemone or perish.
SOCIAL STRUCTURE AND SEX REVERSAL
The phenomenon of sex reversal is an intriguing component of anemonefish life history, the details of which have been discovered only in the past decade. Sex change occurs in many fishes. For example, it is now well established that most wrasses (Labridae) and parrotfishes (Scaridae) begin adult life as females and later assume the more colourful male phase. Similar changes are widespread among gropers (Serranidae), particularly in the subfamily Anthiinae, commonly known as fairy basslets. Therefore, it was not surprising to discover that this phenomenon extends to some pomacentrids as well. However, the unusual aspect of sex reversal in clownfishes is that the change is from male to female (protandrous hermaphroditism; the more common sort is protogynous hermaphroditism). As mentioned above, the largest and socially dominant fish in a particular anemone (or cluster of anemones in the case of Entacmaea quadricolor) is generally the female, whose gonads are functioning ovaries with remnants of degenerate testicular tissue. The smaller male, which in species such as A. frenatus and P. biaculeatus may be less than half the size of the female, has gonads that are functioning testes but also possess non-functioning or latent ovarian cells. If the dominant female dies or is experimentally removed, the male's gonads cease to function as testes and the egg producing cells become active. Simultaneously, the largest of the non-breeding individuals becomes the functioning male. This adaptation allows continuous reproduction; without it, an adult would have to await the arrival of a fish of the appropriate sex (which it would be only 50% of the time), thereby losing valuable breeding time, or it would have to seek out a mate, leaving its anemone and thereby risking predation both on itself and on its symbiont.
There is no difference in colouration between sexes in most anemonefishes, but there are exceptions. The sex-related colour difference is not always present in A. clarkii. In addition, slight differences may occur between sexes of A. perideraion and A. akallopisos. Males of both species often have orange margins on the soft dorsal and caudal fins. In P. biaculeatus, colour differences may be related more to size than to sex per se.
FEEDING AND GROWTH
Small, non-breeding fish are not necessarily young. The rigid social structure exerts a "stunting" effect on growth. Small fish use considerable energy fleeing from attacks of larger fish, and time that they might otherwise spend feeding is used in avoiding larger anemonefish. Moreover, it is especially unsafe for small individuals to range very far from the refuge of their anemone. Consequently, the smaller a fish, the less time it is able to devote to foraging, the more restricted its feeding area, and the more energy it must dedicate to evasionary activities. Members of the dominant pair range widely to feed, with fish of larger species, such as A. clarkii, swimming many meters from their actinian to forage. When a fish is removed from the "queue", all those smaller than it grow rather rapidly, filling in the size gap. This is especially true of members of the mated pair: if the dominant female is removed, the new female (previously functioning as male) not only changes sex, but grows at an accelerated rate. The new male may grow even faster. Presumably this growth spurt is a result of a fish's being harassed less as it moves up the queue, and thereby having more time to feed.
Planktonic food is of major importance to most anemonefish. Copepods and larval tunicates are among the most common items found when their stomach contents are analysed. Fish of at least one species, A. perideraion, eat significant amounts of algae, which is both grazed from the surrounding reef and consumed in midwater.
Details of longevity are lacking for anemonefish of most species, but some are recorded to have lived at least 6-10 years in nature. The record for captive fish is 18 years, for Amphiprion frenatus and A. perideraion maintained at the Nancy Aquarium in France. The individual of A. perideraion was still alive when this book was written.