SYMBIOSIS

CONCEPT

Symbiosis is a biological relationship in which two species live in close proximity to each other and interact regularly in such a way as to benefit one or both of the organisms. When both partners benefit, this variety of symbiosis is known as mutualism. The name for a situation in which only one of the partners benefits is far more well known. Such an arrangement is known as parasitism, and a parasite is an organism that obtains nourishment or other life support from a host, usually without killing it. By their very nature, parasites are never beneficial, and sometimes they can be downright deadly. In addition to the extremes of mutualism and parasitism, there is a third variety of symbiosis, called commensalism. As with parasitism, in a relationship characterized by commensalism only one of the two organisms or species derives benefit, but in this case it manages to do so without causing harm to the host.

HOW IT WORKS

Varieties of Symbiosis

When two species—that is, at least two individuals representing two different species—live and interact closely in such a way that either or both species benefit, it is symbiosis. It is also possible for a symbiotic relationship to exist between two organisms of the same species. Organisms engaging in symbiotic relationships are called symbionts.

There are three basic types of symbiosis, differentiated as to how the benefits (and the detriments, if any) are distributed. These are commensalism, parasitism, and mutualism. In the first two varieties, only one of the two creatures benefits from the symbiotic relationship, and in both instances the creature who does not benefit—who provides a benefit to the other creature—is called the host. In commensalism the organism known as the commensal benefits from the host without the host's suffering any detriment. By contrast, in parasitism the parasite benefits at the expense of the host.

MUTUALISM: HUMAN AND DOG.

Mutualism is distinguished from the other two types of symbiosis, because in this variety both creatures benefit. Thus, there is no host, and theoretically the partners are equal, though in practice one usually holds dominance over the other. An example of this inequality is the relationship between humans and dogs. In this relationship, both human and dog clearly benefit: the dog by receiving food, shelter, and care and the human by receiving protection and loving companionship—the last two being benefits the dog also receives from the human. Additionally, some dogs perform specific tasks, such as fetching slippers, assisting blind or disabled persons, or tracking prey for hunting or crime-solving purposes.

For all this exchange of benefits, one of the two animals, the human, clearly holds the upper hand. There might be exceptions in a few unusual circumstances, such as dog lovers who are so obsessive that they would buy food for their dogs before feeding themselves. Such exceptions, however, are rare indeed, and it can be said that in almost all cases the human is dominant.

Obligate and Facultative Relationships

Most forms of mutualism are facultative, meaning that the partners can live apart successfully. Some relationships of mutualism are so close that the interacting species are unable to live without each other. A symbiotic relationship in which the partners, if separated, would be unable to continue living is known as an obligate relationship. In commensalism or parasitism, the relationship is usually obligate for the commensal or the parasite, since by definition they depend on the host. At the same time, and also by definition, the host is in a facultative relationship, since it does not need the commensal or parasite—indeed, in the case of the parasite, would be much better off without it. It is possible, however, for an organism to become so adjusted to the parasite attached to its body that the sudden removal of the parasite could cause at least a short-term shock to the system.

Inquilinism

A special variety of commensalism is inquilinism, in which the commensal species makes use of the host's nest or habitat, without causing any inconvenience or detriment to the host. Inquilinism (the beneficiary is known as an inquiline) often occurs in an aquatic environment, though not always. In your own yard, which is your habitat or nest, there may be a bird nesting in a tree. Supposing you benefit from the bird, through the aesthetic enjoyment of its song or the pretty colors of its feathers—in this case the relationship could be said to be a mutualism. In any case, the bird still benefits more, inasmuch as it uses your habitat as a place of shelter.

The bird example is an extremely nonintrusive case of inquilinism; more often than not, however, a creature actually uses the literal nest of another species, which would be analogous to a bird nesting in your attic or even the inside of your house. This is where the analogy breaks down, of course, because such an arrangement would no longer be one of commensalism, since you would be suffering a number of deleterious effects, not the least of which would be bird droppings on the carpet.

Inquilinism sometimes is referred to as a cross between commensalism and parasitism and might be regarded as existing on a continuum between the two. Certainly, there are cases of a creature making use of another's habitat in a parasitic way. Such is the case with the North American cowbird and the European cuckoo, both of which leave their offspring in the nests of other birds to be raised by them. (See Instinct and Learning for a discussion of how these species exploit other birds' instinctive tendency to care for their young.)

REAL-LIFE APPLICATIONS

Mycorrhizae

One of the best examples of mutualism is known by the unusual name mycorrhiza, which is a "fungus root," or a fungus living in symbiosis with the roots of a vascular plant. (A vascular plant is any plant species containing a vascular system, which is a network of vessels for moving fluid through the body of the organism.) The relationship is a form of mutualism because, while the fungus benefits from access to carbohydrates, proteins, and other organic nutrients excreted by or contained in the roots of the host plant, the host plant benefits from an enhanced supply of inorganic nutrients, especially phosphorus, that come from the fungus.

The fungus carries out this function primarily by increasing the rate at which organic matter in the immediate vicinity of the plant root decomposes and by efficiently absorbing the inorganic nutrients that are liberated by this process-nutrients it shares with the plant. (The term organic refers to the presence of carbon and hydrogen together, which is characteristic not only of all living things but of many nonliving things as well.) The most important mineral nutrients that the fungus supplies to the plant are compounds containing either phosphorus or, to a lesser degree, nitrogen. (These elements are present in biogeochemical cycles—see The Biosphere.) So beneficial is the mycorrhizal mutualism that about 90% of all vascular plant families, including mustards and knotweeds (family Brassicaceae and Polygonaceae, respectively), enjoy some such relationship with fungi.

SOME EXAMPLES OF MYCORRHIZAE.

Many mycorrhizal fungi in the Basiodiomycete group develop edible mushrooms, which are gathered by many people for use in gourmet cooking. Mushroom collectors have to be careful, of course, because some mycorrhizal fungi are deadly poisonous, as is the case with the death angel, or destroying angel—Amanita virosa.

Perhaps the most famous of the edible mushrooms produced by mycorrhizae are the many varieties known by the name truffle. Among these mushrooms is Tuber melanosporum, which is commonly mycorrhizal on various species of oak tree. The spore-bearing bodies of the truffle fungi develop underground and are usually brown or black and covered with warts. Truffle hunters require the help of truffle-sniffing pigs or dogs, but their work is definitely worth the trouble: good truffles command a handsome price, and particularly in France the truffle industry is big business. Given the lucrative nature of the undertaking, one might ask why people do not cultivate truffles rather than hunting for them. To create the necessary conditions for cultivation, however, so much effort is required that it is difficult to make a profit, even at the high prices charged for truffles. The soil composition must be just right, and under conditions of cultivation this takes about five years.

Orchids are an example of a plant in an obligate mutualism: they can thrive only in a mycorrhizal relationship. Tiny and dustlike, orchid seeds have virtually no stored energy to support the seedling when it germinates, or begins to grow. Only with the assistance of an appropriate mycorrhizal fungus can these seedlings begin developing. Until horticulturists discovered this fact, orchids were extremely difficult to propagate and grow in greenhouses; today, they are relatively easy to breed and cultivate.

THE IMPORTANCE OF MYCORRHIZAE.

Some species of vascular plants do not contain chlorophyll, the chemical necessary for photosynthesis, or the conversion of light energy from the Sun into usable chemical energy in a plant. Such a plant is like a person missing a vital organ, and under normal circumstances, it would be impossible for the plant to survive. Yet the Indian pipe, or Monotropa uniflora, has managed to thrive despite the fact that it produces no chlorophyll; instead, it depends entirely on mycorrhizal fungus to supply it with the organic nutrients it needs. This obligate relationship is just one example of the critical role mycorrhizae perform in the lives of plants throughout the world.

Mycorrhizae are vital to plant nutrition, especially in places where the soil is poor in nutrients. Whereas many plant roots develop root hairs as a means of facilitating the extraction of water and nutrients from the soil, plant roots that have a mycorrhizal fungus usually do not. Instead, these plants rely heavily on the fungus itself to absorb moisture and vital chemical elements from the ground. This means that it may be difficult or impossible for plants to survive if they are removed from an environment containing mycorrhizal fungus, a fact that indicates an obligate relationship.

Often, when species of trees and shrubs grown in a greenhouse are transplanted to a non-forested outdoor habitat, they exhibit signs of nutritional distress. This happens because the soils in such habitats do not have populations of appropriate species of mycorrhizal fungi to colonize the roots of the tree seedlings. If, however, seedlings are transplanted into a clear-cut area that was once a forest dominated by the same or closely related species of trees, the plants generally will do well. This happens because the clear-cut former forest land typically still has a population of suitable mycorrhizal fungi.

Plants' dependence on mycorrhizal fungi may be so acute that the plants do not do well in the absence of such fungi, even when growing in soil that is apparently abundant in nutrients. Although most mycorrhizal relationships are not so obligate, it is still of critical important to consider mycorrhizal fungi on a site before a natural ecosystem is converted into some sort of anthropogenic habitat (that is, an area dominated by humans—see Biomes). For example, almost all the tree species in tropical forests depend on mycorrhizae to supply them with nutrients from the soils, which are typically infertile. (See The Biosphere for more about the soil in rain forests.) If people clear and burn the forest to develop new agricultural lands, they leave the soil bereft of a key component. Even though some fungi will survive, they may not necessarily be the appropriate symbionts for the species of grasses and other crops that farmers will attempt to grow on the cleared land.

Interkingdom and Intrakingdom Partnerships

Mycorrhizae are just one example of the ways that mutualism brings into play interactions between widely separated species—in that particular case, between members of two entirely different kingdoms, those of plant and fungi. In some cases, mutualism may bring together an organism of a kingdom whose members are incapable of moving on their own (plants, fungi, or algae) with one whose members are mobile (animals or bacteria). An excellent example is the relationship between angiosperm plants and bees, which facilitate pollination for the plants (see Ecosystems and Ecology.)

Another plant-insect mutualism exists between a tropical ant (Pseudomyrmex ferruginea ) and a shrub known as the bull's horn acacia (Acacia cornigera ). The latter has evolved hollow thorns, which the ants use as protected nesting sites. The bull's horn acacia has the added benefit, from the ant's perspective, of exuding proteins at the tips of its leaflets, thus providing a handy source of nutrition. In return, the ants protect the acacia both from competition with other plants (by removing any encroaching foliage from the area) and from defoliating insects (by killing herbivorous, or plant-eating, insects and attacking larger herbivores, such as grazing mammals).

A much less dramatic, though biologically quite significant, example of interkingdom mutualism is the lichen. Lichen is the name for about 15,000 varieties, including some that are incorrectly called mosses (e.g., reindeer moss). Before the era of microscopy, botanists considered lichens to be single organisms, but they constitute an obligate mutualism between a fungus and an alga or a blue-green bacterium. The fungus benefits from access to photosynthetic products, while the alga or bacterium benefits from the relatively moist habitat that fungus provides as well as from enhanced access to inorganic nutrients.

BIG AND SMALL.

In contrast to these cross-kingdom or interkingdom types of mutualism, there may be intrakingdom (within the same kingdom) symbiotic relationships between two very different types of animal. Often, mutualism joins forces in such a way that humans, observing these interactions, see in them object lessons, or stories illustrating the concept that the meek sometimes provide vital assistance to the mighty. One example of this is purely fictional, and it is a very old story indeed: Aesop's fable about the mouse and the lion.

In this tale a lion catches a mouse and is about to eat the little creature for a snack when the mouse pleads for its life; the lion, feeling particularly charitable that day, decides to spare it. Before leaving, the mouse promises one day to return the favor, and the lion chuckles at this offer, thinking that there is no way that a lowly mouse could ever save a fierce lion. Then one day the lion steps on a thorn and cannot extract it from his paw. He is in serious pain, yet the thorn is too small for him to remove with his teeth, and he suffers hopelessly—until the mouse arrives and ably extracts the thorn.

Many real-life examples of this strong-weak or big-small symbiosis exist, one of the more well-known versions being that between the African black rhinoceros (Diceros bicornis ) and the oxpecker, or tickbird. The oxpecker, of the genus Buphagus, appears in two species, B. africanus and B. erythrorhynchus. It feeds off ticks, flies, and maggots that cling to the rhino's hide. Thus, this oddly matched pair often can be seen on the African savannas, the rhino benefiting from the pest-removal services of the oxpecker and the oxpecker enjoying the smorgasbord that the rhino's hide offers.

HUMANS AND OTHER SPECIES.

Humans engage in a wide variety of symbiotic relationships with plants, animals, and bacteria. Bacteria may be parasitic on humans, but far from all microorganisms are parasites: without the functioning of "good" bacteria in our intestines, we would not be able to process and eliminate food wastes properly. The relationship of humans to animals that provide a source of meat might be characterized as predation (i.e., the relationship of predator to prey), which is technically a form of symbiosis, though usually it is not considered in the same context. In any case, our relationship to the animals we have domesticated, which are raised on farms to provide food, is a mixture of predation and mutualism. For example, cows (Bos taurus ) benefit by receiving food, veterinary services, and other forms of care and by protection from other predators, which might end the cows' lives in a much more unpleasant way than a rancher will.

All important agricultural plants exist in tight bonds of mutualism with humans, because human farmers have bred species so selectively that they require assistance in reproducing. For example, over time, agricultural corn, or maize (Zea mays ), has been selected in such a way as to favor those varieties whose fruiting structure is enclosed in a leafy sheath that does not open and whose seeds do not separate easily from the supporting tissue. In other words, thanks to selective breeding, the corn that grows on farms is enclosed in a husk, and the kernels do not come off of the cob readily. Such corn may be desirable as a crop, but because of these characteristics, it is incapable of spreading its own seeds and thereby reproducing on its own. Obviously, agricultural corn is not on any endangered species list, the reason being that farmers continue to propagate the species through breeding and planting.

Another example of human-animal mutualism, to which we alluded earlier, is the relationship between people and their pets, most notably dogs (Canis familiaris ) and house cats (Felis catus ). Fed and kept safe in domestication, these animals benefit tremendously from their interaction with humans. Humans, in turn, gain from their pets' companionship, which might be regarded as a mutual benefit—at least in the case of dogs. (And even cats, though they pretend not to care much for their humans, have been known to indulge in at least a touch of sentimentality.) In addition, humans receive other services from pets: dogs protect against burglars, and cats eradicate rodents.

Symbiosis Among Insects

Where insects and symbiosis are involved, perhaps the ideas that most readily come to mind are images of parasitism. Indeed, many parasites are insects, but insects often interact with other species in relationships of mutualism, such as those examples mentioned earlier (bees and angiosperms, ants and bull's horn acacia plants). Additionally, there are numerous cases of mutualism between insect species. One of the most intriguing is the arrangements that exists between ants and aphids, insects of the order Homoptera, which also are known as plant lice.

In discussing the ant-aphid mutualism, scientists often compare the aphids to cattle, with the ants acting as protectors and "ranchers." What aphids have that ants want is something called honeydew, a sweet substance containing surplus sugar from the aphid's diet that the aphid excretes through its anus. In return, ants protect aphid eggs during the winter and carry the newly hatched aphids to new host plants. The aphids feed on the leaves, and the ants receive a supply of honeydew.

In another mutualism involving a particular ant species, Formica fusca, two organisms appear to have evolved together in such a way that each benefits from the other, a phenomenon known as coadaptation. This particular mutualism involves the butterfly Glaucopsyche lygdamus when it is still a caterpillar, meaning that it is in the larval, or not yet fully developed, stage. Like the aphid, this creature, too, produces a sweet "honeydew" solution that the ants harvest as food. In return, the ants defend the caterpillar against parasitic wasps and flies.

WHEN MUTUALISM ALSO CAN BE PARASITISM.

As the old saying goes, "One man's meat is another man's poison"—in other words, what is beneficial to one person may be harmful to another. So it is with symbiotic relationships, and often a creature that plays a helpful, mutualistic role in one relationship may be a harmful parasite in another interaction. Aphids, for instance, are parasitic to many a host plant, which experiences yellowing, stunting, mottling, browning, and curling of leaves as well as inhibiting of its ability to produce crops.

One particular butterfly group, Heliconiinae (a member of the Nymphalidae, largest of the butterfly families) furnishes another example of the fact that a mutualistic symbiont, in separate interaction, can serve as a parasite. Moreover, in this particular case the heliconius butterfly can be a mutualistic symbiont and parasite for the very same plant. Heliconius butterflies scatter the pollen from the flowers of passionflower vines (genus Passiflora ), thus benefiting the plant, but their females also lay eggs on young Passiflora shoots, and the developing larva may eat the entire shoot. As an apparent adaptive response, several Passiflora species produce new shoots featuring a small structure that closely resembles a heliconius egg. A female butterfly that sees this "egg" will avoid laying her own egg there, and the shoot will be spared.

Commensalism

Years ago a National Geographic article on the Indian city of Calcutta included a photograph that aptly illustrated the idea of commensalism, though in this case not between animals or plants but between people. The photograph showed a street vendor in a tiny wooden stall with a window, through which he sold his wares to passers-by. It was a rainy day, and huddled beneath the window ledge (which also served as a counter-top) was another vendor, protecting himself and his own tray of goods from the rain.

The photograph provided a stunning example, in microcosm, of the overpopulation problem both in Calcutta and in India as a whole—a level of crowding and of poverty far beyond the comprehension of the average American. At the same time it also offered a beautiful illustration of commensalism (though this was certainly not the purpose of including the picture with the article). The vendor sitting on the ground acted in the role of commensal to the relatively more fortunate vendor with the booth, who would be analogous to the host.

The relationship was apparently commensal, because the vendor on the ground received shelter from the other vendor's counter without the other vendor's suffering any detriment. If the vendor in the booth wanted to move elsewhere, and the vendor on the ground somehow prevented him from doing so, then the relationship would be one of parasitism. And, of course, if the vendor with the booth charged his less-fortunate neighbor rent, then the relationship would not be truly commensal, because the vendor on the ground would be paying for his shelter. To all appearances, however, the interaction between the two men was perfectly commensal.

COMMENSALISM IN NATURE.

Plants that grow on the sides of other plants without being parasitic are known as epiphytic plants.

Among these plants are certain species of orchids, ferns, and moss. By "standing on the shoulders of giants," these plants receive enormous ecological benefits: the height of their hosts gives them an opportunity to reach a higher level in the canopy (the upper layer of trees in the forest) than they would normally attain, and this provides them with much greater access to sunlight. At the same time, the hosts are not affected either negatively or positively by this relationship.

Another commensal relationship, known as phoresy, is a type of biological hitchhiking in which one organism receives access to transportation on the body of another animal, without the transporting animal being adversely affected by this arrangement. The burdock (Arctium lappa ) is one of several North American plant species that produce fruit that adheres to fur and therefore is dispersed easily by the movement of mammals. The burdock is special from a human standpoint, however, inasmuch as the anatomical adaptation that makes possible its adhesion to fur provided designers with the model for that extremely useful innovation, Velcro.

As with the illustration of the street vendors in Calcutta, it is always possible that commensalism, through a slight alteration, may yield a relationship in which the host is affected negatively. There are instances in which individual animals may become loaded heavily with sticky fruit from the burdock (or other plants that employ a similar mechanism), thus causing their fur to mat excessively and perhaps resulting in significant detriment. This is not common, however, and usually this biological relationship is truly commensal. Furthermore, phoresy should not be confused with parasitic relationships in which a creature such as a tick attaches itself to the body of another organism for transport or other purposes. (For much more about parasitism, see Parasites and Parasitology.)

WHERE TO LEARN MORE

"Biology 160, Animal Behavior: Symbiosis and Social Parasitism." Department of Biology, University of California at Riverside (Web site). <http://www.biology.ucr.edu/Bio160/lecture25.html>.

Knutson, Roger M. Furtive Fauna: A Field Guide to the Creatures Who Live on You. New York: Penguin Books, 1992.

Lanner, Ronald M. Made for Each Other: A Symbiosis of Birds and Pines. New York: Oxford University Press, 1996.

Lembke, Janet. Despicable Species: On Cowbirds, Kudzu, Hornworms, and Other Scourges. New York: Lyons Press, 1999.

Margulis, Lynn. Symbiotic Planet: A New Look at Evolu tion. New York: Basic Books, 1998.

Mutualism and Commensalism. Neartica: The Natural World of North America (Web site). <http://www.nearctica.com/ecology/pops/symbiote.htm>.

"Parasites and Parasitism." University of Wales, Aberystwyth (Web site). <http://www.aber.ac.uk/parasitology/Edu/Para_ism/PaIsmTxt.html>.

Sapp, Jan. Evolution by Association: A History of Symbiosis. New York: Oxford University Press, 1994.

Symbiosis and Commensalism. The Sea Slug Forum (Web site). <http://www.seaslugforum.net/symbio.htm>.

Trager, William. Living Together: The Biology of Animal Parasitism. New York: Plenum Press, 1986.

KEY TERMS

COMMENSALISM:

A symbiotic rela tionship in which one organism, the commensal, benefits without causing any detriment to the other organism, the host.

FACULTATIVE:

A term for a symbiotic relationship in which partners are capable of living apart.

HOST:

The term for an organism that provides a benefit or benefits for another organism in a symbiotic relationship of commensalism or parasitism.

INQUILINISM:

A type of symbiosis in which one species, the inquiline, makes use of a host's nest or habitat without causing any detriment to the host. Inquilinism is considered a variety of commensalism.

OBLIGATIVE:

A term for a symbiotic relationship in which the partners, if they were separated, would be incapable of continuing to live.

PARASITISM:

A symbiotic relation ship in which one organism, the parasite, benefits at the expense of the other organism, the host.

SYMBIOSIS:

A biological relationship in which (usually) two species live in close proximity to one another and interact reg ularly in such a way as to benefit one or both of the organisms. Symbiosis may exist between two or more individuals of the same species as well as between two or more individuals representing two different species. The three principal varieties of symbiosis are mutualism, commensalism, and parasitism.

Symbiosis

Introduction

Symbiosis is an association between two or more different species of organisms. The association may be permanent, the organisms never being separated, or it may be long lasting. Life is complex and often involves a delicate balancing act between hosts and symbionts, in associations that range from parasitism to mutualism. In the long history of life on Earth, symbionts have evolved many protective strategies in their attempts to overcome a host's defenses, including molecular camouflage, deception, mimicry, and subversion. By studying symbiosis one gains a wider evolutionary perspective on the extent and nature of biological interactions between species.

Symbiosis and modern biology

The recognition of symbiotic relationships has had a revolutionary impact on modern biological thought. The idea that mitochondria and chloroplasts are transformed by symbiotic bacteria provides a common thread to the biological world and raises hope of finding other symbiotic wonders among life's diversity. Plants and animals have acquired new metabolic capabilities through symbioses with bacteria and fungi. Mammalian herbivores and termites digest cellulose with the help of microbial symbionts. The luminescent bacteria contained in the specialized light organs of some fishes and squids produce marine bioluminescence. Diverse animal life around deep-sea vents is based on symbiosis with bacteria that oxidize hydrogen sulfide and chemosynthetically fix carbon dioxide into carbohydrates. Associations between fungi and algae have resulted in unique morphological structures called lichens. Early land plants formed associations with mycorrhizal fungi, which greatly facilitated their phosphorous uptake and thus played a significant role in the plants' ability to colonize terrestrial habitats. Evolutionary changes in organisms and their gene pools are not restricted to nuclear events and sexual mechanisms. Horizontal gene transfer between species has been documented in all forms of life. Bacterial cells possess plasmids and viruses that transfer new genetic properties from one cell to another. Many virulence factors in pathogenic bacteria are expressed through plasmid-borne genes. Similarly, bacteria become resistant to antibiotics when they incorporate plasmids with genes for antibiotic resistance. Horizontal gene transfer has been suggested in the evolution of flowers, fruits, and storage structures from gall-forming insects and viruses. The role of viruses as genetic engineers is gaining importance in evolutionary biology. The Rhizobium-legume symbiotic relationship is an excellent example of how host cells and bacterial symbionts within root nodules undergo transformation, which allows the bacterial cells to fix nitrogen-converting atmospheric nitrogen into a chemical form that can be taken up by plants. Within the host cells, Rhizobia acting as bacteroids behave as temporary cell organelles that fix nitrogen. Intragenomic conflict is an evolutionary force. The evolution of sex was a form of genomic conflict management. Uniparental inheritance of cytoplasmic genes, mating types, and many features of sexual behavior may have evolved as a result of evolutionary conflict. The two-sex model that is widespread throughout the diversity of life may have been the result of ancient intracellular symbiosis. The Red Queen hypothesis suggests that harmful parasites and virulent pathogens exert selection pressure on their hosts so that sexual selection is maintained. Parasites, pathogens, and their hosts are involved in a microevolutionary "arms race" and in time, the symbionts' offense and the host defenses produce cycles of coadaptations.

Types of symbioses

The term "symbiosis" was, in a broad sense, originally intended by Anton de Bary in 1879 to refer to different organisms living together. Proposals to change this definition and redefine symbiosis, such as equating it to mutualism, have led to confusion. Various types of symbioses, whether beneficial or harmful, are described by the terms commensalism, mutualism, and parasitism.

The term "commensalism" was first used by P. J. van Beneden in 1876 for associations in which one animal shared food caught by another animal. An example of a commensalistic symbiosis is the relationship between silverfish and army ants. The silverfish live with the army ants, participate in their raids, and share their prey. They neither harm nor benefit the ants.

In mutualistic symbiosis, both partners benefit from the relationship. The extent to which each symbiont benefits, however, may vary and is generally difficult to assess. The complex interactions that take place between the symbionts may involve a reciprocal exchange of nutrients. For example, in the symbioses of algae and invertebrates (such as corals, anemones, and flatworms), the algae provides the animals with organic compounds that are products of photosynthesis, while the animals provide the algae with waste products such as nitrogenous compounds and carbon dioxide, which the algae use in photosynthesis. Unfortunately, in many academic circles, the terms symbiosis, mutualism, and cooperation have similar meanings and are often used interchangeably. Mutualism has also been widely used to describe intraspecific cooperative behavior in various animal species. The study of cooperation has enjoyed a resurgence during the past several decades. The evolution of cooperation via byproduct mutualism is generally found in the context of interspecific associations.

Parasitism is a form of symbiosis in which one symbiont benefits at the expense of its host. Parasitic symbioses affect the host in different ways. Some parasites are so pathogenic that they produce disease in the host shortly after parasitism begins. In other associations, the host and parasite have coevolved into a controlled parasitism in which the death of the host cells is highly regulated. Associations among many species are not clear and are more difficult to define categorically. For instance, when in their larval form, flukes might be considered parasites to snails because they harm their host; but, adult flukes have a commensal relationship with snails because when present in the alimentary tract of invertebrates they only share digesting food.

Classification of symbioses

Many scientists have attempted to standardize the many conflicting terms that have been used to describe different symbioses, including:

• Ectosymbiosis: The partners remain external to each other, such as in lichens.
• Endosymbiosis: The smaller symbionts are inside the host, but remain extracellular. Most of the time endosymbionts are in the digestive tract, or inside particular organs.
• Endocytobiosis is intracellular symbiosis. Symbiosome membranes are the host cell's vacuoles that enclose the symbiont.
• Obligate symbionts are so highly adapted to a symbiotic experience that they cannot live outside of it.
• Facultative symbionts, however, can live in a free-living condition.

Some examples of symbiosis in lower metazoans and tunicates

Commensalistic associations

Sharing of food and the provision of shelter are two main features of commensalistic relationships. Many species that display commensalistic relationships inhabit the internal spaces of sponges, clams, and sea cucumbers. The symbionts are often smaller and more streamlined than their free-living relatives and show evidence of long-term associations. For example, there are crab and shrimp species that live in the mantle cavities of bivalve mollusks; the pearl fish, Corpus, shows both structural and behavioral modifications that adapted in order to live in the cloacal spaces of sea cucumbers. These adaptations include a dramatic shift of the anal opening to just beneath the head, and the loss of both scales and the pelvic fins. In tropical water the hat-pin urchin Diadema, with its long needle-like spines, provides protection to fish such as Aeoliscus (the shrimpfish) and Diademichthys (the clingfish). These elongated fish species hide among the host's spines, which are constantly moving, by orienting themselves parallel to the spines. Another common example of commensalism is the relationship that exists between fishes and jellyfish. Fishes of the family Nomeidae congregate among the tentacles of jellyfish for protection. The anemonefishes keep the surface of their host anemones free of debris and may also lure fishes into the tentacles, thus providing food to the host.

Sponges

Marine sponges contain a variety of endosymbionts, including bacteria, dinoflagellates, diatoms, and cryptomonads. Symbionts are especially common among tropical sponges. Many sponges contain endosymbiotic cyanobacteria that are intercellular (in sponge tissue). The sponge obtains nutrients from the digestion of bacteria or from the excretion of compounds such as glycerol and nitrogen from bacteria. In turn the bacteria receives nutrients and a place to live.

Phytosynthetic associations

Green hydra-Chlorella symbiosis

Hydra are common inhabitants of freshwater lakes and ponds, where they feed on small animals. Hydra viridis contains the green alga Chlorella. Algae reproduces asexually within the gastrodermal cells and a single hydra may contain about 150,000 algal cells. Under normal conditions, symbiotic algae are not digested by hydra. There are two reasons for this: first, the cell wall of algae contains sporopollenin, a protein that resists digestive enzymes; second, vacuoles containing algae do not fuse with lysosomes, the organelles that contain digestive enzymes and normally fuse with food particles. But if a digestive cell takes in more algal cells than normal, the extra cells are either digested or ejected. A bilateral movement of nutrients takes place between the symbionts. Algae supplies the animals with photosynthetic products such as maltose. At an acidic pH level, almost 60% of the carbon fixed by the algae is excreted as maltose, but at a neutral pH level, very little maltose is excreted. The rapidly hydrolyzed maltose is converted to glucose, and then glycogen is produced. Algae also provide the animal with oxygen, which they produce during photosynthesis. Hydra provides the algae with nutrients, including precursors of proteins and nucleic acids, and a protected place to live. As digestion is avoided and the host cells are able to regulate algal reproduction, the symbiosis

that exists between H. viridis and Chlorella appears to be a finely tuned, nonpathogenic equilibrium.

Marine algal-invertebrate symbioses

Many marine invertebrates, such as sea anemones, coral, and flatworms have formed mutualistic symbioses with the photosynthetic algae known as the dinoflagellates. Their chloroplasts have efficient light-harvesting complexes that include chlorophyll a, chlorophyll c, and large amounts of xanthophylls. A common dinoflagellate of marine invertebrates is Symbiodinium microadriaticum, and this is greatly modified when it lives inside animal cells. The algal cell wall becomes thinner, loses the groove and flagella, and divides only by binary fission. In the host animal the algae excrete large amounts of glycerol, in addition to glucose, alanine, and organic acids. When the algae are isolated from animals and grown in culture, they stop excreting these substances.

Sea anemones and jellyfish

The sea anemone Anthopleura xanthogrammica, contains two types of symbiotic algae: zoochlorellae and zooxanthellae. The relative proportion of each algal symbiont in the animal depends on the water temperature. The anemones position themselves in ways to increase the exposure of their symbionts to light.

Cassiopea xamachana is a jellyfish that has been used to study how an invertebrate selects its algal symbionts. The lifecycle of Cassiopea includes a sexual medusoid stage, which contains algae that does not swim freely, but rather lies upside down in shallow waters, a behavioral adaptation that allows the algae in its tentacles to receive maximum daylight for photo-synthesis, and gives the animal its common name, the upside-down jellyfish.

Anemone-clownfish symbiosis

Fishes of the genera Amphiprion, Dascyllus, and Premnas, commonly called clownfish, form mutualistic associations with giant sea anemones that live in coral reefs throughout the Pacific Ocean. The association is obligatory for the fish, but facultative for the anemones. The anemones eat prey that have been paralyzed by means of poisonous nematocysts discharged from specialized cells in their tentacles. The clownfishes are immune to the stinging nematocysts and can nestle among tentacles without harm. Some clownfish go through a period of acclimation before they become immune to the anemones' poison. Symbiosis with the anemone changes the mucous coating around the fish and the fish is no longer recognized as prey by the anemone. Clownfishes are brightly colored and marked, and attract larger fish to the anemone. These fish, if they come too close, are stung by the tentacles and eaten by the anemone. The clownfish share in the meal. A similar relationship exists between the Portugese man-of-war (Physalia physalia) and the horse mackerel (Trachurus trachurus). The bright blue and silver color of the fish, as well as its small size, attract prey for the man-of-war.

Reef-building corals

The symbiotic association between Symbiodinium-reef-building corals (Scleractinia) is of great importance in marine tropical ecosystems and has been the subject of many studies. Coral reefs support large communities of organisms. Coral polyps excrete a calcium carbonate shell around their body. As the polyp dies, the shells harden, and new polyps grow over them. After many years of this process, coral reefs are formed. Symbiotic dinoflagellates live inside nutrient-rich cells of the gasterodermis of the coral polyp. In some corals more than 90% of photosynthate may be released by the symbiont to its host cell. The algae supply the coral with oxygen, carbon, and nitrogen compounds. The animal obtains vitamins, trace elements, and other essential compounds from the digestion of old algal symbionts. Animal waste products such as ammonia are converted by the algae into amino acids, which are translocated to the animals. Such a recycling of nitrogen is an important feature in the nitrogen-poor habitats of coral. Coral bleaching is caused by the loss of symbiotic algae from the host and may be caused by environmental stresses such as global warming, pollution, and increased ultraviolet radiation.

Green flatworms

Convoluta roscoffensis is a small marine flatworm that lives in the intertidal zones of beaches in the Channel Islands of the United Kingdom and in western France. The worms are 0.08–0.16 in (2–4 mm) long and deep green in color from the algae they contain. During high tide, the worms are buried in the sand, but at low tide, during daylight, they move up to the surface. During this time the green algal symbiont, Tetraselmis convolutae, photosynthesizes until the next high tide. The Convoluta-algal symbiotic relationship is an early example of detailed studies (1910) that attracted public attention to the broader significance of symbiosis in nature.

Tunicates

Some marine tunicates contain an unusual photosynthetic symbiont, Prochloron, that has characteristics of both cyanobacteria

and green algae. In some tunicates the symbionts lie within a cellulose matrix that surrounds the outer surface of the animal, whereas in other tunicates symbionts are loosely attached to the cloacal wall. The larvae of some tunicates have specialized pouches that carry Prochloron cells that they obtain from the parent.

Symbiosis and animal parasitism

Scientists estimate that up to 50% of all animal species are parasitic symbionts. Some phyla such as the Platyhelminthes, Nematoda, and Arthropoda contain large a number of parasitic species. Hosts and parasites have coevolved together and under natural conditions many have become mutually tolerant. Host organisms can live independently, but, in most cases, the parasite's association with its host is obligatory. Animal parasites affect the health of humans and domesticated animals throughout the world. In most warm climates parasitic infections from flukes, nematodes, and arthropods greatly diminish the quality of life for people.

Helminths are widely distributed parasites of vertebrates. Infections caused by helminths such as schistosoma, hookworms, and filarial nematodes are a major cause of sickness of humans inhabiting the tropics. Helminths have complex lifecycles. They live for a long period within host animals, and they often possess a remarkable ability to evade the host's defense mechanisms. The prevalence of helminthic infections in some areas is high; however, only a few hosts develop disease. Helminths do not multiply in humans, and therefore the severity of the disease depends on the extent of the original infection. However, some helminthes may accumulate after repeated infection of a host.

Some fluke symbioses

Flukes (including the liver fluke, lung fluke, and human blood fluke) are obligate endoparasites of vertebrates as adults. After mating, the female fluke produces eggs into the host environment which are then are passed out of the host with feces or urine. There is a series of larval stages that multiply asexually in snails, serving as the first intermediate hosts. A larval stage (cercaria) with a characteristic tail emerges from the snail and either penetrates a vertebrate host immediately, encysts on to vegetation, or is eaten by a second intermediate host such as a crab or a fish, which may then be ingested by a vertebrate. Fasciola hepatica, the sheep liver fluke, commonly inhabits the bile duct, liver, or gallbladder of cattle, horses, pigs, and other farm animals. The Chinese liver fluke, Clonorchis sinensis, is an important parasite of humans and other fish-eating mammals in Far Eastern countries. Fish farming in east Asia is a major source of fluke infections in people. In other areas, dogs and cats serve as reservoir hosts of C. sinensis. Paragonimus westermani, the lung fluke, infects humans, cats, dogs, and rats. Occurences of this fluke are extremely prevalent in the people of China, the Philippines, Thailand, and other Asian countries.

Next to malaria, schistosomiasis is the most important parasitic disease in the world, affecting more than 200 million people in more than 75 countries. Schistosomes are blood flukes, and they reside in the mesenteric blood vessels of humans. Adult flukes are elongated and wormlike, and the female fluke is permanently held in the ventral groove of the male fluke. The presence of blood fluke eggs in various host tissues triggers an immune response, causing the affected person to show symptoms of disease that include enlargement of the liver and spleen, bladder calcification, and kidney disorders. Three important blood flukes that infect humans are Schistosoma mansoni, S. japonicum, and S. haematobium. Schsitosoma mansoni has been known to cause intestinal bilharziasis among people in South America, Central America, and the Middle East. Urinary schistosomiasis is caused by S. haematobium and is thought to occur in about 40 million people in Africa and the Middle East.

Cestodes: Tapeworms

Tapeworms represent the ultimate example of biological adaptation in order to live in another organism. All tapeworms are obligate symbionts of vertebrates and arthropods. Sexually mature tapeworms live in the intestines of vertebrates; in their larval stages they develop in the visceral organs of an alternate host, which may be a vertebrate or an arthropod. Serious diseases are caused by the progressive larval stages that take place in the muscles and nervous tissue of the vertebrate host. Some scientists view the adult tapeworms in the alimentary canal as endocommensals living in a nutrient-rich environment. Tapeworms lack a digestive system and absorb all their nutrients through their tegument, which is remarkably similar to that of flukes. Diphyllobothrium latum, the fish tapeworm, is a common inhabitant of the alimentary canal of fish-eating mammals, birds, and fishes. In temperate climates, people who eat raw fish often carry D. latum. The fish tapeworm is well known for its ability to absorb vitamin B¹², thereby causing the host to be deficient in a vitamin that is essential for the development of red blood cells. Humans become infected with pork tapeworm (Taenia solium) when they eat undercooked meat. Humans acquire the beef tapeworm, Taenia saginata, by eating raw or undercooked beef. Hymenolepis diminuta, the rat tapeworm, has been a favorite experimental subject to investigate the nutrition, biochemistry, immunology, and developmental biology of tapeworms.

Nematodes

Roundworms are second only to insects as the most abundant animals on earth. Most nematodes are free living. They occur in freshwater, marine, and soil habitats, feeding on microorganisms and decaying organic matter. Many nematodes are adapted for a parasitic lifestyle in plants, fungi, and animals.

Scientists estimate that every kind of animal is inhabited by at least one parasitic nematode. Many nematodes live in the alimentary canals of their hosts, while others parasitize organs such as the eyes, liver, and lungs, often causing destruction to the host tissue. Ascaris lumbricoides is one of the largest intestinal nematodes present in humans and is prevalent throughout warmer climates. The two most important hookworms are Ancylostoma duodenale—the oriental hookworm of China, Japan, Asia, North Africa, the Caribbean Islands, and South America, and Necator americanus—which is primarily in South and Central America but also present in Africa and Asia. An estimated one billion people who live in the warmer climates of the world are infected with these nematodes, but most are asymptomatic. Trichinella spiralis, one of the most common parasites of vertebrates, has been studied extensively by physicians, experimental biologists, and ecologists.

Filarial nematodes are obligate parasites with complex lifecycles involving humans, other vertebrates, and arthropod vectors. Wuchereria bancrofti and Brugia malayi occur in the lymphatic system and cause the elephantiasis disease. The filarial worm, Onchocerca volvulus, causes skin tumors and blindness and is prevalent among the people of Africa and the Middle East. A typical filarial lifecycle begins when humans acquire the parasite from the bite of an infected blood-sucking insect. Once in the bloodstream or lymphatic system the nematode larvae become sexually mature. The mature female gives birth to larval stage microfilariae, which infest the biting insects that continue the lifecycle. Symptoms of filarial diseases are the result of host immune response and the physical blockage of ducts.

Nematode-insect symbioses

Insects are the dominant form of life on earth, and nematodes have successfully evolved symbioses with many of them. Nematodes that are symbionts of insects have intricate lifecycles that are synchronized with those of their hosts. Heterorhabditis and Steinernema are nematodes that parasitize insects and transmit bacteria that kill the hosts. The possibility of developing a biological control for mosquitoes has heightened interest in the mermithid nematode, Romanomermis, which kills mosquito larvae.

Most nematodes that attack plants are obligate parasites and include root-knot nematodes (Meloidogyne spp.) and cyst nematodes (Globodera and Heterodera spp.) that cause destructive infections in crop plants. There are more than 2,000 species of plant-parasitic nematodes, but few species are pests. Cell proliferation, giant cell formation, suppression of cell division, and cell wall breakdown are some of the host responses to nematode parasitism.

Bursaphaloenchus exylophilus is a nematode that lives in weakened or dead pine trees. A beetle that may carry up to 15,000 juvenile nematodes to a new location spreads the nematode, which feed on wood tissue and are suspected of killing pine trees. The relationship between the plant-parasitic nematode and the bark beetle is thought to be an example of mutualistic symbiosis.

Resources

Books

Cheng, Thomas. General Parasitology, 2nd edition. Orlando, FL: Academic Press, 1986.

Douglas, Angela. Symbiotic Interactions. Oxford: Oxford University Press, 1994.

Kennedy, M. W., and W. Harnett, eds. Parasitic Nematodes: Molecular Biology, Biochemistry and Immunology. Oxon, U.K.: CABI Publishing, 2001.

Margulis, Lynn. Symbiosis in Cell Evolution, 2nd edition. New York: W. H. Freeman, 1993.

Paracer, Surindar, and Vernon Ahmadjian. An Introduction to Biological Associations, 2nd edition. New York: Oxford University Press, 2000.

Organizations

International Society of Endocytobiology. Web site: <http://www.endocytobiology.org/>

International Symbiosis Society. Web site: <http://www.ma.psu.edu/lkh1/iss/>

Surindar Paracer, PhD

Symbiosis

Introduction

Without symbiosis, living organisms would be quite different from what they are today. This is true not only because symbiotic relationships were fundamental to the separation of eukaryotes (organisms whose cells have true nuclei) from prokaryotes (cellular organisms lacking a true nucleus), but also because they represent a unique biological process without which many organisms could not exist. All herbivorous mammals and insects, for example, would starve without their cellulose-digesting mutualists; coral reefs could not form if corals were not associated with algae; and the human immune system would not be as complex as it is today if humans had not been infested so often by parasites over the course of their evolution.

The English word "symbiosis" is derived from two Greek words, sym, meaning "with," and bios, meaning "life." The term was introduced into scientific usage in 1879 by Heinrich Anton de Bary, professor of botany at the University of Strasbourg. De Bary used symbiosis in a global sense to refer to any close association between two heterospecific organisms. He explicitly referred to parasitism as a type of symbiosis, but excluded associations of short duration. According to de Bary's definition of symbiosis, the infection of humans by Plasmodium falciparum, the agent that causes malaria, is an instance of symbiosis whereas the pollenization of flowering plants by insects is not. As of 2003, "symbiosis" is used in two basic ways. First, the term can be used to refer to a close association between two organisms of different species that falls into one of three categories—mutualism, commensalism, or parasitism. Second, symbiosis may be used in a more restricted sense as a synonym of mutualism, to identify a relationship in which the two associated species derive benefits from each other.

Terminology

Symbiosis always implies a biological interaction between two organisms. The first organism is called the host, and is generally larger than the other or at least supports the other. The second organism is called the symbiont. It is usually the smaller of the two organisms and always derives benefits from its host. The symbiont is called an ectosymbiont when it lives on the surface of the host; it is called an endosymbiont when it is internal—that is, when it lives inside the host's digestive system, coelom, gonads, tissues or cells. The symbiosis is beneficial to the host in mutualism, neutral in commensalism, and harmful in parasitism.

These three categories are often abbreviated by the signs "+/+" for mutualism; "0/+" for commensalism; and "-/+" for parasitism, where the symbols to the left and right of the slash represent the primary effect of the association on the host and symbiont respectively. The "+" indicates that the relation is beneficial, "0" that it is neutral, and "-" that it is harmful. A symbiosis is defined as facultative if the host is not necessary over the full course of the symbiont's life cycle; it is defined as obligatory if the symbiont is dependent on the host throughout its life cycle. In addition, symbionts are described as either specific or opportunistic. A specific symbiont is associated with a few host species, the highest specificity being assigned to symbionts that infest only one species. Opportunistic symbionts, on the other hand, are associated with a wide range of hosts belonging to a wide variety of different taxonomic groups.

Some symbiotic associations are difficult to place within one of these three categories. Biologists often prefer to speak of the existence of a symbiotic continuum along which mutualism, commensalism, and parasitism shade into one another without strict dividing lines. Suckerfishes are an illustrative example of the problem of precise categorization. The suckerfish is an organism that attaches itself to large marine vertebrates (a host) by means of an anterior sucker. Some authors consider this symbiosis an example of mutualism because the suckerfishes eat ectoparasites located on the skin of the vertebrates to which they are attached; the suckerfishes are also able to conserve energy because while they are attached to a host, they allow their hosts to swim for them. But other researchers regard suckerfishes as ectocommensals because they eat the remains of their hosts' prey. They are even considered inquilines (symbionts that live as "tenants" in a host's nest, burrow, fur, etc. without deriving their nourishment from the host) on occasion because some of them live inside the buccal (cheek) cavities of certain fishes.

Life cycles are another factor that complicates the categorization of symbiotic relationships, in that some organisms move from one symbiotic state to another over the course of their life cycle. Myzostomids, for example, are tiny marine

worms associated with the comatulid crinoids, organisms related to sea stars. Most myzostomids are parasitic when they are young and cause deformities on the skin of their hosts. They develop, however, into ectocommensals that do not harm the crinoids except for stealing their food. Myzostomids are the oldest extant animal parasites currently known; deformities attributed to these strange worms have been identified on fossil crinoids from the Carboniferous Period, 360–286 million years ago.

The problem of categorization becomes even more complicated when organisms change their symbiotic relationships according to environmental conditions. This is the case in the mutualism between the freshwater cnidarian Hydra, which lives in ponds and slowly moving rivers, and the alga Chlorella, which lives in the cnidarian's cells. Under normal environmental conditions, the algae perform photosynthesis and release substantial amounts of carbon to the animal's cells in the form of a sugar known as maltose. In darkness, however, the flow of carbon-based compounds is reversed, with the nutrients coming from the feeding of Hydra being diverted by the algae. As a result, the growth of the cnidarians is reduced and the mutualist algae have become parasites.

Commensalism

Commensalism (from the Latin com, or "with," and mensa, or "table") literally refers to "eating together" but encompasses a wide range of symbiotic interactions. A commensal symbiont feeds at the same place as its host or steals the food of its host. This narrower definition is restricted to a very few organisms; most of the time, commensalism covers all associations that are neutral for the hosts, in which the commensal organisms benefit from the acquisition of a support, a means of transport, a shelter, or a food source. There are three major types of commensal relationships: phoresy (from the Greek phoros, "to carry"), in which the host carries or transports the phoront; aegism (from the Greek aegidos, or aegis, the shield of Athena), in which the host protects the aegist; and inquilism (from the Latin incolinus, "living inside"), in which the host shelters the inquiline in its body or living space without negative effects. Inquilism has been described by some researchers as a form of "benign squatting."

The loosest symbiotic associations are certainly the facultative phoresies. The modified crustacean Lepas anatifera, which is often attached to the skins of cetaceans (whales, dolphins, and porpoises) or the shields of turtles, is an instructive example of a phoresy. These crustaceans can be found hanging from floating pieces of wood as well as from members of other species. If other organisms often serve L. anatifera as a substrate, the association is not at all obligatory over the course of the crustacean's life cycle. The polychaete worm Spirorbis is a similar instance of a phoresy; its tube can be found sticking either to various types of organisms or to rocks in intertidal zones.

A stronger association exists between aegist symbionts and their hosts. Aegist coeloplanids are tiny flat marine invertebrates found on the spines of sea urchins or the skin of sea stars. These organisms are related to comb jellies or sea gooseberries, which are planktonic organisms. The coeloplanids are protected from potential predators by their host's defensive organs or structures. They eat plankton and organic materials from the water column trapped by their sticky fishing threads. The coeloplanids do not harm their echinoderm hosts even when hundreds of individuals are living on a single host. Many aegist relationships involve marine invertebrates, especially poriferans (sponges), cnidarians, and echinoderms. The associated organisms include polychaete worms; such crustaceans as crabs and shrimps; brittle stars; and even fishes.

The relationships between aegists and their hosts are often quite close. For example, the snapping shrimp Synalpheus lives and mates on comatulid crinoids. The crinoids have feathery rays or arms that hide the shrimps from predators. The shrimps often leave their hosts in order to feed, but are able to relocate them by smell as well as sight; they recognize the odor of a substance secreted by their hosts. This behavior is also found in some crabs, like Harrovia longipes, which also lives on comatulid crinoids.

Inquiline symbionts are particularly interesting to researchers. The most extraordinary inquilines, however, are the symbiotic pearlfishes. Pearlfishes belong to the family Carapidae, which includes both free-living and symbiotic fishes. The latter are associated with bivalves and ascidians. They can also be found in the digestive tubes of sea stars and the respiratory trees of sea cucumbers. Pearlfishes that have been extracted from their hosts cannot live more than a few days. They are totally adapted to their symbiotic way of life: their bodies are spindle-shaped; their fins are reduced in size; and their pigmentation is so poorly developed in some species that their internal organs are visible to the naked eye. Pearlfishes are often specific, and make use of olfaction (sense of smell) as well as vision to recognize their hosts. They must have some type of physiological adaptation that protects them against their hosts' internal fluids, such as the digestive juices of sea stars; however, these adaptations are not understood as of 2003.

Parasitism

In parasitic relationships (from the Greek para, "beside," and sitos, "food"), the parasitic organism first acquires a biotic substrate where it lives for part of its life cycle. This biotic substrate is often a food source for the parasite and sometimes a source of physiological factors essential to its life and growth. The parasite then seeks out a host.

Most parasites do not kill the hosts they infest even if they are pathogenic and cause disease. Diseases are alterations of the healthy state of an organism. Parasitic diseases may be divided into two types: structural diseases, in which the parasite damages the structural integrity of the host's tissues or organs; and functional diseases, in which the parasite affects the host's normal growth, metamorphosis, or reproduction. Parasitism is by far the most well-known symbiotic category, as many parasites have a direct or indirect impact on human health and economic trends. The causes of disease have always fascinated people since ancient times. Early humans thought that diseases were sent by supernatural forces or evil spirits as punishment for wrongdoing. It was not until the nineteenth century that scientific observations and studies led to the germ theory of disease. In 1807, Bénédicte Prévost demonstrated that the bunt disease of wheat was produced by a fungal pathogen. Prévost was the first to demonstrate the cause of a disease by experimentation, but his ideas were not accepted at that time as most people clung to the notion of spontaneous generation of life. By the end of the nineteenth century, however, Anton de Bary's work with fungi, Louis Pasteur's with yeast, and Robert Koch's with anthrax and cholera closed the debate on spontaneous generation and established the germ theory of disease.

In parasitic associations, animals are either parasites or hosts. There are three animal phyla, Mesozoa, Acanthocephala, and Pentastomida, that are exclusively parasitic. In addition, parasites are commonly found in almost all large phyla, including Platyhelminthes, Arthropoda and Mollusca. Many gastropod mollusks, for example, are parasites of such echinoderms as brittle stars and sea stars. Stilifer linckiae buries itself so deeply in the body wall of some sea stars that only the apex of the shell remains visible at the center of a small round hole. The gastropod's proboscis pierces the sea star's tissues and extends into the body cavity of its host, where it sucks the host's internal fluids and circulating cells. The morphology of Stilifer linckiae closely resembles that of free-living mollusks. In most cases, however, the body plans of parasites have been modified from those of their free-living relatives. The parasites tend to lose their external appendages and their organs of locomotion; in addition, their sense organs are commonly reduced or absent.

The rhizocephalan sacculines are a remarkable example of the evolutionary modification of a crustacean body plan. They are so profoundly adapted to parasitism that only an understanding of their early larval form allows them to be recognized as crustaceans. Sacculina carcini, for example, can often be observed as an orange sac on the ventral side of a crab. The early larval stages of this organism are free-living nauplii that move into the water column until they find a crab. Only female larvae seek out and attach themselves to the base

of one of the crab's bristles. Once attached, the female larvae molt and lose their locomotory apparatus, giving rise to new forms known as kentrogon larvae. Kentrogon larvae are masses of cells, each armed with a hollow stylet or thin probe. The stylet pierces the body wall of the crab as far as the body cavity; the cell mass then passes through the stylet into the host's body. In this way the kentrogon injects itself into the crab. The internal mass proceeds to grow and differentiate into two main parts: an internal sacculina that absorbs nutrients through a complex root system gradually extending throughout the crab's body; and an external sacculina that forms after the root system, emerges from the ventral side of the crab, and develops into the true body of the female parasite. The female reproductive system opens to the outside through a pore that allows the entry of a male larva. The male larva injects its germinal cells, which eventually become spermatozoa capable of fertilizing the ova. S. carcini reproduces throughout the year on the crab Carcinus maenas, but more frequently between August and December.

Mutualism

In mutualism (from the Latin mutuus, "reciprocal"), the interactions between the symbiotic organisms can be as simple as a service exchange or as complex as metabolic exchanges. Mutualistic animals are associated with a range of different organisms, including bacteria, algae, or other animals. Many marine fishes, for example, are cleaned regularly of ectoparasites and damaged tissues by specialized fishes or shrimps called cleaners. The cleaners provide a valuable service by keeping the fishes free of parasites and disease; in turn, they acquire food and protection from predators. Cleaning mutualisms occur throughout the world, but are most commonly found in tropical waters. The cleaning fishes or shrimps involved in this type of mutualism establish cleaning stations on such exposed parts of the ocean floor as pieces of coral. The cleaner organisms are generally brightly colored and stand out against the background pattern of the coral. The bright colors, along with the cleaners' behavioral

displays, attract fishes to the cleaning stations. The cleaners are then allowed to enter the mouth and gill chambers of such species as sharks, parrotfishes, grunts, angelfishes, and moray eels. Most cleaning fishes belong to the genus Labroides. Parasites that are removed from the cleaned fishes include copepods, isopods, bacteria, and fungi. Beside fishes, cleaning shrimps are also common in the tropics. The best-known species are the Pederson cleaner shrimp, Periclimenes pedersoni, and the banded coral shrimp, Stenopus hispidus. When the fishes approach their cleaning stations, these shrimps wave their antennae back and forth until the fishes get close enough for the shrimps to climb on them. Experiments have shown that the cleaners control the spread of parasites and infections among members of their host species. Cleaning symbioses also occur between land organisms: for example, various bird species remove parasites from crocodiles, buffalo and cattle; and the red rock crab Grapsus grapsus cleans the iguana Amblyrhynchus subcristatus.

The most evident mutualism between oceanic species is the one that exists between sea anemones and clown fishes. Fishes of the genera Amphiprion, Dascyllus, and Premnas are commonly called clown fishes due to their striking color patterns. The symbiosis is obligatory for the fish but facultative for the anemones. The brightly colored clown fishes attract larger predator fishes that sometimes venture too close to the anemones; they can be stung by the anemone tentacles, killed, and eaten. Clown fishes share in the meal and afterward remove wastes and fragments of the prey from the anemone. A number of experiments have been conducted in order to understand why the clown fishes are immune to the stinging tentacles of the sea anemones when other fishes are not. It is known that the clown fishes must undergo a period of acclimation before they are protected from the anemones. Further studies showed that the mucous coating of the clown fishes changes during this period of acclimation, after which the anemones no longer regard them as prey. The change in the mucous coating was first thought to result from fish secretions, but researchers were able to demonstrate that it results from the addition of mucus from the anemones themselves.

Resources

Books

Ahmadjian, Vernon, and Surindar Paracer. Symbiosis: An Introduction to Biological Associations. Hanover and London: University Press of New England, 1986.

Baer, Jean G. Animal Parasites. London: World University Library, 1971.

Douglas, Angela E. Symbiotic Interactions. Oxford, U.K.: Oxford University Press, 1994.

Morton, Bryan. Partnerships in the Sea: Hong Kong's Marine Symbioses. Leiden, The Netherlands: E. J. Brill, 1989.

Noble, Elmer R., and Glenn A. Noble. Parasitology: The Biology of Animal Parasites. Philadelphia: Lea and Febiger, 1982.

Periodicals

Eeckhaut, I., D. van den Spiegel, A. Michel, and M. Jangoux. "Host Chemodetection by the Crinoid Associate Harrovia longipes (Crustacea: Brachyura: Eumedonidae) and a Physical Characterization of a Crinoid-Released Attractant." Asian Marine Biology 17 (2000): 111–123.

Van den Spiegel, D., I. Eeckhaut, and M. Jangoux. "Host Selection by the Shrimp Synalpheus stimpsoni (De Man 1888), an Ectosymbiont of Comatulid Crinoids, Inferred by a Field Survey and Laboratory Experiments." Journal of Experimental Biology and Ecology 225 (1998): 185–196.

Igor Eeckhaut, PhD

Symbiosis

Symbiosis is simply defined as living together. Scientists use this term to describe intimate relationships between members of different species. By definition there are at least two species in a symbiotic relationship; it is unknown the maximum number of species that a symbiosis can sustain. This number may be very great; fungal partners (mycorrhizae) of plant roots link many photosynthetic plants of different species in one continuous networked symbiosis. Partners may belong to the same kingdom (for example, plants in symbiosis with other plant species) or may include partners from different kingdoms. A lichen symbiosis consists of partners from two or three kingdoms—a fungus, a protist (algae), and often a cyanobacterium (eubacteria). The smaller partner(s) are usually called the symbiont(s) and the larger partner the host. The host's cells, body, body surface, or even its home may be shared with its symbionts.

To what extent must two species live together be considered a symbiosis? A general rule is that the partners must spend a significant amount of time together (part or all of their life cycles). This sustained contact enables a relationship to develop that affects how both species adapt and evolve. The symbiotic relationship is usually classified as belonging to one of three types: mutualism (benefiting both partners), parasitism (one partner, the parasite, benefits at the expense of the host), or commensalism (one partner benefits while the other is unaffected). However, it is too simplistic to place symbioses into such restrictive categories since the environment and ecological interactions with other species may affect the nature of the relationship. Under one set of conditions a relationship may be characterized as mutualistic, while under different conditions it may be parasitic. For example, the relative benefit for plants to host ants as a way to defend them against herbivores depends on the degree of herbivory and must be weighed against the cost of synthesizing the nutritional compounds needed to support resident ants. Both of these are subject to external influences.

Symbiosis provides an important source of evolutionary novelty. Special symbiont capabilities include photosynthesis and the transfer of photo-synthetic products from cyanobacteria and algae to animal and fungal hosts, and the supply of nutrients (nitrogen fixation by bacteria in legumes and

by cyanobacteria in cycads) to plant hosts. Other novel capabilities in marine animal symbioses include light production (luminous bacteria in marine fishes and invertebrates) and chemosynthesis by sulfur-reducing bacteria in hydrothermal vent host animals. In exchange for these services, the host provides the symbiont shelter and/or nutrition. These exchanges allow symbiotic relationships to thrive in marginal environments where resources such as energy and nutrients are limiting. Lichens are able to colonize bare rocks because the fungus provides shelter and protection against desiccation , its algal partners provide nutritional energy through photosynthesis, and its cyanobacteria provide nitrogen to the algae and to the fungal host. In the coral reef ecosystem , symbiotic algae called zooxanthellae photosynthesize and provide energy-rich sugars to their host corals. In nutrient-poor and sunlit tropical seawater, this symbiosis forms the base of the food web and supports the high diversity of all coral reef organisms. Other examples of mutualistic symbioses include the relationship between fungi and the roots of higher plants. Mycorrhizae (the fungal symbionts) associate with roots of higher plants and increase the water and nutrient uptake capabilities of plants. In return, they receive photosynthetic products from their host plants. In 1997, Suzanne Simard and her colleagues found that mycorrhizae connect and transport photosynthetic products between plants and trees in different environments. Other symbionts such as parasitic orchids take advantage of this association by connecting to the fungal network and withdrawing nutrients for their own use.

In parasitic symbioses, the parasite must avoid host defenses and obtain nutrients while remaining in or on the host. In so doing, the parasite often loses the ability to live independently. Plants such as dwarf mistletoes and the largest flower in the world, Rafflesia, have lost the ability to photosynthesize; they must derive nourishment from their photosynthetic host plants. These are considered to be obligate symbioses (one or more partners is dependent on another and cannot survive alone). Often these relationships include more than one partner, each with a different role in the symbiosis. For example, insect aphids specialized to suck plant juices from their hosts must rely on intracellular bacteria for essential amino acids not available in plant tissues.

The few examples of commensalistic symbioses are behavioral; one partner taking advantage of the activities of another to obtain food. It is unlikely that the unaffected partner is truly unaffected. If it is really unaffected, commensalism is difficult to define in the context of symbiosis. The definition of symbiosis usually assumes that an interaction is taking place, which means both partners must participate.

Flexibility in the type and amount of nutritional exchanges and in the roles of partners enables the symbiotic relationship to adapt and evolve over time to meet the different needs of the partners. A symbiont, host, or both may lose the ability to live independently because the partner has irrevocably assumed certain critical life functions. This concept is fundamental to the endosymbiotic theory of the origin of eukaryotic cells. Chloroplasts and mitochondria are the remnants of former symbionts that provided novel metabolic functions (photosynthesis and respiration) to their host cells.

Finally, symbiosis plays an important and often overlooked role in ecology. Nitrogen-fixing bacteria and mycorrhizal fungi provide nutrients to primary producers, and symbiotic associations like lichens are usually the first colonizers. Feeding interactions among symbiotic partners may increase the energy efficiency of food chains and promote nutrient recycling. When one thinks about saving species and biodiversity , the emphasis should be placed on understanding and preserving symbiotic relationships. If one partner is lost, all dependent partners will perish. It is rare that any species lives in isolation.

see also Coevolution; Endosymbiosis; Interactions, Plant-Fungal; Interactions, Plant-Insect; Interactions, Plant-Plant; Interactions, Plant-Vertebrate; Lichen; Mycorrhizae; Parasitic Plants.

Gisèle Muller-Parker

Bibliography

Douglas, A. E. Symbiotic Interactions. Oxford, England: Oxford University Press, 1994.

Margulis, Lynn. Symbiosis in Cell Evolution, 2nd ed. San Francisco: Freeman, 1993.

——, and Rene Fester, eds. Symbiosis as a Source of Evolutionary Novelty. Cambridge, MA: M.I.T. Press, 1991.

Paracer, Surinder, and Vernon Ahmadjian. Symbiosis: An Introduction to Biological Associations, 2nd ed. Oxford: Oxford University Press, 2000.

Simard, S. W., D. A. Perry, M. D. Jones, D. D. Myrold, D. M. Durall, and R. Molina. "Net Transfer of Carbon Between Ectomycorrhizal Tree Species in the Field." Nature 388 (1997): 579-82.

Symbiosis

Symbiosis describes the relationship, close association, or interaction between two organisms of different species. Although the term is often used to describe a relationship that benefits both species, there are different types of symbiosis. Symbiotic relationships that have occurred over very long periods of time can sometimes result in evolutionary changes in the organisms involved in the relationship.

Symbiosis literally means "living together," and there are many examples in nature of organisms of entirely different species that are involved

LYNN MARGULIS

American biologist Lynn Margulis (1938– ) has suggested some of the more revolutionary ideas in the history of modern biology. Her symbiotic theory of evolution has offered a new approach to both evolution and the origin of cells within the nucleus. She also subscribes to the "Gaia" hypothesis, which states that the Earth acts a superorganism, or single living system, that can regulate itself.

Lynn Margulis was born in Chicago, Illinois. Her parents, Morris and Leone Alexander, had three other daughters. An exceptional student, Margulis was fifteen when she completed her second year at Hyde Park High School and was accepted into an early entrant program at the University of Chicago. There she was immediately inspired by her science courses and took to reading the original works of the world's great scientists. She also became interested in the deeper aspects of heredity and genetics. While at Chicago, she met Carl Sagan (1934–1996), who would become an astronomer (a person who studies the universe beyond Earth) and one of the best-known scientists in the world. Sagan was a graduate student and Margulis was nineteen in the year she both received her bachelor's degree and married Sagan. She then entered the University of Wisconsin to pursue a joint master's degree in zoology and genetics, and in 1960 she and Sagan moved to the University of California at Berkeley where she conducted genetic research for her doctoral dissertation. The marriage to Sagan produced two sons but ended before she received her Ph.D. in 1965. After teaching at Brandeis University, she joined Boston University and married crystallographer (a person who studies crystal structure) Thomas N. Margulis, with whom she had two children before they divorced in 1980. Since 1988, Margulis has been a distinguished university professor at the University of Massachusetts at Amherst.

Margulis has regularly questioned the commonly accepted theories of genetics yet she has been called the most gifted theoretical biologist of her generation by numerous colleagues. As a graduate student she became interested in what is called non-Mendelian inheritance, which is when the genetic makeup of a cell's descendants cannot be traced solely to the genes in the cell's nucleus (the cell's control center). This puzzling phenomenon led her to search for genes in the cytoplasm of cells, that is, inside the cell but not inside its nucleus. In the early 1960s, Margulis actually found deoxyribonucleic acid (DNA, which is the carrier of genetic information) in the cytoplasm (jelly-like substance) of plant cells, suggesting that heredity in higher organisms might not be totally determined by genetic information carried only in the cell nucleus. This led her to eventually formulate her most startling idea, called the serial endosymbiotic theory (SET). Margulis stated that prokaryotes (cells that do not have a nucleus, such as very simple life forms like bacteria), which simply carry their genetic information inside the cell's cytoplasm, were the evolutionary forerunners of the more complex eukaryotes (which are cells that have a separate nucleus). All plants and animals have eukaryotic cells. She argued that eukaryotes evolved from prokaryotes when different types of prokaryotes formed symbiotic systems to increase their chances of survival. Symbiosis means that they had some sort of relationship, usually a type of partnership in which both members benefitted. An example of this, she says, is a cell's mitochondria (specialized structures inside a cell that break down food and release energy) that process oxygen.

Most scientists now agree that these cell structures evolved from oxygen-using bacteria, which joined with fermenting bacteria. Margulis is unique in her argument that traditional evolutionary theory cannot explain what she calls the "creative novelty" of life. Margulis also extends her concept of symbiosis to the entire biosphere (that part of Earth that contains life) and therefore accepts the Gaia hypothesis put forth by English chemist James E. Lovelock. This theory states that all life, and Earth itself, including its oceans and the atmosphere, are parts of a single, all-encompassing symbiosis that in turn form a single "organism," or a single living system. For Margulis, the concept of symbiosis is a powerful explanatory tool.

in some form of close, beneficial relationship or association. In fact, there are some symbiotic relationships that are necessary for the survival of the participating organisms. There are three types of symbiosis—mutualism, commensalism, and parasitism—depending on the nature of the relationship. As with any classification system, there are always exceptions, and sometimes it is difficult to categorize a certain situation. It is also a mistake to make a judgment of one type of symbiosis being better than another, since each is simply an organism's adaptation to survive.

Mutualism is a type of symbiotic relationship that results in a mutual benefit. Both species realize some type of gain by living together and cooperating within the same habitat. An example of mutualism would be the close relationship between a certain bacteria (Rhizobia) that lives under the soil and is attached to the roots of certain plants like peas, beans, clover, and alfalfa. These bacteria are nitrogen-fixing, meaning they are able to take in nitrogen gas that exists in the atmosphere and change it into nitrates that plants can use. This plant/bacteria relationship is mutualistic because both organisms benefit: the plant gains the necessary nitrogen in a usable form, and the bacteria gains access to a source of energy (using the plant's ready-made glucose). This is also an example of what is called "obligatory mutualism," since both partners are completely dependent on each other. Another example of this type of mutualism is the lichen, which is really made up of a fungus (plural, fungi), and an alga (plural, algae) living together. An alga can make its own food but can only live in wet places. A fungus cannot make its own food but can store a great deal of water. Together, they can live anywhere since the alga makes food (and lives inside the fungus), while the fungus provides it with its necessary water.

The other form of mutualism is called "facultative" and describes a relationship in which both partners benefit, but which each could still survive if the relationship did not exist. The relationship between the oxpecker (also called the tickbird) of Africa and the black rhinoceros is a good example, since these birds spend most of their time clinging to the bodies of large animals like the rhinoceros and eating ticks and maggots that infest the rhinoceros' hides. The birds also make a hissing sound that alerts the rhinos to possible danger. The rhinoceros benefits by having blood-sucking insects removed from its body, as well as having an early warning system. However, although both animals benefit from their relationship, the bird could obtain insects elsewhere if the rhino were to vanish, and the rhino could survive being infested with ticks.

Commensalism is the second type of symbiosis and describes a relationship in which one species benefits while the other experiences basically no effect (it neither benefits nor suffers). A bromeliad (an air plant) growing on the high branch of a rainforest tree is an example of such a relationship since it benefits by being closer to the sunlight while the tree is not harmed in any way (it also does not receive anything beneficial from the bromeliad). Another example is the tiny mollusks or crustaceans called barnacles that attach themselves to the body of a humpback whale enjoy the benefit of being moved through the water so they can filter microscopic food. The whale is neither bothered nor benefitted by the mollusks. Commensalism is usually practiced by one species on another to obtain something it cannot provide for itself such as transportation, protection, or nutrition.

Finally, a symbiotic relationship is described as parasitism if it results in the host organism being somehow harmed. In this type of relationship, the organism that benefits is called the parasite, while the organism that the parasite lives in or on is called the host. Disease-producing organisms are probably the best examples of parasitism. Such is the case with a tapeworm that lives inside the digestive organs of mammals. Because the tapeworm takes nutrition from the host, the host is left weakened and may also suffer tissue damage. An example of a strange and interesting form of parasitism is that conducted by a brood parasite. In this phenomenon, one species of animal uses the adult or parent of another species to raise its young. The common cuckoo bird does this regularly by laying its eggs in the nest of a species with similar-looking eggs. As soon as the cuckoo hatches, it pushes all the other eggs from the nest and eats all the food provided by its foster parents (which have been tricked into raising the cuckoo as their own).

[See alsoParasite ]