Symbiosis and other interactions between organisms in Nature
Ian D. Lawn
Department of Microbiology & Parasitology, The University of Queensland, Brisbane, Australia 4072
The interactions that occur between organisms in Nature exert a major effect on their ecology and evolution. Often, the most fascinating interactions occur between organisms of different species and this lecture will explore some of the more intriguing examples, many of which are encountered in symbiotic relationships and escape behaviours.
Introduction
The phenomenon of symbiosis touches all aspects of life. It has had a profound effect on the intracellular organization and evolution of the eukaryotic cell (those cells that contain a nucleus and make up our own bodies, as well as those of all other animals, plants, fungi and protists). At the other end of the biological spectrum, symbiosis can be seen at work in the realms of sociobiology and population ecology. It is encountered in all forms of life, from the simplest bacteria through to birds and mammals. While it is often said that parasitism is the most common way of life (some 50% of animal species are parasites), this distinction really belongs to symbiosis which, in its broadest context, embraces not only parasitism, but also mutualism, commensalism, aegism and phoresis. For example, mutualism operates in 90% of land plants (these are mycorrhizal in nature) and virtually all mammalian and insect herbivores would starve without their cellulose-digesting symbionts.
The role of symbiosis in shaping evolution has been the subject of rigorous debate for over a century because it challenge the very core of Darwinian thinking on evolutionary processes. In essence, neo-Darwinian theory propounds that evolution progresses gradually and continuously: that coding errors in DNA replication result in random genetic mutations that are manifest as slight variations in the items they produce (the phenotype). Natural selection then tests these phenotypic variations via a process of competitive interactions: the outcome is that the successful variations survive, perhaps to develop into a new species, and the unsuccessful are eliminated. In contrast, symbiosis theory advocates that these gradual evolutionary changes are occasionally punctuated by bursts of rapid speciation brought about by cooperative, rather than competitive, interactions between organisms. This source of evolutionary innovation is believed to be the driving force in the origin of the eukaryotic cell, but it may also operate at higher levels; for example, in the evolution of the reef-building corals and the lichens.
Symbiosis, then, is encountered in all of the known taxonomic groups and operates in a wide range of biological interactions. Yet, as a discipline, it is still in its infancy and is only beginning to emerge as a field of study in some of the more progressive universities. Unfortunately, here in Australia, no university is currently offering a course in this important subject. This lecture will adopt a broadly-based approach to the study of symbiotic associations, and we shall see how the common theme of symbiosis brings together a wide range of biological phenomena which, in themselves, reflect the astonishing ingenuity, complexity and diversity to be found in Nature.
Some Confusions in Terminology
The term “symbiosis” (plural: “symbioses”) derives from the Greek sumbiosis meaning “living together”. Virtually all textbooks attribute the origin of its scientific usage to the German mycologist, Anton de Bary, who used the term in 1879 in a paper on lichens entitled: “Die Erscheinung der Symbiose” (The phenomenon of symbiosis) (De Bary, 1879). An examination of the literature, however, reveals that the term was first used in 1877 by another German mycologist, Albert Frank, also in a paper on lichens (Frank, 1877).
De Bary’s original use of the term defined symbiosis in the broadest possible way as “the living together of differently-named organisms” (i.e. different species). He included in his definition all cases of intimate associations between species, such as epiphytes growing on trees, insects pollinating flowers, parasitism, mutualism and commensalism. During the next 50 years or so, confusion arose as to the exact meaning of the term “symbiosis” because de Bary had coined the term in his paper on the lichen association, which just happened to be mutualistic. Those who had not read his paper thoroughly, therefore, erroneously equated “symbiosis” with “mutualism” (see definitions below) and this error continues to crop up in some contemporary texts. Today, however, most biologists have reverted back to de Bary’s original, broad definition as follows:
Symbiosis is the living together of different species, usually in close association with one another, to the benefit of at least one of them.
(The words in italics indicate the key features that must be present in order to define a relationship as a symbiosis).
All of the partners actively involved in a symbiotic association are classified as symbionts, but they also may be referred to by more specific terms. For example, many of the partners in a symbiosis are of unequal size: in such situations, the larger is often referred to as the host and the smaller the symbiont, or a more specific term, such as parasite, inquiline, endokaete or phoront. The “host”, however, is not always the larger of the symbionts; nest parasites, such as cuckoo chicks, are usually much larger than their host “foster” parents. One further area of confusion relates to the term “living together”: how does one categorize the duration, stability and intimacy of an association implicit in such a term? Some biologists maintain that even the most transient associations are symbioses, provided the relationship is significant to the “well being” of at least one of the partners. By this definition, symbiosis would include the pollination of flowers by insects, the activities of cleaner fish and their clients and, at the extreme, even predator-prey relationships. Others maintain that a symbiotic association must persist for “an appreciable length of time” relative to the life span of the partners involved. In practice, such black-and-white definitions are fraught with difficulties because Nature has a wonderful way of revealing new and complexing shades of grey just as we are starting to become comfortable with our latest definitions. To me, this is what makes the study of Natural History such a challenging and exciting area!
The Major Types of Symbiosis
Because of the broad nature of its definition, symbiosis is generally broken down into sub-categories that describe the various types of association. The most frequently used are given below:
Parasitism: No single definition of parasitism is accepted by all biologists. In its simplest form, parasitism is a one-sided association in which one of the symbionts (the parasite) benefits at the expense of the other (the host). Some parasitologists prefer to narrow this definition further and describe parasitism as an intimate, protracted, obligatory association between two species in which the smaller (the parasite) is metabolically dependent upon the larger (the host).
Mutualism: This term is often (erroneously) equated with symbiosis. It describes those situations in which both symbionts derive reciprocal benefit from the association. Strictly speaking, mutualism describes any mutualistic interaction occurring between individuals, whether intra- or inter-specific, and includes such behaviour as cooperative hunting, cooperative defence and reciprocal altruism. Where the organisms involved are of different species, the correct description of the relationship is a mutualistic symbiosis.
Commensalism: Literally means “dining together” and is used to describe those associations in which the symbionts share a food resource without harming one another. If the sharing of food significantly affects the well-being of the organism that has caught it, the relationship shifts towards kleptoparasitism. The latter is well illustrated by the feeding behaviour of frigate birds which, in flight, will harass a bird that has caught a fish to such an extent that the fish is regurgitated, only to be caught in mid-air by the aerobatic frigate bird. The term “commensalism” may sometimes be used in a broader context to describe any association (not just a nutritional one) where one symbiont benefits and the other is neither harmed nor benefited. Most symbiosis researchers, however, prefer to use other terms to define these non-nutritional associations (see below).
Aegism: Literally means “protection” and has been introduced recently to describe those associations in which one symbiont is afforded protection by the other (the host) without the host being harmed. Aegism may be further sub-categorized as follows:
• Epizoism/Epiphytism: Describes those associations in which one symbiont (the epizoite, if living on an animal; the epiphyte, if living on a plant) habitually lives on the outer surface of the other (the host).
• Endoecism: Derives from the Greek endon (within) and oikos (house) and describes those associations in which one symbiont (the endokaete) habitually shelters in the burrow of the other (the host).
• Inquilinism: Derives from the Latin inquilinus (to dwell within) and describes those associations in which one symbiont (the inquiline, or endosymbiont) habitually lives within the other (the host) without the host being harmed. An inquiline tends to form a more intimate association with its host than an endokaete does (for example, an endokaete may be perfectly at home in a number of host burrows, but an inquiline is typically found within only one host).
Phoresis (or Phoresy): Derives from the Greek phoresis (to be carried) and describes those associations in which one symbiont utilizes the transporting potential of the other (the host).
The categories listed above should not be regarded as mutually exclusive: a symbiosis may contain elements of two or more of these categories at any given time, and there may be frequent transitions from one category to another as the dynamics of the association changes. A good example of the latter is shown by the North American harvestfish Peprilus which, in its juvenile stage, seeks out the protective umbrella of a jellyfish to shield it from predators in open water. As Peprilus grows, however, it starts to nibble on pieces of its host until it eventually consumes it. Later, when Peprilus develops into an adult, it becomes a predator of jellyfish. The relationship over time, therefore, has gradually shifted from inquilinism to parasitism and, finally, to predation. This illustrates that the various symbiotic relationships are best viewed as part of a spectrum of associations, with each category having links that are closer to one type than another.
There is now a compelling body of evidence that the miniature powerhouses of eukaryotic cells – the mitochondria – have actually evolved from a symbiotic, aerobic bacterium that was engulfed by the ancient ancestors of eukaryotic cells some 1.5 billion years ago. Perhaps the strongest evidence has come from molecular studies, which indicate that mitochondria closely resemble bacteria in their molecular biology rather than the eukaryotic cells that they are contained within. For example, the mitochondria not only possess their own DNA, which is kept separate from that contained in the eukaryotic cell’s nucleus, but also their DNA is similar to that found in bacteria.
Related studies have shown that chloroplasts, the photosynthesizing units contained within plant cells that are responsible for converting sunlight into carbohydrates, are also evolved from a similar symbiosis involving photosynthesizing cyanobacteria. There is also some evidence that the whip-like, locomotory apparatus (undulipodia) found in some eukaryotic cells (such as the ciliated cells that line our own respiratory tract) are derived from an ancient symbiosis involving spirochaete bacteria. If this sounds far fetched, consider an organism that exists today: the parabasilid protistan Mixotricha paradoxa, which harbours a veritable community of symbionts. The single-celled host is actually a cooperative involving as many as 0.5 million individual organisms! On the surface of the host cell are two forms of spirochaete bacteria that propel the host through the fluid that it lives in. The spirochaetes attach to the cell surface via anchor bacteria embedded in the host cell membrane. Numerous internal symbiotic bacteria within the host cell aid metabolism. Finally, Mixotricha itself is a symbiont found in the gut of Australian termites and is responsible for the digestion of the wood that the termite ingests. Faced with such real-life examples of highly-complex symbiotic interactions on such a small scale, it is fascinating to contemplate that all of the higher life forms were ultimately derived from associations that developed over a billion years ago between the ancestors of eukaryotic cells and symbiotic bacteria!
Mycorrhizae
It has been estimated that some 90% of land plants form a mutualistic symbiotic association with mycorrhizal fungi: this probably represents the most abundant type of symbiosis in Nature. The mycorrhizal fungi absorb and transfer to the plant mineral nutrients, especially phosphorus (one estimate is that they increase the efficiency of phosphorus uptake in wheat plants growing on phosphate-deficient Australian soils by a factor of 10,000). Nitrogen, zinc and copper may also be transferred, and some mycorrhizae supply plant-growth hormones. Because of the efficiency with which fungi absorb mineral nutrients, they enable plants to grow on soils that would otherwise be unable to support them. Such plants are more resistant to high temperature, drought (particularly through increased phosphorus uptake), disease and pollution. The mycorrhizae also help native plants to become established by reducing competition with weeds (the latter typically require high levels of nutrients but cannot extract these as efficiently as mycorrhizae and do not form mycorrhizal associations). In return for these nutrients, the plant generally supplies the fungus with organic carbon (mainly in the form of carbohydrates) and vitamins.
One of the more interesting forms of mycorrhizae are those associated with orchids. They involve fungi from several genera of the Basidiomycota and are restricted to forming symbioses with orchids, a family comprising some 20,000 species. The symbiosis is unusual in that the plant derives carbon from the fungus, and not vice-versa, as in other mycorrhizal associations. For many years, nobody was able to grow orchids from seeds and it was not until 1904 that the French botanist, Nöel Bernard, showed that, if the seeds were infected with certain types of fungi, they could be persuaded to germinate. It has now been confirmed that, in Nature, orchid mycorrhizae are essential for the successful germination of all orchid species, and this sets them apart from other types of mycorrhizae. The reason for this is that the seeds of orchids are extremely small (several can sit on a pin head) and have few nutrient reserves. The fungal partner is able to supply the essential carbohydrates and nutrients that the seed requires in order to germinate and become established. To date, there is no clear evidence of the orchid supplying anything to the fungus (even in adult orchids that are actively photosynthesizing) so the symbiosis may not be mutualistic, although it has been suggested that the plant may provide “anchorage” to the fungus.
Mycorrhizae are well represented in the fossil record and there is some evidence that the successful colonization of the land by plants was assisted by the ability of mycorrhizae to extract nutrients from the (almost) totally inorganic soils of the time.
The micro-organisms involved in photosynthetic symbioses with host organisms are known, collectively, as photobionts. These include certain cyanobacteria, prochlorophytes and some of the protists (in the latter group, the photobionts are mainly dinoflagellates and green algae). Photobionts are found in a wide range of marine, freshwater and terrestrial hosts where their photosynthetic products are generally utilized as a source of organic carbon. In return, the hosts may provide a source of nitrogen and other nutrients, as well as providing a protective environment for the photobionts.
I have already mentioned the historical role played by lichens in the study of symbiosis. The lichen is a mutualistic symbiosis between a host fungus and a photobiont (in this case, green algae and/or cyanobacteria) which results in a unique morphological structure, the lichen thallus, and unique products, the lichen chemicals. Neither of these items can be produced by the individual symbionts outside of the symbiosis: a phenomenon known as “integration”. There are some 15,000 lichen species worldwide and they occur in virtually every pioneer, terrestrial ecosystem, from the polar regions to the tropics. Their ability to withstand xeric (dry) conditions enable them to dominate very dry habitats, a feature directly related to their photophilous, or light-loving, characteristics. The photobionts are protected from desiccation and excessive exposure to light by the overlying fungal tissues and they can slow down their metabolism to enter a state of dormancy if conditions become extreme.
Reef-building (hermatypic) corals also utilize photobionts (in this case, dinoflagellates) as a source of organic carbon. Recent concerns regarding the bleaching of hermatypic corals (i.e. the loss of their photobionts) testify to the importance of this symbiosis in maintaining the health of the coral host. In addition to their nutritional role, however, the photosynthetic activities of the symbiotic dinoflagellates help the corals to deposit calcium carbonate at a higher rate than would be achieved without their photobionts. It is this factor that enables hermatypic corals to build up reefs, because the photobionts allow the individual coral polyps to construct their limestone skeletons faster than the erosive forces of the oceans can break them down. It is humbling to consider that such a massive structure as a coral reef is ultimately dependent upon the photosynthetic activities of a tiny, single-celled, symbiotic organism contained within the coral polyp!
The ability of photobionts to enhance calcification is also utilized by other hosts that build substantial skeletons. The giant clams found in tropical seas, for example, employ their photobionts in a similar way to corals to help them construct their massive shells. On a much smaller scale, the unicellular marine protists known as Foraminifera can form intracellular symbiotic associations with a wide range of photobionts. Most foraminiferans produce calcareous shells and have developed several morphological and behavioural adaptations to maximize light capture for their photobionts. These include a large surface area per unit volume, reduction in the thickness of the side walls of the shell to form “windowed” chambers that act as miniature greenhouses, and movement of the host cell towards light. In some planktonic species, the foraminiferans act as “shepherds” to their “flock” of photobionts: the latter migrate into extended spines (pseudopodia) during daylight and are withdrawn into the protection of the shell at night. As with corals and clams, foraminiferans utilize the photosynthetic activities of their photobionts to help build their calcareous shells: it has been found that, in the presence of light, calcium deposition can be increased by as much as 50 times compared with calcification in darkness!
My own research is currently involved with an unusual behaviour occurring between a common ascidian (sea squirt) of tropical seas, Didemnum molle, and its photobiont, a prochlorophyte called Prochloron. It appears that the photobiont may be capable of modifying the behaviour of its ascidian host when it encounters light. What is remarkable is that the photosensitive response mediated by Prochloron occurs over a relatively-short time scale compared with the long-term events that bring about changes of morphology or orientation. If the presence of Prochloron were, indeed, capable of evoking this behavioural event in D. molle, it would be the first known example of a photobiont driving the behaviour of its animal host on such a time scale and would provide a model system for analyzing the processes of behavioural communication between photobionts and their hosts.
This symbiosis has another unusual feature: the manner in which the photobionts are transferred from one generation to another. When host organisms reproduce, their symbionts may be passed on to the next generation via a free-living phase, which enters the surrounding environment and subsequently has to re-infect the host, or via direct transmission in which there is no significant, intervening free-living phase. Direct transmission may involve mechanisms whereby symbionts are smeared on to fertilized eggs, or are included in the cytoplasm of oocytes prior to fertilization. In the case of D. molle, the larval stage physically carries its photobionts attached to specialized structures at the base of the tail. This guarantees the perpetuation of the symbiosis from one generation to the next. Some insects that enter into symbioses with certain fungi, may also carry their symbionts from one location to another using special pouches known as mycetangia.
Probably the best-known marine symbiosis is that occurring between anemonefishes and their host sea anemones. First described by the naturalist Cuthbert Collingwood in 1868 from his observations off the shores of Borneo, there has been much subsequent research into the nature of this symbiosis. Although almost 1,000 species of sea anemones have been described worldwide, only 10 species are known to act as hosts to anemonefishes and all are restricted to warm waters of the Indo-Pacific region. The 28 species of anemonefishes known to form symbiotic associations with anemones cannot survive in nature without them (although they can survive without a host anemone in an aquarium where predators are absent). Anemonefishes are obviously utilizing the protection provided by their hosts: sea anemones have potent stinging cells that deter most would-be predators. But how do anemonefishes avoid being stung themselves when they dart into their host’s crown of stinging tentacles?
There are two main hypotheses, both of which relate to the fishes building up a protective coating of mucus. One proposes that the mucus comes from the host anemone. If an anemonefish is separated from its host for a period of time (usually a few days or weeks, depending on the species involved), when the partners are reunited, the fish usually approaches its host’s tentacles cautiously and, on contact, retreats rapidly, sometimes appearing to be stung. It keeps repeating this process until it is becomes acclimated to the stings and is able to maintain continual contact with the tentacles. This unusual behaviour is believed to build up a coating of the anemone’s mucus over the surface of the fish and, hence, the anemone does not recognise the fish as potential prey, i.e. it becomes a fish in anemone’s clothing! The second hypothesis proposes that the anemonefish itself has evolved a mucus that does not contain the compounds that would normally elicit the stinging response, i.e. a form of biochemical camouflage. There are good arguments for and against these two hypotheses: the truth may reside somewhere between the two, with one element more dominant than the other depending on the species involved in the symbiosis.
An anemonefish sheltering among the stinging tentacles of its host sea anemone represents one of the best-known examples of a marine symbiosis.
Photo Myriam Preker.
The dependence of anemonefishes on their anemone hosts is reflected in many aspects of their life history. Their eggs are usually laid on bare rock under the overhang of the anemone’s tentacles and, after hatching, spend only 8-12 days as planktonic larvae before settling to the bottom to undergo metamorphosis into juveniles (most related fish species take 6-8 weeks to reach this stage). Once it metamorphoses, it is imperative that the juvenile anemonefish finds a suitable host anemone or it will be consumed by predators. Even locating such an anemone is no guarantee that a juvenile will be able to form an association if a group of anemonefishes is already present. Their unusual social structure often makes it difficult for a newcomer to be accepted into the group. Each group typically consists of a hierarchy of two adults (a dominant female and a smaller, sub-dominant male) and 2-4 non-breeding, smaller fish. The two adults generally get along well with one another, but the male spends much of its time bullying the largest of the non-breeding fish and so on down the line. Hence, a newcomer may receive rough treatment from the resident fish and could be driven away. If the female dies, or is experimentally removed, the male changes sex to become the new female (a process known as protandrous hermaphroditism) and grows larger, while the largest of the non-breeding fish becomes the new male in the group. This stratagem ensures that the group always has two, reproducing adults: the male does not have to leave its anemone in order to find a new mate (hence, facing the risk of predation) and does not have to wait for a female to chance by.
The anemonefishes obviously benefit from their association with anemones, but is this a mutualistic symbiosis? Does the sea anemone benefit in any way? Accounts of anemonefishes bringing food to their hosts is probably an artifact of aquarium situations where food is abundant. It has been observed, however, that when anemonefishes are removed from their hosts in Nature, the anemones are often devoured by butterflyfishes. The aggressive, territorial behaviour of the anemonefishes may well protect their host anemones from potential predators.
I would like to conclude with an interesting interaction between different species that is not a symbiosis but an escape behaviour. There are many such instances in Nature, but this one is unusual in that it involves an organism that, normally, is cemented firmly to a rock or a shell. I have a particular interest in this organism because I have spent many years working on it. The organism is called Stomphia and it is a sea anemone that can be found in the seas off the coast of British Columbia and Washington, in the northeast Pacific. Like many sea anemones, the adhesive that attaches it to the substrate is so powerful that the anemone’s removal by force often results in the tissues of its pedal disk being torn apart. If the predatory starfish Dermasterias imbricata comes into contact with Stomphia, however, the anemone is able to release its pedal disk in a matter of a few seconds and swims away! How a sedentary organism like a sea anemone is able to achieve this remarkable feat is an entire lecture in itself, but it serves to illustrate that Nature is replete with examples of interesting and unusual interactions between species, if we are only prepared to look.
There is a tendency for scientists nowadays to focus on narrow, highly-specialized areas and this is reflected in the courses that universities are currently offering. Broadly-based courses in natural history are becoming difficult to find in the university curriculum (not to mention the academics who can teach them) and, yet, my own experience is that students still find such courses extremely interesting and rewarding – if they can locate one! Symbiosis, and other interactions that occur between species, hold a particular fascination for the student of natural history and it is my hope that we will eventually see the re-emergence of natural history to take its rightful place alongside such “modern” disciplines as molecular biology and genetics. Even in the world of contemporary biology, it still has much to offer in our endeavours to understand the “workings” of Nature.
References Cited
DE BARY, A. (1879). Die Erscheinung der Symbiose. In Vortrag auf der Versammlung der Naturforscher und Ärtze zu Cassel, pp. 1-30. Verlag von Karl J. Trubner, Strassburg.
FRANK, A. B. (1877). Über die biologischen Verhältnisse des Thallus eineger Krustenflechten. Beitrage zur Biologie der Pflanzen 2: 123-200.
Key Sources of Inspiration and Further Reading:
AHMADJIAN, V. & PARACER, S. (1986). Symbiosis: an Introduction to biological Associations. University Press of New England, Hanover & London.
FAUTIN, D.G. & ALLEN, G.R. (1992). Field Guide to Anemonefishes and their Host Sea Anemones. Western Australian Museum, Perth.
GOTTO, R.V. (1969). Marine Animals: Partnerships and other Associations. The English Universities Press, London.
HENRY, S.M. (ed.) (1966). Symbiosis. Volume I. Associations of Microorganisms, Plants, and marine Organisms. Academic Press, New York & London.
HENRY, S.M. (ed.) (1967). Symbiosis. Volume II. Associations of Invertebrates, Birds, Ruminants and other Biota. Academic Press, New York & London.
LAWN, I.D. (1976). A slow conduction system triggers swimming in the sea anemone Stomphia coccinea. Nature, Lond 262: 708-709.
MORTON, B. (1988). Partnerships in the Sea: Hong Kong’s marine Symbioses. Hong Kong University Press, Hong Kong.
ZANN, L.P. (1980). Living together in the Sea. T.F.H. Publications, Hong Kong.