White tailed deer symbiotic relationships

Ecology Online Simulation

CHAPTER 15

Smith, T. M., & Smith, R. L. (2015). Elements of Ecology (9th ed.). Boston, MA: Pearson.

15.1 Parasites Draw Resources from Host Organisms

Parasitism is a type of symbiotic relationship between organisms of different species. One species—the parasite—benefits from a prolonged, close association with the other species—the host—which is harmed. Parasites increase their fitness by exploiting host organisms for food, habitat, and dispersal. Although they draw nourishment from the tissues of the host organism, parasites typically do not kill their hosts as predators do. However, the host may die from secondary infection or suffer reduced fitness as a result of stunted growth, emaciation, modification of behavior, or sterility. In general, parasites are much smaller than their hosts, are highly specialized for their mode of life, and reproduce more quickly and in greater numbers than their hosts.

The definition of parasitism just presented may appear unambiguous. But as with predation the term parasitism is often used in a more general sense to describe a much broader range of interactions (see Section 14.1). Interactions between species frequently satisfy some, but not all, parts of this definition because in many cases it is hard to demonstrate that the host is harmed. In other cases, there may be no apparent specialization by the parasite or the interaction between the organisms may be short-lived. For example, because of the episodic nature of their feeding habits, mosquitoes and hematophagic (blood-feeding) bats are typically not considered parasitic. Parasitism can also be used to describe a form of feeding in which one animal appropriates food gathered by another (the host), which is a behavior termed cleptoparasitism (literally meaning “parasitism by theft”). An example is the brood parasitism practiced by many species of cuckoo (Cuculidae). Many cuckoos use other bird species as “babysitters”; they deposit their eggs in the nest of the host species, which raise the cuckoo young as one of their own (see Chapter 12 opening photograph). In the following discussion, we use the narrower definition of parasite as given in the previous paragraph, which includes a wide range of organisms—viruses, bacteria, protists, fungi, plants, and an array of invertebrates, among them arthropods. A heavy load of parasites is termed an infection, and the outcome of an infection is a disease.

Parasites are distinguished by size. Ecologically, parasites may be classified as microparasites and macroparasites. Microparasites include viruses, bacteria, and protists. They are characterized by small size and a short generation time. They develop and multiply rapidly within the host and are the class of parasites that we typically associate with the term disease. The infection generally lasts a short time relative to the host’s expected life span. Transmission from host to host is most often direct, although other species may serve as carriers.

Macroparasites are relatively large. Examples include flatworms, acanthocephalans, roundworms, flukes, lice, fleas, ticks, fungi, rusts, and smuts. Macroparasites have a comparatively long generation time and typically do not complete an entire life cycle in a single host organism. They may spread by direct transmission from host to host or by indirect transmission, involving intermediate hosts and carriers.

Although the term parasite is most often associated with heterotrophic organisms such as animals, bacteria, and fungi, more than 4000 species of parasitic plants derive some or all of their sustenance from another plant. Parasitic plants have a modified root—the haustorium—that penetrates the host plant and connects to the vascular tissues (xylem or phloem). Parasitic plants may be classified as holoparasites or hemiparasites based on whether they carry out the process of photosynthesis. Hemiparasites, such as most species of mistletoe (Figure 15.1), are photosynthetic plants that contain chlorophyll when mature and obtain water, with its dissolved nutrients, by connecting to the host xylem. Holoparasites, such as broomrape and dodder (Figure 15.2), lack chlorophyll and are thus nonphotosynthetic. These plants function as heterotrophs that rely totally on the host’s xylem and phloem for carbon, water, and other essential nutrients.

Parasites are extremely important in interspecific relations. In contrast with the species interactions of competition and predation, however, it was not until the late 1960s that ecologists began to appreciate the role of parasitism in population dynamics and community structure. Parasites have dramatic effects when they are introduced to host populations that have not evolved to possess defenses against them. In such cases, diseases sweep through and decimate the population.

15.2 Hosts Provide Diverse Habitats for Parasites

Hosts are the habitats of parasites, and the diverse arrays of parasites that have evolved exploit every conceivable habitat on and within their hosts. Parasites that live on the host’s skin, within the protective cover of feathers and hair, are ectoparasites. Others, known as endoparasites, live within the host. Some burrow beneath the skin. They live in the bloodstream, heart, brain, digestive tract, liver, spleen, mucosal lining of the stomach, spinal cord, nasal tract, lungs, gonads, bladder, pancreas, eyes, gills of fish, muscle tissue, or other sites. Parasites of insects live on the legs, on the upper and lower body surfaces, and even on the mouthparts.

Parasites of plants also divide up the habitat. Some live on the roots and stems; others penetrate the roots and bark to live in the woody tissue beneath. Some live at the root collar, commonly called a crown, where the plants emerge from the soil. Others live within the leaves, on young leaves, on mature leaves, or on flowers, pollen, or fruits. A major problem for parasites, especially parasites of animals, is gaining access to and escaping from the host. Parasites can enter and exit host animals through various pathways including the mouth, nasal passages, skin, rectum, and urogenital system; they travel to their point of infection through the pulmonary, circulatory, or digestive systems.

For parasites, host organisms are like islands that eventually disappear (die). Because the host serves as a habitat enabling their survival and reproduction, parasites must escape from one host and locate another, which is something that they cannot do at will. Endo-macroparasites can escape only during a larval stage of their development, known as the infective stage, when they must make contact with the next host. The process of transmission from one host to another can occur either directly or indirectly and can involve adaptations by parasites to virtually all aspects of feeding, social, and mating behaviors in host species.

15.3 Direct Transmission Can Occur between Host Organisms

Direct transmission occurs when a parasite is transferred from one host to another without the involvement of an intermediate organism. The transmission can occur by direct contact with a carrier, or the parasite can be dispersed from one host to another through the air, water, or other substrate. Microparasites are more often transmitted directly, as in the case of influenza (airborne) and smallpox (direct contact) viruses and the variety of bacterial and viral parasites associated with sexually transmitted diseases.

Many important macroparasites of animals and plants also move from infected to uninfected hosts by direct transmission. Among internal parasites, the roundworms (Ascaris) live in the digestive tracts of mammals. Female roundworms lay thousands of eggs in the host’s gut that are expelled with the feces, where they are dispersed to the surrounding environment (water, soil, ground vegetation). If they are swallowed by a host of the correct species, the eggs hatch in the host’s intestines, and the larvae bore their way into the blood vessels and come to rest in the lungs. From there they ascend to the mouth, usually by causing the host to cough, and are swallowed again to reach the stomach, where they mature and enter the intestines.

The most important debilitating external parasites of birds and mammals are spread by direct contact. They include lice, ticks, fleas, botfly larvae, and mites that cause mange. Many of these parasites lay their eggs directly on the host; but fleas just lay their eggs and their larvae hatch in the host’s nests and bedding, and from there they leap onto nearby hosts.

Some parasitic plants also spread by direct transmission; notably those classified as holoparasites, such as members of the broomrape family (Orobanchaceae). Two examples are squawroot (Conopholis americana), which parasitizes the roots of oaks (see Figure 15.2), and beechdrops (Epifagus virginiana), which parasitizes mostly the roots of beech trees. Seeds of these plants are dispersed locally; upon germination, their roots extend through the soil and attach to the roots of the host plant.

Some fungal parasites of plants spread through root grafts. For example, Fomes annosus, an important fungal infection of white pine (Pinus strobus), spreads rapidly through pure stands of the tree when roots of one tree grow onto (and become attached to) the roots of a neighbor.

15.4 Transmission between Hosts Can Involve an Intermediate Vector

Some parasites are transmitted between hosts by an intermediate organism, or vector. For example, the black-legged tick (Ixodes scapularis) functions as an arthropod vector in the transmission of Lyme disease, which is the major arthropod-borne disease in the United States. Named for its first noted occurrence at Lyme, Connecticut, in 1975, the disease is caused by a bacterial spirochete, Borrelia burgdorferi. It lives in the bloodstream of vertebrates, from birds and mice to deer and humans. The spirochete depends on the tick for transmission from one host to another (see this chapter’s Ecological Issues & Applications).

Malaria parasites infect a wide variety of vertebrate species, including humans. The four species of protists parasites (Plasmodium) that cause malaria in humans are transmitted to the bloodstream by the bite of an infected female mosquito of the genus Anopheles (Figure 15.3; see this chapter, Ecological Issues & Applications). Mosquitoes are known to transmit more than 50 percent of the approximately 102 arboviruses (a contraction of “arthropod-borne viruses”) that can produce disease in humans, including dengue and yellow fever.

Insect vectors are also involved in the transmission of parasites among plants. European and native elm bark beetles (Scolytus multistriatus and Hylurgopinus rufipes) carry spores of the fungi Ophiostoma ulmi that spreads the devastating Dutch elm disease from tree to tree. Mistletoes (Phoradendron spp.) belong to a group of plant parasites known as hemiparasites (see Figure 15.1) that, although photosynthetic, draw water and nutrients from their host plant. Transmission of mistletoes between host plants is linked to seed dispersal. Birds feed on the mistletoe fruits. The seeds pass through the digestive system unharmed and are deposited on trees where the birds perch and defecate. The sticky seeds attach to limbs and send out rootlets that embrace the limb and enter the sapwood.

15.5 Transmission Can Involve Multiple Hosts and Stages

Previously, we introduced the concept of life cycle—the phases associated with the development of an organism, typically divided into juvenile (or prereproductive), reproductive, and postreproductive phases (Chapter 10). Some species of parasites cannot complete their entire life cycle in a single host species. The host species in which the parasite becomes an adult and reaches maturity is referred to as the definitive host. All others are intermediate hosts, which harbor some developmental phase. Parasites may require one, two, or even three intermediate hosts. Each stage can develop only if the parasite can be transmitted to the appropriate intermediate host. Thus, the dynamics of a parasite population are closely tied to the population dynamics, movement patterns, and interactions of the various host species.

Many parasites, both plant and animal, use this form of indirect transmission and spend different stages of the life cycle with different host species. Figure 15.4 shows the life cycle of the meningeal worm (Parelaphostrongylus tenuis), which is a parasite of the white-tailed deer in eastern North America. Snails or slugs that live in the grass serve as the intermediate host species for the larval stage of the worm. The deer picks up the infected snail while grazing. In the deer’s stomach, the larvae leave the snail, puncture the deer’s stomach wall, enter the abdominal membranes, and travel via the spinal cord to reach spaces surrounding the brain. Here, the worms mate and produce eggs. Eggs and larvae pass through the bloodstream to the lungs, where the larvae break into air sacs and are coughed up, swallowed, and passed out with the feces. The snails acquire the larvae as they come into contact with the deer feces on the ground. Once within the snail, the larvae continue to develop to the infective stage.

15.6 Hosts Respond to Parasitic Invasions

Just as the coevolution of predators and prey has resulted in the adaptation of defense mechanisms by prey species, host species likewise exhibit a range of adaptations that minimize the impact of parasites. Some responses are mechanisms that reduce parasitic invasion. Other defense mechanisms aim to combat parasitic infection once it has occurred.

Some defensive mechanisms are behavioral, aimed at avoiding infection. Birds and mammals rid themselves of ectoparasites by grooming. Among birds, the major form of grooming is preening, which involves manipulating plumage with the bill and scratching with the foot. Both activities remove adults and nymphs of lice from the plumage. Deer seek dense, shaded places where they can avoid deerflies, which are common to open areas.

If infection should occur, the first line of defense involves the inflammatory response. The death or destruction (injury) of host cells stimulates the secretion of histamines (chemical alarm signals), which induce increased blood flow to the site and cause inflammation. This reaction brings in white blood cells and associated cells that directly attack the infection. Scabs can form on the skin, reducing points of further entry. Internal reactions can produce hardened cysts in muscle or skin that enclose and isolate the parasite. An example is the cysts that encase the roundworm Trichinella spiralis (Nematoda) in the muscles of pigs and bears and that cause trichinosis when ingested by humans in undercooked pork.

Plants respond to bacterial and fungal invasion by forming cysts in the roots and scabs in the fruits and roots, cutting off fungal contact with healthy tissue. Plants react to attacks on leaf, stem, fruit, and seed by gall wasps, bees, and flies by forming abnormal growth structures unique to the particular gall insect (Figure 15.5). Gall formation exposes the larvae of some gall parasites to predation. For example, John Confer and Peter Paicos of Ithaca College (New York) reported that the conspicuous, swollen knobs of the goldenrod ball gall (Figure 15.5d) attract the downy woodpecker (Picoides pubescens), which excavates and eats the larva within the gall.

The second line of defense is the immune response (or immune system). When a foreign object such as a virus or bacteria—termed an antigen (a contraction of “antibody-generating”)—enters the bloodstream, it elicits an immune response. White cells called lymphocytes (produced by lymph glands) produce antibodies. The antibodies target the antigens present on the parasite’s surface or released into the host and help to counter their effects. These antibodies are energetically expensive to produce. They also are potentially damaging to the host’s own tissues. Fortunately, the immune response does not have to kill the parasite to be effective. It only has to reduce the feeding, movements, and reproduction of the parasite to a tolerable level. The immune system is extremely specific, and it has a remarkable “memory.” It can “remember” antigens it has encountered in the past and react more quickly and vigorously to them in subsequent exposures.

The immune response, however, can be breached. Some parasites vary their antigens more or less continuously. By doing so, they are able to keep one jump ahead of the host’s response. The result is a chronic infection of the parasite in the host. Antibodies specific to an infection normally are composed of proteins. If the animal suffers from poor nutrition and its protein deficiency is severe, normal production of antibodies is inhibited. Depletion of energy reserves breaks down the immune system and allows viruses or other parasites to become pathogenic. The ultimate breakdown in the immune system occurs in humans infected with the human immunodeficiency virus (HIV)—the causal agent of AIDS—which is transmitted sexually, through the use of shared needles, or by infected donor blood. The virus attacks the immune system itself, exposing the host to a range of infections that prove fatal.

15.7 Parasites Can Affect Host Survival and Reproduction

Although host organisms exhibit a wide variety of defense mechanisms to prevent, reduce, or combat parasitic infection, all share the common feature of requiring resources that the host might otherwise have used for some other function. Given that organisms have a limited amount of energy, it is not surprising that parasitic infections function to reduce both growth and reproduction. Joseph Schall of the University of Vermont examined the impact of malaria on the western fence lizard (Sceloporus occidentalis) inhabiting California. Clutch size (number of eggs produced) is approximately 15 percent smaller in females infected with malaria compared with noninfected individuals (Figure 15.6). Reproduction is reduced because infected females are less able to store fat during the summer, so they have less energy for egg production the following spring. Infected males likewise exhibit numerous reproductive pathologies. Infected males display fewer courtship and territorial behaviors, have altered sexually dimorphic coloration, and have smaller testes.

Parasitic infection can reduce the reproductive success of males by impacting their ability to attract mates. Females of many species choose mates based on the secondary sex characteristics, such as bright and ornate plumage of male birds (see discussion of intrasexual selection in Chapter 10). Full expression of these characteristics can be limited by parasite infection, thus reducing the male’s ability to successfully attract a mate. For example, the bright red color of the male zebra finch’s beak depends on its level of carotenoid pigments, which are the naturally occurring chemicals that are responsible for the red, yellow, and orange coloration patterns in animals as well as in foods such as carrots. Birds cannot synthesize carotenoids and must obtain them through the diet. Besides being colorful pigments, carotenoids stimulate the production of antibodies and absorb some of the damaging free radicals that arise during the immune response. In a series of laboratory experiments, Jonathan Blount and colleagues from the University of Glasgow (Scotland) found that only those males with the fewest parasites and diseases can devote sufficient carotenoids to producing bright red beaks and therefore succeed in attracting mates and reproducing.

Although most parasites do not kill their host organisms, increased mortality can result from a variety of indirect consequences of infection. One interesting example is when the infection alters the behavior of the host, increasing its susceptibility to predation. Rabbits infected with the bacterial disease tularemia (Francisella tularensis), transmitted by the rabbit tick (Haemaphysalis leporis-palustris), are sluggish and thus more vulnerable to predation. In another example, ecologists Kevin Lafferty and Kimo Morris of the University of California–Santa Barbara observed that killifish (Fundulus parvipinnis; Figure 15.7a) parasitized by trematodes (flukes) display abnormal behavior such as surfacing and jerking. In a comparison of parasitized and unparasitized populations, the scientists found that the frequency of conspicuous behaviors displayed by individual fish is related to the intensity of parasitism (Figure 15.7b). The abnormal behavior of the infected killifish attracts fish-eating birds. Lafferty and Morris found that heavily parasitized fish were preyed on more frequently than unparasitized individuals (Figure 15.7c). Interestingly, the fish-eating birds represent the trematodes’ definitive host, so that by altering its intermediate host’s (killifish) behavior, making it more susceptible to predation, the trematode ensures the completion of its life cycle.

15.8 Parasites May Regulate Host Populations

For parasite and host to coexist under a relationship that is hardly benign, the host needs to resist invasion by eliminating the parasites or at least minimizing their effects. In most circumstances, natural selection has resulted in a level of immune response in which the allocation of metabolic resources by the host species minimizes the cost of parasitism yet does not unduly impair its own growth and reproduction. Conversely, the parasite gains no advantage if it kills its host. A dead host means dead parasites. The conventional wisdom about host–parasite evolution is that virulence is selected against, so that parasites become less harmful to their hosts and thus persist. Does natural selection work this way in parasite–host systems?

Natural selection does not necessarily favor peaceful coexistence of hosts and parasites. To maximize fitness, a parasite should balance the trade-off between virulence and other components of fitness such as transmissibility. Natural selection may yield deadly (high virulence) or benign (low virulence) parasites depending on the requirements for parasite reproduction and transmission. For example, the term vertical transmission is used to describe parasites transmitted directly from the mother to the offspring during the perinatal period (the period immediately before or after birth). Typically, parasites that depend on this mode of transmission cannot be as virulent as those transmitted through other forms of direct contact between adult individuals because the recipient (host) must survive until reproductive maturity to pass on the parasite. The host’s condition is important to a parasite only as it relates to the parasite’s reproduction and transmission. If the host species did not evolve, the parasite might well be able to achieve some optimal balance of host exploitation. But just as with the coevolution of predator and prey, host species do evolve (see discussion of the Red Queen hypothesis in Section 14.9). The result is an “arms race” between parasite and host.

Parasites can have the effect of decreasing reproduction and increasing the probability of host mortality, but few studies have quantified the effect of a parasite on the dynamics of a particular plant or animal population under natural conditions. Parasitism can have a debilitating effect on host populations, a fact that is most evident when parasites invade a population that has not evolved to possess defenses. In such cases, the spread of disease may be virtually density independent, reducing populations, exterminating them locally, or restricting distribution of the host species. The chestnut blight (Cryphonectria parasitica), introduced to North America from Europe, nearly exterminated the American chestnut (Castanea dentata) and removed it as a major component of the forests of eastern North America. Dutch elm disease, caused by a fungus (Ophiostoma ulmi) spread by beetles, has nearly removed the American elm (Ulmus americana) from North America and the English elm (Ulmus glabra) from Great Britain. Anthracnose (Discula destructiva), a fungal disease, is decimating flowering dogwood (Cornus florida), an important understory tree in the forests of eastern North America. Rinderpest, a viral disease of domestic cattle, was introduced to East Africa in the late 19th century and subsequently decimated herds of African buffalo (Syncerus caffer) and wildebeest (Connochaetes taurinus). Avian malaria carried by introduced mosquitoes has eliminated most native Hawaiian birds below 1000 m (the mosquito cannot persist above this altitude).

On the other hand, parasites may function as density-dependent regulators on host populations. Density-dependent regulation of host populations typically occurs with directly transmitted endemic (native) parasites that are maintained in the population by a small reservoir of infected carrier individuals. Outbreaks of these diseases appear to occur when the host population density is high; they tend to reduce host populations sharply, resulting in population cycles of host and parasite similar to those observed for predator and prey (see Section 14.2). Examples are distemper in raccoons and rabies in foxes, both of which are diseases that significantly control their host populations.

In other cases, the parasite may function as a selective agent of mortality, infecting only a subset of the population. Distribution of macroparasites, especially those with indirect transmission, is highly clumped. Some individuals in the host population carry a higher load of parasites than others do (Figure 15.8). These individuals are most likely to succumb to parasite-induced mortality, suffer reduced reproductive rates, or both. Such deaths often are caused not directly by the macroparasites, but indirectly by secondary infection. In a study of reproduction, survival, and mortality of bighorn sheep (Ovis canadensis) in south-central Colorado, Thomas Woodard and colleagues at Colorado State University found that individuals may be infected with up to seven different species of lungworms (Nematoda). The highest rates of infection occur in the spring when lambs are born. Heavy lungworm infections in the lambs bring about a secondary infection—pneumonia—that kills them. The researchers found that such infections can sharply reduce mountain sheep populations by reducing reproductive success.

15.9 Parasitism Can Evolve into a Mutually Beneficial Relationship

Parasites and their hosts live together in a symbiotic relationships in which the parasite derives its benefit (habitat and food resources) at the expense of the host organism. Host species have evolved a variety of defenses to minimize the negative impact of the parasite’s presence. In a situation in which adaptations have countered negative impacts, the relationship may be termed commensalism, which is a relationship between two species in which one species benefits without significantly affecting the other (Section 12.1, Table 12.1). At some stage in host–parasite coevolution, the relationship may become beneficial to both species. For example, a host tolerant of parasitic infection may begin to exploit the relationship. At that point, the relationship is termed mutualism. There are many examples of “parasitic relationships” in which there is an apparent benefit to the host organism. For example, rats infected with the intermediate stages of the tapeworm Spirometra grow larger than uninfected rats do because the tapeworm larva produces an analogue of vertebrate growth hormone. In this example, is the increased growth beneficial or harmful to the host? Similarly, many mollusks, when infected with the intermediate stages of digenetic flukes (Digenea), develop thicker, heavier shells that could be deemed an advantage. Some of the clearest examples of evolution from parasites to mutualists involve parasites that are transmitted vertically from mother to offspring (see discussion in Section 15.8). Theory predicts that vertically transmitted parasites are selected to increase host survival and reproduction because maximization of host reproductive success benefits both the parasite and host. This prediction has been supported by studies examining the effects of Wolbachia, a common group of bacteria that infect the reproductive tissues of arthropods. Investigations of the effects of Wolbachia on host fitness in the wasp Nasonia vitripennis have shown that infection increases host fitness and that infected females produce more offspring than do uninfected females. Similar increases in fitness have been reported for natural populations of fruit flies (Drosophila).

Mutualism is a relationship between members of two species in which the survival, growth, or reproduction is enhanced for individuals of both species. Evidence, however, suggests that often this interaction is more of a reciprocal exploitation than a cooperative effort between individuals. Many classic examples of mutualistic associations appear to have evolved from species interactions that previously reflected host–parasite or predator–prey interactions. In many cases of apparent mutualism, the benefits of the interaction for one or both of the participating species may be dependent on the environment (see Section 12.4). For example, many tree species have the fungal mycorrhizae associated with their roots (see Section 15.11). The fungi obtain organic nutrients from the plant via the phloem, and in nutrient-poor soil the trees seem to benefit by increased nutrient uptake, particularly phosphate by the fungus. In nutrient-rich soils, however, the fungi appear to be a net cost rather than benefit; this seemingly mutualistic association appears much more like a parasitic invasion by the fungus. Depending on external conditions, the association switches between mutualism and parasitism (see further discussion of example in Section 12.4, Figure 12.9).

15.10 Mutualisms Involve Diverse Species Interactions

Mutualistic relationships involve many diverse interactions that extend beyond simply acquiring essential resources. Thus, it is important to consider the different attributes of mutualistic relationships and how they affect the dynamics of the populations involved. Mutualisms can be characterized by a number of variables: the benefits received, the degree of dependency, the degree of specificity, and the duration of the intimacy.

Mutualism is defined as an interaction between members of two species that serves to benefit both parties involved, and the benefits received can include a wide variety of processes. Benefits may include provision of essential resources such as nutrients or shelter (habitat) and may involve protection from predators, parasites, and herbivores, or they may reduce competition with a third species. Finally, the benefits may involve reproduction, such as dispersal of gametes or zygotes.

Mutualisms also vary in how much the species involved in the mutualistic interaction depend on each other. Obligate mutualists cannot survive or reproduce without the mutualistic interaction, whereas facultative mutualists can. In addition, the degree of specificity of mutualism varies from one interaction to another, ranging from one-to-one, species-specific associations (termed specialists) to association with a wide diversity of mutualistic partners (generalists). The duration of intimacy in the association also varies among mutualistic interactions. Some mutualists are symbiotic, whereas others are free living (nonsymbiotic). In symbiotic mutualism, individuals coexist and their relationship is more often obligatory; that is, at least one member of the pair becomes totally dependent on the other. Some forms of mutualism are so permanent and obligatory that the distinction between the two interacting organisms becomes blurred. Reef-forming corals of the tropical waters provide an example. These corals secrete an external skeleton composed of calcium carbonate. The individual coral animals, called polyps, occupy little cups, or corallites, in the larger skeleton that forms the reef (Figure 15.9). These corals have single-celled, symbiotic algae in their tissues called zooxanthellae. Although the coral polyps are carnivores, feeding on zooplankton suspended in the surrounding water, they acquire only about 10 percent of their daily energy requirement from zooplankton. They obtain the remaining 90 percent of their energy from carbon produced by the symbiotic algae through photosynthesis. Without the algae, these corals would not be able to survive and flourish in their nutrient-poor environment (see this chapter, Field Studies: John J. Stachowicz). In turn, the coral provides the algae with shelter and mineral nutrients, particularly nitrogen in the form of nitrogenous wastes.

Lichens are involved in a symbiotic association in which the fusion of mutualists has made it even more difficult to distinguish the nature of the individual. Lichens (Figure 15.10) consist of a fungus and an alga (or in some cases cyanobacterium) combined within a spongy body called a thallus. The alga supplies food to both organisms, and the fungus protects the alga from harmful light intensities, produces a substance that accelerates photosynthesis in the alga, and absorbs and retains water and nutrients for both organisms. There are about 25,000 known species of lichens, each composed of a unique combination of fungus and alga.

In nonsymbiotic mutualism, the two organisms do not physically coexist, yet they depend on each other for some essential function. Although nonsymbiotic mutualisms may be obligatory, most are not. Rather, they are facultative, representing a form of mutual facilitation. Pollination in flowering plants and seed dispersal are examples. These interactions are generally not confined to two species, but rather involve a variety of plants, pollinators, and seed dispersers.

In the following sections, we explore the diversity of mutualistic interactions. The discussion centers on the benefits derived by mutualists: acquisition of energy and nutrients, protection and defense, and reproduction and dispersal.

15.11 Mutualisms Are Involved in the Transfer of Nutrients

The digestive system of herbivores is inhabited by a diverse community of mutualistic organisms that play a crucial role in the digestion of plant materials. The chambers of a ruminant’s stomach contain large populations of bacteria and protists that carry out the process of fermentation (see Section 7.2). Inhabitants of the rumen are primarily anaerobic, adapted to this peculiar environment. Ruminants are perhaps the best studied but are not the only example of the role of mutualism in animal nutrition. The stomachs of virtually all herbivorous mammals and some species of birds and lizards rely on the presence of a complex microbial community to digest cellulose in plant tissues.

Field Studies John J. Stachowicz Section of Evolution and Ecology, Center for Population Biology, University of California–Davis

Facilitative, or positive, interactions are encounters between organisms that benefit at least one of the participants and cause harm to neither. Such interactions are considered mutualisms, in which both species derive benefit from the interaction. Ecologists have long recognized the existence of mutualistic interactions, but there is still far less research on positive interactions than on competition and predation. Now, however, ecologists are beginning to appreciate the ubiquitous nature of positive interactions and their importance in affecting populations and in the structuring of communities. The research of marine ecologist John Stachowicz has been at the center of this growing appreciation of the importance of facilitation.

Stachowicz works in the shallow-water coastal ecosystems of the southeastern United States. The large colonial corals and calcified algae that occupy the warm subtropical waters of this region provide a habitat for a diverse array of invertebrate and vertebrate species. In well-lit habitats, corals and calcified algae (referred to as coralline algae) grow slowly relative to the fleshy species of seaweed. The persistence of corals appears to be linked to the high abundance of herbivores that suppress the growth of the seaweeds, which grow on and over the coral and coralline algae and eventually cause their death. In contrast, the relative cover of corals is generally low in habitats such as reef flats and seagrass beds, where herbivory is less intense.

Stachowicz hypothesized that mutualism plays an influential role in the distribution of coral species. Although corals are typically associated with the colorful and diverse coral reef ecosystems of the tropical and subtropical coastal waters, many temperate and subarctic habitats support corals, and some tropical species occur where temperatures drop to 10°C or below for certain months of the year. One such species is the coral Oculina arbuscula.

O. arbuscula occurs as far north as the coastal waters of North Carolina, forming dense aggregations in poorly lit habitats where seaweeds are rare or absent. In certain areas of the coastal waters, however, O. arbuscula does co-occur with seaweeds on natural and artificial reefs. It is the only coral in this region with a structurally complex branching morphology that provides shelter for a species-rich epifauna. More than 300 species of invertebrates are known to live among the branches of Oculina colonies.

How can O. arbuscula persist in the well-lit, shallow-water systems? In well-lit habitats, corals grow slowly relative to seaweeds, and the persistence of coral reefs appears to be tightly linked to high abundance of herbivores that prevent seaweed from growing on and over the corals. When herbivorous fish or sea urchins are naturally or experimentally removed from tropical reefs, seaweed biomass increases dramatically and corals are smothered. In contrast, on the temperate reefs of North Carolina, herbivorous fish are less abundant than in the tropics, and the standing biomass of seaweed is typically much higher. On these reefs, herbivorous fish and urchins also alter the species composition of the seaweed community by selectively removing their preferred species, but they do not diminish the total seaweed biomass. The dependence of corals on positive interactions with herbivores may thus explain why corals are generally uncommon in temperate latitudes.

Stachowicz suspected the role of a key herbivore in these temperate reef ecosystems: the herbivorous crab Mithrax forceps. He hypothesized that the success of O. arbuscula on temperate reefs derives from its ability to harbor symbiotic, herbivorous crabs that mediate competition with encroaching seaweeds. To evaluate the hypothesis, he conducted field experiments monitoring the fouling (overgrowth by seaweeds) and growth of corals in the presence and absence of crabs. Experiments were located at Radio Island Jetty near Beaufort, North Carolina.

In these experiments, metal stakes were driven into substrate, and one coral (which had previously been weighed) was fastened to each stake. A single crab was then placed on a subset of the corals, and the remainder was left vacant. At the end of the experiment, all seaweed (and other epiphytic growth) was removed from the corals, dried, and weighed. After removal of the seaweeds, the corals were reweighed to measure growth.

To determine if association with O. arbuscula reduced predation on M. forceps, Stachowicz tethered crabs both with and without access to coral. He checked each tether after 1 and 24 hours to see if crabs were still present.

Mutualistic interactions are also involved in the uptake of nutrients by plants. Nitrogen is an essential constituent of protein, a building block of all living material. Although nitrogen is the most abundant constituent of the atmosphere—approximately 79 percent in its gaseous state—it is unavailable to most life. It must first be converted into a chemically usable form. One group of organisms that can use gaseous nitrogen (N2) is the nitrogen-fixing bacteria of the genus Rhizobium. These bacteria (called rhizobia) are widely distributed in the soil, where they can grow and multiply. But in this free-living state, they do not fix nitrogen. Legumes—a group of plant species that include clover, beans, and peas—attract the bacteria through the release of exudates and enzymes from the roots. Rhizobia enter the root hairs, where they multiply and increase in size. This invasion and growth results in swollen, infected root hair cells, which form root nodules (Figure 15.11). Once infected, rhizobia within the root cells reduce gaseous nitrogen to ammonia (a process referred to as nitrogen fixation). The bacteria receive carbon and other resources from the host plant; in return, the bacteria contribute fixed nitrogen to the plant, allowing it to function and grow independently of the availability of mineral (inorganic) nitrogen in the soil (see Chapter 6, Section 6.11).

Endomycorrhizae have an extremely broad range of hosts; they have formed associations with more than 70 percent of all plant species. Mycelia—masses of interwoven fungal filaments in the soil—infect the tree roots. They penetrate host cells to form a finely bunched network called an arbuscule (Figure 15.12a). The mycelia act as extended roots for the plant but do not change the shape or structure of the roots. They draw in nitrogen and phosphorus at distances beyond those reached by the roots and root hairs. Another form, ectomycorrhizae, produces shortened, thickened roots that look like coral (Figure 15.12b). The threads of the fungi penetrate between the root cells. Outside the root, they develop into a network that functions as extended roots. Ectomycorrhizae have a more restricted range of hosts than do endomycorrhizae. They are associated with about 10 percent of plant families, and most of these species are woody.

Together, either ecto- or endomycorrhizae are found associated with the root systems of the vast majority of terrestrial plant species and are especially important in nutrient-poor soils. They aid in the decomposition of dead organic matter and the uptake of water and nutrients, particularly nitrogen and phosphorus, from the soil into the root tissue (see Sections 21.7 and 6.11).