(pl. Fungal Lifestyles)
Terms discussed: controlled parasitism, disease (pl. diseases), humus, mutual parasitism
This entry is a discussion of the five main ways that fungi obtain their nutrition. Each of the subheadings (carnivore, saprobe, parasite, mycorrhiza, and lichen) have their own separate entries, in which they are discussed in greater technical detail and in which their satellite terminologies are (hopefully) elucidated. Under this entry, I'm going to discuss some of the broader ("ideological", perhaps) issues surrounding these terms with a more general scope than the more constrained individual entries permit.
Topics:
Carnivorous
Saprobe
Parasite
Fungal “Disease” and Forest “Management”
Mycorrhizae
Lichens
See Also:
Lichen
symbiosis
Identification
mycorrhiza
Carnivorous
Yes, Virginia, there are carnivorous fungi. Using traps of various kinds, they capture tiny creatures that respond to baits or just come near them, much like carnivorous plants. Some soil Deuteromycetes derive all their nutrition from animals, but many wood-rotting fungi also trap animals to boost their intake of nitrogen.
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Saprobe
A saprobe is an organism that derives its nutrition from the dead remains of other organisms. These are the work-horses of elementary school textbooks' attempts to convince small children that all mushrooms aren't just worthless scum. Where these children would pick up this attitude were it not for these textbooks, I don't know, but there you have it. Lee Oras Overholts has a fairly typical passage in the introduction to his 1953 book when, after going on and on about the tremendous economic damage wrought by wood-rotting fungi to "structural timbers of all sorts, in telegraph and telephone poles, railroad ties, fencing materials, and bridge timbers, in lumber yards, pulp miles, and a variety of other places," he consoles us with "Yet we should not turn from this picture without viewing it from a slightly different angle. The decay of wood in the forest not only frees new elements into the soil to be taken up again by other forms of plant life, but, were it not for the decay propensities of these fungi, every dead branch that falls to the ground, every wind-thrown trunk, and every stump left by the lumberman would lie indefinitely on the forest floor and the forests would soon be so choked with dead and down materials that they would be absolutely impenetrable." There are several fallacies in this line of discourse that I would like to address, if only because some of them are still in circulation among people who don't know anything beyond what they learned in elementary school.
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First of all, there's this business of wood-rotting releasing nutrients into the soil, there to be taken up by plants. This is subtly but importantly incorrect. The main contribution of wood decay to soil is humus, which is simply pulverized lignin. It has no nutritional benefits whatsoever to growing plants; it is simply a softer and lighter medium than the pulverized rocks which are the other main constituent of soil. Humus is easier for the roots of a young plant to penetrate, and likewise easier for the mycelium of the mycorrhizal fungi that the young plants need to survive. Alexopoulos, Mims & M. Blackwell (1996) , pp.570-571: "Young conifer trees often can be found growing in a row, the result of selective seed germination and survival of seedlings in the brown rot residue along the length of a large fallen conifer. The reason for this is that brown rot residues increase aeration and water-holding capacity of soil, promote ectomycorrhizal formation and nitrogen fixation by nonsymbiotic organisms, ameliorate temperature, lower soil pH, and increase cation exchange of nutrients. This information seriously calls into question policies that allow excessive removal of dead conifers from forest lands." So wood-rotting fungi do improve the soil, but by textural means, not by enriching it with nutrients. After all, most wood-rotting fungi are carnivorous – that is, they are so hungry for nitrogen that they trap the tiny wood-inhabiting animals for food. Fungi so hungry for nutrients are not going to allow many to remain behind in the humus after they are done feeding.
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Secondly, there’s this business of clearing the forest, something like “Fungi are okay because they clear brush from the forest, thus making it possible for us to hold picnics and shoot deer.” This line of reasoning (and, even in its more enlightened form, the one in the previous paragraph) treats fungi as organisms that don’t really have any right to exist, unless they help “better”, more “worthwhile” organisms, like trees and picnickers. It is an attitude that measures a tree’s “health” by how many planks it would make if it were chopped up in a sawmill. This is wrong.
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Fungi often enter a tree with bark beetles, which carry their favorite flavor of fungi with them in specialized pouches. The beetle larvae drill holes through the tree, cultivating the fungus in these tunnels as they go, and eating it. The fungus softens the wood, which lets woodpeckers (and other animals) drill into it, looking for the beetles and their larvae. The holes they create let in more insects, and the cycle continues. Once the wood is softened more generally, it gets colonized by nematodes and other microscopic animals, which in turn feed larger fungi (conks and oyster mushrooms, for example). Other beetles feed on the fruiting bodies of these fungi, and spread the fungal spores during their travels around the forest. The more porous a tree becomes, through fungal activity, the more organisms use it as a home. By the time a tree has died, whether standing or fallen, it (and its stump) are tremendously active and vital ecosystems with great (though often microscopic) biodiversity.
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This ecosystem (and its biodiversity) is still largely unknown. Many, if not most, of the organisms involved are still undescribed (because funding and public interest is mostly directed towards larger organisms with cute fur or pretty flowers). “Cleaning up” a forest by removing fallen timber removes the tree, all the tree-dwelling organisms, and the nutrients that they represent from the forest ecosystem. This is not a short-term loss, either: current research suggests that it takes 200-500 years for a large tree to decay completely. Logging a forest represents a tremendous loss to the forest of this stage of the forest ecocycle, and the elimination of rotting trees (whether standing or fallen) represents a loss of biodiversity and nutrients.
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Given the time-frame of the ecosystem’s utilization of these resources, the effects of this loss may take several hundred years to become fully apparent, and it cannot be alleviated by sprinkling pine bark mulch around a new crop of seedlings. The Chicago Park District, for example, has a nifty stump-shattering machine with which they remove “unsightly” stumps from their forest preserves. The mushroom at the right was photographed on a stump in a Chicago nature preserve. When the photographer went back next year to attempt another picture, the stump was gone, the victim the stump-shatterer (If only they were so conscientious about removing Garlic Mustard!). And these are just the victims that we have noticed. Those southern pine forests mentioned above may have had hundreds of species of endemic micro-flora and fauna (and fungi of all sizes) that were just as dependent on those decaying treees as the Ivory-billed Woodpecker. And they are just as vanished now, but without any human ever having noticed their existence in the first place.
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Parasite
We usually define a parasite as something like “an organism that lives on or in another organism, called the host, on which it feeds.” Applying the term is tricky, as it comes loaded with emotional associations which make us want things not to be parasites if we like them. For instance, Overholts & J. L. Lowe (1953) p. 21-23 goes through quite a discussion of whether polypores can really be considered parasitical if they only attack the (dead) heartwood of a living tree without attacking the living cambium. He also points out a distinction between parasite and pathogen, saying that a heart-rot produces severe harm to a tree (and thus is pathogenic) even if we don’t consider the fungus a parasite. We shall return to this distinction. Overholts says that we can’t call an organism a parasite just because it harms another one, as this is going too far in the direction of generality.
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Another thing that makes it tricky to apply the term parasite is that we have developed the term with parasitic animals at the core of its meaning. This gives parasitism connotations that predispose us to consider fungi parasites: I am thinking particularly of immobility and suckers. Let us consider drinking first: we want our parasites to be suckers, not chewers. Consider one plant covered with aphids and another plant covered with caterpillars. Both types of insect are just as dependent on their host plant; both live in permanent association with the host plant, on its surface; and both can feed to the point where they kill the host. But we are much more likely to call the aphids parasites than the caterpillars (especially if they’re Monarch Butterfly caterpillars. Hoo boy!). This is because the aphids feed in a “parasitical” fashion, by sucking on the plant. Similarly, fruit flies (in warmer locations than Chicago) and locusts both travel in swarms, devastate local vegetation, and move on. But because of their feeding style, we think of the fruit flies as much more of a parasite than the locusts.
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There is a similar requirement of immobility for a parasite. We want a parasite to spend a good portion of its life attached (or inside) the host, doing little but feeding, and with its other organs and its ability for movement atrophied or entirely lost. Thus, we consider scale insects (aphids that remain permanently fixed in place and develop a hard covering (the “scale”) to protect themselves) as more parasitic than normal aphids; and we consider aphids more parasitic than male mosquitos, which also feed by sucking on plant juices but on a more free-roving basis.
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But perhaps the most important criterion for declaring something a parasite is that it has to be worth less for human endeavors than the organism on which it feeds. Thus, the cabbage moth that invades our garden is a parasite, and a fungus that we could sprinkle on them to get rid of them is bioremediation. Cultivated silkworms, on the other hand, are not considered parasites; but the fungi that attack them are. Similarly, in this country, many foresters consider Ganoderma species to be to be parasites of their precious standing board-feet; but in East Asia, where these fungi are prized as Ling Chih, their nutritional life-style is not an issue.
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All of these criteria pre-dispose us (Westerners) to consider fungi parasites: fungi are permanently immobile, they are rarely prized in their own right (especially in their mycelial form), and they always feed by dissolving some of the stuff surrounding them and absorbing it. In fact, the criterion of atrophy of non-feeding body parts also meshes with the body plan of fungi, as a simple mycelium is “pre-atrophied”, with almost no structure whatsoever. Parasitical fungi, however, develop some of the most differentiated structures of any fungus in order to penetrate into the host and begin feeding. This gives the fungus a typical “parasite” body plan of highly specialized feeding apparatus and undifferentiated body. But this body has been achieved, not by atrophy of other body parts (like the scale insect, which loses its legs and sensory organs once it settles down under its scale) but by most of the "body" not being differentiated in the first place.
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In other words, whenever a fungus feeds on a living plant or animal, it is bound to be considered a parasite, simply because it can’t move and can’t bite big chunks out of its host, the way “honest” herbivores and carnivores do. I thus consider the term to be biologically meaningless in connection with fungi, and frankly, with any organism whatsoever. Organisms, in general, require two things of their environment: food and shelter. It really makes no difference to them whether that food or the shelter is a living organism or not. To call the carnivorous tick’s life-style somehow qualitatively different (or morally different) from the carnivorous hawk’s, simply because the tick devours its living prey a little at a time, and the hawk devours its (usually still living) prey all at once is to project human values (“sneakiness”) onto organisms that are just eating and making homes for themselves, like any other organism. One might try to rescue the term parasite by defining it in a limited sense, that of an organism that exhausts its host’s tissues (or body fluids) in a gradual fashion, rather than all at once. In this sense, if we consider a monocultural field of grass to be one big organism, a cow feeding on that grass is a parasite on that organism (just like the caterpillar feeding on a tree). But again, a fungus has no other option for feeding on a living thing, as it is physiological incapable of taking big bites. I will use the term parasitism for this kind of feeding in connection with fungi, and I will call fungi which draw nutrition from living organisms (and organisms which gradually draw nutrition from living fungi) parasites. But only because we have no other term for this sort of nutritional relationship.
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Similarly, I consider the separation of pathogenicity from parasitism to be specious. We don’t discuss issues of pathogenicity (that is, whether one organism harms another one) outside of the context of parasitism, and specifically parasitism of an organism that we want to keep alive: in the US, corn smut (the fungus Ustilago maydis) is a pathogen, since our agricultural system regards it as inedible and the ears infected with it thus become economically worthless; in Mexico, where the fungus is regarded as a delicacy and is worth much more than the corn, the question of pathogenicity is not even an issue. The term pathogen, then, is not a biological term but an economic one, dependent on the relative value for human use of the organisms involved. So is the term parasite.
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Fungal “Disease” and Forest “Management”
Labeling tree-inhabiting fungi parasites is part of the attitude that labels fungally-inhabited trees “diseased”, and is part and parcel of the attitude that regards fungi as having a right to exist only when they “help” trees through mycorrhizae, or clear the ground for picnickers. I’ve thought for quite a while about what name to give this attitude, and the only one that I can come up with is “lumber-centric”. True, a national park should not be regarded solely as a reservoir of standing board-feet, but one often sees the “health” of a national park evaluated with this as the standard of measurement, with consequences that are disastrous for overall forest ecology. A tree with a heart-rot is not diseased; it is inhabited. Habitation by a fungus is no more intrinsically a “disease” than is habitation by a squirrel. Wood has many roles to fulfill in the forest ecosystem, and it fulfills most of them in the process of decay. Trees are, for example, nesting and dwelling sites for a variety of animals. These sites are either hollowed out by fungi, or drilled into the wood by woodpeckers. Woodpeckers, in turn, cannot dig out nesting sites for themselves unless the wood is already softened by fungi. The latest research on the demise of the Ivory-billed Woodpecker indicates that it didn’t go extinct because of over-hunting; it went extinct because the southern pine forests where it nested were extensively “managed” by the US Forestry Service, which involved cutting down all the “diseased” trees. Deprived of all its nesting sites, the woodpecker was unable to reproduce.
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Calling wood-inhabiting fungi parasites, and inhabited trees diseased is especially dubious in the context of the forest ecosystem. You already know (from the Saprobe topic, above) that decaying trees in the forest are the prefered habitat of their seedlings. Thus, anything that can speed up the process of decay to the point where the seedlings can utilize the decaying tree may enhance the species’ survival. This would include “pre-decaying” the mature tree by starting the process before it actually falls over. Appreciation of this process is not enhanced by calling the fungus a parasite. For example, Fomitopsis officinalis is usually labelled a “virulent pathogen” of conifers in the Pacific Northwest (except, of course, by the Native Americans who consider it sacred). However, like most large conks, it has to grow in the tree for at least 40-50 years before it develops the biological resources to fruit. In addition, it is a perennial conk that has been found with over a dozen layers in its fruiting body. This means that it routinely inhabits the tree for over fifty years before decaying it to the point where the tree falls over. This is fifty years that the tree is actively growing and reproducing, and fifty years saved in rotting the tree on the ground for the saplings. This is not a “virulent pathogen”, except of course in terms of the almighty board-feet. In fact, it would be interesting to see a comparative study of the ecological success of the host tree in areas where Fomitopsis officinalis does and does not occur.
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The perception of tree-inhabiting fungi as “evil parasites” (okay, “virulent pathogen”s) has had profound and negative effects on “forest management” in the United States. Because they need to grow inside the tree for so long before they fruit, the large conks are especially vulnerable to forestry practices that eliminate them before they can reproduce. One of the very few fungi to certifiably go extinct is Echinodontium ballouii. Echinodontium species are even more vulnerable to forest “management” because they have to grow inside the tree for 70-80 years before they can fruit. Echinodontium ballouii was endemic to Atlantic White Cedar (Chamaecyparis thyoides), an endangered tree that occurs only in three isolated stands along the East Coast. An aggressive program of core sampling and cutting down “infected” trees quickly eliminated the fungus (like the Ivory-billed Woodpecker) from the planet. Meanwhile, populations of Atlantic White Cedar have continued to decline.
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Nor do the negative effects of the lumber-centric attitude stop with the “management” of living trees. In the Saprobe topic above, I emphasized the ecological cost of removing fallen timber from forests. Some of the motivation for this removal is undoubtedly just general tidiness (after all, a forest is supposed to look as much as possible like a suburban living room, right? That makes it more convenient to hold picnics and shoot animals), but some of the impetus has to come from the perception of fungi growing on wood as a disease.
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Mycorrhizae
A mycorrhiza is a situation where a fungal mycelium attaches itself to the roots of a plant, and the two exchange nutrients. Generally, the fungus is thought to function mostly to gather water and trace minerals from an area greater than that covered by the plant’s root system, and the plant is thought to supply mainly sugars to the fungus. In addition, the fungus is often species-specific, so most or all of the trees in a forest may be connected by an underground mycelial network. This network may lend support to stressed trees, or nurture young trees: studies have shown that sugars tagged with radioactive carbons and injected into mature trees later turn up in the young trees of that species. This is thought to be a way that the mature trees in a forest support and nurture their young until the baby trees are tall enough to get enough sunlight to feed themselves.
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As one might expect from the discussion of parasitism, the exact nature of the mycorrhizal relationship is also a matter of some controversy. Although the mycorrhizal relationship is generally taken to benefit both parties, accusations of parasitism have flown in both direction. I have hardly looked at any writings on this issue of parasitism in mycorrhizae, but I should mention that where I have seen it, the parasitism has been mostly on the side of the plants. Orchids, for example, produce a tiny, tiny seed which does not have enough stored food to nourish the embryo. In the wild, an orchid seed will not germinate at all unless it is already in contact with a fungus that it can immediately form a mycorrhiza with and draw upon for nutrition. The flower industry has perfected growth media that provide the nutrients normally supplied by the mycorrhizal fungus, and thus are able to germinate orchid seeds on this medium in axenic culture. But in nature, an orchid essentially starts out life as a parasitic organism. There are even two species of orchid (both lacking chlorophyll) known from Australia that grow, flower and fruit entirely underground, deriving their entire life’s nutrition from parasitizing a mycorrhizal fungus. One orchid is apparently pollinated by burrowing beetles, and its strongly-scented fruits are dispersed by burrowing animals, much like truffles. The other orchid is known only from a single collection early in this century, and almost nothing is known about its life-cycle. There is even an orchid known from Japan that is parasitic on Honey Mushrooms (no word yet on the exact species)
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Several chlorophyll-less plants in the US are were thought to be saprophytes, and you can still read statements to this effect in well-meaning textbooks and all over the internet. This is incorrect, however. No known plant can digest and absorb dead plant material on its own; these plants are parasitic on a fungus that they have a mycorrhizal relationship with. The best-known of these are members of the genus Monotropa: the rare red-and-yellow Pine Sap, and the more common white Indian Pipe. The closely related Allotropa virgata (“Candy Stripe”) is parasitic on the mycelium of the highly prized Matsutake mushroom (a parasite! A disease of the fungus! Let’s form a forestry management program to eradicate the plant!). But while emphasizing the parasitic nature of the mycorrhizal relationship, I should also emphasize that I am using the word in the non-judgmental sense mentioned above: that of an organism that feeds by continually drawing non-lethal levels of sustenance from another organism.
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I consider the usual definition of mutualism (a symbiosis that benefits both parties), where both parties cooperate “harmoniously” for the greater good, to be bunk. Even before we get to the notion of cooperation, which even some humans have trouble with, such a definition ascribes consciousness of self, consciousness of the other, and a notion of “mutual benefit” to the participants in the relationship; and I have trouble ascribing that level of cognition to a fungus. Or a tree. Or even animals, for that matter. In any case, I consider mycorrhizae to be an example not of “controlled parasitism”, a term used by several authors, but mutual parasitism. Thus, if there’s any anthropomorphizing to be done, it should not be of two friendly people engaged in warm, fulfilling, mutual cooperation, but of two con-men, each of them continually swindling the other, each unaware that he is also being swindled, and each convinced that he is getting the better of the deal. The mycorrhizal relationship can be formulated as one where the plant starts out drawing heavily upon the fungus’ resources, when it doesn’t have much to offer of its own; and as the plant matures and becomes self-sustaining, the fungus starts to draw more on the resources of the tree. This way, the phenomenon of mature trees “nurturing” young ones becomes one where the young tree draws heavily on the fungus (much after the fashion of orchids), which in turn draws more heavily on the bigger trees, and nutrients that started out in the big trees end up in the saplings. This is much more plausible than a model where the big trees “send” nutrients to the young ones through the fungus, which involves the big trees somehow being “aware” of the little trees (and their location) and somehow targeting them for nutrient delivery (and enforcing this delivery location on the fungus). Again, that scenario involves a level of cognition that I am unwilling to ascribe to a tree. I hold that partners in a symbiosis each “regard” the other as simply a food source or shelter no different from any other that they exploit, just as parasites regard their host. I agree with Ramsbottom (1953) when he says “... it does not help if we simply label all associations of fungi and other organisms as symbiosis and assume that everything is for mutual benefit, with give and take. Relations are often more strained than not and the constituent “partners” behave as if they regarded themselves alone.” p. 218
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The big difference is that here both partners are of substantial size. In a "classical" parasitic relationship, the host is usually much bigger than the parasite, as pointed out by de Bary, way back in his article that originally coined the term "symbiosis". The parasite really has nothing to offer the host, just because it is so much smaller that the nutritional resources it has to offer are trivial compared to the host's needs. But if both parties are of comparable size, they both have a comparable reservoir of biological resources, and hence both have something to deal.
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All of this discussion is obviously much more directed towards the huge, forest-spanning ectomycorrhizae rather than the often microscopic endomycorrhizae. But the principle is the same: individually small microsymbionts often have a large collective mass. The gut bacteria (and fungi) of termites are individually microscopic, but collectively they make up about a third of the weight of the insect. And there's a fine example of symbiosis as mutual parasitism...
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Lichens
Lichens are another group of organisms that have seen much ink spilled over the question of parasitism. A lichen is a polygenetic organism: a biont that functions as a single biological organism, but which contains cells of more than one genotype. It consists of a fungal “partner” and one or more photosynthetic partners, which can be either green algae or cyanobacteria.
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The partners in lichen symbioses are highly co-evolved. While most mycobionts and photobionts can survive on their own (at least when coddled along in an axenic culture), when hook up with one another their growth pattern and rate changes dramatically; they form a thallus whose shape and microscopic characteristics are consistent for all symbioses of those specific partners; they produce metabolic products that neither of them produces on its own... the list goes on. You would think that lichens would be the poster children for happy, harmonious symbiosis. But nooooo. The very discoverer of the symbiotic nature of lichens, Simon Schwendener, said "As the result of my researches, the lichens are not simple plants, not individuals in the ordinary sense of the word; they are, rather, colonies, which consist of hundreds of thousands of individuals, of which, however, one alone plays the master, while the rest, forever imprisoned, prepare the nutriment for themselves and their master. This master is a fungus of the class Ascomycetes, a parasite which is accustomed to live upon others' work. Its slaves are green algae, which it has sought out, or indeed caught hold of, and compelled into its service. It surrounds them, as a spider its prey, with a fibrous net of narrow meshes, which is gradually converted into an impenetrable covering; but while the spider sucks its prey and leaves it dead, the fungus incites the algae found in its net to more rapid activity, even to more vigorous increase...." (translated by Vernon Ahmadjian in The Lichen Symbiosis (p.4), and garnished with a cartoon showing a smirking fungus holding keys and a billy club standing in front of a bunch of algae (floating unhappy faces) imprisoned in a vaguely biological-looking jail) In case we missed the point, Ahmadjian adds to this in his own voice "The mutualistic myth of lichens hinders our better understanding of these symbioses. To call a lichen association mutualistic is similar to believing that domestic cattle and humans have a comparable relationship because we provide them with food and shelter and increase their populations before we slaughter them. With respect to the healthy appearance of photobiont cells, parasitic associations often develop long-term equilibria between the bionts and there may not be any visible sign of damage or undue disruption of normal activities of the host. A distinction should be made between parasite and pathogen, the latter causing disease or damage. A similar relationship of controlled parsitism was proposed for ectomycorrhizas by Elias Melin."
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By now, you know my views on these issues, so I'll just let his statements stand. I will, however, point out that cattle are doing a hell of a lot better, population-wise and perhaps genetic diversity-wise, than any other land animal of comparable size. And I'll point out that Schwendener once again characterizes “feeding by sucking” as evil in his example of the spider. For another interesting case of ambiguous symbiosis, see Septobasidium.
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