Houses for mites?

an intriguing relationship

One July day I was moseying along a streambank, looking at the alders. Both red and Sitka alders grew there, but I was focused on the Sitka alders; I examined many leaves and put a few into a plastic bag to take home. A passer-by asked if I intended to eat them. Well, no, to my knowledge, humans don’t eat alder leaves—I planned to inspect the under-surfaces of the leaves with a dissecting microscope in my study.

Whatever for?? I suspect that most of my hiker friends already think I’m a bit nuts, with my interest in the composition of bear scats, the details of floral structures, the strange habits of slime molds, an unusual bird song, a skanky salmon carcass squirming with maggots, or other arcane natural history matters that often make me stop along a trail. A concern with the underside of alder leaves would probably clinch their opinions. Oh well….

I am interested in Sitka alder leaves because some of them have little tufts of hairs in the vein axils, where the side veins come off the midrib. On many other woody species in North America, including some maples, oaks, cherries, and grapes, tiny structures in vein axils (usually tufts of hair in North America but often pits or pockets elsewhere) serve as domiciles for mites. They are called domatia (singular = domatium), which means ‘houses’. And they serve the functions of a house: mites retreat to them for shelter from environmental extremes and predators, to lay eggs, to defecate, and to molt (leaving their exoskeletons there). Years ago, by surveying many leaves of many species in the eastern forests of North America, we found that at least twenty-five percent of domatia (and often fifty percent) in most species showed signs of mite occupancy. Similar occupancy rates were also found in foliar domatia in many other parts of the world.

Sitka-alder-Domatia 2 Carol Griswold

It is important to recognize that domatia are made naturally by the plant itself; they are often visible in the developing leaf bud. They are not galls, which are induced by the activities of insects or mites. So it is reasonable to ask if they serve a purpose and what that purpose might be.

Almost all of the mites we (and others) found in the domatia were potentially beneficial to the leaves and the plants that made them. Most of the mites were predatory–eating other mites or small insects–or fungus-eating–consuming molds and mildews and fungal filaments. Many studies have shown that the abundance of such beneficial mites is higher on leaves with domatia than on leaves without domatia. So the observations clearly suggest that this is a mutualistic relationship, in which both participants benefit: mites get housing in the domatia and plants get protection of their leaves.

The idea that the mite/domatia relationship is mutualistic dates back to 1887, when a Swedish scientist first looked at this. A few biologists accepted the idea without further investigation. But as is often the case with any new idea, the mainline scientists of The Establishment viewed the idea with scoffing, scorn, and rejection. Someone even went so far as to suggest that domatia occurred on leaves for the benefit of plant taxonomists, because they turned out to be useful in identifying species.

Such foolishness aside, a few experiments more than a hundred years later eventually showed that leaf damage is less when mites occupy the houses and forage over the leaf surfaces. Further study revealed that associations of mites with foliar domatia go back many millions of years, showing up in fossils. By now, leaf domatia are known from woody plants in most major taxonomic groups all around the world.

So—back to my Sitka alder leaves: I wanted to know if there were mites in those domatia too. I looked at ten mature domatia-bearing leaves from each of five locations in Juneau, counted the domatia and inspected them for evidence of mites. In over four hundred domatia, I found only four mites and one possible mite egg.

In the course of searching many alder leaves for domatia, I also found that leaves on many branches and trees had no domatia at all. In short, development of foliar domatia is sporadic in Sitka alders and mite occupancy is apparently very low. It takes a while for mite populations to develop on new leaves each year, so possibly a census of domatia in August would show a higher occupancy rate than in July, although that begs the question of what good it might do to protect leaves so close to the time when they turn brown and fall off. Maybe the summer season here is simply too short to allow time for a good population build-up of beneficial mites? Furthermore, considerations of mite population levels do not address the question of why domatia occur so sporadically on these leaves.

Perhaps evolution is in process of eliminating useless domatia from Sitka alders…or, contrarily, increasing their potentially useful occurrence on that species. Would on-going climate change affect the outcome? More questions than answers, once again!



benefits in both directions

Mutually beneficial relationships (a type of symbiosis, which just means ‘living together’) are common under the aegis of Mother Nature. Some obvious ones are bees and hummingbirds getting nectar from flowers while moving pollen from plant to plant and robins and bears eating fruits and excreting, and thus dispersing, viable seeds. There are many other mutualisms too, but there is a not-obvious one that is and has been fundamentally important to most of the plants on earth.

Many kinds of fungi form close, mutually beneficial, relationships with plant roots, obtaining some carbohydrates from the plant while transferring phosphorus and other nutrients from the soil to the plants. These are the mycorrhizal (‘fungus-root’) relationships (between the roots of plants and the underground filaments of the fungus) that have often been mentioned in the essays in this space. Many local species of fungus (including, for example, Amanita) participate in such relationships. Experiments have shown the benefits of these relationships to the plant partners; the benefit to the fungi is not always clear, but many of these fungi cannot live without their plant partners. It has been estimated that at least eighty percent of all plants are involved with mycorrhizal partners.

Beyond the critical ecological importance of present-day mycorrhizal mutualisms, however, lies an important historical and evolutionary perspective: researchers have good evidence that the first green plants to colonize the land—a few hundred million years ago– had some kind of close fungal associate. This relationship was not technically mycorrhizal, because the first land plants (derived from freshwater green algae) did not have proper roots, but it was, nevertheless, a close physiological association of fungus with plant. Fungi invaded land well before the green plants did, and must have been adept at foraging for nutrients in the poor soils that then prevailed. So they were there, perhaps availing themselves first of exudates from the photosynthetic plants and eventually drawing nutrition directly from the plants themselves and providing soil nutrients in exchange. If those researchers are right, then all the great diversity of plants we see around us was made possible in the beginning by a mutualism.

All of this raises a big question in my head: if fungal partners have been so important historically and so many kinds of current-day plants have such fungal partners, then why are there a number of plants that do NOT have these partners? For example, mosses are reported to lack fungal partners, although their cousins, the liverworts and hornworts often have them. Examples of non-mycorrhizal plants in our local flora include starworts, paintbrushes, louseworts, sundews, lupines, sweetgale, mistletoes, many members of the mustard family, and numerous others. A look at that abbreviated list tells us that one way to thrive without a fungal partner is to have another means of supplementing nutrition: many of the non-mycorrhizal plants are insectivorous (sundews), or partly parasitic (paintbrush), or harbor nitrogen-fixing bacteria (lupines). In addition, some plants-without-fungal-partners have extraordinary roots (the so-called cluster-roots of lupines, for instance) that give the plant a huge amount of root surface for taking up nutrients. All those ways of supplementing plant nutrition may account for some of the species that lack a fungal partner, but not all, so the question is only partly answered.

By definition, mutualisms involve some reciprocity between participants. But it is not uncommon for the balance to favor one partner more than the other. In fact, there are hundreds of examples of relationships in which one participant simply exploits the other, giving nothing back: what was probably once mutualistic has become exploitative. For instance, orchids produce seeds that require a mycorrhiza for germination, but because the seed contains no food stores for the embryo, the fungi get little or nothing; the orchids apparently control the relationship by chemically attracting the fungal filaments. Some orchids (such as the coralroots) lack green leaves altogether and are totally dependent on their fungi, without reciprocating: the plant gets both nutrients and carbohydrates from the fungus, which draws such sustenance from the soil or other plants. The two-sided arrangement has become one-sided. Undoubtedly there are instances in which the fungus gets one-sided benefits too, and this may have been the case very early in the evolution of the land plants.

In some cases, the relationships are still more complex. Some plants require ‘companion plants’ to support their mycorrhizae, so there are three participants in the relationship. For example, certain Australian Lobelias require the presence of mycorrhizas associated with broombush (Melaleuca uncinata) in order to germinate. Some species in the gentian family (such as centaury, Centaurium) develop full mycorrhizal associations only when certain other plants (such as clover, Trifolium) are present too.

Some plants have very specific requirements as to what fungus makes a good partner. Many orchids are fussy this way. And when plants are introduced to new countries, as the pines have been to the southern hemisphere and eucalypts have been to the northern hemisphere, they may not grow well unless their own particular mycorrhizae are moved with them. The local varieties of fungus won’t do.

In contrast, garlic mustard is a useful herb in the Old World that grows without harm to other plants, with which it coevolved. But when introduced to North America, it became a highly invasive weed, in large part because it kills or damages the plant/fungus partnerships that prevail here, so the native species fail to thrive.


often-ignored beings

Our coastal rainforest is characterized by a rich assembly of lichens. Lichens colonize rocks – including the rocky intertidal zone, logs and fallen branches, and even bare sand. They also adorn the trunks and branches of trees. Some branches support numerous kinds of lichens in a sort of miniature garden, of varied colors and textures, often very beautiful.

What, then, are these often-ignored beings? The traditional view is that a lichen is a happy collaboration of a fungus with one or two kinds of alga: a green alga or what was called a blue-green alga, now known as cyanobacterium. Only certain kinds of algae associate in this way with fungi, and only some fungi make these associations with algae. Lichens have been used as classical examples of natural symbiosis (living together), in which the alga provides carbohydrates (by photosynthesis) and sometimes nitrogen (by the cyanobacteria) to the fungus and the fungus provides a protected habitat, water, and perhaps minerals to the alga.

The reality, however, may not always be quite so bland. When the fungus reproduces by spores, which germinate to form a new individual fungus, the new fungus eventually captures algal cells (thus becoming a lichen) and exploits them until they die. Although most lichenizing fungi can live for some time without algae, the algae apparently can live quite well on their own and getting captured by a fungus may not be entirely beneficial from the algal point of view. Thus, many lichens may be viewed as a sort of controlled parasitism of the alga by the fungus. One researcher even commented that sometimes the algae ‘escape’ from the fungal grasp!

The relationship between fungus and alga may vary with circumstances, but the factors controlling that variation remain to be described, it seems. Whatever the precise relationship between the two (or three) different organisms that constitute a lichen, the ecological roles of lichens are important and widespread.

Lichens are important stabilizers of bare ground; in some situations, they help reduce erosion. Indeed, they are said to be the dominant form of ‘vegetation’ on eight percent of the land surface (think especially of Arctic, Antarctic, and alpine areas). They also—very slowly—break down rocks, mostly by secreting acids that weaken the rock, and thus they contribute to the long-term weathering process that creates soil.

Crustose lichen on rock. Photo by Bob Armstrong

Ground-dwelling lichens (and mosses) trap wind-blown dust; the dust and associated nutrients, along with nutrients from rainwater, gradually build up soils. Then wind-borne seeds and spores have a good habitat for germination. Lichens containing cyanobacteria can extract nitrogen from the air and make it usable by plants (this is called nitrogen fixation). Foresters in some regions have even encouraged lichens to spread (for example, over a recent burn), in order to improve the soil and make new trees grow better.

Tree-dwelling lichens also extract lots of nutrients from rainwater and fog, and many of our common arboreal lichens are good nitrogen-fixers. Nutrients from these lichens eventually find their way into the soil. For example, we often see, on the ground, fragments of lichens that have been torn from the trees by a stiff wind. When these decompose, their nutrients are added to the soil.

Lichens provide shelter for numerous tiny animals, such as springtails and mites, which are food for spiders and insects, which in turn are food for shrews and birds. We often see warblers, chickadees, and woodpeckers searching among the lichens on branches for lurking insects or spiders.

Caribou have been called lichen specialists. Lichens comprise much of the caribou diet—as much as ninety percent in winter but even in summer about half the diet is lichens. The ground cover commonly called ‘reindeer moss’ is really a lichen. Caribou were introduced to St Matthew Island in the Bering Sea some decades ago; the herd increased rapidly but eventually ate up most of the lichens, which grow too slowly to compensate for the rate of eating them, and thousands of caribou then died of starvation.

Arboreal lichens provide important food for woodland caribou, elk, black-tailed deer, and moose. Mountain goats in our area eat lichens all year long, including several types that grow on trees. Northern flying squirrels and boreal red-backed voles eat a lot of lichen; arboreal lichens may constitute as much as ninety percent of the winter diet of flying squirrels. The flying squirrels also use horsehair lichens to build their nests inside of tree cavities.

Dozens of species of birds incorporate lichens in their nests. I once found a crossbill nest that had blown out of a tree. The outside was made of lichen-covered twigs; in fact, an expert later identified many kinds of lichen in this nest. Hummingbirds commonly decorate the exterior of the nest with bits of leafy lichens, which help camouflage the tiny nest.

Rufous hummingbird nest. Photo by Katherine Hocker

Humans in many cultures have found uses for lichens—as food, fiber, medicine and poison, dyes, decoration, and, in some parts of the world, as perfume. Many kinds of lichen can be eaten; only a few are poisonous. However, they are said to be not very flavorful, at best and are better eaten after boiling in several waters to reduce bitterness or with soda to reduce extreme acidity. The lichen known as rock tripe is famous as a survival food for Arctic explorers. Arctic Natives ate the partially digested lichens from caribou stomachs; this stuff is apparently more readily digested than fresh lichen. Mixed with raw fish eggs, it reportedly formed a favorite concoction (an acquired taste, no doubt!).

Over the centuries, lichens have been used as medicines in various ways, both internally and externally. Some of the rationales for medicinal applications seem ludicrous to us now. For example, lungwort was used to treat lung diseases because its lumpy surface reminded people of lung tissue. However, it turns out the lungwort actually does contain substances that work against TB bacteria. The basis for using a yellow-orange rock lichen to treat jaundice, which turns the skin yellow, is still more tenuous.

Beard lichens contain usnic acid, which has some antibiotic properties. So beard lichens have often have been used in ointments to treat skin infections and sores. Indeed, they have been over-collected in some regions, to the point that they are scarce and hard to find. However, some people are very allergic to this acid, so medicines with this as an ingredient must be used with care.

Fibrous lichens were used in clothing by some Native cultures, mixed with bark fiber. Because such garments were not very durable, they were often restricted to ceremonial use. Branching, shrubby lichens are used in floral arrangements and architectural models to represent shrubs and trees.

Lichens have provided dyes for centuries: in our region they have been used to color mountain goat wool and porcupine quills. Prepared in boiling water, certain lichens yield russets, brown, and yellows. Others yield reds and purples when fermented with a source of ammonia (traditionally, this was stale urine—the aroma eventually dissipated).

An unusual use of lichens is directly applicable in our area. Crustose lichens generally grow slowly, less than a millimeter a year. By measuring lichens on dated (and undisturbed) gravestones, one can estimate the average rate of growth. Then if that estimate is applied to the same kind of lichen on rocks near a glacier or a rock slide, it is possible to estimate how long that rock was available for colonization by lichens; that is, how long it has been there.

Humans have a huge impact on lichen populations and communities. The most obvious is habitat destruction through increasing urbanization. Directly relevant to our area is the dramatic loss of tree habitat when old-growth forest is logged. Second-growth stands support only a much-reduced diversity of lichens.

More pervasive is the dramatic effect of air pollution on lichens, many of which cannot tolerate the pollutants poured forth from industrial processes. Sulfur dioxide is an example of a deadly pollutant, but excess amounts of lead or zinc, for example, could also be detrimental. Some of the most pollution-sensitive lichens include the beard lichens and those that contain cyanobacteria (for instance, lungwort and kidney lichens). The trunks of our red alder trees often look white or grayish, but this is actually a white crustose lichen; in areas with serious air pollution, this lichen dies and the trunks show their brown bark. Because of their sensitivity to air pollution, lichens are extremely useful as indicators of air quality.