JARS v52n1 - Honey Fungus: The Story of A Deadly Takeover

Honey Fungus: The Story of A Deadly Takeover
Leslie Drew
Duncan, British Columbia, Canada

Author Leslie Drew has recorded Nancy Jakusz's and Brian Greenwood's unusual encounter with honey fungus, from the first mysterious symptoms in their garden, through a long investigation to find the source, and finally to their acceptance of a scientist's conclusions. The article is not intended as a scientific treatise on honey fungus but as a story of the valiant effort of two gardeners to find the truth and then live with it - and be wiser for it.

Forces of nature, as everybody knows, place all gardens at risk. A fierce storm or a flash flood can devastate plantings in no time. A freak of nature, we say, and hope it does not happen again. Much less easy to accept is the fact that something as small as a fungus is just as powerful, just as freakish, and can wreak the same havoc slowly. Only when recognized early enough can this force be stopped in its tracks.
In Nancy Jakusz's case, it wasn't. For three years she watched helplessly as most of her rhododendrons - nearly 40 prime specimens in all - shriveled up suddenly and died, one by one. She could not figure out why. Nor could experienced growers who came to her suburban garden at Duncan on southern Vancouver Island. Losses of such magnitude had never been seen in a rhododendron garden, or any garden, in this region, at least not in modern times.
The quiet killer, it turns out, is honey fungus, which exists worldwide and can break out anywhere, given the right ("wrong" to gardeners) set of circumstances. Only by chance late in 1955 did Nancy herself stumble on this as the likeliest cause. Scientific investigation confirmed her diagnosis. It was an extraordinary occurrence, and perhaps the most puzzling aspect is that it happened without anyone even being aware of the possibility.
Gardeners in the British Isles know the honey fungus all too well. For decades they have been battling its incursions into rhododendron gardens; for years garden clubs have been warning members to be on guard. In high-stakes fields of commerce it is well known too: vineyards in Europe, kiwi fruit plantations in New Zealand, citrus groves in California, forests in British Columbia. Moreover, once the fungus, in disease form, gains a hold over a wide area it is extremely difficult (some say impossible) to eradicate. But Nancy, an otherwise well-informed home gardener, knew none of this - until too late.
The honey fungus belongs to the genus Armillaria . Its fruits of golden mushrooms, from which the name derives, look and are good enough to eat ("choice, with caution" in the edibility rating of the Audubon Society Field Guide to North American Mushrooms). Like most fungi, it normally lives in harmony with its nutrient provider, the host. Until the food runs out (whereupon it dies), the fungus is content to stay home, a placid consumer.
The delicate balance can, however, be rudely upset. The harmless homebody has the extraordinary ability of reversing its behavior. Shaken up and served a feast of fresh plant tissue, the fungus can gain the appetite and the strength to go in search of thriving plants and, finding them, kill them. A species known to be only weakly pathogenic can become strongly pathogenic. For the transformation to occur, there must be a sudden acquisition of a new food resource. The stump of an old and feeble deciduous native tree, delivered by a blow down, or logging, or a gardener's chainsaw, will do the trick.
Drawing upon the new supply of energy, the fungus reaches out underground for the root systems of neighboring plants by producing runners called "rhizomorphs" - light brown to black strands resembling thin boot laces - which usually travel within the moist top six inches of the ground. En route, the fungus manufactures more runners which, amply fueled, can advance up to as much as three feet a year. The fungus is now in full-blown disease mode.
Undetected and unchecked, the disease can take a heavy toll in trees (fruit trees and ornamentals), vines, shrubs, and small plants, even vegetables. "No plants are known to be immune...and it is doubtful whether any woody species is entirely resistant," the august Royal Horticultural Society states grimly. Rhododendrons, which are shallow-rooted anyway, are definitely vulnerable, as Nancy learned. As well, though, she lost two Japanese maples ( Acer palmatum 'Osakazuki'), two hydrangeas, and a young camellia, 'Jury's Yellow'. In a much less severe case that coincided with Nancy's, this in a garden at Nanaimo, 30 miles to the north, the casualties, besides a selected clone from the R. Moonstone Group, included Cyclamen repandum .
Nancy is an intensely animated person who goes into everything with passion. She's this way with gardening. Whatever plant genus takes her fancy she reads everything she can find, consults experienced growers, buys quality plants. Before coming to the Cowichan Valley and buying their modest property in 1982, she and her husband, Brian, had gardened at Golden in the Canadian Rockies, where they were lucky to get 90 frost-free days a year. In the much milder coastal climate they looked forward not only to gardening year-round but also to growing exotics previously denied them.
Nothing much had been done for years with the ground surrounding the house, so they started out front, on the sunny street side. Brian built arbors and trellises, raised beds and frames, which Nancy adorned with roses and clematis, espaliered fruit trees and grapes; masses of perennials of wide variety. Soon - in the unhurried gardener's meaning of "soon" - they created what closely resembled an English cottage garden, all behind a white picket fence.
About 1990, Nancy's attention turned to rhododendrons. The only space left for a sizable planting was a wilderness strip at the back. Shaded by mature conifers and big, old native dogwoods ( Cornus nuttallii ), it looked ideal. The whole setting was park-like, green and secluded. From the brow of a high embankment just above the property line there was a view down through leaf trees to a meandering salmon stream in the distance. Terracing their top portion of the steep bank with stone walls, they decided, would yield several deep, well-drained beds arranged in tiers and linked by pathways.
A former mountaineering guide, Brian has an affinity for rock. He is also a big man. He drove to highway construction sites, brought home huge slabs of granite, and built thick walls as much as 10 feet high. It was a Herculean task, yet one he took pleasure in doing. By comparison, the labor of hauling barrow loads of the planting mixture (topsoil, sand, compost, commercial peat moss, cow manure) was a snap. Thus far, apart from the work involved, there was nothing out of the ordinary in the making of the beds.
There was something else, though. While shaping and filling the uppermost beds, Brian chopped down aged dogwoods that were in the way. They had not flowered much and appeared blighted, besides. The smaller stump, conveniently concealed by a sword fern, he left in the ground. The other, more than a foot in diameter, he sawed off eight inches above bed level.
Nancy, meanwhile, was buying rhododendrons. The collection expanded, as it does with most beginners, in direct ratio to her enthusiasm. She studied species and their recently revised classifications; the multitudinous hybrids, their backgrounds and traits. Early in 1991, to learn more, she joined the newly formed local chapter of the American Rhododendron Society and, being a library clerk, became the club's librarian. Nothing in her reading, or her conversations with other growers, prepared her for what happened very soon.
The losses began in 1992, roughly six months after the plantings had been substantially completed. The first to die was 'Hoppy', a hardy hybrid of the Waterers' popular Seven Dwarfs. (Nancy was particularly fond of 'Hoppy' for having bought it at the first of the chapter's plant sales she attended.) During 1993 and 1994, the losses mounted, among them a fine R. lutescens , R. fletcherianum , two plants of 'Sir Charles Lemon', R. smirnowii , a plant of the Blue Tit Group ("a giant bonsai"), R. yakushimanum Exbury form and 'Ken Janeck', two 'Patty Bee' hybrids; the list of casualties went on and on. Some of the species were tall, almost due to reach flowering age. None had a chance. As she dug them up and burned them, one by one, Nancy wept.
"The symptoms were always the same," she said. "The plants would shrivel up, looking as if they needed water. The leaves didn't turn yellow. The time of year didn't matter; it would happen even in wet weather. In a week or two, probably 10 days on the average, they would be dead. Dry sticks. Sometimes only part of the plant would die. But partial or total, the end result was the same. The hot summer of 1994 was the worst. Practically every time we went into the garden we'd see another rhododendron dead or dying."
She kept asking veteran growers, including nurserymen, whether they had seen anything similar. Every time she drew blanks. Some suggested poor drainage, but that seemed unlikely because of the depth of soil (several feet in places) and the un-cemented walls buttressing the beds. Phytophthora , a type of fungal root rot, was another idea, so she went to a pathogen control firm at Victoria and tried an expensive ($80) liquid treatment. That didn't work. With almost her entire rhododendron collection wiped out, she began to despair of ever finding the cause.
In the early autumn of 1995, the first pieces of the puzzle fell into place. A cluster of golden mushrooms sprang up on the exposed dogwood stump. Upon digging them up, Nancy discovered an underground network of thin, fibrous strands reaching out from the stump. She remembered having seen the likes of them before on one or two occasions, but never close enough to dead rhododendrons to suppose they had any connection.
Three days later, she picked up the mail and was glad to see the latest issue of The Garden , the journal of the Royal Horticultural Society to which she and Brian subscribe. Casually, she leafed through the pages, then stopped abruptly at an article on honey fungus with color illustrations. "Honey fungus...is potentially the most devastating disease to occur in gardens," the article began. The potential, for Nancy, seemed to have become a sad reality.
Immediately she wrote for more information, and promptly received back a pathogen advisory pamphlet plus lists of plants deemed susceptible and resistant, according to records kept by Wisley, the famed RHS centre, and the United Kingdom Forestry Commission. Scanning the susceptibility lists, Nancy began to fear for more than her few surviving rhododendrons. Her treasured roses, hydrangeas, and hamamelis were also among 27 "notably susceptible" genera and species on the Wisley books. As for her Japanese maples that had died, the entire Acer genus except for Acer negundo appeared among six notably susceptible plants listed by the forestry commission.

Acting on two of the RHS recommendations, Nancy began digging up rhizomorphs, yards and yards of them, while Brian tackled the big dogwood stump. ("Remove all tree stumps whether or not they are infected by honey fungus," the RHS had counseled.) As he hacked away he noticed a creamy-white substance issuing from beneath the bark of the root collar and lower bole: mycelial fans, they are called, another tell-tale sign. Spurred into greater determination to remove the stump, Brian sent chunks of decaying wood flying in all directions, landing on beds now bereft of rhododendrons. At about this time, late one night, Nancy had yet another strange experience: she looked out the back door and saw that the stump and the surrounding debris were glowing in the dark, looking "as if a UFO had landed."

Behind the curving, glass-and-concrete entrance to the Pacific Forest Research centre at Victoria, 30 miles south of Duncan, the milieu is saner and calmer. Here scientists employed by the Canadian government guard British Columbia's vast forests against disease. Most folks know little about the intensive research that goes on here, only that it is the place you take mushrooms for identification.
Here, late in 1995, Nancy's problem came to the attention of Dr. Duncan Morrison, a forest pathologist and the province's leading authority on Armillaria . In his laboratory he picks up a bundle of the runners Nancy had unearthed, teases a few strands loose, and with a fingernail scrapes their outer coatings to reveal thriving white cores. The reddish-brown strands, he says, indicate an extremely good growing base. The jet black ones are far from dead; they are just older and mature.
His visual examination tells him the species is either A. sinapina or the newly named A. nabsnona , two of four species found on Vancouver Island. Both are normally quiescent and only weakly pathogenic. Both are identical in appearance, habitat, and mode of spreading. Whereas A. ostoyae , formerly designated as A. mellea , the most troublesome species in forests south of the 53rd parallel, spreads in flushes, these species typically maintain themselves in networks. Armillaria ostoyae , which grows on conifers, definitely had the potential to do garden damage, Dr. Morrison comments. The fourth and last Vancouver Island species, A. bulbosa , seems the least threatening. It associates with garry oaks around Victoria and the Gulf Islands, and although found growing in the Finnerty Gardens at the University of Victoria has not in the slightest affected their large rhododendron collection.
By this time, the first frosts had arrived. Further study would have to wait until the next autumn when the mushrooms popped up again. They did, as if on cue. Upon receiving a bag full October 1996, Dr. Morrison tentatively identified the species as A. sinapina . (In one way he was not surprised; it explained the eerie glow Nancy had seen, a phenomenon well known to the natural sciences, especially entomology, where it goes by the name of bio-luminescence. A limited number of genera of fungi, Armillaria included, have this power, and he knew for sure that A. sinapina is bio-luminescent.) It remained for the fungus to be isolated from the tissue of infected plants to demonstrate conclusively that this was the primary cause of all the plant deaths.
November 1996 Dr. Morrison visited the garden for the first time, accompanied by an assistant. Nancy worried that in her zeal for mopping up she might have destroyed all the evidence. Without much searching, though, she soon found and dug up three sickly plants - two rhododendrons, 'Royal Pink', a R. williamsianum hybrid, and 'Aloha', a R. yakushimanum hybrid - and a Hydrangea quercifolia . Roots exhibiting the mycelial fans were snipped off and bagged.
Dr. Morrison, meanwhile, had a chance to look around at the garden setting. What he saw was the "classic situation" he had seen many times before in forests. He explained what happens on his familiar turf: "In forests a healthy tree is immune; the fungus will run around on the surface of its root system and not kill it. But when the host gets older and weaker, say 40 or 50 years old, especially in a mixed stand where conifers have shaded hardwoods (broad-leaved trees) and the hardwoods are cut down, the fungus can become invasive." In other words, by making their rhododendron garden where they did, and leaving the dogwood stumps behind, Nancy and Brian had unwittingly brought on the disease.
Back at the research centre a team of technicians cultured infected tissue from several pieces of each of the three sample plants and, using a fool-proof method similar to DNA fingerprinting for human forensic purposes (the RFLP or Restriction Fragment Length Polymorphisms test), identified the species as A. sinapina . Dr. Morrison was satisfied that he had established incontrovertibly that this organism, and none other, was the primary cause of the plant deaths.
Armillaria sinapina happens to be the most common Armillaria species in British Columbia, covering a huge area of this province and adjacent Alberta. It is also seen in eastern Canada and the northern United States. "It seems to be a North American species," Dr. Morrison adds. "Europe has others with similar characteristics."
Never, though, had he seen so severe an infestation in forests here. "We do tend to see a moderate amount in the north-central part of the province, around Prince George, where hardwoods are shaded by conifers. But it doesn't kill forest trees. I have seen it killing fireweed, though, and I have seen it on pampas grass." For A sinapina to have done the damage it did to Nancy's garden, he could only surmise there had to be a large amount of inoculum to overcome the plants; that the dogwood stumps, which he never saw, were exceptionally large.
The realm of fungi is so vast and so complex that only in recent years has science begun to understand what goes on there. With new technology for analyzing and classifying species more accurately, and more extensive field studies, has come a clearer picture of the distinctive characteristics of those species and how they behave. Wood decay fungi, the group to which Armillaria species belong, have long been recognized as important recycling agents. Without them, as one scientist had explained, the planet would be littered with un-decayed wood; forests would suffocate in their own debris.
So why don't some species of Armillaria always perform the roles expected of them? Why have they developed the remarkable ability to turn into death-dealing parasites? Under natural conditions, it is how they obtain new food sources. The weakly parasitic species like A. sinapina usually wait for the potential host to weaken before they colonize it. But the strongly parasitic ones often have the ability to kill healthy hosts, Dr. Morrison explains.
As for origin, the widely accepted theory is that it is a survival strategy "learned" at some stage in their long evolutionary past in order to meet nutritional needs, which means that by now, having become an inherent trait, it is unlikely to be "unlearned" in a hurry. For this reason many scientists, respectful of individuality, tend to be skeptical of any notions of a quick fix, biological or chemical. In many instances chemical applications have proved to do more harm than good, leaving mechanical means as the only recourse.
Control sounds easy: get rid of the food source, because the fungus cannot survive for long without its food base. On acres of infected land this can be difficult and costly. In forests the standard procedure is to haul in earth-moving equipment, extricate infected stumps, and burn them. (A Swedish machine capable of actually pulling up trees, roots and all, is currently in use in British Columbia.) After the job has been done, the sites must be checked frequently for possible recurrences.
On large cultivated properties, private and commercial, bringing in heavy equipment may not always be an option. Experience on estates in the British Isles, where A. mellea is the damaging species, has taught growers that the disease can at least be kept at bay by what could be called the "barrier method." One grower who has adopted it is Peter Cox, the noted rhododendron hybridizer and plant hunter. At the Cox nursery in Scotland so many plants were being lost in recent years that beds are lined with polythene, perforated where the ground is flat to allow for drainage. "We lost very little until our elms all died," Cox writes.
Dr. Morrison, who generously stepped out of his own busy role to investigate Nancy's case, had a few more words of interest to rhododendron growers in the Pacific Northwest. In the sitting of a new garden, the edge of a forest may not be the best place. Dogwoods tend to grow on forest verges, in full sunlight. So, too, do broad-leaved maples ( Acer macrophyllum ), a stump of which was the suspected source of the Nanaimo outbreak.
And another point: most of Nancy's plants that died were not indigenous. The history of all Armillaria invasion has shown that non-natives generally lack the resistance of natives, the two not having "grown up" together. This has implications for all our showy wild plants, especially the beautiful Rhododendron macrophyllum , which is already attracting attention for its ability to resist droughts.
Today Nancy and Brian are sadder and wiser gardeners. (Right along Nancy had said she would never again be the same gardener she was when their ordeal began, when she could find no answers.) This past autumn they knew they were still losing the struggle. The golden mushrooms sprang up in greater profusion than ever before, as did mushrooms everywhere on Vancouver Island, and the rhizomorphs' rampage for food continued unabated. In the face of this, Nancy and Brian have turned to water gardening and indoor propagation.
"I can never give up gardening," Nancy said calmly, "I shall garden until the day I die."

Leslie Drew is a member of the Victoria Chapter.