MENTION the word phytophthora, and you’ll get a different response depending on where you are. It may be hard to say and even harder to spell, but in California it’s a household name. Three years ago, biologists fingered a new species of this microscopic fungus as the cause of sudden oak death, a mysterious disease that was sweeping through the state’s coastal forests. The appearance of the same lethal pathogen in British trees earlier this year prompted fears for Europe’s woodlands. In Australia, a phytophthora is high on the government’s list of most-threatening environmental evils, guilty of ravaging the famous jarrah forests and heathlands of the south-west. In Ireland, the word has been part of the vocabulary far longer. A phytophthora was responsible for the blight that ruined the potato harvests of the mid-19th century, leading to famine and exodus. But the fact that the name of a microscopic fungus is now known so widely outside the pathology lab signals a worrying trend. “Phytophthoras are on the move,” says Clive Brasier, who has spent more than 30 years studying them.
In their natural habitats and hosts, phytophthoras do little harm. Transport them to new places and introduce them to species they’ve never encountered before and they can turn nasty. Worse, the mass movement of plants is responsible for a malevolent form of matchmaking, bringing together species of pathogen that would never normally meet and paving the way for the evolution of new and potentially dangerous diseases.
The first epidemics caused by alien phytophthoras probably go back to the early years of plant collecting. Then, only the wealthy could afford to adorn their estates with exotic species, and a mere trickle of plants crossed from one continent to another. Even so, they came with a cargo of pathogens, some of which escaped into the wild and cut a swathe through trees with no resistance to them. Today, almost everyone’s small plot is filled with exotics, a trend fuelled by TV makeover shows and gardening magazines. This obsession with the exotic has created a multibillion-dollar global industry, and the risk of importing lethal pathogens is far higher. “We’ve not really learned our lessons,” says Brasier, emeritus mycologist at Forest Research, part of the UK Forestry Commission.
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The first signs of sudden oak death appeared in trees in the San Francisco Bay area in 1995. Tanoaks, black oaks and coast live oaks around the bay were turning brown and dying. Stricken trees seemed to bleed, oozing a deep-red tarry sap from ugly cankers on the lower parts of their trunks. The epidemic spread fast, and in 2001 the disease showed up in the south-west corner of Oregon. Sudden oak death has now killed many tens of thousands of trees, with the biggest losses in the bay area. “The disease is patchy. Some areas are devastated while some areas have none,” says Dave Rizzo, a forest pathologist at the University of California, Davis.
At first, people suspected the trees were dying from the effects of drought followed by attacks by bark beetles and other opportunistic pests. Then in 2000, Rizzo and Matteo Garbelotto of the University of California, Berkeley, isolated a phytophthora from the bleeding cankers. This was bad news. Phytophthoras belong to a group of alga-like fungi called the oomycetes – organisms responsible for some of the world’s worst plant diseases. No one recognised this one. “It was very striking and very unusual. It was clearly a new species,” says Brasier. “And it was almost certainly imported to the US.”
Introduced phytophthoras have a reputation as serial tree-killers and the discovery made everyone jittery. What if the pathogen reached the eastern US, where oaks dominate the forests and red-oak timber is important to the local economy? What if it reached Europe? The threat was so serious that the European Union banned imports of plants and wood from infected parts of the US. Meanwhile, Brasier began to assess the risk of the disease reaching Europe. He had hardly started when a colleague from the Netherlands told him about a phytophthora discovered in 1993 on rhododendrons in Dutch and German nurseries. “When he described it, it rang a bell immediately,” says Brasier. “It turned out to be the same organism.” Soon it had acquired a name – Phytophthora ramorum.
The pathogen Europe hoped to keep out had been there at least seven years – plenty of time to spread far and wide. In the UK, plant-health authorities immediately began a survey of nurseries and garden centres. In 2001 they found nothing. Then in April 2002 they found a single infected viburnum. Within a year P. ramorum had been detected at 300 nurseries across the country, mostly on potted rhododendrons and viburnums, Pieris and camellias, all popular garden shrubs. A handful of infections were found on established shrubs in public gardens and a few in wilder areas where rhododendrons are naturalised. Soon it had been reported from nurseries in nine European countries.
Something strange was going on. In the US, the fungus attacked woodland oaks. It worked its way into living tissues under the bark killing the phloem that transports nutrients to and from the canopy, and ultimately starving the tree to death. In Europe, only nursery plants showed symptoms, and then only black blotches on leaves and dead shoots. It hardly seemed the same disease. Closer inspection revealed that the organisms were in fact slightly different. Phytophthoras come in two “mating types” known as A1 and A2. Each can reproduce asexually, but sexual reproduction requires the two types to come together. In their native habitat both forms probably exist side by side. In the US, only the A2 type of P. ramorum was present; in Europe, only A1. There were also some genetic differences, and the European form was more aggressive.
These differences suggest the pathogen was introduced separately to the two continents. But it still seemed odd that one form infected nursery plants while the other was running riot in wild oak woods. Further investigation revealed the grim truth: the infection was present in US nurseries too. Although no one had noticed it before, it had probably been in Californian nurseries for years. The story began to make more sense. The disease out in the woods almost certainly started on an imported ornamental. “We suspect it was introduced by nurseries,” says Everett Hansen, a forest pathologist at Oregon State University in Corvallis. “And we assume it came from Asia, because that’s the centre of diversity for rhododendrons.” California’s nursery industry is worth $2 billion a year, and plants are shipped nationwide. Suddenly the outlook for the rest of the US looked bleaker. Europe also had more reason to worry: if P. ramorum had jumped from the nursery once, why not again? In the UK, the authorities ordered the destruction of all suspicious plants and regular checks on trees near infected nurseries.
Too late. Last October, Brasier and his colleague Sandra Denman spotted bleeding cankers right around the girth of a tree in southern England. In the lab they isolated P. ramorum from one of the cankers. Within days another diseased tree had been found in the Netherlands. Both were American red oaks. A few weeks later, the news was worse: some of the UK’s best-loved trees were infected, including beech and horse chestnut. “It was clear it could attack several species of UK trees, and the list could grow further,” says Brasier. As żěè¶ĚĘÓƵ went to press, the number of infected trees had reached 14 at four sites in southern England. Most are beeches, but the list now includes holm oak, turkey oak and sweet chestnut.
The US too is in a state of high anxiety. In March, the California Department of Food and Agriculture announced that P. ramorum had been found at a giant wholesale nursery near Los Angeles, well outside the cordon sanitaire imposed by the authorities. Sales of potential host plants were stopped immediately, but records showed the nursery had sent potentially infected plants to 783 garden centres in 39 states. Infected plants have now been found in 28 nurseries in California and 54 nurseries in 11 other states, including some in eastern states with historic oak forests. “People in the east are very nervous,” says Rizzo.
With vigilance and speedy action, it might be possible to contain or eradicate new outbreaks. Hansen is optimistic that Oregon’s efforts to combat the disease will work. There is also a chance that Europe might avoid a full-blown epidemic. But it’s too late for California. “Whole hillsides are dead and the landscape is changing,” says Rizzo. If the worst happens and sudden oak death takes off, it could go global. If we are lucky this time and it doesn’t, there’s every chance another phytophthora will. “I think we can expect to see more of these things,” warns Rizzo.
Should anyone doubt how bad things could be, they need only look at Phytophthora cinnamomi, which has been ravaging the landscape on four continents for centuries. Native to New Guinea and the Celebes region of the Pacific, it was introduced to the US more than two centuries ago. By the early 1900s, it had wiped out the chestnut forests south of the Appalachian mountains, altering the landscape forever. The same fungus destroyed sweet chestnuts in southern Europe in the 1920s, wiping out 75 per cent of the trees in Spain and several million in Portugal. It is still a problem in chestnut-growing regions from the UK to Greece and has moved into oaks, killing large areas of cork oaks in Spain and Portugal.
Perhaps worst of all, P. cinnamomi is wrecking ecosystems of international importance in the southern hemisphere. In south-west Australia, the fungus has infested about 20 per cent of jarrah forest and around 60 per cent of the montane shrublands and sandy heaths – hotspots of biodiversity with thousands of endemic species. More than 20 per cent of the 9000 native species that grow there are susceptible, and some are at risk of extinction. The pathogen is beginning to repeat the process in the equally important fynbos flora of South Africa’s Cape region.
The spectre of another P. cinnamomi is worrying enough, but there are other alarming prospects. So far, the outbreaks of P. ramorum in the US and Europe both consist of a single mating type. Bring the two together and they could produce even more formidable offspring able to adapt to new hosts and attack with greater ferocity. Mating also generates long-lived spores that make control more difficult.
Phytophthoras, however, don’t need their other halves in order to swap genes and generate more potent progeny. Species that do not normally share the same environment will not have evolved barriers to hybridisation. In 1993, alder trees growing along the banks of English rivers began to die. An unidentified phytophthora was attacking them at the base of their trunks. In 1999, Brasier and colleagues at the Scottish Crops Research Institute in Invergowrie, Angus, revealed it as a highly aggressive new hybrid of two phytophthora species that had been independently introduced to Europe (żěè¶ĚĘÓƵ, 15 May 1999, p 7). “The disease is now becoming serious and widespread across Europe,” says Brasier. “It’s a good example of what can happen when you get a hybrid. It’s a warning.”
A fluke? Unlikely to happen again? Not according to Brasier. Phytophthoras are coming together ever more frequently as alien species encounter native ones and other aliens. In one instance, a single pot at a Bavarian nursery contained five different species. And the problem is not confined to nurseries. The outbreak of sudden oak death in the UK prompted an exhaustive investigation of the infected trees. On eight of the beeches, Brasier and his colleagues found not only P. ramorum but a second very aggressive phytophthora, known for the moment only as PtC. Like P. ramorum, PtC produces aerial spores and is spreading on rhododendrons. “We know little about it yet, but it can clearly do a big number on beech,” says Brasier.
Despite internationally agreed safeguards designed to prevent the spread of pathogens, alien phytophthoras are clearly slipping through the net. In the past 20 years, there has been an explosion in demand for exotic plants. Gardening has never been so popular, with millions of people heading for garden centres where they can buy plants from all over the world. Where once local nurseries would import a few specimens and propagate their stock from these, today retailers import plants in bulk directly from growers as far afield as China and New Zealand, where they can produce millions of them fast and cheaply. There are no fungicides that kill phytophthoras so many plants are treated with fungistatic chemicals that suppress them temporarily. The plants look healthy – at least until they are sold and planted out.
Perhaps the only way to prevent future outbreaks is to restrict the movement of plants and return to local production. Specialist nurseries could propagate from small quantities of licensed and quarantined material. They could also use seed or meristems – shoot tips grown from cell cultures – neither of which harbour phytophthoras. With imports reduced to a minimum, a system of health checks and quarantine might guarantee plants free from pathogens. This won’t appeal to big retailers who pile them high and sell them cheap. But the alternative could be a rash of new and devastating diseases. “It’s a global issue,” says Brasier. “At stake are forests everywhere and natural ecosystems around the world.”
Getting to know the enemy
As soon as a new phytophthora was identified as the cause of sudden oak death the race was on to find out more about it. Which trees were susceptible to attack? How did the pathogen spread and how fast could it travel? Forest pathologists needed answers urgently.
Phytophthora ramorum turns out to be an oddity. Most phytophthoras attack roots and are spread in soil and water. P. ramorum attacks the upper parts of plants and produces aerial spores, though it does rely on water to complete its life cycle. Rain splashes or droplets from sprinklers in nurseries carry spores over short distances, but in stormy weather gusts can take them further, perhaps a few hundred metres, lofting them high into the woodland canopy. From there, spore-laden raindrops run down trunks and onto leaves and branches. This method of dispersal limits how far and how fast the disease can spread naturally. Big gaps between outbreaks mean that infected plants have almost certainly been moved by people.
Lab tests show that P. ramorum can infect many species. In the UK both native and plantation trees – although not native English oak – and some important heathland species such as bilberry are susceptible. In the US, around 30 species of forest shrubs and trees have succumbed. “Most plants can probably be infected if they are exposed to a big enough dose of spores,” says Everett Hansen of Oregon State University in Corvallis. In some species the fungus infects leaves and twigs, where it produces prodigious amounts of spores. In others, it infects the trunk causing terminal disease. Once under the bark it cannot get back to the surface to sporulate so, unlike leaf and twig hosts, these trees cannot transmit the disease.
All the diseased trees in the UK were close to heavily infected spore-producing rhododendrons. But phytophthoras can evolve fast. If P. ramorum adapts to its new hosts and begins to sporulate on native species or, worse, begins to infect both leaves and trunks of the same tree, then the disease could establish in the wild with no help from ornamental carriers. That has already happened in the US where the epidemic is more advanced. In California’s oak woods, P. ramorum sporulates prolifically on native bay laurel, which is now the main source of infection in some woodlands. Worse, tanoak supports both kinds of infection, with the fungus producing spores on the twigs and then killing the trees through damage to the trunk. And in Oregon, Hansen has found that trees with trunk cankers may sprout, allowing the fungus to move into new shoots and then sporulate. The pathogen may need people to introduce it to new hosts, he says. “But once it gets going from tree to tree it moves well enough on its own.”