White Pine Blister Rust

White pine blister rust is among the most famous of forest diseases. A student of forest pathology should be intimately familiar with the life cycle and disease cycle.

Hosts

Since this is one of those wacky rusts, it must have two unrelated hosts to complete it’s life cycle. We can call the pine the “primary” host, reflecting our bias, or we can call it the aecial host, reflecting the prominent spore stage that occurs on it.

Aecial hosts are members of the genus Pinus, subgenus Strobus (soft or white pines) that have 5 needles per fascicle (bundle). Most taxonomic arrangements distribute the 5-needle pines into two sections, one of which includes non-hosts without 5 needles per fascicle, although the fungus seems to disagree with that arrangement. The most prominent hosts in North America are Pinus strobus (eastern white pine), P. monticola (western white pine), P. lambertiana (sugar pine), P. albicaulis (whitebark pine), P. flexilis (limber pine) and P. strobiformis (southwestern white pine). Of these, the most effort has gone into sugar, western white and whitebark pines. In 2004, the disease was found for the first time on a bristlecone pine, P. aristata, in Colorado ​[4]​.

The alternate, or telial hosts are typically species of the genus Ribes, gooseberries and currants, including several species grown horticulturally (but see Other Issues below). Wild Ribes are typically not much damaged by the disease. There can be damage to highly susceptible, commercially grown Ribes varieties when disease is severe ​[8]​.

White pine blister rust is the only stem rust of white pines in North America.

Pathogen

Cronartium ribicola (phylum Basidiomycota, class Pucciniomycetes, order Pucciniales, family Cronartiaceae) is a rust fungus. It is native to China or thereabouts (see Distribution below). The life cycle is the most remarkable aspect of the pathogen (see below). The fungus has a macrocyclic, heteroecious life cycle (meaning a full, 5-spore cycle with alternating hosts). It seems like a life cycle from another planet, but some students trying to learn it might say it is the life cycle from hell!

Environment

The disease is often most severe in areas and following years with extended, cool, moist conditions during late summer and early fall. Such conditions facilitate basidiospore production, dispersal and infection in pine needles. Hazard rating systems may be based in part on such weather patterns. Because of the delicacy of basidiospores and their need for good conditions, successful dispersal distances are generally about 300 meters and at most 3-4 kilometers.

Infections of pine are not consistent from year to year, but occur in “wave years,” when weather is ideal. For a perennial host, such infrequent infection is sufficient to cause high incidence.

Generally, conditions are more favorable for infection close to the ground because needles stay wet longer. Because trees have branches close to the ground when they are young, infections are more likely in young trees. Infections are also likely to be lethal in young trees because the needles are close the stem, so girdling is more likely, and girdling close to the ground is usually lethal.

In some areas, the moisture that facilitates basidiospore production, survival and infection is often from dew. Conditions in openings, particularly where cool, moist air may settle, are generally considered to be favorable to disease development. Maintaining a partial overstory over developing seedlings reduces dew formation and infection levels.

Disease Cycle

Let’s start with the infected seedlings that were first shipped to North America. They were already infected back in Europe, but there were probably no symptoms. The fungus would have been in the bark of the stem or branch. Eventually the infected area would be discolored and somewhat swollen.

In late summer or early fall, spermogonia appear near the margins of the canker. They produce spores called spermatia. These are like the spores produced by some of the foliage ascomycetes that you have probably learned about — they don’t infect, they are only involved in fertilization. Spermatia are produced in tiny drops of sweet liquid which attract insects. The insects carry the spermatia to other spermogonia. Spermatia fuse with receptive hyphae on the spermogonia. They establish the dikaryon (n+n). Time for a long winter nap –zzzzzzz–.

It’s springtime, and now the fungus is ready to rock and roll! Aecia appear about where the spermogonia were the year before. Aecia look like swollen white to yellow blisters covered by a membrane when young. The bright orange-yellow aeciospores are produced within, eventually pop the blister, and are released into the air.

The aecia break down and the bark dies. The fungus meanwhile has spread into living bark around the margin. It’s an obligate parasite (biotroph) and can’t survive on dead bark. Every year more aecia are produced in spring, then spermogonia farther out in late summer. It keeps spreading until the branch or stem is girdled and killed.

Airborne dispersal of aeciospores can be long-range, up to hundreds of kilometers. They may live for months under good conditions. Now comes the amazing part — these spores cannot infect pines, or anything else but Ribes (except see below). Ribes (gooseberry) is a genus of shrubs fairly common throughout the white pine areas. The new leaves are infected in spring.

Now mycelium grows in the Ribes leaves. Yellow-orange leafspots may appear, but they are often not conspicuous. Within 2 weeks, urediniospores are produced in uredinia on the undersides of leaves. They are orange.

The urediniospores are called the “repeating stage” because they reinfect Ribes, leading to production of more uredinia, in a cycle that could go on until the summer ends. Thus infection builds up on the Ribes. Although the urediniospores cannot infect pine, this ultimately means more basidiospores, which certainly can.

When the fungus realizes it is late summer to early fall, it begins to produce telia instead of uredinia. They are like orange-brown rough hairs, also on the underside. They are composed of rows of brick-like teliospores.

When conditions are cool and wet, each teliospore germinates in place to produce a basidium, which produces — can you guess? — basidiospores! The basidiospores are dispersed by air. They are small and quite short-lived, depending on conditions. It is generally considered that a few kilometers is about the upper limit for basidiospore dispersal.

Basidiospores can only infect pine. They enter through stomata into the needles. Within a month or so a small yellowish spot can be seen where infection occurred. The fungus grows down the needle into the bark, and the cycle is complete. Here is a summary:

Note several aspects of the disease cycle:

• Nothing overwinters on Ribes. The rust is perennial on pine only.
• Two of the “spore stages” don’t germinate to form a mycelium or infect anything, so might not even be considered spores in a narrow sense of the word. Can you figure out which they are?
• There can be no pine-to-pine spread. Further, the basidiospores that infect pine are very delicate, require certain conditions and can’t get far. It might not sound like it could build up much. If I’d never heard of rusts and someone described this as a hypothetical dissease cycle, I would say “It’ll never work. The pathogen will be extinct in a few years.” While we’re on the subject, how the heck does something like this evolve?

Symptoms

On pines, the first symptom may be a small, yellow or red spot on a needle, but this is difficult to find. Within a year or two, perennial cankers can be found on branches. These are usually elongate, may become somewhat swollen, and may have a yellow-orange margin in young shoots. Remnants of aecia and roughened bark may be visible. Cankers close to the stem may invade the stem. When a stem or branch is girdled (killed around the entire circumference) by the canker, it is killed beyond that point.

From a distance, symptoms seen are chlorotic, stunted, or dead branches (flagging) and dead tops.

On Ribes spp., yellowish leafspots may appear but these are often inconspicuous.

Distribution

Today, the disease occurs generally all around the northern hemisphere where hosts grow, except for a few areas that it has not yet reached or that are environmentally unfavorable. See ​[6]​ for a list of countries and sub-country regions where it is present.

The geographic origin of C. ribicola is uncertain, but most likely it is northeastern China, where there is a rust on Pinus koraiensis that is close to C. ribicola in Europe and North America ​[11, 20]​. The pathogen moved to Europe in the early days of plant movements. It was introduced to North America on seedlings of Pinus strobus (eastern white pine) from Germany about 1898 and on eastern white pine seedlings from France into Vancouver, BC in 1910. Why on earth, you might ask, were seedlings of a species from North America being grown in Europe and then shipped to America for planting? The United States had been cutting its forests rapaciously, and was just beginning to realize that it needed to focus more on forest management and reforestation. Because Europeans had long-established nurseries and knew how to produce seedlings, much of the early production was done there. Unfortunately, some of the seedlings were infected before being shipped back.

In the United States, the pathogen has only recently reached all the major regions with white pines. It was first found in New Mexico in 1990 ​[9]​, Colorado in 1998 ​[10]​, and Arizona in 2009 ​[7]​. Evidence suggests that the pathogen reached the Southwest (Arizona and New Mexico) not by moving down the Rocky Mountains, but by long-distance, aerial transport of aeciospores from California ​[8]​. To my knowledge, it has not been found in Mexico, although there are 5-needle pines there.

Impacts

This is one of the most important diseases in the history of forest pathology and, at least in North America, it continues to be a major focus for research and management. Because of the devastation it caused, it is one of the most famous forest diseases in the world. Today, it is surprisingly damaging even on native hosts in its native range ​[11, 20]​.

In Europe, Pinus strobus (eastern white pine) from North America had been widely grown for about 200 years, highly valued for its tall, straight stems. Discovery of the invasive rust in the first years of the 20th century virtually eliminated its cultivation ​[8]​.

In North America, white pine blister rust caused more damage and cost more to control than any other conifer disease ​[2]​. It destroyed many stands. Measures to control this disease constitute the most extensive forest disease control effort in time, money, men, and materiel in the history of US forestry ​[13]​. The majestic Pinus lambertiana (sugar pine) in California was highly susceptible. In its invasion of the southern Rocky Mountains, white pine blister rust has posed the greatest threat to limber pine. Extensive monitoring in the Rocky Mountains revealed 20% mortality from 2004 to 2017, mostly from blister rust and mountain pine beetle, apparently exacerbated by changing climate ​[5]​. The featured image at the top shows the typical appearance of such stands.

But the biggest tragedy was the loss of Pinus monticola (western white pine) as a major species. This beautiful, huge tree reached its greatest development in the Inland Empire (northern Idaho and adjacent parts of western Montana, eastern Washington, and southern British Columbia). It commanded the highest timber values in the region, was resistant to root diseases and decays that attack the species that have replaced it, and was easy to regenerate. The epidemic on western white pine was described as “the world’s most spectacular epiphytotic” ​[3]​. From being the primary species on over 5 million acres of the Inland Northwest and a major species on millions more, it was reduced to about 5 percent of its former importance ​[17]​.

Management

Many management approaches are available to combat white pine blister rust, but none is completely satisfactory.

Resistance. Programs are underway to select and/or breed for resistance to white pine blister rust in P. lambertiana, P. monticola and P. albicaulis ​[3, 19]​.

Ribes eradication. Pine can only be infected by basidiospores produced on Ribes plants. These spores are somewhat delicate and short-lived, so spores typically are not dispersed from Ribes to pine more than about 300 meters. For up to about 50 years in the middle of the 20^th century there were substantial programs in parts of the United States to eradicate Ribes species in areas where white pine growth was important. The project was military in its size, scope and organization ​[13]​. It probably succeeded somewhat in the East. In the West, however, the Ribes species proved too elusive, difficult to kill, and resilient, and the approach was abandoned.

Quarantine. In the past, especially in the Northeast, a major source of inoculum was from cultivated Ribes species. Many states have quarantines to prevent cultivation of such species. In some cases only the most susceptible cultivated species, Ribes nigrum, European black currant, is prohibited, and in some cases putatively resistant or immune varieties of R. nigrum are permitted. For instance, Maine law prohibits the planting and cultivation of currants and gooseberries in most of southern Maine, and prohibits the planting and cultivation of European black currants and their hybrids anywhere within the state. However, enforcement of such regulations is sometimes lax and there are increasing initiatives from growers to repeal or relax such regulation.

Transport of infected pines may spread the disease to uninfested areas. Unfortunately, white pines are becoming quite popular for landscape plantings in many parts of the West. In some cases, forests have rules prohibiting the transplanting of white pines from infested areas, and broader regulatory control over plant movement may be needed.

Hazard rating of sites. Sites likely to have good conditions for basidiospore production, dispersal and infection are high-hazard sites. Basidiospore dispersal distances tend to be longer in such sites, and conditions for infection are more frequent. These tend to be low-lying areas where cool air settles, although hazard ratings are usually unique for each geographic region. Once hazard rating is accomplished, management of white pine can be focussed on low-hazard sites.

Raising trees under understory. In some areas, a recommendation is to avoid regenerating white pines in small openings. Dew that forms on seedlings under open conditions is likely to persist in smaller openings, creating better conditions for basidiospore infection. Maintaining a partial overstory over developing seedlings reduces dew formation and infection levels.

Pruning. Branch infections are not too serious unless very abundant; stem infections are — they are often lethal. However, stem infections usually arise from branch infections. Pruning infected branches can prevent infections near the stem from growing into the stem, where they are likely to girdle and kill the tree. If the branch dies before the fungus reaches the next larger branch or stem, the fungus is done for. If it colonizes the stem, especially when it is small, the tree is done for.

Pruning uninfected trees can also be a benefit because it decreases the occurrence of new infections, especially on young trees. It is best to prune early, prune up to 50% of tree height from the ground, and repeat until pruning extends up to about 3 meters ​[17]​.

Young trees are in greatest danger. The infection court is needles and, because there is not much distance from the needles to the main stem when the tree is young, almost any infection is likely to reach the stem, where it is lethal. In older trees, top-killing can occur, which deforms the tree, and killing of branches can weaken the tree.

Other Issues

White pine blister rust is a premier example of an introduced pathogen. Pathogens evolve with their hosts to strike some kind of balance, especially obligate parasites. There is clearly selection for ability to infect and cause disease. But if they kill too many hosts, they are biting the hand that feeds them. So in natural systems these fungi tend not to completely destroy a population of their hosts.

When you bring a pathogen in from Asia to North America, the trees are similar enough to Asian white pines to become infected, but there is no sophisticated genetic resistance. The host has evolved no good mechanisms of resistance because there was never selection for them. So the disease may be more serious than similar, native diseases. That is an important concept.

Wildlife

Whitebark pine (Pinus albicaulis) seeds are an important high-quality food for grizzly bears where berries are not abundant (continental climates in the Middle Rocky Mountains) and the pine is reasonably abundant ​[1, 14]​. In most areas bears acquire the seeds by excavating squirrel food caches. Because pine seeds provide food and draw bears to high elevations, their availability tends to reduce human-bear conflict. During years with little use of pine seeds, human-bear conflicts and resulting bear mortality escalate dramatically in the area around Yellowstone National Park.

Pines with large, wingless seeds are often dependent on birds for dispersal, especially Clark’s nutcracker ​[18]​. Nutcrackers, in turn, often depend on the seeds as a food source. Most such pines are white pines. Birds cache the seeds for later use and often enough, don’t return for them. Caches are often kilometers from the seed source and in open areas that are good for seedling establishment. Pinus albicaulis is a primary food source and obligate mutualist of Clark’s nutcracker. In the southern Rocky Mountains, nutcrackers harvest seeds from P. flexilis, P. strobiformis, P. edulis, P. ponderosae, and P. aristata.

Telial Hosts Other Than Ribes

Rusts don’t read the books, so they don’t know how they’re supposed to behave. We used to think that the alternate (telial) hosts were always Ribes species, but no; turns out C. ribicola knows how to have its way with some completely unrelated plants ​[15, 16, 20]​. Pedicularis and Castilleja species seem to be the most common alternate, alternate hosts.

Eastern vs. Western North America

• The disease is widespread in the Northeast but generally not abundant or severe. It seems clear that disease incidence is much lower than it was in the decades following its invasion of the Northeast. For instance, disease incidence in New Hampshire ranged from 20 to 80% of trees around 1950, but in 1999 was just 0.3 to 7.2% by region ​[12]​. In New York in the early part of the 20th century, the disease caused mortality as high as 93%, certainly more than now ​[8]​. Possible explanations include:
  1. The initial wave of disease invasion provided strong selection for significant, existing resistance in populations of eastern white pine.
  2. At that time, substantial proportions of the white pine were in young age classes, when infection and mortality may be more likely. Today more eastern white pine stands in the area are mature.
  3. Ribes spp. may be less common today than earlier, because (a) forest developmental changes (increased cover and density) reduced Ribes populations, (b) the Ribes eradication program in the Northeast may have been more effective and with longer-lasting effects than in the West, and (c) quarantines against Ribes cultivation, which is generally not an issue in the West.
  4. Climate might explain low incidence in the Northeast. Which part of the life cycle is most sensitive to climatic conditions? Basidiospore dispersal and infection. When does it occur? Late summer and early fall. These tend to be times of fairly low humidity in those areas. Early fall is a pretty good time for humans, fair and sunny. There may be rain, but not long periods of cool moist conditions. Rain in and of itself is not that great because spores can’t disperse very far during rain. Foggy, wet conditions are good.
• In parts of the West, suitable conditions are more common. WPBR is definitely more of a problem there. In many areas, it puts the kibosh on management and sustainability of white pines, which are highly desirable and ecologically important species.