Cronartium pini in Sweden - an overview

The disease causes the greatest problems in younger forests, but it is one of the few pests that can attack pines of all ages.

Research on cronartium pini has been going on for a hundred years, but the current state of knowledge has not been comprehensively summarised until now. This has been addressed in a review article by Berit Samils and Jan Stenlid from the Department of Forest Mycology and Plant Pathology at SLU.

The Swedish name 'Törskate' means ‘dry top’ or ‘tar top’, and comes from the very characteristic appearance infested trees can get after very advanced infection. The upper part of the tree dies and, once the bark has fallen off, takes on a dry, ash-grey appearance. If enough green parts remain in the lower part of the tree, it can survive for decades with this appearance. The interface between the dead and living parts of the tree secretes a lot of resin, which is why the disease has sometimes also been referred to as tarry goad or just goad.

Stunted branches

But this is a late stage, and an effect of an infected tree living with the fungus for a very long time. The fungus attacks the needles of the annual shoots and then grows further down the shoot. Here, it attacks both the inner bark and the fluid-transporting xylem, spreading both inwards towards the trunk and outwards. If it manages to grow around the branch, like a girdle, water and nutrient transport is cut off and the branch above the girdle dies. The fungus continues towards the trunk at a rate of 2-6 centimetres per year, and once there it continues to spread upwards and downwards, and also around the trunk.

The dry tops are thus the result of an infection that has travelled from a shoot to the trunk, where it has cut off the upper parts of the tree. If the infection affects the top shoot, a new one is shot with a consequent impact on the value of the timber, but as long as the infection stays in the branches, the costs are moderate. The tree only dies when the trunk is affected, so the disease causes most problems on young trees because the fungus has a shorter route to the trunk and the tree has less time to reach a productive size. If the trunk is rough, it can take the fungus 10-50 years, or even longer, to grow around the whole tree.

A fungus that changes hosts

At the centre of the drama is a fungus, Cronartium pini. In its original form, C. pini is host-switching and needs two species to complete its life cycle. One is, of course, pine, and although it can attack several varieties, our Swedish P. sylvestris is the only relevant one in Sweden. Contorta pine is not attacked. A wide range of species have been identified as alternate hosts, but the most important are Melampyrum Sylvaticum in the north, Vincetoxicum hirundinariat in the south and peony wherever available.

The most iconic phase of the disease is the fruiting bodies that appear on the pines in June. These are a large number of bright orange-coloured blisters on the branches or trunk, often around a swelling in the bark. The blisters are full of bi-nucleate aecidial spores that infect the alternate host during June and July. On the alternate host, the fungus goes through a couple more spore stages before the nuclei fuse and new basidiospores, new genetic individuals, are formed.

The basidiospores leave the alternate host and infect new pine shoots in August or September. Up to a couple of years later, the sexual structures of the fungus are formed. Sexual mating probably takes place using insects as vectors and results in a bi-nucleate mycelium. After 2 to 6 years, new spore vesicles with bi-nucleate aecidial spores start to form, and the cycle is complete.

As the fungus grows through the bark in all directions from the entry point, spore vesicles form both “above” and “below” the wound, and as the infection progresses, the accumulations will move a few centimetres further apart each year. Normally, the branch is strangled and dies within a few years, and so does the infection, but if the tree is resistant, a single point of attack can generate new aecidial spores for many years or even decades.

C. pini is a parasite, a so-called biotroph, which needs living hosts to take its nutrients from. Unlike many other pests, the fungus is therefore more aggressive on large, fast-growing trees full of energy than on weak and diseased individuals. This is partly because there is simply more energy to steal in a healthy tree, but probably also because a large tree has more new annual shoots to land on. When the tree or branch dies, so does the fungus.

Mortality rates vary widely, but in one study of 30-year-old trees, an average lifespan of just over five years was recorded after the first damage was noted. The most resistant infected trees survived for thirteen years. How far from the trunk the damage occurs is an important factor, as is whether the branch manages to avoid girdling. The longer the branch survives, the further the fungus can continue its journey towards the trunk.

A sibling with a shortened life cycle

Thus, sexual mating takes place on the pine tree, and the spore stages then carry a nucleus from each parent, but meiosis itself takes place on the alternate host. However, this is not always the case. There is a variant of C. pini that completely skips both the alternate host plant and the sexual lifestyle. The aecidial spores spread directly to new pine shoots and infect them, forming new orange spore vesicles after a few years. Thus, all such infections are caused by clones of the same individual.

The asexual variant of C. pini is externally identical to the sexual variant and cannot be distinguished except by DNA technology. No consistent difference in virulence between them has been demonstrated, and both forms occur in both southern and northern Sweden. However, individual populations of both variants, from different parts of the country, may show varying degrees of aggressiveness.

Such populations are clearly localised and do not mix much with each other. Sexual variant populations have more interactions with greater gene flow between them, but single populations of both variants can hold an area for decades and create recurrent outbreak waves. The sexual variant populations are characterised by high genetic diversity, with each individual infection being its own genetically unique binuclear individual. The asexual variant populations, on the other hand, contain only a limited number of clones.

It was previously speculated that the sexual form was more likely to cause damage to lower branches, as the alternate hosts from which it spreads grow low and the basidiospores are less volatile and more short-lived than the aecidiospores. However, more recent studies have shown that although lower branches are more frequently infested, there is no clear link between the position of the lesion and the variant of C. pini, either at low or high height in the tree.

However, there is a detectable difference between the variants. As aecidial spores are mainly dispersed in June and early July and basidial spores in August and September, infections will take place at different times. If the same year offers a wide variation in weather conditions in early and late summer, the frequency of infestation of each variant will be affected accordingly.

Increasing infestation in northern Sweden

Increasingly severe outbreaks have been recorded in northern Sweden in recent decades, particularly in Norrbotten. As much as 60% or more of all trees in a younger stand may be affected, and in 2008 it was estimated that 130 000 hectares of forest in northern Sweden were severely affected by the disease. This is not news in itself. Already in the early 1900s, widespread problems with thorn blight were described in the north, but they have undoubtedly increased significantly in recent decades. Several possible causes have been discussed. Both temperature and annual precipitation have risen in Norrland over the last thirty years, which must have affected humidity, and all kinds of fungi favour high humidity in all parts of their life cycle. Spores become more numerous, they survive longer, they germinate faster and the fungi grow faster. Moreover, with increasing atmospheric carbon dioxide levels, forest pine is predicted to benefit, especially at higher altitudes where its range is expected to expand at the same time.

In addition, pine has increasingly been planted on land outside its natural habitat. So-called “spruce land”, i.e. moist, nutrient-rich soils, are the soils where Scots pine thrives best, and planting pines there naturally exposes them to higher infection pressure than on their drier natural soils.

In addition, we may have unwittingly bred more susceptible trees. Breeding efforts have centred exclusively on fast-growing pines, and the more vigorous, the more susceptible they are to biotrophic, parasitic pests.

Risk factors

Aecidial spores are ephemeral and can spread far, and the alternate host does not need to be close to the pine tree to be infected. However, the basidiospores that spread from the alternate host and infect new pines usually spread only a few hundred metres. Therefore, the risk of dry rot in a stand is reduced if there are no alternate hosts nearby.

In addition to the presence of alternate hosts, the risk of Eurasian watermilfoil increases with both altitude and latitude. The higher above sea level and the further north the stand is located, the greater the risk of Eurasian watermilfoil. This may have several reasons. Firstly, the temperature drops with both of these factors, leading to lower evaporation and higher humidity. Secondly, it reduces the amount of other vegetation and means that there are fewer physical obstacles to the spores actually landing on a pine tree. It also means that particularly large waves of infestation can occur in some years when weather conditions particularly favour the fungus. Conversely, the fungus does not thrive if temperatures exceed 25°C and during dry summers the availability of alternate hosts is also reduced. There are no detailed studies on how weather variations actually correlate with outbreaks of thrips, but the sensitivity to high temperatures during sensitive phases of the infection cycle makes it conceivable that thrips will become less common in southern Sweden in the coming decades.

Infections through needles are by far the most common route of attack for both the asexual and sexual variants, but bark damage can also be a gateway. At least this is the case for aecidial spores of the asexual variant. There is no research yet on whether the basidiospores can attack the trees this way, but it is likely that there is an increased risk of thorny spurge infections if a stand has a lot of bark damage.

For many diseases, the origin of the host trees is crucial. For example, pine trees with a southern provenance are more susceptible to powdery mildew and Gremmeniella. However, this does not seem to be the case for susceptibility to thorn blight. Individual provenances may show varying susceptibility, but it is not possible to draw any specific conclusions based on where in Sweden the trees come from. However, some studies suggest that P. sylvestris from Sweden, Finland and Russia are less susceptible to attack than other pine species of more southern origin. It is likely that P. sylvestris has a long history of coexistence with the Norway spruce and has developed greater resistance as a species.

Countermeasures

The most promising approach is linked to the heritability of resistance. Both susceptibility and resistance are highly heritable. Therefore, when natural regeneration is applied, it is crucial that the perpetual trees are not susceptible to infestation because the resulting offspring will also be. This is particularly important in seed orchards. By screening out all seed trees that prove to be susceptible to codling moth, the resistance of the material that is released into the trade and planted can be gradually strengthened. Selective thinning has already been carried out in some seed orchards in northern Sweden where reliable data on susceptibility to codling moth attack have been available.

The physical location of the stand is also linked to risk. The further north, the higher up, the wetter, the more nutrient-rich, and the more forest pine in the vicinity, the higher the risk of törskate. However, there is no detailed analysis yet of exactly how much separate factors contribute to the risk compared to each other.

The impact of alternate hosts makes it natural to try to eliminate them. This has been done successfully with many other alternate host pathogens, such as barberry (for black rust on wheat), aspen (for Dutch elm disease) and hedgerow (for spruce budworm near seed orchards). But it is not as easy to eradicate wood sorrel as barberry. Experiments have been carried out where the land was burnt before planting, but after only a few years, the cow parsnip returns, and several studies also show that it comes back in much greater numbers after burning.

There have also been experiments with thinning out all slow-growing trees and, at the same time, all those with thornbush infestations on their trunks, as well as pruning infested branches. This has proved to have little effect on the condition of the stand a few years later. It is difficult to find all infestations by visual inspection, air circulation increases in the more open stand and facilitates spore dispersal from ground level, and the fast-growing trees that were saved may be more susceptible than those that were removed.

However, trunk pruning has been shown to be effective in related rust infestations in North America. The idea is to remove all branches part way up the trunk, as it is the low branches that are most often attacked. In a study on Cronartium ribicola on Pinus monticola in the USA, mortality from the disease over the next 30 years was reduced by 50%. It is quite possible that this is a viable way to reduce pine shoot blight in Sweden as well, but there are no studies to support this yet.

The research forefront today

Stem budding is one example of an area where the research forefront needs to be moved forward. Another is to get a clearer idea of the dispersal potential and survivability of basidiospores. How far from the source can they infect new trees?

Apart from the fact that resistance is genetically determined, nothing is known about the nature of this genetics, for example whether resistance is controlled by a few genes or many. From a breeding perspective, it is desirable to have several genes contributing small parts rather than a single gene accounting for everything, as it is much easier for the pest to evolve to bypass a single resistance gene than a whole battery.

Finally, it is also unclear exactly what the relationship between the asexual and sexual variants is. One might have arisen from the other, but is this a shift that occurs regularly, and if so, why and how often? Can it go both ways? Are there differences between the species that would facilitate faster identification?

Research within SLU's Forest Pest Centre is currently underway on several of these fronts.