Science & Opinion

The rapid and often devastating of emergence of alien invasive pests and pathogens, assisted by international trade, is now happening at an unprecedented rate. But the spread of such species from : a familiar sight one continent to another is not entirely new, as the events of 1907–09 showed in the case of powdery mildew of oak. The mildew did not, however, prove to be with some hidden as damaging as various other disease- causing fungi that human beings have unintentionally transported to new shores. surprises Unlike the fungi that, for example, cause Dutch elm disease or blight of sweet chestnut, powdery mildew of oak has not Dr David Lonsdale wiped out entire tree populations.

After a few decades, oak mildew became A white, powdery covering of mildew Some experts of the day initially regarded as part of the regularly occurring on oak leaves is such a familiar sight attributed the new outbreak of oak assemblage of leaf-inhabiting fungi, insects that it could easily be dismissed as mildew to a mutation in one of the rare and other organisms, taking a share of a a normal occurrence across the UK or inconspicuous oak mildew fungi tree’s reserves and perhaps reducing its and the rest of temperate Europe. The that were already known in Europe. growth rate but not seriously harming its situation was, however, very different Their hypothesis was, however, general health. Although mildew has often until the early years of the last century. disproved by French mycologists E. been regarded as ‘just another’ disease of Until then, powdery mildew of oak was Griffon and A. Maublanc, who found oak foliage, early observers of the disease rarely noticed in Europe, being caused that the new form of mildew was in the UK expressed serious concern about by a few inconspicuous fungi and caused by a previously undescribed its effects, especially on seedlings and having apparently very little impact species, which they named coppice shoots, which were observed to on the health of affected trees. The Microsphaera alphitoides (now known become seriously stunted or distorted and mildew that we know all too well today as Erisyphe alphitoides). Evidently, this often to die. The impact of mildew on the was first observed in 1907, initially in had become newly established health of older trees was more difficult to France. By 1909, it was being seen all across Europe in a remarkably short assess but concern was expressed also over Europe and beyond. time. about this.

General view of oak foliage, including whitish mildew-covered leaves (D. Lonsdale)

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A lammas shoot of oak, showing a heavy covering of mildew. (D. Lonsdale)

After the ‘double’ droughts of 1975–76 and Alice Holt Research Station found that this conspicuous on the leaves of ‘lammas’ 1983–84, there were increasing signs of decline in diameter growth often dated shoots, which develop from a second and/ poor growth and, in some cases, crown back to the 1920s, not long after the trees or third flush of growth during the summer. dieback in oak trees across much of the concerned would have first been affected Mildew is, however, now observed on a UK. Eventually, the term ‘oak decline’ (now by the new form of powdery mildew. larger proportion of the foliage of affected called chronic oak decline to distinguish trees. Also, since the 1990s, E. alphitoides it from acute oak decline) was applied Other fungi were also suspected to be has shown a change in its life cycle. It to particular trees or tree populations playing a part in chronic oak decline, used to reproduce almost entirely by that were showing certain signs of crown such as honey fungus (Armillaria spp.) means of its asexual spores (conidia), dieback, usually with a long-term trend or the spindle-shank (Collybia fusipes). which make up the white covering on the of reduced expansion of stem diameter. Also, there was Phytophthora quercina, a oak leaves, together with the superficial Using increment cores, Brian Greig at fungus-like organism that kills a proportion mycelium. Nowadays, the fungus also of the fine roots of oak trees. The latter regularly forms its formerly rare sexual was unrecognised until 1999, when it was fruiting structures on oak leaves in discovered as a result of research on oak the autumn. These blackish spherical decline in continental Europe. But, as far structures, which can just be seen with as was known, these organisms had been the naked eye, are called chasmothecia living alongside oak trees long before the (previously described as cleistothecia onset of the decline that had apparently or perithecia). They persist on the fallen begun in the 1920s. There was therefore leaves into the following growing season, reason to believe that one or more further eventually releasing spores (ascospores), factors were involved in chronic oak which can colonise oak leaves during the decline, with suspicion being focussed summer. on pollution, changes in land use, climate change and the possible role of powdery Enthusiasm for ancient and other veteran mildew as a relative newcomer. trees was burgeoning at about the time that oak mildew seemed to start affecting Oak mildew has come under increasing large trees more extensively. Before attention during the present century, long, there were suspicions that mildew Surface of oak leaf, showing the superficial mycelium of partly because it often appears to affect might be adversely affecting veteran oak powdery mildew (scanning electron micrograph). (Image trees more conspicuously than before. trees, especially by heavily colonising Syngenta, courtesy of Martin Woolner) The mildew has always been particularly the new shoots that grow after such trees

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Close-up of mildew on oak leaves; the small, dark dots are immature sexual fruit bodies (chasmothecia). (Forestry Commission: Crown Copyright)

have been pruned with the intention of oak foliage. Research, mainly by Marie- The reason why E. quercicola may be preventing life-shortening mechanical Laure Desprez-Loustau, B. Marçais and adding to the severity of oak mildew is that failure. There was concern also about the their colleagues in France, has shown the two species tend to be at their most viability of new oak pollards, which were that the sexually produced spores of the active in different months of the growing being created in order to maintain long- fungus are released in summer, when season, at least in France, thus potentially term continuity of the habitat and other they can add significantly to the likelihood releasing large numbers of spores over values of veteran oak trees. These young of mildew becoming established on a longer period than would be the case if oak trees might have been expected to young, highly susceptible leaves. This only E. alphitoides were present. It is not tolerate pruning better than their veteran boosts the build-up of the fungus, which yet known for certain whether E. quercicola counterparts but there was concern about would otherwise initiate infection only on occurs in the UK, as well as in France, unexpected deaths amongst them after a small proportion of shoots that develop but this seems highly likely, given the very pollarding. from buds harbouring its overwintering rapid spread of the similar E. alphitoides mycelium. across Europe in 1907–09. Early in 2013, I was commissioned by the City of London (through the good offices Other research, also mainly by the same As mentioned above, it has been assumed of Drs Helen Read and Jeremy Dagley) to group in France, has revealed another for over a hundred years that E. alphitoides prepare a review of research on powdery possible reason for the apparent upsurge was accidentally introduced from another mildew of oak. This commission reflected in the severity of oak mildew. This is the continent into Europe. Before this the importance of old oak populations that presence of another species of Erisyphe, fungus was recognised as a previously are managed by the City at Epping Forest, known as Erisyphe quercicola. In the field, undescribed species by E. Griffon and Essex, together with others at Ashtead it looks the same as E. alphitoides, except A. Maublanc in 1912, it was initially mis- Common, Surrey and Burnham Beeches, that it has never been found to form sexual identified as a North American species, Buckinghamshire. With kind permission fruit bodies (chasmothecia) anywhere in Microsphaera quercina (now included in M. from the City, I also published a paper, Europe. These structures have, however, alni). The idea of a North American origin based on the resulting review, in the July been found in a subtropical region of was then perpetuated by the discovery of 2015 edition of the Arboricultural Journal. southern Japan, where the disease affects E. alphitoides in that continent but there is The rest of the present article covers the Ubame oak (Quercus phillyraeoides). The now general agreement that the latter was main findings of the research articles that I chasmothecia of the two mildews can introduced there, as in Europe. have cited. be differentiated under a microscope, as shown by S. Takamatsu and co-workers, The first inkling of the true origin of E. The research review indicated that, but the absence of chasmothecia of E. alphitoides came with an observation in by regularly producing its sexual fruit quercicola in Europe makes it necessary to New Zealand, where this mildew occurs bodies, Erisyphe alphitoides is now able use DNA-based methods to separate the on introduced species of European to colonise an increased proportion of species. oak. About thirty-five years ago, the

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mycologist H.J. Boesewinkel noticed that sp.) and several other hosts in various Such shoots often become prematurely microscopically identical mildews were plant families. defoliated in autumn and they sometimes growing on one of these oak trees and die back. As mentioned above, however, on a mango tree in a glasshouse. He With regard to the mango mildew observations in recent years indicate that suggested that the oak mildew and the becoming established on ‘new’ host mildew now often affects the crown of mango mildew were one and the same species, it is not clear whether it needs to trees more extensively than previously; fungus but the mildew on mango has adapt to such hosts in order to succeed as this is partly why I was commissioned to never been known to form sexual fruit it has done on various oak species. If so, review the literature with veteran oak trees bodies (chasmothecia) and it is therefore perhaps it was introduced into Europe long especially in mind. known only by a name based on its before it became conspicuous. Intriguingly, asexual form: . Many the mycologist F. von Thümen found a Even where mildew is not heavy enough years elapsed before H.J. Boesewinkel’s new species of mildew Oidium quercinum to cause distortion, stunting or death of suggestion was corroborated by the use of on Quercus racemosa in Portugal in oak shoots, it is likely to have significant DNA-based methods, again by the French 1877. Over fifty years later, there was a harmful effects on the tree as a whole, research group. suggestion that this fungus had been as shown by several research studies. imported from Portuguese colonies, Perhaps the most predictable effect is that It is remarkable not only that our now- long before the new form of oak mildew mildewed leaves have a reduced capacity familiar oak mildew E. alphitoides seems to emerged in 1907–09. Oidium quercinum to supply the tree with the products of have a tropical origin but also that it seems is, however, generally thought not to have photosynthesis. Most of the affected to have transferred to a very different family been the same as E. alphitoides. leaf tissue remains alive beneath the of plants. The same seems to be true of covering of mildew but its photosynthetic the ‘other’ oak mildew, E. quercicola, which As mentioned above, oak mildew has long efficiency is reduced. Also, some of the appears to be more or less identical with been known to have particularly severe photosynthetic output is appropriated by Oidium heveae, a tropical mildew which effects on seedlings and saplings. Their the fungus. affects rubber trees (). shoots continue to develop over a relatively Various European and North American long part of the growing season and thus Perhaps an even more serious effect oak species play host to E. alphitoides. remain highly susceptible to infection of oak mildew, especially in hot, dry Some of these have been ranked for their throughout the peak periods of mildew weather, is to allow uncontrolled water susceptibility (in descending order) as spore deposition. The resulting heavy loss by transpiration from the leaf surface. follows: Quercus robur> Q. petraea > colonisation by mildew leads to stunting, Healthy leaves are able to control their Q. cerris > Q. borealis > Q. ilex, with Q. distortion and sometimes death of the rate of transpiration to some extent rubra probably between Q. cerris and Q. affected shoots. On older trees, this kind of by the opening and closing of their borealis. The same fungus has also been damage is usually confined to shoots that stomata. Mildew bypasses this regulatory found on sweet chestnut (Castanea sativa), form during a final flush of late summer mechanism by the evaporation of water beech (Fagus sylvatica), horse chestnut growth or that develop in response to from the fungal mycelium. The resulting (Aesculus hippocastanum), a maple (Acer pruning, coppicing or insect defoliation. excessive water loss probably adds

Premature defoliation of oak shoots affected by mildew; this can be followed by dieback. (Forestry Commission: Crown Copyright)

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In most situations, the only reasonable means of mitigating the effects of oak mildew is probably to take extra care when managing veteran oak trees and their successors. The use of fungicides, although potentially very effective, is unlikely to be practicable (or perhaps legally permissible) except in tree nurseries. Tree shelters might also provide partial protection against infection but further research would be needed to show whether this is worthwhile. Another possibility that could be explored through research is to use natural control agents; these are mainly fungi that can parasitize oak mildew, thus suppressing the formation of its spores.

When experts try to assess the risks posed by alien pathogens and pests not yet present in the UK, one of the key risk- factors is the capacity of such organisms to damage trees (and other plants) that grow in our cool-temperate climate. It is therefore sobering to find that the familiar sight of mildewed oak leaves is the result of introducing a fungus that probably originated in the tropics on an unrelated plant species. It is also rather worrying to A veteran pollard oak with epicormic shoots; these sustain the longevity of the tree by replacing lost branches realise that oak mildew is probably more if they are not severely affected by mildew. Survival of the tree provides continuity of decaying wood habitat, damaging that we used to think. On the associated here with the fungus Laetiporus sulphureus (chicken-of-the-woods). (D. Lonsdale) other hand, it probably does not rank very highly alongside some of the ‘nasties’ that are waiting to hitch a lift here through significantly to the physiological stress that veteran tree or group of trees in a staged international trade. hot, dry weather can induce in the entire process known as ‘haloing’. In some tree. To make matters worse, oak leaves instances, this may need to be done become more readily colonised by mildew even more gradually, now that we know Acknowledgment as a result of strong exposure to ultraviolet that mildew can exacerbate the adverse light, as typically occurs in such weather. effects of sudden, unaccustomed The City of London is gratefully These findings may help to explain why increased exposure to strong sunlight. acknowledged for commissioning a a proportion of oak trees seem to have On the other hand, we can run into the literature review, which revealed much of entered into long-term decline following problem of failing to ‘halo’ or to prune the information included in the present drought years. With climate change enough to safeguard the veteran tree(s) article. leading to greater extremes of weather, the concerned. Furthermore, research has impact of oak mildew is likely to increase shown that mildew-induced reduction in David Lonsdale is a founder-member of the further. photosynthetic efficiency is especially Ancient Tree Forum, having worked for the severe under shady conditions. Thus, Veteran Tree Initiative in the 1990s. After In the management of veteran oak trees, the presence of mildew adds to the early retirement from Forest Research in mildew can be especially harmful to the ever-present difficulty of finding the 2002, he helped to represent the ATF on new growth that develops after such right balance between over-exposure the drafting panels of two British Standards trees are pruned in order to prevent and excessive shading when pruning or then under revision (BS 5837:2005 and BS life-shortening, structural failure. Mildew haloing veteran trees. 3998:2010), adding new guidance for the can similarly weaken or kill pre-existing care of veteran trees. He also accepted epicormic shoots, which represent a Mildew is an adverse factor in the the ATF’s invitation to compile and edit a veteran tree’s supply of potential new management not only of veteran multi-author book on the subject. Under branches that can develop in places where but also of their younger successors. the title Ancient and other Veteran Trees: old branches have been lost or removed. As mentioned above, mildew can Further Guidance on Management, this As well as directly damaging the shoots of harm the shoots of newly pollarded was eventually published in 2013 as a veteran oak trees, mildew can render entire young trees and it is also a threat to sequel to Helen Read’s Veteran Trees: trees more susceptible to drought-related the natural regeneration of oak. In the a Guide to Good Management (2000). stress, as mentioned above. latter situation, there is a particular need Since then, he has been involved in the to protect oak seedlings and saplings international VETree educational project. Another aspect of veteran tree from shading by other vegetation, since Also, with a background in tree disease management is the reduction of mildew impairs their shade-tolerance. research, David represents the ATF at excessive shade at sites where veterans This should, however, probably be done various plant health conferences and he is are very close to other trees. The shade- gradually, in order to mitigate the adverse a member of the ATF Working Group casting trees are felled or reduced effects of direct sunlight on mildew- on Pests and Diseases, among in height within a certain radius of a affected foliage. others.

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