Powdery Mildew of Oak: a Familiar Sight with Some Hidden Surprises

Science & Opinion The rapid and often devastating Powdery mildew 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 oak: 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 fungus 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) 48 49 Science & Opinion 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 48 49 Science & Opinion 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 50 51 Science & Opinion mycologist H.J.

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