Biotic and abiotic factors affecting the dying back of - Forestry

Biotic and abiotic factors affectingthe dying back of pedunculate oakQuercus robur LJ. N. GIBBS AND B. J. W. GREIG

Forestry Commission Research Agency, Alice Holt Lodge, Wrecclesham, Farnham, Surrey, GU10 4LH,England

Summary

Episodes of dying back of pedunculate oak Quercus robur have occurred in Europe. In this arti-cle, produced to mark the 70th volume of Forestry, the 1920s episode, as described by contempo-rary research workers, is evaluated. The second part of the paper is concerned with an accountof the 1989—1994 episode in Great Britain and comparisons are made with occurrences elsewherein Europe. In Britain, one feature not previously recorded, was attack on declining trees by thebuprestid beetle, Agrilus pannonicus.

IntroductionIn contrast to many of the papers in the firstvolume of Forestry, the article by W. R. Day,then pathologist at the Imperial ForestryInstitute, Oxford, is on a very specific subject,'The oak mildew Microsphaera quercina(SchW.) Burrill and Armillaria mellea (Vahl)Quel. in relation to the dying back of oak'. Wehave chosen a more general title for our paperand it will fall into two parts. First, we will pro-vide some background to the situation Day wasdescribing, consider his evaluation of the prob-lem and place his views in the context of pre-sent-day concepts of tree pathology. Second, wewill outline more recent European experienceswith the 'dying back' of pedunculate oak(Quercus robur L.), with special reference to the1989—1994 occurrence in Britain. It may benoted that in this country, sessile oak Q. petraeaC Crown copyright, 1997

(Matt.) Liebl. has not suffered significant dam-age during this period, with the exception of thevery specific form of dieback that occurs in theForest of Wyre in the West Midlands (Gibbsand Wainhouse (1995)).

Oak dieback in the 1920s

Day based his article on two papers written inthe same year as his own (Osmaston, 1927;Robinson, 1927). Of these, the principalaccount is that provided by R. L. Robinson,although it contains no quantitative data. AsRobinson saw it, damage began with defolia-tion by the oak roller moth (Tortrix viridanaL.). This insect, he reported, was very abundantfrom the end of World War I up until 1924. 'In1923 and 1924, reports began to come in to the

Forestry, Vol. 70, No. 4, 1997

Dow

nloaded from https://academ

ic.oup.com/forestry/article-abstract/70/4/399/592958 by guest on 10 April 2019

400 FORESTRY

effect that the oak were dying in alarming num-bers in certain sections of the defoliated woodsand in due course extensive fellings had to bemade.' He also placed considerable emphasis onthe role of Microsphera alphitoides Grif. &Maubl. (the present name for M. quercina) incausing severe damage to the second crop ofleaves. He stated that the trouble reached itsworst in 1923, corresponding with the last inten-sive attacks of T. viridana, and that in 1925 and1926 many sickly oaks, which had been keptunder observation, showed a decided improve-ment. It may be noted that Robinson's com-ments on the abundance of oak roller moth inthe early 1920s and on its marked scarcity there-after are supported by the comments of Lucas(1927). He stated that, in the New Forest, therehad been a period of years in which it had beenextremely common, but that 'these had been fol-lowed by three sessions in which it has beenquite absent'.

Robinson commented that a very noticeablefeature of the dead trees was the development ofhoney fungus Armillaria mellea (Vahl.) Quel.and made reference to work in Slavonia(Yussifovitch, 1926), where it was suggested thatthis fungus delivered the final blow to treesweakened successively by defoliation andmildew. L. S. Osmaston took a similar line,arguing from his experience in the Forest ofDean.

In his review, Day painted on a much largercanvas than either of the other British authors.He described research on the biology of oakmildew in some detail and here it should benoted that, at that time, oak mildew had onlybeen known in the forests of Europe for some20 years (Woodward et al., 1929) and was thesubject of considerable anxiety. Day also drewheavily on research experience abroad, mostnotably on work conducted in Slavonia andGermany. He commented that most authorsagreed that several factors, acting together,caused the dying back and felt that the sequenceof the disease was best followed in the papers ofFalck (1918, 1923). Falck considered that itsfoundation lay in a physiological weakening ofthe tree through the action of defoliating cater-pillars or drought. The next stage was the infec-tion of the foliage by oak mildew andsometimes, attack on the stem by buprestid lar-

vae. The last stage, the death of the tree, was byno means inevitable, and was brought about bysecondary parasites including A. mellea, thehoney fungus.

Day was interested in the fact that the dyingback was principally a problem of pedunculateoak (Quercus robur) rather than sessile oak (Q.petraea), and attributed this principally to thegreater susceptibility of the former species tocaterpillar defoliation. He commented that anearly variety of Q. robur, which escaped theattention of the defoliating insects, might be ofuse in 'combating the present widespread dyingback'.

Despite the title of the paper, Armillaria fea-tures very little in the text. Day observed thatdifferences of opinion occurred between thosewho considered honey fungus to be one of themost dangerous factors involved and those whothought that its principal role was to kill offtrees that were already 'irretrievably damaged'.Day himself stated that since honey fungus didnot 'appear to be virulently parasitic on oakexcept under such circumstances as have beendescribed, this view is probably the correct one'.Here it should be mentioned that our under-standing of Armillaria has changed dramaticallysince Day's time, with the recognition that noless than seven European species can be identi-fied within A. mellea sensu lato (see Watling etal., 1991). Each has its own ecological andpathological characteristics and the one mostcommonly found in the broadleaved woods ofsouthern England is the weakly pathogenic A.gallica Marxmuller & Romagnesi (syn. A. bul-bosa) (Rishbeth, 1982). In the light of these find-ings, Day's comment seems very sound.

Day and the other scientists of his periodwere describing what would now be classified asa 'complex disease' or a 'dieback—decline' inwhich a number of factors, biotic and abiotic,interact to bring about dieback or death.Various 'models' have been developed todescribe the processes involved in such diseases,but perhaps the most satisfactory is that devisedby Houston (1992), on the basis of investiga-tions of several diseases of hardwoods in theeastern USA. In this model a series of stressevents progressively alters the tree so that even-tually it becomes vulnerable to 'organisms ofsecondary action'. These are insects, fungi etc.,

Dow



BIOTIC AND ABIOTIC FACTORS AFFECTING OAK DIEBACK 401

which are not capable of invading a healthy treebut which are very destructive to a weakenedone. In this context, it is important to recognizethat very different agents of stress can bringabout the same final symptoms. A good UKillustration is provided by beech bark disease,where the key agent of stress predisposing toinfection by the fungus Nectria, can either bedrought or heavy infestation by the beech scaleCryptococcus fagisuga Lind. (Lonsdale andWainhouse, 1987).

Oak dieback since 1927

Experience in Britain

After 1927, there were no more reports of oakdieback in the UK until 1958 when death ofyoung Q. robur occurred in several woods nearthe Norfolk coast. Adjacent Q. petraea wasunaffected. Young (1965) postulated that thedamage had been initiated by drought and expo-sure to unusually persistent northerly winds inJuly 1955. He attributed the continuing deterio-ration of these trees to the effects of defoliatinginsects and oak mildew in the following years.Files of the Forestry Commission DiseaseDiagnostic Service show that the next cases tobe reported were in oak plantations atChiddingfold, Surrey (1982), and in the Forest ofDean (1985). The damage at Chiddingfold waspreceded by several years of severe caterpillardefoliation and, in 1981, by exceptionally severemildew attack (Strouts et al., 1982). Honey fun-gus was involved in the death of many weak-ened trees. In the Forest of Dean, no apparentcause could be found for the dieback and deathof the trees. The two sites were inspected againin 1990 and although many long-dead trees wereencountered, the surviving trees were in goodcondition and it was determined that the periodof decline and death had lasted about 2-3 years.

From 1989 onwards, increasing numbers ofreports of dieback and decline in oak werereceived by the Forestry Commission ResearchStation and a new project to examine the prob-lem was initiated (Greig, 1992). The first symp-tom to be observed on a declining tree wasusually an overall deterioration of the foliage.The leaves, which were often smaller than nor-

mal, were pale green or yellow and might berather sparse. Over the next year or so, diebackof fine twigs might occur leading to death ofsmall branches, at which stage the foliage wasvery thin. Eventually, most of the large branchesmight die back so that only the trunk and a fewbranches remained alive. Many of the severelyaffected trees died (Figure 1) although othersmade good recovery growth from epicormicshoots (Figure 2).

Dieback of this type occurred throughout theMidlands and southern England (Figure 3). Onthe sites reported to us, the crops ranged from40 to 200 years of age. Approximately half werein woodland and half in parkland, and theyencompassed a range of soil types. The majoritywere Q. robur but a few were hybrids betweenQ. robur and Q. petraea. In 1990, five plots,

Figure I. Oak in the final stage of decline at TattonPark in Cheshire.

Dow



401 FORESTRY

Figure 2. Sherwood Forest oak with severe dieback,but also showing evidence of recovery.

each of c.80 oaks, were set up at dieback sites tomonitor changes in tree condition. Three percent of the trees were dead initially and this fig-ure had increased to 6 per cent by 1994. Theremaining trees showed some improvement overthe same period. Thus, the 380 trees which werestill alive in 1994 showed a mean of 6.7 per centdieback of the crown at that time, whereas in1990 those same trees had shown 13.1 per centdieback. An additional five plots were set up in1991 and these showed a similar process ofchange to the earlier plots. The picture is thusone in which a number of trees showed dieback,often severe. A proportion of these trees diedquite quickly, but the condition of the remain-der stabilized and remained little changed untilthe end of the study period.

Figure 3. Map of sites from which oak dieback wasreported during the 1989-1994 period. Open circlesdesignate sites at which plots were established tomonitor crown condition. These are clockwise fromthe north-west: 1. Tatton Park, Cheshire; 2.Sherwood Country Park and Fanny's Grove,Nottinghamshire; 3. Stixwold Wood, Horsington,Lincolnshire; 4. Scremby Park, Lincolnshire; 5.Emily's Wood, Thetford, Norfolk; 6. EverlandsEstate, Kent (2 plots); 7. Richmond Park, Surrey; 8.Crickley Hill, Gloucestershire. Cores for growth ringmeasurements were taken from all these sites exceptFanny's Grove and Emily's Wood. Trees were exca-vated for root investigation at sites 2, 5, 6, 7 and 8.

Some information is also available from theannual Forest Condition Survey for the period1987 to 1996, where the chief measure is crowndensity, i.e. the degree of transparency of thecrown. Data for up to 80 plots of oak distrib-uted throughout the UK show that there was amarked increase in the proportion of treesshowing poor foliage density from 1989 to 1992since when there has been some improvement(Redfern, Boswell and Proudfoot, 1997). Theseresults provide additional evidence for theepisodic nature of the problem, although it mustbe recognised that there is no simple relation-

Dow




ship between crown density and dieback of thetype described here.

Despite expectations to the contrary, enquiryrevealed no indication that significant defolia-tion by caterpillars had occurred on the affectedsites during the years just before the occurrenceof dieback. Nor was defoliation common in theplots during the years in which assessmentswere conducted. Oak mildew also was notsevere during much of the period—although itwas conspicuous in 1993. It seemed probablethat drought was a much more important factorin placing the trees under stress, for the sum-mers of both 1989 and 1990 were extremely dry(Jones and Hulme, 1993). Damage to trees waswidespread and, in some places, even oakshowed direct symptoms: the foliage on affectedbranches suddenly turning a bright red-brown(Gibbs, 1993). Using a Presler borer at 1.3 mfrom ground level, cores were taken from five toten healthy and affected trees at ten sites. Atsome sites no difference in ring widths could bedetected between the two samples, while at oth-ers the ring widths in the affected trees haddropped below those of the healthy trees inc.1989. At yet other sites, where the affectedtrees were at the point of death when the coreswere taken, it was found that the affected treeshad been growing less rapidly than their healthycounterparts for up to 20 years.

Root systems were examined by winching outfour or five severely affected trees at each of fivesites, these representing a broad geographicalrange. Root rot caused by the basidiomyceteCollybia fusipes was found in one tree.Otherwise, the roots were alive even at a latestage of decline. There was virtually no evidenceof Armillarij. Samples of fine roots tested forthe presence of Phytophthora species gave nega-tive results.

The presence of yellow leaves on many of theaffected trees suggested the possible involvementof a virus or related agent. However, whenshoot samples from healthy and affected treeswere examined by Dr Philip Jones, the virologistat Rothamsted Experimental Station, nothingconclusive was found.

One striking feature of the trees on many siteswas the presence of the buprestid beetle, Agriluspannonicus Piller &C Mitterpacher (syn. A.biguttatus Fabr.). This insect was found on 14

out of 20 sites, and at Sherwood was present onall 20 dead and 10 declining trees examined.Eggs are laid in the bark of declining trees andthe resulting larvae tunnel extensively throughthe bark, often to the extent of girdling thetrees. Early stages of attack by A. pannonicus ona tree that still possesses a residuum of vitalityare often marked by the presence of a dark exu-date on the bark surface (Figure 4). Although itis quite easy to overlook Agrilus galleries in adead tree, unless the bark is removed systemat-ically, there is little doubt that the recent obser-vations have shown the insect to be much morecommon in this country than it formerly was,and to have become a new component in theoak dieback story. In this context it is interest-ing that, as recently as 1987, A. pannonicus waslisted in the British Red Data Books as 'vulner-able' (Shirt, 1987), meaning that extinction wasbelieved likely if current pressures on it contin-ued to operate.

Recent work on dieback in pedunculate oakelsewhere in Europe

Oak dieback has also been the subject of majorconcern in mainland Europe, and there havebeen no fewer than four international confer-ences on the subject during the last decade—inHungary (1989), Poland (1990), Italy (1992) andFrance (1994). However, much of the work hasbeen focused on the plight of the oak species ofsouthern Europe and is thus of limited relevanceto the situation in the UK. For research onpedunculate oak, special attention should bedirected to Germany where serious diebackaffecting both Q. robur and Q. petraea began in1982-83, reached a peak in 1985-89 and subse-quently declined. Research conducted at over40 sites has been usefully summarized byHartmann and Blank (1993). The three findingsof greatest interest were: (1) growth ring studiesof healthy and diseased trees showed no signifi-cant difference before the onset of visible symp-toms; (2) the exceptionally cold winters of1985-87 had a major damaging effect with largeareas of bark being killed; (3) attack by A. pan-nonicus was very common and was consideredto be the most important factor leading to treedeath. In a linked study, Thomas and Blank(1996) produced some evidence that the frost

Dow



FORESTRY

Figure 4. Tarry spots associated with points of attackby Agrilus pannonicus on a declining oak atRichmond Park in Surrey.

sensitivity of the bark might have been increasedeither by prior insect defoliation or by highnitrogen inputs resulting from air pollution.

In France, the main recent episode of oakdieback occurred rather earlier—towards theend of the 1970s. Forests in several regions wereaffected but most notably in the Forest ofTroncais. The situation is well summarized byLandmann (1993), and by Levy et al. (1994).The first symptoms (thin crowns, stunted yel-lowish green leaves) were observed in 1978. In1979, trees flushed poorly, crowns remainedsparse and tree death began. Significant areas ofmature and young (80-100-year-old) trees hadto be logged. Although both Q. robur and Q.petraea were present, only the former specieswas affected and it was found that the problem

was worst on sites where temporary highgroundwater levels had prevented deep-rooting.It is considered that Q. robur would not natu-rally be found on such sites. Growth ring stud-ies of healthy and affected trees showed that thevery dry 1974 to 1976 period had provided theinitial stress, and it was concluded that variousbiotic agents of damage then became involved—most notably oak roller moth and mildew in thesummer of 1977. Continuing decline was due inpart to root invasion by Collybia fusrpes, a fun-gus which, before that time, had not been con-sidered to be an effective pathogen (Guillauminetal., 1983).

Conclusions

In 1927, Day stated that the dying back ofpedunculate oak was 'one of the most interest-ing pathological problems at the present time inEurope'. What can we say of it 70 years later?First, that the scientists of the 1920s were rightto recognize the way in which various damagingfactors combined to bring about the symptomsof dieback. Second, that while we recognize thecontinuing involvement of the factors identifiedthen, our views on the relative importance ofsome of them may have changed. An obviousexample here is drought. Droughts have been amajor feature of the last two decades and, if thecurrent climate change predictions are correct,may be just as important in the future—partic-ularly in the south and east of Britain. On thebiotic side a much more significant role is beingidentified for the buprestid A. pannonicus.

Among the factors not considered at all in the1920s was air pollution. While the extremeviews about the 'death of the forest', once cur-rent in parts of Europe, have now been laid torest (Skelly and Innes, 1994), the interactionbetween air pollutants and various biotic andabiotic agents of damage remains a live issue—as is made clear by the German work describedabove on nitrogen inputs and frost damage. Onthe biotic side there is increasing interest in fineroot death caused by previously unrecognizedPhytophthora species (Jung et al., 1996). At thetime of writing this subject is a key componentof a multi-country research application to theEuropean Union. No doubt there will be much

Dow




new information to evaluate when dying back ofoak comes up for consideration in the 141st vol-ume of Forestry]

Acknowledgements

This work is funded by the Forestry Authority. Wewould like to thank Dr D. Lonsdale for helpful sug-gestions on the manuscript.

References

Day, W.R. 1927 The oak mildew Microsphaeraquercina (Sch.W.) Burrill and ArmiUaria mellea(Vahl) Quel in relation to the dying back of oak.Forestry 1, 108-112.

Falck, R. 1918 Eichenerkrankung in der OberforstereiLodderitz und in Westfalcn. Zeitscbrift far Forstund Jagdwesen 50, 123-132.

Falck, R. 1923 Ober das Eichensterben imRegierungsbezirk Stralsund, nebst Beitrtlgen zurBiologie des Hallmaschs und Eichemmehtaus.Zeitsckrift far Forst und Jagdwesen 55, 298-317.

Gibbs, J.N. 1993 Impacts on forest and amenity trees.In Impacts of the Mild Winters and Hot Summers inthe United Kingdom in 1988-1990. M.G.R. Cannelland C.E.R. Pitcairn (eds). Department of theEnvironment, London, HMSO, 96-98.

Gibbs, J.N. and Wainhouse, D. 1995 Dieback of ses-sile oak in the Forest of Wyre. In Ecology,Management and History of the Wyre Forest. J.R.Packham and D.L. Harding (eds). University ofWolverhampton and the British Ecological Society,70-75.

Greig, B.J.W. 1992 Occurrence of decline and diebackof oak in Great Britain. Forestry CommissionResearch Information Note No 214, ForestryCommission, Edinburgh.

Guillaumin, J.J., Bernard, C., Delatour, C. andBelgrand, M. 1983 Le deperissement du chene aTroncais: pathologic racinaire. Rev. For. Fr. 35,415-424.

Hartman, G.R. and Blank, R. 1993. Etiology of oakdecline in northern Germany: History, symptoms,biotic and climatic predisposition, pathology. InRecent Advances in Studies on Oak Decline. N.Luisi, P. Lerario and A. Vannini (eds).Dipartimento di Patologia Vegetale, UniversitaDegli Studi, Bari, Italy, 277-284.

Houston, D.R. 1992 A host-stress-saprogen model forforest dieback-decline diseases. In Forest DeclineConcepts. P.D. Manion and D. Lachance (eds).APS Press, St Paul, Minnesota, 3-25.

Jones, P.D. and Hulme, M. 1993 Temperature and

sunshine duration. In Impacts of the Mild Wintersand Hot Summers in the United Kingdom in1988-1990. M.G.R. Cannell and C.E.R. Pitcairn,(eds). Department of the Environment, London,HMSO, 65-74.

Jung, T., Blaschke, H. and Neumann, P. 1996Isolation, identification and pathogenicity ofPhytophthora species from declining oak stands.Eur. ]. For. Pathol. 26, 253-272.

Landmann, G. 1993 Role of climate, stand dynamicsand past management in forest declines: a reviewof 10 years of field ecology in France. In ForestDecline in the Atlantic and Pacific Region. S. Huettland D. Mueller-Dombois (eds). Springer Verlag,Berlin, Heidelberg, 18-39.

Levy, G., Delatour, C. and Becker, M. 1994 Ledeperissement du Chfine des annees 1980 dans lecentre de la France, point de depart d'une meilleurecomprehension de l'equilibre et de la productivitede la Chenaie. Rev. For. Fr. 46, 495-503.

Lonsdale, D. and Wainhouse, D. 1987 Beech bark dis-ease. Forestry Commission Bulletin No 69, London,HMSO, 15pp.

Lucas, W.J. 1927 Tortrix viridana, L. TheEntomologist 60, 208.

Osmaston, L.S. 1927 Mortality among oak. Q. J. For.21, 28-30.

Rishbeth, J. 1982 Species of ArmiUaria in southernEngland. Plant Pathology 31, 9-17.

Robinson, R.L. 1927 Mortality among oak. Q. /. For.21, 25-27.

Shirt, D.B. (ed.) 1987 British Red Data Books: 2.Insects. Nature Conservancy Council, Peterborough,402pp.

Skelly, J.M. and Innes, J.L. 1994 Waldsterben in theforests of Central Europe and eastern NorthAmerica: fantasy or reality? Plant Dis. 78,1021-1032.

Strouts, R.G., Reffold, T.C. and Rose, D.R. 1982Advisory Services: Southern England and Wales. InReport on Forest Research 1982, ForestryCommission, HMSo, London, 27—28.

Thomas, F.M. and Blank, R. 1996 The effect ofexcess nitrogen and of insect defoliation on thefrost-hardiness of bark tissue of adult oaks. InEcology and Physiology of Oaks in a ChangingEnvironment. E. Dreyer and G. Aussenac (eds).Ann. Sci. For. 53, 395-406.

Watling, R., Kile, G.A. and Burdsall, H.H. Jr 1991Nomenclature, taxonomy and identification. InArmiUaria root disease. C.G. Shaw III and G.A.Kile (eds). Agriculture Handbook No 691, ForestService USDA, Washington D.C., 1-9.

Woodward, R.C., Waldie, J.S.L. and Steven, H.M.1929 Oak mildew and its control in forest nurs-eries. Forestry 3, 38—56.

Dow



406 FORESTRY

Young, C.W.T. 1965 Death of pedunculate oak and Yussifovitch, M. 1926 Le derissement du chene dansvariations in annual radial increments related to les forets de Slavonic, Yougoslavie. Revue des Eauxclimate. Forestry Commission Forest Record No et Forets, LXTV, 288-290.55. HMSO, London, 15pp.

Dow



Documents

Biotic and abiotic factors affecting the dying back of - Forestry