Nachrichtenbl. Deut. Pflanzenschutzd., 58 (6), S. 141–147, 2006, ISSN 0027-7479. ©Eugen Ulmer KG, Stuttgart

Biologische Bundesanstalt für Land- und Forstwirtschaft, Institut für Pflanzenschutz im Forst1 ; Technische Universität Dresden, Institut für Forstbotanik und Forstzoologie2

New alder disease in Spreewald biosphere reserve – causes and incidental factorsofanepidemic

Neuartiges ErlensterbenimBiosphärenreservat Spreewald –Ursachen und Begleitfaktoren einer Epidemie

Jörg Schumacher1 ,Sindy Leonhard1 ,Britt Maria Grundmann2 ,Andreas Roloff2

Abstract Zusammenfassung Since the new Alder disease was established in the biosphere re- Seitdem im Jahre 1998 das neuartige ErlensterbenimBio- serve Spreewald in 1998, it has spread widely in this region. A sphärenreservat Spreewald erstmalig nachgewiesen wurde, hat research project was started in 2001 in order to develop measures die Krankheit bereits eine weite Verbreitung in der Region ge- that limit the further spread of the epidemic. funden. Im Rahmen eines Forschungsprojektes wird deshalb seit The average proportion of infected trees in the biosphere re- dem Jahr 2001 versucht, Maßnahmen zur Eingrenzung oder serve is 24 %in spring of 2004. Stand age and site caused a sig- Bekämpfung der Epidemie zu entwickeln. nificant variation in this proportion. Phytophthora alni appeared Erhebungen zufolge, beträgt der mittlere Anteil der infizierten to be the most frequent cause of the disease. On 20 %of the trees Bäume im Untersuchungsgebiet gegenwärtig 24 %, wobei al- infected by Phytophthora spp. additionally fruiting bodies of 10 ters- und gebietsbezogene Unterschiede bestehen. Als häufigster different white-rot fungi were found which accelerate the Verursacher der Erkrankung konnte Phytophthora alni nachge- progress of the disease or cause further damage to the trees. wiesen werden. Zusätzlich wurden an ca. 20 %der primär durch Due to continuous sampling statements about the seasonal ac- Phytophthora spp. erkrankten Bäume Pilzfruchtkörper von ins- tivity of P. alni can be derived. The development of the pathogens gesamt zehn verschiedenen Weißfäuleerregern festgestellt, die seems to come to ahalt during the winter months from Decem- zu einer Beschleunigung des Krankheitsprozesses beitragen oder ber to March. Therefore winter flooding does not lead to further nachhaltige Schäden bewirken. spread of the disease. In contrast high infection rates were found Aufgrund kontinuierlich erfolgter Probenahmen lassen sich in stands that were flooded during the growing season. Notable Aussagen über die jahreszeitliche Aktivität von P. alni ableiten. differences were also caused by stand establishment practises. Danach scheint die Entwicklung des Erregers während der frost- Alders planted on sufficiently high hills or banks were only reichen Monate Dezember bis März weitestgehend unterbunden rarely damaged. Afurther important factor is the frequency of zu sein. Winterliches Hochwasser führt deshalb nicht zu einem flooding. While single or episodic infections may be overcome Fortschreiten der Krankheit. Hohe Infektionsgrade ergeben sich by the tree, frequent or permanent contact with the infectious wa- insbesondere nach Überschwemmungen während der Vegeta- ter usually leads to an acute disease process and rapid dying of tionsperiodeinden Beständen und Uferabschnitten mit geringem the trees. Flurniveau. Die auf ausreichend hohen Rabatten oder Hügeln The high pH-values in the rivers of the forest provide gepflanzten Erlen weisen entweder keine oder nur vereinzelt favourable conditions for vegetative propagation and distribu- Schädigungen auf. Außerdem übt die Überflutungshäufigkeit ei- tion of the micro-organisms. Alaboratory experiment revealed nen hohen Einfluss auf die Pathogenese aus. Während einmalige that the sporangia are optimally produced within apH-range oder episodische Infektionen vom Wirt mitunter überwunden from 6 to 7. Beyond this, the formation of sporangia is particu- werden, führt periodischer oder permanenter Kontakt mit dem larly stimulated by the host-specific exudates of the fruits and the infektiösen Wasser meistens zu einem akuten Krankheitsverlauf bark, and to alesser extent by the fine roots. und zügigen Absterben der Bäume. Investigations into the susceptibility of the seeds to diseases Die hohen pH-Werte in den Fließgewässern des Spreewaldes have shown, that P. alni is able to infest germinal fruits at the sur- liefern günstige Voraussetzungen für die vegetative Fortpflan- face of the water.Hence, spreading of disease via the seeds is zung und Verbreitung von P. alni. Ein Laborversuch zeigte, dass possible in principle, survival of the pathogen outside the water die Sporangien in einem pH-Bereich zwischen 6 und 7optimal being restricted however. produziert wurden. Darüber hinaus wird die Sporangienbildung Asurvey regarding the distribution of P. alni was also con- insbesondere durch wirtsspezifische Exsudate der Früchte, ducted in alder nurseries. In 2003 five of the ten nurseries inves- Rinde und Feinwurzeln stimuliert. tigated were infested by different subspecies of the pathogen. As Untersuchungen zur Krankheitsempfänglichkeit des Saatgutes aconsequence special management strategies were introduced in ergaben, dass P. alni in der Lage ist, keimfähige Früchte an der . Wasseroberfläche zu infizieren. Eine Ausbreitung der Krankheit durch das Saatgut ist daher prinzipiell möglich, eine Überdaue- Key words: New alder disease, Phytophthora alni, Alnus gluti- rung des Erregers in den Früchten außerhalb des Wassers jedoch nosa, secondary white-rot fungi, infection dynamics, seed sus- eingeschränkt. Eine im Jahr 2003 durchgeführte Untersuchung in ceptibility, vector function, nursery investigation zehn Baumschulen zeigte, dass fünf dieser Betriebe mit unter-

Nachrichtenbl. Deut. Pflanzenschutzd. 58. 2006 142 J ÖRG S CHUMACHER et al., New alder disease in Spreewald biosphere reserve –causes and incidental factors of an epidemic schiedlichen Subspezies des Erregers verseucht waren. In Bran- 120 years in age were selected and 900 m² plots marked in these. denburg wurden daraufhin spezielle Vorbeugungs- und Bekämp- In these plots the percentage of diseased trees, extend of symp- fungsmaßnahmen eingeführt. toms, vigour,predisposition and secondary factors were recorded in spring (March/April) and in autumn (October/November). Stichwörter: Neuartiges Erlensterben, Phytophthora alni, Al- The spectrum of pathogens and their annual and environmen- nus glutinosa, sekundäre Weißfäulepilze, Infektionsdynamik, tal dynamics, respectively, were investigated by continuously Saatgutempfänglichkeit, Vektorfunktion, Baumschuluntersu- recording the rate of isolation of pathogens, pH of the water and chung the water level of the waterways. Pathogens in infected tissues (cambium, bark parenchyma) were isolated as described by S TREITO et al. (2002 b) and J UNG et al.(2004). In the rhizosphere 1Introduction of infected trees soil samples were taken and apple baits In 1993 anew Phytophthora diseaseofalder was discovered („Granny Smith“) placed for 8days. These were later analysed along riverbanks and in some young forest plantations in South- in the laboratory (cf. J UNG,1998; S CHUMACHER,2002). Juvenile ern Britain (GIBBS,1995; G IBBS et al., 1999). Since then it has leaves of oak (JUNG ,1998; J UNG et al., 2000 b) andalder beendetected in many other European countries (MATHIEU, seedlings were used as baits in soil. As amodification to this 1996; C ECH,1997; S CHMIDT et al.,1998and 1999; W ERRES, method freshly cut bark was used as well. The bark was cut from 1998; J UNG et al., 2000 a; S TREITO and G IBBS,2000; S ZABÓ et al., cleaned 2- to 3-year-old alder shoots in thin strips (c. 1–2 cm × 2000; S ANTINI et al., 2001; G IBBS et al., 2003).InGermany the 0,5 cm) using a scalpel. The bark baits were carefully placed onto disease was first diagnosed in 1994 (HARTMANN ,1995). The the surface of the water of flooded soil samples. Infected brown- cause is ahybrid Phytophthora, initially known as “the alder Phy- ish leaflets and bark pieces were plated onto selective PARPN- tophthora“, although sometimes also other Phytophthora spp. agar (V8-agar amended with 10 µg mL–1 pimaricin, 200 µg mL–1 have been isolated (BRASIER et al., 1995; W ERRES,1998; J UNG et ampicilin, 10 µg mL–1 rifampicin, 25 µg mL–1 pentachlorni- al., 2000 a; S CHUMACHER,2003 and J UNG andBLASCHKE,2004). trobenzene and 50 µg mL–1 nystatin) and incubated at 20 °C in Recently the pathogen was named Phytophthora alni with three the dark. After 24–48 h, hyphae were transferred onto V8-agar different subspecies (BRASIER et al., 2004). The typical symp- for identification. toms of the disease are bark necroses in the lower stem, increas- Since the alder Phytophthora does not form chlamydospores ing yellowing, crown transparency and small leaves as well as of- and the vigour of oospores is limited (DELCAN and B RASIER, ten an intensification of inflorescence and fructification (cf. 2001; J UNG andBLASCHKE,2003), it is likely that these micro-or- G IBBS,1995; H ARTMANN 1995; W ERRES,1998; J UNG et al., 2000 ganisms have alow potential to survive the winter in continental a; S CHUMACHER,2002). Europe. The sensitivity to low temperatures was tested with three Most records concern the species A. glutinosa,although A. in- isolates over a range of temperatures (0 to –15 °C) and frost du- cana (L.) M OENCH, A. viridis (CHAIX)DC ., and A. cordata D ESF. rations (3 and 30 d). may also be affected by alder Phytophthora.The new alder dis- In order to examine whether the pH continuously measured in ease is clearly distinct from the classical alder disease that oc- the waterways provides favourable conditions for vegetative curred in the first half of the 19th and at the beginning of the 20th propagation and spreading of the pathogen, the formation of spo- century and affected younger trees (five- to 20-year-old trees) ex- rangia within apH-range between 3.5 and 7.0 was tested with 15 clusively and was not attributable to biotic but to site factors different isolates of Phytophthora alni.Furthermore, the chemi- combined with wrong provenance (MÜNCH,1936 aand b; S CHU- cal-tactical effect of various organic substrates of alder on the MACHER,2002). production of sporangia was examined. Dried leaves, bark parti- In 1998 the disease was diagnosed for the first time in the bio- cles, fine root fragments or fruits were given in dishes that had sphere reserve Spreewald Forest (cf. W ERRES 2000; S CHU- been filled with aqua destillata and inoculated with P. alni.The MACHER,2003). number of sporangia was determined microscopically on acul- The Spreewald Forest is an inland delta located about 100 km ture substrate area of 11 mm² after experimental periods of 36 southeast of in which the rivers Malxe and form and 60 h. about 1575 km of mostly artificial waterways in an area that ex- Atraditional form of obtaining alder seeds in Spreewald For- tends 50 km from south to north. Since the downward gradient est is the water harvest, were the fruits fallen over the winter of the Pleistocene valley is small, the area has ahumid character, months are taken up by anet from the water surface and dried although the average annual precipitation is only 530 mm. Alnus thereafter at room temperature. To examine whether the alder glutinosa is the natural main tree species, stands occupying ap- seeds are susceptible to infections by P. alni or infected seeds re- proximately 2800 hectares, of which 2000 hectares occur in Up- main infectious after drying or freezing, samples were collected per Spreewald in the southeast and 800 hectares in Lower Spree- in Upper and Lower Spreewald Forests in 2001 to 2003. In one wald in the north of the area. experiment alder fruits derived from the water harvest were Because of frequent flooding, a special method of tree estab- cleaned in a qua destillata, dried with filter paper and placed im- lishment was developed in the mid-19th century,in which A. mediately onto selective culture substrates (PARPN-agar). In the glutinosa,often in rows, is planted on artificially raised hills or second experiment fruits both harvested in water and from tree banks alongside the waterways. This establishment, adapted to crowns were placed onto the surface of dishes that had been the local conditions, prevents damages caused by high water lev- flooded and inoculated with the pathogen. Twelve isolates of the els (BERGER,1866; M ÄRKISCHER F ORSTVEREIN,1902; H ILL, three different subspecies of P. alni as well as provenances 2002). Since 2001 the disease has been studied in the Spreewald (Bavaria, Brandenburg, Mecklenburg-Western Pommerania and in order to devise a strategy against this epidemic. Saxony) were used as inoculation strains. Following an infection period of one week apart of the seeds was directly transferred onto PARPN-agar and the other part was used for afactorial ex- 2Materials and methods periment. Treatments were strain (twelve), type of incubation To study the geographic extend and severity of the disease 15 rep- (water and dry), duration of incubation (1 d, 7dor 30 d) and tem- resentative sites with stands of different size ranging from 10 to perature of incubation (–15 °C, 5°C, 20 °C or 41 °C). At the end

Nachrichtenbl. Deut. Pflanzenschutzd. 58. 2006 J ÖRG S CHUMACHER et al., New alder disease in Spreewald biosphere reserve –causes and incidental factors of an epidemic 143

Fig. 1. Mean pro- 40 40 portion of the trees diseased with typical symp- LowerSpreewald Stands<50 years toms of the alder UpperSpreewald Stands>50 years 30 30 disease in the

] ] representative

[% [% plots (N =15). on on

20 20 oporti oporti Pr Pr

10 10

Spring 2002 Autumn2002 Spring2003 Autumn2003Spring 2004 Spring 2002 Autumn 2002 Spring 2003 Autumn 2003 Spring 2004 of each experimental series the seed material was prepared as de- Distinct differences are also obvious in Spreewald Forest scribed above and placed onto PARPN-agar.The micro-organ- due to the relief and stand establishment. Alder stands planted isms were determined. Moreover, the inoculated seeds were ex- on sufficiently high banks or hills were only rarely infected amined by light microscopy.Based on previous investigations (fig. 2). conducted in Bavaria (JUNG andBLASCHKE,2003), a survey of In addition to bark necroses and features of adecreased vi- the spread of P. alni in ten nurseries in Brandenburg was con- tality symptoms in young trees are premature and increased ducted. In each nursery 20 to 30 sample plants were taken from fructification. In the 10- to 15-year-old stands investigated the the seedling beds and flooded in big plastic troughs in the labo- proportion of fructifying trees with Phytophthora-infections ratory.The micro-organisms were isolated by means of the bait- was 87 %, whereas it was only about half (51 %) in the ing methods described. In addition, the tree nurseries were in- healthy trees (fig. 3). quired for information on provenances of the seed and planting Beyond this, in all sample stands of Spreewald Forest consid- material, past flooding by rivers as well as irrigation practises. erable proportions of diseased and declined trees have been found, the syndrome of which not completely corresponded to 3Results the symptoms of the new alder disease. Such trees often had sparse, small and yellowing leaves, which however did not cor- Spreading and degrees of infection relate with necrotic bark sections and exudates. As the causes of The average proportion of trees with infestation symptoms in the the loss in vitality of these black alders can be of various nature, plots was 14.9 %in spring of 2002 and 24.1 %in spring of 2004. their proportion was not quantified within the scope of the sur- The average mortality attributable to the disease by Phytoph- vey.JUNG et al.(2004) assume however, that symptoms restricted thora spp. was 4,3 %(1.4 %per year) during the study period. to crown features are due to infections by Phytophthora spp. in Thus, since the beginning of the survey the disease has increased the root system. by a total of 90.6 %(30.2 %per year). The area-related propor- tions vary between 0.0 %(2002) and 4.6 %(2004), respectively, Primaryand secondaryfactors of the disease and 33.3 %(2002) and 57.8 %(2004), respectively.As for the With one exception ( Phytophthora citricola) the pathogens iso- Upper Spreewald Forest an average of 16.8 %(2002) and 30 % lated from peripheral zones of necrotic sections of tissue (cam- (2004), respectively,and for the Lower Spreewald Forest 12.1 % bium, bark parenchyma) exclusively belong to the complex of P. (2002) and 26 %(2004), respectively, was infected. Differences alni.According to their morphology and physiology the isolates were found between old (> 50 years) and young (> 50 years) stands. The largest proportion of infested trees (16 %[2002] and 29 %[2004]) was encountered in the young stands, while among the older trees 13.2 %(2002) and 27.5 %(2004) were diseased (fig. 1).

infected noninfected

increasedwater level

normal water level 020406080100 relief Proportion of fructifying trees[%]

Fig. 2. Schematic diagramof the effects of increased water levels in Fig. 3. Relationship between the state of health and the degree of the waterways, given various heights of the banks. fructification.

Nachrichtenbl. Deut. Pflanzenschutzd. 58. 2006 144 J ÖRG S CHUMACHER et al., New alder disease in Spreewald biosphere reserve –causes and incidental factors of an epidemic

Tab. 1. Fungi-like micro-organisms (Division Oomycota,Fam. Pythiaceae) 1 identified in the substrates of examination

Medium of examination Soil material Rhizosphere Flowing Cambium, bark ex situ in situ waters in situ parenchyma

Phytophthoraalni B RASIER &S.A.KIRK –– –+++ Phytophthoracambivora (Petri) B UISMAN –+ –– Phytophthoracitricola S AWADA –– –+ Phytophthoragonapodyides (PETERSEN)BUISMAN ++ +++ +++ – Phytophthorapseudosyringae J UNG &DELATOUR –+ –– Pythium spp.++++++–

1 )–:without identification, +: individual identification or very low rate of isolation, ++: identification several times up to relativehigh rate of isola- tion, +++: steady identification or very high rate of isolation.

Tab. 2. Secondary-parasitic fungi occurring on the necrotised bark of diseased trees

Nr.Scientific Name Way of living Frequency1 Saprophyte Parasite

1 Bjerkanderaadusta (WILLD.: F R .) P. K ARST.+++ 2 Chondrostereum purpureum (FR .) P OUZ.++++ 3 Daedaleopsis confragosa (BOLT .: F R .) S CHROET.+(+) ++ 4 Inonotus radiatus (FR .) P. K ARST.+++++ 5 Panellus serotinus (SCHRAD.: F R .) K ÜHNER +(+) ++ 6 Pholiota aurivella (BATSCH:FR .) K UMM.+++ 7 Pleurotus ostreatus (JACQUIN:FR .) P. K UMM.+++ 8 Schizophyllum commune F R .: F R .+++ 9 Stereum hirsutum (WILLD.: F R .) S. F. G RAY ++ 10 Stereum rugosum (PERS.: F R .) F R .+++

1 +: individual or very low rate of identification, ++: several times up to relativehigh rate of identification, +++: steady or very high rate of identification. are very similar to the very virulent subspecies P. alni ssp. alni. thoras, in many cases, however,amore complex pathogenesis By contrast, abroad spectrum of fungi-like micro-organisms (Di- can be ascertained independent of stand age, which might com- vision Oomycota,Fam. Pythiaceae) was identified from the rhi- prise various wound and weak parasites. On 19.8 %of the trees zosphere of diseased trees as well as from waterways, using bait- primarily infested with Phytophthora spp. in 2003 fruiting bod- ing methods. In addition to numerous representatives of the ies of 10 different white rot fungi on the dying and dead bark genus Pythium,among them in particular Phytophthora go- parts have been found, among which Inonotus radiatus was the napodyides,occurred with very high constancy.Alder Phytoph- most constant and pathologically important (tab. 2). thoras could neither be isolated from soil nor from water.The baiting methods ( apple trap) failed also during alater infection Infection dynamics experiment in the laboratory (tab. 1). Continuous sampling demonstrated the intra-annual variation of Based on juvenile oak and alder leaves distinct differences be- the activity of the new phathogen in situ (cf. fig. 2). Thus, in the tween the baiting methods could not be found. However, the use frost-rich months from December to March the development of of living bark turned out as the most successful method for iso- P. alni seems to be largely suppressed. Despite diverse efforts lation of P. alni,although by this method also P. gonapodyides, isolates could not be obtained over this period. In anumber of P. citricola, P. cambivora and P. pseudosyringae sp. nov. were diseased trees, the necroses of which were still exuding in au- identified. This method might be an important alternative. tumn, the pathogen could no longer be isolated after the winter Though the new alder disease is primarily caused by fungi-like season and the lesions of the infection did not expand in the fur- micro-organisms and among them in particular alder Phytoph- ther course of the year.In spring pathogen activity started again

Fig. 4. Survival percentage of va- 100 Isolate1 100 Isolate2 rious isolates of 90 Isolate3 90 alder Phytoph- 80 80 thora after an in- cubation period

%] 70 %] 70 of three (left) and e[ 60 e[ 60 30 (right) days, rat rat

al 50 al 50 respectively,at iv iv

rv rv various tempera- 40 40 Su Su tures (30 inocula- 30 30 tions per experi- 20 20 ment). 10 10 0 0 -15-10 -5 0 -15-10 -5 0 Temperature[°C] Temperature[°C]

Nachrichtenbl. Deut. Pflanzenschutzd. 58. 2006 J ÖRG S CHUMACHER et al., New alder disease in Spreewald biosphere reserve –causes and incidental factors of an epidemic 145

13 600 12 gia abundant production

an 11 lowproduction 500 or 10 ] sp a 9 400 after36h ng 8 after60h angia mi phthor or

for 7 300 sp yto 6 tes of Ph la 5 200 er iso der 4 mb of [al 3 100 Nu er 2 1 0 Numb 0 3,5...5,5 66,5 7 Trockenlaub Aqua dest. Feinwurzeln Rinde Früchte pH range Medium Fig. 5. Formation of sporangia of the P. alni given different pH-values of the water ex situ. Provenances of the involved isolates [N =15]: Fig. 6. Production of sporangia of P. alni when using substrates with Bavaria, Brandenburg, Mecklenburg-WesternPommerania and Sax- different chemical-tactical effects after an experimental period of 36 ony. and 60 hours, respectively.

(verified in three growing seasons) and was restricted repeatedly was a significant interaction effect of substrates and duration of in May and June. Starting from July the pathogens could be iso- the experiment. lated continually with high rates until the inception of severe frosts at the end of the year. Susceptibility and vector function of the seed material The sensitivity of the pathogen to frost was confirmed in the From the alder fruits of the water harvest, which subsequent to laboratory experiment. At a temperature of –15 °C all isolates drying and surface purification were directly placed onto the sub- died within three days, at –5 °C all isolates died within 30 days. strates, fungi-like micro-organisms and acouple of fungal By contrast, 100 %of the isolates survived at a temperature of species emerged after several days. The following genera could 0°C yet after an experimental period of 30 days. Differences be- be identified: Phytophthora ( P. gonapodyides) ,Pythium, Sapro- tween the isolates became obvious at a temperature of –5 °C and legnia (Div. Oomycota), Fusarium, Cylindrocarpon, Cephalo- an incubation period of three days. While one isolate survived en- sporium s. l. and Verticillium (Div. Deuteromycota)as well as tirely,mortality of the two other isolates was 70 %and 97 %, re- various Z ygomycota being not referred to here in closer detail. P. spectively (fig. 4). alni were not detected. The pH of the waterways of the investigation area was between The inoculation of the alder fruits in the laboratory provided 7.1 und 8.2. P. alni seems to be adapted to these conditions, as an another result. All isolates of the P. alni were able to infect alder optimal production of sporangia was shown in the laboratory seeds from the water and tree harvests via zoospores. The ability within the pH-range between 6and 7. By contrast, within apH- of the P. alni to infect germinal alder fruits in water was shown range of 3.5 to 5.5 any formation of sporangia was absent (fig. by the light microscopic investigation (fig. 7). 5). The factorial experiment has shown, that the fruits after adry- The chemical-tactical effect of different organic substrates on ing in the air or deep-freezing are no longer infectious and that P. alni in the laboratory experiment varied widely.The presence the pathogens survive in water for few days only (tab. 3). of dried leaves in the water did not cause any formation of spo- rangia. In aqua destillata a slight formation of sporangia oc- Spreading in nurseries curred and by the addition of fine roots amoderate formation was The results confirm the findings regarding the spread of the ascertained. An increased production of sporangia was caused by pathogens in tree nurseries obtained in southern Germany (JUNG the addition of bark particles and germinal fruits (fig. 6). There and B LASCHKE, 2003).Infive (50 %) of the sites investigated P.

Tab. 3. Development and survival of the alder Phytophthora in alder fruits (water and tree harvest in Spreewald Forest) subsequent to infection with zoospores

Incubation conditions Period of experimentation (days) (temperature,1d 7d 30 d medium) Water Tree Water Tree Water Tree harvest harvest harvest harvest harvest harvest –15°C(Water) –15°C(Air) +5°C(Water) ++ + +5°C(Air) + 20 °C (Water) ++ + 20 °C (Air) +41°C(Water) +41°C(Air) +:positive results,–:negative results

Nachrichtenbl. Deut. Pflanzenschutzd. 58. 2006 146 J ÖRG S CHUMACHER et al., New alder disease in Spreewald biosphere reserve –causes and incidental factors of an epidemic

5

4 infected ries noninfected se 3

nur 2

1 igated

est 0 nv

fi 1 ro 2

Numbe 3

4 river water well-water

Fig. 7. Alder seeds infected by P. alni.Left: sporangia formation in wa- Fig. 8. Comparison of the diagnosis results according to the irrigation ter, right: oospores in the radicula. procedure (number of tree nurseries investigated: N=10). alni could be verified. In this context, in all tree nurseries with situ (DELCAN and B RASIER,2001; J UNG et al., 2004). Thus, the positive results the aggressive P. alni ssp. alni and at one site in inability to withstand harsh environmental conditions is shown addition the less virulent P. alni ssp. uniformis as well as P. cam- by an increased sensitivity to frost. Especially in younger trees bivora were isolated. with thin bark frost leads to acomplete inactivity or to death In four nurseries many three-year-old plants with disease of the microorganisms in host tissue. In April first isolations symptoms like exuding necroses and without current growth were obtained, as at this point of time on the one hand the en- rings could be found. In addition, in two of these nurseries large vironmental conditions (temperature, water availability) al- failure gaps were found in the transplant beds. In contrast, in the ready meet the demands of the pathogens, on the other hand tree nursery with the highest rate of infection and the broadest the defense capacity of the host trees is still weakly devel- pathogen spectrum no symptoms and conspicuous failures were oped. Contrary to this, the reduced activity of the pathogens in visible. However, the age of these plants was only two years. Fur- May and June might be caused by the foliation and inception thermore, acorrelation between the risk of infection and the use of stem and root growth (mobilizing of defense substances). of river water was apparent (fig. 8). Similar differences in the activity phases of P. alni were also described by S TREITO et al. (2002 b), although in Western Eu- rope generally milder winters prevail. 4Discussion Secondary parasites, which use the necrotic tissues as pre- When in 1998 the new alder disease was diagnosed in Spreewald ferred gateways into the weakened trees, can be of high impor- Forest for the first time, only few trees showed the typical symp- tance. The wood degradation caused by the fungi leads to an ad- toms. The results obtained since then reveal that the disease has ditional loss of physiological and mechanical stability.As a re- spread in the meantime and has infested the riparian, the land- sult of this the disease process is accelerated and a rapid loss of scape trees and the forest stands of Upper and Lower Spreewald. value occurs already on the standing tree (cf. S CHUMACHER et al., The widely ramified network of waterways and the high pH in 2001; S CHUMACHER,2004). the water provide optimum conditions for the spread of the As P. alni infects host trees at the root collar in the lower stem pathogen. Assuming the present proportion of infestationof section via lenticels in the bark or in the adventitious roots (JUNG 24 %and aconstant annual infection rate of 2 to 3%,about half und B LASCHKE,2004), the regulation of the water levels in Spree- of all black alders in Spreewald forest would be diseased or have wald Forest is particularly important. Flooding stands during the died within the next decade. In 1994 G IBBS et al. (1999) in south- growing season causes the highest risk of infection and spread of ern England and east Wales found 5.2 %diseased and dead trees. the epidemic. By contrast, flooding in winter is harmless. The Their proportion in the subsequent year was 6.0 %and in the highest degrees of infection correlate with periodic flooding, third year 7.9 %. In the riparian forest of Bavaria about 50 %of which in addition often leads to acute disease (cf. J UNG and all rivers as well as 50 %of the alder stands established over the B LASCHKE,2004). last 15 years showed typical disease symptoms (JUNG and The alder fruits floating in the waterways fulfillasimilar vec- B LASCHKE,2003). tor function in spreading of the disease like other organic parti- In young trees thefructification can be used as an indicator cles (e. g.: leaves, twigs or bark), provided that fruits able to ger- of infection. The main pathogen in Spreewald biosphere re- minate and favorable environmental conditions for the pathogen serve is P. alni (cf. G IBBS et al.,1999and 2004; C ECH,1997; are encountered. The reason why alder Phytophthoras were not J UNG et al., 2000; S TREITO et al., 2000 and 2002 a). Isolation found on seed material in situ is that the microorganisms are not of the pathogen from water using the apple trap has not been active in January and February when the fruits were harvested. successful, using other baits there was only alimited success Drying over 20 days at ca. 20 °C and subsequently freezing for (cf. S TREITO et al., 2002 b). By contrast, P. gonapodyides as a one week at –15 °C will kill pathogens in infected seed material. frequent representative of the genus Phytophthora has been The high proportion of infected nurseries considerably con- isolated from water (cf. S TREITO et al., 2002 b). That P. alni tributes to the spreading of the disease. When water from deep was not isolated in the rhizosphere might confirm that the wells instead of infectious water from rivers is used for irrigation oospores of the pathogen can not survive both in vitro and in and no infectious seeds from water harvests are used, there is no

Nachrichtenbl. Deut. Pflanzenschutzd. 58. 2006 J ÖRG S CHUMACHER et al., New alder disease in Spreewald biosphere reserve –causes and incidental factors of an epidemic 147 risk of infection. The longer the plants are grown in the tree nurs- J UNG,T., H. B LASCHKE,W.OSSWALD,2000 b: Involvement of soilborne eries the more probable it is that infections can be detected on the Phytophthora species in Central European oak decline and the effect of basis of the symptoms. Often, however, the infected plants are site factors on the disease. Plant Pathology 49, 706–718. J UNG,T., M. B LASCHKE, 2004: Phytophthora root andcollar rot of alders marketed, with the symptoms yet latent. in Bavaria: distribution, modes of spread and possible management Besides apartial change in tree species, the extension of the strategies. Plant Pathology 53,197–208. traditional planting on banks can limit the epidemic in the Spree- M ÄRKISCHER F ORSTVEREIN,1902: Führer zur Bereisung des Oberspree- waldes, Oberförsterei Lübben, seitens des Märkischen Forstvereins am wald Forest. 14. Juni 1902. Königliche Hofbuchdruckerei, Frankfurt a. M. M ATHIEU,D., 1996: Résultats de l’enquête „dépérissement de l’aulne“ de l’automne 1996. La santé des Forêts,Bilan. Acknowledgements M ÜNCH,E., 1936 a: Das Erlensterben.Forstw. Cbl. 58, 173–194. Our thanks are due to the Ministry of Agriculture, Environment M ÜNCH,E., 1936 b: Das Erlensterben.Forstw. Cbl. 58,230–248. S ANTINI,A., G. P. B ARZANTI,P.CAPRETTI,2001: Anew Phytophthora Protection and Spatial Planning in Brandenburgas well as to the root disease of alder in Italy.Plant disease 85, 560. Foundation Stiftung Wald in Not for funding the research project. S CHMIDT,O., M. B LASCHKE,M.FEEMERS,1998: Biotische Schädenan Moreover our gratitude goes to the staffof the forest service and Erle. LWFaktuell 14, 1–4. S CHMIDT,O., M. B LASCHKE,M.FEEMERS,1999: Waldschutzsituation the biosphere reserve in Spreewald Forest. We are indebted to Dr. 1998/99 in Bayern. Allgemeine Forstzeitschrift 54, 332–333. P. H EYDECK,Dr. T. J UNG andProf. Dr.WULF for their closeco- S CHUMACHER,J., P. H EYDECK,A.ROLOFF,2001: Lignicole Pilze an operationand helpful comments on the manuscript. Schwarz-Erle ( Alnus glutinosa [L.] G AERTN.) – welcheArten sind be- deutsame Fäuleerreger? Forstw.Cbl. 120,8–17. S CHUMACHER,J., 2002: Untersuchungen über den Gesundheitszustand References der Schwarz-Erle ( Alnus glutinosa [L.] G AERTN.) im Nationalpark Vor- pommersche Boddenlandschaft –Erhebung und Ursachenanalyse bio- B ERGER,R.I., 1866: Der Spreewald undseine Umgebung. . tischer Schadfaktoren. Ulmer Verlag, Stuttgart. B RAISIER,C.M., J. R OSE,J.N.GIBBS,1995: An unusual Phytophthora S CHUMACHER,J., 2003: Gegenwärtige Verbreitung, Ausbreitungs- und associated with widespread alder mortality in Britain. Plant Pathology Begrenzungsfaktoren der Phytophthora-Erkrankung an Erle im Spree- 44, 999–1007. wald. Forst und Holz 58, 251–255. B RASIER,C.M., S. A. K IRK,J.DELCAN,D.E.L.COOKE,T.JUNG,W.A. S CHUMACHER,J., 2004: Zur Verwendung des Begriffes „Fäule“ bei M AN I N ’ T V ELD, 2004: Phytophthora alni sp.nov.and its variants: des- Schwarz-Erle –Analyse wichtiger Termini und Grenzen der okularen ignation of emerging heteroploid hybrid pathogens spreading on Alnus Fäulediagnose. Allgemeine Forstzeitschrift 59, 66–68. trees. Mycological Research 108, 1172–1184. S TREITO ,J.C., J. N. G IBBS,2000: Alder Phytophthora in France and the C ECH,T.L., 1997: Phytophthora-Krankheit der Erle in Österreich. United Kingdom: Symptoms, isolation methods, distribution and dam- Forstschutz Aktuell 19/20, 14–16. age. In: Hansen, E. M., W. Sutton, 2000: Phytophthora Diseases of For- D ELCAN,J., C. M. B RASIER, 2001: Oospore viability and variationin est Trees. Forest Research Laboratory,Oregon State University Press: zoospore and hyphal Tipp derivatives of the hybrid alder Phytophthoras. 37–39. Forest Pathology 31, 65–83. S TREITO ,J.C., Ph. L EGRAND,F.TABARY ,G.JARNOUEN de V ILLARTAY , G IBBS,J.N., 1995: Phytophthora root diseaseofalder in Britain. EPPO 2002 a: Phytophthora disease of alder ( Alnus glutinosa)inFrance: in- Bull. 25, 661–664. vestigations between 1995 and 1999. Eur.J.For.Path. 32, 179–191. G IBBS,J.N., M. A. L IPSCOMBE,A.J.PEACE,1999: The impact of Phy- S TREITO ,J.C., G. J ARNOUEN DE V ILLARTAY ,F.TABARY ,2002 b: Methods tophthora disease on riparian populations of common alder ( Alnus gluti- for isolating the alder Phytophthora. Eur.J.For.Path. 32, 193–196. nosa)in southern Britain. Eur.J.For.Path. 29, 39–50. S ZABÓ,I., Z. N AGY,J.BAKONYI,T.ÉRSEK,2000: First report of Phy- G IBBS,J.N., C. VAN D IJK,J.F.WEBBER,2003: Phytophthora disease of tophthora root and collar rot of alder in Hungary.Plant Disease 84, 1251. alder in Europe. Edinburgh, UK: Forestry Commission Bulletin No. 126. W ERRES,S., 1998: Mikroorganismen aus der Gattung Phytophthora:Er- H ARTMANN ,G., 1995: Wurzelhalsfäule der Schwarzerle ( Alnus gluti- lensterben. AFZ/Der Wald 53, 548–549. nosa)–eine bisher unbekannte Pilzkrankheit durch Phytophthora cam- bivora.Forst und Holz 50,555–557. Accepted: 20th January 2006 H ILL,G., 2002: Entwicklung und Bedeutung der Forstwirtschaft im Spreewald. Forstarchiv 73,98–120. J UNG,T., 1998: Die Phytophthora-Erkrankung der europäischen Eichen- arten: wurzelzerstörende Pilze als Ursache des Eichensterbens. Diss. Contact address: Dr.JörgSchumacher,Federal Biological Research Univ.München. LINCOM. Centrefor Agricultureand Forestry,Institute for Plant Protection in J UNG,T., A. S CHLENZIG,M.BLASCHKE,B.ADOLF,W.OSSWALD, 2000 a: Forests, Messeweg 11/12, 38104 Braunschweig, Germany,E-Mail: Droht Bayerns Erlen eine Epidemie?LWF aktuell 24, 22–25. [email protected]

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