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The most important parasitic and saprophytic fungi in Austrian pine and Scots pine plantations in Serbia

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In Austrian pine plantations in Serbia, the greatest damage is caused by the fungi Mycosphaerella pini, Sphaeropsis sapinea, Cenangium ferruginosum, Germmeniella abietina (in the mountain regions) and occasionally Armillaria spp., Lophodermium spp. (seditiosum, conigenum, pinastri) and Cyclaneusma niveum. In Scots pine plantations, the greatest damage is caused by the fungi Heterobasidion annosum (especially in plantations on sandy soils), Armillaria spp, Lophodermium seditiosum, L. pinastri, Cyclaneusma minus and Sphaeropsis sapinea. Damage caused by rust fungi (Coleosporium sennecionis, Melampsora pinitorqua and Cronartium flaccidum) occurs less frequently. In mountainous regions in Scots pine plantations, great damage is caused by Phacidium infestans, Lophodermella sulcigena and Gremmeniella abietina.
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

THE MOST IMPORTANT PARASITIC AND SAPROPHYTIC
FUNGI IN AUSTRIAN PINE AND SCOTS PINE PLANTATIONS IN
SERBIA
Abstract:
  Mycosphaerella pini Sphaeropsis sapinea Cenangium ferruginosum
Germmeniella abietinaArmillaria
Lophodermium  seditiosum conigenum pinastri  Cyclaneusma niveum
Heterobasid-
ion annosumArmillariaLophoder-
mium seditiosumLpinastriCyclaneusma minus and Sphaeropsis sapinea-
Coleosporium sennecionisMelampsora pinitorqua and

Phacidium infestansLophodermella sulci-
gena and Gremmeniella abietina
Key words:
НАЈЗНАЧАЈНИЈЕ ПАРАЗИТСКЕ И САПРОФИТСКЕ ГЉИВЕ
У КУЛТУРАМА ЦРНОГ И БЕЛОГ БОРА У СРБИЈИ
Извод:
Mycosphaerella piniSphaeropsis sapineaCenangium ferruginosumGerm-
meniella abietinaArmillariaLophoder-
miumseditiosumconigenumpinastriCyclaneusma niveum
Heterobasidion annosum
ArmillariaLophodermium seditiosumLpinas-
tri Cyclaneusma minus and Sphaeropsis sapinea    Coleosporium
sennecionisMelampsora pinitorqua  
Phaci-
dium infestansLophodermella sulcigenaGremmeniella abietina
Кључне речи:

BIBLID: 





Austrian
pine and Scots pine plantations in Serbia


1. INTRODUCTION

-


-


-


Gremmeniella abietinaPhacidium infestans and Lophodermella sulcigena
-


Gabietina
Cenangium ferruginosumLophodermella sul-
cigenaLo-
phodermium
Pinus nigra
Mycosphaerella piniSphaeropsis sapineaCenangium ferrugi-
nosumGermmeniella abietinaArmillaria
LophodermiumseditiosumconigenumpinastriCyclaneusma niveum
Pinus sylvestrisHeteroba-
sidion annosumArmillariaLophodermium
seditiosumLpinastriCyclaneusma minus and Sphaeropsis sapinea
Coleosporium sennecionisMelampsora pinitorqua and 

Phacidium infestansLophodermella sulcigena and Gremmeniella abietina


2. MATERIAL AND METHODS




-



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 
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   
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

C-


C
-
-





    
    
et al et al et al 
 
3. RESULTS AND DISCUSSION

Table 1.
Табела 1.
Fungus species
Врста гљиве
Colonized part of plant
Колонизирани део биљке
Hosts
Домаћин
Signicance
Значајност
Alternaria alternate


 +
Anthostomella formosa
       

 +
Armillaria
(Amelle a sensu lato



+++
Aureobasidium pullulan s



 +


Table 1.
Табела 1.
Fungus species
Врста гљиве
Colonized part of plant
Колонизирани део биљке
Hosts
Домаћин
Signicance
Значајност
Botrytis cinerea 


+
Camarosporium pini   +
Cenangium acuu m
-





Cenangium ferruginosum
-



+++
Ceratocystis picea e




+
Cladosporium cladosporioide s



 +
Cladosporium herbaru m

  +++
Coleosporium tussilagini s

    -

 ++
Coniothyrium fuckelii


 +





++
Cyclaneusma minus

  ++
Cyclaneusma niveum



 
Cytospora pinastri
 



+
Dasyscyphus acuum



 +
Dasyscyphus pulverulentu s

  +
Dendrodochium pinastri   +
Epicoccum purpurascen s


 +
Fusarium   +
Gremmeniella abietin a




   Brunchor stia pi-
nea
    



+++


Table 1.
Табела 1.
Fungus species
Врста гљиве
Colonized part of plant
Колонизирани део биљке
Hosts
Домаћин
Signicance
Значајност
Hendersonia acicol a

-

 +
Heterobasidion annosu m

  +++


  +
Lophium mytilinum
     



+
Lophodermella sulcigen a

   

 ++
Lophodermium conigenu m


    



+
Lophodermium pinastr i

     
-




Lophodermium pin i -
excel sae
  +
Lophodermium seditiosum




++
Melampsora pinitorqua   ++
Microthyrium pinophyllu m

   



+
Mucor 


+
Mycosphaerella pin i

Dothistroma pini (=D
se ptospora    

      -
    
    -
     
    -
  Mycosphaerella pin i 



+++
Penicillium




+
Pestalotiopsis funere a




+
Pezizella chionea




+


Table 1.
Табела 1.
Fungus species
Врста гљиве
Colonized part of plant
Колонизирани део биљке
Hosts
Домаћин
Signicance
Значајност
Phacidium infestans
     
-
    
m
    
    



+++
Phacidium lacerum

-

 +
Phellinus pini

   -



+
Phomopsis
    
    
   Dothistroma
septospora
 ++
Phomopsis conorum   +
Rhizosphaera oudemansi i

  +
Rosellinia obliquat a

  +
Schizophyllum commune
    



+
Scoleconectria cucurbitul a

-



+
Sclerophoma pithyophil a

   
-
     



++
Sphaeridium candidum


 +
Sphaeropsis sapinea

-
    

-
     
     -
    



+++


  +


Table 1.
Табела 1.
Fungus species
Врста гљиве
Colonized part of plant
Колонизирани део биљке
Hosts
Домаћин
Signicance
Значајност
Stereum sanguinolentum





+
Therrya pini




 ++
Thyronectria balsamea

  ++
Trichoderma polysporu m

  +
Trichothecium roseum 


+
Truncatella hartigii

      



+
Tympanis hypopodia
     



+
Valsa pini   
Xylpohypha pinicola   +
Legend:



-





Mycosphaerella piniSphaeropsis sapineaGrem-
meniella abietinaCenangium ferruginosum and Armillaria
  Mycosphaerella pini    
Dothistroma septospora /=Dpini
Mpini
PinusLarix deciduas Pseudotsuga
menziesii Picea abiesPomorika 
Psitchensis  
Mycosphaerella-
Mycosphaerella
pini



MpiniPinus nigra
Pmugo
Mpini

Pmugo Mpini
mPsylvestris-
 
  
-

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tospora
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
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
Figure 1. Mycosphaerella piniPinus nigra

-
C
Слика 1. Mycosphaerella piniPinus nigra


C
D
E
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G
H

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Figure 2. Mycosphaerella pini
-

Слика 2. Mycosphaerella pini


D
E
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
 

Mycosphaerella piniPnigra
-






 
Sphaeropsis sapinea-


Pinus
Pinus radiataPnigraPsylvestrisPponderosaPresinosa
Ppinaster and PelliottiPinus
-
Ssapinea


Pinus jeffreyPpeuce and Pheldreichii
 
  



Pinus

Pinus

Ssapinea-
  
          



Ssapinea





-


SsapineaPinus-


m 
C
C




-
          
 et al  

Gremmeniella abietina


Gabietina-

 

 

Gabietina


Gremmeniella abietina
-
m
cm
Gabietina


GabietinaBrunchorstia
pinea-

-

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
Figure 3. Sphaeropsis sapinea

-


Слика 3. Sphaeropsis sapinea



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Figure 4.Gremmeniella abietina
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Слика 4.Gremmeniella abietina
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

               
-


           
Figure 5. Gremmeniella abietina
-

Слика 5. Gremmeniella abietina


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-




Cenangium ferruginosum       C
feruginosumPi-
nus

-

-
Cferruginosum






Cferruginosum

-
Cferruginosum
 et al
Cenangium ferruginosum








-


 et al





ArmillariaArmillaria mellea
 et al
  Armillaria      A gallica A cepistipes
AmelleaAostoyae and Atabescens
Armillaria-

Heterobasidion
annosum
Armillaria







Armillaria




-
 et al-
  


-
Lophodermium seditiosumLpinastriCyclaneusma (=Naemacyclus
niveusSclerophoma pithyophilaCenangium acuumCronar-
Spithyophila








Pinus sylvestris
Heterobasidion annosumArmillaria
Lophodermium seditiosumpinastriCyclaneusma minus and Sphaeropsis sapinea

164
   Coleosporium sennecionis Melampsora pinitorqua and
   -
      Phacidium infestans Lophodermella sulcigena and
Gremmeniella abietina
Heterobasidion annosum
-
Heter-
obasidionHannsumHparviporum
and Habietinum
-

Hannosus









Hannosum

-




Hannosum 

Peniophora gigantea

-
Phlebiop-
sis giganteaPhgiganteus



Phacidium infestans    







  
Lophodermella sulcigena
 -
Lsulcige-
na










C
C





Lophodermium seditiosum
-



Phellinus
piniColeosporium
Dothistroma pini
4. CONCLUSION
-

Mycosphaerella piniSphaeropsis sapineaGremmeniella abietinaCenangium
ferruginosum and ArmillariaAmellea sensu latoLophoder-
mium seditiosumCenangium accumCyclaneusma niveunScle-
rophoma pithyophilaPhomopsisThyronectria balsamea

166

-
-


    
Pinus sylvestrisHeterobasidion
annosumArmillariaLophodermium sedi-
tiosumLpinastriTherrya piniCyclaneusma minus and Sphaeropsis sapinea
Coleosporium sennecionisMelampsora pinitorqua and Cronartium

Phacidium infestansLophodermella sulcigena and Gremmeniella
abietina-
ColeopsporiumMycosphaerella piniThyronectria bal-
samea




REFERENCES
Larix decidua a new host for Dothistroma pini
Methods in Microbiology
Krankheiten der Wald- und Parkbäume

The Hypodermataceae of Conifers

A revision of the genera of the Hypodermataceae-

 Dothistroma pini on Pseudotsuga menziesii-

British Ascomycetes
 Microfungi on Land Plants


and Lecanosticta on Pines
  Honey Fungus-

  British Stem and Leaf-Fungi (Coelomycets)    

167

British Stem and Leaf-Fungi (Coelomycets)



Illustrated Genera of Ascomycetes-

Illustrated Genera of Ascomycetes-

-
       


kulturama crnog bora

Deliblatskom pesku
-
nus vrsta




           

Dothistroma Needle Blight in Yugoslavia

Picea omorika - a new host of Dothistroma septospora


crnog bora
Pojava i rasprostranjenje patogene gljive Lophodermella sulcigena u Ju-
goslaviji



Gremmeniella abietina - opasna patogena gljiva u sastojinama belog bora
na Kopaoniku
  
    

  
          

 Prilog poznavanju gljive Sphaeropsis sapinea Dyko et




       
Sphaeropsis sapinea u parkovima Beograda


   
in Serbia



    Molecular-based


   Dictionary of the FUNGI

-

Dothistroma pini an jungen Fichten (Picea abies)

 Dothistroma pini - Eine Gefahr Für Pinus sylvestris?-

   Mycologie et Pathologie Forestieres

 Pojava novih opasnih patogena u kulturama crnog i belog


 Delovanje nekih fungicida na klijanje reproduktivnih or-






-
tima





propadanja Pinus vrsta

 Occurrence of Sphaeropsis sapinea on the species of the
family Cupressaceae in Yugoslavia   
rd
 -


Lophodermium on pines
  Four species of Lophodermium on Pinus sylvestris



 Dothistroma blight of pines

 Diseases of Forest and Ornamental Trees-

Stump protection against Fomes annosus





НАЈЗНАЧАЈНИЈЕ ПАРАЗИТСКЕ И САПРОФИТСКЕ ГЉИВЕ У КУЛТУРАМА ЦРНОГ
И БЕЛОГ БОРА У СРБИЈИ
Резиме
       

 Pinus     
ha



      Cenangium ferruginosum  

         
  
Pi-
nus
             
Gremmeniella abietinaPhacidium infestansLophodermella
sulcigena 

Gabietina
Cenangium ferruginosumLo-
phodermella sulcigenaLophodermium
Pinus nigra



 Mycosphaerella pini Sphaeropsis sapinea Gremmeniella abietina Cenangium fer-
ruginosumArmillariaAmellea sensu lato
              
          
   Mycosphaerella piniDothistroma pini   


Sphaeropsis sapineaGrem-
meniella abietina

Armil-
laria

Armillaria



Lophodermium seditiosum
Cenangium accumCyclaneusma niveunSclerophoma pithyophilaPhomop-
sisThyronectria balsamea


Lophodermium seditiosum





            
         

Phel-
linus pini
Pinus sylvestris
Heterobasidion annosum
ArmillariaLophodermium seditio-
sumpinastriTherrya piniCyclaneusma minusSphaeropsis sapineaColeo-
sporium sennecionisMelampsora pinitorqua

Phacidium infestansLophoderme lla
sulcigenaGremmeniella abietinaPhacidium infestans


Lsulcigena

Gremmeniella abietina



Coleopsporium Mycosphaerella piniThyronectria bal-
samea

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... These are Phacidium infestans P. Karst., Lophodermella sulcigena (Link) Höhn., Gremmeniella abietina (Lagerb.) M. Morelet, that cause great damage to pine plantations in mountainous areas of Serbia (Karadžić, Milijašević, 2008), Mycosphaerella dearnessii M.E. Barr and Coleosporium tussilaginis (Pers.) ...
... L. sulcigena has been reported in Bulgaria (Dobreva et al., 2016), but there are no data on morphological and DNA analyses. In Serbia, it has been found to attack young, underdeveloped needles from the current growing season (Karadžić, Milijašević, 2008). Infection occurs at the base of the needle, with the part above the site of infection dying and changing color, becoming grayish or light brown, while the part below the site of infection remains green. ...
... According to Karadžić and Milijašević (2008), the symptoms of Lophodermella sulcigena can be confused with those caused by Lophodermium fungi. Lophodermium pinastri (Schrad.) ...
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In the summer of 2018, browning and drying of the needles on the dwarf pine ( Pinus mugo Turra) formations in the vicinity of the dam Belmeken (Rila Mt.) were found. The damages were concentrated mainly in the southern part of the plants and affect the young needles on the tops of the shoots. During the route survey conducted in 2019, almost complete recovery of the affected plants was observed. Symptoms of drying were found only on single bushes. Studies and laboratory analyses gave reason to conclude, that the drying was due to adverse weather conditions in the winter of 2017-2018, when there was significantly less than normal rainfall, and sudden temperature changes and extremes were found. Established in the dry needles, fungi of the genera Lophodermium , Hendersonia and Neofusicoccum can be characterized as weak parasites, manifested secondarily, or as endophytes, which under physiological stress due to changes in certain environmental factors can become latent pathogens, worsening the condition of dwarf pine.
... It was noticed relatively long ago that the most destructive of the Lophodermella species are those capable of completing their life cycles in one year, and L. sulcigena was included in this group [40]. L. sulcigena has so far been observed in Europe on two-needle pines: P. mugo, P. nigra, and Pinus sylvestris [41,44,[57][58][59][61][62][63][64][65]. In Poland, this is the first observation of this pathogen on P. mugo. ...
... The currently observed symptoms on P. mugo were generally very similar to those of L. sulcigena on other pine species [41,44,62,64]. However, it has now been observed that the infestation of needles by L. sulcigena was occasionally accompanied by an unusually high density of dark spots, which was not observed to such an extent in P. sylvestris needles [46,62]. ...
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Pinus mugo plays a significant ecological role in the natural environment at high altitudes in the mountains including the Alps, Pyrenees, Carpathians, and Balkans. In such severe conditions, it is subjected to the harmful effects of various abiotic and biotic factors. In one of the areas of its natural occurrence in Tatra Mts. (southern Poland), for the last few years, a significant intensification of needle disease has been observed. Symptoms similar to those recorded in Tatra Mts. also occur on other Pinus species in Europe and North America, where they are caused by fungi belonging to the genus Elytroderma, Lophodermella, Lophophacidium or Ploioderma (Rhytismataceae). The current paper presents the results of research which was mainly aimed at characterization of disease symptoms observed for the first time in Poland on P. mugo needles, and identification of the main causal agent with use of the morphological and molecular technique. Based on the analyses performed at different times of the year (2015–2020), it was found that dieback symptoms initially appeared only on first-year needles, a few weeks after their development. Symptoms occur on one or both needles in the bundle. The distal parts of the needles died, while the basal parts remained green. In the following year, mainly in June and July, on the previous year’s needles attached to the shoots, mature ascomata can be seen. The fungus Lophodermella sulcigena has been identified as the cause of these symptoms. So far, the related species L. conjuncta has not been found. The morphological features of the pathogen microstructure produced on P. mugo needles are presented. Attention was drawn to certain features that may make its identification difficult, especially in terms of shapes and sizes of ascospores. The phylogenetic position of the identified causal agent in relation to closely related other species was determined. The current results confirmed that L. sulcigena shows great phylogenetic similarity to L. montivaga, which is found in North America. Nine rDNA barcode sequences of L. sulcigena obtained in this work will enrich the NCBI GenBank database. The obtained results, indicating the presence of other fungi in L. sulcigena ascomata, which may limit the spread of its ascospores, were also discussed.
... Karadžić et al. [98] consider Cenangium ferruginosum as one of the most dangerous pathogenic fungi on pines. Pathogenicity tests conducted with mycelial plugs in summer confirmed that C. ferruginosum is not only a saprophyte but also a pathogen. ...
... Once infected and colonized by pathogens that cause bark necrosis in the crown, trees are severely stressed and may soon be attacked by secondary invaders, such as Ips acuminatus Gyll., Ips sexdentates Börn, Tomicus piniperda L., Tomicus minor Htg., and Buprestidae, or by other pathogens, such as Armillaria sp. or Ophiostoma sp. Cenangium ferruginosum is an important pathogen in some countries of Southern Europe [98,99]. In Central Europe, it used to be considered a saprophyte rather than a pathogen [100]. ...
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A 20-year study of a pine stand on post-agricultural land showed that woody debris in the form of organic matter can be successfully used to restore symbiotic mycorrhizal communities, as is the case with forest soils. Woody substrates restored organic matter in soils altered by long agricultural use and had a positive effect on the composition of mycobiota antagonistic to pathogens, especially to Heterobasidion annosum, the causal agent of the dangerous disease root and stump rot of many forest tree species, including stands of Pinus sylvestris (L.). In a study that started in 2001 in the forest district of Czarne Człuchowskie (northern Poland), the following organic materials were used: wood residues (W), sawdust (S), bark compost (B), and compost applied to the root zone during planting (G). The organic materials were spread in the form of mulch over the entire area during planting. After twenty years, it was found that the substrates used provided suitable growth conditions for mycobiome useful for pines. The addition of organic matter did not change the alpha biodiversity of the soil, but in the long term led to significant changes in the composition of mycobiota (beta biodiversity). The changes in the soil after the addition of organic material naturally accelerated the formation of the forest habitat. A number of fungi evolved that degraded added lignin and cellulose while being antagonists of H. annosum and other pine pathogens. In particular, the well-known hyperpathogens of the genus Trichoderma played an important role by promoting resistance of the soil environment to pathogens. Soil enrichment by bark compost and wood residues increased the relative abundance of Trichoderma more than fourfold.Mycorrhizal fungi became dominant in soil enriched with organic matter. After enriching the soil with bark compost, the relative abundance of Amphinema and Inocybe increased to 5%. The relative abundance of Russula in soil enriched with wood residues and sawdust increased to 9% and 5%, respectively. Mycorrhizal fungi, e.g., of the genus Amanita, Rusula, which formed root mycorrhizae, not only increased the root receiving area many times over, but also protected the roots (mechanically and chemically from pathogens). Altogether, the observed positive changes increase the chances that the first generation of pines will survive on the ground.
... Pine forests can be sporadically found at all altitudes. Although they are some published data about diversity of Agaricomycetes in Serbia (Čolić 1967, Karaman & al. 2005, Karadžić & Milijašević 2008, Lukić 2009, 2013Ivančević & Davidović 2011, Sadiković & al. 2012), a thorough and systematic investigation of this group of fungi is still lacking. Tricholoma is quite frequent in Serbia (Uzelac 2009), with basidiomes often appear in late October and November in thermophilous deciduous forests. ...
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A new species of Tricholoma recorded from a temperate forest in central Serbia is described and illustrated. It is characterized by the presence of punctate, often elevated, almost black spots arranged in one to three circular zones on the pileus. The new species showed morphological differences from closely related taxa and molecular phylogenetic analysis of ITS and LSU regions confirm the distinct taxonomic status of the finding.
... Mycosphaerella pini causes red band needle cast and needle shedding, causing the greatest damage to the pines of the northern hemisphere. According to Karadžić & Milijašević (2008), Pinus nigra plantations aged 5-25 years are particularly vulnerable in Serbia. This fungus has not been recorded at an altitude higher than 900m in Serbia. ...
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The paper presents research related to the harmful effects of snowfall in Austrian pine and Scots pine plantations in the western part of the Republic of Srpska. The most common types of tree damage are snow break and snowfall. The harmful effect of snow is more present in Scots pine plantations and at lower altitudes. Also, the harmful effect of snow is reflected in the reduction of the vitality of damaged trees, which become suitable for the attack of other harmful biotic factors, primarily harmful insects and fungi.
... Needlecast of pine trees is common in European forests. The causal pathogens include D. septosporum, D. pini, C. ferruginosum, and the recently introduced L. acicola [1,34,38,39,49]. Dothistroma septosporum occurs globally, whereas D. pini has been found in the USA and in more than ten European countries, such as France, Hungary, Ukraine, and Switzerland [17,30]. ...
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In recent years, the decline of pine stands in Europe, including Poland, has been caused by the emerging needle pathogen Dothistroma septosporum. Although this fungus appears to preferentially infect Pinus pini, P. pinaster or P. radiata in Southern Europe, it has been reported in stands of P. nigra, P. mugo and P. sylvestris from Southern Poland. Our preliminary tests of symptomatic needles of diseased pines, including black pine (P. nigra), showed the presence of both D. septosporum and D. pini-the latter as the first report in Poland. No other endophytic pathogen, i.e., Lecanosticta acicola or Cenangium ferruginosum, were found. More extensive molecular surveying based on β-tub2 amplification of DNA in needle samples from 72 seed trees of P. sylvestris in nine different Forest Districts of Southern Poland did not find the presence of D. septosporum. Our study revealed that the seed trees from which we collected propagation material were free from the pathogen, and its endophytic behavior was not confirmed in our testing. Consequently, these investigated trees of P. sylvestris should be suitable for seed collection and propagation, following the requirements of "good" phytosanitary quality as "pathogen-free" pine seeds used for reforestation .
... In the research of parasitic and saprophytic fungi in Austrian pine cultures in Serbia, Karadžić, D., Milijašević, T. (2008) found 41 species of fungi on Austrian pine, 45 species on Scots pine, while 24 species were found on both Austrian pine and Scots pine. Mycosphaerella pini, Sphaeropsis sapinea, Cenangium feruginosum, Gremmeniella abietina, and Armillaria spp cause the most extensive damage and dieback of Austrian pine trees. ...
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In the area of Stara Planina mountain, a multispectral survey of forest vegetation was performed. Data acquisition was done with unmanned aerial system DJI Phantom 4 Pro, equipped with integrated RGB 20Mpix sensor, and MicaSense RedEdge M, 5-channel narrowband multispectral sensor. Data was collected in the form of images, and 4 composite orthomosaics were produced-broadband visible RGB, narrowband visible RGB, and with vegetation indices applied NDVI and NDRE. RGB orthomosaic showed no significant changes in canopies apart from the variability of levels of green. Orthomosaics with vegetation indices applied showed changes in the level of physiological activities of leaves. NDVI map showed the negative changes of the top of the canopies, while NDRE map showed more dramatic changes within the canopy as well. Besides the map, 5 polygons with different NDRE values were selected and their respective spectral signature graphs were produced. The areas with the lowest NDRE values had the highest reflectance values in all wavelengths, while the absorption of light is much higher in physiologically active vegetation. Values of NDRE lower than 0.479 were inspected from the ground. This kind of ground-truth provided evidence that the areas coded in red were with lower physiological activity due to the infestation by beech leaf-mining weevil Orchestes fagi L. Another interesting finding was that both NDVI and NDRE values were higher in the areas not directly exposed to the sunlight. The areas shaded by surrounding canopies received only diffuse light but it showed a more positive ratio between absorbed and reflected wavelength which could be characteristic of the Fagus Sylvatica species. The findings in this study showed a strong correlation between low values NDRE vegetation index and negative changes deep within the canopy of high vegetation, which can serve as an indicator of pest infestation in forestry.
... In the research of parasitic and saprophytic fungi in Austrian pine cultures in Serbia, Karadžić, D., Milijašević, T. (2008) found 41 species of fungi on Austrian pine, 45 species on Scots pine, while 24 species were found on both Austrian pine and Scots pine. Mycosphaerella pini, Sphaeropsis sapinea, Cenangium feruginosum, Gremmeniella abietina, and Armillaria spp cause the most extensive damage and dieback of Austrian pine trees. ...
Article
Austrian pine is one of the species most often used for afforestation in our conditions. In the area of Avala, afforestation with Austrian and Scots pine began in 1899. The stands of Austrian pine located on the northern and northwestern foothills of the Avala Landscape of Outstanding Features are 115 years old, while the stands on the southern and southeastern side are about 65 years old. Two-year research in the area of Avala recorded the presence of 18 species of fungi on Austrian pine. Out of that number, 6 fungi were found on needles, 5 on needles and seeds, 2 on roots and stem bases, 1 on cones, 3 on trunks and branches and 1 species in vascular bundles. Of all the species, the greatest damage is caused by Sphaeropsis sapinea and species of the Armillaria genus.
... Fungal pathogens attacking secondarily thickened roots of trees are amongst the most destructive agents known in forestry. The genera with serious impacts in this category in Souteast European forestry are Heterobasidion and Armillaria (Woodward et al., 1998;Kile & Shaw, 1991;Fox, 2000;Karadžić & Milijašević 2008). Three species of Heterobasidion are present in Europe, and cause serious damage: H. annosum, H parviporum and H. abietinum, of which H. annosum is arguably the most aggressive species (Woodward et al., 1998;Asiegbu et al., 2005). ...
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The epidemic dieback of conifer forest, as the modern phenomenon, is present in the central part of the Republic of Serbia as well as in other countries of Southeastern Europe. Affected forest area increased in the period 2011-2014. It was most intense in forest stands dominated by spruce and silver fir, and about eight-fold less intense in Austrian and Scots pine. Change in climate conditions is supposed to be one of the main possible causes of coniferous forests dieback. The climate change initiated the increased activity of fungi Armillaria spp. and Heterobasidion annosum which led to the decay of individual trees and spreading in groups of trees. In pine and spruce monocultures afforested within the broadleaved habitats, massive dieback of trees was also a consequence of these two fungi. Spatial and temporal scales of insect outbreaks increase due to dry summers and mild winters in high elevations. In the last decade, in the coniferous plantation and natural forests in the central part of Serbia, intense outbreaks of bark beetles on spruce and silver fir were recorded. Spruce forests were heavily attacked by Ips typographus and Pityogenes chalcographus, and Austrian and Scots pine forests have been mostly affected by forest fires followed by outbreaks of Ips sexdentatus and other bark beetles. Insufficient silvicultural measures and inappropriate forest management in silver fir forests contribute to mistletoe infestations.
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Pinus peuce Griseb is five-needle pine native in high-altitude montane habitats of the Balkans. The aim was to assess the diversity and composition of fungal communities associated with the soil, rootlets and living needles of P. peuce at three high-altitude forest sites with different edaphic conditions and stand characteristics in southeastern Montenegro. In total, 90 needle, 90 rootlet and 90 soil samples were sampled. DNA amplification using ITS2 rDNA as a marker and high-throughput sequencing resulted in 17,620 high-quality reads, representing 825 fungal taxa. There were 52.5% Basidiomycota, 43.9% Ascomycota and 3.6% Mucoromycotina. There were 118 unique fungal taxa in the rootlets, 230 in the soil and 113 in the needles, with 8 taxa were shared. The most common fungi in rootlets were Rhizopogon mohelensis (11.0%), Suillus sibiricus (8.4%), R. fallax (6.9%), in the soil – Phlebiopsis gigantea (5.1%), Tylospora asterophora (2.9%), Sollicocossima terricola (2.7%), and in the needles – Dothideomycetes sp. 3360_7 (17.6%), Dothideomycetes sp. 3360_10 (10.7%), Leotiomycetes sp. 3360_16 (6.5%). The results showed that the functional tissues and the rhizosphere soil of P. peuce were inhabited by a high diversity of fungi, which were largely specific to each particular substrate, while. the site conditions had only limited effect on associated fungal communities. Associated fungal communities were largely determined by the host tree species, substrate properties and functional capabilities of associated fungi.
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Armillaria causes problems of root rot, kill trees and decay wood in the forests of Serbia and Montenegro, but the species involved have not hitherto been identified. The aim of this study was to identify field isolates collected on 25 localities. Identification was based on restriction fragment length polymorphism (RFLP) analysis of intergenic spacer 1 (IGS1) region and comparisons of IGS1 sequence with those available on NCBI database. Phylogenetic analysis was performed on sequence information from selected isolates to determine possible interrelationships between isolates with different banding patterns and previously identified tester isolates of five European Armillaria species. Five Armillaria species were identified in 90 isolates obtained from forests in Serbia and Montenegro. Armillaria gallica was most frequently isolated, followed by A. cepistipes, A. mellea, A. ostoyae and A. tabescens; two isolates remained unidentified. Restriction digestion of IGS1 amplification products with AluI produced 10 RFLP patterns. Patterns G4 (400, 250, 180) for A. gallica and pattern X (400, 180, 140) for isolates 74 and 79 are reported for the first time in European isolates. Eight RFLP patterns were observed after restriction with TaqI. Two patterns each were observed for A. ostoyae and A. gallica, and one each for A. cepistipes, A. mellea, A. tabescens and isolates 74 and 79. Parsimony analyses based on the IGS1 region placed the isolates into four clades: one including A. mellea, the second containing A. gallica–A. cepistipes isolates, while isolates of A. ostoyae and A. borealis were in the third clade. Armillaria tabescens differed from all annulate species. Phylogenetic analysis supported the conclusion that European Armillaria species are closely related and separated from a common ancestor in the near past. According to this survey five European Armillaria species are present in the forests of Serbia and Montenegro, while A. borealis is not present in the studied ecosystems. L'Armillaire cause des dégâts de pourriture racinaire, de mortalité et de dégradation du bois dans les forêts de Serbie et Montenegro, mais les espèces imliquées n'ont pas encore été indentifiées. L'objectif de cette étude est d'identifier les isolates récoltés dans 25 localitiés. L'identification est basée sur l'analyse RFLP de la région IGS1 et sur la comparaison des séquences IGS1 avec celles disponibles dans la base de données NCBI. Une analyse phylogénétique a été réalisée à partir des données de séquences de certains isolates pour déterminer les relations entre isolates présentant des profiles différents et des isolates testeurs précédemment identifiés de cinq espèces européennes d’Armillaria. Cinq espèces d’Armillaria ont été identifiées parmi les 90 isolats provenant des forêts de Serbie et Montenegro. Armillaria gallica a été la plus fréquemment isolée, suivie de A. cepistipes, A. mellea, A. ostoyae et A. tabascens; deux isolats n'ont pu être identifiés. La digestion-restriction des produits d'amplification de l'IGS1 avec AluI a produit dix profils RFLP differents. Le profil G4 (400, 250, 180) pour A. gallica et le profil X (400, 180, 140) pour les isolats 74 et 79 sont mentionnés pour la première fois pour des isolats européens. Huit profils RFLP ont été observés après restriction avec TaqI. Deux profiles ont été observés pour chacune des espèces A. ostoyae et A. gallica, et un seul profil par espèce pour A. cepistipes, A. mellea, A. tabascens et par isolate 74 et 79. Les analyses de parsimonie basées sur la région IGS1 ont placé les isolats dans quatre clades: un contenant A. mellea, un second contenant les isolates de A. gallica et A. cepistipes, tandis que les isolates de A. ostoyae et A. borealis sont groupés dans un troisième clade. A. tabescens diffère de toutes les autres espèces à anneau. L’ analyse phylogénétique conforte l'hypothèse que les espèces européennes d'Armillaria sont proches et se seraient séparées d'un ancêtre commun relativement récemment. D'après cette étude, cinq espèces européennes d'Armillaria sont présentes dans les forêts de Serbie et Montenegro, mais A. borealis n'est pas présente dans les écosystemes étudiés. Armillaria verursacht Wurzelfäule, tötet Bäume und zersetzt Holz in den Wäldern Serbiens und Montenegros, ohne dass die beteiligten Arten bisher bekannt waren. In der vorliegenden Untersuchung wurden Isolate von 25 Standorten bestimmt. Die Bestimmung basierte auf RFLP-Analysen der IGS1–Region und Vergleichen der IGS1–Sequenzen mit den in der NCBI- Datenbank vorhandenen Sequenzen. Mit Sequenzen ausgewählter Isolate wurde eine phylogenetische Analyse durchgeführt, um mögliche Beziehungen zwischen Isolaten mit unterschiedlichen Bandenmustern und zuvor bestimmten Vergleichsisolaten von fünf europäischen Armillaria-Arten zu erkennen. Insgesamt 90 Isolate aus Wäldern in Serbien und Montenegro wurden fünf Armillaria-Arten zugeordnet. Armillaria gallica war am häufigsten, gefolgt von A. cepistipes, A. mellea, A. ostoyae und A. tabescens. Zwei Isolate konnten nicht identifiziert werden. Die Verdauung der IGS1-Amplifikationsprodukte mit dem Restriktionsenzym AluI ergab zehn verschiedene RFLP-Muster. Die Muster G4 (400, 250, 180) für A. gallica und X (400, 180, 140) für die Isolate 74 und 79 wurden erstmals bei europäischen Isolaten nachgewiesen. Mit TaqI wurden acht RFLP-Muster erhalten, je zwei Muster für A. ostoyae und A. gallica und je eines für A. cepistipes, A. mellea, A. tabescens und die Isolate 74 und 79. Auf der IGS1-Region basierende Parsimonie-Analysen ordneten die Isolate vier Gruppen zu: eine enthielt A. mellea, die zweite A. gallica und A. cepistipes, eine dritte A. ostoyae und A. borealis. A. tabescens unterschied sich von allen beringten Arten. Die phylogenetische Analyse unterstützt die Hypothese, dass die europäischen Armillaria-Arten nah verwandt sind und sich in jüngerer Zeit aus einer gemeinsamen Vorgänger-Art separierten. In Serbien und Montenegro sind nach der vorliegenden Studie fünf Armillaria-Arten vorhanden, A. borealis wurde in den untersuchten Ökosystemen nicht gefunden.
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M. pini is one the most widespread and dangerous pathogenic fungi in the plantations of Pinus species in the world. This fungus has been observed on more than fifty Pinus species, and on European Larch, Douglas Fir, Norway Spruce, Serbian Spruce and Sitka Spruce. In Serbia, M. pini caused greatest damage in plantations of Austrian pine (P. nigra Arn). In Serbia both states of the fungus have been observed, i.e. conidiomata and ascostromata. Conidia are far more significant in the infection process. The critical period for infections is May - June. Of the all tested fungicides, the best results have been obtained by copper protectants. In heavily infected plantations of Austrian pine the protections should be carried out in the period when the plantations are 5-20(25) years old.
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Fungus G. abietina is one of the most dangerous pathogenic fungi inhabiting conifer plantations, and especially endangered species are the pines. Among the pines, the most susceptible species is Austrian pine, and endangered plantations are aged between 8 and 25 years. This fungus was detected in Serbia and Montenegro only on the mountains (Kopaonik, Vlasina, Goè, Durmitor). The fungus was identified on Austrian pine, Scots pine and spruce. In its development G. abietina forms both stages (anamorph and teleomorph). Its imperfect form i.e. pycnidial stage, is far more significant for the infection process, and mainly all infection is carried by conidia (=pycnospores). Infection of trees is possible throughout the year, but the critical period of infection is May-June. Conidia are transmitted by raindrops, and the infection is spread through the buds and bark of young shoots. Incubation period lasts for 9 months, i.e. if infection occurs in June of the current year, the first visible symptoms of infection occur in March of the following year. The symptoms of infection are visible at the base of buds (cross section), on the needles (initial orange discolouration at the base of the needles, and then the whole needle turns brown and drops) and on the bark of young shoots. Soon after infection symptoms, the fruiting bodies (i.e. pycnidia) appear on the necrotic tissues of the host. Apothecia form on the bark two years after tree dying. In the severely infested plantations, all dead trees should be felled and removed, and the remaining trees should be treated with copper fungicides. As this is a quarantine disease, care must be taken to prevent the spread of the disease to the new uninfected regions. This measure is imposed by the legal regulations on quarantine diseases.
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Sphaeropsis sapinea is a cosmopolitan fungus, identified in more than 50 countries of the world, on all continents, but it is primarily the species of warm lands. It is also a polyphagous fungus recorded from 11 coniferous genera. The most endangered and the most frequent host plants are Pinus species - it occurs on 48 pine species, among which the most susceptible are Pinus Radiata, P. nigra, P. sylvestris, P. ponderosa, P. resinosa, P. mugo, P. pinaster and P. elliotti. The greatest damage is caused on the introduced Pinus species and on those cultivated in artificial plantations, shelterbelts and in urban environments. In Yugoslavia S. sapinea is widely distributed both in the continental and in the Mediterranean parts. It was identified from ten pine species and six hosts from other coniferous genera. By the study in our country, the new hosts of this fungus were detected - Pinus jeffrey, P. peuce and P. heldreichii. The most endangered species in our country is Austrian pine, both in urban environments, and in plantations The symptoms of the disease are bud wilt, curling, stunting and necrosis of current year shoots and needles, dieback of top shoots, parts of crown or tree tops, branch and stem bark canker, root collar rot on the young plants in nurseries and their dying. This fungus also prevents seed germination of Pinus species and causes blue sap stain of the freshly cut wood, although sap stain was also observed on standing trees. More rarely it causes root rot and crown wilt of Pinus species. The main symptoms of infection, both of young plants and older trees, are the dieback of current year shoots S. sapinea can penetrate through buds, bark of young shoots and needles. The critical time of infection is the period from mid April to mid May. Then infection mainly penetrates through the bark of young shoots, which results in their dying. Infection through the needles occurs mainly at the time of their sudden growth or during summer months. The first visible symptoms of infection of the young shoots are in the form of brown necroses, resin bleeding and several short pairs of needles at the place. S. sapinea can infect male and female flowers, current year and second-year cones. The pycnidia with mature conidia can form on the shoots, needles, first-year and second-year cones during the year of infection. The first mature fructifications are mostly formed in the bark of young shoots, in the zone of infection, and they were recorded in late June at the earliest. They were recorded on the cones at the beginning of the third decade of July. Pycnidia are formed in the bark, on the needles and on the second-year and older cones, on male and female flowers, as well as on the cones in the first year of development. The size of S. sapinea conidia on different Pinus species is very variable throughout the world and ranges widely from 16.8-55.0×7.0-21.0 m. Our study shows that the size of pycnospores in our country is also variable and it ranges 14.8-51.4×9.7-20.2 m The optimal temperature for spore germination and germ tube growth is 27°C, and the optimal temperature for mycelial growth on the media PDA and MEA is 28°C. The formation of fruiting bodies in the culture is affected by light and the presence of sterilised needles on the mycelium The correct and timely control measures can contribute to reduce the consequences of this serious disease, by the combined application of silvicultural and chemical measures. Chemical control is recommended in the nurseries, severely infected plantations and in urban environments. The fungicides which showed the greatest efficiency are the preparations based on copper and Benomil.
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A Contribution to the Mycoflora of Pine Forests in the Netherland
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G r e m m e n J. (1959): A Contribution to the Mycoflora of Pine Forests in the Netherland, Nova Hedwigia I, 3+4 (251-288)
Illustrated Genera of Ascomycetes
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H a n l i n T.r. (1992): Illustrated Genera of Ascomycetes, APS Press, The American Phytopathological Society, St. Paul (1-263)