The incidence and distribution of white mistletoe (Viscum album ssp. abietis) on Silver fir (Abies alba Mill.) stands from Eastern Carpathians

Abstract

In Romania Viscum album ssp. abietis is one of the most significantbiotic factors that affect Silver fir situated on Eastern border of its natural area. The aim of our research is to assess the incidence and distribution of mistletoe in representative Silver fir stands from the Eastern Carpathians (at four forest districts level - Gura Humorului, Vaduri, Mănăstirea Caşin and Agăş). According with this purpose a statistical inventory of Silver fir stands based on 2 x 2 km grid was performed. At the intersection of the gridlines,stands older than 70 years were searched for on a distance of 500 m around. Each Silver fir stand chosen in this way represents a sample plot. In each plot 30 dominant Silver fir trees were chosen. For all this trees, the mistletoe infection degree was quantified using a 4-class rating system: no infection,low infection, moderate infection and heavy infection. The incidence of Silver fir was presented according to the damage degree. The site and stand parameters - elevation, exposure and canopy closure - were analysed to establishwhether correlation between these parameters and mistletoe incidenceexists. The volume of dead trees (due to the mistletoe infection) in 2004 - 2007 was also compared with mistletoe incidence in order to establish the correlation between these variables. Silver fir trees infected by mistletoe have been found in 55% of all 86 sample plots. Within the studied area 22% out of 2147 Silver fir trees were infected by mistletoe (42.2% - 1st infection class, 32.7% - 2nd class and 25.1% - 3rd class). The highest percentage of infected trees was found in the forest district Mănăstirea Caşin where 42% of examinedtrees were infected, mostly of the trees being in the 2nd and 3rd infection classes. There was a significant negative correlation between the elevation and mistletoe incidence. Up to 600 m, the most of the trees are heavily infected, while above 800 m the trees are incipiently infected. Regarding the canopy closure, sample plots with understocked and sparsely closed stands have shown a high level of infection compared with plots with closed stands.A significant correlation has been found between the volume of dead Silver fir tees and mistletoe incidence. The highest mistletoe infection was registrated in Silver fir stands at the eastern border of the Eastern Carpathians. There was noticed a decrease of mistletoe infection from the East to the West.

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© ICAS 2010
Ann. For. Res. 53(1): 27-36, 2010
ANNALS OF FORESTANNALS OF FOREST RESEARCH
www.e-afr.org
RESEARCH
The incidence and distribution of white mistletoe
(Viscum album ssp. abietis) on Silver fir (Abies alba
Mill.) stands from Eastern Carpathians
C. Barbu
Abstract. In Romania Viscum album ssp. abietis is one of the most signifi-
cant biotic factors that affect Silver fir situated on Eastern border of its natu-
ral area. The aim of our research is to assess the incidence and distribution of
mistletoe in representative Silver fir stands from the Eastern Carpathians (at
four forest districts level - Gura Humorului, Vaduri, Mănăstirea Caşin and
Agăş). According with this purpose a statistical inventory of Silver fir stands
based on 2 x 2 km grid was performed. At the intersection of the gridlines,
stands older than 70 years were searched for on a distance of 500 m around.
Each Silver fir stand chosen in this way represents a sample plot. In each plot
30 dominant Silver fir trees were chosen. For all this trees, the mistletoe
infection degree was quantified using a 4-class rating system: no infection,
low infection, moderate infection and heavy infection. The incidence of
Silver fir was presented according to the damage degree. The site and stand
parameters - elevation, exposure and canopy closure - were analysed to estab-
lish whether correlation between these parameters and mistletoe incidence
exists. The volume of dead trees (due to the mistletoe infection) in 2004 -
2007 was also compared with mistletoe incidence in order to establish the
correlation between these variables. Silver fir trees infected by mistletoe have
been found in 55% of all 86 sample plots. Within the studied area 22% out of
2147 Silver fir trees were infected by mistletoe (42.2% - 1stinfection class,
32.7% - 2ndclass and 25.1% - 3rdclass). The highest percentage of infected
trees was found in the forest district Mănăstirea Caşin where 42% of exam-
ined trees were infected, mostly of the trees being in the 2ndand 3rdinfection
classes. There was a significant negative correlation between the elevation
and mistletoe incidence. Up to 600 m, the most of the trees are heavily infect-
ed, while above 800 m the trees are incipiently infected. Regarding the
canopy closure, sample plots with understocked and sparsely closed stands
have shown a high level of infection compared with plots with closed stands.
A significant correlation has been found between the volume of dead Silver
fir tees and mistletoe incidence. The highest mistletoe infection was registrat-
ed in Silver fir stands at the eastern border of the Eastern Carpathians. There
was noticed a decrease of mistletoe infection from the East to the West.
Keywords: Silver fir, Abies alba, mistletoe, Viscum album abietis, inci-
dence, distribution.
Author. Cătălina Barbu, Ştefan cel Mare University of Suceava, Forestry
Faculty, Universităţii 13, 720229 Suceava, Romania.

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Ann. For. Res. 53(1), 2010Research papers
28 28
Introduction
Viscum album L. is an evergreen, perennial,
epiphytic, hemiparasitic shrub that lives on the
wide range of woody plants species. It is native
to Europe and is a known parasite, a pharma-
ceutical plant and a symbol in mythology
(Zuber 2004). The term hemiparasitic is used
because most mistletoe do photosynthesize,
although they may obtain up to 60% of their
carbohydrates from the host (Watson 2001). It
has a wide distribution in Europe and has also
been introduced to North America (Hawks-
worth & Scharpf 1986).
In Europe three subspecies occur: Viscum
album ssp. austriacum (Wiesb.) Vollman and
ssp. abietis (Wiesb.) Abromeit are confined to
conifers, and ssp. album to the dicotyledonous
host trees and shrubs (Tubeuf 1923, Zuber
2004)
Viscum album abietis grows on branches and
stems of silver fir trees. The species is dioe-
cious with fly pollinated flowers, viscous fruits
and persistent haustoria in the host. In
Romania it occurs only on Silver fir (Abies
alba Mill.) and is one of the most significant
biotic factors that has affected silver fir stands
(Barbu 2009). In Romania, Silver fir occurs
naturally only in the Carpathian Mountains,
mainly in mixed forests with beech and spruce
on an estimated area of 0.9 mil ha. It is consid-
ered the most productive coniferous species in
Romania. Only Silver fir represents about 0.3
mil ha, that means 5% of the Romanian forests.
Growing stock of Silver fir stands is estimated
at over 110 mil. cubic meters, being the sec-
ond most important conifer species in
Romania, after Norway spruce (Barbu &
Barbu 2005).
In Romania the decline of Silver fir stands
has been observed for a long time (1928, 1948
and 1966). The situation developed mainly
after 1980 (Barbu 1991, 1994, 1997, Bândiu
1996) when heavy and increasing damages
occurred in pure Silver fir stands from Eastern
Carpathians, located on albic luvisoils as well
as on the slopes exposed to acid rains coming
from Central Europe.
Silver fir in the Carpathians displays a
healthy look, mainly at altitudes higher than
800 m and on protected slopes. At low eleva-
tions, principally in Eastern and Southern
Carpathians, Viscum album abietis becomes
more and more frequent, causing important
damages and wood degradation.
In the last 60 years, in Europe, many reports
were made about the mistletoe problem on
Silver fir: in France - Plagnat 1950, Plagnat
and Brossier 1969, in Switzerland in 1970’s,
1980’s and 2000’s (Hofstetter 1988, Noetzli et
al. 2004), in Croatia (Idzojtić et al. 2008), in
Spanish Pyrenees (Oliva and Colinas 2007).
Mistletoe is also a major problem in the fir for-
est of Mount Parnis - Greece (Tsopelas et al.
2004).
In Romania the distribution of Viscum album
abietis is quite unknown and the mistletoe
problem on Silver fir is hardly studied (Nanu
1969, Barbu 1991, Şofletea 1993, Barbu
2009).
According to the Flora of RPR (1952) in
Romania, V. a. abietis is spread in the Northern
part of Eastern Carpathians (Maramureş and
Bucovina) and Focşani area (Dealul Lung and
Pelticu forest). Silver fir mistletoe is also
spread in Silver fir stands from forest districts
Anina and Oraviţa (calcareous region of Banat
Mountains) (Nanu 1969) and forest districts
Sinaia and Braşov (Prahova Valey) (Şofletea
1993). It is also known from Suceava County:
forest districts Solca, Marginea, Mălini, Râşca
in which Silver fir stand located up to 700 m
are infected in proportion of 60-100% (Barbu
1991, Barbu 2009). According to the map that
presents the geographic distribution of Viscum
album abietis in Europe prepared by E. J. Jäger
and presented by Zuber (2004), in Romania
mistletoe is spread in Northern part of
Romanian Carpathians
Mountains.
The Eastern Carpathians represent the east-
ern limit of natural range of Silver fir and this
is the reason why our study is located in this
area. The main objective of our research was to
assess the incidence and distribution of mistle-
toe in representative Silver fir stands from
Eastern Carpathians.
and in Banat
Material and methods
The study area of our investigations has cov-

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Barbu The incidence and distribution of white mistletoe...
29
ered the entire altitudinal belt where Silver fir
is spread in the Eastern Carpathians (Figure1).
The incidence of mistletoe on infested Silver
fir trees was assessed in four representative
forest districts (F.D.) - Gura Humorului,
Vaduri, Mănăstirea Caşin and Agăş.
The forest district Gura Humorului is repre-
sentative for pure Silver fir stands located on
the border of the Carpathians at the contact
zone to the Suceava Plateau while the forest
district Vaduri is representative for the pre-
mountainous zone of the Eastern Carpathians
where Silver fir and beech are the predominant
forest species. The forest district Mănăstirea
Caşin is representative for mixed forests of
resinous (Silver fir and spruce) and beech
forests, and Forest district Agăş is representa-
tive for mixed forests of spruce and Silver fir
(Table 1).
To assess the distribution and incidence of
mistletoe infection, a statistical inventory of
Silver fir stands - from mentioned forest dis-
tricts - based on 2 x 2 km grid was performed.
The grids oriented on an N-S/E-W direction
were placed on the maps of the forest districts.
At the intersection of the gridlines, stands
older than 70 years were searched for on a dis-
tance of 500 m around. Each Silver fir stand
chosen in this way represents a sample plot.
Plots in which Silver fir was not present or the
stand age was lower than 70 years were
excluded. In each plot 30 Silver fir trees
(located at minimum 50 meters from the bor-
der of the stand) that belonged to the first three
social Kraft classes (predominant, dominant
and co-dominant) were chosen. For each tree
the degree of infection was quantified using 4-
class rating system (Barbu 2009) (Figure 2): (i)
class 0 - no infection (absence of mistletoe)
(Figure 2a); (ii) class 1 - low infection with
high frequency of bushes on lateral branches
(Figure 2b); (iii) class 2 - moderate infection
with very frequently bushes in the crown, dry-
ing branches and moderate swellings on the
branches level (Figure 2c); (iv) class 3 - heavy
infection with bushes in all the crown and
Geographic coordinates range
Forest
district
Latitude N
47o43’43” - 47o23’55”
Longitude E
25o44’36” - 26o01’36”
Altitude (m)
Distance from the
Eastern Carpathians
border (km)
3-10 Gura
Humorului
Vaduri
Mănăstirea
Caşin
Agăş
400-1000
47o00’57” - 46o47’43”
46o15’01” - 46o01’49”
26o10’46” - 26o23’29”
26o20’45” - 26o47’25”
500-1000
600-1200
10-30
30-80
46o42’84” - 46o18’44” 25o58’51” - 26o24’03” 700-1600 80-100
Table 1 Geographic coordinates and distance from the Eastern Carpathians border of investigated forest
districts
Figure 1 Research area: 1 - F. D. Gura Humorului, 2 - F. D. Vaduri, 3 – F. D. Agăş, 4 – F. D. Mănăstirea
Caşin

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Ann. For. Res. 53(1), 2010 Research papers
3030
stem, asymmetrical crowns, often with dying
back top and heavy swellings on the branches
and on the stem (Figure 2d).
In total, within the area of the 4 forest dis-
tricts (FD), 23 production units (PU) and 86
plots in which Silver fir proportion is between
20 and 100% as many as 2147 trees were
examined (Table 2). The results from each
sample plot are associated to a square of 2 km
side (400 hectares).
For the study area a database containing
information about the elevation, crown closure
and stand age was made using the management
plans. The data were statistically processed in
order to establish whether there was a correla-
tion between the mentioned parameters and
mistletoe incidence.
Also, the volume (m3/ha) of dead trees (due
to the mistletoe infection) in 2004-2007 was
compared with mistletoe incidence for the pro-
duction units of the forest district Vaduri in
order to establish the correlation between these
variables. The data have been provided by the
County Forest Administration Neamţ. The vol-
ume of the extracted dead fir trees was regis-
tered in management plans as sanitation cut-
tings.
Pearson correlation coefficient (r) was used
to determine relationships between mistletoe
incidence and selected variables. The mistletoe
incidence was presented according to the per-
centage of infected trees for each infection
class. The statistical procedures were per-
formed using MyStat v.12 computer program
(2008).
Results
In half of all analysed sample plots the propor-
tion of Silver fir is higher than 50%, in 34% of
the plots the proportion of Silver fir range
between 26 and 50%, while only in 16% of the
plots the proportion of Silver fir is lower than
25%. The situation for each forest district is
presented in Figures 3-6.
Silver fir trees infected by mistletoe were
found in 49 of 86 sample plots installed in the
field area (Table 2). The mean percentage of
infected sample trees range between 3 and
100%. On the whole area, 22% of the sample
trees were infected by mistletoe. As for the
infection degree, the trees are distributed as
follows: 42.2% in 1stinfection class, 32.7% in
2ndinfection class and 25.1% in 3rdinfection
class.
Out of the 721 predominant sample trees
from all plots, 36.8% were infected by mistle-
toe, 6.3% with low infection and 30.5% with
moderate and heavy infection. Of the 814
dominant trees, 29.3% were infected, 5.2%
with low infection and 24.1% with moderate
and heavy infection. In co-dominant trees the
intensity of infection was lower, only 15% of
the trees being infected (Figure 7).
On the forest districts the situation is pre-
sented as follows. In forest district Gura
Humorului mistletoe was found in 58% of the
sample plots (Figure 8). The mean percentage
of parasited trees is 8% with large variability
from 28% to 60% in P.U. V Păltinoasa (locat-
ed between 450 and 600 m altitude) and 3-10%
Figure 2 Examples of trees from each infection classes

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Barbu The incidence and distribution of white mistletoe...
in PU IV Mănăstirea Humorului (750-1000 m
altitude). In P.U. II and III the percentage of
Silver fir trees damaged by mistletoe was
lower than 3%. According to the damage
degree, the highest incidence (78.9%) was
observed for 1stinfection class (Table 2).
The mean percentage of parasited trees in
forest district Vaduri was 27%. Higher values
were found at low altitude stands (P.U. III -
40% and P.U. IV- 30%) and less infection in
P.U. II - 25% (Figure 9). In the composition of
the P.U. I, the main species is beech and only
in upper part of this production unit there are
mixed forests with Silver fir and beech. For
this reason in that production unit the propor-
tion of infested trees is lower (19%).
According to the damage degree, the highest
incidence (47.9%) was observed for 3rdinfec-
tion class (Table 2). The incidence was also
considerable for trees from 2ndinfection class
(34%).
On the forest district Mănăstirea Caşin level,
in the sample plots situated on the eastern part
of the forest district, the incidence of mistletoe
is higher than 25% (in P.U. II - 45%), while in
P.U. IV the percentage of infected trees
Figure 3 Silver fir percentage in stands older than
70 years in the F.D. Gura Humorului
Figure 4 Silver fir percentage in stands older than
70 years in the F.D. Vaduri
Figure 5 Silver fir percentage in stands older than
70 years in the F.D. Mănăstirea Caşin
Figure 6 Silver fir percentage in stands older
than 70 years in the F.D. Agăş