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Forest Pathology. 2022;00:e12773.
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https://doi.org/10.1111/efp.12773
wileyonlinelibrary.com/journal/efp
1 | INTRODUCTIO N
Hymenoscyphus fraxineus (T. Kowalski Baral, Queloz & Hosoya) is
an invasive fungal pathogen originating from East Asia where it is
seemingly non- pathogenic on native ash in its natural distribution
range (Cleary et al., 2016). The fungus is now widespread through-
out most of Europe and has dramatically reduced the host popu-
lation size of European ash (Fraxinus excelsior L.) in most countries.
Since ash is known as a keystone species in temperate broadleaved
forests and has huge importance for biodiversity, the continu-
ous loss of ash is expected to have negative ecological impacts of
other vulnerable ecosystem elements including a large number of
species that are highly dependent on ash in the landscape (Hultberg
et al., 2020).
Tolerance against the disease has been recorded in several
European ash populations where healthy trees have been observed
to survive well among the affected ones, showing relatively little die-
back damage (McKinney et al., 2014 and references within). The high
vitality of such trees has also been observed over longer periods.
Estimations of genetic heritability show that between 30 and
50% of the variation in tolerance to ADB may be explained by
genetic components of the host species (Plumb et al., 2020). In
Sweden, Stener (2013, 2018) surveyed two clonal seed orchards
5,10 and15 yearsaf terthefirstreportof ADB inthecountr yand
Received:23May2022
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Revised:5September2022
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Accepted:7September2022
DOI : 10.1111/efp.127 73
SHORT COMMUNICATION
Monitoring of long- term tolerance of European ash to
Hymenoscyphus fraxineus in clonal seed orchards in Sweden
Mateusz Liziniewicz1 | Beatrice Tolio1,2 | Michelle Cleary2
This is an open access ar ticle under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,
provided the original work is properly cited.
© 2022 The Authors. Forest Patholog y published by Wiley-VCH GmbH.
1Skogforsk - The Forestry Research
Institute of Sweden, Svalöv, Sweden
2Southern Swedish Forest Research
Centre, Swedish University of Agricultural
Sciences, Alnarp, Sweden
Correspondence
Mateusz Liziniewicz, Skogforsk - The
Forestry Research Institute of Sweden,
Ekebo 2250, 26890 Svalöv, Sweden.
Email: mateusz.liziniewicz@skogforsk.se
Funding information
Föreningen skogsträdförädling; Sveaskog
Abstract
The invasive alien pathogenic fungus Hymenoscyphus fraxineus causing ash dieback
(ADB) has devastated European ash (Fraxinus excelsior) populations across Europe.
Breeding for resistance is the most feasible measure to reduce future losses of ash,
and the presence of resistance, albeit at low level, has been demonstrated in nu-
merous genetic trials around Europe. This study is a continuation of the inventories
tracking the vitality status of different clones, which started in 2006 at two ash seed
orchards in southern Sweden. A new inventory conducted in the summer of 2021
revealed that the ten clones previously identified as the most tolerant to ADB based
on periodic surveys from 2006 and onwards still remain the most tolerant, while sus-
ceptible clones continued to decline and are completely disappearing from the or-
chards. Browsing caused mortality in some of the most tolerant clones in one of the
orchards during the last assessment period. Despite the animal damage, the stable
resistanceobservedin tolerantclones overa15 years period forms asolidbasis for
the continuation of the breeding programme where good candidates are selected for
further study.
KEY WORDS
disease type, disease type— shoot disease, fraxinus, host genus— dieback
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LIZINIEWICZ et al .
substantiated other European investigations reporting a large geno-
typic variation in susceptibility to ADB. The numerous reports show-
ing the genetic basis of resistance to ADB across Europe suggest
that selective breeding can mitigate the disease impact (McKinney
et al., 2014; Stener, 2013, 2018).
The main aim of this study was to investigate the stability of vi-
tality scores on F. excelsior clones in two seed orchards in southern
Sweden, with a special emphasis on the performance of tolerant
clones initially identified during earlier surveys. Knowledge about
stability of resistance is needed to validate the assumption of the
current breeding programmes that have been initiated in European
countries.
2 | MATERIALS AND METHODS
TwoseedorchardslocatedatSnogeholm(55°32′ N,13°32′ E,50 m)
andTrolleholm(55°57′ N,13°12′ E,100 m)insouthernSwedenwere
established in 1992 and 1995, respectively, to produce seeds for
commercial forestry purposes. The selection criteria for the clones
were growth and stem quality properties aiming to increase produc-
tion of valuable ash timber. There were 100 and 106 clones planted
in Snogeholm and Trolleholm, respectively. The clones came from
27 stands f rom souther n Sweden betwe en latitudes 55°41′ Nan d
58°02′ N.Thenumberoframetsperclonewasbetween40and60
at Snogeholm and up to 10 at Trolleholm.
Assessments of damage caused by ADB were initially con-
ducted in September 2006 and in the middle of August in 2007
at Snogeholm, and thereafter in 2010, 2011 and 2016 at both
Snogeholm and Trolleholm sites, as reported by Stener (2013, 2018).
There was also an inventory of living ramets done in Trolleholm in
1996, one year after planting.
In summer of 2021, assessment s of damage caused by ADB were
made according to the protocol of Stener (2018). Tree vitality was
scored using a scale from 1 to 9, where 1 indicated low vitality and 9
very good vitality. The crown damage was scored as a percentage of
crown dieback where class 0 indicated no damage, class 1 indicated
low damage (up to 10% of the crown exhibited dieback), and class
9 indicated very serious damage (up to 90% of the crown exhibited
dieback) (e.g. Figure 1a).
In addition, the occurrence of damage caused by fallow deer and
wild boar was recorded for all trees in Snogeholm. The type of dam-
age was scored as 0— no damage, 1— damage to the bark (layers of
periderm removed) and 2— damage to the vascular cambium (layers
of cambial tissue removed exposing underlying sapwood). Estimates
of damage severity were calculated as the per cent circumference of
girdling, in 10% classes (0%– 10%, 11%– 20% and so on).
In the analysis, the focus was on the overall long- term dynamics
of ADB symptoms including all clones in orchards as well as on mor-
tality of individuals among the ten most tolerant or most suscepti-
ble clones previously selected by Stener (2013, 2018). The selection
of tolerant, intermediate and susceptible clones was based on the
genetic breeding values known as best linear unbiased predictor
(BLUP) estimated for vitality and crown damage jointly for both or-
chards. For any tolerant tree that died, the cause of mortality was in-
vestigated to determine whether it was due to ADB or other factors.
The data from all available inventories are presented as descriptive
statistics and in figures.
3 | RESULTS AND DISCUSSION
The cumulative mortality for all clones between the first and last
assessm ent was 68% at Trolleholm (11 years af ter the firs t inven-
toryin2010)and89%atSnogeholm(15 yearsafterthefirstinven-
tory in 20 06), giving an average mortality rate of approximately 6%
annually. The rate of mortality was similar over the years in both
orchards (Figure 1b).Notsurprisingly,therelativemortalityratebe-
tween 2016 and 2021 decreased in comparison with the previous
assessment period (2011– 2016) as many susceptible genotypes had
already succumbed to the disease and the ongoing natural selec-
tion favours only the most tolerant individuals. At the last assess-
ment conducted in 2021, it was observed that 22 clones (21% of all
planted) at Trolleholm and 8 clones (8% of all planted) at Snogeholm
had died. Of these clones that died, three were common to both
orchards.
In the year 2021, for all clones, the mean number of living ramets
per clone was 3.3 ± 2.2 and2.3± 1.8 inSnogeholmandTrolleholm
seed orchards, respectively. Considering tolerant clones only,
the mean number of living ramets per clone was twofold higher;
6.5 ± 3.4inSnogeholmand4.5± 1.4inTrolleholm.
In the most recent assessment period (2016– 2021), the absolute
number of dead trees among the ten most tolerant clones previ-
ously identified by Stener (2013, 2018) varied between orchards. In
the summer of 2016, there were 89 and 50 living ‘tolerant’ ramets
at Snogeholm and Trolleholm, respectively. In the smaller orchard
(Trolleholm), four of the 50 ramets (8%) died in 2016. There, mor-
tality was registered for just two out of ten tolerant clones. In one
of those clones, three out of six ramets died and in the other clone
just one ramet died. Mor tality at Snogeholm was observed in seven
of the tolerant clones including the same two clones with observed
mortality at Trolleholm. For three clones, just one ramet died. In the
most extreme case, eight out of 13 ramets died. In total, 23 of 89 (or
approximately 26%) of living ‘tolerant’ ramets in 2016 died since the
last assessment (Figure 1c).
In general, the mortality among clones in the tolerant group was
associated with smaller tree size. The average diameter of all dead
treesinthisgroupwas127 ± 29 mm,whiletheaverageofallremain-
ingtreeswas195 ± 36 mmregardlessoftheseedorchard.
The average vitality score of the ten most tolerant clones fluc-
tuated slightly over time (Figure 1d), which may be attributable to
temporal variability in damage severity related to variable weather
conditions across seasons, especially precipitation that is an im-
portant factor for ash vitality. On the contrary, the scores had not
shifted more than one grade in the nine- grade scale over the years
(Figure 1d). There were some clones that had a score close to the
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LIZINIEWICZ et al.
average score for other intermediate living clones. Some within-
clone variation was evident across phenotype groups. In 2021,
the mean vitality scores of the remaining intermediate/suscepti-
ble clones were relatively high in both seed orchards (6.2 and 7.5
at Snogeholm and Trolleholm, respectively) compared with the ten
most tolerant clones. However, the average number of living ramets
for these intermediate/susceptible clones was three with 42 clones
having only one or two living ramets, which had a great effect on the
calculated mean.
Some variation may have also occurred between assessment
years due to subjectivity in the assessment that was conducted by
different people. Among the 23 ‘tolerant’ ramets that died between
2016 and 2021 at both seed orchards, 16 were characterized as hav-
ing highest vitality scores (8 or 9) in 2016.
From the time of the first available inventory, cumulative mortal-
ity of ramets belonging to the group of ten most tolerant clones was
66% and 39% in Snogeholm and Trolleholm, respectively. Most of
this mortality should be attributed to ADB. However, at Snogeholm,
other causes, namely fallow deer and wild boar, damaged large por-
tions of the main stem causing direct mor tality by girdling, but also
indirectly contributed to mortality by inducing stress over several
years of continuous browsing. Animal damage was observed on 84%
(n = 296) of trees at Snogeholm after the opening of the fence in
2018. Of those, about 41% (n = 144) had only minor bark damage
with removal of the periderm and some inner phloem, while 43%
(n = 152) had severe damage to the stem with complete removal of
the bark and vascular cambium. Exposed wounds were up to 1 m in
length on the stem, affecting approximately 40% of stem circumfer-
ence. In the group of ten most tolerant clones, for 14 ramets (out of
23 that were recorded to have died during the period 2016– 2021),
animal damage was determined to be the main reason for mortality.
NobrowsingdamagewasobservedatTrolleholm.In somepartsof
the seed orchard at Snogeholm, natural regeneration filled in gaps
created by the loss of ash trees. In some cases, the naturally regen-
erated trees have caused significant competition to ash, overshad-
owing its tree crowns. Some stand management activities have been
carried out at both seed orchards to remove this competing vege-
tation and at the same time some ash trees, which were deemed to
have poor vitality could also have been removed.
Between 2006 and 2016, 89% (160 out of 180) of ramets rep-
resenting the 10 most susceptible clones according to Stener (2013,
2018) died; 103 at Snogeholm and 57 at Trolleholm. Of the 20
FIGURE 1 (a)Representativesofsusceptible(left)andtolerant(right)ashclonesatTrolleholmseedorchard,(b)Changesinmortalit yrate
over time from the first assessments in Snogeholm (red) and Trolleholm (blue) seed orchards, (c) the number of living ramets of the ten most
tolerant clones (red and solid lines), the ten most susceptible (black and solid lines) and clones with intermediate susceptibility (grey and
dashed lines) (d) the vitality score of ten best (most tolerant) clones in both seed orchards at the different assessments conducted between
2011 and 2021; here, lines of different colours represent different clones; the dashed line shows the average vitality score of all living clones
with intermediate susceptibility.
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LIZINIEWICZ et al .
susceptible ramets remaining in 2016, 9 died during the last assess-
ment period and only 11 ramets remained, three susceptible clones
with each two ramets and five clone with just one ramet each.
The long- term monitoring of the oldest genetic trial of European
ash in Sweden indicate that there is considerable within- clone vari-
ation in tolerance to ADB. At both Snogeholm and Trolleholm, there
was continued mortality of clones previously identified as being ge-
netically superior due to low severity of damage caused by ADB,
albeit at a ver y low level compared with susceptible clones.
Careful monitoring of other mortality agents should be imple-
mented in future assessments to improve tolerance assessments.
In forests in Sweden, species of Armillaria are opportunistic on the
roots of diseased ash trees, causing decay and increasing tree sus-
ceptibility to windthrow. Observations from annual field surveys in
ashforestsinSwedenduringthelast10 yearssuggesttheincidence
of root infection caused by Armillaria spp., and tree mortality as a
result of girdling of mycelial fans at the root collar and/or subsequent
windthrow is increasing. Both seed orchards in this study are, how-
ever, located on former agricultural land where Armillaria spp. are
less prevalent and the main contributing mortality factor appears
to be animals. Contributing agents of mortality other than ADB
represent a potential problem for the breeding programme where
long- term tolerance stability to ADB is needed to secure the estab-
lishment of a tolerant breeding population.
ACKNOWLEDGEMENTS
The inventor y of the seed orchards has been done with the finan-
cial support of the Föreningen skogsträdförädling (project 20- 448
Uppföljning av förädling för motståndskraft mot askskottsjuka). The
project was also financially suppor ted by Sveaskog within the frame-
work of the project aimed at ash and elm preservation.
DATA AVAIL ABILI TY STATEMENT
The data that support the findings of this study are available from
the corresponding author upon reasonable request.
ORCID
Beatrice Tolio https://orcid.org/0000-0002-3137-3040
Michelle Cleary https://orcid.org/0000-0002-0318-5974
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How to cite this article: Liziniewicz, M., Tolio, B., & Cleary, M.
(2022). Monitoring of long- term tolerance of European ash to
Hymenoscyphus fraxineus in clonal seed orchards in Sweden.
Forest Pathology, 00, e12773. https://doi .org/10.1111/
efp.12773