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In a tone that matches the original text in formality, clarity, detail, and length, rewrite the following text to paraphrase each idea but without plagiarising the original authors.  Be specific and include all information presented.  Include inline citations for ideas from referenced papers.  Also include list of cited refs at end.  

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```
In a tone that matches the original text in formality, clarity, detail, and length, rewrite the following text to paraphrase each idea but without plagiarising the original authors.  Be specific and include all information presented.  Include inline citations for ideas from referenced papers.  Also include list of cited refs at end.  
```

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**ASSISTANT**: Sure, I understand. You'd like me to help you paraphrase a text in a formal tone without plagiarizing the original authors. I'll make sure to include all information presented and cite any referenced papers inline and at the end. Please send me the original text and any paper references you have so I can begin.
**USER**: 2021, VOL. 97, No

 1 — THE FORESTRY CHRONICLE 43

Climate, radial growth, and mortality associated with conifer 

regeneration infected by root disease (Armillaria ostoyae) 

By Michael P. Murray1 and Adrian Leslie2

ABSTRACT 

Tree root disease caused by the pathogen Armillaria ostoyae (Romagn.) Herink has notable influence on bio-economic 

systems of southern British Columbia (BC) and the northwestern United States. Annual radial growth and mortality 

trends of regeneration associated with A. ostoyae during the first 21 years of a plantation were investigated. Our den-

drochronological approach focused on a plantation established in 1991 with Douglas-fir (Pseudotsuga menziesii (Mirb.) 

Franco), western larch (Larix occidentalis Nutt.), and lodgepole pine (Pinus contorta Dougl. ex Loud. var. latifolia

Engelm. ex S. Wats.). We examined tree rings for reduced growth onset (RGO) to estimate infection periods. Among 

trees studied, we found that the number of RGO events peaked in 2006 followed by a steady decline in frequency. A sim-

ilar trend was seen in annual mortality rates which reached maximum values in 2007 followed by an uninterrupted 

decrease. The average number of years from RGO to death based on host species ranged from 2.3 to 3.6 years. According 

to logistic regression modeling, values associated with drought codes and duff moisture codes were significant in deter-

mining the year of death for infected trees. The predicted increase in frequency of summer droughts may lead to elevated 

mortality associated with A. ostoyae in young plantations.   

Keywords: Armillaria ostoyae, conifer regeneration, annual growth, tree mortality, plantation, drought, weather. 

RÉSUMÉ 

Le pourridié causé par le pathogène Armillaria ostoyae (Romagn.) Herink nuit grandement aux systèmes bioécono-

miques du sud de la Colombie-Britannique et du nord-ouest des États-Unis. Cette étude s’intéresse à l’effet d’A. ostoyae 

sur la croissance annuelle radiale et la mortalité de la régénération au cours des 21 premières années d’une plantation. 

Notre approche dendrochronologique a porté sur une plantation de 1991 constituée de sapin Douglas (Pseudotsuga men-

ziesii (Mirb.) Franco), de mélèze de l’Ouest (Larix occidentalis Nutt.) et de pin Lodgepole pine (Pinus contorta Dougl. ex 

Loud. var. latifolia Engelm. ex S. Wats.). À partir des anneaux de croissance, nous avons cherché à établir le début de la 

réduction de croissance (RGO) pour estimer la période d’infection. Sur les arbres étudiés, nous avons constaté que le 

nombre de cas de réduction de croissance (RGO) culminait en 2006 et déclinait régulièrement par la suite. La même ten-

dance s’est manifestée avec le de mortalité annuelle qui a atteint son maximum en 2007 avant de diminuer constamment 

par la suite. Le nombre moyen d’années entre l’amorce de la diminution de croissance (RGO) et la mort variait de 2,3 à 

3,6 ans suivant l’essence de l’arbre-hôte. La modélisation par régression logistique a montré que les valeurs des indices de 

sécheresse et d’humidité de l’humus influençaient significativement la prédiction du moment de la mortalité chez les 

arbres infectés. Les épisodes de sécheresse de plus en plus fréquents qu’on nous annonce risquent d’accroître la mortalité 

associée à A. ostoyae dans les jeunes plantations.  

Mots-clés: Armillaria ostoyae, régénération des conifères, croissance annuelle, mortalité des arbres, plantation, séche-

resse, météo.

1British Columbia Ministry of Forests, Lands, Natural Resource Operations and Rural Development, #401-333 Victoria Street, Nelson, BC 

V1L 4K3, Canada, email: Michael.Murray@gov.bc.ca 

2White Bark Consulting, Castlegar, BC V1N 4T5, Canada

Michael P. Murray

Introduction 

The tree root disease caused by the pathogen Armillaria 

ostoyae (Romagn.) Herink has notable influence on ecologi-

cal and economic systems of southern British Columbia (BC) 

and the northwestern United States. In unmanaged forests 

where A. ostoyae is endemic, it plays an important role in for-

est ecosystems through its ability to weaken or kill trees, and 

contribute to stand structure, forest succession, decomposi-

tion, and nutrient cycling processes (Edmonds et al. 2010). In 

stands of the Interior Cedar Hemlock (ICH) forests of south-

ern BC, up to 100% of mature trees can be infected with A. 

ostoyae (Morrison et al. 2001). Young trees are also suscepti-

Adrian Leslie

The Forestry Chronicle Downloaded from pubs.cif-ifc.org by 24.68.99.51 on 05/31/23 For personal use only.
**ASSISTANT**: How can Armillaria ostoyae affect tree growth and mortality in plantations? 



The pathogen Armillaria ostoyae can significantly impact ecological and economic systems in southern British Columbia and the northwestern United States. In plantations of Douglas-fir, western larch, and lodgepole pine, a dendrochronological study found that reduced growth onset (RGO) peaked in 2006, followed by a steady decline in frequency. Annual mortality rates also peaked in 2007 before decreasing steadily. The average number of years from RGO to death ranged from 2.3 to 3.6 years based on host species, and drought codes and duff moisture codes were significant predictors of the year of death for infected trees. The predicted increase in frequency of summer droughts may lead to elevated mortality associated with A. ostoyae in young plantations.



(Source: Murray and Leslie, "Climate, radial growth, and mortality associated with conifer regeneration infected by root disease (Armillaria ostoyae)", The Forestry Chronicle, 2021)
**USER**: ble with post-harvest regeneration losses of up to 2% per year 

in plantations (Peet et al. 1996; Morrison et al. 2014). 

The economic importance of A. ostoyae is closely tied to 

timber production. This disease impacts sustainable forest 

management due to its ability to increase following harvest, 

reduce tree growth rates, and cause mortality, especially in 

young regeneration (Cruickshank 2000; Morrison 2000). The 

earliest stages of plantation development are especially vul-

nerable due to the tendency for A. ostoyae to cause high mor-

tality rates during the first 5–20 years of a rotation (Morrison 

et al. 1988; Morrison and Pellow 1994). This is a reflection of 

A. ostoyae readily colonizing freshly cut stumps and their 

roots plus lower resistance inherent in very young trees 

(Cleary et al. 2008). This pathogen spreads primarily through 

root-to-root contact and rhizomorphs that extend from 

established infections. Morrison (2011) found that seedlings 

were infected most frequently by rhizomorphs and root-to-

root contact with old stumps. After 15–21 years, the impor-

tance of rhizomorphs declined compared to stumps. More 

information regarding spread and mortality within young 

plantations can be useful for guiding reforestation practices. 

The Province of BC mandates that every harvest unit receive 

a post-planting survey to ensure that reforestation of the site 

achieves appropriate stocking levels (BC FRPA 2004). Plan-

tations that are declared as meeting the mandated stocking 

levels during this survey are not usually inspected again prior 

to harvest age (ca. 60–80 years). In areas prone to root dis-

ease, surveys would be most useful if timed to occur after any 

anticipated period of highest mortality. 

Several field trials have quantified the temporal progres-

sion of A. ostoyae within young plantations in the southern 

interior of BC. Researchers have applied varying combina-

tions of field methods for detecting and documenting mortal-

ity and infection including observing above-ground symp-

toms and signs such as mycelial evidence beneath bark 

(Morrison et al. 1988; Chapman et al. 2011; Morrison 2011). 

Morrison and Pellow (1994) examined Douglas-fir (Pseudot-

suga menziesii (Mirb.) Franco) tree rings on root collar cross-

sections to estimate dates of deaths but not onset years of 

associated infections. Field sampling associated with these 

studies occurred at 2–10 year intervals spanning 11–35 year 

periods. We are unaware of any plantation studies estimating 

dates of both the infection periods and subsequent deaths 

using an annual resolution. 

The interaction of A. ostoyae root disease and climate 

within young plantations is poorly understood. Mycelia of 

A. ostoyae physically disrupt tree vascular systems and can 

kill portions of root networks or result in host mortality. 

Reduced growth in diameter and height manifests as trees 

experience infection stress (Shaw and Kile 1991). Due to ris-

ing annual temperatures and more frequent and severe 

droughts, infected trees may have an amplified risk of mor-

tality (Dukes et al. 2009; Kliejunas 2011). Assessing incidence 

(infection and mortality) of A. ostoyae on a yearly resolution 

may contribute to a level of understanding gained from sim-

ilar studies that employed coarser, multi-year sampling fre-

quencies (e.g., Morrison and Pellow 1994; Peet et al. 1996). 

Moreover, annual deaths can be compared with correspond-

ing yearly weather variables to investigate potential relation-

ships. In this study we examined tree ring growth to estimate 

infection and death trends of regeneration associated with 

A. ostoyae during the first 21 years of a plantation. Our den-

drochronological approach focused on the three tree species 

most commonly planted on harvested sites in the southern 

interior of BC: Douglas-fir, western larch (Larix occidentalis 

Nutt.), and lodgepole pine (Pinus contorta Dougl. ex Loud. 

var. latifolia Engelm. ex S. Wats.). We also assessed potential 

weather variables, which may affect both radial growth and 

the timing of death. 

Material and methods 

Study area 

In 1988, an A. ostoyae root disease research trial was estab-

lished approximately 46 km north of Grand Forks, BC which 

is located on the border of Washington State, USA (Fig. 1a). 

The study area (49o 24-

 10 N, 118o 26-

 00 W) is on the east 

side of Burrell Creek at an elevation range of 667–725 m. The 

research trial is characterized by undulating terrain, slopes 

ranging from flat to 35% and various aspects. The average 

slope is 12%, and average aspect is 255o. It is located in the 

Interior Cedar-Hemlock biogeoclimatic zone’s very dry 

warm subzone (ICHxw) where summers average 15–30 cm 

precipitation and winters are very mild with little snowfall 

(MacKillop and Ehman 2016). The soil moisture regime 

ranges from subxeric at the steeper sites with shallow soils to 

mesic sites that are flat and with deeper soils. The research 

trial consists of a 40.8 ha plantation formerly dominated by 

lodgepole pine and larch. In 1988 and 1989 all merchantable 

trees were harvested. Replanting occurred with larch and 

lodgepole pine in 1991. The site was fill planted in 1995 with 

lodgepole pine in areas where cattle and rodent damage had 

occurred and naturally regenerated Douglas-fir became com-

mon throughout the site. The combined average density of 

these three species was 1600 stems per hectare. There are 

insignificant numbers of naturally regenerated western red-

cedar (Thuja plicata Donn ex D. Don) and western white 

pine (Pinus monticola Douglas ex D. Don). We collected fun-

gal tissue from the basal portion of a lodgepole pine and sub-

mitted to the BC Plant Diagnostic Lab (Ministry of Agricul-

ture). As A. ostoyae has been historically sampled here 

(Siltech 1989), we confirmed our identification using a poly-

merase chain reaction (PCR) test coupled with sequencing 

(Ross-Davis et al. 2012). 

Field methods 

In 1997, twenty fixed-area square plots (31.6 m x 31.6 m) 

were randomly positioned throughout the research trial area. 

Within each plot, all trees were located on X–Y axes, mapped, 

and tagged (3219 trees). Additional data recorded for each 

tree included species, height, diameter at 1.3 m (dbh), leader 

growth in 1995 and 1996, origin (planted or natural regener-

ation), and tree health. 

In October 2011, 2997 tagged trees were re-sampled for 

tree health agents and growth (diameter and height). Causes 

of death were determined wherever possible including exam-

ining for evidence of mycelial fans indicating A. ostoyae

infection under the bark at the root collar or on exposed 

roots. A total of 329 trees were dead. Of these, 207 trees were 

found to have A. ostoyae. In October 2012, all dead trees with 

A. ostoyae evidence were sampled by sawing a pair of cross-

sectional discs from each tree. One disc was collected from 

the root collar, and the second was taken at 1.3 m height. If 

44 2021, VOL. 97, No

 1 — THE FORESTRY CHRONICLE

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