Assessment of presence and distribution of Armillaria and Heterobasidion root rot fungi in the forest of Vallombrosa (Apennines Mountains, Italy) after severe windstorm damage

doi:10.3832/ifor2929-012

Assessment of presence and distribution of Armillaria and Heterobasidion root rot fungi in the forest of Vallombrosa (Apennines Mountains, Italy) after severe windstorm damage

László Benedek Dálya⁽¹⁾ , Paolo Capretti⁽²⁾, Luisa Ghelardini⁽²⁾, Libor Jankovský⁽¹⁾

iForest - Biogeosciences and Forestry, Volume 12, Issue 1, Pages 118-124 (2019)
doi: https://doi.org/10.3832/ifor2929-012
Published: Feb 11, 2019 - Copyright © 2019 SISEF

Research Articles

PDF Version

Full Text

Citation

Geo-mapping

One of the main problems for the management and conservation of silver fir stands has long been pathogens causing root rot, in particular Armillaria spp. and Heterobasidion annosum s.l. These opportunistic pathogens are especially threatening now that climate change related stress is increasing tree susceptibility to disease and vulnerability to windstorms. The northern Apennines Mountains (central Italy) are forecast to be one of the areas with the highest temperature increase in the next future. However, no systematic assessment exists of the risk posed by the disturbance due to secondary pathogens in the Apennine forests. In the Nature Reserve of Vallombrosa (northern Apennines), where silver fir forests have been managed and conserved for centuries since the Middle Ages, making it an ideal site for studying these parasites, the high presence of H. annosum was reported already in 1990, while only sporadic observations are available on Armillaria species. The aim of this work was to examine the occurrence of both pathogens, since detailed knowledge about their distribution may assist forest management planning and decision-making. Systematic sampling was undertaken at the intersection of 52 grid points covering the whole forest. Different fungal species from soil and fungal samples (fruiting bodies or rhizomorphs) were identified by combining morphological descriptions with molecular methods. The analyses confirmed the presence of H. abietinum in about 70% of the investigated points. The fungus was detected at two new localities above 1000 metres suggesting a possible expansion of the parasite at upward elevation, which might be associated with climate change. Armillaria was widespread: almost 90% of the samples resulted positive, and four different Armillaria species were successfully identified. The most frequent species were A. cepistipes, whose rhizomorphs were especially abundant, and A. ostoyae, which was often detected just in soil samples. At sites where A. cepistipes was found to coexist with A. gallica, these two species might specialize themselves to necrotrophic and saprotrophic lifestyle, respectively. Besides, there were unexpected findings of A. mellea, supposed to be a residual from the previous rotation of broadleaves.

Keywords

Butt Rot, Climate Change Disturbances, Heterobasidion annosum, Root Rot, Silver Fir, Windstorm Damage

Authors’ address

(1)

Department of Forest Protection and Wildlife Management, Mendel University in Brno (ÚOLM), Zemedelská 3, 61300 Brno (Czech Republic)

(2)

Department of Agrifood Production and Environmental Sciences, University of Florence (DISPAA), p.le delle Cascine 28, I-50144, Firenze (Italy)

Corresponding author

László Benedek Dálya
laszlo.dalya@mendelu.cz

Citation

Dálya LB, Capretti P, Ghelardini L, Jankovský L (2019). Assessment of presence and distribution of Armillaria and Heterobasidion root rot fungi in the forest of Vallombrosa (Apennines Mountains, Italy) after severe windstorm damage. iForest 12: 118-124. - doi: 10.3832/ifor2929-012

Academic Editor

Alberto Santini

Paper history

Received: Jul 22, 2018
Accepted: Dec 28, 2018

First online: Feb 11, 2019
Publication Date: Feb 28, 2019
Publication Time: 1.50 months

Open Access

This article is distributed under the terms of the Creative Commons Attribution-Non Commercial 4.0 International (https://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Breakdown by View Type

(Waiting for server response...)

Article Usage

Total Article Views: 38491
(from publication date up to now)

Breakdown by View Type
HTML Page Views: 32910
Abstract Page Views: 2382
PDF Downloads: 2525
Citation/Reference Downloads: 9
XML Downloads: 665

Web Metrics
Days since publication: 2074
Overall contacts: 38491
Avg. contacts per week: 129.91

Article Citations

Article citations are based on data periodically collected from the Clarivate Web of Science web site
(last update: Feb 2023)

Total number of cites (since 2019): 4
Average cites per year: 0.80

(no Plumx Metrics available for this paper)

Publication Metrics

by Dimensions ^©

Articles citing this article

List of the papers citing this article based on CrossRef Cited-by.

(1)

Antonín V, Jankovsky L, Lochman J, Tomšovsky M (2006)
Armillaria socialis - morphological-anatomical and ecological characteristics, pathology, distribution in the Czech Republic and Europe and remarks on its genetic variation. Czech Mycology 58 (3-4): 209-224. -
Online | Gscholar

(2)

Antonín V, Tomšovsky M, Sedlák P, Májek T, Jankovsky L (2009)
Morphological and molecular characterization of the Armillaria cepistipes - A. gallica complex in the Czech Republic and Slovakia. Mycological Progress 8 (3): 259-271.
CrossRef | Gscholar

(3)

Bolla G (2001)
Distribuzione, caratterizzazione e genesi degli orizzonti compatti nei suoli della foresta di Vallombrosa (Firenze). Loro influenza sul ribaltamento dell’abete bianco [Distribution, characterization and genesis of compacted horizons in soils of the Vallombrosa forest (Florence). Their influence on the uprooting of silver fir]. Bachelor’s thesis, Faculty of Agricultural and Forest Science, University of Florence, Italy. [in Italian]
Gscholar

(4)

Cantiani M (1960)
Note sulla diffusione del marciume radicale nelle abetine di Vallombrosa [The extent of root rot in the Abies alba stands of Vallombrosa]. L’Italia Forestale e Montana 15: 122-124. [in Italian]
Gscholar

(5)

Capretti P (1998)
Italy. In: “Heterobasidion annosum: biology, ecology, impact, and control” (Woodward S, Stenlid J, Karjalainen R, Hüttermann A eds). CAB International, Wallingford, UK, pp. 377-385.
Gscholar

(6)

Certini G, Corti G, Ugolini FC (2000)
Influence of soil properties on the mortality of silver fir in Tuscany, Italy. Forstwissenschaftliches Centralblatt 119: 323-331.
CrossRef | Gscholar

(7)

Chirici G, Bottalico F, Giannetti F, Del Perugia B, Travaglini D, Nocentini S, Kutchartt E, Marchi E, Foderi C, Fioravanti M, Fattorini L, Bottai L, McRoberts RE, Corona P, Gozzini B (2018)
Assessing forest windthrow damage using single-date, post-event airborne laser scanning data. Forestry 91 (1): 27-37.
CrossRef | Gscholar

(8)

Cruickshank MG, Morrison DJ, Punja ZK (1997)
Incidence of Armillaria species in precommercial thinning stumps and spread of Armillaria ostoyae to adjacent Douglas-fir trees. Canadian Journal of Forest Research 27 (4): 481-490.
CrossRef | Gscholar

(9)

Delatour C, Von Weissenberg K, Dimitri L (1998)
Host resistance. In: “Heterobasidion annosum: biology, ecology, impact, and control” (Woodward S, Stenlid J, Karjalainen R, Hüttermann A eds). CAB International, Wallingford, UK, pp. 143-166.
Gscholar

(10)

Farina P, Capretti P, Mugnai L (1990)
Gruppi intersterili di Heterobasidion annosum: osservazioni nella foresta di Vallombrosa [Intersterility groups of Heterobasidion annosum: an investigation in the forest of Vallombrosa]. L’Italia Forestale e Montana 45 (5): 347-360. [in Italian]
Gscholar

(11)

Garbelotto M, Linzer R, Nicolotti G, Gonthier P (2010)
Comparing the influences of ecological and evolutionary factors on the successful invasion of a fungal forest pathogen. Biological Invasions 12: 943-957.
CrossRef | Gscholar

(12)

Ghelardini L, Pepori AL, Luchi N, Capretti P, Santini A (2016)
Drivers of emerging fungal diseases of forest trees. Forest Ecology and Management 381: 235-246.
CrossRef | Gscholar

(13)

Giorgi F (2006)
Climate change hot-spots. Geophysical Research Letters 33 (8): L08707.
CrossRef | Gscholar

(14)

Gonthier P, Garbelotto M, Nicolotti G (2003)
Swiss stone pine trees and spruce stumps represent an important habitat for Heterobasidion spp. in subalpine forests. Forest Pathology 33: 191-203.
CrossRef | Gscholar

(15)

Gonthier P, Thor M (2013)
Annosus root and butt rots. In: “Infectious forest diseases” (Gonthier P, Nicolotti G eds). CAB International, Wallingford, UK, pp. 128-158.
CrossRef | Gscholar

(16)

Gori Y, Cherubini P, Camin F, La Porta N (2013)
Fungal root pathogen (Heterobasidion parviporum) increases drought stress in Norway spruce stand at low elevation in the Alps. European Journal of Forest Research 132: 607-619.
CrossRef | Gscholar

(17)

Gregow H, Laaksonen A, Alper ME (2017)
Increasing large scale windstorm damage in Western, Central and Northern European forests, 1951-2010. Scientific Reports 7: 46397.
CrossRef | Gscholar

(18)

Guillaumin JJ, Legrand P (2013)
Armillaria root rots. In: “Infectious forest diseases” (Gonthier P, Nicolotti G eds). CAB International, Wallingford, UK, pp. 159-177.
CrossRef | Gscholar

(19)

Guillaumin JJ, Mohammed C, Anselmi N, Courtecuisse R, Gregory SC, Holdenrieder O, Intini M, Lung B, Marxmüller H, Morrison D, Rishbeth J, Termorshuizen AJ, Tirro A, Van Dam B (1993)
Geographical distribution and ecology of the Armillaria species in Western Europe. European Journal of Forest Pathology 23 (6-7): 321-341.
CrossRef | Gscholar

(20)

Haavik LJ, Billings SA, Guldin JM, Stephen FM (2015)
Emergent insects, pathogens and drought shape changing patterns in oak decline in North America and Europe. Forest Ecology and Management 354: 190-205.
CrossRef | Gscholar

(21)

Holuša J, Lubojacký J, Curn V, Tonka T, Lukášová K, Horák J (2018)
Combined effects of drought stress and Armillaria infection on tree mortality in Norway spruce plantations. Forest Ecology and Management 427: 434-445.
CrossRef | Gscholar

(22)

Honkaniemi J, Lehtonen M, Väisänen H, Peltola H (2017)
Effects of wood decay by Heterobasidion annosum on the vulnerability of Norway spruce stands to wind damage: a mechanistic modelling approach. Canadian Journal of Forest Research 47 (6): 777-787.
CrossRef | Gscholar

(23)

Intini MG (1988)
The association of Armillaria ostoyae (Romagnesi) Herink with death of white firs in Italy. Informatore fitopatologico 38 (4): 67-70. [in Italian with English summary]
Gscholar

(24)

IPCC (2014)
Climate change 2014: synthesis report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (Core Writing Team, Pachauri RK, Meyer LA eds). IPCC, Geneva, Switzerland, pp. 151.
Gscholar

(25)

Jankovsky L (2003)
Distribution and ecology of Armillaria species in some habitats of southern Moravia, Czech Republic. Czech Mycology 55 (3-4): 173-186.
Gscholar

(26)

Korhonen K (1978a)
Interfertility and clonal size in the Armillariella mellea complex. Karstenia 18: 31-42.
CrossRef | Gscholar

(27)

Korhonen K (1978b)
Intersterility groups of Heterobasidion annosum. Communicationes Instituti Forestalis Fenniae 94: 1-25.
Online | Gscholar

(28)

Korhonen K, Delatour C, Greig BJW, Schönhar S (1998)
Silvicultural control. In: “Heterobasidion annosum: biology, ecology, impact, and control” (Woodward S, Stenlid J, Karjalainen R, Hüttermann A eds). CAB International, Wallingford, UK, pp. 283-313.
Gscholar

(29)

Kubiak K, Zólciak A, Damszel M, Lech P, Sierota Z (2017)
Armillaria pathogenesis under climate changes. Forests 8 (4): 100.
CrossRef | Gscholar

(30)

La Porta N, Capretti P, Thomsen IM, Kasanen R, Hietala AM, Von Weissenberg K (2008)
Forest pathogens with higher damage potential due to climate change in Europe. Canadian Journal of Plant Pathology 30 (2): 177-195.
CrossRef | Gscholar

(31)

Lionello P, Malanotte-Rizzoli P, Boscolo R (2006)
Mediterranean climate variability. Elsevier, Amsterdam, the Netherlands, pp. 438.
Online | Gscholar

(32)

Lochman J, Sery O, Jankovsky L, Mikeš V (2004a)
Variations in rDNA ITS of Czech Armillaria species determined by PCR and HPLC. Mycological Research 108 (10): 1153-1161.
CrossRef | Gscholar

(33)

Lochman J, Sery O, Mikeš V (2004b)
The rapid identification of European Armillaria species from soil samples by nested PCR. FEMS Microbiology Letters 237: 105-110.
CrossRef | Gscholar

(34)

Manion PD (1981)
Tree disease concepts. Prentice Hall, New York, USA, pp. 399.
Gscholar

(35)

Moriondo F, Tiberi R (2000)
Aspetti fitopatologici delle abetine di Vallombrosa [Phytopathological aspects of silver fir stands in Vallombrosa]. L’Italia Forestale e Montana 55 (6): 369-380. [in Italian]
Gscholar

(36)

Mugnai L, Capretti P (1989)
Intersterility groups of Heterobasidion annosum (Fr.) Bref.: some morphological differences in the basidiocarps. Micologia Italiana 3: 87-94.
Gscholar

(37)

Müller MM, Sievänen R, Beuker E, Meesenburg H, Kuuskeri J, Hamberg L, Korhonen K (2014)
Predicting the activity of Heterobasidion parviporum on Norway spruce in warming climate from its respiration rate at different temperatures. Forest Pathology 44 (4): 325-336.
CrossRef | Gscholar

(38)

Niemelä T, Korhonen K (1998)
Taxonomy of the genus Heterobasidion. In: “Heterobasidion annosum: biology, ecology, impact, and control” (Woodward S, Stenlid J, Karjalainen R, Hüttermann A eds). CAB International, Wallingford, UK, pp. 27-33.
Gscholar

(39)

Otrosina WJ, Garbelotto M (2010)
Heterobasidion occidentale sp. nov. and Heterobasidion irregulare nom. nov.: a disposition of North American Heterobasidion biological species. Fungal Biology 114: 16-25.
CrossRef | Gscholar

(40)

Prospero S, Holdenrieder O, Rigling D (2006)
Rhizomorph production and stump colonization by co-occurring Armillaria cepistipes and Armillaria ostoyae: an experimental study. Forest Pathology 36 (1): 21-31.
CrossRef | Gscholar

(41)

Puddu A, Luisi N, Capretti P, Santini A (2003)
Environmental factors related to damage by Heterobasidion abietinum in Abies alba forests in Southern Italy. Forest Ecology and Management 180: 37-44.
CrossRef | Gscholar

(42)

Redfern DB, Ward D (1998)
The UK and Ireland. In: “Heterobasidion annosum: biology, ecology, impact, and control” (Woodward S, Stenlid J, Karjalainen R, Hüttermann A eds). CAB International, Wallingford, UK, pp. 347-354.
Gscholar

(43)

Sala M, Menguzzato G, Capretti P (1995)
Attacchi di Heterobasidion annosum in piantagioni di douglasia [Attacks by Heterobasidion annosum to Douglas-fir stands]. Annali dell’Istituto Sperimentale di Selvicoltura 24: 37-48. [in Italian]
Gscholar

(44)

Sedlák P, Tomšovsky M (2014)
Species distribution, host affinity and genetic variability of Heterobasidion annosum sensu lato in the Czech Republic. Forest Pathology 44 (4): 310-319.
CrossRef | Gscholar

(45)

Shaw CG, Kile GA (1991)
Armillaria root disease. Agriculture Handbook 691, USDA Forest Service, Washington, DC, USA, pp. 233.
Gscholar

(46)

Soil Survey Staff (1999)
Soil taxonomy. A basic system of soil classification for making and interpreting soil surveys (2nd edn). Agriculture Handbook Number 436, USDA Natural Resources Conservation Service, US Government Printing Office, Washington, DC, USA, pp. 886.
Gscholar

(47)

StatSoft (2013)
STATISTICA (data analysis software system), version 12. Web site.
Online | Gscholar

(48)

Svetasheva T (2015)
Armillaria ectypa. The IUCN red list of threatened species 2015: e.T750 97245A75098379.
CrossRef | Gscholar

(49)

White TJ, Bruns T, Lee S, Taylor J (1990)
Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: “PCR protocols: a guide to methods and application” (Innis MA, Gelfand DH, Sninsky JJ, White TJ eds). Academic Press, San Diego, CA, USA, pp. 315-322.
CrossRef | Gscholar

(50)

Yan Y, Li Y, Wang W, He J, Yang R, Wu H, Wang X, Jiao L, Tang Z, Yao Y (2017)
Range shifts in response to climate change of Ophiocordyceps sinensis, a fungus endemic to the Tibetan Plateau. Biological Conservation 206: 143-150.
CrossRef | Gscholar

iForest - Biogeosciences and Forestry

Contents

Search

Journal Info

Journal Subjects and Fields

For Authors

For Reviewers

For Readers

SISEF Publishing

Search iForest Contents