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The invasion of the North American
Heterobasidion irregulare
in central Italy
Paolo GONTHIER
University of Turin, Italy
E-mail: paolo.gonthier@unito.it
OUTLINE
• State of the art on Heterobasidion annosum sensu lato
• How it was discovered the introduction of H. irregulare in
Italy
• How H. irregulare was introduced from North America
• The invasion process of H. irregulare in Central Italy
• The hybridization between H. irregulare and H. annosum
• The ability of H. irregulare to colonize unexpected habitats
• Drivers of invasion
• General control strategies
• The research on H. irregulare conducted in the frame of
EMPHASIS
Damages caused by Heterobasidion annosum sensu lato (s.l.)
State of the art on Heterobasidion annosum sensu lato (s.l.)
Modes of infection of Heterobasidion spp.
By Jan Stenlid
Eurasian species
- H. annosum sensu stricto: broad host spectrum, but mostly associated with
the gen. Pinus
- H. abietinum: mostly on Abies
- H. parviporum: on Picea abies
North American species
- H. irregulare: attacks Pinus, Juniperus, Libocedrus
- H. occidentale: broad host spectrum, but mostly associated with Picea,
Abies, Pseudotsuga, Tsuga, Sequoiadendron
State of the art on Heterobasidion annosum sensu lato (s.l.)
The five species
State of the art on Heterobasidion annosum sensu lato (s.l.)
Worldwide distribution of Heterobasidion spp.
Italian stone pine (Pinus pinea L.) mortality centers in
Castelporziano (Rome) in 2002
How was Heterobasidion introduced from Eastern North America?
Heterobasidion resupinate basidioma on a pine board
From The Lancet
Infectious Diseases,
2004
Wood decay Basidiomycota may successfully undergo
intercontinental introductions
LESSON 1
It may take decades for symptoms to become visible
LESSON 2
First symptoms of mortality about
40 yrs after the pathogen
introduction
2002
Samplings of airspora
wood disk exposure method
(Rishbeth, 1959; Gonthier et al., 2001)
5 m
4 wood disks per sampling
point
104 sampling points selected at regular intervals along transects
dissecting the entire length of each forest
Taxon-specific primers
ML5-ML6 DNA region of mt LrRNA nuclear elongation factor 1-α
EU
NA
Isolation and identification of single spore colonies
Heterobasidion irregulare infested sites in Italy
From Gonthier et al.,
Forestry, 2014
Extent of mortality associated with Heterobasidion irregulare
From Gonthier et al., Forestry, 2014
Determining where introduction occurred through a population
genetics approach
1. Evolutionary and invasion theories predict oldest infestation,
i.e. founder population, to be genetically the most diverse
2. Genetic diversity should decrease with increasing distance
from the original introduction site
3. If multiple introductions occurred, then specific alleles would
be exclusively found in some sites
Population genetics I – Determining where introduction occurred
Sequence information from 11
unlinked loci shows genetic
diversity decreases with
increasing distance from
Castelfusano
From Garbelotto et al.,
Mol. Ecol., 2013
Population genetics II – Determining where introduction occurred
Bayesian clustering analysis
using data from 12 SSR loci
shows:
a) most likely numbers
of founding genotypes is 3;
b) all 3 are everywhere,
i.e. no genotype is exclusive to
a single area
From Garbelotto et al.,
Mol. Ecol., 2013
invasion corridors provided not only
by forests, but also by group of trees
1.3 Km yr-1 (Gonthier et al., Mol. Ecol., 2007)
79 km / 61 years
Estimation of the rate of spread of Heterobasidion irregulare
in Italy
*
Capacità di insediamento e di invasione di H. irregulare
Distribution and relative frequency of Heterobasidion irregulare
and H. annosum in coastal pine stands of Central Italy
Gonthier et al., Mol. Ecol., 2007
Spatial autocorrelation analysis of genetic and geographical
distance in Heterobasidion irregulare. Moran’s I-index averaged
over SSR loci. Dashed lines: 95% CI; *** P < 0.001; * P < 0.05.
Estimating the spread potential
From Garbelotto et al., Mol. Ecol., 2013
The spreading potential of wood decay Basidiomycota - like H.
irregulare - may be some tens of kms
LESSON 3
LESSON 4
When a native interfertile fungal species is present in the
invasion area hybridization may occur
Vegetation type
Heterobasidion annosum
Odds ratio and
95% confidence interval
(lower bound; upper bound)
Heterobasidion irregulare
Odds ratio and
95% confidence interval
(lower bound; upper bound)
Mediterranean maquis 0.825 (0.159; 4.294) 1.800 (0.339; 9.551)
Mediterranean
evergreen oak forests
1.636 (0.462; 5.795) 0.469 (0.122; 1.799)
Mediterranean
deciduous oak forests
0.145* (0.250; 0.846) 0.667 (0.115; 3.861)
Italian stone pine
stands
7.704* (1.723; 34.444) 1.556 (0.414; 5.838)
Anthropic or
agricultural areas
1.636 (0.462; 5.795) 0.743 (0.199; 2.779)
GIS analysis – Host-pathogen associations
LESSON 5
Alien pathogens – like H. irregulare - may colonize unexpected
habitats, and this ability may be a trait acquired upon
introduction
2- it is particularly adapted to the new environment: it is a good
saprobe and a high sporulator (high transmission potential)
Hypotheses:
1- it shows a very high pathogenicity on the new hosts
comparative experiments with H. annosum aided at
elucidating the mechanisms of invasiveness
Why is H. irregulare invasive?
Pathogenicity on cuttings of Pinus sylvestris and on seedlings of
P. pinea and P. taeda
0
10
20
30
40
50
60
70
80
90
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27
sizeoflesions(mm)
America Europe Castelporziano
H. irregulare H. annosum H. irregulare
introduced in Italy
0
10
20
30
40
50
60
70
80
90
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27
sizeoflesions(mm)
America Europe Castelporziano
H. irregulare H. annosum H. irregulare
introduced in Italy
Garbelotto et al.,
Biol. Invasions, 2010
Saprobic ability on P. sylvestris logs
After 60 days incubation
Fruiting ability on P. sylvestris logs
Giordano et al.,
Biol. Invasions, 2014
Airspora samplings
0
20
40
60
80
100
Decem ber
05
Septem ber
06
Decem ber
06
Septem ber
07
Winter Sum m er
IF,percentage
H. annosum s.s.
H. annosum P ISG
0
20
40
60
80
100
120
140
December
05
September
06
December
06
September
07
W inter Summer
DR,sporesm2
h-1
H. annosum
H. Irregulare
Kruskal-Wallis test (P<0.05)
Garbelotto et al.,
Biol. Invasions, 2010
LESSON 6
Invasiveness of alien pathogens – like H. irregulare – may be
linked to high transmission potential rather than to high
virulence on naïve hosts
- Complete eradication?
- Minimize the risk of spread outside the current zone
of infestation
How dealing with H. irregulare?
Preventing the establishment of the fungus during its
saprobic phase in a buffer zone (BZ) surrounding the zone of
infestation (ZOI)
Combining actual distribution with estimations of spread rates:
Green = area where H. irregulare should be regarded as already present
Yellow = area where prescriptions are needed to prevent further spread
Zoning of management actions
From Gonthier et al.,
Forestry, 2014
Zoning of management actions
From Gonthier et al., Forestry, 2014
Practical solutions for surveillance and monitoring
Practical solutions for containment and eradication
Isolation, screening and selection of biological control agents for treatments on both pine and oak stumps
Containment: stump treatments
191 fungal isolates grouped into
mycelial morphotypes were
obtained. Screening and
identifications are in progress.
3 Phlebiopsis gigantea isolates
from P. pinea
1 Peniophora sp. from oak
Containment: stump treatments
Urea solution 30% concentration
ready to go
Practical solutions for containment and eradication
Practical solutions for containment and eradication
Demonstration
Stump in situFelling of infected trees
Log chipping – wood chips in situ
Verification of pathogen eradication
(after 12 and 24 months):
•Fruiting bodies
•Viable mycelium
•Airborne inoculum
Local eradication in the case of recently detected populations (including incursions)
Solution 1
Practical solutions for containment and eradication
Stump drillingFelling of infected trees
Log chipping – wood chips in situ
Verification of pathogen eradication
(after 12 and 24 months):
•Fruiting bodies
•Viable mycelium
•Airborne inoculum
Local eradication in the case of recently detected populations (including incursions)
Solution 2
Practical solutions for containment and eradication
Local eradication in the case of recently detected populations (including incursions)
Solution 3
Tree moved and buried in the closest landfill
Uprooting of infected trees
with a tractor
Verification of pathogen eradication
(after 12 and 24 months):
•Fruiting bodies
•Viable mycelium
•Airborne inoculum
Practical solutions for containment and eradication
CONCLUSIONS
Molecular tools allowed to:
- discover the introduction and reconstruct the invasion of
H. irregulare in Europe
- detect and investigate an ongoing hybridization process in
fungi
Molecular tools combined with a number of other tools and
techniques (e.g. GIS, inoculation assays) provided much
insights into the invasion biology and epidemiology of this
forest pathogen
THANKS FOR YOUR ATTENTION
ACKNOWLEDGEMENTS
Dr. Matteo Garbelotto, UC Berkeley
Dr. Luana Giordano, Univ. Turin
Dr. Fabiano Sillo, Univ. Turin
Dr. Guglielmo Lione, Univ. Turin
FUNDING
Italian Ministry of Education, University and Research
European Commission

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The invasion of the North American Heterobasidion irregulare in central Italy

  • 1. The invasion of the North American Heterobasidion irregulare in central Italy Paolo GONTHIER University of Turin, Italy E-mail: paolo.gonthier@unito.it
  • 2. OUTLINE • State of the art on Heterobasidion annosum sensu lato • How it was discovered the introduction of H. irregulare in Italy • How H. irregulare was introduced from North America • The invasion process of H. irregulare in Central Italy • The hybridization between H. irregulare and H. annosum • The ability of H. irregulare to colonize unexpected habitats • Drivers of invasion • General control strategies • The research on H. irregulare conducted in the frame of EMPHASIS
  • 3. Damages caused by Heterobasidion annosum sensu lato (s.l.)
  • 4. State of the art on Heterobasidion annosum sensu lato (s.l.) Modes of infection of Heterobasidion spp. By Jan Stenlid
  • 5. Eurasian species - H. annosum sensu stricto: broad host spectrum, but mostly associated with the gen. Pinus - H. abietinum: mostly on Abies - H. parviporum: on Picea abies North American species - H. irregulare: attacks Pinus, Juniperus, Libocedrus - H. occidentale: broad host spectrum, but mostly associated with Picea, Abies, Pseudotsuga, Tsuga, Sequoiadendron State of the art on Heterobasidion annosum sensu lato (s.l.) The five species
  • 6. State of the art on Heterobasidion annosum sensu lato (s.l.) Worldwide distribution of Heterobasidion spp.
  • 7. Italian stone pine (Pinus pinea L.) mortality centers in Castelporziano (Rome) in 2002
  • 8.
  • 9. How was Heterobasidion introduced from Eastern North America?
  • 11. From The Lancet Infectious Diseases, 2004
  • 12. Wood decay Basidiomycota may successfully undergo intercontinental introductions LESSON 1
  • 13. It may take decades for symptoms to become visible LESSON 2 First symptoms of mortality about 40 yrs after the pathogen introduction 2002
  • 14. Samplings of airspora wood disk exposure method (Rishbeth, 1959; Gonthier et al., 2001) 5 m 4 wood disks per sampling point 104 sampling points selected at regular intervals along transects dissecting the entire length of each forest
  • 15. Taxon-specific primers ML5-ML6 DNA region of mt LrRNA nuclear elongation factor 1-α EU NA Isolation and identification of single spore colonies
  • 16. Heterobasidion irregulare infested sites in Italy From Gonthier et al., Forestry, 2014
  • 17. Extent of mortality associated with Heterobasidion irregulare From Gonthier et al., Forestry, 2014
  • 18. Determining where introduction occurred through a population genetics approach 1. Evolutionary and invasion theories predict oldest infestation, i.e. founder population, to be genetically the most diverse 2. Genetic diversity should decrease with increasing distance from the original introduction site 3. If multiple introductions occurred, then specific alleles would be exclusively found in some sites
  • 19. Population genetics I – Determining where introduction occurred Sequence information from 11 unlinked loci shows genetic diversity decreases with increasing distance from Castelfusano From Garbelotto et al., Mol. Ecol., 2013
  • 20. Population genetics II – Determining where introduction occurred Bayesian clustering analysis using data from 12 SSR loci shows: a) most likely numbers of founding genotypes is 3; b) all 3 are everywhere, i.e. no genotype is exclusive to a single area From Garbelotto et al., Mol. Ecol., 2013
  • 21. invasion corridors provided not only by forests, but also by group of trees 1.3 Km yr-1 (Gonthier et al., Mol. Ecol., 2007) 79 km / 61 years Estimation of the rate of spread of Heterobasidion irregulare in Italy
  • 22. * Capacità di insediamento e di invasione di H. irregulare
  • 23. Distribution and relative frequency of Heterobasidion irregulare and H. annosum in coastal pine stands of Central Italy Gonthier et al., Mol. Ecol., 2007
  • 24. Spatial autocorrelation analysis of genetic and geographical distance in Heterobasidion irregulare. Moran’s I-index averaged over SSR loci. Dashed lines: 95% CI; *** P < 0.001; * P < 0.05. Estimating the spread potential From Garbelotto et al., Mol. Ecol., 2013
  • 25. The spreading potential of wood decay Basidiomycota - like H. irregulare - may be some tens of kms LESSON 3
  • 26. LESSON 4 When a native interfertile fungal species is present in the invasion area hybridization may occur
  • 27.
  • 28.
  • 29. Vegetation type Heterobasidion annosum Odds ratio and 95% confidence interval (lower bound; upper bound) Heterobasidion irregulare Odds ratio and 95% confidence interval (lower bound; upper bound) Mediterranean maquis 0.825 (0.159; 4.294) 1.800 (0.339; 9.551) Mediterranean evergreen oak forests 1.636 (0.462; 5.795) 0.469 (0.122; 1.799) Mediterranean deciduous oak forests 0.145* (0.250; 0.846) 0.667 (0.115; 3.861) Italian stone pine stands 7.704* (1.723; 34.444) 1.556 (0.414; 5.838) Anthropic or agricultural areas 1.636 (0.462; 5.795) 0.743 (0.199; 2.779) GIS analysis – Host-pathogen associations
  • 30.
  • 31. LESSON 5 Alien pathogens – like H. irregulare - may colonize unexpected habitats, and this ability may be a trait acquired upon introduction
  • 32. 2- it is particularly adapted to the new environment: it is a good saprobe and a high sporulator (high transmission potential) Hypotheses: 1- it shows a very high pathogenicity on the new hosts comparative experiments with H. annosum aided at elucidating the mechanisms of invasiveness Why is H. irregulare invasive?
  • 33. Pathogenicity on cuttings of Pinus sylvestris and on seedlings of P. pinea and P. taeda 0 10 20 30 40 50 60 70 80 90 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 sizeoflesions(mm) America Europe Castelporziano H. irregulare H. annosum H. irregulare introduced in Italy 0 10 20 30 40 50 60 70 80 90 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 sizeoflesions(mm) America Europe Castelporziano H. irregulare H. annosum H. irregulare introduced in Italy Garbelotto et al., Biol. Invasions, 2010
  • 34. Saprobic ability on P. sylvestris logs After 60 days incubation
  • 35. Fruiting ability on P. sylvestris logs Giordano et al., Biol. Invasions, 2014
  • 36. Airspora samplings 0 20 40 60 80 100 Decem ber 05 Septem ber 06 Decem ber 06 Septem ber 07 Winter Sum m er IF,percentage H. annosum s.s. H. annosum P ISG 0 20 40 60 80 100 120 140 December 05 September 06 December 06 September 07 W inter Summer DR,sporesm2 h-1 H. annosum H. Irregulare Kruskal-Wallis test (P<0.05) Garbelotto et al., Biol. Invasions, 2010
  • 37. LESSON 6 Invasiveness of alien pathogens – like H. irregulare – may be linked to high transmission potential rather than to high virulence on naïve hosts
  • 38. - Complete eradication? - Minimize the risk of spread outside the current zone of infestation How dealing with H. irregulare? Preventing the establishment of the fungus during its saprobic phase in a buffer zone (BZ) surrounding the zone of infestation (ZOI)
  • 39. Combining actual distribution with estimations of spread rates: Green = area where H. irregulare should be regarded as already present Yellow = area where prescriptions are needed to prevent further spread Zoning of management actions From Gonthier et al., Forestry, 2014
  • 40. Zoning of management actions From Gonthier et al., Forestry, 2014
  • 41. Practical solutions for surveillance and monitoring
  • 42. Practical solutions for containment and eradication Isolation, screening and selection of biological control agents for treatments on both pine and oak stumps Containment: stump treatments 191 fungal isolates grouped into mycelial morphotypes were obtained. Screening and identifications are in progress. 3 Phlebiopsis gigantea isolates from P. pinea 1 Peniophora sp. from oak
  • 43. Containment: stump treatments Urea solution 30% concentration ready to go Practical solutions for containment and eradication
  • 44. Practical solutions for containment and eradication Demonstration
  • 45. Stump in situFelling of infected trees Log chipping – wood chips in situ Verification of pathogen eradication (after 12 and 24 months): •Fruiting bodies •Viable mycelium •Airborne inoculum Local eradication in the case of recently detected populations (including incursions) Solution 1 Practical solutions for containment and eradication
  • 46. Stump drillingFelling of infected trees Log chipping – wood chips in situ Verification of pathogen eradication (after 12 and 24 months): •Fruiting bodies •Viable mycelium •Airborne inoculum Local eradication in the case of recently detected populations (including incursions) Solution 2 Practical solutions for containment and eradication
  • 47. Local eradication in the case of recently detected populations (including incursions) Solution 3 Tree moved and buried in the closest landfill Uprooting of infected trees with a tractor Verification of pathogen eradication (after 12 and 24 months): •Fruiting bodies •Viable mycelium •Airborne inoculum Practical solutions for containment and eradication
  • 48. CONCLUSIONS Molecular tools allowed to: - discover the introduction and reconstruct the invasion of H. irregulare in Europe - detect and investigate an ongoing hybridization process in fungi Molecular tools combined with a number of other tools and techniques (e.g. GIS, inoculation assays) provided much insights into the invasion biology and epidemiology of this forest pathogen
  • 49. THANKS FOR YOUR ATTENTION ACKNOWLEDGEMENTS Dr. Matteo Garbelotto, UC Berkeley Dr. Luana Giordano, Univ. Turin Dr. Fabiano Sillo, Univ. Turin Dr. Guglielmo Lione, Univ. Turin FUNDING Italian Ministry of Education, University and Research European Commission