Ecological basis of the relationship between forest diversity and resistance to pest insects
Hervé JACTEL, INRA, France The functional significance of biodiversity in ecosystems
The idea that the number of species can influence ecosystem functioning is an old (Darwin, 1859) but still central issue in ecological sciences (Tilman et al. 1996, McCann 2000, Loreau et al. 2001, Worm & Dufy, 2003)
Pioneer studies demonstrated that ecosystem productivity increased with species richness (Hector et al. 1999) The functional significance of biodiversity in ecosystems
However, enhanced resource exploitation in higher trophic levels (consumers) can decrease productivity (Loreau et al. 2001, Aoki 2003)
Plant biomass Plant biomass
Species richness Multi-trophic effects Species richness producers modify the diversity – productivity herbivores relationship ?
Plant biomass
?
Species richness producers + herbivores The practical relevance of biodiversity in pest management
Two reviews - cumulating almost 200 studies - showed that diverse agrosystems had lower pest populations than monocultures in 62% of the cases (Risch et al. 1983, Tonhasca & Byrne 1994)
The adoption of monoculture systems has directly led to an increase in the severity of pest in forest crops (Gibson, I.A.S. & Jones, T. 1977)
The dogma stating that risks from pest attacks increase markedly in monocultures is well supported by the literature in tropical forestry (Speight, M.R. 1997) The practical relevance of biodiversity in pest management
The area of single-tree species (plantation) forests is expanding world-wide
200
150
100 million ha 50
0 1975 1980 1985 1990 1995 2000 2005 The practical relevance of biodiversity in pest management
Single-species forests more prone to insect outbreaks than diverse forests ? A new quantitative review to address the question
• data mining - bibliographic data bases, search engines
• meta-analysis - combining results of independent experiments
Unbiased effect size Mean - Mean d = J E C N E ,NC StdevE ,C
C = control group E = experimental group The meta-analysis
• mean damage or abundance • particular insect species (forest pest) • particular tree species single-species stand (E) vs. mixed-species stand (C)
29 experimental studies 28 pest insect species 30 tree species 54 insect - tree interactions
(Jactel, Brockerhoff and Duelli, in press) 25 more damage in the pure stand
20
15
10
5
0 Unbiased Effect Size -5 d++ = + 0.66 -10 0.32 < d ++ < 1.00 fail safe = 438 > 280
è significant increase of forest pest insect damage when a tree species is grown in single-species stands Higher herbivory in forest monocultures: è 3 main ecological mechanisms
1. Host accessibility
2. Impact of natural enemies
3. Host shift 1. Accessibility of host trees
1.1. Increased and prolonged plant availability favors herbivores
eruptive pests, spreading from foci to cover large area bark beetles
Dendroctonus frontalis Dendroctonus micans damage in the same year, in the same stand in pure plots of spruce vs. mixed plots of spruce + fir
120
100
80
pure spruce 60 mixed spruce + fir
total attacks 40
20
0 1 2 3 4 5 6 7 8 9 10
N = 10 pairs Paired sample t test Class variable: plot purity t = 2.61 , P = 0.028
After data from Granet & Perrot (1977) 70%
60%
50%
40%
30%
attacked spruce trees 20% 90-100% 80-90% 70-80% proportion of spruce trees
è More attacked trees in plots where the host resource is more concentrated 1. Accessibility of host trees
1.1. increased and prolonged plant availability 1.2. lack of physical barriers favors host tree colonisation
• no restriction of pest dispersal wind-dispersed larvae (scale insects, gypsy moth, winter moth, spruce budworm)
• no interruption of visual cues recognition of tree silhouette Acacia processionary moth Thaumetopoea pityocampa Ochrogaster lunifer 1. Accessibility of host trees
1.1. increased and prolonged plant availability
1.2. lack of physical barriers
1.3. lack of chemical barriers favors host tree localization
• uniform olfactory signals more easily located • no chemical inhibition by repellent stimuli of associated plants bark beetles, stem borer Preventing bark beetle attacks of maritime pine logs with Non-Host Volatiles extracted from birch (Betula pendula)
Ips sexdentatus
Repellents around Birch trunks around pine logs a pheromone trap Effect of birch volatiles on Ips sexdentatus attacks on maritime pine logs (Jactel et al. 2003)
5
4
3
2
1
0 Bark beetle attacks per log 3.6 6 control 15.6 18 birch 30 Release rate of non-host volatiles (mg/day) 1. Accessibility of host trees
1.1. increased and prolonged plant availability
1.2. lack of physical barriers
1.3. lack of chemical barriers
1.4 lack of temporal barriers favours adjustment of life cycles
coincidence between insect and host plant phenology egghatch and budburst (Tortrix viridana) Population dynamics of green leaf-roller: coincidence with host phenology
Tortrix viridana egg-hatching budburst
time Quercus pubescens Quercus ilex
DuMerle & Mazet, 1983 2. Lack of stable populations of natural enemies
2.1. fewer alternative hosts or prey for parasitoids & predators lower abundance of prey (predators), lower diversity of hosts (parasitoids) temporal misfits with arrival or seasonal increase of the pest
2.2. lack of shelter or refuges overwintering or oviposition sites buffers against high temperature, low humidity
2.3. lack of critical food supply nectar, pollen, honeydew increase parasitoid longevity and fitness The maritime pine bast scale Matsucoccus feytaudi causes more damage in pure maritime pine stands than in maritime pine – black pine mixtures
pure Maritime pine Maritime pine + Black pine
50 45 40 35 30 25 20 15
Density of larvae/dm² 10 5 0 Olmi Capella Col de Prato Morosaglia Scala Regina Popolasca Elatophilus nigricornis (Anthocoridae) can prey on both Matsucoccus pini (Black pine) and Matsucoccus feytaudi (Maritime pine)
pure Maritime pine Maritime pine + Black pine
250
200
150
Anthocoridae 100
50
Capture 0 Olmi Col de Prato Morosaglia Scala Popolasca Capella Regina Effect of provision of food on longevity of bark beetle parasitoids
water water + honey
100 90 80 70 60 50 40 30 20 longevity (days) 10 0 Dendrosoter Dendrosoter Metacolus caenopachoides protuberans unifasciatus
Mendel 1988 3. Host shifts during pest dynamics
3.1. Heteroecious pests Adelges cooleyi 2 host species needed to complete life cycle fir + spruce
Adelgids
Pachypappa tremulae: spruce + aspen Prociphilus fraxini: fir + ash Pemphigus bursarius: poplar + grasses
SUCCESSION 3. Host shifts during pest dynamics
3.1. Heteroecious pests 3.2. Diversion to other, more palatable tree species mixture of more susceptible host trees & low population of polyphagous pest
Less susceptible tree species More susceptible tree species
Low population of pests
DIVERSION Amblypelta cocophaga in Eucalyptus deglupta Bigger 1985
45%
40%
35%
30%
% attacked trees 25%
20% Pure Eucalypt Eucalypt + native shrubs 3. Host shifts during pest dynamics 3.1. Heteroecious pests 3.2. Diversion process 3.3. Contagion from other, more palatable tree species mixture of more susceptible host trees & high population of polyphagous pest
Less susceptible tree species More susceptible tree species
High population of pests
CONTAGION Fall cankerworm, Alsophila pometaria in pure Populus vs. Populus + Acer negundo
White & Whitham, 2000
45 40 35 30 25 20
% defoliation 15 10 5 0 Pure cottonwoods Mixture Cottonwoods + Box elder Tree diversity – pest resistance relationship: the exception of the polyphagous insects
Oligophagous insects Polyphagous insects
25 25 d++ = 0.03 d++ = 1.28 * 20 20
15 15
10 10 Effect size 5 5
0 0
-5 -5 Presence in the mixture of other host trees more susceptible to polyphagous pests 2
1
0 Unbiased effect size -1 no or less more susceptible susceptible hosts hosts Tree Diversity – Pest Resistance : The ecological mechanisms
High diversity of tree species
Non host tree species Habitat / natural enemies Other host tree species
Reduce Provide Provide shelters, Provide more Provide host tree physical alternative preys, susceptible alternative availability or chemical supplementary hosts hosts barriers food
1 2 3 4 5 6 Limit resource Disrupt host Improve Lead to Lead to Lead to exploitation colonisation bio-control diversion contagion succession
î pest outbreaks ì pest outbreaks Up-scaling the tree diversity – pest resistance relationship to the landscape level
Forest: mosaic of stands = habitat patches
Forest insects : meta-population dynamics
populations distributed among patches of suitable habitat, separated by unfavourable areas
Does habitat diversity (landscape heterogeneity) influence forest resistance to pest insects ? Comparison of pure stands within monoculture vs. surrounded by non-habitat patches
Spruce budworm
Non-habitat: deciduous forest Habitat: Conifer dominated forest Habitat: Balsam fir stand Spruce budworm, Choristoneura fumiferana Balsam fir, Abies balsamea (10 pairs) Cappuccino et al. 1998
80% 70% 60% 50% 40% 30% 20% Tree mortality 10% 0% Coniferous forest Habitat islands Paired comparisons of pure stands: bordered by a non-habitat patch vs. among monoculture
Non-habitat: oak stand Habitat: maritime pine monoculture Habitat: Experimental maritime pine stand Dioryctria sylvestrella, the pine stem borer Pinus pinaster, maritime pine (4 pairs, 4224 trees) Jactel et al. 2002
50% b b 40% b a 30% a a 20% a a
10% % attacked trees
0% Nezer Le Bray Malakoff Castillonville
edged by mixed species stand of broad-leaved trees control Ecological mechanisms 1. Habitat accessibility
Grid (400m x 400m) sampling of bark beetles in a 1000 ha maritime pine forest (July 2003) Ecological mechanisms 1. Habitat accessibility
300 y = 119,78e0,8158x R2 = 0,929
250
200
32 000 beetles caught sum bark beetle capture / trap 150 40% 50% 60% 70% 80% 90% 100% % habitat (maritime pine) in a 200m radius
è The population level of Ips sexdentatus in 53 sampled plots increased with habitat concentration around the plots Ecological mechanisms 2. Impact of natural enemies
bordered by oak stand bordered by pine stand bordered by oak stand bordered by pine stand
25 40%
20 30%
D. sylvestrella 15 20%
10
Macrocentrus 10% 5 % attack parasited by
0 0%
% attacked trees by Lemenage Malakof1 Pontenx8 Lemenage Malakoff1 Pontenx8
Macrocentrus sylvestrellae (Braconidae) specific parasitoid of Dioryctria sylvestrella
M. sylvestrellae larvae Ecological mechanisms 2. Impact of natural enemies
Effect of diet composition on Macrocentrus sylvestrellae longevity
18 a 16 14 b 12 10 8 cd c 6 cde cde
longevity (day) e de 4 2 0 Erica tetralix Achillea Water Erica cinerea Frangula Castanea Honey Oak Aphid millefolium alnus sativa Honeydew 3 main ecological mechanisms at both stand and landscape levels
1. Host / Habitat accessibility host / non host tree availability (stand purity) habitat / non habitat availability (landscape heterogeneity)
barriers to host tree colonisation barriers to habitat colonisation (connectivity)
2. Impact of natural enemies Alternative prey, food supplementation or complementation Habitat supplementation or complementation
3. Host / Habitat shift for polyphagous insects diversion – contagion between more and less susceptible host species diversion – contagion between more and less suitable habitats Tentative conclusions
1. Overall, tree diversity reduces outbreaks of insect herbivores
2. A major exception: high populations of polyphagous pests and associations of susceptible tree species
3. Complex ecological mechanisms
4. Likely to apply at the landscape level
5. Implications for pest control in plantation forests: preservation / restoration of mixed-species woodlands IUFRO Unit 8.07.02 Biodiversity effects on forest pest dynamics
Coordinator: Hervé JACTEL, FRANCE Deputy: Eckehard BROCKERHOFF, NEW ZEALAND The functional significance of biodiversity in ecosystems
Relationship between species richness and productivity in 171 studies (Mittelbach et al., 2001)
productivity
productivity productivity1 productivity hump-shaped
2 3 positive negative diversity
diversity diversity diversity HIGHER BIODIVERSITY
Higher species richness New species composition Higher species richness (species number) (species identity) (species number)
Complementarity Selection (sampling) Antagonism effect effect effect
Niche differentiation Functional dominance Competition Facilitation Allelopathy
Higher ecosystem Lower ecosystem productivity productivity productivity
diversity