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The impact of volatile signals and cues on the behaviour of aphids and their parasitoids Toby Bruce
Finding hosts in natural habitats:
Insects have evolved remarkable sensory abilities !
Volatile detection elicits behavioural responseThe nervous system provides a simplified representation of the external environment
but perhaps it is not that simple?
Jeanine Linz et al. Proc. R. Soc. B 2013;280:20130626
An insect can map a volatile in 4 dimensions: 3 dimensions of space & fourth dimension of timeBetter sensing has a selective advantage to enhance fitness finding mates & food
Split second decisions
Split second decisions
Insects have sharp spatio-temporal resolution of olfactory signals
How a chemical is perceived depends on space & timeBruce et al. (2005) TRENDS in Plant Science 10: 269
Chemical ecology methodsCollection of volatiles(headspace sampling)
Bioassay (naturals)
GC linked electrophysiology
GC-MS identification of biologically relevant compounds
Bioassay (synthetics)Field testing (trapping experiments or plot trials)
Two hypothesesSpecies-specific odour recognition: host plant odour recognition relies upon taxonomically characteristic volatiles not found in unrelated plant speciesORNPlant VolatileCNS
ORNPlant VolatileCNS
Plant VolatilePlant VolatilePlant VolatilePlant VolatileORNORNORNORN
Bruce et al. (2005) TRENDS in Plant Science 10: 269Ratio-specific odour recognition: plant odour specificity is achieved by a particular ratio between constituent volatiles, distributed generally among plant species
Attraction!Blend makes a difference
Webster et al. (2010) Animal Behaviour 79: 451
Insects have exquisite spatio-temporal resolution of olfactory signals
Insects have exquisite spatio-temporal resolution of olfactory signalsBruce & Pickett (2011) Phytochem. 72: 1605
Riffell et al. (2013) Science 339: 200-204Adaptability in a changing environmentManduca sexta hawkmoths have innate preference for night blooming flowers like jimsonweed
Adaptability in a changing environment !Switch to Agave palmeri if there is a shortage
Detecting host qualityEAG active compounds: 2-pentadecanone, 2-heptanone, phenyl actetic acid, -gurjunene, 2-tridecanone, -cedrene
Drakulic et al. (2015) Applied Environmental Microbiology 81: 3492Volatiles from Fusarium graminearum infested wheat are repellent to grain aphid, Sitobion avenae
A short, sharp shock
Can crops be engineered to release alarm pheromone and repel aphids and attract their enemies?
Aphid Alarm PheromoneAphid Alarm Pheromone
Naturally produced to warn other aphids when they are attacked by a predator
Identified as (E)--farnesene for many economically important aphids
Peppermint plants also naturally produce (E)--farnesene and the gene responsible for its biosynthesis has been isolated.
Aphid Alarm Pheromone
transgenic linewild typeWheat transformed with targeted synthase gene emits (E)--farnesene
Bruce et al. (2015) Nature Scientific Reports 5: 11183
Aphids repelled by volatiles of transformed wheatP = 0.010P < 0.001treatedtreatedcontrolcontrol
Parasitoid wasps spent longer foraging on transformed plants*transgenic lineswild typeBruce et al. (2015) Nature Scientific Reports 5: 11183
Pest Managementrepel pests
attract their enemies
Field trialField trialField trial
Long-term exposure
Bruce et al. (2015) Scientific reports 5: 11183
Same for parasitoids
Bruce et al. (2015) Nature Scientific Reports 5: 11183
Crop protection
The Challenge:
Can pest management become symbiotic?From an ecological and evolutionary point of view, perhaps easier to work with beneficial insects than against pest insects?
Challenging assumptionsInnate responses of insects to odors can be exploited for pest management
but to what extent are responses innate?
should cues be associated with fitness?
https://thelifeofyourtime.wordpress.com/2011/11/13/plant-insect-interaction-parasitoid-wasps-on-goldenrod/
Biological control of pests - either by release in glasshouses or encouraging natural populations outside.
Biocontrol in edible protected crops 2010/11 (UK)Aphidius ervi used on 2072 ha: 350 ha tomatoes, 131 ha of cucumbers, 1511 ha of peppers
Data from Fera Pesticide Usage survey (ha are treated hectares and include repeat treatments)Aphidius colemani used on 3160 ha: 2235 ha peppers, 487 ha of cucumbers, 426 other vegetables
BiocontrolProven success in greenhouses with artificial release
Conservation biocontrol strategies needed in outdoor cropping environmentsGrowth rate and arrival rate slower than pestsCan arrival be speeded up?
Conservation biocontrol - preserving what is already out there
1= (E)--ocimene; 2= -terpinolene; 3= -caryophyllene; 4= humulene; 5= (E)-4,8-dimethyl-1,3,7-nonatriene; 6= -cedrene; 7= hexanal; 8= (E)-2-hexenal; 9= (Z)-3-hexen-1-ol; 10= (Z)-3-hexen-1-yl acetate ; 11= 5,7,2,4-tetrahydroxy-6-(3-methylbut-2-enyl)isoflavanone (uncinanone A); 12= 4,5-dihydro-5,2,4-trihydroxy-5-isopropenylfurano-(2,3;7,6)-isoflavanone (uncinanone B); 13= 4,5-dihydro-2-methoxy-5,4-dihydroxy-5-isopropenylfurano-(2,3;7,6)-isoflavanone (uncinanone C), and 14= di-C-glycosylflavone 6-C--L-arabinopyranosyl-8-C--D-glucopyranosylapigenin.
Khan et al. (1997) Nature 388: 631-632Khan et al. (2010) J. Exp. Bot. 61: 4185
Classic example: Effective recruitment of biocontrol in Push-pull
Volatiles from winter host repel summer forms1) 5-methylfurfural 2) 1-octen-3-ol 3) -pinene 4) chrysanthenone 5) methyl salicylate 6) cis-jasmone 7) caryophyllene 8) (E)--farnesene
cis-Jasmonecis-Jasmone
36
cis-Jasmone
stress related volatile plant activator that induces defence mechanismsbiological effects observed >24h after spraying plants with cis-jasmone
Grain aphid Sitobion avenaeBiological effects (treated wheat):volatile production changes and repels aphidsaphid settlement is significantly reduced aphid growth and fecundity is reducedaphid infestation is reduced in wheat field trialsaphid parasitoids attracted to volatiles and forage longer
Arabidopsis :
Upregulated sequences OPR1/2Cell wall biosynthesis genesCytochrome P450 (e.g. CYP81D11)F-box containing proteinNo induction of:Defence genes (PR proteins, etc.)Stress genes (HSPs, etc.)Jasmonate-regulated genes (OPR3, LOX)
Control cis-J meth-JSwitches on plant gene expression
cis-Jasmone
significantly longer time spent on induced plants
0510152025TreatedControlmin
Aphidius ervi foraging on cis-Jasmone treated wheat
Reduction in aphid numbers
Bruce et al. 2003 Pest Management Science 59 1031
Arabidopsis - Myzus persicae Aphidius erviBruce et al. 2008 PNAS 105: 4553-4558
cis-Jasmone upregulated sequences: OPR1/2 Cell wall biosynthetic genes Cytochrome P450 (CYP81D11) F-box containing protein
Sequences unaffected by cis-jasmone: Defence genes (PR proteins, etc) Stress genes (HSPs, etc) Jasmonate-regulated genes (OPR3, LOX)Arabidopsis microarray analysis
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Aphidius ervi responses to CYP81D11 overexpressing plants
Bruce et al. 2008 PNAS 105: 4553-4558
Pheromone impact period
Aphid load reduced by half
Aphid load reduced by half
Pheromone impact period
JuneJulyAug
p