Agricultural environments are often simplified with less habitat diversity than natural ecosystems. Furthermore, many of the natural resistance traits that exist in wild plants may have inadvertently been lost while selecting for crop yield and quality in a pesticide-treated background. To reduce pesticide dependency, agriculturalists are faced with the challenge of bringing the resistance mechanisms found in wild plants back into the elite crop cultivars (Bruce, 2012) and improving biocontrol by natural enemies of pests. Reducing the losses to global harvests caused by pests, which remain high even with pesticide use, could provide a tangible way of producing more ‘crop per drop’ or unit area of land.

1. Insect dynamics in agriculture
– can we provide ecological solutions to an
ecological challenge?
Toby Bruce

2. “High yielding varieties”

3. really ?

4. Split second
decisions
Labandeira (2013) Curr.
Opin. Plant Biol. 16:
414
400
MILLION
years

6. Toby J. A. Bruce J. Exp. Bot. 2012;63:537-541
© The Author [2011]. Published by Oxford University Press [on behalf of the Society for
Experimental Biology]. All rights reserved. For Permissions, please e-mail:
journals.permissions@oup.com
Factors influencing crop protection in an agro-ecosystem

7. Promoting
IPM and use
of
alternatives
2009/128/EC on the Sustainable Use of Pesticides
Reducing risks
and impacts of
pesticide use on
human health
and environment
Development of “Alternatives” is urgently
needed

8. Development of “Alternatives” is urgently
needed

12. Why is it needed?

13. New directions for 21st Century Agriculture
Royal Society: “There is a pressing
need for the ‘sustainable
intensification’ of global agriculture in
which yields are increased without
adverse environmental impact and
without the cultivation of more land”.
Royal Society (2009) Policy document 11/09
A second green revolution which is knowledge intensive
rather than input intensive?

14.  Agronomy
 Resistant crops
 Enhancing Biocontrol
 Improved targeting
 RNAi
 Information and data sharing
 Improved targeting
 Intelligent agriculture
Crop protection from pests – new directions are needed

15. Finding prey in natural habitats:
Insects have evolved
remarkable sensory abilities

16. Challenging assumptions
The 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

17. Challenging assumptions
Innate 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/

18. Split second
decisions

19. Insects have sharp spatio-temporal resolution of olfactory signals
How a chemical is
perceived
depends on
space &
time
Bruce et al. (2005) TRENDS in Plant Science 10: 269

20. HO

21. o

22. Ratio matters
-2
-1
0
1
2
3
4
5
6
7
4-comp 5-comp (naturalratio) 5-comp (unnaturalratio)
Timespent(min)
7ng a-pinene
5ng 6-methyl-5-hepten-2-one
10ng 3-carene
4ng acetophenone
4ng 2-dodecanone
7ng a-pinene
15ng 6-methyl-5-hepten-2-one
10ng 3-carene
4ng acetophenone
4ng 2-dodecanone
7ng a-pinene
10ng 3-carene
4ng acetophenone
4ng 2-dodecanone
*
*

23. caryophyllene
humulene
4-allylanisole
cinnamaldehyde
linalool
(E)-ocimene
limonene
myrcene
Ratio matters

24. *
A = unbaited
B = 3-comp blend (natural ratio)
C = 3-comp blend (1: 1: 1, low)
D = 3-comp blend (1: 1: 1, high)
Linalool (600ul/thin/100G) 17.7mg/day
Cinnamyl alcohol (500ul/thin/500G) 0.4mg/day
Cinnamylaldehyde (300ul/thin/2000G) 0.77mg/day
Ratio matters

25. Attraction!
Blend
makes a difference
Webster et al.
(2010) Animal
Behaviour 79:
451

26. Insects have exquisite spatio-temporal resolution of olfactory signals

27. Insects have exquisite spatio-temporal resolution of olfactory signals
Bruce & Pickett (2011) Phytochem. 72:
1605

28. Riffell et al. (2013) Science 339: 200-204
Adaptability in a changing environment
Manduca sexta hawkmoths have
innatepreference for night blooming
flowers like jimsonweed

29. Adaptability in a changing environment !
Switchto Agave palmeri if there
is a shortage

30. Disease influences outcome
Volatiles from Fusarium
graminearum infested wheat
are repellent to grain aphid,
Sitobion avenae
EAG active compounds:
– 2-pentadecanone,
– 2-heptanone,
– phenyl actetic acid,
– α-gurjunene,
– 2-tridecanone,
– α -cedrene

31. The Challenge:

32. Rachel Carson in “Silent Spring”
“A truly extraordinary variety of alternatives to
the chemical control of insects is available.
Some are already in use and have achieved brilliant success.
Others are in the stage of laboratory testing. Still others are little
more than ideas in the minds of imaginative scientists, waiting for
the opportunity to put them to the test. All have this in common:
they are biological solutions, based on the understanding of the
living organisms they seek to control and of the whole fabric of life
to which these organisms belong. Specialists
representing various areas of the vast field
of biology are contributing—entomologists,
pathologists, geneticists, physiologists,
biochemists, ecologists—all pouring their
knowledge and their creative inspirations
into the formation of a new science of
biotic controls.”
Carson, 1962

33. OWBM Resistant varieties
Females lay eggs, but
larvae die when they start to
feed
A wound plug is formed at
the feeding site due to
lignification

34. Resistant varieties
Now approx. 60% of UK wheat is resistant

35. Bruce et al. (2007) Pest Man. Sci. 63: 49
pheromone traps are now
commercially available to wheat
growers in the UK
Monitoring systems
OCOC3H7
OCOC3H7

36. Can we do this?
repel pests
attract their enemies

37. Can pest management become symbiotic?
From an ecological and evolutionary
point of view, perhaps easier to
work with beneficial
insectsthan against pest insects?

38. Biological control of pests - either by release in glasshouses or
encouraging natural populations outside.

39. Aphidius
Aphelinus
Dendrocerus Alloxysta PachyneuronAsaphes
Praon
4th trophic level – pests of the pests of the pests

40. Biocontrol
• Proven success in greenhouses with artificial release
• Conservation biocontrol strategies needed in outdoor
cropping environments
– Growth rate and arrival rate slower than pests
– Can arrival be speeded up?

41. Conservation biocontrol - preserving what is already out there

42. 1= (E)-ß-ocimene;
2= α-terpinolene;
3= β-caryophyllene;
4= humulene;
5= (E)-4,8-dimethyl-1,3,7-nonatriene;
6= α-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-α-L-
arabinopyranosyl-8-C-β-D-
glucopyranosylapigenin.
Khan et al. (1997) Nature 388: 631-632
Khan et al. (2010) J. Exp. Bot. 61: 4185
Classic example: Effective recruitment of biocontrol in Push-pull

43. significantly longer time spent on
induced plants
0
5
10
15
20
25
Treated Control
min
O
Aphidius ervi foraging on cis-Jasmone treated wheat

44. Reduction in aphid numbers
0
0.2
0.4
0.6
0.8
1
1.2
28-May 8-Jun 16-Jun 24-Jun 6-Jul
MeanNo.Aphids/Tiller
0
10
20
30
40
50
60
70
-1 4 9 14 19 24
time after release (h)
%settlement
control
cis-jasmone

45. 0
50
100
150
200
250
300
20-
Jun
27-
Jun
04-
Jul
11-
Jul
18-
Jul
25-
Jul
01-
Aug
CumulativeAphidNos.-75Tillers
Control Pheromone
Pheromone
impact period
Aphid load reduced
by half
0
50
100
150
200
250
300
20-
Jun
27-
Jun
04-
Jul
11-
Jul
18-
Jul
25-
Jul
01-
Aug
CumulativeAphidNos.-75Tillers
Control Pheromone
Aphid load reduced
by half
Pheromone
impact period
June July Aug
p<0.01
Nepetalactone reduced aphid populations in wheat

46. A short, sharp shock…

47. Eβf-wheat
Did it scare the aphids?
Did it attract their enemies?

48. Long-term exposure…
Bruce et al. (2015) Scientific reports 5: 11183

49. Same for parasitoids

50. Do we need to consider the
ecology of insects and
provide cues in a more
realistic setting?
Induced not
always on
Associated with
rewards

51. Smart Cereals – egg induced

52. GC-MS analysis: a = (E)-ocimene, b = (R)-linalool, c = (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT),
d = methyl salicylate, e = decanal, f = methyleugenol, g = (E)-caryophyllene, h = (E)-β-farnesene,
i = (E,E)-4,8,-trimethyl-1,3,7-tridecatetraene (TMTT).
Ecology Letters 14: 1075-1083.
Smart Cereals – egg induced

53. 0 1 2 3 4 5
CKIR12019
CKIR12008
CKIR12003
CKIR06004
CKIR12007
CKIR12004
CKIR12012
CKIR12024
CKIR12010
HB515
CKIR07008
WS505
CKIR12026
CKIR12023
CKIR12009
CKIR12011
CKIR12027
CKIR12021
PH4
CKIR12025
CKIR12018
CKIR12020
CKIR12017
CKIR12014
CKIR12016
CKIR12013
CKIR12006
CKIR12022
SC Duma
CKIR12001
*
*
0 1 2 3 4 5
TRIN24
GUAD14
CUBA85
HAIT19
PANA88
VERA192
BRAZ917
BRAZ1720
BRAZ1470
BRAZ2276
VERA93
BRAZ1006
SOAP GP5
VENE648
HAIT21
SEFENSI
GUAD13
HAIT24
BRAZ1852
KONGERE
ENDERE
JOWI
NYAMULA
CUBA91
ARZM14100
*
*
*
* **
*
*
*
*
**
*
0 2 4 6
CML395
CML204
CML78
CML159
DTPW…
CZL01…
DTPW…
CML488
LPSC7-…
CML202
CML197
CML144
CML441
CZL03…
CML443
CML445
CML440
CML511
CML334
CML312
CKSBL…
CML442
solvent
control
without eggs
with eggs
**
*
landraces hybrids Inbred lines
Time (min)
Time (min)
Time (min)
Cotesia sesamiaeCurrent Opinion in Insect Science (2015) 9: 51 - 55

54. Improved maize line CKIR12001 emits DMNT when
stemborer eggs are laid on it.
HIPV induced by eggs in improved line

55. Underground interactions
Babikova et al. (2013) Ecology Letters 16: 835-43

56. Biocontrol opportunities
 Develop attractants for natural enemies as part of an IPM
strategy - lure and reward
 Develop attractants for pests as part of an IPM strategy -
lure and kill

57. 4-Methylheptane-3,5-dione
Beauveria bassiana spores adhering to
Entostat particles
Sitona lineatus
adults
♂ produced
aggregation
pheromone that
attracts ♀s and
♂s
Team: Toby Bruce (PI), Lesley Smart, Janet Martin
Lure-and-kill of pea and bean weevil, Sitona lineatus

58. Pea and bean weevil,
Sitona lineatus

59. Bruchid beetle,
Bruchus rufimanus

63. 4-methyl-3,5-
heptanedione
The weevil lure – aggregation pheromone
• Male produced
• Attract both sexes of Sitona lineatus

64. Trap catches - weevils
0
100
200
300
400
500
600
700
unbaited polyvial lure test lure 1 test lure 2 test lure 3 test lure 4
Total weevils trapped 9 March to 17 April 2015

65. The kill – Beauvaria bassiana
• Naturally present in the soil
• Shown to kill pea and bean weevil

66. 0
20
40
60
80
100
120
day 2 day 5 day 8 day 12 day 16
untreated insecticide Beauveria strain 1 Beauveria strain 2
%dead Mortality assessment with test formulations

67. Current stage – field testing of prototype inoculation station

68. Wild potatoes resistant to aphids
0
20
40
60
80
100
Desiree Stoloniferum 1 Stoloniferum 2
% Nymph survival - 7 days
Resistant crops

69. Resistant crops

70. TARGET MENTIONS
Aphid 35
Slugs 32
Black grass 30
septoria 27
yellow rust 19
cleavers 16
cabbage stem flea beetle 15
light leaf spot 15
fusarium head blight 14
annual meadow grass 13
brome 13
charlock 13
phoma 13
pollen beetle 12
sclerotinia 12
wild oats 12
chocolate spot 11
brown rust 10
dock 10
early blight (alternaria) 10
bruchid beetle 9
chickweed 9
Nematodes 9
net blotch 9
rhynchosporium 9
cranesbill 8
leatherjackets 8
pea & bean weevil 8
powdery mildew 8
barley yellow dwarf virus (BYDV) 7
broad leaved weeds (generic BLW) 7
crown rust 7
late blight (phytophthora) 7
mayweed 7
orange wheat blossom midge 7
ryegrass 7
thistles 7
turnip yellows virus (TuYV) 7
downy mildew 6
fat hen 6

71. Big data – the power of mapping in time and space
Hugh Oliver-Bellasis, 3 Nov 2015

72. • Can pest management be made more symbiotic?
• Insect responses to volatiles are not fixed
– Timing matters
– Context matters – background odor can be a major issue
• How can we manipulate signalling?
– Sometimes insects make mistakes
e.g. Chilo partellus landing on Napier grass in Push-Pull
e.g. S. mosellana laying eggs on resistant wheat
• How can we manipulate signalling to help beneficials?
– Could ‘honest signalling’ reinforce behaviours?
– Inducible better than consittutive?
– Lure and reward?
• How to make it work in the field??
Conclusions

73. Thanks