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Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1 , Mäntylä E 1 , Ruuskanen S 1 , Li T 2 , Girón- Calva P.S 2 , Huttunen L 1 , Blande J.D 2 , Holopainen J.K 2 , Klemola T 1 1 Department of Biology, University of Turku, Finland 2 Department Environmental Science of University of Eastern Finland, Finland Volatile organic compounds: olfactory foraging cues for insectivorous birds?

Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

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Page 1: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

Tuuli-Marjaana Koski

Department of Biology, University of Turku, Finland

Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen L 1 , Blande J.D 2 , Holopainen J.K 2 , Klemola T 1

1 Department of Biology, University of Turku, Finland2 Department Environmental Science of University of Eastern Finland, Finland

Volatile organic compounds: olfactory foraging cues for

insectivorous birds?

Page 2: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

Introduction•Plant defences

►Direct►Indirect

• E.g. HIPVs=Herbivore-induced

plant volatiles Graph from: Arab A. & Bento J.M.S (2006) Plant Volatiles:

New Perspectives for Research in Brazil,

Neotropical Entomology 35(2):151-158.Plants are ”crying for help”

Page 3: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

Introduction

• Insectivorous birds remove herbivores beneficial to plants

(e.g. Marquis & Whelan 1994; Mäntylä et al. 2011)

Page 4: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

Introduction•Birds are attracted to insect-damaged trees (several studies)

►Without seeing the herbivores

►Without seeing the damages

Page 5: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

Introduction•How birds detect insect-rich trees?

►Two obvious candidates• Vision

• Olfaction

Page 6: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

Introduction

Olfactory cue hypothesis

► Do birds smell HIPVs?

Page 7: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

• Some evidence support this

► Positive correlation between some HIPVs

and bird predation rate towards artificial prey

items (Mäntylä et al. 2008, 2014)

► Bird preference for chemical cues from

larval-damaged trees (Amo et al. 2013)

Page 8: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

Do birds use HIPVs as olfactory foraging cues ?

•Experiments

1. VOC blends to artificial trees (aviary)

2. VOC blends to natural trees (field)

3. Larval-defoliated natural trees (aviary)

Page 9: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

Experiment 1.

1. VOC blends to artificial

trees (aviary)

Page 10: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

VOC blends mimicking herbivory

(terpenes)

VOC blends mimicking mechanical

damage (GLVs)

Aviary

Page 11: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

Control (hexane)

VOC blends mimicking herbivory(terpenes)

Pied flycatcher(Ficedula hypoleuca)

N=20

First choice?

Bird photo: Markus Varesvuo, lintukuva.fi

Numb. of

visits?

Page 12: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

Experiment 1. Results

Page 13: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

0

2

4

6

8

10

12

Terpene VOC blend GLV VOC blend

Nu

mb

er

of b

irds

No difference in first choice

χ2 = 1.00, df = 1, P = 0.32

Page 14: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

No difference in first choice

0

1

2

3

4

5

6

7

Terpene VOC blend Control

Nu

mb

er

of b

irds

Page 15: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

Slight difference in the mean numbers of visits

Wilcoxon signed rank test: S = 35, P = 0.047

Two very active birds out of 20 tested

Page 16: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

Wilcoxon signed rank test S = -10, P = 0.401

No difference in the mean numbers of visits

Page 17: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

Experiment 2.

2. VOC blends to natural

trees (field)

Page 18: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

•The same lab-made VOC blends as in Experiment 1.

► Two silicone tubes per tree• Trees again divided to either “herbivore-”,

“mechanical-” or control blend-treatments

► Four plasticine larvae per tree• Artificial prey for birds

Page 19: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

Silicone tube

Plasticine larva

Photo by Elina Mäntylä

150 trees

Page 20: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

Photos from: Mäntylä E, Alessio GA, Blande JD, Heijari J, et al. (2008) From Plants to Birds: Higher Avian Predation Rates in Trees Responding to Insect Herbivory. PLoS ONE 3(7):1-8.

Page 21: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

Experiment 2.Results

Page 22: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

No difference in probability of bird predation rate

F 2, 145 = 0.8 P = 0.45

Page 23: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

Experiment 3.

3. Larval-defoliated natural

trees (aviary)

Page 24: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

AviaryControlLarval-defoliated

30 30

Great tit, Parus major

First choice?

Blue tit, Cyanistes caeruleus

Numb. of

visits?

Bird photos: Markus Varesvuo, lintukuva.fi; planetscott.com

N = 123

Page 25: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

• Larval-defoliated and control branches were removed before the experiment

• VOC measurements

Page 26: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

Experiment 3.Results

Page 27: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

0

5

10

15

20

25

30

35

40

Larval-defoliated Control

Nu

mb

er

of b

irds

No difference in first choiceχ2 = 1, df =1, P = 0.317

Page 28: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

No difference in number of visits

F 1,119.6 = 0.48, P = 0.488   

Page 29: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

•Significant difference in VOC emissions between larval- defoliation and control treatment among nine compounds

VOCs

Page 30: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

* means p<0.05 and ** means p<0.01

Page 31: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

Conclusions

Page 32: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

•Attraction of insectivorous birds to herbivore-damaged trees has been shown several times

► One study suggest that HIPVs could act as olfactory foraging cues for insectivorous birds

(Amo, L. et al. 2013 ”Birds exploit herbivore-induced plant volatiles to locate herbivorous prey.” Ecology Letters, 16: 1348-1355.)

Page 33: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

• Birds were not interested in HIPVs in our three experiments(apart from two individuals in comparison of number of visits between terpene- and GLV-trees)

► Olfactory cues may not be necessarily behind the attraction of birds to insect-defoliated trees

Page 34: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

• Further studies are needed

► Olfactory foraging behaviour

► Use of vision during foraging

► Olfaction + vision

Page 35: Tuuli-Marjaana Koski Department of Biology, University of Turku, Finland Laaksonen T 1, Mäntylä E 1, Ruuskanen S 1, Li T 2, Girón-Calva P.S 2, Huttunen

AcknowledgementsFunding

► Academy of Finland

► Emil Aaltonen Foundation

► Jenny & Antti Wihuri

Foundation

► UTUGS

► Finnish Cultural Foundation

► Oscar Öflund stiftelse

People

► Ruissalo and Kevo

field teams

► And all the other

people helping in

these experiments

Thank you for your attention!