Jianqing Ding, Wei Huang and Yi Wang Invasion Biology and Biocontrol …jianqing-novel_biotec... · Novel biotic interactions between invasive plants and herbiviores: implications

Novel biotic interactions between invasive plants and herbiviores: implications for biological

control

Jianqing Ding, Wei Huang and Yi Wang

Invasion Biology and Biocontrol Lab,

Wuhan Botanical Garden/Wuhan Botanical Institute, Chinese Academy of Sciences

In collaborations withEvan Siemann, Juli Carrillo, Department of Ecology and Evolutionary Biology, Rice University

Greg Wheeler, Invasive Plant Research Laboratory, United States Department of Agriculture, Agricultural Research Service,

Jianwen Zou, College of Resources and Environmental Sciences, Nanjing Agricultural University

• Introduced insects establish populations well, impact is not sufficient

• Need to improve our ability to predict control efficacy prior to release

• Biotic and abiotic factors affecting interactions between invasive plants and herbivores

Why low success rate?

• “Enemy release” hypothesis (Elton 1958, Maron and Vila 2001) : exotic plants escaped suppression from natural enemies in their native range

• Insect communities: Native range: specialist and generalist herbivores Invaded range: only generalist, less or no specialist herbivores

Biological invasions: novel biotic interaction

• Evolved increased competitive ability (EICA) hypothesis (Blossey and Nötzold, 1995): exotic plants to reallocate their resources from defense against natural enemies to growth and reproduction

• Defense (due to differing insect community) Changes in resistanceplant trait that reduces the preference or performance

of herbivores Changes in toleranceplant ability to withstand and survive herbivore damage

(compensatory re-growth)

Altered selection in introduced range

• “plants that have evolved increased vigor in the exotic range will experience a particularly fast population build-up of biological control agents.” due to decreased defense

• the impact of insect agents on plant performance “will depend on the levels of resistance and tolerance evolved during the invasion process in the absence of specialist herbivores.”

Based on EICAMüller-Schärer et al. (TREE, 2004) predicted:

1 why a high abundance of some insect biological control agents has been found on invasive populations relative to their abundance in the native range

2 why these high number of insects failed to control the invader

those theories rarely tested in biocontrol programs.

Answers to questions

Case study: Chinese tallow Triadica sebifera

Native to China

Invasive in Southern and Southeastern US

Specialists（only in China)

(Environmental Entomology, 2009; Biological Control, in revision)

Generalists（in both China and the US）

Evolution in invasive Triadica

• Vigor growth• High competitive ability• Increased tolerance to herbivory• Less resistant(Siemann and Rogers 2001, 2003a, b, Siemann et al. 2006;

Rogers and Siemann 2004, 2005, Zou et al. 2008a, b )

(1) Do specialists consume and digest more food oninvasive populations than on native populations?Do generalists show the opposite pattern?(resistance)

(2) Does the plant show different compensatoryresponse to herbivory by specialists andgeneralists? (tolerance)

Questions: plant defense to generalist vs. specialists

Question 1: Resistance

Lab and field common garden tests: generalist andspecialist caterpillar

development of larvae reared on invasive/native plantleaves;

leaf biomass/areas consumed; leaf tannin and otherchemicals content

Experimental design

SpecialistGeneralist

%

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%

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%

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%

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%

%%

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%%

%%

% %%

%

%%

%X

OK

FL

ALGA

AR

LA

NCTN

MSSC

TX

##

#

##

#

##

#

#

##

#

#

#

#

#

#

Anhui

Zhejiang

Jiangsu

Fujian

Jiangxi

GuangdongGuangxi

Hunan

Hubei

Henan

Guizhou

Taiwan Six populations from China

Six populations from US

(After Evan Siemann)

Results: plant resistance

0

0.1

0.2

0.3

0.4

0.5

Generalist Specialist

Las

t ins

tar

larv

al b

iom

ass (

g) InvasiveNative

n.s.

﹡﹡

﹡

A

C

﹡


0

5

10

15

20

25

30


Lar

val g

row

th r

ate

(mg/

d)n.s.

﹡0

0.1

0.2

0.3

0.4

0.5


Las

t ins

tar

larv

al b

iom

ass (

g) InvasiveNative

n.s.

﹡﹡

﹡

A

C

﹡


n.s.

0

5

10

15

20

25

30

Generalist SpecialistL

eaf m

ass c

onsu

med

(mg/

d)

n.s.

﹡0

5

10

15

20

25

30


Lar

val g

row

th r

ate

(mg/

d)n.s.

﹡0

0.1

0.2

0.3

0.4

0.5


Las

t ins

tar

larv

al b

iom

ass (

g) InvasiveNative

n.s.

﹡﹡

﹡

A

C

﹡


n.s.

0

5

10

15

20

25

30

Generalist SpecialistL

eaf m

ass c

onsu

med

(mg/

d)

n.s.

﹡0

5

10

15

20

25

30


Lar

val g

row

th r

ate

(mg/

d)n.s.

﹡0

0.1

0.2

0.3

0.4

0.5


Las

t ins

tar

larv

al b

iom

ass (

g) InvasiveNative

n.s.

﹡﹡

﹡

A

C

﹡

Invasive low resistance to specialist; no difference for generalist

(Journal of Ecology, 2010)

0

2

4

6

8

10

12

14

1 2 3 4

Tann

in co

nten

t (m

g / g

DW

)

Seedlings age (Year)

InvasiveNative *

***

*

Results: secondary chemistry

High tannin content in invasive populations(Journal of Ecology, 2010)

Question 2: ToleranceField common garden tests: generalist and specialistcaterpillar

place larvae on invasive/native plant seedlings for 10 days;

plant re-grow after herbivory for 100 days

plant growth

Experimental design

Results: plant tolerance

0

8

16

24

32

40

No-herbivory Herbivory

Tot

al b

iom

ass (

g)InvasiveNative

0

30

60

90

120

150


Stem

hei

ght (

cm)

B

a

c

aa

ab

b b

Generalist

Generalist

c


0

8

16

24

32

40


Tot

al b

iom

ass (

g)InvasiveNative

0

30

60

90

120

150


Stem

hei

ght (

cm)

0

30

60

90

120

150


Stem

hei

ght (

cm)

0

8

16

24

32

40


Tot

al b

iom

ass (

g)

a bc

a

c d

aa

ab

b b

bc

ba



Invasive plants bigger than natives(Journal of Ecology, 2010)



c

0

0.2

0.4

0.6

0.8

1T

oler

ance

scor

e

Generalist Specialist Generalist Specialist

Invasive Native

c c

ba

Tolerance score was calculated as the ratio of fitness (the total biomass) for damaged plants divided by the mean value of undamaged control in the same herbivore treatment in the common garden experiment.

Invasive plants better tolerate herbivory

(Journal of Ecology, 2010)

Summary• Invasive Triadica populations had lower resistance and higher

tolerance to the specialist caterpillar, compared to native populations.

• With respect to the response to the generalist caterpillar,invasive populations had greater tolerance as was the case for the specialist. No differences in resistance for introduced versus native populations.

• Plants from invasive populations have altered chemistry that has a larger impact on specialist resistance than on generalist resistance.

(3) Will insect population build-up be faster oninvasive plant populations than on those fromnative populations (lower resistance in theintroduced range) ?

(4) Under the same herbivore load will invasivepopulations perform better than nativepopulations (higher tolerance in the introducedrange) ?

Questions: biological control of Triadica

Predict potential biological control impactField common garden tests: leaf-rolling weevil

release weevils

(different density)

on caged plants

weevil numbers;

(question 3)

plant growth

(question 4)

Leaf-rolling weevil Heterapoderopsis bicallosicollis

Results: weevil populations

High Insect population on invasive plants than on natives


cc c

ba

0

2

4

6

8

10

12

Num

ber o

f wee

vil

Invasive Native

0

2

4

6

8

10

12N

umbe

r of w

eevi

l

A one pair

B two pairs

Jul 29 Aug 26 Sep 23 Oct 21 Dec 03

0

2

4

6

8

10

12

Num

ber o

f wee

vil

Invasive Native

0

2

4

6

8

10

12N

umbe

r of w

eevi

l

A one pair

B two pairs

Jul 29 Aug 26 Sep 23 Oct 21 Dec 03

Invasive

Native

(Ecological Applications, preprint, 2010)

Results: plant growth

Invasive plants always grow better than natives,

regardless of insect number


Weevil number2 4 6 8

potential biological control impact

Field common gardentests:

larval numbers; 0, 4, 8per seedling

plant fitness

Caterpillar Gadirtha inexacta

potential biological control impact

Field common gardentests:

larval numbers; 0, 4, 8per seedling

plant fitness

Caterpillar Gadirtha inexacta


y = -0.337x + 18.663

y = -0.421x + 15.122

8

12

16

20

0 2 4 6 8 10

Tota

l bio

mas

s (g

)

Invasive/Light Native/Light

y = -0.346x + 86.872

y = -1.4x + 77.544

60

70

80

90

100

0 2 4 6 8 10

Larval number

Hei

ght (

cm)

(a)

(b)

y = -0.337x + 18.663

y = -0.421x + 15.122

8

12

16

20

0 2 4 6 8 10

Tota

l bio

mas

s (g

)

Invasive/Light Native/Light

y = -0.346x + 86.872

y = -1.4x + 77.544

60

70

80

90

100

0 2 4 6 8 10

Larval number

Hei

ght (

cm)

(a)

(b)

Invasive

Native

Invasive

Native

Summary• Weevils (potential biocontrol agent) achieved greater

population densities when they fed on invasive trees than on natives, due to lower resistance of the invasive populations.

• Invasive plants had greater herbivore tolerance such that the impact of both potential insect agents (weevil and moth) on plant performance was lower than on native populations (despite higher herbivore loads on those plants).

Discussions: novel interactions• Differences in selective pressures between ranges have

caused dramatic reductions in resistance to specialist herbivores and those changes in plant secondary chemistry likely underlie these differences.

• Increase in tolerance to herbivory appears to (at least partly) reflect an increase in growth rate in the introduced range.

• Greater tolerance to generalist herbivores suggests the possibility of selection for traits that allow plants to tolerate generalist herbivores more than specialist herbivores.

Implications for biological control• Reduced resistance and increased tolerance to herbivory in

introduced populations mayimpede success of biological control, although the insects can reach high density.

• To improve the prediction of insect impact, biological control practitioners should

include plants from the introduced range in the pre-release evaluation and examine novel interactions of insects and invasive populations.

Acknowledgements

The 100 Talent Program of the Chinese Academy of Sciences The US National Scientific Foundation USDA Agricultural Research Service and Forest Service

Thanks

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Jianqing Ding, Wei Huang and Yi Wang Invasion Biology and Biocontrol …jianqing-novel_biotec... · Novel biotic interactions between invasive plants and herbiviores: implications