Disease and Insect Effects on Ecosystem Processes

in the context of Climate Change

Christa MulderUAF

Conceptual Overview

Herbivores and

Pathogens

Plant populations (mortality, growth rates)

Community composition

Ecosystem Processes

Climate Change

Dominant or keystone

Δ competition or facilitation

Herbivores and

Pathogens

Plant populations (mortality, growth rates)

Community composition

Ecosystem Processes

OUTBREAK SPECIES

Dominant or keystone

Herbivores and

Pathogens

Plant populations (mortality, growth rates)

Community composition

Ecosystem Processes

NON-OUTBREAK SPECIES

Δ competitionor facilitation

Δ abundancedominant or keystone

Overview

Outbreak species:1) Alder (Alnus tenuifolia) and canker2) Spruce and spruce budworm3) Aspen and leafminer

Non-outbreak species: parasite communities on…1) Alder (Alnus viridis)2) Cranberry (Vaccinium vitis-idaea)3) Rose (Rosa acicularis)

0 1 2 3 4 5 6 7 8 9 10

DBH Diameter Class (cm)

0

500

1000

1500

Den

sity

(st

ems

ha-1

)

Quartz Creek - Kenai Region

Live without cankerLive with cankerDead from cankerOther dead

719 stems / 3 plots

0

20

40

60

80

100

Pro

port

ion

Infe

cted

or

Dea

d (%

)

0 1 2 3 4 5 6 7 8 9 10

DBH Diameter Class (cm)

0

1000

2000

3000

4000

Den

sity

(st

ems

ha-1

)

Alder Shrub - Tanana River

Live without cankerLive with cankerDead from cankerOther dead

1745 stems / 3, 18X18 m plot

0

20

40

60

80

100

Pro

port

ion

Infe

cte

d or

Dea

d (%

)

0 1 2 3 4 5 6 7 8 9 10

DBH Diameter Class (cm)

0

1000

2000

3000

Den

sity

(st

ems

ha-1

)

Alder Shrub - Eagle River Anchorage Basin

Live without cankerLive with cankerDead from cankerOther dead

719 stems / 3 plots

0

20

40

60

80

100

Pro

port

ion

Infe

cte

d or

Dea

d (%

)

2005 Canker (Valsa melanodiscus) Survey on A. tenuifolia

(Roger Ruess and colleagues)

10 30 50 70 90

Proportion of Canopy Dead from Canker (% tree-1)

0

20

40

60

80

100

Pro

po

rtio

n o

f T

ota

l N

od

ule

Bio

mas

s L

ive

(% t

ree

-1)

Eagle RiverQuartz CreekTanana

Y = 96.08 - 0.76 X

r2 = 0.63, P < 0.0001

0 20 40 60 80 100

Proportion of Basal Area Dead from Canker (%)

0

20

40

60

80

100

Pro

po

rtio

n o

f L

eaf

Are

a D

ead

fro

m C

anke

r (%

)

Eagle RiverQuartz CreekTanana

Y = 1.3897 + 0.7187*X

r2 = 0.67, P<0.0001

Effects of canker on whole-stand N inputs are driven by declines in nodule biomass associated with ramet mortality

5

7

9

11

13

N F

ixat

ion

Rat

e (

mo

l N g

no

du

leD

WT

-1 h

r-1)

Eagle River Quartz Creek Tanana

a

b

a

a

0

5

10

15

20

25

Pro

po

rtio

n B

asal

Are

a o

r L

eaf

Are

a D

ead

Fro

m C

anke

r (%

)

% Basal Area Dead% Leaf Area Dead

Eagle River Quartz Creek Tanana

A

b

a

a

A

B

Also appears to be an effect of canker infection on N fixation rate (at the nodule level)

1) Investigate the susceptibility of green alders (Alnus viridis ssp. fruticosa, synonym =A. crispa) to infection by Valsa melanodiscus under water stress.

2) Monitor the response of the water transport system to infection and colonization.

3) Determine if alders respond to disease by adjusting water use efficiency.

4) Measure the effect of disease development on photosynthesis (light saturation pt., quantum efficiency).

An inoculation experiment with Alnus viridis (green alder) and Valsa melanodiscus:Susceptibility to infection and the physiological effects of disease development

(Jenny Rohrs-Richey)

Greenhouse Experiment

June 1

Aug 23

Two Weeks After Inoculation

PycnidiaNecrotic lesion

Water Availability and Disease Incidence

Infected Alders

Well-watered plants are less likely to become infected than water-limited plants(early in the growth season)

Non-infected plants fix more carbon than infectedplants… but only if theyare well-watered.

Stomatal Regulation of Photosynthesis

Spruce bud-worm on white spruce (Picea glauca)

Glenn Juday and colleagues

Date of spruce budworm heat requirement at Fairbanks

158

163

168

173

178

183

188

193

198

1905 1915 1925 1935 1945 1955 1965 1975 1985 1995 2005

year

Juli

an

date

moth @437.4 Linear (moth @437.4)

20042004

199319931995199519881988

19901990

1953?1953? 1975?1975?

Deg. CThreshold = 8.0GDD = 243

BA

RK

BA

RK

20052005

2000

2000

2001

2001

2002

2002

2003

2003

2004

2004

2006

2006

1999

1999

1998

1998

1997

1997

1996

1996

1992

1992

1991

1991

1990

1990

1995199519931993

spruce budwormspruce budwormdamagedamage heat/droughtheat/drought

limitationlimitation

Fairbanks Summer Temperature and W. Spruce Growth (BNZ LTER - 2PLS; 1902:2007; n = 2 trees)

11.0

11.5

12.0

12.5

13.0

13.5

14.0

14.5

15.0

15.5

20071997198719771967195719471937192719171907

year

May:A

ug

T (

de

g.

C)

0.0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.9

1.0

1.1

mean

rin

g-w

idth

(m

m)

3-yr weighted May:Aug Temperature mean tree 5&8

Summer temperature vs. w. spruce growth(Bonanza Creek LTER -2 Parks Loop South; 1906-2006; n = 12 trees)

r2 = 0.32

0.0

0.2

0.4

0.6

0.8

1.0

1.2

9.0 10.0 11.0 12.0 13.0 14.0 15.0 16.0 17.0 18.0 19.0 20.0

previous May:Aug T (deg C)

mean

sam

ple

rin

g w

idth

(m

m)

1912 volcanic 1912 volcanic ash?ash?

1993 & 95 spruce budworm defoliation1993 & 95 spruce budworm defoliation

KILL ZONEKILL ZONE2004 record hot2004 record hot

Aspen leaf miner moth(Phyllocnistis populiella)(Diane Wagner, Pat Doak, Linda DeFoliart, Jenny

Schneiderheinze)

Univoltine

Adults emerge in May

before leaf-out, mate

Lay eggs on both sides of

new leaves

Eggs digest cuticle, sink

into leaf

Aspen leaf miner moth (Phyllocnistis populiella)

Larvae restricted to one

side of leaf

cannot switch sides

cannot exit and reenter

Consume epidermal cells as

move during instars I – III

Separation of cuticle from

mesophyll causes white

appearance of mines

Aspen leaf miner infestation of Alaskan forests

R. Werner, US Forest Service flyovers

1974

1977

1980

1983

1986

1989

1992

1995

1998

2001

2004

2007

AK

are

a in

fest

ed (

ha*1

000)

0

50

100

150

200

250

300

Aspen leaf miner infestation of Bonanza Creek LTER

R. Werner, www.lter.uaf.edu and pers. comm.

0

50

100

150

200

250

300

1975

1977

1979

1981

1983

1985

1987

1989

1991

1993

1995

1997

1999

2001

2003

2005

2007

Year

Asp

en l

eaf

min

ers

(N p

er m

2 fo

liag

e) Aspen leaf miner

Tortrix

Bottom mining reduces photosynthesis

L. Defoliart, Wagner et al. in review

% Mining on leaf bottom

0 20 40 60 80 100

Net

pho

tosy

nthe

sis

(µm

ol C

O2

m-2

s-1

)

0

5

10

15

20

25

Surface mined

Neither Top Bottom

Net

Pho

tosy

nthe

sis

(µm

ol C

O2

m-2

s-1)

0

2

4

6

8

10

Bottom mining reduces photosynthesis

J. Schneiderheinze, Wagner et al. in review

a

a

b

Bottom mining disrupts stomatal function

Wagner, Defoliart, Doak, Schneiderheinze in review

Surface mined

Neither Top Bottom0.00

0.02

0.04

0.06

0.08

0.10

b

aa

Con

duct

ance

(mol

m-2

s-1)

% Bottom mining

0 20 40 60 80 100Le

af

13C

-33

-32

-31

-30

-29

-28

-27

-26

Top mining affects water balance

% Leaf top mined

0 20 40 60 80 100

% L

eaf H

2O

40

45

50

55

60

65

Leaf mining leads to early leaf abscission

Percent leaf mining damage

0 1-25 26-50 51-75 76-100

Dat

e of

leaf

abs

ciss

ion 15

30 5

5

45

16-Aug

1-Sep

16-Sep

1-Oct

16-Oct

Data: L. Defoliart

Mining reduces aspen growth

2005 2006 2007

Dia

met

er

ch

an

ge

(mm

)

0.0

0.2

0.4

0.6

0.8

1.0

Year

2005 2006 2007

BNZ ED

ControlSprayed

Wagner, Defoliart, Doak, Schneiderheinze in review.

Summary

1) Outbreak pathogen (canker) on a keystone shrub species (alder):

• reduces fixation rates of nodules on infected trees• reduces carbon fixation rates via reduced stomatal

conductance• climate change: reduced water availability may increase

susceptibility to this disease

2) Outbreak herbivore on a dominant tree white spruce greatly reduces growth (C fixation)

• Combined with increased temperature could result in massive die-offs

3) Outbreak herbivore reduces photosynthetic rates (C fixation) and stomatal conductance in a dominant tree species (trembling aspen)

Non-outbreak species on leaves(Christa Mulder & Bitty Roy)

Alnus viridis (alder):13 herbivores9 pathogens

Rosa acicularis (rose):11 herbivores13 pathogens

Vaccinium vitis-idaea(cranberry):5 herbivores7 pathogens

Summer temperature and precipitation, 2002-2006

-3

-2

-1

0

1

2

3

4

5

6

may jun

ejul

yau

gm

ay june

july

aug

may jun

ejul

yau

gm

ay june

july

aug

may jun

ejul

yau

g

dif

fere

nce

fro

m l

on

g-t

erm

mea

n t

emp

(C

)

-60

-40

-20

0

20

40

60

80

100

120

dif

fere

nce

fro

m l

on

gte

rm m

ean

p

reci

pit

atio

n (

mm

)

temperature precipitation

2002 2003 2004 2005

A

2006

Winter temperature and snow depths, 2002-2006

-8

-6

-4

-2

0

2

4

6

8

10

oct

dec

feb

apr

oct

dec

feb

apr

oct

dec

feb

apr

oct

dec

feb

apr

oct

dec

feb

dif

fere

nc

e f

rom

lo

ng

term

me

an

te

mp

in

de

gre

es

C

-300

-250

-200

-150

-100

-50

0

50

100

150 dif

fere

nc

e f

rom

lo

ng

term

me

an

sn

ow

de

pth

in

mmtemperature snow depth

2001-2002 2002-2003 2003-2004 2004-2005 2005-2006

B

Total damage patterns 2002-2006

0

5

10

15

20

25

2002 2003 2004 2005 2006

% o

f le

af a

rea

dam

aged

other

pathogen

herbivore

a a bd c d

a a b

a

a

A ALNUS

0

1

2

3

4

5

6

7

8

9

10

2002 2003 2004 2005 2006

% o

f le

af a

rea

dam

age

other

pathogen

herbivore

ab a

c

bc

ab ab

a

ab

bc

b

E VACCINIUM

0

2

4

6

8

10

12

14

16

2002 2003 2004 2005 2006

% o

f le

af a

rea

dam

age

other

pathogen

herbivore

a b b a

ab

bab

a

C ROSA •Fairly constant total biological damage•Relative contribution of herbivores vs. pathogens varies

Herbivory patterns by feeding mode

0

2

4

6

8

10

12

14

16

2002 2003 2004 2005 2006

Per

cen

t o

f le

af a

rea

dam

aged

leafroll

mining

sucking

chewing

a a ab a

a b

a

a

a

a

a

a

b

a

a

a

b

b

a

ALNUSB

0

0.5

1

1.5

2

2.5

3

2002 2003 2004 2005 2006

Per

cen

t o

f le

af a

rea

dam

aged

mining

sucking

chewing

ab a cbc bc

VACCINIUMF

0

1

2

3

4

5

6

7

8

2002 2003 2004 2005 2006

Per

cen

t o

f le

af a

rea

dam

aged

mining

sucking

chewing

ba b b

b

a

a

a

ROSAD

•Fairly low damage in record hot year for all three species•Lowest sucking damage in record hot year for all three species•Highly variable relative contributions by different guilds

Impacts of herbivores and pathogens on reproduction in alder

0

0.5

1

1.5

2

2.5

0 5 10 15 20 25 30 35 40

Herbivore damage (mean % leaf area per tree)

Lo

g10

(m

ean

# c

atki

ns

pe

r b

ran

ch

) female catkinsmale catkins

A

0

0.5

1

1.5

2

2.5

-1 5 10 15 20

Pathogen damage (mean % leaf area per tree)

Lo

g1

0 (

mea

n #

cat

kin

s p

er b

ran

ch)

female catkinsmale catkins

C

Herbivore damage is negatively related to catkin production

Pathogen damage is positively related to catkin production

Woolly alder sawfly, Eriocampa

ovata

Ruess, R. W., M. D. Anderson, J. S. Mitchell, and J. W. McFarland. 2006. Effects of defoliation on growth and N2-fixation in Alnus tenuifolia: Consequences for changing disturbance regimes at high latitudes. Ecoscience 13:402-412.

Mortality in cranberry

• Cranberry ramet mortality rates are high (15-75% over the course of 4-5 years, or 3-15% per year)

• Winter-warm sites had higher rates of mortality and high rates of “red-brown dieback”

• Cause and effect are unclear– Could be physical damage– Could be a disease attacking

already dying leaves– Could be caused by a disease

Climate change and herbivores / pathogens: Alder

Warmer, drier summer conditions may favour pathogens… • Higher pathogen levels in warmer years, and at warmer sites

in 2004 (record hot dry year)• BUT: sucking insects were lower at warm sites or in warm

years

• Cold winters may favour herbivores:higher damage following winters with higher minimum temperatures

Climate change and herbivores / pathogens: cranberry and rose

Cranberry:• Sucking and mining damage were

greater at sites with warmer winter temperatures (in 2004) and in warmer years

Rose:• Between years, total herbivore

damage and sucking damage were lower when summer temperatures were higher

Summary

• TOTAL damage levels are fairly constant across years for all three species

• COMPOSITION of the parasite communities varies greatly between years

• Relationships with environmental characteristics depend on the feeding mode

• For alder, these damage levels may be high enough to substantially reduce N fixation rates

• Cranberry ramet mortality rates are high… but cause is unclear.

Herbivores and

Pathogens

Plant populations (mortality, growth rates)

Community composition

Ecosystem Processes

OUTBREAK SPECIES

Dominant or keystone

Herbivores and

Pathogens

Plant populations (mortality, growth rates)

Community composition

Ecosystem Processes

NON-OUTBREAK SPECIES

Δ competitionor facilitation

Δ abundancedominant or keystone

N fixation, C fixation, transpiration

??

Gaps

• Are the outbreak species fundamentally different from non-outbreak species, or can many of the numerous non-outbreak species become outbreak species with major impacts?

• Loss of dominant species will change species composition… how will that affect ecosystem processes?

• Non-outbreak species: – How does low-level (<20%) damage affect photosynthesis,

water balance, N fixation?– how do they affect community dynamics (composition)? How in

turn does this affect ecosystem processes?

Links to thresholds and regime changes

• Spruce bud-worm: may reduce the temperatures at which massive tree die-offs occur

• Alder and canker: could hot, dry conditions (have) increase(d) susceptibility to the point where outbreaks are possible?

• Could warm winters increase overwintering survival of herbivore species on alder to the point where they become outbreak species?

Links to Invasive Plants• Future research (Mulder lab): how do

biotic factors, including herbivores and pathogens, accelerate or retard the advance of invasives in burned habitat?– Potential for acceleration:

• “Enemy release” from soil pathogens• Introduction of new plant pathogens to natives

– Potential for deceleration:• Herbivory• Pathogens on invasives