Soil Ecology and Tree Health: Implications
for Management of Urban Forests and
Ornamental Landscapes
Dan Herms
Department of Entomology
The Ohio State University
Ohio Agricultural Research and Development Center
herms.2@osu.edu
Acknowledgements:
Students and Post-Docs
Jim Blodgett, Rodrigo Chorbadjian, Carolyn Glynn, Bethan
Hale, Nate Kleczewski, Joe LaForest, John Lloyd, Marie
Egawa
Collaborators
Enrico Bonello, Robert Hansen, Harry Hoitink, Bill Mattson,
Ben Stinner
Funding Sources:
TREE Fund
USDA National Urban Community Forestry Advisory Council
The Ornamental Landscape as an Ecosystem:
Implications for Pest Management
Herms et al. (1984) J. Arboriculture 10:303-307.
“Understanding the ecological interactions between
the biotic and abiotic factors within a landscape
enables more effective management of pests.”
Objective:
Understand how trees allocate their resources in
different environments, and the implications for
the care of trees.
Approach:
Develop framework based on carbon allocation that can be
used to predict tree behavior in different environments.
Conduct experiments to test this framework.
Framework: carbon allocation patterns of trees
Herms, D.A. 2002. Effects of fertilization on insect resistance of woody
ornamental plants: reassessing an entrenched paradigm. Environmental
Entomology 31:923-933.
Herms, D.A. 2001. Resource allocation trade-offs in trees.
Arborists News 10(5):41-47.
Herms, D.A. 2001. Fertilization and pest control. Tree Care
Industry 12(5):8-10,12,14.
Herms, D.A. 1998. Understanding tree responses to abiotic and
biotic stress complexes. Arborist News 7(1):9-15.
Herms, D.A., and W.J. Mattson. 1997. Trees, stress, and pests.
pp. 13-25. In J.E. Lloyd, ed. Plant Health Care for Woody
Ornamentals, International Society of Arboriculture, Savoy, IL.
Herms, D.A., and W.J. Mattson. 1992. The dilemma of plants: to
grow or defend. Quarterly Review of Biology 67(3):283-335.
Different patterns of resource allocation and
acquisition work in different environments
Concepts to emphasize:
• resource acquisition vs. resource allocation
• carbon budgets and allocation tradeoffs
• integration of above- and below-ground growth
• acclimation to stressful environments
Resource acquisition vs. allocation
(Income vs. budgeting)
CO 2
G r o w th
Ma in te n a n c e
R e p r o d u c tio n
Sto r a g e
D e fe n s e
Water
Nutrients
Whole plant carbon budget:
• photosynthesis rate per unit leaf area
• total leaf area
Allocation tradeoffs: plants have limited
resources to support:
• growth
• maintenance
• reproduction
• storage
• defense
The chemical arsenal of plants:
defense and stress tolerance
• Tannins
• Phenolic glycosides
• Terpenes
• Alkaloids
• Cyanogenic compounds
• Defensive proteins
Resource allocation patterns
In faster growing plants:
• high allocation to total leaf area
• high photosynthesis rate
• lower allocation to root growth
• lower levels of defensive compounds
In slower growing plants:
• lower allocation to total leaf area
• high photosynthesis rate
• higher allocation to root growth
• higher levels of defensive compounds
Computer-controlled
fertigation system to study
responses of willow to
nutrient availability
Glynn et al. (2007) New Phytologist 176:623-634
To ta l Pla n t Bio ma ss ( g )
500
400
300
200
100
0
0
25
50
150
200
Fer t i l i z at i on Lev el (ppm)
Phot osyn t hesis (µg CO 2 m -2 s -1 )
30
20
10
0
0
25
50
15 0
200
Fer t i l i z at i on Lev el (ppm)
Nutrient availability and carbon acquisition:
• no effect on photosynthesis rate / leaf area
• increased total leaf area
Source / Sink Interactions:
carbon moves from
sources to sinks via phloem
transport
Phenylpropanoid Conc. (mg / g)
500
r = -0.5 8
p < 0.0 0 01
400
300
200
100
0
0 .0 0
0 .0 2
0 .0 4
0 .0 6
Relative Shoot Growth (mg- 1 g- 1 d)
0 .0 8
L a r va l G r o wth ( mg )
8
6
4
2
0
0
25
50
Fertilization Level
150
( ppm)
200
Mechanisms of photosynthetic acclimation:
• Nitrogen allocation and specific leaf mass
• Root:shoot ratios
Large, thin leaves
High N concentration
High P s rate / area
S maller, denser leaves
Lower N concentration
E qual N / area
High P s rate / area
120
100
80
60
40
20
0
1.0
1.5
2.0
2.5
3.0
0.20
0.15
0.10
0.05
0.00
40
50
60
70
80
90
100
Nitrogen deficiency does not cause chlorosis
in plants that have had time to acclimate to
their environment.
Harris, R. W. 1992. Rootshoot ratios. J. Arboriculture
18: 39-42
50
% Ro o t Ma ss
40
30
20
10
0
0
25
50
150
Fer t ityl i Lev el (ppmN)
200
Stable root:shoot ratios between days 40-85 consistent
with equilibrium patterns of resource allocation
Soil fertility and insect resistance:
“Properly fertilized trees are better able to ward off
both insect and disease damage."
“Fertilizing landscape plants promotes their general
health and vitality, making them more resistant to
insect and disease attack."
"Fertilization promotes vigorous growth, disease,
and insect resistance, and stress tolerance."
Fertilization decreased the insect resistance of
woody plants in almost every study.
No study showed increased resistance.
Herms, D.A. 2002. Effects of fertilization on insect
resistance of woody ornamental plants: reassessing an
entrenched paradigm. Environmental Entomology
31:923-933.
Field Studies: Effects of fertilization on
paper birch and red pine
Fertilizer Treatment (ANSI standard):
Rate: 4.1 lb N / 1000 ft2 / yr
200 kg N / ha / yr
178 lb N / acre / yr
Formulation: 18:5:4 NPK (56 % N slow release)
Timing: early May and mid-Sept (split application)
Paper Birch
P aper B i r c h
Foliar Phen olic Con c. ( %)
15
r =-0. 50
P <0. 001
10
5
0
Diamet er Gr owt h ( mm)
L a r v a l Su r v i v a l ( %)
Fer t ilzed
10 0
80
Not Fer t ilzed
a
a
b
b
60
40
20
0
Fo r e s t T e n t
C at er pi l l ar
Gy ps y M ot h
Fertilization increased
growth of Sphaeropsis tip
blight lesions by 50%
Not Fer t i l i z ed Fer t i l i z ed
Blodgett et al. 2005. Forest Ecology and Management 208:273-382.
Effects of nursery fertility regime on crabapple
following transplanting
(Lloyd, J.E., et al. 2006. HortScience 41:442-445)
1997: three fertility treatments in
container nursery
1998: transplanted to low
maintenance landscape.
RadialGr owt h ( mm)
5
c
4
b
3
2
a
1
0
50
100
200
N Fer t ilzat ion Rat e ( ppm)
Foliar P hen olic Con c. ( % )
20
r -0.4 9
=
p<0.001
15
10
5
0
2
4
Radial Gr owt h ( mm)
6
Lar val Gr owt h (mg)
50
40
c
30
b
20
a
10
0
50
100
200
N Fer t i l i zat i on Rat e (ppm)
During fav orable c onditions
15
Greater impact of drought
stress on photosynthesis of
high fertility plants.
10
5
0
50
10 0
200
N Fer t ilzat ion Rat e ( ppm)
During drought
8
6
4
2
0
50
10 0
200
N Fer t ilzat ion Rat e ( ppm)
Fertilization and stress tolerance:
• decreased root:shoot ratio
• increased water requirements
• decreased secondary metabolites
Fertilization decreased drought stress tolerance:
• Red oak, chestnut oak (Kleiner et al. 1992)
• American elm (Walters and Reich 1989)
• Monterey pine (Linder et al. 1987)
• Red pine (Miller and Timmer 1994)
• Loblolly pine (Green et al. 1994)
• Scots pine (Nilsen 1990)
• Norway spruce (Nilsen 1995)
Nutrient cycling in a forest:
the ultimate slow release fertilizer
Disrupted nutrient cycles
in constructed landscapes
Soil quality: the central role of
organic matter (SOM)
• Key determinant of soil structure:
oxygen, drainage, water / nutrient holding
capacity.
• Source of essential nutrients for plants.
• Foundation of soil food web.
• Continuously depleted and replenished.
The living soil:
In an average cup of healthy soil:
Bacteria:
Fungi:
Protozoa:
Nematodes:
Arthropods:
200 billion
60 miles of hyphae
20 million
100,000
50,000
From: S. Frey, Ohio State University
Most labile N is tied up by microbes
Nutrient Flow: The Central Role of Microbes
Organic Matter
Soil Microbes
Plants
Nutrient Cycling in Ornamental Landscapes
Organic
Matter
(Mulch)
Decomposition
Organic N
Microbial
Turnover
Microbial
Uptake
Fertilizer
Mineralization
Mineral N
Immobilization
(NH4,, NO3)
Plant Uptake
Key principles of nutrient cycling theory:
• Microbes are C limited.
• Plants are N limited.
• Microbes out-compete plants for N.
• High C:N organic matter: greater proportion
of N immobilized by microbes.
• Low C:N organic matter:
greater proportion
of N released (mineralized) by microbes.
Objective:
Establish general principles for predicting
effects of diverse sources of organic matter
on soil fertility and plant health.
How does mulch affect nutrient availability? :
1. Is the carbon available? Stability of OM
2. Who gets the nitrogen? C:N ratio of OM
Availability of C for microbes: rate of
decomposition
Slow
Inorganic mulch (stone, shredded tires)
Softwood bark (mature trees)
Softwood bark (immature trees)
Hardwood bark
Ground wood
Wood chips
Composted yard waste
Sawdust
Composted Manure
Fast
N available for plants determined by net
balance between:
• N mineralization by microbes.
• N immobilization by microbes.
C:N Ratio of OM and Nutrient Availability:
C:N ratio > 30:1
• Microbes N-limited, scavenge N from soil
• Available N tied up by microbes
• N available for plants decreases
C:N ratio < 30:1
• N exceeds microbial requirements
• N release rates increase
• N available for plants increases
Material
Recycled pallets
Ground pine bark
Fresh wood chips
Hardwood bark
Fresh wood chips w/ foliage
Pine straw
Freshly senesced leaves
Composted wood chips
Composted yard waste
Composted manure
C:N Ratio
125:1
105:1
95:1
70:1
65:1
64:1
55:1
40:1
17:1
12:1
Case study: effects of mulch on soil microbes,
nutrient cycling, and plant health.
Recycled organic wastes:
• Composted yard waste (C:N = 17:1)
• Ground pallets (C:N = 125:1)
Recyled organic
waste as mulch
Experimental Mulches
Ground Wood Pallets
C:N ratio = 125:1
Composted Yard Trimmings
C:N ratio = 17:1
Composted mulch
Ground wood pallets
Experimental
approach:
Three Mulch Treatments:
1. Composted yard waste (C:N ratio = 17:1)
2. Ground wood pallets (C:N ratio = 125:1)
3. Bare soil control
Each with and without fertilization
(18-5-4 NPK, 3 lbs N / 1000 ft2 / yr)
Mulch effects on tree growth
Soil N pool sin mulc h only plots
Soil N pool sin mulc h + fertiliz er plots
Nitrate as signaling molecule: gene expression and
regulation of carbon allocation in Arabidopsis:
High soil nitrate:
Up regulation of genes for shoot growth, protein synthesis.
Down regulation of genes for secondary metabolism, root growth.
Low soil nitrate:
Down regulation of genes for shoot growth, protein synthesis.
Up regulation of genes for secondary metabolism, root growth.
Scheible, et al. 2004. Plant Physiology 136:2483-2499.
Zhang and Forde. 2000. Journal of Experimental Botany 51: 51-59.
Hypothesis: trees are adapted to the nutrient fluxes
and signals associated with gradual decomposition
of leaf litter, including low nitrate levels and high
organic N sources.
Can trees be tricked into maladaptive allocation patterns?
Japanese Beetle
Fall Webworm
Trophic cascade from microbes through
plants to insect herbivores:
Organic Matter
Microbe Effects on Nutrient Availability
Plant Growth and Defense
Plant-Feeding Insects
Conclusions:
1. Both mulches increased:
• soil organic matter
• microbial biomass and activity
2. Yard waste increased, ground wood decreased:
• nutrient availability
• plant growth
• susceptibility to insects
How can mulch applied to the soil surface
affect nutrient availability below?
1. Soil homogenization by abiotic and
biotic forces (rapid increase in SOM in
mulched plots)
2. Subterranean foraging by hyphae of
fungi that have colonized the mulch.
3. It just does.
Consistent with hypotheses:
1. Soil microbes are carbon-limited.
2. Plants are nitrogen limited.
3. Microbes out-compete plants for nitrogen.
4. Competition for N mediated by C:N ratio of OM.
5. Trade-off between growth and defense in plants.
Prescription mulching:
Low C:N mulch (e.g. composted yard trimmings):
• degraded soils
• increased plant growth
• new landscapes
High C:N mulch (e.g. recycled pallets):
• slow to moderate growth
established plantings
Mulch volcanoes are not good for trees!
If you must make volcanoes, at least keep the
mulch in the bags
Ecological
Interactions in
Sub-Soil
Comparison of Sub-Soil and Top Soil Plots:
Organic Matter (%)
Clay (%)
Total N (ppm)
Nitrate N (ppm)
Phosphorus (ppm)
Sub Soil
Top Soil
0.75
24
560
8
8
2.24
17
1790
161
50
Control
Height Growth (mm)
120
Fertilized
c
c
Fertilization increased
growth and decreased
phenolic compounds.
100
80
b
60
40
a
20
0
Subsoil
Control
4
F oliar Phenolics (%)
In subsoil:
Topsoil
In topsoil:
Fertilized
Fertilization had no effect
on growth or phenolics.
a
3
b
2
b
b
1
0
Subsoil
Topsoil
Fertilization effects on
fall webworm
Control
Fertilized
Larval growth (mg)
500
400
b
b
b
300
a
200
100
0
Subsoil
Topsoil
Mycorrhizae research:
1. Root colonization in subsoil
2. Effects of fertilizer
3. Interactions between native and commercial
mycorrhizae
Nate Kleczewski
Allocation to mycorrhizae
Benefits:
• phosphorus acquisition
• organic nitrogen uptake
• increased drought tolerance
• increased resistance to root disease
Costs:
• up to 40% of carbon assimilated by the plant.
Symbiosis (living together):
mutualism
parasitism
Under some conditions, mycorrhizal fungi act as
parasites, taking more than they give.
Plants can suppress mycorrhizae when costs exceed
benefits:
High nutrient availability
(should mycorrhizal spores be applied with fertilizer?)
Low carbon availability (e.g. shade, defoliation)
Questions regarding commercial mycorrhizae:
• Will they establish?
• Will they compete with native mycorrhizal fungi?
• Will they enhance plant growth and survival?
Key Findings:
1. Only native EMF were detected.
2. No difference between top-soil and sub-soil.
Soil
Subsoil
Topsoil
Control
Subsoil
Topsoil
Topsoil
MPN / 100 mL
41 *
47
0
Match
Tomentella sp.
Tomentella sp.
Ectomycorrhizal fungus (Pezizales )
Bit
1144
1143
910
* Estimated number of viable propagules
E Value
0
0
0
Identity
597/606
602/612
568/603
% Similarity
98
98
94
Key Findings:
3. High fertility suppressed mycorrhizae.
80
% EMF Abundance
70
*
60
50
40
30
20
10
0
Fertilized
Unfertilized
Subsoil
Fertilized
Unfertilized
Topsoil
Key Findings:
1. Only native EMF were detected.
2. No difference between top-soil and sub-soil.
3. High fertility suppressed mycorrhizae.
Conclusions:
Increased soil fertility:
• Increases growth
• Decreases chemical defenses
• Decreases root:shoot ratio
• Can decrease pest resistance
• Can decreases drought stress tolerance
Effects are independent of nutrient source, form,
or timing:
• container fertigation
• conventional fertilization (ANSI guidelines)
• stored nutrients obtained the previous year
• mulch effects on soil microbes and nutrient cycling
• inherently fertile vs. infertile soil.
This doesn’t mean:
• fertilization is bad.
• fertilization will increase pest problems in landscapes
(these studies haven’t been done yet).
This does mean:
The data do not support the conventional wisdom that
fertilization increases pest resistance.
The Natural Tree Environment:
• nutrient limited soils
• frequent episodes of drought stress
• insects and pathogens
The Natural Tree Response:
• high root:shoot ratios
• high levels of storage carbohydrates
• high levels of defensive chemicals
• moderate growth