Post on 28-Jun-2020
Belowground aboveground interactions
Stefan Scheu
J.F. Blumenbach Institute of Zoology and Anthropology
Content
I. Structure of soil food webs
II. Carbon flux into decomposer system
III. Below - aboveground linkages
(A) The plant pathway
(B) The generalist predator pathway
IV. Summary
Kirsten Schütz
Taxa (selection) Göttinger Wald Solling
Testacea 65 51
Nematoda 65 90
Enchytraeidae 36 15
Oribatida 75 72
Collembola 48 50
Gamasina & Uropodina 91 57
Gastropoda 30 4
Lumbricidae 11 4
Isopoda 6 0
Diplopoda 6 1
Elateridae (la) 11 4
Diptera (la) 299 ?
Araneida 102 93
Chilopoda 10 7
Carabidae 24 26
Staphylinidae 85 117
Hymenoptera 704 ?
➔ The local diversity is exceptionally high: in temperate forests
> 2000 animal species („the poor mans tropical rainforest“)
➔ High diversity despite low diversity of primary producers
Schaefer 1990
Intr
od
uc
tio
n
Soil animals are diverse …
Lumb Gast Isop Dipl
Sori
Ro
ots
Bact
Dipt Ench Coll Orib
Plants
ProtNema
Fungi
Detritus, dead organic matter
Shoots
Chil Aran Staph
Aves
Cara NemaGama
Pla
nt
based
su
bs
yste
m
Top predators
Detritus based subsystem
Schaefer &
Scheu 1996
… and form complex food webs
➔ Detritus (litter) as basal resource
➔ Discrete trophic levels; few trophic levels
➔ Taxonomic groups as trophic species
Intr
od
uc
tio
n
I.
Trophic niches
and
food web structure
Analysis of trophic structure using stable isotopes
Wada et al. 1991
15N in aquatic food webs Enrichment in 15N per trophic level
I. T
rop
hic
nic
he
s a
nd
fo
od
we
b s
tru
ctu
re
Rhysotritia duplicata
1
5N
(‰
) (n
orm
alized
)
Hem
ileius initialis & S
cheloribatesspp.
Carabodes labyrinthicus
Nothrus palustris
Platynothrus peltifer
Carabodes m
arginatus
Achipteria
coleoprata
Nothrus pal. juv.
Tectocepheus velatus
Liacarus spp.
Phenopelopidae
Steganacarus m
agnus
Atropacarus striculus
Adoristes
spp.
Oribatella spp.
Phthiracaridae
Nanherm
annia nana
Malaconothrus sp.
Carabodes fem
oralis
Eupelops
plicatus
Eniochthonius m
inutissimus
Cepheus dentatus
Oribatula tibialis
Hypodam
aeusriparius
Paradam
aeus clavipes
Cham
obatesborealis
Nanherm
annia coronata
Cham
obatescuspidatus
Nothrus silvestris
Cham
obates voigtsi
Oppiidae &
Suctobelbidae
Galum
na lanceata
Hem
ileius initialis
Hypochthonius ru
fulus
Pilogalum
naspp.
Am
erus troisii
Euzetes
spp.
Galum
naspp.
6
-6
-4
-2
0
2
4
Göttinger Wald
Solling
Kranichsteiner Wald
Wohldorfer Wald
-8
Scavengers, predators, mycorrhizal feeders?
Algal feeders
Primary decomposers
Secondary decomposers
Rhysotritia duplicata
1
5N
(‰
) (n
orm
alized
)
Hem
ileius initialis & S
cheloribatesspp.
Carabodes labyrinthicus
Nothrus palustris
Platynothrus peltifer
Carabodes m
arginatus
Achipteria
coleoprata
Nothrus pal. juv.
Tectocepheus velatus
Liacarus spp.
Phenopelopidae
Steganacarus m
agnus
Atropacarus striculus
Adoristes
spp.
Oribatella spp.
Phthiracaridae
Nanherm
annia nana
Malaconothrus sp.
Carabodes fem
oralis
Eupelops
plicatus
Eniochthonius m
inutissimus
Cepheus dentatus
Oribatula tibialis
Hypodam
aeusriparius
Paradam
aeus clavipes
Cham
obatesborealis
Nanherm
annia coronata
Cham
obatescuspidatus
Nothrus silvestris
Cham
obates voigtsi
Oppiidae &
Suctobelbidae
Galum
na lanceata
Hem
ileius initialis
Hypochthonius ru
fulus
Pilogalum
naspp.
Am
erus troisii
Euzetes
spp.
Galum
naspp.
6
-6
-4
-2
0
2
4
Göttinger Wald
Solling
Kranichsteiner Wald
Wohldorfer Wald
-8
Scavengers, predators, mycorrhizal feeders?
Algal feeders
Primary decomposers
Secondary decomposers
Stable isotopes and trophic niches
„Fungal feeders“: Oribatida
➔ Understanding trophic niches of soil animal species
➔ Reconstruct the trophic structure of soil food webs
Schneider et al. 2004
I. T
rop
hic
nic
he
s a
nd
fo
od
we
b s
tru
ctu
re
➔ Phospholipids (PLFAs) from dietary species are incorporated into
neutral lipids (NLFAs) of consumers and used as biomarkers
➔ Absolute markers are not synthesized in consumer
➔ Relative markers are enriched in consumer if present in diet
Analysing trophic niches and trophic channels:
Lipids as biomarkers
Ruess and Chamberlain
2010I. T
rop
hic
nic
he
s a
nd
fo
od
we
b s
tru
ctu
re
Susanti et al. 2019
➔ Quantifying the contribution of major basal resources for soil animal nutrition
➔ Understanding the channelling of energy to higher trophic levels
Lipid analysis
Tropical soil fauna (rainforest, rubber and oil palm plantations)
I. T
rop
hic
nic
he
s a
nd
fo
od
we
b s
tru
ctu
re
Molecular gut content analysis I
Tracing prey DNA in the gut of predators by using species specific
primers (COI and/or 18S rDNA)
Eitzinger et al. 2013
Collembola as prey of centipede predators
➔Screening predator populations in the field for prey taxa
➔Opening up food web links
I. T
rop
hic
nic
he
s a
nd
fo
od
we
b s
tru
ctu
re
Molecular gut content analysis II
Tracing nematode prey DNA in the gut of „detritivores“
➔ Most „detritivore“ microarthropods also feed on nematodes
➔ Trophic generalism and omnivory very widespread
Heidemann et al. 2014
I. T
rop
hic
nic
he
s a
nd
fo
od
we
b s
tru
ctu
re
➢ Understanding the channelling of energy through soil food webs
➢ Quantifying ecosystem functions: decomposition, herbivory, predation
Linking food web structure and body size:
Energy channelling and quantifying ecosystem functions
Potapov et al.
2019
I. T
rop
hic
nic
he
s a
nd
fo
od
we
b s
tru
ctu
re
II.
Carbon flux into
decomposer system
The traditional view of decomposer systems
Herbivores
Root
Shoot
Predators
Litter
Detritivores
Nutrients
Predators
➔ Separate above- and belowground
food webs
➔ Belowground food web based on
aboveground litter input
➔ Detritivores linked to plants by
mineralization of nutrients
Herbivores
5-10% of NPP
90-95% of
NPP!!
<5% of NPP
II C
arb
on
flu
x in
to d
ec
om
po
se
r s
ys
tem
Stable isotope signatures after 5 months of maize plantation
Albers et al. 2006
➔ Collembola acquire much of their C resources via roots
➔ Fast C turnover in Collembola
Analysing the trophic structure of soil food-webs
* less than 3 replicatesδ15N of maize litter
0
1
2
3
4
5
6
7
8
9
1
5N
(‰
)
trop
hic
lev
el
I
II
III
Blaniulus
guttulatus
(Diplopoda)
Enchytraeidae
spec.
Onychiurus
spec.
(Collembola)Notiophilus
palustris
(Carabidae)
*Aporrectodea
caliginosa
(Lumbricidae)
20%
12%36%
9%
4%
Aleocharinae
spec.
(Staphylinidae)
Symphyla
spec.Lithobius
microps
(Lithobiidae)
*Necrophloeophagus
longicornis
(Geophilidae)
Geophilus
electricus
(Geophilidae)
25%
9%
13%
1% 10%
Orchesella
villosa
(Collembola)Isotoma
viridis
(Collembola)
Brachyiulus
pusillus
(Diplopoda)
Polydesmidae
spec.
(Diplopoda)
Arion
fasciatus
(Arionidae)Heteromurus
nitidus
(Collembola)
45%
21%
15%
24%
40%
31%
II C
arb
on
flu
x in
to d
ec
om
po
se
r s
ys
tem
Swiss Canopy Crane Webface experiment
Methods:
# Release of CO2 depleted in 13C, -30 vs. -8 δ
(increasing CO2 concentration to 530 ppm)
# Exchange of litter labelled vs. unlabelled
Carbon flow in belowground food webs: mature forests
Litter
(aboveground)
Soil
(belowground)
Non-enriched Area Canopy-Crane-Area
Roots labelled
Litter labelled
Control
unlabelled
labelled
unlabelled
labelled
Pollierer et al. 2007
II C
arb
on
flu
x in
to d
ec
om
po
se
r s
ys
tem
Hypochthonius
rufulus DamaeidaeAchipteria
coleoptrata
Euzetes
globulus
Platynothrus
peltifer
-2
-1
0
1
-3
Ro
ots
lab
ell
ed
Δ13C
-2
-1
0
1
-3
Le
af
litt
er
lab
ell
ed
Δ13C
-2
-1
0
1
-3
Le
af
litt
er
& r
oo
ts
lab
ell
ed
Δ13C
Tomocerus
Dicyrtoma
minuta
Entomobryidae
OnychiurusTrich.
pusillus
Glomeris
Apor.
longaPergamasus
Uropoda
cassidea
Lithobius
crassipes
Oribatida Collembola Mesostigmata
Soil fauna signatures after 17 months
Trophic structure and carbon flux in mature forests
➔ Root C input much more important than litter C input
Pollierer et al.
2007
II C
arb
on
flu
x in
to d
ec
om
po
se
r s
ys
tem
➔ „Decomposer“ food web relies substantially on currently fixed plant
carbon
Carbon flux and food web of terrestrial systems
Plant residues
Macro-
decomposers
Detritus
Predators
Fungi
Bacterial
feeders
Fungi
Bacteria
channel
Fungal
feeders
BacteriaMycorrhiza
Root carbon
Litter
chewers
Saprotrophic
fungi
Saprotrophic
fungi channel
Mycorrhiza
channel
Root feeding
„decomposers“
Root feeder
channel
II C
arb
on
flu
x in
to d
ec
om
po
se
r s
ys
tem
III.
Below - aboveground linkages:
A - The plant pathway
Integration of below- and aboveground systemThe plant pathway
Scheu 2001
➔ Modifying aboveground interactions by changing plant growth,
plant chemistry and plant community composition
negative interaction
energy flow
positive interaction
Herbivores
Root
Shoot
Predators
Indirect interactions via
➢ Changing soil structure
➢ Mineralization of nutrients
➢ Grazing on rhizosphere bacteria
➢ Grazing on rhizosphere
fungi
➢ Dispersal of microorganisms
antagonistic to root pathogens
➢ Root feeding
➢ Transposal of plant seeds
Direct interactions via
Wardle et al. 2004
III.
Be
low
-a
bo
ve
gro
un
d lin
ka
ge
s: A
-T
he
pla
nt
pa
thw
ay
Indirect trophic interactions in the rhizosphere
Grazing on rhizosphere fungi
Ro
ot
Mycorrhiza
Nutrient mineralization
Soil fungi
Nutrient translocation
DetritivoresTranquilized
Collembola
➔ Increase in nutrient mineralization via feeding on fungi …
but also the reverse …
Litter and soil Corg
III.
Be
low
-a
bo
ve
gro
un
d lin
ka
ge
s: A
-T
he
pla
nt
pa
thw
ay
➔ Additive increase in tissue 15N concentrations
➔ Complementary effects on plant growth and 15N uptake!
Partsch et al. 2006
Tissue 15N enrichment
ctrl ew col ew+col0.001
0.002
0.003
0.004
0.005
0.006
0.007
0.008
0.009
pla
nt
15N
en
ric
hm
en
t [%
]
Indirect trophic interactions in the rhizosphere
Earthworm – Collembola interactions
Plant nitrogen uptake
III.
Be
low
-a
bo
ve
gro
un
d lin
ka
ge
s: A
-T
he
pla
nt
pa
thw
ay
Schütz et al. 2008
Aphid reproduction
➔ Collembola reduce aphid reproduction and may contribute to
biological pest control
Indirect trophic interactions in the rhizosphere
Collembola and aboveground herbivores
Aphids on winter wheat
Ctr +N +NPK
0
1
2
3
4
5
6
7
8
Nu
mb
er
of
juve
nile
s i
n 2
da
ys
-Collembola
+CollembolaF = 6.5, P < 0.05
III.
Be
low
-a
bo
ve
gro
un
d lin
ka
ge
s: A
-T
he
pla
nt
pa
thw
ay
Signalling view of detritivore – plant interactions
Herbivores,
pathogens
Root
Shoot
Detritivores
➔ Interaction between
plants and detritivores
via mutual perception
of signal compounds
Root signals
Detritivore signals
Herbivores,
pathogens
III.
Be
low
-a
bo
ve
gro
un
d lin
ka
ge
s: A
-T
he
pla
nt
pa
thw
ay
Without
Collembola
With
Collembola
Protaphorura
fimataArabidopsis
thaliana
Gene expression patterns in gnotobiotic systems
Effects of Collembola on gene expression in Arabidopsis thaliana
The model system
Methods:
# Axenic system with sand + litter (15N labelled)
# Custom made micro-array covering 1054 gene-specific target sequences:
stress response, signalling and biosynthesis of secondary metabolites
LitterSand
Endlweber et al. 2011
III.
Be
low
-a
bo
ve
gro
un
d lin
ka
ge
s: A
-T
he
pla
nt
pa
thw
ay
Expression patterns in shoots and roots
Effects of Collembola on gene expression in A. thaliana
54 genes; root
27 genes, root;
4 genes; shoot and root
31 genes; shoot
6 unregulated
5 genes; shoot and root
29 genes; shoot 54 genes; root
27 genes, root;
4 genes; shoot and root
31 genes; shoot
6 unregulated
5 genes; shoot and root
29 genes; shoot
Number of genes regulated at
day 6 in roots and shoots
Auxin response &
biosynthesis 16%
Other hormone-related responses 5%
Signaling 4%
WRKY transcription factors 7%
Stress response and
defensive compounds 10%
Phenylpropanoid/
Flavonoid metabolism 5%
Secondary Metabolism
CYP; UGT; GST 39%
Aquaporins 7%
Transport 3%Other metabolism 4%
Auxin response &
biosynthesis 16%
Other hormone-related responses 5%
Signaling 4%
WRKY transcription factors 7%
Stress response and
defensive compounds 10%
Phenylpropanoid/
Flavonoid metabolism 5%
Secondary Metabolism
CYP; UGT; GST 39%
Aquaporins 7%
Transport 3%Other metabolism 4%
Functional groups of genes
regulated in roots at day 6
➔ Strong gene expression response due to presence of Collembola
➔ Induction of genes regulating root growth
➔ Induction of defence genes, in particular in shoots!
➔ Response resembles that of root herbivores!
Endlweber et al. 2011
III.
Be
low
-a
bo
ve
gro
un
d lin
ka
ge
s: A
-T
he
pla
nt
pa
thw
ay
Protaphorura
armata
Gene expression patterns in trees
Transcriptional response of Quercus robur to Collembola
The model system
Methods:
# Axenic system with sterilized soil inoculated with mycorrhiza (Piloderma
croceum)
# Transcriptomics
Herrmann et al. 2016
III.
Be
low
-a
bo
ve
gro
un
d lin
ka
ge
s: A
-T
he
pla
nt
pa
thw
ay
Expression patterns in leaves during shoot- and root-flush
Effects of Collembola on transcriptional response in Q. robur
➔ Strong gene expression response due to presence of Collembola
➔ Increase in GO terms related to primary growth during SF
➔ Increase in GO terms related to physical fortification during RF
➔ Increase in GO terms related to plant defence
➔ Increasing plant growth and fortification
as well as priming against herbivore attack
Graf et al., in revision
Total number of contigs 467 120
of which up-regulated 410 65
of which down-regulated 57 55
Differential gene expression Shoot flush (SF) Root flush (RF)
Including Gene Ontology (GO) terms for
➢ primary metabolism: e.g., cell proliferation, regulation of cell cycle
➢ defence related contigs: e.g., defence response of insects, flavonoid biosynthesis,
salycilic acid mediated pathway, jasmonic acid mediated pathway
III.
Be
low
-a
bo
ve
gro
un
d lin
ka
ge
s: A
-T
he
pla
nt
pa
thw
ay
III.
Below - aboveground linkages:
B - The generalist predator pathway
negative interactionenergy flow
positive interaction
Generalist
predatorsBelow-ground
energy subsidy
Herbivores
Plants
DetritusMicrobi/
detritivores
Feedbacks to aboveground system via generalist predators
The detritivore – generalist predator – herbivore pathway
Scheu 2001
➔ Changing herbivore control by energy subsidy from decomposer system
➔ „Dual subsystem omnivory“
III.
Be
low
-a
bo
ve
gro
un
d lin
ka
ge
s:
B -
Th
e g
en
era
lis
t p
red
ato
r p
ath
wa
y
➔ Strong link between detritivores and generalist predators
➔ Increase in Collembola density by a factor of 3.9
0
100
200
300
400
500
2nd
Collembola
ind/m²
control
+ maize
5th0
2
4
6
8
10 Cursorial spiders
ind/m²
2nd 5th
➔ Increase in density of cursorial spiders by a factor of 2.9
Oelbermann & Scheu 2008
Feedbacks to aboveground system via generalist predators
Addition of detrital resources (maize litter; 5 months)
III.
Be
low
-a
bo
ve
gro
un
d lin
ka
ge
s:
B -
Th
e g
en
era
lis
t p
red
ato
r p
ath
wa
y
Von Berg et al. 20100
400
800
1200
1600
1 2- Predators + Predators
Without mulch
With mulch
-8%
-44%
➔ Effective control of aphids by generalist predators
➔ Fostering the detrital system by mulching strengthens the control of
aphids by generalist predators
Nu
mb
er
of
ap
hid
s o
n 2
5 s
ho
ots
Detritivores as energy subsidy for generalist predators
Arable systems: Effects on aphid (Sitobion avenae) control
-32%
III.
Be
low
-a
bo
ve
gro
un
d lin
ka
ge
s:
B -
Th
e g
en
era
lis
t p
red
ato
r p
ath
wa
y
Autumn
Summer drought
WinterSummerSpring
Season
Build-up of herbivore populations
Soil
moisture
Relative
contribution to
predator diet
Retreat of decomposers
Decomposers
Retreat of decomposers
Herbivores
Decomposers
Net water
flux
The detritivore – generalist predator – herbivore pathway
Moisture driven prey switching
➔ Sustaining of predator populations by detritivore prey
➔ Switching to herbivore prey during vegetation periodIII.
Be
low
-a
bo
ve
gro
un
d lin
ka
ge
s:
B -
Th
e g
en
era
lis
t p
red
ato
r p
ath
wa
y
Summary
➢ New tools/methods allow unprecedented progress in understanding
the structure and functioning of soil food webs
➢ Roots of major importance for fuelling decomposer food web
➢ Detritivores affect plant growth, plant gene expression, and the
susceptibility of plants to herbivore attack
➢ Complementary effects of detritivore functional groups
➢ Detritivores may strengthen the contol of aboveground herbivores via
generalist predators
➔ For developing more sustainable agricultural systems soil
animal communities need considerably more attention
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Lipid analysis
Dietary rooting: neutral lipids in Collembola
Ruess et al. 2005
➔ Neutral lipid analysis allows refinement of trophic niches
➔ Contribution of bacteria, fungi, animals and plants to diet
➔ Channelling of basal resources through food web
I. N
ich
e d
iffe
ren
cia
tio
n a
nd
tro
ph
ic s
tru
ctu
re
Variables studied:
# Plant species number (1, 2, 4, 8)
# Plant functional group number (1, 2, 3)
# Plant functional group identity (grass, legume, herb)
# Earthworms (with/without Lumbricus terrestris +
Aporrectodea caliginosa)
# Collembola (with/without Heteromurus nitidus +
Folsomia candida + Protaphorura fimata)
➔ 256 microcosms
Partsch et al. 2006
Grass litter
Eight plant individuals
15N labelled roots
Arable soil
Indirect trophic interactions in the rhizosphere
Earthworm – Collembola interactions
Experimental setupEarthworms
Collembola
III.
Be
low
-a
nd
ab
ove
gro
un
d lin
ka
ge
s:
Th
e p
lan
t p
ath
wa
y
➔ Additive increase in plant biomass
➔ Maximum plant biomass in combined treatment
➔ Strong changes in root biomass; reduced by earthworms and
Collembola but not in combined treatment
➔ Interactive effects of decomposers on plant performance
➔ Strong changes in plant resource allocation pattern
Partsch et al. 2006
Total plant biomass Root biomass
ctrl ew col ew+col
treatment
9.0
9.5
10.0
10.5
11.0
11.5
12.0
12.5
tota
l b
iom
as
s [
g]
ctrl ew col ew+col
treatment
3.8
4.0
4.2
4.4
4.6
4.8
5.0
5.2
5.4
roo
t b
iom
ass [
g]
Indirect trophic interactions in the rhizosphere
Earthworm – Collembola interactions
Plant growth
III.
Be
low
-a
nd
ab
ove
gro
un
d lin
ka
ge
s:
Th
e p
lan
t p
ath
wa
y
roo
t vo
lum
e [
cm
²]
0
0.2
0.4
0.6
0.8
- Coll + Coll - Coll + Coll0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
roo
t d
iam
ete
r [m
m]
- Coll + Coll - Coll + Coll
B
A
A
A
A
B
B
AEpilobium adnatum & Cirsium arvense
0
100
200
300
400
tota
l ro
ot
len
gth
[cm
]
- Coll + Coll
E. adnatum C. arvense
A
B
+ Coll
A
A
- Coll0
200
400
600
800
me
an
nu
mb
er
of
roo
t ti
ps p
er
pla
nt
- Coll + Coll
E. adnatum C. arvense
- Coll + Colll
B
AB
A
➔ Collembola decrease root diameter and volume,
but increase root length and number of root tips
Endlweber & Scheu 2006
Indirect trophic interactions in the rhizosphere
Collembola and root morphology
III.
Be
low
-a
bo
ve
gro
un
d lin
ka
ge
s: A
-T
he
pla
nt
pa
thw
ay