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

Thanks to ...

… and you for listening!

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