Functions and Services of theSoil Food Web:

Nematodes as Biological Indicators

Howard FerrisDepartment of Nematology

University of California, Davis

hferris@ucdavis.edu

February, 2008

Soil Food Web Functions - metabolic and behavioral activitiesof organisms that impact the biotic or abiotic components of the ecosystem

Feeding: Ingestion, assimilation, defecation and excretion Behavior: Movement, activity, migration

Functions may be classified, subjectively, as Services, Disservices (or Neutral)

Disservices:Damage plants of agricultural or ornamental significanceInjure humans and vertebrate animals

Services:Sequester and redistribute minerals

Mineralize organic moleculesAccelerate turnoverRegulate and suppress pests

Alter substrate to provide access to other organismsRedistribute organisms in spaceReduce soil erosionIncrease agricultural production

Individual speciesservices

Aggregatefood web services

Positive and Negative Feedback in Food Web Services

bacteria and bacterivore nematodes

with twenty nematodes

0 nematodes with five nematodes

Fu et al. 2005

0

20

40

60

80

100

0 5 10 20 40 80 160

Nematode Abundance

Bact

eria

l Cel

lsPositive feedback Overgrazing

0

20

40

60

80

100

0 5 10 20 40 80 160

Nematode Abundance

Bact

eria

l Cel

ls

0

20

40

60

80

100

0 5 10 20 40 80 160

Nematode Abundance

Bact

eria

l Cel

lsPositive feedback Overgrazing

Roots

Detritus

PhytophagousNematodes

SaprophyticFungi

Bacteria

Collembolans

Noncrypto-stigmatic Mites

CryptostigmaticMites

FungivorousNematodes

Bacteriophagous

NematodesBacteriophagous

Earthworms

Mites

Flagellates

Amoebae

PredaceousNematodes

PredaceousMites

PredaceousCollembolans

NematodeFeeding Mites

Linkages and Connectance among Functional Guilds

Nematodes at each trophic level

Soil Food Web Structure is strongly influencedby nature and frequency of Carbon and Energy Input

•Carbon is respired by all organisms in the web

•The amounts of Carbon and Energy available limit the size and activity of the web

Photograph courtesy of Dr. Jerry GloverThe Land Institute, Kansas

1

2

Soil D

ep

th

(m)

0

annual wheat

perennial intermediate wheatgrass

Bottom up effects:Resource availability

Soil Food Webs

OP

r

BF

P

OP

r

BF

P

Mineralization

Regulation

Effects of:tillagetertilizerspesticidespunctuated croppingtype and amount of organic input

Soil Food Web: Functions and Services in relation to Structure

Environmental heterogeneity

Zones andGradients:

texturestructuretemperaturewaterO2

CO2

NO3

NH4

minerals

Soil Food Webs – environmental factors affecting Structure

Separatemetacommunities?

Nematode Sensitivity to Mineral Fertilizer

Concentration (mM-N)

0 0.1 1

Sta

ndar

dize

d C

ount

s

0

50

100

150

200

X

X X X X

c-p 1 c-p 2 c-p 3 c-p 4 c-p 5 X

Ammonium sulfate

0.50.050.02

Nematode guild

Tenuta and Ferris, 2004

Soil Food Webs – environmental effects on Structure

Soil Nematodes as Bioindicators: Functional Diversity

Ingham

Ingham, R.E., J.A. Trofymow, E.R. Ingham, and D.C. Coleman. 1985. Interactions of bacteria, fungi, and their nematode grazers: Effects on nutrient cycling and plant growth. Ecological Monographs 55:119-140.

A milestone contribution:

When feeding on their prey, bacterial- and fungal-feeding nematodes excrete N that is in excess of their structural and metabolic needs.

1 2 3 4 5

enrichment stabilityopportunism structure

Colonizer-persister Series

Weighting:• should the separations between the classes be equal?

Bongers

Another milestone - calibration of ecosystem condition:

Maturity Index =

fi

ii pvMI,1

Bongers, T. 1990 The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83: 14-19.

Issues of proportions:

• If the proportion of opportunists increases, the proportion of sensitive species decreases.

• It should be possible to increase structure without decreasing enrichment, and vice versa. The axes should be independent.

An Enrichment Experiment

cp1 Nematodes

0

10,000

20,000

30,000

40,000

50,000

RobbinsLeaves

RobbinsSoil

Hart Soil PlacervilleSoil

Not Enrich.

Enriched

cp2 Nematodes

0

2,000

4,000

6,000

8,000

10,000

RobbinsLeaves

RobbinsSoil

Hart Soil PlacervilleSoil

Not Enrich.

Enriched

Aphelenchoididae

0

2,000

4,000

6,000

8,000

10,000

RobbinsLeaves

RobbinsSoil

Hart Soil PlacervilleSoil

Not Enrich.

Enriched

Rhabditidae

05,000

10,00015,00020,00025,00030,00035,000

RobbinsLeaves

RobbinsSoil

Hart Soil PlacervilleSoil

Not Enrich.

Enriched

Panagrolaimidae

0

5,000

10,000

15,000

RobbinsLeaves

RobbinsSoil

Hart Soil PlacervilleSoil

Not Enrich.

Enriched

RhabditidaePanagrolaimidae

etc.

Short lifecycleSmall/ Mod. body sizeHigh fecunditySmall eggsDauer stagesWide amplitudeOpportunistsDisturbed conditions

AporcelaimidaeNygolaimidae

etc.

Long lifecycleLarge body sizeLow fecundityLarge eggsStress intolerantNarrow amplitudeUndisturbed conditions

Enrichment Indicators Structure Indicators

CephalobidaeAphelenchidae,

etc.

Moderate lifecycleSmall body sizeStress tolerantFeeding adaptationsPresent in all soils

Basal Fauna

Ba2

Fu2

Fu2

Ba1

Ba3

Fu3

Ca3

Ba4

Fu4

Ca4

Om4

Ba5

Fu5

Ca5

Om5

Enriched

Structured

Basal

Basalcondition

Structure trajectory

Enr

ichm

ent t

raje

ctor

y

omnivorescarnivoresfungivores

bacterivores

fungivores

bacterivores

fungivores

bacterivores

NematodeFaunal Profiles

•Enrichment index

100 (w1.cp1 + w2.Fu2)

/ (w1.cp1 + w2.cp2 )

•Structure Index = 100 wi.cpi / (wi.cpi + w2.cp2 ) for i = 3-5Ferris et al., 2001

Ba2

Fu2

Fu2

Ba1

Ba3

Fu3

Ca3

Ba4

Fu4

Ca4

Om4

Ba5

Fu5

Ca5

Om5

Enriched

Structured

Basal

Basalcondition

Structure index

Enr

ichm

ent i

ndex

•Disturbed•N-enriched•Low C:N•Bacterial•Conducive

•Maturing•N-enriched•Low C:N•Bacterial•Regulated

•Matured•Fertile•Mod. C:N•Bact./Fungal•Suppressive

•Degraded•Depleted•High C:N•Fungal•Conducive

Nematode Indicators of Soil Food Web Structure and Function

Ferris et al., 2001

0

50

100

0 50 100

Structure Index

Enr

ichm

ent I

ndex Prune

OrchardsYuba Co.

MojaveDesert

TomatoSystemsYolo Co.

Redwood Forest and

GrassMendocino

Co.

Faunal Analysis of some California Soil Systems

Model Verification….

OCT/ONT CST Association I Association II

BaNem PredNem PredM

Fu Nem PpNem AlgM

EI SI

BI CI

+

_

+

_ ORG OmnNem

OmnMFungSapM

Biological Associations in Crop Management Systems

Model Verification….

Sánchez-Moreno et al., subm.

Higher trophic levels

Organic Conventional

Tests of Ecosystem Services:The N-Mineralization Service of Bacterivore Nematodes

Effects of Bacterivore Nematodes onN-Mineralization Rates

0

2

4

6

8

10

12

14

5 10 15 20 25 30 35 40 45

Organic Matter C:N Ratio

N (

µg

/g S

oil

)

+Cephalobus-Cephalobus

Ferris, Venette and Lau, 1997

C:N = 4:1

C:N = 6:1

Sustainable Agriculture Farming Systems Project

1988-2000

Soil Food Web Management – an experiment

Aug Sep Oct Nov Dec Jan Feb Mar Apr May

Cover cropCover crop

Irrigation

temperature

moisture

activity

T0

M0

Soil Food Web Management – an experiment

Tomato Yields - 1997

0

10

20

30

40

50

60

+I+S+W +I-S+W +I-S-W -I-S+W -I-S-W

Tons

/Acr

eA A

B B B

Ferris et al. (2004)

Bacterivore Nematode Abundance

0

1000

2000

3000

4000

5000

6000

1-A

pr

8-A

pr

15-A

pr

22-A

pr

29-A

pr

6-M

ay

13-M

ay

20-M

ay

27-M

ay

3-Ju

n

10-J

un

17-J

un

24-J

un

1-Ju

l

8-Ju

l

15-J

ul

22-J

ul

29-J

ul

Mesorhabditis

Cruznema

Rhabditis

The Service - N mineralization- Functional Redundancy

0

100

200

300

400

500

600

1-A

pr

8-A

pr

15-A

pr

22-A

pr

29-A

pr

6-M

ay

13-M

ay

20-M

ay

27-M

ay

3-Ju

n

10-J

un

17-J

un

24-J

un

1-Ju

l

8-Ju

l

15-J

ul

22-J

ul

29-J

ul

Mesorhabditis

Cruznema

Rhabditis

The Service - N mineralization- Functional Complementarity

0

100

200

300

400

500

600

1-A

pr

8-A

pr

15-A

pr

22-A

pr

29-A

pr

6-M

ay

13-M

ay

20-M

ay

27-M

ay

3-Ju

n

10-J

un

17-J

un

24-J

un

1-Ju

l

8-Ju

l

15-J

ul

22-J

ul

29-J

ul

Mesorhabditis

Cruznema

Rhabditis

Total N

The Importance of Diversity

Mesorhabditis and Acrobeloides Abundance

0

1000

2000

3000

4000

5000

6000

1-A

pr

8-A

pr

15-A

pr

22-A

pr

29-A

pr

6-M

ay

13-M

ay

20-M

ay

27-M

ay

3-Ju

n

10-J

un

17-J

un

24-J

un

1-Ju

l

8-Ju

l

15-J

ul

22-J

ul

29-J

ul

Mesorhabditis

Acrobeloides bod

The Service - N mineralization- Functional Continuity

0100200300400500600700800900

1-A

pr

8-A

pr

15-A

pr

22-A

pr

29-A

pr

6-M

ay

13-M

ay

20-M

ay

27-M

ay

3-Ju

n

10-J

un

17-J

un

24-J

un

1-Ju

l

8-Ju

l

15-J

ul

22-J

ul

29-J

ul

Mesorhabditis

Acrobeloides bod

Total N

The Importance of Diversity

Another Ecosystem Service:

• The regulation of opportunistic species

Woodland Vineyard 0 50 100

Structure Index

0

50

100

En

rich

men

t In

dex

Density-dependent predation

80

85

90

95

100

0 0.1 0.2 0.3

Predator:Prey Ratio (Density Class Averages)

So

il S

up

pre

ss

ive

ne

ss

Predator: Prey Ratio

Sánchez-Moreno et al., in press

Managing Input Resources for Food Web Structure and Function: Carbon Pathways and Pools

Omnivory

Decomposition

Herbivory

Bacterial

Fungal

(plant source)

(detritus and exudates)

%fungal

%bacterial%plantOP

r

BF

P

Structure of the Soil Food Web in relation to Resource Inputs

Intake Channel Analysis

% Herbivore

% Fungivore

% Bacteriivore

% Herbivore

% Fungivore

% Bacteriivore

Resource Inputs: Indices are based on proportionsWhat about biomass?

Intake Channel Analysis

Some soil organisms are Herbivores

Herbivory may be a Disservice

1. It provides resources to the soil food web, often without measurable plant damage, e.g., Tylenchidae

2. It may place weed species at a competitive disadvantage

Fiddleneck and Anguina amsinckiaeSilverleaf nightshade and Ditylenchus phyllobia

(but it is difficult to find convincing examples)

Or Herbivory may provide Services

% Herbivore

% Fungivore

% Bacteriivore

Higher trophic levels- food web shape

Intake Channel Analysis

% Herbivore

% Fungivore

% Bacteriivore

Higher trophic levels- food web shape

Intake Channel Analysis

Plant Materials - Surface

0

20

40

60

80

100

0 300 600 900 1200

DD>10

Enric

hmen

t Ind

ex

C:N High

C:N Low

Control

A

C supplied

Resourcetransformation

Community structureshifts

Ferris and Matute (2003)

Resource Inputs: Transformation and Succession

Plant Low C:N

0

20

40

60

80

100

0 300 600 900 1200

DD>10 C

Ch

an

ne

l In

de

x

Cont. Undist.

Cont. Incorp.

Pl. Incorp.

Pl. Undist.

0

20

40

60

80

100

0 300 600 900 1200

A

0

100

200

300

400

500

600

700

800

0 50 100 150 200 250 300 350 400

Time

Inp

ut

Bio

mas

s

Infrequent (Punctuated) Resource Input

0

100

200

300

400

500

600

700

800

0 50 100 150 200 250 300 350 400

Time

Inp

ut

Bio

mas

s

Frequent (Continuous) Resource Input

An Experiment on Continuous Resource Input:

Soil Food Webs and Carbon Dynamics in Response to Conservation Tillage in Legume Rotations in California

So…. Inoculate nematodes into the vacant niche….

Minoshima et al. (2007)

Observation: The Structure Index did not increase in two years of

organic, no-till, continuous cropping.

Conclusion:Increase in the Structure Index after changes in management may

involve a prolonged period of recolonization by sensitive species,

that requires many years.

Continuous input but without diversity;disrupted by pesticides and mineral fertilizersContinuous input with enormousdiversity;not chemically or physically disrupted

• Occupy key positions in soil food webs• Standard extraction procedures• Identification based on morphology• Clear relationship between structure and function• The most abundant of the metazoa • Each sample has high intrinsic information value

Nematodes are useful bioindicators ofthe structure and function of the soil ecosystem

But we have

more to

learn about m

anagement of

higher trophic

levels

in the S

oil Food W

eb

•Bongers, T., M. Bongers. 1998. Functional diversity of nematodes. Appl. Soil Ecol. 10, 239-251.

•Bongers, T., H. Ferris. 1999. Nematode community structure as a bioindicator in environmental monitoring. Trends Ecol. Evol. 14, 224-228.

•Ferris, H., T. Bongers, R.G.M. de Goede. 2001. A framework for soil food web diagnostics: extension of the nematode faunal analysis concept. Appl. Soil Ecol. 18, 13-29.

•Ferris, H., M.M. Matute. 2003. Structural and functional succession in the nematode fauna of a soil food web. Appl. Soil Ecol. 23:93-110.

•Tenuta, M., H. Ferris. 2004. Relationship between nematode life-history classification and sensitivity to stressors: ionic and osmotic effects of nitrogenous solutions. J. Nematol. 36:85-94.

•Ferris, H. and T. Bongers. 2006. Nematode indicators of organic enrichment. J. Nematol. 38:3-12.

•Sánchez-Moreno, S., H. Minoshima, H. Ferris and L.E. Jackson. 2006. Linking soil properties and nematode community composition: effects of soil management on soil food webs. Nematology 8:703-715.

•Sánchez-Moreno, S. and H. Ferris. 2007. Suppressive service of the soil food web: Effects of environmental management. Agric. Ecosyst. Environ. 119:75-87.

Some Literature

More information: http://plpnemweb.ucdavis.edu/nemaplex