Functions and Services of the Soil Food Web: Nematodes as Biological Indicators

1. Functions and Services of the Soil Food Web:Nematodes as Biological Indicators Howard Ferris Department of Nematology University of California, Davis hferris@ucdavis.edu February, 2008

2. Soil Food Web Functions - metabolic and behavioral activities • of 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 significance • Injure humans and vertebrate animals • Services: • Sequester and redistribute minerals • Mineralize organic molecules • Accelerate turnover • Regulate and suppress pests • Alter substrate to provide access to other organisms • Redistribute organisms in space • Reduce soil erosion • Increase agricultural production Individual species services Aggregate food web services

3. Positive and Negative Feedback in Food Web Services bacteria and bacterivore nematodes 0 nematodes with five nematodes with twenty nematodes Fu et al. 2005

4. Linkages and Connectance among Functional Guilds Nematodes at each trophic level

5. Soil Food Web Structure is strongly influenced by 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

6. perennial intermediate wheatgrass annual wheat 0 1 Soil Depth (m) 2 Photograph courtesy of Dr. Jerry Glover The Land Institute, Kansas Soil Food Webs Bottom up effects: Resource availability

7. P P F O Pr O Pr F B B Soil Food Web: Functions and Services in relation to Structure Effects of: tillage tertilizers pesticides punctuated cropping type and amount of organic input Regulation Mineralization

8. Soil Food Webs – environmental factors affecting Structure Environmental heterogeneity Zones and Gradients: texture structure temperature water O2 CO2 NO3 NH4 minerals Separate metacommunities?

9. Soil Food Webs – environmental effects on Structure Ammonium sulfate 200 Nematode guild 150 c-p 1 Standardized Counts c-p 2 X 100 c-p 3 c-p 4 50 c-p 5 X X X X X 0 0 0.02 0.05 0.1 0.5 1 Concentration (mM-N) Nematode Sensitivity to Mineral Fertilizer Tenuta and Ferris, 2004

10. Soil Nematodes as Bioindicators: Functional Diversity

11. Ingham 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. 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.

12. Maturity Index = Bongers Another milestone - calibration of ecosystem condition: Colonizer-persister Series opportunism structure enrichment stability 1 2 3 4 5 • Weighting: • should the separations between the classes be equal? • 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. Bongers, T. 1990 The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83: 14-19.

13. An Enrichment Experiment

15. Enrichment Indicators Structure Indicators • Rhabditidae • Panagrolaimidae • etc. • Short lifecycle • Small/ Mod. body size • High fecundity • Small eggs • Dauer stages • Wide amplitude • Opportunists • Disturbed conditions • Aporcelaimidae • Nygolaimidae • etc. • Long lifecycle • Large body size • Low fecundity • Large eggs • Stress intolerant • Narrow amplitude • Undisturbed conditions Basal Fauna • Cephalobidae • Aphelenchidae, etc. • Moderate lifecycle • Small body size • Stress tolerant • Feeding adaptations • Present in all soils

16. Nematode Faunal Profiles bacterivores Enriched fungivores • Enrichment index • 100 (w1.cp1 + w2.Fu2) • / (w1.cp1 + w2.cp2 ) Ba1 Enrichment trajectory Structured Fu2 fungivores bacterivores Fu2 Basal Ba2 Om4 Om5 omnivores Basal condition Ca3 Ca4 Ca5 carnivores Fu3 Fu4 Fu5 fungivores Ba3 Ba4 Ba5 bacterivores Structure trajectory • Structure Index = 100 wi.cpi / (wi.cpi + w2.cp2 ) for i = 3-5 Ferris et al., 2001

17. Nematode Indicators of Soil Food Web Structure and Function • Disturbed • N-enriched • Low C:N • Bacterial • Conducive • Maturing • N-enriched • Low C:N • Bacterial • Regulated Enriched Ba1 Enrichment index Structured Fu2 • Degraded • Depleted • High C:N • Fungal • Conducive • Matured • Fertile • Mod. C:N • Bact./Fungal • Suppressive Fu2 Basal Ba2 Om4 Om5 Basal condition Ca3 Ca4 Ca5 Fu3 Fu4 Fu5 Ba3 Ba4 Ba5 Structure index Ferris et al., 2001

18. Model Verification…. 100 Tomato Systems Yolo Co. Prune Orchards Yuba Co. Enrichment Index 50 Redwood Forest and Grass Mendocino Co. Mojave Desert 0 0 50 100 Structure Index Faunal Analysis of some California Soil Systems

19. Model Verification…. Biological Associations in Crop Management Systems Organic Conventional OmnNem OmnM FungSapM Higher trophic levels Sánchez-Moreno et al., subm.

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

21. C:N = 4:1 C:N = 6:1 Effects of Bacterivore Nematodes onN-Mineralization Rates Ferris, Venette and Lau, 1997

22. Soil Food Web Management – an experiment Sustainable Agriculture Farming Systems Project 1988-2000

23. Soil Food Web Management – an experiment Cover crop Cover crop Irrigation temperature moisture T0 activity M0

24. Ferris et al. (2004)

25. The Importance of Diversity

26. The Importance of Diversity

27. 100 Enrichment Index 50 Woodland 0 0 50 100 Vineyard Structure Index Another Ecosystem Service: • The regulation of opportunistic species

28. Predator: Prey Ratio Density-dependent predation Sánchez-Moreno et al., in press

29. Managing Input Resources for Food Web Structure and Function: Carbon Pathways and Pools Herbivory (plant source) Fungal Omnivory Decomposition (detritus and exudates) Bacterial

30. P F O Pr B Structure of the Soil Food Web in relation to Resource Inputs Intake Channel Analysis

31. Resource Inputs: Indices are based on proportions What about biomass? Intake Channel Analysis

32. Some soil organisms are Herbivores

33. Herbivory may be a Disservice

34. Or Herbivory may provide Services • It provides resources to the soil food web, often without • measurable plant damage, e.g., Tylenchidae • It may place weed species at a competitive disadvantage • Fiddleneck and Anguina amsinckiae • Silverleaf nightshade and Ditylenchus phyllobia • (but it is difficult to find convincing examples)

35. Intake Channel Analysis Higher trophic levels - food web shape

36. Intake Channel Analysis Higher trophic levels - food web shape

37. Resource Inputs: Transformation and Succession C supplied Resource transformation Community structure shifts Ferris and Matute (2003)

38. Infrequent (Punctuated) Resource Input

39. Frequent (Continuous) Resource Input

40. An Experiment on Continuous Resource Input: Soil Food Webs and Carbon Dynamics in Response to Conservation Tillage in Legume Rotations in California 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. So…. Inoculate nematodes into the vacant niche…. Minoshima et al. (2007)

41. Continuous input but without diversity; disrupted by pesticides and mineral fertilizers Continuous input with enormous diversity; not chemically or physically disrupted

42. Nematodes are useful bioindicators of the structure and function of the soil ecosystem • 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 But we have more to learn about management of higher trophic levels in the Soil Food Web

43. Some Literature • 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. More information: http://plpnemweb.ucdavis.edu/nemaplex