The Role of Nematodes in Ecosystems and as Bioindicators

1. The Importance of Nematodes in Ecosystemsand asBiological Indicators Howard Ferris Department of Nematology University of California, Davis hferris@ucdavis.edu June, 2007

2. Cobb Bastian Maupas Ingham Yeates Bongers Wall 19th Century to mid 20th Century recognition of abundance and habitat diversity 20th Century to present functional diversity and bioindicator potential

3. Nematodes - Diverse Metazoa • They are among the simplest multicellular animals; they exhibit enormous diversity on a simple structural template. • They occupy any niche that provides a source of carbon, in marine, freshwater and terrestrial environments. • They feed on most organisms and are food for many others. • They differ in ecological amplitude and tolerances. • “.....if all the matter in the universe except the nematodes were swept away……we would find its mountains, hills, vales, rivers, lakes, and oceans represented by a film of nematodes.”

4. to verbal portraits: • If the nematodes resident in a single acre of soil near San Antonio, Texas, USA, were to proceed in head-to-tail procession to Washington D.C., some 2000 miles away, the first nematode would reach Washington before the rear of the procession left San Antonio! (Cobb, N.A. 1914). There are many descriptions of nematode abundance from simple statements: • millions of nematodes can occupy 1 m2 of soil; a handful may contain 50 • species (Bongers & Ferris, 1999). • 80% of multicellular animals are nematodes (Platt 1994). • If all the nematodes in the Murray River were laid end-to-end they would encircle the earth’s equator (Hodda, 2001).

5. There are many other organisms in the Soil Food Web

6. There are many other organisms in the Soil Food Web • What determines the structure and diversity of this trophic network?

7. Heat and CO2 • Carbon is respired by each organism in the web • The amounts of Carbon and Energy available limit the size and activity of the web Resources Soil Food Webs - Resource availability and utilization Organic Source

8. perennial intermediate wheatgrass annual wheat 0 1 Soil Depth (m) 2 Soil Food Webs Bottom up effects: Resource availability

9. Soil Food Webs – Top down effects

10. Soil Food Webs – Environmental Effects on Structure Environmental heterogeneity Zones and Gradients: texture structure temperature water O2 CO2 NO3 NH4 minerals Separate metacommunities?

11. 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 – Mineral Fertilizer Tenuta and Ferris, 2004

12. Behavioral Effects in Food Web Structure Sinorhizobium meliloti and bacterivore nematodes 0 nematodes 5 nematodes With 20 nematodes Fu et al., 2005

13. Heterogeneity and Food Web Structure/Functions • Resource distribution • Organism motility • Omnivory • Strong and weak links • Microsite asynchrony

14. Model of the 248-dimensional E8 exceptional case of Lie algebra announced March 19, 2007; American Institute of Mathematics Calculated by 18 mathematicians over 4 years; the written calculation would cover a land area the size of Manhattan • Scientists seek symmetry and predictability in the systems they study. • Mathematicians and physicists approach this goal; biologists deal with more complex and dynamic systems. • The symmetry and predictability of bioindicators is more likely to be realized in ecosystem function than in ecosystem structure.

15. Functional Diversity of Nematodes

16. Functions - metabolic and behavioral activities 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 to plants of agricultural or ornamental significance • Injury to humans and vertebrate animals • Services: • Sequestration and redistribution of minerals • Mineralization of organic molecules • Acceleration of turnover • Regulation and suppression of pests • Substrate alteration providing access to other organisms • Phoretic redistribution of organisms

17. Sustainable Agriculture Farming Systems Project 1988-2000

18. Effects of Bacterivore Nematodes onN-Mineralization Rates

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

20. C:N = 8.5:1 C:N = 8.3:1 Fungivores Chen and Ferris, 2000

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

24. Ferris et al., 2004

25. P P F O Pr Regulation O Pr F B B Mineralization Services associated with food web channels

26. Channel management and characteristics • Bacterivore Channel • Moisture • Low C:N, labile substrates • High respiration and turnover • Mineralization of nutrients • Major predators are protozoa and nematodes • Herbivore Channel • Host status and defense mechanisms • Damage to host • Substrate respiration and immobilization, excretion and defecation • Major predators are fungi and nematodes • Fungivore Channel • High C:N, lignin, cellulose, resistantsubstrates • Conservation of carbon, greater web structure • Major predators are microarthropods and nematodes Ruess and Ferris, 2004

27. Succession C supplied Resource transformation Community structure shifts Ferris and Matute, 2003

28. Resource transformation • Channel Index: • a weighted ratio of fungivore and bacterivore nematodes • higher CI indicates more fungal Ferris and Matute, 2003

29. Management of nematodes in sustainable systems requires maintaining the flow of energy to each trophic level and providing a favorable environment for the higher trophic levels

30. Ecosystem Function - Level of Resolution:Individual Taxa or Functional Guilds? • Organisms of similar ecological amplitude and sensitivities which perform the same function A B Is A an indicator of B?

31. Which organisms perform the suppressive service? 80 70 60 50 r = 0.41 Nematode Fauna Structure index 40 30 20 10 0 78 83 88 93 Soil suppressiveness Sanchez-Moreno et al., subm.

32. 4.0 June 3.5 Tardigrades / suppressiveness R = 0.59, p < 0.05 3.0 2.5 2.0 1.5 Dead / Alive Nematodes r = 0.73 P <0.05 1.0 0.5 0.0 -0.5 -2 0 2 4 6 8 10 12 14 16 18 20 October Number of Tardigrades Same role, different actors – successional effects soil suppressiveness / tardigrades r = 0.59, P < 0.05 Sanchez-Moreno et al., subm.

33. Predator: Prey Ratio Density-dependent predation Sanchez-Moreno et al., subm.

34. Soil Food Web Structure - the need for indicators

35. The Nematode Fauna as a Soil Food Web Indicator Herbivores Bacterivores Fungivores Omnivores Predators

36. Maturity Index = S ( v(i) * a(i) ) / Sa(i) • i=1,n i=1,n Colonizer-persister series opportunism structure enrichment stability 1 2 3 4 5 …but should the separations between the classes be equal? Numerator/Denominator issues: a progression of ideas • % w1.cp1 = 100 w1.cp1 / S wi.cpi for i = 1-5 • It should be possible to increase structure without decreasing enrichment, and vice versa. The axes should be independent Bongers, 1990

37. 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

38. Enrichment Indicator Weighting • Resource availability • Food consumption necessary to achieve body weight • Mean Wt, cp1 = 2.68 µg • Mean Wt, cp2 = 0.64 µg • Differential » 4x • cp2 weighting = 0.8 • cp1 weighting = 3.2

39. Structure Indicator Weighting • Connectance • The relationship between trophic links and species richness 5.0 3.2 1.8 0.8

40. 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

41. Testable Hypotheses of 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

42. 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 Trajectory Analysis of Some California Soil Systems

43. Soil organisms that exhibit characteristics of diversity and abundance may be useful as bioindicators (Breure et al., 2005). Why nematodes? • Occupy key positions in soil food webs • Standard extraction procedures • Identification based on morphology • Relationship between structure and function • The most abundant of the metazoa • Each sample has high intrinsic information value

44. Some References • Bongers, T., 1990. The maturity index, an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83, 14-19. • 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. • Ferris, H., R.C. Venette, K.M. Scow. 2004. Soil management to enhance bacterivore and fungivore nematode populations and their nitrogen mineralization function. Appl. Soil Ecol. 24:19-35. • Fu, S., H. Ferris, D. Brown, R. Plant. 2005. Does the positive feedback effect of nematodes on the biomass and activity of their bacteria prey vary with nematode species and population size? Soil Biol. Biochem. 37:1979-1987. • Ruess, L., H. Ferris. 2004. Decomposition pathways and successional changes. In R.C. Cook and D.J. Hunt (eds) Proceedings of the Fourth International Congress of Nematology. Nem. Monogr. Persp. 2. Brill, Netherlands. 866p. • 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. More information: http://plpnemweb.ucdavis.edu/nemaplex