Nematode Assemblages as Plant Health Indicators - a soil food web perspective Howard Ferris Department of Nematology University of California, Davis hferris@ucdavis.edu July, 2007

Functional Diversity of Soil Nematodes

Soil Food Web 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 or Disservices 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

Functional Diversity in relation to Structure of the Soil Food Web Effects of: tillage tertilizers pesticides punctuated cropping type and amount of organic input O Pr B F P Regulation O Pr B F P When the bacterial channel is active, there is strong mineralization service. When omnivore biomass is low, the regulation function is reduced. When the bacterial channel is less active, mineralization and contribution to soil fertility may be lower. When omnivore biomass is larger, the regulation service is stronger. Mineralization

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

Soil Food Web Structure is strongly influenced by nature and frequency of Carbon and Energy Input Resources Carbon is respired by all organisms in the web The amounts of Carbon and Energy available limit the size and activity of the web O Pr B F P When the bacterial channel is active, there is strong mineralization service. When omnivore biomass is low, the regulation function is reduced. When the bacterial channel is less active, mineralization and contribution to soil fertility may be lower. When omnivore biomass is larger, the regulation service is stronger.

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

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

Some soil nematodes are Herbivores

Herbivory may be a Disservice

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)

Observation A preponderance of herbivores in the nematode assemblage is an indicator that recent soil management has diminished functional diversity in the soil food web.

Indices of Structural Diversity are available Species richness Simpson’s diversity index Shannon’s diversity index etc. From these we infer ecosystem characteristics, e.g., regulation …but they provide no information on food and feeders, prey and predators Functional Diversity is more difficult to assess

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

A milestone contribution: 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. Ingham When feeding on their prey. bacterial- and fungal- feeding nematodes excrete N that is in excess of their structural and metabolic needs.

Colonizer-persister Series Calibration of Ecosystem Function: Colonizer-persister Series Maturity Index = opportunism structure enrichment stability 1 2 3 4 5 Bongers, 1990 Bongers 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.

Enrichment trajectory Nematode Faunal Profiles bacterivores fungivores Enriched Enrichment index 100 (w1.cp1 + w2.Fu2) / (w1.cp1 + w2.cp2 ) Ba1 Enrichment trajectory Structured Fu2 fungivores bacterivores Fu2 Basal Ba2 Om4 Om5 Basal condition omnivores 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

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 Long lifecycle Large body size Low fecundity Large eggs Stress intolerant Narrow amplitude Undisturbed conditions Enrichment Indicators Structure Indicators Cephalobidae Aphelenchidae, etc. Moderate lifecycle Small body size Stress tolerant Feeding adaptations Present in all soils Basal Fauna

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

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

Calibration of the N-Mineralization Service of Bacterivore Nematodes

Effects of Bacterivore Nematodes on N-Mineralization Rates Management of the soil food web. We may not describe it in those terms, but often in environmental conservation or restoration, or in agricultural production, we are attempting to manage the soil food web to enhance one or more of its functions. By creating soil moisture conducive conditions in the fall, while soil temperatures were sufficiently high for biological activity, we increased the size of the microbial biomass and that of its predator guilds, including bacterivore nematodes and protozoa. The consequence was that the bacteriviore guilds were at high abundance the following spring and when the microbial biomass responded to incorporation of a winter cover crop. Grazing of the bacterivores enhanced mineralization of nutrients that would otherwise have been immobilized in the microbial biomass with the result that nutrient deficiencies were eliminated in the summer crop. C:N = 4:1 C:N = 6:1 Ferris, Venette and Lau, 1997

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

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

Ferris et al. (2004)

The Importance of Diversity

The Importance of Diversity

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

Density-dependent predation Predator: Prey Ratio We expected to have greater suppressiveness in samples with higher abundances of P and O. But predation depended not on the abundance of the high trophic levels but on the ratio of predator/prey, following a density-dependent function. Suppressiveness is optimized when predator/prey ratio is high; so few preys are available for each predator. When the biomass of prey is very high, suppressiveness in reduced. In agricultural fields, where fertilizers and organic matter are incorporated to the soil, the consequent increase of microbial populations are used by microbial-feeders to increase their population size, and this relationship is altered. When many other prey are available, the predation pressure on the target nematode reduces. Sánchez-Moreno et al., subm.

Managing Input Resources for Food Web Structure and Function: Carbon Pathways and Pools Herbivory Fungal Omnivory Decomposition Bacterial

Structure of the Soil Food Web in relation to Resource Inputs Pr B F P

Indices are based on proportions What about biomass?

Higher trophic levels - food web shape

Higher trophic levels - food web shape

Higher trophic levels - food web shape

Resource Transformation and Succession C supplied Resource Community structure shifts Ferris and Matute (2003)

Infrequent Resource Input

Frequent Resource Input

Another Experiment: Observation: Conclusion: 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 Structure Index after changes in management may involve a prolonged period of recolonization by sensitive species, requiring many years. So…. Inoculate nematodes into the vacant niche…. Minoshima et al. (2007)

Nematodes are useful bioindicators of soil condition and Plant Health 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 still have much to learn about Soil Food Web Management! Nematode faunal analysis provides a useful tool in assessing this structure, function, and probably the resilience of the soil food web because: The most abundant of the metazoa Occupy key positions in soil food webs Standard extraction procedures Identification based on morphology Clear relationship between structure and function Each sample has high intrinsic information value : More information: http://plpnemweb.ucdavis.edu/nemaplex