Soil nematode community succession and their role in plant species replacements Paul Kardol et al. Netherlands Institute of Ecology (NIOO-KNAW) Department of Multitrophic Interactions
Nematodes Plants Research approaches (function / scale / ecosystem) Plant-parasitic nematodes (plant performance / feedbacks) [Ex. prim. succession] Nematode community (soil food web / biological indicators) [Ex. sec. succession]
Plant-parasitic nematodes in primary foredune succession? Ammophila arenaria Festuca rubra ssp. arenaria Carex arenaria Elymus athericus Hippophaë rhamnoides ssp. rhamnoides
Previous research Nematodes contribute to degeneration of Ammophila arenaria and to successional species replacements [species-specific accumulation] (v.d. Putten et al. 1990, 1993) Nematode effects are part of a complex pathogen system (v.d. Putten & v.d. Stoel 1998). Nematodes should be regarded within the whole set of environmental conditions that affect successional plant species replacements...
Plant Ammophila arenaria Bottom-up control Control by mutualists Mutualists Nematodes Endoparasites Ectoparasites Horizontal control Top-down control Antagonists Bacteria, fungi, arthropods
Case study Tylenchorhynchus ventralis (ecto-parasite on Ammophila aranaria): Low densities in field soil compared to sterilized soil: top down control Which mechanisms top-down control their population density? Approach (Anna Piśkiewicz): Greenhouse experiments A. Selectively removing different groups of potential antagonists B. Selectively adding different groups of potential antagonist
T. ventralis / 100g soil 200 150 100 50 a b b Removing nematodes and arthropods from non-sterilized soil Pots with A. arenaria inoculated with 25 T. ventralis/ pot Harvest after 12 weeks 0 Sterilized Stirred (microbes) Non-sterilized (whole soil comm.) T. ventralis / 100g soil 2000 1000 0 a Sterilized c Micr b Nema ab Arthrop Adding microbes, nematodes and arthropods to sterilized soil Pots with A. arenaria inoculated with 50 T. ventralis/ pot Harvest after 12 weeks Piśkiewicz et al., 2007 (Oecologia)
Conclusion Ectoparasitic nematodes T. ventralis are controlled by microbes (bacteria, fungi) Other antagonists does not seem to be important Work in progress: 1) Which microbes? Trapping fungus Pasteuria 2) How about other nematode species? ecto s endo s?
Soil food web Roots Recalcitrant OM Plant Parasitic Nematodes Fungi Fungivores Nematodes Astigmatic Mites Oribatidae Juveniles Oribatidae Adults Uropodinae Prostigmatic + Mesostigmatic mites Predatory Collembolans Collembolans Labile OM Enchytraeids Predatory Nematodes Glucose Bacteria Bacteriovores Nematodes Omnivorous Nematodes Flagellates Amoebae Holtkamp et al. submitted
Nematodes Plants Foredune, Voorne (NL) Experimental CLUE field, Mossel (NL) Species / populations Primary succession Communities Secondary succession Sowing 15 species 4 species 0 species
Plant community soil nematode community: Belowground time-lag!!!
Larger temporal scale (chronosequence) Secondary succession Ex-arable field Species-rich grassland 26 ex-arable fields (aban. 1-34 yrs ago) 3 reference sites (2 heathlands, 1 mattgrass sward) 3 current arable fields Plant community & soil nematode community (taxa, feeding groups)
Species-rich grassland heath land I heath land II Sørenson s similarity 0.08 0.04 0 0.6 0.4 0.2 0 10 20 30 0 10 20 30 0.08 0.04 0.04 0.5 0.3 0.1 0 0 10 20 30 0 10 20 30 Time since abandonment (yrs) 0.08 0 0.6 0.4 0.2 0 10 20 30 0 10 20 30 plant community nematode community Kardol et al. 2005 (Biological Conservation)
Taxonomic succession functional succession ~ Indicators for changes in soil food web structure, soil condition, successional stage Secondary succession after land abandonment: Soil organic matter C:N ratio Disturbance Fungal-bacterial ratio (v.d. Wal et al. 2006) Nematode feeding groups?
Nematode feeding groups Plant feeders Bacterial feeders Number of nematodes (100 g -1 dry soil) 2000 1500 1000 500 1200 800 400 0 10 20 30 natural Fungal feeders 1200 800 400 2500 1500 500 0 10 20 30 natural Omni-carnivores = ex-arable = matgrass sward = heath land = current arable 0 10 20 30 natural 0 10 20 30 natural Time since abandonment (yrs) Kardol et al. 2005 (Biological Conservation)
Soil food web structure Faunal analysis 100 disturbed maturing = ex-arable = species-rich grassland Enrichment Index 1 8 5 1 2 13 5 8 12 13 5 18 8 8 1 8 16 13 21 7 7 13 34 15 = heath land = current arable 0 degrading 2 9 Structure Index structured 0 100 after Ferris et al. 2001
The dogma is often that biodiversity is good; biodiversity is necessary; diverse systems are deemed more stable, more resilient, more productive, more desirable K. Ritz (2005) Nematodes as indicators for successional changes in soil biodiversity? early mid late reference 4 sites x 4 samples x 4 seasons
Nematodes vs Oribatid mites Scale? α-diversity diversity of a defined spatial unit (e.g. sample, site) γ-diversity diversity across units within a larger area (e.g. all samples in a site) β-diversity change in species composition (e.g. from sample to sample within sites)
Nematodes High in abundance after land abandonment ( primary succession) Changes in dominance patterns Increasingly heterogeneous distribution (~ patchy vegetation pattern) Controlled by site conditions Oribatid mites Low in abundance after land abandonment Colonization from external species pool (=surrounding forest) Increasingly homogeneous distribution (relative rapid dispersal) Controlled by dispersal
Successional changes in community composition Oribatid mites: colonization of new taxa from external pools Nematodes: shifts in dominance patterns Assessment of the successional changes in soil biodiversity spatio-temporal scale groups of organisms (mites vs nematodes)
To keep in mind when studying nematode-plant interactions Effects of nematodes on plants can depend on other soil organisms present Interdependence between development of nematodes and plants depend the scale (level of organization, spatial, temporal) considered Time lags / legacies Secondary succession: discrepancy in above- & belowground developments Successional patterns of nematode diversity is not necessarily indicative for diversity patterns of other groups of soil organisms.
Acknowledgements Wim v.d. Putten DEPARTMENT OF MULTITROPHIC INTERACTIONS Martijn Bezemer Anna Piśkiewicz Annemieke v.d. Wal Henk Duyts Wiecher Smant Gerlinde De Deyn Remko Holtkamp
Nematodes in restoration ecology? Greenhouse studies Soil organisms (incl. nematodes) enhance secondary grassland succession and increase plant diversity (Kardol et al. 2006; De Deyn et al. 2003) Hypothesis (field study) Simultaneous introduction of plant propagules and soil organisms from latersuccessional grassland enhances plant community development Turf transplantation Hay and /or soil spreading Donor site Top soil-removed receptor site No top soil removal
PCA nematode community 2003 PCA axis 2 (eigenvalue = 0.14) 1.0 0.0 No top soil removal Eucephalobus Acrobeles Cervidellus Chiloplacus Panagrolaimus Bunonema Helicotylenchus turfs Dorylaimoidea Tylenchidae = Donor site = Control = Hay = Soil = Hay + soil = Turf receiving = Transplanted turfs = No top soil removal donor site -1.0-1.0 0.0 1.0 2.0 PCA axis 1 (eigenvalue = 0.50) Kardol et al. (Submitted)