UMR7618 « Biogeochemistry and ecology of continental ecosystems »

1. UMR7618 « Biogeochemistry and ecology of continental ecosystems » Ecological interactions in soils S. Barot http://millsonia.free.fr/sebastien.barot@ird.fr

2. What is ecology? • It is the science that studies interactions between organisms and between organisms and their environment Species 1 Higher scales Abiotic environment Species 2 • This means we must study biotic interactions but also interactions between the biotic and abiotic world • We must also study purely abiotic interactions • All these interactions must be studied to predict properties at higher scales (population, ecosystem, biosphere…)

3. How can we classify ecological interactions? Biotic interactions Species 1 Species 2 Classical classification in ecology!!!

4. How can we classify ecological interactions? Biotic-abiotic interactions • Historically ecology has emphasized biotic interactions … competition is at the heart of the most famous ecological theories • “general ecology” has often forgot about interactions with the abiotic environment Species Abiotic environment Organisms also modify their physico-chemical environment • Notion of ecosystem engineer

5. Goal of this lecture • To show that all types of ecological interactions occur in soils • To show that all these interactions are involved in well-known soil processes • To show that biotic-abiotic interactions are particularly important in soils

6. Some issues to be discussed at the end of the lecture Can we identify some important knowledge gaps? Are some types of ecological interactions unique in soils? Can soil ecology throw new lights on general ecology?

7. Competition Examples?

8. Competition for a limiting resource Interspecific competition Intraspecific competition Species 1 Species 2 Limiting resource • It is a key biotic interaction in ecology … tightly linked to many principles of ecology • Should be very influential for evolution and the structure of communities

9. Example 1 : competition between earthworms Baker 2002 Butt 1994 Interspecific competition Intraspecific competition What do they compete for? What is the limiting factor?

10. Example 2 : bacteria Rich and poor mediums to cultivate a community of bacteria Nutrient-rich medium Nutrient-poor medium Travisiano 2000 • Competition is stronger when resource is poorly available • This leads to the exclusion of many species

11. Example 2: bacteria • Many experimental studies in controlled conditions But, what is the real impact of competition on the structureof bacterial communities in soils? • Cooperation between bacteria is also studied (quorum sensing, production of exoenzymes …) • Soil is extremely heterogeneous : Many micro-habitats Many types of molecules Consequences? • More complementarity, less competition, more bacteria coexist?

12. Example 3: a well known case in soils Competition between plants and soil microorganisms for mineral nutrients • Plant mostly absorb mineral nutrients under their mineral forms • Bacteria and fungi can exploit these nutrients under both their mineral and organic forms • This should strongly influence primary production Who is the better competitor? • Large surface-area:volume ratios and rapid growth rates compared with plant roots Micro-organisms are better competitors?

13. Predation Examples?

14. Intricate food webs Are these food webs different from aboveground food webs?

15. The brown food web • Aboveground food web is based on the consumption of the biomass of primary producers (green food web) • Belowground food web is based on the consumption of dead organic matter (brown food web) What are the consequences of predation in soils in terms of nutrient and carbon cycling? • Release of CO2 • Release of mineral nutrient • Stimulates the growth of microbes and mineralization • Top-down control of microbes by predators : mineral nutrients are more available to plants

16. Example of the microbial loop • Root exudates stimulate the growth of bacteria • Subsequently this attracts protozoa that eat bacteria • These protozoa release ammonium Without predation, plants would not benefit from their exudates Bonkowski

17. Symbiosis / mutualism Examples? Difference between the two?

18. Famous example 1 : mycorrhizae • What is exchanged between the mycorrhizae and the primary producer? • The PP gives organic matter • Mycorrhizae give mineral nutrients Why are mycorrhizae so efficient at gathering mineral nutrients?

19. Famous example 2 : nitrogen fixation • What is exchanged between the bacteria and the legumes? • The legume gives organic matter • Bacteria give nitrogen

20. Consequences at higher scales What is the effect of nitrogen fixation for the ecosystem? • Nitrogen enrichment • Nitrogen fixing plants are very important at the beginning of successions (young soil) • Young soils tend to be N limited, while old soils tend to be P limitedVitousek • Cycles between fixer and non-fixers

21. Consequences at higher scales • Cycles between fixer and non-fixers Jenerette 2004 Oikos

22. War and peace in symbioses What can we expect about the evolutionary stability of symbioses? • Each member of the symbiosis could evolve the capacity to cheat = to receive more than it gives • Various hypotheses The organic matter and minerals that are exchanged correspond to a luxury consumption Complex pathways of signalization have evolved to control the interaction and allow to punish cheaters Denison, Kiers …

23. War and peace in symbioses Why plants have not all evolved symbiotic nitrogen fixation? • Very important issue because answering this question allows understanding why nitrogen so often limits primary production • Two complementary hypotheses Maintaining the symbiosis and feeding the bacteria is too costly Nitrogen fixing plants are too vulnerable to cheaters = non-fixing plants (that do not support the cost of fixation but indirectly benefit from fixation)

24. Biotic-abiotic interactions Examples?

25. Uniqueness of soil as an habitat/ecosystem Living in the soil • For macro-organisms living and moving in the soil requires modifying the soil Earthworm galleries Roots dig their way through the soil / bring together soil particles / limit erosion

26. Uniqueness of soil as an habitat/ecosystem Living in the soil • For micro-organisms living in the soil might also influence soil structure Plant fragment Fungal hypha Ciment that brings together the agregatePartially composed of bacteria material

27. Uniqueness of soil as an habitat/ecosystem Eating in the soil • Detritivores are often obliged to eat both organic matter and mineral material : eat the soil altogether • Eating organic matter transforms the organic matter (it is only partially digested) • Eating organic matter and moving in the soil mix the soil and its organic matter (bioturbation) • Feces = new aggregates are produced Earthworm cast

28. Consequences for other organisms Why could ecosystem engineering be more influential than any biotic interaction in the soil? • Ecosystem engineers modifies the physico-chemical environment that is shared by all organisms • They indirectly influence all organisms while biotic interactions tend to be more specific Species 1 / group of species Species 2 / group of species Potentially all species are influenced Physico-chemical characteristics of the soil Ecosystem engineer

29. Consequences for soil ecology All these arguments suggest that ecosystem engineers are very influential for soil functioning !!!

30. Example : earthworm invasion!!! • European earthworms are invading the north of USA and Canada Modification of soil properties What is the mechanism? Bohlen 2004

31. Example : earthworm invasion!!! Increase in microbial biomass What is the mechanism? Groffman 2004

32. Example : earthworm invasion!!! Negative impact on plants What is the mechanism? Hale 2006 Ecology

33. Example : earthworm invasion!!! Where are the earthworms? Are all these effects good or bad?

34. Feedbacks + Ecosystemengineer Environment + - • Engineers may be impacted by their own engineering activities What can be the consequences? • Negative feedbacks : negative density dependence • Positive feedbacks : positive density dependence Niche construction !!!

35. Feedbacks + Ecosystemengineer Environment - / + • This can lead to complicated dynamics : Equilibrium Cycles Chaotic dynamics Barot 2007 SBB

36. Conclusion

37. All types of interactions • Of course all types of ecological interaction can be encountered in soils • Importance of feedbacks between soil organisms and soil physico-chemical properties • These interactions even when they involve very small organisms may have consequences for the whole ecosystem functioning Soil structure Soil fertility Primary production

38. All types of interactions occurring at the same time Interactions between plants and bacteria • Perfect symbiosis? PP need decomposers and decomposers need PP • But plants and bacteria also compete for mineral nutrients!!! • But bacteria also produce many hormone-like molecules that manipulate plant growth and architecture … this may have positive and negative effect on plants How all these interactions have evolved?

39. All types of interactions occurring at the same time Interaction between earthworms and bacteria • Earthworms stimulate bacteria activities in their guts These bacteria produce enzymes that help earthworms to digest more organic matter Again, a perfect symbiosis? • But earthworms also digest a part of the bacteria they ingest :predation • But earthworms and bacteria somehow also compete for the same organic matter … the more OM is digested by bacteria the less food have earthworms …. competition Taken together, what is the status of the interaction? Evolution?

40. Some issues to be discussed at the end of the lecture Can we identify some important knowledge gaps? Are some types of ecological interactions unique in soils? Can soil ecology throw new lights on general ecology?