Interaction between soil fauna and their environment Jean-François Ponge To cite this version: Jean-François Ponge. Interaction between soil fauna and their environment. Rastin, N., Bauhus, J. Going underground: ecological studies in forest soils, Research Signpost, pp.45-76, 1999. hal- 00504819 HAL Id: hal-00504819 https://hal.archives-ouvertes.fr/hal-00504819 Submitted on 21 Jul 2010 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. INTERACTION BETWEEN SOIL FAUNA AND THEIR ENVIRONMENT PONGE Jean-François, Museum National d'Histoire Naturelle, Laboratoire d'Ecologie Générale, 4 avenue du Petit-Château, 91800 Brunoy (France), tel. +33 1 60479213, fax +33 1 60465009, E-mail: Jean- [email protected] Running title: SOIL FAUNA AND ENVIRONMENT Abstract and associate functions in forest ecosystems (1, 2). From agents helping in tree nutrition (symbiotic Interactions between soil animals and their organisms) and recycling of primary production environment can be described in terms of positive (decomposers) they passed to the status of full and negative feed-back loops taking place in the members of the forest ecosystem, acting side-by- build-up and steady-state of soil ecosystems, side with trees to ensure its build-up and stability respectively. The size of animals determines the (3, 4, 5, 6). This is mainly due to the discovery of scale at which they interact with their physical and mutualistic relationships between soil organisms, biotic environment. Nevertheless varying scales at their immediate environment, and major processes which animals intervene in functional processes is such as litter decomposition, root growth, and not relevant to any hierarchical position within the forest dynamics. ecosystem, due to symmetrical patterns in the relationships between microbes, animals, humus Mutualistic relationships may be expressed in forms and vegetation types. The present terms of feed-back loops, a mathematical concept knowledge has been reviewed and discussed to the erected by Wiener (7) to describe interactions light of an integrated view of the soil ecosystem, within systems of a high degree of complexity with a particular accent put on soil acidity. such as living organisms or self-regulating machines. When two sub-systems interact in a repressive manner, their interaction, called Introduction negative feed-back, leads to an equilibrium. This is a basic concept in homeostasis. On the contrary positive feed-back loops are characterized by a During the last decade a considerable reciprocal stimulation or synergy between two reappraisal has been made of the role of organisms sub-systems. This concept, firstly used to describe biological systems, more especially nervous reinforced by plant-soil relationships. It has been systems, has been successfully applied to observed for a long time that when a plant species ecosystems (1, 3). grew in moder humus, i.e. with a slow disappearance of litter and mostly epigeic fauna Compared to biological systems, where (arthropods, enchytraeids), it exhibited a higher negative feed-back loops (steady-state or buffer content in phenolic substances than when growing mechanisms) predominate, thus ensuring stability in mull humus, i.e. with a rapid disappearance of of the organism, ecological systems show phases litter and high earthworm activity (14). This of build-up followed by phases of collapse, also increase in polyphenol content was experimentally called aggradation and disintegration, respectively demonstrated to be favoured by a decrease in (1, 8, 9). Such shifts in ecosystem properties can nitrogen availability (15). Instead of stabilizing the be explained by positive feed-back loops, i.e. self- forest ecosystem, this process, in the absence of reinforcing mechanisms. Contrary to claims by further disturbance, can lead to a shift towards Perry et al. (3), positive feed-back loops, despite other ecosystems which are better adapted to their promising name, should not be considered as nutrient-poor conditions, such as ericaceous heaths stabilizing forces for a given ecosystem. Rather, with mor humus, i.e. with poor faunal and they force it definitely from one state to another; microbial activity (5). more precisely from a given temporary equilibrium (stabilized by negative feed-back Negative feed-back loops (steady-state loops) to another. As an example we can consider mechanisms) may be found, for instance in the the role of phenolics in forest ecosystems. The ability of earthworms to buffer the pH of their polyphenol content of tree foliage is known to immediate environment (16), due to amphoteric control the release of nitrogen in a mineral form properties of their mucus (17). This points to the during litter decomposition, i.e. the higher the importance of changing constantly the scale at amount of polyphenols, the slower the rate of which processes should be studied if we want to nitrogen mineralization (10). The accumulation of understand the functioning and the fate of forest recalcitrant forms of nitrogen (which are repellent ecosystems (18, 19). We know now that to a lot of organisms) is due to the build-up of a mechanisms by which a soil animal is able to find layer of unincorporated organic matter (11). This suitable food and habitat within a space of, say, a creates locally acid conditions through slow few cubic centimeters (20), are as important for oxydative processes involved in humification (12). the fate of forest ecosysems as mechanisms which These conditions favour acid-tolerant soil operate the growth and death of trees (19). The organisms which contribute in turn to increase the present paper will be focused on the feed-back acidity of their environment, such as brown-rot processes (positive as well as negative) by which fungi (13). This positive feed-back loop is itself soil animals interact not only with their immediate environment (the litter, the soil, and their profile, associating food resources and habitats in inhabitants) but also with other compartments of a number of combinations which encourage a wide forest ecosystems such as tree canopies. range of animal groups to cohabit and interact. This could explain why high densities of earthworms have been found constantly associated Macrofauna with high diversity and density of other saprophagous macrofauna such as slugs, woodlice Interactions between macrofauna species and millipeds (41, 42, 43, 44, 45, 46). Most interactions between macrofauna and The absence (egoism of species) or the the soil environment concern mainly saprophagous existence of antagonistic/mutualistic relationships animals, i.e. animals eating on litter or soil organic among animals of the same size, feeding on matter. The huge amount and variety of dead similar food resources (for instance decaying organic matter produced by forests, both above- leaves or needles, or roots) has been debated (47, and below-ground (21,22), and the amount and 48). Unfortunately few studies directly addressed variety of microorganisms living in litter and this question, given the specialization of most soil underlying horizons (23), may explain why big- zoologists for a given animal group if not for a sized saprophagous invertebrates are to be found given species. in such varied groups, with so strongly varying ecological requirements, such as molluscs, By comparing earthworm communities annelids and arthropods. Nevertheless the present in above-ground ant nests with the abundance and diversity of resources created by surrounding soil and litter Laakso & Setälä (49) plant-microbe interactions cannot itself explain the demonstrated that litter-dwelling earthworms, and diversity of macrofauna in forest soils. more especially Dendrodrilus rubidus, were favoured to a large extent by the wetter By their movements and feeding behaviour, environmental conditions and the abundance of saprophagous macrofauna transform various plant food prevailing in ant mounds. The worms debris into compact aggregates, mixed or not with escaped predation by ants owing to the repellence mineral matter, create cavities in the soil, make of their mucus. No true mutualism was holes in dead leaves, wood and bark remnants, demonstrated but this study gave evidence that a transport entire leaves or needles down to mineral combination of repulsion (earthworms to ants) and horizons or defecate mineral matter within litter attraction (ants to earthworms) mechanisms may horizons (24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, explain the observed co-occurrence of Formica 35, 36, 37, 38, 39, 40). This activity creates a aquilonia and D. rubidus. permanent movement of matter within the humus By analysing gut contents of co-existing presence of living earthworms. Although earthworm species, and comparing them with Marinissen & Bok (51) claimed that the observed aggregates forming the mull A horizon into which effects were due to changes in soil structure, they were living, Bernier (40) concluded to the nothing is known of the mechanisms actually existence of synergistic relationships between involved in these