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Enregistrement scientifique n° : 1143Symposium n° : 9Présentation : poster

Structures related to termite activity and organic matterdynamics at different spatio-temporal scales

Structures termitiques et dynamique de la matièreorganique à différentes échelles spatio-temporelles

LEPAGE Michel, ABBADIE Luc, KONATE Souleymane, MERDACI Kamel,OUEDRAOGO Paul

Laboratoire d'Écologie, E.N.S., 46 rue d'Ulm, 75230 Paris cedex 05, France

Introduction

Heterogeneity is a major driving factor in system functioning, particularly in tropicalecosystems. A number of functional studies operating in savanna ecosystems pointed out theimportance of heterogeneity in ecosystem functioning. Some authors described landscapes asa loosely coupled and multi-leveled organization (Urban et al., 1987).Termites are a main factor of heterogenetity, through their action on soils and nutriments.This action could be considered at different spatial and temporal scales, following the viewsof Coleman et al. (1983), Lavelle (1987), Bignell et al. (1998).

The termite scale

The termite worker behaviour during the building process has been described (Grassé,1986). The individual soil pellet (10-6 m2) is crushed and masticated by the buccal appendicesand the mandibles. During this process saliva is added to the material, but the precise natureof the compounds has to be assessed. Merdaci (1994) found an enrichment of the claysparticles in soil utilized by Ancistrotermes to built its nest units (the fungus-comb chambers):6% clays in the control soil, 14% in the termite chamber. It was found an incorporation ofsugars and proteins in the rehandled soil (as stated also by Matoub (1993). The resultingeffect is also a higher micro-aggregation (< 20 m) of the material (Fuhr, 1994).

The fungus-comb chamber scale

At the level of a soil profile (1 m2), the soil rehandled by termites exhibits a highermetabolism. This was evidenced by studies on the fungus-comb chamber (10-4 m2) ofunderground species of Macrotermitinae in a Guinea savanna (Abbadie & Lepage, 1989). InLamto savanna, underground fungus-comb chambers of the dominant Macrotermitinaespecies in the biotope studied, Ancistrotermes cavithorax, reach an average density(between 5 and 25 cm depth) of 125,000-150,000 units ha-1 and represent a volume of about2-2.5 m3 ha-1 (Abbadie & Lepage, 1989). The surface area of the chambre-soil interface isabout 250-300 m2 ha-1. Soil rehandled is richer in clay particles and volumes involved areseveral m3 ha-1, without taking into account the inter-connecting galleries and passages,which length is presently unknown, but probably several km ha-1 (as compared to otherspecies: Darlington, 1982). Microbial metabolism is noticeably enhanced by the termite

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action: availability of carbon is improved through a biochemical transformation of the nativesoil organic matter and/or by the supply of easily assimilable carbon (saliva, digestiveproducts). Since microbes have only a very limited capacity for controlling their environmenttemperature, pH, oxygen partial pressure, nutrient availability (Harder et al., 1984), termitescould greatly influence these environmental parameters.The soil acted upon and brought by the fungus-growing termites has, consequently, a highermineral-nitrogen potential production: the more the soil has been reworked by termites, thehigher is the ammonium production (Abbadie & Lepage, 1989). Protozoa could also playtheir part in nitrogen cycling, as outlined by Couteauxet al. (1988).Rough calculation shows that soil brought by underground Macrotermitinae species inbuilding their fungus-comb chambers could potentialy add between 3.5 and 10 kg N ha-1,without taking into account the turnover of such structures.

The nest scale

The main advantage of the exo-symbiosis with the Termitomyces (Basidiomycete family:Amanitaceae, Heim, 1942) is to have access to a large food resource (fresh plant litter). Theenymatic capabilities of the fungus-termite association allow the degradation of lignin-cellulose complexes which are the main driving variable determining the decomposition rate(Swift et al., 1979). Under unfavourable climatic factors, termite create in their nests optimalconditions (temperature, humidity) for decomposition processes. As a consequence, fungus-growing termites are able to proceed large quantities of litter of low nutritive value with ahigh production efficiency. The mycelium growing on the comb permits the digestion of alarger amount of organic material that could not be accomplished by the termite alone. Muchof this material is bound to lignin which would be difficult for the termites to digest(Rohrmann & Rosman, 1980).The fungus growth under optimal conditions (temperature, humidity, gases (CO2) foundwithin the elaborated nest of the Macrotermitinae (10 m2), among the more sophisticatedfound in the whole termite order (Collins, 1982). Several studies enhanced the role oftermite mounds structure in modifying the internal conditions within their nests (Lüscher,1961; Noirot, 1970; Lee & Wood, 1971). The microclimatic conditions created by termitesin their nest is a advantage, specially under severe external conditions, where microbialactivity is depressed by high temperature and drought. Within the termite nest, the microbialactivity is constantly enhanced. According to Thomas (1981), the temperature withinMacrotermes bellicosus nest (around 30°C) showed to be the optimum for Termitomycesgrowth. The importance of the detritivore gut was stressed as a useful adaptation in extremeenvironments where the microbial activity is low in the surrounding soil (Crawford &Taylor, 1984). As outlined by these authors, the rates of essential processes, likedecomposition, are often highly variable in time and space. Global models available oftenunderestimate decomposition in arid ecosystems since they ignore the favorable conditionscreate within the termite nest, in association with the cellulolytic symbionts. This explain thatthe relative importance of Macrotermitinae in nutrients dynamics is increasing towards dryparts of a climatic gradient in African savannas (Menaut et al., 1985; Wood & Sands, 1978;Lepage, 1983).

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The scale of the termitaria

At the scale of the termitaria (102 m2), the soil particles distribution is modified (soil broughtfrom deeper horizons): mounds are 3 to 4 times richer in clay than the surrounding soil(15.5% as compared to 4.5%) (Abbadie et al., 1992). This has consequences on waterdynamics: the field capacity on the mound top is higher than in the savanna soil around(Konaté et al., this volume). The termitaria are also richer in organic matter. Total organiccarbon and nitrogen on the top are three times higher than in the surrounding soil.In their study, Abbadie et al. (1992) calculated that mound bases occupied 9% of the areaand represented a volume of 300 m3 ha-1 above the ground. As a consequence, termitaria arepatches of typical woody savanna vegetation. Tree density is increased since mounds arefavourable sites for tree development, specially for seedlings. High concentration ofnutrients, water availability and good drainage are the major causes of increased biomass anddifferent species composition around the mound (Arshad, 1982). In most situations theisotopic composition of the control soil is characteristic of C4 plants (grasses), while organicmatter on mounds tops is characteristic of C3 plants (trees) (Abbadie et al., 1992).The organic matter accumulation in mound soil has three main explanations. First it is wellknown that clays protect organic matter against mineralization. Secondly, termites collectlitter on the ground and concentrate this material in their nests. Thirdly, the mounds supporta large plant biomass composed mostly of trees (Abbadie et al., 1992).In several tropical ecosystems, large termitaria are a prominent feature. Synthetic data aregiven by Lee & Wood (1971) and by Wood & Sands (1978). For example, in the Zaïreprovince of Shaba, mounds contain large quantities of nutrients in their soil. Althoughtermitaria do represent 9% of the area, they hold (in 0-120 cm thickness soil) 14.5% of thecarbon, 16.8% of the total nitrogen and contain as much as 74.8% of the exchangeablecalcium, 47.0% of the exchangeable magnesium and 61.6% of the exchangeable potassium(data calculated from Malaisse, 1978).At the scale of the soil catena and the watershed (106 m2), termites create and maintainheterogeneity patterns (Ouedraogo & Lepage, this volume). The high patchiness of termiteconsumption on litter and their concentration of nutrients is important in forest dynamics asthey provide abundant and potentially important microsites for tree-seedling establishment.In all cases, termite action accentuate habitat patchiness (Salick et al., 1983). In Seregenti,termite activity is probably the main factor explaining the mosaic vegetation patterns ingrassland site as densely vegetated mid-grass patches are found on abandoned termitemounds. (Belsky, 1983).

The regional scale

According to Sanford et al. (1983), two main constraints limit the fertility of tropical soilsand their utilization in agriculture: the erodability and low available nutrient supply. Soilorganic matter content is the best indicator of this status of the soil. The soil organic carboncontent of the soil depend upon the water holding capacity, the soil aeration, the cationexchange capacity, the nitrogen content, and other nutrients content (mainly P and S).In evaluating the termite effect on soil carbon and nitrogen contents, it should be taken intoaccount the trends observed, since it was shown (Menaut et al., 1985) that the fungus-growing termites increased relatively in importance towards the dry part of a climaticgradient. C:N ratio is obviously modified by termite action but the main question is to whatextent. As far as Macrotermitinae are concerned, C:N ratio on mound exhibited lower valuethan the surrounding soil. For example, Boyer (1955) found that the outer layer ofMacrotermes bellicosus mound had a C:N ratio of about 10-12, while for inner portion ofthe mound, the ratio was about 6.5. The same author (Boyer, 1956) found a C:N ratio of 2.7

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in the royal cell of M. bellicosus and M. subhyalinus, compared with 6.7 in outer moundlayers and 10-12 in the soil of termite galleries. C:N ratios in mound and surrounding soilsaffected by termite in Kenya are similar to C:N ratio in termite bodies (5-12), while C:N insoils without termites are 12 to 20 (Arshad, 1981; Jones, 1990).Macrotermitinae differ in that respect from other termite species which utilized faeces tobuilt their nest structures (like the Nasutitermitinae). In that case, C:N ratio of mound aremuch higher than the control soil, as discussed by Lee & Wood (1971). Nasutitermitinaehave high carbon/nitrogen ratios: 20-25 in nests of grass-feeding species, more than 50 andup to 100 in nests of wood-feeding species.The termite action, in one hand, decrease the soil organic matter light fraction and increasethe pool of slow soil organic matter (physically protected by clays). In the other hand, thehigh respiration rates of the termite/fungus sub-system has the result to decrease the C:Nratio of the organic matter returned to the ecosystem (through predation, saliva, fungus-comb material ...).One can question if the tremendous effect of termites (especially Macrotermitinae) on soiland litter consumption during thousands of years could account for the observed value oforganic matter content in tropical soils and expressed by the ratio C:N. Recently, Jones(1990) formulated a hypothesis to picture the termite influence on soil fertility and carboncycling. Holt (1987) raise also this question. Without termite activity, litter is decomposed insitu by either soil fauna and microorganisms. When termites are present (mainly nests offungus-growing termites), litter is redistributed, stored in mounds and more efficientlydecomposed, with CO2 as the main end product. Nutrients are not immediatly available tothe ecosystem, except through predation. Jones (1990) formulate the hypothesis thattermites could be responsible for soil nutrient depletion in some dry areas of Africa. If true,this will have consequence in the global nutrient budget.Additional indirect evidence of the role of termites in nutrient depletion came from the lowermicrobial populations reported in inter-mound soil as compared with outside-mound(Arshad et al., 1982; Keya et al., 1982; Meiklejohn, 1965).The main resulting effect of Macrotermitinae in ecosystem is to cycle a significant amount ofcarbon, mostly in the form of CO2, though some authors (Zimmerman et al., 1982; Seiler etal., 1984) claimed than termites could play a substancial role in CH4 release into theatmosphere. This CO2 source, which is under-estimated when assessing the role of termitesin greenhouse gases, could represent 10 times more than the CO2 emitted from the termiterespiration itself (Lepage & Rouland, under prep.).

Discussion

The effects of termites in ecosystem functioning, and specially on organic mater dynamics,could be viewed in the light of the « ecosystem engineers » concept as outlined by Lawton &Jones (1995). Through their activities in nest building, termites directly and indirectlymodulate the avaibility of resources to microorganisms. The structures of termite nest-unitsand termite mounds are extended phenotypes (in the sense of Dawkins, 1989). The shape,dimensions, material utilized in termite nest do correspond to termite life history traits. Inturn, these structures have deep influence upon the ecosystem functioning and dynamics.What should be stressed is the scale of this engineering impact. It depend upon the termitespecies involved, the population density, the spacial distribution, both locally and regionallyand also, upon the durability of contructs (short-term or long-term effects). A study of theeffect of termites on ecosystem should consider the inter-related scales of this action,keeping in mind that the structure observed (in space and time) is the mediator between thetermite biology (phenotypic traits: foraging, food consumption and metabolism, buildingbehaviour) and its influence on the other ecosystem components.

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Key words : termites, structures, organic matter, microbial metabolismMots clés : termites, structures, matière organique, métabolisme microbien