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M. mayaguensis M. arenaria

Class of adhering endospores: 0=0; 1=1-5; 2=6-10; 3=11-50; 4=>50

Davies, Redden, & Pearson (1994) observed a bacterial surface heterogeneity in P. penetrans isolates. The nature of the specificity appears to depend on the biochemical interactions occurring during the contact between the bacterial parasporal fibers surrounding the endospores and some epitopes present on the nematode cuticle surface. Immunological studies on root-knot nematodes cuticle showed that some proteins are involved in the process of host recognition (Davies, Robinson, & Laird, 1992). Either the quality and amounts of these proteins differed among the nematodes species tested, suggesting that they may be responsible for the variability expressed in some specificity studies (Davies & Danks, 1992). However, as several aspects of the mechanism of endospore adhesion remain still undeciphered, the exact determinism of the host specificity process still remains to be completed (Davies et al., 2001).

3.3. Obligate Multitrophic Relationships

Pasteuria penetrans either reduces juvenile penetration in roots because of their strong spore encumberment (Stirling, Sharma, & Perry, 1990), or decreases the density of new generation juveniles in the soil (O' Brien, 1980; Sayre, 1980; Raj & Mani, 1988; Sayre & Starr, 1988). In this case, nematodes produce more P. penetrans spores than eggs (Sayre & Starr, 1985). This density-dependence relationship was suspected by Spaull (1981) on sugarcane and Verdejo-Lucas (1992) observed similar seasonal fluctuations between populations of M. incognita, M. arenaria, M. hapla and populations of P. penetrans.

Ciancio (1995, 1996) was the first to model density-dependence relationships between plant-parasitic nematodes and P. penetrans. But, as plants, nematodes and P. penetrans correspond to an obligate tritrophic system, plants can indirectly act on the prey-predator relationship too.

Nematode and P. penetrans surveys carried out in various vegetable producing areas revealed correspondences between vegetable species and the abundance of Meloidogyne juveniles infested by P. penetrans (Diop, Mateille, N'Diaye, Dabire, & Duponnois, 1996; Hewlett, Cox, Dickson, & Dunn, 1994; Ko, Bernard, Schmitt, & Sipes, 1995; Tzortzakakis, Channer, & Gowen, 1995; Mateille, Duponnois, & Diop, 1995; Giannakou & Gowen, 1996). Most of them observed that either plant susceptibility to nematodes or crop practices (sequences of different plant susceptibilities) influence the proportions of infested juveniles, since development of bacterial populations depends on the abundance of nematode juveniles in the soil.

4. ECOLOGY AND MANAGEMENT OF NEMATODE COMMUNITIES 4.1. Soil Health Approach

Plant production is directly related to soil quality, defined by its functional capacity within an ecosystem with three concerns: biological productivity, environment quality, and plant/animal health (Doran, Sarrantonio, & Liebig, 1996). Soil quality includes three basic components: physical, chemical and biological soil properties.

Biological properties relate to four fields (Chaussod, 2002): fertility, health, environmental impact and resilience. Soil health relates more to ecological characteristics (Doran & Zeiss, 2000) and deals with agronomy (Doran & Safley, 2002). A good health situation is usually correlated with fast nutrient cycles, a strong stability (high resistance or resilience) and a wide biodiversity. Low biodiversities are commonly observed in very high value and high input agrosystems (Anderson, 1994).

In both temperate (Evans et al., 1993) and tropical regions (Luc et al., 2005), strong anthropized agrosystems are mostly characterized by low diversified nematode communities (less than 10 plant-parasitic species). Among these species, some of them can be very frequent and abundant. That is, for example, the case for root-knot nematodes in intensive vegetable producing areas. In these agrosystems, conditions favor nematodes as root-knot nematodes which display high rates of multiplication and cause important plant damages and yield losses. Nematode control methods necessarily imply substantial inputs and lead to both economic and ecological dead ends.

In low anthropized agrosystems, which relate to organic or extensive agriculture, mostly based on fallowing, crop associations or rotations, nematode diversity is usually higher. For example, studies conducted on fallowing (Cadet & Floret, 1999) showed that nematode diversity in communities increases with age of fallows and that damages caused by such communities to the next cereal crop were lower.

The species diversity in plant-parasitic nematode communities can be very high in ecosystems: for example, about 20 species were detected in Atlantic and Mediterranean French coastal sand dunes (Maher et al., 2004) and approximately 30 species in the French Landes forest (Baujard, Comps, & Scotto La Massese, 1979), apparently without damage in these areas.

4.2. New Paradigms for Nematode Management

High-grade results achieved by crop protection researches carried out on crop practices, plant resistance to nematodes or biocontrol, are very diverse. But, all these control practices, included or not in integrated pest management strategies, seem not to be sufficient: they all target some nematode species (population approach), and then induce changes in nematode communities but do not necessarely decrease their overall pathogenicity. Also, drastic control methods induce biotic imbalances by killing parasites but also their antagonists (direct effect or indirect through host population depletion). So, binary researches focused on plant-nematode or nematode-parasite relationships should be extended to ecological investigations on nematode communities.

Figure 6. Nematode management, from therapeutic to ecological approaches.

An alternative consists in eco-epidemiological approaches through interactions existing within communities (interspecific competitions, biological and edaphic constrains) which focus on the management of the parasite biodiversity (Fig. 6).

Specific and functional evolution, and pullulation of plant-parasite populations, especially of plant-parasitic nematodes, are enhanced by agriculture intensification and by environment anthropisation. In fact, plant-parasitic nematodes as "predators" belong to a food web as parts of soil factors. Up to now, all control strategies developed in agriculture focus on the eradication of target species. This induces biotic gaps, community rearragements, insurgence of virulent races, increased aggressivity of minor species, etc. and this, the "soil cleaning" strategy, appears to be not sustainable.

The development of sustainable management strategies should move from such "therapeutic approach" (much in favour in research program strategies carried out in the world) to some more "ecological approach". This approach would seek for information and knowledge about biotic trade-offs in ecosystems, in order to introduce them in agrosystems (resilience). This strategy would question: why seeking plant-parasitic nematode eradication? Can agronomic problems be solved by agronomic strategies only? Can nematode diversity in communities be considered as an auxiliary for nematode management?

4.3. Proposed Approaches

The nematode diversity in communities would represent the central object to focus on, and species diversity as well as population levels in communities would be tested for their indication capacity. They could be related to or account for inform on environment disturbances and capacity to facilitate or not epidemics, for soil resistance and resilience. Comparative studies of environments displaying contrasted characteristics or different anthropisation levels should provide understanding of interactions and clues for management, strategies for more or less intensively run agrosystems or endangered environments.

Three types of contexts can be studied:

• Ecosystems: these systems are particularly appropriate to study plant-nematode tradeoffs. They involve "horizontal" biotic regulations defined by the interspecific competitions in the communities (Putten, Vet, Harvey, & Wackers, 2001): competitions for habitat occupation and for food resources. Specific biological characteristics (life traits, rate of multiplication) will account for such interaction and it is essential to understand the different species fit with each other within a community. They also involve "vertical" biotic regulations related to crop and soil (microbial antagonists) constraints on the species within communities. Obviously, as plant-parasitic nematodes are obligate parasites, the plant plays a major role in the nematode community structure; this depends on both plant susceptibility to different species and on species pathogenicity. Because of their specificities, microbial antagonists also have a marked impact on community structures (De Rooij-van der Goes, Van der Putten, & Van Dijk, 1995). Eventually, abiotic regulations (soil physicochemical factors and functions) also affect the space-time structure of nematode communities (Cadet, Thioulouse, & Albrecht, 1994; Cadet & Thioulouse, 1998).

Organic agriculture: in organic agriculture, the management of plant-parasitic nematodes implies crop diversification, rotations with non-host or poor host plants, amendments with green manures, biofumigation methods. All these methods enhance biodiversity in soils, as a source of significant biological competitions. Organic agriculture makes it possible to analyze consequences of methods specifically targeting "major" species on the whole nematode communities, without skews induced by chemical treatments.

• Land use changes: these situations induce shifts in community structures, the determinant of which should provide clues for processes involved in community structuring. The original nematode structure, before changing the land use, followed along a time course, should provide elements for understanding new interactions and patterns.

Figure 7. The soil health approach. The pathogenicity of a nematode community is higher in agrosystems than in ecosystems (1). Its increase in agrosystems depends on the structure of the community: same species but different proportions (2a), or lower richness (2b). Conservation strategies for resilience (3).

Figure 7. The soil health approach. The pathogenicity of a nematode community is higher in agrosystems than in ecosystems (1). Its increase in agrosystems depends on the structure of the community: same species but different proportions (2a), or lower richness (2b). Conservation strategies for resilience (3).

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