Is plant biodiversity driven by decomposition processes? An emerging new theory on plant diversity

Diversity of forest trees ranges from monospecific stands to the astonishing richness of tierra firma tropical forests. Such patterns are observed along gradients of latitude, altitude, soil fertility and rainfall. So far, the proposed coexisting mechanisms do not provide a comprehensive and unequivocal explanation of these patterns at the community level. We propose a new theory linking species diversity with organic matter cycle and negative plant-soil feedback induced by litter autotoxicity. This approach focuses on resource-waste rather than resource-only dynamics. High diversity does occur where litter decomposition is rapid and ecosystem nutrient cycles are closed. On the other hand, single species dominance is found where litter decomposition is slow and/or autotoxicity is removed from the nutrient cycle pathway. Unlike previous theoretical views, the one we present proves potentially capable of explaining differences in species diversity both along environmental gradients and within the tropics. Plant-soil negative feedback Negative plant-soil feedback is defined as the rise of negative conditions for plant vegetative and reproductive performances induced in the soil by the plants themselves. Ancient evidences of this phenomenon are well known for agro-ecosystems, where it has been referred as ‘soil sickness’ or “replant disease problem” (Zucconi 1996, Miller 1996). To find any herbaceous plantations or orchards that do not experience the consequences of negative feedback when cultivated in monoculture and monosuccession is a hard challenge. Several studies have demonstrated the pervasiveness of negative plant-soil feedback in natural plant communities. This has been reported for coastal sand dunes during primary succession (Van der Putten et al. 1993), secondary succession and temperate grasslands (Bever 1994, Klironomos 2002, Bonanomi et al. 2005b), and temperate (Streng et al. 1989, Packer and Clay 2000) and tropical forests (Webb et al. 1967, Kiers et al. 2000). In a literature survey, reported as Appendix to this paper, we found 138 experimental cases of plant-soil negative feedback on terrestrial ecosystems, but none for flowering plants and algae in marine and freshwater environments Appendix 1). Four main mechanisms have been proposed to explain plant-soil negative feedback: soil nutrient depletion (Berendse 1994, Ehrenfeld at al. 2005), the build-up of soilborne pathogen populations (De Rooij-van Der Goes 1995, Packer and Clay 2000), the changing composition of soil microbial communities (Bever 1994, Klironomos 2002, Kardol et al. 2007), and the release of phytotoxic compounds during organic matter decomposition (Webb et al. 1967, Singh et al. 1999, Armstrong and Armstrong 2001). In our review (Appendix 1), 31.9% of the cases of negative feedback were ascribed to litter autotoxicity. Negative feedback escape strategies depend on life form and propagation patterns. For instance, perennial clonal plants can move away by vegetative growth (Van der Putten 2003), while trees and shrubs can avoid the “home” soil (sensu Bever 1994) via seed dispersion, thus producing a Janzen-Connell distribution of seedling emergence (Packer and Clay 2000). Negative plant-soil feedback has been demonstrated to be strongly species-specific and mainly affecting individuals of the same species (Oremus and Otten 1981, Van der Putten et al. 1993, Bever 1994, Singh et al. 1999, Klironomos 2002, Bonanomi and Mazzoleni 2005, Kardol et al. 2007). Phytotoxicity of decaying litter Many studies reported on the phytotoxic effects of decaying plant materials (review in Rice 1984 and Blum et al. 1999). However, during decomposition, both the abundance and the activity of phytotoxic compounds continuously change over time by their sorption and polymerisation on soil organic matter and clay minerals (Makino et al. 1996), and because of the chemical transformation by microorganisms (Blum et al. 1999). This was explicitly assessed by Harper (1977) in a review of allelopathy, who pointed out that plant-produced phytotoxic compounds, being rapidly degraded by the soil microbial activity into non-toxic molecules, should have a limited expected impact on plant population dynamics. Moreover, studies of allelopathy in field conditions are rare and their interpretability has been limited by the lack of comparative experimental bioassays (Inderjit and Callaway 2003). A renewed interest in this issue followed the work of Bonanomi et al. (2006) showing not only a widespread occurrence of phytotoxicity in decaying plant litter, but also predictable dynamics in relation to both the decomposition duration and the environmental conditions. Although different levels of litter phytotoxicity were observed for different plant functional groups (nitrogen fixer > forbs = woody >> grasses–sedges), all tested species (n=25) showed consistent patterns of phytotoxicity dynamics, with a rapid decrease in aerobic conditions, but sharp increase and stabilization of toxicity in anaerobic conditions. We are currently doing in depth experimental investigations on the prevalence of autotoxicity compared to generic phytotoxicity of decaying litter. Based on our experiments so far (Bonanomi et al. 2006; unpublished data) and evidenced by other published literature (Appendix 1), we propose that autotoxicity is a general phenomenon, and stronger than phytotoxic effects on other species, thus largely affecting ecosystem stability, productivity and diversity. Despite the availability of mineralized nutrients, the root colonization of decomposing plant litter can require several weeks for herbaceous species (about 35 days for many grasses; reviewed by Hodge 2004), but even months for temperate forest trees under field conditions (Conn and Dighton 2000). This sharply contrasts with observations of roots actively proliferating within few days into enriched patches of mineral nutrients (Jackson and Caldwell 1989), but it is consistent with the phytotoxicity of decomposing litter. An emerging theory: litter autotoxicity links decomposition processes with species coexistence Decomposition of plant litter is a key ecosystem process for carbon and nutrients cycling. The factors affecting the decomposition rates and the related dynamics of nutrients have been investigated in depth in relation to both environmental conditions and litter chemical characteristics (Aerts 1997, Berg and McClaugherty 2003). We suggest that the view of plant litter as a nutrient source, without inclusion of the phytotoxicity concept, is limiting because the simultaneous release of nutrients and phytotoxicity during decomposition can produce unavoidable constraints to plant growth. The potential consequences of these concepts are relevant in the context of plant community organization. The proposed new theory is based on two interlinked ideas: 1. decaying litter produces autotoxic effects, and 2. the impact of autotoxicity is dependent on the litter decaying-rate.