Effects of environmental factors and leaf chemistry on leaf litter colonization by fungi in a Mediterranean shrubland
Introduction
Litter is an important source of dead organic matter in terrestrial ecosystems, with inputs of 50×109 tons of litter per year (Isidorov and Jdanova, 2002). Litter decomposition contributes directly to nutrient availability both for plant growth and ecosystem productivity (Koukoura et al., 2003). The studies that have taken microorganisms into account agree in giving the fungi as the main contributors to leaf litter decomposition (Toutain, 1987; Isidorov and Jdanova, 2002).
These eukaryotes are able to hydrolyse and assimilate refractory compounds such as lignin (Criquet et al., 1999) or tannins (Iacazio et al., 2000), although bacteria are not thought to degrade the leaf material before it has become partially broken down by microarthropods and partially decomposed by fungi (Périssol et al., 1993; Dilly et al., 2001).
Litter fungal colonization is regulated both by exogenous or environmental factors and endogenous factors. Environmental factors include climate and soil nutrient availability (Cortez et al., 1996), endogenous factors are leaf litter nutrient content (e.g. C, N, P) and secondary metabolites (e.g. phenolic compounds) content (Melin, 1930; Koukoura et al., 2003).
With regard to environmental factors, Mediterranean shrublands are characterized by low water availability and low soil organic matter content, the latter parameter becoming worse with recurrent fires (Borghetti et al., 2004). One of the methods employed for improving nutrient budgets in these low productive ecosystems is to spread composted sewage sludges as organic amendments. Compost may effectively reactivate the biogeochemical cycles since it brings nutrients to microorganisms, and enhances the water retention into the soil (Borken et al., 2002).
With regard to endogenous factors, the vegetation of these shrublands is dominated by evergreen sclerophyllous species which produce high amounts of leaf secondary metabolites, including phenolic compounds (Gershenzon, 1984). Plants produce these compounds in response to different stress factors, such as interspecific competition (Ferrat et al., 2001), animal overconsumption of leaves (Van Hoven, 1984) and atmospheric pollution (Pasqualini et al., 2003). Plant secondary metabolite content has been suggested to be a major inhibiting factor of the activity of microorganisms (Anderson, 1973; Hättenschwiler and Vitousek, 2000; Isidorov and Jdanova, 2002), particularly in nutrient-poor soils (Northup et al., 1998). Consequently, soil organic matter is easily humified instead of mineralized (Shindo and Kuwastsuka, 1976).
In view of the characteristic features of Mediterranean ecosystems, we assumed that the influence of factors controlling leaf litter colonization by fungi and then decomposition, could be of major importance in the matter cycle in these ecosystems.
The aim of this study is to provide comprehensive data on leaf litter colonization by fungi in a Mediterranean shrubland by determining the effects of (i) an organic amendment by biosolids and (ii) phenolic content on litter colonization by fungi. As fungi associated with decomposed leaves are the main actors of leaf litter breakdown (Toutain, 1981), these eukaryotes offer a reliable way to describe the process (Baldy et al., 1995; Gessner et al., 1999). Consequently, the impact of factors controlling litter breakdown could be studied by monitoring changes in fungal biomass dynamics (Gessner and Chauvet, 1994; Isidorov and Jdanova, 2002) and relating them to factors controlling the process.
Section snippets
Study site and experimental design
The experiment was carried out on 6000 m2 in the plateau of Arbois (Southern Province, France; 5°18′6′′E–43°29′10′′N in WSG-84 Geodetic system), at an altitude of 240 m above sea level under Mediterranean climatic conditions (Fig. 1). The soil was a silty-clayey chalky rendzina, with a high percentage of stones (77%) and low average depth (24 cm). The last fire occurred in June 1995 and the site was colonized by a Mediterranean sclerophyllous vegetation, with a 70% total cover, Quercus coccifera
Effects of compost amendment and season on the fine soil organic fraction
Temperature and rainfall, between January 2002 and April 2003, showed marked seasonal changes (Fig. 1), with maximum rainfall in May, September, November 2002 and in January and April 2003. Maximum temperature occurred in June, July and August 2002.
Soil cationic exchange capacity (Fig. 2D) and moisture content (Fig. 2G) varied according to the season (Table 2), while organic matter (Fig. 2A), total nitrogen (Fig. 2B), C/N ratio (Fig. 2C) and total phosphorus (Fig. 2E) varied significantly with
Discussion
Improving knowledge on litter degradation under Mediterranean climate is necessary for understanding the functioning of Mediterranean ecosystems. Litter constitutes an important source of carbon and energy supply for microbial communities (Pascual et al., 2000). In extensive areas of the Mediterranean regions, the natural vegetation is exposed to the harsh climatic conditions (Pascual et al., 2000). Therefore, humidity and soil nutrients are limiting factors in these ecosystems (Rapp et al.,
Conclusion
In conclusion, these data on ergosterol dynamics associated with decomposed Quercus coccifera leaves in a Mediterranean shrub ecosystem show that leaf litter colonization by fungi is not affected by compost amendment but is closely linked to soil humidity and total phenolic concentrations of leaf litter. These findings suggest that nutrient release from decomposing litter should vary according to climatic conditions and plant species. Therefore, it would be of great interest to study leaf
Acknowledgements
This research was supported by the Conseil Général des Bouches-du-Rhône (France), the ADEME (Agence De l’Environnement et de la Maîtrise de l’Energie), the Conseil Régional Provence-Alpes-Côte-d’Azur and the Rhône-Méditerranée-Corse French Water Agency. We also thank Mr. Michael Paul for revision of English.
References (53)
- et al.
Microbial response to organic amendments in a forest soil
Biores. Technol.
(1996) - et al.
Decomposition of beech leaves (Fagus sylvatica) and spruce needles (Picea abies) in pure and mixed stands of beech and spruce
Soil Biol. Biochem.
(2004) Dynamics of litter mass loss in some Ulex parviflorus Pourr. scrubs in Southeastern France
Pedobiologia
(1997)- et al.
Effect of pollutants on the ergosterol content as indicator of fungal biomass
J. Microbiol. Methods
(2002) - et al.
Fungal biomass and nitrogen in decomposing scots pine needle litter
Soil Biol. Biochem.
(1979) - et al.
Facing drought in a Mediterranean post-fire community: tissue water relations in species with different life traits
Acta Oecol.
(2004) - et al.
Application of compost in spruce forest: effects on soil respiration, basal respiration and microbial biomass
Forest Ecol. Manage.
(2002) - et al.
Aggregate stability changes after organic amendment and mycorrhizal inoculation in the afforestation of a semiarid site with Pinus halepensis
Appl. Soil Ecol.
(2002) - et al.
Intraspecific variability of phenolic concentrations and their responses to elevated CO2 in two mediterranean perennial grasses
Environ. Exp. Bot.
(2002) - et al.
Decomposition of mediterranean leaf litters: a microcosm experiment investigating relationships between decomposition rates and litter quality
Soil Biol. Biochem.
(1996)
Laccase activity of forest litter
Soil Biol. Biochem.
Annual variations of phenoloxidase activities in an evergreen oak litter: influence of certain biotic and abiotic factors
Soil Biol. Biochem.
Shifts in physiological capabilities of the microbiota during the decomposition of leaf litter in a black alder (Alnus glutinosa (Gaertn.) L.) forest
Soil Biol. Biochem.
Enzyme dynamics on decomposing leaf litter of Cistus incanus and Myrtus communis in a Mediterraean ecosystem
Soil Biol. Biochem.
Decomposition of Cistus incanus leaf litter in a Mediterranean maquis ecosystem: mass loss, microbial enzyme activities and nutrient changes
Soil Biol. Biochem.
A colorimetric method for the determination of phenols (and phenol derivatives) in urine
J. Biol. Chem.
Control of leaf litter decomposition rate in a Mediterranean shrubland as indicated by N, P and lignin concentrations
Pedobiologia
Effect of plant cover decline on chemical and microbiological parameters under Mediterranean climate
Soil Biol. Biochem.
The role of polyphenols in terrestrial ecosystem nutrient cycling
Tree
A new tannase substrate for spectrophotometric assay
J. Microbiol. Methods
Volatile organic compounds from leaves litter
Chemosphere
Decomposition of dominant plant species litter in a semi-arid grassland
Appl. Soil Ecol.
Soil microbial activity as a biomarker of degradation and remediation processes
Soil Biol. Biochem.
Phenolic compounds content in Pinus halepensis Mill. needles: a bioindicator of air pollution
Chemosphere
Biomass, nutrient content, litterfall and nutrient return to the soil in Mediterranean oak forests
For. Ecol. Manage.
Litter decomposition and nutrient distribution in humus profiles in some Mediterranean forests in southern Tuscany
Forest Ecol. Manage.
Cited by (33)
Secondary metabolites and nutrients explain fungal community composition in aspen wood
2022, Fungal EcologyCitation Excerpt :The importance of wood and bark chemistry for fungal communities in dead wood is paralleled by the importance of plant chemistry for litter communities. Phenolics, the group to which all secondary metabolites measured in our study belong, influence decomposition and structure colonization by microorganisms specialized on holocellulose in litter (Chomel et al., 2014, 2016; Ormeño et al., 2006). These fungi are analogous to the wood saprotrophs specialized in lignin- and cellulose-decomposition, which we found to be affected by wood and bark chemistry especially in decomposing logs.
Humipedon dynamics in lowland Amazonian forests: are there Amphi humus forms even in tropical rain forests?
2022, GeodermaCitation Excerpt :Notwithstanding that, the most plausible explanation for fungial presence in clayey-CK is the enhancement of humidity in the plots. This mechanism being demonstrated by Jacobson et al., (2015) were the manipulation of humidity in litter was highly positively correlated with saprophytic fungial respiration (CO2), meaning that higher moisture in humus horizons may favor fungial colonization (Ormeño et al., 2006), suggesting that post-logging managements can differ in nutrient-use efficiency. We found that the current Ai (interface) as described in tropical environments, in many cases may correspond to the biomesostructured A of the humus forms classification.
Increasing cuticular wax concentrations in a drier climate promote litter flammability
2020, Forest Ecology and ManagementCitation Excerpt :This can explain why high ignitability (found under aggravated drought where leaf area was smaller) was associated to samples that burned longer (Fig. 4). The high epicuticular alkane concentration in leaf litter under aggravated drought was probably due to the combination of both, limited microbial activity under limited water conditions which slows down the litter decomposing process (Ormeño et al., 2006; Santonja et al., 2015) and plant history, although none of these points were checked in this study. When litter fall occurs, some green leaf traits must be reflected in litter at least during the first stages of decomposition.
Coniferous litter extracts inhibit the litter decomposition of Catalpa fargesii Bur. and Eucommia ulmoides Oliver
2018, Acta OecologicaCitation Excerpt :PSMs encumber litter decomposition for their recalcitrance and toxicity to decomposers (Chomel et al., 2016). For example, endophytic alkaloids and terpenes retard the decomposition of litter by depressing the activities of microbes and detritivores (Chomel et al., 2016; Iqbal et al., 2012), and phenolic compounds exhibit obvious antifungal activities, hindering growth, reproduction, and colonization (Mierziak et al., 2014; Ormeno et al., 2006). Similarly, many exogenous PSMs also dramatically affect soil properties, such as microbial population, activity and community; soil enzymatic activities; and nutrient status, which drive the decomposition of a type of litter under a given temperature and moisture conditions (Adamczyk et al., 2013; Asensio et al., 2012; Joanisse et al., 2007; Zhou et al., 2010).
Relationships between the litter colonization by saprotrophic and arbuscular mycorrhizal fungi with depth in a tropical forest
2012, Fungal BiologyCitation Excerpt :The results indicate that (1) litter colonization by saprotrophic fungi is unaffected differentially by litter (Santana et al. 2005) but their colonization rate is low (up to 30 %) compared with other studies in tropical zones (Pabón 2000; Aristizábal et al. 2004) and (2), that some aspect of the litter – such as chemical composition – affects the Syzygium sp. litter colonization by AMF while simultaneously affecting the presence of vesicles (Aerts et al. 2003; Meier & Bowman 2008). Some types of litter have toxic or inhibitory effects on seedlings (Hossain et al. 2002; Cavieres et al. 2007; Hofland-Zijlstra & Berendse 2010) and meso- and micro-organisms (Rose et al. 1983; Ormeno et al. 2006). Piotrowski et al. (2008) report the inhibitory effect of some litter extracts with phenolic compounds on AMF growth and root colonization.