Mark Maraun

Adding to 'the enigma of soil animal diversity': fungal feeders and saprophagous soil invertebrates prefer similar food substrates

Fungal feeding decomposer animals in soil appear to prefer dark pigmented microfungi (often termed Dematiacea) when given the choice. Both fruiting species (e.g. Cladosporium, Alternaria, Ulocladium) and species with sterile dark mycelia are preferred to hyaline species. In laboratory feeding choice experiments other fungi than dark pigmented forms were less preferred (e.g. Trichoderma, Fusarium, and Zygomycetes like Mucor and Mortierella) or rejected even when there was no other choice (e.g. Penicillium, Aspergillus). Interestingly, the soil mesofauna seems to be more selective than the soil macrofauna. These findings are in contrast to the assumption that decomposer animals and soil fungi co-evolved in a way similar to plants and pollinating animals above the ground. The lack of co-evolution between decomposer animals and soil fungi is surprising since below-ground systems are much older than above-ground systems, and therefore, there was more time for co-evolutionary processes. Furthermore, the findings contradict the explanation of the high diversity of fungal feeding decomposer animals by partitioning of food resources. In general, fungal feeding decomposer animals appear to be food generalists rather than specialists. Dark pigmented fungi often comprise 30-60% of fungal isolates from soils; virtually all of them appear to be of high food quality. Four reasons may explain the preference of fungal feeding decomposer animals for dark pigmented fungi. (1) Dark pigmented fungi contain more carbon or nutrients than other fungi. This, however, is unlikely because melanins, the characteristic components of dark pigmented fungi, are recalcitrant compounds, which are hard to digest. (2) Dark pigmented fungi may produce more efficient exo-enzymes than other fungi thereby effectively digesting organic compounds, which may serve as food for the decomposer animals. In this case, the attempt of decomposer animals to feed on dark pigmented fungi only reflects that the animals seek to exploit the superior enzymatic capabilities of dark pigmented fungi (‘external rumen hypothesis’). (3) Dark pigmented fungi may be used as indicators of organic material, which is at a specific stage of decomposition, and therefore, contains nutrients in high concentrations. (4) Dark pigmented fungi may be preferred because they are less toxic than other fungi, or decomposer animals avoid chitinolytic fungi like Trichoderma, Penicillium, Paecilomyces and Mortierella because the animals are in danger of being digested by these fungi. Each of the four hypotheses is little supported by experimental proof and this review, therefore, calls for a more detailed experimental analysis of decomposer animal-soil fungal relationships.

Divergent composition but similar function of soil food webs of individual plants: plant species and community effects

Soils are extremely rich in biodiversity, and soil organisms play pivotal roles in supporting terrestrial life, but the role that individual plants and plant communities play in influencing the diversity and functioning of soil food webs remains highly debated. Plants, as primary producers and providers of resources to the soil food web, are of vital importance for the composition, structure, and functioning of soil communities. However, whether natural soil food webs that are completely open to immigration and emigration differ underneath individual plants remains unknown. In a biodiversity restoration experiment we first compared the soil nematode communities of 228 individual plants belonging to eight herbaceous species. We included grass, leguminous, and non-leguminous species. Each individual plant grew intermingled with other species, but all plant species had a different nematode community. Moreover, nematode communities were more similar when plant individuals were growing in the same as compared to different plant communities, and these effects were most apparent for the groups of bacterivorous, carnivorous, and omnivorous nematodes. Subsequently, we analyzed the composition, structure, and functioning of the complete soil food webs of 58 individual plants, belonging to two of the plant species, Lotus corniculatus (Fabaceae) and Plantago lanceolata (Plantaginaceae). We isolated and identified more than 150 taxa/groups of soil organisms. The soil community composition and structure of the entire food webs were influenced both by the species identity of the plant individual and the surrounding plant community. Unexpectedly, plant identity had the strongest effects on decomposing soil organisms, widely believed to be generalist feeders. In contrast, quantitative food web modeling showed that the composition of the plant community influenced nitrogen mineralization under individual plants, but that plant species identity did not affect nitrogen or carbon mineralization or food web stability. Hence, the composition and structure of entire soil food webs vary at the scale of individual plants and are strongly influenced by the species identity of the plant. However, the ecosystem functions these food webs provide are determined by the identity of the entire plant community.

Plant diversity surpasses plant functional groups and plant productivity as driver of soil biota in the long term.

Background One of the most significant consequences of contemporary global change is the rapid decline of biodiversity in many ecosystems. Knowledge of the consequences of biodiversity loss in terrestrial ecosystems is largely restricted to single ecosystem functions. Impacts of key plant functional groups on soil biota are considered to be more important than those of plant diversity; however, current knowledge mainly relies on short-term experiments. Methodology/Principal Findings We studied changes in the impacts of plant diversity and presence of key functional groups on soil biota by investigating the performance of soil microorganisms and soil fauna two, four and six years after the establishment of model grasslands. The results indicate that temporal changes of plant community effects depend on the trophic affiliation of soil animals: plant diversity effects on decomposers only occurred after six years, changed little in herbivores, but occurred in predators after two years. The results suggest that plant diversity, in terms of species and functional group richness, is the most important plant community property affecting soil biota, exceeding the relevance of plant above- and belowground productivity and the presence of key plant functional groups, i.e. grasses and legumes, with the relevance of the latter decreasing in time. Conclusions/Significance Plant diversity effects on biota are not only due to the presence of key plant functional groups or plant productivity highlighting the importance of diverse and high-quality plant derived resources, and supporting the validity of the singular hypothesis for soil biota. Our results demonstrate that in the long term plant diversity essentially drives the performance of soil biota questioning the paradigm that belowground communities are not affected by plant diversity and reinforcing the importance of biodiversity for ecosystem functioning.

High genetic divergences indicate ancient separation of parthenogenetic lineages of the oribatid mite Platynothrus peltifer (Acari, Oribatida)

Theories on the evolution and maintenance of sex are challenged by the existence of ancient parthenogenetic lineages such as bdelloid rotifers and darwinulid ostracods. It has been proposed that several parthenogenetic and speciose taxa of oribatid mites (Acari) also have an ancient origin. We used nucleotide sequences of the mitochondrial gene cytochrome oxidase I to estimate the age of the parthenogenetic oribatid mite species Platynothrus peltifer. Sixty‐five specimens from 16 sites in North America, Europe and Asia were analysed. Seven major clades were identified. Within‐clade genetic distances were below 2 % similar to the total intraspecific genetic diversity of most organisms. However, distances between clades averaged 56 % with a maximum of 125 %. We conclude that P. peltifer, as it is currently conceived, has existed for perhaps 100 million years, has an extant distribution that results from continental drift rather than dispersal and was subject to several cryptic speciations.

Reevolution of sexuality breaks Dollo's law.

The dominance of sexual reproduction is still an unresolved enigma in evolutionary biology. Strong advantages of sex have to exist, because only a few parthenogenetic taxa persist over evolutionary timescales. Oribatid mites (Acari) include outstanding exceptions to the rule that parthenogenetically reproducing taxa are of recent origin and doomed to extinction. In addition to the existence of large parthenogenetic clusters in oribatid mites, phylogenetic analyses of this study and model-based reconstruction of ancestral states of reproduction imply that Crotoniidae have reevolved sexuality from parthenogenetic ancestors within one of those clusters. This reversal in reproductive mode is unique in the animal kingdom and violates Dollos law that complex ancestral states can never be reacquired. The reevolution of sexuality requires that ancestral genes for male production are maintained over evolutionary time. This maintenance likely is true for oribatid mites because spanandric males exist in various species, although mechanisms that enable the storage of genetically ancestral traits are unclear. Our findings present oribatid mites as a unique model system to explore the evolutionary significance of parthenogenetic and sexual reproduction.

Oribatid mite (Acari, Oribatida) feeding on ectomycorrhizal fungi.

The coexistence of a large number of soil animals without extensive niche differentiation is one of the great riddles in soil biology. The main aim of this study was to explore the importance of partitioning of food resources for the high diversity of micro-arthropods in soil. In addition, we investigated if ectomycorrhizal fungi are preferentially consumed compared to saprotrophic fungi. Until today, ectomycorrhizal fungi have never been tested as potential food resource for oribatid mites. We offered six ectomycorrhizal fungi [Amanita muscaria (L.) Hook., Boletus badius (Fr.) Fr., Cenococcum geophilum Fr., Laccaria laccata (Scop.) Fr., Paxillus involutus (Batsch) Fr. and Piloderma croceum J. Erikss. & Hjortstam], one ericoid mycorrhizal fungus [Hymenoscyphus ericae (D.J. Read) Korf & Kernan] and three saprotrophic fungi [Agrocybe gibberosa (Fr.) Fayod, Alternaria alternata (Fr.) Keissl. and Mortierella ramanniana (A. Müller) Linnem.] simultaneously to each of the mainly mycophagous oribatid mite species Carabodes femoralis (Nicolet), Nothrus silvestris Nicolet and Oribatula tibialis Nicolet. The ericoid mycorrhizal fungus H. ericae and the ectomycorrhizal fungus B. badius were preferentially consumed by each oribatid mite species. However, feeding preferences differed significantly between the three species, with O. tibialis being most selective. This study for the first time documented that oribatid mites feed on certain ectomycorrhizal fungi.

Molecular phylogeny of oribatid mites (Oribatida, Acari): evidence for multiple radiations of parthenogenetic lineages

Nucleotide sequences of the D3 expansion segment and its flanking regions of the 28S rDNA gene were used to evaluate phylogenetic relationships among representative sexual and asexual oribatid mites (Oribatida, Acariformes). The aim of this study was to investigate the hypothesis that oribatid mites consist of species rich clusters of asexual species that may have radiated while being parthenogenetic. Furthermore, the systematic position of the astigmate mites (Astigmata, Acariformes) which have been hypothesised to represent a paedomorphic lineage within the oribatid mites, is investigated. This is the first phylogenetic tree for oribatid mites s.1. (incl. Astigmata) based on nucleotide sequences. Intraspecific genetic variation in the D3 region was very low, confirming the hypothesis that this region is a good species marker. Results from neighbour joining (NJ) and maximum parsimony (MP) algorithms indicate that several species rich parthenogenetic groups like Camisiidae, Nanhermanniidae and Malaconothridae are monophyletic, consistent with the hypothesis that some oribatid mite groups diversified despite being parthenogenetic. The MP and maximum likelihood (ML) method indicated that the D3 region is a good tool for elucidating the relationship of oribatid mite species on a small scale (genera, families) but is not reliable for large scale taxonomy because branches from the NJ algorithm collapsed in the MP and ML tree. In all trees calculated by different algorithms the Astigmata clustered within the oribatid mites, as proposed earlier.

Tropical Andean Forests Are Highly Susceptible to Nutrient Inputs—Rapid Effects of Experimental N and P Addition to an Ecuadorian Montane Forest

Tropical regions are facing increasing atmospheric inputs of nutrients, which will have unknown consequences for the structure and functioning of these systems. Here, we show that Neotropical montane rainforests respond rapidly to moderate additions of N (50 kg ha−1 yr−1) and P (10 kg ha−1 yr−1). Monitoring of nutrient fluxes demonstrated that the majority of added nutrients remained in the system, in either soil or vegetation. N and P additions led to not only an increase in foliar N and P concentrations, but also altered soil microbial biomass, standing fine root biomass, stem growth, and litterfall. The different effects suggest that trees are primarily limited by P, whereas some processes—notably aboveground productivity—are limited by both N and P. Highly variable and partly contrasting responses of different tree species suggest marked changes in species composition and diversity of these forests by nutrient inputs in the long term. The unexpectedly fast response of the ecosystem to moderate nutrient additions suggests high vulnerability of tropical montane forests to the expected increase in nutrient inputs.

Oribatid Mites as Potential Vectors for Soil Microfungi: Study of Mite-Associated Fungal Species

The ability of soil-living oribatid mites to disperse fungal propagules on their bodies was investigated. Classical plating methods were applied to cultivate these fungi and to study their morphology. Molecular markers were used for further determination. The nuclear ribosomal large subunit and the nuclear ribosomal internal transcribed spacer of DNA extracts of the cultured fungi as well as total DNA extracts of the mites themselves, also containing fungal DNA, were amplified and sequenced. Based on phylogenetic analysis, a total of 31 fungal species from major fungal groups were found to be associated with oribatid mites, indicating that mites do not selectively disperse specific species or species groups. The detected taxa were mainly saprobiontic, cosmopolitan (e.g., Alternaria tenuissima), but also parasitic fungi (Beauveria bassiana) for whose dispersal oribatid mites might play an important role. In contrast, no mycorrhizal fungi were detected in association with oribatid mites, indicating that their propagules are dispersed in a different way. In addition, fungi that are known to be a preferred food for oribatid mites such as the Dematiacea were not detected in high numbers. Results of this study point to the potential of oribatid mites to disperse fungal taxa in soil and indicate that co-evolutionary patterns between oribatid mites and their associated fungi might be rare or even missing in most cases, since we only detected ubiquitous taxa attached to the mites.

Changes in microbial biomass, respiration and nutrient status of beech (Fagus sylvatica) leaf litter processed by millipedes (Glomeris marginata)

The effect of processing of beech leaf litter (Fagus sylvatica L.) of different ages by the diplopodGlomeris marginata (Villers) on status and turnover of microorganisms was investigated in the laboratory. Microbial biomass, basal respiration and metabolic quotient of litter-material from three different beechwood sites of a basalt hill forming a gradient from basalt (upper part of the hill) to limestone (lower part of the hill) were determined each season (February, May, August and November). The same microbial parameters were also measured after these litter materials had been processed byG. marginata (faecal pellets of an average age of 4 days). Short-term changes in microbial biomass and respiration in leaf material and faecal pellets from February and August were investigated after 1, 2, 5, 10, 20 and 40 days of incubation. The ergosterol content of August samples was determined. Processing of beech leaf litter byG. marginata increased microbial biomass in February and May but reduced microbial biomass in August and November. It was concluded that processing of litter materials in February and May increased accessibility of carbon resources to microorganisms by fragmentation. In contrast, in litter materials from August and November carbon resources were depleted and fragmentation by diplopods did not increase availability of carbon resources. Addition of carbon (glucose) and nutrients (nitrogen and phosphorus) to litter and faecal pellets indicated that processing of beech litter reduced nutrient deficiency of the microflora. Ergosterol content in faecal pellets was reduced strongly after beech leaf litter processing byG. marginata, indicating a decrease in fungal biomass. Presumably, in faecal pellets bacteria flourished at the expense of fungi.