Sex pheromone in Tetrodontophora bielanesis (Waga, 1842) (Collembola: Onychiuridae): Indirect reproduction mediated by cuticular compounds

An olfactory sexual recognition signal was investigated in Tetrodontophora bielanensis (Collembola: Onychiuridae). A preliminary olfactometry experiment showed an unequivocal attraction of males by the odor of females. This led us to conduct male attraction tests using polar and apolar fractions of female cuticular extract. The polar fraction of the extract was shown to contain the component that plays an active role in sexual attraction in this Collembola species. The results of the present study are the first to show a direct relationship between an olfactory signal and sexual attraction in Collembola.     

The Collembola community of pure and mixed stands of beech (Fagus sylvatica) and spruce (Picea abies) of different age

The idea of establishing mixed forests that are better adapted to site conditions than spruce monocultures has attracted increasing attention of forest owners and governmental institutions over the last decades. Currently, beech is being replanted and an increasing proportion of German forests are mixed stands. Focusing on the reaction of the soil fauna to forest conversion, this study investigates the response of the Collembola community to replacement of beech by spruce or by mixed stands of beech and spruce. Stands of different age were investigated in a factorial design with the factors stand type (beech, spruce and mixed stands) and stand age (30 and 120 years). Collembola communities did not differ strongly between stand types and stand age and were dominated by Folsomia quadrioculata and Mesaphorura species (e.g. Mesaphorura macrochaeta). Moreover, neither total abundance of Collembola nor densities of the fungal feeding euedaphic Onychiurinae and Tullbergiinae significantly responded to stand type and stand age. The density of the epedaphic and partly herbivorous groups Symphypleona/Neelipleona and Entomobryidae in the 120-year-old stands significantly exceeded that in the 30-year-old stands; presumably, this was due to the well developed herb layer in the 120-year-old stands with more open canopies. Canonical correspondence analysis (CCA) of the Collembola community of the L/F horizon also indicated that most of the epigeic species were associated with the 120-year-old stands. Moreover, the diversity of Collembola significantly increased with forest age which likely reflects increased amount and diversity of food resources in the 120-year-old stands. The density of the hygrophilous species Fo. quadrioculata was significantly higher in the spruce than in the beech stands; probably this was due to the higher water content in litter of the spruce stands. Moreover, the results of the CCAs indicated that soil pH is an important structuring force for the Collembola communities. Overall, the results suggest that stand type and forest age impact Collembola communities, presumably via changes in the amount and quality of food resources, such as living plant and herb litter materials. The pronounced changes which occurred with forest age likely were related to the development of more dense and diverse herb layer in mature forests which provides additional food resources in particular for epedaphic species. On the other hand, dominant species/functional groups of Collembola, such as hemiedaphic species, appear to depend predominantly on abiotic factors, most importantly soil pH and soil water content.     

Respiration and growth of a fungus, Mortierella isabellina, in response to grazing by Onychiurus armatus (Collembola)

Colonies of the fungus Mortierella isabellina (Oudem) were grazed by the collembolan Onychiurus armatus (Tullb.) for short periods interrupted by incubation without grazing in laboratory experiments. The grazed fungus had a lower respiration than ungrazed when Collembola were present on the mycelium. Fungal respiration was significantly increased with grazing when Collembola were periodically removed from the mycelium. Metal contamination of the substrate increased fungal respiration, regardless of grazing. Length of fungal mycelium was significantly greater in a natural soil in the presence of Collembola but reduced in a metal-polluted soil. Factors that may determine the impact of grazing on fungi are discussed.     

Abundance of springtails (Collembola) under four agroforestry tree species with contrasting litter quality

The soil- and litter-dwelling Collembola under four agroforestry tree species (Treculia africana, Dactyladenia (Acioa) barteri, Gliricidia sepium and Leucaena leucocephala) were monitored monthly for a period of 12 months and results were compared with those of a secondary forest and a grass plot. Treculia and Dactyladenia produced lower quality litter, leading to lower soil temperature and higher soil moisture under those species, relative to Gliricidia and Leucaena. The agroforestry tree plots contained more soil- and litter-dwelling Collembola than the secondary forest and grass plots. The slowly decomposing litter under Treculia and Dactyladenia supported more litter Collembola than the quickly decomposing litter under Gliricidia and Leucaena. Soil moisture and temperature were, respectively, positively and negatively correlated with populations of soil Collembola. Based on the results of this study, it is suggested that the use of prunings of agroforestry tree species as mulch in agroecosystems would encourage the growth of Collembola populations and enhance their role in decomposition processes. Received: 28 May 1997     

The diet and food preferences of Onychiurus procampatus (Collembola) from upland grassland soils

Specimens of Onychiurus procampatus (Collembola) observed grazing on fungal mycelia were collected from the surface soil of three differently manged upland grasslands. A general trend of an increasing proportion of Collembola with a full gut was found along a gradient of reduced sheep management intensity, which was correlated with increased fungal biomass. In the laboratory, this collembolan showed a consistent order of preference for the mycelium of seven common fungal species isolated from the field sites.     

Collembola effects on plant mass and nitrogen acquisition by ash seedlings (Fraxinus pennsylvanica)

We studied the effects of varied collembolan numbers on three compensatory mechanisms of nutrient uptake: fine root mass, endomycorrhizal development, and physiological uptake capacity. We grew ash (Fraxinus pennsylvanica) with or without the arbuscular mycorrhizal fungus Glomusintraradices, with 0, 10 or 50 initial Collembola (Folsomia candida). After 83 d root and uptake rates, endomycorrhizal development, and plant biomass were determined. Plant mass increased with Collembola number. Collembola interacted with mycorrhizae in their effects on N uptake and leaf N. Collembola in the absence of mycorrhizal roots were associated with lower N uptake and leaf N at 10 than at 0 or 50 initial Collembola. In contrast, Collembola in the presence of mycorrhizal roots were associated with the highest rate of N uptake and leaf N at 10 versus 0 or 50 initial Collembola. Hence as initial Collembola number increased, the relative importance of root system traits that determined N uptake changed from root physiological uptake capacity, presence of mycorrhizal roots, to fine root biomass.     

Fatty acid composition and change in Collembola fed differing diets: identification of trophic biomarkers

To assess the potential of fatty acid (FA) compositions to act as biomarkers in the soil food web, two species of Collembola, Folsomia candida and Proisotoma minuta, were switched to four possible diets: Cladosporium cladosporioides (a common soil fungus), Panagrellus redivivus (a bacteria feeding nematode), Zea mays (maize) and Alnus glutinosa (alder). The change in FA content of the Collembola was observed over the following 39 days. The four diets produced significant shifts in the FA compositions of the Collembola, with P. redivivus causing the most extreme changes; Collembola fed P. redivivus gained complex FA compositions similar to those of the nematode diet. Changes in the relative abundances of some FAs were found to follow negative exponential curves, as the components either accumulated in, or were removed from, the FA pool in the Collembola; abundance half-lives varied between 0.5 and 22.4 days, indicating that Collembolan FA compositions changed readily with the input of new exogenous components. The results demonstrate that Collembolan FA compositions are influenced by diet, and that the abundances of FAs such as i15:0, i17:0 and 18:1(n-7) may be used as biomarkers of nematode consumption by Collembola. In contrast, the C₂₀ polyunsaturated FAs cannot be used as biomarkers for nematode predation as Collembola possess the ability to biosynthesise high abundances of these compounds when not provided by the diet.     

ABSTRACT of the Articles Printed in Journal of the Science of Soil and Manure,Japan

Changes in soil moisture determine the reproductive, respiratory, and metabolic activities of soil microorganisms and hence the rate of microbial nitrogen (N) mineralization. Soil moisture also affects the feeding activity and movement of soil invertebrates. Bacterial and fungal grazing by soil invertebrates such as Collembola and nematodes is known to increase N mineralization by increasing the reproductive, respiratory, and metabolic activities of microorganisms. Therefore, to assess the effect of soil moisture on N mineralization, faunal responses need to be considered. We used microcosms to investigate the effect of soil moisture on N mineralization mediated by a species of Collembola, Folsomia candida Willem. We used four moisture levels corresponding to matric potentials of ?42.5, ?11.8, ?0.8, and ?0.5 kPa and investigated the effects of these on Collembola with respect to feeding activity, growth, and contribution to N mineralization. The microbial biomass and ratio of bacterial to fungal biomass tended to increase with increasing soil moisture. Collembola feeding activity and growth increased with increasing soil moisture conditions. Collembola significantly enhanced N mineralization in soil at water potentials of ?11.8 and ?0.5?kPa. The greatest relative increase in N mineralization attributed to Collembola occurred in the ?11.8?kPa treatment. The change in contribution of the Collembola to N mineralization with soil moisture was most likely induced by changes in Collembola feeding activity and microbial community structure. The growth in body length of the Collembola was significantly greater at higher moisture conditions than at the lowest moisture condition, indicating that increases in both metabolic activity and biomass of the Collembola population contributed to the enhanced N mineralization.     

Long-term fluctuation of the soil fauna (Collembola and Oribatida) at groundwater-near sites in an alder wood

Collembola and oribatid mites were investigated at four sites along a cross section in an alder wood at a lake margin (northern Germany) over a period of 7 years. Monthly samples of the litter and the mineral layer were taken. Additionally, fluctuations of groundwater level, soil moisture, precipitation and soil temperature at 2 cm depth were measured. The alder wood was characterised by a depression between the lake margin and the foot of a hill slope, where waterlogged periods occurred. Groundwater level was the main environmental factor influencing the composition of collembolan and oribatid mite assemblages. Climatic factors, e.g. July temperature and July precipitation were also found to be significant factors, but with a much lower influence. Collembola predominantly showed higher variation in time than in space indicating that more collembolan species migrate within the investigated cross section or react with higher abundance fluctuations on the groundwater level changes, while Oribatida had a higher part of space variation, indicating that migration potential is lower and the environmental gradient is of higher influence on the distribution. Reaction time of soil fauna species on the groundwater fluctuation varies between 1 and 12 months. Retreat of Collembola from the waterlogged situation was between 4 and 6 months in the litter layer and 3 months in the mineral layer. Recolonisation of the waterlogged site lasted approximately 12 months. A positive reaction by precipitation was observed in four collembolan species that was 1 month in the edaphic species and between 9–10 months in the larger litter dwelling species. Only few oribatid mites reacted on the waterlogged situation.     

Relationships between Collembola,soil chemistry and humus types in forest stands (France)

Soil samples were taken under four tree species in various forest sites located in southern France. For each sampled A horizon of the soil profile, pH, organic matter content, C:N ratio and amounts of exchangeable cations (K, Ca, Mg) were measured, and collembolan fauna was extracted using Berlese-Tullgren funnels. A total of 78 species representing 11 families and 47 genera were identified. The relationships between Collembola and soil parameters were determined by co-inertia analysis which corresponds to the simultaneous Correspondence Analysis of the collembolan data table and the Multiple Correspondence Analysis of the environmental data table. The analysis revealed that the distribution of 10 species was related to pH, organic matter content via C and N and to base cations (K, Ca, Mg). Samples, linking these collembolan species and chemical parameters, were clustered according to humus forms. Collembola seem to be linked closer to the physical structure of humus than to its chemical parameters. Their specific contribution to pedogenetic processes as yet remains to be clarified.     

Collembola species composition and diversity effects on ecosystem functioning vary with plant functional group identity

The relationship between decomposer diversity and ecosystem functioning is little understood although soils accommodate a significant proportion of worldwide biodiversity. Collembola are among the most abundant and diverse decomposers and are known to modify plant growth. We examined the effects of Collembola species diversity (one, two and three species belonging to different life history groups) and composition on litter decomposition and the performance of plant communities (above- and belowground productivity) of different functional groups (grasses, forbs and legumes). Collembola densities did not increase with diversity indicating niche overlap. Generally, Collembola species composition was a better predictor for ecosystem functioning than Collembola species number with the impacts of Collembola diversity and composition on ecosystem functioning strongly depending on plant functional group identity. Non-linear effects of Collembola diversity on litter decomposition and plant productivity suggest pronounced and context dependent species interactions and feeding habits. Net surface litter decomposition was decreased by Collembola, whereas root litter decomposition was at maximum in the highest Collembola diversity treatment. Forbs benefitted most from the presence of three Collembola species. Similarly, Collembola diversity influenced root depth distribution in a plant functional group specific way: while grass root biomass decreased with increasing Collembola diversity in the upper and lower soil layer, legume root biomass increased particularly in the lower soil layer. Idiosyncratic and context dependent effects of Collembola diversity and composition even in rather simple assemblages of one to three species suggest that changes in Collembola diversity may have unpredictable consequences for ecosystem functioning. The finding that changes in Collembola performance did not directly translate to alterations in ecosystem functioning indicates that response traits do not necessarily conform to effect traits. Distinct plant functional group specific impacts of Collembola diversity on root depth distribution are likely to modify plant competition in complex plant communities and add a novel mechanism how decomposers may affect plant community assembly.     

Flowering phenology of a herbaceous species (Poa annua) is regulated by soil Collembola

The role of soil organisms as possible driver of flowering has never been investigated. We hypothesized that Collembola (microarthropods) will change plant allocation to reproductive modes by changing soil nutrient availability. Individual seedlings of Poa annua were planted in microcosms, in the presence or absence of Collembola. Collembola affected biotic (fungal biomass) and abiotic ($\text{N}-{{\text{NO}}_3}^{-}$, P₂O₅) soil properties and some morphological (number of leaves, root biomass) and chemical (C:N, K, Mg, N) traits of P. annua. As a result, flowering of P. annua was promoted by the presence of Collembola. This provides experimental evidence that soil microarthropods can affect the reproduction strategy and phenology of a plant.     

Olfactory cues associated with fungal grazing intensity and secondary metabolite pathway modulate Collembola foraging behaviour

Fungal secondary compounds play an important role for springtail food choice and fitness. Little is known, however, on the role of olfactory cues for Collembola foraging behaviour and whether Collembola can olfactorily perceive volatiles associated with fungal secondary metabolite pathways. We investigated the ability of three species of Collembola (Folsomia candida, Heteromurus nitidus and Supraphorura furcifera) to use olfactory cues for discriminating between fungi of different phylogenetic affiliation (Aspergillus nidulans, Cladosporium cladosporioides, Ascomycota; Laccaria bicolor, Basidiomycota) and toxicity using fungal strains of A. nidulans with reduced secondary metabolite production. Furthermore, we studied if olfactory cues from hyphae injured by grazing affect the foraging behaviour of Collembola. We hypothesized that (i) Collembola are able to olfactorily perceive and respond to fungal species/strains with different secondary metabolite pathways and that (ii) Collembola are able to sense fungal mycelia injured by grazing. Each of the Collembola species studied preferentially oriented their foraging towards fungal strains of A. nidulans with suppressed secondary metabolites, and in particular towards the mutant where the global regulator for secondary metabolites (ΔlaeA) has been silenced. Two of the three Collembola species (H. nitidus and S. furcifera) sensed olfactory cues of previously grazed fungi and moved towards ungrazed fungi, however, the response of S. furcifera was restricted to fungi extensively exposed to grazing (5 days) suggesting that the response varies between Collembola species.Overall, the results support the first and second hypothesis indicating that Collembola (1) are able to olfactorily differentiate fungi of different toxicity and move towards more palatable fungi, and (2) showed a lesser preference for fungi previously exposed to grazing.     

Microhabitats of Collembola (Insecta: Entognatha) in beech and spruce forests and their influence on biodiversity

Collembolan communities were studied in 41 microhabitats in beech and spruce forests of south ( ofín and umava) and central (Jevany) Bohemia. The communities of Collembola were analysed using TWINSPAN and CANOCO programs. The aim of this study was to establish differences between patch (microhatitat) communities and the main forest community in spruce and beech forests, the differences between both types of forests and among different regions of Bohemia. Further questions were: is there a difference in microhabitat communities during secondary forest succession? do some species live exclusively in one or few microhabitats? and does microhabitat diversity influence the biodiversity in forest soils? Material comprising  25 590 specimens of Collembola belonging to 142 species was analysed. Highly significant differences were determined between microhabitat communities in beech and spruce forests, as well as among forests in different regions of Bohemia. Significant differences were also found among microhabitats in forests of different ages. Also, some microhabitat communities of Collembola, e.g. moss on boulders, were significantly different from their main forest community. Certain collembolan species existed exclusively in one or two microhabitats. Patches therefore influenced substantially biodiversity in these forest soils.     

Karyotype differentiation and chromosomal variability in springtails (Collembola,Insecta)

Summary Karyological studies in the mitotic complements of arthropleonic springtails (Collembola) were carried out, applying chromosome-banding techniques (Giemsa C banding) for the first time. These techniques provide important indications on karyological variability and the genetic heterogeneity of local populations. Karyotype architecture may be of taxonomic significance at the species level. Chromosomal studies in various populations of the group Onychiurus armatus (Tullb.) high-light the importance of future karyological studies, especially in taxonomically complicated groups.New chromsome counts for 29 species of Collembola are presented. In 32 species karyotype morphology was analysed in detail. Acrocentric chromosomes were found to be an essential feature of karyotype evolution in Collembola. Generally, primitive taxa show a higher proportion of acrocentrics than more evolved species. For both Poduromorpha and Entomobryomorpha, ancestral karyotypes with only acrocentric chromosomes are postulated. The most primitive karyotype found in the Poduromorpha (Ceratophysella bengtssoni, n=7) consists of one metacentric and six acrocentric chromosomes, probably derived from a hypothetical, purely acrocentric complement (n=8) by a single centric fusion. In the Entomobryomorpha, acrocentric karyotypes (n=7) are still found in Isotoma cinerea and in Proisotoma. Chromosome numbers exceeding n=7 [Onychiuridae, n=7–9; Poduridae, n=(9-)11] are supposed to be due to secondary increases.Dedicated to the late Prof. Dr. W. Kühnelt     

Influence of holm oak leaf decomposition stage on the biology ofOnychiurus sinensis Stach (Collembola: Onychiuridae)

The trophic attractiveness of different stages of development and decomposition of holm oak leaves and the influence of their nutritional quality on the biology of the springtail Onychiurus sinensis were studied. Collembola fed preferentially on leaves at an advanced stage of decomposition. Biological parameters such as moulting, fecundity, survival rate and linear growth, indicated the influence of the quality of food upon the biology of these microarthropods. Whole parameters were maximized when the leaves were more decayed and when the nitrogen content was the highest.     

Low importance for a fungal based food web in arable soils under mineral and organic fertilization indicated by Collembola grazers

We investigated the Collembola community at an arable field where mineral and organic fertilizers have been applied at low and high rates for 27 years. As food resources for Collembola, the soil microbial community was analyzed using phospholipid fatty acids (PLFAs). A special focus was put on AM fungi, which were estimated by the marker 16:1ω5 in PLFA (viable hyphae) and neutral lipid fatty acid (NLFA – storage fat in spores) fractions. Additionally, whole cellular lipids in crop plant tissues and manure were assessed. Greater Collembola species richness occurred in plots where mineral fertilizer was added. In contrast, soil microbial biomass including AM fungal hyphae increased with addition of organic fertilizer, while the amount of AM fungal spores and biomass of saprotrophic fungi were not affected by fertilizer type. The lipid pattern in wheat roots was altered by fertilizer type, application rate and their interaction, indicating different rhizosphere communities. In sum, the availability and composition of food resources for Collembola changed considerably due to farm management practice. The major diet of three dominant Collembola species, Isotoma viridis, Willemia anophthalma and Polyacanthella schäffer was determined by lipid profiling. Multivariate analysis demonstrated species specific lipid patterns, suggesting greater importance of species than management practice on the diet choice. Nevertheless, feeding strategy was affected by fertilizer type and availability of resources, as trophic biomarker fatty acids indicated feeding on wheat roots (and to some extent saprotrophic fungi) with mineral and a shift to soil organic matter (litter, detritus) with organic fertilization. Although AM fungi dominated the soil fungal community, the AMF marker 16:1ω5 was not detected in Collembola lipids, indicating that these were not consumed. The very low amount of saprotrophic fungi in the soil and the fact that Collembola as major fungal grazers did not feed on AM fungi indicates that the fungal energy channel in the investigated arable field is of little importance to the faunal food web.     

Limits to the bioindication potential of Collembola in environmental impact analysis: a case study of forest soil-liming and fertilization

We tested the suitability of the collembolan community as a bioindicator for assessing the effects of forest soil-liming and fertilization on the belowground decomposer community. Our investigation was based on a 5-year survey that took place in a German oak-hornbeam and spruce forest in which amelioration measures took place in 1988, 1994 and 1995, with chemical parameters and Collembola being sampled between 1993 and 1997. To address these questions, we applied new methods which have not yet, to our knowledge, been used in biomonitoring studies on forest soils. We used a time-lag analysis for the detection of directional change and a regression-tree induction to show the relationship between Collembola and soil factors. Soil parameters changed considerably after the onset of liming and fertilization. However, no change was detected in community composition over time, nor was there a relationship between Collembola and soil parameters that would make possible the development of a model with at least a moderate predictive success. Taking into account the effort invested in this study (5-year sampling period, identification of 35,000 Collembola, 99 species, 1,170 chemical analyses), we question the suitability of collembolan communities as a bioindicator for forest disturbance.     

Collembola grazing on arbuscular mycorrhiza fungi modulates nutrient allocation in plants

Arbuscular mycorrhiza (AM) mycelia networks are important for nutrient allocation in many plants, but fungivorous soil invertebrates such as Collembola can modulate the symbiosis by grazing on the extra-radical mycelium (ERM). This study employs a dual biomarker approach with stable isotopes and fatty acids to disentangle trophic interactions of Collembola in a plant-fungal soil system with maize (Zea mays) and the AM fungus Glomus mosseae. To separate ERM and root mediated effects, root (RC) and hyphal compartments (HC) were used, and the latter was spiked with labeled ¹⁵N substrate. The euedaphic Collembola species Protaphorura fimata was introduced as the fungal and root grazer. Generally, the presence of Collembola in RC fostered biomass and phosphorous uptake in roots colonized with AM. Nitrogen transport from HC to RC was not altered, indicating that Collembola did not disrupt the ERM network via grazing. Collembola–fungus interactions fostered AM hyphal proliferation in HC, whereas in RC it induced a change from fungal senescence with build-up of storage reserves, to an active foraging phase. A distinct diet switch by Collembola between HC and RC indicated different ERM palatability meditated by the presence or absence of the host plant. Overall, Collembola grazing increased ERM nutrient sequestration, particularly phosphorus, and in turn plant performance. Collembola modified fungal phenology, favoring fungal colonization over reproductive phases. These trophic interactions were strongly determined by fungal life stage, with the establishment of a functional mycorrhiza as a crucial factor.