Population performance of collembolans feeding on soil fungi from different ecological niches

The potential reproductive value of arbuscular mycorrhizal fungi (Glomus intraradices and Glomus invermaium), root pathogenic fungi (Rhizoctonia solani and Fusarium culmorum) and saprotrophic fungi (Penicillium hordei and Trichoderma harzianum) were examined for the collembolans Folsomia candida Willem and Folsomia fimetaria L. Dried baker's yeast (Saccharomyces cerevisiae) was used as a reference standard food in laboratory cultures. Collembolan performance was determined as final size, fecundity and population growth rate after when fed the fungal food sources for 31 days. The mycorrhizal fungi gave the least growth and fecundity compared with the other fungi, but G. intraradices gave good fecundity for F. candida. In terms of growth, Baker's yeast was a high-quality food for both adults and juveniles of both species, but it was a poorer food in terms of fecundity of F. candida. Preference of the fungi in all possible pairwise combinations showed that although F. fimetaria did not perform well on Glomus spp. and F. candida did not grow well on Glomus spp. their preference for these fungi did not reflect this. The highest fecundity was seen with the root pathogen F. culmorum. Different quality indicators such as the C:N ratio of the fungal food sources as well as other biological parameters are discussed in relation to their reproductive value and Collembola preferential feeding.     

Attraction to prey and prey-associated odours by the predatory mite Hypoaspis aculeifer in a soil experimental system

In terms of food searching and trophic interactions among soil organisms volatile signalling plays a crucial role. Still, volatile-based foraging decisions are poorly understood, especially as the dispersal and perception of cues is more restricted within the soil pore space than in simple laboratory approaches where volatiles disperse freely in the air. Focusing on the tritrophic interaction between the soil fungus Trichoderma viride, the fungivorous collembolan Folsomia candida and the predatory mite Hypoaspis aculeifer, we tested the effect of prey and prey-associated volatile signals on the food choice decision of the predatory mite in a laboratory experiment under soil conditions as well as the possible occurrence and relevance of grazing-induced indirect defence signals. The mites showed a clear preference for ungrazed and grazed fungal mycelium. However, we found no evidence of induced indirect defence as ungrazed mycelium was preferred to grazed fungus.     

Effects of sewage sludge and copper enrichment on both soil mesofauna community and decomposition of oak leaves (Quercus suber) in a mesocosm

A laboratory mesocosm experiment was performed to study the effects of copper-enriched sewage sludge application on a mesofauna community. For 12 weeks, characteristics and changes in this defined and artificial mesofauna community structure were monitored as well as the dynamics of leaf litter decomposition. The mesofauna community comprised six species of Collembola (Folsomia fimetaria, Isotomurus prasinus, Lepidocyrtus cyaneus, Mesaphorura macrochaeta, Parisotoma notabilis, Protaphorura armata), two species of acari Oribatida (Achipteria coleoptrata, Adoristes sp.), one species of acari Gamasida (Hypoaspis aculeifer) and one species of enchytraeid (Enchytraeus crypticus). Three treatments included the addition of 22 g dry weight (DW) sludge spiked with 0, 200 and 1,000 mg Cu kg^?1 DW sludge in each mesocosm, and one treatment had 66 g DW sludge spiked with 1,000 mg Cu kg^?1 DW sludge added in each mesocosm. Copper, complexed with sludge due to a favourable pH, had no effect on community and litter parameters when added to low amount of sludge. In contrast, tripling the sludge dose in addition to a high dose of Cu changed in time the sludge and leaf chemical composition as well as mesofauna community structure. Responses of the mesofauna to this treatment differed between species. The abundance of species such as I. prasinus, L. cyaneus, M. macrochaeta and P. notabilis decreased, whereas the abundance of H. aculeifer increased and became dominant.     

Dietary switching of collembola in grassland soil food webs

Soil food webs are characterised by complex direct and indirect effects among the organisms. Consumption of microorganisms by soil animals is considered as an important factor that contributes to the stability of communities, though cascading effects within the food web can be difficult to detect. In a greenhouse experiment, an addition of a high number the fungal feeding collembola Folsomia quadrioculata was applied to grassland soil food webs in monocultures of three plant species: Plantago lanceolata (forb), Lotus corniculatus (legume) and Holcus lanatus (grass). The abundance of microorganisms, determined as the abundances of phospholipid fatty acids (PLFAs) and the abundances of resident invertebrates, nematodes and collembolans, did not change due to the addition of F. quadrioculata. Trophic positions of collembolans were determined by analyses of natural abundances of ¹⁵N stable isotopes. The use of food resources by microorganisms and collembolans was determined by ¹³C analysis of microbial PLFAs and solid samples of collembolans. δ¹³C values of the resident collembola Folsomia fimetaria were lower in the presence of F. quadrioculata than in the control food webs indicating a use of more depleted ¹³C food resources by F. fimetaria. The δ¹⁵N values of F. fimetaria did not change at the addition of F. quadrioculata thus no change of trophic levels was detected. The switch of F. fimetaria to a different food resource could be due to indirect interactions in the food web as the two collembolan species were positioned on different trophic positions, according to different δ¹⁵N values.     

Application of bioassays with <Emphasis Type="Italic">Enchytraeus crypticus</Emphasis> and <Emphasis Type="Italic">Folsomia candida</Emphasis> to evaluate the toxicity of a metal-contaminated soil,before and after remediation

Purpose  

A contaminated soil was amended to reduce bioavailability of metals (As, Cd, Cu, Pb, and Zn) and to modify its potential environmental impacts. Reproduction toxicity tests using two different soil invertebrates, Enchytraeus crypticus and Folsomia candida, were used to evaluate efficiency of soil amendments to reduce metal availability.     

What causes variability in the Folsomia candida reproduction test?

Large variability is often observed in results of the Folsomia candida reproduction test [ISO 11267, Soil quality—inhibition of reproduction of Collembola (Folsomia candida) by soil pollutants. Inter. Stand. Org. Ed. Genève. (1998) 1–16] and can be detrimental to the test sensitivity. So, we investigated the effects of certain parameters (small differences of ambient temperature and age of the animals) on the variability of reproduction of F. candida. We show that a 1 °C difference has no perceptible effect but that a 1 day difference in age has. Studying the reproduction of isolated individuals shows that a strong apparent interindividual variability exists. Lastly, we compared the variability of reproduction in two tests differing from one another in duration; variability was clearly decreased by lengthening the test.     

Sensitivity to cadmium of the standard test species Folsomia candida compared to two other species, Onychiurus yodai and Sinella umesaoi (Collembola)

Knowing whether test species used for single-species toxicity tests are representative of other species provides valuable information because contaminant effects are often extrapolated to the community level based on these tests. To evaluate how representative the sensitivity of the standard test collembolan species Folsomia candida is for Collembola, we devised toxicity tests using the collembolan species Onychiurus yodai and Sinella umesaoi, which exhibit life-forms different from F. candida. Sensitivity to cadmium (Cd) was compared between F. candida and the novel test species. The 50% effective concentrations for reproduction were 154.7, 72.2 and 40.9 mg Cd/kg dry soil for O. yodai, F. candida and S. umesaoi, respectively. Thus, the reproductive sensitivity of F. candida to Cd was between that of the other two species. Increasing reproductive sensitivity to Cd corresponded to increasing activity levels and a more surface-dwelling life-form. Our data may facilitate the generalisation of effect data for F. candida to other species.     

New trophic biomarkers for Collembola reared on algal diets

We used fatty acid (FA) analysis to investigate green algae and cyanobacteria as food sources for Collembola. We studied the effects of food quality on body mass and on neutral lipid (NLFA) and phospholipid (PLFA) fatty acid patterns of Collembola. Folsomia candida, Heteromurus nitidus and Protaphorura fimata were fed with common green algae (Chlorella vulgaris), filamentous soil algae (Klebsormidium flaccidum), cyanobacteria (Nostoc commune) and baker's yeast (Saccharomyces cerevisiae). Body mass of F. candida and H. nitidus was highest when reared on C. vulgaris and S. cerevisiae. P. fimata gained the most weight when fed baker's yeast. K. flaccidum and N. commune as resources resulted to low biomass in all Collembola. The four diets caused significant differences in the NLFA and PLFA composition of Collembola after six weeks of feeding. Two new trophic biomarker FAs indicating algal diets were assigned with 16:3ω3,6,9 and 16:2ω6,9, which were only present in NLFAs of Collembola consuming C. vulgaris and K. flaccidum. The amount of FAs from the ω7 family was high in Collembola lipids with cyanobacteria and yeast as food sources, whereas only trace amounts occurred in the NLFA fraction with algae as the resource. In summary, common soil algae and cyanobacteria differed in food quality for Collembola, depending on their growth form (unicellular versus filamentous) and/or secondary metabolites (e.g. cyanobacteria). The new FA biomarkers detected will allow further investigation of these trophic interactions under field conditions; for example, assessing the role of collembolan grazers in the formation of biological soil crusts.     

Food choice and reproductive success of Folsomia candida feeding on copper-contaminated mycelium of the soil fungus Alternaria alternata

We examined collembolan food preference for fungal mycelium grown on copper-contaminated medium, and the relationship between copper content, food selectivity and collembolan fitness when fed contaminated mycelium.To clarify whether collembolan food selectivity is related to fitness parameters, Folsomia candida were fed mycelium of the dark-pigmented fungus Alternaria alternata grown on medium with different copper concentrations. Copper-contaminated food (fungus grown on 50, 125, 250 and 500 μg Cu g⁻¹ medium, fresh wt.) was offered together with untreated food for 4 weeks. F. candida fed selectively on the provided mycelium and discriminated clearly between mycelium grown on high and low levels of contamination, distinctly preferring fungus grown on medium with a total copper concentration of 50 and 125 μg g⁻¹. In contrast, fungus grown on highly contaminated medium (250 and 500 μg g⁻¹) was avoided. Collembolan food preference generally matched fitness parameters. Reproduction was significantly affected by the total copper concentration of the fungal growth medium. When fed their preferred mycelium, collembolan reproduction was enhanced, whereas a diet of highly contaminated mycelium (250 or 500 μg g⁻¹) resulted in a strong decrease in reproduction. Adult survival was affected only marginally. Even though heavy metal contamination is a potential stress factor for many soil microarthropods, F. candida is able to discriminate between high and low quality food sources, and even benefits from moderately elevated copper concentrations.     

Defensive strategies of soil fungi to prevent grazing by Folsomia candida (Collembola)

Fungi represent a major part of the living biomass in the upper soil horizon and serve as an important food source for many soil organisms. We hypothesized that certain mycelial characteristics may serve to protect fungi from grazing. Specifically, this study focused on the influence of poisonous or other repellent metabolites and crystalline structures at the hyphal surface on the feeding preference of the soil microarthropod Folsomia candida Willem. The formation of crystalline structures was studied microscopically and the content of certain metabolites such as amanitin and muscarin was investigated using analytical methods. The feeding preference of F. candida was studied in different in-vitro food choice experiments. Additionally, the palatability of the fungal isolates was estimated by the amount of egg clusters laid by F. candida and by analysing the carbon and nitrogen content of the mycelia. F. candida was repelled by fungal species with toxic metabolites or crystals on their hyphal surface, which indicates that these traits serve as feeding protection. F. candida preferred dark-pigmented fungi. Total number of egg clusters and feeding preference were not correlated. However, insects that fed on fungi without repellent characteristics laid the most eggs. The amount of carbon and nitrogen in the mycelium had no influence on feeding behaviour. We conclude that the content of repellent metabolites and crystalline structures at the hyphal surface are defensive strategies of soil fungi and strongly influence feeding preference of F. candida. Other traits such as palatability were less important. Our results help to explain collembolan feeding behaviour and interactions between soil fungi and Collembola.     

Symbiosis with bacteria enhances the use of chitin by the springtail,Folsomia candida (Collembola)

Summary The relationship between Folsomia candida and chitin-degrading microorganisms was studied. On chitin agar, 10¹⁰ bacteria were isolated per g faeces, and 3.8×10¹¹ bacteria per g gut contents, 1/3 of them showing a clear (chitin-free) zone around the colony. The most abundant chitin-degrading bacteria were Xanthomonas maltophilia and Curtobacterium sp. To determine the bacterial contribution in the use of chitin by F. candida, a feeding experiment was carried out. F. candida were fed with chitin, either amended with or without tetracycline as an inhibitor of bacteria. When tetracycline was omitted the biomass of F. candida was increased compared to those fed chitin with tetracycline. However, this result was observed only when the food replacement intervals were long enough to allow bacterial colonization before ingestion of the food. In a food-selection experiment, a preference for chitin colonized with microorganisms as opposed to sterile chitin was found. The results indicate that a mutualistic symbiosis of F. candida with chitinolytic microorganisms is likely to enhance chitin degradation. This relationship is not only intra-intestinal but also involves an extra-intestinal phase.Dedicated to the late Prof. Dr. W. Kühnelt     

Species-specific impacts of collembola grazing on fungal foraging ecology

Fungi are primary agents of organic matter decomposition in forests. Although invertebrate grazing affects fungal biomass and morphology, the species-specific consequences of these interactions are little understood. Using three collembola species (Folsomia candida, Protaphorura armata, Proisotoma minuta) we employed a multi-trophic approach to investigate the individual effects of invertebrate grazing on four species of saprotrophic basidiomycete fungi growing in two species (one fungus: one collembola) soil microcosms. We studied these effects at three trophic levels: the rate of wood decay brought about by the fungi was assessed; fungal growth was characterized across multiple time points using a range of image analysis parameters (radial extension, hyphal coverage, fractal dimension); and collembola abundance was determined at the end of the experiment. Collembola species had different impacts both within and across fungal species; F. candida had the greatest effect on fungal mycelia whereas P. armata often had little impact. Fungal species varied in their resilience to grazing; all collembola species modified Phanerochaete velutina and Hypholoma fasciculare morphology, that of Resinicium bicolor was only markedly affected by F. candida, and effects on Phallus impudicus were negligible. In the case of H. fasciculare, these grazing effects translated into effects on the rate of fungus-induced wood decay: F. candida and P. armata, but not P. minuta, reduced wood decay rate compared to ungrazed controls. Rate of wood decay was unaffected in the other three fungal species. Changes in collembola population size were generally consistent across fungal species, with each species achieving a greater abundance on P. velutina than on H. fasciculare and P. impudicus. The collembola species did, however, respond differently to R. bicolor, with F. candida being more successful than P. armata. Our study suggests that a wide range of impacts can occur during fungus–collembola interactions, and that caution should be exercised when treating saprotrophic fungi and mycophagous collembola as uniform functional components.     

Food choice and reproductive success of Folsomia candida feeding on copper-contaminated mycelium of the soil fungus Alternaria alternata

We examined collembolan food preference for fungal mycelium grown on copper-contaminated medium, and the relationship between copper content, food selectivity and collembolan fitness when fed contaminated mycelium.To clarify whether collembolan food selectivity is related to fitness parameters, Folsomia candida were fed mycelium of the dark-pigmented fungus Alternaria alternata grown on medium with different copper concentrations. Copper-contaminated food (fungus grown on 50, 125, 250 and 500 μg Cu g^?1 medium, fresh wt.) was offered together with untreated food for 4 weeks. F. candida fed selectively on the provided mycelium and discriminated clearly between mycelium grown on high and low levels of contamination, distinctly preferring fungus grown on medium with a total copper concentration of 50 and 125 μg g^?1. In contrast, fungus grown on highly contaminated medium (250 and 500 μg g^?1) was avoided. Collembolan food preference generally matched fitness parameters. Reproduction was significantly affected by the total copper concentration of the fungal growth medium. When fed their preferred mycelium, collembolan reproduction was enhanced, whereas a diet of highly contaminated mycelium (250 or 500 μg g^?1) resulted in a strong decrease in reproduction. Adult survival was affected only marginally. Even though heavy metal contamination is a potential stress factor for many soil microarthropods, F. candida is able to discriminate between high and low quality food sources, and even benefits from moderately elevated copper concentrations.     

Increasing species and trophic diversity of mesofauna affects fungal biomass,mesofauna community structure and organic matter decomposition processes

A laboratory mesocosm experiment was set up to study the effects of five mesofauna model communities on litter fungal biomass (ergosterol content) and litter decomposition parameters (litter mass remaining, N concentration) for 4 months. The five treatments were: (1) no soil mesofauna, (2) the collembolan Folsomia fimetaria, (3) an assemblage of the collembolan species Isotomurus prasinus, Hypogastrura assimilis, F. fimetaria, Mesaphorura macrochaeta and Protaphorura armata, (4) the same collembolan assemblage plus the enchytraeid Enchytraeus crypticus, and (5) the six species plus the predaceous mite Hypoaspis aculeifer. After 30, 60, 90 and 120 days of incubation, six mesocosms of each treatment were sacrificed and biomass, species richness and dominance were measured. Changes occurred during the study with an increase in total detritivore biomass and a decrease in species richness with strong dominance by a few species in multispecies mesocosms. A vertical stratification of species was also observed in the mesocosms. Litter mass loss and N mineralisation were reduced with the introduction of fauna and showed the largest effects in the multispecies detritivore treatments. Ergosterol production was only temporary reduced in the multispecies treatments reflecting an effect of mesofauna on fungal biomass related to diversity rather than the biomass of mesofauna. An inhibitory predator effect was observed on functional decomposition parameters and indicated top-down control of decomposition via detritivorous mesofauna.     

Effects of Cd and Pb on the survival and juvenile production of Sinella coeca and Folsomia candida

Degradation factors can cause both quantitative and qualitative changes in fauna and thus affect soil functioning. The use of bio-indicators may help to detect environmental changes. The aim of this study was to evaluate the effects of lead and cadmium on the biology (mortality, reproduction, egg hatching) of two euedaphic collembolans, Sinella coeca and Folsomia candida and to evaluate sensitivity differences between the two species. The results showed that low concentrations of lead did not cause dramatic effects on the survival and reproduction of both species. Reproduction of both species was reduced when the soil contained a nominal concentration of Pb at 1000 μg g^–1. S. coeca and F. candida showed a high sensitivity to cadmium and both their reproduction and survival were significantly reduced on exposure to 50 μg g^–1. Moreover, egg hatching of F. candida was affected by the cadmium concentrations in the soil, and by the amount of time that the eggs stayed in contact with cadmium. This study showed that the inhibition determined by Cd on F. candida juvenile production was caused in part by inhibition of deposition and, in part, by reduction of egg viability.     

Recovery of reproduction after drought in the soil living Folsomia candida (Collembola)

Soil dwelling (euedaphic) Collembola have evolved to live in soil pores where the atmosphere is saturated with water vapour. Here we show that reproduction in the euedaphic Folsomia candida ceases during drought where soil water potentials are lower than −7 bar (∼99.4% RH). Recovery of the moulting cycle after cessation of drought showed increasing delay with increasing previous drought pressure. However, reproduction was rapidly resumed. Only in F. candida recovering from the most severe drought (−55 bar, 96% RH) was the time lapse between drought and resumed reproduction significantly different from the control (99.4% RH). Furthermore, the final numbers of eggs were unaffected by the degree of drought exposure. Hence, these results suggest that while even very mild drought will stop the reproductive cycle, subsequent recovery is rapid and complete.     

Use of an avoidance test for the assessment of microbial degradation of PAHs

An avoidance test using the soil springtail Folsomia candida was used to assess changes in contamination levels at low doses of PAHs following incubation with indigenous microflora. A soil from a former coke site was diluted to 1% in an unpolluted soil from the same site, which was used as a control, then both substrates were remoistened to 80% field capacity. The diluted soil was previously shown to be strongly repellent to F. candida, although not toxic. After 2-month incubation at 20 °C, the mixture lost its repellence capacity and became attractive to the test animal, while the global 16 PAHs content had decreased to a great extent (50%). PAH disappearance was linked to the occurrence of indigenous microbiota able to degrade hydrocarbons.     

The effect of pH and calcium on copper availability to the springtail Folsomia candida in simplified soil solutions

The effect of pH and calcium on copper bioavailability to the springtail Folsomia candida was determined by assessing uptake kinetics upon copper exposure for 15 days in simplified soil solutions. A slight bioaccumulation of copper was observed in all treatments and controls. The effect of exposure concentration and calcium level on copper accumulation was not significant. Although pH and time slightly but significantly affected copper concentrations in the body, copper uptake rates were not significantly different from zero. This suggests that copper uptake in F. candida exposed to sub-lethal copper concentrations in soil pore water is not affected by pH and calcium.     

Effects of temperature and life stage on the fatty acid composition of Collembola

Fatty acid (FA) analysis is used as a promising tool to investigate trophic interactions in soil food webs. The FA profile of neutral lipids in consumers is affected by the diet, and the occurrence and amount of certain FAs can reflect feeding strategies. We investigated the lipid composition of the Collembola Folsomia candida, Heteromurus nitidus and Protaphorura fimata with the fungus Chaetomium globosum as food source. The impact of environmental temperature and life stage was assessed, with special respect to linoleic acid (18:2ω6,9) as a marker FA for fungal feeding. In all Collembola species the ratio of C16/C18 in neutral lipid fatty acids (NLFAs) increased with decreasing temperature. In the NLFAs of F. candida and H. nitidus the Unsaturation Index and the amount of 18:2ω6,9 decreased with temperature, whereas in P. fimata effects were the opposite. The composition of phospholipid fatty acids (PLFAs) differed between species, but was little affected by temperature. The degree of unsaturation in NLFAs increased with the age of Collembola, mainly due to higher amounts of 18:2ω6,9 and a lower proportion of 18:1ω9. The biomarker linoleic acid represented over 20% of FAs in all fungal feeding Collembola. Despite considerable influence of temperature and life stage on its proportion, the amount was always higher than in individuals reared on other diets. This suggests that linoleic acid can serve as marker for fungal feeding independent of such physiological variations in Collembola.     

Do oribatid mites live in enemy-free space? Evidence from feeding experiments with the predatory mite Pergamasus septentrionalis

To examine whether their strongly hardened cuticle permits adult oribatid mites (Acari) to live in enemy-free space, we investigated (1) if Pergamasus septentrionalis, a widespread and abundant predatory mesostigmate mite species, is able to feed on oribatid mites, (2) if this predator preferentially feeds on certain oribatid mite species and (3) to what extent oribatid mites are consumed compared to collembolans and juvenile Mesostigmata. Single adult individuals of six different oribatid mite species (Steganacarus magnus; Nothrus silvestris; Damaeus riparius; Liacarus coracinus; Eupelops plicatus; Achipteria coleoptrata), one collembolan species (Folsomia quadrioculata) and juvenile Pergamasus spp. were offered separately to adult P. septentrionalis in a no-choice feeding experiment. The predators quickly and preferentially fed on collembolans and juvenile Pergamasus; three oribatid mite species were occasionally eaten (L. coracinus, N. silvestris, A. coleoptrata); the other oribatid mite species were rejected as food (E. plicatus, S. magnus, H. riparius). When preying on oribatid mites, P. septentrionalis typically first cut off the legs of the mite, then opened the body through the region of the genital plates or the mouthparts. The results suggest that predator pressure on adult oribatid mites in the field is low, since few relevant predators at the study site are more abundant and powerful than P. septentrionalis. Adult oribatid mites therefore likely indeed live in enemy-free space, i.e. are little affected by predators, but that may not apply to soft-bodied immatures. Collembolans were quickly consumed indicating that they comprise a major part of the diet of P. septentrionalis. Strong feeding on juveniles of Pergamasus suggests that P. septentrionalis also functions as an intra-guild predator.