Non‐trophic effects of oribatid mites on cord‐forming basidiomycetes in soil microcosms

1. Saprotrophic cord‐forming basidiomycetes are the primary agents of decomposition in forest ecosystems. Collembola and oribatid mites affect fungal growth and foraging, and therefore decomposition, through direct mycelial grazing. 2. Grazing on the fungal species Hypholoma fasciculare, Resinicium bicolor and Phanerochaete velutina by the collembola Folsomia candida, and the oribatid mites Steganacarus magnus, Euzetes globulus and Hermannia gibba was investigated in soil microcosms. 3. Folsomia candida grazed on all fungal species: radial extent of R. bicolor, hyphal coverage of all fungal species, and fractal dimension of R. bicolor and P. velutina were all reduced. Oribatid mites did not graze the fungi but did affect mycelial morphology. Steganacarus magnus caused a reduction in the radial extent of H. fasciculare, and the hyphal coverage and fractal dimension in both H. fasciculare and R. bicolor. Euzetes globulus and H. gibba reduced the hyphal coverage of P. velutina. 4. Oribatid mites are associated with a cornucopia of chemical secretions with possible anti‐fungal properties. Chemical analysis of H. gibba opisthonotal secretions revealed four main compounds, all of which are new to the known spectrum of opisthonotal components. The most abundant was (E)‐β‐farnesene. 5. Treatment effects were species‐specific in terms of both fungal and invertebrate species. This study provides the first evidence of non‐grazing effects of oribatid mites on fungal growth and morphology. This could potentially influence the spatial organisation of mycelium in forest soils and therefore the ability of fungi to locate, colonise and decompose dead organic matter.     

Invertebrate biodiversity affects predator fitness and hence potential to control pests in crops

Natural enemies that control pests usually allow farmers to avoid, or reduce, the use of pesticides. However, modern farming practices, that maximize yields, are resulting in loss of biodiversity, particularly prey diversity. Does this matter? Pests continue to thrive, and without alternative prey the predators should, perforce, concentrate their attentions upon the pests.We showed that a diverse diet significantly enhances predator fecundity and survival. Experiments were conducted using common generalist predators found in arable fields in Europe, the carabid beetle Pterostichus melanarius (Coleoptera: Carabidae) and the linyphiid spider Erigone atra (Araneae: Linyphiidae). We tested the hypothesis that mixed species diets were optimal, compared with restricted diets, with respect to parameters such as predator weights, egg weights, numbers of eggs laid, egg development times, egg hatching rates and predator survival. In carabids, an exclusive earthworm diet was as good as mixed diets containing earthworms for egg production and hatching, but less good than such mixed diets for increase in beetle mass and sustained egg laying. For spiders, aphids alone (Sitobion avenae) or with the Collembola Folsomia candida, drastically reduced survival. Aphids plus the Collembola Isotoma anglicana improved survival but only aphids with a mixed Collembola diet maximized numbers of hatching eggs.Predators offered only pests (slugs or aphids) had lowest growth rates and fecundity. We therefore demonstrated that conservation of a diversity of prey species within farmland, allowing predators to exploit a diverse diet, is essential if predators are to continue to thrive in crops and regulate agricultural pests.     

Invertebrate biodiversity affects predator fitness and hence potential to control pests in crops

Natural enemies that control pests usually allow farmers to avoid, or reduce, the use of pesticides. However, modern farming practices, that maximize yields, are resulting in loss of biodiversity, particularly prey diversity. Does this matter? Pests continue to thrive, and without alternative prey the predators should, perforce, concentrate their attentions upon the pests.We showed that a diverse diet significantly enhances predator fecundity and survival. Experiments were conducted using common generalist predators found in arable fields in Europe, the carabid beetle Pterostichus melanarius (Coleoptera: Carabidae) and the linyphiid spider Erigone atra (Araneae: Linyphiidae). We tested the hypothesis that mixed species diets were optimal, compared with restricted diets, with respect to parameters such as predator weights, egg weights, numbers of eggs laid, egg development times, egg hatching rates and predator survival. In carabids, an exclusive earthworm diet was as good as mixed diets containing earthworms for egg production and hatching, but less good than such mixed diets for increase in beetle mass and sustained egg laying. For spiders, aphids alone (Sitobion avenae) or with the Collembola Folsomia candida, drastically reduced survival. Aphids plus the Collembola Isotoma anglicana improved survival but only aphids with a mixed Collembola diet maximized numbers of hatching eggs.Predators offered only pests (slugs or aphids) had lowest growth rates and fecundity. We therefore demonstrated that conservation of a diversity of prey species within farmland, allowing predators to exploit a diverse diet, is essential if predators are to continue to thrive in crops and regulate agricultural pests.     

Growth and reproduction of fungal feeding Collembola as affected by fungal species,melanin and mixed diets

Fungal feeding soil invertebrates feed on a wide spectrum of fungal species suggesting that mixed diets increase fitness. We investigated relationships between food preferences for seven saprophytic fungal species/forms and fitness parameters (mortality, growth, time to reproduction, reproduction, egg size) in two Collembola species, Folsomia candida and Protaphorura armata. The fungal species/forms studied included the wild type and a melanin-deficient form of Aspergillus fumigatus to investigate the role of melanin in collembolan nutrition. Also, three mixed diets consisting of a preferred fungal species (Cladosporium cladosporioides) and species of intermediate or low food quality were investigated. Both Collembola species preferred similar fungal species/forms as food. Food preference generally matched fitness parameters, i.e. growth and reproduction of Collembola was at a maximum when feeding on preferred fungi. This was not the case for A. fumigatus. The wild type and the melanin-deficient form ranked among the least preferred fungi. Growth and reproduction of Collembola were low when feeding on the wild type but high when feeding on the melanin-deficient form indicating that the Collembola misjudged the food quality of the latter in the preference tests. The results show for the first time that genes driving melanin syntheses (pksP) strongly affect the food quality of fungi for fungal feeding invertebrates. Feeding on mixed diets generally increased growth and reproduction of Collembola except when the diets included toxic species (Penicillium sp.). The results support the nutrient balance hypothesis and also show that the detection of toxic species in the diet is important. They indicate that the widespread generalist feeding mode of Collembola maximizes fitness if toxic fungal species are avoided. The fitness parameters growth, reproduction and time until onset of reproduction were correlated closely but egg volume, which also varied with fungal diet, correlated poorly with the other fitness parameters. Variation in egg size with fungal diet shows that the diet of Collembola may have transgenerational effects.     

Impacts of elevated temperature on the growth and functioning of decomposer fungi are influenced by grazing collembola

Elevated temperature has potential to influence the biological mechanisms regulating ecosystem–atmosphere carbon exchange. The relationship between warming and heterotrophic microbial respiration remains poorly understood, not least in terms of the differential sensitivity of microbial groups to temperature and the complexity of interactions with other biota. Cord‐forming basidiomycete fungi are dominant primary decomposers in temperate woodland. Decomposition rates are determined by the composition of the decomposer community, ecophysiological relationships between these fungi and abiotic variables and interactions with other organisms. Amongst the latter, a major determinant is the balance between mycelial growth and removal by soil invertebrate grazers, which can themselves be affected by elevated temperature. We investigated the impact of elevated temperature on fungal foraging and decomposition of beech (Fagus sylvatica) wood in soil microcosms to which the invertebrate grazers, Folsomia candida and Protophorura armata (Collembola), were added in factorial combinations with five basidiomycete fungi. Species‐specific impacts on mycelial development and function resulted from differential sensitivity of fungi to warming and grazing. Temperature impacts on collembola abundance were resource‐specific, causing increased grazing pressure by both species, but on different fungi. Grazing often counteracted warming‐induced stimulation of mycelial growth, but occasionally amplified the temperature effect, with implications for colonization rates of new resources. High grazing pressure did not prevent increased fungal‐mediated decomposition of colonized wood, as fungi utilized more resource‐derived energy to maintain explorative growth. Impacts of elevated temperature on decomposition are likely to depend on local composition of the fungal and invertebrate decomposer community.     

Influence of fungi on growth and survival of Onychiurus armatus (Collembola) in a metal polluted soil

Summary The influence of food quantity and quality on growth and survival of Onychiurus armatus (Tullb.) in metal polluted environments has been investigated in laboratory experiments. The Collembola was reared on five species of fungi isolated from a metal polluted soil close to a brass mill in SE Sweden.Survival of O. armatus was improved when fungal biomass was continuously added in a polluted mor (1,300 ppm Zn and 200 ppm Cu), and when specimens were fed metal polluted fungi for 1, 3 and 7 days a week, only those that were starved had increased mortality. Allometric growth, on the other hand, was significantly reduced when Collembola was given surplus of metal polluted fungi, whereas growth losses caused by metals were offset by protein rich food. Hence, sufficient food quantities alone could overcome mortality losses but not growth retardation in a metal polluted environment.Feeding preference of O. armatus was not determined by the protein content of the fungi although this was beneficial for growth. Metals changed the relative palatability of fungal species, but one of the metal tolerant species, Paecilomyces farinosus, which was also protein rich, remained reasonably attractive for O. armatus also when it was metal polluted. The mechanisms by which growth and survival of O. armatus were promoted by a combination of protein and Zn/Cu rich fungi seemed to be crucial in understanding the fate of a population of this species in a metal polluted soil.     

Zn uptake by maize under the influence of AM-fungi and Collembola Folsomia candida

Zn uptake by maize plants may be affected by the presence of arbuscular mycorrhizal fungi (AMF). Collembola often play an important controlling role in the inter-relationship between AMF and host plants. The objective of this experiment was to examine whether the presence of Collembola at different densities (0.4 and 1 individuals g⁻¹ dry soil) and their activity have any effect on Zn uptake by maize through the plant–AMF system. The presence of the AMF (Glomus intraradices) and of the Collembola species Folsomia candida was studied in a laboratory microcosm experiment, applying a Zn exposure level of 250 mg kg⁻¹ dry soil. Biomass and water content of the plants were no different when only AMF or when both AMF and Collembola were present. In the presence of AMF the Zn content of the plant shoots and roots was significantly higher than without AMF. This effect was reduced by Collembola at both low and high density. High densities of Collembola reduced the extent of AMF colonization of the plant roots and hyphal length in the soil, but low densities had no effect on either. The results of this experiment reveal that the F. candida–G. intraradices interaction affects Zn uptake by maize, but the mechanisms are still unknown.     

Changes in volatile production during interspecific interactions between four wood rotting fungi growing in artificial media

Effects of volatile organic compounds (VOCs) produced during interspecific mycelial interactions were examined by measuring extension rate of ‘target’ fungi growing in agar plates taped above two interacting mycelia – Bjerkandera adusta, Hypholoma fasciculare, Stereum gausapatum and Trametes versicolor in all combinations. Extension rates of T. versicolor, S. gausapatum and H. fasciculare above self-pairings were not significantly different (P > 0.05) to growth above agar controls, but the extension rate of B. adusta was significantly (P ≤ 0.05) greater. Extension rates of T. versicolor and B. adusta were often significantly greater above inter-specific interactions and above other species compared with growth above self or agar controls. VOC production was quantified and qualified, by gas chromatography–mass spectrometry (GC/MS), over the course of interactions with T. versicolor replacing S. gausapatum, deadlocking with B. adusta and replaced by H. fasciculare. VOC production was species- and interaction-specific. It varied over the time course of interactions, and changes in production were correlated with production of pigments in interactions involving S. gausapatum. VOCs included 3 monoterpenes, benzoic acid, alkenols of different chain lengths, two long-chain hydrocarbons and a quinolinium-like compound. Their possible roles are discussed.     

Microarray analysis of differential gene expression elicited in Trametes versicolor during interspecific mycelial interactions

Trametes versicolor is an important white rot fungus of both industrial and ecological interest. Saprotrophic basidiomycetes are the major decomposition agents in woodland ecosystems, and rarely form monospecific populations, therefore interspecific mycelial interactions continually occur. Interactions have different outcomes including replacement of one species by the other or deadlock. We have made subtractive cDNA libraries to enrich for genes that are expressed when T. versicolor interacts with another saprotrophic basidiomycete, Stereum gausapatum, an interaction that results in the replacement of the latter. Expressed sequence tags (ESTs) (1920) were used for microarray analysis, and their expression compared during interaction with three different fungi: S. gausapatum (replaced by T. versicolor), Bjerkandera adusta (deadlock) and Hypholoma fasciculare (replaced T. versicolor). Expression of significantly more probes changed in the interaction between T. versicolor and S. gausapatum or B. adusta compared to H. fasciculare, suggesting a relationship between interaction outcome and changes in gene expression.     

Arbuscular mycorrhiza and Collembola interact in affecting community composition of saprotrophic microfungi

The functioning of the plant-mycorrhiza system depends on interactions with other organisms, including saprotrophic (ST) soil fungi. The interactions between mycorrhizal and ST fungi are likely affected by fungivorous soil animals, such as Collembola. In a two-factorial laboratory experiment lasting for 30 weeks we assessed the effects of an arbuscular mycorrhizal fungus (Glomus mosseae) and Collembola (Protaphorura fimata, Heteromurus nitidus and Folsomia candida) on the community composition of ST microfungi in soil planted with the invasive grass Cynodon dactylon. The presence of mycorrhiza substantially reduced total plant biomass and reduced N and P availability to the soil microflora, though these effects were less pronounced in the presence of Collembola. The density of Collembola was high (corresponding to about 2×10⁵ individuals m^–2) and was not affected by the presence of G. mosseae. In spite of the large amount of mycorrhizal mycelium in soil, it contributed little to Collembola nutrition. The presence of mycorrhiza strongly affected the community structure of ST soil fungi. In particular, mycorrhiza reduced the relative abundance of Trichoderma harzianum and Exophiala sp., but increased the abundance of Ramichloridium schulzeri and several sterile forms. However, the difference between fungal communities in mycorrhizal and non-mycorrhizal treatments was much more pronounced in the presence of Collembola. Presumably, the intense grazing by Collembola destabilized the ST fungal community, thereby making it more susceptible to the influence of G. mosseae. These results document for the first time that fungal feeding soil invertebrates can significantly affect the interactions between mycorrhizal fungi and ST soil microorganisms.     

A laboratory study on temperature relations of egg production and development in two related species of carabid beetle

Summary Egg production and development of the carabid beetles Notiophilus biguttatus F. and Notiophilus rufipes Curtis were studied in relation to temperature. Adult beetles and larvae were fed springtails of the species Orchesella cincta (Linné). The rate of egg production, at the different temperatures did not differ between the species. As observed in N. biguttatus egg production at a daily fluctuating temperature regime is high compared to egg production at the constant temperatures. Food supply not only has a strong effect on egg production but also on the relation of egg production with temperature, as shown in N. biguttatus. Development times in N. rufipes are longer than in N. biguttatus particularly at low temperatures. The temperature during development has a distinct effect on adult body size. As observed in N. biguttatus body size and fecundity show a strong positive correlation.     

Hsp70 instability and induction by a pesticide in Folsomia candida

The heat shock protein Hsp70 has been shown to be a promising biomarker in aquatic and terrestrial organisms. However, its analysis in the soil insect Folsomia candida (Collembola) poses many problems as the protein is particularly unstable in this species. Western blotting has shown that the principal degradation fragment has a size of 48 kDa. We have developed a Western blot method that avoids the degradation of Hsp70 and was successful in detecting the protein in the springtail F. candida after a heat shock (12, 18 and 24 h at 32°C). In the second part of the study the organisms were exposed to artificial compressed soil contaminated with the dinitrophenol dinoseb (10, 15 and 20 μg g^-1 dry weight [DW]). Hsp70 was analysed in pooled samples (40 to 150 collembola according to age) after 1, 2, 3, 4, 5, 6, 7, 11 and 14 days. The only significant induction was observed after 5 days at 20 μg g^-1 DW of dinoseb. The induction patterns over time were dissimilar for the different concentrations and a relatively high variability between the replicates was observed. Our results show that we must be cautious when interpreting biomarker results, especially those for Hsp70.     

Grazing by Folsomia candida (Collembola) differentially affects mycelial morphology of the cord-forming basidiomycetes Hypholoma fasciculare, Phanerochaete velutina and Resinicium bicolor

Cord-forming basidiomycetes are important decomposers of dead wood in forest ecosystems but the impact of mycophagous soil invertebrates on their mycelia are little known. Here we investigate the effects of different grazing intensities of Collembola (Folsomia candida) on mycelial foraging patterns of the saprotrophic cord-forming basidiomycetes Hypholoma fasciculare, Phanerochaete velutina and Resinicium bicolor growing from beech (Fagus sylvatica) wood block inocula in dishes of non-sterile soil. Mycelial extension rate and hyphal coverage decreased with increased grazing intensity. R. bicolor was most affected, high grazing density resulting in only a few major cords remaining. Grazing of H. fasciculare often resulted in points of more rapid outgrowth as cords with a fanned margin. In grazed mycelia of P. velutina the main cords had fanned tips and lateral cords became branched. These results suggest that mycophagy by Collembola may hinder the growth of cord-forming fungi in woodlands, which might impact on the ability of these fungi to forage for and decompose dead organic material.     

The effects of age and weather on egg laying inDanaus plexippus L. (Lepidoptera: Danaidae)

The effects of age and weather conditions on egg laying in D. plexippus were determined for caged females. Age (measured in physiological time), temperature and solar radiation influence egg laying in this species of butterfly. An algorithm taking these factors into account in presented and accounts for 88% of the daily variation in egg laying. Caged D. plexippus begin to lay eggs six—seven days after emergence, peak egg production (about 60 eggs/♀) occurs about 15 days later. Females continue to lay eggs throughout their adult life, which in a flight cage was about 40 days. This egg laying pattern is compared with other published fecundity schedules. The effect and importance of a female being prevented from laying her eggs, on her life-time egg production, is also discussed.     

Grazing alters network architecture during interspecific mycelial interactions

The changes that occur in mycelial architecture of Phanerochaete velutina interacting with Hypholoma fasciculare mycelium in soil microcosms in the presence and absence of the collembola Folsomia candida are investigated employing tools developed in graph theory and statistical mechanics. There was substantially greater overgrowth of H. fasciculare by P. velutina mycelium when grazed than when un-grazed. There was a marked disappearance of hyphal links in all un-grazed systems between 8 d and 34 d, predominantly in areas distant from the interaction, but this was much less evident in grazed systems. Further, new tangential cross-links connecting radial cords distant from the inoculum formed in grazed systems. The thickness of cords increased with time, and more so in grazed systems. There was no significant difference in transport efficiency between the grazed and un-grazed systems. The ability of the mycelial network to modify dynamically link strengths is crucial to achieving a balance between transport capacity/robustness to damage and overall cost of production.     

The effect of temperature,darkness, starvation and various food types on growth,survival and reproduction of Helisoma duryi,Biomphalaria alexandrina and Bulinus truncatus (Gastropoda: Planorbidae)

Helisoma duryi has been proposed as a biological control agent in schistosomiasis due to its superiority in laboratory competition experiments with various species of the intermediate host snails. Therefore it was considered important to evaluate the response of this snail species and the intermediate host species, Biomphalaria alexandrina and Bulinus truncatus, to various physical, chemical and biological factors under laboratory conditions in order to obtain information on the similarities in the ecological niches of these species. The factors considered in the present paper are: temperature, darkness, starvation and food. All three species had optimal growth and egg laying at 26–28 °C. Only H. duryi survived for a longer period at 33°C and it was capable of starting egg laying at this temperature although the onset was delayed. However, low temperature (18°C) caused a relatively larger decrease in egg laying of H. duryi than in the other two species. Growth and egg laying was reduced for H. duryi and B. truncatus kept under darkness and B. alexandrina could not tolerate maintenance under darkness. A few days of starvation of juvenile snails had no effect on later growth and egg laying capacity of the survivors, although mortality in B. truncatus was increased. B. alexandrina had a lower tolerance to starvation than the other two species. Egg laying of snails fed only one of the three laboratory food types decreased for all three species in the order: Vov-vov (dog food in dry pellets), Tetramin (fish food) and lettuce. Combinations of lettuce and one or more proteinaceous food types gave optimal growth and egg laying for all three species.     

Biology of the Eucalyptus leaf beetle Paropsisterna selmani (Chrysomelidae: Paropsini): a new pest of Eucalyptus species (Myrtaceae) in Ireland

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Diet, fecundity and egg size in some polyphagous predatory carabid beetles

Egg size was measured at different rates of egg laying in three polyphagous carabid species, known to be useful predators of cereal aphids; the small Bembidion lampros Herbst and the medium-sized Pterostichus cupreus L. and P. melanarius Illiger. Variations in fecundity, as well as the ability of the medium-sized species to also build up fat reserves, were obtained when beetles were subjected to different dietary regimes consisting of aphids, or foods with a lower or higher protein content. Egg size was found to be dependent on the rate of egg laying within a species. A diet of cereal aphids appeared to be adequate for egg production in these polyphagous carabids, but female P. cupreus were unable to build up fat reserves when they ingested aphids contaminated with the aphicide pirimicarb. Beetles were able to devote resources to more and larger eggs (B. lampros), or to larger eggs and/or fat reserves (P. melanarius/P. cupreus) when given access to a carbohydrate-rich food with low protein content. The highest rate of egg laying was obtained when female P. cupreus and P. melanarius were given a more varied diet at frequent intervals; including regular shifts between unsprayed aphids, carbohydrate-rich food and protein-rich maggots. Within the varied diet treatment a negative relationship was obtained between egg size and egg number among similar-sized individuals of P. cupreus and P. melanarius; females producing the largest number also laid the smallest eggs. Egg size affected larval survival, since first instars hatching from large eggs were found to survive longer than those hatching from small eggs. The influence of differences in food intake on reproduction, maintenance metabolism, and survival of fieldinhabiting carabids is discussed.     

Variations cytologiques des corps allates au cours du cycle reproducteur du Collembole Folsomia candida

In the parthenogenetic females of the Collembola, Folsomia candida, study of the nucleoplasmic ratio and fine structure of the corpora allata cells reveals an activity cycle synchronized with the ovarian cycle. The maximum cytoplasmic volume, connected with a relatively great development of the endoplasmic reticulum, is reached during the vitellogenic phase.The simultaneous control of the ovary by moulting hormones and by a corpus allatum hormone is discussed.