Beetles provide directed dispersal of viable spores of a keystone wood decay fungus

Wood decay fungi are considered to be dispersed by wind, but dispersal by animals may also be important, and more so in managed forests where dead wood is scarce. We investigated whether beetles could disperse spores of the keystone species Fomitopsis pinicola. Beetles were collected on sporocarps and newly felled spruce logs, a favourable habitat for spore deposition. Viable spores (and successful germination) of F. pinicola were detected by dikaryotization of monokaryotic bait mycelium from beetle samples. Viable spores were on the exoskeleton and in the faeces of all beetles collected from sporulating sporocarps. On fresh spruce logs, nine beetle species transported viable spores, of which several bore into the bark. Our results demonstrate that beetles can provide directed dispersal of wood decay fungi. Potentially, it could contribute to a higher persistence of some species in fragmented forests where spore deposition by wind on dead wood is less likely.     

Spore dispersal of a resupinate ectomycorrhizal fungus, Tomentella sublilacina, via soil food webs

Patterns of fungal spore dispersal affect gene flow, population structure and fungal community structure. Many Basidiomycota produce resupinate (crust-like) basidiocarps buried in the soil. Although spores are actively discharged, they often do not appear to be well positioned for aerial dispersal. We investigated the potential spore dispersal mechanisms of one exemplar of this growth form, Tomentella sublilacina. It is a widespread ectomycorrhizal fungus that sporulates in the soil organic horizon, can establish from the spore bank shortly after disturbance, but also can be a dominant species in mature forest stands. We investigated whether its spores could be dispersed via spore-based food webs. We examined external surfaces, gut contents and feces from arthropod fungivores (mites, springtails, millipedes, beetles, fly larvae) and arthropod and vertebrate predators (centipedes, salamanders) from on and around T. sublilacina sporocarps. Spore densities were high in the guts of many individuals from all fungivore groups. Centipede gut contents, centipede feces and salamander feces contained undigested invertebrate exoskeletons and many apparently intact spores. DAPI staining of spores from feces of fungivores indicated that 7-73% of spores contained intact nuclei, whereas spores from predators had lower percentages of intact nuclei. The spiny spores often were lodged on invertebrate exoskeletons. To test the viability of spores that had passed through invertebrate guts we used fecal droppings of the millipede Harpaphe haydeniana to successfully inoculate seedlings of Pinus muricata (Bishop pine). These results indicate the potential for T. sublilacina spore dispersal via invertebrates and their predators in soil food webs and might help to explain the widespread distribution of this species. It is likely that this is a general mechanism of dispersal for fungi producing resupinate sporocarps, indicating a need to develop a fuller understanding of the linkages of soil food webs and spore dispersal.     

Entomogenous Fusarium species

Fusarium species are known for their abundance in nature and their diverse associations with both living and dead plants and animals. Among animals Fusarium is found primarily in relationship with insects. This literature review of the past 50 years includes both non-pathogenic and pathogenic relationships between Fusarium and insects. Special attention is given to the host range, particularly between plant- and insect-hosts, and to the possible microbial potential of the fungus to control insect pests. Correct classification of this fungus has been difficult because of its diverse and non-uniform morphological features. However, by now a usable and reliable taxonomic system has been developed. The fungus can be easily cultured and mass produced. Among the non-pathogenic associations mutualism and allotrophy are found between Fusarium and wood-inhabiting and flour beetles, respectively, enhancing development and production of beetle larvae. Some insects contribute to the dispersal of the fungus in the environment by means of spore passage through their guts. Plant-pathogenic Fusarium species gain access to host tissue by plant-feeding insects. A large number of Fusarium spp. are entomopathogenic; some are weak, facultative pathogens, especially of the lepidopteran and coleopteran orders, and they will colonize their dead hosts as saprophytes. In a few cases pathogenicity to both plant and insect by one isolate was found. Strong pathogens were reported primarily from homopterans and dipterans from field observations of natural mortalities as well as from pathogenicity tests. Potential Fusarium isolates which cause high insect mortalities also show high host specificity and no damage to crop plants. The question of host invasion has been addressed by few investigators. Entrance of the fungus via the oral route, oviposition tubes, wounds, or ectoparasitic activity, were stated, but no claim for penetration of the insect cuticle. Mycotoxins, such as trichothecenes (T-2) and other secondary metabolites, contributed to mortalities of termites, mealworms, flour beetles, maize borers and blow flies, while zearalenone (F-2) exhibited a beneficial effect on egg production in flour beetles and a detrimental effect on fecundity in mammals. Studies on adverse effects of the fungus on beneficial organisms (including mammals and plants) revealed that both harmful as well as safe Fusarium isolates exist in nature. Highly host-specific and strongly entomopathogenic Fusarium isolates should be more extensively studied and tested for their possible use in biological control.     

Infection of Tribolium castaneum with Bacillus thuringiensis: Quantification of Bacterial Replication within Cadavers,Transmission via Cannibalism,and Inhibition of Spore Germination

Reproduction within a host and transmission to the next host are crucial for the virulence and fitness of pathogens. Nevertheless, basic knowledge about such parameters is often missing from the literature, even for well-studied bacteria, such as Bacillus thuringiensis, an endospore-forming insect pathogen, which infects its hosts via the oral route. To characterize bacterial replication success, we made use of an experimental oral infection system for the red flour beetle Tribolium castaneum and developed a flow cytometric assay for the quantification of both spore ingestion by the individual beetle larvae and the resulting spore load after bacterial replication and resporulation within cadavers. On average, spore numbers increased 460-fold, showing that Bacillus thuringiensis grows and replicates successfully in insect cadavers. By inoculating cadaver-derived spores and spores from bacterial stock cultures into nutrient medium, we next investigated outgrowth characteristics of vegetative cells and found that cadaver-derived bacteria showed reduced growth compared to bacteria from the stock cultures. Interestingly, this reduced growth was a consequence of inhibited spore germination, probably originating from the host and resulting in reduced host mortality in subsequent infections by cadaver-derived spores. Nevertheless, we further showed that Bacillus thuringiensis transmission was possible via larval cannibalism when no other food was offered. These results contribute to our understanding of the ecology of Bacillus thuringiensis as an insect pathogen.     

Beyond animals and plants: dynamic maternal effects in the fungus Neurospora crassa

Maternal effects are widely documented in animals and plants, but not in fungi or other eukaryotes. A principal cause of maternal effects is asymmetrical parental investment in a zygote, creating greater maternal vs. paternal influence on offspring phenotypes. Asymmetrical investments are not limited to animals and plants, but are also prevalent in fungi and groups including apicomplexans, dinoflagellates and red algae. Evidence suggesting maternal effects among fungi is sparse and anecdotal. In an experiment designed to test for maternal effects across sexual reproduction in the model fungus Neurospora crassa, we measured offspring phenotypes from crosses of all possible pairs of 22 individuals. Crosses encompassed reciprocals of 11 mating‐type ‘A’ and 11 mating‐type ‘a’ wild strains. After controlling for the genetic and geographic distances between strains in any individual cross, we found strong evidence for maternal control of perithecia (sporocarp) production, as well as maternal effects on spore numbers and spore germination. However, both parents exert equal influence on the percentage of spores that are pigmented and size of pigmented spores. We propose a model linking the stage‐specific presence or absence of maternal effects to cellular developmental processes: effects appear to be mediated primarily through the maternal cytoplasm, and, after spore cell walls form, maternal influence on spore development is limited. Maternal effects in fungi, thus far largely ignored, are likely to shape species' evolution and ecologies. Moreover, the association of anisogamy and maternal effects in a fungus suggests maternal effects may also influence the biology of other anisogamous eukaryotes.     

Inferring dispersal patterns of the generalist root fungus Armillaria mellea

Investigating the dispersal of the root-pathogenic fungus Armillaria mellea is necessary to understand its population biology. Such an investigation is complicated by both its subterranean habit and the persistence of genotypes over successive host generations. As such, host colonization by resident mycelia is thought to outcompete spore infections. We evaluated the contributions of mycelium and spores to host colonization by examining a site in which hosts pre-date A. mellea. Golden Gate Park (San Francisco, CA, USA) was established in 1872 primarily on sand dunes that supported no resident mycelia. Genotypes were identified by microsatellite markers and somatic incompatibility pairings. Spatial autocorrelation analyses of kinship coefficients were used to infer spore dispersal distance. The largest genotypes measured 322 and 343 m in length, and 61 of the 90 total genotypes were recovered from only one tree. The absence of multilocus linkage disequilibrium and the high proportion of unique genotypes suggest that spore dispersal is an important part of the ecology and establishment of A. mellea in this ornamental landscape. Spatial autocorrelations indicated a significant spatial population structure consistent with limited spore dispersal. This isolation-by-distance pattern suggests that most spores disperse over a few meters, which is consistent with recent, direct estimates based on spore trapping data.     

Ultrastructural study of the microsporidian chytridiopsis typographi (Chytridiopsida: Microspora) infecting the bark beetle,Ips typographus (Scolytidae: Coleoptera), with new data on spore dimorphism

Two types of sporogony of the microsporidian Chytridiopsis typographi in the midgut of adult bark beetle, Ips typographus, have been examined by means of light and electron microscopy. New data are reported on spore dimorphism and on the formation of pansporoblasts in two types of sporogony. Thin-walled spores, larger in size, are formed in a parasitophorous vacuole in the host columnar cells. Thick-walled spores are formed in a minimal vacuole in the host. The ultrastructure of the spore walls and the cyst wall are different from the organization in other microsporidia. Both spore types have identical internal structures and viable spores.     

The significance of temperature during sporulation on the biology of pycnidiospores of Mycosphaerella ligiilicola

The germination, infectivity and survival of pycnidiospores obtained from cultures of Mycosphaerella ligulicola grown at 15 and 26 °C were compared. Spores formed at 26° (‘26° spores’) were less able to germinate at low relative humidities and showed a narrower temperature range for maximum germination after 6 h. At high spore densities 26° spores showed self-inhibition of germination and, over a range of lower densities, growth of their germ tubes was checked, which resulted in lower infection of leaf discs compared with 15° spores in which this phenomenon did not occur. The fungus could be recovered from un-sterile compost over a longer period after inoculation with 15° spores. Only after storage at a temperature well below zero was there a difference in viability between 15° and 26° spores. It is thought that the potential advantage of producing larger numbers of spores at 26° would be realized only under optimum conditions for dispersal and infection. The smaller number of spores produced at 15° are likely to be successful under natural conditions.     

Behaviours of phoretic mites (Acari) associated with Ips pini and Ips grandicollis (Coleoptera: Curculionidae) during host‐tree colonization

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Origin and evolution of fungus farming in wood-boring Coleoptera – a palaeontological perspective

Insect–fungus mutualism is one of the better-studied symbiotic interactions in nature. Ambrosia fungi are an ecological assemblage of unrelated fungi that are cultivated by ambrosia beetles in their galleries as obligate food for larvae. Despite recently increased research interest, it remains unclear which ecological factors facilitated the origin of fungus farming, and how it transformed into a symbiotic relationship with obligate dependency. It is clear from phylogenetic analyses that this symbiosis evolved independently many times in several beetle and fungus lineages. However, there is a mismatch between palaeontological and phylogenetic data. Herein we review, for the first time, the ambrosia system from a palaeontological perspective. Although largely ignored, families such as Lymexylidae and Bostrichidae should be included in the list of ambrosia beetles because some of their species cultivate ambrosia fungi. The estimated origin for some groups of ambrosia fungi during the Cretaceous concurs with a known high diversity of Lymexylidae and Bostrichidae at that time. Although potentially older, the greatest radiation of various ambrosia beetle lineages occurred in the weevil subfamilies Scolytinae and Platypodinae during the Eocene. In this review we explore the evolutionary relationship between ambrosia beetles, fungi and their host trees, which is likely to have persisted for longer than previously supposed.     

The effects of two microsporidian pathogens on the two-spotted lady beetle, Adalia bipunctata L. (Coleoptera: Coccinellidae)

Two-spotted lady beetles, Adalia bipunctata L. are available for biological pest control in North America. Lady beetles are known to host microsporidia and although these pathogens are able to infect more than one host under laboratory conditions, little is known regarding the effects of more than one microsporidian pathogen on host fitness. In this study, egg cannibalism was used to examine the effects of the microsporidium Tubulinosema hippodamiae from Hippodamia convergens and an undescribed microsporidium from A. bipunctata (alone and in combination) on A. bipunctata host fitness (larval development and mortality, sex ratio, adult fecundity and longevity). Development was prolonged significantly for larvae that were infected with the undescribed microsporidium but T. hippodamiae had no effect and as a result, conclusions could not be made regarding the effects of both pathogens on larval development. The two microsporidia had no effect on sex ratios (1♀:1♂) or on adult fecundity and longevity. Spores were detected in the majority of smear preparations of individuals that were fed microsporidia-infected eggs and molecular analysis confirmed the identity of both pathogens in sampled individuals. T. hippodamiae spores were smaller than spores of the undescribed microsporidium (3.76±0.03×2.32±0.02 μm and 5.43±0.06×2.75±0.03 μm, respectively) and although the former stained less intensely than did those of latter, spores of the two pathogens are difficult to differentiate when examined by light microscopy alone. The ability of some microsporidia to infect more than one lady beetle host makes it difficult to conclude with certainty as to the number of species that are present in infected Adalia when specimens are examined solely by light microscopy.     

感染羽茅的香柱菌属内生真菌对丛枝菌根真菌孢子萌发的影响

内生真菌与丛枝菌根(AM)真菌是构成草原生态系统的重要组成部分.内生真菌会抑制其宿主植物的AM真菌侵染率.本研究以感染2种香柱菌属内生真菌[Epichloё gansuensis(Eg)和E. sibirica(Es)]的天然禾草羽茅为供试材料,进行体外纯培养的内生真菌培养滤液、感染内生真菌的羽茅叶片(包括鲜叶和枯叶)浸提液,以及根系分泌物对摩西球囊霉(Gm)和幼套球囊霉(Ge)2种AM真菌孢子萌发影响试验.结果表明: 香柱菌属内生真菌的培养滤液会显著抑制2种AM真菌孢子的萌发,而感染香柱菌属内生真菌的羽茅根系分泌物只对Ge孢子萌发有显著抑制作用,且上述抑制作用与内生真菌种类无关;鲜叶浸提液对Gm和Ge的孢子萌发率均无显著影响,而枯叶浸提液对Ge的孢子萌发有显著抑制作用.在自然生态系统中,香柱菌属内生真菌通常存在于宿主植物体内,可能通过影响宿主植物的根系分泌物来影响AM真菌孢子的萌发.     

Synchytrium solstitiale: reclassification based on the function and role of resting spores

Studies were made about resting spores of Synchytrium solstitiale, a chytrid that causes false rust disease of yellow starthistle (YST). During evaluation of this fungus for biological control of YST, a protocol for resting spore germination was developed. Details of resting spore germination and study of long-term survival of the fungus were documented. Resting spores from dried leaves germinated after incubating them on water agar at least 7 d at 10-15 C. Resting spores were viable after storage in air-dried leaves more than 2 y at room temperature, suggesting they have a role in off-season and long-term survival of the fungus. Each resting spore produced a single sorus that contained a single sporangium, which on germination released zoospores through a pore. YST inoculated with germinated resting spores developed symptoms typical of false rust disease. All spore forms of S. solstitiale have been found to be functional, and the life cycle of S. solstitiale has been completed under controlled laboratory and greenhouse conditions. Resting spore galls differ from sporangial galls both morphologically and biologically, and in comparison, each sporangial gall cleaves into several sori and each sorus produces 5-25 sporangia that rupture during release of zoospores. For this reason S. solstitiale should be reclassified as diheterogallic sensu Karling (Am J Bot 42:540-545). Because resting spores function as prosori and produce an external sorus, S. solstitiale is best placed in into the subgenus Exosynchytrium.     

The use of fluorescent powders to track autocontamination of emerald ash borer (Coleoptera: Buprestidae) by the entomopathogen Beauveria bassiana (Ascomycota: Hypocreales)

We evaluated the use of fluorescent powders for tracking dispersal by the emerald ash borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), of Beauveria bassiana isolates from an autocontamination device. Neither of the two DayGlow powders tested (Arc Yellow and Aurora Pink) interfered with fungal germination or growth, nor did they affect survival of beetles in the laboratory, or affect virulence of the fungus. The powders persisted at least 10 days out-of-doors on dead beetles in sticky band traps, and at least 14 days on pouches inside autocontamination traps. During field trials of autocontamination traps with powder-dusted fungal pouches in southwestern Ontario, 8.0% of the 4010 beetles captured in green prism and sticky-band traps were positive for fluorescent powders. Only half (46.2–57.8%) of the powder-positive beetles actually carried viable fungal conidia, as determined by plating of beetle rinses, possibly as a result of patchy growth of fungal isolates and reduced conidia production on pouch surfaces during the 16-day trapping experiment. The presence of viable conidia (either one or both isolates) on about 10% of beetles that did not carry any visible powder particles may be an indication of horizontal transmission of the fungus by beetles that had visited the autocontamination traps.     

The ultrastructure of the zygospore in Endogone flammicorona Trappe & Gerdemann

The ultrastructural organization of the spores of the sporocarp of Endogone flammicorona was studied. Two types of organization are described. Initially the spore possessed a vacuolate protoplasm and was bound by two cell wall layers. The spore was surrounded by a hyphal mantle formed of a sheet of vacuolized hyphae with uniformly thin walls. Secondly, although the ultrastructural features of the spore appeared the same, it was now surrounded by a hyphal mantle with unevenly thickened walls (i. e., the so-called flaming crown) due to the gradual and irregular deposition of granules and lamellae. This crown gives the spore its most commonly observed morphological feature and is the preminent character employed taxonomically to speciate Endogone flammicorona Trappe & Gerdemann.     

In vivo development of spores of Absidia ramosa.

Approximately 10(6) spores of Absidia ramosa were inoculated intravenously into normal and cortisone pretreated mice. At subsequent time intervals the liver, lungs and kidneys were removed and examined for fungal localization and growth. In normal mice, spore germination and continued hyphal growth was restricted to the kidneys-evidence of germination not being visible until around 30h post inoculation. Cortisone therapy allowed germination of spores in the lung and kidney by 7h but subsequent hyphal growth in the lung was severely restricted compared with the kidney where extensive hyphal growth occurred. Germination of spores in the liver of cortisone treated animals was slow, not becoming apparent until about 40h after inoculation. These results suggest that host defence mechanisms in the form of phagocytosis as well as biochemical inhibitors and/or lack of suitable stimulators are important in preventing germination of introduced fungal spores. Once germination has occurred, it appears that additional as yet undetermined factors play a role in allowing continued growth of the fungus.     

Energy use by the mountain pine beetle (Coleoptera: Curculionidae: Scolytinae) for dispersal by flight

The mountain pine beetle Dendroctonus ponderosae Hopkins is a major native pest of Pinus Linnaeus (Pinaceae) in western North America. Host colonization by the mountain pine beetle is associated with an obligatory dispersal phase, during which beetles fly in search of a suitable host. Mountain pine beetles use stored energy from feeding in the natal habitat to power flight before host colonization and brood production. Lipids fuel mountain pine beetle flight, although it is not known whether other energy sources are also used during flight. In the present study, we compare the level of energy substrates, proteins, carbohydrates and lipids of individual mountain pine beetles flown on flight mills with unflown control beetles. We use a colorimetric method to measure the entire metabolite content of each individual beetle. The present study reveals that mountain pine beetles are composed of more protein and lipid than carbohydrate. Both female and male mountain pine beetles use lipids and carbohydrates as energy sources during flight. There is variation between sexes, however, in the energy substrates used for flight. Male mountain pine beetles use protein, in addition to lipids and carbohydrates, to fuel flight, whereas protein content is not different between flown and control females.     

Spore wall traits of ectomycorrhizal and saprotrophic agarics may mirror their distinct lifestyles

Although fungal spores are tiny compared to plant seeds, their morphological variability is enormous, which points toward selective forces. We investigated the frequency of ornamentation, thick walls, pigmentation and germ pores of spores of ectomycorrhizal and saprotrophic agarics. We hypothesised that these traits are shaped by the needs of these distinct lifestyles. All traits showed a strong phylogenetic signal; we therefore applied a phylogenetically informed statistical analysis. There was a significantly higher occurrence of spore ornamentation in ectomycorrhizal agarics and a higher occurrence of thick-walled spores in saprotrophic agarics. The interplay between thick-walled and pigmented spores and the occurrence of germ pores was only significant for saprotrophs. We argue that ornamentation is probably important to ectomycorrhizal fungi for dispersal by soil invertebrates, whereas pigmented thick walls and germ pores would be more advantageous for predominantly r-selected saprotrophic agarics exposed to hazardous environments and in need of quick germination success.     

<Emphasis Type="Italic">Geosmithia</Emphasis> Fungi are Highly Diverse and Consistent Bark Beetle Associates: Evidence from their Community Structure in Temperate Europe

Geosmithia spp. (Ascomycota: Hypocreales) are little-studied, dry-spored fungi that occur in galleries built by many phloeophagous bark beetles. This study mapped the distribution and environmental preferences of Geosmithia species occurring in galleries of temperate European bark beetles. One hundred seven host tree samples of 16 tree species infested with 23 subcortical insect species were collected from across Europe during the years 1997–2005. Over 600 Geosmithia isolates from the beetles were sorted into 17 operational taxonomic units (OTUs) based on their phenotype similarity and phylogeny of internal transcribed spacer (ITS) region of rDNA (ITS1-5.8S-ITS2). The OTUs represent six known species and eight undescribed taxa. Ninety-two samples infested with subcortical insects were characterized by the presence/absence of OTUs and the similarity among the samples was evaluated. Geographically distant populations of the same beetle species host relatively uniform Geosmithia communities across large geographic areas (ranging from southern Bulgaria to the Czech Republic). This suggests effective dispersal of Geosmithia spp. by bark beetles. Clustering of similar samples in ordination analysis is correlated predominantly with the isolation source (bark beetles and their respective feeding plant), but not with their geographical origin. The composition of the Geosmithia OTU community of each bark beetle species depends on the degree of isolation of the species’ niches. Thus, Geosmithia communities associated with regularly co-occurring bark beetle species are highly similar. The similarity decreases with decreasing frequency of beetle species’ co-occurrence, a pattern resembling that of entomochoric ophiostomatoid fungi. These findings suggest that: 1) communities of Geosmithia spp. are vector-specific; 2) at least in some cases, the association between Geosmithia OTUs and bark beetles may have been very stable and symbioses are likely to be a fundamental factor in the speciation of Geosmithia fungi; and 3) that even nonsticky spores of Geosmithia are suitable for maintaining an insect–fungus association, contrary to previous hypotheses. An erratum to this article can be found at     

The effect of sunlight on allergen release from spores of the fungus Alternaria

Airborne fungal spores are known carriers of allergen. Correlations between spore counts and allergen concentrations are poor. It is known that germination increases allergen release, implicating spore viability as a determinant of allergen release. During aerial dispersal, spores can be exposed to prolonged periods of ultraviolet (UV) light which can reduce viability of spores. We examined the relation between spore viability and allergen release in two experiments: firstly spores from culture were treated with a UV wavelength of 254?nm (not present in sunlight reaching the earth's surface) or autoclaved, and secondly, spores were exposed to simulated sunlight over three days. In both studies viability was measured (by germination on agar and by metabolic activity with nitro-blue tetrazolium vital stain) and allergen release by the Halogen immunoassay. The UV light reduced the proportion of spores able to germinate but did not affect metabolic activity or allergen release. Autoclaving reduced the proportion of spores releasing allergen by half (p<0.0001). Three days' exposure to simulated sunlight correlated negatively with spore germination and metabolic activity (p<0.0001), but did not affect allergen release (p=0.799). In conclusion, simulated sunlight reduced the metabolic activity and germinability of spores however the proportion releasing allergen remained unaffected. These findings suggest that spore counts may reflect allergen concentrations in the air if spores are dead or dormant. The contribution of viable spores to concentrations of airborne allergen, as well as the role of germination in allergen delivery to the respiratory tract, remains to be resolved.