Migratory moths as dispersal vectors of an introduced plant-pathogenic fungus in Japan

The plant-pathogenic fungus Claviceps paspali infects florets of the dallisgrass Paspalum dilatatum and induces the plant to produce honeydew (containing massive amounts of conidia), which in turn attracts insects for dispersal of the fungal spores. In Japan, the association between C. paspali and its host plant is common, although both P. dilatatum and C. paspali are introduced species. To determine the dispersal agents of the introduced C. paspali, we examined which insects sapped the P. dilatatum honeydew produced by C. paspali. The study was conducted from September to October 2003 in central Japan. Adults of 48 moth species and two lacewing species visited infected spikelets of P. dilatatum and sapped the honeydew at night. The dominant moths, which carried C. paspali conidia on their proboscises, migrate long distances every year. Therefore, migratory moths may transmit C. paspali spores from diseased to healthy host plants and may have spread C. paspali to other areas in Japan where C. paspali did not previously exist.     

Synchronisation of adult activity of the archaic moth, <Emphasis Type="Italic">Micropterix calthella</Emphasis> L. (Lepidoptera,Micropterigidae), with anthesis of sedges (<Emphasis Type="Italic">Carex</Emphasis> spp., Cyperaceae) in an ancient wood

Micropterix calthella L. (Micropterigidae) is a small, day-flying moth from the basal-most extant lineage of the Lepidoptera. The species name reflects its conspicuous presence on Caltha palustris L. (Ranunculaceae). However, adults also favour sedges (Carex spp., Cyperaceae), on which they gather gregariously to feed on pollen and find mates. In a UK ancient wood, the phenology of eight sedge species together with individual moth and mating pair densities were monitored from 15th April to 8th June 2009. 4841 moth sightings were recorded. Moths on Carex spikes at various developmental stages were compared with null models to test for preference patterns. Approximately 99% of individuals selected Carex spikes where dehiscing anthers were present. The sedge phenology data suggest three distinct periods of pollen production. Overlaying this with the moth data reveals moth phenology strongly linked to a suite of early and mid-season woodland sedges. Of the twenty-eight other angiosperm species (seventeen families) in flower, only Ranunculus ficaria L. (Ranunculaceae) and R. repens L. attracted moths. Adult moths kept in captivity on potted Carex flacca Schreb. for 10 days laid eggs at the plant-soil interface. When C. flacca pollen production ceased, surviving adults were moved onto freshly dehiscing anthers of potted C. pallescens L., where they survived a further 14 days. Soil-dwelling first instar larvae were observed to consume C. sylvatica Huds leaves. In a choice experiment, larvae were significantly more likely to consume C. sylvatica than Stellaria media (L.) Vill. (Caryophyllaceae) leaf material (previously noted to be favoured by larvae). Synchrony between adult moths and Carex spp., and the use of Carex by both adults and larvae, suggests sedges may be host plants for M. calthella in lowland ancient woodlands.     

Gelechiidae moths are capable of chemically dissolving the pollen of their host plants: first documented sporopollenin breakdown by an animal

Background

Many insects feed on pollen surface lipids and contents accessible through the germination pores. Pollen walls, however, are not broken down because they consist of sporopollenin and are highly resistant to physical and enzymatic damage. Here we report that certain Microlepidoptera chemically dissolve pollen grains with exudates from their mouthparts.

Methodology/Principal Findings

Field observations and experiments in tropical China revealed that two species of Deltophora (Gelechioidea) are the exclusive pollinators of two species of Phyllanthus (Phyllanthaceae) on which their larvae develop and from which the adults take pollen and nectar. DNA sequences placed the moths and plants phylogenetically and confirmed that larvae were those of the pollinating moths; molecular clock dating suggests that the moth clade is younger than the plant clade. Captive moths with pollen on their mouthparts after 2-3 days of starvation no longer carried intact grains, and SEM photographs showed exine fragments on their proboscises. GC-MS revealed cis-β-ocimene as the dominant volatile in leaves and flowers, but GC-MS analyses of proboscis extracts failed to reveal an obvious sporopollenin-dissolving compound. A candidate is ethanolamine, which occurs in insect hemolymphs and is used to dissolve sporopollenin by palynologists.

Conclusions/Significance

This is the first report of any insect and indeed any animal chemically dissolving pollen.     

Alfalfa cyclitols in the honeydew of an aphid

The free cyclitols pinitol, ononitol and myo-inositol occur in the honeydew (excreta) of pea aphids (Acyrthosiphon pisum) which feed on pea aphid-susceptible alfalfa (Medicago sativa cv Caliverde). These cyclitols also occur in the leaves and stems of alfalfa. Aphids were incapable of de novo synthesis of these cyclitols. Honeydew production by the pea aphid results from ingesting phloem-sap, so the occurrence of cyclitols in honeydew results from their translocation in the phloem. The relatively high content of myo-inositol in honeydew indicates that it is selectively translocated. The most abundant alfalfa cyclitol, pinitol, had no effect on aphid feeding behavior at concentrations up to 1% (w/v; artificial diet).     

Temporal variation in different life stages of moths (Lepidoptera) from a southwestern temperate forest of Korea: A preliminary study

Two study sites in a temperate forest in Mt. Seungdal-san, Muan, Jeonnam in southwestern Korea were selected for the collection of caterpillars and adult moths (Lepidoptera). Here, we determined (1) the characteristics of moth fauna based on lepidopteran larvae and adults, and (2) the differences in temporal variation between these two developmental stages. In addition, we investigated the life history of moth species collected at the surveyed sites. Of the 206 caterpillars collected, 17 moth species from 9 families were successfully reared. A total of 342 adult moth species and 2108 individuals from 15 families were collected. Twenty-two plants were identified as host plants of 188 caterpillars. Two tree species, Prunus serrulata var. spontanea and Quercus serrata, were widely distributed in the study sites. Leaf water content (%) of Quercus serrata and Carpinus laxiflorawas the highest in June, whereas the leaf water content of Platycarya strobilacea was the highest in August. We postulated that many of the variables in the temperate forest, such as host plant availability, parasitoids, disease, and weather, affected the lepidopteran caterpillar populations. There were differences in species composition among the sampling methods which suggest the need for diverse methods to uncover total biodiversity. However, it should be noted that a long term and well-planned study with efficient rearing of caterpillars is needed to better understand these correlations.     

Honeydew feeding increased the longevity of two egg parasitoids of the pine processionary moth

The longevity of a generalist (Ooencyrtus pityocampae) and a specialist (Baryscapus servadeii) egg parasitoid of the pine processionary moth (Thau‐metopoea pityocampa) was compared under laboratory feeding conditions including water and honeydew from aphid species growing on maritime pine (Pinus pinaster) or pedunculate oak (Quercus robur). The longevity of both parasitoid species increased when specimens were fed with honeydew. This increase was larger for the generalist (3.7, 32.0 and 38.0 days) than for the specialist (3.0, 23.3 and 21.5 days) parasitoid species when fed with water, oak and pine aphid honeydew respectively. The phenology of the specialist species B. servadeii is well‐adapted with its host availability with or without food supply. The generalist species O. pityocampae could overlap its host emergence curve during 14.0–20.0 days when fed with oak and pine aphid honeydew respectively, vs. no overlap when no supplementary food was provided. Analysis of honeydew composition indicated that sugars and amino acids may have distinct effects on parasitoid longevity.     

Stable isotopes of Lithosiini and lichens in Hong Kong show the biodindicator potential of lichenivorous moths

Urban landscapes provide unique environments for a wide variety of plants and animals, but their suitability may be limited by anthropogenic impacts such as pollution. We examined the potential utility of lichen and lichen-feeding moths as biodindicators of air pollution in Hong Kong by comparing carbon (C) and nitrogen (N) stable isotope values in lichens, lichenivorous and non-lichenivorous moths (Lepidoptera: Erebidae) and a moth outgroup (Lepidoptera: Geometridae). Our results show that stable isotope values for C and N were similar for lichens and lichen feeding moths, while non-lichen feeding moths formed a distinct group. In addition, we found consistent δ¹³C and δ¹⁵N values across moth body parts, indicating that any portion of the specimen is suitable for isotopic fingerprinting. Our results highlight that lichen feeding moths may be useful for integrating signals of atmospheric nitrogen pollution and could therefore have utility in monitoring and quantifying air quality over time and space.     

Contrasting patterns of vertical stratification in two moth families in a Costa Rican lowland rain forest

The vertical stratification of two species-rich moth families (Lepidoptera: Arctiidae, Geometridae) was analysed in a lowland rain forest in Costa Rica. Moths were trapped with automatic 8 W ultraviolet light traps at three sites in the understorey and canopy of a primary forest at the La Selva Biological Station (10.4° N, 84.0° W). A total of 846 arctiid moths (148 species) and 946 geometrid moths (140 species) were analysed. Species richness and diversity of arctiid moths was significantly lower in the understorey than in the canopy (Fisher's alpha: 24 vs. 49) whereas geometrid moths showed an inverse pattern (Fisher's alpha: 44 vs. 27). This resulted in an overall increase in the proportion of conspicuously coloured species towards the canopy. Moth ensembles were clearly separated in multidimensional scaling ordinations, and differed significantly in their faunal composition and dominance between the strata. The available host plant data suggest that the flight height of moths was determined by larval resource availability. Examples include understorey flyers such as the geometrid genus Eois feeding on Piper, and canopy flyers such as the arctiid moth genera Aclytia, Macrocneme and Poliopastea which feed on lianas.     

The nutritional quality of phloem sap utilized by natural aphid populations

Abstract.

• 1 The amino acid content of phloem exudates from leaves and of aphid honeydew were adopted as indices of the nutritional quality of phloem sap for aphids. Four plant species and associated leaf-dwelling aphids were investigated: the sycamore Acer pseudoplanatus and sycamore aphid Drepanosiphum platanoides; Prunus domestica (victoria plum) and the mealy plum aphid Hyalopterus pruni; and the spindle tree Euonymus europaeus and broad-bean Vicia faba, both hosts of the black bean aphid Aphis fabae.
• 2 The concentration of amino acids in the phloem exudates varied with: (a) plant species (greater in the herb Vicia than in the tree species), (b) season (greater in the autumn than summer for Acer and Euonymus), and (c) position (greater in flush leaves than mature leaves of Prunus).
• 3 For Acer and Prunus and their aphids, the concentration of amino acids in phloem exudates was significantly correlated with the amino acid content of the aphid honeydew.
• 4 The amino acids in all exudates and honeydew were dominated by non-essential amino acids (glutamic acid, glutamine, asparagine or serine, varying with season and between plant species). The sole major discrepancy between the amino acid profiles of exudates and honeydew was the production of asparagine-rich honeydew by aphids feeding on leaves, whose exudates were dominated by glutamic acid; this applied to both H.pruni on mature Prunus leaves and Drepanosiphum platanoides on summer-leaves of Acer.
• 5 It is suggested that EDTA-exudation may be a useful technique to study nutritional correlates of aphid life cycles, e.g. the time of migration between primary and secondary plant hosts.

     

Effective pollinia transfer by settling moths’ legs in an orchid Habenaria aitchisonii

A great diversity of flower morphology in orchids has long been thought to be selected by diverse pollinators. Habenaria Willd. (Orchidaceae) species are generally characterized by long nectar spurs and pollinated by long‐tongued insects (Lepidoptera), the mechanical fit between the spur and pollinator proboscis length being supposedly caused by “arms race” reciprocal selection. Here, we report that flowers of Habenaria aitchisonii Rchb. f. with nectar spurs (approximately 9 mm) were pollinated by three species of settling noctuid moths whose proboscises varied in length from 10 to 16 mm. When a settling moth crawled on the spikes and probed the flowers for nectar, pollinia were placed on the moths’ legs rather than on other body parts. Our 5‐year survey of pollinia movement and 3‐year supplemental pollination experiments indicated that fruit and seed production in this orchid were not often pollen‐limited at flower level. In a natural population in Shangri‐La, Southwest China, the proportions of pollinia removal and deposition on stigmas by moth legs were 93.8% and 83.5%, respectively. This finding of efficient pollen transfer by the pollinators’ legs in H. aitchisonii adds a new example of diverse pollinia placement on pollinators (here settling moths) in the Orchidaceae.     

An experience of rearing some hawk moths (Lepidoptera,Sphingidae) on artificial diets

A method for rearing five hawk moth species, namely Acherontia atropos (Linnaeus, 1758), A. lachesis (Fabricius, 1798), Agrius convolvuli (Linnaeus, 1758), Daphnis nerii (Linnaeus, 1758), and Hyles livornica (Esper, 1780) (Lepidoptera, Sphingidae) on artificial diets is described. Two recipes of these artificial rearing media are proposed. Special attention is given to maintenance of adult moths in captivity and raising immature stages.     

Honeydew composition and its effect on life-history parameters of hyperparasitoids

1. Diets that maximise life span often differ from diets that maximise reproduction. Animals have therefore evolved advanced foraging strategies to acquire optimal nutrition and maximise their fitness. The free-living adult females of parasitoid wasps (Hymenoptera) need to balance their search for hosts to reproduce and for carbohydrate resources to feed. 2. Honeydew, excreted by phloem-feeding insects, presents a widely available carbohydrate source in nature that can benefit natural enemies of honeydew-producing insects. However, the effects of variation in honeydew on organisms in the fourth trophic level, such as hyperparasitoids, are not yet understood. 3. This study examined how five different honeydew types influence longevity and fecundity of four hyperparasitoid taxa. Asaphes spp. (Pteromalidae) and Dendrocerus spp. (Megaspilidae) are secondary parasitoids of aphid parasitoids and are thus associated with honeydew-producing insects. Gelis agilis and Acrolyta nens (both Ichneumonidae) are secondary parasitoids of species that do not use honeydew-producing hosts. 4. Most honeydew types had a positive or neutral effect on life span and fecundity of hyperparasitoids compared with controls without honeydew, although negative effects were also found for both aphid hyperparasitoids. Honeydew produced by aphids feeding on sweet pepper plants was most beneficial for all hyperparasitoid taxa, which can partially be explained by the high amount of honeydew, but also by the composition of dietary sugars in these honeydew types. 5. The findings of this study underline the value of aphid honeydew as a carbohydrate resource for fourth-trophic-level organisms, not only those associated with honeydew-producing insects but also ‘interlopers’ without such a natural association.     

House Fly (Musca domestica L.) Attraction to Insect Honeydew

House flies are of major concern as vectors of food-borne pathogens to food crops. House flies are common pests on cattle feedlots and dairies, where they develop in and feed on animal waste. By contacting animal waste, house flies can acquire human pathogenic bacteria such as Escherichia coli and Salmonella spp., in addition to other bacteria, viruses, or parasites that may infect humans and animals. The subsequent dispersal of house flies from animal facilities to nearby agricultural fields containing food crops may lead to pre-harvest food contamination with these pathogens. We hypothesized that odors from honeydew, the sugary excreta produced by sucking insects feeding on crops, or molds and fungi growing on honeydew, may attract house flies, thereby increasing the risk of food crop contamination. House fly attraction to honeydew-contaminated plant material was evaluated using a laboratory bioassay. House flies were attracted to the following plant-pest-honeydew combinations: citrus mealybug on squash fruit, pea aphid on faba bean plants, whitefly on navel orange and grapefruit leaves, and combined citrus mealybug and cottony cushion scale on mandarin orange leaves. House flies were not attracted to field-collected samples of lerp psyllids on eucalyptus plants or aphids on crepe myrtle leaves. Fungi associated with field-collected honeydews were isolated and identified for further study as possible emitters of volatiles attractive to house flies. Two fungal species, Aureobasidium pullulans and Cladosporium cladosporioides, were repeatedly isolated from field-collected honeydew samples. Both fungal species were grown in potato dextrose enrichment broth and house fly attraction to volatiles from these fungal cultures was evaluated. House flies were attracted to odors from A. pullulans cultures but not to those of C. cladosporioides. Identification of specific honeydew odors that are attractive to house flies could be valuable for the development of improved house fly baits for management of this pest species.     

Stored-product insects associated with eight feed mills in the midwestern United States

Commercial food- and pheromone-baited pitfall traps and pheromone-baited sticky traps were used during 2003 to survey stored-product insect adults in eight participating feed mills in the midwestern United States. Across the eight feed mills, 27 species of beetles (Coleoptera) and three species of moths (Lepidoptera) were captured in commercial traps. The red flour beetle, Tribolium castaneum (Herbst), was the most abundant insect species captured inside the eight mills. The warehouse beetle, Trogoderma variabile (Ballion), was the most abundant insect species outside the mill and in the mill load-out area. The Indianmeal moth, Plodia interpunctella (Hübner), was the most abundant moth species inside the mill and in the mill receiving area. The Simpson's index of species diversity among mills ranged from 0.39 (low diversity) to 0.81 (high diversity). The types of species found among mills were different, as indicated by a Morisita's index of <0.7, for the majority of mills. The differences in the types and numbers of insect species captured inside, outside, in receiving, and in load-out areas could be related to differences in the types of animal feeds produced and the degree of sanitation and pest management practiced.     

The secret pollinators: an overview of moth pollination with a focus on Europe and North America

Pollination is a crucial plant–animal interaction in ecosystems, and moths (Lepidoptera) are a widespread and species-rich group of flower visitors. In this article, plant and moth species connected via pollination interactions were identified from the literature, and information on the relevance of moth pollination in various ecosystems, including agro-ecosystems, was compiled, particularly for Europe and North America. Overall, 227 moth–flower pollination interactions were found, including certain specialized relationships between plants and pollinating seed predators. Most of the interactions could be attributed to the moth families Noctuidae (90 interactions, 56 species) and Sphingidae (85 interactions, 32 species), and to the plant families Orchidaceae (109 interactions, 22 species) and Caryophyllaceae (59 interactions, 16 species). Limited information is available on the role of moth pollination in natural ecosystems (7 studies). In temperate agro-ecosystems, moths are most likely not essential to crop pollination, but they can contribute to the pollination of non-crop plants, which are crucial to maintaining biodiversity in these ecosystems. In general, the role of moths as pollinators appears to be underestimated because only a few studies on moth pollination are available, and long-term, ecosystem-scale research is necessary to address temporal fluctuations in their abundance and community composition.     

Are Honeydew/Sap-feeding Butterflies (Lepidoptera: Rhopalocera) Affected by Particulate Air-pollution?

Air-pollution has frequently been suggested as a cause of the decline of some butterfly species: a suggestion based mainly on lowered species richness close to industrial areas in Europe. There have been frequent calls, in vain, for research on the direct effect of air-pollution on Lepidoptera, recent research being confined to the indirect role via climate change.Based on studies of the species loss and natural recolonisation of Epping Forest (a large woodland area close to London, UK) I suggest that those species feeding as adults on sugar-rich fluids direct from the surface of trees or leaves (i.e. aphid honeydew on leaves or sap-runs on tree-trunks) were affected by particulate air-pollution.Species loss was high during the period of maximum smoke emissions. Since 1950 five species have recolonised naturally, of which four are honeydew feeders. It is possible that high levels of particulate air-pollution caused the extinction of butterflies feeding on honeydew from polluted leaves. Predictions are made which will allow this hypothesis to be tested.     

Malaria Mosquitoes Host-Locate and Feed upon Caterpillars

Adult female mosquitoes need blood to develop their eggs and both sexes use nectar and honeydew as carbohydrate resources for flight, survival and to enhance reproduction. However, there are also a few reports in the literature of mosquitoes feeding on haemolymph of soft-bodied insects such as caterpillars. The frequency and significance of this entomophagous behavior is not well understood, but is thought to be a vestige of ancestral feeding behavior or an opportunistic behavior that has evolved over time. In our current paper we investigated the extent to which the malaria mosquito, Anopheles stephensi, is attracted to, and can successfully feed on, larvae of two common moth species, Manduca sexta and Heliothis subflexa. Using y-tube olfactometer assays we found that female An. stephensi readily flew upwind to and landed on the caterpillars of both moth species. The nature of the volatile cues used in host location remains unclear but respirometer studies suggest a possible role of CO₂. Laboratory cage assays further showed that the female mosquitoes were able to actively feed on moth larvae and gain sufficient nutritional benefit to influence survival. The extent to which such an opportunistic behavior occurs in the field has yet to be explored but our results suggest that this haemolymph feeding behavior could play a role in malaria mosquito life history and could provide a novel mechanism for horizontal transmission of pathogens and other micro-organisms between hosts.     

Females of Cotesia vestalis,a parasitoid of diamondback moth larvae,learn to recognise cues from aphid‐infested plants to exploit honeydew

1. To maximise their reproductive success, the females of most parasitoids must not only forage for hosts but must also find suitable food sources. These may be nectar and pollen from plants, heamolymph from hosts and/or honeydew from homopterous insects such as aphids. 2. Under laboratory conditions, females of Cotesia vestalis, a larval parasitoid of the diamondback moth (Plutella xylostella) which does not feed on host blood, survived significantly longer when held with cruciferous plants infested with non‐host green peach aphids (Myzus persicae) than when held with only uninfested plants. 3. Naïve parasitoids exhibited no preference between aphid‐infested and uninfested plants in a dual‐choice test, but those that had been previously fed aphid honeydew significantly preferred aphid‐infested plants to uninfested ones. 4. These results suggest that parasitoids that do not use aphids as hosts have the potential ability to learn cues from aphid‐infested plants when foraging for food. This flexible foraging behaviour could allow them to increase their lifetime reproductive success.     

The influence of aphid-produced honeydew on parasitoid fitness and nutritional state: A comparative study

Honeydew is a sugar-rich resource excreted by many hemipteran species and is a key food source for other insect species such as ants and parasitoid wasps. Here, we evaluated the nutritional value of 14 honeydews excreted by 13 aphid species for the generalist aphid parasitoid Lysiphlebus testaceipes to test a series of hypotheses concerning variation in the nutritional value of honeydew. There was a positive correlation between the body sugar content of honeydew-fed parasitoids and their longevity. This information is valuable for biological control researchers because it demonstrates that the nutritional state of honeydew-fed parasitoids in the wild can indicate their fitness, independently of the honeydew source they have fed on.Although the carbohydrate content and longevity of L. testaceipes differed greatly among the different honeydews, we did not find a significant effect of aphid or host plant phylogeny on these traits. This result suggests that honeydew is evolutionarily labile and may be particularly subject to ecological selection pressures. This becomes apparent when considering host aphid suitability: Schizaphis graminum, one of the most suitable and commonly used hosts of L. testaceipes, produced honeydew of the poorest quality for the parasitoid whereas Uroleucon sonchi, one of the few aphids tested that cannot be parasitized by L. testaceipes, excreted the honeydew with the highest nutritional value. These data are consistent with the hypothesis that hemipterans are subject to selection pressure to minimize honeydew quality for the parasitoids that attack them.     

Detection of Ophiocordyceps sinensis in the roots of plants in alpine meadows by nested-touchdown polymerase chain reaction

Ophiocordyceps sinensis, one of the most important income sources of rural Tibetan families, is an entomopathogenic fungus that parasitizes the ghost moth Thitarodes larvae, which live in alpine meadows on the Tibetan Plateau and in the Himalayas. The annual yield of O. sinensis has gradually declined in recent years. However, there is no effective method to sustain or increase the yield of O. sinensis artificially because the life cycle of the O. sinensis anamorph remains unclear. Here we detected O. sinensis in alpine plant roots by nested-touchdown polymerase chain reaction (PCR). Forty-two alpine plant species were screened. The roots from 23 alpine plant species (54.76 %) tested positive including 13 families and 18 genera. The detection results indicate that O. sinensis is present in the plant roots during the anamorph life cycle, to deal with harsh conditions in alpine habitats and have an increased opportunity to infect the larvae. The finding provides new information regarding the biology and ecology of O. sinensis that may be used to sustain this valuable resource.