Comparison of stimulus-response (V-log I) functions in five types of lepidopteran compound eyes (46 species)

Summary Stimulus intensity-response relations (V-log I curves) were electrophysiologically (ERG) determined for the compound eyes of 46 lepidopteran species belonging to five different groups: butterflies (22 species), hesperids (3 species), diurnal sphingids (2 species), diurnal moths (3 species) and nocturnal moths (16 species). The V-log I curves were fitted to the Naka and Rushton equation, in whichn represents the slope of the linear part of each curve. The slopes so determined range fromn=0.35 (the shallowest slope) in nocturnal moths with the greatest dynamic range ton=0.54 (the steepest slope) in diurnal moths andn=0.53 in butterflies both of which have narrow dynamic range. Hesperids (n=0.41) and diurnal sphingids (n=0.38) have intermediate values between butterflies and nocturnal moths.The ratio of rhabdom to retinula volume is significantly higher in nocturnal moths (70–75%), however, those of butterflies and of diurnal moths are very small (2–5%), and hesperids and diurnal sphingids show intermediate ratio (ca. 25%).The slopes of V-log I curves are inversely proportional to the ratio of rhabdom to retinula volume in the various eye types. In all groups except diurnal moths, the light intensities which produce maximal and saturated responses are nearly the same, therefore the nocturnal moths which have the lowest threshold to light increase their sensitivity to dim light mainly by decreasing the slopes of V-log I curves.     

Are butterflies and moths suitable ecological indicator systems for restoration measures of semi-natural calcareous grassland habitats?

The selection of suitable ecological indicator groups is of great importance for environmental assessments. To test and compare two such groups, we performed transect walks of butterflies and light traps of moths at eight sample localities in the Carinthian Alps. All of them were conducted with identical methods in the years 2002 and 2004 allowing the evaluation of the response on the conservation measures performed on five of the eight sites in late 2002. We recorded a total of 2346 butterflies (including Zygaenidae and Sesiidae) representing 83 species and 7025 moths of 534 species. 150 of these species were listed in the Red Data Book of Carinthia. In general, butterflies increased from 2002 to 2004 while moths declined. The highest increase rates of butterflies were obtained for the numbers of individuals of calcareous grassland specialists at the conservation sites, while their numbers were unchanged at the control sites. Similar trend differences between conservation and control sites were obtained for the Red Data Book butterfly species. On the contrary, the development of moth individuals was more positive at the control than the conservation sites for calcareous grassland specialists (only macro-moths) and species of the Red Data Book. However, change rates of species numbers were positively correlated between butterflies and moths. Principal Component Analysis revealed strong differences between the different sites, but mostly consistent results for butterflies and moths; however, stronger differences between years were only detected for some of the conservation sites for the butterfly communities. Our results show that butterflies as well as moths are suitable ecological indicator groups, but they do not yield identical results. Thus, butterflies are more suitable for the analysis of open habitats, whereas moths are suitable for open and forested habitats as well. Furthermore, butterflies might be a more sensitive indicator group than moths for the short-term detection of conservation measures, especially for the restoration of open habitat types.     

Relative contributions of local and regional factors to species richness and total density of butterflies and moths in semi-natural grasslands

Metapopulation theory predicts that species richness and total population density of habitat specialists increase with increasing area and regional connectivity of the habitat. To test these predictions, we examined the relative contributions of habitat patch area, connectivity of the regional habitat network and local habitat quality to species richness and total density of butterflies and day-active moths inhabiting semi-natural grasslands. We studied butterflies and moths in 48 replicate landscapes situated in southwest Finland, including a focal patch and the surrounding network of other semi-natural grasslands within a radius of 1.5 km from the focal patch. By applying the method of hierarchical partitioning, which can distinguish between independent and joint contributions of individual explanatory variables, we observed that variables of the local habitat quality (e.g. mean vegetation height and nectar plant abundance) generally showed the highest independent effect on species richness and total density of butterflies and moths. Habitat area did not show a significant independent contribution to species richness and total density of butterflies and moths. The effect of habitat connectivity was observed only for total density of the declining butterflies and moths. These observations indicate that the local habitat quality is of foremost importance in explaining variation in species richness and total density of butterflies and moths. In addition, declining butterflies and moths have larger populations in well-connected networks of semi-natural grasslands. Our results suggest that, while it is crucial to maintain high-quality habitats by management, with limited resources it would be appropriate to concentrate grassland management and restoration to areas with well-connected grassland networks in which the declining species currently have their strongest populations. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

鳞翅目若干迁飞昆虫翅形特征分析(英文)

对鳞翅目蛾类 2科 42种和蝶类 7科 31种昆虫的翅形进行数值分析。结果表明 ,无论是蛾类还是蝶类 ,迁飞昆虫前翅形状均具有区别于非迁飞昆虫的共同特征 ,即前翅相对窄长 ,前缘较平直 ;然而与不同的翅振模式相适应 ,蛾类与蝶类迁飞昆虫的翅形特征又有所不同 :蛾类迁飞昆虫翅外侧较宽阔 ;蝶类迁飞昆虫翅外侧较窄小。     

ANALYSIS OF WING‐SHAPE CHARACTERITICS OF MIGRATORY LEPIDOPTEROUS INSECTS*

Abstract Morphological characteristics of the forewings of 42 species of moths and 31 species of butterflies were comparatively analyzed with special reference to their migration ability. The curvature values of costal margin of the forewings revealed that the migratory moths and butterflies have relatively narrower forewings with straighter costal margin as compared with respective non‐migratory species. The posterior area of forewings was wider in the migratory moths and narrower in the migratory butterflies than that of respective non‐migratory species.     

The Evolution and Expression of the Moth Visual Opsin Family

Because visual genes likely evolved in response to their ambient photic environment, the dichotomy between closely related nocturnal moths and diurnal butterflies forms an ideal basis for investigating their evolution. To investigate whether the visual genes of moths are associated with nocturnal dim-light environments or not, we cloned long-wavelength (R), blue (B) and ultraviolet (UV) opsin genes from 12 species of wild-captured moths and examined their evolutionary functions. Strong purifying selection appeared to constrain the functions of the genes. Dark-treatment altered the levels of mRNA expression in Helicoverpa armigera such that R and UV opsins were up-regulated after dark-treatment, the latter faster than the former. In contrast, B opsins were not significantly up-regulated. Diel changes of opsin mRNA levels in both wild-captured and lab-reared individuals showed no significant fluctuation within the same group. However, the former group had significantly elevated levels of expression compared with the latter. Consequently, environmental conditions appeared to affect the patterns of expression. These findings and the proportional expression of opsins suggested that moths potentially possessed color vision and the visual system played a more important role in the ecology of moths than previously appreciated. This aspect did not differ much from that of diurnal butterflies.     

Diel behavior in moths and butterflies: a synthesis of data illuminates the evolution of temporal activity

Lepidoptera (butterflies and moths) are one of the most taxonomically diverse insect orders with nearly 160,000 described species. They have been studied extensively for centuries and are found on nearly all continents and in many environments. It is often assumed that adult butterflies are strictly diurnal and adult moths are strictly nocturnal, but there are many exceptions. Despite the broad interest in butterflies and moths, a comprehensive review of diel (day-night) activity has not been conducted. Here, we synthesize existing data on diel activity in Lepidoptera, trace its evolutionary history on a phylogeny, and show where gaps lie in our knowledge. Diurnality was likely the ancestral condition in Lepidoptera, the ancestral heteroneuran was likely nocturnal, and more than 40 transitions to diurnality subsequently occurred. Using species diversity estimates across the order, we predict that roughly 75-85% of Lepidoptera are nocturnal. We also define the three frequently used terms for activity in animals (diurnal, nocturnal, crepuscular), and show that literature on the activity of micro-moths is significantly lacking. Ecological factors leading to nocturnality/diurnality is a compelling area of research and should be the focus of future studies.     

Moths behaving like butterflies. Evolutionary loss of long range attractant pheromones in castniid moths: a Paysandisia archon model

Background

In the course of evolution butterflies and moths developed two different reproductive behaviors. Whereas butterflies rely on visual stimuli for mate location, moths use the ‘female calling plus male seduction’ system, in which females release long-range sex pheromones to attract conspecific males. There are few exceptions from this pattern but in all cases known female moths possess sex pheromone glands which apparently have been lost in female butterflies. In the day-flying moth family Castniidae (“butterfly-moths”), which includes some important crop pests, no pheromones have been found so far.

Methodology/Principal Findings

Using a multidisciplinary approach we described the steps involved in the courtship of P. archon, showing that visual cues are the only ones used for mate location; showed that the morphology and fine structure of the antennae of this moth are strikingly similar to those of butterflies, with male sensilla apparently not suited to detect female-released long range pheromones; showed that its females lack pheromone-producing glands, and identified three compounds as putative male sex pheromone (MSP) components of P. archon, released from the proximal halves of male forewings and hindwings.

Conclusions/Significance

This study provides evidence for the first time in Lepidoptera that females of a moth do not produce any pheromone to attract males, and that mate location is achieved only visually by patrolling males, which may release a pheromone at short distance, putatively a mixture of Z,E-farnesal, E,E-farnesal, and (E,Z)-2,13-octadecadienol. The outlined behavior, long thought to be unique to butterflies, is likely to be widespread in Castniidae implying a novel, unparalleled butterfly-like reproductive behavior in moths. This will also have practical implications in applied entomology since it signifies that the monitoring/control of castniid pests should not be based on the use of female-produced pheromones, as it is usually done in many moths.     

Different responses of plants and herbivore insects to a gradient of vegetation height: an indicator of the vertebrate grazing intensity and successional age

Empirical studies have suggested that species richness of grassland insects usually decreases under grazing management. By contrast, grazing has been shown to increase the species density and richness of vascular plants, especially on productive soils. In order to test the suggested differences in response to management between plants and insects, we simultaneously studied species richness of vascular plants and their insect herbivores, butterflies and moths, in 68 semi-natural grasslands with varying grazing intensity and frequency in SW Finland. Species richness of plants and insects was for the first time related to a quantitative measure of disturbance intensity and successional age, mean vegetation height, by using generalized additive models (GAM). The effects of soil nutrients on vegetation height were accounted for by using phosphorus concentration as a productivity surrogate.
The results showed that species richness of butterflies and moths peaked in taller vegetation compared with vascular plants, corresponding to a lower disturbance intensity and increasing time since abandonment. These patterns are discussed in the light of two hypotheses, the "structural diversity hypothesis" and "dynamic equilibrium model" of Huston, both suggesting a weaker disturbance tolerance of insects compared with plants. Butterflies and moths which are specialists in their larval host-plant use (monophagous and oligophagous species) preferred lower vegetation (higher disturbances) compared with generalists (polyphagous species), as predicted by Huston's model. This difference indicates a stronger relationship with plant species richness for specialist than for generalist butterflies and moths. Our results support the application of regionally and temporally varying grazing intensities in grassland conservation management.     

Odour maps in the brain of butterflies with divergent host-plant preferences

Butterflies are believed to use mainly visual cues when searching for food and oviposition sites despite that their olfactory system is morphologically similar to their nocturnal relatives, the moths. The olfactory ability in butterflies has, however, not been thoroughly investigated. Therefore, we performed the first study of odour representation in the primary olfactory centre, the antennal lobes, of butterflies. Host plant range is highly variable within the butterfly family Nymphalidae, with extreme specialists and wide generalists found even among closely related species. Here we measured odour evoked Ca(2+) activity in the antennal lobes of two nymphalid species with diverging host plant preferences, the specialist Aglais urticae and the generalist Polygonia c-album. The butterflies responded with stimulus-specific combinations of activated glomeruli to single plant-related compounds and to extracts of host and non-host plants. In general, responses were similar between the species. However, the specialist A. urticae responded more specifically to its preferred host plant, stinging nettle, than P. c-album. In addition, we found a species-specific difference both in correlation between responses to two common green leaf volatiles and the sensitivity to these compounds. Our results indicate that these butterflies have the ability to detect and to discriminate between different plant-related odorants.     

Higher mobility of butterflies than moths connected to habitat suitability and body size in a release experiment

Mobility is a key factor determining lepidopteran species responses to environmental change. However, direct multispecies comparisons of mobility are rare and empirical comparisons between butterflies and moths have not been previously conducted. Here, we compared mobility between butterflies and diurnal moths and studied species traits affecting butterfly mobility. We experimentally marked and released 2011 butterfly and 2367 moth individuals belonging to 32 and 28 species, respectively, in a 25 m × 25 m release area within an 11‐ha, 8‐year‐old set‐aside field. Distance moved and emigration rate from the release habitat were recorded by species. The release experiment produced directly comparable mobility data in 18 butterfly and 9 moth species with almost 500 individuals recaptured. Butterflies were found more mobile than geometroid moths in terms of both distance moved (mean 315 m vs. 63 m, respectively) and emigration rate (mean 54% vs. 17%, respectively). Release habitat suitability had a strong effect on emigration rate and distance moved, because butterflies tended to leave the set‐aside, if it was not suitable for breeding. In addition, emigration rate and distance moved increased significantly with increasing body size. When phylogenetic relatedness among species was included in the analyses, the significant effect of body size disappeared, but habitat suitability remained significant for distance moved. The higher mobility of butterflies than geometroid moths can largely be explained by morphological differences, as butterflies are more robust fliers. The important role of release habitat suitability in butterfly mobility was expected, but seems not to have been empirically documented before. The observed positive correlation between butterfly size and mobility is in agreement with our previous findings on butterfly colonization speed in a long‐term set‐aside experiment and recent meta‐analyses on butterfly mobility.     

The Lepidoptera Odorant Binding Protein gene family: Gene gain and loss within the GOBP/PBP complex of moths and butterflies

Butterflies and moths differ significantly in their daily activities: butterflies are diurnal while moths are largely nocturnal or crepuscular. This life history difference is presumably reflected in their sensory biology, and especially the balance between the use of chemical versus visual signals. Odorant Binding Proteins (OBP) are a class of insect proteins, at least some of which are thought to orchestrate the transfer of odor molecules within an olfactory sensillum (olfactory organ), between the air and odor receptor proteins (ORs) on the olfactory neurons. A Lepidoptera specific subclass of OBPs are the GOBPs and PBPs; these were the first OBPs studied and have well documented associations with olfactory sensilla. We have used the available genomes of two moths, Manduca sexta and Bombyx mori, and two butterflies, Danaus plexippus and Heliconius melpomene, to characterize the GOBP/PBP genes, attempting to identify gene orthologs and document specific gene gain and loss. First, we identified the full repertoire of OBPs in the M. sexta genome, and compared these with the full repertoire of OBPs from the other three lepidopteran genomes, the OBPs of Drosophila melanogaster and select OBPs from other Lepidoptera. We also evaluated the tissue specific expression of the M. sexta OBPs using an available RNAseq databases. In the four lepidopteran species, GOBP2 and all PBPs reside in single gene clusters; in two species GOBP1 is documented to be nearby, about 100 kb from the cluster; all GOBP/PBP genes share a common gene structure indicating a common origin. As such, the GOBP/PBP genes form a gene complex. Our findings suggest that (1) the lepidopteran GOBP/PBP complex is a monophyletic lineage with origins deep within Lepidoptera phylogeny, (2) within this lineage PBP gene evolution is much more dynamic than GOBP gene evolution, and (3) butterflies may have lost a PBP gene that plays an important role in moth pheromone detection, correlating with a shift from olfactory (moth) to visual (butterfly) communication, at least regarding long distance mate recognition. These findings will be clarified by additional lepidopteran genomic data, but the observation that moths and butterflies share most of the PBP/GOBP genes suggests that they also share common chemosensory-based behavioral pathways.     

A molecular phylogenetic analysis of the vampire moths and their fruit-piercing relatives (Lepidoptera: Erebidae: Calpinae)

Within butterflies and moths, adult hematophagy is limited to species within the vampire moth genus Calyptra. These moths are placed within the subfamily Calpinae, whose other members are known to exhibit a broad range of feeding behaviors including those that can be considered 'piercers' of fruits or other hosts and 'tear feeders'. Here, we reconstruct a phylogenetic hypothesis of Calpinae using molecular data to test whether hematophagy in Calyptra arose from plant or animal-related behaviors. We use a Bayesian method of ancestral state reconstruction to determine the most likely feeding behaviors for the subtribes and genera within this lineage.     

Comprehensive gene and taxon coverage elucidates radiation patterns in moths and butterflies

Lepidoptera (butterflies and moths) represent one of the most diverse animals groups. Yet, the phylogeny of advanced ditrysian Lepidoptera, accounting for about 99 per cent of lepidopteran species, has remained largely unresolved. We report a rigorous and comprehensive analysis of lepidopteran affinities. We performed phylogenetic analyses of 350 taxa representing nearly 90 per cent of lepidopteran families. We found Ditrysia to be a monophyletic taxon with the clade Tischerioidea + Palaephatoidea being the sister group of it. No support for the monophyly of the proposed major internested ditrysian clades, Apoditrysia, Obtectomera and Macrolepidoptera, was found as currently defined, but each of these is supported with some modification. The monophyly or near-monophyly of most previously identified lepidopteran superfamilies is reinforced, but several species-rich superfamilies were found to be para- or polyphyletic. Butterflies were found to be more closely related to ‘microlepidopteran’ groups of moths rather than the clade Macrolepidoptera, where they have traditionally been placed. There is support for the monophyly of Macrolepidoptera when butterflies and Calliduloidea are excluded. The data suggest that the generally short diverging nodes between major groupings in basal non-tineoid Ditrysia are owing to their rapid radiation, presumably in correlation with the radiation of flowering plants.     

Optimal strategies for insects migrating in the flight boundary layer: mechanisms and consequences

Directed aerial displacement requires that a volant organism'sairspeed exceeds ambient wind speed. For biologically relevantaltitudes, wind speed increases exponentially with increasedheight above the ground. Thus, dispersal of most insects isinfluenced by atmospheric conditions. However, insects thatfly close to the Earth's surface displace within the flightboundary layer where insect airspeeds are relatively high. Overthe past 17 years, we have studied boundary-layer insects byfollowing individuals as they migrate across the Caribbean Seaand the Panama Canal. Although most migrants evade either droughtor cold, nymphalid and pierid butterflies migrate across Panamanear the onset of the rainy season. Dragonflies of the genusPantala migrate in October concurrently with frontal weathersystems. Migrating the furthest and thereby being the most difficultto study, the diurnal moth Urania fulgens migrates between Centraland South America. Migratory butterflies and dragonflies arecapable of directed movement towards a preferred compass directionin variable winds, whereas the moths drift with winds over water.Butterflies orient using both global and local cues. Consistentwith optimal migration theory, butterflies and dragonflies adjusttheir flight speeds in ways that maximize migratory distancetraveled per unit fuel, whereas the moths do not. Moreover,only butterflies adjust their flight speed in relation to endogenousfat reserves. It is likely that these insects use optic flowto gauge their speed and drift, and thus must migrate wheresufficient detail in the Earth's surface is visible to them.The abilities of butterflies and dragonflies to adjust theirairspeed over water indicate sophisticated control and guidancesystems pertaining to migration.     

The male sex pheromone of the butterfly Bicyclus anynana: towards an evolutionary analysis

Background

Female sex pheromones attracting mating partners over long distances are a major determinant of reproductive isolation and speciation in Lepidoptera. Males can also produce sex pheromones but their study, particularly in butterflies, has received little attention. A detailed comparison of sex pheromones in male butterflies with those of female moths would reveal patterns of conservation versus novelty in the associated behaviours, biosynthetic pathways, compounds, scent-releasing structures and receiving systems. Here we assess whether the African butterfly Bicyclus anynana, for which genetic, genomic, phylogenetic, ecological and ethological tools are available, represents a relevant model to contribute to such comparative studies.

Methodology/Principal Findings

Using a multidisciplinary approach, we determined the chemical composition of the male sex pheromone (MSP) in the African butterfly B. anynana, and demonstrated its behavioural activity. First, we identified three compounds forming the presumptive MSP, namely (Z)-9-tetradecenol (Z9-14:OH), hexadecanal (16:Ald ) and 6,10,14-trimethylpentadecan-2-ol (6,10,14-trime-15-2-ol), and produced by the male secondary sexual structures, the androconia. Second, we described the male courtship sequence and found that males with artificially reduced amounts of MSP have a reduced mating success in semi-field conditions. Finally, we could restore the mating success of these males by perfuming them with the synthetic MSP.

Conclusions/Significance

This study provides one of the first integrative analyses of a MSP in butterflies. The toolkit it has developed will enable the investigation of the type of information about male quality that is conveyed by the MSP in intraspecific communication. Interestingly, the chemical structure of B. anynana MSP is similar to some sex pheromones of female moths making a direct comparison of pheromone biosynthesis between male butterflies and female moths relevant to future research. Such a comparison will in turn contribute to understanding the evolution of sex pheromone production and reception in butterflies.     

Phylogenetic studies of ribosomal RNA variation in higher moths and butterflies (Lepidoptera: Ditrysia).

The selection of exemplars has been shown both theoretically and empirically to affect tree topology, but the importance of the number and nature of taxa used to represent higher taxonomic lineages in molecular studies is rarely stressed. In our rRNA study of higher moths and butterflies (Lepidoptera: Ditrysia), the selection of different exemplars and outgroups caused major tree rearrangements. We also examined the effectiveness with which conserved rRNA regions track the diversification of Lepidoptera. Homoplasy is as prevalent at the few variable sites of conserved regions (18E, 18J, 28F) as at the many variable sites of a more rapidly evolving region (28B). Finally, 28B sequence variation differs qualitatively among lepidopteran superfamilies of presumed comparable age, the Papilionoidea (true butterflies) and Noctuoidea (cutworm moths and relatives).     

Habitat resources, remnant vegetation condition and area determine distribution patterns and abundance of butterflies and day-flying moths in a fragmented urban landscape, south-west Western Australia

The creation of cities, towns and farms following European settlement of Australia has fragmented the original vegetation. Many native species that were previously widespread are now found only within isolated remnants of their original habitat. These relictual populations are at increased risk of decline and local extinction, so identifying the factors that determine their persistence is important for ongoing management and conservation. I compared the effects of site area, connectivity, vegetation condition and habitat resources on the presence, abundance and total number of species of butterflies and day-flying moths within 46 urban fragments of remnant vegetation in south-west Western Australia. Site area and vegetation condition were the dominant determinants of species presence: large sites with more undisturbed vegetation favoured 16 of 20 native species and only one (Geitoneura minyas) benefited from disturbance. Another nine species that were not sufficiently widespread or abundant to enable individual analysis were collectively more prevalent in larger sites. Resource quality and quantity dominated the patterns of site occupancy, consistent with habitat resources, not metapopulation effects, determining current distribution patterns. The total number of species at each site reflected the collective responses of the individual species: increasing with area and declining with vegetation disturbance. The effects of area and vegetation condition were not simply additive: disturbance had a far greater impact on small remnants. Restoration or maintenance of high vegetation condition will be essential to maintain regional species diversity and to prevent local extinctions of butterflies and day-flying moths, especially in small remnants.     

Moth wing scales slightly increase the absorbance of bat echolocation calls

Coevolutionary arms races between predators and prey can lead to a diverse range of foraging and defense strategies, such as countermeasures between nocturnal insects and echolocating bats. Here, we show how the fine structure of wing scales may help moths by slightly increasing sound absorbance at frequencies typically used in bat echolocation. Using four widespread species of moths and butterflies, we found that moth scales are composed of honeycomb-like hollows similar to sound-absorbing material, but these were absent from butterfly scales. Micro-reverberation chamber experiments revealed that moth wings were more absorbent at the frequencies emitted by many echolocating bats (40-60 kHz) than butterfly wings. Furthermore, moth wings lost absorbance at these frequencies when scales were removed, which suggests that some moths have evolved stealth tactics to reduce their conspicuousness to echolocating bats. Although the benefits to moths are relatively small in terms of reducing their target strengths, scales may nonetheless confer survival advantages by reducing the detection distances of moths by bats by 5-6%.