Functional constraints on the evolution of long butterfly proboscides: lessons from Neotropical skippers (Lepidoptera: Hesperiidae)

Extremely long proboscides are rare among butterflies outside of the Hesperiidae, yet representatives of several genera of skipper butterflies possess proboscides longer than 50 mm. Although extremely elongated mouthparts can be regarded as advantageous adaptations to gain access to nectar in deep‐tubed flowers, the scarcity of long‐proboscid butterflies is a phenomenon that has not been adequately accounted for. So far, the scarceness was explained by functional costs arising from increased flower handling times caused by decelerated nectar intake rates. However, insects can compensate for the negative influence of a long proboscis through changes in the morphological configuration of the feeding apparatus. Here, we measured nectar intake rates in 34 species representing 21 Hesperiidae genera from a Costa Rican lowland rainforest area to explore the impact of proboscis length, cross‐sectional area of the food canal and body size on intake rate. Long‐proboscid skippers did not suffer from reduced intake rates due to their large body size and enlarged food canals. In addition, video analyses of the flower‐visiting behaviour revealed that suction times increased with proboscis length, suggesting that long‐proboscid skippers drink a larger amount of nectar from deep‐tubed flowers. Despite these advantages, we showed that functional costs of exaggerated mouthparts exist in terms of longer manipulation times per flower. Finally, we discuss the significance of scaling relationships on the foraging efficiency of butterflies and why some skipper taxa, in particular, have evolved extremely long proboscides.     

Complete mitochondrial genomes of five skippers (Lepidoptera: Hesperiidae) and phylogenetic reconstruction of Lepidoptera

We sequenced mitogenomes of five skippers (family Hesperiidae, Lepidoptera) to obtain further insight into the characteristics of butterfly mitogenomes and performed phylogenetic reconstruction using all available gene sequences (PCGs, rRNAs, and tRNAs) from 85 species (20 families in eight superfamilies). The general genomic features found in the butterflies also were found in the five skippers: a high A + T composition (79.3%–80.9%), dominant usage of TAA stop codon, similar skewness pattern in both strands, consistently length intergenic spacer sequence between tRNA^Gln and ND2 (64–87 bp), conserved ATACTAA motif between tRNA^{Ser (UCN)} and ND1, and characteristic features of the A + T-rich region (the ATAGA motif, varying length of poly-T stretch, and poly-A stretch). The start codon for COI was CGA in four skippers as typical, but Lobocla bifasciatus evidently possessed canonical ATG as start codon. All species had the ancestral arrangement tRNA^Asn/tRNA^{Ser (AGN)}, instead of the rearrangement tRNA^{Ser (AGN)}/tRNA^Asn, found in another skipper species (Erynnis). Phylogenetic analyses using all available genes (PCGs, rRNAS, and tRNAs) yielded the consensus superfamilial relationships ((((((Bombycoidea + Noctuoidea + Geometroidea) + Pyraloidea) + Papilionoidea) + Tortricoidea) + Yponomeutoidea) + Hepialoidea), confirming the validity of Macroheterocera (Bombycoidea, Noctuoidea, and Geometroidea in this study) and its sister relationship to Pyraloidea. Within Rhopalocera (butterflies and skippers) the familial relationships (Papilionidae + (Hesperiidae + (Pieridae + ((Lycaenidae + Riodinidae) + Nymphalidae)))) were strongly supported in all analyses (0.98–1 by BI and 96–100 by ML methods), rendering invalid the superfamily status for Hesperioidea. On the other hand, current mitogenome-based phylogeny did not find consistent superfamilial relationships among Noctuoidea, Geometroidea, and Bombycoidea and the familial relationships within Bombycoidea between analyses, requiring further taxon sampling in future studies.     

Diel patterns of activity of Thymelicus lineola adults (Lepidoptera: Hesperiidae) in relation to weather *

ABSTRACT. 1. Daily patterns of activity, thoracic temperature (T_th) and thermoregulatory behaviour in relation to environmental conditions were studied in the European skipper Thymelicus lineola (Ochsenheimer) adults. 2. Daily activity was limited mainly by T_th, which in turn was dependent on air temperature (T_a) and sunlight. However, when light intensity fell to < 100 W m^?2, skippers also became inactive. 3. T_th was sometimes as much as 12°C above T_a, and this was most pronounced under cool conditions when basking activity predominated. 4. Black globe temperature (T_bg) which, in the absence of wind, is influenced by both T^a, and radiant heat load in a manner similar to a basking butterfly, was used to approximate the maximum T_th attained by T.lineola through basking. 5. Both males and females basked at T_bg >20°C, and if this temperature was not attained, skippers remained inactive. As T_bg increased, basking activity declined more rapidly in males than in females. Basking bouts were also shorter in males. 6. Males also flew, fed and courted females at T_bg >20°C, while females only fed and flew at T_bg >22°C. The percentage of both sexes feeding and flying, and courting in the case of males, were positively correlated with T_bg. 7. In warm weather, males divided their time equally between flying and feeding, while females spent the majority of their time feeding. Feeding bouts were shorter and flying bouts were longer in males than in females. Flight duration in males was positively correlated with T_bg. 8. Skippers avoided, and, consequently laid fewer eggs in, shady areas. 9. Sexual differences in activity patterns in relation to weather reflect differences in the reproductive requirements of the two sexes.     

Complete mitochondrial genomes of three skippers in the tribe Aeromachini (Lepidoptera: Hesperiidae: Hesperiinae) and their phylogenetic implications

The mitochondrial genome is now widely used in the study of phylogenetics and molecular evolution due to its maternal inheritance, fast evolutionary rate, and highly conserved gene content. To explore the phylogenetic relationships of the tribe Aeromachini within the subfamily Hesperiinae at the mitochondrial genomic level, we sequenced and annotated the complete mitogenomes of 3 skippers: Ampittia virgata, Halpe nephele, and Onryza maga (new mitogenomes for 2 genera) with a total length of 15,333 bp, 15,291 bp, and 15,381 bp, respectively. The mitogenomes all contain 13 protein‐coding genes (PCGs), 22 transfer RNAs (tRNAs), 2 ribosomal RNAs (rRNAs), and a noncoding A + T‐rich region and are consistent with other lepidopterans in gene order and type. In addition, we reconstructed the phylogenetic trees of Hesperiinae using maximum likelihood (ML) and Bayesian inference (BI) methods based on mitogenomic data. Results show that the tribe Aeromachini in this study robustly constitute a monophyletic group in the subfamily Hesperiinae, with the relationships Coeliadinae + (Euschemoninae + (Pyrginae + ((Eudaminae + Tagiadinae) + (Heteropterinae + ((Trapezitinae + Barcinae) + Hesperiinae))))). Moreover, our study supports the view that Apostictopterus fuliginosus and Barca bicolor should be placed out of the subfamily Hesperiinae.     

The mitochondrial genomes of three skippers: Insights into the evolution of the family Hesperiidae (Lepidoptera)

We sequenced the mitogenomes of Astictopterus jama, Isoteinon lamprospilus and Notocrypta curvifascia to obtain further insight into the mitogenomic architecture evolution and performed phylogenetic reconstruction using 29 Hesperiidae mitogenome sequences. The complete mitogenome sequences of A. jama, I. lamprospilus and N. curvifascia are 15,430, 15,430 and 15,546 bp in size, respectively. All contain 13 protein-coding genes, 2 ribosomal RNA genes, 22 transfer RNA genes, and an A + T-rich region. Nucleotide composition is A + T biased, and the majority of the protein-coding genes exhibit a negative AT-skew, which is reflected in the nucleotide composition, codon, and amino acid usage. The A + T-rich region is comprised of nonrepetitive sequences, including the motif ATAGA followed by a poly-T stretch, a microsatellite-like element next to the ATTTA motif, and a poly-A adjacent to tRNAs. Although most genes evolve under a strong purifying selection, the entire nad gene family (especially nad6) exhibits somewhat relaxed purifying selection, and atp8, evolving under a highly relaxed selection, is an outlier in the family Hesperiidae. Several different approaches relatively consistently indicated that nad6, atp8 and nad4 are comparatively fast-evolving genes in this family, which may have implications for future phylogenetic, population genetics and species diagnostics studies. For phylogenetic analyses of Hesperiidae, we tested a few datasets, and found that the one comprising all 37 genes produced the highest node support, indicating that the inclusion of RNAs improves the phylogenetic signal. Results indicate that subfamilies Euschemoninae, Heteropterinae, and Coeliadinae are monophyletic with strong nodal support, but Pyrginae and Eudaminae are paraphyletic. Finally, we confirm that A. jama and I. lamprospilus are close relatives.     

Egg size of skippers (Lepidoptera: Hesperiidae) in relation to their host specificity and to leaf toughness of host plants

The adaptive significance of egg size of skippers (Lepidoptera; Hesperiidae) in Japan was evaluated in relation to the leaf toughness of their major host grasses. The hesperids that fed on tougher grasses laid larger eggs. Hesperids that laid larger eggs were larger in body size, but lower in fecundity. They also had a wider host range. Thus, despite the lower fecundity, hesperids may benefit from large eggs by having a wider host range of larvae. Grass feeders had wider range of host plants than broadleaf feeders.     

Thermoregulation and flight activity in territorial male graylings,Hipparchia semele (Satyridae), and large skippers,Ochlodes venata (Hesperiidae)

Some male butterflies defend specific mating sites, e.g. sandy patches (Hipparchia semele) or plants (Ochlodes venata). When perching within its territory, a male orients the body axis and tilts its wings and body in order to control the body area exposed to the sun, and thereby keeps its body temperature (T _b) as close to a preferred level as possible. In accordance with a model presented here, these behaviours can be separated into three successive phases. At low temperatures, the males maximized the heat load by exposing the maximum body area (sun-basking). This raised T _b above the temperature of a non-regulating animal by c. 3° C. At an intermediate range of temperatures, T _b was kept constant at the preferred level by means of a gradual change of body orientation and posture (graded phase). At high temperatures, the heat load was minimized by exposing the minimum body area. This lowered T _b below that of a non-regulating animal by c. 2.5° C. H. semele went through all three phases, but O. venata only reached the basking phase due to a more moderate microclimate. Three types of thermoregulation in ectothermic animals and their functions are discussed. Thermoregulation in territorial male butterflies serves to prepare the animal for efficient flight performance if another male should try to take over the territory, or a predator attacks. The males also made frequent short flights, spontaneously or elicited by other insects. Their duration was independent of temperature, and they may function as a sexual signal.     

Synchronous nocturnal activity and gregarious roosting in the neotropical skipper butterfly Celaenorrhinus fritzgaertneri (Lepidoptera: Hesperiidae)

Gregarious roosting behaviour and nocturnal activity is virtually unknown within the family Hesperiidae. Observations on Celaenorrhinus fritzgaertneri (Bailey) from Guanacaste Province, Costa Rica, are presented which demonstrate that, during the dry season, individuals roost gregariously in cave-like situations during the day and are nocturnally active. Circadian behaviour is highly synchronized with regard to timing of departures and arrivals at the roosting site, and appears to be regulated by light levels. Individuals on the roost are in reproductive diapause and show marked roost-site fidelity and longevity. The break-up of roosts appears to be mediated by the onset of the first rains of the season. These observations are compared and discussed in relation to gregarious roosting in other Lepidoptera. Two possible life history strategies to explain roosting in C. fritzgaertneri , with appropriate experiments, are suggested for future studies.     

The Abantis species (Lepidoptera: Hesperiidae) of western West Africa

Abstract. The genus Abantis Hopffer contains eight species in western West Africa. One species, Abantis pseudonigeriana sp.n., is described as new. Distributional notes and a key are given for all species. In general the species of this genus are rare and poorly represented in collections, but there are interesting examples of pairs of very similar species (nigeriana and pseudonigeriana; elegantula and maesseni).     

The ecology and status of Thymelicus acteon (Lepidoptera: Hesperiidae) in Britain

ABSTRACT.

• 1 A survey was made of the local butterfly, the Lulworth Skipper (Thymelicus acteon Rott.) in Britain. Adult numbers were estimated on most sites and the habitat was analysed. Changes in numbers were also recorded in five populations over 6 years, and some aspects of behaviour were studied.
• 2 T.acteon forms closed populations. It was found in great abundance throughout its historical range, and appears both to have increased in numbers and to have spread locally. It has not extended its range.
• 3 The wrong larval foodplant is quoted by some modern textbooks. T.acteon requires mature Brachypodium pinnatum Beauv. plants for breeding. Within its range, the butterfly was almost ubiquitous in areas with tall Brachypodium.
• 4 The present abundance and probable increase of T.acteon is attributed to the spread of B.pinnaturn in unimproved calcareous grassland. This has occurred through a decline in grazing, both by domestic stock and, since myxomatosis, by rabbits.

     

Piloting the use of DNA barcoding in support of natural enemy surveys: New parasitoid records for banana skippers (Erionota spp., Lepidoptera,Hesperiidae) in Malaysia

We report a preliminary study carried out in Peninsular Malaysia, with the objective of rearing parasitoids of the two species of banana skippers (Erionota thrax and E. torus: Lepidoptera, Hesperiidae) and using DNA barcoding of Erionota spp. early stages (which are indistinguishable) and host remains to associate parasitoids with their host Erionota species. We were able to use barcodes to reliably identify the dead host remains, unreliably identify a limited subset of associated material (exuviae, frass, pupal exoskeleton, silk, wax) and to make provisional generic identifications of the parasitoids. We found parasitism by Argyrophylax sp. possibly phoeda (Tachinidae) on both species of Erionotus, by ?Casinaria sp. (Ichneumonidae) on E. thrax, and by Elasmus sp. (Eulophidae) on E. torus. The first is a new host-parasitoid association, and the second is a new association for Peninsular Malaysia. We conclude that the use of DNA barcoding, particularly for recently dead host remains, is a valuable tool to assess host-parasitoid associations where the hosts cannot be reliably identified from morphological characters.     

The role of habitat and daily activity patterns in explaining the diversity of mountain Neotropical dung beetle assemblages

The interaction between land use and climate change is expected to strongly affect species distributions along high elevation landscapes. We aimed to test the effect of climatic variables on community metrics among five types of land use in a high elevation landscape. We described dung beetle spatial and temporal taxonomic and functional diversity patterns, and partitioned β‐diversity into turnover and nestedness components. The interaction between land use and daily period of activity mostly drives abundance, functional richness and functional diversity, but not dung beetle species richness. Unlike Neotropical lowlands, species richness and abundance in open environments are similar to those existing in forests. Temperature is an important predictor of abundance and functional divergence. There is a higher spatial component of the taxonomic β‐diversity, which is highly driven by species turnover. The temporal component of the taxonomic β‐diversity was strongly driven by nestedness, where night assemblages are sub‐sets, although not entirely, of diurnal assemblages. For functional diversity, the temporal β‐diversity was much higher than the spatial β‐diversity, but both were similarly represented by functional group turnover and nestedness. The composition of nocturnal and diurnal assemblages is clearly different, even more than the differences observed between habitats. However, taxonomic turnover is the dominant force between sampling sites while nestedness dominates the daily pattern. This means that forest habitats are unlikely to act as shelters for grassland species under a scenario of rising temperature.     

江西省弄蝶四新纪录(鳞翅目:弄蝶总科)(英文)

通过对外形特征和外生殖器特征的检视,发现江西省弄蝶四新纪录:无斑珂弄蝶指名亚种Caltoris bromus bromus(Leech,1894)、襟弄蝶中南亚种Pseudocoladenia dan fabia(Evans,1949)、灰陀弄蝶黎氏亚种Thoressa gupta leechii(Evans,1932)和南岭陀弄蝶Thoressa xiaoqingae Huang&Zhan,2004。标本均采自江西九连山国家级自然保护区。文中提供了成虫标本照片。     

Flight activity and oviposition characteristics of the seasonal form of a migrant skipper,Parnara guttata guttata (Lepidoptera: Hesperiidae)

The flight activity of adults of a migrant skipper (Parnara guttata guttata) was measured on the day of emergence, and at 4 and 7 days after emergence by a flight mill and the activity was compared among the three seasonal forms which emerged under 12, 14 and 16 hr photoperiods. The flight activity of adults reared under 12 and 14 hrs was higher than that under 16 hr especially on the day of emergence. The flight activity of males under 12 and 14 hrs was higher on the day of emergence and decreased at 4 and 7 days. The activity of males under 16 hr was maintained at a low and constant level. The activity of females under 12 and 14 hrs increased or was constant on the days after the emergence, on the other hand, the activity of females under 16 hr was highest at 4 days after the emergence. The wing size did not affect the flight activity. The oviposition characteristics of females reared under the three photoperiods was compared. The female under 14 hr has a longer preoviposition period and lesser fecundity than that under 16 hr. The female under 12 hr has intermediate values of the former two. The size of eggs laid by females under 12 hr was also intermediate.     

陀弄蝶属Thoressa二新种记述（鳞翅目：弄蝶科）

记述弄蝶科陀弄蝶属Thoressa2新种;无突陀弄蝶T.abprojecta Yuan et Wang,sp.nov.;短突陀弄蝶T.breviprojecta Yuan et Wang,sp.nov.,绘制了新种的雄性外生殖器图,编制了中国已知种分种 检索,模式标本均保存在西北农林科技大学昆虫博物馆。     

Neotropical ennomine moths: a review of the genera (Lepidoptera: Geometridae)

The classification of the Neotropical genera of the Ennominae is reviewed and 267 genera are recognised to occur in this region. Three new genera are described and three others are reinstated, while 48 generic synonyms are newly established. Other changes established in this work include 14 species synonyms and 237 new or reinstated combinations. External features and genitalia of representative members of the genera are illustrated (753 figures). All the known Neotropical species and subspecies of Ennominae are listed ( c . 3470), plus their synonyms. The tribes to which the genera belong are assessed, with c . 200 of the genera assigned to tribe or other suprageneric grouping.  © 2002 The Linnean Society of London, Zoological Journal of the Linnean Society , 2002, 135 , 121–401.     

Predicting adult emergence of Dakota skipper and Poweshiek skipperling (Lepidoptera: Hesperiidae) in Canada

Dakota skipper (Hesperia dacotae Skinner) and Poweshiek skipperling (Oarisma poweshiek Parker) (Lepidoptera: Hesperiidae) are endemic prairie species that are threatened in Canada. Surveys during the brief adult flight period are necessary to quantify population sizes, but dates of adult emergence vary widely from year to year (up to 24 days) and populations are geographically distant from one another (150–250 km). To predict adult emergence of H. dacotae and O. poweshiek, we used local weather station data to calculate the number of degree days accumulated between March 1 and adult emergence using two different models in seven different years between 2002 and 2013. We also compared the number of degree days accumulated at the soil surface where larvae and pupae reside to those accumulated using weather station data. We recommend that surveys for Dakota skipper begin when degree day accumulations (from weather stations) reach a threshold of 575 (standard model) or 600 (double sine model) in the south central portion of Manitoba and 550 (standard model) or 575 (double sine model) in the southwest region of Manitoba. For Poweshiek skipperling surveys should be considered after degree day accumulations reach 575 (standard model) or 625 (double sine model). Degree days accumulated at the soil surface were 20–30 % greater than those calculated using weather station data in Dakota skipper sites, and 1–12 % greater in Poweshiek skipperling sites. Using our models, we predicted adult emergence to within 48 h of emergence in 2011, 2012 and 2013.     

Spotted cutworm,Xestia c‐nigrum (L.) (Lepidoptera: Noctuidae) responses to sex pheromone and blacklight

Traps baited with the sex pheromone blend of (Z7)‐ and (Z5)‐tetradecenyl acetate captured significant numbers of male spotted cutworm moths, Xestia c‐nigrum (L.) compared to unbaited traps. Nearly no males were captured in traps baited with (Z7)‐tetradecenyl acetate, the major pheromone component. Antennae of spotted cutworm males responded to (Z7)‐, (E7)‐, (Z5)‐ and (E5)‐tetradecenyl acetate in the laboratory; however there was no response by moths in the field to the E isomers when presented in traps as major and minor components respectively of a binary blend or to the (E7) isomer as a single component. These findings clarify the makeup of a sex attractant that can be used for monitoring X. c‐nigrum on agricultural crops in Washington. However, multi‐year season‐long monitoring of spotted cutworm moths in Yakima Valley apple orchards revealed differential responses to pheromone and blacklight traps. A spring flight period showed a strong moth response to the pheromone compared to blacklight, while a later summer flight period showed a weak moth response to the pheromone relative to blacklight. At this time, we do not know which trap type might best indicate spotted cutworm abundance and risk to crops.     

Phylogenetic relationships of subfamilies and circumscription of tribes in the family Hesperiidae (Lepidoptera: Hesperioidea)

A comprehensive tribal‐level classification for the world’s subfamilies of Hesperiidae, the skipper butterflies, is proposed for the first time. Phylogenetic relationships between tribes and subfamilies are inferred using DNA sequence data from three gene regions (cytochrome oxidase subunit I‐subunit II, elongation factor‐1α and wingless). Monophyly of the family is strongly supported, as are some of the traditionally recognized subfamilies, with the following relationships: (Coeliadinae + (“Pyrginae” + (Heteropterinae + (Trapezitinae + Hesperiinae)))). The subfamily Pyrginae of contemporary authors was recovered as a paraphyletic grade of taxa. The formerly recognized subfamily Pyrrhopyginae, although monophyletic, is downgraded to a tribe of the “Pyrginae”. The former subfamily Megathyminae is an infra‐tribal group of the Hesperiinae. The Australian endemic Euschemon rafflesia is a hesperiid, possibly related to “Pyrginae” (Eudamini). Most of the traditionally recognized groups and subgroups of genera currently employed to partition the subfamilies of the Hesperiidae are not monophyletic. We recognize eight pyrgine and six hesperiine tribes, including the new tribe Moncini. © The Willi Hennig Society 2008.