Macroglossum Stellatarum Research Articles

Numerical Study of Flapping-Wing Flight of Hummingbird Hawkmoth during Hovering: Longitudinal Dynamics

Numerical Study of Flapping-Wing Flight of Hummingbird Hawkmoth during Hovering: Longitudinal Dynamics

Wavelength discrimination in the hummingbird hawkmoth Macroglossum stellatarum

Despite the strong relationship between insect vision and the spectral properties of flowers, the visual system has been studied in detail in only a few insect pollinator species. For instance, wavelength discrimination thresholds have been determined in two species only: the honeybee (Apis mellifera) and the butterfly Papilio xuthus. Here, we present the wavelength discrimination thresholds (Δλ) for the hawkmoth Macroglossum stellatarum. We compared the data with those found for the honeybee, the butterfly P. xuthus and the predictions of a colour discrimination model. After training moths to feed from a rewarded disc illuminated with a monochromatic light, we tested them in a dual-choice situation, in which they had to choose between light of the training wavelength and a novel unrewarded wavelength. To characterise the Δλ function, we decreased the difference between wavelengths in subsequent tests. We also varied the light intensity to test its effect on the discrimination capacity. In agreement with the predictions of the model, we found two expected minima of discrimination where photoreceptor sensitivities overlap, as well as a third, minor, unpredicted minimum around the peak of the blue photoreceptor. Macroglossum stellatarum is capable of discriminating between lights with a wavelength difference of 1-2 nm. These discrimination minima are similar to those found for the tetrachromatic P. xuthus, and are better than those of the honeybee. The moth is also capable of using achromatic information to discriminate between lights of long wavelengths.

Genetic diversity of Viola cazorlensis Gand., an endemic species of Mediterranean dolomitic habitats: implications for conservation

Viola cazorlensis is a South Iberian endemic (Spain), which is protected at European level, nationally as well as regionally, and considered vulnerable (VU) in accordance with IUCN criteria. This study has researched the genetic variability of seven representatives of V. cazorlensis populations, both inter- and intra-populationally, through the use of ISSR molecular markers and the sequencing of plastidial intergenic spacers. Results obtained from the ISSR markers indicate that these V. cazorlensis populations are not genetically impoverished, and that no clear genetic structure pattern exists. From the sequencing of plastidial intergenic spacers, the presence of different haplotypes has been observed, which becomes more evident as geographic distance among populations increases. Furthermore, there is a certain gene flow among them, more effective at a nuclear level, which could be mediated by Macroglossum stellatarum pollinator. The results obtained lead to the discussion of a series of conservation measures.

Long corollas as nectar barriers in Lonicera implexa: interactions between corolla tube length and nectar volume

Long corollas are a classical example of nectar barriers, because they prevent undesired visitors from consuming the reward intended for more effective pollinators. As the investment in nectar barriers increases, flower attractiveness and nectar rewards may also increase to maintain loyal visitation of most effective pollinators; and flowers may become more prone to nectar robbing. We evaluated the effect of nectar barriers (corolla tube length), two related traits (nectar volume and upper lip size) and the associated risk of nectar robbing, on the fecundity of Lonicera implexa plants from three populations differing in the abundance of its most efficient pollinator, the hummingbird hawkmoth Macroglossum stellatarum. Corolla tube length varied most among individuals within populations (45–46 % of total variance) and inflorescences within individuals (23–32 %), and showed little variation among populations (0.2–11 %). Longer corolla tubes were always associated with larger nectar volumes and larger upper lips, although the strength of the relationships varied across populations and years. Robbing frequency increased with corolla tube length, decreased with nectar volume and upper lip size, and its weak effects on fecundity were predominantly positive. Plant fecundity peaked at two different optima: long corollas with little nectar and short corollas with abundant nectar. However, the exact shape of the interaction between corolla length and nectar volume, as well as the combination of traits showing the highest fecundity, differed between populations and years. This variation could be explained by among-population differences in pollinator assemblages, and inter-annual changes in resources dedicated to reproduction. Our study shows that large nectar volumes can modulate the effect of corolla length as a nectar barrier, and that the combination of these two traits that maximises fecundity may be related to the identity of pollinators within each population.

The hawkmoth fauna of Pakistan (Lepidoptera: Sphingidae).

This study represents the first complete modern account of the Sphingidae of Pakistan and takes the form of an annotated checklist, based on several national collections and those of a number of individuals. Of the 60 species and subspecies found, 14 are new records to the fauna of Pakistan, namely Agnosia orneus, Langia zenzeroides subsp. zenzeroides, Polyptychus trilineatus subsp. trilineatus, Dolbina inexacta, Ambulyx sericeipennis subsp. sericeipennis, Thamnoecha uniformis, Macroglossum belis, Macroglossum stellatarum, Cechetra scotti, Hippotion boerhaviae, Hyles euphorbiae subsp. euphorbiae, Rhagastis olivacea, Rethera brandti subsp. euteles and Theretra latreillii subsp. lucasii. Anambulyx elwesi subsp. kitchingi and Clanis deucalion subsp. thomaswitti are not recognised as valid subspecies and are synonymized with their respective nominotypical subspecies. An additional list is given of 30 taxa which may yet be found in Pakistan as they are present in neighbouring countries close to the border. Of the species/subspecies found, 24 are part of the Palaearctic fauna, 27 are part of the Oriental fauna and nine are Palaeo-Oriental/Palaeotropical. This reconfirms the transitional biogeographical position of the Pakistan fauna.

A hundred years of color studies in insects: with thanks to Karl von Frisch and the workers he inspired.

and colleagues (Hempel de Ibarra et al. 2014). Lars Chittka and colleagues specifically remind us that whilst bees and other insects see in color, in complex natural environments color perception can be a challenging cue due to the large changes in the spectral quality of light in different foraging environments (Chittka et al. 2014). Anne Leonard and Pavel Masek (2014) discuss the latest evidence that bees can use multimodal information combining both color and olfactory cues to help reduce uncertainty in complex foraging conditions. Indeed there is currently a lot of interest in how bees make decisions in complex environments. Aurore Avargues-Weber and Martin Giurfa (2014) discuss that a variety of important factors like conditioning method can influence bee perception, possibly through cognitive ‘top-down’ attention-type mechanisms. Further evidence of complex decision making in bees comes from a nice study on bumblebees by Lisa Evans and Nigel Raine (2014) who show that the way in which some bees make errors may be of adaptive advantage for selecting novel rewarding colors in natural conditions. Other studies show us that since the time of von Frisch color processing has been tested in a wide variety of different insect species. Motohiro Wakakuwa and colleagues (2014) discuss photoreceptor sensitivity in the leafhopper (Nephotettix cincticeps) which shows some behavioral sensitivity to long wavelength ‘infrared’ radiation. Francismeire Telles and colleagues (2014) show in the hummingbird hawkmoth (Macroglossum stellatarum) that the behavioral sensitivity to blue wavelength light is much higher than predicted from the retinal photoreceptor sensitivity, which may be related to the innate preference of hawkmoths for blue flowers. Besides bees, flies and butterflies have been well studied. Klaus Lunau (2014) provides a timely review on the color vision of flies which is a system generating a lot of interest at present. Michiyo Kinoshita About 100 years ago it was often thought the world might appear pretty dull for insects until the publication of Karl von Frisch in 1914. this ground breaking study by von Frisch revealed that free flying honeybees could be trained with sucrose solution to visit a colored card, and choose this stimulus correctly in tests when placed amongst a variety of grey cards. the logic of the experiment, done at a time when the spectral sensitivities of bee photoreceptors were unknown, was that if bees were only using an achromatic mechanism to find the conditioned, colored stimulus associated with a sucrose reward then the bees would make mistakes for grey cards having similar brightness values to the colored stimulus. However, the bees reliably chose the colored stimulus amongst many shades of grey (von Frisch 1914), and the eyes of the next generations of researchers were opened to the refinement and diversity of color perception in bees and other insects (Kuhn 1927; Daumer 1956; Menzel 1967; Helversen 1972; Giurfa 2004). this current year of 2014 also marks the 50th anniversary of the first publication of the spectral sensitivities of individual photoreceptor cells in the honeybee by Autrum and von Zwehl (1964), which further helped to establish honeybees as a classic model for research into insect color vision (Peitsch et al. 1992; Briscoe and Chittka 2001). In this special issue of The Journal of Comparative Physiology A, leading scientists in the field have teamed up to pay tribute to the important start Karl von Frisch gave to the field of neuroethology and insect vision with his publication in 1914. Basic physiology and ecology of bee color vision is summarized by Natalie Hempel de Ibarra

Out of the blue: the spectral sensitivity of hummingbird hawkmoths

The European hummingbird hawkmoth Macroglossum stellatarum is a diurnal nectar forager like the honeybee, and we expect similarities in their sensory ecology. Using behavioural tests and electroretinograms (ERGs), we studied the spectral sensitivity of M. stellatarum. By measuring ERGs in the dark-adapted eye and after adaptation to green light, we determined that M. stellatarum has ultraviolet (UV), blue and green receptors maximally sensitive at 349, 440 and 521nm, and confirmed that green receptors are most frequent in the retina. To determine the behavioural spectral sensitivity (action spectrum) of foraging moths, we trained animals to associate a disk illuminated with spectral light, with a food reward, and a dark disk with no reward. While the spectral positions of sensitivity maxima found in behavioural tests agree with model predictions based on the ERG data, the sensitivity to blue light was 30 times higher than expected. This is different from the honeybee but similar to earlier findings in the crepuscular hawkmoth Manduca sexta. It may indicate that the action spectrum of foraging hawkmoths does not represent their general sensory capacity. We suggest that the elevated sensitivity to blue light is related to the innate preference of hawkmoths for blue flowers.

‘So long, Janis’ and ‘Welcome, Almut’

When Janis Weeks joined the team of JEB Editors in 2005, the journal was a very different place: Hans Hoppeler had been the Editor in Chief for less than a year, the average number of annual submissions was less than 900 and the journal had only six Monitoring Editors. Since then, Weeks has been an

Chromatic Signals Control Proboscis Movements during Hovering Flight in the Hummingbird Hawkmoth Macroglossum stellatarum

Most visual systems are more sensitive to luminance than to colour signals. Animals resolve finer spatial detail and temporal changes through achromatic signals than through chromatic ones. Probably, this explains that detection of small, distant, or moving objects is typically mediated through achromatic signals. Macroglossum stellatarum are fast flying nectarivorous hawkmoths that inspect flowers with their long proboscis while hovering. They can visually control this behaviour using floral markings known as nectar guides. Here, we investigate whether this is mediated by chromatic or achromatic cues. We evaluated proboscis placement, foraging efficiency, and inspection learning of naïve moths foraging on flower models with coloured markings that offered either chromatic, achromatic or both contrasts. Hummingbird hawkmoths could use either achromatic or chromatic signals to inspect models while hovering. We identified three, apparently independent, components controlling proboscis placement: After initial contact, 1) moths directed their probing towards the yellow colour irrespectively of luminance signals, suggesting a dominant role of chromatic signals; and 2) moths tended to probe mainly on the brighter areas of models that offered only achromatic signals. 3) During the establishment of the first contact, naïve moths showed a tendency to direct their proboscis towards the small floral marks independent of their colour or luminance. Moths learned to find nectar faster, but their foraging efficiency depended on the flower model they foraged on. Our results imply that M. stellatarum can perceive small patterns through colour vision. We discuss how the different informational contents of chromatic and luminance signals can be significant for the control of flower inspection, and visually guided behaviours in general.

Is the bumblebee (Bombus haemorrhoidalis) the only pollinator of large cardamom in central Himalayas, India?

Amomum subulatum (Zingiberaceae) is one of the major cash crops of the Eastern Himalayas. Our earlier study had shown that Bombus haemorrhoidalis is the only pollinator of A. subulatum. This was surprising in light of findings that other members of Zingiberaceae have at least a few pollinators for each plant species. We hypothesized that A. subulatum also is a generalist. Studies were carried out in six plantations of Northeast India. Floral visitors and their frequency were recorded. The pollination efficiency of each visitor was determined on the basis of pollen transfer to the stigma following a single visit of the pollinator to virgin flower. B. haemorrhoidalis, Apis cerana, Megachile lanata, Episyrphus balteatus (hover fly), Macroglossum stellatarum (hawk moth), and Aethopyga siparaja (crimson sunbird) visited the flowers of A. subulatum. Of these, B. haemorrhoidalis, M. lanata, and A. siparaja were effective pollinators. B. haemorrhoidalis was an important pollinator across all the plantations. Flower opening pattern influenced the pollination efficiency of visitors.

Reproductive ecology in the endemic Primula apennina Widmer (Primulaceae)

Disassortative mating in distylous self-incompatible species should result in the equilibrium of morph types in natural populations. Deviation from isoplethy may affect pollen transfer, and in isolated populations it could lead to Allee effect and genetic drift. Pollen limitation has been found to occur in several distylous species, for which mating opportunities are actually reduced to half population. In this study, we investigated the reproductive features and pollination ecology of the narrow endemic Primula apennina. We recorded equilibrium of morph frequencies in the studied population, reflecting the comparable fecundity found in the two morphs. Long-styled flowers produce more pollen grains of smaller size than short-styled ones: we hypothesize that in thrum flowers, pollen is more easily removed by the insect pollinator Macroglossum stellatarum, resulting in equal pollen amounts carried to both short styles and long styles. This lower pollen transfer efficiency from long-styled to short-styled flowers is also reflected in legitimate pollen–ovule ratio values. Despite results show no evidence of imminent threats to population persistence at study site, the strict dependence on one or very few pollinator species, and ecological traits, may increase extinction risks in the long-term period.

How does a diurnal hawkmoth find nectar? Differences in sensory control with a nocturnal relative

Recent research shows that a nocturnal hawkmoth, Manduca sexta, inspects flowers in search for nectar by means of a series of hovering and proboscis movements controlled by different sensory modalities, mainly vision and mechanoreception. The diurnal Macroglossum stellatarum is a closely related hawkmoth challenged with the same task but under illuminances 6-8 orders of magnitude higher. Here, we use flower models presenting color markings, 3D features, or both to study innate flower movements and sensory cues involved in the innate inspection behavior of M. stellatarum. On flat plain colored models, moths scanned the whole corolla with their proboscis, attaining intermediate success levels. When models presented color markings, moths biased proboscis placement, which affected inspection efficiency. Three-dimensional features affected inspection behavior and efficiency, by provoking strong diving'' responses. When both visual and tactile features were present, visual cues showed prevalence in the control of the inspection behavior. We evaluated learning abilities of moths, finding that M. stellatarum cannot only improve their efficiency by calibrating innate responses but also by changing their innate strategy. We discuss results on flower inspection behavior of M. stellatarum comparatively with known aspects of this behavior in M. sexta. Motor responses appear to be shared by these hawkmoths, but their sensory control shows important differences. Future studies will evaluate whether these differences are the result of an evolutionary divergence of their innate behavior associated with a switch to diurnal activity or the result of a flexible use of sensory information by the naive animals. (Less)

What a hawkmoth remembers after hibernation depends on innate preferences and conditioning situation

Nectar-feeding insects find flowers by 2 means, innate preferences and learned associations. When insects that hibernate as imagos (i.e., adults) start foraging after a long winter break, what guides them to new nectar rewards? Are innate preferences kept over such a long period? And are learned associations useful after long breaks? In a series of experiments I show here that, depending on previous experience, the European hummingbird hawkmoth, Macroglossum stellatarum can use both types of information to choose a first flower after periods of 1 or 3 weeks. What is remembered seems to depend on innate preferences of the moths. Moths trained to feed from 1 of 2 colors that are equally attractive to naive moths keep the learned preference. Animals trained to prefer a less attractive color to an innately preferred color loose the learned preference and return to the innate choice behavior. I conclude that hummingbird hawkmoths can keep innate and learned preferences over a long period and are able to use both types of information when searching nectar rewards after long periods of hibernation. (Less)

Measuring the kinematics of a free-flying hawk-moth (Macroglossum stellatarum) by a comb-fringe projection method

We describe a 2D fringe projection method that involves projecting two groups of sharp comb fringes onto a free-flying hawk-moth from different directions and recording the images of distorted fringes by two high speed cameras from two orthogonal views. By calculating the 3D coordinates of the points on the hawk-moth and three-dimensional reconstruction of the wing, the flight trajectory, body attitude and wing kinematics including flapping angle, elevation angle, torsion angle, and camber deformation are obtained.

How Do Hawkmoths Learn Multimodal Stimuli? A Comparison of Three Models

The moth Macroglossum stellatarum can learn the color and sometimes the odor of a rewarding food source. We present data from 20 different experiments with different combinations of blue and yellow artificial flowers and the two odors, honeysuckle and lavender. The experiments show that learning about the odors depends on the color used. By training on different color—odor combinations and testing on others, it becomes possible to investigate the exact relation between the two modalities during learning. Three computational models were tested in the same experimental situations as the real moths and their predictions were compared with the experimental data. The average error over all experiments as well as the largest deviation from the experimental data were calculated. Neither the Rescorla—Wagner model nor a learning model with independent learning for each stimulus component were able to explain the experimental data. We present the new hawkmoth learning model, which assumes that the moth learns a template for the sensory attributes of the rewarding stimulus. This model produces behavior that closely matches that of the real moth in all 20 experiments.

Sensory Ecology of Feeding in the Hummingbird Hawkmoth Macroglossum stellatarum (Lepidoptera: Sphingidae)

The European hummingbird hawkmoth, Macroglossum stellatarum (Linnaeus 1758), drinks nectar while hovering in front of flowers of all colours, odours, sizes and shapes. Naive moths orient predominantly towards visual stimuli and prefer blue flowers with a radial pattern and a central contrasting spot. Hummingbird hawkmoths have trichromatic colour vision and can learn any colour and different patterns and sizes of flowers. Odour learning, however, depends on flower colour and docs, not take place when the colour is very attractive on its own.

Colour preferences influences odour learning in the hawkmoth, Macroglossum stellatarum

The hummingbird hawkmoth, Macroglossum stellatarum, learns colour fast and reliably. It has earlier been shown to spontaneously feed from odourless artificial flowers. Now, we have studied odour learning. The moths were trained to discriminate feeders of the same colour but marked with different odours. They did not learn to discriminate two natural flower odours when they were presented with the innately preferred colour blue, but they did learn this discrimination combined with yellow or green colours that are less attractive to the moth. The yellow colour could be trained to become as attractive as the innately preferred blue colour and the blue colour could be trained to become less attractive. This is the first proof of odour learning in a diurnal moth. The results show that M. stellatarum can use more than one modality in their foraging behaviour and that the system is plastic. By manipulating the preferences for the different colours, their influence on odour learning could be changed.

The relative importance of olfaction and vision in a diurnal and a nocturnal hawkmoth

Nectar-feeding animals can use vision and olfaction to find rewarding flowers and different species may give different weight to the two sensory modalities. We have studied how a diurnal or nocturnal lifestyle affects the weight given to vision and olfaction. We tested naïve hawkmoths of two species in a wind tunnel, presenting an odour source and a visual stimulus. Although the two species belong to the same subfamily of sphingids, the Macroglossinae, their behaviour was quite different. The nocturnal Deilephila elpenor responded preferably to the odour while the diurnal Macroglossum stellatarum strongly favoured the visual stimulus. Since a nocturnal lifestyle is ancestral for sphingids, the diurnal species, M. stellatarum, has evolved from nocturnal moths that primarily used olfaction. During bright daylight visual cues may have became more important than odour.

Alternative use of chromatic and achromatic cues in a hawkmoth

The diurnal hummingbird hawkmoth Macroglossum stellatarum can learn the achromatic (intensity-related) and the chromatic (wavelength-related) aspect of a spectral colour. Free-flying moths learn to discriminate two colours differing in the chromatic aspect of colour fast and with high precision. In contrast, they learn the discrimination of two stimuli differing in the achromatic aspect more slowly and less reliably. When trained to use the chromatic aspect, they disregard the achromatic aspect, and when trained to use the achromatic aspect, they disregard the chromatic aspect, at least to some degree. In a conflicting situation, hummingbird hawkmoths clearly rely on the chromatic aspect of colour. Generally, the moths pay attention to the most reliable cue that allows them to discriminate colours in the learning situation. This is usually the chromatic aspect of the colour but they can learn to attend to the achromatic aspect instead. There is no evidence for relative colour learning, i.e. moths do not learn to choose the longer or shorter of two wavelengths, but it is possible that they learn to choose the darker or brighter shade of a colour, and thereby its relative intensities.

Sugar preferences and feeding strategies in the hawkmoth Macroglossum stellatarum.

Hummingbird hawkmoths were tested for their preferences for different types of sugar. In triple choice tests, moths sucked for longer periods from sucrose than from fructose and glucose. Naive moths released in a large flight cage and monitored over 24 days, drank on average 137 mul sucrose, 67 mul fructose and 7 mul glucose daily. In an independent test, moths spent more time feeding from sucrose than from fructose and more time feeding from fructose than from glucose. Animals in hibernation made less but longer feeding bouts, whereas animals that fed every day and newly eclosed animals were more likely to make more but shorter visits to feeders. The hawkmoths learned to associate colour with the preferred sugar. In a dual choice test, flower-naive moths chose blue rather than yellow artificial flowers. After the initial test, these animals received sucrose from the yellow and glucose from the blue feeders. A week later they chose yellow more frequently than blue indicating that they had learned to associate a colour with the preferred type of sugar.