Anna Balkenius

Scotopic colour vision in nocturnal hawkmoths

Humans are colour-blind at night, and it has been assumed that this is true of all animals. But colour vision is as useful for discriminating objects at night as it is during the day. Here we show, through behavioural experiments, that the nocturnal hawkmoth Deilephila elpenor uses colour vision to discriminate coloured stimuli at intensities corresponding to dim starlight (0.0001 cd m-2). It can do this even if the illumination colour changes, thereby showing colour constancy—a property of true colour vision systems. In identical conditions humans are completely colour-blind. Our calculations show that the possession of three photoreceptor classes reduces the absolute sensitivity of the eye, which indicates that colour vision has a high ecological relevance in nocturnal moths. In addition, the photoreceptors of a single ommatidium absorb too few photons for reliable discrimination, indicating that spatial and/or temporal summation must occur for colour vision to be possible. Taken together, our results show that colour vision occurs at nocturnal intensities in a biologically relevant context.

Floral to green: mating switches moth olfactory coding and preference

Mating induces profound physiological changes in a wide range of insects, leading to behavioural adjustments to match the internal state of the animal. Here, we show for the first time, to our knowledge, that a noctuid moth switches its olfactory response from food to egg-laying cues following mating. Unmated females of the cotton leafworm (Spodoptera littoralis) are strongly attracted to lilac flowers (Syringa vulgaris). After mating, attraction to floral odour is abolished and the females fly instead to green-leaf odour of the larval host plant cotton, Gossypium hirsutum. This behavioural switch is owing to a marked change in the olfactory representation of floral and green odours in the primary olfactory centre, the antennal lobe (AL). Calcium imaging, using authentic and synthetic odours, shows that the ensemble of AL glomeruli dedicated to either lilac or cotton odour is selectively up- and downregulated in response to mating. A clear-cut behavioural modulation as a function of mating is a useful substrate for studies of the neural mechanisms underlying behavioural decisions. Modulation of odour-driven behaviour through concerted regulation of odour maps contributes to our understanding of state-dependent choice and host shifts in insect herbivores.

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.

Colour vision in diurnal and nocturnal hawkmoths

Abstract Diurnal and nocturnal hawkmoths (Sphingidae, Lepidoptera) have three spectral types of receptor sensitive to ultraviolet, blue and green light. As avid flower visitors and pollinators, they use olfactory and visual cues to find and recognise flowers. Moths of the diurnal species Macroglossum stellatarum and the nocturnal species Deilephila elpenor, Hyles lineata and Hyles gallii use and learn the colour of flowers. Nocturnal species can discriminate flowers at starlight intensities when humans and honeybees are colour-blind. M. stellatarum can use achromatic, intensity-related cues if colour cues are absent, and this is probably also true for D. elpenor. Both species can recognise colours even under a changed illumination colour.

Colour constancy in diurnal and nocturnal hawkmoths

SUMMARY Diurnal and nocturnal hawkmoths have been shown to use colour vision for flower discrimination. Here, we present evidence that the nocturnal hawkmoth Deilephila elpenor and the diurnal hawkmoth Macroglossum stellatarum also have colour constancy. Colour constancy was shown in D. elpenor in two multiple-choice experiments with five different bluish colour patches under white and blue illumination and with five yellowish colour patches under white, blue and yellow illumination. The mechanism underlying colour constancy in both species was investigated in two dual-choice experiments. The choice behaviour is consistent with the use of the von Kries coefficient law. Although the moths have colour constancy, they react to the colour of the illumination. They make fewer choices when tested under the changed illumination, where they never receive a reward, compared with the training illumination. Even if colour constancy can be explained by a von Kries adaptation mechanism, the fact that the animals discriminate between different illuminations indicates that some additional process must be involved.

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.

Interaction of visual and odour cues in the mushroom body of the hawkmoth Manduca sexta.

SUMMARY The responses to bimodal stimuli consisting of odour and colour were recorded using calcium-sensitive optical imaging in the mushroom bodies of the hawkmoth Manduca sexta. The results show that the activity in the mushroom bodies is influenced by both olfaction and vision. The interaction between the two modalities depends on the odour and the colour of the visual stimulus. A blue stimulus suppressed the response to a general flower scent (phenylacetaldehyde). By contrast, the response to a green leaf scent (1-octanol) was enhanced by the presence of the blue stimulus. A green colour had no influence on these odours but caused a marked increase in the response to an odour component (benzaldehyde) of the hawkmoth-pollinated Petunia axillaris.

The Absolute Threshold of Colour Vision in the Horse

Arrhythmic mammals are active both during day and night if they are allowed. The arrhythmic horses are in possession of one of the largest terrestrial animal eyes and the purpose of this study is to reveal whether their eye is sensitive enough to see colours at night. During the day horses are known to have dichromatic colour vision. To disclose whether they can discriminate colours in dim light a behavioural dual choice experiment was performed. We started the training and testing at daylight intensities and the horses continued to choose correctly at a high frequency down to light intensities corresponding to moonlight. One Shetland pony mare, was able to discriminate colours at 0.08 cd/m2, while a half blood gelding, still discriminated colours at 0.02 cd/m2. For comparison, the colour vision limit for several human subjects tested in the very same experiment was also 0.02 cd/m2. Hence, the threshold of colour vision for the horse that performed best was similar to that of the humans. The behavioural results are in line with calculations of the sensitivity of cone vision where the horse eye and human eye again are similar. The advantage of the large eye of the horse lies not in colour vision at night, but probably instead in achromatic tasks where presumably signal summation enhances sensitivity.

Flight behaviour of the hawkmoth Manduca sexta towards unimodal and multimodal targets.

SUMMARY Here, we analyse the flight behaviour of the hawkmoth Manduca sexta while it approaches three different artificial flower stimuli: a clearly visible blue flower, an invisible scented flower and a flower that is both visible and scented. By tracking the moths in fine temporal detail, we find that flight towards an artificial flower differs depending on whether the stimulus is unimodal (either visual or olfactory) or multimodal (both visual and olfactory). In all three cases, the moth reduces its speed as it nears the target but the speed is higher overall when the visual stimulus is not present. Visual feedback, as well as the concentration gradient of the odour, is used to guide the moths towards the stimulus. The main difference in flight behaviour between an approach towards a visual and a multimodal stimulus is that the olfactory information makes the moths turn more rapidly towards the multimodal stimulus. We also find that moths extend their proboscises in front of a clearly visible feeder independent of whether an odour is present. In contrast, a scented transparent artificial flower only occasionally triggers this response.

A Model of Selection between Stimulus and Place Strategy in a Hawkmoth

In behavioral experiments, the hawkmoth Deilephila elpenor can learn both the color and the position of artificial flowers. When very similar colors are used, moths select the correct color during the first test on a given day, thus using a stimulus strategy, but after repeated rewards, they switch to a place strategy and choose the flower in the position where they received the reward. When dissimilar colors are used, the moths continue to select flowers based on color and ignore position. We show how a computational model can reproduce the behavior in the experimental situation. The aim of the model is to investigate which learning and behavior selection strategies are necessary to reproduce the behavior observed in the experiment. The model is based on behavioral data and the sensitivities of the moth photoreceptors. The model consists of a number of interacting behavior systems that are triggered by specific stimuli and control specific behaviors. The ability of the moth to learn the colors of different flowers and the adaptive processes involved in the choice between stimulus-approach and place-approach strategies are reproduced very accurately by the model. The model has implications both for further studies of the ecology of the animal and for robotic systems.