Fuelling on the wing: sensory ecology of hawkmoth foraging

Abstract

Hawkmoths (Lepidoptera, Sphingidae) comprise around 1500 species, most of which forage on nectar from flowers in their adult stage, usually while hovering in front of the flower. The majority of species have a nocturnal lifestyle and are important nocturnal pollinators, but some species have turned to a diurnal lifestyle. Hawkmoths use visual and olfactory cues including CO₂ and humidity to detect and recognise rewarding flowers; they find the nectary in the flowers by means of mechanoreceptors on the proboscis and vision, evaluate it with gustatory receptors on the proboscis, and control their hovering flight position using antennal mechanoreception and vision. Here, we review what is presently known about the sensory organs and sensory-guided behaviour that control feeding behaviour of this fascinating pollinator taxon. We also suggest that more experiments on hawkmoth behaviour in natural settings are needed to fully appreciate their sensory capabilities.

Keywords: Colour vision; Mechanoreception; Olfaction; Sensory ecology; Sphingidae.

Fig. 1

Different hawkmoth species and their food flowers. The hummingbird hawkmoth Macroglossum stellatarum (a) is one of the few day active Sphingids. It overlaps in large parts of its Eurasian habitat and many food plants with the nocturnal elephant hawkmoth Deilephila elpenor (b). Moths of the genus Manduca, here M. quinquemaculata (c) are popular models for olfactory and flight control research. They are distributed over most of the American continent and are nectar feeders like M. stellatarum and D. elpenor. The death’s head hawkmoth Acherontia atropos (d) is well known from popular culture. It does not feed on nectar, but extracts honey from honeycombs using its short needle-like proboscis. On the other end of the spectrum of proboscis lengths lies Xanthopan morganii (e), which has the longest proboscis amongst Sphingidae with an impressive average of 22 cm (Photos: Michael Pfaff, illustration in e from Wallace 1867)

Fig. 2

Hawkmoth senses. a The antennae of hawkmoths (left a male, right a female M. stellatarum, scale bar 100 µm) contain thousands of olfactory sensilla. Each sensillum contains dendrites of one or more olfactory receptor neurons. Axons of olfactory neurons with the same olfactory receptors project to the same glomerulus in the antennal lobes (modified after Balkenius et al. ; Haupt et al. 2010). b Hawkmoth eyes show a pseudopupil, a result of their superposition compound eyes. Light from several facets is focussed onto a single ommatidium, strongly increasing sensitivity. Each ommatidium contains 9 photoreceptor cells—2 receptors expressing UV- or blue-sensitive opsins (dv, sensitive to 357 and 450 nm in M. sexta), 6 receptors expressing green-sensitive opsin (ap, ob, 520 nm), and one basal cell (not shown) likely green-sensitive (White et al. 2003). Each ommatidium is surrounded by a tracheal tapetum, which reflects light through the superposition pupil and is responsible for the eye glow. c The hawkmoth proboscis contains gustatory and mechanosensory sensilla assessing nectar quality (top row: sensillum ampullaceum, s. chaeticum, bottom row: s. basiconicum, s. styloconicum, scale bars: 100 µm; modified from Kelber 2003). d The antennal base carries Johnston’s organ with mechanoreceptors involved in the control of head and body posture and Böhm’s bristles with receptors controlling antennal position (modified from Kloppenburg et al. 1997)

Fig. 3

Sensory cues of hawkmoth flower selection. Hawkmoths use different sensory cues to select and evaluate flowers at different stages of approach and feeding. a Attraction and selection of flowers from a distance (several metres) occurs via olfactory cues, including CO₂ sensing, as well as air humidity. Hawkmoths are also attracted by the colour of the flower. Naïve moths prefer blue (and to a lesser extend yellow) flowers at bright light intensities, and white flowers (to a lesser extend blue) at nocturnal intensities. These preferences can change with experience. b As moths get close to the flower, visual patterns help diurnal species to guide the proboscis to the entrance of the nectary. Nocturnal moths rely more strongly on mechanosensory cues provided by the shape and mechanical guides of the flower. c When moths have inserted their proboscis into the nectary, they evaluate the nectar for its viscosity and for sugars and secondary metabolites

Fig. 4

Sensory modalities controlling flight at the flower. To control their position at the flower and counteract disturbances (a) caused, for instance, by wind, hawkmoths use vision, and antennal mechanosensation. These senses operate in different temporal frequency ranges, with vision operating at low and mechanosensory input at high frequencies. Hawkmoths can also track the position of the flower (b) using vision and mechanosensory feedback from the proboscis. While hovering, hawkmoths visually sense aerial predators (c). Whether hawkmoths use sensory mechanisms other than vision to avoid predators at flowers is unknown, only a few species have evolved ears sensitive to bat sound