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

Abstract

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.

Structure of the lepidopteran proboscis in relation to feeding guild

“…Selection pressures exerted by diverse floral structure (Soltis et al, ; Tiple et al, ) probably have resulted in the diversity of proboscis structure among flower visitors. The best‐known relationship between flower and proboscis structure is the corresponding length of the floral tube and the proboscis (Kunte, ; Krenn, ; Arditti et al, ; Bauder et al, ); however, other patterns can be found. The Papilionidae and Nymphalidae, for example, which feed on nectar from similar (e.g., larger) flowers (Tiple et al, ), have similar dorsal legular shapes that differ from those of pierids.…”

Foraging efficiency and size matching in a plant–pollinator community: the importance of sugar content and tongue length

“…; Bauder et al . ). For hummingbirds, it was found that the handling time of nectar resources was related to the degree of matching between bill length and nectar tube depth (Maglianesi et al .…”

“…In contrast, several studies suggest that it takes pollinators with a long proboscis longer to handle short-tubed flowers than pollinators with a short proboscis; in other words these studies suggest that tongues can be too long (e.g. Inouye 1980;Plowright & Plowright 1997;Kunte 2007;Karolyi et al 2013;Bauder et al 2015). For hummingbirds, it was found that the handling time of nectar resources was related to the degree of matching between bill length and nectar tube depth (Maglianesi et al 2014).…”

The ecological role of extremely long-proboscid Neotropical butterflies (Lepidoptera: Hesperiidae) in plant-pollinator networks

“…The average nectar amount that an extremely long-proboscid skipper butterfly could take up during a flower visit is roughly estimated at 7.1 ll (Bauder et al 2015; amount of ingested nectar was calculated by multiplying the average nectar intake rate of skippers that visited Calathea flowers with the average suction time on C. crotalifera flowers). Given that the average nectar amount of a flower belonging to the genus Calathea measures about 14.4 ll (Ruppel 2013), a skipper butterfly could empty half of a flower's nectar reserves in a single visit.…”