Experimental analysis of the liquid-feeding mechanism of the butterfly Pieris rapae

Abstract

The butterfly Pieirs rapae drinks liquid using a long proboscis. A high pressure gradient is induced in the proboscis when cibarial pump muscles contract. However, liquid feeding through the long proboscis poses a disadvantage of high flow resistance. Hence, butterflies may possess special features to compensate for this disadvantage and succeed in foraging. The main objective of this study is to analyze the liquid-feeding mechanism of butterflies. The systaltic motion of the cibarial pump organ was visualized using the synchrotron X-ray imaging technique. In addition, an ellipsoidal pump model was established based on synchrotron X-ray micro-computed tomography. To determine the relationship between the cyclic variation of the pump volume and the liquid-feeding flow, velocity fields of the intake flow at the tip of the proboscis were measured using micro-particle image velocimetry. Reynolds and Womersley numbers of liquidfeeding flow in the proboscis were ~1.40 and 0.129, respectively. The liquid-feeding flow could be characterized as a quasi-steady state laminar flow. Considering these results, we analyzed the dimensions of the feeding apparatus on the basis of minimum energy consumption during the liquid-feeding process. The relationship between the proboscis and the cibarial pump was determined when minimum energy consumption occurs. As a result, the volume of the cibarial pump is proportional to the cube of the radius of the proboscis. It seems that the liquid-feeding system of butterflies and other long-proboscid insects follow the cube relationship. The present results provide insights into the feeding strategies of liquid-feeding butterflies.

Nectar feeding beyond the tongue: hummingbirds drink using phase-shifted bill opening, flexible tongue flaps and wringing at the tips

“…Synchrotron imaging has also been used to study drinking in insects, but its micrometric resolution is often associated with small fields of view and low frame rates (e.g. 30 frames s −1 ; Kim et al, 2011 ; Lee et al, 2014 ; Kikuchi et al, 2018 ), and lateral views only. Additionally, these X-ray setups are not portable, impart high radiation exposures, and require the addition of electron-dense substances, which further remove the results from the inferences about natural function.…”

Structure of the lepidopteran proboscis in relation to feeding guild

“…Spaces between the dorsal legulae facilitate capillary action, supporting the withdrawal of liquids from pools and porous substrates, such as rotting fruit, into the food canal (Monaenkova et al, ). A pump in the head then forces the liquid up the food canal to the gut (Eberhard and Krenn, ; Borrell and Krenn, ; Lee et al, ).…”

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

“…Rapid feeding should therefore be favoured by natural selection (Emlen, 1966;Schoener, 1971;Pyke et al, 1977). Nectar feeding through a tubular proboscis is subject to physical laws of fluid dynamics, and both the morphological configuration of the feeding apparatus and nectar viscosity modify the rate of nectar intake (Daniel et al, 1989;Kim et al, 2011;Lee et al, 2014). Biophysical models describe factors influencing the speed of fluid feeding and therefore help to understand the constraints regarding the evolution of extremely long proboscides (Kingsolver & Daniel, 1979, 1995Lee et al, 2014).…”

“…Nectar feeding through a tubular proboscis is subject to physical laws of fluid dynamics, and both the morphological configuration of the feeding apparatus and nectar viscosity modify the rate of nectar intake (Daniel et al, 1989;Kim et al, 2011;Lee et al, 2014). Biophysical models describe factors influencing the speed of fluid feeding and therefore help to understand the constraints regarding the evolution of extremely long proboscides (Kingsolver & Daniel, 1979, 1995Lee et al, 2014). According to the law of Hagen-Poiseuille, the nectar intake rate of butterflies should increase linearly with increasing pressure difference produced by a suction pump and increase with the radius of the food canal to the exponent four.…”