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Experimental study on the liquid-feeding phenomena of butterflies

Experimental study on the liquid-feeding phenomena of butterflies
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Butterflies have developed effective liquid-feeding strategies with a long coiled proboscis and a cibarial pump inside their head. Butterflies suck liquid through the proboscis using a pressure gradient induced by the systaltic operation of the cibarial pump. In addition, butterflies with the brush-tipped proboscis can effectively suck liquid from wet surfaces. The drinking mechanism of butterflies is closely related to the morphological features of the proboscis and dynamic the behaviors of the cibarial pump. However, the proboscis has been considered as a simple tube in most previous studies, and the dynamic behaviors of the cibarial pump have not been studied in detail. In this study, the functional features of the proboscis and the pumping mechanism of the cibarial pump were experimentally investigated. Based on these results, the liquid-feeding strategies of butterflies were examined. In addition, the efficient uptake of liquid from wet surfaces by the brush-tipped proboscis was experimentally demonstrated. To understand the functions of the proboscis in liquid-feeding, the intake flow around the tip of the proboscis was experimentally investigated in detail. The intake flow was quantitatively visualized using a micro-PIV (particle image velocimetry) velocity field measurement technique. As a result, the liquid-feeding process consisted of an intake phase, an ejection phase and a rest phase. When butterflies suck liquid, the liquid was not sucked into the apical tip of the proboscis, but into the dorsal linkage aligned longitudinally along the proboscis. To analyze the main characteristics of the intake flow around a butterfly proboscis, a theoretical model was established by assuming that liquid is sucked into a line sink whose suction rate linearly decreases proximally. The liquid uptake through a line sink is favorable for butterflies. It is unwieldy to regulate the position of the proboscis apex because the butterfly proboscis is long and coiled. Therefore, it is convenient to probe liquid food with the dorsal side of the proboscis. The line sink on the dorsal side is useful to solve the problem of positioning of the proboscis tip on liquid food. To establish the pumping mechanism of butterflies, the dynamic behaviors of the cibarial pump organ were visualized by using synchrotron X-ray micro-imaging technique. In addition, an ellipsoidal pump model was established based on the results of X-ray micro-CT (computed tomography) measurement. To determine the relationship between the cyclic variation of the pump volume and the liquid-feeding flow, the intake flow rate at the tip of the proboscis were measured using a micro-PIV technique. Reynolds and Womersley numbers of liquid-feeding flow in the proboscis were approximately 1.40 and 0.129, respectively. Thus, the liquid-feeding flow could be characterized as a quasi-steady state laminar flow. Considering these results, the liquid-feeding strategies were analyzed on the basis of energy consumption. The relationship between the proboscis and the cibarial pump was established for the case of minimum energy consumption for liquid feeding. The effect of the brush-tipped proboscis of a butterfly on wet-surface feeding was experimentally demonstrated. The tip region of the proboscis was observed, especially two microstructures; the brush-like sensilla styloconica and the intake slits through which liquid passes into the proboscis. The sensilla styloconica were connected laterally to the intake slits in the tip region. The liquid-feeding flow between the proboscis and the wet surface was measured by a micro-PIV technique. During liquid feeding, the sensilla styloconica region accumulated liquid by pinning the air-liquid interface to the tips of the sensilla styloconica, thus the intake slit region remained immersed. The film flow that passes through the sensilla styloconica region showed a parabolic velocity profile, and the corresponding flow rate could be proportional to the cubed length of the sensilla styloconica. Based on these observations, the sensilla styloconica is found to promote the uptake of liquid from wet surfaces. The present results would be helpful to understand the liquid-feeding strategies of butterflies in the view point of fluid mechanics, and they may inspire the development of efficient microfluidic devices for sucking liquids.
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