Abstract
Fluid-feeding insects have evolved a unique strategy to distribute the labor between a liquid-acquisition device (proboscis) and a sucking pump. We theoretically examined physical constraints associated with coupling of the proboscis and sucking pump into a united functional organ. Classification of fluid feeders with respect to the mechanism of energy dissipation is given by using only two dimensionless parameters that depend on the length and diameter of the proboscis food canal, maximum expansion of the sucking pump chamber, and chamber size. Five species of Lepidoptera — White-headed prominent moth (Symmerista albifrons), White-dotted prominent moth (Nadata gibosa), Monarch butterfly (Danaus plexippus), Carolina sphinx moth (Manduca sexta), and Death’s head sphinx moth (Acherontia atropos) — were used to illustrate this classification. The results provide a rationale for categorizing fluid-feeding insects into two groups, depending on whether muscular energy is spent on moving fluid through the proboscis or through the pump. These findings are relevant to understanding energetic costs of evolutionary elaboration and reduction of the mouthparts and insect diversification through development of new habits by fluid-feeding insects in general and by Lepidoptera in particular.
Highlights
Insects that feed on fluids have unique sucking mouthparts[1, 2]
We hypothesize that in insects with a small ratio of chamber size to proboscis length, energy dissipation should be associated with the viscous drag of liquid moving through the proboscis (“proboscis dissipation”), whereas in insects with a large ratio of chamber size to proboscis length, energy dissipation should come from the viscous drag of liquid on the moving pump plunger (“pump dissipation”)
We adopt the terminology used by Davis & Hildebrand[27] to describe the two-part sucking pump of adult Lepidoptera (Fig. 1), which is composed of an anterior cibarium that leads into a larger, posterior buccal chamber
Summary
Insects that feed on fluids have unique sucking mouthparts[1, 2]. Over the past 350 or so million years, fluid feeders have diversified to exploit different food sources including nectar, phloem, xylem, and cellular contents of plants, and carrion, dung, sweat, tears, urine, and blood of animals[3,4,5]. Evolution of insects has involved both the increase and decrease of organ size[31,32,33,34,35]; feeding devices of insects encompass a wide range of sizes, from those of extremely small insects such as aphids[36, 37] to 20-centimeter long proboscises and powerful sucking pumps of some sphinx moths[7]. This large span of sizes is associated with different behavioral strategies and physical and materials organization of the feeding devices. The results allow quantitative classification of the role of different feeding parts, emphasizing division of labor between them, as well as their integration
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