Structural and physical determinants of the proboscis–sucking pump complex in the evolution of fluid-feeding insects

Scientific Reports, Jul 2017

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.

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Structural and physical determinants of the proboscis–sucking pump complex in the evolution of fluid-feeding insects

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. Introduction Insects that feed on fluids have unique sucking mouthparts1, 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 animals3,4,5. Ever since Darwin predicted that a sphinx moth with an extraordinarily long proboscis feeds from the equally long nectar spur of the orchid Angraecum sesquipedale 6, 7, feeding devices of insects have been a popular subject of evolutionary biology3, 4, 8,9,10,11. Evolution and diversification of insects and their feeding organs within the context of device morphology, properties, and functional performance are among the most attractive and demanding areas of study12, 13. Consideration of the organism as a hierarchical system with different levels of structure and activity requires identification of the mechanisms for division of labor and correlation between the structural units, and their adaptability to environmental changes12,13,14. This idea has been succesfully investigated for vertebrate feeding devices15, 16 but has not caught the attention of those investigating insect feeding devices. Beginning with the seminal works of Bennet-Clark17, Tawfik18, and Kingsolver and Daniel2, 19,20,21, performance of insect fluid feeders has been evaluated on the basis of the proboscis22, 23. The sucking pump, which generates the suction pressure, was largely set aside in the structural hierarchy of insect feeding organs. Kingsolver and Daniel hypothesized that muscular energy of the insect is spent on combating viscous friction of fluid moving through the proboscis20, 21. This hypothesis allowed them to decouple the pump from the proboscis. However, physiological features of the pump cannot guarantee that viscous dissipation of moving fluid in the pump is always negligible; X-ray phase-contrast imaging experiments24,25,26 and neurophysiological analysis of the lepidopteran sucking pump27 revealed complex liquid flow through the pump, adding a degree of doubt to this assumption. Estimates of pressure generated by the sucking pump of Lepidoptera with long proboscises28 show that to defeat enormously high viscous dissipation during unidirectional flow of liquid through the food canal requires the insect to invoke other physiological and behavioral mechanisms. Over evolutionary time, as insects came to inhabit nearly all terrestrial and freshwater habitats, fluid feeders adapted to feed from a variety of resources, probing into crevices, cavities, and pores to acquire liquids29,30,31. Insects can feed on thick, highly viscous liquids, such as honey, or on thin, almost inviscid mineral water2, 22, 29,30,31. Thus, in the evolutionary development of insect feeding organs, the variety of possible scenarios for structural-functional performance of the pump–proboscis pair cannot be ignored. Evolution of insects has involved both the increase and decrease of organ size31,32,33,34,35; accordingly, feeding devices of insects encompass a wide range of sizes, from those of extremely small insects such as aphids36, 37 to 20-centimeter long proboscises and powerful sucking pumps of some sphinx moths7. This large span of sizes is associated with different behavioral strategies and physical and materials organization of the feeding devices. Flow in the proboscis and sucking pump during fluid uptake is interdependent. The geometry of sucking pumps of fluid-feeding insects is complex, many details are poorly understood, and quantitative morphological data are scarce17, 27, 38,39,40. To illustrate a range of sizes of the sucking pump, the p (...truncated)


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Konstantin G. Kornev, Arthur A. Salamatin, Peter H. Adler, Charles E. Beard. Structural and physical determinants of the proboscis–sucking pump complex in the evolution of fluid-feeding insects, Scientific Reports, 2017, Issue: 7, DOI: 10.1038/s41598-017-06391-w