A previously unknown feeding mode in millipedes and the convergence of fluid feeding across arthropods.

Leif Moritz,Jörg U Hammel,Thomas Wesener,Elena Borisova,Alexander Blanke

doi:10.1126/sciadv.abm0577

Abstract

We report fluid feeding with a sucking pump in the arthropod class Diplopoda, using a combination of synchrotron tomography, histology, electron microscopy, and three-dimensional reconstructions. Within the head of nine species of the enigmatic Colobognatha, we found a pumping chamber, which acts as positive displacement pump and is notably similar to that of insects, showing even fine structural convergences. The sucking pump of these millipedes works together with protractible mouthparts and externally secreted saliva for the acquisition of liquid food. Fluid feeding is one of the great evolutionary innovations of terrestrial arthropods, and our study suggests that it evolved with similar biomechanical solutions convergent across all major arthropod taxa. While fluid-feeding insects are megadiverse today, it remains unclear why other lineages, such as Colobognatha, are comparably species poor.

Highlights

Arthropods are the most diverse group of animals, and they evolved an immense variety of feeding mechanisms
Liquids are drawn into the food canal and transported into the foregut by a combination of capillary forces and a pressure gradient created by a volumetric change of the pumping chamber. These pumping chambers are usually formed by modifications of the cibarium, a preoral chamber anterior of the actual mouth, and show a common morphological pattern: The chamber consists of a rigid sclerotized floor, a flexible roof, which is raised by strong dilator muscles to expand the lumen, and anterior and posterior valves or muscles, which direct the flow of fluids
Our histology, scanning electron microscopy (SEM), and micro– computed tomography ( CT) observations showed that the three lineages Polyzoniida, Siphonocryptida, and Siphonophorida share several features regarding their head morphology and their feeding apparatus, which cannot be found in any other non–colobognathan millipedes [13, 15]

Summary

Introduction

Arthropods are the most diverse group of animals, and they evolved an immense variety of feeding mechanisms. Different pumping mechanisms evolved for the transport of fluids from the exterior into the alimentary canal All these pumping systems rely on creating negative pressure to draw in liquids. Liquids are drawn into the food canal and transported into the foregut by a combination of capillary forces and a pressure gradient created by a volumetric change of the pumping chamber These pumping chambers are usually formed by modifications of the cibarium, a preoral chamber anterior of the actual mouth, and show a common morphological pattern: The chamber consists of a rigid sclerotized floor, a flexible roof, which is raised by strong dilator muscles to expand the lumen, and anterior and posterior valves or muscles, which direct the flow of fluids. Similar structures are unknown from millipedes, which mainly feed on dead plant material with biting-chewing mouthparts [13]

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Conclusion