Burst mode pumping: A new mechanism of drinking in mosquitoes

Abstract

Mosquitoes transport liquid foods into the body using two muscular pumps in the head. In normal drinking, these pumps reciprocate in a stereotyped pattern of oscillation, with a high frequency but small stroke volume. Do mosquitoes modulate their neuromotor programs for pumping to produce different drinking modes? More broadly, what are the mechanical consequences of a two-pump system in insects? To address these questions, we used synchrotron x-ray imaging and fluid mechanical modeling to investigate drinking performance in mosquitoes. X-ray imaging of the pumps during drinking revealed two modes of pumping: continuous reciprocation with multiple small strokes, and a newly discovered ‘burst mode’ involving a single, large-volume stroke. Results from modeling demonstrate that burst mode pumping creates a very large pressure drop and high volume flow rate, but requires a massive increase in power, suggesting that continuous pumping is more economical for drinking. Modeling also demonstrates that, from one mode of pumping to the other, the mechanical role of the individual pumps changes. These results suggest that the advantage of a two-pump system in insects lies in its flexibility, enabling the animal to pump efficiently or powerfully as demanded by environmental considerations.

Waveforms From Stylet Probing of the Mosquito Aedes aegypti (Diptera: Culicidae) Measured by AC–DC Electropenetrography

“…These studies show that, indeed, the pumps are sequentially coordinated; the cibarial and pharyngeal pumps fire nearly at the same time, but with a small phase lag (Kim et al 2011(Kim et al , 2012(Kim et al , 2013. The most recent work (Kikuchi et al 2018) demonstrated that there are two types of pumping: continuous pumping, in which the cibarial pump performs most of the work, and burst-mode pumping, in which the pharyngeal pump does most of the work. Furthermore, in continuous feeding, the cibarial pump does not expand to its greatest possible extent, and is acting as a pass-through to the pharyngeal pump (Kim et al 2013, Kikuchi et al 2018).…”

“…The most recent work (Kikuchi et al 2018) demonstrated that there are two types of pumping: continuous pumping, in which the cibarial pump performs most of the work, and burst-mode pumping, in which the pharyngeal pump does most of the work. Furthermore, in continuous feeding, the cibarial pump does not expand to its greatest possible extent, and is acting as a pass-through to the pharyngeal pump (Kim et al 2013, Kikuchi et al 2018). In burst-mode feeding, both pumps are expanded to their fullest extent.…”

“…In burst-mode feeding, both pumps are expanded to their fullest extent. In burstmode feeding, both pumps are expanded to their fullest extent, providing 1.6× (cibarial) and 19× (pharyngeal) the maximum volume of continuous pumping (Kikuchi et al 2018).…”

“…Similarly, we believe that degree of pump expansion in mosquitoes feeding is indicated by amplitude of the M1 peak. Kikuchi et al (2018) proposed two hypotheses to explain the behavioral role of maximal pharyngeal pump expansion (thus a very large vacuum at the tip of the proboscis) in burst-mode feeding: 1) the 'clearance' hypothesis, to clear blockages in the system, and 2) the 'priming' hypothesis, to prime the food canal at the start of pumping. We agree with the likelihood of both of these hypotheses.…”

“…However, our work strongly suggests a third, which we term the 'big gulp' hypothesis. The idea was actually suggested by Kikuchi et al (2018), who explain that burst-mode feeding could 'provide quick boosts in volume flow rate, enabling faster drinking bouts that would help the mosquito to avoid detection'. They also state that blood, unlike sugar water, is a non-Newtonian liquid, whose properties may influence the way pumping of blood could differ from that of sugar water.…”