Insect wings are composed of thin membranes that are supported by a system of interconnected veins. Veins are lined by a layer of epidermal cells, and traversing many veins are a trachea and a nerve, with the latter eventually connecting to sensory cells. The proper function of cells within the wings requires that nutrients, waste and signaling molecules be efficiently transported into and out of these appendages. This transport, along with processes that are required for wing inflation and maturation following eclosion, is dependent on the insect circulatory system.

The circulatory system of insects is composed of a fluid known as hemolymph, an open body cavity known as the hemocoel, and a series of muscular pumps. The primary pump is the dorsal vessel, which is a muscular tube that extends the length of the insect and is divided into a heart in the abdomen and an aorta in the thorax and head. While effective in disseminating molecules and immune cells to most parts of the body, the propulsion created by the dorsal vessel is insufficient to deliver hemolymph to some regions of the body that are either narrow or distant from the dorsal vessel. Thus, insects have evolved accessory pulsatile organs (APOs, or auxiliary hearts) that drive hemolymph into areas such as the antennae, the wings and the ventral abdomen.

In this study, we scrutinized the circulatory physiology of the wing of the malaria mosquito, Anopheles gambiae. We show that:

1. 1.Mosquitoes contain a single wing heart that circulates hemolymph into both wings.
   

2. 2.The wing heart contracts approximately 3 times per second (Hz), and does so in a manner that is independent of the contractions of the dorsal vessel.
   

3. 3.Rather than pushing hemolymph into the wing in a manner similar to how the antennal hearts push hemolymph into the antennae, the wing heart aspirates hemolymph out of the wings.
   

4. 4.Hemolymph enters the wing via anterior veins and exits via posterior veins.
   

5. 5.The velocity of hemolymph increases as it exits the wing.
   

6. 6.We provide a comprehensive map of hemolymph flow in the wings.
   

Article citation:

Chintapalli, R.T.V., and J.F. Hillyer. 2016. Hemolymph circulation in insect flight appendages: physiology of the wing heart and circulatory flow in the wings of the mosquito Anopheles gambiae. Journal of Experimental Biology. 219: 3945-3951. (PMID: 27742896) (See it in JEB) (Email me for a pdf copy)

Graphical abstract:

Article abstract:

The wings of insects are composed of membranes supported by interconnected veins. Within these veins are epithelial cells, nerves and tracheae, and their maintenance requires the flow of hemolymph. For this purpose, insects employ accessory pulsatile organs (auxiliary hearts) that circulate hemolymph throughout the wings. Here, we used correlative approaches to determine the functional mechanics of hemolymph circulation in the wings of the malaria mosquito Anopheles gambiae. Examination of sectioned tissues and intravital videos showed that the wing heart is located underneath the scutellum and is separate from the dorsal vessel. It is composed of a single pulsatile diaphragm (indicating that it is unpaired) that contracts at 3 Hz and circulates hemolymph throughout both wings. The wing heart contracts significantly faster than the dorsal vessel, and there is no correlation between the contractions of these two pulsatile organs. The wing heart functions by aspirating hemolymph out of the posterior wing veins, which forces hemolymph into the wings via anterior veins. By tracking the movement of fluorescent microspheres, we show that the flow diameter of the wing circulatory circuit is less than 1 µm, and we present a spatial map detailing the flow of hemolymph across all the wing veins, including the costa, sub-costa, ambient costa, radius, media, cubitus anterior, anal vein and crossveins. We also quantified the movement of hemolymph within the radius and within the ambient costa, and show that hemolymph velocity and maximum acceleration are higher when hemolymph is exiting the wing.