The Arthropod Circulatory System

Mosquito antennae provide sensory input that modulates hostseeking, mating and oviposition behaviors. Thus, mosquitoes must ensure the efficient transport of molecules into and out of these appendages. To accomplish this, mosquitoes and other insects have evolved antennal accessory pulsatile organs (APOs) that drive hemolymph into the antennal space. This study characterizes the structural mechanics of hemolymph propulsion throughout the antennae of Anopheles gambiae. Using intravital video imaging, we show that mosquitoes possess paired antennal APOs that are located on each side of the head's dorsal midline. They are situated between the frons and the vertex in an area that is dorsal to the antenna but ventral to the medial-most region of the compound eyes. Antennal APOs contract in synchrony at 1 Hz, which is 45% slower than the heart. By means of histology and intravital imaging, we show that each antennal APO propels hemolymph into the antenna through an antennal vessel that traverses the length of the appendage and has an effective diameter of 1-2 μm. When hemolymph reaches the end of the appendage, it is discharged into the antennal hemocoel and returns to the head. Because a narrow vessel empties into a larger cavity, hemolymph travels up the antenna at 0.2 mm s −1 but reduces its velocity by 75% as it returns to the head. Finally, treatment of mosquitoes with the anesthetic agent FlyNap (triethylamine) increases both antennal APO and heart contraction rates. In summary, this study presents a comprehensive functional characterization of circulatory physiology in the mosquito antennae.KEY WORDS: Antenna, Hemocoel, Circulatory physiology, Antennal heart, Heart, Vessel INTRODUCTIONThe antennae of insects are involved in the detection of chemical, tactile, thermal and auditory stimuli (Chapman and Simpson, 2013). The antennae also mechanically assist during the mating of fleas, and contain the timing elements of the sun compass that drives the autumn migration of monarch butterflies (Hsu and Wu, 2001;Merlin et al., 2009). In mosquitoes, the detection of near-field sound by the antennae's Johnston's organs influences courtship and mating, and the reception of odorant and thermal cues by antennal receptor neurons controls oviposition and host-seeking behaviors (Cator et al., 2009;Wang et al., 2009;Carey et al., 2010;Rinker et al., 2013). Because antennae are intricately involved in essential physiological processes, insects must ensure that molecules required for proper RESEARCH ARTICLEDepartment of Biological Sciences, Vanderbilt University, Nashville, TN 37235, USA. antennal functioning are efficiently transported into and out of these peripheral sensory appendages.The primary manner by which insects transport nutrients, hormones, waste and other molecules from one region of the body to another is by circulating a fluid medium called hemolymph through an open body cavity called the hemocoel Klowden, 2013). The main pump that drives hemolymph circulation is called the dorsal vessel, which is a muscula...

Section: Research Articlementioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Hemolymph circulation in insect sensory appendages: functional mechanics of antennal accessory pulsatile organs (auxiliary hearts) in the mosquitoAnopheles gambiae

Boppana

Hillyer

2014

“…Insects have an open circulatory system that transports nutrients, waste, hormones, immune factors and other molecules to all regions of the body Klowden, 2013;Wirkner et al, 2013;Hillyer, 2015). This circulatory system is composed of hemolymph (insect blood), the hemocoel (open body cavity) and several contractile pumps.…”

Section: Introductionmentioning

confidence: 99%

CCAP and FMRFamide-like peptides accelerate the contraction rate of the antennal accessory pulsatile organs (auxiliary hearts) of mosquitoes

Suggs

Jones

Murphree

et al. 2016

Insects rely on specialized accessory pulsatile organs (APOs), also known as auxiliary hearts, to propel hemolymph into their antennae. In most insects, this is accomplished via the pulsations of a pair of ampulla located in the head, each of which propels hemolymph across an antenna via an antennal vessel. Once at the distal end of the appendage, hemolymph returns to the head via the antennal hemocoel. Although the structure of the antennal hearts has been elucidated in various insect orders, their hormonal modulation has only been studied in cockroaches and other hemimetabolous insects within the superorder Polyneoptera, where proctolin and FMRFamide-like peptides accelerate the contraction rate of these auxiliary hearts. Here, we assessed the hormonal modulation of the antennal APOs of mosquitoes, a group of holometabolous (Endopterygota) insects within the order Diptera. We show that crustacean cardioactive peptide (CCAP), FMRFamide and SALDKNFMRFamide increase the contraction rate of the antennal APOs and the heart of Anopheles gambiae. Both antennal hearts are synchronously responsive to these neuropeptides, but their contractions are asynchronous with the contraction of the heart. Furthermore, we show that these neuropeptides increase the velocity and maximum acceleration of hemolymph within the antennal space, suggesting that each contraction is also more forceful. To our knowledge, this is the first report demonstrating that hormones of a holometabolous insect modulate the contraction dynamics of an auxiliary heart, and the first report that shows that the hormones of any insect accelerate the velocity of hemolymph in the antennal space.

“…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 (Pass et al, 2006;Wirkner et al, 2013;Hillyer, 2015). 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.…”

Section: Introductionmentioning

confidence: 99%

Hemolymph circulation in insect flight appendages: physiology of the wing heart and circulatory flow in the wings of the mosquito,Anopheles gambiae

Chintapalli

Hillyer

2016

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.