Accessory Pulsatile Organs Research Articles

The Insect Circulatory System: Structure, Function, and Evolution.

Although the insect circulatory system is involved in a multitude of vital physiological processes, it has gone grossly understudied. This review highlights this critical physiological system by detailing the structure and function of the circulatory organs, including the dorsal heart and the accessory pulsatile organs that supply hemolymph to the appendages. It also emphasizes how the circulatory system develops and ages and how, by means of reflex bleeding and functional integration with the immune system, it supports mechanisms for defense against predators and microbial invaders, respectively. Beyond that, this review details evolutionary trends and novelties associated with this system, as well as the ways in which this system also plays critical roles in thermoregulation and tracheal ventilation in high-performance fliers. Finally, this review highlights how novel discoveries could be harnessed for the control of vector-borne diseases and for translational medicine, and it details principal knowledge gaps that necessitate further investigation.

Insect heart rhythmicity is modulated by evolutionarily conserved neuropeptides and neurotransmitters.

Insects utilize an open circulatory system to transport nutrients, waste, hormones and immune factors throughout the hemocoel. The primary organ that drives hemolymph circulation is the dorsal vessel, which is a muscular tube that traverses the length of the body and is divided into an aorta in the head and thorax, and a heart in the abdomen. The dorsal vessel is myogenic, but its rhythmicity is modulated by neuropeptides and neurotransmitters. This review summarizes how neuropeptides such as crustacean cardioactive peptide (CCAP), FMRFamide-like peptides, proctolin, allatotropin and allatostatin modulate the heart contraction rate and the directionality of heart contractions. Likewise, it discusses how neurotransmitters such as serotonin, octopamine, glutamate and nitric oxide influence the heart rate, and how transcriptomic and proteomic approaches are advancing our understanding of insect circulatory physiology. Finally, this review argues that the immune system may modulate heart rhythmicity, and discusses how the myotropic activity of cardioactive factors extends to the accessory pulsatile organs, such as the auxiliary hearts of the antennae.

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

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.

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

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.

A new kind of auxiliary heart in insects: functional morphology and neuronal control of the accessory pulsatile organs of the cricket ovipositor

IntroductionIn insects, the pumping of the dorsal heart causes circulation of hemolymph throughout the central body cavity, but not within the interior of long body appendages. Hemolymph exchange in these dead-end structures is accomplished by special flow-guiding structures and/or autonomous pulsatile organs (“auxiliary hearts”). In this paper accessory pulsatile organs for an insect ovipositor are described for the first time. We studied these organs in females of the cricket Acheta domesticus by analyzing their functional morphology, neuroanatomy and physiological control.ResultsThe lumen of the four long ovipositor valves is subdivided by longitudinal septa of connective tissue into efferent and afferent hemolymph sinuses which are confluent distally. The countercurrent flow in these sinuses is effected by pulsatile organs which are located at the bases of the ovipositor valves. Each of the four organs consists of a pumping chamber which is compressed by rhythmically contracting muscles. The morphology of the paired organs is laterally mirrored, and there are differences in some details between the dorsal and ventral organs. The compression of the pumping chambers of each valve pair occurs with a left-right alternating rhythm with a frequency of 0.2 to 0.5 Hz and is synchronized between the dorsal and ventral organs. The more anteriorly located genital chamber shows rhythmical lateral movements simultaneous to those of the ovipositor pulsatile organs and probably supports the hemolymph exchange in the abdominal apex region. The left-right alternating rhythm is produced by a central pattern generator located in the terminal ganglion. It requires no sensory feedback for its output since it persists in the completely isolated ganglion. Rhythm-modulating and rhythm-resetting interneurons are identified in the terminal ganglion.ConclusionThe circulatory organs of the cricket ovipositor have a unique functional morphology. The pumping apparatus at the base of each ovipositor valve operates like a bellow. It forces hemolymph via sinuses delimited by thin septa of connective tissue in a countercurrent flow through the valve lumen. The pumping activity is based on neurogenic control by a central pattern generator in the terminal ganglion.

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

Mosquito antennae provide sensory input that modulates host-seeking, 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.

Neuropeptide action in insects and crustaceans.

Physiological processes are regulated by a diverse array of neuropeptides that coordinate organ systems. The neuropeptides, many of which act through G protein-coupled receptors, affect the levels of cyclic nucleotides (cAMP and cGMP) and Ca(2+) in target tissues. In this perspective, their roles in molting, osmoregulation, metabolite utilization, and cardiovascular function are highlighted. In decapod crustaceans, inhibitory neuropeptides (molt-inhibiting hormone and crustacean hyperglycemic hormone) suppress the molting gland through cAMP- and cGMP-mediated signaling. In insects, the complex movements during ecdysis are controlled by ecdysis-triggering hormone and a cascade of downstream neuropeptides. Adipokinetic/hypertrehalosemic/hyperprolinemic hormones mobilize energy stores in response to increased locomotory activity. Crustacean cardioacceleratory (cardioactive) peptide, proctolin, and FMRFamide-related peptides act on the heart, accessory pulsatile organs, and excurrent ostia to control hemolymph distribution to tissues. The osmoregulatory challenge of blood gorging in Rhodnius prolixus requires the coordinated release of serotonin and diuretic and antidiuretic hormones acting on the midgut and Malpighian tubules. These studies illustrate how multiple neuropeptides allow for flexibility in response to physiological challenges.

Accessory pulsatile organs: evolutionary innovations in insects.

In addition to the dorsal vessel ("heart"), insects have accessory pulsatile organs ("auxiliary hearts") that supply body appendages with hemolymph. They are indispensable in the open circulatory system for hemolymph exchange in antennae, long mouthparts, legs, wings, and abdominal appendages. This review deals with the great diversity in the functional morphology and the evolution of these accessory pulsatile organs. In primitive insects, hemolymph is supplied to antennae and cerci by arteries connected to the dorsal vessel. In higher insects, however, these arteries were decoupled and associated with autonomous pumps that entered their body plan as evolutionary innovations. To ensure hemolymph supply to legs, wings, and some other appendages, completely new accessory pulsatile organs evolved. The muscular components of these pulsatile organs and their elastic antagonists were recruited from various organ systems and assembled to new functional units. In general, it seems that the evolution of accessory pulsatile organs has been determined by developmental and spatial constraints imposed by other organ systems rather than by changes in circulatory demands.

Circulatory organs of Diplura (Hexapoda): the basic design in Hexapoda?

The circulatory systems of Campodea augens and Catajapyx aquilonaris (Hexapoda: Diplura) have been examined by means of light and electron microscopy. Hemolymph flow has also been investigated in vivo. Both species share features that deviate conspicuously from the common textbook design of the insect circulatory system: (i) antennal vessels connected to the anterior end of the dorsal vessel; (ii) presence of a circumoesophageal vessel ring in the head; (iii) a bidirectional flow within the dorsal vessel, made possible by intracardiac valves; (iv) posterior end of the dorsal vessel tube opens into a caudal chamber connected to cercal vessels (in Campodea) or to cercal channels (in Catajapyx); (v) dorsal diaphragm barely realized, ventral diaphragm absent altogether, and (vi) legs without specific organs serving hemolymph circulation. Comparative analysis has revealed that these characters in Diplura represent the most plesiomorphic condition in the circulatory organs of all extant Hexapoda. In the basic evolutionary lineages of insects, some organ components have been lost and the peripheral vessels decoupled from the dorsal vessel; as a result, autonomous accessory pulsatile organs have evolved to supply hemolymph to long body appendages and a unidirectional hemolymph flow mode prevailed within the dorsal vessel.

Wing-hearts in Mecoptera (insecta)

The accessory pulsatile organs for hemolymph circulation in the wings of 7 Mecoptera species were investigated by means of serial semi-thin sections, SEM and TEM. The wing-hearts are located in the dorsal meso- and metathorax, and have no connection to the aorta. Each wing-heart consists of a small hemolymph chamber formed above by the convex scutellum, and below by a horizontal muscular diaphragm. The chamber is connected to the posterior wing veins by a cuticular tube on each side of the body. The diaphragm (10–15 μm thick) is convex in cross-section and consists of transversely extended muscle fibers. Their ultrastructure reveals typical characters of myocardial and other visceral muscle fibers. The diaphragm muscle is innervated by a pair of thin nerves originating from the thoracic ganglion of each corresponding segment. The diaphragm is held in a convex position by numerous elastic strands (2 μm in diameter), which extend through the wing-heart lumen between the scutellum and the diaphragm. The diastolic phase of the wing-heart is caused by contraction of the diaphragm muscle fibers. Thus, the diaphragm flattens and hemolymph is drawn from the posterior wing veins. The systolic phase is caused by the elasticity of the suspending strands after relaxation of the muscle fibers. The elastic strands pull the diaphragm back into convex position and hemolymph is expelled out of the scutellum lumen into the thorax cavity through a valvular opening on the anterior side. The hemolymph flow from the posterior wing base to the scutellum lumen, was visualized by staining the hemolymph. In Panorpa communis the volume of the wing-heart lumen measures 1.6 × 10 −2 mm 3 in the mesothorax, and 1.2 × 10 −2 mm 3 in the metathorax. Each heartbeat transports a maximum of 65% of these volumes. The pumping frequency was 78 ± 20 beats per min, registered with a non-invasive photo-optical method in restrained animals. Corresponding pulsating movements occur as a passive phenomenon of wing-heart activity in a distinct area of the wing base. Only minor differences were found in the construction of wing-hearts among the investigated species, except for Boreus hyemalis, which lacks these accessory circulatory organs. The functional morphology of the wing-hearts in Mecoptera is compared with that of other Holometabola and aspects of the evolution of these organs are discussed.

NervousVersusNeurohormonal Control of Insect Heartbeat

Recording semi-isolated insect heartbeat at one time was an art only to be attempted by the most patient of research workers. Thanks to modern advances in biomedical instrumentation, insect heartbeat measurement by impedance conversion and contact thermography allows not only heartbeat recordings, but recording of accessory pulsatile organs and diaphragm movements. The characteristic heartbeat patterns as recorded from adult insects vary enormously from very regular in orthopteroids to highly irregular in Diptera. Pupal stages in holometabolous insects are characterized by a heartbeat which appears to have little or no nervous influence and is punctuated by cessation for periods up to several hours in some insects. The controversy over nervous and/or hormonal control of insect heartbeat has never been completely resolved. There is now a good deal of evidence for nervous control of the heartbeat of Dipteran adults, Lepidopteran adults, Orthopteran nymphs and adults, Dictyopteran nymphs and adults, and Hymenopteran adults. The evidence of hormonal control of heartbeat remains inferential, and is based mostly on the responses of semi-isolated heart preparations. One of the most important events in recent years in this field has been Brian Brown's elucidation of Proctolin in cooperation with Alvin Starratt in Canada. Proctolin is a suspected neurohormone or neurohumor of the proctodeum which may also be used to regulate heartbeat in insects.

Heartbeat reversal and its coordination with accessory pulsatile organs and abdominal movements in lepidoptera

Haemolymph in certain Lepidoptera at rest is periodically transported from the anterior body to the abdomen and reversed by the coordinated activity of the heart, the accessory pulsatile organs and the abdomen. This oscillatory haemolymph transport is suggested to support haemolymph exchange and air ventilation in the anterior body and wings.

Some aspects of the internal anatomy of the leafhopper Agillia constricta (Homoptera: Cicadellidae).

The gross anatomy of the alimentary canal and malpighian tubules of Agallia constricta (Van Duzee) is described, as well as the histology of their various regions. Rickettsia-like microorganisms and carbonates were found in the midgut. Each salivary gland, consisting of a principal 4-lobed gland and an accessory gland, contains 5 different types of acini. In the male reproductive system there are a pair of testes, each with 6 follicles, a pair of vasa deferentia, and a median ejaculatory duct, plus a pair of accessory glands. Each ovary of the female system is made up of 6 ovarioles, each consisting of terminal filament, germarium, vitellarium, and pedicel. The calyx connects the ovarioles with the lateral oviducts and these open to a common oviduct leading to the genital chamber; 2 small accessory glands and a paragenital gland are present. The central nervous system comprises 4 ganglionic masses: the brain, the subesophageal ganglion, the prothoracic ganglion, and the fused ganglia of mesothorax, metathorax, and abdomen; nerves from these various ganglia innervate the different organs. The circulatory system consists of a dorsal vessel, formed by a 7-chambered heart in the abdomen and an aorta extending from the heart into the head. What appear to be accessory pulsatile organs occur in the dorsal part of the abdomen and in each tibia near the femur. Each of the 2 mycetomes is an isolated structure in the anterior part of the abdomen, appressed laterally to the integument. The fat-body, surrounding all organs, is present in the head, thorax, and abdomen, but is most plentiful in the abdomen.

The Circulatory System of the Box Elder Bug Leptocoris trivittatus (Say)

Relatively little is known concerning the histology and morphology of the dorsal vessel of most insects. The vessel is well described for some species, but general knowledge of its structure in various insect groups is meager. The dorsal vessel is delicate, requiring carefujl dissection and preservation. In addition, various parts, such as the ostia and the accessory pulsatile organs and membranes, when present, are difficult to observe. Some of these difficulties have been overcome in this work and thle results are here presented. Live insects were used in this study and the employment of vital stains aided immeasurably in observing and identifying the internal structures (Woolley, 1949). Dissections were made in saline solution. The entire organ or its parts were fixed in Kahle's or Carnoy's solutions, washed in alcohol and imbedded and preserved in paraffin. In addition to the gross dissections, whole mounts and serial sections were employed for details. Sections of the tissue were cut at 5, 7, and 10 microns, mounted and stained with one of the following: Hansen's Trioxyhaematin-; Heidenhain's Iron Haematoxylin; Eosin and Fast Green; Eosin and Delafield's Haematoxylin. A camera lucida was used for the histological drawings. Details were added after a careful sketch had been made of the structure to be illustrated. The drawings of the gross anatomy were made free hand.