11.1 Invertebrates

The circulatory systems in invertebrates are as diverse as the large phylum to which they belong, with numerous species having no heart and only a rudimentary circulatory system, in contrast to others, with well-developed hearts and highly responsive peripheral circulation. The circulation in the common earthworm (Lumbricus terrestris/oligochaeta) is typical of a large group of lower invertebrates. The large coelomic cavity is divided into some 150 compartments by externally visible septa. The degree of septal filling with coelomic fluid regulates the form and movement of the animal and serves as “hydraulic skeleton.” Although the circulating fluid in earthworms is referred to as blood, this is a misnomer, since the respiratory pigment, a large heme-carrying molecule (erythrocruorin is about 36 times larger than hemoglobin), is not contained within the erythrocytes, but floats freely in plasma. Moreover, the vascular basement membrane is located on the luminal side of endothelial cells which contain contractile elements.

It has been suggested that the basement membrane plays a similar role in keeping the heme molecules within the vascular system, as does the erythrocyte membrane in containing the hemoglobin [1]. There are no specialized organs of respiration in the earthworm, the skin being the only organ available for gas exchange.

The blood moves along the contractile dorsal vessel to the front of the animal and returns backwards via the ventral vessel (Fig. 11.1). The two are connected via a series of segmental vessels which collect the blood from the vessel sinuses distributed along the intestinal tract, nephridia, and skin. Five pairs of frontal segmental vessels have thickened muscular walls, which exhibit strong contractile activity (lateral “hearts”) and are joined via valve-like folds to the dorsal and segmental vessels. Anterior to those hearts, the flow in the ventral vessel occurs in the frontal direction. The dorsal vessel and the lateral contractile vessels are assumed to be the major propulsive organs for the blood [2]. Additional valves in the lumen of the dorsal vessel and inside the lateral hearts ensure directional flow of blood [3]. The rate of contraction of the dorsal vessel in a resting animal is 10–15 per minute and varies with environmental temperature and activity of the animal. The paired lateral vessels beat in synchrony at their own pace but can adopt the rhythm of the dorsal vessel [4]. Johansen and Martin measured simultaneous pressures in the dorsal and ventral vessels in a giant earthworm (Glossoscolex giganteus) (measuring up to 120 cm and weighing 500–600 g). At rest, the pressures in the dorsal and ventral vessel reached about 15 and 75 cm H₂O, respectively. During activity, which is marked by thinning and elongation of a segment of the animal, the pressure in the ventral vessel increased up to 120 cm H₂O. The experiment confirms that contraction of the body wall exerts a marked effect on the intravascular pressure. Of interest is the fact that, unlike in the vertebrate circulation, the pressure in the active loop (dorsal vessel and lateral hearts) was significantly lower than in the non-contractile ventral vessel, suggesting that the source of blood propulsion lies in the periphery, rather than in the contractile vessels [5].

To assess the contribution of the lateral hearts for the maintenance of the circulation, Johnston removed the frontal somites of worms and observed the survivors during the regenerative phase for several weeks. The vessels at the anterior part of the animal were “greatly crowded and distended with blood,” while the posterior parts remained relatively unfilled. Serial sections showed the greatest distension of the dorsal vessel and of the vascular plexuses of the intestinal wall, while the ventral vessel appeared normal in size [2]. Unfortunately Johnston did not comment on the level of activity in the surviving animals, but the experiment nevertheless points to the importance of the lateral hearts in directing the flow and in maintaining the pressure in the ventral vessel. The congestion of the dorsal vessel and of the capillary beds further suggest that the capillary flow continues in the original direction, in spite of the major disruption of the vascular integrity and a partial loss of the “hydraulic skeleton.”

The importance of intravascular pressure in maintaining mobility among invertebrates can be appreciated in the class of Cephalopoda, a group of very active animals, whose level of activity can be compared to that reached by vertebrates. They too, have a “closed” circulatory system, with vascular and extracellular compartments, averaging 5.6% and 28% of total body weight, respectively, a proportion similar to that in the vertebrates. Their level of metabolic activity is higher than that of other molluscs [6].

A schematic diagram of the circulatory system in a cephalopod is shown in Fig. 11.2. The deoxygenated blood returning from the head and body region is collected in the vena cava which symmetrically divides into two branches and enters the kidney sac (nephridia). The blood then continues into the muscular branchial heart, which ejects it into the gill (ctenidium), which, like the heart, exhibits rhythmical contractions. The oxygenated blood passes via the efferent branchial vessel into the median ventricle. There are no valves between the heart and the vessels entering it. The ventricle ejects the blood through the anterior and posterior aorta back to the systemic vessels. Like in the Oligochaeta the blood of the cephalopod contains freely circulating oxygen-binding pigment hemocyanin consisting of 24–48 oxygen-carrying subunits, with molecular weights of 75,000. (These pigments are significantly larger than the mammalian hemoglobin which consists of four hemes, each attached to 14,000 molecular weight units.) [7]

Johansen and Martin investigated circulatory dynamics during rest and exercise in the large octopus (Octopus dofleini) [9]. Simultaneous intravascular pressures in the aorta, branchial vessels, and vena cava were measured in unrestrained animals. Baseline aortic pressures were in the range of 55 cm H₂O for systolic and 40 cm H₂O for diastolic. The caval pressures (pulsatile synchronously with respirations) were between 2 and 15 cm H₂O. The heart rate varies, but was in the range of 6–8 beats/min. During slow, short movement (less than a minute), the systolic pressure increased to 73 cm H₂O and the diastolic pressure to 60 cm H₂O, with the pulse pressure of 13–14 cm H₂O, without any change in heart rate. During sustained exercise (3 min), the heart rate increased from 6 (at baseline) to 8 beats/min, and peak systolic pressure rose to 75 by the end of the exercise period. In the immediate post-exercise period, the diastolic pressures remained markedly elevated for 10–15 min before dropping back to baseline levels. The authors were at loss to explain the sudden increase of pressures at the onset of exercise, considering that there was little or no change in heart rate. This, together with the lack of valves would make the central ventricle an inefficient propulsion pump, at best. The authors invoke contraction of the general body musculature as a factor in sustaining the increased diastolic pressure during activity, a view also supported by Chapman [10]. However, this does not explain the curious observation that the systemic ventricle can stop beating for a considerable period (up to 2 h), without a significant drop in aortic pressure. Despite the fact that during asystolic periods an increased activity was noted in branchial hearts, this could not account for the sustained aortic pressure, since the hearts are placed in the venous limb, before the extensive capillary network of the ctenidia (gills). The authors evoke “a massive peripheral vasoconstriction” as a possible cause of sustained aortic pressure during periods of asystole, but do not provide evidence for its existence [9].

11.2 Tracheate Insects

The tracheate insects are highly evolved invertebrates in which the respiratory and circulatory systems developed separately but nevertheless achieved a remarkable level of specialization. Together they serve the insect’s highly efficient metabolic system which is unparalleled in the animal kingdom. The circulatory system of an insect (fly) is depicted in Fig. 11.3. A pair of thin membranes, the dorsal and the ventral diaphragm, separates the insects’ body into three horizontal compartments. Along the posterior wall of the abdomen and thorax runs the main structural component of the insect’s circulation, the heart or the dorsal vessel, which serves as a conduit for hemolymph. In the abdomen, the vessel is divided segmentally into chambers into which drain a pair of segmental vessels. While some species have a valve-like structure called the ostium, at the confluence of the segmental valve with the dorsal vessel, others have none [11]. A pair of alary muscles is attached laterally to the walls of each chamber. The chamber fills as the alary muscles relax (diastole) and allow the inflow of hemolymph from segmental vessels. Rhythmical contractions of the alary muscles regulate the pulsatile flow through the heart, typically in the range of 30–200 beats/min. While the abdominal part of the dorsal vessel is referred to as the heart, its continuation in the thorax, which lacks the valves and supporting muscles, is called the aorta.

The insect’s hemolymph is a thin plasma-like fluid consisting mainly of water, proteins, amino acids, sugars, and electrolytes. The cellular components known as the hemocytes represent only 10% of hemolymph’s total volume, and their function is clotting, cellular defense, and phagocytosis. In comparison, the cellular component in vertebrate plasma is significantly higher, up to 50%. The hemocytes do not contain hemoglobin or other oxygen carrying pigments, since a separate tracheal system exists for the delivery of oxygen. The flow of hemolymph in the dorsal vessel is generally in the direction from the abdomen toward the head where, emerging from the aorta, it bathes the organs of the head and flows caudally via the three abdominal sinus cavities until it is collected again in the heart.

In keeping with the time-honored biological notion that a rhythmically contracting heart equals a pump, the insect heart is likewise assumed to function as such. However, much like in the case of the vertebrate embryo, the control of insect circulation has been subject of renewed interest in recent years and several phenomena, which point to an autonomous movement of hemolymph, have been observed but, unfortunately, not recognized.

Over the past several years, the difficult question of primary neurogenic control of insects’ hearts has been resolved. In some species the heart has no innervation, and all myogenic cells clearly possess the pacemaker activity. In addition, there are numerous species with richly innervated heart tubes. It has been argued that those too exhibit autonomous activity when anatomically or chemically denervated [13].

The real difficulty with the purported pressure propulsion arises, when we consider the mechanism of hemolymph propulsion through the insect. In theory, the peristaltic contraction of the alary muscles forces the hemolymph from chamber to chamber, while during relaxation phase (diastole), the ostia open and allow the flow of hemolymph from the segmental vessels to refill the heart. However, the role of the dorsal heart as an effective organ of propulsion has been questioned, since the pressures generated in the abdomen are 100–500 times greater than those generated by the heart [14]. In some insects, such as in the ordinary house fly, the heart beat varies between 0 and 300, occurring irrespective of the insect’s resting state or of flight. More remarkably, the fly can sustain the metabolic activity at 100-fold its basal level, far surpassing any mammal [15]. In comparison, the exercising dog can increase its metabolism up to 40 times and world class athletes by about 20 times [16]. This raises the question of the mechanism involved in the almost instantaneous overcoming of the fluid inertia, every time the flow of hemolymph comes to a halt. To make the matter even more complex, there is the peculiar phenomenon of hemolymph flow reversal (observed already by Malpighi in the seventeenth century), which occurs in several species of flies, and in the pupal stages of a number of insects [12, 17] (Fig. 11.3d). Given such complex “to and fro” movements of the hemolymph, how can the heart act as a bidirectional pump, and what would be its possible control mechanism, given the fact that the heart exhibits autonomous (myogenic) contractions in response to stretch and filling volume? Should the heart work as a peristaltic pump, as the theory proposes, how can one account for the pumping mechanism of the cockroach heart, for example, whose dorsal vessel contracts simultaneously along its entire length, rather than peristaltically as is the case in other insects? (Fig. 11.3b) [12]. The concept of pressure-driven circulation implies that the system of vessels is sufficiently tight to withstand the pressure generated by the circulating pump. Such a system is clearly not possible in the case of an open circulation with its system of coelomic spaces, which would soon become filled with excess amount of circulating fluid. Moreover, vessels devoid of the basement membrane and tight endothelial junctions would not be effective in containing the pressurized hemolymph. Given the fact that the circulation of the insect is closely coupled with its metabolic activity and, to some extent, with the environmental temperature, it becomes clear that the movement of the hemolymph is the expression of the metabolic activity of the insect itself and that the heart is inserted in the circuit in order to check or impede its flow. It is evident that, as in the case of vertebrates, the primary control of the insect circulation is metabolic and that the heart plays a secondary role, rhythmically restraining the flow of hemolymph.

11.3 Early Vertebrates

The open circulatory system persists among many classes of animals which represent the transition between the ancient chordates and the vertebrates. The Tunicates , also known as sea salps, are ubiquitous marine animals that are sessile and actually lack a backbone but nevertheless belong to chordates on account of their free-swimming tadpole larvae which already have a primitive spine, the notochord. The adult animal has a remarkable vascular system in which the circulating fluid reverses direction, much like in the case of some insects. The heart is a tubular U-shaped organ, formed by folding of the pericardial membrane. The two vessels exiting from the heart continue for a short distance on either side, before they widen into a larger sinus cavity or coelom, filled with sheets of loose connective tissue, the mesenchyme. The sinus cavities lack true walls and are freely permeable to the circulating fluid. The hemolymph consists of plasma and a number of cellular components derived from the mesenchyme resembling lymphocytes and phagocytic amebocytes, none of which contains oxygen-carrying pigments. The circulation is a type of ebb and flow in which the tubular heart contracts about 20 times per minute, impelling rhythm to the flow of hemolymph for a period of 2–3 min, until it reverses, after a short pause, and flows in the opposite direction [7, 18]. The functional significance of flow reversal over one-way circulation has been subject of lively debates among marine biologists in terms of the “adaptive advantage” of one system over the other. High metabolic rates in some salp species, clogging of vessels with blood cells in the gut region, and periodic exhaustion of pacemakers have been cited as the cause of flow reversal [19]. The fact that the flow comes to a halt at the end of each heart stroke, without any backflow or noticeable slowing at the end of contraction period [19] clearly points to an autonomous movement of hemolymph (Fig. 11.4).