- Email: [email protected]
Circulatory System
CHAPTER
Circulatory System C
r"
1, ,-I
Kenneth R Olson
O
Indiana University School of Medicine, South Bend Center for Medical Education, University of Notre Dame, Notre Dame, Indiana, USA
I11 I#l
--I m
@ Abbreviations A AE APC AV BA BAA BL BV CL CT CV DES E EBA EF EL EO FT
artery arterial endothelial cell anterior wall of pericardial cavity atrioventricular valve/orifice bulbus arteriosus bulbus arteriosus adventita basal lamina bulboventricular ring compact layer with radial fibers circular tubules cover cell desmosome endothelial cell efferent branchial artery efferent filamental artery elongated filament osmophilic endothelial organelles filamentous tube-like structures
Copyright 9 2000 Academic Press
G ICP IEP IL LE LT MF NF P R RE RSR S SC SM SSC V VB VW VE WG WP
glycogen granules interstitial cover cell process interstitial endothelial cell process interlamellar vascular system longitudinal element longitudinal tubule myofibril nerve fibers pericyte red blood cell radial element reticular sarcoplasmic reticulum secondary vessel Schwann cell smooth muscle subsarcolemmal cisterna vein ventriculo-bulbar valve ventricular wall villuous endothelial cell whorled pattern with central glycogen Weibel Palade bodies
E O O -H C z z I"
z O -<
Overview
I11
I--
rr 0
I-.J
1
U
@ >-
0 tl Z
<
_J
z 0 u z
u 0u U'3 0 u
The fish cardiovascular system is in many respects an evolutionary prototype and its design employs numerous features common to all vertebrates. Cardiac muscle provides the energy for blood flow, vascular smooth muscle is used to regulate blood distribution and return and capillary endothelial cells are the perm-selective barriers across which nutrients are exchanged. However, with 400 million years of evolution it is not surprising that there are a few obvious, and perhaps fundamental, differences between the cells and tissues that make up the fish and mammalian systems. The emphasis of this chapter will be on the more unique features of the fish cardiovascular system. The fish heart has a single atrium and ventricle and the latter is seldom required to develop pressures in excess of 40 mmHg (one-third that of mammals), moreover, it is rarely perfused with oxygenated blood and the myocardium is accordingly different. Fish blood vessels can be functionally (and structurally) divided into compliance, conductance, resistance, exchange and capacitance vessels. These descriptors are similar to those used in mammals, although anatomical solutions to a common problem are not always identical and the differences will be stressed. Fish apparently lack a lymphatic system, yet they possess another, perhaps related, vascular network, the secondary circulation. This circulation is both an anatomical curiosity and a physiological enigma. Finally, elaborate countercurrent arteriole/capillary systems, the retia mirabilia, are uniquely designed to concentrate gases in the swimbladder, oxygen in the eye, and in tuna the retia help retain heat in select tissues.
dium. In teleosts with both spongy and compact myocardium the percent of ventricular mass occupied by the compact layer varies between 16~ (conger eel, Conger conger) and 74O/o(bigeye tuna, Thunnus obesus ); 20-45% being the most common (Farrell and Jones, 1992; S~mchez-Quintana et al., 1996). The spongy and compact layers in teleosts are separated by a layer of connective tissue in all but the region immediately surrounding the atrioventricular and bulboventricular valves, where there is a direct connection between fascicles in the two layers (S~nchez-Quintana et al~, 1996). Hearts from elasmobranchs (sharks, skates and rays) always have both spongy and compact layers and there is direct continuity between the layers. There is less variation in the anatomy of the teleost atrium and a definitive compact layer is lacking. Trabeculae are common and important in atrial function (see Chapter 10).
Myocardial fibers Myocardial fibers in the spongy layer are commonly organized into fascicles in the shape of bundles or thin sheets that branch frequently and are interconnected with each other (Figure 22.1). Fascicles may extend several hundred micrometers but they are generally less than 25-35 pm in diameter. This increased surface area is essential because the fibers obtain their oxygen directly from venous blood in the ventricular lumen. There is no coronary circulation in the spongy myocardium of bony fish with the exception of a very
The heart The overall shape and arrangement of the ventricle and ventricular myocardial fibers in teleost fish hearts has been correlated with their life style (Santer and Greer Walker, 1980; Santer et al., 1983; Santer, 1985; Farrell and Jones, 1992; Agnisola and Tota, 1994; see also Chapter 10). Most fish are relatively sedentary and they have either saccular or tubular hearts with only a spongy (trabecular) myocardium. Active fish have pyramidal-shaped ventricles and both a spongy myocardium and an outer layer of compact myocar-
Figure 22.1 Scanning electron micrograph of the trabeculated ventricular myocardium in a sedentary fish, Heteropneustes fossilis. Fibers in center of micrograph have been cut nearly perpendicular to long axis. Cardiac myocytes are arranged in branched interconnected bundles (*) or sheets (arrow) thereby exposing large areas of the plasma membrane to blood in the ventricular lumen. (Micrograph from Olson and Datta Munshi, unpublished observation.)
few of the most active species. The fascicles are collectively arranged to form branching lacunae in the ventricular wall. The lacunae enhance the mechanical efficiency of the fascicles (see Chapter 10). Myocardial fibers in the compact myocardium are arranged into tightly packed fascicles. This, plus the connective tissue layer separating the spongy and compact layers, excludes blood from the ventricular lumen and these cells must be nourished by a coronary circulation. Myocardial fascicles in the compact myocardium of pyramidal hearts are arranged in two layers, or less commonly one or three layers, the number of which depends on the extent of the compact layer (Farrell and Jones, 1992; S~mchez-Quintana et al., 1996). In the outer layer, the fascicles usually run longitudinally and in some species they insert into the bulboventricular fibrous ring (Figure 22.2a). Contraction of the outer layer during ventricular systole produces an axial shortening of the ventricle. Fascicles in the inner layer encircle the vertices of the pyramidal ventricle (Figure 22.2b). This effectively subdivides the lumen into smaller chambers and presumably provides greater mechanical advantage. The fascicles usually encircle the atrioventricular and bulboventricular junctions and they may insert directly into the fibrous bulboventricular valvular ring. Contraction of the inner layer decreases the radial dimensions of the vertices of the pyramidal ventricle.
BV
Cardiocytes The structure offish cardiocytes has been summarized by Satchell (1991), Farrell and Jones (1992) and Tibbits et al. (1992) and is shown in Figure 22.3. Fish cardiocytes are smaller in diameter than their mammalian counterparts (1-12.51xm versus 10-25 ~m). Myofibrils may occupy half of the volume of the cell and in many fish they are restricted to the periphery and lie just beneath the sarcolemma. A, I and Z bands are present and six actin-containing thin filaments surround each myosin-containing thick filament. Spherical or oval mitochondria and a single nucleus (not shown in Figure 22.3) are often centrally located. Cardiocytes lack typical T tubules, although caveolae, 0.15 lim diameter flask-shaped infoldings of the sarcolemma, may serve this function. The sarcoplasmic reticulum (SR) is reduced in size and four types of SR have been described (Figure 22.3b). Subsarcolemmal cisternae lie beneath the cell membrane and communicate with circular tubules that encircle the myofibrils. A few longitudinal tubules connect adjacent circular tubules and both communicate with an often sparsely distributed reticular lattice. The contractile proteins of mammalian cardiocytes are activated almost exclusively by release of calcium from intracellular stores, whereas activation of the contractile apparatus of fish cardiocytes is dependent primarily on external calcium. Thus in fish cardiocytes the greater surface to volume ratio and peripheral orientation of myofibrils enhances delivery of extracellular calcium to the myofibrils and an extensive system of transverse tubules and sarcoplasmic reticulum is probably not necessary.
c
F-
11, -,I
O
lcl m
i
SSC L T C
O 9 -H C Z
Z F'Z
(a)
(b)
Figure 22.2 Dorsal view of the compact myocardium and bulbus arteriosus (BA) of a pyramidal ventricle illustrating the orientation of myocardial fascicles (solid lines), a. Fascicles in the outer layer often run longitudinally and may insert into the bulboventricular fibrous ring (BV). Their contraction decreases the longitudinal axis of the ventricle, b. Fascicles in the inner layer encircle the vertices of the pyramid and their contraction decreases the radial dimension. Increased mechanical efficiency is obtained by subdividing the ventricular lumen into several smallerdiameter chambers. AV, orifice of atrioventricular valve. (Figures were drawn from micrographs and description by S~nchez-Quintana eta/., 1996.)
~
~
O -<
(a)
(b)
RSR
Figure 22.3 Structure of cardiocytes, a. Cross-section through a cardiocyte showing the peripheral arrangement of the myofibrils (MF) and centrally distributed mitochondria, b. Relationship between two myofibrils and subsarcolemmal cisterna (SSC), circular tubules (CT), longitudinal tubules (LT) and reticular sarcoplasmic reticulum (RSR). (b adapted from Farrell and Jones, 1992, with permission.)
Connective tissue
i11
0 t,r e~
I >-
0
F-< Z
<
_J
< Z
9 U Z
U
0
U
Connective tissue in the fish heart, as in mammals, consists of a hierarchical arrangement of epimysium, perimysium and endomysium (Sfinchez-Quintana et al., 1996). The epimysium forms a thick epicardial layer and a thinner endocardial layer in all hearts. Thick coiled perimysial sheaths form an extensive irregular framework that penetrates the compact myocardium and supports the fascicles. These are especially pronounced in very active fish and they may store energy near the end of systole. Perimysial fibers also radiate from the coronary vessels, perhaps helping maintain patency of the vessel during systole. The perimysium in trabeculated myocardium provides anchoring points for the fascicles. Individual and bundled collagen fibrils in the endomysium ensheath the myocytes. In trabeculated hearts these fibers are either oblique or transverse to the long axis of the cell.
Endothelium At least two types of endothelial cells line the atrium and cover the trabeculae in the ventricle (S~etersdal et al., 1974). They range from flat to cuboidal. One type of endothelial cell has catecholamine-containing granules. The other endothelial cells are highly phagocytic (atrial even more so than ventricular) and they actively remove considerable amounts of foreign matter such as ferritin particles (Leknes, 1987) and colloidal carbon (Ellis et al., 1976; although these may be macrophages). These cells have numerous bristlecoated vesicles (probably clathrin coated), moderately dense-bodied inclusions and lysosomes are abundant (Leknes, 1982). The phagocytic-type cells appear unique to the heart and they are not present in the adjacent bulbus arteriosus.
9 U
travel one of three routes, either with the vagus nerves (forming the vagosympathetic trunk), along the anterior pair of spinal nerves, or along the coronary arteries. There are a few exceptions, such as pleuronectids, which lack adrenergic innervation.
Peripheral circulation Blood vessels are anatomically divided into arteries, capillaries and veins, whereas they are often functionally characterized as compliance, conductance, resistance, exchange and capacitance vessels (reviewed in Olson, 1997). Compliance vessels dampen the ventricular pulse. This reduces the ventricular load by decreasing systolic pressure, protects the delicate capillaries from excessive pressure, and maintains blood flow even when the ventricle is at rest. Compliance vessels are arteries and by far the most important and unique compliance vessel in fish is the bulbus arteriosus. The ventral aorta, dorsal aorta and larger systemic arteries also contribute to compliance, however they mainly serve as low resistance conductance pathways to distribute the blood. Most of the vascular resistance is in small arteries and arterioles (< 500pm diameter) and here is where nerves, hormones and local factors regulate blood flow distribution between and within organs. Capillaries, and probably smallvenules, are sites for exchange between blood and tissues. The capacitance vessels, venules and veins, store blood and through them the return of blood to the heart is regulated.
Arteries Innervation Distribution of autonomic nerves to the teleost heart has been reviewed by Morris and Nilsson (1994). Inhibitory parasympathetic (cholinergic) innervation is supplied by paired vagus (X cranial) nerves that travel along the ductus Cuvier. The parasympathetic ganglion lies near the sinoatrial border and the postganglionic fibers travel to (in order of decreasing nerve density) sinoatrial nerve plexus (pacemaker), atrioventricular border, atrium and ventricle. Excitatory sympathetic (adrenergic) nerves may
Compliance vessels Bulbus arteriosus The bulbus arteriosus is a tear-drop shaped vessel that serves as major depulsator (aka windkessel vessel; reviewed in Satchell, 1991; Bushnell et al., 1992). The vessel wall is rich in elastic tissue and vascular smooth muscle and is innervated by autonomic nerves. Elastin in fish has fewer cross links than mammalian elastin and appears more elastic. Thus the bulbus is not only highly compliant but it is possible
VW
7"
APC
APC
~
RE
CL
Figure 22.4 The bulbus arteriosus of a number of fish contains both longitudinal (LE) and radial (RE) elements. During ventricular ejection (systole), blood flows into the bulbus, and energy is stored during distension of the bulbar wall and RE. The LE prevent elongation of the bulbus and serve as the attachment site for the RE. Elastic recoil of the bulbus helps maintain arterial pressure during diastole. Other abbreviations on page 369 (From Priede, 1976, with permission.)
that compliance is actively regulated. The bulbus of many fish is also structurally reinforced with trabecular longitudinal (axial) and radial elements (Figure 22.4; Priede, 1976) to withstand large volume/pressure oscillations. During ventricular ejection, potential energy is stored in the elastic walls and perhaps radial trabeculae. This energy is then dissipated during diastole to maintain arterial pressure.
Conductance and resistance vessels The general anatomical features of fish blood vessels have been described by Satchell (1991) and Bushnell et al. (1992). With the exception of a few minor variations, the anatomy of fish and mammalian arteries (and veins) is similar and the mammalian nomenclature is used for fish as well. The blood vessel wall has three layers (from inside outward): the tunica intima, tunica media and tunica adventitia. The relative thickness of each layer varies with the vessel's function. The tunica intima is bounded on the blood (luminal) side by a single layer of endothelial cells and on the exterior (abluminal) side by a thin, fenestrated elastic sheet, the internal elastic lamina. In vessels where flow rate and shear forces are high, such as conducting arteries, endothelial cells are shaped like elongated diamonds with their long axis parallel to the direction of blood flow; whereas venous endothelial cells are more irregularly shaped and show no flowdirected orientation (Olson and Villa, 1991). The
endothelial surface also appears to be vessel specific, i.e. endothelial cells lining the ventral aorta are smooth, scattered endothelial projections, similar to those found in mammals (Smith et al., 1971) protrude from the celiacomesenteric artery and endothelial projections are especially abundant on the surface of the anterior cardinal vein (Olson and Villa, 1991). Prostaglandin-like endothelium-derived relaxing factors (EDRF) are released by both arterial and venous endothelia in fish (Olson and Villa, 1991). The tunica media consists mainly of smooth muscle and in the more muscular vessels the cells may be oriented circumferentially and longitudinally (Bushnell et al., 1992) or helically (Packer and Olson, unpublished observation). Elastic fibers may be randomly interspersed between the smooth muscle cells, or in vessels with higher blood pressure, e.g. the ventral aortas of trout, carp, eel and tuna, the tunica media may be organized into distinct laminae. In some vessels dense elastic fibers are condensed into a sheet forming an outer elastic lamina. The tunica adventitia is commonly a thin layer of collagen with some elastin. In some vessels, such as the dorsal aorta (see below) and afferent filamental artery of the gill, the adventitia is affixed to surrounding skeletal or cartilaginous tissue.
C
r-
O
1r m
O
Ventral and dorsal aortas
O
The ventral aorta is a thick elastic artery and in the carp as many as 20 superimposed elastic laminae have been identified. Smooth muscle is also abundant in the ventral aorta and this vessel has been the subject of numerous in vitro myographic studies of fish vascular physiology and pharmacology. The dorsal aorta is the longest artery and in most fish its structure is unlike that of other arteries. It is a relatively thin-walled vessel with a limited amount of smooth muscle and elastin and abundant collagen. The dorsal wall of the aorta is especially thin and here it is attached to the ventral surface of the spinal column by transverse bands of collagen fibers. The ventral ligament of the spinal cord may project into the lumen of the dorsal aorta and serve as a mechanical booster pump (see Chapter 8 and Priede, 1975). Other conducting arteries contain various mixes of elastin, smooth muscle and connective tissue. Wall thickness decreases with vessel diameter and there is a progressive reduction in the amount of adventitia and smooth muscle. Many of these vessels
9"O C Z
9 Z F"
Z
O -<
are innervated by sympathetic adrenergic nerves and to a lesser extent by nerv:es containing neuropeptides such as vasoactive intestinal peptide (Morris and Nilsson, 1994). A few endothelial cells in arteries and larger arterioles have electron-dense granules that appear to contain catecholamines (Davison, 1987). These may also play a role in regulating blood flow.
Arterioles
W
I--
0
I.,,,,I
n,.
O >-
O
I--. z
Arterioles are short (<500 pm), narrow (<300 pm) and their muscular medial layer is important for regulating vascular resistance in response to neurocrine, endocrine and paracrine stimuli (Satchell, 1991; Olson, 1997). The smallest arterioles have a single layer of smooth muscle (Figure 22.5). Arteriolar endothelial cells may be squamous but in many fish they are cuboidal (Davison, 1987; Satchell, 1991). The vessel lumen may be the size of a single red blood cell. In a detailed study of arterioles in swimming muscles of the leatherjacket, Parika scaber, Davison (1987) observed longitudinally oriented contractile-like fibrils in the endothelial cells and circumferentially oriented fibrils in the smooth muscles. He proposed that contraction of the former would shorten the vessel and contraction of the latter would decrease its radius. Davison (1987) also observed that fish arteriolar smooth muscle has considerably less fibrillar material than similar size mammalian arterioles,
<
_...1
< z 9 k-u z
which may reflect the lower blood pressures commonly found in fish.
Capillaries Much of the interest in fish capillaries has been directed toward understanding the factors that affect capillary density (cf. Egginton, 1992), and there has not been a systemic examination of capillary ultrastructure. However, from the available information it appears that fish capillaries are anatomically similar to those found in mammals (Satchell, 1991) and consist of a single layer of squamous endothelial cells surrounded by a basement membrane. Typically they are 4-10pm in diameter and 500-1000 pm long. Most capillaries are continuous, especially in skeletal muscle, although some fenestrated and discontinuous capillaries are present in other tissues. Pinocytotic vesicles are abundant on both luminal and abluminal surfaces and to a lesser extent in the cytoplasm. Contractile-like filaments are also present. Periendothelial cells (pericytes) have also been found attached to the abluminal surface of arterioles, capillaries and venules (Figure 22.6; Couch, 1990). Fish pericytes are similar to those in mammals and have common identifying characteristics: (i) they are encompassed within a basal lamina that is continuous with the basal lamina of the adjacent vessel; (ii) they contain many plasmalemmal vesicles; and (iii) they possess an apparent 'sole' region, an area where they are in closest contact with the endothelium. The sole region also contains contractile actin- and myosin-like filaments but plasmalemmal vesicles are absent.
u (3_
0u 0 u
Figure 22.5 Transmission electron micrograph of a terminal arteriole in the swimming muscle of the leatherjacket, Pariko scober. This 14 lim-diameter vessel has a single layer of smooth muscle (SM) and cuboidal endothelial cells (E). A single red blood cell fills the lumen. (From Davison, 1987, with permission.)
Figure 22.6 Diagram of capillary and two pericytes (P) in the gut of the sheepshead minnow. Pericyte cell bodies are surrounded by a basal lamina (arrows), overlie endothelial cell (E) junctions and contain contractile filaments. (After Couch, 1990.)
Veins Fish veins andvenules are structurally similar to those in mammals, although they have proportionally thinner walls and less smooth muscle.
Secondary circulation and lymphatics The early literature describing an extensive lymphatic system in teleosts (summarized in Kampmeier, 1969) has been seriously challenged by modern anatomical studies and it is now thought that fish not only lack true lymphatics, but instead they possess a unique vasculature, the secondary circulation. The secondary circulation derives its name from the fact that it is a vascular network that originates from the main circulation (primary circulation) and forms a second artery-capillary-vein circuit in-parallel with the primary system (reviewed in: Vogel, 1985; Olson, 1992, 1996; Steffensen and Lomholt, 1992; see also Chapter 10). The anatomy and physiology of this circulation is unquestionably the most perplexing question in the fish cardiovascular system. The secondary system has several distinguishing characteristics: 1. It only originates from postlamellar gill arteries (efferent filamental and efferent branchial), the dorsal aorta, or systemic segmental arteries. 2. It appears to be primarilyassociatedwith epithelial tissues and is found in the gill, skin, fins, oral mucosa and peritoneal lining (although it has also been observed in the tuna heat-exchanger). It does not appear to be present in brain, skeletal muscle, coronary or splanchnic circulations. 3. Parent vessels that form the secondary system have an unusually narrow diameter (2-20 ~tm) and follow a relatively long (200-300 ~tm) and very tortuous path before they anastomose with each other to form progressively larger arteries. 4. Secondary capillaries have very thin walls, appear to lack a basement membrane, and are generally similar to mammalian lymphatic capillaries. Secondary veins are also thin-walled, but they are not otherwise notable. They drain into primary veins of the systemic circulation.
Little is known of the physiological attributes of the secondary system. The narrow lumen of the parent arterioles restricts access of blood cells and hematocrit may be as low as I or 2%. Initial indirect estimates of the volume of the secondary system suggested it was an astounding 1.5 times that of the primary circulation (Steffensen and Lomholt, 1992), although more recent studies indicate that it may be only 10-20% the volume of the primary system (Bushnell et al., 1998). Either way, it is a significant system.
Gill secondary system The body of the gill filament contains two circulatory systems, the nutrient and interlamellar (Chapters 9 and 21) that have many, but not always all, of the characteristics of secondary vessels.
C
0 -<
.<
Nutrient circulation Narrow-bore, tortuous arterioles arise from the gill efferent branchial and the efferent filamental arteries in the basal region of the filament near the anastomosis of the efferent filamental and branchial arteries (Figure 22.7). Curiously, numerous long microvilli stud the endothelial cell surface in both the lumen of
m
@ :13
9 9
"1"1 c rZ --4
6 Z
Z >
9 -<
Figure 22.7 Scanning electron micrograph of a vascular corrosion replica of secondary vessels in the gill of the climbing perch (Anabas testudineus). Numerous narrowbore, tortuous arterioles (arrowheads) arise from the gill efferent filamental artery (EF) and subsequently anastomose to form secondary arteries (S). Bar-40 i~m. (From Olson et al., 1986, with permission.)
EF
EBA
w! Sl~ E(
SI 15L
I--
Figure 22.8 Diagram of a longitudinal section through the lumen of the efferent branchial artery (EBA) illustrating the origin of the secondary vessels shown in Figure 22.7. Villous endothelial cells (VE) guard the lumen of the secondary vessel and are also preferentially located on the upstream lumen of the EBA. AE, typical arterial endothelial cell; BL, basal lamina; SM, smooth muscle; R, red blood cell; arrow shows direction of blood flow. (Drawn from descriptions by Vogel, 1978.)
(
IE
DE
0 I-...I n,.
@ >-
O I-< z
<
--J
< z 0 U Z
u.. U (3.
0
the parent artery (efferent branchial or filamental) near the origin of the secondary arteriole and in the secondary arteriole itself (Figure 22.8). The combined effect of a narrow lumen and the bristly microvilli appears to prevent red blood cells from entering this circulation, although Steffensen and Lomholt (1992) proposed that the microvilli may actually enhance red cell entry. The tortuous secondary arterioles anastomose with each other to form progressively larger arteries that supply what resembles a nutrient system for the arch support tissue and the body of the filament. In some fish, such as the catfish, this system drains from the filament through its own venous network. In many other species the nutrient vessels drain directly into (or supply?) the interlamellar system of the filament.
Figure 22.9 Diagram showing the narrow arteriovenous anastomoses from the efferent filamental artery (EF) to the interlamellar system (IL) in the gill of Tilapia mossambica. Type I endothelial cells contain numerous filaments in concentric whorl-like patterns with centrally located glycogen granules (WG). Type II (11)and intermediate endothelial cells (*) lack the whorled patterns. Other abbreviations: AE, arterial endothelial cell; DES, desmosome; E, endothelial cell; EL, elongated filament; EO, osmophilic endothelial organelles; FT, filamentous tubelike structures; G, glycogen granules; ICP, interstitial cover cell process; IEP, interstitial endothelial cell process; NF, nerve fibers; SC, Schwann cell; SM, smooth muscle; WG, whorled pattern with central glycogen; WP, Weibel Palade bodies. (From Vogel et al., 1974, with permission.)
U
Interlamellar circulation
Systemic secondary circulation
The interlamellar system appears to have its origin via short arterioles that originate from the medial wall of the efferent filamental artery in the distal 90% of the filament (Figure 22.9). The lumen of these vessels is also nearly occluded and the endothelium frequently has microvillar projections and whorled cytoplasmic structures (Vogel et al., 1974). The interlamellar system has a thin-walled endothelium with overlapping cell junctions and it is readily distended by even a slight increase in blood pressure.
The systemic secondary system is similar to that in the gill, although it has received considerably less attention. Steffe,nsen et al. (1986) described long secondary vessels in the fins of the glass catfish that drain into a large diameter longitudinal lateral vein and Vogel (1985) has shown that secondary vessels form a planar meshwork covering the surface of each scale. However, Lahnsteiner et al. (1990) reported that secondary vessels from dorsal segmental arteries anastomose directly with a dorsal cutaneous vein and blood
0 U
returns directly to the heart without an intervening capillary bed. Clearly the systemic secondary system needs additional study.
Retia mirabilia The close physical association between arteries and veins of similar size is a common feature in vertebrate tissues. Usually this is either the most anatomically or hemodynamically efficient route and countercurrent exchange between the arteries and veins is usually neither intended nor desired. In fish, however, there are at least three instances where small blood vessels are specifically arranged to make use of this countercurrent flow. These countercurrent vascular networks, called retia mirabilia (wonderful web), are found in most fish in the swimbladder and in the choroid gland (behind the eye) where they are important in concentrating gases, especially oxygen. They are also found in muscle and near the brain, eye, and gut in tuna and a few sharks, where they are important in regulating temperature of these organs. Fish retia are summarized in Satchell (1991) and Bushnell et al. (1992). All retia in fish share common anatomical features that optimize exchange between the inflow and outflowvessels (Figure 22.10): 1. Retial vessels are arteriole to capillary size in diameter and the supply and return vessels form a dense network of parallel tubes separated by only a sparse interstitial matrix. 2. In most instances retial vessels are considerably longer than typical capillaries, in a 1.9 kg tuna vessels of the heat exchanging rete are I cm long (Stevens et al., 1974). 3. An additional capillary bed is located between the inlet (afferent) and outlet (efferent) retial vessels. These capillaries supply the secretory epithelium of the swimbladder, the choriocapillarias behind the eye, and muscle, brain, eye, and gut tissue in
Figure 22.10 Vascular corrosion replica of the vessels comprising the choroid rete mirable of Channa gachua (viewed from behind the eye). A horseshoe-shaped artery (A) supplies smaller arterioles that radiate out to form long parallel capillaries that in turn supply the choriocapillarias (not shown). Closely apposed venous capillaries (below dashed line and arrowheads) complete the countercurrent loop and return blood to a central vein (V). Capillaries from this 75 g fish are approximately 1 mm long. (Adapted from Munshi et al., 1994, with permission.)
O -< -< u~
tissues associated with the rete to operate at temperatures 10-20~ warmer than the rest of the body. Countercurrent multipliers in the swimbladder and eye require external energy and they can produce a standing gradient that is greater than that which can be produced by simple diffusion. The net effect of this complex process is to force the unloading of gases from blood entering the organ and to prevent their loss in the effluent blood. For example, the choroid gland can increase the partial pressure of oxygen (pO2) to over 500 m m H g in the fish eye. This is five times the pO2 of arterial blood and it is necessary to supply oxygen to the highly active retina, which, unlike mammals, is avascular. Somewhat similar processes are employed in the swimbladder for rapid secretion of oxygen, nitrogen and carbon dioxide, This rapidlychanges the densityof the fish and enables the now neutrally buoyant fish to move up or down the water column.
-!
FIt
C~I~
N
:~ O tn N O -n zN
C
O z t-" Z
O -<
tunas.
Retia may be involved in either countercurrent exchange or countercurrent multiplication. Countercurrent exchange, such as occurs in the tuna heat exchanger, is a passive process. Heat generated through tissue metabolism warms the blood and as this warm blood passes into the efferent retial vessels the heat is transferred to blood in the afferent vessels thereby returning heat to the tissue. This enables
C
Acknowledgment The author is grateful to the National Science Foundation for past and current support through NSF Grant Nos PCM 79-23703, PCM 84-048897, DCB 86-16028, I N T 83-00721, I N T 86-02965, INT 86-18881, IBN 91-05247 and IBN 97-23306.
References
~E U.I
Iu'l Ill >-
0
IU m
U
@ >0 tz
z 0 z u_
0 u 0 r~ u
Agnisola, C. and Tota, B. (1994). Cardioscience 5, 145-153. Bushnell, P.G., Jones, D.R. and Farrell, A.P. (1992). In Fish Physiology Vol. XII, Part A. The Cardiovascular System (eds W.S. Hoar, D.J. Randall and A.P. Farrell), pp. 89-120, Academic Press, San Diego. Bushnell, P.G., Conklin, D.J., Duff, D.W. and Olson, K.R. (1998).J. Exp. Biol. 201, 1381-1391. Couch, J.A. (1990).Anat. Rec. 228, 7-14. Davison, W. (1987). Cell Tissue Res. 248,703-708. Egginton, S. (1992).J. Zool. 226,691-698. Ellis, A.E. and Munroe, A.L.S. (1976).J. FishBiol. 8, 67-78. Farrell, A.P., Jones, D.R. and Roberts, R.J. (1992). In Fish Physiology Vol. XII, Part A. The Cardiovascular System (eds W.S. Hoar, D.J. Randall and A.P. Farrell), pp. 173. Academic Press, San Diego. Kampmeier, O.F. (1969). Evolution and Comparative Morphology of the Lymphatic System. Charles C. Thomas, Springfield, IL. Lahnsteiner, A., Lametschwandtner, A. and Patzner, R.A. (1990). Scan. Microsc. 4, 111-124. Leknes, I.L. (1982).Anat. Anaz.,Jena 152, 125-128. Leknes, I.L. (1987).Acta Histochem. (lena) 81, 175-182. Morris, J.L. and Nilsson, S. (1994). In Comparative Physiology and Evolution of the Autonomic Nervous System (eds S. Nilsson and S. Holmgren), pp. 193246. Harwood Academic Publishers, Chur. Munshi, J.S.D., Roy, P.K., Ghosh, T.K. and Olson, K.R. (1994).Anat. Rec. 238, 77-91. Olson, K.R. (1992). In Fish Physiology Vol.XII, Part B. The Cardiovascular System (eds W.S. Hoar, D.J. Randall and A.P. Farrell), pp. 136-232. Academic Press, San Diego. Olson, K.R. (1996).J. Exp. Zool. 275, 172-185. Olson, K.R. (1997). In The Physiology of Fishes (ed. D.H. Evans), pp. 129-154. CRC Press, Boca Raton. Olson, K.R. and Villa, J. (1991). Am. J. Physiol. Regul. Integr. Comp. Physiol. 260, R925-R933.
Olson, K.R., Munshi, J.S.D., Ghosh, T.K. and Ojha, J. (1986).Arn. J. Anat. 176,305-320. Priede, I.G. (1975).J. Zool., Lond. 175, 39-52. Priede, I.G. (1976).J. Fish Biol. 9, 209-216. S~etersdal, T.S., Justesen, N.-P. and Krohnstad, A.W. (1974).J. Mol. Cell Cardiol. 6, 415-437. Sfinchez-Quintana, D., Garcia-Martinez, V., Climent, V. and HurlS, J.M. (1996).J. Exp. Biol. 275, 112-124. Santer, R.M. (1985). Adv. Anat., Embryol. Cell Biol. 89, 1-102. Santer, R.M. and Greer Walker, M. (1980).J. Zool., Lond. 190,259-272. Santer, R.M., Greer Walker, M.G., Emerson, L. and Witthames, P.R. (1983). Cornp. Biochem. Physiol. 76A, 453-457. Satchell, G.H. (1991). Physiology and Form of Fish Circulation. Cambridge University Press, New York. Smith, U., Ryan, J.W., Michie, D.D. and Smith, D.S. (1971). Science 173, 925-927. Steffensen, J.F. and Lomholt, J.P. (1992). In Fish Physiology Vol. XII, Part~Z The Cardiovascular System (eds W.S. Hoar, D.J. Randall and A.P. Farrell), pp. 185-213. Academic Press, San Diego. Steffensen, J.F., Lomholt, J.P. and Vogel, W.O.P. (1986). Acta. Zool. (Stockh.) 67, 193-200. Stevens, E.D., Lam, H.M. and Kendall, J. (1974).J. Exp. Biol. 61,145-153. Tibbits, G.F., Moyes, C.D. and Hove-Madsen, L. (1992). In Fish Physiology Volume XII, Part A. The Cardiovascular System (eds W.S. Hoar, D.J. Randall and A.P. Farrell), pp. 267-297. Academic Press, San Diego. Vogel, W.O.P. (1978). Z. Mikrosk. Anat. Forsch. 92, 565570. Vogel, W.O.P. (1985). In Cardiovascular Shunts. Phylogenetic, Ontogenetic and Clinical Aspects (eds K. Johansen and W. Burggren), pp. 143-159, Munksgaard, Copenhagen. Vogel, W., Vogel, V. and Schlote, W. (1974). Cell Tissue Res. 155, 491-512.
Circulatory System C
r"
1, ,-I
Kenneth R Olson
O
Indiana University School of Medicine, South Bend Center for Medical Education, University of Notre Dame, Notre Dame, Indiana, USA
I11 I#l
--I m
@ Abbreviations A AE APC AV BA BAA BL BV CL CT CV DES E EBA EF EL EO FT
artery arterial endothelial cell anterior wall of pericardial cavity atrioventricular valve/orifice bulbus arteriosus bulbus arteriosus adventita basal lamina bulboventricular ring compact layer with radial fibers circular tubules cover cell desmosome endothelial cell efferent branchial artery efferent filamental artery elongated filament osmophilic endothelial organelles filamentous tube-like structures
Copyright 9 2000 Academic Press
G ICP IEP IL LE LT MF NF P R RE RSR S SC SM SSC V VB VW VE WG WP
glycogen granules interstitial cover cell process interstitial endothelial cell process interlamellar vascular system longitudinal element longitudinal tubule myofibril nerve fibers pericyte red blood cell radial element reticular sarcoplasmic reticulum secondary vessel Schwann cell smooth muscle subsarcolemmal cisterna vein ventriculo-bulbar valve ventricular wall villuous endothelial cell whorled pattern with central glycogen Weibel Palade bodies
E O O -H C z z I"
z O -<
Overview
I11
I--
rr 0
I-.J
1
U
@ >-
0 tl Z
<
_J
z 0 u z
u 0u U'3 0 u
The fish cardiovascular system is in many respects an evolutionary prototype and its design employs numerous features common to all vertebrates. Cardiac muscle provides the energy for blood flow, vascular smooth muscle is used to regulate blood distribution and return and capillary endothelial cells are the perm-selective barriers across which nutrients are exchanged. However, with 400 million years of evolution it is not surprising that there are a few obvious, and perhaps fundamental, differences between the cells and tissues that make up the fish and mammalian systems. The emphasis of this chapter will be on the more unique features of the fish cardiovascular system. The fish heart has a single atrium and ventricle and the latter is seldom required to develop pressures in excess of 40 mmHg (one-third that of mammals), moreover, it is rarely perfused with oxygenated blood and the myocardium is accordingly different. Fish blood vessels can be functionally (and structurally) divided into compliance, conductance, resistance, exchange and capacitance vessels. These descriptors are similar to those used in mammals, although anatomical solutions to a common problem are not always identical and the differences will be stressed. Fish apparently lack a lymphatic system, yet they possess another, perhaps related, vascular network, the secondary circulation. This circulation is both an anatomical curiosity and a physiological enigma. Finally, elaborate countercurrent arteriole/capillary systems, the retia mirabilia, are uniquely designed to concentrate gases in the swimbladder, oxygen in the eye, and in tuna the retia help retain heat in select tissues.
dium. In teleosts with both spongy and compact myocardium the percent of ventricular mass occupied by the compact layer varies between 16~ (conger eel, Conger conger) and 74O/o(bigeye tuna, Thunnus obesus ); 20-45% being the most common (Farrell and Jones, 1992; S~mchez-Quintana et al., 1996). The spongy and compact layers in teleosts are separated by a layer of connective tissue in all but the region immediately surrounding the atrioventricular and bulboventricular valves, where there is a direct connection between fascicles in the two layers (S~nchez-Quintana et al~, 1996). Hearts from elasmobranchs (sharks, skates and rays) always have both spongy and compact layers and there is direct continuity between the layers. There is less variation in the anatomy of the teleost atrium and a definitive compact layer is lacking. Trabeculae are common and important in atrial function (see Chapter 10).
Myocardial fibers Myocardial fibers in the spongy layer are commonly organized into fascicles in the shape of bundles or thin sheets that branch frequently and are interconnected with each other (Figure 22.1). Fascicles may extend several hundred micrometers but they are generally less than 25-35 pm in diameter. This increased surface area is essential because the fibers obtain their oxygen directly from venous blood in the ventricular lumen. There is no coronary circulation in the spongy myocardium of bony fish with the exception of a very
The heart The overall shape and arrangement of the ventricle and ventricular myocardial fibers in teleost fish hearts has been correlated with their life style (Santer and Greer Walker, 1980; Santer et al., 1983; Santer, 1985; Farrell and Jones, 1992; Agnisola and Tota, 1994; see also Chapter 10). Most fish are relatively sedentary and they have either saccular or tubular hearts with only a spongy (trabecular) myocardium. Active fish have pyramidal-shaped ventricles and both a spongy myocardium and an outer layer of compact myocar-
Figure 22.1 Scanning electron micrograph of the trabeculated ventricular myocardium in a sedentary fish, Heteropneustes fossilis. Fibers in center of micrograph have been cut nearly perpendicular to long axis. Cardiac myocytes are arranged in branched interconnected bundles (*) or sheets (arrow) thereby exposing large areas of the plasma membrane to blood in the ventricular lumen. (Micrograph from Olson and Datta Munshi, unpublished observation.)
few of the most active species. The fascicles are collectively arranged to form branching lacunae in the ventricular wall. The lacunae enhance the mechanical efficiency of the fascicles (see Chapter 10). Myocardial fibers in the compact myocardium are arranged into tightly packed fascicles. This, plus the connective tissue layer separating the spongy and compact layers, excludes blood from the ventricular lumen and these cells must be nourished by a coronary circulation. Myocardial fascicles in the compact myocardium of pyramidal hearts are arranged in two layers, or less commonly one or three layers, the number of which depends on the extent of the compact layer (Farrell and Jones, 1992; S~mchez-Quintana et al., 1996). In the outer layer, the fascicles usually run longitudinally and in some species they insert into the bulboventricular fibrous ring (Figure 22.2a). Contraction of the outer layer during ventricular systole produces an axial shortening of the ventricle. Fascicles in the inner layer encircle the vertices of the pyramidal ventricle (Figure 22.2b). This effectively subdivides the lumen into smaller chambers and presumably provides greater mechanical advantage. The fascicles usually encircle the atrioventricular and bulboventricular junctions and they may insert directly into the fibrous bulboventricular valvular ring. Contraction of the inner layer decreases the radial dimensions of the vertices of the pyramidal ventricle.
BV
Cardiocytes The structure offish cardiocytes has been summarized by Satchell (1991), Farrell and Jones (1992) and Tibbits et al. (1992) and is shown in Figure 22.3. Fish cardiocytes are smaller in diameter than their mammalian counterparts (1-12.51xm versus 10-25 ~m). Myofibrils may occupy half of the volume of the cell and in many fish they are restricted to the periphery and lie just beneath the sarcolemma. A, I and Z bands are present and six actin-containing thin filaments surround each myosin-containing thick filament. Spherical or oval mitochondria and a single nucleus (not shown in Figure 22.3) are often centrally located. Cardiocytes lack typical T tubules, although caveolae, 0.15 lim diameter flask-shaped infoldings of the sarcolemma, may serve this function. The sarcoplasmic reticulum (SR) is reduced in size and four types of SR have been described (Figure 22.3b). Subsarcolemmal cisternae lie beneath the cell membrane and communicate with circular tubules that encircle the myofibrils. A few longitudinal tubules connect adjacent circular tubules and both communicate with an often sparsely distributed reticular lattice. The contractile proteins of mammalian cardiocytes are activated almost exclusively by release of calcium from intracellular stores, whereas activation of the contractile apparatus of fish cardiocytes is dependent primarily on external calcium. Thus in fish cardiocytes the greater surface to volume ratio and peripheral orientation of myofibrils enhances delivery of extracellular calcium to the myofibrils and an extensive system of transverse tubules and sarcoplasmic reticulum is probably not necessary.
c
F-
11, -,I
O
lcl m
i
SSC L T C
O 9 -H C Z
Z F'Z
(a)
(b)
Figure 22.2 Dorsal view of the compact myocardium and bulbus arteriosus (BA) of a pyramidal ventricle illustrating the orientation of myocardial fascicles (solid lines), a. Fascicles in the outer layer often run longitudinally and may insert into the bulboventricular fibrous ring (BV). Their contraction decreases the longitudinal axis of the ventricle, b. Fascicles in the inner layer encircle the vertices of the pyramid and their contraction decreases the radial dimension. Increased mechanical efficiency is obtained by subdividing the ventricular lumen into several smallerdiameter chambers. AV, orifice of atrioventricular valve. (Figures were drawn from micrographs and description by S~nchez-Quintana eta/., 1996.)
~
~
O -<
(a)
(b)
RSR
Figure 22.3 Structure of cardiocytes, a. Cross-section through a cardiocyte showing the peripheral arrangement of the myofibrils (MF) and centrally distributed mitochondria, b. Relationship between two myofibrils and subsarcolemmal cisterna (SSC), circular tubules (CT), longitudinal tubules (LT) and reticular sarcoplasmic reticulum (RSR). (b adapted from Farrell and Jones, 1992, with permission.)
Connective tissue
i11
0 t,r e~
I >-
0
F-< Z
<
_J
< Z
9 U Z
U
0
U
Connective tissue in the fish heart, as in mammals, consists of a hierarchical arrangement of epimysium, perimysium and endomysium (Sfinchez-Quintana et al., 1996). The epimysium forms a thick epicardial layer and a thinner endocardial layer in all hearts. Thick coiled perimysial sheaths form an extensive irregular framework that penetrates the compact myocardium and supports the fascicles. These are especially pronounced in very active fish and they may store energy near the end of systole. Perimysial fibers also radiate from the coronary vessels, perhaps helping maintain patency of the vessel during systole. The perimysium in trabeculated myocardium provides anchoring points for the fascicles. Individual and bundled collagen fibrils in the endomysium ensheath the myocytes. In trabeculated hearts these fibers are either oblique or transverse to the long axis of the cell.
Endothelium At least two types of endothelial cells line the atrium and cover the trabeculae in the ventricle (S~etersdal et al., 1974). They range from flat to cuboidal. One type of endothelial cell has catecholamine-containing granules. The other endothelial cells are highly phagocytic (atrial even more so than ventricular) and they actively remove considerable amounts of foreign matter such as ferritin particles (Leknes, 1987) and colloidal carbon (Ellis et al., 1976; although these may be macrophages). These cells have numerous bristlecoated vesicles (probably clathrin coated), moderately dense-bodied inclusions and lysosomes are abundant (Leknes, 1982). The phagocytic-type cells appear unique to the heart and they are not present in the adjacent bulbus arteriosus.
9 U
travel one of three routes, either with the vagus nerves (forming the vagosympathetic trunk), along the anterior pair of spinal nerves, or along the coronary arteries. There are a few exceptions, such as pleuronectids, which lack adrenergic innervation.
Peripheral circulation Blood vessels are anatomically divided into arteries, capillaries and veins, whereas they are often functionally characterized as compliance, conductance, resistance, exchange and capacitance vessels (reviewed in Olson, 1997). Compliance vessels dampen the ventricular pulse. This reduces the ventricular load by decreasing systolic pressure, protects the delicate capillaries from excessive pressure, and maintains blood flow even when the ventricle is at rest. Compliance vessels are arteries and by far the most important and unique compliance vessel in fish is the bulbus arteriosus. The ventral aorta, dorsal aorta and larger systemic arteries also contribute to compliance, however they mainly serve as low resistance conductance pathways to distribute the blood. Most of the vascular resistance is in small arteries and arterioles (< 500pm diameter) and here is where nerves, hormones and local factors regulate blood flow distribution between and within organs. Capillaries, and probably smallvenules, are sites for exchange between blood and tissues. The capacitance vessels, venules and veins, store blood and through them the return of blood to the heart is regulated.
Arteries Innervation Distribution of autonomic nerves to the teleost heart has been reviewed by Morris and Nilsson (1994). Inhibitory parasympathetic (cholinergic) innervation is supplied by paired vagus (X cranial) nerves that travel along the ductus Cuvier. The parasympathetic ganglion lies near the sinoatrial border and the postganglionic fibers travel to (in order of decreasing nerve density) sinoatrial nerve plexus (pacemaker), atrioventricular border, atrium and ventricle. Excitatory sympathetic (adrenergic) nerves may
Compliance vessels Bulbus arteriosus The bulbus arteriosus is a tear-drop shaped vessel that serves as major depulsator (aka windkessel vessel; reviewed in Satchell, 1991; Bushnell et al., 1992). The vessel wall is rich in elastic tissue and vascular smooth muscle and is innervated by autonomic nerves. Elastin in fish has fewer cross links than mammalian elastin and appears more elastic. Thus the bulbus is not only highly compliant but it is possible
VW
7"
APC
APC
~
RE
CL
Figure 22.4 The bulbus arteriosus of a number of fish contains both longitudinal (LE) and radial (RE) elements. During ventricular ejection (systole), blood flows into the bulbus, and energy is stored during distension of the bulbar wall and RE. The LE prevent elongation of the bulbus and serve as the attachment site for the RE. Elastic recoil of the bulbus helps maintain arterial pressure during diastole. Other abbreviations on page 369 (From Priede, 1976, with permission.)
that compliance is actively regulated. The bulbus of many fish is also structurally reinforced with trabecular longitudinal (axial) and radial elements (Figure 22.4; Priede, 1976) to withstand large volume/pressure oscillations. During ventricular ejection, potential energy is stored in the elastic walls and perhaps radial trabeculae. This energy is then dissipated during diastole to maintain arterial pressure.
Conductance and resistance vessels The general anatomical features of fish blood vessels have been described by Satchell (1991) and Bushnell et al. (1992). With the exception of a few minor variations, the anatomy of fish and mammalian arteries (and veins) is similar and the mammalian nomenclature is used for fish as well. The blood vessel wall has three layers (from inside outward): the tunica intima, tunica media and tunica adventitia. The relative thickness of each layer varies with the vessel's function. The tunica intima is bounded on the blood (luminal) side by a single layer of endothelial cells and on the exterior (abluminal) side by a thin, fenestrated elastic sheet, the internal elastic lamina. In vessels where flow rate and shear forces are high, such as conducting arteries, endothelial cells are shaped like elongated diamonds with their long axis parallel to the direction of blood flow; whereas venous endothelial cells are more irregularly shaped and show no flowdirected orientation (Olson and Villa, 1991). The
endothelial surface also appears to be vessel specific, i.e. endothelial cells lining the ventral aorta are smooth, scattered endothelial projections, similar to those found in mammals (Smith et al., 1971) protrude from the celiacomesenteric artery and endothelial projections are especially abundant on the surface of the anterior cardinal vein (Olson and Villa, 1991). Prostaglandin-like endothelium-derived relaxing factors (EDRF) are released by both arterial and venous endothelia in fish (Olson and Villa, 1991). The tunica media consists mainly of smooth muscle and in the more muscular vessels the cells may be oriented circumferentially and longitudinally (Bushnell et al., 1992) or helically (Packer and Olson, unpublished observation). Elastic fibers may be randomly interspersed between the smooth muscle cells, or in vessels with higher blood pressure, e.g. the ventral aortas of trout, carp, eel and tuna, the tunica media may be organized into distinct laminae. In some vessels dense elastic fibers are condensed into a sheet forming an outer elastic lamina. The tunica adventitia is commonly a thin layer of collagen with some elastin. In some vessels, such as the dorsal aorta (see below) and afferent filamental artery of the gill, the adventitia is affixed to surrounding skeletal or cartilaginous tissue.
C
r-
O
1r m
O
Ventral and dorsal aortas
O
The ventral aorta is a thick elastic artery and in the carp as many as 20 superimposed elastic laminae have been identified. Smooth muscle is also abundant in the ventral aorta and this vessel has been the subject of numerous in vitro myographic studies of fish vascular physiology and pharmacology. The dorsal aorta is the longest artery and in most fish its structure is unlike that of other arteries. It is a relatively thin-walled vessel with a limited amount of smooth muscle and elastin and abundant collagen. The dorsal wall of the aorta is especially thin and here it is attached to the ventral surface of the spinal column by transverse bands of collagen fibers. The ventral ligament of the spinal cord may project into the lumen of the dorsal aorta and serve as a mechanical booster pump (see Chapter 8 and Priede, 1975). Other conducting arteries contain various mixes of elastin, smooth muscle and connective tissue. Wall thickness decreases with vessel diameter and there is a progressive reduction in the amount of adventitia and smooth muscle. Many of these vessels
9"O C Z
9 Z F"
Z
O -<
are innervated by sympathetic adrenergic nerves and to a lesser extent by nerv:es containing neuropeptides such as vasoactive intestinal peptide (Morris and Nilsson, 1994). A few endothelial cells in arteries and larger arterioles have electron-dense granules that appear to contain catecholamines (Davison, 1987). These may also play a role in regulating blood flow.
Arterioles
W
I--
0
I.,,,,I
n,.
O >-
O
I--. z
Arterioles are short (<500 pm), narrow (<300 pm) and their muscular medial layer is important for regulating vascular resistance in response to neurocrine, endocrine and paracrine stimuli (Satchell, 1991; Olson, 1997). The smallest arterioles have a single layer of smooth muscle (Figure 22.5). Arteriolar endothelial cells may be squamous but in many fish they are cuboidal (Davison, 1987; Satchell, 1991). The vessel lumen may be the size of a single red blood cell. In a detailed study of arterioles in swimming muscles of the leatherjacket, Parika scaber, Davison (1987) observed longitudinally oriented contractile-like fibrils in the endothelial cells and circumferentially oriented fibrils in the smooth muscles. He proposed that contraction of the former would shorten the vessel and contraction of the latter would decrease its radius. Davison (1987) also observed that fish arteriolar smooth muscle has considerably less fibrillar material than similar size mammalian arterioles,
<
_...1
< z 9 k-u z
which may reflect the lower blood pressures commonly found in fish.
Capillaries Much of the interest in fish capillaries has been directed toward understanding the factors that affect capillary density (cf. Egginton, 1992), and there has not been a systemic examination of capillary ultrastructure. However, from the available information it appears that fish capillaries are anatomically similar to those found in mammals (Satchell, 1991) and consist of a single layer of squamous endothelial cells surrounded by a basement membrane. Typically they are 4-10pm in diameter and 500-1000 pm long. Most capillaries are continuous, especially in skeletal muscle, although some fenestrated and discontinuous capillaries are present in other tissues. Pinocytotic vesicles are abundant on both luminal and abluminal surfaces and to a lesser extent in the cytoplasm. Contractile-like filaments are also present. Periendothelial cells (pericytes) have also been found attached to the abluminal surface of arterioles, capillaries and venules (Figure 22.6; Couch, 1990). Fish pericytes are similar to those in mammals and have common identifying characteristics: (i) they are encompassed within a basal lamina that is continuous with the basal lamina of the adjacent vessel; (ii) they contain many plasmalemmal vesicles; and (iii) they possess an apparent 'sole' region, an area where they are in closest contact with the endothelium. The sole region also contains contractile actin- and myosin-like filaments but plasmalemmal vesicles are absent.
u (3_
0u 0 u
Figure 22.5 Transmission electron micrograph of a terminal arteriole in the swimming muscle of the leatherjacket, Pariko scober. This 14 lim-diameter vessel has a single layer of smooth muscle (SM) and cuboidal endothelial cells (E). A single red blood cell fills the lumen. (From Davison, 1987, with permission.)
Figure 22.6 Diagram of capillary and two pericytes (P) in the gut of the sheepshead minnow. Pericyte cell bodies are surrounded by a basal lamina (arrows), overlie endothelial cell (E) junctions and contain contractile filaments. (After Couch, 1990.)
Veins Fish veins andvenules are structurally similar to those in mammals, although they have proportionally thinner walls and less smooth muscle.
Secondary circulation and lymphatics The early literature describing an extensive lymphatic system in teleosts (summarized in Kampmeier, 1969) has been seriously challenged by modern anatomical studies and it is now thought that fish not only lack true lymphatics, but instead they possess a unique vasculature, the secondary circulation. The secondary circulation derives its name from the fact that it is a vascular network that originates from the main circulation (primary circulation) and forms a second artery-capillary-vein circuit in-parallel with the primary system (reviewed in: Vogel, 1985; Olson, 1992, 1996; Steffensen and Lomholt, 1992; see also Chapter 10). The anatomy and physiology of this circulation is unquestionably the most perplexing question in the fish cardiovascular system. The secondary system has several distinguishing characteristics: 1. It only originates from postlamellar gill arteries (efferent filamental and efferent branchial), the dorsal aorta, or systemic segmental arteries. 2. It appears to be primarilyassociatedwith epithelial tissues and is found in the gill, skin, fins, oral mucosa and peritoneal lining (although it has also been observed in the tuna heat-exchanger). It does not appear to be present in brain, skeletal muscle, coronary or splanchnic circulations. 3. Parent vessels that form the secondary system have an unusually narrow diameter (2-20 ~tm) and follow a relatively long (200-300 ~tm) and very tortuous path before they anastomose with each other to form progressively larger arteries. 4. Secondary capillaries have very thin walls, appear to lack a basement membrane, and are generally similar to mammalian lymphatic capillaries. Secondary veins are also thin-walled, but they are not otherwise notable. They drain into primary veins of the systemic circulation.
Little is known of the physiological attributes of the secondary system. The narrow lumen of the parent arterioles restricts access of blood cells and hematocrit may be as low as I or 2%. Initial indirect estimates of the volume of the secondary system suggested it was an astounding 1.5 times that of the primary circulation (Steffensen and Lomholt, 1992), although more recent studies indicate that it may be only 10-20% the volume of the primary system (Bushnell et al., 1998). Either way, it is a significant system.
Gill secondary system The body of the gill filament contains two circulatory systems, the nutrient and interlamellar (Chapters 9 and 21) that have many, but not always all, of the characteristics of secondary vessels.
C
0 -<
.<
Nutrient circulation Narrow-bore, tortuous arterioles arise from the gill efferent branchial and the efferent filamental arteries in the basal region of the filament near the anastomosis of the efferent filamental and branchial arteries (Figure 22.7). Curiously, numerous long microvilli stud the endothelial cell surface in both the lumen of
m
@ :13
9 9
"1"1 c rZ --4
6 Z
Z >
9 -<
Figure 22.7 Scanning electron micrograph of a vascular corrosion replica of secondary vessels in the gill of the climbing perch (Anabas testudineus). Numerous narrowbore, tortuous arterioles (arrowheads) arise from the gill efferent filamental artery (EF) and subsequently anastomose to form secondary arteries (S). Bar-40 i~m. (From Olson et al., 1986, with permission.)
EF
EBA
w! Sl~ E(
SI 15L
I--
Figure 22.8 Diagram of a longitudinal section through the lumen of the efferent branchial artery (EBA) illustrating the origin of the secondary vessels shown in Figure 22.7. Villous endothelial cells (VE) guard the lumen of the secondary vessel and are also preferentially located on the upstream lumen of the EBA. AE, typical arterial endothelial cell; BL, basal lamina; SM, smooth muscle; R, red blood cell; arrow shows direction of blood flow. (Drawn from descriptions by Vogel, 1978.)
(
IE
DE
0 I-...I n,.
@ >-
O I-< z
<
--J
< z 0 U Z
u.. U (3.
0
the parent artery (efferent branchial or filamental) near the origin of the secondary arteriole and in the secondary arteriole itself (Figure 22.8). The combined effect of a narrow lumen and the bristly microvilli appears to prevent red blood cells from entering this circulation, although Steffensen and Lomholt (1992) proposed that the microvilli may actually enhance red cell entry. The tortuous secondary arterioles anastomose with each other to form progressively larger arteries that supply what resembles a nutrient system for the arch support tissue and the body of the filament. In some fish, such as the catfish, this system drains from the filament through its own venous network. In many other species the nutrient vessels drain directly into (or supply?) the interlamellar system of the filament.
Figure 22.9 Diagram showing the narrow arteriovenous anastomoses from the efferent filamental artery (EF) to the interlamellar system (IL) in the gill of Tilapia mossambica. Type I endothelial cells contain numerous filaments in concentric whorl-like patterns with centrally located glycogen granules (WG). Type II (11)and intermediate endothelial cells (*) lack the whorled patterns. Other abbreviations: AE, arterial endothelial cell; DES, desmosome; E, endothelial cell; EL, elongated filament; EO, osmophilic endothelial organelles; FT, filamentous tubelike structures; G, glycogen granules; ICP, interstitial cover cell process; IEP, interstitial endothelial cell process; NF, nerve fibers; SC, Schwann cell; SM, smooth muscle; WG, whorled pattern with central glycogen; WP, Weibel Palade bodies. (From Vogel et al., 1974, with permission.)
U
Interlamellar circulation
Systemic secondary circulation
The interlamellar system appears to have its origin via short arterioles that originate from the medial wall of the efferent filamental artery in the distal 90% of the filament (Figure 22.9). The lumen of these vessels is also nearly occluded and the endothelium frequently has microvillar projections and whorled cytoplasmic structures (Vogel et al., 1974). The interlamellar system has a thin-walled endothelium with overlapping cell junctions and it is readily distended by even a slight increase in blood pressure.
The systemic secondary system is similar to that in the gill, although it has received considerably less attention. Steffe,nsen et al. (1986) described long secondary vessels in the fins of the glass catfish that drain into a large diameter longitudinal lateral vein and Vogel (1985) has shown that secondary vessels form a planar meshwork covering the surface of each scale. However, Lahnsteiner et al. (1990) reported that secondary vessels from dorsal segmental arteries anastomose directly with a dorsal cutaneous vein and blood
0 U
returns directly to the heart without an intervening capillary bed. Clearly the systemic secondary system needs additional study.
Retia mirabilia The close physical association between arteries and veins of similar size is a common feature in vertebrate tissues. Usually this is either the most anatomically or hemodynamically efficient route and countercurrent exchange between the arteries and veins is usually neither intended nor desired. In fish, however, there are at least three instances where small blood vessels are specifically arranged to make use of this countercurrent flow. These countercurrent vascular networks, called retia mirabilia (wonderful web), are found in most fish in the swimbladder and in the choroid gland (behind the eye) where they are important in concentrating gases, especially oxygen. They are also found in muscle and near the brain, eye, and gut in tuna and a few sharks, where they are important in regulating temperature of these organs. Fish retia are summarized in Satchell (1991) and Bushnell et al. (1992). All retia in fish share common anatomical features that optimize exchange between the inflow and outflowvessels (Figure 22.10): 1. Retial vessels are arteriole to capillary size in diameter and the supply and return vessels form a dense network of parallel tubes separated by only a sparse interstitial matrix. 2. In most instances retial vessels are considerably longer than typical capillaries, in a 1.9 kg tuna vessels of the heat exchanging rete are I cm long (Stevens et al., 1974). 3. An additional capillary bed is located between the inlet (afferent) and outlet (efferent) retial vessels. These capillaries supply the secretory epithelium of the swimbladder, the choriocapillarias behind the eye, and muscle, brain, eye, and gut tissue in
Figure 22.10 Vascular corrosion replica of the vessels comprising the choroid rete mirable of Channa gachua (viewed from behind the eye). A horseshoe-shaped artery (A) supplies smaller arterioles that radiate out to form long parallel capillaries that in turn supply the choriocapillarias (not shown). Closely apposed venous capillaries (below dashed line and arrowheads) complete the countercurrent loop and return blood to a central vein (V). Capillaries from this 75 g fish are approximately 1 mm long. (Adapted from Munshi et al., 1994, with permission.)
O -< -< u~
tissues associated with the rete to operate at temperatures 10-20~ warmer than the rest of the body. Countercurrent multipliers in the swimbladder and eye require external energy and they can produce a standing gradient that is greater than that which can be produced by simple diffusion. The net effect of this complex process is to force the unloading of gases from blood entering the organ and to prevent their loss in the effluent blood. For example, the choroid gland can increase the partial pressure of oxygen (pO2) to over 500 m m H g in the fish eye. This is five times the pO2 of arterial blood and it is necessary to supply oxygen to the highly active retina, which, unlike mammals, is avascular. Somewhat similar processes are employed in the swimbladder for rapid secretion of oxygen, nitrogen and carbon dioxide, This rapidlychanges the densityof the fish and enables the now neutrally buoyant fish to move up or down the water column.
-!
FIt
C~I~
N
:~ O tn N O -n zN
C
O z t-" Z
O -<
tunas.
Retia may be involved in either countercurrent exchange or countercurrent multiplication. Countercurrent exchange, such as occurs in the tuna heat exchanger, is a passive process. Heat generated through tissue metabolism warms the blood and as this warm blood passes into the efferent retial vessels the heat is transferred to blood in the afferent vessels thereby returning heat to the tissue. This enables
C
Acknowledgment The author is grateful to the National Science Foundation for past and current support through NSF Grant Nos PCM 79-23703, PCM 84-048897, DCB 86-16028, I N T 83-00721, I N T 86-02965, INT 86-18881, IBN 91-05247 and IBN 97-23306.
References
~E U.I
Iu'l Ill >-
0
IU m
U
@ >0 tz
z 0 z u_
0 u 0 r~ u
Agnisola, C. and Tota, B. (1994). Cardioscience 5, 145-153. Bushnell, P.G., Jones, D.R. and Farrell, A.P. (1992). In Fish Physiology Vol. XII, Part A. The Cardiovascular System (eds W.S. Hoar, D.J. Randall and A.P. Farrell), pp. 89-120, Academic Press, San Diego. Bushnell, P.G., Conklin, D.J., Duff, D.W. and Olson, K.R. (1998).J. Exp. Biol. 201, 1381-1391. Couch, J.A. (1990).Anat. Rec. 228, 7-14. Davison, W. (1987). Cell Tissue Res. 248,703-708. Egginton, S. (1992).J. Zool. 226,691-698. Ellis, A.E. and Munroe, A.L.S. (1976).J. FishBiol. 8, 67-78. Farrell, A.P., Jones, D.R. and Roberts, R.J. (1992). In Fish Physiology Vol. XII, Part A. The Cardiovascular System (eds W.S. Hoar, D.J. Randall and A.P. Farrell), pp. 173. Academic Press, San Diego. Kampmeier, O.F. (1969). Evolution and Comparative Morphology of the Lymphatic System. Charles C. Thomas, Springfield, IL. Lahnsteiner, A., Lametschwandtner, A. and Patzner, R.A. (1990). Scan. Microsc. 4, 111-124. Leknes, I.L. (1982).Anat. Anaz.,Jena 152, 125-128. Leknes, I.L. (1987).Acta Histochem. (lena) 81, 175-182. Morris, J.L. and Nilsson, S. (1994). In Comparative Physiology and Evolution of the Autonomic Nervous System (eds S. Nilsson and S. Holmgren), pp. 193246. Harwood Academic Publishers, Chur. Munshi, J.S.D., Roy, P.K., Ghosh, T.K. and Olson, K.R. (1994).Anat. Rec. 238, 77-91. Olson, K.R. (1992). In Fish Physiology Vol.XII, Part B. The Cardiovascular System (eds W.S. Hoar, D.J. Randall and A.P. Farrell), pp. 136-232. Academic Press, San Diego. Olson, K.R. (1996).J. Exp. Zool. 275, 172-185. Olson, K.R. (1997). In The Physiology of Fishes (ed. D.H. Evans), pp. 129-154. CRC Press, Boca Raton. Olson, K.R. and Villa, J. (1991). Am. J. Physiol. Regul. Integr. Comp. Physiol. 260, R925-R933.
Olson, K.R., Munshi, J.S.D., Ghosh, T.K. and Ojha, J. (1986).Arn. J. Anat. 176,305-320. Priede, I.G. (1975).J. Zool., Lond. 175, 39-52. Priede, I.G. (1976).J. Fish Biol. 9, 209-216. S~etersdal, T.S., Justesen, N.-P. and Krohnstad, A.W. (1974).J. Mol. Cell Cardiol. 6, 415-437. Sfinchez-Quintana, D., Garcia-Martinez, V., Climent, V. and HurlS, J.M. (1996).J. Exp. Biol. 275, 112-124. Santer, R.M. (1985). Adv. Anat., Embryol. Cell Biol. 89, 1-102. Santer, R.M. and Greer Walker, M. (1980).J. Zool., Lond. 190,259-272. Santer, R.M., Greer Walker, M.G., Emerson, L. and Witthames, P.R. (1983). Cornp. Biochem. Physiol. 76A, 453-457. Satchell, G.H. (1991). Physiology and Form of Fish Circulation. Cambridge University Press, New York. Smith, U., Ryan, J.W., Michie, D.D. and Smith, D.S. (1971). Science 173, 925-927. Steffensen, J.F. and Lomholt, J.P. (1992). In Fish Physiology Vol. XII, Part~Z The Cardiovascular System (eds W.S. Hoar, D.J. Randall and A.P. Farrell), pp. 185-213. Academic Press, San Diego. Steffensen, J.F., Lomholt, J.P. and Vogel, W.O.P. (1986). Acta. Zool. (Stockh.) 67, 193-200. Stevens, E.D., Lam, H.M. and Kendall, J. (1974).J. Exp. Biol. 61,145-153. Tibbits, G.F., Moyes, C.D. and Hove-Madsen, L. (1992). In Fish Physiology Volume XII, Part A. The Cardiovascular System (eds W.S. Hoar, D.J. Randall and A.P. Farrell), pp. 267-297. Academic Press, San Diego. Vogel, W.O.P. (1978). Z. Mikrosk. Anat. Forsch. 92, 565570. Vogel, W.O.P. (1985). In Cardiovascular Shunts. Phylogenetic, Ontogenetic and Clinical Aspects (eds K. Johansen and W. Burggren), pp. 143-159, Munksgaard, Copenhagen. Vogel, W., Vogel, V. and Schlote, W. (1974). Cell Tissue Res. 155, 491-512.