Gill Blood Flow Control

Comp. Biochem. Physiol. Vol. 119A, No. 1, pp. 137–147, 1998 Copyright  1998 Elsevier Science Inc. All rights reserved.

ISSN 1095-6433/98/$19.00 PII S1095-6433(97)00397-8

Gill Blood Flow Control Stefan Nilsson and Lena Sundin Department of Zoophysiology, University of Go¨teborg, Medicinaregatan 18, S-413 90 Go¨teborg, Sweden ABSTRACT. The arrangement of the fish gill vasculature is quite complex, and varies between the different fish groups. The use of vascular casting techniques has greatly enhanced our knowledge of the anatomy of the branchial microcirculation, not least through the contributions of Pierre Laurent and co-workers at Strasbourg. At different physiological situations, the contact surface between water and blood (functional surface area) varies to balance oxygen uptake against osmotic water flow (‘‘respiratory-osmoregulatory compromise’’). This is controlled by nerves and by blood-borne or locally released substances that affect blood flow patterns in the gill. Histochemical techniques have been used to demonstrate neurotransmitter substances in the branchial innervation. In combination with physiological experiments on isolated tissues, perfused gill preparations and whole animals it has become possible to produce models for the vascular control in fish gills and the role of this control in optimising the ‘‘respiratory-osmoregulatory compromise’’ at different physiological situations. comp biochem physiol 119A;1:137–147, 1998.  1998 Elsevier Science Inc. KEY WORDS. Teleost fish, branchial vasculature, autonomic nervous system, vasomotor control

INTRODUCTION The fish gill is an intriguing and complex organ. It comprises several tissues and cell types, with specific functions related to respiration, ion regulation and sensation. The most well-known function of the gill is that of a respiratory organ, where water flows over the gill surface, leaving oxygen to the branchial blood system and removing carbon dioxide. In addition, fish gills perform many tasks of the kidney of land-dwelling vertebrates, in regulating plasma osmolarity, ion composition and acid-base balance. The ionic composition of the fish blood plasma is continuously challenged by the ionic composition of the surrounding water. There is a net influx of water along the osmotic gradient of freshwater fish and outflux in seawater fish (at least in teleosts). Reduction of the contact surface between water and blood (functional surface area) reduces the water permeability of the gills. However, if respiratory demands increase, then the functional surface area needs to increase to facilitate gas exchange. The control of the branchial vasculature by nerves and by bloodborne or locally released substances works to optimise this ‘‘respiratory-osmoregulatory compromise’’ under different physiological situations. The arrangement of the branchial vasculature is very complex. There is substantial variance between the different fish groups, both relating to gross anatomy such as the number of gill arches and more intricate details such as the Address reprint requests to: S. Nilsson, Department of Zoophysiology, University of Go¨teborg, Medicinaregatan 18, S-413 90 Go¨teborg, Sweden. Tel. 146-31-773-3669; Fax 146-31-773-3807; E-mail: [email protected], [email protected]. Received 26 June 1996; accepted 26 November 1996.

microvasculature of the gill filaments. A detailed discussion of the internal gill anatomy and vascular arrangement in several fish groups can be found in articles by Pierre Laurent and co-workers. Noteworthy contributions include the classical paper on gill blood pathways by Laurent and Dunel (63) and the comprehensive review of gill internal morphology by Laurent (62). We discuss the arrangement and control of the branchial vasculature in fishes, focusing on the situation in teleosts. ARRANGEMENT OF THE BRANCHIAL VASCULATURE A major cause for our knowledge of the complex microanatomy of the gill vasculature is the introduction of vascular casting techniques. These allow a detailed study of the vascular spaces by binocular microscope or scanning electron microscope (28,29,47,63). These studies have laid the necessary foundation for our understanding of how the branchial vasculature works and how blood flow is controlled. In teleost fish, blood from the ventral aorta enters the gills via four pairs of afferent branchial arteries, which run within the gill arch, sending branches (afferent filamental arteries [AFA]) into the gill filaments (sometimes also known as ‘‘primary lamellae’’). From the AFAs, lamellar arterioles (afferent lamellar arterioles) enter the secondary lamellae where gas exchange takes place. The oxygenated blood enters into the systemic vasculature via the efferent lamellar arterioles (ELa), efferent filamental arteries (EFA) and efferent branchial arteries (Fig. 1). This ‘‘respiratory’’ blood path is known as the arterio-arterial pathway, and, in

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FIG. 1. Arrangement of the branchial vasculature in the cod,

showing the main relationship between the different vessels. The approximate locations of the efferent filamental arterial sphincters are indicated. ABA, afferent branchial artery; ALa, afferent lamellar arteriole; BN, branchial nerve; BV, branchial vein; EBA, efferent branchial artery; Fil, filaments; GA, gill arch; SL, (secondary) lamellae; Sph, sphincter at the base of the efferent filamental artery; SuV, subepithelial vessels. Modified from Nilsson (85).

addition, blood may flow from the efferent vessels back to the heart via an arterio-venous pathway. This flow may either take place via short anastomoses from the EFAs into the central venous system (CVS) of the filament and via the branchial veins or via a ‘‘systemic’’ (nutritive) vasculature that supplies the gill tissues (Fig. 1). In some species (e.g., eel, catfish and Tilapia), anastomoses also occur on the afferent side of the filament (62). The sphincters located at the bases of the EFAs are presumed to be major sites of blood flow control in the branchial vascular tree. These sphincters receive a substantial innervation from the branchial nerves, and, in addition, there is a possibility of a paracrine control via serotoninreleasing cells in the proximal portions of the filaments. In elasmobranchs, the vascular arrangement is somewhat similar, except that the filamental arteries form large corpora cavernosa. These could function as a hydraulic skeleton of the gill filament, which otherwise lacks skeletal support. They may also be important in smoothing the pressure pulses from the heart similar to the function of the conus arteriosus (62,105). INNERVATION OF THE GILLS Both sensory and motor pathways reach the gill arches in nerve trunks from the vagus (X) and glossopharyngeal (IX)

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(79,83). The glossopharyngeal is the major sensory nerve of the pseudobranch in many teleosts, and motor fibres to the first gill arch run in the post-trematic branch. The second to fourth gill arches are supplied by vagal branches, which carry both sensory and motor nerves, including both cranial (‘‘parasympathetic’’) and spinal (‘‘sympathetic’’) autonomic pathways. A relatively sparse innervation of the branchial vasculature by adrenergic fibres of sympathetic autonomic origin has been demonstrated using either electron microscopy or the Falck-Hillarp fluorescence histochemical technique in trout (Oncorhynchus mykiss), cod (Gadus morhua), perch (Perca fluviatilis), pike-perch (Sander lucioperca), catfish (Ictalurus melas), black bass (Micropterus dolomieui) and the airbreathing teleost Channa argus (2,33,35,38,53,85). The innervation runs mostly to the nutritive vasculature of the gill, and fibres are also found in the AFAs and EFAs, especially in the sphincter region near the base of the EFAs. A plexus of fibres surrounds the CVS. Nerve fibres also run close to the arterio-venous anastomoses, and an innervation of these has been postulated (133). The function of this innervation has, however, been questioned (62). Electrical stimulation of the sympathetic supply to the gills of the cod demonstrated a functional adrenergic nervous control of the arterio-venous pathway (88,101). Constriction of this pathway may also be responsible for an increase of the arterio-arterial blood flow. The role of an adrenergic innervation of the arterio-arterial pathway is less clear, and circulating catecholamines may be more important in this control (see later). In addition to the adrenergic innervation of the branchial vasculature, a cholinergic innervation of the EFA sphincter has been concluded from the ultrastructure of nerve profiles in the sphincter (34). Serotonergic fibres also run to the EFA sphincter (3), and a role of serotonin in the control of the branchial blood flow seems likely (see later). Recent histochemical studies also demonstrate the presence of NADPH-diaphorase (a nitric oxide synthase [NOS]) in branchial neurones from the cod (48). The NADPH-diaphorase reactivity occurs in 55–85% of all neurones within the branchial nerves. In the mammalian parasympathetic system, NOS has been found in both cholinergic and noncholinergic neurones. The role of the nitric oxide neurones of fish gills is not known, but the innervation conceivably adds a vasoinhibitory nerve element to the control pattern. Direct observation by light microscopy of the trout gill filaments and simultaneous measurement of key cardiovascular parameters in vivo has shown a marked branchial vasoconstriction during hypoxia. Most of this vasoconstriction is abolished by atropine. The response is insensitive to both serotonin and adenosine antagonists, and the nature of the control needs further attention (L. Sundin and G. Nilsson, unpublished data). The structure of the gill that is most densely innervated by adrenergic fibres is the smooth transverse abductor muscle that attaches to the proximal ends of the filamental car-

Gill Blood Flow Control

tilage rods (36,62,84). Electrical stimulation of the sympathetic nerve supply to the cod gill arches produces an α-adrenoceptor-mediated contraction of these muscles, causing abduction of the gill filaments (84). CONTROL OF THE GILL VASCULATURE BY CIRCULATING CATECHOLAMINES The branchial vascular resistance of perfused gills can be altered by many substances, notably acetylcholine, catecholamines, serotonin (5-hydroxytryptamine [5-HT]) and several peptides (58,83,87,98,122,127). A large number of studies have been aimed at the effects of catecholamines on blood flow in fish gills. In addition to the demonstration of an α-adrenoceptor mediated nervous control of the arteriovenous pathway, there is good evidence of a humoral modulation of the vascular resistance of the gills by circulating catecholamines (notably adrenaline). In fact, these may be more important than the adrenergic innervation in the adrenergic control of the arterio-arterial pathway, not only in elasmobranchs (where no adrenergic innervation of the gill vasculature exists) but also in the teleosts (30,88). The idea of a humoral adrenergic control of the branchial vasculature rests on two pieces of evidence. First, estimation of the levels of circulating catecholamines in fish show that the range of the adrenaline concentrations found during different physiological conditions [trout (81), cod (136)] overlaps the concentration-response curve for adrenaline in perfused fish gills [trout (138,139), cod (83,134,135)]. In their experiments with the dogfish, Scyliorhinus canicula, Davies and Rankin (30) demonstrated directly that the adrenaline level in blood plasma from ‘‘stressed’’ animals was sufficient to produce dilation of the branchial vasculature in a the perfused gill preparation. Second, the release of catecholamines from the head kidney stores in the cod by electrical stimulation is sufficient to affect the branchial vascular resistance, even at low-stimulation frequencies (135). In these experiments, a perfused gill arch was used as an ‘‘on-line bioassay’’ of the catecholamine released from the perfused cod head kidney (posterior cardinal vein). At stimulation frequencies from 1 to 5 Hz, there was a steep increase in the catecholamine release as judged from changes in the input pressure to the gill arch, and maximal release was found at 8–10 Hz. The result can be interpreted in favour of a functional control of the branchial vascular resistance by catecholamines released from the head kidney (135). LOCALISATION AND EFFECTS OF SEROTONIN The observation that neither α-adrenoceptor nor cholinoceptor antagonists were able to completely abolish the nerve-induced branchial vasoconstriction led Pettersson and Nilsson (101) to suggest the presence of a non-adrenergic, non-cholinergic (NANC) component in the vasocon-

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strictor innervation of the gill vasculature. Serotonin is present in both neuronal processes and cells in fish gills and is in addition a potent vasoconstrictor of the branchial vasculature. The putative cardiovascular control by NANC transmitters in fish has been reviewed by Nilsson and Holmgren (87) and, more specifically, the serotonergic vasomotor control in fish gills by Sundin (122). Localisation The teleosts are so far the only group of fish where intrafilamental serotonergic neurones and nerve fibres have been demonstrated. The innervation reaches the sphincter, the proximal part of the EFAs and adjacent ELas and extends towards the CVS. A corresponding serotonergic innervation of the afferent vasculature appears to be absent (3,38). Denervation of pro- and metatrematic branches of the branchial nerves produces a complete loss of formaldehydeinduced green fluorescence characteristic of catecholaminergic nerves, whereas yellow fluorescence, indicating serotonergic innervation, remains intact (3,38). Thus, the serotonergic neurones of the gills are intrinsic, adhering to the general pattern of cranial autonomic (parasympathetic) postganglionic neurones [cf. (82)]. However, precation must be taken because severed nerves in fish survive much longer than nerves in mammals (55). Other stores of serotonin in the gills are the neuroepithelial cells (NECs) and polymorphous granular cells (PGCs). Similar to the location of the neurones, serotonin-immunoreactive NECs are situated on the efferent side of the filament facing the respiratory water flow. In contrast to the neurones, these cell types have also been found in non-teleost fish (3,4,37,143). Single NECs occur along the whole length of the gill filament but are mainly located in the distal half where, in some species, they may form clusters. The PGCs are scattered throughout the filamental parenchyma. The latter type of cell has only been described in rainbow trout (3,4,37,143). Vasomotor Control In mammals, serotonin induces vasoconstriction or vasodilatation directly via vascular smooth muscle receptors or may indirectly cause vasodilatation via the release of endothelium-derived relaxing factors (7,24,67,70). The major cardiovascular action of serotonin in fish is the constriction of the arterio-arterial branchial vasculature (46,57,98, 109,125,127). The proximal part of the EFAs is innervated by serotonergic neurones, and it has been postulated that these neurones may play a role in the recruiting of additional lamellae when an increase of gas exchange is required (3). However, serotonin injected in rainbow in vivo trout impaired gas exchange (46), possibly due to the vasoconstriction in the distal portion of the filament observed by Sundin et al. (127), which led to a reduction of the number of lamellae perfused.

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NECs are present particularly in the distal part of the filament. A paracrine effect of serotonin released from NECs on the branchial vascular resistance is conceivable [(37); cf. (4,142)]. Indeed, severe hypoxia causes de-granulation of NECs in rainbow trout (37). A physiological role for serotonin has been postulated in the cardiorespiratory events in rainbow trout during gradual exposure to hypoxia (46) and acidosis (131). However, the adaptive value of the observed vasoconstriction is not fully understood. In the Atlantic cod, an additional effect of serotonin is an increase of the arterio-venous flow, which is caused by a decrease of the arterio-venous vascular resistance (121,125) (Fig. 2). Recent results point towards an increase of the blood flow through the arterio-venous pathway during hypoxia (121) (L. Sundin and G. Nilsson, unpublished data), and this effect could be related to serotonin release. The 5-HT 1 /5-HT 2 receptor antagonist methysergide abolished the serotonin-induced vasoconstriction of gill vessels (46,127) but not the vasodilator effect of the arterio-venous pathway (121). This suggests the presence of different serotonergic receptors in fish gills. In contrast, methysergide is a potent antagonist in both the endothelium-dependent and the endothelium-independent inhibitory mechanisms of the rabbit jugular vein (67,74). This finding adds complexity to the mechanisms behind the vasodilator action of serotonin in the branchial vasomotor control. OTHER VASOACTIVE SUBSTANCES Nucleotides ATP or a related purine derivative has been postulated as a neurotransmitter in some mammalian systems [see (16,17)]. Its role as a transmitter in the autonomic nervous system in non-mammalian vertebrates is, however, uncertain (51,86). Adenosine, on the other hand, is released by energy-deficient cells due to the breakdown of ATP, ADP and AMP and can act as a humoral agent [see (96)]. There is evidence for adenosine production in rainbow trout gill (69) and hypoxic flounder hearts (68). Most investigations that aim at clarifying the role of nucleotides on blood flow regulation in the gill vasculature have focused on the role of adenosine. In perfused head preparations of rainbow trout, adenosine and related nucleotides (AMP, ATP) cause vasoconstriction of arterial gill vessels. The response produced by adenosine is completely inhibited by the adenosine P 1-receptor antagonist theophylline (25,26). The constrictor effect of adenosine in the teleost gill vasculature has been confirmed in the cichlid, Oreochromis niloticus (89). By using various adenosine analogues, Colin and Leray (27) provided a base for the hypothesis of specific purinergic receptors in the branchial vasculature of rainbow trout. Two subgroups of P1-receptors (A 1 being excitatory and A 2 being inhibitory) have been identified in the ventral aorta of the dogfish, Squalus acanthias (39), and it has been shown that the excitatory vasomotor effect of adenosine in rainbow trout is spe-

cifically mediated via the A1-receptor (126). In the same in vivo experiment, it was noted that the net effect of adenosine was a redistribution of blood towards the arterio-venous circulation. This finding is consistent with previous perfusion experiments where adenosine induced an increase of the arterio-venous flow (25,112). Hypoxia increases the branchial vascular resistance in teleosts (50,99,100,112,126). In the Atlantic cod, the portion of cardiac output flowing through the arterio-venous pathway also increases (121). Adenosine-induced vasoconstriction does not seem to contribute to the hypoxic increase of the branchial resistance in rainbow trout, although adenosine increases the arterio-venous flow (126) (L. Sundin and G. Nilsson, unpublished data). Peptides The atrial natriuretic peptides (ANP) relax all isolated fish vessels examined, including the ventral aorta from cyclostomes, elasmobranchs and teleosts (91). A role for ANP in gill blood flow control has been postulated (40,132). ANP relaxes pre-contracted major blood vessels of the Atlantic salmon (S. salar) and the Atlantic cod (Gadus morhua) (128). These observations are consistent with the inhibitory effect ofthe peptidesin the perfused gills of the trout O. mykiss (Salmo gairdneri) (94) and the toadfish, Opsanus beta (40). In addition to the possible vasomotor effects, the ANPs are involved in ionic regulation in fish [see, e.g., (137)]. Gastrin, cholecystokinin (CCK) and caerulein belong to the gastrin/cholecystokinin family of peptides. Gastrin-like immunoreactivity has been observed in the gills of the Atlantic cod (S. Holmgren, personal communication), and the sulphated forms of CCK-8 and caerulein cause a very marked constriction of the branchial vessels (125). Sulphated CCK-8 also constricts arteries in the gill pouch of the Pacific hagfish, Eptatretus cirrhatus (124). The neurohypophysial peptides, isotocin, oxytocin and arginine vasotocin constrict the branchial vessels in fish (22,23,108). In addition, Chan (cit in 108) observed that isotocin diverted blood away from the secondary lamellae in the Japanese eel, Anguilla japonica, possibly towards the central compartments (see 108). Neuropeptide Y (NPY) contracts the afferent gill artery of the common dogfish, Scyliorhinus canicula, and a NPYlike immunoreactive peptide has also been demonstrated in neurones (6). Similarly, NPY-like immunoreactivity has been demonstrated in the branchial arteries of Raja erinacea and Raja radiata. However, no NPY-like immunoreactivity could be demonstrated in the cardiovascular system of the two teleosts cod (G. morhua) and rainbow trout (O. mykiss) (5). The lack of immunoreactivity to NPY in the teleosts agrees with the finding that porcine NPY does not affect the ventral aortic blood pressure in cod (J. Gunnarsson, unpublished observations). However, NPY–immunoreactive neuroendocrine cells have been shown in the filamental epithelium of the teleost Oreochromis mossambicus (137).

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Vasoactive intestinal peptide (VIP) causes a concentration-dependent vasodilation in perfused brown trout (Salmo trutta) gill arches. The response can be blocked by indomethacin, which suggests a possible involvement of prostaglandins (8). VIP-immunoreactive fibres are present in Atlantic cod gill vasculature (87).

Endothelial-Derived Factors

FIG. 2. A generalised model for the autonomic innervation

of the teleost branchial vasculature (A) and putative sites of effects for humoral/local agents such as circulating catecholamines (CATs), adenosine (ADO) and serotonin (5-HT) (B), showing possible sites for control of the vascular resistance. The sphincter at the base of the efferent filamental arteries are likely to have major effects on the flow profile. The innervation of the sphincter includes adrenergic, cholinergic and serotonergic fibres; in addition, NADPH-diaphorase reactive neurones indicative of nitric oxide-releasing neurones have been observed in the branchial nerve. The target for these neurones is, however, not known. The postganglionic neurones of the cranial autonomic (parasympathetic) pathways are likely to reside within the gill arch, because denervation experiments fail to remove the cholinergic and serotonergic nerve terminals (3,38). The cholinergic and serotonergic pathways are vasconstricor, whereas the adrenergic effect on the sphincter is likely to be inhibitory, mediated via b-adrenoceptors. Adrenergic fibres to the nutritive vasculature and, indeed, to the entire ‘‘systemic’’ circulation of the gills cause vasoconstriction via a-adrenoceptors, just as in other systemic vascular beds. An adrenergic control via circulating catecholamines acts chiefly on the arterio-arterial pathway. a, a-adrenoceptor; ACh, cholinergic nerve; Adr, adrenergic nerve; ALa, afferent lamellar arteriole; b, b-adrenoceptor; BN, branchial nerve; BV,

Endothelin is one of the most potent vasoconstrictor substances known and has been proposed to be one of the putative endothelium-derived constrictor factors (EDCFs) (66,75). The presence of endothelin-like immunoreactivity has been established in fish gills (56), and a novel endothelin receptor has been demonstrated in rainbow trout gills, with the highest density of receptors in the secondary lamellae (71). Isolated perfused trout gill arches are very sensitive to endothelin-1, which produces a dose-dependent vasoconstriction (92). In addition, it was found that in the Atlantic cod, EDCFs (yet unindentified) may be produced and released by the branchial vascular endothelium. The production seems to be restricted to the efferent vasculature in the Atlantic salmon (128,129). Possible candidates for the unidentified EDCFs in teleosts are PGI 2 and leukotrienes (103,104). In addition to their demonstration of EDCFs, Sverdrup and co-workers (128,129) showed that the cod gill vasculature and the efferent vasculature of salmon also produces endothelium-derived relaxing factors (EDRFs). EDRFs may be prostanoic (prostaglandins) or non-prostanoic (nitric oxide), and in concert with the findings of Olson and Villa (95) in trout, no evidence for a non-prostanoic factors in salmon vessels were found by Sverdrup and co-workers (128,129). However, EDRFs of both prostanoic and nonprostanoic origin were present in the cod ventral aorta. In addition, nitric oxide-dependent regulation of brain blood flow has been demonstrated in rainbow trout (118). Therefore, a non-prostanoic mechanism in the vasomotor control of fish gills seems possible.

CARDIOVASCULAR REFLEXES ORIGINATING IN THE GILLS Several types of receptors sensitive to different mechanical and many kinds of chemical stimuli occur in the branchial region of fish (15,45,83). The vascular events of the gills

branchial vein; CATs, circulating catecholamines; CNS, central nervous system; m, muscarinic cholinoceptor; NO, nitric oxide-releasing nerve and possible site of action; NV, nutritional vasculature; sc, sympathetic chain; SL, (secondary) lamella; Sph, sphincter at the base of the efferent filamental artery; X, vagus nerve. 1 and 2 indicate vasoconstrictor and vasodilator effects, respectively. Modified from Sundin (123).

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are intimately linked to flow and pressure changes caused by altered cardiac performance and changes in systemic and branchial vascular resistance. This section deals with those receptors residing in the gills that are associated with the cardiovascular reflexes (i.e., baro- and chemoreceptors). Reflex effects on ventilation, other receptor types and reflexes emanating from extrabranchial receptor areas are reviewed elsewhere (15,54,83). Baroreceptor Reflexes Free nerve endings in the walls of blood vessels that are sensitive to mechanical distortion of the blood vessel caused by changes in the blood pressure are generally called baroreceptors. If the blood pressure is disturbed, it can be restored to the former level by reflex effects on cardiac output, peripheral resistance or both. In fish, baroreceptive areas other than the gills (including the pseudobranch) have not been positively identified. However, catfish possess carotid labyrinths associated with the carotid arteries that may represent an extrabranchial baroreceptive area, although definitive physiological evidence is wanting (93,119). Baroreceptive activity in teleosts has been observed in the post-trematic branches of the glossopharyngeal (cranial nerve IX) (afferent pathway from the first gill arch) and vagus (X) (afferent pathway from the other branchial arches). The sensitivity declines progressively from the first to the fourth pair in the carp, Cyprinus carpio (111). The exact location of the baroreceptors is unknown, but in salmonids, supposed baroreceptive regions include the afferent branchial arteries, where rete mirable jackets receive an extensive supply of nerve fibres (32). The most dense innervation of the branchial vasculature is found at the junction of the efferent filamental arteries and the efferent branchial arteries in both elasmobranchs and teleosts. These regions may be involved in baroreception, although definitive evidence is lacking (10,34). In elasmobranchs, stimulation of potential baroceptive areas by abrupt increases in perfusion pressure or electrical stimulation of the branchial nerves IX and X causes a reflex bradycardia. As in mammals, the inhibitory vagal fibres to the heart constitutes the efferent limb of the reflex arc (72, 73). By recording afferent nerve activity from these nerves, Irving et al. (52) confirmed the presence of receptors that increased neural activity in response to increased blood pressure. In contrast, no evidence of blood pressure homeostasis was found during haemorrahage in the elasmobranchs Mustelus canis and Squalus acanthias (97,120). It is thus possible that the elasmobranch vascular system is less able to respond to pressure changes than that of the teleosts [cf. (1)]. Branchial baroreceptors have been demonstrated directly and indirectly in several species of teleosts. In the eel (Anguilla anguilla), stimulation of the central ends of the branchial nerves caused a reflex bradycardia and, in addi-

tion, high perfusion pressure through the first branchial arteries inhibited the heart (80). Increasing the perfusion pressure in the perfused gill arches in the carp (C. carpio) also produced a reflex bradycardia and a fall in arterial pressure. These reflex responses were abolished by vagotomy or atropine (110). More recently, Burleson and Milsom (11) identified baroreceptors in the first gill arch of rainbow trout, with afferent neural activity that was altered in response to changes in perfusion pressure. In un-anaesthetised fish in vivo, Farrell (41) demonstrated a reflex bradycardia by increasing the water pressure around the trunk of the sea raven (Hemitripterus americanus). The opposite, a vagal tachycardia, occurred during hypotension produced by either haemorrhage or α-adrenoceptor blockade in trout (141). These two studies suggest the presence of a barostatic reflex in teleosts. Chemoreceptor Reflexes The presence of oxygen-sensitive chemoreceptors in the pseudobranchs of tench (Tinca tinca) and rainbow trout have been indicated in the early studies by Laurent (59,60) and Laurent and Rouzeau (64,65). Afferent activity from receptors in the isolated first gill arch of the yellow-fin tuna have been recorded, and most external chemoreceptors increased their activity in response to decreasing external Po 2 (78). Another group of O2-sensing chemoreceptors (internal chemoreceptors) detects altered oxygen levels in the blood. The two groups of chemoreceptors contribute to reflexes that warrant an efficient breathing pattern and proper ventilation-perfusion matching at the gas exchange surface. The latter is achieved through reflex effects on heart rate, cardiac output, arterial blood pressure and altered blood flow distribution through the gills. It has been suggested that external chemoreceptors are responsible for both ventilatory and cardiovascular reflexes, whereas internal chemoreceptors appear to be involved in the ventilatory reflexes only (11,14,20,21,49,76,107,113, 115,117,140). This section therefore focuses on cardiovascular reflex effects triggered by externally oriented chemoreceptors. Elasmobranchs have a diffuse receptor system dispersed throughout the orobranchial and parabranchial cavities and innervated by the cranial nerves V, VII, IX and X (19). In teleosts, it has been shown that all gill arches possess O 2 chemosensitivity but the O2-sensitive chemoreceptors responsible for cardiovascular reflexes are primarily confined to the first gill arch in salmonids (11,31,116,117), in the Atlantic cod (43) and in the yellow-fin tuna (78). These teleost O2-sensitive chemoreceptors are innervated by the branchial branches of the cranial nerves IX and X and may be homologus to the receptors found in the carotid body in mammals (11,19). The cardiac responses to environmental hypoxia in both elasmobranchs and teleosts involve instant bradycardia and

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an increase in cardiac stroke volume (18,43,102,106,114, 130). Sectioning of cranial nerves V, VII, IX and X to the gills abolishes the reflex bradycardia in dogfish (19), whereas sectioning of IX and X inhibits the cardiac reflex in trout (117), cod (43) and channel catfish (14). In addition, externally oriented O2 receptors, sensitive to the O2 levels of the water and responsible for triggering bradycardia, are found in the gar Lepisosteus osseus (115) and bowfin Amia calva (76), the sturgeon Acipenser naccarii (77) and the channel catfish Ictalurus punctatus (13). In some species, the bradycardia induced by hypoxia may be weak or even absent [see (45)]. In addition to cardiac reflexes, some teleosts show an elevated systemic resistance that leads to an increase of the arterial blood pressure during hypoxia (12,14,43,44,50,113, 139,141). The reflex hypertension remains after denervation of the first gill arch (43) or complete branchial denervation (113), suggesting that the receptors triggering this blood pressure reflex are extra-branchial. There is no elevation of the arterio-arterial resistance in cod during hypoxia (43,121). However, an α-adrenoceptormediated response increases the arterio-venous resistance, thus contributing to the hypoxia-induced hypertension in cod (121). Furthermore, in rainbow trout, it has been demonstrated that a cholinergic reflex response of the gill vasculature to hypoxia depends on a constriction of the proximal part of the EFA, possibly the EFA sphincter (L. Sundin and G. Nilsson, unpublished data). The location of the receptors activating the reflex responses of the branchial vasculature is unknown. All reflex effects increasing the lamellar perfusion pressure may promote lamellar recruitment and secure the distribution of blood within the lamellae to promote oxygen uptake (9,42). CONCLUDING REMARKS Structural studies using vascular casting techniques, sometimes in combination with scanning electron microscopy, laid the foundation to our understanding of the branchial vascular arrangement in fishes. Various histochemical techniques have made it possible to actually see the transmitter substances of nerves and other biologically active compounds in cells of the gills. The structural observations could then be combined with physiological experiments using tissues, perfused gill preparations and whole animals. In these experiments, the normal function of the gill vasculature could be perturbed by administration of ‘‘pharmacological tools,’’ agents that interfere with neurotransmission and hormonal effects. On such combinations of structural and functional observations and experiments rests our knowledge of the gill vasculature and its capacity to optimise this ‘‘respiratory-osmoregulatory compromise’’ under different physiological situations. An attempt to summarise the pattern of control of the gill vasculature is offered in Fig. 2.

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This review is dedicated to Professor Pierre Laurent, pioneer in the study of fish gill structure and function. Our own research is currently supported by the Swedish Natural Science Research Council (NFR).

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