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Phylogeny, morphology and physiology of the secondary vascular system in fishes

Vascular casts of three chondrichthian, one dipnoan, one chondrostean and 14 teleostean species were examined by light and scanning electron microscopy in order to give a qualitative and quantitative analysis of interarterial anastomoses (iaas) that indicate the presence (or absence) of a secondary vascular system (SVS). Anastomoses were found to originate from a variety of different primary blood vessels, many of which have not been previously identified as giving rise to secondary vessels. Segmental arteries derived from the dorsal aorta and supplying body musculature were major sites of origin of the SVS, although there was considerable variation in where, in the hierarchy of arterial branching, the anastomoses occurred. The degree of investment in a SVS was species specific, with more active species having a higher degree of secondary vascularisation. This difference was quantified using an absolute count of iaas between Anguilla reinhardtii and Trachinotus baillonii. A range of general features of the SVS is also described. No evidence of iaas was found on the coeliac, mesenteric or renal circulation in any species. Evidence of interarterial anastomoses were lacking in the dipnoan (Sarcopterygii) and chondrichthyan species examined, suggesting that a SVS is restricted to actinopterygian fishes. The presence and distribution of a secondary vascular system does not appear to be exclusively linked to phylogenetic position, but rather to the physiological adaptation of the species. Histological sections of primary segmental arteries and associated interarterial anastomoses and secondary vessels from the long-finned eel, Anguilla reinhardtii, were examined by light and transmission electron microscopy. Secondary vessels were found to originate from the primary vasculature as depressions through the tunica intima and media, from where they ran perpendicularly to the adventitial layer, before coiling extensively. From here the anastomoses travelled a relatively linear path in the outer margin of the adventitia to re-anastomose with a secondary vessel running in parallel with the primary counterpart. Secondary vessels had a structure quite similar to that of primary vessels; they were lined by endothelial cells on a continuous basement membrane, surrounded by single layer of smooth muscle cells surrounding the vessel. Smooth muscle cells were also found in the vicinity of interarterial anastomoses in the adventitia, but these were more longitudinally orientated. The presence of smooth muscle cells on all aspects of the secondary circulation suggests that this vascular system is regulated in a similar manner as the primary vascular system. Because interarterial anastomoses are structurally integrated with the primary vessel from which they originate, it was anticipated that flow through secondary vessels would to some extent be affected by an increase in primary vascular tone. Immunohistochemical studies showed that primary segmental arteries displayed moderate immunoreactivity to antibodies against 5-hydroxytryptamine and substance P, while interarterial anastomoses and secondary vessels showed dense immunoreactivity. Secondary vessels were followed to the surface of the animal through consecutive sections, where they eventually give rise to capillary beds overlying the scales. Secondary capillary beds were found to supply chloride cells in the skin, suggesting that this vascular system may be involved in cutaneous ionic exchange. Branchial vascular casts from two species of Tetraodontiformes showed that the vessels previously reported as nutrient vessels are with certainty part of the secondary vascular system. In the three-barred porcupine fish, Dicotylichthys punctulatus, interarterial anastomoses originated at high densities from efferent filamental and the efferent branchial arteries, from where they formed progressively larger secondary vessels. Small branches of this vascular system entered the filament body, where it gave rise to numerous side-vessels along the way. Large secondary vessels running in parallel with the efferent branchial arteries were found to constitute an additional arterio-arterial pathway, in that they exited the branchial basket in company with the afferent mandibular artery, the carotid artery and the efferent branchial arteries, from where they gave rise to vascular beds immediately after exit. The secondary vessels in this species were not found to supply the filament musculature; rather this vascular system was supplied by a single vessel derived from the efferent branchial artery, running in parallel with the afferent branchial artery. Secondary vessels were not found on any branchial component in the banded toadfish, Marylina pleurosticta, but in all other aspects the branchial vascular anatomy was similar to that of D. punctulatus. It is proposed that four independent vascular pathways may be present in the teleostean gill. The blood volume and flow rates of the primary (PVS) and secondary vascular system (SVS) were examined in the catadromous euryhaline teleost Lates calcarifer in order to determine whether any of these parameters were subject to change in individuals acclimated to seawater, compared to a group acclimated to freshwater. There was no significant difference in any measured parameter for the two groups. The volumes of the SVS were 0.67 b 0.13 and 0.76 b 0.13 mL 100g-1 body mass for FW and SW acclimated animals respectively. This constituted approximately one-third of the total blood volume in both groups. Turnover times for the SVS ranged from 21.0 to 25.2 minutes, demonstrating in accordance with previous publications, that this system is considerably more dynamic than previously assumed.