The blood volumes of the primary and secondary circulatory system in the Atlantic cod<i>Gadus morhua</i>L., using plasma bound Evans Blue and compartmental analysis

Skov, Peter Vilhelm; Steffensen, John F.

doi:10.1242/jeb.00113

Cited by 16 publications

(15 citation statements)

References 37 publications

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“…It has been reported that the secondary vascular system can range from 10-50% to nearly twice the volume of the primary circulation (Steffensen and Lomholt, 1992; Bushnell et al, 1998;Gallaugher and Farrell, 1998;Skov and Steffensen, 2003). The magnitude of other effects, such as splenic release of RBCs, increases in RBC volume and blood volume reduction (see above) may also play a role in differences in the magnitude of the haematocrit change with increased RBCs flow into the SVS of different fish species.…”

Section: The Journal Of Experimental Biologymentioning

confidence: 98%

“…The volume of the SVS can range from 10-50% to nearly twice the volume of the primary circulation (Bushnell et al, 1998;Gallaugher and Farrell, 1998;Skov and Steffensen, 2003;Steffensen and Lomholt, 1992) and therefore may serve to buffer osmotic and ionic changes in the primary circulation. Under resting conditions, no red blood cells (RBCs) are present in the SVS.…”

Section: Introductionmentioning

confidence: 99%

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Function and control of the fish secondary vascular system, a contrast to mammalian lymphatic systems

Rummer

Wang

Steffensen

et al. 2013

Journal of Experimental Biology

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Teleost fishes and mammalian lineages diverged 400 million years ago, and environmental requirements (water versus air) have resulted in marked differences in cardiovascular function between fish and mammals. Suggestions that the fish secondary vascular system (SVS) could be used as a model for the mammalian lymphatic system should be taken with caution. Despite molecular markers indicating similar genetic origin, functions of the SVS in teleost fish are probably different from those of the mammalian lymphatic system. We determined that, in resting glass catfish (Kryptopterus bicirrhis), plasma moves from the primary vascular system (PVS) to the SVS through small connecting vessels less than 10 μm in diameter, smaller than the red blood cells (RBCs). During and following hypoxia or exercise, flow increases and RBCs enter the SVS, possibly via β-adrenoreceptor-mediated dilation of the connecting vessels. The volume of the SVS can be large and, as RBCs flow into the SVS, the haematocrit of the PVS falls by as much as 50% of the resting value. Possible functions of the SVS, including skin respiration, ionic and osmotic buffering, and reductions in heart work and RBC turnover, are discussed. KEY WORDS: Lymphatic, Secondary vascular system, Stress INTRODUCTIONThe mammalian lymphatic system consists of blind-ending lymphatic vessels, lymph nodes and other tissues, including the spleen, that collect, filter and return fluid that drains from the tissues to the venous system and transport fats and proteins from the gut into the blood system (Alitalo et al., 2005;Wang and Oliver, 2010). In teleost fishes, some circulatory vessels contain clear fluid and have been described as lymphatic vessels (Kampmeier, 1969). Yaniv et al. (Yaniv et al., 2006) and Isogai et al. (Isogai et al., 2009) have also demonstrated that these vessels share some morphological and molecular characteristics with the lymphatic vessels found in other vertebrates, and suggested that these clear vessels in zebrafish could be used as a model for the mammalian lymphatic system. However, several decades ago these same vessels were hypothesized as part of a secondary vascular system (SVS), receiving inflow from the arterial system via arterio-arterial anastomoses and emptying into the venous circulation (Vogel, 1981;Vogel and Claviez, 1981;Vogel, 1985;Steffensen et al., 1986;Steffensen and Lomholt, 1992; RESEARCH ARTICLE Jensen et al., 2009). These vessels are not blind-ending and sometimes include red blood cells (RBCs) (Ishimatsu et al., 1992). Furthermore, there is no evidence that the SVS vessels are draining edematous tissues or are playing a role in lipid transport. If not lymphatic, what then is the role of this secondary vascular system?The volume of the SVS can range from 10-50% to nearly twice the volume of the primary circulation (Bushnell et al., 1998;Gallaugher and Farrell, 1998;Skov and Steffensen, 2003;Steffensen and Lomholt, 1992) and therefore may serve to buffer osmotic and ionic changes in the primary circulation. Under restin...

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Section: The Journal Of Experimental Biologymentioning

confidence: 98%

Section: Introductionmentioning

confidence: 99%

Function and control of the fish secondary vascular system, a contrast to mammalian lymphatic systems

Rummer

Wang

Steffensen

et al. 2013

Journal of Experimental Biology

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“…Perfusion rate to the secondary circulation is likely under a neurotransmitter or humoral control (Vogel 1985a;Skov and Bennett 2004b). Since the secondary circulation forms a capillary network on the body surface (Vogel 1985a), the fluid could be diluted with environmental water and the gradient of protein concentration may be maintained by the low flow rate in the secondary circulation (Skov and Steffensen 2003). However, this hypothesis conflicts with the finding in the present study that the levels of the lower-molecular-weight substances appear to be similar between two circulations.…”

Section: Discussionmentioning

confidence: 99%

“…However, a contribution, if any, of the secondary circulation in the osmoregulation may dependent on its volume, flow rate and turn over rate, which are subjects of active debates. For instance, the volume of the secondary circulation was considered to be high (150% of primary circulation; Steffensen and Lomholt 1992), but recent studies suggest that it is much smaller (10-50%; Bushnell et al 1998;Skov and Steffensen 2003). The large difference is attributed to the assumption of whether albumin, a commonly used protein marker for measuring blood volume, is permeable to fish capillaries or not.…”

Section: Discussionmentioning

confidence: 99%

Immunochemical Comparison Between sera from the Primary and Secondary Circulations in a Salmonid Fish, Sakhalin Taimen (Hucho perryi)

Tokushima

Ito

Shimizu

et al. 2004

Fish Physiol Biochem

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Fish has a unique, non-respiratory vascular system called secondary circulation, which forms capillary networks to the internal and external body surfaces. We compared protein composition in serum from the secondary circulation with that from the primary (blood) circulation. Chromatographic and electrophoretic patterns of sera from the two circulations were essentially same. Immunochemical analysis using specific antibodies against albumin-like protein (a1-protein), immunoglobulin M (IgM), transferrin, vitellogenin and choriogenin (precursor to eggshell protein) revealed that these major blood serum proteins in the primary circulation are present in the secondary circulation. Total protein concentrations in the secondary circulation were lower than those in the primary circulation. a1-Protein levels in the secondary circulation relative to the primary circulation were similar to those of total protein. IgM, however, had significantly lower relative levels in the secondary circulation than total protein. Despite some differences in the protein composition between the primary and secondary circulations, the presence of major blood serum proteins in the secondary circulation suggests that the secondary circulation plays a role in transporting them from the primary circulation to the body surfaces.

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“…Parasitemia estimates were obtained by counting trypanosomes in aliquots of isolated buffy coat/leukocyte fractions. Intensity estimates were calculated using cod red blood volumes (primary circulatory system) extrapolated with the allometric relationship found by Skov and Steffensen (2003).…”

Section: Methodsmentioning

confidence: 99%

A trypanosome of Atlantic cod, Gadus morhua L., transmitted by the marine leech Calliobdella nodulifera (Malm, 1863) (Piscicolidae)

Karlsbakk

2004

Parasitology Research

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The fish leech, Calliobdella nodulifera, transmitted a trypanosome while feeding on laboratory-reared cod ( Gadus morhua). The flagellate body length increased from 43 microm 17 days post-infection (d.p.i.) to 57 microm 113 d.p.i. Characteristic features are cell striation, a nearly central nucleus and a short (3.5 microm) distance from the kinetoplast to the posterior end (PK). Following growth, the trypanosomes became increasingly slender, with fewer striae and a shorter flagellum, while the PK was unaffected. The trypanosomes differ morphologically from Trypanosoma murmanensis transmitted by the leech Johanssonia arctica.

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The blood volumes of the primary and secondary circulatory system in the Atlantic codGadus morhuaL., using plasma bound Evans Blue and compartmental analysis

Cited by 16 publications

References 37 publications

Function and control of the fish secondary vascular system, a contrast to mammalian lymphatic systems

Function and control of the fish secondary vascular system, a contrast to mammalian lymphatic systems

Immunochemical Comparison Between sera from the Primary and Secondary Circulations in a Salmonid Fish, Sakhalin Taimen (Hucho perryi)

A trypanosome of Atlantic cod, Gadus morhua L., transmitted by the marine leech Calliobdella nodulifera (Malm, 1863) (Piscicolidae)

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