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The Secondary Vascular System of Actinopterygii: Interspecific Variation in Origins and Investment

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The Secondary Vascular System of Actinopterygii: Interspecific Variation in Origins and Investment Zoomorphology (2004) 123:55–64 DOI 10.1007/s00435-003-0094-z ERRATUM Peter Vilhelm Skov · Michael Brian Bennett The secondary vascular system of Actinopterygii: interspecific variation in origins and investment Published online: 28 November 2003 Springer-Verlag 2003 Abstract Vascular casts of 3 species of Chondrichthyes, Zoomorphology (2003) 122:181–190 1 of Dipnoi, 1 of Chondrostei and 14 species of the Teleostei were examined by light and scanning electron Owing to unfortunate technical problems, inappropriate microscopy in order to give a qualitative and quantitative symbols appeared throughout the text, making it neces- analysis of interarterial anastomoses (iaas) that indicate sary to reprint the article. 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 Introduction have not been previously identified as giving rise to secondary vessels. Segmental arteries derived from the The presence of a secondary vascular system (SVS) was dorsal aorta and supplying body musculature were major initially documented for two species of Teleostei by sites of origin of the SVS, although there was consider- Burne (1926, 1929), through dye injection studies in able variation in where, in the hierarchy of arterial Lophius piscatorius Linnaeus, 1758 (anglerfish) and branching, the anastomoses occurred. The degree of Gadus morhua Linnaeus, 1758 (Atlantic cod). Burne investment in a SVS was species specific, with more described a system of fine vessels associated with the active species having a higher degree of secondary (primary) vasculature of these two species, and suspected vascularisation. This difference was quantified using an that these vessels constituted a separate vessel system. absolute count of iaas between Anguilla reinhardtii and The very low haematocrit of the SVS (approximately 1%) Trachinotus baillonii. A range of general features of the combined with the fact that no arterial connection to the SVS is also described. No evidence of iaas was found on primary vasculature could be demonstrated, forced him to the coeliac, mesenteric or renal circulation in any species. term these vessels ‘lymphatic’. His findings were left Evidence of iaas was lacking in the dipnoan and unexplored until Vogel and Claviez (1981) rediscovered chondrichthyan species examined, suggesting that a the SVS and demonstrated the connection to the primary SVS is restricted to Actinopterygii. The presence and vasculature, the interarterial anastomoses (iaas). distribution of a SVS does not appear to be exclusively The implications of a systemic SVS in Actinopterygii linked to phylogenetic position, but rather to the physi- has been discussed widely during the last decade, and its ological adaptation of the species. unequivocal presence has been documented in a number of species (Vogel and Claviez 1981; King and Hossler 1986; Keywords Secondary vessels · Secondary circulation · Olson et al. 1986, 1990; Steffensen et al. 1986; Lahnsteiner Vascular casting · Phylogeny · Investment · et al. 1990; Dewar et al. 1994; Munshi et al. 1994; Chopin Chondrichthyes · Chondrostei · Holostei · Teleostei and Bennett 1996; Chopin et al. 1998) and on a variety of blood vessels. The predominant method for its visualisation The online version of the original article can be found at has been through vascular casting, where injection of an http://dx.doi.org/10.1007/s00435-003-0083-2 acrylic polymer leaves a rigid three-dimensional structure P. V. Skov ()) · M. B. Bennett of the vascular system for study once the surrounding School of Biomedical Sciences, tissues have been corroded away. However, the transparent Department of Anatomy and Developmental Biology, tissues of Kryptopterus bichirrhis (Valenciennes, 1840) The University of Queensland, (glass catfish), allowed Steffensen et al. (1986) to describe 4072 St. Lucia, Queensland, Australia the SVS of this species in vivo, by light microscopy. e-mail: [email protected] Secondary vessels arise directly from the primary vascu- Tel.: +61-7-33652702 lature via numerous iaas. These funnel-shaped openings Fax: +61-7-33651299 56 typically arise from the walls of arteries 50 m or greater in tation from the Chondrichthyes, Chondrostei and Tele- diameter (Olson 1996). The opening into an anastomosis is ostei, to determine the presence or absence of a SVS, and surrounded by numerous cells bearing microvilli (Lahnstein- explore any interspecific differences in the frequency of er et al. 1990), each approximately 10 m long (Vogel 1981), origin of iaas and the vessels of their origin. protruding into the lumen of the anastomosis, and may also be present ‘upstream’ from the origin of anastomoses (Vogel 1981). The function of the microvilli is unknown, but it has Materials and methods been suggested that they may be responsible for plasma skimming (Vogel 1981), or they may possess adhesive Animals properties to ensure that some blood cells pass through to the Pseudocaranx dentex (Bloch and Schneider, 1801) (silver trevally), SVS (Steffensen and Lomholt 1992). Interarterial anasto- Echeneis naucrates (Linneaus, 1758) (slender suckerfish), Gym- moses taper to become small bore vessels that follow a nocranius audleyi (Ogilby, 1916) (collared sea bream), Lutjanus tortuous path over the following 200–300 mmbefore fulviflammus (Forsskl, 1775) (blackspot sea perch), Scarus anastomosing with neighbouring vessels to form secondary schlegeli (Bleeker, 1861) (Schlegel’s parrotfish), Halophryne diemensis (Leseur, 1824) (banded frogfish), Conger cinereus vessels (Olson 1996). In Arius graeffei Kner and Stein- Rppel, 1830 (black-edged conger) and Hemiscyllium ocellatum dachner, 1867 (fork-tailed catfish), secondary vessels form (Bonnaterre, 1788) (epaulette shark) were caught by angling or capillary beds that supply the periphery of the red muscle hand-net on Heron Island Reef (23270S 151550E). Seriola (Chopin and Bennett 1996), while in Tandanus tandanus dumerili (Risso, 1810) (amberjack), Arius graeffei Kner and (Mitchell, 1838) (eel-tail catfish) secondary capillary beds Steindachner, 1867 (fork-tailed catfish), Tragulichthys jaculiferus (Cuvier, 1818) (longspine burrfish) and Aptychotrema rostrata supply the skin (Chopin et al. 1998), before draining into the (Shaw and Nodder, 1794) (eastern shovelnose ray) were caught by cutaneous veins. In Blennius pavo (Risso, 1810) (peacock angling in Moreton Bay (27250S 153120E). Dasyatis kuhlii blenny) and Zosterisessor ophiocephalus (Pallas, 1814) (Mller and Henle, 1841) (blue-spotted whipray) were caught by 0 0 (grass goby) secondary vessels do not form capillary beds, seine net at Hays Inlet (2707 S 15304 E). Trachinotus baillonii (Lacpde, 1801) (smallspotted dart) were caught by angling from but reportedly empty directly into secondary veins (Lahn- Forty-mile beach (24220S 153820E). Anguilla reinhardtii Stein- steiner et al. 1990). A cutaneous capillary supply is assumed dachner, 1867 (long-finned eel) were caught by hand-net in the lake to be typical for teleosts (Vogel 1985). at University of Queensland, St. Lucia, and Megalops cyprinoides Burne’s descriptions also suggest that a secondary (Broussonet, 1782) (Pacific tarpon) were caught by angling at Colleges Crossing in the Brisbane River. Scleropages leichardti vessel system occurs in the mouth and head regions, yet Gnter, 1864 (Southern saratoga) were purchased from a commer- no attempts have been made to determine which primary cial fish farm in Queensland, Acipenser gueldenstaedtii Brandt and vessels supply this part of the secondary vasculature Ratzeberg, 1833 (Russian sturgeon) were purchased from an (Burne 1926, 1929). The aim of this study is to undertake aquarium fish retailer in Denmark, and Neoceratodus forsteri a detailed examination of vascular casts from a wide (Krefft, 1870) (Australian lungfish) were obtained from breeding stock at Macquarie University, Sydney (Table 1). range of phylogenetically diverse species, with represen- Table 1 Taxonomic position, Species Family BM FL TL SVS mass and length of experimen- (g) (cm) (cm) tal animals. Body mass (BM), fork length (FL) and total length Chondrichthyes TL ( ) of experimental animals. A Aptychotrema rostrata Rhinobatidae 356 - 51 No no or yes in the secondary Dasyatis kuhlii Dasyatidae 184 - 30 No SVS vascular system ( ) column Hemiscyllium ocellatum Hemiscylliidae 434 - 57 No denotes the presence or absence of a SVS in that species Chondrostei Acipenser gueldenstaedtii Acipenseridae 602 46 51 Yes Teleostei Scleropages leichardti Osteoglossidae 80 - 23 Yes Megalops cyprinoides Megalopidae 469 33 38 Yes Anguilla reinhardtii Anguillidae 995 - 72 Yes Conger cinereus Congridae 492 - 73 Yes Arius graeffei Ariidae 448 28 31 Yes Halophryne diemensis Batrachoididae 304 - 217 Yes Pseudocaranx dentex Carangidae 521 27 32 Yes Seriola dumerili Carangidae 318 31 35 Yes Trachinotus bailllonii Carangidae 128 21 24 Yes Echeneis naucrates Echeneidae 254 - 44 Yes Gymnocranius audleyi Lethrinidae 343 24 27 Yes Lutjanus fulviflammus Lutjanidae 436 - 29 Yes Scarus schlegeli Scaridae 467 - 30 Yes Tragulichtys jaculiferus Diodontidae 255 - 19 Yes Dipnoi Neoceratodus forsteri Ceratodontidae 255 - 28 No 57 Surgical procedures allowed to dry before examination under a dissection microscope (WILD M3Z; Heerbrugg, Switzerland). The presence of iaason Fish were anaesthetised in either MS-222 (0.5 g l1) or benzocaine different vessels could be determined at a magnification of 250. (0.06 g l1) until
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