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Morphology, function, and evolution of the gills of high- performance fishes


This dissertation describes gill specializations related to fast, continuous swimming in tunas, bonitos, and mackerels (family Scombridae), the billfishes (Istiophoridae, Xiphiidae) and the shortfin mako, Isurus oxyrinchus (Lamnidae). These fishes all require gill adaptations for increased gas exchange to meet relatively high aerobic demands and for added rigidity to withstand the forceful branchial flow produced by ram ventilation. Preliminary research for this dissertation, included as an appendix chapter and published as Wegner et al. (2006), examined gill specializations in the striped marlin, Kajikia audax (formerly Tetrapturus audax), and the wahoo, Acanthocybium solandri, and sets the stage for Chapters 1- 4. Chapter 1 documents changes in scombrid and billfish gill morphometrics which augment gill surface area above that of other fish groups and increase branchial resistance to slow and streamline ram-ventilatory flow. Many scombrids and billfishes also have gill fusions which provide support and secure the spatial relationship of filaments and lamellae. Chapter 2 details the structure, function, and distribution of these fusions within different species; they are most complex in large tunas and billfishes, which are obligate ram ventilators, but are absent in mackerels, which utilize active ventilation at slower swimming speeds. Chapter 3 investigates the convergence of mako and tuna gill structure in relation to high aerobic demands and ram ventilation and shows that although makos have relatively larger gill surface areas and shorter diffusion distances than those of other shark species, these features are not as specialized as those of tunas. This work suggests that differences in the gill design of elasmobranchs and teleosts may limit mako gill surface area and ultimately constrain mako aerobic performance in comparison to tunas. Chapter 4 tests this hypothesis with in vivo studies of gill function in makos swimming in a water tunnel. Mako gills are similar to those of tunas in terms of oxygen utilization, the total pressure gradient driving the ventilatory stream, and flow conditions along the respiratory surfaces. However, the interbranchial septum, an intrinsic feature of the shark gill, greatly contributes to mako branchial resistance, and this is compensated by changes to gill dimensions that ultimately limit gill surface area.

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