Oxygen utilization and the branchial pressure gradient during ram ventilation of the shortfin mako,Isurus oxyrinchus: is lamnid shark–tuna convergence constrained by elasmobranch gill morphology?

Abstract

SUMMARYRam ventilation and gill function in a lamnid shark, the shortfin mako, Isurus oxyrinchus, were studied to assess how gill structure may affect the lamnid-tuna convergence for high-performance swimming. Despite differences in mako and tuna gill morphology, mouth gape and basal swimming speeds, measurements of mako O 2 utilization at the gills (53.4±4.2%) and the pressure gradient driving branchial flow (96.8±26.1Pa at a mean swimming speed of 38.8±5.8cms ) and residence time (0.79±0.14s) of water though the interlamellar channels of the mako gill. However, mako and tuna gills differ in the sites of primary branchial resistance. In the mako, approximately 80% of the total branchial resistance resides in the septal channels, structures inherent to the elasmobranch gill that are not present in tunas. The added resistance at this location is compensated by a correspondingly lower resistance at the gill lamellae accomplished through wider interlamellar channels. Although greater interlamellar spacing minimizes branchial resistance, it also limits lamellar number and results in a lower total gill surface area for the mako relative to tunas. The morphology of the elasmobranch gill thus appears to constrain gill area and, consequently, limit mako aerobic performance to less than that of tunas.

Structural adaptations for ram ventilation: Gill fusions in scombrids and billfishes

“…Tunas, bonitos, and mackerels (family Scombridae) and billfishes (families Istiophoridae, Xiphiidae) are continuous swimmers and breathe using ram ventilation, the mechanism through which forward swimming provides the force required to drive water into the mouth and through the branchial chamber (Brown and Muir,1970; Stevens,1972; Roberts,1975,1978; Stevens and Lightfoot,1986; Wegner et al,2012). Ram ventilation transfers the energetic cost of active gill ventilation to the swimming musculature, and because mouth and opercular motions are minimized, both respiratory and swimming efficiency are increased (Freadman,1979,1981; Steffensen,1985).…”

“…However, at the relatively high swimming speeds attained by scombrids and billfishes, ram ventilation poses two challenges. First, the ram‐ventilatory current must be slowed to create optimal flow conditions for efficient gas exchange at the respiratory lamellae (Brown and Muir,1970; Stevens and Lightfoot,1986; Wegner et al,2012). Second, the gills must be reinforced in order to maintain normal orientation with respect to a high‐pressure branchial stream, the force of which increases with swimming speed (Muir and Kendall,1968; Brown and Muir,1970).…”

Gill morphometrics of the thresher sharks (GenusAlopias): Correlation of gill dimensions with aerobic demand and environmental oxygen

“…In contrast to highly active teleosts such as tunas and billfishes that couple high total filament lengths with high lamellar frequencies to increase gill area (Muir and Hughes, ; Wegner et al, ), lamellar frequencies in Alopias and lamnids are not greater than those of less‐active elasmobranchs. This likely reflects the presence of interbranchial septa in elasmobranch gills that inherently increase gill resistance as water is forced through septal canals (Wegner et al, ). Because having a higher lamellar frequency would further increase gill resistance, the presence of interbranchial septa in elasmobranchs, likely causes alopiids and lamnids to augment gill surface area differently than high‐performance teleosts.…”

“…[Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.] forced through septal canals (Wegner et al, 2012). Because having a higher lamellar frequency would further increase gill resistance, the presence of interbranchial septa in elasmobranchs, likely causes alopiids and lamnids to augment gill surface area differently than high-performance teleosts.…”

Optimal lamellar arrangement in fish gills

“…Among the species that use ram ventilation, some pelagic elasmobranch fish have developed a unique gill structure called the interbranchial septum; this structure generates primary resistance to water flow, such that only a small fraction of the dynamic pressure on the order of 20 Pa is applied to the interlamellar channels (11).…”