Nicholas C. Wegner

Gill morphometrics in relation to gas transfer and ram ventilation in high-energy demand teleosts: Scombrids and billfishes

This comparative study of the gill morphometrics in scombrids (tunas, bonitos, and mackerels) and billfishes (marlins, swordfish) examines features of gill design related to high rates of gas transfer and the high‐pressure branchial flow associated with fast, continuous swimming. Tunas have the largest relative gill surface areas of any fish group, and although the gill areas of non‐tuna scombrids and billfishes are smaller than those of tunas, they are also disproportionally larger than those of most other teleosts. The morphometric features contributing to the large gill surface areas of these high‐energy demand teleosts include: 1) a relative increase in the number and length of gill filaments that have, 2) a high lamellar frequency (i.e., the number of lamellae per length of filament), and 3) lamellae that are long and low in profile (height), which allows a greater number of filaments to be tightly packed into the branchial cavity. Augmentation of gill area through these morphometric changes represents a departure from the general mechanism of area enhancement utilized by most teleosts, which lengthen filaments and increase the size of the lamellae. The gill design of scombrids and billfishes reflects the combined requirements for ram ventilation and elevated energetic demands. The high lamellar frequencies and long lamellae increase branchial resistance to water flow which slows and streamlines the ram ventilatory stream. In general, scombrid and billfish gill surface areas correlate with metabolic requirements and this character may serve to predict the energetic demands of fish species for which direct measurement is not possible. The branching of the gill filaments documented for the swordfish in this study appears to increase its gill surface area above that of other billfishes and may allow it to penetrate oxygen‐poor waters at depth. J. Morphol. 2010.

Diel movement patterns and habitat preferences of the common thresher shark (Alopias vulpinus) in the Southern California Bight

The common thresher shark, Alopias vulpinus, is the basis of the largest commercial shark fishery in California waters. We used acoustic telemetry to determine the diel movement patterns and habitat preferences of this species inthe Southern California Bight (SCB),where commercial fishing for the common thresher sharkis concentrated. Eightcommonthreshers (forklength: 122-203cm) weretaggedwith temperature anddepth-sensingacoustic transmitters and tracked for periods ranging from 22 to 49h. Tracked sharks preferentially utilized deep offshore waters, and avoided shallower waters over the continental shelf. Mean rate of movement (ROMs.d.) was 2.15 � 0.46kmh � 1 . ROM and angularconcentration(r,ameasureofrelativelinearity)bothshowedastrongdaytimepattern,withhighestvaluesatdawn that decreased throughout the day, whereas nocturnal ROM and r were less variable. Daytime vertical movements consisted of either vertical excursions below the thermocline or relatively level swimming within the upper portion of the thermocline. Nocturnally, all sharks remained within the mixed layer. These findings suggest that the common thresher shark is primarily a daytime predator, and have relevance for estimating how the alteration of the set depth of fishing-gear could affect catch rates of this species in the SCB.

Spiracular air breathing in polypterid fishes and its implications for aerial respiration in stem tetrapods.

The polypterids (bichirs and ropefish) are extant basal actinopterygian (ray-finned) fishes that breathe air and share similarities with extant lobe-finned sarcopterygians (lungfishes and tetrapods) in lung structure. They are also similar to some fossil sarcopterygians, including stem tetrapods, in having large paired openings (spiracles) on top of their head. The role of spiracles in polypterid respiration has been unclear, with early reports suggesting that polypterids could inhale air through the spiracles, while later reports have largely dismissed such observations. Here we resolve the 100-year-old mystery by presenting structural, behavioural, video, kinematic and pressure data that show spiracle-mediated aspiration accounts for up to 93% of all air breaths in four species of Polypterus. Similarity in the size and position of polypterid spiracles with those of some stem tetrapods suggests that spiracular air breathing may have been an important respiratory strategy during the fish-tetrapod transition from water to land.

Functional morphology of the gills of the shortfin mako, Isurus oxyrinchus, a lamnid shark.

This study examines the functional gill morphology of the shortfin mako, Isurus oxyrinchus, to determine the extent to which its gill structure is convergent with that of tunas for specializations required to increase gas exchange and withstand the forceful branchial flow induced by ram ventilation. Mako gill structure is also compared to that of the blue shark, Prionace glauca, an epipelagic species with lower metabolic requirements and a reduced dependence on fast, continuous swimming to ventilate the gills. The gill surface area of the mako is about one‐half that of a comparably sized tuna, but more than twice that of the blue shark and other nonlamnid shark species. Mako gills are also distinguished from those of other sharks by shorter diffusion distances and a more fully developed diagonal blood‐flow pattern through the gill lamellae, which is similar to that found in tunas. Although the mako lacks the filament and lamellar fusions of tunas and other ram‐ventilating teleosts, its gill filaments are stiffened by the elasmobranch interbranchial septum, and the lamellae appear to be stabilized by one to two vascular sacs that protrude from the lamellar surface and abut sacs of adjacent lamellae. Vasoactive agents and changes in vascular pressure potentially influence sac size, consequently effecting lamellar rigidity and both the volume and speed of water through the interlamellar channels. However, vascular sacs also occur in the blue shark, and no other structural elements of the mako gill appear specialized for ram ventilation. Rather, the basic elasmobranch gill design and pattern of branchial circulation are both conserved. Despite specializations that increase mako gill area and efficacy relative to other sharks, the basic features of the elasmobranch gill design appear to have limited selection for a larger gill surface area, and this may ultimately constrain mako aerobic performance in comparison to tunas. J. Morphol. 271:937–948, 2010.

Atmospheric Oxygen Levels Affect Mudskipper Terrestrial Performance: Implications for Early Tetrapods

The Japanese mudskipper (Periophthalmus modestus), an amphibious fish that possesses many respiratory and locomotive specializations for sojourns onto land, was used as a model to study how changing atmospheric oxygen concentrations during the middle and late Paleozoic Era (400-250 million years ago) may have influenced the emergence and subsequent radiation of the first tetrapods. The effects of different atmospheric oxygen concentrations (hyperoxia = 35%, normoxia = 21%, and hypoxia = 7% O2) on terrestrial performance were tested during exercise on a terrestrial treadmill and during recovery from exhaustive exercise. Endurance and elevated post-exercise oxygen consumption (EPOC; the immediate O2 debt repaid post-exercise) correlated with atmospheric oxygen concentration indicating that when additional oxygen is available P. modestus can increase oxygen utilization both during and following exercise. The time required post-exercise for mudskippers to return to a resting metabolic rate did not differ between treatments. However, in normoxia, oxygen consumption increased above hyperoxic values 13-20 h post-exercise suggesting a delayed repayment of the incurred oxygen debt. Finally, following exercise, ventilatory movements associated with buccopharyngeal aerial respiration returned to their rest-like pattern more quickly at higher concentrations of oxygen. Taken together, the results of this study show that P. modestus can exercise longer and recover quicker under higher oxygen concentrations. Similarities between P. modestus and early tetrapods suggest that increasing atmospheric oxygen levels during the middle and late Paleozoic allowed for elevated aerobic capacity and improved terrestrial performance, and likely led to an accelerated diversification and expansion of vertebrate life into the terrestrial biosphere.

Effects of prolonged entanglement in discarded fishing gear with substantive biofouling on the health and behavior of an adult shortfin mako shark, Isurus oxyrinchus

A mature male shortfin mako, Isurus oxyrinchus, was captured with a three-strand twisted natural fiber rope wrapped around the body causing deep abrasions, scoliosis of the back, and undernourishment. Fifty-two pelagic peduculate barnacles from four species were found fouling on the rope. Assuming larval settlement occurred following entanglement, barnacle growth-rate data suggest the rope had been around the shark for at least 150 days. However, the onset of severe scoliosis (likely linked to the increased constriction of the rope with growth and the added drag induced by biofouling) indicates that this rope may have been in place much longer. Following removal of the rope, a pop-up satellite archival tag was attached to the shark to assess post-release health. The resulting 54 days of tag deployment data show that despite its injuries, the shark survived, and following an initial stress period, exhibited movement patterns characteristic of healthy makos.

Reexamination of the Byczkowska-Smyk gill surface area data for European teleosts, with new measurements on the pikeperch, Sander lucioperca

This paper reexamines the gill morphometrics of 20 European teleosts first reported in the early gill literature by Byczkowska-Smyk and colleagues in attempt to clarify the long-recognized discrepancies between these data and those obtained in subsequent works. Determination of gill dimensions for the pikeperch, Sander lucioperca, in this study (a species for which Byczkowska-Smyk reported data), along with a literature review for other European teleosts, reveals inaccurate estimation of the total gill surface area by up to 18× for 19 of the 20 species reexamined. This error results primarily from imprecise determination of the bilateral surface area of individual gill lamellae and, to a lesser extent, the incorrect assumption that lamellar area and frequency are species-specific constants that do not vary with fish body mass. This review compiles gill morphometric data from various sources to be used in place of the inaccurate gill area estimates of Byczkowska-Smyk and colleagues and thereby clears the way for higher resolution in the comparative analysis of gill morphology and its correlation to fish habitat and life history characteristics.

George Hughes and the history of fish ventilation: From Du Verney to the present☆

This paper traces the research history of fish ventilation from its origins in the early 1700s to the present with emphasis on the work of George M. Hughes, who is considered by many to be the founder of the modern era of fish respiratory science. A particularly important year in the timeline for fish respiratory studies was 1960, when Hughes presented the currently accepted biomechanical model driving fish ventilation. He showed that both bony and cartilaginous fishes breathe through the use of a dual-pumping mechanism: a buccal or orobranchial pressure pump to force water over the gills and an opercular or parabranchial suction pump to pull water through the branchial chambers. Hughes divided this mechanism into four stages and demonstrated that during each the pressure of the buccal cavity usually exceeded that of the opercular chamber, thus indicating the continuous, or nearly continuous, nature of the ventilatory stream. Studies by Hughes and later researchers focused on variation in the four stages and related these to interspecific differences in fish habitat and activity level. Differences noted in the respiration of pelagic and benthic species largely led to the description and quantification of ram ventilation. Hughes further made significant contributions to the correlation of gill structure and function and was one of the first to examine gill morphometrics in relation to the ventilatory stream and the diffusivity of oxygen from the water into the blood. Such pioneering measurements paved the way toward the modern analyses of gill hydromechanics and the modeling of respiratory gas exchange in fishes.

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

For ram‐gill ventilators such as tunas and mackerels (family Scombridae) and billfishes (families Istiophoridae, Xiphiidae), fusions binding the gill lamellae and filaments prevent gill deformation by a fast and continuous ventilatory stream. This study examines the gills from 28 scombrid and seven billfish species in order to determine how factors such as body size, swimming speed, and the degree of dependence upon ram ventilation influence the site of occurrence and type of fusions. In the family Scombridae there is a progressive increase in the reliance on ram ventilation that correlates with the elaboration of gill fusions. This ranges from mackerels (tribe Scombrini), which only utilize ram ventilation at fast cruising speeds and lack gill fusions, to tunas (tribe Thunnini) of the genus Thunnus, which are obligate ram ventilators and have two distinct fusion types (one binding the gill lamellae and a second connecting the gill filaments). The billfishes appear to have independently evolved gill fusions that rival those of tunas in terms of structural complexity. Examination of a wide range of body sizes for some scombrids and billfishes shows that gill fusions begin to develop at lengths as small as 2.0 cm fork length. In addition to securing the spatial configuration of the gill sieve, gill fusions also appear to increase branchial resistance to slow the high‐speed current produced by ram ventilation to distribute flow evenly and optimally to the respiratory exchange surfaces. J. Morphol. 2012.

Gill Morphometrics of the Thresher Sharks (Genus Alopias): Correlation of Gill Dimensions with Aerobic Demand and Environmental Oxygen

Gill morphometrics of the three thresher shark species (genus Alopias) were determined to examine how metabolism and habitat correlate with respiratory specialization for increased gas exchange. Thresher sharks have large gill surface areas, short water–blood barrier distances, and thin lamellae. Their large gill areas are derived from long total filament lengths and large lamellae, a morphometric configuration documented for other active elasmobranchs (i.e., lamnid sharks, Lamnidae) that augments respiratory surface area while limiting increases in branchial resistance to ventilatory flow. The bigeye thresher, Alopias superciliosus, which can experience prolonged exposure to hypoxia during diel vertical migrations, has the largest gill surface area documented for any elasmobranch species studied to date. The pelagic thresher shark, A. pelagicus, a warm‐water epi‐pelagic species, has a gill surface area comparable to that of the common thresher shark, A. vulpinus, despite the latters expected higher aerobic requirements associated with regional endothermy. In addition, A. vulpinus has a significantly longer water–blood barrier distance than A. pelagicus and A. superciliosus, which likely reflects its cold, well‐oxygenated habitat relative to the two other Alopias species. In fast‐swimming fishes (such as A. vulpinus and A. pelagicus) cranial streamlining may impose morphological constraints on gill size. However, such constraints may be relaxed in hypoxia‐dwelling species (such as A. superciliosus) that are likely less dependent on streamlining and can therefore accommodate larger branchial chambers and gills. J. Morphol. 276:589–600, 2015.