The allometric scaling of oxygen supply and demand in the California horn shark, Heterodontus francisci.

The gill surface area of aquatic ectotherms is thought to be closely linked to the ontogenetic scaling of metabolic rate, a relationship that is often used to explain and predict ecological patterns across species. However, there are surprisingly few within-species tests of whether metabolic rate and gill area scale similarly. We examined the relationship between oxygen supply (gill area) and demand (metabolic rate) by making paired estimates of gill area with resting and maximum metabolic rates across ontogeny in the relatively inactive California horn shark, Heterodontus francisci. We found that the allometric slope of resting metabolic rate was 0.966±0.058 (±95% CI), whereas that of maximum metabolic rate was somewhat steeper (1.073±0.040). We also discovered that the scaling of gill area shifted with ontogeny: the allometric slope of gill area was shallower in individuals <0.203 kg in body mass (0.564±0.261), but increased to 1.012±0.113 later in life. This appears to reflect changes in demand for gill-oxygen uptake during egg case development and immediately post hatch, whereas for most of ontogeny, gill area scales in between that of resting and maximum metabolic rate. These relationships differ from predictions of the gill oxygen limitation theory, which argues that the allometric scaling of gill area constrains metabolic processes. Thus, for the California horn shark, metabolic rate does not appear limited by theoretical surface-area-to-volume ratio constraints of gill area. These results highlight the importance of data from paired and size-matched individuals when comparing physiological scaling relationships.

The metabolic pace of life histories across fishes.

All life acquires energy through metabolic processes and that energy is subsequently allocated to life-sustaining functions such as survival, growth and reproduction. Thus, it has long been assumed that metabolic rate is related to the life history of an organism. Indeed, metabolic rate is commonly believed to set the pace of life by determining where an organism is situated along a fast-slow life-history continuum. However, empirical evidence of a direct interspecific relationship between metabolic rate and life histories is lacking, especially for ectothermic organisms. Here, we ask whether three life-history traits-maximum body mass, generation length and growth performance-explain variation in resting metabolic rate (RMR) across fishes. We found that growth performance, which accounts for the trade-off between growth rate and maximum body size, explained variation in RMR, yet maximum body mass and generation length did not. Our results suggest that measures of life history that encompass trade-offs between life-history traits, rather than traits in isolation, explain variation in RMR across fishes. Ultimately, understanding the relationship between metabolic rate and life history is crucial to metabolic ecology and has the potential to improve prediction of the ecological risk of data-poor species.

Respiratory capacity is twice as important as temperature in explaining patterns of metabolic rate across the vertebrate tree of life.

Metabolic rate underlies a wide range of phenomena from cellular dynamics to ecosystem structure and function. Models seeking to statistically explain variation in metabolic rate across vertebrates are largely based on body size and temperature. Unexpectedly, these models overlook variation in the size of gills and lungs that acquire the oxygen needed to fuel aerobic processes. Here, we assess the importance of respiratory surface area in explaining patterns of metabolic rate across the vertebrate tree of life using a novel phylogenetic Bayesian multilevel modeling framework coupled with a species-paired dataset of metabolic rate and respiratory surface area. We reveal that respiratory surface area explains twice as much variation in metabolic rate, compared to temperature, across the vertebrate tree of life. Understanding the combination of oxygen acquisition and transport provides opportunity to understand the evolutionary history of metabolic rate and improve models that quantify the impacts of climate change.

Gill surface area provides a clue for the respiratory basis of brain size in the blacktip shark (Carcharhinus limbatus).

Brain size varies dramatically, both within and across species, and this variation is often believed to be the result of trade-offs between the cognitive benefits of having a large brain for a given body size and the energetic cost of sustaining neural tissue. One potential consequence of having a large brain is that organisms must also meet the associated high energetic demands. Thus, a key question is whether metabolic rate correlates with brain size. However, using metabolic rate to measure energetic demand yields a relatively instantaneous and dynamic measure of energy turnover, which is incompatible with the longer evolutionary timescale of changes in brain size within and across species. Morphological traits associated with oxygen consumption, specifically gill surface area, have been shown to be correlates of oxygen demand and energy use, and thus may serve as integrated correlates of these processes, allowing us to assess whether evolutionary changes in brain size correlate with changes in longer-term oxygen demand and energy use. We tested how brain size relates to gill surface area in the blacktip shark Carcharhinus limbatus. First, we examined whether the allometric slope of brain mass (i.e., the rate that brain mass changes with body mass) is lower than the allometric slope of gill surface area across ontogeny. Second, we tested whether gill surface area explains variation in brain mass, after accounting for the effects of body mass on brain mass. We found that brain mass and gill surface area both had positive allometric slopes, with larger individuals having both larger brains and larger gill surface areas compared to smaller individuals. However, the allometric slope of brain mass was lower than the allometric slope of gill surface area, consistent with our prediction that the allometric slope of gill surface area could pose an upper limit to the allometric slope of brain mass. Finally, after accounting for body mass, individuals with larger brains tended to have larger gill surface areas. Together, our results provide clues as to how fishes may evolve and maintain large brains despite their high energetic cost, suggesting that C. limbatus individuals with a large gill surface area for their body mass may be able to support a higher energetic turnover, and, in turn, a larger brain for their body mass.

Gill slits provide a window into the respiratory physiology of sharks.

Metabolically important traits, such as gill surface area and metabolic rate, underpin life histories, population dynamics and extinction risk, as they govern the availability of energy for growth, survival and reproduction. Estimating both gill surface area and metabolic rate can be challenging, especially when working with large-bodied, threatened species. Ideally, these traits, and respiratory physiology in general, could be inferred from external morphology using a faster, non-lethal method. Gill slit height is quick to measure on live organisms and is anatomically connected to the gill arch. Here, we relate gill slit height and gill surface area for five Carcharhiniform sharks. We compared both total and parabranchial gill surface area to mean and individual gill slit height in physical specimens. We also compared empirical measurements of relative gill slit height (i.e. in proportion to total length) to those estimated from field guide illustrations to examine the potential of using anatomical drawings to measure gill slit height. We find strong positive relationships between gill slit height and gill surface area at two scales: (i) for total gill surface area and mean gill slit height across species and (ii) for parabranchial gill surface area and individual gill slit height within and across species. We also find that gill slit height is a consistent proportion of the fork length of physical specimens. Consequently, relative gill slit height measured from field guide illustrations proved to be surprisingly comparable to those measured from physical specimens. While the generality of our findings needs to be evaluated across a wider range of taxonomy and ecological lifestyles, they offer the opportunity that we might only need to go to the library and measure field guide illustrations to yield a non-lethal, first-order approximation of the respiratory physiology of sharks.

Ecological lifestyles and the scaling of shark gill surface area.

Fish gill surface area varies across species and with respect to ecological lifestyles. The majority of previous studies only qualitatively describe gill surface area in relation to ecology and focus primarily on teleosts. Here, we quantitatively examined the relationship of gill surface area with respect to specific ecological lifestyle traits in elasmobranchs, which offer an independent evaluation of observed patterns in teleosts. As gill surface area increases ontogenetically with body mass, examination of how gill surface area varies with ecological lifestyle traits must be assessed in the context of its allometry (scaling). Thus, we examined how the relationship of gill surface area and body mass across 11 shark species from the literature and one species for which we made measurements, the Gray Smoothhound Mustelus californicus, varied with three ecological lifestyle traits: activity level, habitat, and maximum body size. Relative gill surface area (gill surface area at a specified body mass; here we used 5,000g, termed the 'standardized intercept') ranged from 4,724.98 to 35,694.39 cm2 (mean and standard error: 17,796.65 ± 2,948.61 cm2 ) and varied across species and the ecological lifestyle traits examined. Specifically, larger-bodied, active, oceanic species had greater relative gill surface area than smaller-bodied, less active, coastal species. In contrast, the rate at which gill surface area scaled with body mass (slope) was generally consistent across species (0.85 ± 0.02) and did not differ statistically with activity level, habitat, or maximum body size. Our results suggest that ecology may influence relative gill surface area, rather than the rate at which gill surface area scales with body mass. Future comparisons of gill surface area and ecological lifestyle traits using the quantitative techniques applied in this study can provide further insight into patterns dictating the relationship between gill surface area, metabolism, and ecological lifestyle traits.

Biodiversity, Life History, and Conservation of Northeastern Pacific Chondrichthyans.

The sharks, batoids, and chimaeras, collectively the class Chondrichthyes, are one of the most successful groups of fishes, with over 1250 species globally. Recent taxonomic revisions have increased their diversity by about 20% over the past 17 years (2000-2016). The Northeast Pacific Ocean is one of the top 20 most diverse regions/countries on the globe with 77 chondrichthyan species, a number less than a quarter that of the most species-rich area (Australia) but that has increased by 10% since 2000 to include three new species (two skates and a chimaera). In this chapter we discuss the species richness of chondrichthyans occurring in the Northeast Pacific Ocean, characterize their life histories, briefly review several fisheries, and summarize the conservation status of those chondrichthyans occurring in the region. Detailed descriptions and evaluations of fisheries can be found in Chapter 7 of AMB Volume 78.

Stable isotope analysis of vertebrae reveals ontogenetic changes in habitat in an endothermic pelagic shark.

Ontogenetic changes in habitat are driven by shifting life-history requirements and play an important role in population dynamics. However, large portions of the life history of many pelagic species are still poorly understood or unknown. We used a novel combination of stable isotope analysis of vertebral annuli, Bayesian mixing models, isoscapes and electronic tag data to reconstruct ontogenetic patterns of habitat and resource use in a pelagic apex predator, the salmon shark (Lamna ditropis). Results identified the North Pacific Transition Zone as the major nursery area for salmon sharks and revealed an ontogenetic shift around the age of maturity from oceanic to increased use of neritic habitats. The nursery habitat may reflect trade-offs between prey availability, predation pressure and thermal constraints on juvenile endothermic sharks. The ontogenetic shift in habitat coincided with a reduction of isotopic niche, possibly reflecting specialization upon particular prey or habitats. Using tagging data to inform Bayesian isotopic mixing models revealed that adult sharks primarily use neritic habitats of Alaska yet receive a trophic subsidy from oceanic habitats. Integrating the multiple methods used here provides a powerful approach to retrospectively study the ecology and life history of migratory species throughout their ontogeny.