Farrugia et al by Kenneth Goldman
Despite long evolutionary separations, several sharks and tunas share the ability to maintain slo... more Despite long evolutionary separations, several sharks and tunas share the ability to maintain slow-twitch, aerobic red muscle (RM) warmer than ambient water. Proximate causes of RM endothermy are well understood, but ultimate causes are unclear. Two advantages often proposed are thermal niche expansion and elevated cruising speeds. The thermal niche hypothesis is generally supported, because fishes with RM endothermy often exhibit greater tolerance to broad temperature ranges. In contrast, whether fishes with RM endothermy cruise faster, and achieve any ecological benefits from doing so, remains unclear. Here, we compiled data recorded by modern animal-tracking tools for a variety of free-swimming marine vertebrates. Using phylogenetically informed allometry, we show that both cruising speeds and maximum annual migration ranges of fishes with RM endothermy are 2–3 times greater than fishes without it, and comparable to nonfish endotherms (i.e., penguins and marine mammals). The estimated cost of transport of fishes with RM endothermy is twice that of fishes without it. We suggest that the high energetic cost of RM endothermy in fishes is offset by the benefit of elevated cruising speeds, which not only increase prey encounter rates, but also enable larger-scale annual migrations and potentially greater access to seasonally available resources. marine predator | swim speed | migration | body temperature I n 1835, the British physician John Davy reported that skipjack tuna have body temperatures 10 °C higher than ambient waters and considered this fish an exception to the general rule that fishes are cold-blooded (1). It is currently known that at least 14 species of tuna (family Scombridae) and five species of shark (four species in the family Lamnidae and one species in the family Alopiidae) have the ability to retain metabolic heat via vascular countercurrent heat exchangers, and to maintain the temperature of slow-twitch, aerobic red muscle (hereafter denoted RM) significantly above that of the ambient water (2–7). This " RM endothermy " (see SI Materials and Methods for terminology) in fishes represents a remarkable example of conver-gent evolution, because bony fishes and cartilaginous fishes diverged as long as 450 million years ago (8). In addition to elevated RM temperature, tunas and endothermic sharks share a number of morphological (e.g., medially located RM), physiological (e.g., high metabolic rates), and ecological (e.g., highly mobile and predatory lifestyle) characteristics (9). RM endothermy is an energetically expensive thermal strategy (9), and its convergent evolution indicates that the extra energetic costs incurred by RM endothermy can be outweighed by some ecological advantages. This topic has been discussed intensively , and two primary, nonmutually exclusive hypotheses have been proposed: expansion of the thermal niche and elevated cruising speeds (2). The thermal niche hypothesis states that fishes with RM endothermy can tolerate a broader range of water temperatures and, thus, can expand their geographic niche. An increasing suite of evidence supports this hypothesis; tunas and endothermic sharks often range widely and dive well beneath the thermocline and, consequently, experience a broad temperature range (e.g., more than 20 °C in some species; refs. 10 and 11). However, some ectothermic species (e.g., blue shark) experience similar temperature ranges by diving deep (11, 12), suggesting that other factors may also affect the thermal preference and tolerance of pelagic fishes. The elevated cruising speed hypothesis states that elevated RM temperature enhances the power output of RM and, thereby, increases cruising speed of the fishes (2). This hypothesis is reasonable, because the contraction speed and power output of the isolated RM (13) and the sustained swim speed of ectothermic fishes in captivity (14) all increase with temperature within a species, at least within their normal temperature range. Surprisingly, however, a previous laboratory study found no differences in the sustained swim speeds between two Scom-bridae species with and without RM endothermy (15). As a result , evidence for the hypothesis is still lacking. If fishes with RM endothermy are shown to cruise faster in nature, what ecological benefits could they achieve from doing so? Fishes can increase prey encounter rates and, thus, potential energy gains by cruising faster (16); however, this benefit may be counteracted if energetic costs incurred by cruising faster and being endothermic are high. It is therefore important to examine whether the cost of transport (i.e., the energy needed to move a unit body mass over a unit distance) at their cruising speeds is higher for fishes with RM endothermy. In addition to the benefit of increased prey encounter rates, fishes with RM endothermy may be able to move greater distances in a given time period, such as a year, because of their fast cruising speed. Annual migrations are common in fishes, often Significance Most fishes are cold-blooded, but tunas and some sharks (e.g., white sharks) maintain their exercising muscles warmer than ambient waters. This ability is a remarkable example of con-vergent evolution because bony and cartilaginous fishes diverged as long as 450 million years ago. What are the ecological benefits driving the evolution of warm muscles in fishes? Despite extensive discussion, no previous studies have tested a simple possibility that fishes with warm muscles may swim faster in nature. We demonstrate that fishes with warm muscles swim faster and perform larger-scale annual migrations than similar-sized cold-blooded fishes. Our results suggest that warm muscles enhance power output and, thus, cruising speeds, which may enable longer-distance migrations and potentially greater access to seasonally available resources.
Big skate Beringraja binoculata is the most frequently landed skate in the Gulf of Alaska portion... more Big skate Beringraja binoculata is the most frequently landed skate in the Gulf of Alaska portion of the Northeast Pacific Ocean, with recent stock assessment surveys showing relatively healthy skate stocks and continued interest from the commercial fishing industry to increase skate landings. Considered a data-poor species, there is a need for additional ecological information on big skates, including movement patterns and habitat use. We deployed pop-up satellite archival transmitting (PSAT) tags on 8 big skates in the Gulf of Alaska and set the tags to release 1 yr after deployment. The minimum distance traveled by big skates varied between 6 and 205 km, with 1 individual traveling at least 2100 km based on light geolocation data. Three individuals showed evidence of having made long-range movement and crossed at least 1 management boundary, and 3 remained relatively close to their tagging locations. Two tags did not report. The PSAT tags also extended the maximum documented depth of big skates to over 500 m and confirmed that they are thermally tolerant, occupying waters between 2 and 18°C. Because the total catch of big skate is divided into multiple areas and limited movement between areas is assumed, information from this study will aid in the development of appropriate spatial management plans for this species.
Proceedings. Biological sciences / The Royal Society, Jan 22, 2015
Ontogenetic changes in habitat are driven by shifting life-history requirements and play an impor... more 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 habit...
Sharks of the Open Ocean, 2008
Variability in the Depth Distribution of Salmon Sharks
The salmon shark, Lamna ditropis, is an endothermic, apex predator in the productive waters of th... more The salmon shark, Lamna ditropis, is an endothermic, apex predator in the productive waters of the North Pacific. To understand their role in these productive habitats and to identify and better understand their interactions with commercially important species and fisheries, detailed information regarding the distribution of the salmon shark is required. Archival data records from pop-up archival transmitting (PAT) tags were analyzed to examine the geographic and vertical distribution of female salmon sharks and elucidate how their distribution changes in relation to the biotic and abiotic environment. Salmon sharks exhibited a diel periodicity in their dive behavior, and their depth distribution varied spatially and seasonally. These shifts in depth distribution likely reflected changes in their foraging ecology in response to seasonal and spatial changes in the distribution and availability of important prey. The distribution of salmon sharks appears to follow consistent patterns ...
Fishery Bulletin National Oceanic and Atmospheric Administration, 2006
Age and growth estimates for salmon sharks (Lamna ditropis) in the eastern North Pacific were der... more Age and growth estimates for salmon sharks (Lamna ditropis) in the eastern North Pacific were derived from 182 vertebral centra collected from sharks ranging in length from 62.2 to 213.4 cm precaudal length (PCL) and compared to previously published age and growth data for salmon sharks in the western North Pacific. Eastern North Pacific female and male salmon sharks were aged up to 20 and 17 years, respectively. Relative marginal increment (RMI) analysis showed that postnatal rings form annually between January and March. Von Bertalanffy growth parameters derived from vertebral length-at-age data are L ∞ =207.4 cm PCL, k= 0.17/yr, and t 0 =−2.3 years for females (n=166), and L ∞ =182.8 cm PCL, k= 0.23/yr , and t 0 =−1.9 years for males (n=16). Age at maturity was estimated to range from six to nine years for females (median precaudal length of 164.7 cm PCL) and from three to five years old for males (median precaudal length of 124.0 cm PCL). Weight-length relationships for females and males in the eastern North Pacific are W=8.2 × 10 _05 × L 2.759 -0 6 × L 3.383 (r 2 = 0.99) and W= 3.2 × 10 (r 2 = 0.99), respectively. Our results show that female and male salmon sharks in the eastern North Pacific possess a faster growth rate, reach sexual maturity earlier, and attain greater weight-at-length than their same-sex counterparts living in the western North Pacific.
Thermal physiology and behavioral ecology of white sharks, Carcharodon carcharias /
Typescript. Microfiche copy available in Special Collections Dept. Thesis (M.A.)--San Francisco S... more Typescript. Microfiche copy available in Special Collections Dept. Thesis (M.A.)--San Francisco State University, 1996. Includes bibliographical references (leaves 33-37).
Proceedings of the National Academy of Sciences of the United States of America, Jan 20, 2015
Despite long evolutionary separations, several sharks and tunas share the ability to maintain slo... more Despite long evolutionary separations, several sharks and tunas share the ability to maintain slow-twitch, aerobic red muscle (RM) warmer than ambient water. Proximate causes of RM endothermy are well understood, but ultimate causes are unclear. Two advantages often proposed are thermal niche expansion and elevated cruising speeds. The thermal niche hypothesis is generally supported, because fishes with RM endothermy often exhibit greater tolerance to broad temperature ranges. In contrast, whether fishes with RM endothermy cruise faster, and achieve any ecological benefits from doing so, remains unclear. Here, we compiled data recorded by modern animal-tracking tools for a variety of free-swimming marine vertebrates. Using phylogenetically informed allometry, we show that both cruising speeds and maximum annual migration ranges of fishes with RM endothermy are 2-3 times greater than fishes without it, and comparable to nonfish endotherms (i.e., penguins and marine mammals). The esti...
Energetics, Metabolism and Endothermy in Sharks and Rays
Marine Biology, 2012
Marine Ecology Progress Series, 2015
The use of nursery areas by elasmobranchs is an important life history strategy that is thought t... more The use of nursery areas by elasmobranchs is an important life history strategy that is thought to reduce juvenile mortality and increase population growth rates. The endothermic salmon shark Lamna ditropis uses the California Current System (CCS) as a nursery area, though little is known about how juveniles use this ecosystem. Juvenile salmon sharks consistently strand along the west coast of North America. Strandings in the southern CCS occurred throughout the year, while those in the northern CCS were limited to summer and autumn, when mean sea surface temperatures were warmest. Strandings primarily occurred when water temperature was between 12 and 16°C, suggesting that juveniles occupy a relatively narrow thermal niche. Stable isotope analysis (SIA) indicated that juveniles primarily feed on offshore meso-and epipelagic prey from the outer shelf, slope, and oceanic habitats as opposed to inshore and coastal habitats, although sharks appeared to move closer to shore prior to stranding. Generalized additive models indicate that the probability of stranding was greatest when mean water temperatures were relatively high (~14°C) and sharks were exposed to acute cold-water events (~9°C) during coastal upwelling. This suggests that juveniles are thermally limited and stressed by upwelling events, resulting in bacterial infections that are the proximate cause of the strandings.
Environmental Biology of Fishes, 2004
Salmon sharks, Lamna ditropis, belong to a small group of sharks that possess vascular counter-cu... more Salmon sharks, Lamna ditropis, belong to a small group of sharks that possess vascular counter-current heat exchangers (retia mirabilia) allowing retention of metabolically generated heat, resulting in elevated body temperatures. The capacity of free-swimming lamnid sharks to regulate rates of heat gain and loss has not been demonstrated. Using acoustic telemetry, we recorded swimming depth and stomach temperature from four free-swimming salmon sharks in Prince William Sound, Alaska. Temperature data were obtained over time periods ranging from 3.8 to 20.7 h. Temperature profiles of the water column were obtained concurrently for use as estimates of ambient temperature. Mean stomach temperature among four individuals tracked ranged from 25.0 to 25.7°C. These sharks defended specific elevated temperatures regardless of changes in ambient temperature, which ranged from about 5-16°C. The maximum observed elevation of stomach temperature over ambient was 21.2°C. Because stomach temperatures were so strictly maintained relative to changes in ambient temperature, a thermal rate coefficient, k, (°C min )1°C thermal gradient )1 ) for cooling of 0.053 min )1 was obtained via a 'control' experiment with a dead salmon shark. We show that free-swimming adult salmon sharks maintain a specific stomach temperature independent of changes in ambient temperature through a combination of physical and physiological means, and essentially function as homeotherms. This unique ability is probably the underlying factor in the evolutionary niche expansion of salmon sharks into boreal waters and in their ability to actively pursue and capture highly active prey such as salmon.
Environmental Biology of Fishes, 1999
This paper presents information on the movements of white sharks, Carcharodon carcharias, at the ... more This paper presents information on the movements of white sharks, Carcharodon carcharias, at the South Farallon Islands (SFI), central California. Acoustic telemetry techniques provided preliminary data on the diurnal space utilization, movement patterns and ...
A re-examination of the age and growth of sand tiger sharks, Carcharias taurus , in the western North Atlantic: the importance of ageing protocols and use of multiple back-calculation techniques
Age and growth estimates for sand tiger sharks, Carcharias taurus, in the western North Atlantic ... more Age and growth estimates for sand tiger sharks, Carcharias taurus, in the western North Atlantic were derived from 96 vertebral centra collected from sharks ranging from 94 to 277 cm total length (TL), and compared to previously published age and growth data. The oldest female and male sand tiger sharks aged in this study were 17 and 15 years of age, respectively. von Bertalanffy growth parameters derived from vertebral length-at-age data are L ∞ = 295.8 cm TL, k = 0.11 year−1, and t 0 = −4.2 years for females, and L ∞ = 249.5 cm TL, k = 0.16 year−1, and t 0 = −3.4 years for males. Sexual maturity is estimated to be 9–10 years for females and 6–7 years for males. Weight-to-length relationships determined for female and male sand tiger sharks in the western North Atlantic are; W = 1.3 × 10−4 × L 2.4 (r 2 = 0.84, n = 55) and W = 9.0 × 10−5 × L2.5 (r 2 = 0.84, n = 47), respectively, and 7.9 × 10−5 × L 2.5 (r 2 = 0.84) for the sexes combined. Our results show sand tigers possess a slower rate of growth than previously thought. This information is crucial for accurately assessing this population’s ability to recover, and further justifies the need for this species to be fully protected.
PLOS One, 2009
Background: Although much is known about the behavior of white sharks in coastal regions, very li... more Background: Although much is known about the behavior of white sharks in coastal regions, very little is known about their vertical movements offshore in the eastern Pacific where they spend up to five months. We provide the first detailed description of the offshore habitat use of white sharks in the eastern North Pacific.
A re-evaluation of the size of the white shark (Carcharodon carcharias) population off California, USA
PloS one, 2014
White sharks are highly migratory and segregate by sex, age and size. Unlike marine mammals, they... more White sharks are highly migratory and segregate by sex, age and size. Unlike marine mammals, they neither surface to breathe nor frequent haul-out sites, hindering generation of abundance data required to estimate population size. A recent tag-recapture study used photographic identifications of white sharks at two aggregation sites to estimate abundance in "central California" at 219 mature and sub-adult individuals. They concluded this represented approximately one-half of the total abundance of mature and sub-adult sharks in the entire eastern North Pacific Ocean (ENP). This low estimate generated great concern within the conservation community, prompting petitions for governmental endangered species designations. We critically examine that study and find violations of model assumptions that, when considered in total, lead to population underestimates. We also use a Bayesian mixture model to demonstrate that the inclusion of transient sharks, characteristic of white shark aggregation sites, would substantially increase abundance estimates for the adults and sub-adults in the surveyed sub-population. Using a dataset obtained from the same sampling locations and widely accepted demographic methodology, our analysis indicates a minimum all-life stages population size of >2000 individuals in the California subpopulation is required to account for the number and size range of individual sharks observed at the two sampled sites. Even accounting for methodological and conceptual biases, an extrapolation of these data to estimate the white shark population size throughout the ENP is inappropriate. The true ENP white shark population size is likely several-fold greater as both our study and the original published estimate exclude non-aggregating sharks and those that independently aggregate at other important ENP sites. Accurately estimating the central California and ENP white shark population size requires methodologies that account for biases introduced by sampling a limited number of sites and that account for all life history stages across the species' range of habitats.
Journal of Fish Biology, 2008
A pregnant salmon shark Lamna ditropis, captured in Alaska in December 2006, held two male and tw... more A pregnant salmon shark Lamna ditropis, captured in Alaska in December 2006, held two male and two female oophagous embryos (two per uterus) nourished by a single large 7·5 kg ovary. This discovery provides new data and insights into reproduction of the species and new perspective on the genus Lamna.
Age and growth of elasmobranch fishes
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Farrugia et al by Kenneth Goldman