Satellite Tagging and Cardiac Physiology Reveal Niche Expansion in Salmon Sharks

Weng, Kevin C.; Castilho, Pedro C.; Morrissette, Jeffery M.; Landeira-Fernandez, Ana M.; Holts, David B.; Schallert, Robert J.; Goldman, Kenneth J.; Block, Barbara A.

doi:10.1126/science.1114616

Cited by 192 publications

(188 citation statements)

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“…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.…”

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Comparative analyses of animal-tracking data reveal ecological significance of endothermy in fishes

Watanabe

Goldman

Caselle

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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115

139

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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 convergent 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 thei...

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confidence: 99%

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confidence: 99%

Comparative analyses of animal-tracking data reveal ecological significance of endothermy in fishes

Watanabe

Goldman

Caselle

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

115

139

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“…Salmon sharks range from the Gulf of Alaska south to central Baja California and east to Hawaii, with adults reported primarily in the northern part of the range and juveniles in the southern portion. 21 Documentation of juveniles, usually slightly under or over 1 meter in total body length, is composed primarily of reports of stranded individuals found along the coast of California and Oregon. Although these stranding events have been recorded by local biologists for more than 20 years, no specific causes have been identified.…”

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Meningoencephalitis Associated With Carnobacterium maltaromaticum–Like Bacteria in Stranded Juvenile Salmon Sharks (Lamna ditropis)

Schaffer

Lifland

Sommeran³

et al. 2012

Vet Pathol

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Juvenile salmon sharks beach yearly along the California coast, primarily during late summer and early fall. Fresh, frozen, and formalin-fixed tissues from 19 stranded salmon sharks were collected for examination. Histopathology revealed meningitis or meningoencephalitis in 18 of 19 shark brains with intralesional bacteria observed in 6 of the affected brains. Bacterial culture of fresh or frozen brain, liver, and/or heart blood from 13 sharks yielded pure cultures characterized molecularly and/or biochemically as belonging to the genus Carnobacterium. The 16s ribosomal DNA sequence of 7 tissue isolates from 7 separate sharks was 99% homologous to C. maltaromaticum (GenBank FJ656722.1). Sequence of the large ribosomal DNA intergenic spacer region (ISR) was 97% homologous to C. maltaromaticum (AF374295.1). This is the first report of Carnobacterium infection in any shark species, and the authors posit that brain infection caused by Carnobacterium is a significant cause of morbidity and mortality in juvenile salmon sharks found stranded along the Pacific coast of California.

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“…This should be approached at three levels to: (i) monitor the physical environment, (ii) monitor the basic physiological processes of free living organisms, and (iii) monitor their behaviour. Recent developments in data logging and telemetry have increased our understanding of the ecological implications of environmental constraints (Daunt et al 2003;Kawabe et al 2004;Ropert-Coudert & Wilson 2005;Weng et al 2005;Wilson et al 2005;Kuhn et al 2006;Metcalfe et al 2006;Sims et al 2006). Similarly, fieldwork on marine mammals and birds using miniature cameras mounted on the animals is starting to reveal the behaviour of these organisms within their environment (Williams et al 2000;Gremillet et al 2006).…”

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confidence: 99%

Environmental constraints upon locomotion and predator–prey interactions in aquatic organisms: an introduction

Domenici

Claireaux

McKenzie

2007

Phil. Trans. R. Soc. B

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Environmental constraints in aquatic habitats have become topics of concern to both the scientific community and the public at large. In particular, coastal and freshwater habitats are subject to dramatic variability in various environmental factors, as a result of both natural and anthropogenic processes. The protection and sustainable management of all aquatic habitats requires greater understanding of how environmental constraints influence aquatic organisms. Locomotion and predator-prey interactions are intimately linked and fundamental to the survival of mobile aquatic organisms. This paper summarizes the main points from the review and research articles which comprise the theme issue 'Environmental constraints upon locomotion and predator-prey interactions in aquatic organisms'. The articles explore how natural and anthropogenic factors can constrain these two fundamental activities in a diverse range of organisms from phytoplankton to marine mammals. Some major environmental constraints derive from the intrinsic properties of the fluid and are mechanical in nature, such as viscosity and flow regime. Other constraints derive from direct effects of factors, such as temperature, oxygen content of the water or turbidity, upon the mechanisms underlying the performance of locomotion and predator-prey interactions. The effect of these factors on performance at the tissue and organ level is reflected in constraints upon performance of the whole organism. All these constraints can influence behaviour. Ultimately, they can have an impact on ecological performance. One issue that requires particular attention is how factors such as temperature and oxygen can exert different constraints on the physiology and behaviour of different taxa and the ecological implications of this. Given the multiplicity of constraints, the complexity of their interactions, and the variety of biological levels at which they can act, there is a clear need for integration between the fields of physiology, biomechanics, behaviour, ecology, biological modelling and evolution in both laboratory and field studies. For studies on animals in their natural environment, further technological advances are required to allow investigation of how the prevailing physico-chemical conditions influence basic physiological processes and behaviour.

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Satellite Tagging and Cardiac Physiology Reveal Niche Expansion in Salmon Sharks

Cited by 192 publications

References 13 publications

Comparative analyses of animal-tracking data reveal ecological significance of endothermy in fishes

Comparative analyses of animal-tracking data reveal ecological significance of endothermy in fishes

Meningoencephalitis Associated With Carnobacterium maltaromaticum–Like Bacteria in Stranded Juvenile Salmon Sharks (Lamna ditropis)

Environmental constraints upon locomotion and predator–prey interactions in aquatic organisms: an introduction

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