A Brain Heater in the Swordfish

Carey, Francis G.

doi:10.1126/science.7079766

Cited by 164 publications

(137 citation statements)

References 17 publications

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“…2). RM of this species is not significantly warmer than surrounding waters (35), but located medially in the body (similarly to fishes with RM endothermy) with a simple form of heat exchangers present, a morphology that suggests the ability to reduce heat loss from RM during steady swimming (36). Overall, our finding suggests that, in marine vertebrates in general, thermal strategy (endothermy or ectothermy) is a major determinant of the spatial scales of annual migrations through its effect on cruising speeds and tolerance to broad temperature ranges.…”

Section: Resultsmentioning

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.

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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Section: Resultsmentioning

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.

115

139

View full text Add to dashboard Cite

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“…In contrast, deeper dwelling pelagic fishes, such as swordfish and some tunas, forage extensively below the mixed layer by maintaining cardiac function via greater capacity for cardiac calcium cycling at reduced temperatures [118,121]. Selective heating of the neural infrastructure of the brain and eyes in billfishes and tunas also contribute to their ability to conduct sustained forays into cold water [78,89,122] and provide superior vision for deep foraging [79]. Additionally, surface basking may be a behavioral mechanism for thermoregulation [54,70].…”

Section: Biophysical Drivers Temperaturementioning

confidence: 99%

“…Based on surveys of stomach contents, small pelagic fishes and squid are important prey items [87,88], and swordfish exploit their ability to maintain brain temperatures above ambient water to capture prey in cold, deep waters [89]. Swordfish in the northwest Atlantic appear to spawn primarily south of the Sargasso Sea and east of the Antillean Arc [90].…”

Section: Swordfishmentioning

confidence: 99%

Satellite telemetry reveals physical processes driving billfish behavior

Braun

Kaplan

Horodysky

et al. 2015

Animal Biotelemetry

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Pop-up satellite archival transmitting (PSAT) tags are capable of storing high-resolution behavioral and environmental information for extended periods of time (approximately 1 year), rendering them especially valuable for studying highly mobile species. In this review, we synthesize published PSAT data to understand the biophysical drivers that influence movements of billfishes (families Xiphiidae and Istiophoridae). To date, over 1,080 PSATs have been deployed on billfishes, with individuals demonstrating both trans-equatorial and trans-basin movements. Using this dataset, we identify four main physical variables that drive billfish behavior: temperature, light, oxygen, and complex water mixing (e.g. fronts and eddies). Of the seven species that have been studied with PSAT technology, all exhibited a strong thermal preference for water >22°C, though vertically migrating swordfish additionally occupied waters <10°C while at depth. Ambient light levels influence vertical movements, especially those associated with foraging, as billfish possess large eyes and thermoregulatory abilities that facilitate feeding behaviors below warm surface layers. Mounting evidence suggests that some billfishes actively avoid regions with low dissolved oxygen (<3.5 mL L −1). Human-induced climate change is expected to increase the horizontal and vertical extent of hypoxic water and may further compress habitat and concentrate fishing pressure on pelagic fishes. Finally, complex submeso-and mesoscale processes provide critical habitat for spawning, larval feeding, and retention, but our understanding of these and other behavioral aspects of billfish biology remains limited. Future research efforts should leverage technical advancements while integrating existing and future tag data with chemical and physical oceanographic datasets to gain a better understanding of the relevant biophysical interactions for billfishes, thereby enhancing management capabilities for this ecologically and economically important group of fishes.

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“…Certain ocean fishes utilize modified eye musculature to elevate eye and brain temperature well above water temperature (Carey, 1982;Block and Franzini-Armstrong, 1988). Harbour seals can elevate the surface temperatures of their mystacial and supraorbital vibrissal pads as much as 25 -C above water temperature, and exhibit high tactile sensitivity in waters as cool as 0 -C (Mauck et al, 2000).…”

Section: Introductionmentioning

confidence: 99%