1. Regional endothermy has evolved several times in marine fishes, and two competing hypotheses are generally proposed to explain the evolutionary drivers behind this trait: thermal niche expansion and elevated cruising speeds. Evidence to support either hypothesis is equivocal, and the ecological advantages conferred by endothermy in fishes remain debated.

2. By compiling published biologging data and collecting precise speed measurements from free-swimming fishes in the wild, we directly test whether endothermic fishes encounter broader temperature ranges, swim faster, or both. Our analyses avoid several complications associated with earlier tests of these hypotheses, as we use precise measurements of the thermal experience and speed of individual fish.

3. Phylogenetically-informed analyses of 89 studies reporting temperature ranges encountered by tagged fishes reveal that endotherms do not encounter broader temperature ranges than their ectothermic counterparts. In contrast, speed measurements from 45 individuals (16 species, of which 4 were regional endotherms) show that endothermic fishes cruise ~ 1.6 times faster than ectotherms, after accounting for the influence of body temperature and body mass on speed.

4. Our study shows that regionally endothermic fishes – those with the ability to conserve metabolically derived heat through vascular countercurrent heat exchangers and elevate the temperature of internal tissues – swim at elevated cruising speeds, although not as fast as previously thought. Contrary to previous studies of endothermy’s role in thermal niche expansion, our results suggest the significance of endothermy in fishes lies in the advantages it confers to swimming performance rather than facilitating occupation of broader thermal niches. Given speed’s major influence on metabolic rate, our updated speed estimates imply endotherms have lower routine energy requirements than current estimates.

5. Our findings shed light on the evolutionary drivers of regional endothermy in fishes and question the view that the trait confers resilience to climate change through broader thermal tolerance than that of ectotherms.

Two datasets were collected for this study: (1) thermal niche expansion dataset & (2) elevated cruising speeds dataset. 

(1) Data collation: Thermal niche expansion dataset

Data collection for this study consisted of an extensive literature review of peer-reviewed published sources. Library and electronic database searches were carried out across multiple platforms, such as JSTOR, Web of Science, ScienceDirect, Research Gate, among others. Title searchers and keywords included ‘biologging’, ‘thermoregulation’, ‘endothermy’, ‘regional endothermy’ ‘tagging’, ‘shark(s)’, ‘teleost(s)’, ‘ectothermic’, ‘internal temperature’, ‘body temperature’, ‘thermal ecology’, ‘thermal niche expansion’, ‘elevated cruising speeds’ and/or ‘shark tagging’. In addition, studies cited in papers found during these searches, but not identified directly by the search, were also included. Papers for this study were chosen based on a number of selection criteria: (1) species tagged (e.g. marine species only), (2) tag type (e.g. Pop-up Archival Tag; PAT), (3) location of animal at time of tagging (e.g. only wild fishes in their natural habitat were utilised), (4) frequency of data collection/recording, (5) duration of recording, (6) type of publication (e.g. peer-reviewed journal articles only), (7) recorded parameters (e.g. depth, ambient temperature, internal temperature), and (8) availability and reliability of the data (e.g. robustness of methodologies and technologies used). We chose several data parameters to extract during this review: species common name, species scientific name, thermoregulatory ability, tag type, body size, number of individuals, ambient and body temperature (min., max., mean, 10% upper and lower percentiles), recording duration, depth (min., max., mean, 10% upper and lower percentiles) and latitude (if available).  

(2) Speed measurements: Elevated cruising speeds dataset

We confined our data collection to speed propellers of the same type, from the same manufacturer, to directly collect precise speed measurements of fishes free-swimming in the wild, whilst simultaneously recording the ambient temperature, along with several other parameters.

We captured fish by drum lines, long lines, or by angling. Biologging packages were fitted to dorsal or pectoral fins of each animal, which was then immediately released; associated methods detailed further in published sources (Watanabe et al., 2019a, Watanabe et al., 2019b, Huveneers et al., 2018, Papastamatiou et al., 2018, Watanabe et al., 2015, Nakamura et al., 2011). Biologging packages varied slightly among species but all packages included accelerometers (recording tri-axial acceleration at 25Hz and depth at 1Hz; Techno-Smart AGM-1), temperature loggers (recording ambient temperature at 1Hz) and propeller-based speed sensors (all manufactured by Little Leonardo Corp.) of similar models (PD3GT logger, maximum dimensions 115 x 21mm, 60g in air; W1000-PD3GT logger, 22 x 123 mm, 90 g in air; and ORI400/1300-PD3GT logger, 16 mm × 74 mm, 37 g in air), measuring speed in m s-1 (accuracy of 0.03 – 0.05m s-1), recording at 1Hz (Payne, N. L., Iosilevskii, G. et al., 2016, Nakamura et al., 2011, Watanabe et al., 2015). To enable retrieval, tag packages also included a VHF transmitter (Advanced Telemetry Systems, MM100), satellite position only tag (Wildlife Computers Model 258; ARGOS enabled) and a time-release mechanism. Once detached from the animal, packages floated to the surface as they were constructed of a positively buoyant material (Diab Syntactic © non-compressible foam). Packages were then located using the ARGOS system and a VHF receiver and retrieved from the ocean surface by boat. 

References

Huveneers, C., Watanabe, Y., Payne, N. & Semmens, J. (2018). Interacting with wildlife tourism increases activity of white sharks. Conservation Physiology, 6.

Nakamura, I., Watanabe, Y., Papastamatiou, Y., Sato, K. & Meyer, C. (2011). Yo-yo vertical movements suggest a foraging strategy for tiger sharks Galeocerdo cuvier. Marine Ecology Progress Series, 424, 237-246.

Papastamatiou, Y. P., Watanabe, Y. Y., Demšar, U., Leos-Barajas, V., Bradley, D., Langrock, R., Weng, K., Lowe, C. G., Friedlander, A. M. & Caselle, J. E. 2018. Activity seascapes highlight central place foraging strategies in marine predators that never stop swimming. Movement Ecology, 6, 9.

Payne, N. L., Iosilevskii, G., Barnett, A., Fischer, C., Graham, R. T., Gleiss, A. C. & Watanabe, Y. Y. (2016). Great hammerhead sharks swim on their side to reduce transport costs. Nature Communications, 7, 12289.

Watanabe, Y. Y., Goldman, K. J., Caselle, J. E., Chapman, D. D. & Papastamatiou, Y. P. (2015). Comparative analyses of animal-tracking data reveal ecological significance of endothermy in fishes. Proceedings of the National Academy of Sciences, 112, 6104-6109.

Watanabe, Y. Y., Payne, N., Semmens, J., Fox, A. & Huveneers, C. (2019a). Hunting behaviour of white sharks recorded by animal-borne accelerometers and cameras. Marine Ecology Progress Series, 621, 221-227.

Watanabe, Y. Y., Payne, N. L., Semmens, J. M., Fox, A. & Huveneers, C. (2019b). Swimming strategies and energetics of endothermic white sharks during foraging. The Journal of Experimental Biology, 222, jeb185603.