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CORRESPONDENCE
On the importance of understanding physiology when estimating energetics in cetaceans
Lars P. Folkow, Arnoldus Schytte Blix
Biology Open 2017 6: 306 doi: 10.1242/bio.023929
Lars P. Folkow
1Department of Arctic and Marine Biology, UiT – The Arctic University of Norway, Tromsø NO-9037, Norway
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  • For correspondence: lars.folkow@uit.no
Arnoldus Schytte Blix
1Department of Arctic and Marine Biology, UiT – The Arctic University of Norway, Tromsø NO-9037, Norway
2St. Catharine's College, Cambridge CB2 1RL, UK
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We have, with great interest, read the paper entitled ‘Estimating energetics in cetaceans from respiratory frequency: why we need to understand physiology’ by Fahlman et al. (2016), hereafter referred to as Fahlman et al., and we are particularly pleased by their emphasis of the need to understand physiology when estimating field metabolic rates (FMR) of cetaceans.

In this paper, Fahlman et al. have employed their own detailed data collected from captive bottlenose dolphins (Tursiops truncatus), at rest and at rest after a swimming bout at surface, to test the validity of using respiratory variables of free-living large mysticete cetaceans for the estimation of their FMR. This approach was first used in the blue whale (Balaenoptera musculus) by Nobel laureate August Krogh, who definitely knew physiology (Krogh, 1934), and has hitherto been the only way to obtain useful estimates of energy expenditure in free-living large cetaceans, which are not easily accommodated in laboratories. It takes advantage of the fact that diving mammals are breath-hold divers which benefit from maximizing their time under water by conducting respiratory exchange during brief surface periods, in which large volumes of air are rapidly exchanged (e.g. Blix and Folkow, 1995).

The approach is based on the equation:Embedded Image(1)where VO2 is the rate of oxygen uptake (l min−1); VT is tidal volume (l breath−1); ΔO2 is the difference in oxygen concentration between inspired (O2in) and expired air (O2ex); ΔO2=O2in−O2ex (%); and f is breathing rate (breaths min−1).

In their analysis, Fahlman et al. have evaluated three methods, all based on Eqn 1 (Methods A, B and C). In Method A, data from Armstrong and Siegfried (1991) and Dolphin (1987) were used, and in B our data (Blix and Folkow, 1995) were used, in both cases to estimate FMR in large mysticetes; whereas in Method C, Fahlman et al. used their own data from their dolphins. In all cases the method outputs were compared to Fahlman et al.'s own direct measurements of VO2 in the same dolphins. In so doing it is hardly surprising that Method C performed well, whereas Methods A and B were found to overestimate the ‘true’ value by some 200-500% and, although Fahlman et al. offer some reservations on the validity of their comparison, this remains to be the take-home message, both from the abstract and the full paper.

However, we want to emphasize that Fahlman et al. conducted their comparison across levels of activity, across suborders and across >20-orders-of-magnitude in body mass, and in doing so, even chose to use empirical allometric relationships for prediction of lung volumes in large mysticetes to predict the lung volumes of their dolphins, instead of using their own measured values. That the outputs of the different methods differ substantially should therefore come as no bigger surprise than that use of the Du Bois formula for estimation of surface area in man (Du Bois and Du Bois, 1916) would prove inappropriate for estimating surface area, for example, in giraffes. Moreover, if Fahlman et al. instead had estimated the lung volumes of their dolphins by use of Wahrenbrock and coworker's (1974) empirical equation for gray whales (Eschrichtius robustus), they would have obtained negative values.

To further illustrate our point, we have tested the validity of Fahlman et al.'s Method C, using existing data for a large mysticetes. Wahrenbrock et al. (1974) have measured that a 4000 kg gray whale calf at rest has a VO2 corresponding to about 2× Kleiber's basal metabolic rate (BMR), i.e. as expected for any immature and growing mammal (Kleiber, 1961). Using Method C with Fahlman et al.'s data for resting VT (32% of total lung capacity) and ΔO2 (4.94%), and Wahrenbrock and coworker's (1974) measured values of lung volume (236 liter) and resting breathing rate (∼1 breath min−1) for a calf of 4000 kg, we obtain a VO2 of 3.7 liter min−1, which is less than 35% of the VO2 of 10.7 liter min−1 that was measured. If Fahlman's Method C is applied to our data (Blix and Folkow, 1995), it suggests that a minke whale (Balaenoptera acutorostrata) would be able to swim at 2–3 m s−1 at a FMR that is 20% below Kleiber's BMR of mammals in general (Kleiber, 1961), or for good measure, at similar FMR (in W kg−0.75) as in the three-toed sloth (Bradypus variegatus) (Nagy and Montgomery, 1980).

One would assume that, with proper physiological insight, the extraordinarily large discrepancies between the outcomes of the different methods would have inspired similar exercises, and that Fahlman et al.'s paper, in consequence, would not have been published in its present form.

Footnotes

  • Competing interests

    The authors declare no competing or financial interests.

  • © 2017. Published by The Company of Biologists Ltd
http://creativecommons.org/licenses/by/3.0

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

References

  1. ↵
    1. Armstrong, A. J. and
    2. Siegfried, W. R.
    (1991). Consumption of Antarctic krill by minke whales. Antarctic Sci. 3, 13-18. doi:10.1017/S0954102091000044
    OpenUrlCrossRef
  2. ↵
    1. Blix, A. S. and
    2. Folkow, L. P.
    (1995). Daily energy expenditure in free living minke whales. Acta Physiol. Scand. 153, 61-66. doi:10.1111/j.1748-1716.1995.tb09834.x
    OpenUrlCrossRefPubMed
  3. ↵
    1. Dolphin, W. F.
    (1987). Dive behavior and estimated energy expenditure of foraging humpback whales in southeast Alaska. Can. J. Zool. 65, 354-362. doi:10.1139/z87-055
    OpenUrlCrossRef
  4. ↵
    1. Du Bois, D. and
    2. Du Bois, E. F.
    (1916). A formula to estimate the approximate surface area if height and weight be known. Arch. Intern. Med. 17, 863-871. doi:10.1001/archinte.1916.00080130010002
    OpenUrlCrossRefPubMed
  5. ↵
    1. Fahlman, A.,
    2. van der Hoop, J.,
    3. Moore, M. J.,
    4. Levine, G.,
    5. Rocho-Levine, J. and
    6. Brodsky, M.
    (2016). Estimating energetics in cetaceans from respiratory frequency: why we need to understand physiology. Biol. Open 5, 436-442. doi:10.1242/bio.017251
    OpenUrlAbstract/FREE Full Text
  6. ↵
    1. Kleiber, M.
    (1961). The Fire of Life – An Introduction to Animal Energetics. New York: John Wiley & Sons, Inc..
  7. ↵
    1. Krogh, A.
    (1934). Physiology of the blue whale. Nature 133, 635-637. doi:10.1038/133635a0
    OpenUrlCrossRef
  8. ↵
    1. Nagy, K. A. and
    2. Montgomery, G. G.
    (1980). Field metabolic rate, water flux, and food consumption in three-toed sloths (Bradypus variegatus). J. Mammal. 61, 465-472. doi:10.2307/1379840
    OpenUrlAbstract/FREE Full Text
  9. ↵
    1. Wahrenbrock, E. A.,
    2. Maruschak, G. F.,
    3. Elsner, R. and
    4. Kenny, D. W.
    (1974). Respiration and metabolism in two baleen whale calves. Mar. Fish. Rev. 36, 3-8.
    OpenUrl
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CORRESPONDENCE
On the importance of understanding physiology when estimating energetics in cetaceans
Lars P. Folkow, Arnoldus Schytte Blix
Biology Open 2017 6: 306 doi: 10.1242/bio.023929
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CORRESPONDENCE
On the importance of understanding physiology when estimating energetics in cetaceans
Lars P. Folkow, Arnoldus Schytte Blix
Biology Open 2017 6: 306 doi: 10.1242/bio.023929

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