RESEARCH PAPER
Do bigger bodies require bigger radiators? Insights into thermal ecology from closely related marine mammal species and implications for ecogeographic rules
Stephanie K. Adamczak,
D. Ann Pabst,
William A. McLellan,
Lesley H. Thorne,
Corresponding Author
Stephanie K. Adamczak
School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, NY, USA
Correspondence
Stephanie K. Adamczak, School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, NY, USA.
Email: [email protected]
Search for more papers by this authorD. Ann Pabst
Department of Biology and Marine Biology, University of North Carolina Wilmington, Wilmington, NC, USA
Search for more papers by this authorWilliam A. McLellan
Department of Biology and Marine Biology, University of North Carolina Wilmington, Wilmington, NC, USA
Search for more papers by this authorLesley H. Thorne
School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, NY, USA
Search for more papers by this authorStephanie K. Adamczak,
D. Ann Pabst,
William A. McLellan,
Lesley H. Thorne,
Corresponding Author
Stephanie K. Adamczak
School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, NY, USA
Correspondence
Stephanie K. Adamczak, School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, NY, USA.
Email: [email protected]
Search for more papers by this authorD. Ann Pabst
Department of Biology and Marine Biology, University of North Carolina Wilmington, Wilmington, NC, USA
Search for more papers by this authorWilliam A. McLellan
Department of Biology and Marine Biology, University of North Carolina Wilmington, Wilmington, NC, USA
Search for more papers by this authorLesley H. Thorne
School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, NY, USA
Search for more papers by this authorHandling Editor: Jon Sadler
Abstract
Aim
The aim of this study was to determine if marine mammals follow ecogeographic rules. We examined Bergmann's rule and Allen's rule in two pilot whale species with contrasting latitudinal distributions.
Location
Northwest Atlantic Ocean.
Taxon
Globicephala spp.
Methods
We analysed morphometric data collected from strandings of short- and long-finned pilot whales in the Northwest Atlantic Ocean to assess intraspecific and interspecific variation in surface area to volume ratios (SA:V) of the body core and appendage surface area relative to body core SA (normalized appendage SA) using a novel 3D modelling method.
Results
Our results suggest that ecogeographic variation in morphometrics between the two pilot whale species is consistent with morphological adaptations required to balance heat conservation and heat dissipation. Interspecific differences in morphology supported Bergmann's rule for fully grown individuals: the more temperate long-finned pilot whale had a larger body size and lower body core SA:V than the short-finned pilot whale, which has a more tropical distribution. Allen's rule was not supported; when all appendages were considered together, long-finned pilot whales had larger normalized SA than short-finned pilot whales. However, the pectoral flippers were the primary driver of this relationship; while long-finned pilot whales had proportionally larger pectoral flippers, short-finned pilot whales had proportionally larger dorsal fins and flukes. In addition, larger long-finned pilot whales (i.e. males and mature individuals) had proportionally larger pectoral flippers than smaller long-finned pilot whales.
Main Conclusions
Pilot whales follow Bergmann's rule but do not follow Allen's rule when fully mature. Thinly insulated appendages in marine mammals can be used to dissipate heat as the core warms, and larger and better insulated marine mammals may require relatively larger appendages in order to offload heat and thermoregulate effectively. Our results provide novel insight into ecogeographic rules and suggest that species in higher latitude climates towards the poles will demonstrate tradeoffs between core body heat conservation and appendage heat dissipation.
Open Research
DATA AVAILABILITY STATEMENT
The data that support these findings can be found in Appendix S2 of this manuscript.
Supporting Information
| Filename | Description |
|---|---|
| jbi13796-sup-0001-AppendixS1.docxWord document, 1.2 MB | |
| jbi13796-sup-0002-AppendixS2.xlsxapplication/excel, 24.7 KB |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- Adamczak, S. K., Pabst, D. A., McLellan, W. A., & Thorne, L. H. (2019). Using 3D models to improve estimates of marine mammal size and external morphology. Frontiers in Marine Science, 6, 12. https://doi.org/10.3389/fmars.2019.00334
- Alhajeri, B. H., & Steppan, S. J. (2016). Association between climate and body size in rodents: A phylogenetic test of Bergmann’s rule. Mammalian Biology, 81, 219–225. https://doi.org/10.1016/j.mambio.2015.12.001
- Allen, J. A. (1877). The influence of physical conditions in the genesis of species. Radical Review, 1, 108–140.
- Ashton, K. G., Tracy, M. C., & de Queiroz, A. (2000). Is Bergmann’s rule valid for mammals? The American Naturalist, 156(4), 391–415. https://doi.org/10.1086/303400
- Bagge, L. E., Koopman, H. N., Rommel, S. A., McLellan, W. A., & Pabst, D. A. (2012). Lipid class and depth-specific thermal properties of blubber of the short-finned pilot whale and the pygmy sperm whale. Journal of Experimental Biology, 215, 4330–4339. https://doi.org/10.1242/jeb.071530
- Barbieri, M. M., McLellan, W. A., Wells, R. S., Blum, J. E., Hofmann, S., Gannon, J., & Pabst, D. A. (2010). Using infrared thermography to assess seasonal trends in dorsal fin surface temperatures of free-swimming bottlenose dolphins (Tursiops truncatus) in Sarasota Bay, Florida. Marine Mammal Science, 26(1), 53–66. https://doi.org/10.1111/j.1748-7692.2009.00319.x
- Berta, A., Sumich, J. L., & Kovacs, K. M. (2006). Marine mammals: Evolutionary biology. Cambridge, MA: Academic Press.
- Blackburn, T. M., Gaston, K. J., & Loder, N. (1999). Geographic gradients in body size, a clarification of Bergmann’s rule. Diversity and Distributions, 5(4), 165–174. https://doi.org/10.1046/j.1472-4642.1999.00046.x
10.1046/j.1472-4642.1999.00046.x Google Scholar
- Blender Online Community. (2016). Blender– A 3D modelling and rendering package. Amsterdam, Netherlands: Stichting Blender Foundation. Retrieved from http://www.blender.org.
- Bloch, D., Zachariassen, M., & Zachariassen, P. (1993). Some external characters of the long-finned pilot whale off the Faroe Islands and a comparison with the short-finned pilot whale. Report of the International Whaling Commission (Special Issue) (pp. 117–135).
- Briscoe, N. J., Krockenberger, A., Handasyde, K. A., & Kearney, M. R. (2014). Bergmann meets Scholander: Geographical variation in body size and insulation in the koala is related to climate. Journal of Biogeography, 42(4), 12. https://doi.org/10.1111/jbi.12445
- Cooper, L. N., Sedano, N., Johansson, S., May, B., Brown, J. D., Holliday, C. M., … Fish, F. E. (2008). Hydrodynamic performance of the minke whale (Balaenoptera acutorostrata) flipper. The Journal of Experimental Biology, 211, 1859–1867. https://doi.org/10.1242/jeb.014134
- Costa, D. P., & Kooyman, G. L. (1982). Oxygen consumption, thermoregulation, and the effect of fur oiling and washing on the sea otter, Enhydra lutris. Canadian Journal of Zoology, 60, 2761–2767. https://doi.org/10.1139/z82-354
- Danner, R. M., & Greenberg, R. (2015). A critical season approach to Allen’s rule: Bill size declines with winter temperature in a cold temperate environment. Journal of Biogeography, 42, 114–120. https://doi.org/10.1111/jbi.12389
- Domenici, P. (2001). The scaling of locomotor performance in predator–prey encounters: From fish to killer whales. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 131(1), 169–182.
- Edel, R. K., & Winn, H. E. (1978). Observations on underwater locomotion and flipper movement of the humpback whale (Megaptera novaeangliae). Marine Biology, 48(3), 279–287. https://doi.org/10.1007/BF00397155
- Fish, F. E. (2004). Structure and mechanics of nonpiscine control surfaces. IEEE Journal of Oceanic Engineering, 29(3), 605–621. https://doi.org/10.1109/JOE.2004.833213
- Fish, F. E., Howle, L. E., & Murray, M. M. (2008). Hydrodynamic flow control in marine mammals. Integrative and Comparative Biology, 48(6), 788–800. https://doi.org/10.1093/icb/icn029
- Fox, J., & Weisberg, S. (2011). An R companion to applied regression ( 2nd ed .). Thousand Oaks, CA: Sage. Retrieved from http://socserv.socsci.mcmaster.ca/jfox/Books/Companion.
- Freckleton, R. P., Harvey, P. H., & Pagel, M. (2003). Bergmann’s rule and body size in mammals. The American Naturalist, 161(5), 821–825. https://doi.org/10.1086/374346
- Friedman, N. R., Harmácková, L., Economo, E. P., & Remes, V. (2017). Smaller beaks for colder winters: Thermoregulation drives beak size evolution in Australian songbirds. Evolution, 71(8), 2120–2129. https://doi.org/10.1111/evo.13274
- Garrison, L. P., & Rosel, P. E. (2017) Partitioning short-finned and long-finned pilot whale bycatch estimates using habitat and genetic information (p. 24). 75 Virginia Beach Dr., Miami, FL 33140: Southeast Fisheries Science Center, Protected Resources and Biodiversity Division. PRBD Contribution #PRBD-2016-17.
- Gaston, K. J., Chown, S. L., & Evans, K. L. (2008). Ecogeographical rules: Elements of a synthesis. Journal of Biogeography, 35, 483–500. https://doi.org/10.1111/j.1365-2699.2007.01772.x
- Greenberg, R., Danner, R., Olsen, B., & Luther, D. (2011). High summer temperature explains bill size variation in salt marsh sparrows. Ecography, 34, 146–152.
- Griffing, J. P. (1974). Body measurements of black-tailed jackrabbits of Southeastern New Mexico with implications of Allen’s rule. Journal of Mammalogy, 55(3), 674–678. https://doi.org/10.2307/1379562
- Hayes, S. A., Josephson, E., Maze-Foley, K., & Rosel, P. E. (2017). US Atlantic and Gulf of Mexico Marine Mammal Stock Assessments-2016. NOAA Technical Memorandum NMFS-NE-241 (p. 274).
- Hayssen, V., & Lacy, R. C. (1985). Basal metabolic rates in mammals, taxonomic differences in the allometry of BMR and body mass. Comparative Biochemistry and Physiology, 81A(4), 741–754. https://doi.org/10.1016/0300-9629(85)90904-1
- Hill, R. W., Christian, D. P., & Veghte, J. H. (1980). Pinna temperature in exercising jackrabbits, Lepus californicus. Journal of Mammalogy, 61(1), 30–38. https://doi.org/10.2307/1379954
- Hohn, A. A., Rotsetin, D. S., Harms, C. A., & Southall, B. L. (2006). Report on Marine Mammal Unusual Mortality Event IMESE0501Sp: Multispecies mass stranding of pilot whales (Globicephalamacrorhynchus), minke whale (Balaenopteracutorostrata), and dwarf sperm whales (Kogia sima) in North Carolina on 15-16 January 2005. NOAA Technical Memorandum NMFS-SEFSC-537 (p. 230).
- Hokkanen, J. E. I. (1990). Temperature regulation of marine mammals. Journal of Theoretical Biology, 145, 465–485. https://doi.org/10.1016/S0022-5193(05)80482-5
- James, F. C. (1970). Geographic size variation in birds and its relationship to climate. Ecology, 51(3), 365–390. https://doi.org/10.2307/1935374
- Kasuya, T., & Marsh, H. (1984).Life history and reproductive biology of short-finned pilot whale, Globicephalamacrorhynchus, off the Pacific Coast of Japan. Report on the International Whaling Commission (pp. 259–310). Special Issue 6.
- Kleiber, M. (1961). The fire of life. New York, NY, USA: Wiley.
- Koopman, H. N. (2007). Phylogentic, ecological, and ontogenetic factors influencing the biochemical structure of blubber of odontocetes. Marine Biology, 151(1), 277–291. https://doi.org/10.1007/s00227-006-0489-8
- Kvadsheim, P. H., & Folkow, L. P. (1997). Blubber and flipper heat transfer in harp seals. Acta Physiologica Scandinavia, 161, 385–395. https://doi.org/10.1046/j.1365-201X.1997.00235.x
- Leatherwood, S., Caldwell, D. K., & Winn, H. E. (1976).Whales, dolphins and porpoises of the western North Atlantic. A guide to their identification. NOAA Technical Report, NMFS 396 (p. 176).
- Martin, A. R., Reynolds, P., & Richardson, M. G. (1987). Aspects of the biology of pilot whales (Globicephala melaena) in recent mass strandings on the British coast. Journal of Zoology, 211(1), 11–23. https://doi.org/10.1111/j.1469-7998.1987.tb07449.x
- Mayr, E. (1956). Animal species and evolution. Cambridge, Massachusetts, USA: Belknap Press.
- McNab, B. K. (1971). On the significance of Bergmann’s rule. Ecology, 52(5), 845–854.
- Meagher, E. M., McLellan, W. A., Westgate, A. J., Wells, R. S., Blum, J. E., & Pabst, D. A. (2008). Seasonal patterns of heat loss in wild bottlenose dolphins (Tursiops truncatus). Journal of Comparative Physiology B, 178(4), 529–543. https://doi.org/10.1007/s00360-007-0245-5
- Meagher, E. M., McLellan, W. A., Westgate, A. J., Wells, R. S., Frierson, D., & Pabst, D. A. (2002). The relationship between heat flow and vasculature in the dorsal fin of wild bottlenose dolphins Tursiops truncatus. The Journal of Experimental Biology, 205, 3475–3486.
- Miralles, L., Oremus, O., Silva, M. A., Planes, S., & Garcia-Vasquez, E. (2016). Interspecific hybridization in pilot whales and asymmetric genetic introgression in northern Globicephala melas under the scenario of global warming. PLoS ONE, 11(8), e0160080. https://doi.org/10.1371/journal.pone.0160080
- Noren, D. P., Williams, T. M., Berry, P., & Butler, E. (1999). Thermoregulation during swimming and diving in bottlenose dolphins, Tursiops truncatus. Journal of Comparative Physiology B, 169, 93–99. https://doi.org/10.1007/s003600050198
- Norris, K. S. (1961). Standardized methods for measuring and recording data on the smaller cetaceans. Journal of Mammalogy, 42(4), 471–476. https://doi.org/10.2307/1377364
10.2307/1377364 Google Scholar
- Nudds, R. L., & Oswald, S. A. (2007). An interspecific test of Allen’s rule: Evolutionary implications for endothermic species. Evolution, 61(12), 2839–2848. https://doi.org/10.1111/j.1558-5646.2007.00242.x
- Olson, P. A. (2009). Pilot whales: Globicephala melas and G. macrorhynchus. In W. Perrin, B. Würsig, & J. G. M. Thewissen (Eds.), Encyclopedia of Marine Mammals ( 2nd ed., pp. 847–852). Cambridge, MA: Academic Press.
- Pabst, D. A., Rommel, S. A., & McLellan, W. A. (1999). Functional morphology of marine mammals. In J. E. Reynolds, & S. A. Rommel (Eds.), Biology of Marine Mammals (pp. 15–72). Washington DC, USA: Smithsonian Institution Press.
- Parry, D. A. (1949). The structure of whale blubber, and a discussion of its thermal properties. Journal of Cell Science, 3(9), 13–25.
- Phillips, P. K., & Heath, J. E. (1995). Dependency of surface temperature regulation on body size in terrestrial mammals. Journal of Thermal Biology, 20(3), 281–289. https://doi.org/10.1016/0306-4565(94)00061-M
- R Core Team. (2016). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from http//www.R-project.org/.
- Ralls, K., & Mesnick, S. L. (2002). Sexual dimorphism. In B. Würsig, W. Perrin, & J. G. M. Thewissen (Eds.), Encyclopedia of Marine Mammals ( 2nd ed., pp. 1071–1078). Cambridge, Massachusetts, USA: Academic Press.
- Rommel, S. A., Pabst, D. A., McLellan, W. A., Mead, J. G., & Potter, C. W. (1992). Anatomical evidence for a countercurrent heat exchanger associated with dolphin testes. Anatomical Record, 232(1), 150–156. https://doi.org/10.1002/ar.1092320117
- Royston, P. (1982). An extension of Shapiro and Wilk’s W test for normality to large samples. Applied Statistics, 31, 115–124. https://doi.org/10.2307/2347973
- Schmidt-Nielsen, K. (1997). Animal physiology, adaptation and environment. Cambridge, UK: Cambridge University Press.
- Scholander, P. F. (1955). Evolution of climatic adaptation in homeotherms. Evolution, 9, 15–26. https://doi.org/10.1111/j.1558-5646.1955.tb01510.x
- Scholander, P. F., & Schevill, W. E. (1955). Counter-current vascular heat exchange in the fins of whales. Journal of Applied Physiology, 8(3), 279–282. https://doi.org/10.1152/jappl.1955.8.3.279
- Stevenson, R. D. (1986). Allen’s rule in North American rabbits (Sylvilagus) and hares (Lepus) is an exception, not a rule. Journal of Mammalogy, 67(2), 312–316. https://doi.org/10.2307/1380884
- Symonds, M. R. E., & Tattersall, G. J. (2010). Geographical variation in bill size across bird species provide evidence for Allen’s rule. The American Naturalist, 176(2), 188–197. https://doi.org/10.1086/653666
- Thorne, L. H., Baird, R. W., Webster, D. L., Stepanuk, J. E., & Read, A. J. (2019). Predicting fisheries bycatch: A case study and field test for pilot whales in a pelagic longline fishery. Biodiversity Research, 25, 909–923. https://doi.org/10.1111/ddi.12912
10.1111/ddi.12912 Google Scholar
- Thorne, L. H., Foley, H. J., Baird, R. W., Webster, D. L., Swaim, Z. T., & Read, A. J. (2017). Movement and foraging behavior of short-finned pilot whales in the Mid-Atlantic Bight: Importance of bathymetric features and implications for management. Marine Ecology Progress Series, 584, 245–257. https://doi.org/10.3354/meps12371
- Tilkens, M. J., Wall-Scheffler, C., Weaver, T. D., & Steudal-Numbers, K. (2007). The effects of body proportions on thermoregulation: An experimental assessment of Allen’s rule. Journal of Human Evolution, 53, 286–291. https://doi.org/10.1016/j.jhevol.2007.04.005
- Torres-Romero, E. J., Morales-Castilla, I., & Olalla-Tàrraga, M. A. (2016). Bergmann’s rule in the oceans? Temperature strongly correlates with global interspecific patterns of body size in marine mammals. Global Ecology and Biogeography, 25(10), 1206–1215. https://doi.org/10.1111/geb.12476
- Warton, D. I., Duursma, R. A., Falster, D. S., & Taskinen, S. (2012). Smatr 3– An R package for estimation and inference about allometric lines. Methods in Ecology and Evolution, 3, 257–259. https://doi.org/10.1111/j.2041-210X.2011.00153.x
- Warton, D. I., & Weber, N. C. (2002). Common slope tests for bivariate errors-in-variables models. Biometrical Journal, 44(2), 161–174. https://doi.org/10.1002/1521-4036(200203)44:2<161:AID-BIMJ161>3.0.CO;2-N
- Warton, D. I., Wright, I. J., Falster, D. S., & Westoby, M. (2006). Bivariate line-fitting methods for allometry. Biological Reviews, 81(2), 259–291. https://doi.org/10.1017/S1464793106007007
- Woodward, B. L., Winn, J. P., & Fish, F. E. (2006). Morphological specializations of baleen whales associated with hydrodynamic performance and ecological niche. Journal of Morphology, 267, 1284–1294. https://doi.org/10.1002/jmor.10474
- Woolson, R. F. (1998). Wilcoxon signed rank test. In P. Armitage, & T. Colton (Eds.), Encyclopedia of Biostatistics (Vol. 6, pp. 4739–4740). Hoboken, New Jersey, USA: John Wiley & Sons.
- Worthy, G. A. J., & Edwards, E. F. (1990). Morphometric and biochemical factors affecting heat loss in a small temperate cetacean (Phocoena phocoena) and a small tropical cetacean (Stenella attenuata). Physiological and Biochemical Zoology, 63(2), 432–442. https://doi.org/10.1086/physzool.63.2.30158506
- Wright, I. J., Westoby, M., & Reich, P. B. (2002). Convergence towards higher leaf mass per area in dry and nutrient-poor habitat has different consequences for leaf life span. Journal of Ecology, 90(3), 534–543. https://doi.org/10.1046/j.1365-2745.2002.00689.x
- Yom-Tov, Y., Benjamini, Y., & Kark, S. (2002). Global warming, Bergmann’s rule and body mass – Are they related? The chukar partridge (Alectoris chukar) case. Journal of Zoology, 257, 449–455. https://doi.org/10.1017/S095283690200105X
