1932

Abstract

Baleen whales are gigantic obligate filter feeders that exploit aggregations of small-bodied prey in littoral, epipelagic, and mesopelagic ecosystems. At the extreme of maximum body size observed among mammals, baleen whales exhibit a unique combination of high overall energetic demands and low mass-specific metabolic rates. As a result, most baleen whale species have evolved filter-feeding mechanisms and foraging strategies that take advantage of seasonally abundant yet patchily and ephemerally distributed prey resources. New methodologies consisting of multi-sensor tags, active acoustic prey mapping, and hydrodynamic modeling have revolutionized our ability to study the physiology and ecology of baleen whale feeding mechanisms. Here, we review the current state of the field by exploring several hypotheses that aim to explain how baleen whales feed. Despite significant advances, major questions remain about the processes that underlie these extreme feeding mechanisms, which enabled the evolution of the largest animals of all time.

Keyword(s): baleendragfeedingfiltrationMysticetiwhale
Loading

Article metrics loading...

/content/journals/10.1146/annurev-marine-122414-033905
2017-01-03
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/marine/9/1/annurev-marine-122414-033905.html?itemId=/content/journals/10.1146/annurev-marine-122414-033905&mimeType=html&fmt=ahah

Literature Cited

  1. Acevedo-Gutiérrez A, Croll DA, Tershy BR. 2002. High feeding costs limit dive time in the largest whales. J. Exp. Biol. 205:1747–53 [Google Scholar]
  2. Alexander RM. 1998. All-time giants: the largest animals and their problems. Palaeontology 41:1231–45 [Google Scholar]
  3. Aoki K, Amano M, Mori K, Kourogi A, Kubodera T, Miyazaki N. 2012. Active hunting by deep-diving sperm whales: 3D dive profiles and maneuvers during bursts of speed. Mar. Ecol. Prog. Ser. 444:289–301 [Google Scholar]
  4. Arnold PW, Birtles RA, Sobtzick S, Matthews M, Dunstan A. 2005. Gulping behaviour in rorqual whales: underwater observations and functional interpretation. Mem. Queensl. Mus. 51:309–32 [Google Scholar]
  5. Baumgartner MF, Cole TVN, Campbell RG, Teegarden GJ, Durbin EG. 2003. Associations between North Atlantic right whales and their prey, Calanus finmarchicus, over diel and tidal time scales. Mar. Ecol. Prog. Ser. 264:155–66 [Google Scholar]
  6. Baumgartner MF, Mate BR. 2003. Summertime foraging ecology of North Atlantic right whales. Mar. Ecol. Prog. Ser. 264:123–35 [Google Scholar]
  7. Benoit-Bird KJ, Battaile BC, Nordstrom CA, Trites AW. 2013. Foraging behavior of northern fur seals closely matches the hierarchical patch scales of prey. Mar. Ecol. Prog. Ser. 479:283–302 [Google Scholar]
  8. Bloodworth B, Marshall CD. 2005. Feeding kinematics of Kogia and Tursiops (Odontoceti: Cetacea): characterization of suction and ram feeding. J. Exp. Biol. 208:3721–30 [Google Scholar]
  9. Brodie PF. 1975. Cetacean energetics, an overview of intraspecific size variation. Ecology 56:152–61 [Google Scholar]
  10. Charnov EL. 1976. Optimal foraging, the marginal value theorem. Theor. Popul. Biol. 9:129–36 [Google Scholar]
  11. Croll DA, Marinovic B, Benson S, Chavez FP, Black N. et al. 2005. From wind to whales: trophic links in a coastal upwelling system. Mar. Ecol. Prog. Ser. 289:117–30 [Google Scholar]
  12. Demere TA, McGowen MR, Berta A, Gatesy J. 2008. Morphological and molecular evidence for a stepwise evolutionary transition from teeth to baleen in mysticete whales. Syst. Biol. 57:15–37 [Google Scholar]
  13. Domenici P. 2001. The scaling of locomotor performance in predator-prey encounters: from fish to killer whales. Comp. Biochem. Physiol. A 131:169–82 [Google Scholar]
  14. Domenici P. 2002. The visually mediated escape response in fish: predicting prey responsiveness and the locomotor behaviour of predators and prey. Mar. Freshw. Behav. Physiol. 35:87–110 [Google Scholar]
  15. Domenici P, Batty RS, Simila T, Ogam E. 2000. Killer whales (Orcinus orca) feeding on schooling herring (Clupea harengus) using underwater tail-slaps: kinematic analyses of field observations. J. Exp. Biol. 203:283–94 [Google Scholar]
  16. Durban J, Fearnbach H, Barrett-Lennard L, Perryman W, Leroi D. 2015. Photogrammetry of killer whales using a small hexacopter launched at sea. J. Unmanned Veh. Syst. 3:131–35 [Google Scholar]
  17. Ekdale EG, Deméré TA, Berta A. 2015. Vascularization of the gray whale palate (Cetacea, Mysticeti, Eschrichtius robustus): soft tissue evidence for an alveolar source of blood to baleen. Anat. Rec. 298:691–702 [Google Scholar]
  18. Eschricht DF, Reinhardt JT. 1866. On the Greenland right whale (Balaena mysticetus Linn.) with especial reference to its geographical distribution and migrations in times past and present, and to its external and internal characteristics. Recent Memoirs on the Cetacea by Professors Eschricht, Reinhardt, and Lilljeborg WH Flower 1–150 London: Ray Soc. [Google Scholar]
  19. Fish FE, Goetz KT, Rugh DJ, Brattström LV. 2013. Hydrodynamic patterns associated with echelon formation swimming by feeding bowhead whales (Balaena mysticetus). Mar. Mamm. Sci. 29:E498–507 [Google Scholar]
  20. Fitzgerald EMG. 2006. A bizarre new toothed mysticete (Cetacea) from Australia and the early evolution of baleen whales. Proc. R. Soc. Lond. B 273:2955–63 [Google Scholar]
  21. Fitzgerald EMG. 2012. Archaeocete-like jaws in a baleen whale. Biol. Lett. 8:94–96 [Google Scholar]
  22. Ford TJ, Werth AJ, George JC. 2013. An intraoral thermoregulatory organ in the bowhead whale (Balaena mysticetus), the corpus cavernosum maxillaris. Anat. Rec. 296:701–8 [Google Scholar]
  23. Fordyce RE, Marx FG. 2013. The pygmy right whale Caperea marginata: the last of the cetotheres. Proc. R. Soc. Lond. B 280:20122645 [Google Scholar]
  24. Friedlaender AS, Goldbogen JA, Nowacek DP, Read AJ, Johnston D, Gales N. 2014. Feeding rates and under-ice foraging strategies of the smallest lunge filter feeder, the Antarctic minke whale (Balaenoptera bonaerensis). J. Exp. Biol. 217:2851–54 [Google Scholar]
  25. Friedlaender AS, Hazen EL, Goldbogen JA, Stimpert AK, Calambokidis J, Southall BL. 2016. Prey-mediated behavioral responses of feeding blue whales in controlled sound exposure experiments. Ecol. Appl. 26:1075–85 [Google Scholar]
  26. Friedlaender AS, Hazen EL, Nowacek DP, Halpin PN, Ware C. et al. 2009. Diel changes in humpback whale Megaptera novaeangliae feeding behavior in response to sand lance Ammodytes spp. behavior and distribution. Mar. Ecol. Prog. Ser. 395:91–100 [Google Scholar]
  27. Friedlaender AS, Tyson RB, Stimpert AK, Read AJ, Nowacek DP. 2013. Extreme diel variation in the feeding behavior of humpback whales along the western Antarctic Peninsula during autumn. Mar. Ecol. Prog. Ser. 494:281–89 [Google Scholar]
  28. Fudge DS, Szewciw LJ, Schwalb AN. 2009. Morphology and development of blue whale baleen: an annotated translation of Tycho Tullberg's classic 1883 paper. Aquat. Mamm. 35:226–52 [Google Scholar]
  29. Goldbogen JA. 2010. The ultimate mouthful: lunge feeding in rorqual whales. Am. Sci. 98:124–31 [Google Scholar]
  30. Goldbogen JA, Calambokidis J, Croll DA, Harvey JT, Newton KM. et al. 2008. Foraging behavior of humpback whales: kinematic and respiratory patterns suggest a high cost for a lunge. J. Exp. Biol. 211:3712–19 [Google Scholar]
  31. Goldbogen JA, Calambokidis J, Croll DA, McKenna MF, Potvin J. et al. 2012. Scaling of lunge feeding performance in rorqual whales: mass-specific energy expenditure increases with body size and progressively limits diving capacity. Funct. Ecol. 26:216–26 [Google Scholar]
  32. Goldbogen JA, Calambokidis J, Friedlaender AS, Francis J, DeRuiter SL. et al. 2013a. Underwater acrobatics by the world's largest predator: 360 degrees rolling manoeuvres by lunge-feeding blue whales. Biol. Lett. 9:20120986 [Google Scholar]
  33. Goldbogen JA, Calambokidis J, Oleson E, Potvin J, Pyenson ND. et al. 2011. Mechanics, hydrodynamics and energetics of blue whale lunge feeding: efficiency dependence on krill density. J. Exp. Biol. 214:131–46 [Google Scholar]
  34. Goldbogen JA, Calambokidis J, Shadwick RE, Oleson EM, McDonald MA, Hildebrand JA. 2006. Kinematics of foraging dives and lunge-feeding in fin whales. J. Exp. Biol. 209:1231–44 [Google Scholar]
  35. Goldbogen JA, Friedlaender AS, Calambokidis J, McKenna MF, Simon M, Nowacek DP. 2013b. Integrative approaches to the study of baleen whale diving behavior, feeding performance, and foraging ecology. BioScience 63:90–100 [Google Scholar]
  36. Goldbogen JA, Hazen EL, Friedlaender AS, Calambokidis J, DeRuiter SL. et al. 2015a. Prey density and distribution drive the three-dimensional foraging strategies of the largest filter feeder. Funct. Ecol. 29:951–61 [Google Scholar]
  37. Goldbogen JA, Meir JU. 2014. The device that revolutionized marine organismal biology. J. Exp. Biol. 217:167–68 [Google Scholar]
  38. Goldbogen JA, Potvin J, Shadwick RE. 2010. Skull and buccal cavity allometry increase mass-specific engulfment capacity in fin whales. Proc. R. Soc. B 277:861–68 [Google Scholar]
  39. Goldbogen JA, Pyenson ND, Shadwick RE. 2007. Big gulps require high drag for fin whale lunge feeding. Mar. Ecol. Prog. Ser. 349:289–301 [Google Scholar]
  40. Goldbogen JA, Shadwick RE, Lillie MA, Piscitelli MA, Potvin J. et al. 2015b. Using morphology to infer physiology: case studies on rorqual whales (Balaenopteridae). Can. J. Zool. 93:687–700 [Google Scholar]
  41. Hazen EL, Friedlaender AS, Goldbogen JA. 2015. Blue whales (Balaenoptera musculus) optimize foraging efficiency by balancing oxygen use and energy gain as a function of prey density. Sci. Adv. 1:e1500469 [Google Scholar]
  42. Hazen EL, Friedlaender AS, Thompson MA, Ware CR, Weinrich MT. et al. 2009. Fine-scale prey aggregations and foraging ecology of humpback whales Megaptera novaeangliae. Mar. Ecol. Prog. Ser. 395:75–89 [Google Scholar]
  43. Huveneers C, Holman D, Robbins R, Fox A, Endler JA, Taylor AH. 2015. White sharks exploit the sun during predatory approaches. Am. Nat. 185:562–70 [Google Scholar]
  44. Johnson KR, Nelson CH. 1984. Side-scan sonar assessment of gray whale feeding in the Bering Sea. Science 225:1150–52 [Google Scholar]
  45. Johnson M, Tyack PL. 2003. A digital acoustic recording tag for measuring the response of wild marine mammals to sound. IEEE J. Ocean. Eng. 28:3–12 [Google Scholar]
  46. Kane EA, Marshall CD. 2009. Comparative feeding kinematics and performance of odontocetes: belugas, Pacific white-sided dolphins and long-finned pilot whales. J. Exp. Biol. 212:3939–50 [Google Scholar]
  47. Koolstra JH, van Eijden T. 2004. Functional significance of the coupling between head and jaw movements. J. Biomech. 37:1387–92 [Google Scholar]
  48. Krogh A. 1929. The progress of physiology. Am. J. Physiol. 90:243–51 [Google Scholar]
  49. Laidre KL, Heide-Jørgensen MP, Nielsen TG. 2007. Role of the bowhead whale as a predator in West Greenland. Mar. Ecol. Prog. Ser. 346:285–97 [Google Scholar]
  50. Lambertsen RH. 1983. Internal mechanism of rorqual feeding. J. Mamm. 64:76–88 [Google Scholar]
  51. Lambertsen RH, Rasmussen KJ, Lancaster WC, Hintz RJ. 2005. Functional morphology of the mouth of the bowhead whale and its implications for conservation. J. Mamm. 86:342–52 [Google Scholar]
  52. Lambertsen RH, Ulrich N, Straley J. 1995. Frontomandibular stay of Balaenopteridae: a mechanism for momentum recapture during feeding. J. Mamm. 76:877–99 [Google Scholar]
  53. Lindberg DR, Pyenson ND, Estes JA, Demaster DP, Doak DF. et al. 2006. Evolutionary patterns in Cetacea: fishing up prey size through deep time. Whales, Whaling, and Ocean Ecosystems JA Estes, DP DeMaster, DF Doak, TM Williams, RL Brownell 67–81 Berkeley: Univ. Calif. Press [Google Scholar]
  54. Lockyer CH. 1976. Body weights of some species of large whales. ICES J. Mar. Sci. 36:259–73 [Google Scholar]
  55. Lockyer CH. 1981. Growth and energy budgets of large baleen whales from the Southern Hemisphere. Mammals in the Seas 3 General Papers and Large Cetaceans JG Clark 379–487 Rome: Food Agric. Organ. UN [Google Scholar]
  56. Madsen PT, de Soto NA, Arranz P, Johnson M. 2013. Echolocation in Blainville's beaked whales (Mesoplodon densirostris). J. Comp. Physiol. A 199:451–69 [Google Scholar]
  57. Miller PJO, Johnson MP, Tyack PL. 2004. Sperm whale behaviour indicates the use of echolocation click buzzes ‘creaks’ in prey capture. Proc. R. Soc. Lond. B 271:2239–47 [Google Scholar]
  58. Mori Y. 1998. Optimal choice of foraging depth in divers. J. Zool. 245:279–83 [Google Scholar]
  59. Mori Y. 2002. Optimal diving behaviour for foraging in relation to body size. J. Evol. Biol. 15:269–76 [Google Scholar]
  60. Motta PJ, Maslanka M, Hueter RE, Davis RL, de la Parra R. et al. 2010. Feeding anatomy, filter-feeding rate, and diet of whale sharks Rhincodon typus during surface ram filter feeding off the Yucatan Peninsula, Mexico. Zoology 113:199–212 [Google Scholar]
  61. Nerini M. 1984. A review of gray whale feeding ecology. The Gray Whale: Eschrichtius robustus ML Jones, SL Swartz, S Leatherwood 423–50 Orlando, FL: Academic [Google Scholar]
  62. Nousek-McGregor AE. 2010. The cost of locomotion in North Atlantic right whales Eubalaena glacialis PhD Thesis, Duke Univ., Durham, NC
  63. O'Brien DP. 1987. Description of escape responses of krill (Crustacea, Euphausiacea), with particular reference to swarming behavior and the size and proximity of the predator. J. Crustac. Biol. 7:449–57 [Google Scholar]
  64. Orton LS, Brodie PF. 1987. Engulfing mechanics of fin whales. Can. J. Zool. 65:2898–907 [Google Scholar]
  65. Paig-Tran EM, Bizzarro JJ, Strother JA, Summers AP. 2011. Bottles as models: predicting the effects of varying swimming speed and morphology on size selectivity and filtering efficiency in fishes. J. Exp. Biol. 214:1643–54 [Google Scholar]
  66. Paig-Tran E, Kleinteich T, Summers AP. 2013. The filter pads and filtration mechanisms of the devil rays: variation at macro and microscopic scales. J. Morphol. 274:1026–43 [Google Scholar]
  67. Parks SE, Warren JD, Stamieszkin K, Mayo CA, Wiley D. 2012. Dangerous dining: surface foraging of North Atlantic right whales increases risk of vessel collisions. Biol. Lett. 8:57–60 [Google Scholar]
  68. Pivorunas A. 1977. Fibro-cartilage skeleton and related structures of ventral pouch of balaenopterid whales. J. Morphol. 151:299–313 [Google Scholar]
  69. Pivorunas A. 1979. Feeding mechanisms of baleen whales. Am. Sci. 67:432–40 [Google Scholar]
  70. Potvin J, Goldbogen JA, Shadwick RE. 2009. Passive versus active engulfment: verdict from trajectory simulations of lunge-feeding fin whales Balaenoptera physalus. J. R. Soc. Interface 6:1005–25 [Google Scholar]
  71. Potvin J, Goldbogen JA, Shadwick RE. 2010. Scaling of lunge feeding in rorqual whales: an integrated model of engulfment duration. J. Theor. Biol. 267:437–53 [Google Scholar]
  72. Potvin J, Goldbogen JA, Shadwick RE. 2012. Metabolic expenditures of lunge feeding rorquals across scale: implications for the evolution of filter feeding and the limits to maximum body size. PLOS ONE 7:e44854 [Google Scholar]
  73. Pyenson ND, Goldbogen JA, Shadwick RE. 2013. Mandible allometry in extant and fossil Balaenopteridae (Cetacea: Mammalia): the largest vertebrate skeletal element and its role in rorqual lunge feeding. Biol. J. Linn. Soc. 108:586–99 [Google Scholar]
  74. Pyenson ND, Goldbogen JA, Vogl AW, Szathmary G, Drake RL, Shadwick RE. 2012. Discovery of a sensory organ that coordinates lunge feeding in rorqual whales. Nature 485:498–501 [Google Scholar]
  75. Pyenson ND, Lindberg DR. 2011. What happened to gray whales during the Pleistocene? The ecological impact of sea-level change on benthic feeding areas in the North Pacific Ocean. PLOS ONE 6:e21295 [Google Scholar]
  76. Pyke GH. 1984. Optimal foraging theory: a critical review. Annu. Rev. Ecol. Syst. 15:523–75 [Google Scholar]
  77. Ray GC, Schevill WE. 1974. Feeding of a captive gray whale, Eschrichtius robustus. Mar. Fish. Rev. 36:31–38 [Google Scholar]
  78. Rubenstein DI, Koehl MAR. 1977. Mechanisms of filter feeding: some theoretical considerations. Am. Nat. 111:981–94 [Google Scholar]
  79. Sanderson SL, Cheer AY, Goodrich JS, Graziano JD, Callan WT. 2001. Crossflow filtration in suspension-feeding fishes. Nature 412:439–41 [Google Scholar]
  80. Sanderson SL, Roberts E, Lineburg J, Brooks H. 2016. Fish mouths as engineering structures for vortical cross-step filtration. Nat. Commun. 7:11092 [Google Scholar]
  81. Shadwick RE, Goldbogen JA, Potvin J, Pyenson ND, Vogl AW. 2013. Novel muscle and connective tissue design enables high extensibility and controls engulfment volume in lunge-feeding rorqual whales. J. Exp. Biol. 216:2691–701 [Google Scholar]
  82. Simon M, Johnson M, Madsen PT. 2012. Keeping momentum with a mouthful of water: behavior and kinematics of humpback whale lunge feeding. J. Exp. Biol. 215:3786–98 [Google Scholar]
  83. Simon M, Johnson M, Tyack P, Madsen PT. 2009. Behaviour and kinematics of continuous ram filtration in bowhead whales (Balaena mysticetus). Proc. R. Soc. B 276:3819–28 [Google Scholar]
  84. Smith JM. 1978. Optimization theory in evolution. Annu. Rev. Ecol. Syst. 9:31–56 [Google Scholar]
  85. Somero GN. 2000. Unity in diversity: a perspective on the methods, contributions, and future of comparative physiology. Annu. Rev. Physiol. 62:927–37 [Google Scholar]
  86. Szewciw LJ, de Kerckhove DG, Grime GW, Fudge DS. 2010. Calcification provides mechanical reinforcement to whale baleen α-keratin. Proc. R. Soc. B 277:2597–605 [Google Scholar]
  87. Webb PW, De Buffrénil V. 1990. Locomotion in the biology of large aquatic vertebrates. Trans. Am. Fish. Soc. 119:629–41 [Google Scholar]
  88. Werth AJ. 2000. Feeding in marine mammals. Feeding: Form, Function and Evolution in Tetrapod Vertebrates K Schwenk 475–514 New York: Academic [Google Scholar]
  89. Werth AJ. 2001. How do mysticetes remove prey trapped in baleen?. Bull. Mus. Comp. Zool. 156:189–203 [Google Scholar]
  90. Werth AJ. 2004. Models of hydrodynamic flow in the bowhead whale filter feeding apparatus. J. Exp. Biol. 207:3569–80 [Google Scholar]
  91. Werth AJ. 2007. Adaptations of the cetacean hyolingual apparatus for aquatic feeding and thermoregulation. Anat. Rec. 290:546–68 [Google Scholar]
  92. Werth AJ. 2011. Flow-dependent porosity of baleen. Integr. Comp. Biol. 51:Suppl. 1e265 (Abstr.) [Google Scholar]
  93. Werth AJ. 2012. Hydrodynamic and sensory factors governing response of copepods to simulated predation by balaenid whales. Int. J. Ecol. 208913:1–13 [Google Scholar]
  94. Werth AJ, Potvin J. 2016. Baleen hydrodynamics and morphology of cross-flow filtration in balaenid whale suspension feeding. PLOS ONE 11:e0150106 [Google Scholar]
  95. Werth AJ, Straley JM, Shadwick RE. 2016. Baleen wear reveals intraoral water flow patterns of mysticete filter feeding. J. Morphol. 277:453–71 [Google Scholar]
  96. Wiedenmann J, Cresswell KA, Goldbogen J, Potvin J, Mangel M. 2011. Exploring the effects of reductions in krill biomass in the Southern Ocean on blue whales using a state-dependent foraging model. Ecol. Model. 222:3366–79 [Google Scholar]
  97. Wiley D, Ware C, Bocconcelli A, Cholewiak DM, Friedlaender AS. et al. 2011. Underwater components of humpback whale bubble-net feeding behaviour. Behaviour 148:575–602 [Google Scholar]
  98. Williams R, Vikingsson GA, Gislason A, Lockyer C, New L. et al. 2013. Evidence for density-dependent changes in body condition and pregnancy rate of North Atlantic fin whales over four decades of varying environmental conditions. ICES J. Mar. Sci. 70:1273–80 [Google Scholar]
  99. Williams TM. 1999. The evolution of cost efficient swimming in marine mammals: limits to energetic optimization. Philos. Trans. R. Soc. Lond. B 354:193–201 [Google Scholar]
  100. Williams TM. 2001. Intermittent swimming by mammals: a strategy for increasing energetic efficiency during diving. Am. Zool. 41:166–76 [Google Scholar]
  101. Williams TM. 2006. Physiological and ecological consequences of extreme body size in whales. Whales, Whaling, and Ocean Ecosystems JA Estes, DP DeMaster, DF Doak, TM Williams, RL Brownell 191–201 Berkeley: Univ. Calif. Press [Google Scholar]
  102. Williams TM, Haun J, Davis RW, Fuiman LA, Kohin S. 2001. A killer appetite: metabolic consequences of carnivory in marine mammals. Comp. Biochem. Physiol. A 129:785–96 [Google Scholar]
  103. Williamson G. 1973. Counting and measuring baleen and grooves of whales. Sci. Rep. Whales Res. Inst. 25:279–92 [Google Scholar]
  104. Woodward BL, Winn JP. 2006. Apparent lateralized behavior in gray whales feeding off the central British Columbia coast. Mar. Mamm. Sci. 22:64–73 [Google Scholar]
  105. Young S, Deméré TA, Ekdale EG, Berta A, Zellmer N. 2015. Morphometrics and structure of complete baleen racks in gray whales (Eschrichtius robustus) from the eastern North Pacific Ocean. Anat. Rec. 298:703–19 [Google Scholar]
/content/journals/10.1146/annurev-marine-122414-033905
Loading
/content/journals/10.1146/annurev-marine-122414-033905
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error