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Baleen turnover and gut transit in mysticete whales and its environmental implications

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Abstract

Baleen, a unique oral α-keratin, has flat cortical layers enclosing hollow horn tubules. Baleen grows continuously to replace erosive loss from feeding-related wear. This is essential for maintaining efficient filtration over a whale’s long life history. Baleen fragments are seen in stomach contents and feces. We focused on fin (Balaenoptera physalus) and bowhead whales (Balaena mysticetus), but examined eleven mysticete species. Histological features including variably sized tubules plus differential growth along plate axes (growing faster along the medial fringed edge) and between plates of a rack (central plates growing faster than others) relate to baleen strength and flexibility. Sheet-like cortical layers provide strength and probably hinder erosive shedding, whereas medullary (tubular/intertubular) keratin provides flexibility and likely promotes shedding. To calculate amounts of grown/lost baleen, we considered both erosive wear and basal growth, recognizing that each plate represents several years of growth. We estimate average annual loss of 70–100,000 cm2 (20–40,000 cm3) of baleen in balaenids and 25–50,000 cm2 (7–14,000 cm3) in balaenopterids. Baleen growth rates depend on age, size, and other life history parameters; the most reliable calculations come from morphometric data with plate dimensions measured along full racks. We argue that baleen turnover has been under-rated and baleen growth rates underestimated in the published literature. Baleen turnover maintains filter integrity/porosity, while gut passage possibly clears gastrointestinal tracts of endoparasites. Large volumes of shed keratin hold potential ecological consequences by providing food for microbial decomposers and detritivores throughout ocean ecosystems, especially in polar regions where most mysticete feeding occurs.

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All data generated or analyzed for this study are included in the paper or available from the corresponding author upon reasonable request.

References

  • Aguilar A, Giménez J, Gómez-Campos E, Cardona L, Borrell A (2014) δ15N value does not reflect fasting in mysticetes. PLoS ONE 9:e92288

    PubMed  PubMed Central  Google Scholar 

  • Albert TF (1981) Some thoughts regarding the possible effect of oil contamination on the bowhead whale, Balaena mysticetus. In: Albert T (ed) Tissue structural studies and other investigations on the biology of endangered whales in the Beaufort sea. Bureau of Land Management, Anchorage, pp 945–953

    Google Scholar 

  • Best PB, Schell DM (1996) Stable isotopes in southern right whale (Eubalaena australis) baleen as indicators of seasonal movements, feeding and growth. Mar Biol 124:483–494

    Google Scholar 

  • Busquets-Vass G, Newsome SD, Calambokidis J, Serra-Valente G, Jacobsen JK, Aquiñiga-Garcia S, Gendron D (2017) Estimating blue whale skin isotopic incorporation rates and baleen growth rates: implications for assessing diet and movement patterns in mysticetes. PLoS ONE 12:e0177880

    PubMed  PubMed Central  Google Scholar 

  • Caraveo-Patiño J, Hobson KA, Soto LA (2007) Feeding ecology of gray whales inferred from stable-carbon and nitrogen isotopic analysis of baleen plates. Hydrobiol 586:17–25

    Google Scholar 

  • Caraveo-Patiño J, Soto LA (2005) Stable carbon isotope ratios for the gray whale (Eschrichtius robustus) in the breeding grounds of Baja California Sur, Mexico. Hydrobiology 539:99–107

    Google Scholar 

  • Croll DA, Acevedo-Gutierez A, Tershy BR, Urban-Ramirez K (2001) The diving behavior of blue and fin whales: is dive durations shorter than expected based on oxygen stores? Compd Biochem Physiol 129:797–809

    CAS  Google Scholar 

  • Eisenmann P, Fry B, Holyoake C, Coughran D, Nicol S, Nash SB (2016) Isotopic evidence of a wide spectrum of feeding strategies in Southern Hemisphere humpback whale baleen records. PLoS ONE 11:e0156698

    PubMed  PubMed Central  Google Scholar 

  • Forgács G, Alinezhad S, Mirabdollah A, Feuk-Lagerstad E, Horváth IS (2011) Biological treatment of chicken feather waste for improved biogas production. J Environ Sci 23:1747–1753

    Google Scholar 

  • Fudge DS, Szewciw LJ, Schwalb AN (2009) Morphology and development of blue whale baleen: an annotated translation of Tycho Tullberg’s classic 1883 paper. Aq Mamm 35:226–252

    Google Scholar 

  • George JC, Stimmelmayr R, Suydam R, Usip S, Givens G, Sformo T, Thewissen JGM (2016) Severe bone loss as part of the life history strategy of bowhead whales. PLoS ONE 11:e0156753

    PubMed  PubMed Central  Google Scholar 

  • Geraci J, St. Aubin DJ (1987) Effects of parasites on marine mammals. Int J Parasit 17:407–414

    CAS  Google Scholar 

  • Glander K (1994) Nonhuman primate self-medication with wild plant foods. In: Etkin NL (ed) Eating on the wild side. Univ Arizona Press, Tucson, pp 227–239

    Google Scholar 

  • Goldbogen JA, Cade D, Calambokidis J, Friedlaender AS, Potvin J, Segre PS, Werth AJ (2017) How baleen whales feed: the biomechanics of engulfment and filtration. Ann Rev Mar Sci 9:367–386

    CAS  PubMed  Google Scholar 

  • Greenberg DA, Fudge DS (2012) Regulation of hard alpha-keratin mechanics via control of intermediate filament hydration: matrix squeeze revisited. Proc R Soc B 280:e2158

    Google Scholar 

  • Hart BL (2011) Behavioral defences in animals against pathogens and parasites: parallels with the pillars of medicine in humans. Phil Trans R Soc B 366:3406–3417

    PubMed  Google Scholar 

  • Hayashi S, Miyamoto I, Takeda K (1991) Measurement of human hair growth by optical microscopy and image analysis. Brit J Dermatol 125:123–129

    CAS  Google Scholar 

  • Heckmann RA, Jensen LA, Warnock RG, Coleman B (1987) Parasites of the bowhead whale, Balaena mysticetus. Great Basin Nat 47:355–372

    Google Scholar 

  • Hermosilla C, Silva LMR, Prieto L, Kleinertz S, Taubert A, Silva MA (2015) Ecto- and endoparasites of large whales: overcoming difficulties in obtaining appropriate samples by non- and minimally-invasive methods. Int J Parasit 4:414–420

    Google Scholar 

  • Huffman MA (1997) Current evidence for self-medication in primates: a multidisciplinary perspective. Yrbk Phys Anthr 40:171–200

    Google Scholar 

  • Huffman MA (2008) Animal self-medication and ethno-medicine: exploration and exploitation of the medicinal properties of plants. Proc Nutr Soc 62:371–381

    Google Scholar 

  • Hughes-Hanks JM, Rickard LG, Panuska C, Saucier JR, O’Hara TM, Dehn L, Rolland RM (2005) Prevalence of Cryptosporidium spp and Giardia spp in five marine mammal species. J Parasitol 91:1225–1228

    CAS  PubMed  Google Scholar 

  • Hunt KE, Moore MJ, Rolland RM, Kellar NM, Hall AJ, Kershaw J, Raverty SA, Davis CE, Yeates LC, Fauquier DA, Rowles TK, Kraus SD (2013) Overcoming the challenges of studying conservation physiology in large whales: a review of available methods. Conserv Physiol 1:cot006

    PubMed  PubMed Central  Google Scholar 

  • Jensen MM, Saladrigas AH, Goldbogen JA (2017) Comparative three-dimensional morphology of baleen: cross-sectional profiles and volume measurements using CT images. Anat Rec 300:1942–1952

    Google Scholar 

  • Kaschner K, Tittensor DP, Ready J, Gerrodette T, Worm B (2011) Current and future patterns of global marine mammal biodiversity. PLoS ONE 6:e19653

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lavery TJ, Roudnew B, Seymour J, Mitchell JG, Smetacek V, Nicol S (2014) Whales sustain fisheries: blue whales stimulate primary production in the Southern Ocean. Mar Mamm Sci 30:888–904

    CAS  Google Scholar 

  • Lempereur L, Delobelle M, Doom M, Haelters J (2017) Crassicauda boopis in a fin whale (Balaenoptera physalus) ship-struck in the eastern North Atlantic Ocean. Parasitol Open 3:e9

    Google Scholar 

  • Lubetkin SC, Zeh JE, Rosa C, George JC (2008) Age estimation for young bowhead whales (Balaena mysticetus) using annual baleen growth increments. Can J Zool 86:525–538

    Google Scholar 

  • Lysiak NSJ, Trumble SJ, Knowlton AR, Moore MJ (2018) Fishing gear entanglement on a North Atlantic right whale (Eubalaena glacialis) using stable isotopes, steroid and thyroid hormones in baleen. Front Mar Sci 5:e168

    Google Scholar 

  • Magera AM, Flemming JEM, Kaschner K, Christensen LB, Lotze HK (2013) Recovery trends in marine mammal populations. PLoS ONE 8:e77908

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mathison GE (1964) The microbiological decomposition of keratin. Ann Soc Belge Med Trop 44:767–792

    CAS  PubMed  Google Scholar 

  • Migaki G, Heckmann RA, Albert TA (1982) Gastric nodules caused by “Anisakis type” larvae in the bowhead whale (Balaena mysticetus). J Wildl Dis 18:353–357

    CAS  PubMed  Google Scholar 

  • Nerini M (1984) A review of gray whale feeding ecology. In: Jones ML, Swartz SL, Leatherwood S (eds) The gray whale Eschrichtius robustus. Academic Press, Orlando, pp 423–450

    Google Scholar 

  • Newell GW, Elvehjem CA (1947) Nutritive value of keratin. J Nutr 33:673–683

    CAS  PubMed  Google Scholar 

  • Noval JJ, Nickerson WJ (1959) Decomposition of native keratin by Streptomyces fradiae. J Bacteriol 77:251–263

    CAS  PubMed  PubMed Central  Google Scholar 

  • Onifade AA, Al-Sane NA, Al-Musallam AA, Al-Zarban S (1998) A review: Potentials for biotechnological applications of keratin-degrading microorganisms and their enzymes for nutritional improvement of keratins as livestock feed. Biores Technol 66:1–11

    CAS  Google Scholar 

  • Pinto SJD, Shadwick RE (2013) Material and structural properties of fin whale (Balaenoptera physalus) zwischensubstanz. J Morph 274:947–955

    PubMed  Google Scholar 

  • Pivorunas A (1976) A mathematical consideration of the function of baleen plates and their fringes. Sci Rep Whales Res Inst 28:37–55

    Google Scholar 

  • Pomerleau C, Matthews CJD, Gobeil C, Stern GA, Ferguson SH, Macdonald RW (2018) Mercury and stable isotope cycles in baleen plates are consistent with year-round feeding in two bowhead whale (Balaena mysticetus) populations. Polar Biol 41:1–13

    Google Scholar 

  • Potvin J, Werth AJ (2017) Oral cavity hydrodynamics and drag production in balaenid whale suspension feeding. PLoS ONE 12:e5220

    Google Scholar 

  • Randall VA, Ebling FJG (1991) Seasonal changes in human hair growth. Brit J Dermatol 124:146–151

    CAS  Google Scholar 

  • Rice DW, Wolman AA (1971) The life history and ecology of the gray whale (Eschrichtius robustus). Am Soc Mamm 3:1–142

    Google Scholar 

  • Roman J, Estes JA, Morisette L, Smith C, Costa D, McCarthy J, Nation JB, Nicol S, Pershing A, Smetacek V (2014) Whales as ecosystem engineers. Front Ecol Envir 12:377–385

    Google Scholar 

  • Roman J, McCarthy J (2010) The whale pump: marine mammals enhance primary productivity in a coastal basin. PLoS ONE 5:e13255

    PubMed  PubMed Central  Google Scholar 

  • Ruud JT (1940) The surface structure of the baleen plates and a possible clue to age in whales. Hval Skrift 23:1–24

    Google Scholar 

  • Schell DM, Saupe SM, Haubenstock N (1989) Bowhead whale (Balaena mysticetus) growth and feeding as estimated by δ13C techniques. Mar Biol 103:433–443

    Google Scholar 

  • Sheffield G, Stimmelmayr R, Rausch R, George JC (2016) Anisakis spp. infection in legally harvested BCB Bowhead whales (Balaena mysticetus): Preliminary data from stomach content analysis and field post-mortem examinations. UAF Alaska Sea Grant Report to the Scientific Committee of the International Whaling Commission, Nome, Alaska, pp 1–9

  • Smith CR, Glover AG, Treude T, Higgs ND, Amon DJ (2014) Whale-fall ecosystems: recent insights into ecology, paleoecology, and evolution. Ann Rev Mar Sci 7:571–596

    PubMed  Google Scholar 

  • Sueda KLC, Hart BL, Cliff KD (2008) Characterization of plant eating in dogs. Appl Anim Behav Sci 111:120–132

    Google Scholar 

  • Szewciw LJ, de Kerkhove DG, Grime GW, Fudge DS (2010) Calcification provides mechanical reinforcement to whale baleen alpha keratin. Proc Roy Soc B 277:2597–2605

    CAS  Google Scholar 

  • Thewissen JGM, Hieronymus TL, George JC, Suydam R, Stimmelmayr R, McBurney D (2017) Evolutionary aspects of the development of teeth and baleen in the bowhead whale. J Anat 230:549–566

    CAS  PubMed  PubMed Central  Google Scholar 

  • Werth AJ (2000) Marine mammals. In: Schwenk K (ed) Feeding: Form, Function, and Evolution in Tetrapod Vertebrates. Academic Press, New York, pp 475–514

    Google Scholar 

  • Werth AJ (2001) How do mysticetes remove prey trapped in baleen? Bull Mus Comp Zool 156:189–203

    Google Scholar 

  • Werth AJ (2004) Models of hydrodynamic flow in the bowhead whale filter feeding apparatus. J Exp Biol 207:3569–3580

    PubMed  Google Scholar 

  • Werth AJ (2013) Flow-dependent porosity and other biomechanical properties of mysticete baleen. J Exp Biol 216:1152–1159

    PubMed  Google Scholar 

  • Werth AJ (2017) Baleen. In: Würsig B, Thewissen JGM, Kovacs K (eds) Encyclopedia of marine mammals, 3rd edn. Academic Press, San Diego, pp 60–61

    Google Scholar 

  • Werth AJ (2018) Variable porosity of throughput and tangential filtration in biological and 3D printed systems. In: Petrova V (ed) Advances in engineering research vol. 28 porosity—properties and measurement. Nova Science, Hauppauge NY, pp 1–58

    Google Scholar 

  • Werth AJ, Harriss RW, Rosario MV, George JC, Sformo TL (2016a) Hydration affects the physical and mechanical properties of baleen tissue. Roy Soc Open Sci 3:160591

    Google Scholar 

  • Werth AJ, Potvin J (2016) Baleen hydrodynamics and morphology of cross-flow filtration in balaenid whale suspension feeding. PLoS ONE 11:e0150106

    PubMed  PubMed Central  Google Scholar 

  • Werth AJ, Potvin J, Shadwick RE, Jensen MM, Cade DE, Goldbogen JA (2018a) Filtration area scaling and evolution in mysticetes: trophic niche partitioning and the curious cases of sei and pygmy right whales. Biol J Linn Soc 125:264–279

    Google Scholar 

  • Werth AJ, Rita D, Rosario MV, Moore MJ, Sformo TL (2018b) How do baleen whales stow their filter: a comparative biological analysis. J Exp Biol 221:e189233

    Google Scholar 

  • Werth AJ, Straley JM, Shadwick RE (2016b) Baleen wear reveals intraoral water flow patterns of mysticete filter feeding. J Morph 277:453–471

    PubMed  Google Scholar 

  • Williamson GR (1973) Counting and measuring baleen and ventral grooves of whales. Sci Rep Whales Res Inst 24:279–292

    Google Scholar 

  • Yaemsiri S, Hou N, Slining M, He K (2010) Growth rate of human fingernails and toenails in healthy American young adults. J Eur Acad Dermatol Venereol 24:420–423

    CAS  PubMed  Google Scholar 

  • Zenitani R, Kato H (2010) The growth of baleen plates in Antarctic minke whales, with special reference to the V-shape notch appearing at outer edge of plates. Jap Soc Sci Fish 76:870–876

    Google Scholar 

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Acknowledgements

We dedicate this work in memory of Bob Elsner, whose pioneering work on the physiology of Arctic wildlife has inspired and informed countless researchers. We thank the Alaska Eskimo Whaling Commission and Barrow Whaling Captain’s Association, especially Billy Adams, Harry Brower, Jr., and Qaiyaan Harcharek for providing bowhead baleen; specimens were collected under NMFS Permit No. 21386 issued to the North Slope Borough Department of Wildlife Management, Utqiaġvik, Alaska. Tom Pitchford, Bill McLellan, Kristján Loftsson, and Erin Fougeres gave access to other specimens. We thank Jan Straley and anonymous reviewers for helpful comments that greatly improved this paper. For discussion of baleen growth and shedding, we thank Hans Thewissen, Raphaela Stimmelmayr, Robert Suydam, Tom Ford, Tom Albert, Todd O’Hara, Michael Moore, and John Gosline. We thank Sophia Hohlbauch at Asylum Research (Santa Barbara, CA), an Oxford Instruments Company, for AFM access and assistance.

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All authors contributed ideas, data collection/analysis, and field or tissue access/support. AJW wrote drafts and prepared figures; all authors edited and approved the final version.

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Correspondence to Alexander J. Werth.

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Werth, A.J., Sformo, T.L., Lysiak, N.S. et al. Baleen turnover and gut transit in mysticete whales and its environmental implications. Polar Biol 43, 707–723 (2020). https://doi.org/10.1007/s00300-020-02673-8

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