Advertisement

Polar Biology

, Volume 39, Issue 8, pp 1399–1409 | Cite as

Gross morphology and histology of the olfactory organ of the Greenland shark Somniosus microcephalus

  • S. FerrandoEmail author
  • L. Gallus
  • L. Ghigliotti
  • M. Vacchi
  • J. Nielsen
  • J. S. Christiansen
  • E. Pisano
Original Paper

Abstract

The Greenland shark (Somniosus microcephalus) is the largest predatory fish in Arctic waters. Knowledge of the fundamental biology and ecological role of the Greenland shark is limited, and the sensory biology of the Greenland shark has been poorly studied. Given the potential relevant contribution of chemoreception to the sensory capability of the Greenland shark to forage and navigate in low-light environments, we examined the architecture of the peripheral olfactory organ (the olfactory rosette) through morphological, histological and immunohistochemical assays. We found that each olfactory rosette consists of a small number of lamellae (22) associated with a relatively high surface area of the olfactory epithelium. The general organization of the epithelium is similar to that described for other elasmobranchs. However, details that have emerged concerning the cell type composition (absence of crypt neurons, presence of unusually large cells along the olfactory fiber bundles) deserve further investigation. Overall, the structure of the olfactory rosette suggests a well-developed olfactory capability for the Greenland shark coherent with a bentho-pelagic lifestyle.

Keywords

Greenland shark Somniosus microcephalus Olfactory rosette Chemoreception 

Notes

Acknowledgments

The Italian National Program of Research in Antarctica (PNRA) funded this research (Project 2013/AZ.1.11). The samples were collected during the TUNU-V Expedition in 2013 within the framework of the international TUNU-Programme lead by the UiT The Arctic University of Norway. The authors are very grateful to colleagues and crew on board the R/V Helmer Hanssen for their kind collaboration.

References

  1. Barraud P, Seferiadis AA, Tyson LD, Zwart MF, Szabo-Rogers HL, Ruhrberg C, Liu KJ, Baker CVH (2010) Neural crest origin of olfactory ensheathing glia. PNAS 107:21040–21045. doi: 10.1073/pnas.1012248107 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Bazàes A, Olivares J, Schmachtenberg O (2013) Properties, projections, and tuning of teleost olfactory receptor neurons. J Chem Ecol 39:451–464. doi: 10.1007/s10886-013-0268-1 CrossRefPubMedGoogle Scholar
  3. Benz GW, Borucinska JD, Lowry LF, Borucinska JD, Lowry LF, Whiteley HE et al (2002) Ocular lesions associated with attachment of the copepod Ommatokoita elongata (Lernaeopodidae: Siphonostomatoida) to corneas of Pacific sleeper sharks Somniosus pacificus captured off Alaska in Prince William Sound. J Parasitol 88:474–481. doi: 10.1645/0022-3395%282002%29088%5B0474%3AOLAWAO%5D2.0.CO%3B2 CrossRefPubMedGoogle Scholar
  4. Berghard A, Buck LB (1996) Sensory transduction in vomeronasal neurons: evidence for G alpha o, G alpha i2, and adenylyl cyclase II as major components of a pheromone signaling cascade. J Neurosci 16:909–918PubMedGoogle Scholar
  5. Berland B (1961) Copepod Ommatokoita elongata (Grant) in the Eyes of the Greenland Shark—a Possible Cause of Mutual Dependence. Nature 191:829–830. doi: 10.1038/191829a0 CrossRefGoogle Scholar
  6. Bettini S, Lazzari M, Ciani F, Franceschini V (2009) Immunohistochemical and histochemical characteristics of the olfactory system of the guppy, Poecilia reticulate (Teleostei, Poecilidae). Anat Rec 292:1569–1576. doi: 10.1002/ar.20944 CrossRefGoogle Scholar
  7. Bettini S, Lazzari M, Franceschini V (2012) Quantitative analysis of crypt cell population during postnatal development of the olfactory organ of the guppy, Poecilia reticulata (Teleostei, Poecilidae), from birth to sexual maturity. J Exp Biol 215:2711–2715. doi: 10.1242/jeb.069039 CrossRefPubMedGoogle Scholar
  8. Bigelow HB, Schroeder WB (1948) Sharks. In: Fishes of the Western North Atlantic. Part one: Lancelets, Cyclostomes, Sharks. Memoir Sears Foundation for Marine Research, Yale University, pp 53–576Google Scholar
  9. Borucinska JD, Benz GW, Whiteley HE (1998) Ocular lesions associated with attachment of the parasitic copepod Ommatokoita elongata (Grant) to corneas of Greenland sharks, Somniosus microcephalus (Bloch & Schneider). J Fish Dis 21:415–422. doi: 10.1046/j.1365-2761.1998.00122.x CrossRefGoogle Scholar
  10. Camacho S, Ostos-Garrido DA, Carmona R (2010) Study of the olfactory epithelium in the developing sturgeon. Characterization of the crypt cells. Chem Senses 35:147–156. doi: 10.1093/chemse/bjp091 CrossRefPubMedGoogle Scholar
  11. Campana SE, Fisk AT, Klimley AP (2013) Movements of Arctic and northwest Atlantic Greenland sharks (Somniosus microcephalus) monitored with archival satellite pop-up tags suggest long-range migrations. Biol Deep-Water Chondrichthyans Deep Sea Res Part II Topical Stud Oceanogr 115:109–115. doi: 10.1016/j.dsr2.2013.11.001 CrossRefGoogle Scholar
  12. Christiansen JS (2012) The TUNU-programme: Euro-Arctic marine fishes—diversity and adaptation. Adaptation and evolution in marine environments, vol 1. Springer, Berlin, pp 35–50CrossRefGoogle Scholar
  13. Christiansen JS, Mecklenburg CW, Karamushko OV (2014) Arctic marine fishes and their fisheries in light of global change. Glob Change Biol 20(2):352–359. doi: 10.1111/gcb.12395 CrossRefGoogle Scholar
  14. Coad BW, Reist JD (2004) Annotated list of the Arctic marine fishes of Canada. Fisheries and Oceans Canada, WinnipegGoogle Scholar
  15. Compagno LJV (1984) FAO species catalogue. Vol. 4. Sharks of the world. An annotated and illustrated catalogue of shark species known to date. Part 1—Hexanchiformes to Lamniformes. Food & Agriculture OrgGoogle Scholar
  16. Corsolini S, Ancora S, Bianchi N, Mariotti G, Leonzio C, Christiansen JS (2014) Organotropism of persistent organic pollutants and heavy metals in the Greenland shark Somniosus microcephalus in NE Greenland. Mar Pollut Bull 87:381–387. doi: 10.1016/j.marpolbul.2014.07.021 CrossRefPubMedGoogle Scholar
  17. Cox JPL (2008) Hydrodynamic aspects of fish olfaction. J R Soc Interface 5:575–593. doi: 10.1098/rsif.2007.1281 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Cox JPL (2013) Ciliary function in the olfactory organs of sharks and rays. Fish Fisheries 14(3):364–390. doi: 10.1111/j.1467-2979.2012.00476.x CrossRefGoogle Scholar
  19. Ebert DA, Stehmann MFW (2013) Sharks, batoids and chimaeras of the North Atlantic. Food and Agriculture OrgGoogle Scholar
  20. Ferrando S (2008) Ionocytes in the olfactory epithelium of developing Raja clavata. Italian J Zool 75:233–236. doi: 10.1080/11250000801934120 CrossRefGoogle Scholar
  21. Ferrando S, Gallus L (2013) Is the olfactory system of cartilaginous fishes a vomeronasal system? Front Neuroanat 7:37. doi: 10.3389/fnana.2013.00037 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Ferrando S, Bottaro M, Gallus L, Girosi L, Vacchi M, Tagliafierro G (2006a) Na+/K+ ATPase immunoreactivity in olfactory epithelium of small-spotted catshark Scyliorhinus canicula (Linnaeus, 1758): possible presence of ion exchanging cells? J Fish Biol 69:278–282. doi: 10.1111/j.1095-8649.01157.X CrossRefGoogle Scholar
  23. Ferrando S, Bottaro M, Gallus L, Girosi L, Vacchi M, Tagliafierro G (2006b) Observations of crypt neuron-like cells in the olfactory epithelium of a cartilaginous fish. Neurosci Lett 403:280–282. doi: 10.1016/j.neulet.2006.04.056 CrossRefPubMedGoogle Scholar
  24. Ferrando S, Bottaro M, Pedemonte F, De Lorenzo S, Gallus L, Tagliafierro G (2007) Appearance of crypt neurons in the olfactory epithelium of the skate Raja clavata during development. Anat Rec A Discov Mol Cell Evol Biol 290:1268–1272. doi: 10.1002/ar.20584 CrossRefGoogle Scholar
  25. Ferrando S, Gambardella C, Ravera S, Bottero S, Ferrando T, Gallus L, Manno V, Salati AP, Ramoino P, Tagliafierro G (2009) Immunolocalization of G-protein alpha subunits in the olfactory system of the cartilaginous fish Scyliorhinus canicula. Anat Rec Adv Integr Anat Evol Biol 292:1771–1779. doi: 10.1002/ar.21003 CrossRefGoogle Scholar
  26. Ferrando S, Gallus L, Gambardella C, Ghigliotti L, Ravera S, Vallarino M, Vacchi M, Tagliafierro G (2010a) Cell proliferation and apoptosis in the olfactory epithelium of the shark Scyliorhinus canicula. J Chem Neuroanat 40:293–300. doi: 10.1016/j.jchemneu.2010.08.004 CrossRefPubMedGoogle Scholar
  27. Ferrando S, Gallus L, Gambardella C, Vacchi M, Tagliafierro G (2010b) G protein alpha subunits in the olfactory epithelium of the holocephalan fish Chimaera monstrosa. Neurosci Lett 472:65–67. doi: 10.1016/j.neulet.2010.01.059 CrossRefPubMedGoogle Scholar
  28. Fisk AT, Tittlemier SA, Pranschke JL, Norstrom RJ (2002) Using anthropogenic contaminants and stable isotopes to assess the feeding ecology of Greenland sharks. Ecology 83:2162–2172. doi: 10.2307/3072048 CrossRefGoogle Scholar
  29. Fisk AT, Lydersen C, Kovacs KM (2012) Archival pop-off tracking of Greenland sharks Somniosus microcephalus in the High Arctic waters of Svalbard, Norway. Mar Ecol Progr Ser 468:255–265. doi: 10.3354/meps09962 CrossRefGoogle Scholar
  30. Gardiner JM, Atema J, Hueter RE, Motta PJ (2014) Multisensory integration and behavioral plasticity in sharks from different ecological niches. PLoS One 9(4):e93036. doi: 10.1371/journal.pone.0093036 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Hamdani EH, Døving KB (2007) The functional organization of the fish olfactory system. Prog Neurobiol 82:80–86. doi: 10.1016/j.pneurobio.2007.02.007 CrossRefGoogle Scholar
  32. Hamdani EH, Lastein S, Gregersen F, Døving KB (2008) Seasonal variations in olfactory sensory neurons—fish sensitivity to sex pheromones explained? Chem Senses 33:119–123. doi: 10.1093/chemse/bjm072 CrossRefGoogle Scholar
  33. Hansen A, Finger TE (2000) Phyletic distribution of crypt-type olfactory receptor neurons in fishes. Brain Behav Evol 55:100–110. doi: 10.1159/000006645 CrossRefPubMedGoogle Scholar
  34. Hansen A, Zielinski BS (2005) Diversity in the olfactory epithelium of bony fishes: development, lamellar arrangement, sensory neuron cell types and transduction components. J Neurocytol 34:183–208. doi: 10.1007/s11068-005-8353-1 CrossRefPubMedGoogle Scholar
  35. Hansen A, Anderson KT, Finger TE (2004) Differential distribution of olfactory receptor neurons in goldfish: structural and molecular correlates. J Comp Neurol 477:347–359. doi: 10.1002/cne.20202 CrossRefPubMedGoogle Scholar
  36. Hashiguchi Y, Nishida M (2007) Evolution of Trace Amine-Associated Receptor (TAAR) gene family in vertebrates: lineage-specific expansion and degradation of vertebrate chemosensory receptors expressed in the olfactory epithelium. Mol Biol Evol 24:2099–2107. doi: 10.1093/molbev/msm140 CrossRefPubMedGoogle Scholar
  37. Holl A (1973) Feinstruktur des Riechpithels von Chimaera monstrosa (Holocephali). Mar Biol 23:59–72. doi: 10.1007/BF00394112 CrossRefGoogle Scholar
  38. Howard LE, Holmes WM, Ferrando S, Maclaine JS, Kelsh RN, Ramsey A, Abel RL, Cox JP (2013) Functional nasal morphology of Chimaerid fishes. J Morphol 274:987–1009. doi: 10.1002/jmor.20156 CrossRefPubMedGoogle Scholar
  39. Hussey NE, Kessel ST, Aarestrup K, Cooke SJ, Cowley PD, Fisk AT, Harcourt RG, Holland KN, Iverson SJ, Kocik JF, Flemming JEM, Whoriskey FG (2015) Aquatic animal telemetry: a panoramic window into the underwater world. Science 348(6240):1255642. doi: 10.1126/science.1255642 CrossRefPubMedGoogle Scholar
  40. Idrobo CJ, Berkes F (2012) Pangnirtung inuit and the Greenland shark: co-producing knowledge of a little discussed species. Hum Ecol 40:405–414. doi: 10.1007/s10745-012-9490-7 CrossRefGoogle Scholar
  41. Jacobs LF (2012) From chemotaxis to the cognitive map: the function of olfaction. PNAS 109:10693–10700. doi: 10.1073/pnas.1201880109 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Jia C, Halpern M (1996) Subclasses of vomeronasal receptor neurons: differential expression of G-proteins (Gi2α and Goα) and segregated projections to the accessory olfactory bulb. Brain Res 719:117–128. doi: 10.1016/0006-8993(96)00110-2 CrossRefPubMedGoogle Scholar
  43. Jungblut LD, Paz DA, López-Costa JJ, Pozzi AG (2009) Heterogeneous distribution of G protein alpha subunits in the main olfactory and vomeronasal systems of Rhinella (Bufo) arenarum tadpoles. Zool Sci 26:722–728. doi: 10.2108/zsj.26.722 CrossRefPubMedGoogle Scholar
  44. Kajiura SM, Forni JB, Summers AP (2005) Olfactory morphology of carcharhinid and sphyrnid sharks: Does the cephalofoil confer a sensory advantage? J Morphol 264:253–263. doi: 10.1002/jmor.10208 CrossRefPubMedGoogle Scholar
  45. Kiraly SJ, Moore JA, Jasinski PH (2003) Deepwater and other sharks of the U.S. Atlantic Ocean exclusive economic zone. Mar Fish Rev 65(4):1–63Google Scholar
  46. Kyne PM, Sherrill-Mix SA, Burgess GH (2006) Somniosus microcephalus. The IUCN Red List of Threatened Species. Version 2015.2. www.iucnredlist.org. Downloaded 05 July 2015
  47. Leclerc LM, Lydersen C, Haug T, Glover KA, Fisk AT, Kovacs KM (2011) Greenland sharks (Somniosus microcephalus) scavenge offal from minke (Balaenoptera acutorostrata) whaling operations in Svalbard (Norway). Polar Res 30:7342. doi: 10.3402/polar.v30i0.7342 CrossRefGoogle Scholar
  48. Leclerc LM, Lydersen C, Haug T, Bachmann L, Fisk AT, Kovacs KM (2012) A missing piece in the Arctic food web puzzle? Stomach contents of Greenland sharks sampled in Svalbard, Norway. Polar Biol 35:1197–1208. doi: 10.1007/s00300-012-1166-7 CrossRefGoogle Scholar
  49. Liberles SD (2009) Trace amine-associated receptors are olfactory receptors in vertebrates. Ann NY Acad Sci 1170:168–172. doi: 10.1111/j.1749-6632.2009.04014.x CrossRefPubMedGoogle Scholar
  50. Liberles SD, Buck LB (2006) A second class of chemosensory receptors in the olfactory epithelium. Nature 442:645–650. doi: 10.1038/nature05066 CrossRefPubMedGoogle Scholar
  51. Lynghammar A, Christiansen JS, Mecklenburg CW, Karamushko OV, Møller PR, Gallucci VF (2013) Species richness and distribution of chondrichthyan fishes in the Arctic Ocean and adjacent seas. Biodiversity 14(1):57–66. doi: 10.1080/14888386.2012.706198 CrossRefGoogle Scholar
  52. MacNeil MA, McMeans BC, Hussey NE, Vecsei P, Svavarsson J, Kovacs KM, Lydersen C, Treble MA, Skomal GB, Ramsey M, Fisk AT (2012) Biology of the Greenland shark Somniosus microcephalus. J Fish Biol 80:991–1018. doi: 10.1111/j.1095-8649.2012.03257 CrossRefPubMedGoogle Scholar
  53. McMeans BC, Arts MT, Lydersen C, Kovacs KM, Hop H, Petersen SF, Fisk AT (2013) The role of Greenland sharks (Somniosus microcephalus) in an Arctic ecosystem: assessed via stable isotopes and fatty acids. Mar Biol 160:1223–1238. doi: 10.1007/s00227-013-2174-z CrossRefGoogle Scholar
  54. Meng Q, Yin M (1981a) A study of the olfactory organ of the shark. Trans Chin Ichthyol Soc 2:1–24Google Scholar
  55. Meng Q, Yin M (1981b) A study on the olfactory organ of skates, rays and chimaeras. J Fisheries China 5(3):209–228Google Scholar
  56. Meredith TL, Kajiura SM (2010) Olfactory morphology and physiology of elasmobranchs. J Exp Biol 213:3449–3456. doi: 10.1242/jeb.045849 CrossRefPubMedGoogle Scholar
  57. Mombaerts P (2004) Genes and ligands for odorant, vomeronasal and taste receptors. Nat Rev Neurosci 5:263–278. doi: 10.1038/nrn1365 CrossRefPubMedGoogle Scholar
  58. Nielsen J, Hedeholm RB, Simon M, Steffensen JF (2014) Distribution and feeding ecology of the Greenland shark (Somniosus microcephalus) in Greenland waters. Polar Biol 37:37–46. doi: 10.1007/s00300-013-1408-3 CrossRefGoogle Scholar
  59. Quintana-Urzainqui I, Rodríguez-Moldes I, Candal E (2014) Developmental, tract-tracing and immunohistochemical study of the peripheral olfactory system in a basal vertebrate: insights on Pax6 neurons migrating along the olfactory nerve. Brain Struct Funct 219:85–104. doi: 10.1007/s00429-012-0486-2 CrossRefPubMedGoogle Scholar
  60. Rasband WS (1997–2014) ImageJ, U.S. National Institutes of Health, Bethesda, Maryland, USA. http://imagej.nih.gov/ij/
  61. Schluessel V, Bennet MB, Bleckmann H, Blomberg S, Collin SP (2008) Morphometric and ultrastructural comparison of the olfactory sensory system in elasmobranchs: the significance of structure-function relationships based on phylogeny and ecology. J Morphol 269:1365–1386. doi: 10.1002/jmor.10661 CrossRefPubMedGoogle Scholar
  62. Schmachtenberg O (2006) Histological and electrophysiological properties of crypt cells from the olfactory epithelium of the marine teleost Trachurus symmetricus. J Comp Neurol 495:113–121. doi: 10.1002/cne.20847 CrossRefPubMedGoogle Scholar
  63. Skomal GB, Benz GW (2004) Ultrasonic tracking of Greenland sharks, Somniosus microcephalus under Arctic ice. Mar Biol 145:489–498. doi: 10.1007/s00227-004-1332-8 CrossRefGoogle Scholar
  64. Takami S, Luer CA, Graziadei PPC (1994) Microscopic structure of the olfactory organ of the clearnose skate, Raja eglanteria. Anat Embryol 190:211–230. doi: 10.1007/BF00234300 CrossRefPubMedGoogle Scholar
  65. Theisen B, Zeiske E, Breuker H (1986) Functional morphology of the olfactory organs in the spiny dogfih (Squalus acanthias L.) and the small-spotted catshark (Scyliorhinus canicula L.). Acta Zool 67:73–86. doi: 10.1111/j.1463-6395.1986.tb00851.x CrossRefGoogle Scholar
  66. Theiss SM, Hart NS, Collin SP (2009) Morphological indicators of olfactory capability in Wobbegong sharks (Orectolobidae, Elasmobranchii). Brain Behav Evol 73:91–101. doi: 10.1159/000209865 CrossRefPubMedGoogle Scholar
  67. Venkatesh B, Lee AP, Ravi V, Maurya AK, Lian MM, Swann JB, Ohta Y, Flajnik MF, Sutoh Y, Kasahara M et al (2014) Elephant shark genome provides unique insights into gnathostome evolution. Nature 505:174–179. doi: 10.1038/nature12826 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Wakabayashi Y, Ichikawa M (2008) Localization of G protein alpha subunits and morphology of receptor neurons in olfactory and vomeronasal epithelia in Reeve’s turtle, Geoclemys reevesii. Zool Sci 25:178–187. doi: 10.2108/zsj.25.178 CrossRefPubMedGoogle Scholar
  69. Watanabe YY, Lydersen C, Fisk AT, Kovacs KM (2012) The slowest fish: swim speed and tail-beat frequency of Greenland sharks. J Exp Mar Biol Ecol 426–427:5–11. doi: 10.1016/j.jembe.2012.04.021 CrossRefGoogle Scholar
  70. Yang H, He B-R, Hao D-J (2015) Biological roles of olfactory ensheathing cell in facilitating neural regeneration: a systematic review. Mol Neurobiol 51:168–179. doi: 10.1007/s12035-014-8664-2 CrossRefPubMedGoogle Scholar
  71. Yano K, Stevens JD, Compagno LJV (2004) A review of the systematics of the sleeper shark genus Somniosus with redescriptions of Somniosus (Somniosus) antarcticus and Somniosus (Rhinoscymnus) longus (Squaliformes: Somniosidae). Ichthyol Res 51:360–373. doi: 10.1007/s10228-004-0244-4 CrossRefGoogle Scholar
  72. Yano K, Stevens JD, Compagno LJV (2007) Distribution, reproduction and feeding of the Greenland shark Somniosus (Somniosus) microcephalus, with notes on two other sleeper sharks, Somniosus (Somniosus) pacificus and Somniosus (Somniosus) antarcticus. J Fish Biol 70:374–390. doi: 10.1111/j.1095-8649.2007.01308.x CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.DISTAV-University of GenoaGenoaItaly
  2. 2.ISMAR – CNRGenoaItaly
  3. 3.University of CopenhagenHelsingørDenmark
  4. 4.UiT The Arctic University of NorwayTromsøNorway

Personalised recommendations