ADAPTACIÓN Y MECANISMO DE LA GLÁNDULA SALINA EN AVES MARINAS

César Abdiel Amaya-Rodríguez; José Pompilio Young Castillo

Submitted January 24, 2023

Published 2023-01-25

Artículos

Vol. 33 No. 1 (2023): Scientia

ADAPTATION AND MECHANISM OF THE SALT GLAND IN SEA BIRDS

César Abdiel Amaya-Rodríguez⁺⁻
José Pompilio Young Castillo⁺⁻

PDF (Español (España))

Citación:

DOI: ND

Published: 2023-01-25

How to Cite

Amaya-Rodríguez, C. A., & Young Castillo, J. P. (2023). ADAPTATION AND MECHANISM OF THE SALT GLAND IN SEA BIRDS. Scientia, 33(1), 97–114. Retrieved from https://revistas.up.ac.pa/index.php/scientia/article/view/3535

This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.

Abstract

Salt glands have allowed seabirds to face the great physiological challenge of living in coastal environments where there is little freshwater available. This adaptation to the saline environment has allowed seabirds to ingest sea water without affecting their osmotic balance. In this article, the evolutionary origin, its anatomy, the function of the Na⁺-K⁺-ATPase pump and the Na⁺- K⁺- 2Cl^- countertransporter involved in the cellular mechanism to eliminate the high concentrations of Na⁺ and Cl^- ions in the blood plasma through the saline gland, the regulation by the G protein-coupled muscarinic receptors of the vasoactive intestinal peptide, and the regulation by the G protein-coupled muscarinic receptors of the vasoactive intestinal peptide were discussed.

Downloads

Download data is not yet available.

References

Ali, M. A., and Reshag, A. F. (2021). Morphometrical and histological changes in domestic duck salt glands in response to salinated water. Plant Archives, 21(1), 338–342. https://doi.org/https://doi.org/10.51470/
Babonis, L. S., and Brischoux, F. (2012). Perspectives on the convergent evolution of tetrapod salt glands. Integrative and Comparative Biology, 52(2), 245–256. https://doi.org/10.1093/icb/ics073
Benson, G. K., and Phillips, J. G. (1964). Observations on the Histological Structure of the Supraorbital (Nasal) Glands From Saline-Fed and Freshwater-Fed Domestic Ducks (Anas Platyrhynchus). Journal of Anatomy, 98(4), 571–578.
Born. (1879). Die Nasenhöhlen und die Theäennasengang der amnioten Wirbeltiere. Morph. Jahrb., 2(5).
Brischoux, F., Lendvai, Á. Z., Bókony, V., Chastel, O., and Angelier, F. (2015). Marine lifestyle is associated with higher baseline corticosterone levels in birds. Biological Journal of the Linnean Society, 115(1), 154–161. https://doi.org/10.1111/bij.12493
Butler, D. G., Lam, W., and Tong, J. (2006). ANG II-induced attenuation of duck salt gland secretion does not depend upon the release of adrenal catecholamines. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 176(1), 35–43. https://doi.org/10.1007/s00360-005-0029-8
Butler, D. G. (1987). Adrenalectomy fails to block salt gland secretion in Pekin ducks (Anas platyrhynchos) adapted to 0.9% saline drinking water. General and Comparative Endocrinology, 66(2), 171–181. https://doi.org/10.1016/0016-6480(87)90265-6
Butler, D. G. (2007). ANG II-induced attenuation of salt gland function in Pekin ducks is not catecholamine-dependent. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 177(7), 733–742. https://doi.org/10.1007/s00360-007-0170-7
Ching, A. C. T., Hughes, M. R., Poon, A. M., and Pang, S. F. (1999). Melatonin receptors and melatonin inhibition of duck salt gland secretion. General and Comparative Endocrinology, 116(2), 229–240. https://doi.org/10.1006/gcen.1999.7362
Clarke, R. J., and Kane, D. J. (2007). Two gears of pumping by the sodium pump. Biophysical Journal, 93(12), 4187–4196. https://doi.org/10.1529/biophysj.107.111591
Cohn, F. (1903). Zur Entwicklungsgeschichte des Geruchs. Archiv Für Mikroskopische Anatomie, 61, 133.
Cramp, R. L., Hudson, N. J., and Franklin, C. E. (2010). Activity, abundance, distribution and expression of Na+K +-ATPase in the salt glands of crocodylus porosus following chronic saltwater acclimation. Journal of Experimental Biology, 213(8), 1301–1308. https://doi.org/10.1242/jeb.039305
Crocker, A. D., and Holmes, W. N. (1971). Intestinal absorption in ducklings (Anasplatyrhynchos) maintained on fresh water and hypertonic saline. Camp. Biochem. Physiol., 4, 203–211. https://doi.org/https://doi.org/10.1016/0300-9629(71)90161-7
Dergousova, E. A., Petrushanko, I. Y., Klimanova, E. A., Mitkevich, V. A., Ziganshin, R. H., Lopina, O. D., and Makarov, A. A. (2017). Effect of reduction of redox modifications of cys-residues in the Na,K-ATPase ?1-subunit on its activity. Biomolecules, 7(1), 1–11. https://doi.org/10.3390/biom7010018
Dergousova, E. A., Poluektov, Y. M., Klimanova, E. A., Petrushanko, I. Y., Mitkevich, V. A., Makarov, A. A., and Lopina, O. D. (2018). Glutathionylation of Na,K-ATPase Alpha-Subunit Alters Enzyme Conformation and Sensitivity to Trypsinolysis. Biochemistry (Moscow), 83(8), 969–981. https://doi.org/10.1134/S0006297918080084
Doyle, W. L. (1960). The principal cells of the salt-gland of marine birds. Experimental Cell Research, 21(2), 386–393. https://doi.org/10.1016/0014-4827(60)90270-6
El–Gohary, Z. M., El-Sayad, F. I., Hassan, H. A., and Hamoda, A. M. M. (2013). The Functional Alterations of the Avian Salt Gland Subsequent to Osmotic Stress. The Egyptian Journal of Hospital Medicine, 51(April), 346–360. https://doi.org/10.12816/0000851
Fa?nge, R., Schmidt-Nielsen, K., and Robinson, M. (1958). Control of Secretion From the Avian Salt Gland. American Journal of Physiology-Legacy Content, 195(2), 321–326. https://doi.org/https://doi.org/10.1152/ajplegacy.1958.195.2.321
Fernández, M., and Gasparini, Z. (2000). Salt glands in a Tithonian metriorhynchid crocodyliform and their physiological significance. Lethaia, 33(4), 269–276. https://doi.org/10.1080/002411600750053835
Fletcher, G. L., Stainer, I. M., and Holmes, W. N. (1967). Sequential changes in the adenosinetriphosphatase activity and the electrolyte excretory capacity of the nasal glands of the duck (Anas platyrhynchos) during the period of adaptation to hypertonic saline. Journal of Experimental Biology, 47(3), 375–391.
Gadow, H. (1890). Description of the modification of certain organs. The stomach of the ostrich. Zoologische Jahrbuch, 5, 641–644.
Ganin, M. (1890). Einige Thatsachen zur Frage über das Jacobsonsche Organ der Vögel. Zool. Anz., 13, 285–287.
Gerstberger, R., Gray, D. A., and Simon, E. (1984). Circulatory and osmoregulatory effects of angiotensin II perfusion of the third ventricle in a bird with salt glands. Journal of Physiology, 349(1), 167–182. https://doi.org/https://doi.org/10.1113/jphysiol.1984.sp015150
Gerstberger, R., Simon-Oppermann, C., and Kaul, R. (1984). Cephalic osmoreceptor control of salt gland activation and inhibition in the salt adapted duck. Journal of Comparative Physiology B, 154(5), 449–456. https://doi.org/10.1007/BF02515149
Gerstberger, R., Simon, E., and Gray, D. A. (1984). Salt gland and kidney responses to intracerebral osmotic stimulation in salt- and water-loaded ducks. American Journal of Physiology - Regulatory Integrative and Comparative Physiology, 16(6). https://doi.org/10.1152/ajpregu.1984.247.6.r1022
Gray, D. A., Hammel, H. T., and Simon, E. (1986). Osmoregulatory effects of angiotensin II in a bird with salt glands (Anas platyrhynchos). Journal of Comparative Physiology B, 156(3), 315–321. https://doi.org/10.1007/BF01101093
Gray, D. A., Schütz, H., and Gerstberger, R. (1991a). Interaction of atrial natriuretic factor and osmoregulatory hormones in the Pekin duck. General and Comparative Endocrinology, 81(2), 246–255. https://doi.org/10.1016/0016-6480(91)90009-U
Gray, D. A., Schütz, H., and Gerstberger, R. (1991b). Plasma atrial natriuretic factor responses to blood volume changes in the pekin duck. Endocrinology, 128(3), 1655–1660. https://doi.org/10.1210/endo-128-3-1655
Gutiérrez, J. S., Masero, J. A., Abad-Gómez, J. M., Villegas, A., and Sánchez-Guzmán, J. M. (2011). Understanding the energetic costs of living in saline environments: Effects of salinity on basal metabolic rate, body mass and daily energy consumption of a long-distance migratory shorebird. Journal of Experimental Biology, 214(5), 829–835. https://doi.org/10.1242/jeb.048223
Hackett, S. J., Kimball, R. T., Reddy, S., Bowie, R. C., Braun, E. L., Braun, M. J., ... and Yuri, T. (2008). A phylogenomic study of birds reveals their evolutionary history. Science, 320(5884), 1763–1768. https://doi.org/10.1126/science.1157704
Hammel, H. T., Simon-Oppermann, C. H. R. I. S. T. A., and Simon, E. (1980). Properties of body fluids influencing salt gland secretion in Pekin ducks. American Journal of Physiology - Regulatory Integrative and Comparative Physiology, 8(3). https://doi.org/10.1152/ajpregu.1980.239.5.r489
Hanwell, A., and Peaker, M. (1975). The control of adaptive hypertrophy in the salt glands of geese and ducks. The Journal of Physiology, 248(1), 193–205. https://doi.org/10.1113/jphysiol.1975.sp010969
Hanwell, A., Linzell, J. L., and Peaker, M. (1972). Nature and location of the receptors for salt-gland secretion in the goose. J Physiol, 226(2), 453–472. https://doi.org/10.1113/jphysiol.1972.sp009993
Heinz, M. K., and Gray, D. A. (2001). Role of plasma ANG II in the excretion of acute sodium load in a bird with salt glands (Anas platyrhynchos). American Journal of Physiology - Regulatory Integrative and Comparative Physiology, 281(1), 346–351. https://doi.org/10.1152/ajpregu.2001.281.1.r346
Hildebrandt, J. P. (2001). Coping with excess salt: Adaptive functions of extrarenal osmoregulatory organs in vertebrates. Zoology, 104(3–4), 209–220. https://doi.org/10.1078/0944-2006-00026
Holmes, W., and Stewart, D. J. (1968). Changes in the nucleic acid and protein composition of the nasal glands from the duck (Anas platyrhynchos) during the period of adaptation to hypertonic saline. Journal of Experimental Biology, 48(3), 509–519.
Holmes, W. N., Phillips, J. G., and Butler, D. G. (1961). The effect of adrenocortical steroids on the renal and extra-renal responses of the domestic duck (Anas platyrhynchus) after hypertonic saline loading. Endocrinology, 69(3), 483–495. https://doi.org/10.1210/endo-69-3-483
Hootman, S. R., and Ernst, S. A. (1980). Dissociation of avian salt gland: separation procedures and characterization of dissociated cells. American Journal of Physiology - Cell Physiology, 7(3), 184–195. https://doi.org/10.1152/ajpcell.1980.238.5.c184
Hughes, M. R., and Ruch Jr, F. E. (1969). Sodium and potassium in spontaneously produced salt gland secretion and tears of ducks, Anas platyrhynchos , acclimated to fresh and saline waters. Canadian Journal of Zoology, 47(6), 1133–1138. https://doi.org/10.1139/z69-177
Ibañez, L. M., Tambussi, C. P., and Acosta Hospitaleche, C. I. A. (2010). Análisis morfométrico del surco nasal en aves. Ornitologia Neotropical, 21(2), 181–194.
Jacobson, L. (1813). Anatomisk beskrivelse over et nyt organ i huusdyrenes naese. Veter Salesk Skrift, 2, 209–246.
Jobert, C. (1869). Recherches anatomiques sur les glandes nasales des oiseaux,...
Karlsson, K. A., Samuelsson, B. E., and Steen, G. O. (1971). Lipid pattern and Na+-K+-dependent adenosine triphosphatase activity in the salt gland of duck before and after adaptation to hypertonic saline. The Journal of Membrane Biology, 5(2), 169–184. https://doi.org/10.1007/BF02107722
Kolliker, R. V. (1860). A manual of microscopic anatomy. London: Parker.
Krohn, M., and Hildebrandt, J.-P. (2004). Cross-talk of phosphoinositide- and cyclic nucleotide-dependent signaling pathways in differentiating avian nasal gland cells. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 174(6), 461–470. https://doi.org/10.1007/s00360-004-0432-6
Kühnel, W. (1972). On the innervation of the salt gland. Zeitschrift Für Zellforschung Und Mikroskopische Anatomie, 134(3), 435–438. https://doi.org/10.1007/BF00307177
Marais, M., and Gray, D. A. (2009). A role for natriuretic peptide in lipopolysaccharide-induced fever in Pekin ducks (Anas platyrhynchos): Is natriuretic peptide an endogenous antipyretic in birds? Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 179(2), 125–132. https://doi.org/10.1007/s00360-008-0295-3
Marples, B. J. (1932). The Structure and Development of the Nasal Glands of Birds. Proceedings of the Zoological Society of London, 102(4), 829–844. https://doi.org/10.1111/j.1096-3642.1932.tb01565.x
Martin, D. W., Marecek, J., Scarlata, S., and Sachs, J. R. (2000). ?? protomers of Na+,K+-ATPase from microsomes of duck salt gland are mostly monomeric: Formation of higher oligomers does not modify molecular activity. Proceedings of the National Academy of Sciences of the United States of America, 97(7), 3195–3200. https://doi.org/10.1073/pnas.050558397
Mihalkovics. (1898). Nasenhöhl und Jacobson’sches Organ. Eine morphologisch Studie. Anat. Hefte, 11(1).
Müller, C., Sendler, M., and Hildebrandt, J. P. (2006). Downregulation of aquaporins 1 and 5 in nasal gland by osmotic stress in ducklings, Anas platyrhynchos: Implications for the production of hypertonic fluid. Journal of Experimental Biology, 209(20), 4067–4076. https://doi.org/10.1242/jeb.02491
Murphy, R. C. (1936). Oceanic birds of South America. The American Museum of Natural History, 2, 1–6.
Nitzsch, C. L. (1820). Über die Nasendrüse der Vögel. Archiv Physiol.(Meckel’s Archiv), 6, 234–269.
Peaker, M. & Linzell, J. L. (1975). Salt glands in birds and reptiles. In Monographs of the Physiological Society (Issue 32). Monogr Physiol Soc. https://books.google.es/books?hl=es&lr=&id=dZk8AAAAIAAJ&oi=fnd&pg=PR9&dq=Peaker+and+Linzell+(1975).&ots=B7BHiSoLVO&sig=Q-osI7fsOD6WI1vcJYK-6eF8KyQ#v=onepage&q=Peaker and Linzell (1975).&f=false
Peaker, A. and H. M. (1973). The control of adaptive hypertrophy in the salt glands of geese and ducks. The Journal of Physiology, 248(1), 193–205.
Petrushanko, I. Y., Yakushev, S., Mitkevich, V. A., Kamanina, Y. V., Ziganshin, R. H., Meng, X., ... and Bogdanova, A. (2012). S-glutathionylation of the Na,K-ATPase catalytic ? subunit is a determinant of the enzyme redox sensitivity. Journal of Biological Chemistry, 287(38), 32195–32205. https://doi.org/10.1074/jbc.M112.391094
Pratap, P. R., Dediu, O., and Nienhaus, G. U. (2003). FTIR Study of ATP-Induced Changes in Na+/K+-ATPase from Duck Supraorbital Glands. Biophysical Journal, 85(6), 3707–3717. https://doi.org/10.1016/S0006-3495(03)74787-0
Pratap, P. R., Heiss, G., Sikor, M., Lamb, D. C., and Burnett, M. (2011). Single-Molecule Studies of the Na+/K+-ATPase. Biophysical Journal, 100(3), 464a. https://doi.org/10.1016/j.bpj.2010.12.2724
Pratap, P. R., Mikhaylyants, L. O., and Olden-Stahl, N. (2009). Fluorescence measurements of nucleotide association with the Na+/K+-ATPase. Biochimica et Biophysica Acta - Proteins and Proteomics, 1794(11), 1549–1557. https://doi.org/10.1016/j.bbapap.2009.06.023
Randall, D. J., Burggren, W. W. French, K. and Eckert, R. (1998). Eckert fisiología animal: Capítulo 14. Equilibrio iónico y osmótico (4 edition).
Reshag, A. F., Abood, D. A., and Dawood, M. S. (2016). Anatomical and histological study of the kidneys and salt glands in great flamingos (Phoenicopterus roseus). The Iraqi Journal of Veterinary Medicine, 40(1), 140–146. https://doi.org/10.30539/iraqijvm.v40i1.151
Sabat, P. (2000). Birds in marine and saline environments: living in dry habitats. In Revista chilena de historia natural (Vol. 73, Issue 3). https://doi.org/10.4067/s0716-078x2000000300004
Scanes, C. (2015). Sturkie’s Avian Physiology. In Chapter 12 - Osmoregulatory Systems of Birds (6 edition). Academic Pres.
Schmidt-Nielsen, K., and Fange, R. (1958). The Function of the Salt Gland in the Brown Pelican. American Ornithologists’ Union, 75(3), 282–289. https://doi.org/10.2307/4081974
Schmidt-Nielsen, K. (1960). The salt-secreting gland of marine birds. Circulation, 21, 955–967. https://doi.org/10.1161/01.CIR.21.5.955
Schütz, H., Gray, D. A., and Gerstberger, R. (1992). Modulation of kidney function in conscious Pekin ducks by atrial natriuretic factor. Endocrinology, 130(2), 678–684. https://doi.org/https://doi.org/10.1210/endo.130.2.1310279
Shuttleworth, T. J., and Hildebrandt, J. P. (1999). Vertebrate salt glands: Short- and long-term regulation of function. Journal of Experimental Zoology, 283(7), 689–701. https://doi.org/10.1002/(SICI)1097-010X(19990601)283:7<689::AID-JEZ7>3.0.CO;2-T
Shuttleworth, T. J. (1995). Intracellular Signals Controlling Ionic and Acid-Base Regulation in Avian Nasal Gland Cells. In: Heisler N. (eds) Mechanisms of Systemic Regulation: Acid—Base Regulation, Ion-Transfer and Metabolism. Springer US. https://doi.org/10.1007/978-3-642-52363-2_5
Simon-Oppermann, C., Simon, E., Deutsch, H., Möhring, J., and Schoun, J. (1980). Serum arginine-vasotocin (AVT) and afferent and central control of osmoregulation in conscious Pekin ducks. Pflügers Archiv European Journal of Physiology, 387(2), 99–106. https://doi.org/10.1007/BF00584259
Stewart, D. J., Semple, E. W., Swart, G. T., and Sen, A. K. (1975). Induction of the catalytic protein of (Na++ K+)-ATPase in the salt gland of the duck. Biochimica et Biophysica Acta, 419, 150–163. https://doi.org/https://doi.org/10.1016/0005-2736(76)90379-5
Taniguchi, K., Kaya, S., Abe, K., and Mårdh, S. (2001). The oligomeric nature of Na/K-transport ATPase. Journal of Biochemistry, 129(3), 335–342. https://doi.org/10.1093/oxfordjournals.jbchem.a002862
Thesleff, S., and Schmidt-Nielsen, K. (1962). An electrophysiological study of the salt gland of the herring gull. The American Journal of Physiology, 202, 597–600. https://doi.org/10.1152/ajplegacy.1962.202.3.597
Wang, X., Huang, J., Hu, Y., Liu, X., Peteya, J., and Clarke, J. A. (2018). The earliest evidence for a supraorbital salt gland in dinosaurs in new Early Cretaceous ornithurines. Scientific Reports, 8(1), 1–12. https://doi.org/10.1038/s41598-018-22412-8
Woodin, M. C., Michot, T. C., and Lee, M. C. (2008). Salt gland development in migratory redheads (Aythya Americana) in saline environments on the winter range, Gulf of Mexico, USA. Acta Zoologica Academiae Scientiarum Hungaricae, 54(SUPPL.1), 251–264.

Keywords

PDF (Español (España))

Resumen visto - 752 veces
PDF (Español (España)) descargado - 343

Licencia

Este obra está bajo una licencia de Creative Commons Reconocimiento-NoComercial-CompartirIgual 4.0 Internacional.

Content Top

[1] Ali, M. A., and Reshag, A. F. (2021). Morphometrical and histological changes in domestic duck salt glands in response to salinated water. Plant Archives, 21(1), 338–342. https://doi.org/https://doi.org/10.51470/

[2] Babonis, L. S., and Brischoux, F. (2012). Perspectives on the convergent evolution of tetrapod salt glands. Integrative and Comparative Biology, 52(2), 245–256. https://doi.org/10.1093/icb/ics073

[3] Benson, G. K., and Phillips, J. G. (1964). Observations on the Histological Structure of the Supraorbital (Nasal) Glands From Saline-Fed and Freshwater-Fed Domestic Ducks (Anas Platyrhynchus). Journal of Anatomy, 98(4), 571–578.

[4] Born. (1879). Die Nasenhöhlen und die Theäennasengang der amnioten Wirbeltiere. Morph. Jahrb., 2(5).

[5] Brischoux, F., Lendvai, Á. Z., Bókony, V., Chastel, O., and Angelier, F. (2015). Marine lifestyle is associated with higher baseline corticosterone levels in birds. Biological Journal of the Linnean Society, 115(1), 154–161. https://doi.org/10.1111/bij.12493

[6] Butler, D. G., Lam, W., and Tong, J. (2006). ANG II-induced attenuation of duck salt gland secretion does not depend upon the release of adrenal catecholamines. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 176(1), 35–43. https://doi.org/10.1007/s00360-005-0029-8

[7] Butler, D. G. (1987). Adrenalectomy fails to block salt gland secretion in Pekin ducks (Anas platyrhynchos) adapted to 0.9% saline drinking water. General and Comparative Endocrinology, 66(2), 171–181. https://doi.org/10.1016/0016-6480(87)90265-6

[8] Butler, D. G. (2007). ANG II-induced attenuation of salt gland function in Pekin ducks is not catecholamine-dependent. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 177(7), 733–742. https://doi.org/10.1007/s00360-007-0170-7

[9] Ching, A. C. T., Hughes, M. R., Poon, A. M., and Pang, S. F. (1999). Melatonin receptors and melatonin inhibition of duck salt gland secretion. General and Comparative Endocrinology, 116(2), 229–240. https://doi.org/10.1006/gcen.1999.7362

[10] Clarke, R. J., and Kane, D. J. (2007). Two gears of pumping by the sodium pump. Biophysical Journal, 93(12), 4187–4196. https://doi.org/10.1529/biophysj.107.111591

[11] Cohn, F. (1903). Zur Entwicklungsgeschichte des Geruchs. Archiv Für Mikroskopische Anatomie, 61, 133.

[12] Cramp, R. L., Hudson, N. J., and Franklin, C. E. (2010). Activity, abundance, distribution and expression of Na+K +-ATPase in the salt glands of crocodylus porosus following chronic saltwater acclimation. Journal of Experimental Biology, 213(8), 1301–1308. https://doi.org/10.1242/jeb.039305

[13] Crocker, A. D., and Holmes, W. N. (1971). Intestinal absorption in ducklings (Anasplatyrhynchos) maintained on fresh water and hypertonic saline. Camp. Biochem. Physiol., 4, 203–211. https://doi.org/https://doi.org/10.1016/0300-9629(71)90161-7

[14] Dergousova, E. A., Petrushanko, I. Y., Klimanova, E. A., Mitkevich, V. A., Ziganshin, R. H., Lopina, O. D., and Makarov, A. A. (2017). Effect of reduction of redox modifications of cys-residues in the Na,K-ATPase ?1-subunit on its activity. Biomolecules, 7(1), 1–11. https://doi.org/10.3390/biom7010018

[15] Dergousova, E. A., Poluektov, Y. M., Klimanova, E. A., Petrushanko, I. Y., Mitkevich, V. A., Makarov, A. A., and Lopina, O. D. (2018). Glutathionylation of Na,K-ATPase Alpha-Subunit Alters Enzyme Conformation and Sensitivity to Trypsinolysis. Biochemistry (Moscow), 83(8), 969–981. https://doi.org/10.1134/S0006297918080084

[16] Doyle, W. L. (1960). The principal cells of the salt-gland of marine birds. Experimental Cell Research, 21(2), 386–393. https://doi.org/10.1016/0014-4827(60)90270-6

[17] El–Gohary, Z. M., El-Sayad, F. I., Hassan, H. A., and Hamoda, A. M. M. (2013). The Functional Alterations of the Avian Salt Gland Subsequent to Osmotic Stress. The Egyptian Journal of Hospital Medicine, 51(April), 346–360. https://doi.org/10.12816/0000851

[18] Fa?nge, R., Schmidt-Nielsen, K., and Robinson, M. (1958). Control of Secretion From the Avian Salt Gland. American Journal of Physiology-Legacy Content, 195(2), 321–326. https://doi.org/https://doi.org/10.1152/ajplegacy.1958.195.2.321

[19] Fernández, M., and Gasparini, Z. (2000). Salt glands in a Tithonian metriorhynchid crocodyliform and their physiological significance. Lethaia, 33(4), 269–276. https://doi.org/10.1080/002411600750053835

[20] Fletcher, G. L., Stainer, I. M., and Holmes, W. N. (1967). Sequential changes in the adenosinetriphosphatase activity and the electrolyte excretory capacity of the nasal glands of the duck (Anas platyrhynchos) during the period of adaptation to hypertonic saline. Journal of Experimental Biology, 47(3), 375–391.

[21] Gadow, H. (1890). Description of the modification of certain organs. The stomach of the ostrich. Zoologische Jahrbuch, 5, 641–644.

[22] Ganin, M. (1890). Einige Thatsachen zur Frage über das Jacobsonsche Organ der Vögel. Zool. Anz., 13, 285–287.

[23] Gerstberger, R., Gray, D. A., and Simon, E. (1984). Circulatory and osmoregulatory effects of angiotensin II perfusion of the third ventricle in a bird with salt glands. Journal of Physiology, 349(1), 167–182. https://doi.org/https://doi.org/10.1113/jphysiol.1984.sp015150

[24] Gerstberger, R., Simon-Oppermann, C., and Kaul, R. (1984). Cephalic osmoreceptor control of salt gland activation and inhibition in the salt adapted duck. Journal of Comparative Physiology B, 154(5), 449–456. https://doi.org/10.1007/BF02515149

[25] Gerstberger, R., Simon, E., and Gray, D. A. (1984). Salt gland and kidney responses to intracerebral osmotic stimulation in salt- and water-loaded ducks. American Journal of Physiology - Regulatory Integrative and Comparative Physiology, 16(6). https://doi.org/10.1152/ajpregu.1984.247.6.r1022

[26] Gray, D. A., Hammel, H. T., and Simon, E. (1986). Osmoregulatory effects of angiotensin II in a bird with salt glands (Anas platyrhynchos). Journal of Comparative Physiology B, 156(3), 315–321. https://doi.org/10.1007/BF01101093

[27] Gray, D. A., Schütz, H., and Gerstberger, R. (1991a). Interaction of atrial natriuretic factor and osmoregulatory hormones in the Pekin duck. General and Comparative Endocrinology, 81(2), 246–255. https://doi.org/10.1016/0016-6480(91)90009-U

[28] Gray, D. A., Schütz, H., and Gerstberger, R. (1991b). Plasma atrial natriuretic factor responses to blood volume changes in the pekin duck. Endocrinology, 128(3), 1655–1660. https://doi.org/10.1210/endo-128-3-1655

[29] Gutiérrez, J. S., Masero, J. A., Abad-Gómez, J. M., Villegas, A., and Sánchez-Guzmán, J. M. (2011). Understanding the energetic costs of living in saline environments: Effects of salinity on basal metabolic rate, body mass and daily energy consumption of a long-distance migratory shorebird. Journal of Experimental Biology, 214(5), 829–835. https://doi.org/10.1242/jeb.048223

[30] Hackett, S. J., Kimball, R. T., Reddy, S., Bowie, R. C., Braun, E. L., Braun, M. J., ... and Yuri, T. (2008). A phylogenomic study of birds reveals their evolutionary history. Science, 320(5884), 1763–1768. https://doi.org/10.1126/science.1157704

[31] Hammel, H. T., Simon-Oppermann, C. H. R. I. S. T. A., and Simon, E. (1980). Properties of body fluids influencing salt gland secretion in Pekin ducks. American Journal of Physiology - Regulatory Integrative and Comparative Physiology, 8(3). https://doi.org/10.1152/ajpregu.1980.239.5.r489

[32] Hanwell, A., and Peaker, M. (1975). The control of adaptive hypertrophy in the salt glands of geese and ducks. The Journal of Physiology, 248(1), 193–205. https://doi.org/10.1113/jphysiol.1975.sp010969

[33] Hanwell, A., Linzell, J. L., and Peaker, M. (1972). Nature and location of the receptors for salt-gland secretion in the goose. J Physiol, 226(2), 453–472. https://doi.org/10.1113/jphysiol.1972.sp009993

[34] Heinz, M. K., and Gray, D. A. (2001). Role of plasma ANG II in the excretion of acute sodium load in a bird with salt glands (Anas platyrhynchos). American Journal of Physiology - Regulatory Integrative and Comparative Physiology, 281(1), 346–351. https://doi.org/10.1152/ajpregu.2001.281.1.r346

[35] Hildebrandt, J. P. (2001). Coping with excess salt: Adaptive functions of extrarenal osmoregulatory organs in vertebrates. Zoology, 104(3–4), 209–220. https://doi.org/10.1078/0944-2006-00026

[36] Holmes, W., and Stewart, D. J. (1968). Changes in the nucleic acid and protein composition of the nasal glands from the duck (Anas platyrhynchos) during the period of adaptation to hypertonic saline. Journal of Experimental Biology, 48(3), 509–519.

[37] Holmes, W. N., Phillips, J. G., and Butler, D. G. (1961). The effect of adrenocortical steroids on the renal and extra-renal responses of the domestic duck (Anas platyrhynchus) after hypertonic saline loading. Endocrinology, 69(3), 483–495. https://doi.org/10.1210/endo-69-3-483

[38] Hootman, S. R., and Ernst, S. A. (1980). Dissociation of avian salt gland: separation procedures and characterization of dissociated cells. American Journal of Physiology - Cell Physiology, 7(3), 184–195. https://doi.org/10.1152/ajpcell.1980.238.5.c184

[39] Hughes, M. R., and Ruch Jr, F. E. (1969). Sodium and potassium in spontaneously produced salt gland secretion and tears of ducks, Anas platyrhynchos , acclimated to fresh and saline waters. Canadian Journal of Zoology, 47(6), 1133–1138. https://doi.org/10.1139/z69-177

[40] Ibañez, L. M., Tambussi, C. P., and Acosta Hospitaleche, C. I. A. (2010). Análisis morfométrico del surco nasal en aves. Ornitologia Neotropical, 21(2), 181–194.

[41] Jacobson, L. (1813). Anatomisk beskrivelse over et nyt organ i huusdyrenes naese. Veter Salesk Skrift, 2, 209–246.

[42] Jobert, C. (1869). Recherches anatomiques sur les glandes nasales des oiseaux,...

[43] Karlsson, K. A., Samuelsson, B. E., and Steen, G. O. (1971). Lipid pattern and Na+-K+-dependent adenosine triphosphatase activity in the salt gland of duck before and after adaptation to hypertonic saline. The Journal of Membrane Biology, 5(2), 169–184. https://doi.org/10.1007/BF02107722

[44] Kolliker, R. V. (1860). A manual of microscopic anatomy. London: Parker.

[45] Krohn, M., and Hildebrandt, J.-P. (2004). Cross-talk of phosphoinositide- and cyclic nucleotide-dependent signaling pathways in differentiating avian nasal gland cells. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 174(6), 461–470. https://doi.org/10.1007/s00360-004-0432-6

[46] Kühnel, W. (1972). On the innervation of the salt gland. Zeitschrift Für Zellforschung Und Mikroskopische Anatomie, 134(3), 435–438. https://doi.org/10.1007/BF00307177

[47] Marais, M., and Gray, D. A. (2009). A role for natriuretic peptide in lipopolysaccharide-induced fever in Pekin ducks (Anas platyrhynchos): Is natriuretic peptide an endogenous antipyretic in birds? Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 179(2), 125–132. https://doi.org/10.1007/s00360-008-0295-3

[48] Marples, B. J. (1932). The Structure and Development of the Nasal Glands of Birds. Proceedings of the Zoological Society of London, 102(4), 829–844. https://doi.org/10.1111/j.1096-3642.1932.tb01565.x

[49] Martin, D. W., Marecek, J., Scarlata, S., and Sachs, J. R. (2000). ?? protomers of Na+,K+-ATPase from microsomes of duck salt gland are mostly monomeric: Formation of higher oligomers does not modify molecular activity. Proceedings of the National Academy of Sciences of the United States of America, 97(7), 3195–3200. https://doi.org/10.1073/pnas.050558397

[50] Mihalkovics. (1898). Nasenhöhl und Jacobson’sches Organ. Eine morphologisch Studie. Anat. Hefte, 11(1).

[51] Müller, C., Sendler, M., and Hildebrandt, J. P. (2006). Downregulation of aquaporins 1 and 5 in nasal gland by osmotic stress in ducklings, Anas platyrhynchos: Implications for the production of hypertonic fluid. Journal of Experimental Biology, 209(20), 4067–4076. https://doi.org/10.1242/jeb.02491

[52] Murphy, R. C. (1936). Oceanic birds of South America. The American Museum of Natural History, 2, 1–6.

[53] Nitzsch, C. L. (1820). Über die Nasendrüse der Vögel. Archiv Physiol.(Meckel’s Archiv), 6, 234–269.

[54] Peaker, M. & Linzell, J. L. (1975). Salt glands in birds and reptiles. In Monographs of the Physiological Society (Issue 32). Monogr Physiol Soc. https://books.google.es/books?hl=es&lr=&id=dZk8AAAAIAAJ&oi=fnd&pg=PR9&dq=Peaker+and+Linzell+(1975).&ots=B7BHiSoLVO&sig=Q-osI7fsOD6WI1vcJYK-6eF8KyQ#v=onepage&q=Peaker and Linzell (1975).&f=false

[55] Peaker, A. and H. M. (1973). The control of adaptive hypertrophy in the salt glands of geese and ducks. The Journal of Physiology, 248(1), 193–205.

[56] Petrushanko, I. Y., Yakushev, S., Mitkevich, V. A., Kamanina, Y. V., Ziganshin, R. H., Meng, X., ... and Bogdanova, A. (2012). S-glutathionylation of the Na,K-ATPase catalytic ? subunit is a determinant of the enzyme redox sensitivity. Journal of Biological Chemistry, 287(38), 32195–32205. https://doi.org/10.1074/jbc.M112.391094

[57] Pratap, P. R., Dediu, O., and Nienhaus, G. U. (2003). FTIR Study of ATP-Induced Changes in Na+/K+-ATPase from Duck Supraorbital Glands. Biophysical Journal, 85(6), 3707–3717. https://doi.org/10.1016/S0006-3495(03)74787-0

[58] Pratap, P. R., Heiss, G., Sikor, M., Lamb, D. C., and Burnett, M. (2011). Single-Molecule Studies of the Na+/K+-ATPase. Biophysical Journal, 100(3), 464a. https://doi.org/10.1016/j.bpj.2010.12.2724

[59] Pratap, P. R., Mikhaylyants, L. O., and Olden-Stahl, N. (2009). Fluorescence measurements of nucleotide association with the Na+/K+-ATPase. Biochimica et Biophysica Acta - Proteins and Proteomics, 1794(11), 1549–1557. https://doi.org/10.1016/j.bbapap.2009.06.023

[60] Randall, D. J., Burggren, W. W. French, K. and Eckert, R. (1998). Eckert fisiología animal: Capítulo 14. Equilibrio iónico y osmótico (4 edition).

[61] Reshag, A. F., Abood, D. A., and Dawood, M. S. (2016). Anatomical and histological study of the kidneys and salt glands in great flamingos (Phoenicopterus roseus). The Iraqi Journal of Veterinary Medicine, 40(1), 140–146. https://doi.org/10.30539/iraqijvm.v40i1.151

[62] Sabat, P. (2000). Birds in marine and saline environments: living in dry habitats. In Revista chilena de historia natural (Vol. 73, Issue 3). https://doi.org/10.4067/s0716-078x2000000300004

[63] Scanes, C. (2015). Sturkie’s Avian Physiology. In Chapter 12 - Osmoregulatory Systems of Birds (6 edition). Academic Pres.

[64] Schmidt-Nielsen, K., and Fange, R. (1958). The Function of the Salt Gland in the Brown Pelican. American Ornithologists’ Union, 75(3), 282–289. https://doi.org/10.2307/4081974

[65] Schmidt-Nielsen, K. (1960). The salt-secreting gland of marine birds. Circulation, 21, 955–967. https://doi.org/10.1161/01.CIR.21.5.955

[66] Schütz, H., Gray, D. A., and Gerstberger, R. (1992). Modulation of kidney function in conscious Pekin ducks by atrial natriuretic factor. Endocrinology, 130(2), 678–684. https://doi.org/https://doi.org/10.1210/endo.130.2.1310279

[67] Shuttleworth, T. J., and Hildebrandt, J. P. (1999). Vertebrate salt glands: Short- and long-term regulation of function. Journal of Experimental Zoology, 283(7), 689–701. https://doi.org/10.1002/(SICI)1097-010X(19990601)283:7<689::AID-JEZ7>3.0.CO;2-T

[68] Shuttleworth, T. J. (1995). Intracellular Signals Controlling Ionic and Acid-Base Regulation in Avian Nasal Gland Cells. In: Heisler N. (eds) Mechanisms of Systemic Regulation: Acid—Base Regulation, Ion-Transfer and Metabolism. Springer US. https://doi.org/10.1007/978-3-642-52363-2_5

[69] Simon-Oppermann, C., Simon, E., Deutsch, H., Möhring, J., and Schoun, J. (1980). Serum arginine-vasotocin (AVT) and afferent and central control of osmoregulation in conscious Pekin ducks. Pflügers Archiv European Journal of Physiology, 387(2), 99–106. https://doi.org/10.1007/BF00584259

[70] Stewart, D. J., Semple, E. W., Swart, G. T., and Sen, A. K. (1975). Induction of the catalytic protein of (Na++ K+)-ATPase in the salt gland of the duck. Biochimica et Biophysica Acta, 419, 150–163. https://doi.org/https://doi.org/10.1016/0005-2736(76)90379-5

[71] Taniguchi, K., Kaya, S., Abe, K., and Mårdh, S. (2001). The oligomeric nature of Na/K-transport ATPase. Journal of Biochemistry, 129(3), 335–342. https://doi.org/10.1093/oxfordjournals.jbchem.a002862

[72] Thesleff, S., and Schmidt-Nielsen, K. (1962). An electrophysiological study of the salt gland of the herring gull. The American Journal of Physiology, 202, 597–600. https://doi.org/10.1152/ajplegacy.1962.202.3.597

[73] Wang, X., Huang, J., Hu, Y., Liu, X., Peteya, J., and Clarke, J. A. (2018). The earliest evidence for a supraorbital salt gland in dinosaurs in new Early Cretaceous ornithurines. Scientific Reports, 8(1), 1–12. https://doi.org/10.1038/s41598-018-22412-8

[74] Woodin, M. C., Michot, T. C., and Lee, M. C. (2008). Salt gland development in migratory redheads (Aythya Americana) in saline environments on the winter range, Gulf of Mexico, USA. Acta Zoologica Academiae Scientiarum Hungaricae, 54(SUPPL.1), 251–264.

Cover image