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Effect of Cestodal Infestation on the Distribution Pattern of Digestive Enzyme Activities along the Small Intestine of the Kittiwake (Rissa tridactyla)

  • Comparative and Ontogenic Biochemistry
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Abstract

Activities of digestive enzymes in the intestine of adult and nestling kittiwakes (Rissa tridactyla) were studied. Glycosidase and protease activities in the three parts of the small intestine (proximal, medial and distal) as well as their total activity were determined, and the glycosidase/protease activity ratio (G/P coefficient) was calculated. Enzyme activities were found to be distributed unevenly along the intestine. In a proximal to distal direction, glycosidase and protease activities decrease in nestlings and increase in adult kittiwakes. In nestlings, protease activity values are several times higher than in adults. G/P coefficient values vary within the range of 0.33–0.92 in adult animals and 0.22–0.41 in nestlings. Infestation with tapeworms Alcataenia larina (Cestoda, Dilepididae) and Tetrabothrius erostris (Cestoda, Tetrabothriidae) leads to reduced digestive enzyme activities in the small intestine of kittiwake nestlings. In adult animals, infestation with T. erostris leads to a reduced and with A. larina to an increased protease activity.

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References

  1. Belopolsky, L.O., Ekologiya morskikh kolonial’nykh ptits Barentseva morya (Ecology of Marine Colonial Birds of the Barents Sea), Moscow, Leningrad, 1957.

    Google Scholar 

  2. Kitaysky, A.S., Wingfield, J.C., and Piatt, J.F., Dynamics of food availability, body condition and physiological stress response in breeding Blacklegged Kittiwakes, Funct. Ecol., 1999, vol. 13, pp. 577–584.

    Article  Google Scholar 

  3. Bech, C., Langseth, I., Moe, B., Fyhn, M., and Gabrielsen, G.W., The energy economy of the arctic-breeding Kittiwake (Rissa tridactyla): a review, Comparative Biochemistry and Physiology, pt. A, 2002, vol. 133, pp. 765–770.

    Article  CAS  Google Scholar 

  4. Moe, B., Langseth, I., Fynn, M., Gabrielsen, G.W., and Bech, C., Changes in body condition in breeding kittiwakes Rissa tridactyla, J. Avian Biol., 2002, vol. 33, pp. 225–234.

    Article  Google Scholar 

  5. Broggi, Y., Langset, M., Rønning, B., Welcker, J., and Bech, C., Parent kittiwakes experience a decrease in cell-mediated immunity as they breed, J. Ornithol., 2010, vol. 151, pp. 723–727.

    Article  Google Scholar 

  6. Kuklin, V.V., Helminthofauna of the kittiwake (Rissa tridactyla) of the Barents Sea, Zool. Zh., 2013, vol. 92, no. 7, pp. 781–789.

    Google Scholar 

  7. Alekseenko, L.N., Determination of proteinase activity by cleavage of protein substrates, Sovremennye metody v biokhimii (Modern Methods in Biochemistry), vol. 2, Moscow, 1968.

  8. Anson, M., The estimation of pepsin, tripsin, papain and cathepsin with hemoglobin, J. Gen. Physiol., 1938, vol. 22, pp. 79–83.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Ugolev, A.M. and Iezuitova, N.N., Determination of activity of invertase and other disaccharidases, Issledovanie pishchevaritel’nogo apparata u cheloveka: obzor sovremennykh metodov (Investigation of the Human Digestive Apparatus: A Review of Modern Methods), Leningrad, 1969, pp. 187–192.

    Google Scholar 

  10. Karasov, W.H. and Diamond, J.M., Interplay between physiology and ecology in digestion, BioScience, 1988, vol. 38, no. 9, pp. 602–611.

    Article  CAS  Google Scholar 

  11. Klasing, K.C., Avian gastrointestinal anatomy and physiology, Seminars in Avian and Exotic Pet Medicine, 1999, vol. 8, no. 2, pp. 42–50.

    Article  Google Scholar 

  12. Ramirez-Otarola, N., Narváez, C., and Sabat, P., Membrane-bound intestinal enzymes of passerine birds: dietary and phylogenetic correlates, J. Comp. Physiol., 2011, vol. 181, pp. 817–827.

    Article  CAS  Google Scholar 

  13. Meynard, C., Lopez-Calleja, M.V., and Bozinovic, P., Digestive enzymes of a small avian herbivore the rufous-tailed plantcutter, The Condor, 1999, vol. 101, pp. 904–907.

    Article  Google Scholar 

  14. Konarzewski, M., Kozlowski, J., and Ziólko, M., Optimal allocation of energy to growth of the alimentary tract in birds, Funct. Ecol., 1989, vol. 3, no. 5, pp. 589–596.

    Article  Google Scholar 

  15. Schondube, J.E. and Martinez del Rio, C., Sugar and protein digestion in flowerpiercers and hummingbirds: a comparative test of adaptive convergence, J. Comp. Physiol. B, 2004, vol. 174, pp. 263–273.

    Article  PubMed  CAS  Google Scholar 

  16. Kuklina, M.M., Interrelation on the digestive processes of the northern fulmar Fulmarus glacialis and the cestode Tetrabothrius minor (Cestoda: Tetrabothriidae), Doklady Akad. Nauk, Biol. Sci., 2012, vol. 446, no. 1, pp. 310–312.

    Article  CAS  Google Scholar 

  17. Martínez del Río, C., Brugger, K.E., Rios, J.L., Vergara, M.E., and Witmer, M., An experimental and comparative study of dietary modulation of intestinal enzymes in european starlings (Sturnus vulgaris), Physiol. Zool., 1995, vol. 68, no. 3, pp. 490–511.

    Article  Google Scholar 

  18. Kuklina, M.M. and Kuklin, V.V., The activities of digestive enzymes as a determinant factor in localization of Tetrabothrius erostris (Loennberg) (Cestoda: Tetrabothriidae) in the intestine of the herring gull Larus argentatus Pontoppidan, J. Water Biol., 2016, vol. 9, no. 2, pp. 189–195.

    Article  Google Scholar 

  19. Clayton, D.H. and Moore, J., Host-parasite Evolution: General Principles and Avian Models, Oxford, 1997.

    Google Scholar 

  20. Dalton, J.P., Skelly, P., and Halton, D.W., Role of the tegument and gut in nutrient uptake by parasitic platyhelminths, Can. J. Zool., 2004, vol. 82, pp. 211–232.

    Article  Google Scholar 

  21. Kuklina, M. M. and Kuklin, V.V., Peculiarities of protein hydrolysis on the digestive-transport surfaces of the intestine of the kittiwake Rissa tridactyla and Alcataenia larina (Cestoda: Dilepidi dae) parasitizing it, Biol. Bull., 2011, vol. 38, no. 5, pp. 470–475.

    Article  Google Scholar 

  22. Izvekova, G.I., Kuklina, M.M., and Frolova, T.V., Inactivation of proteolytic enzymes by cestodes, Doklady Akad. Nauk, Biol. Sci., 2017, vol. 475, no. 4, pp. 161–164.

    Article  CAS  Google Scholar 

  23. Izvekova, G.I., Izvekov, E.I., and Solovyov, M.M., Effect of Caryophyllaeus laticeps (Cestoda, Caryophyllidea) upon activity of digestive enzymes in bream, Biol. Bull., 2011, vol. 38, no. 1, pp. 50–56.

    Article  CAS  Google Scholar 

  24. Ryzhikov, K.M., Rysavy, B., Khokhlova, I.G., Tolkatchova, L.M., and Kornyuchin, V.V., Helminths of Fish-Eating Birds of the Palaearctic Region. 2. Moscow; Prague: USSR Acad. Sci., Helminthol. Lab. Czechoslovak Acad. Sci., Inst. Parasitol. Charles Univ. Prague, Faculty Sci., 1985.

    Google Scholar 

  25. Ugolev, A.M., Evolyutsiya pishchevareniya i printsipy evolyutsii funktsii: Elementy sovremennogo funktsionalizma (Evolution of Digestion and Principles of Evolution of Functions: Elements of Modern Functionalism), Leningrad, 1985.

    Google Scholar 

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Correspondence to M. M. Kuklina.

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Original Russian Text © M.M. Kuklina, V.V. Kuklin, 2018, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2018, Vol. 54, No. 4, pp. 257–263.

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Kuklina, M.M., Kuklin, V.V. Effect of Cestodal Infestation on the Distribution Pattern of Digestive Enzyme Activities along the Small Intestine of the Kittiwake (Rissa tridactyla). J Evol Biochem Phys 54, 292–299 (2018). https://doi.org/10.1134/S0022093018040051

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  • DOI: https://doi.org/10.1134/S0022093018040051

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