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

  • M. M. KuklinaEmail author
  • V. V. Kuklin
Comparative and Ontogenic Biochemistry


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.

Key words

kittiwake proteases glycosidases small intestine Alcataenia larina Tetrabothrius erostris 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 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. 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.CrossRefGoogle Scholar
  3. 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.CrossRefGoogle Scholar
  4. 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.CrossRefGoogle Scholar
  5. 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.CrossRefGoogle Scholar
  6. 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. 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.Google Scholar
  8. 8.
    Anson, M., The estimation of pepsin, tripsin, papain and cathepsin with hemoglobin, J. Gen. Physiol., 1938, vol. 22, pp. 79–83.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 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. 10.
    Karasov, W.H. and Diamond, J.M., Interplay between physiology and ecology in digestion, BioScience, 1988, vol. 38, no. 9, pp. 602–611.CrossRefGoogle Scholar
  11. 11.
    Klasing, K.C., Avian gastrointestinal anatomy and physiology, Seminars in Avian and Exotic Pet Medicine, 1999, vol. 8, no. 2, pp. 42–50.CrossRefGoogle Scholar
  12. 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.CrossRefGoogle Scholar
  13. 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.CrossRefGoogle Scholar
  14. 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.CrossRefGoogle Scholar
  15. 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.CrossRefPubMedGoogle Scholar
  16. 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.CrossRefGoogle Scholar
  17. 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.CrossRefGoogle Scholar
  18. 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.CrossRefGoogle Scholar
  19. 19.
    Clayton, D.H. and Moore, J., Host-parasite Evolution: General Principles and Avian Models, Oxford, 1997.Google Scholar
  20. 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.CrossRefGoogle Scholar
  21. 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.CrossRefGoogle Scholar
  22. 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.CrossRefGoogle Scholar
  23. 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.CrossRefGoogle Scholar
  24. 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. 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

Copyright information

© Pleiades Publishing, Ltd. 2018

Authors and Affiliations

  1. 1.Murmansk Marine Biological Institute, Kola Scientific CentreRussian Academy of SciencesMurmanskRussia

Personalised recommendations