Variation of heterophil-to-lymphocyte ratio in the Great Tit Parus major - a review

• Autorzy: Skwarska J.

Warianty tytułu

PL

Zróznicowanie proporcji heterofili do limfocytów u bogatki - przegląd badań

• Języki publikacji: EN

Abstrakty

EN

Permanent changes in the surrounding environment cause long-term stress in birds, which, when lasting days or weeks, affects the activity of the immune system and increases susceptibility to diseases, leading to changes in the levels of haematological parameters. The heterophil-to-lymphocyte ratio (H:L-ratio) is generally considered an independent and robust indicator of stress level in birds. This parameter allows in a simple way to evaluate activity of the immune system and individual health state of adult and nestling birds. It also enables assessing a body response to short- and long-term stress induced by, among others, the surrounding environment, social stress, blood parasites or a greater energy expenditure of females during breeding. Under conditions of field work the determination of the H:L- ratio is not difficult because what is only needed to conduct a blood smear test is a drop of blood that can be easily obtained even from birds of a small body mass. Moreover, an increase in the H:L-ratio is observed after about an hour from the moment of catching a bird contrary to other measurements like the determination of a baseline level of corticosterone. In this article available literature that discusses the impact of various factors on the H:L-ratio in the Great Tit as a species of 'fast-paced' life is reviewed. In adult and nestling birds the H:L-ratio is influenced by various factors — ecological and ecophysiological ones. In some cases the same factor, e.g. brood size manipulation or a type of habitat, can significantly influence the level of the discussed stress indicator as well as it may not show any impact at all. While interpreting the H:L-ratio one must take into account an impact of various ecological and ecophysiological factors on health state, such as habitat, phase of the annual cycle, differences between brood attempts, sex, age as well as on relations with other indicators of condition e.g. body mass or total blood haemoglobin concentration.

PL

Zgodnie z dostępną literaturą proporcję heterofili do limfocytów (H:L) można uznać za niezależny wskaźnik poziomu stresu u ptaków dorosłych, jak i piskląt. Parametr ten może być stosowany jako wskaźnik stanu biologicznego organizmu pozwalający na ocenę stanu zdrowia ptaków. W połączeniu z innymi parametrami kondycji organizmu, np.: hematologicznymi albo biochemicznymi, poziom proporcji H:L pozwala w prosty sposób ocenić zróżnicowanie stanu zdrowia organizmów dziko żyjących, jak również laboratoryjnych. Ustalenie poziomu proporcji H:L nie jest trudne w pracy terenowej, ponieważ do wykonania rozmazu wystarczy tylko kropla krwi co umożliwia m.in. prowadzenie badań na ptakach o małej masie ciała. Ponadto zmiana poziomu proporcji H:L, następuje dopiero po upływie około godziny od momentu złapania ptaka. W pracy dokonano przeglądu danych zebranych dla bogatki, modelowego gatunku dziuplaka. Na istotne zróżnicowanie albo jego brak w poziomie proporcji H:L u dorosłych, jak i piskląt sikory bogatki mogą wpływać czynniki ekologiczne i ekofizjologiczne (Tab. 2 i 3). Obserwuje się także pewną zmienność geograficzną (Tab. 1). Przy wyjaśnieniu uzyskanych wyników należy pamiętać, że interpretacja wyników proporcji H:L może powodować pewne trudności. Na przykład, wysoka liczba heterofili we krwi, a jednocześnie wysoki stosunek H:L, może sugerować trwającą chorobę, albo przeciwnie, może odzwierciedlać szybką odpowiedź organizmu na obecność patogenów w ustroju. Ponadto interpretując proporcję H:L należy wziąć pod uwagę wpływ różnych czynników ekologicznych i ekofizjologicznych na stan zdrowia ptaków, takich jak habitat, płeć oraz związki z innymi wskaźnikami kondycji organizmu, np. masa ciała lub stężenie hemoglobiny we krwi. Podsumowując, zaleca się kontynuowanie dalszych badań dotyczących stosunku H:L, które umożliwią osiągnięcie pełniejszej oceny wartości poznawczych tego wskaźnika stresu u ptaków. Prowadzone obserwacje powinny również koncentrować się na wyjaśnieniu, czy wzrost stosunku H:L we krwi obwodowej wynika jedynie z dobrego stanu biologicznego osobnika, czy wręcz przeciwnie, jest to znak trwającej choroby w ciele. Jednak pomimo pewnych wad stosunek H:L jest niezależnym i wygodnym wskaźnikiem z uwagi na jego powtarzalność, prostotę i szybkość uzyskania.

Słowa kluczowe

EN

variation; heterophil; lymphocyte ratio; bird; Great Tit; Parus major; physiological stress; hematological parameter; hole nesting bird; passerine bird

• Wydawca: -
• Czasopismo: Acta Ornithologica
• Rocznik: 2018
• Tom: 53
• Numer: 2
• Opis fizyczny: p.103-114,ref.

Twórcy

autor

Skwarska J.

• Department of Experimental Zoology and Evolutionary Biology, Faculty of Biology and Environmental Protection, University of Lodz, Banacha 12/16, 90–237 Lodz, Poland

Bibliografia

• Bairlein F. 1995. European-African songbird migration network. Manual of field methods. ESF Network Field Instruction, Wilhelmshaven, Germany.
• Bańbura J., Bańbura M., Glądalski M., Kaliński A., Markowski M., Michalski M., Nadolski J., Skwarska J., Zielinski E 2011. Body condition parameters of nestling Great Tits Parus major in relation to experimental food supplementation. Acta Ornithol. 46: 207-212.
• Bańbura J., Perret P., Blondel J., Sauvages A., Galan M.-J., Lambrechts M. 2001. Sex differences in parental care in a Corsican Blue Tit Parus caeruleus population. Ardea 89: 517-526.
• Bańbura J., Skwarska J., Bańbura M., Glądalski M., Hołysz M., Kaliński A., Markowski M., Wawrzyniak J., Zieliński P. 2013. Spatial and temporal variation in heterophil-to-lymphocyte ratios of nestling passerine birds: comparison of blue tits and great tits. PLOS ONE 8(9): e74226.
• Bańbura J., Skwarska J., Kaliński A., Wawrzyniak J., Słomczyński R., Bańbura M.; Zieliński P 2008. Effects of brood size manipulation on physiological condition of nestling Blue Tits Cyanistes caeruleus. Acta Ornithol. 43: 129-138.
• Biard C., Monceau K., Motreuil S., Moreau J. 2015. Interpreting immunological indices: The importance of taking parasite community into account. An example in blackbirds Turdus merula. Meth. Ecol. Evol. 6: 960-972.
• Bishop C. R., Athens J. W., Boggs D. R., Warner H. R., Cartwrig G., Wintrobe M. M. 1968. Leukokinetic Studies. 13. A non-steadystate kinetic evaluation of mechanism of cortisone-induced granulocytosis. J. Clin. Invest. 47: 249-260.
• Brinkhof M. W. G., Heeb P., Kölliker M., Richner H. 1999. Immunocompetence of nestling great tits in relation to rearing environment and parentage. Proc. R. Soc. bond. В 266: 2315-2322.
• Buczek J., Deptuła W., Gliński Z., Jarosz J., Stosik M., Wernicki A. 1999. [Comparative and developmental immunology of animals]. PWN, Warszawa-Poznań.
• Campbell T. W. (eds). 1995. Avian hematology and cytology. 2nd edn. Iowa State Univ. Press, Ames.
• Cirule D., Krama T., Vrublevska J., Rantala M. J., Krams I. 2012. A rapid effect of handling on counts of white blood cells in a wintering passerine bird: a more practical measure of stress? J. Ornithol. 153:161-166.
• Cosgrove C. L., Wood M. J., Day K. P., Sheldon В. C. 2008. Seasonal variation in Plasmodium prevalence in a population of blue tits Cyanistes caeruleus. J. Anim. Ecol. 77: 540-548.
• Davis A. K., Cook K. C., Altizer S. 2004. Leukocyte profiles in wild House Finches with and without mycoplasmal conjunctivitis, a recently emerged bacterial disease. Ecohealth 1: 362-373.
• Davis A. K. 2005. Effect of handling time and repeated sampling on avian white blood cell counts. J. Field Ornithol. 76: 334-338.
• Davis A. K. 2009. The wildlife leukocytes webpage: the ecologist's source for information about leukocytes of wildlife species. Available at: http://wildlifehematology.uga.edu
• Davison F., Kaspers B., Schat K. A. 2008. Avian immunology. Elsevier, London.
• Dawson W. R., Marsh R. L. 1989. Metabolic acclimatization to cold and season in birds. In: Bech C., Reinertsen R. E. (eds). Physiology of cold adaptation in birds. Plenum, New York, pp. 83-94.
• Dhabhar F. S. 2002. A hassle a day may keep the doctor away: stress and the augmentation of immune function. Integr. Comp. Biol. 42: 556-564.
• Dufva R., Allander K. 1995. Intraspecific variation in plumage coloration reflects immune response in Great Tit (Parus major) males. Funct. Ecol. 9: 785-789.
• Dufva R., Allander K. 1996. Variable effects of the Hen Flea Ceratophyllus gallinae on the breeding success of the Great Tits Parus major in relation to weather condition. Ibis 138: 772-777.
• Dunn J. C., Goodman S. J., Benton T. G., Hamer K. C. 2013. Avian blood parasite infection during the non-breeding season: an overlooked issue in declining populations? BMC Ecology 13: 30.
• Fair J. M., Paul E., Jones J. (eds). 2010. Guidelines to the use of wild birds in research. Ornithological Council, Washington.
• Fauci A. S. 1975. Mechanisms of corticosteroid action on lymphocyte subpopulations. I. Redistribution of circulating T-lymphocytes and B-lymphocytes to bone marrow. Immunol. 28: 669-680.
• Fudge A. M. 1989. Avian hematology: identification and interpretation. Proc. Assoc. Avian. Vet. Annu. Meet., pp. 284-292.
• Garnett M. C. 1981. Body size, its heritability and influence on juvenile survival among great tits, Parus major. Ibis 123: 31-41.
• Gaunt A. S., Oring L. W. (eds). 1999. Guidelines to the use of wild birds in research. 2nd edn. Ornithological Council, Washington.
• Genovese K. J., He H., Swaggerty C. L., Kogut M. H. 2013. The avian heterophils. Dev. Comp. Immunol. 41: 334-340.
• Gill F. B. 2007. Ornithology. 3rd edn. Acad. Nat. Sci., Philadelphia.
• Gosler A. G. 1993. The Great Tit. Hamlyn, London.
• Gross W. B., Siegel H. S. 1983. Evaluation of heterophil/lymphocyte ratio as a measure of stress in chickens. Avian Dis. 27: 972-979.
• Harmon B. G. 1998. Avian heterophils in inflammation and disease resistance. Poult. Sd. 77: 972-977.
• Hinam H. L., St. Clair C. C. 2008. High levels of habitat loss and fragmentation limit reproductive success by redudng home range size and provisioning rates of Northern saw-whet owls. Biol. Conserv. 141: 524-535.
• Hõrak P. 1994. Effect of nestling history on adult size and reproduction in the great tit. Ornis Fennica 71: 47-54.
• Hõrak P., Jenni-Eiermann S., Ots I., Tegelmann L. 1998a. Health and reproduction: sex-specific clinical profile of Great Tits Parus major in relation to breeding. Can. J. Zool. 76: 2235-2244.
• Hõrak P., Ots I., Murumägi A. 1998b. Haematological health state indices of reproducing Great Tits: a response to brood size manipulation. Funct. Ecol. 12: 750-756.
• Hõrak P., Ots I., Tegelmann L., Møller A. P. 2000. Health impact of phytohaemagglutinin-induced immune challenge on great tit (Parus major) nestlings. Can. J. Zool. 78: 905-910.
• Hõrak P., Tegelmann L., Ots I., Møller A. P. 1999. Immune function and survival of great tit nestlings in relation to growth conditions. Oecologia 121: 316-322.
• Ilmonen P., Hasselquist D., Langefors Å., Wiehn J. 2003. Stress, immunocompetence and leucocyte profiles of pied flycatchers in relation to brood size manipulation. Oecologia 136: 148-154.
• Johnston R. D. 1993. Effects of diet quality on the nestling growth of a wild insectivorous passerine, the house martin Delichon urbica. Funct. Ecol. 7: 255-266.
• Jones R. G., Faust A. M., Matthews R. A. 1995. Quality team approach in evaluating three automated hematology analyzers with five-part differential capability. Am. J. Clin. Pathol. 103:159-166.
• Kaliński A., Bańbura M., Glądalski M., Markowski M., Skwarska J., Wawrzyniak J., Zieliński P., Cyżewska I., Bańbura J. 2015. Long-term variation in hemoglobin concentration in nestling great tits Parus major. Comp. Biochem. Physiol. A 185: 9-15.
• Kilgas P., Mägi R., Mägi M., Tilgar V 2006a. Hematological parameters in brood-rearing great tits in relation to habitat, multiple breeding and sex. Comp. Biochem. Physiol. A144: 224-231.
• Kilgas P., Tilgar V, Mänd R. 2006b. Hematological health state indices predict local survival in a small passerine bird, the great tit (Parus major). Physiol. Biochem. Zool. 79: 565-572.
• Krama T., Suraka V, Hukkanen M., Rytkönen S., Orell M., Cirule D., Rantala M. J., Krams I. 2013. Physiological condition and blood parasites of breeding Great Tits: a comparison of core and northernmost populations. J. Ornithol. 154:1019-1028.
• Krams I., Cirule D., Krama T., Hukkanen M., Rytkönen S., Orell M., Iezhova T., Rantala M.J., Tummeleht L. 2010a. Effects of forest management on haematological parameters, blood parasites, and reproductive success of the Siberian tit (Poecile cinctus) in northern Finland. Ann. Zool. Fenn. 47: 335-346.
• Krams I., Cirule D., Krama T., Vrublevska J. 2011. Extremely low ambient temperature affects haematological parameters and body condition in wintering Great Tits Parus major. J. Ornithol. 152: 889-895.
• Krams I., Cirule D., Suraka V., Krama T., Rantala M. J., Ramey G. 2010b. Fattening strategies of wintering great tits support the optimal body mass hypothesis under condition of extremely ambient temperature. Funct. Ecol. 24: 172-177.
• Krams I. A., Suraka V., Rantala M. J., Sepp T., Mierauskas P., Vrublevska J., Krama T. 2013a. Acute infection of avian malaria impairs concentration of haemoglobin and survival in juvenile altricial birds. J. Zool. 291: 34-41.
• Krams I., Vrublevska J., Cirule D., Kivleniece I., Krama T., Rantala M., Kaasik A., Hõrak P., Sepp T. 2013b. Stress, behaviour and immunity in wild-caught wintering Great Tits (Parus major). Ethol. 119: 397-406.
• Krams I., Vrublevska J., Cirule D., Kivleniece I., Krama T., Rantala M., Sild E., Hõrak P. 2012. Heterophil/lymphocyte ratios predict the magnitude of humoral immune response to a novel antigen in great tits Parus major. Comp. Biochem. Physiol. A 161: 422-128.
• Krohne D. T. 2001. General ecology. 2nd edn. Brooks/Cole, Pacific Grove.
• Latimer K. S., Bienzle D. 2000. Determination and interpretation of the avian leukogram. In: Feldman B. F., Zinkl J. G., Jain N. C. (eds). Schalm's veterinary hematology. 5th edn. Williams and Wilikins, Philadelphia, pp. 417-432.
• Latshaw J. D. 1991. Nutrition — mechanisms of immunosuppresion. Vet. Immunol. Immunopathol. 30:111-120.
• Lowry V. K., Genovese K. J., Bowden L. L., Kogut M. H. 1997. Ontogeny of the phagocytic and bactericidal activities of turkey heterophils and their potentiation by Salmonella enteritidis-immune lymphokines. FEMS Immunol. Med. Microbiol. 19: 95-100.
• Lõhmus A., Remm J. 2005. Nest quality limits the number of hole-nesting passerines in their natural cavity-rich habitat. Acta Oecol. 27: 125-128.
• Marsh R. L., Dawson W. R. 1989. Avian adjustments to cold. 4th edn. Springer, Berlin.
• Maxwell M. H. 1993. Avian blood leucocyte responses to stress. World Poult. Sci. J. 49: 34-43.
• Maxwell M. H., Robertson G. W. 1998. Xhe avian heterophil leucocyte: a review. World Poult. Sci. J. 54:155-178.
• Mägi M., Mänd R. 2004. Habitat differences in allocation of eggs between successive breeding attempts in great tits Parus major. Ecoscience 11: 361-369.
• Mänd R., Tilgar V., Lõhmus A., Leivits A. 2005. Providing nest boxes for hole-nesting birds: does habitat matter? Biodivers. Conserv. 14:1823-1840.
• Merrill L., Grindstaff J. L. 2014. Maternal antibody transfer can lead to suppression of humoral immunity in developing zebra finches (Taeniopygia guttata). Physiol. Biochem. Zool. 87: 740-751.
• Moreno J., Merino S., Martínez J., Sanz J. J., Arriero E. 2002. Heterophil/lymphocyte ratios and heat-shock protein levels are related to growth in nestling birds. Ecoscience 9: 434-439.
• Müller C., Jenni-Eiermann S., Jenni L. 2011. Heterophils/Lymphocytes-ratio and circulating corticosterone do not indicate the same stress imposed on Eurasian kestrel nestlings. Funct. Ecol. 25: 566-576.
• Nadolski J., Skwarska J., Kaliński A., Bańbura M., Śnieguła R., Bańbura J. 2006. Blood parameters as consistent predictors of nestling performance in great tit Parus major in the wild. Comp. Biochem. Physiol. A 143: 50-54.
• Naef-Daenzer B., Keller L. F. 1999. The foraging performance of great and blue tits (Parus major and P. caeruleus) in relation to caterpillar development, and its consequences for nestling growth and fledging weight. J. Anim. Ecol. 68: 708-718.
• Niu H. 2007. Effects of forest fragmentation on the physiology and health status of wood thrush (Hylocichla mustelina) in the upper Midwest. University of Michigan.
• Norris K., Evans M. R. 2000. Ecological immunology: life history trade-offs and immune defence in birds. Behav. Ecol. 11: 19-26.
• Norte A. C., Araújo P M., Sampaio H. L., Sousa J. P., Ramos J. A. 2009a. Haematozoa infections in a Great Tit Parus major population in Central Portugal: relationships with breeding effort and health. Ibis 151: 677-688.
• Norte A. C., Ramos J. A., Sousa J. P., Sheldon B. C. 2009b. Variation of adult Great Tit Parus major body condition and blood parameters in relation to sex, age, year and season. J. Ornithol. 150: 651-660.
• Norte A. C., Sheldon B. C., Sousa J. P., Ramos J. A. 2009c. Environmental and genetic variation in body condition and blood profile of great tit Parus major nestlings. J. Avian Biol. 40: 157-165.
• Ots I., Hõrak P. 1996. Great tits Parus major trade health for reproduction. Proc. R. Soc. Lond. В 263:1443-1447.
• Ots I., Hõrak P. 1998. Health impact of blood parasites in breeding Great Tits. Oecologia 116: 441-448.
• Ots I., Murumägi A., Hõrak P. 1998. Haematological health state indices of reproducing Great Tits: methodology and sources of natural variation. Funct. Ecol. 12: 700-707.
• Ots I., Kerimov A. B., Ivankina E. V., Ilyina T. A., Hõrak P. 2001. Immune challenge affects basal metabolic activity in wintering great tits. Proc. R. Soc. Lond. В 268:1175-1181.
• Pap P. L., Márkus R. 2003. Cost of reproduction, T-lymphocyte mediated immunocompetence and health status in female and nestling barn swallows Hirundo rustica. J. Avian Biol. 34: 428-434.
• Pap P. L., Vágási C. I., Tökölyi J., Czirják G. Á., Barta Z. 2010. Variation in haematological indices and immune function during the annual cycle in the Great Tit Parus major. Ardea 98:105-112.
• Pap P. L., Vágási C. I., Vincze O., Osváth G., Szászka J. V., Czirják G. Á. 2015. Physiological pace of life: the link between constitutive immunity, developmental period, and metabolic rate in European birds. Oecologia 177:147-158.
• Perrins C. M. 1979. British Tits. Collins, London.
• Perrins C. M. 1991. Tits and their caterpillar food supply. Ibis 133: 49-54.
• Perrins C. M., McCleery R. H. 1989. Laying dates and clutch size in the great tit. Wilson Bull. 101: 236-253.
• Powell C., Lill A., Johnstone C. P. 2013. Body condition and chronic stress in urban and rural noisy miners. Open Ornithol. J. 6: 25-31.
• Råberg L., Grahn M., Hasselquist D., Svensson E. 1998. On the adaptive significance of stress-induced immunosuppression. Proc. R. Soc. Lond. В 265:1637-1641.
• Ricklefs R. E. 1979. Adaptation, constraint, and compromise in avian postnatal development. Biol. Rev. Camb. Philos. Soc. 54: 269-290.
• Roff D. A. 1992. The evolution of life histories. Theory and analysis. Chapman and Hall, New York.
• Romero L. M., Romero R. C. 2002. Corticosterone responses in wild birds: the importance of rapid initial sampling. Condor 104:129-135.
• Selinger C., Schaerer В., Kohn M, Pendl H., Weigend S., Kaspers B., Härtle S. 2012. A rapid high-precision flow cytometry based technique for total white blood cell counting in chickens. Vet. Immunol. Immunopathol. 145: 86-99.
• Sharma J. M. 1991. Overview of the avian immune system. Vet. Immunol. Immunopathol. 30:13-17.
• Sheldon B. C., Verhulst S. 1996. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol. Evol. 11: 317-321.
• Shini S., Kaiser P., Shini A., Bryden W. L. 2008. Biological response of chickens (Gallus gallus domesticus) induced by corticosterone and a bacterial endotoxin. Comp. Biochem. Physiol. В 149: 324-333.
• Skwarska J. 2007. [Variation of condition indexes of nestling Blue Tits Cyanistes caeruleus in urban parkland and in forest]. PhD dissertation. University of Lodz.
• Smits J. E. 2007. Are we enlightened about the immunocompetence of a severely inbred population of New Zealand robins? Challenges inherent in studies using immunological endpoints. Anim. Conserv. 10:14-16.
• Stabler J. G., McCormick T. W., Powell K. C., Kogut M. H. 1994. Avian heterophils and monocytes: phagocytic and bactericidal activities against Salmonella enteritidis. Vet. Microbiol. 38: 293-305.
• Stearns S. C. 1992. The evolution of life histories. Oxford Univ. Press, Oxford.
• Suorsa P., Helle H., Koivunen V., Huhta E., Nikula A., Hakkarainen H. 2004. Effects of forest patch size on physiological stress and immunocompetence in an area-sensitive passerine, the Eurasian treecreeper Certhia familiaris: an experiment. Proc. R. Soc. Lond. В 271: 435-440.
• Svensson E., Råberg L., Koch C., Hasselquist D. 1998. Energetic stress, immunosuppression and the costs of an antibody response. Funct. Ecol. 12: 912-919.
• Totzke U., Fenske M., Huppop O., Raabe H., Schach N. 1999. The influence of fasting on blood and plasma composition of Herring Gulls (Larus argentatus). Physiol. Biochem. Zool. 72: 426-437.
• Tummeleht L. 2006. Physiological condition and immune function in great tits Parus major: sources of variation and tradeoffs in relation to growth. PhD dissertation. University of Tartu.
• van Balen J. H. 1973. A comparative study of the breeding ecology of the great tit Parus major in different habitats. Ardea 61: 1-93.
• van der Meer E., Van Oers K. 2015. Gender and personality differences in response to social stressors in Great Tits (Parus major). Plos One 10(5): e0127984.
• Walberg J. 2001. White blood cell counting techniques in birds. Semin. Avian Exotic Pet Med. 10: 72-76.
• Washburn B. E., Morris D. L., Millspaugh J. J., Faaborg J., Schulz J. H. 2002. Using a commercially available radioimmunoassay to quantify corticosterone in avian plasma. Condor 104: 558-563.
• Wells L. L., Lowry V. K., DeLoach J. R., Kogut M. H. 1998. Age-dependent phagocytosis and bactericidal activities of the chicken heterophil. Dev. Comp. Immunol. 22:103-109.
• Wojczulanis-Jakubas K., Jakubas D., Czujkowska A., Kulaszewicz I., Kruszewicz A. G. 2012. Blood parasite infestation and the leukocyte profiles in adult and immature reed warblers (Acrocephalus scirpaceus) and sedge warblers (Acrocephalus schoenobaenus) during autumn migration. Ann. Zool. Fenn. 49: 341-349.

Identyfikatory

DOI

10.3161/00016454AO2018.53.2.001