Journal of Comparative Physiology B

, Volume 181, Issue 5, pp 641–648 | Cite as

Leucocyte profiles and H/L ratios in chicks of Red-tailed Tropicbirds reflect the ontogeny of the immune system

  • Nina DehnhardEmail author
  • Petra Quillfeldt
  • Janos C. Hennicke
Original Paper


Immune defence is fundamentally important for the survival prospects of young animals. While innate immunity offers initial protection from a variety of pathogens, acquired immunity responds more specifically to pathogens, but is considered to be more costly and to respond slower. Moreover, the acquired immunity is not yet fully developed in neonatal chicks. Little is known about the ontogeny of the immune system of wild birds. Long-lived seabirds, with their slow chick development, are good models to investigate how young birds invest in both arms of their immune system. We determined leucocyte profiles and heterophil to lymphocyte (H/L) ratios of Red-tailed Tropicbirds (Phaeton rubricauda westralis) on Christmas Island, Indian Ocean. Young chicks (N = 10) had significantly higher H/L ratios than older chicks (N = 19), while adults (N = 47) showed intermediate values and did not differ from either chick age class. High H/L ratios in young chicks were caused by high initial numbers of heterophils per 10,000 erythrocytes that declined with age. In contrast, the number of lymphocytes per 10,000 erythrocytes was similar for young and older chicks. These data suggest that young chicks invested heavily in innate immunity to protect themselves from pathogens, while investment into acquired immunity became more important in older chicks with a functional acquired immune response. Body condition did not have a significant influence on any leucocyte parameter.


Tropical seabirds H/L ratio Ontogeny of immune system Leucocyte profiles 



This study was conducted within the framework of the Christmas Island Seabird Project ( which is supported by the University of Hamburg, Christmas Island Tourist Association, Island Explorer Holidays, Christmas Island Territory Week Committee and Christmas Island Care. Austasian Airlines and Globetrotter Hamburg provided in-kind support. Parks Australia North Christmas Island and Darwin issued all necessary permits. We would like to thank J. Navarro, L. Braun, M. van der Stap for their help in the field, M. Helmer for help with staining, Parks Christmas Island for accommodation and logistical support, and Prof. M. Spindler, IPÖ, Kiel, for providing lab space and equipment. The manuscript benefited from the comments of J. Lodde Greives and four anonymous referees. All aspects of the study were carried out under license and in accordance with the principles and guidelines of the German and Australian laws on animal welfare.


  1. Bar-Shira E, Sklam D, Friedman A (2003) Establishment of immune competence in the avian GALT during the immediate post-hatch period. Develop Comp Immunol 27:147–157CrossRefGoogle Scholar
  2. Betti F, Sesso A (1989) An allometric study of the development of the cloacal bursa in the domestic fowl. Anat Anzeig 168:255–260Google Scholar
  3. Davis AK (2005) Effect on handling time and repeated sampling on avian white blood cell counts. J Field Ornithol 76:334–338Google Scholar
  4. Davis GS, Anderson KE, Carroll AS (2000) The effects of long-term caging and molt of single comb white leghorn hens on heterophil to lymphocyte ratios, corticosterone and thyroid hormones. Poult Sci 79:514–518PubMedGoogle Scholar
  5. Davis AK, Maney DL, Maerz JC (2008) The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct Ecol 22:760–772CrossRefGoogle Scholar
  6. Dehnhard N, Poisbleau M, Demongin L, Quillfeldt P (2010) Leucocyte profiles and corticosterone in chicks of southern rockhopper penguins. J Comp Physiol B. doi: 10.1007/s00360-010-0508-4 PubMedGoogle Scholar
  7. DeLong JP, Gessaman JA (2001) A comparison of noninvasive techniques for estimating total body fat in sharp-shinned and cooper’s hawks. J Field Ornithol 72:349–364Google Scholar
  8. Engström H, Dufva R, Olsson G (2000) Absence of haematozoa and ectoparasites in a highly sexually ornamented species, the Crested Auklet. Waterbirds 23:486–488Google Scholar
  9. Fellah JS, Jaffredo T, Dunon D (2008) Development of the Avian Immune System. In: Davidson F, Kaspers B, Schat KA (eds) Avian immunology, 1st edn. Elsevier, London, pp 51–66CrossRefGoogle Scholar
  10. Figuerola J, Muñoz E, Gutiérrez R, Ferrer D (1999) Blood parasites, leucocytes and plumage brightness in the cirl bunting, Emberiza cirlus. Funct Ecol 13:594–601CrossRefGoogle Scholar
  11. Fox J, Weisberg S (2010) An R companion to applied regression. 2nd edn. SageGoogle Scholar
  12. Fudge AM (1989) Avian hematology: identification and interpretation. In: Proceedings Association of Avian Veterinarians, Annual Meeting, Seattle, pp 284–292Google Scholar
  13. Gross WB, Siegel HS (1983) Evaluation of the heterophil/lymphocyte ratio as a measure of stress in chickens. Avian Dis 27:972–979PubMedCrossRefGoogle Scholar
  14. Hamal KR, Burgess SC, Pyvzner IY, Erf GF (2006) Maternal antibody transfer from dams to their egg yolks, egg whites, and chicks in meat lines of chickens. Poult Sci 85:1364–1372PubMedGoogle Scholar
  15. Hawkey CM, Dennett TB (1989) A colour atlas of comparative veterinary haematology. Normal and abnormal blood cells in mammals, birds and reptiles. Wolfe Medical, LondonGoogle Scholar
  16. Hõrak P, Jenni-Eiermann S, Ots I, Tegelmann L (1998) Health and reproduction: the sex-specific clinical profile of great tits (Parus major) in relation to breeding. Can J Zool 76:2235–2244Google Scholar
  17. Juul-Madsen HR, Viertlboeck B, Smith AL, Göbel TWF (2008) Avian innate immune response. In: Davidson F, Kaspers B, Schat KA (eds) Avian immunology, 1st edn. Elsevier, London, pp 129–158CrossRefGoogle Scholar
  18. Klasing KC, Leshchinsky TV (1999) Functions, costs and benefits of the immune system during development and growth. Ostrich 69:2817–2832Google Scholar
  19. Le Corre M, Cherel Y, Lormée H, Jouventin P (2003) Seasonal and inter-annual variation in the feeding ecology of a tropical oceanic seabird, the red-tailed tropicbird Phaeton rubricauda. Mar Ecol Prog Ser 255:289–301CrossRefGoogle Scholar
  20. Lee KA (2006) Linking immune defenses and life history at the levels of the individual and the species. Integ Comp Biol 46:1000–1015CrossRefGoogle Scholar
  21. Lobato E, Moreno J, Merino S, Sanz J, Arriero E (2005) Haematological variables are good predictors of recruitment in nestling pied flycatchers (Ficedula hypoleuca). Écoscience 12:27–34CrossRefGoogle Scholar
  22. Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87–98CrossRefGoogle Scholar
  23. Masello JF, Choconi RG, Helmer M, Kremberg T, Lubjuhn T, Quillfeldt P (2009) Do leucocytes reflect condition in nestling burrowing parrots Cyanoliseus patagonus in the wild? Comp Biochem Physiol A 152:176–181CrossRefGoogle Scholar
  24. Mast J, Goddeeris BM (1999) Development of innunocompetence of broiler chickens. Vet Immunol Immunopathol 70:245–256PubMedCrossRefGoogle Scholar
  25. Maxwell MH, Robertson GW (1998) The avian heterophil leucocyte: a review. World’s Poul Sci J 54:155–178CrossRefGoogle Scholar
  26. Mercer-Oltjen SL, Woodard AE (1987) Development of the bursa of Fabricius in the Partridge and Pheasant. Poult Sci 66:418–421PubMedGoogle Scholar
  27. Merino S, Barbosa A (1997) Haematocrit values in chinstrap penguins (Pygoscelis antarctica): variation with age and reproductive status. Pol Biol 17:14–16CrossRefGoogle Scholar
  28. Merino S, Minguez E (1998) Absence of hematozoa in a breeding colony of the storm petrel Hydrobates pelagicus. Ibis 140:180–181CrossRefGoogle Scholar
  29. Merino S, Barbosa A, Moreno J, Potti J (1997) Absence of haematozoa in a wild chinstrap penguin Pygoscelis antarctica population. Pol Biol 18:227–228CrossRefGoogle Scholar
  30. Merino S, Martínez J, Møller AP, Sanabria L, de Lope F, Pérez J, Rodríguez-Caabeiro F (1999) Phytohaemagglutinin injection assay and physiological stress in nestling house martins. Anim Behav 58:219–222PubMedCrossRefGoogle Scholar
  31. Møller AP, Petrie M (2002) Condition dependence, multiple sexual signals, and immunocompetence in peacocks. Behav Ecol 13:248–253CrossRefGoogle Scholar
  32. Moreno J, Merino S, Martínez J, Sanz JJ, Arriero E (2002) Heterophil/lymphocyte ratios and heat-shock protein levels are related to growth in nestling birds. Écoscience 9:434–439Google Scholar
  33. Norris K, Evans MR (2000) Ecological immunology: life history trade-offs and immune defense in birds. Behav Ecol 11:19–25CrossRefGoogle Scholar
  34. Orta J (1992) Order Pelecaniformes, Family Phaethontidae (Tropicbirds). In: del Hoyo J, Elliot A, Sargatal J (eds) Handbook of the birds of the world, vol 1. Lynx Editions, Barcelona, pp 280–289Google Scholar
  35. Peirce MA, Brooke M (1993) Failure to detect blood parasites in seabirds from the Pitcairn Islands. Seabird 15:72–74Google Scholar
  36. Quillfeldt P, Masello JF, Strange IJ (2003) Breeding biology of the thin-billed prion Pachyptila belcheri at New Island, Falkland Islands, in the poor season 2002/2003: egg desertion, breeding success and chick provisioning. Pol Biol 26:746–752CrossRefGoogle Scholar
  37. Quillfeldt P, Ruiz G, Aguilar Rivera M, Masello JF (2008) Variability in leucocyte profiles in thin-billed prions Pachyptila belcheri. Comp Biochem Physiol A 150:26–31CrossRefGoogle Scholar
  38. Roitt I, Brostoff J, Male D (1993) Immunology. Mosby, LondonGoogle Scholar
  39. Rubin LL, Canal CW, Ribeir ALM, Kessler A, Silva I, Trevizan L, Viola T, Raber M, Gonçaves T, Krás R (2007) Effects of methionine and arginine dietary levels on the immunity of broiler chickens submitted to immunological stimuli. Braz J Poult Sci 9:214–247Google Scholar
  40. Ruiz G, Rosenmann M, Novoa FF, Sabat P (2002) Hematological parameters and stress index in rufous-collared sparrows dwelling in urban environments. Condor 104:162–166CrossRefGoogle Scholar
  41. Schreiber EA (1994) El Niño-southern oscillation effects on provisioning and growth in Red-tailed Tropicbirds. Col Waterbirds 17:105–119CrossRefGoogle Scholar
  42. Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321PubMedCrossRefGoogle Scholar
  43. Sommerfeld J, Hennicke JC (2010) Comparison of trip duration, activity pattern and diving behaviour by Red-tailed Tropicbirds (Phaethon rubricauda) during incubation and chick-rearing. Emu 110:78–86CrossRefGoogle Scholar
  44. 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 London B 271:435–440CrossRefGoogle Scholar
  45. Villegas A, Sánchez JM, Costillo E, Corbacho C (2002) Blood chemistry and haematocrit of the black vulture (Aegypius monachus). Comp Biochem Physiol A 132:489–497CrossRefGoogle Scholar
  46. Vleck CM, Vertalino N, Vleck D, Bucher TL (2000) Stress, corticosterone, and heterophil to lymphocyte ratios in free-living Adélie penguins. Condor 102:392–400CrossRefGoogle Scholar
  47. Weimerskirch H, Cherel Y (1998) Feeding ecology of short-tailed shearwaters: breeding in Tasmania and foraging in the Antarctic? Mar Ecol Prog Ser 167:261–274CrossRefGoogle Scholar
  48. Weimerskirch H, Lys P (2000) Seasonal changes in the provisioning behaviour and mass of male and female wandering albatrosses in relation to the growth of their chick. Pol Biol 23:733–744CrossRefGoogle Scholar
  49. Work TM (1996) Weights, hematology, and serum chemistry of seven species of free-ranging tropical pelagic seabirds. J Wildlife Dis 32:643–657Google Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Nina Dehnhard
    • 1
    Email author
  • Petra Quillfeldt
    • 1
  • Janos C. Hennicke
    • 2
    • 3
  1. 1.Max Planck Institute for OrnithologyRadolfzellGermany
  2. 2.Abt. Animal Ecology and Conservation, Biozentrum Grindel, Universität HamburgHamburgGermany
  3. 3.Centre d’Etudes Biologiques de ChizéVilliers-en-BoisFrance

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