Ontogeny of leukocyte profiles in a wild altricial passerine

Abstract

Ecophysiological studies have highlighted the relevance of the avian immune system in individual fitness prospects in the wild. However, studies on the ontogeny of avian immunity are scarce. We analyse age-related changes in the cellular constitutive immunity throughout nestling development, as well as its relationship with sex and brood size. We found that cellular constitutive immunity could be affected by age, sex, brood size, or daily rhythm. Early-stage nestlings relied more on cells of the innate immunity rather than on cells linked to the adaptive immune system. Cellular immunity may not be fully mature in fledglings, as reflected by differences in phagocytic cell counts with regard to adults. Beyond the age-dependent effects, agranulocyte cell counts were affected by sibling competition while granulocyte cell counts showed a daily rhythm. We also show that the heterophil to lymphocyte ratio was negatively related to body weight when nestlings become more independent. Our study contributes knowledge to the fields of developmental immunology and ecological immunology based on essential components of the cellular immune system.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

Availability of data and materials

All data underlying the findings will be hosted on the Spanish National Research Council (CSIC) digital repository.

References

  1. Alkie TN, Yitbarek A, Hodgins DC et al (2019) Development of innate immunity in chicken embryos and newly hatched chicks: a disease control perspective. Avian Pathol 48:288–310. https://doi.org/10.1080/03079457.2019.1607966

    Article  PubMed  Google Scholar 

  2. Alonso JC, Huecas V, Alonso JA et al (1991) Hematology and blood chemistry of adult White Storks (Ciconia ciconia). Comp Biochem Physiol Part A Physiol 98:395–397. https://doi.org/10.1016/0300-9629(91)90421-8

    Article  Google Scholar 

  3. Alonso-Alvarez C, Tella JL (2001) Effects of experimental food restriction and body-mass changes on the avian t-cell-mediated response. Can J Zool 79:101–105. https://doi.org/10.1139/z00-190

    Article  Google Scholar 

  4. Ardia DR (2005) Individual quality mediates trade-offs between reproductive effort and immune function in tree swallows. J Anim Ecol 74:517–524. https://doi.org/10.1111/j.1365-2656.2005.00950.x

    Article  Google Scholar 

  5. Ardia DR (2007) The ability to mount multiple immune responses simultaneously varies across the range of the tree swallow. Ecography (Cop) 30:23–30. https://doi.org/10.1111/j.0906-7590.2007.04939.x

    Article  Google Scholar 

  6. Bar-Shira E, Friedman A (2006) Development and adaptations of innate immunity in the gastrointestinal tract of the newly hatched chick. Dev Comp Immunol 30:930–941. https://doi.org/10.1016/j.dci.2005.12.002

    CAS  Article  PubMed  Google Scholar 

  7. Bates D, Bolker B, Walker S, et al. (2017) lme4: linear mixed-effects models using “Eigen” and S4 Contact. R package version 1.1-15. keziamanlove.com

  8. Bensch S, Åkesson S (2003) Temporal and spatial variation of hematozoans in Scandinavian willow warblers. J Parasitol 89:388–391. https://doi.org/10.1645/0022-3395(2003)089[0388:TASVOH]2.0.CO;2

    Article  PubMed  Google Scholar 

  9. Brommer JE (2004) Immunocompetence and its costs during development: an experimental study in blue tit nestlings. Proc R Soc B Biol Sci 271:S110–S113. https://doi.org/10.1098/rsbl.2003.0103

    Article  Google Scholar 

  10. Burton RR, Harrison JS (1969) The relative differential leucocyte count of the newly hatched chick. Poult Sci 48:451–453. https://doi.org/10.3382/ps.0480451

    CAS  Article  PubMed  Google Scholar 

  11. Campbell TW, Ellis CK (2007) Avian and Exotic Animal Hematology and Cytology. Blackwell Publishing Professional, Ames

    Google Scholar 

  12. Chapman BR, George JE (1991) The effects of ectoparasites on cliff swallow growth and survival. In: Loye JE, Zuk M (eds) Bird-parasite interactions. Oxford University Press, Oxford, pp 69–92

    Google Scholar 

  13. Chin EH, Love OP, Clark AM, Williams TD (2005) Brood size and environmental conditions sex-specifically affect nestling immune response in the European starling Sturnus vulgaris. J Avian Biol 36:549–554. https://doi.org/10.1111/j.0908-8857.2005.03496.x

    Article  Google Scholar 

  14. Christe P, De Lope F, González G et al (2001) The influence of environmental conditions on immune responses, morphology and recapture probability of nestling house martins (Delichon urbica). Oecologia 126:333–338. https://doi.org/10.1007/s004420000527

    Article  PubMed  Google Scholar 

  15. Colominas-Ciuró R, Santos M, Coria N, Barbosa A (2017) Reproductive effort affects oxidative status and stress in an Antarctic penguin species: an experimental study. PLoS ONE. https://doi.org/10.1371/journal.pone.0177124

    Article  PubMed  PubMed Central  Google Scholar 

  16. Cramp S, Simmons KEL, Perrins CM (1982–1994) Handbook of the birds of Europe, the Middle East and North Africa. Oxford University Press, Oxford

    Google Scholar 

  17. D’Amico VL, Marcelo B, Benzal J et al (2016) Leukocyte counts in different populations of Antarctic Pygoscelid penguins along the Antarctic Peninsula. Polar Biol 39:199–206. https://doi.org/10.1007/s00300-015-1771-3

    Article  Google Scholar 

  18. Davis AK (2005) Effect of handling time and repeated sampling on avian white blood cell counts. J F Ornithol 76:334–338. https://doi.org/10.1648/0273-8570-76.4.334

    Article  Google Scholar 

  19. Davis AK, Cook KC, Altizer S (2004) Leukocyte profiles in wild house finches with and without mycoplasmal conjunctivitis, a recently emerged bacterial disease. EcoHealth 1:362–373. https://doi.org/10.1007/s10393-004-0134-2

    Article  Google Scholar 

  20. Davis AK, Maney DL, Maerz JC (2008) The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct Ecol 22:760–772. https://doi.org/10.1111/j.1365-2435.2008.01467.x

    Article  Google Scholar 

  21. Evans JK, Griffith SC, Klasing KKC, Buchanan KL (2016) Impact of nest sanitation on the immune system of parents and nestlings in a passerine bird. J Exp Biol 219:1985–1993. https://doi.org/10.1242/jeb.130948

    Article  PubMed  Google Scholar 

  22. Fairbrother A, O’Loughlin D (1990) Differential white blood cell values of the mallard (Anas platyrhynchos) across different ages and reproductive states. J Wildl Dis 26:78–82. https://doi.org/10.7589/0090-3558-26.1.78

    CAS  Article  PubMed  Google Scholar 

  23. Fellah JS, Jaffredo T, Nagy N, Dunon D (2013) Development of the avian immune system. In: Avian immunology, 2nd edn. Elsevier Inc., pp 45–63

  24. Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622. https://doi.org/10.1086/285346

    Article  Google Scholar 

  25. Foo YZ, Nakagawa S, Rhodes G, Simmons LW (2017) The effects of sex hormones on immune function: a meta-analysis. Biol Rev 92:551–571. https://doi.org/10.1111/brv.12243

    Article  PubMed  Google Scholar 

  26. Gil D, Culver R (2011) Male ornament size in a passerine predicts the inhibitory effect of testosterone on macrophage phagocytosis. Funct Ecol 25:1278–1283. https://doi.org/10.1111/j.1365-2435.2011.01878.x

    Article  Google Scholar 

  27. Griffiths R, Double MC, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075. https://doi.org/10.1046/j.1365-294x.1998.00389.x

    CAS  Article  PubMed  Google Scholar 

  28. Gross WB, Siegel HS (1983) Evaluation of the heterophil/lymphocyte ratio as a measure of stress in chickens. Avian Dis 27:972–979. https://doi.org/10.2307/1590198

    CAS  Article  PubMed  Google Scholar 

  29. Grossman CJ (1985) Interactions between the gonadal steroids and the immune system. Science 227(4684):257–261. https://doi.org/10.1126/science.3871252

    CAS  Article  PubMed  Google Scholar 

  30. Gustafsson L, Nordling D, Andersson MS et al (1994) Infectious diseases, reproductive effort and the cost of reproduction in birds. Philos Trans R Soc London B 346:323–331. https://doi.org/10.1098/rstb.1994.0149

    CAS  Article  Google Scholar 

  31. Harrison XA (2014) Using observation-level random effects to model overdispersion in count data in ecology and evolution. PeerJ 2:e616. https://doi.org/10.7717/peerj.616

    Article  PubMed  PubMed Central  Google Scholar 

  32. Hasselquist D, Nilsson JÅ (2009) Maternal transfer of antibodies in vertebrates: trans-generational effects on offspring immunity. Philos Trans R Soc B Biol Sci 364:51–60. https://doi.org/10.1098/rstb.2008.0137

    Article  Google Scholar 

  33. Hasselquist D, Nilsson JÅ (2012) Physiological mechanisms mediating costs of immune responses: what can we learn from studies of birds? Anim Behav 83:1303–1312. https://doi.org/10.1016/j.anbehav.2012.03.025

    Article  Google Scholar 

  34. Howlett JC, Bailey TA, Samour JH et al (2002) Age-related hematologic changes in captive-reared houbara, white-bellied, and rufous-crested bustards. J Wildl Dis 38:804–816. https://doi.org/10.7589/0090-3558-38.4.804

    Article  PubMed  Google Scholar 

  35. Ilmonen P, Hasselquist D, Langefors Å, Wiehn J (2003) Stress, immunocompetence and leukocyte profiles of pied flycatchers in relation to brood size manipulation. Oecologia 136:148–154. https://doi.org/10.1007/s00442-003-1243-2

    Article  PubMed  Google Scholar 

  36. Kaiser P (2010) Advances in avian immunology-prospects for disease control: a review. Avian Pathol 39:309–324. https://doi.org/10.1080/03079457.2010.508777

    CAS  Article  PubMed  Google Scholar 

  37. Killpack TL, Karasov WH (2012) Ontogeny of adaptive antibody response to a model antigen in captive altricial zebra finches. PLoS ONE 7(10):e47294. https://doi.org/10.1371/journal.pone.0047294

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  38. Klein SL (2004) Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunol 26:247–264. https://doi.org/10.1111/j.0141-9838.2004.00710.x

    CAS  Article  PubMed  Google Scholar 

  39. Klein SL, Roberts CW (2015) Sex and gender differences in infection and treatments for infectious diseases. Springer, New York

    Google Scholar 

  40. Klein SL, Flanagan KL (2016) Sex differences in immune responses. Nat Rev Immunol 16:626–638. https://doi.org/10.1038/nri.2016.90

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. Kohl KD, Brun A, Caviedes-Vidal E, Karasov WH (2019) Age-related changes in the gut microbiota of wild House Sparrow nestlings. Ibis (Lond 1859) 161:184–191. https://doi.org/10.1111/ibi.12618

    Article  Google Scholar 

  42. Kulaszewicz I, Wojczulanis-Jakubas K, Jakubas D (2017) Trade-offs between reproduction and self-maintenance (immune function and body mass) in a small seabird, the little auk. J Avian Biol 48:371–379. https://doi.org/10.1111/jav.01000

    Article  Google Scholar 

  43. Liker A, Márkus M, Vozár Á et al (2001) Distribution of Carnus hemapterus in a starling colony. Can J Zool 79:574–580. https://doi.org/10.1139/z01-018

    Article  Google Scholar 

  44. Lobato E, Moreno J, Merino S et al (2005) Haematological variables are good predictors of recruitment in nestling pied flycatchers (Ficedula hypoleuca ). Écoscience 12:27–34. https://doi.org/10.2980/i1195-6860-12-1-27.1

    Article  Google Scholar 

  45. Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87–98. https://doi.org/10.1034/j.1600-0706.2000.880110.x

    Article  Google Scholar 

  46. López-Rull I, Macías Garcia C (2015) Control of invertebrate occupants of nests. Nests, eggs, and incubation: new ideas about avian reproduction. Oxford University Press, Oxford, pp 82–96

    Google Scholar 

  47. López-Rull I, Gil M, Gil D (2007) Spots in starling Sturnus unicolor eggs are good indicators of ectoparasite load by Carnus hemapterus (Diptera: Carnidae). Ardeola Int J Ornithol 54:131–134

    Google Scholar 

  48. López-Rull I, Celis P, Salaberria C et al (2011) Post-fledging recruitment in relation to nestling plasma testosterone and immunocompetence in the spotless starling. Funct Ecol 25:500–508. https://doi.org/10.1111/j.1365-2435.2010.01783.x

    Article  Google Scholar 

  49. Markowska M, Majewski PM, Skwarło-Sońta K (2017) Avian biological clock—immune system relationship. Dev Comp Immunol 66:130–138. https://doi.org/10.1016/j.dci.2016.05.017

    CAS  Article  PubMed  Google Scholar 

  50. Martin TE, Møller AP, Merino S, Clobert J (2001) Does clutch size evolve in response to parasites and immunocompetence? Proc Natl Acad Sci USA 98:2071–2076. https://doi.org/10.1073/pnas.98.4.2071

    CAS  Article  PubMed  Google Scholar 

  51. Martin LB, Han P, Lewittes J et al (2006) Phytohemagglutinin-induced skin swelling in birds: histological support for a classic immunoecological technique. Funct Ecol 20:290–299. https://doi.org/10.1111/j.1365-2435.2006.01094.x

    Article  Google Scholar 

  52. Martínez-Padilla J (2006) Daytime variation in T-cell-mediated immunity of Eurasian kestrel Falco tinnunculus nestlings. J Avian Biol 37:419–424. https://doi.org/10.1111/j.2006.0908-8857.03904.x

    Article  Google Scholar 

  53. Masello JF, Choconi RG, Helmer M et al (2009) Do leucocytes reflect condition in nestling burrowing parrots Cyanoliseus patagonus in the wild? Comp Biochem Physiol A Mol Integr Physiol 152:176–181. https://doi.org/10.1016/j.cbpa.2008.09.018

    CAS  Article  PubMed  Google Scholar 

  54. Maxwell MH, Robertson GW (1998) The avian heterophil leucocyte: a review. Worlds Poult Sci J 54:155–178. https://doi.org/10.1079/wps19980012

    Article  Google Scholar 

  55. Merrill L, Stewart Merrill TE, Barger AM, Benson TJ (2019) Avian health across the landscape: nestling immunity covaries with changing landcover. Integr Comp Biol 59:1150–1164. https://doi.org/10.1093/icb/icz037

    CAS  Article  PubMed  Google Scholar 

  56. Monclús R, Muriel J, Pérez-Rodríguez L et al (2017) The role of the mating system and intraspecific brood parasitism in the costs of reproduction in a passerine bird. Oecologia 185:629–639. https://doi.org/10.1007/s00442-017-3977-2

    Article  PubMed  Google Scholar 

  57. Moreno J, Veiga JP, Cordero PJ, Mínguez E (1999) Effects of paternal care on reproductive success in the polygynous spotless starling Sturnus unicolor. Behav Ecol Sociobiol 47:47–53. https://doi.org/10.1007/s002650050648

    Article  Google Scholar 

  58. Muriel J, Salmón P, Nunez-Buiza A et al (2015) Context-dependent effects of yolk androgens on nestling growth and immune function in a multibrooded passerine. J Evol Biol 28:1476–1488. https://doi.org/10.1111/jeb.12668

    CAS  Article  PubMed  Google Scholar 

  59. Muriel J, Pérez-Rodríguez L, Ortiz-Santaliestra ME et al (2017) Sex-specific effects of high yolk androgen levels on constitutive and cell-mediated immune responses in nestlings of an altricial passerine. Physiol Biochem Zool 90:106–117. https://doi.org/10.1086/688445

    Article  PubMed  Google Scholar 

  60. Muriel J, Graves JA, Gil D et al (2018) Molecular characterization of avian malaria in the spotless starling (Sturnus unicolor). Parasitol Res 117:919–928. https://doi.org/10.1007/s00436-018-5748-3

    Article  PubMed  Google Scholar 

  61. Muriel J, Pérez-Rodríguez L, Gil D (2019) Age-related patterns of yolk androgen deposition are consistent with adaptive brood reduction in spotless starlings. Behav Ecol Sociobiol. https://doi.org/10.1007/s00265-019-2770-0

    Article  Google Scholar 

  62. Navarro C, Marzal A, De Lope F, Møller AP (2003) Dynamics of an immune response in house sparrows Passer domesticus in relation to time of day, body condition and blood parasite infection. Oikos 101:291–298. https://doi.org/10.1034/j.1600-0706.2003.11663.x

    Article  Google Scholar 

  63. Oro D, Hernández N, Jover L, Genovart M (2014) From recruitment to senescence: food shapes the age-dependent pattern of breeding performance in a long-lived bird. Ecology 95:446–457. https://doi.org/10.1890/13-0331.1

    Article  PubMed  Google Scholar 

  64. Palacios MG, Cunnick JE, Vleck D, Vleck CM (2009) Ontogeny of innate and adaptive immune defense components in free-living tree swallows, Tachycineta bicolor. Dev Comp Immunol 33:456–463. https://doi.org/10.1016/j.dci.2008.09.006

    CAS  Article  PubMed  Google Scholar 

  65. Palacios MG, Winkler DW, Klasing KC et al (2011) Consequences of immune system aging in nature: a study of immunosenescence costs in free-living tree swallows. Ecology 92:952–966. https://doi.org/10.1890/10-0662.1

    Article  PubMed  Google Scholar 

  66. Peel MC, Finlayson BL, Mcmahon TA (2007) Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Syst Sci Discuss 4:439–473

    Article  Google Scholar 

  67. Quillfeldt P, Ruiz G, Rivera MA, Masello JF (2008) Variability in leucocyte profiles in thin-billed prions Pachyptila belcheri. Comp Biochem Physiol A Mol Integr Physiol 150:26–31. https://doi.org/10.1016/j.cbpa.2008.02.021

    CAS  Article  PubMed  Google Scholar 

  68. R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing. https://www.Rproject.org/. Accessed 15 Feb 2019

  69. Råberg L, Stjernman M, Hasselquist D (2003) Immune responsiveness in adult blue tits: heritability and effects of nutritional status during ontogeny. Oecologia 136:360–364. https://doi.org/10.1007/s00442-003-1287-3

    Article  PubMed  Google Scholar 

  70. Rebke M, Coulson T, Becker PH, Vaupel JW (2010) Reproductive improvement and senescence in a long-lived bird. Proc Natl Acad Sci 107:7841–7846. https://doi.org/10.1073/pnas.1002645107

    Article  PubMed  Google Scholar 

  71. Roved J, Westerdahl H, Hasselquist D (2017) Sex differences in immune responses: hormonal effects, antagonistic selection, and evolutionary consequences. Horm Behav 88:95–105. https://doi.org/10.1016/j.yhbeh.2016.11.017

    CAS  Article  PubMed  Google Scholar 

  72. Sheldon BC, Verhulst S (1996) Ecological immunology—costly parasite defenses and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321. https://doi.org/10.1016/0169-5347(96)10039-2

    CAS  Article  PubMed  Google Scholar 

  73. Siopes TD, Underwood HA (2008) Diurnal variation in the cellular and humoral immune responses of Japanese quail: role of melatonin. Gen Comp Endocrinol 158:245–249. https://doi.org/10.1016/j.ygcen.2008.07.008

    CAS  Article  PubMed  Google Scholar 

  74. Smits JEG, Baos R (2005) Evaluation of the antibody mediated immune response in nestling American kestrels (Falco sparverius). Dev Comp Immunol 29:161–170. https://doi.org/10.1016/j.dci.2004.06.007

    CAS  Article  PubMed  Google Scholar 

  75. Soler JJ, Neve L, d., Perez-Contreras T, et al (2003) Trade-off between immunocompetence and growth in magpies: an experimental study. Proc R Soc B Biol Sci 270:241–248. https://doi.org/10.1098/rspb.2002.2217

    Article  Google Scholar 

  76. Spencer JL, Garcia MM (1995) Resistance of chicks and poults fed vermicompost to caecal colonization by Salmonella. Avian Pathol 24:157–170. https://doi.org/10.1080/03079459508419056

    CAS  Article  PubMed  Google Scholar 

  77. St. Paul M, Paolucci S, Barjesteh N et al (2012) Characterization of chicken thrombocyte responses to toll-like receptor ligands. PLoS ONE. https://doi.org/10.1371/journal.pone.0043381

    Article  PubMed  PubMed Central  Google Scholar 

  78. Stambaugh T, Houdek BJ, Lombardo MP et al (2011) Innate immune response development in nestling tree swallows. Wilson J Ornithol 123:779–787. https://doi.org/10.1676/10-197.1

    Article  Google Scholar 

  79. Staszewski V, Gasparini J, Mccoy KD et al (2007) Evidence of an interannual effect of maternal immunization on the immune response of juveniles in a long-lived colonial bird. J Anim Ecol 76:1215–1223. https://doi.org/10.1111/j.1365-2656.2007.01293.x

    Article  PubMed  Google Scholar 

  80. Stinson R, McCorkle F, Mashaly M et al (1980) The effects of diurnal rhythms on immune parameters in New Hampshire chickens. Int Arch Allergy Immunol 61:220–226. https://doi.org/10.1159/000232436

    CAS  Article  Google Scholar 

  81. Tella JL, Scheuerlein A, Ricklefs RE (2002) Is cell-mediated immunity related to the evolution of life-history strategies in birds? Proc R Soc B Biol Sci 269:1059–1066. https://doi.org/10.1098/rspb.2001.1951

    Article  Google Scholar 

  82. Torres-Medina F, Cabezas S, Marchant TA, Blas J (2019) Dexamethasone treatment supports age-related maturation of the stress response in altricial nestling birds. J Avian Biol 50:jav.02091. https://doi.org/10.1111/jav.02091

    Article  Google Scholar 

  83. Tschirren B, Fitze PS, Richner H (2003) Sexual dimorphism in susceptibility to parasites and cell-mediated immunity in great tit nestlings. J Anim Ecol 72:839–845. https://doi.org/10.1046/j.1365-2656.2003.00755.x

    Article  Google Scholar 

  84. Van Der Most PJ, De Jong B, Parmentier HK, Verhulst S (2011) Trade-off between growth and immune function: a meta-analysis of selection experiments. Funct Ecol 25:74–80. https://doi.org/10.1111/j.1365-2435.2010.01800.x

    Article  Google Scholar 

  85. Villanúa D, Pérez-Rodríguez L, Gortázar C et al (2006) Avoiding bias in parasite excretion estimates: the effect of sampling time and type of faeces. Parasitology 133:251–259. https://doi.org/10.1017/S003118200600031X

    Article  PubMed  Google Scholar 

  86. Vinkler M, Schnitzer J, Munclinger P et al (2010) Haematological health assessment in a passerine with extremely high proportion of basophils in peripheral blood. J Ornithol 151:841–849. https://doi.org/10.1007/s10336-010-0521-0

    Article  Google Scholar 

  87. Wigley P, Hulme SD, Barrow PA (1999) Phagocytic and oxidative burst activity of chicken thrombocytes to Salmonella, Escherichia coli and other bacteria. Avian Pathol 28:567–572. https://doi.org/10.1080/03079459994353

    Article  PubMed  Google Scholar 

  88. Wilk T, Dubiec A, Cichoń M (2007) Seasonal decline in cell-mediated immunity of collared flycatcher Ficedula albicollis nestlings: does the sex of offspring matter? J Ornithol 148:199–205. https://doi.org/10.1007/s10336-006-0121-1

    Article  Google Scholar 

Download references

Acknowledgements

We are very grateful to all the volunteers who helped to collect data over the completely breeding season. We also thank one anonymous journal reviewer and Associate Editor for their valuable assistance on the earlier draft of the article. This study is a contribution to the research developed at the “El Ventorrillo” field station.

Funding

The project was funded by projects CGL2011-26318 to DG (Ministerio de Economía y Competitividad) and PGC2018-099596-B-I00 to LP-R (Ministerio de Ciencia, Innovación y Universidades, co-financed by the European Regional Development Fund-ERDF). JM was supported by a postdoctoral grant from the Juan de la Cierva Subprogram (FJCI-2017-34109), with the financial sponsorship of the MICINN. CV was supported by a contract from the program “Contratos Asociados a Proyectos de Investigación”, Universidad de Alcalá, Madrid, Spain. LP-R was supported by a postdoctoral contract for accessing the Spanish System of Science, Technology and Innovation (SECTI) from the University of Castilla-La Mancha.

Author information

Affiliations

Authors

Contributions

LP-R and DG devised the project and the main conceptual ideas. JM and LP-R carried out fieldwork. JM performed the cell counts. JM and CV analysed and interpreted the data. JM took the lead in writing the manuscript. All authors provided critical feedback and helped shape the research, analysis, and manuscript.

Corresponding author

Correspondence to Jaime Muriel.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national and/or institutional guidelines for the care and use of animals were followed. Capture and manipulation of birds were authorized by the Consejería de Medio Ambiente (Comunidad de Madrid, Spain) under licence from the Spanish institutional authorities (Consejería de Medio Ambiente and Centro de Migración de Aves de SEO/BirdLife).

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by Philip Withers.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 348 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Muriel, J., Vida, C., Gil, D. et al. Ontogeny of leukocyte profiles in a wild altricial passerine. J Comp Physiol B 191, 195–206 (2021). https://doi.org/10.1007/s00360-020-01323-z

Download citation

Keywords

  • Age-specific pattern
  • Cell-mediated immunity
  • Daily rhythm
  • Leukocyte count
  • Nestling development
  • Sturnus unicolor