in

Parental morph combination does not influence innate immune function in nestlings of a colour-polymorphic African raptor

  • 1.

    Lindström, J. Early development and fitness in birds and mammals. Trends Ecol. Evol. 14, 343–348 (1999).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 2.

    Cam, E. & Aubry, L. Early development, recruitment and life history trajectory in long-lived birds. J. Ornithol. 152, 187–201 (2011).

    Article 

    Google Scholar 

  • 3.

    Cam, E., Monnat, J. Y. & Hines, J. E. Long-term fitness consequences of early conditions in the kittiwake. J. Anim. Ecol. 72, 411–424 (2003).

    Article 

    Google Scholar 

  • 4.

    Tilgar, V., Mänd, R., Kilgas, P. & Mägi, M. Long-term consequences of early ontogeny in free-living Great Tits Parus major. J. Ornithol. 151, 61–68 (2010).

    Article 

    Google Scholar 

  • 5.

    Stamps, J. A. The silver spoon effect and habitat selection by natal dispersers. Ecol. Lett. 9, 1179–1185 (2006).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 6.

    Briga, M., Koetsier, E., Boonekamp, J. J., Jimeno, B. & Verhulst, S. Food availability affects adult survival trajectories depending on early developmental conditions. Proc. R. Soc. B Biol. Sci. 284, 20162287 (2017).

    Article 

    Google Scholar 

  • 7.

    Cooper, E. B. & Kruuk, L. E. Ageing with a silver-spoon: A meta-analysis of the effect of developmental environment on senescence. Evol. Lett. 2, 460–471 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 8.

    Song, Z. et al. Silver spoon effects of hatching order in an asynchronous hatching bird. Behav. Ecol. Sociobiol. 30, 509–517 (2019).

    Article 

    Google Scholar 

  • 9.

    Descamps, S., Boutin, S., Berteaux, D., McAdam, A. G. & Gaillard, J. M. Cohort effects in red squirrels: The influence of density, food abundance and temperature on future survival and reproductive success. J. Anim. Ecol. 77, 305–314 (2008).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 10.

    Van De Pol, M., Bruinzeel, L. W., Heg, D., Van Der Jeugd, H. P. & Verhulst, S. A silver spoon for a golden future: Long-term effects of natal origin on fitness prospects of oystercatchers (Haematopus ostralegus). J. Anim. Ecol. 75, 616–626 (2006).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 11.

    Murgatroyd, M. et al. Sex-specific patterns of reproductive senescence in a long-lived reintroduced raptor. J. Anim. Ecol. 87, 1587–1599 (2018).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 12.

    Dmitriew, C. & Rowe, L. Effects of early resource limitation and compensatory growth on lifetime fitness in the ladybird beetle (Harmonia axyridis). J. Evol. Biol. 20, 1298–1310 (2007).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 13.

    Hopwood, P. E., Moore, A. J. & Royle, N. J. Effects of resource variation during early life and adult social environment on contest outcomes in burying beetles: A context-dependent silver spoon strategy?. Proc. R. Soc. B Biol. Sci. 281, 20133102 (2014).

    Article 

    Google Scholar 

  • 14.

    Royle, N. J., Lindström, J. & Metcalfe, N. B. A poor start in life negatively affects dominance status in adulthood independent of body size in green swordtails Xiphophorus helleri. Proc. R. Soc. B Biol. Sci. 272, 1917–1922 (2005).

    Article 

    Google Scholar 

  • 15.

    Mugabo, M., Marquis, O., Perret, S. & Le Galliard, J. F. Immediate and delayed life history effects caused by food deprivation early in life in a short-lived lizard. J. Evol. Biol. 23, 1886–1898 (2010).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 16.

    Vitikainen, E. I., Thompson, F. J., Marshall, H. H. & Cant, M. A. Live long and prosper: Durable benefits of early-life care in banded mongooses. Philos. Trans. R. Soc. B Biol. Sci. 374, 20180114 (2019).

    Article 

    Google Scholar 

  • 17.

    Sumasgutner, P., Tate, G. J., Koeslag, A. & Amar, A. Family morph matters: Factors determining survival and recruitment in a long-lived polymorphic raptor. J. Anim. Ecol. 85, 1043–1055 (2016).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 18.

    Emaresi, G. et al. Melanin-specific life-history strategies. Am. Nat. 183, 269–280 (2014).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 19.

    Grunst, M. L. et al. Actuarial senescence in a dimorphic bird: Different rates of ageing in morphs with discrete reproductive strategies. Proc. R. Soc. B Biol. Sci. 285, 20182053 (2018).

    Article 

    Google Scholar 

  • 20.

    Nebel, C., Sumasgutner, P., McPherson, S. C., Tate, G. J. & Amar, A. Contrasting parental color-morphs increase regularity of prey deliveries in an African raptor. Behav. Ecol. 31, 1142–1149 (2020).

    Article 

    Google Scholar 

  • 21.

    Morosinotto, C. et al. Fledging mass is color morph specific and affects local recruitment in a wild bird. Am. Nat. 196, 609–619 (2020).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 22.

    Chakarov, N., Boerner, M. & Krüger, O. Fitness in common buzzards at the cross-point of opposite melanin–parasite interactions. Funct. Ecol. 22, 1062–1069 (2008).

    Article 

    Google Scholar 

  • 23.

    Roulin, A. Proximate basis of the covariation between a melanin-based female ornament and offspring quality. Oecologia 140, 668–675 (2004).

    ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 24.

    Rödel, H. G., Von Holst, D. & Kraus, C. Family legacies: short-and long-term fitness consequences of early-life conditions in female European rabbits. J. Anim. Ecol. 78, 789–797 (2009).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 25.

    Clutton-Brock, T. H. The Evolution of Parental Care (Princeton University Press, 1991).

    Book 

    Google Scholar 

  • 26.

    Cockburn, A. Prevalence of different modes of parental care in birds. Proc. R. Soc. B Biol. Sci. 273, 1375–1383 (2006).

    Article 

    Google Scholar 

  • 27.

    Norris, K. & Evans, M. R. Ecological immunology: Life history trade-offs and immune defense in birds. Behav. Ecol. Sociobiol. 11, 19–26 (2000).

    Article 

    Google Scholar 

  • 28.

    van der Most, P. J., de Jong, B., Parmentier, H. K. & Verhulst, S. Trade-off between growth and immune function: A meta-analysis of selection experiments. Funct. Ecol. 25, 74–80 (2011).

    Article 

    Google Scholar 

  • 29.

    Aastrup, C. & Hegemann, A. Jackdaw nestlings rapidly increase innate immune function during the nestling phase but no evidence for a trade-off with growth. Dev. Comparat. Immunol. 2, 103967 (2020).

    Google Scholar 

  • 30.

    Ratikainen, I. I. & Kokko, H. Differential allocation and compensation: Who deserves the silver spoon?. Behav. Ecol. Sociobiol. 21, 195–200 (2010).

    Article 

    Google Scholar 

  • 31.

    Limbourg, T., Mateman, A. C. & Lessells, C. M. Opposite differential allocation by males and females of the same species. Biol. Let. 9, 20120835 (2013).

    Article 

    Google Scholar 

  • 32.

    Järvistö, P. E., Calhim, S., Schuett, W., Velmala, W. & Laaksonen, T. Foster, but not genetic, father plumage coloration has a temperature-dependent effect on offspring quality. Behav. Ecol. Sociobiol. 69, 335–346 (2015).

    Article 

    Google Scholar 

  • 33.

    Pryke, S. R. & Griffith, S. C. Socially mediated trade-offs between aggression and parental effort in competing color morphs. Am. Nat. 174, 455–464 (2009).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 34.

    Amar, A., Koeslag, A. & Curtis, O. Plumage polymorphism in a newly colonized black sparrowhawk population: Classification, temporal stability and inheritance patterns. J. Zool. 289, 60–67 (2013).

    Article 

    Google Scholar 

  • 35.

    Tate, G., Sumasgutner, P., Koeslag, A. & Amar, A. Pair complementarity influences reproductive output in the polymorphic black sparrowhawk Accipiter melanoleucus. J. Avian Biol. 48, 387–398 (2017).

    Article 

    Google Scholar 

  • 36.

    Tinbergen, J. M. & Boerlijst, M. C. Nestling weight and survival in individual great tits (Parus major). J. Anim. Ecol. 59, 1113–1127 (1990).

    Article 

    Google Scholar 

  • 37.

    Cleasby, I. R., Nakagawa, S., Gillespie, D. O. S. & Burke, T. The influence of sex and body size on nestling survival and recruitment in the house sparrow. Biol. J. Lin. Soc. 101, 680–688 (2010).

    Article 

    Google Scholar 

  • 38.

    Christe, P., Møller, A. P. & de Lope, F. Immunocompetence and nestling survival in the house martin: The tasty chick hypothesis. Oikos 83, 175–179 (1998).

    CAS 
    Article 

    Google Scholar 

  • 39.

    Ringsby, T. H., Sæther, B.-E. & Solberg, E. J. Factors affecting juvenile survival in house sparrow Passer domesticus. J. Avian Biol. 29, 241–247 (1998).

    Article 

    Google Scholar 

  • 40.

    Losdat, S. et al. Nestling erythrocyte resistance to oxidative stress predicts fledging success but not local recruitment in a wild bird. Biol. Lett. 9, 20120888 (2013).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 41.

    Vermeulen, A., Müller, W. & Eens, M. J. Vitally important–does early innate immunity predict recruitment and adult innate immunity?. Ecol. Evol. 6, 1799–1808 (2016).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 42.

    Vennum, C. R. et al. Early life conditions and immune defense in nestling Swainson’s Hawks. Physiol. Biochem. Zool. 92, 419–429 (2019).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 43.

    Bowers, E. K. et al. Neonatal body condition, immune responsiveness, and hematocrit predict longevity in a wild bird population. Ecology 95, 3027–3034 (2014).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 44.

    Calder, P. C. & Sonnenfeld, G. in Nutrition, Immunity, and Infection 1–18 (CRC Press, 2017).

    Book 

    Google Scholar 

  • 45.

    Wilcoxen, T. E., Boughton, R. K. & Schoech, S. J. Selection on innate immunity and body condition in Florida scrub-jays throughout an epidemic. Biol. Let. 6, 552–554 (2010).

    Article 

    Google Scholar 

  • 46.

    Hegemann, A., Marra, P. P. & Tieleman, B. I. Causes and consequences of partial migration in a passerine bird. Am. Nat. 186, 531–546 (2015).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 47.

    Hegemann, A., Matson, K. D., Flinks, H. & Tieleman, B. I. Offspring pay sooner, parents pay later: Experimental manipulation of body mass reveals trade-offs between immune function, reproduction and survival. Front. Zool. 10, 77 (2013).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 48.

    Apanius, V. Ontogeny of Immune Function (Oxford University Press, 1998).

    Google Scholar 

  • 49.

    Klasing, K. C. & Leshchinksy, T. V. Functions, Costs, and Benefits of the Immune System During Development and Growth Ostrich, 69, 2817–2835 (1999).

  • 50.

    Bonneaud, C. et al. Assessing the cost of mounting an immune response. Am. Nat. 161, 367–379 (2003).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 51.

    Costantini, D. & Moller, A. P. Does immune response cause oxidative stress in birds? A meta-analysis. Comparat. Biochem. Physiol. Part A 153, 339–344 (2009).

    Article 
    CAS 

    Google Scholar 

  • 52.

    Hanssen, S. A., Hasselquist, D., Folstad, I. & Erikstad, K. E. Costs of immunity: Immune responsiveness reduces survival in a vertebrate. Proc. R. Soc. Lond. Ser. B Biol. Sci. 271, 925–930 (2004).

    Article 

    Google Scholar 

  • 53.

    Hanssen, S. A. Costs of an immune challenge and terminal investment in a long-lived bird. Ecology 87, 2440–2446 (2006).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 54.

    Matson, K. D., Ricklefs, R. E. & Klasing, K. C. A hemolysis–hemagglutination assay for characterizing constitutive innate humoral immunity in wild and domestic birds. Dev. Comp. Immunol. 29, 275–286 (2005).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 55.

    Müller-Eberhard, H. J. Molecular organization and function of the complement system. Annu. Rev. Biochem. 57, 321–347 (1988).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 56.

    Dobryszycka, W. Biological functions of haptoglobin-new pieces to an old puzzle. Eur. J. Clin. Chem. Clin. Biochem. 35, 647–654 (1997).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 57.

    Matson, K. D., Horrocks, N. P. C., Versteegh, M. A. & Tieleman, B. I. Baseline haptoglobin concentrations are repeatable and predictive of certain aspects of a subsequent experimentally-induced inflammatory response. Comparat. Biochem. Physiol. Part A Mol. Integr. Physiol. 162, 7–15 (2012).

    CAS 
    Article 

    Google Scholar 

  • 58.

    Cray, C., Zaias, J. & Altman, N. H. Acute phase response in animals: A review. Comp. Med. 59, 517–526 (2009).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 59.

    Hegemann, A., Matson, K. D., Both, C. & Tieleman, B. I. Immune function in a free-living bird varies over the annual cycle, but seasonal patterns differ between years. Oecologia 170, 605–618 (2012).

    ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 60.

    Alexander, C. & Rietschel, E. T. Invited review: Bacterial lipopolysaccharides and innate immunity. J. Endotoxin Res. 7, 167–202 (2016).

    Google Scholar 

  • 61.

    Hegemann, A., Matson, K. D., Versteegh, M. A., Villegas, A. & Tieleman, B. I. Immune response to an endotoxin challenge involves multiple immune parameters and is consistent among the annual-cycle stages of a free-living temperate zone bird. J. Exp. Biol. 216, 2573–2580 (2013).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 62.

    Vermeulen, A., Eens, M., Zaid, E. & Müller, W. Baseline innate immunity does not affect the response to an immune challenge in female great tits (Parus major). Behav. Ecol. Sociobiol. 70, 585–592 (2016).

    Article 

    Google Scholar 

  • 63.

    Vinterstare, J., Hegemann, A., Nilsson, P. A., Hulthén, K. & Brönmark, C. Defence versus defence: Are crucian carp trading off immune function against predator-induced morphology?. J. Anim. Ecol. 88, 1510–1521 (2019).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 64.

    Lei, B., Amar, A., Koeslag, A., Gous, T. A. & Tate, G. J. Differential haemoparasite intensity between black sparrowhawk (Accipiter melanoleucus) morphs suggests an adaptive function for polymorphism. PLoS ONE 8, e81607 (2013).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 65.

    Suri, J., Sumasgutner, P., Hellard, É., Koeslag, A. & Amar, A. Stability in prey abundance may buffer Black Sparrowhawks Accipiter melanoleucus from health impacts of urbanization. Ibis 159, 38–54 (2017).

    Article 

    Google Scholar 

  • 66.

    Råberg, L., Grahn, M., Hasselquist, D. & Svensson, E. On the adaptive significance of stress-induced immunosuppression. Proc. R. Soc. Lond. Ser. B Biol. Sci. 265, 1637–1641 (1998).

    Article 

    Google Scholar 

  • 67.

    Sadd, B. M. & Siva-Jothy, M. T. Self-harm caused by an insect’s innate immunity. Proc. R. Soc. Lond. Ser. B Biol. Sci. 273, 2571–2574 (2006).

    Google Scholar 

  • 68.

    Gyan, B. et al. Elevated levels of nitric oxide and low levels of haptoglobin are associated with severe malarial anaemia in African children. Acta Trop. 83, 133–140 (2002).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 69.

    Alonso-Alvarez, C. & Tella, J. L. Effects of experimental food restriction and body-mass changes on the avian T-cell-mediated immune response. Can. J. Zool. 79, 101–105 (2001).

    Article 

    Google Scholar 

  • 70.

    Merino, S. et al. Phytohaemagglutinin injection assay and physiological stress in nestling house martins. Anim. Behav. 58, 219–222 (1999).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 71.

    Ochsenbein, A. F. & Zinkernagel, R. M. Natural antibodies and complement link innate and acquired immunity. Immunol. Today 21, 624–630 (2000).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 72.

    Boes, M. Role of natural and immune IgM antibodies in immune responses. Mol. Immunol. 37, 1141–1149 (2000).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 73.

    Grönwall, C., Vas, J. & Silverman, G. J. Protective roles of natural IgM antibodies. Front. Immunol. 3, 66 (2012).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 74.

    Martin, L. B., Weil, Z. M. & Nelson, R. J. Seasonal changes in vertebrate immune activity: Mediation by physiological trade-offs. Philos. Trans. R. Soc. B Biol. Sci. 363, 321–339 (2008).

    Article 

    Google Scholar 

  • 75.

    Klasing, K. C. The costs of immunity. Acta Zool. Sin. 50, 961–969 (2004).

    CAS 

    Google Scholar 

  • 76.

    Van Noordwijk, A. J. & de Jong, G. Acquisition and allocation of resources: Their influence on variation in life history tactics. Am. Nat. 128, 137–142 (1986).

    Article 

    Google Scholar 

  • 77.

    Glazier, D. S. Trade-offs between reproductive and somatic (storage) investments in animals: A comparative test of the Van Noordwijk and De Jong model. Evol. Ecol. 13, 539–555 (1999).

    Article 

    Google Scholar 

  • 78.

    Newton, I., McGrady, M. J. & Oli, M. K. A review of survival estimates for raptors and owls. Ibis 158, 227–248 (2016).

    Article 

    Google Scholar 

  • 79.

    Kennedy, P. L. & Ward, J. M. Effects of experimental food supplementation on movements of juvenile northern goshawks (Accipiter gentilis atricapillus). Oecologia 134, 284–291 (2003).

    ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 80.

    Terraube, J., Vasko, V. & Korpimäki, E. Mechanisms and reproductive consequences of breeding dispersal in a specialist predator under temporally varying food conditions. Oikos 124, 762–771 (2015).

    Article 

    Google Scholar 

  • 81.

    Delgado, M. D. M., Penteriani, V. & Nams, V. O. How fledglings explore surroundings from fledging to dispersal. A case study with Eagle Owls Bubo bubo. Ardea 97, 7–15 (2009).

    Article 

    Google Scholar 

  • 82.

    Rosenfield, R. N. et al. Body mass of female Cooper’s Hawks is unrelated to longevity and breeding dispersal: Implications for the study of breeding dispersal. J. Raptor Res. 50, 305–312 (2016).

    Article 

    Google Scholar 

  • 83.

    Klein, S. L. Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunol. 26, 247–264 (2004).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 84.

    Klein, S. L. & Flanagan, K. L. Sex differences in immune responses. Nat. Rev. Immunol. 16, 626 (2016).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 85.

    Zuk, M. Reproductive strategies and disease susceptibility: An evolutionary viewpoint. Parasitol. Today 6, 231–233 (1990).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 86.

    Zuk, M. & McKean, K. A. Sex differences in parasite infections: patterns and processes. Int. J. Parasitol. 26, 1009–1024 (1996).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 87.

    Alexander, J. & Stimson, W. H. Sex hormones and the course of parasitic infection. Parasitol. Today 4, 189–193 (1988).

    Article 

    Google Scholar 

  • 88.

    Roulin, A. et al. Which chick is tasty to parasites? The importance of host immunology vs. parasite life history. J. Anim. Ecol. 72, 75–81 (2003).

    Article 

    Google Scholar 

  • 89.

    Hockey, P. A. R., Dean, W. R. J., Ryan, P. G., Maree, S. & Brickman, B. M. Roberts’ Birds of Southern Africa 7th edn. (John Voelcker Bird Book Fund, 2005).

    Google Scholar 

  • 90.

    Christie, D. A. & Ferguson-Lees, J. Raptors of the World (Christopher Helm Publishers, 2010).

    Google Scholar 

  • 91.

    Martin, R. O. et al. Phenological shifts assist colonisation of a novel environment in a range-expanding raptor. Oikos 123, 1457–1468 (2014).

    Article 

    Google Scholar 

  • 92.

    Rose, S., Sumasgutner, P., Koeslag, A. & Amar, A. Does seasonal decline in breeding performance differ for an African raptor across an urbanization gradient?. Front. Ecol. Evol. 5, 47 (2017).

    Article 

    Google Scholar 

  • 93.

    Horrocks, N. P. et al. Immune indexes of larks from desert and temperate regions show weak associations with life history but stronger links to environmental variation in microbial abundance. Physiol. Biochem. Zool. 85, 504–515 (2012).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 94.

    Horrocks, N. P. et al. Environmental proxies of antigen exposure explain variation in immune investment better than indices of pace of life. Oecologia 177, 281–290 (2015).

    ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 95.

    Sergio, F., Blas, J., Forero, M. G., Donázar, J. A. & Hiraldo, F. Sequential settlement and site dependence in a migratory raptor. Behav. Ecol. Sociobiol. 18, 811–821 (2007).

    Article 

    Google Scholar 

  • 96.

    Rose, S., Thomson, R. L., Oschadleus, H.-D. & Lee, A. T. Summarising biometrics from the SAFRING database for southern African birds. Ostrich 2, 1–5 (2019).

    Google Scholar 

  • 97.

    Paijmans, D. M., Rose, S., Oschadleus, H.-D. & Thomson, R. L. SAFRING ringing report for 2017. Biodivers. Observ. 10, 1–11 (2019).

    Google Scholar 

  • 98.

    Katzenberger, J., Tate, G., Koeslag, A. & Amar, A. Black Sparrowhawk brooding behaviour in relation to chick age and weather variation in the recently colonised Cape Peninsula, South Africa. J. Ornithol. 156, 903–913 (2015).

    Article 

    Google Scholar 

  • 99.

    Buehler, D. M. et al. Constitutive immune function responds more slowly to handling stress than corticosterone in a shorebird. Physiol. Biochem. Zool. 81, 673–681 (2008).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 100.

    Zylberberg, M. Common measures of immune function vary with time of day and sampling protocol in five passerine species. J Exp Biol 218, 757–766 (2015).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 101.

    van de Crommenacker, J. et al. Effects of immune supplementation and immune challenge on oxidative status and physiology in a model bird: Implications for ecologists. J. Exp. Biol. 213, 3527–3535 (2010).

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 102.

    French, S. S. & Neuman-Lee, L. A. Improved ex vivo method for microbiocidal activity across vertebrate species. Biol. Open 1, 482–487 (2012).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 103.

    Eikenaar, C. & Hegemann, A. Migratory common blackbirds have lower innate immune function during autumn migration than resident conspecifics. Biol. Let. 12, 20160078 (2016).

    Article 
    CAS 

    Google Scholar 

  • 104.

    Hegemann, A., Pardal, S. & Matson, K. D. Indices of immune function used by ecologists are mostly unaffected by repeated freeze-thaw cycles and methodological deviations. Front. Zool. 14, 43 (2017).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 105.

    R Core Team. R: A language and environment for statistical computing. Vienna, Austria (R Foundation for Statistical Computing, 2019).

  • 106.

    Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest package: Tests in linear mixed effects models. J. Stat. Softw. 82, 2 (2017).

    Article 

    Google Scholar 

  • 107.

    McCurdy, D. G., Shutler, D., Mullie, A. & Forbes, M. R. Sex-biased parasitism of avian hosts: relations to blood parasite taxon and mating system. Oikos 82, 303–312 (1998).

    CAS 
    Article 

    Google Scholar 

  • 108.

    Parejo, D., Silva, N. & Avilés, J. M. Within-brood size differences affect innate and acquired immunity in roller Coracias garrulus nestlings. J. Avian Biol. 38, 717–725 (2007).

    Article 

    Google Scholar 

  • 109.

    Kanikowska, D., Hyun, K. J., Tokura, H., Azama, T. & Nishimura, S. Circadian rhythm of acute phase proteins under the influence of bright/dim light during the daytime. Chronobiol. Int. 22, 137–143 (2005).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 110.

    Laake, J. L. RMark: an R interface for analysis of capture-recapture data with MARK. AFSC Processed Rep 2013-01, Seattle, WA (Alaska Fish. Sci. Cent., NOAA, Natl. Mar. Fish. Serv., 2013).

  • 111.

    White, G. C. & Burnham, K. P. Program MARK: Survival estimation from populations of marked animals. Bird Study 46, S120–S139 (1999).

    Article 

    Google Scholar 

  • 112.

    Burnham, K. P. Design and Analysis Methods for Fish Survival Experiments Based on Release-Recapture (American Fisheries Society, 1987).

    Google Scholar 

  • 113.

    Coquet, R., Lebreton, J.-D., Gimenez, O. & Reboulet, A.-M. U-CARE: Utilities for performing goodness of fit tests and manipulating CApture-REcapture data. Ecography 32, 1071–1074 (2009).

    Article 

    Google Scholar 

  • 114.

    Sauer, J. R. & Byron, K. W. Generalized procedures for testing hypotheses about survival or recovery raes. J. Wildl. Manag. 53, 137–142 (1989).

    Article 

    Google Scholar 

  • 115.

    Nebel, C., Amar, A., Hegemann, A., Isaksson, C. & Sumasgutner, P. Parental morph combination does not influence innate immune function in nestlings of a colour-polymorphic African raptor: Data, Zivahub, https://doi.org/10.25375/uct.12780803 (2021).


  • Source: Ecology - nature.com

    MIT students and alumni “hack” Hong Kong Kowloon East

    Coexistence holes fill a gap in community assembly theory