Variation in innate immune function during incubation, chick-rearing and moult in Little Penguins (Eudyptula minor)
Jessica K. Evans A C D , Peter Dann B and Theresa Frankel A
+ Author Affiliations
- Author Affiliations
A Department of Agricultural Sciences, La Trobe University, Bundoora, Vic. 3086, Australia.
B Research Department, Phillip Island Nature Parks, PO Box 97, Cowes, Phillip Island, Vic. 3922, Australia.
C Centre for Integrative Ecology, School of Life and Environmental Sciences, Deakin University, Geelong, Vic. 3217, Australia.
D Corresponding author. Email: jessica.evans@deakin.edu.au
Emu 115(1) 63-71 https://doi.org/10.1071/MU13077
Submitted: 13 August 2013 Accepted: 9 June 2014 Published: 29 January 2015
Abstract
Physiologically demanding and energetically expensive life-events, such as incubation, chick-rearing and moult, may cause a trade-off with costly immune defences and, in turn, decrease immune function. We examined innate immunity in Little Penguins (Eudyptula minor) during the physiologically demanding periods of incubation, chick-guarding, chick-rearing and moult using a bacterial-killing assay and white blood-cell counts. The capacity of individuals to kill Escherichia coli varied significantly in relation to life-stage, with bacterial killing significantly higher during incubation compared with late chick-rearing, the most energetically expensive period in the annual cycle of Little Penguins. The elevated bacterial-killing capacity during nesting stages could be particularly beneficial for protection from the presumed high pathogen (bacterial) loads in nests. However, this relationship remains to be tested. Counts of white blood cells varied during breeding but were significantly higher in chicks compared to adults during guarding and post-guarding stages, and significantly higher at the end of moult compared to all other stages, which could indicate inflammation from infection, or dehydration. These results suggest that immune function may be adversely affected during energetically demanding life-stages but may also offer protection from bacteria encountered in the nesting environment.
Additional keywords: avian immunity, eco-immunology, immuno-competence, microbial killing.
References
Ardia, D. R., Schat, K. A., and Winkler, D. W. (2003). Reproductive effort reduces long-term immune function in breeding Tree Swallows (Tachycineta bicolor). Proceedings of the Royal Society of London – B. Biological Sciences 270, 1679–1683.| Reproductive effort reduces long-term immune function in breeding Tree Swallows (Tachycineta bicolor).Crossref | GoogleScholarGoogle Scholar |
Arnould, J., Dann, P., and Cullen, M. (2004). Determining the sex of Little Penguins (Eudyptula minor) in northern Bass Strait using morphometric measurements. Emu 104, 261–265.
| Determining the sex of Little Penguins (Eudyptula minor) in northern Bass Strait using morphometric measurements.Crossref | GoogleScholarGoogle Scholar |
Betz, S. J., and Isliker, H. (1981). Antibody-independent interactions between Escherichia coli J5 and human complement components. Journal of Immunology 127, 1748–1754.
| 1:CAS:528:DyaL3MXmtFyku7o%3D&md5=28fdb8abe1d70f885ac5aa8641cdc7a3CAS |
Bourgeon, S., Raclot, T., Le Maho, Y., Ricquier, D., and Criscuolo, F. (2007). Innate immunity, assessed by plasma NO measurements, is not suppressed during the incubation fast in Eiders. Developmental and Comparative Immunology 31, 720–728.
| Innate immunity, assessed by plasma NO measurements, is not suppressed during the incubation fast in Eiders.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjvFGntbY%3D&md5=2217efc640e637be5ca9fb41e71b2d7eCAS | 17197024PubMed |
Buehler, D. M., Piersma, T., Matson, K., and Tieleman, B. I. (2008a). Seasonal redistribution of immune function in a migrant shorebird: annual-cycle effects override adjustments to thermal regime. American Naturalist 172, 783–796.
| Seasonal redistribution of immune function in a migrant shorebird: annual-cycle effects override adjustments to thermal regime.Crossref | GoogleScholarGoogle Scholar | 18999941PubMed |
Buehler, D. M., Piersma, T., and Tieleman, B. I. (2008b). Captive and free-living Red Knots Calidris canutus exhibit differences in non-induced immunity that suggest different immune strategies in different environments. Journal of Avian Biology 39, 560–566.
| Captive and free-living Red Knots Calidris canutus exhibit differences in non-induced immunity that suggest different immune strategies in different environments.Crossref | GoogleScholarGoogle Scholar |
Buehler, D. M., Tieleman, B. I., and Piersma, T. (2009). Age and environment affect constitutive immune function in Red Knots (Calidris canutus). Journal of Ornithology 150, 815–825.
| Age and environment affect constitutive immune function in Red Knots (Calidris canutus).Crossref | GoogleScholarGoogle Scholar |
Campbell, T. W. (1988). ‘Avian Hematology and Cytology.’ (Iowa State University Press: Ames, Iowa.)
Chandra, R. K. (1997). Nutrition and the immune system: an introduction. American Journal of Clinical Nutrition 66, 460s–463s.
| 1:CAS:528:DyaK2sXltVarsrg%3D&md5=81cfce8f16bf00c4aa3bf75d649a5d4fCAS | 9250133PubMed |
Cherel, Y., Gilles, J., Handrich, Y., and Le Mayo, Y. (1994). Nutrient reserve dynamics and energetics during long-term fasting in the King Penguin (Aptenodytes patagonicus). Journal of Zoology 234, 1–12.
| Nutrient reserve dynamics and energetics during long-term fasting in the King Penguin (Aptenodytes patagonicus).Crossref | GoogleScholarGoogle Scholar |
Chiaradia, A. R., and Kerry, K. R. (1999). Daily nest attendance and breeding performance in the Little Penguin Eudyptula minor at Phillip Island, Australia. Marine Ornithology 27, 13–20.
Collins, M., Cullen, J. M., and Dann, P. (1999). Seasonal and annual foraging movements of Little Penguins from Phillip Island, Victoria. Wildlife Research 26, 705–721.
| Seasonal and annual foraging movements of Little Penguins from Phillip Island, Victoria.Crossref | GoogleScholarGoogle Scholar |
Dann, P. (1988). An experimental manipulation of clutch size in the Little Penguin Eudyptula minor. Emu 88, 101–103.
| An experimental manipulation of clutch size in the Little Penguin Eudyptula minor.Crossref | GoogleScholarGoogle Scholar |
Dann, P., Cullen, J. M., and Jessop, R. (1995). Chapter 3. Cost of reproduction in Little Penguins. In ‘The Penguins: Ecology and Management’. (Eds P. Dann, I. Norman and P. Reilly.) pp. 39–55. (Surrey Beatty: Sydney.)
Davis, A. K., Cook, K. C., and Altizer, S. (2004). Leukocyte profiles in wild House Finches with and without mycoplasmal conjunctivitis, a recently emerged bacterial disease. EcoHealth 1, 362–373.
| Leukocyte profiles in wild House Finches with and without mycoplasmal conjunctivitis, a recently emerged bacterial disease.Crossref | GoogleScholarGoogle Scholar |
Demas, G. E., Zysling, D. A., Beechler, B. R., Muehlenbein, M. P., and French, S. S. (2011). Beyond phytohaemagglutinin: assessing vertebrate immune function across ecological contexts. Journal of Animal Ecology 80, 710–730.
| Beyond phytohaemagglutinin: assessing vertebrate immune function across ecological contexts.Crossref | GoogleScholarGoogle Scholar | 21401591PubMed |
Dytham, C. (2011). ‘Choosing and Using Statistics: A Biologist’s Guide’, 3rd edn. (Wiley-Blackwell: West Sussex, UK.)
Fujikta, T. (2002). Evolution of the lectin-complement pathway and its role in innate immunity. Nature Reviews. Immunology 2, 316–353.
Gales, R., and Green, B. (1990). The annual energetics cycle of Little Penguins (Eudyptula minor). Ecology 71, 2297–2312.
| The annual energetics cycle of Little Penguins (Eudyptula minor).Crossref | GoogleScholarGoogle Scholar |
Ganz, T. (2003). Defensins: antimicrobial peptides of innate immunity. Nature Reviews. Immunology 3, 710–720.
| Defensins: antimicrobial peptides of innate immunity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmvVWmtLc%3D&md5=abb93fdc4ff427d70c02e86e9960d653CAS | 12949495PubMed |
Groscolas, R., and Clement, C. (1976). Utilization of energy supplies during breeding fasting of Emperor Penguin, Aptenodytes fosteri. Comptes Rendus Hebdomadaires des Seances de l’Academie des Sciences, Serie D. 282, 297–300.
| 1:CAS:528:DyaE28XhtValurY%3D&md5=be563cb0040b46ebfc5af2ed775587a1CAS |
Hanssen, S. A., Folstad, I., and Erikstad, K. E. (2003). Reduced immunocompetence and cost of reproduction in Common Eiders. Oecologia 136, 457–464.
| Reduced immunocompetence and cost of reproduction in Common Eiders.Crossref | GoogleScholarGoogle Scholar | 12783295PubMed |
Hegemann, A., Matson, K. D., Versteegh, M. A., and Tieleman, B. I. (2012a). Wild Skylarks seasonally modulate energy budgets but maintain energetically costly inflammatory immune responses throughout the annual cycle. PLoS ONE 7, e36358.
| Wild Skylarks seasonally modulate energy budgets but maintain energetically costly inflammatory immune responses throughout the annual cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XnsVGhsbo%3D&md5=1fa31142ec73beb7789d65a930fa8d24CAS | 22570706PubMed |
Hegemann, A., Matson, K. D., Both, C., and Tieleman, B. I. (2012b). Immune function in a free-living bird varies over the annual cycle, but seasonal patterns differ between years. Oecologia 170, 605–618.
| Immune function in a free-living bird varies over the annual cycle, but seasonal patterns differ between years.Crossref | GoogleScholarGoogle Scholar | 22562421PubMed |
Hoskins, A. J., Dann, P., Ropert-Coudert, Y., Kato, A., Chiaradia, A., Costa, D. P., and Arnould, J. P. Y. (2008). Foraging behaviour and habitat selection of the Little Penguin Eudyptula minor during early chick rearing in Bass Strait, Australia. Marine Ecology Progress Series 366, 293–303.
| Foraging behaviour and habitat selection of the Little Penguin Eudyptula minor during early chick rearing in Bass Strait, Australia.Crossref | GoogleScholarGoogle Scholar |
Janeway, C. A., Travers, P., Walport, M., and Schlomchik, M. J. (2004). ‘Immunobiology.’ (Garland Science: New York.)
Kemp, A., and Dann, P. (2001). Egg size, incubation periods and hatching success of Little Penguins, Eudyptula minor. Emu 101, 249–253.
| Egg size, incubation periods and hatching success of Little Penguins, Eudyptula minor.Crossref | GoogleScholarGoogle Scholar |
Keusch, G. T., Douglas, S. D., and Ugurbil, K. (1975). Intracellular bactericidal activity of leukocytes in whole blood for the diagnosis of chronic granulomatous disease of childhood. Journal of Infectious Diseases 131, 584–587.
| Intracellular bactericidal activity of leukocytes in whole blood for the diagnosis of chronic granulomatous disease of childhood.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2M7lt1eksw%3D%3D&md5=7e3e8c3e49755fc83323a9df640366b2CAS | 1092771PubMed |
Klasing, K. (2004). The cost of immunity. Acta Zoologica Sinica 50, 961–969.
| 1:CAS:528:DC%2BD2MXjtVKqt70%3D&md5=aed9044e908469eb200b41ac374ac60cCAS |
Klasing K. C. Calvert C. C. 1999
Klotman, M. E., and Chang, T. L. (2006). Defensins in innate antiviral immunity. Nature Reviews. Immunology 6, 447–456.
| Defensins in innate antiviral immunity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XkvVyrtrk%3D&md5=fdaac941ecad610f732433881bf887d8CAS | 16724099PubMed |
Lassiter, H. A., Christensen, R. D., Parker, C., and Rothstein, G. (1988). Neutrophil-mediated killing, opsonization, and serum-mediated killing of Escherichia coli K1 by neonatal rats. Biology of the Neonate 53, 156–162.
| Neutrophil-mediated killing, opsonization, and serum-mediated killing of Escherichia coli K1 by neonatal rats.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1c3it1ejtg%3D%3D&md5=d13982a52d4f94ad1bc3746982619bffCAS | 3285898PubMed |
Linde, A., Ross, C. R., Davis, E. G., Dib, L., Blecha, F., and Melgarejo, T. (2008). Innate immunity and host defense peptides in veterinary medicine. Journal of Veterinary Internal Medicine 22, 247–265.
| Innate immunity and host defense peptides in veterinary medicine.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1c3htVOltQ%3D%3D&md5=0cfe1f8f7df4fcd9629de2998cde86a2CAS | 18312280PubMed |
Lochmiller, R. L., and Deerenberg, C. (2000). Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88, 87–98.
| Trade-offs in evolutionary immunology: just what is the cost of immunity?Crossref | GoogleScholarGoogle Scholar |
Martin, L. B. (2005). Trade-offs between molt and immune activity in two populations of House Sparrows (Passer domesticus). Canadian Journal of Zoology 83, 780–787.
| Trade-offs between molt and immune activity in two populations of House Sparrows (Passer domesticus).Crossref | GoogleScholarGoogle Scholar |
Martin, L. B., Weil, Z. M., and Nelson, R. (2008). Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs. Philosophical Transactions of the Royal Society – B. Biological Sciences 363, 321–339.
| Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs.Crossref | GoogleScholarGoogle Scholar |
Matson, K. D., Tieleman, B. I., and Klasing, K. C. (2006). Capture stress and the bactericidal competence of blood and plasma in five species of tropical birds. Physiological and Biochemical Zoology 79, 556–564.
| Capture stress and the bactericidal competence of blood and plasma in five species of tropical birds.Crossref | GoogleScholarGoogle Scholar | 16691521PubMed |
Merchant, M. E., Roche, C., Elsey, R. M., and Prudhomme, J. (2003). Antibacterial properties of serum from the American Alligator (Alligator mississippiensis). Comparative Biochemistry and Physiology – Part B: Biochemistry & Molecular Biology 136, 505–513.
| Antibacterial properties of serum from the American Alligator (Alligator mississippiensis).Crossref | GoogleScholarGoogle Scholar |
Millet, S., Bennett, J., Lee, K. A., Hau, M., and Klasing, K. C. (2007). Quantifying and comparing constitutive immunity across avian species. Developmental and Comparative Immunology 31, 188–201.
| Quantifying and comparing constitutive immunity across avian species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVagtbrF&md5=031fdd7f5e548364bb5042419bfe4c3bCAS | 16870251PubMed |
Moreno, J. (2004). Moult–breeding overlap and fecundity limitation in tropical birds: a link with immunity? Ardeola 51, 471–476.
Mortimer, L., and Lill, A. (2007). Activity-related variation in blood parameters associated with oxygen transport and chronic stress in Little Penguins. Australian Journal of Zoology 55, 249–256.
| Activity-related variation in blood parameters associated with oxygen transport and chronic stress in Little Penguins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFSgsLzE&md5=3a19ccdf0daf418b44b4bf8278baa18dCAS |
Nebel, S., Bauchinger, U., Buehler, D. M., Langlois, L. A., Boyles, M., Gerson, A. R., Price, E. R., McWilliams, S. R., and Guglielmo, C. G. (2012). Constitutive immune function in European Starlings, Sturnus vulgaris, is decreased immediately after an endurance flight in a wind tunnel. Journal of Experimental Biology 215, 272–278.
| Constitutive immune function in European Starlings, Sturnus vulgaris, is decreased immediately after an endurance flight in a wind tunnel.Crossref | GoogleScholarGoogle Scholar | 22189771PubMed |
Nordling, D., Andersson, M., Zohari, S., and Gustafsson, L. (1998). Reproductive effort reduces specific immune response and parasite resistance. Proceedings of the Royal Society B – Biological Sciences 265, 1298.
| Reproductive effort reduces specific immune response and parasite resistance.Crossref | GoogleScholarGoogle Scholar |
Nunn, C. L. (2002). A comparative study of leukocyte counts and disease risk in primates. Evolution 56, 177–190.
| A comparative study of leukocyte counts and disease risk in primates.Crossref | GoogleScholarGoogle Scholar | 11913662PubMed |
Nunn, C. L., Gittleman, J. L., and Antonovics, J. (2003). A comparative study of white blood cell counts and disease risk in carnivores. Proceedings of the Royal Society of London – B. Biological Sciences 270, 347–356.
| A comparative study of white blood cell counts and disease risk in carnivores.Crossref | GoogleScholarGoogle Scholar |
Ots, I., Murumagi, A., and Horak, P. (1998). Haematological health state indices of reproducing Great Tits: methodology and sources of natural variation. Functional Ecology 12, 700–707.
| Haematological health state indices of reproducing Great Tits: methodology and sources of natural variation.Crossref | GoogleScholarGoogle Scholar |
Palacios, M. G., Cunnick, J. E., Vleck, D., and Vleck, C. M. (2009). Ontogeny of innate and adaptive immune defense components in free-living Tree Swallows, Tachycineta bicolour. Developmental and Comparative Immunology 33, 456–463.
| Ontogeny of innate and adaptive immune defense components in free-living Tree Swallows, Tachycineta bicolour.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlOlur0%3D&md5=2441830261b12fa246097ba8998f271bCAS | 18848578PubMed |
Reilly, P. N., and Cullen, J. M. (1981). The Little Penguin Eudyptula minor in Victoria, II: breeding. Emu 81, 1–19.
| The Little Penguin Eudyptula minor in Victoria, II: breeding.Crossref | GoogleScholarGoogle Scholar |
Schalm, O. W. (1961). ‘Veterinary Hematology.’ (Bailliere, Tindall and Cox: London.)
Schmid-Hempel, P., and Ebert, D. (2003). On the evolutionary ecology of specific immune defence. Trends in Ecology & Evolution 18, 27–32.
| On the evolutionary ecology of specific immune defence.Crossref | GoogleScholarGoogle Scholar |
Sergent, N., Rogers, T., and Cunningham, M. (2004). Influence of biological and ecological factors on haematological values in wild Little Penguins, Eudyptula minor. Comparative Biochemistry and Physiology A – Molecular and Integrative Physiology 138, 333–339.
| 1:STN:280:DC%2BD2cvgvVantg%3D%3D&md5=6ae781962165657f4b2507474bde09f8CAS |
Sharma, J. M. (1991). Overview of the avian immune system. Veterinary Immunology and Immunopathology 30, 13–17.
| Overview of the avian immune system.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK387kt1Ckuw%3D%3D&md5=d5ccacaebd0d724797134c7a9406bd14CAS | 1781153PubMed |
Stahel, C. D., and Gales, R. P. (1987). ‘Fairy Penguin: Little Penguins in Australia.’ (New South Wales University Press: Kensington, Sydney, NSW.)
Stahel, C. D., and Nicol, S. C. (1982). Temperature regulation in the Little Penguin, Eudyptula minor, in air and water. Journal of Comparative Physiology 148, 93–100.
Svensson, E., Raberg, L., Koch, C., and Hasselquist, D. (1998). Energetic stress, immunosuppression and the costs of an antibody response. Functional Ecology 12, 912–919.
| Energetic stress, immunosuppression and the costs of an antibody response.Crossref | GoogleScholarGoogle Scholar |
Thouzeau, C., Le Maho, Y., Froget, G., Sabatier, L., Le Bohec, C., Hoffmann, J. A., and Bulet, P. (2003). Spheniscins, avian β-defensins in preserved stomach contents of the King Penguin Aptenodytes patagonicus. Journal of Biological Chemistry 278, 51053–51058.
| Spheniscins, avian β-defensins in preserved stomach contents of the King Penguin Aptenodytes patagonicus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpslOhs7Y%3D&md5=3a421fe8e416ecb391e2a54ae3d634a3CAS | 14525994PubMed |
Tieleman, B. I., Williams, J. B., Ricklefs, R. E., and Klasing, K. C. (2005). Constitutive innate immunity is a component of pace-of-life syndrome in tropical birds. Proceedings of the Royal Society of London – B. Biological Sciences 272, 1715–1720.
| Constitutive innate immunity is a component of pace-of-life syndrome in tropical birds.Crossref | GoogleScholarGoogle Scholar |
Tieleman, B. I., Croese, E., Helm, B., and Versteegh, M. A. (2010). Repeatability and individual correlates of microbicidal capacity of bird blood. Comparative Biochemistry and Physiology – Part A: Molecular & Integrative Physiology 156, 537–540.
| Repeatability and individual correlates of microbicidal capacity of bird blood.Crossref | GoogleScholarGoogle Scholar |
Tinbergen, J. M., and Williams, J. B. (2002). Energetics of incubation. In‘Avian Incubation: Behaviour, Environment and Evolution’. (Ed. D. C. Deeming.) pp. 299–313. (Oxford University Press: Oxford, UK.)
van Dijk, A., Edwin, A., Veldhuizen, J. A., and Haagsman, H. P. (2008). Avian defensins. Veterinary Immunology and Immunopathology 124, 1–18.
| Avian defensins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmsFOjsrk%3D&md5=9c69a5346f7f99cc83c339b8bbdec2faCAS | 18313763PubMed |
Warton, D. I., and Hui, F. K. C. (2011). The arcsine is asinine: the analysis of proportions in ecology. Ecology 92, 3–10.
| The arcsine is asinine: the analysis of proportions in ecology.Crossref | GoogleScholarGoogle Scholar | 21560670PubMed |
Wright, S. D., and Levine, R. P. (1981). How complement kills E. coli. I. Location of the lethal lesion. Journal of Immunology 127, 1146–1151.
| 1:CAS:528:DyaL3MXlvVGnsbo%3D&md5=80393694b787fc29fd1e414c9383a401CAS |