Abstract
Intestinal parasites suppose a cost to hosts as they compete directly for nutritional resources. Therefore, hosts must defend themselves against intestinal parasites by mounting an immune response. Many penguin species acquire parasites through their diet and transfer these parasites to their chicks when feeding them. High parasite loads in penguin chicks could have effects on their growth and body condition, and ultimately on their survival. Here, we evaluated the effect of parasites on the cell-mediated immune system in Gentoo penguin (Pygoscelis papua) chicks at Stranger Point (25 de Mayo/King George Island, South Shetland Islands). To this end, 12 chicks were experimentally deparasitized with a mixture of anthelminthic drugs (albendazole and praziquantel), whereas 10 others were kept as control. We measured cutaneous cell-mediated immunity in response to immunization with phytohemagglutinin (PHA). We also analyzed the leukocyte profile in both treated and control groups before and after the treatment. After the treatment, deparasitized birds showed larger foot-web swelling in response to PHA injection than control birds. Deparasitized penguins also showed lower eosinophil and monocyte counts than controls, whereas heterophils, lymphocytes, and total white blood cell counts did not differ between groups. Our results suggest that Gentoo penguin chicks parasitized with intestinal parasites suffer a cost in terms of reduced cell-mediated immune responses that could ultimately affect their survival.
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Atkinson A, Siegel V, Pakhomov E, Rothery P (2004) Long-term decline in krill stock and increase in salps within the Southern Ocean. Nature 432:100–103. doi:10.1038/nature02996
Barbosa A, Palacios MJ (2009) Health of Antarctic birds: a review of their parasites, pathogens and diseases. Polar Biol 32:1095–1115. doi:10.1007/s00300-009-0640-3
Bertellotti M (2013) Pingüino de Magallanes: Embajador de la Patagonia. Vázquez Mazzini, Buenos Aires 60
Campbell TW (1995) Avian hematology and cytology, 2nd edn. Iowa State University Press, Ames 105
Colditz G (2008) Six costs of immunity to gastrointestinal nematode infections. Parasite Immunol 30:63–70. doi:10.1111/j.1365-3024.2007.00964.x
D’Amico V, Bertellotti M, Díaz J, Coria N, Vidal V, Barbosa A (2014) Leukocyte levels in some Antarctic and non-Antarctic penguins. Ardeola 61:145–152. doi:10.13157/arla.61.1.2014.145
Davis AK, Maney DL, Maerz JC (2008) The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct Ecol 22:760–777. doi:10.1111/j.1365-2435.2008.01467.x
Degen WGJ, van Daal N, Rothwell L, Kaiser P, Virgil EJC, Schijns VEJC (2005) Th1/Th2 polarization by viral and helminth infection in birds. Vet Microbiol 105:163–167. doi:10.1016/j.vetmic.2004.12.001
Diaz JI, Fusaro B, Longarzo L, Coria NR, Vidal V, Jerez S, Ortiz J, Barbosa A (2013) Gastrointestinal helminths of Gentoo penguins (Pygoscelis papua) from Stranger Point, 25 de Mayo/King George Island, Antarctica. Parasitol Res 112:1877–1881. doi:10.1007/s00436-013-3341-3
Goto N, Kodama H, Okada K, Fujimoto Y (1978) Suppression of phytohemagglutinin skin response in thymectomized chickens. Poult Sci 57:246–250. doi:10.3382/ps.0570246
Grimaldi W, Seddon PJ, Lyver POB, Nakagawa S, Tompkins DM (2014) Infectious diseases of Antarctic penguins: current status and future threats. Polar Biol. doi:10.1007/s00300-014-1632-5
Hale KA, Briskie JV (2007) Decreased immunocompetence in severely bottlenecked population of an endemic New Zealand bird. Anim Conserv 10:2–10. doi:10.1111/j.1469-1795.2006.00059.x
Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2163
Janovy J (1997) Protozoa, helminths, and arthropods of birds. In: Clayton DH, Moore J (eds) Host-parasite evolution. General principles and avian models. Oxford University Press, Oxford, pp 303–337
Kahn CM (ed) (2010) The Merck veterinary manual, 10th edn. Merck & Co., Inc., Whitehouse Station
Lee K (2006) Linking immune defenses and life history at the levels of the individual and the species. Integr Comp Biol 46:1000–1015. http://www.jstor.org/stable/3884887
Lescroël A, Bajzak C, Bost CA (2009) Breeding ecology of the gentoo penguin Pygoscelis papua at Kerguelen Archipelago. Polar Biol 32:1495–1505. doi:10.1007/s00300-009-0647-9
Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87–98. doi:10.1034/j.1600-0706.2000.880110.x
Martin LB, Scheuerlein A, Wikelski M (2003) Increased immune activity elevates energy expenditure of house sparrows: a link between proximate and ultimate costs of immune activity? P Roy Soc Lond B Bio 270:153–158. doi:10.1098/rspb.2002.2185
Martin LB, Han P, Lewittes J, Kuhlman JR, Klasing KC, Wikelski M (2006) Phytohemagglutinin-induced skin swelling in birds: histological support for a classic immunoecological technique. Funct Ecol 20:290–299. doi:10.1111/j.1365-2435.2006.01094.x
Møller AP, Saino N (2004) Immune response and survival. Oikos 104:299–304. doi:10.1111/j.0030-1299.2004.12844.x
Moreno J, de León A, Fargallo JA, Moreno E (1998) Breeding time, health and immune response in the chinstrap penguin Pygoscelis antarctica. Oecologia 115:312–329. doi:10.1007/s004420050522
Muraille E, Leo O (1998) Revisiting the Th1/Th2 paradigm. Scand J Immunol 47:1–9. doi:10.1111/j.1365-3083.1998-47-1.00383.x
Nelson RJ, Demas GE, Klein SL, Kriegsfeld LK (2002) Seasonal patterns of stress, immune function and disease. Cambridge University Press, Cambridge 308
Palacios MJ, Valera F, Barbosa A (2012) Experimental assessment of the effects of gastrointestinal parasites on offspring quality in chinstrap penguins (Pygoscelis antarctica). Parasitology 139:819–824. doi:10.1017/S0031182011002381
Roitt I, Brostoff J, Male D (eds) (2001) Immunology, 6th edn. Mosby International Ltd, London
SAS Institute (2012) Using JMP. JMP, a business unit of SAS. SAS Campus Drive, Cary 462
Smits JE, Bortolotti GR, Tella JL (1999) Simplifying the phytohemagglutinin skin testing technique in studies of avian immunocompetence. Funct Ecol 13:567–572. doi:10.1046/j.1365-2435.1999.00338.x
Tella JL, Lemus JA, Carrete M, Blanco G (2008) The PHA test reflects acquired T-cell mediated immunocompetence in birds. PLoS ONE 3:e3295. doi:10.1371/journal.pone.0003295
Thrall MA, Weiser G, Allison R, Campbell TW (eds) (2012) Veterinary hematology and clinical chemistry, 2nd edn. Wiley-Blackwell, New York
Tucker CA, Yazwinski TA, Reynolds L, Johnson Z, Keating M (2007) Determination of the anthelmintic efficacy of albendazole in the treatment of chickens naturally infected with gastrointestinal helminths. J Appl Poult Res 16:392–396. doi:10.1093/japr/16.3.392
Vidal V (2014) Parasitofauna de pingüinos Pigoscélidos: morfología, infección, caracterización molecular y aplicaciones (Parasite fauna of Pygoscelid penguins: morphology, infection, molecular characterization and applications). Doctoral Thesis of Faculty of Veterinary Medicine, University of Murcia, 184
Wakelin D (1978) Immunity to intestinal parasites. Nature 273:617–620
Wakelin D, Apanius V (1997) Immune defence: genetic control. In: Clayton DH, Moore J (eds) Host-parasite evolution, general principles and avian models. Oxford University Press, Oxford, pp 30–58
Xavier JC, Barbosa A, Agusti S et al (2013) Polar marine science in Portugal and Spain: recent advances and future perspectives. J Sea Res 83:9–29
Acknowledgments
We very much appreciate the hospitality and logistic support of the Argentinean Antarctic Base “Carlini (ex Jubany).” We thank the logistic support provided by the Instituto Antártico Argentino (IAA-DNA). We thank the three anonymous reviewers for their suggestions that helped improve our manuscript. AB was supported by the Project CTM2011-24427 funded by the Spanish Ministry of Economy and Competitiveness. Permits for working in the study area and for penguin handling were issued by the Dirección Nacional del Antártico, Argentina.
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Bertellotti, M., D’Amico, V.L., Palacios, M.G. et al. Effects of antihelminthic treatment on cell-mediated immunity in Gentoo penguin chicks. Polar Biol 39, 1207–1212 (2016). https://doi.org/10.1007/s00300-015-1839-0
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DOI: https://doi.org/10.1007/s00300-015-1839-0