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Pollution and physiological variability in gentoo penguins at two rookeries with different levels of human visitation

Published online by Cambridge University Press:  20 March 2013

Andrés Barbosa ,
Eva de Mas ,
Jesús Benzal ,
Julia Ines Diaz ,
Miguel Motas ,
Silvia Jerez ,
Luis Pertierra ,
Javier Benayas ,
Ana Justel  and
Pilar Lauzurica
...Show all authors
Andrés Barbosa*
Affiliation:
Departamento Ecología Evolutiva, Museo Nacional de Ciencias Naturales, CSIC, C/José Gutierrez Abascal, 2, 28006 Madrid, Spain Departamento Ecología Funcional y Evolutiva, Estación Experimental de Zonas Áridas, CSIC, Carretera de Sacramento s/n, La Cañada de San Urbano, 04120 Almeria, Spain
Eva de Mas
Affiliation:
Departamento Ecología Funcional y Evolutiva, Estación Experimental de Zonas Áridas, CSIC, Carretera de Sacramento s/n, La Cañada de San Urbano, 04120 Almeria, Spain
Jesús Benzal
Affiliation:
Departamento Ecología Funcional y Evolutiva, Estación Experimental de Zonas Áridas, CSIC, Carretera de Sacramento s/n, La Cañada de San Urbano, 04120 Almeria, Spain
Julia Ines Diaz
Affiliation:
Centro de Estudios Parasitológicos y de Vectores, CONICET, Universidad Nacional de La Plata, Calle 2 584, CCT La Plata, Buenos Aires, Argentina
Miguel Motas
Affiliation:
Departamento Toxicología, Facultad de Veterinaria, Universidad de Murcia, Campus Espinardo, 30100 Murcia, Spain
Silvia Jerez
Affiliation:
Departamento Toxicología, Facultad de Veterinaria, Universidad de Murcia, Campus Espinardo, 30100 Murcia, Spain
Luis Pertierra
Affiliation:
Departamento Ecología, Universidad Autónoma de Madrid, 28049 Madrid, Spain
Javier Benayas
Affiliation:
Departamento Ecología, Universidad Autónoma de Madrid, 28049 Madrid, Spain
Ana Justel
Affiliation:
Departamento Ecología, Universidad Autónoma de Madrid, 28049 Madrid, Spain
Pilar Lauzurica
Affiliation:
Unidad de Activación Inmunológica, Centro Nacional de Microbiología, Instituto de Salud Carlos III, Crtra Pozuelo Km 2, 28229 Majadahonda, Spain
Francisco Javier Garcia-Peña
Affiliation:
Laboratorio Central de Veterinaria, Crtra Algete Km 8, 28110 Algete, Spain
Tania Serrano
Affiliation:
Laboratorio Central de Veterinaria, Crtra Algete Km 8, 28110 Algete, Spain
*
[email protected]
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Abstract

Human activity and specifically tourism has been increasing in Antarctica over the last few years. Few studies have examined the indirect effects of human visits on Antarctic penguin rookeries. This work aims to study the differences between a highly visited (Hannah Point) and a rarely visited (Devil's Point, Byers Peninsula) gentoo penguin rookery on Livingston Island. Our results suggest that potential indirect effects of human impact are observed in gentoo penguins at Hannah Point, a colony heavily visited by tourists. Penguins at Hannah Point showed a higher presence of heavy metals such as Pb and Ni and a higher number of erythrocytic nuclear abnormalities than penguins at Devil's Point. Immunological parameters showed different results depending on whether we consider the cellular response - the number of lymphocytes being higher in penguins from Hannah Point - or the humoral response - the level of immunoglobulins being higher in penguins from Devil's Point. Measurements of corticosterone levels in feathers and heterophil/lymphocyte (H/L) ratio in blood showed lower levels in the heavily visited rookery than in the rarely visited rookery. Finally, we did not detect Campylobacter jejuni, a bacteria potentially transmitted by humans in either of the populations and we did not find any difference in the prevalence of Campylobacter lari between the populations.

Keywords

Antarctic penguinsgenotoxic damagehuman disturbanceimmune responsepollutionstress
Type
Research Articles
Information
Antarctic Science , Volume 25 , Issue 2: Byers Peninsula – A New Reference Site For The Maritime Antarctic , April 2013 , pp. 329 - 338
Copyright
Copyright © Antarctic Science Ltd 2013

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References

Afanasieva, K., Rushkovsky, S.Bezrukov, V. 2006. Parameters of chromosomal instability of Pygoscelis papua. Bulgaria Antarctic Research Life Sciences, 5, 9–13.Google Scholar
ATSDR (Agency for Toxic Substances and Disease Registry). 2005. Toxicological profile for nickel. Atlanta, GA: US Department of Health and Human Services, Public Health Service, 397 pp.Google Scholar
Barbosa, A.Palacios, M.J. 2009. Health of Antarctic birds: a review of their parasites, pathogens and diseases. Polar Biology, 32, 1095–1115.CrossRefGoogle ScholarPubMed
Barbosa, A., Merino, S., Benzal, J., Martinez, J.García-Fraile, S. 2007a. Geographic variation in the immunoglobulin levels in pygoscelid penguins. Polar Biology, 30, 219–225.CrossRefGoogle Scholar
Barbosa, A., Merino, S., Benzal, J., Martinez, J.García-Fraile, S. 2007b. Population variability in heat shock proteins among three Antarctic penguin species. Polar Biology, 30, 1239–1244.CrossRefGoogle Scholar
Barbosa, A., Benzal, J., Vidal, V., D'Amico, V., Coria, N., Diaz, J., Motas, M., Palacios, M.J., Cuervo, J.J., Ortiz, J.Chitima, L. 2011. Seabird ticks (Ixodes uriae) distribution along the Antarctic Peninsula. Polar Biology, 34, 1621–1624.CrossRefGoogle Scholar
Bargagli, R. 2008. Environmental contamination in Antarctic ecosystems. Science of the Total Environment, 400, 212–226.CrossRefGoogle ScholarPubMed
Bonnedahl, J., Broman, T., Waldenström, J., Palmgren, H., Niskanen, T.Olsen, B. 2005. In search of human-associated bacterial pathogens in Antarctic wildlife: report from six penguin colonies regularly visited by tourists. Ambio, 34, 430–432.CrossRefGoogle ScholarPubMed
Bortolloti, G.R., Marchant, T.A., Blas, J.German, T. 2008. Corticosterone in feathers is a long-term, integrated measure of avian stress physiology. Functional Ecology, 22, 494–500.CrossRefGoogle Scholar
Braude, S., Tang-Martinez, Z.Taylor, G.T. 1999. Stress, testosterone, and the immunoredistribution hypothesis. Behavioral Ecology, 10, 345–350.CrossRefGoogle Scholar
Bricher, P.K., Lucieer, A.Woehler, W.J. 2008. Population trends of Adélie penguin (Pygoscelis adeliae) breeding colonies: a spatial analysis of the effect of snow accumulation and human activities. Polar Biology, 31, 1397–1407.CrossRefGoogle Scholar
Broman, T., Bergström, S., On, S.L.V., Palmgren, H., McCafferty, D.J., Sellin, M.Olsen, B. 2000. Isolation and characterization of Campylobacter jejuni subsp. jejuni from macaroni penguins (Eudyptes chrysolophus) in the Subantarctic region. Applied and Environmental Microbiology, 66, 449–452.CrossRefGoogle ScholarPubMed
Carlini, A.R., Coria, N.R., Santos, M.M., Libertelli, M.M.Donini, G. 2007. Breeding success and population trends in Adélie penguins in areas with low and high levels of human disturbance. Polar Biology, 30, 917–924.CrossRefGoogle Scholar
Cobley, N.D.Shears, J.R. 1999. Breeding performance of gentoo penguins (Pygoscelis papua) at a colony exposed to high levels of human disturbance. Polar Biology, 21, 355–360.CrossRefGoogle Scholar
Curry, C.H., McCarthy, J.S., Darragh, H.M., Wake, R.A., Todhunter, R.Terris, J. 2002. Could tourist boots act as vectors for disease transmission in Antarctica? Journal of Travel Medicine, 9, 190–193.CrossRefGoogle ScholarPubMed
De Villiers, M. 2008. Review of recent research into the effects of human disturbance on wildlife in the Antarctic and sub-Antarctic region. Working Paper 12, XXXI Antarctic Treaty Consultative Meeting, 2–13 June 2008, Kiev, Ukraine.Google Scholar
Dhabhar, F.S., Miller, A.H., McEwen, B.S.Spencer, R.L. 1995. Effects of stress on immune cell distribution: dynamics and hormonal mechanisms. Journal of Immunology, 154, 5511–5527.CrossRefGoogle ScholarPubMed
Dranitsina, A.S., Telgeev, G.D., Maliuta, S.S.Bezrukov, F.V. 2006. Genetic diversity in populations of gentoo penguins (Pygoscelis papua). Tsitologiia I Genetika, 40, 57–62.Google ScholarPubMed
Dufva, R.Allander, K. 1995. Intraspecific variation in plumage coloration reflects immune response in great tit (Parus major) males. Functional Ecology, 9, 785–789.CrossRefGoogle Scholar
Eisler, R. 1998. Nickel hazards to fish, wildlife, and invertebrates: a synoptic review. Washington, DC: Geological Survey, Biological Resources Division, Biological Science Report No. 34, 86 pp.Google Scholar
Ellenberg, U., Setiawan, N.A., Cree, A., Houston, D.M.Seddon, P.J. 2007. Elevated hormonal stress response and reduced reproductive output in yellow-eye penguins exponsed to unregulated tourism. General and Comparative Endocrinology, 152, 54–63.CrossRefGoogle Scholar
Fraser, W.R.Patterson, D.L. 1997. Human disturbance and long-term changes in Adélie penguin populations: a natural experiment at Palmer Station, Antarctic Peninsula. In Battaglia, B., Valencia, J.&Walton, D.W.H.,eds. Antarctic communities: species, structure and survival. Cambridge: Cambridge University Press, 445–452.Google Scholar
Giese, M. 1996. Effects of human activity on Adélie penguin Pygoscelis adeliae breeding success. Biological Conservation, 75, 157–164.CrossRefGoogle Scholar
Gochfeld, M., Belant, J.L., Shukla, T., Benson, T.Burger, J. 1996. Heavy metals in laughing gulls: gender, age and tissue differences. Environmental Toxicology and Chemistry, 15, 2275–2283.CrossRefGoogle Scholar
Gorman, R.Adley, C.C. 2004. An evaluation of five preservation techniques and conventional freezing temperatures of -20°C and -85°C for long-term preservation of Campylobacter jejuni. Letters of Applied Microbiology, 38, 306–310.CrossRefGoogle Scholar
Gross, W.B.Siegel, P.B. 1983. Evaluation of the heterophil/lymphocyte ratio as a measure of stress in chicken. Avian Diseases, 27, 972–979.CrossRefGoogle Scholar
Hawkey, C.M.Dennet, P.B. 1989. A color atlas of comparative veterinary haematology. Iowa City, IA: Iowa State University Press, 200 pp.Google Scholar
Holberton, R.L., Helmuth, B.Wingfield, J.C. 1996. The corticosterone stress response in gentoo and king penguins during the nonfasting period. Condor, 98, 850–854.CrossRefGoogle Scholar
Holmes, N. 2007. Comparing king, gentoo, and royal penguin responses to pedestrian visitation. Journal of Wildlife Management, 71, 2575–2582.CrossRefGoogle Scholar
Holmes, N., Giese, M., Achurch, H., Robinson, S.Kriwoken, L.K. 2005. Behaviour and breeding success of gentoo penguins Pygoscelis papua in areas of low and high human activity. Polar Biology, 29, 399–412.CrossRefGoogle Scholar
Honda, K., Yamamoto, Y., Hidaka, H.Tatsukawa, R. 1986. Heavy metal accumulations in Adélie penguin Pygoscelis adeliae and their variations with the reproductive success. Memoirs of National of National Institute of Polar Research, 40, 443–453.Google Scholar
IAATO (International Association for Antarctic Tour Operations). 2010. IAATO overview of Antarctic tourism: 2009–10 season and preliminary estimates for 2010–11 and beyond. http://image.zenn.net/replace/client/1000037/1000115/application/msword/ATCM33_ip113.doc, accessed August 2010.Google Scholar
Janes, M.E., Bower, R.K.Anthony, N.B. 1994. The leukocyte response of Japanese quail to Rous sarcoma virus-induced tumors. Avian Diseases, 38, 610–615.CrossRefGoogle ScholarPubMed
Jerez, S., Motas, M., Cánovas, R.A., Talavera, J., Almela, R.M.Bayón, A. 2010. Accumulation and tissue distribution of heavy metals and essential elements in loggerhead turtles (Caretta caretta) from Spanish Mediterranean coastline of Murcia. Chemosphere, 78, 256–264.CrossRefGoogle ScholarPubMed
Jerez, S., Motas, M., Palacios, M.J., Valera, F., Cuervo, J.J.Barbosa, A. 2011. Concentrations on trade elements in feathers of three Antarctic penguins: geographical and interspecific differences. Environmental Pollution, 159, 2412–2419.CrossRefGoogle Scholar
Kursa, M.Bezrukov, V. 2008. Health status in an Antarctic top predator: micronuclei frequency and white blood cells differentials in the south polar skua (Catharacta maccormicki). Polarforschung, 77, 1–5.Google Scholar
Leotta, G., Vigo, G.Giacoboni, G. 2006. Isolation of Campylobacter lari from seabirds in Hope Bay, Antarctica. Polish Polar Research, 27, 303–308.Google Scholar
Lynch, H.J., Fagan, W.F.Naveen, R. 2010. Population trends and reproductive success at a frequently visited penguin colony on the western Antarctic Peninsula. Polar Biology, 33, 493–503.CrossRefGoogle Scholar
Martinez, J., Tomas, G., Merino, S., Arriero, E.Moreno, J. 2003. Detection of serum immunoglobulins in wild birds by direct ELISA: a methodological study to validate the technique in different species using antichicken antibodies. Functional Ecology, 17, 700–706.CrossRefGoogle Scholar
Maxwell, M.H.Robertson, G.W. 1998. The avian heterophil leucocyte: a review. World Poultry Science Journal, 54, 155–178.CrossRefGoogle Scholar
Metcheva, R., Yurukova, L., Teodorova, S.Nikolova, E. 2006. The penguin feathers as bioindicator of Antarctica environmental state. Science of the Total Environment, 362, 259–265.CrossRefGoogle Scholar
Moreno, J., de Leon, A., Fargallo, J.A.Moreno, E. 1998. Breeding time, health and immune response in the chinstrap penguin Pygoscelis antarctica. Oecologia, 115, 312–319.CrossRefGoogle ScholarPubMed
Müller, C., Jenni-Eiermann, S.Jenni, L. 2011. Heterophils/lymphocytes-ratio and circulating corticosterone do not indicate the same stress imposed on Eurasian kestrel nestlings. Functional Ecology, 25, 566–576.CrossRefGoogle Scholar
Nimon, A.J., Schroter, R.C.Stonehouse, B. 1995. Heart rate of disturbed penguins. Nature, 374, 415.CrossRefGoogle Scholar
Otley, H.M. 2005. Nature-based tourism: experiences at Volunteer Point penguin colony in the Falkland Islands. Marine Ornithology, 33, 181–187.Google Scholar
Partecke, J., Schwabl, I.Gwinner, E. 2006. Stress and the city: urbanization and its effects on the stress physiology in European blackbirds. Ecology, 87, 1945–1952.CrossRefGoogle ScholarPubMed
Romero, L.M.Wikelski, M. 2002. Corticosterone levels predict survival probabilities of Galapagos marine iguanas during El Niño events. Proceedings of the National Academy of Sciences of the United States of America, 98, 7366–7370.CrossRefGoogle Scholar
Saino, N., Suffritti, C., Martinelli, R., Rubolini, D.Moller, A.P. 2003. Immune response covaries with corticosterone plasma levels under experimentally stressful conditions in nestling barn swallows (Hirundo rustica). Behavioral Ecology, 14, 318–325.CrossRefGoogle Scholar
Sapolsky, R.M. 1992. Neuroendocrinology of the stress response. In Becker, J.B., Breedlove, S.M.&Crews, D.,eds. Behavioural endocrinology. Cambridge, MA: MIT Press, 287–324.Google Scholar
Schmid, W. 1975. Micronucleus test. Mutation Research, 31, 9–15.CrossRefGoogle ScholarPubMed
Scheuhammer, A.M. 1987. The chronic toxicity of aluminium, cadmium, mercury and lead in birds: a review. Environmental Pollution, 46, 263–295.CrossRefGoogle ScholarPubMed
Smichowski, P., Vodopivez, C., Muñoz-Olivas, R.Gutierrez, A.M. 2006. Monitoring trace elements in selected organs of Antarctic penguin (Pygoscelis adeliae) by plasma-based techniques. Microchemical Journal, 82, 1–7.CrossRefGoogle Scholar
Snoeijs, T., Dauwe, T., Pinxten, R., Vandesande, R.Eens, M. 2004. Heavy metal exposure affects the humoral immune response in a free-living small songbird, the great tit (Parus major). Archive Environmental Contamination and Toxicology, 46, 399–404.CrossRefGoogle Scholar
Steele, T.W.McDermott, S.N. 1984. The use of membrane filters applied directly to the surface of agar plates for the isolation of C. jejuni from faeces. Pathology, 16, 263–265.CrossRefGoogle Scholar
Stoncius, D.Lazutka, J.R. 2003. Spontaneous and benzo[a]pyrene-induced micronuclei in the embryos of the black-headed gull (Larus ridibundus L.). Mutation Research-Genetic Toxicology and Environmental Mutagenesis, 538, 31–39.CrossRefGoogle Scholar
Tin, T., Fleming, Z.L., Hughes, K.A., Ainley, D.G., Convey, P., Moreno, C.A., Pfeiffer, S., Scott, J.Snape, I. 2009. Impacts of local human activities on the Antarctic environment. Antarctic Science, 21, 3–33.CrossRefGoogle Scholar
Trathan, P.N., Forcada, J., Atkinson, R., Downie, R.H.Shears, J.R. 2008. Population assessments of gentoo penguins (Pygoscelis papua) breeding at an important Antarctic tourist site, Goudier Island, Port Lockroy, Palmer Archipelago, Antarctica. Biological Conservation, 141, 3019–3028.CrossRefGoogle Scholar
Van Ngan, P.V., Gomes, V., Passos, M.J.A.C.R., Ussami, K.A., Campos, D.Y.F., Da Silva, A.J.Pereira, B.A. 2007. Biomonitoring of the genotoxic potential (micronucleus and erythrocyte nuclear abnormalities assay) of the Admiralty Bay water surroundings the Brazilian Antarctic Research Station “Comandante Ferraz”, King George Island. Polar Biology, 30, 209–217.CrossRefGoogle Scholar
Villanueva, C., Walker, B.G.Bertelotti, M. 2012. A matter of history: effects of tourist on physiology, behaviour and breeding parameters in Magellanic penguins (Spheniscus magellanicus) at two colonies in Argentina. Journal of Ornithology, 153, 219–228.CrossRefGoogle Scholar
Waldeström, J., Broman, T., Carlsson, I., Hasselquist, D., Achterberg, R.P., Wagenaar, J.A.Olsen, B. 2002. Prevalence of Campylobacter jejuni, Campylobacter lari and Campylobacter coli in different ecological guilds and taxa for migrating birds. Applied and Environmental Microbiology, 68, 5911–5917.CrossRefGoogle Scholar
Walker, B.G., Boersma, P.D.Wingfield, J.C. 2006. Habituation of adult magellanic penguins to human visitation as expressed through behavior and corticosterone secretion. Conservation Biology, 20, 146–154.CrossRefGoogle ScholarPubMed
Zuk, M.Johnsen, T.S. 1998. Seasonal changes in the relationship between ornamentation and immune response in red jungle fowl. Proceedings of the Royal Society of London, B265, 1631–1635.CrossRefGoogle Scholar