Hemosporidian Blood Parasites in Seabirds—A Comparative Genetic Study of Species from Antarctic to Tropical Habitats

Naturwissenschaften (2010) 97:809–817 DOI 10.1007/s00114-010-0698-3 ORIGINAL PAPER Hemosporidian blood parasites in seabirds—a comparative genetic study of species from Antarctic to tropical habitats Petra Quillfeldt & Javier Martínez & Janos Hennicke & Katrin Ludynia & Anja Gladbach & Juan F. Masello & Samuel Riou & Santiago Merino Received: 21 May 2010 /Revised: 7 July 2010 /Accepted: 7 July 2010 /Published online: 23 July 2010 # The Author(s) 2010. This article is published with open access at Springerlink.com Abstract Whereas some bird species are heavily affected by ranging from Antarctica to the tropical Indian Ocean. We did blood parasites in the wild, others reportedly are not. Seabirds, not detect parasites in 11 of these species, including one in particular, are often free from blood parasites, even in the Antarctic, four subantarctic, two temperate, and four tropical presence of potential vectors. By means of polymerase chain species. On the other hand, two subantarctic species, thin- reaction, we amplified a DNA fragment from the cytochrome billed prions Pachyptila belcheri and dolphin gulls Larus b gene to detect parasites of the genera Plasmodium, scoresbii, were found infected. One of 28 thin-billed prions Leucocytozoon,andHaemoproteus in 14 seabird species, had a Plasmodium infection whose DNA sequence was identical to lineage P22 of Plasmodium relictum, and one of 20 dolphin gulls was infected with a Haemoproteus lineage which appears phylogenetically clustered with parasites P. Quillfeldt (*) : K. Ludynia : A. Gladbach : J. F. Masello Max-Planck-Institut für Ornithologie, Vogelwarte Radolfzell, species isolated from passeriform birds such as Haemopro- Schlossallee 2, teus lanii, Haemoproteus magnus, Haemoproteus fringillae, 78315 Radolfzell, Germany Haemoproteus sylvae, Haemoproteus payevskyi,andHae- e-mail: [email protected] moproteus belopolskyi. In addition, we found a high parasite J. Martínez prevalence in a single tropical species, the Christmas Island Departamento de Microbiología y Parasitología, frigatebird Fregata andrewsi, where 56% of sampled adults Universidad de Alcalá, Alcalá de Henares, were infected with Haemoproteus. The latter formed a Madrid, Spain monophyletic group that includes a Haemoproteus line from J. Hennicke Eastern Asian black-tailed gulls Larus crassirostris.Our Abteilung Ökologie und Naturschutz, Biozentrum Grindel, results are in agreement with those showing that (a) seabirds Universität Hamburg, are poor in hemosporidians and (b) latitude could be a Martin-Luther-King Platz 3, determining factor to predict the presence of hemosporidians 20146 Hamburg, Germany in birds. However, further studies should explore the relative K. Ludynia importance of extrinsic and intrinsic factors on parasite Animal Demography Unit, Department of Zoology, prevalence, in particular using phylogenetically controlled University of Cape Town, comparative analyses, systematic sampling and screening of Rondebosch, 7701 Cape Town, South Africa vectors, and within-species comparisons. S. Riou Keywords Avian hematozoa . Blood parasites . Institute of Integrative and Comparative Biology, Hemoparasites . Innate immunity. Seabirds University of Leeds, Leeds LS2 9JT, UK S. Merino Introduction Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones Científicas, Parasites exert important ecological and evolutionary Madrid, Spain pressures on their hosts. Blood parasites (hematozoa) were 810 Naturwissenschaften (2010) 97:809–817 considered to be organisms of low pathogenicity in wild may not detect parasites if the intensity is low (e.g., populations, but it has been demonstrated that hematozoa can Plasmodium and Haemoproteus spp. during early spring; have important implications for bird community structure and Valkiūnas 2005). Genetic methods, using sensitive poly- conservation (e.g., van Riper et al. 1986), as well as life merase chain reaction (PCR), can detect some parasitemia history traits of avian hosts (e.g., Merino et al. 2000;Hõrak missed by blood smears (e.g., Feldman and Freed 1995; et al. 2001;Sanzetal.2001a, b; Sol et al. 2003;Marzaletal. Bensch et al. 2000; Perkins and Schall 2002; Ricklefs et al. 2005). Knowledge about the prevalence of hematozoa is thus 2005; Parker et al. 2006; Merino et al. 2008). However, essential for understanding the ecological and evolutionary false negatives are not completely excluded by molecular implications of these parasites on their hosts and, ultimately, methods (Gomez-Diaz et al. 2010). Furthermore, molecular on ecosystems (see Sol et al. 2003). methods are still inaccurate for the identification of the Birds are infected by a number of intracellular blood parasite species and should be combined with light parasites, including Hemosporidia of the genera Plasmodium, microscopy (Valkiūnas et al. 2008). Haemoproteus,andLeucocytozoon, and Haemogregarinidae In the present study, we used genetic methods to detect of the genus Hepatozoon and piroplasmids of the genus parasites in a suite of 14 seabird species, ranging from Babesia. It has been established that once birds become Antarctica to the tropical Indian Ocean. Specifically, we infected with hemosporidian parasites, they remain infected aimed to validate the hypothesis that hemosporidian blood either for life or many years (Garnham 1966;Valkiūnas 2005). parasite prevalences are low among seabirds and especially The intracellular hematozoa occurring in vertebrates in cold climates. belong to the phylum Apicomplexa, and their life cycle generally consists of three major phases (Bush et al. 2001). Schizogony is an asexual phase in which multiple mitoses Methods take place, resulting in daughter cells. Schizogony occurs within the vertebrate host and causes disease by destroying Study species host erythrocytes (Plasmodium, Haemoproteus, Leucocyto- zoon) or leucocytes (Leucocytozoon, Hepatozoon). The Wilson’s storm-petrels Oceanites oceanicus were sampled remaining phases of the life cycle, gametogony and in their Antarctic breeding grounds at King George Island sporogony, occur within an arthropod vector and result in (62°14′ S, 58°40′ W), during fieldwork described in detail the production of infective sporozoites. Transmission can previously (summarized in Quillfeldt 2004; Büßer et al. occur through different hematophagous arthropods. Plas- 2008; Gladbach et al. 2009). Out of previously collected modium is transmitted by mosquitoes (Culicidae) and less blood samples (breeding season 1999–2000), we randomly commonly by sandflies (Psychodidae). Haemoproteus is selected samples of six males and six females for the transmitted by louse flies (Hippoboscidae) and biting present analysis. We observed no biting insects at the midges (Ceratopogonidae) and Leucocytozoon by blackflies breeding grounds of Wilson’s storm-petrels, the only (Simulidae). Hepatozoon is most commonly transmitted by ectoparasites found being the Mallophaga Philoceanus ticks (Ixodidae, Smith 1996). robertsi (Phthiraptera: Ischnocera; Quillfeldt et al. 2004a). The prevalence of infection varies greatly among different Subantarctic species were sampled at New Island, bird orders (e.g., Bennett et al. 1993a, b; Valkiūnas 2005), but Falkland Islands (51°43′ S, 61°17′ W). We included the reasons for interspecific variation in parasite prevalence samples of two seasons (2007−2008 and 2008−2009) into or diversity are still poorly understood (Scheuerlein and the analysis for thin-billed prions Pachyptila belcheri, Ricklefs 2004). Absence or scarcity of blood parasites has imperial shags Phalacrocorax atriceps, and southern been reported from avian groups such as seabirds (e.g., rockhopper penguins Eudyptes chrysocome. General field- Peirce and Brooke 1993;Merinoetal.1997a;Merinoand work techniques have been described in detail previously Minguez 1998;Engströmetal.2000), swifts (Tella et al. for thin-billed prions (e.g., Quillfeldt et al. 2003, 2007a, b, 1995), waders (Figuerola et al. 1996), raptors (e.g., Tella et 2008) and southern rockhopper penguins (e.g., Poisbleau et al. 1996), and parrots (Masello et al. 2006). There is also al. 2008). Additionally, in 2008−2009, we collected some evidence that blood parasites are less common in samples from dolphin gulls Larus scoresbii, Magellanic certain habitats such as the Arctic tundra (e.g., Bennett et al. penguins Spheniscus magellanicus, and gentoo penguins 1992), arid environments (e.g., Little and Earlé 1995; Valera Pygoscelis papua. All adult birds in New Island were et al. 2003), island environments (e.g., Little and Earlé sampled at their nest when attending young chicks. Adults 1994), or marine environments (e.g., Piersma 1997;Figuerola were captured by hand, blood-sampled and measured (for 1999;Jovanietal.2001). sample sizes, see Table 1). Potential arthropod vectors in Most previous studies used blood smears to detect blood the New Island seabird community include fleas Para- parasites. However, it has been suggested that blood smears psyllus sp. that are common in nest burrows of thin-billed Naturwissenschaften (2010) 97:809–817 811 Table 1 Data on the bird species sampled in the present study Species Scientific name Breeding site Number Parasites found Prevalencea Antarctic Wilson’s storm-petrel Oceanites oceanicus King George Island (62°14′ S, 58°40′ W) 12 (6f, 6m) –– Subantarctic Rockhopper penguin Eudyptes chrysocome New Island (51°43′ S, 61°17′ W) 28 (14f, 14m) –– Magellanic penguin Spheniscus magellanicus New Island (51°43′ S,

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