Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-02T18:54:08.618Z Has data issue: false hasContentIssue false
  • English
  • Français

Blood parasites in noddies and boobies from Brazilian offshore islands – differences between species and influence of nesting habitat

Published online by Cambridge University Press:  07 November 2013

PETRA QUILLFELDT ,
JAVIER MARTÍNEZ ,
LEANDRO BUGONI ,
PATRÍCIA L. MANCINI  and
SANTIAGO MERINO
PETRA QUILLFELDT*
Affiliation:
Department of Animal Ecology and Systematics, Justus Liebig University Giessen, Heinrich-Buff-Ring, 35392 Giessen, Germany
JAVIER MARTÍNEZ
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Farmacia, Universidad de Alcalá de Henares, Alcalá de Henares, E-28871, Madrid, Spain
LEANDRO BUGONI
Affiliation:
Universidade Federal do Rio Grande (FURG), Instituto de Ciências Biológicas and Instituto de Oceanografia, Campus Carreiros, CP 474, CEP 96203-900, Rio Grande, RS, Brasil
PATRÍCIA L. MANCINI
Affiliation:
Universidade Federal do Rio Grande (FURG), Instituto de Ciências Biológicas and Instituto de Oceanografia, Campus Carreiros, CP 474, CEP 96203-900, Rio Grande, RS, Brasil
SANTIAGO MERINO
Affiliation:
Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones Científicas, Madrid, Spain
*
* Corresponding author. Department of Animal Ecology and Systematics, Justus Liebig University Giessen, Heinrich-Buff-Ring, 35392 Giessen, Germany. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Seabirds are often free from blood parasites, and a recent review suggested that phylogenetic, ecological and life-history parameters can determine the prevalence of blood parasites in seabirds. However, there is a lack of data available from many seabird groups, and a larger database is needed to understand prevalence patterns of blood parasites. We used a molecular screening approach to detect parasites of the genera Plasmodium, Haemoproteus, Leucocytozoon and Babesia in five species of two genera of seabirds that breed on Atlantic Ocean islands off Brazil. The observed patterns differed between the two bird genera. Like other Laridae, brown noddy, Anous stolidus adults were infected with Haemoproteus with low prevalence. Masked boobies, Sula dactylatra and brown boobies, Sula leucogaster were infected with Babesia. Of the latter, mainly juveniles were infected. In all species, intensity of infection (i.e. number of infected erythrocytes) was so low that parasites remained undetected in blood smears. This may explain the absence of major effects on the body condition of birds, although infected juvenile masked boobies were lighter than juveniles that were not infected with Babesia. Two tree-nesting species; black noddy, Anous minutus and red-footed booby, Sula sula did not have blood parasites, suggesting that tree-nesting may reduce the exposure to arthropod vectors compared with ground nesting in these species.

Keywords

avian haematozoablood parasiteshaemoparasitesinnate immunityseabirds
Type
Research Article
Information
Parasitology , Volume 141 , Issue 3 , March 2014 , pp. 399 - 410
Check for updates
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Almeria, S., Castella, J., Ferrer, D., Ortuno, A., Estrada-Pena, A. and Gutierrez, J. F. (2001). Bovine piroplasms in Minorca (Balearic Islands, Spain): a comparison of PCR-based and light microscopy detection. Veterinary Parasitology 99, 249–259.CrossRefGoogle Scholar
Alves, V. S., Couto, G. S., Efe, M. A. and Ribeiro, A. B. B. (2000). As aves do Arquipélago dos Abrolhos. Ibama, Brasília, Brazil.Google Scholar
Ano, H., Makimura, S. and Harasawa, R. (2001). Detection of Babesia species from infected dog blood by polymerase chain reaction. Journal of Veterinary Medical Science 63, 111–113.CrossRefGoogle ScholarPubMed
Antas, P. T. Z. (1991). Status and conservation of seabirds breeding in Brazilian waters. In Seabird Status and Conservation: A Supplement (Techn. Publ. 11) (ed. Croxall, J. P.), pp. 141–158. International Council for Bird Preservation, Cambridge, UK.Google Scholar
Atkinson, C. T., Utzurrum, R. C., Seamon, J. O., Savage, A. F. and Lapointe, D. A. (2006). Hematozoa of forest birds in American Samoa – evidence for a diverse, indigenous parasite fauna from the South Pacific. Pacific Conservation Biology 12, 229.Google Scholar
Bennett, G. F., Bishop, M. A. and Peirce, M. A. (1993). Checklist of the avian species of Plasmodium Marchiafava and Celli, 1885 (Apicomplexa) and their distribution by avian family and Wallacean life zones. Systematic Parasitology 26, 171–179.Google Scholar
Bensch, S., Stjernman, M., Hasselquist, D., Ostman, O., Hansson, B., Westerdahl, H. and Pinheiro, R. T. (2000). Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proceedings of the Royal Society of London B, Biological Sciences 267, 1583–1589.CrossRefGoogle ScholarPubMed
Both, R. and Freitas, T. O. R. (2004). Aves marinhas no arquipélago de São Pedro e São Paulo. In Aves marinhas e insulares brasileiras: bioecologia e conservação (ed. Branco, J. O.), pp. 193–212. Editora da UNIVALI, Itajaí, Brazil.Google Scholar
Clark, G. W. and Swinehart, B. (1969). Avian haematozoa from the offshore islands of northern Mexico. Journal of Wildlife Diseases 5, 111–112.Google Scholar
Criado, A., Martínez, J., Buling, A., Barba, J. C., Merino, S., Jefferies, R. and Irwin, P. J. (2006). New data on epizootiology and genetics of piroplasms based on sequences of small ribosomal subunit and cytochrome b genes. Veterinary Parasitology 142, 238–247.Google Scholar
Croft, R. E. and Kingston, N. (1975). Babesia moshkovskii (Schuren-kova, 1938) Laird and Lari, 1957; from the prairie falcon, Falco mexicanus, in Wyoming; with comments on other parasites found in this host. Journal of Wildlife Diseases 11, 229–233.CrossRefGoogle ScholarPubMed
Dearborn, D. C., Anders, A. D. and Parker, P. G. (2001). Sexual dimorphism, extrapair fertilizations, and operational sex ratio in great frigatebirds (Fregata minor). Behavioral Ecology 12, 746–752.CrossRefGoogle Scholar
Dehnhard, N., Quillfeldt, P. and Hennicke, J. C. (2011). Leucocyte profiles and H/L ratios in chicks of red-tailed tropicbirds reflect the ontogeny of the immune system. Journal of Comparative Physiology B 181, 641–648.Google Scholar
Engström, H., Dufva, R. and Olsson, G. (2000). Absence of haematozoa and ectoparasites in a highly sexually ornamented species, the crested auklet. Waterbirds 23, 486–488.Google Scholar
Feldman, R. A. and Freed, L. A. (1995). A PCR test for avian malaria in Hawaiian birds. Molecular Ecology 4, 663–674.CrossRefGoogle ScholarPubMed
Flechtmann, C. H. W. (1987). Sobre uma pequena coleção de ácaros (Arthropoda, Acari) do território federal de Fernando de Noronha, Brasil. Anais da Escola Superior de Agricultura Luiz de Queiroz 44, 1643–1647.Google Scholar
Garnham, P. C. C. (1966). Malaria Parasites and other Haemosporidia. Blackwell, Oxford, UK.Google Scholar
Graciolli, G. and Carvalho, C. J. B. (2003). Hippoboscidae (Diptera, Hippoboscoidea) no Estado do Paraná, Brasil: chaves de identificação, hospedeiros e distribuição geográfica. Revista Brasileira de Ornitologia 20, 667–674.Google Scholar
Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W. and Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307–321.Google Scholar
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Hazin, M. C. and Macedo, R. H. (2006). Sooty tern nesting success as a function of nest location, density and vegetation type in a Neotropical atoll. Revista Brasileira de Ornitologia 14, 261–268.Google Scholar
Hõrak, P., Ots, I., Vellau, H., Spottiswoode, C. and Møller, A. P. (2001). Carotenoid-based plumage coloration reflects hemoparasite infection and local survival in breeding great tits. Oecologia 126, 166–173.Google Scholar
IBAMA/FUNATURA (1991). Plano de Manejo do Parque Nacional Marinho dos Abrolhos, pp. 96. Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis/Fundação Pró Natureza, Brasília. Aracruz Celulose S.A.Google Scholar
Jefferies, R., Down, J., McInnes, L., Ryan, U., Robertson, H., Jakob-Hoff, R. and Irwin, P. (2008). Molecular characterization of Babesia kiwiensis from the brown kiwi (Apteryx mantelli). Journal of Parasitology 94, 557–560.CrossRefGoogle ScholarPubMed
Kikuchi, R. K. P. and Leão, Z. M. A. N. (1997). Rocas (Southwestern Equatorial Atlantic, Brazil): an atoll built primarily by coralline algae. Proceedings of the 8th International Coral Reef Symposium 1, 731–736.Google Scholar
Lowery, R. S. (1971). Blood parasites of vertebrates on Aldabra. Philosophical Transactions of the Royal Society of London B 260, 577–580.Google Scholar
Madsen, V., Valkiūnas, G., Iezhova, T. A., Mercade, C., Sanchez, M. and Osorno, J. L. (2007). Testosterone levels and gular pouch coloration in courting magnificent frigatebird (Fregata magnificens): variation with age-class, visited status and blood parasite infection. Hormones and Behavior 51, 156–163.CrossRefGoogle ScholarPubMed
Martínez, J., Martínez de la Puente, J., Herrero, J., Del Cerro, S., Lobato, E., Rivero de Aguilar, J., Vasquez, R. A. and Merino, S. (2009). A restriction site to differentiate Plasmodium and Haemoproteus infections in birds: on the inefficiency of general primers for detection of mixed infections. Parasitology 136, 713–722.CrossRefGoogle ScholarPubMed
Martínez-Abraín, A., Merino, S., Oro, D. and Esparza, B. (2002). Prevalence of blood parasites in two western-Mediterranean local populations of the yellow-legged gull Larus cachinnans michahellis . Ornis Fennica 79, 34–40.Google Scholar
Marzal, A., de Lope, F., Navarro, C. and Møller, A. P. (2005). Malarial parasites decrease reproductive success: an experimental study in a passerine bird. Oecologia 142, 541–545.CrossRefGoogle Scholar
Merino, S. (1998). Babesia bennetti sp. nov., from the yellow-legged gull (Larus cachinnans, Aves, Laridae) in Benidorm Island, Mediterranean sea. Journal of Parasitology 84, 422–424.Google Scholar
Merino, S. and Minguez, E. (1998). Absence of hematozoa in a breeding colony of the storm petrel Hydrobates pelagicus . Ibis 140, 180–181.CrossRefGoogle Scholar
Merino, S., Barbosa, A., Moreno, J. and Potti, J. (1997 a). Absence of haematozoa in a wild chinstrap penguin Pygoscelis antarctica population. Polar Biology 18, 227–228.CrossRefGoogle Scholar
Merino, S., Potti, J. and Fargallo, J. A. (1997 b). Blood parasites of some passerine birds from central Spain. Journal of Wildlife Diseases 33, 638–641.Google Scholar
Merino, S., Moreno, J., Sanz, J. J. and Arriero, E. (2000). Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus). Proceedings of the Royal Society of London B, Biological Sciences 267, 2507–2510.Google Scholar
Merino, S., Peirce, M. A., Fernández, M. and Lanzarot, P. (2002). Redescription of Babesia moshkovskii (Schurenkova) from the griffon vulture Gyps fulvus (Hablizl). Journal of Natural History 36, 1635–1638.Google Scholar
Merino, S., Martinez, J., Martinez-de la Puente, J., Criado-Fornelio, A., Tomas, G., Morales, J., Lobato, E. and Garcia-Fraile, S. (2006). Molecular characterization of the 18S rDNA gene of an avian Hepatozoon reveals that it is closely related to Lankesterella . Journal of Parasitology 92, 1330–1335.CrossRefGoogle ScholarPubMed
Merino, S., Moreno, J., Vásquez, R. A., Martínez, J., Sánchez-Monsálvez, I., Estades, C. F., Ippi, S., Sabat, P., Rozzi, R. and McGehee, S. (2008). Haematozoa in forest birds from southern Chile: latitudinal gradients in prevalence and parasite lineage richness. Austral Ecology 33, 329–340.CrossRefGoogle Scholar
Merino, S., Hennicke, J., Martínez, J., Ludynia, K., Masello, J. F. and Quillfeldt, P. (2012). Infection by Haemoproteus parasites in four species of frigatebirds and description of Haemoproteus (Parahaemoproteus) valkiūnasi sp. nov. (Haemosporida, Haemoproteidae). Journal of Parasitology 98, 388–397.Google Scholar
Padilla, L. R., Whiteman, N. K., Merkel, J., Huyvert, K. P. and Parker, P. G. (2006). Health assessment of seabirds on Isla Genovesa, Galápagos. Ornithological Monographs 60, 86–97.CrossRefGoogle Scholar
Parker, P. G., Whiteman, N. K. and Miller, R. E. (2006). Conservation medicine on the Galápagos islands: partnerships among behavioral, population, and veterinary scientists. Auk 123, 625–638.Google Scholar
Peirce, M. A. (2000). A taxonomic review of avian piroplasms of the genus Babesia Starcovici, 1893 (Apicomplexa: Piroplasmorida: Babesiidae). Journal of Natural History 34, 317–332.Google Scholar
Peirce, M. A. (2005). A checklist of the valid avian species of Babesia (Apicomplexa: Piroplasmorida), Haemoproteus, Leucocytozoon (Apicomplexa: Haemosporida), and Hepatozoon (Apicomplexa: Haemogregarinidae). Journal of Natural History 39, 3621–3632.Google Scholar
Peirce, M. A. and Feare, C. J. (1978). Piroplasmosis in the masked booby Sula dactylatra melanops in the Amirantes, Indian Ocean. Bulletin of the British Ornithologists’ Club 98, 38–40.Google Scholar
Peirce, M. A. and Brooke, M. (1993). Failure to detect blood parasites in seabirds from the Pitcairn Islands. Seabird 15, 72–74.Google Scholar
Peirce, M. A. and Parsons, N. J. (2012). Babesia ugwidiensis, a new species of avian piroplasm from Phalacrocoracidae in South Africa. Parasite 19, 375–379.Google Scholar
Perkins, S. L. and Schall, J. J. (2002). A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. Journal of Parasitology 88, 972–978.CrossRefGoogle ScholarPubMed
Posada, D. (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.Google Scholar
Quillfeldt, P., Martinez, J., Hennicke, J., Ludynia, K., Gladbach, A., Masello, J. F., Riou, S. and Merino, S. (2010). Hemosporidian blood parasites in seabirds – a comparative genetic study of species from Antarctic to tropical habitats. Naturwissenschaften 97, 809–817.Google Scholar
Quillfeldt, P., Arriero, E., Martínez, J., Masello, J. F. and Merino, S. (2011). Prevalence of blood parasites in seabirds – a review. Frontiers in Zoology 8, 26.CrossRefGoogle ScholarPubMed
Rambaut, A. and Drummond, A. J. (2007). Tracer v1.4. Institute of Evolutionary Biology, University of Edinburgh. http://beast.bio.ed.ac.uk/Tracer Google Scholar
Remple, J. D. (2004). Intracellular hematozoa of raptors: a review and update. Journal of Avian Medicine and Surgery 18, 75–88.Google Scholar
Ricklefs, R. E. and Fallon, S. M. (2002). Diversification and host switching in avian malaria parasites. Proceedings of the Royal Society of London B, Biological Sciences 269, 885–892.Google Scholar
Ricklefs, R. E., Swanson, B. L., Fallon, S. M., Martinez-Abrain, A., Scheuerlein, A., Gray, J. and Latta, S. C. (2005). Community relationships of avian malaria parasites in southern Missouri. Ecological Monographs 75, 543–555.CrossRefGoogle Scholar
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.Google Scholar
Samour, J. H. and Peirce, M. A. (1996). Babesia shortti infection in a saker falcon (Falco cherrug). Veterinary Record 139, 167–168.Google Scholar
Schnittger, L., Rodriguez, A. E., Florin-Christensen, M. and Morrison, D. A. (2012). Babesia: a world emerging. Infection, Genetics and Evolution 12, 1788–1809.CrossRefGoogle ScholarPubMed
Schulz-Neto, A. (1998). Aspectos biológicos da avifauna na Reserva Biológica do Atol das Rocas, Rio Grande do Norte, Brasil. Hornero 15, 17–28.Google Scholar
Schulz-Neto, A. (2004 a). Aves insulares do arquipélago de Fernando de Noronha. In Aves marinhas e insulares brasileiras: bioecologia e conservação (ed. Branco, J. O.), pp. 147–168. Univali, Itajaí.Google Scholar
Schulz-Neto, A. (2004 b). Aves marinhas do Atol das Rocas. In Aves marinhas e insulares brasileiras: bioecologia e conservação (ed. Branco, J. O.), pp. 169–192. Univali, Itajaí.Google Scholar
Smith, T. G. (1996). The genus Hepatozoon (Apicomplexa: Adeleina). Journal of Parasitology 82, 565–585.Google Scholar
Talavera, G. and Castresana, J. (2007). Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56, 564–577.Google Scholar
Valkiūnas, G. (2005). Avian Malaria Parasites and other Haemosporidia. CRC Press, Boca Raton, FL, USA.Google Scholar
Valkiūnas, G., Iezhova, T. A., Krizanauskiene, A., Palinauskas, V., Seghal, R. N. M. and Bensch, S. (2008). A comparative analysis of microscopy and PCR-based detection methods for blood parasites. Journal of Parasitology 94, 1395–1401.Google Scholar
Votýpka, J. (2011). Babesia. http://tolweb.org/Babesia/68087/2011.05.18 in The Tree of Life Web Project. http://tolweb.org/ Google Scholar
Work, T. M. (1996). Weight, hematology, and serum chemistry of seven species of free-ranging tropical pelagic seabirds. Journal of Wildlife Diseases 34, 643–657.Google Scholar
Work, T. M. and Rameyer, R. A. (1997). Description and epizootiology of Babesia poelea n. sp. in brown boobies (Sula leucogaster (Boddaert)) on Sand Island, Johnston Atoll, Central Pacific. Journal of Parasitology 83, 734–738.Google Scholar
Yabsley, M. J. and Shock, B. C. (2013). Natural history of zoonotic Babesia: role of wildlife reservoirs. International Journal for Parasitology: Parasites and Wildlife 2, 18–31.Google ScholarPubMed
Yabsley, M. J., Greiner, E., Tseng, F. S., Garner, M. M., Nordhausen, R. W., Ziccardi, M. H., Borjesson, D. L. and Zabolotzky, S. (2009). Description of novel Babesia species and associated lesions from common murres (Uria aalge) from California. Journal of Parasitology 95, 1183–1188.Google Scholar