Skip to main content Accessibility help
×
×
Home

Prevalence of Haemoproteus sp. in Galápagos blue-footed boobies: effects on health and reproduction

  • LARISA LEE-CRUZ (a1), ANDREW A. CUNNINGHAM (a2), PAMELA MARTÍNEZ (a3), MARILYN CRUZ (a3), SIMON J. GOODMAN (a1) and KEITH C. HAMER (a1)...
Summary

Populations of blue-footed boobies in the Galápagos Islands have declined by at least 50% compared with numbers recorded during the 1960s. Recently, concern has been expressed about potential adverse effects of introduced blood parasites; in particular, malarial parasites (i.e. Plasmodium sp.), which are frequently pathogenic and can cause mortality and morbidity in birds, and blood parasites of the genus Haemoproteus, which can reduce fitness. We screened blue-footed boobies at six breeding colonies within Galápagos for both genera of parasite. At two sites, we also investigated whether there was any relationship between infection status and physiological condition or breeding success. We found a high prevalence of Haemoproteus spp. in adults and chicks using PCR, although none was found on blood smears. We found no evidence of Plasmodium. Effects of parasitism on the condition of birds were limited. Also, there was no evidence that infection with Haemoproteus adversely affected breeding success or chick growth. Our results suggest that poor success of breeding birds was not strongly associated with Haemoproteus infection. However, regular colony monitoring and examination of dead birds are necessary to assess whether acute Haemoproteus infection might be responsible for some mortality, particularly of chicks.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Prevalence of Haemoproteus sp. in Galápagos blue-footed boobies: effects on health and reproduction
      Available formats
      ×
      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Prevalence of Haemoproteus sp. in Galápagos blue-footed boobies: effects on health and reproduction
      Available formats
      ×
      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Prevalence of Haemoproteus sp. in Galápagos blue-footed boobies: effects on health and reproduction
      Available formats
      ×
Copyright
This is an Open Access article, distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike licence (http://creativecommons.org/licenses/by-nc-sa/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the same Creative Commons licence is included and the original work is properly cited. The written permission of Cambridge University Press must be obtained for commercial re-use.
Corresponding author
*Corresponding author: School of Biology, University of Leeds, Leeds LS2 9JT, UK. E-mail: lleecruz@gmail.com
References
Hide All
Alonso-Alvarez, C. and Tella, J. L. (2001). Effects of experimental food restriction and body-mass changes on the avian T-cell mediated immune response. Canadian Journal of Zoology 79, 101105.
Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 33893402.
Anchundia, D., Huyvaert, K. P. and Anderson, D. J. (2014). Chronic lack of breeding by Galápagos blue-footed boobies and associated population decline. Avian Conservation and Ecology 9, 6.
Anderson, D.J. and Fortner, S. (1988). Waved albatross egg neglect and associated mosquito ectoparasitism. The Condor 90, 727729.
Anderson, D. J., Huyvaert, K. P., Awkerman, J. A., Proaño, C. B., Milstead, W. B., Jiménez-Uzcátegui, G., Cruz, S. and Grace, J. K. (2008). Population status of the critically endangered waved albatross (Phoebastria irrorata), 1999 to 2007. Endangered Species Research 5, 185192.
Atkinson, C. T., Woods, K. L., Dusek, R. J., Sileo, L. S. and Iko, W. M. (1995). Wildlife disease and conservation in Hawaii: pathogenicity of avian malaria (Plasmodium relictum) in experimentally infected Iiwi (Vestiaria coccinea). Parasitology 111 (Suppl.), S59S69.
Bataille, A., Cunningham, A. A., Cedeño, V., Cruz, M., Eastwood, G., Fonseca, D. M., Causton, C. E., Azuero, R., Loayza, J., Martinez, J. D. C. and Goodman, S. J. (2009). Evidence for regular ongoing introductions of mosquito disease vectors into the Galápagos Islands. Proceedings of the Royal Society of London B: Biological Sciences 276, 37693775.
Beldomenico, P. M. and Begon, M. (2010). Disease spread, susceptibility and infection intensity: vicious circles? Trends in Ecology and Evolution 25, 2127.
Bensted-Smith, R. (ed.) (2002). A Biodiversity vision for the Galapagos Islands. Charles Darwin Foundation and World Wildlife Fund, Puerto Ayora, Galapagos.
Bentz, S., Rigaud, T., Barroca, M., Martin-Laurent, F., Bru, D., Moreau, J. and Faivre, B. (2006). Sensitive measure of prevalence and parasitaemia of haemosporidia from European blackbird (Turdus merula) populations: value of PCR-RFLP and quantitative PCR. Parasitology 133, 685692.
Bermúdez-Humarán, L. G., García-García, A., Leal-Garza, C. H., Riojas-Valdes, V. M., Jaramillo-Rangel, G. and Montes-de-Oca-Luna, R. (2002). Molecular sexing of monomorphic endangered Ara birds. Journal of Experimental Zoology 292, 677680.
Booth, C. E. and Elliott, P. F. (2002). Hematological responses to hematozoa in North American and neotropical songbirds. Comparative Biochemistry and Physiology Part A: Molecular and Integrative Physiology 133, 451.
Buttarello, M. (2004). Quality specification in haematology: the automated blood cell count. Clinica Chimica Acta 346, 4554.
Campbell, T. W. (1995). Avian Hematology and Cytology. Iowa State University Press, Iowa, USA.
Davidar, P. and Morton, E. S. (1993). Living with parasites: prevalence of a blood parasites and its effect on survivorship in the purple martin. Auk 110, 109116.
de Jong, M. E., Fokkema, R. W., Ubels, R., van der Velde, M. and Tinbergen, J. M. (2014). No evidence for long-term effects of reproductive effort on parasite prevalence in tits Parus major . Journal of Avian Biology 45, 179186.
Drummond, H., Osorno, J. L., Torres, R., García-Chavelas, C. and Merchant Larios, H. (1991). Sexual size dimorphism and sibling competition: implications for avian sex ratios. American Naturalist 138, 623641.
Dunn, J. C., Goodman, S. J., Benton, T. G. and Hamer, K. C. (2013). Avian blood parasite infection during the non-breeding season: an overlooked issue in declining populations?. BMC Ecology 13, 30.
Earle, R. A., Bastianello, S. S., Bennett, G. F. and Krecek, R. C. (1992). Histopathology and morphology of the tissue stages of Haemoproteus columbae causing mortality in Columbiformes. Avian Pathology 22, 6780.
Fridolfsson, A. K. and Ellegren, H. (1999). A simple and universal method for molecular sexing of non-ratite birds. Journal of Avian Biology 30, 116121.
Garvin, M. C., Homer, B. L. and Greiner, E. C. (2003). Pathogenicity of Haemoproteus danilewskyi Kruse 1890 in blue jays (Cyanocitta cristata). Journal of Wildlife Diseases 39, 161169.
Hamer, K. C., Phillips, R. A., Wanless, S., Harris, M. P. and Wood, A. G. (2000). Foraging ranges, diets and feeding locations of gannets in the North Sea: evidence from satellite telemetry. Marine Ecology Progress Series 200, 257264.
Hellgren, O., Križanauskiene, A., Valkiūnas, G. and Bensch, S. (2007). Diversity and phylogeny of mitochondrial cytochrome B lineages from six morphospecies of avian Haemoproteus (Haemosporida: Haemoproteidae). Journal of Parasitology 93, 889896.
Ishtiaq, F., Gering, E., Rappolel, J. H., Rahmani, A. R., Jhala, Y. V., Dove, C. J., Milensky, C., Olson, S. L., Peirce, M. A. and Fleischer, R. C. (2007). Prevalence and diversity of avian hematozoan parasites in Asia: a regional survey. Journal of Wildlife Diseases 43, 382398.
Jiménez-Uzcátegui, G., Milstead, B., Márquez, C., Zabala, J., Buitrón, P., Llerena, A. and Fessl, B. (2006). Galápagos vertebrates: endangered status and conservation actions. Galápagos Report 2007, 104110.
Kilpatrick, A. M., Daszak, P., Goodman, S. J., Rogg, H., Kramer, L. D., Cedeño, V. and Cunningham, A. A. (2006). Predicting pathogen introduction: West Nile Virus spread to Galápagos. Conservation Biology 20, 12241231.
Knutie, S. A., Waite, J. L. and Clayton, D. H. (2013). Does avian malaria reduce fledging success: an experimental test of the selection hypothesis. Evolutionary Ecology 27, 185191.
Kulma, K., Low, M., Bensch, S. and Qvarnström, A. (2014). Malaria-infected female collared flycatchers (Ficedula albicollis) do not pay the cost of late breeding. PLoS ONE 9, e85822.
Levin, I. I., Outlaw, D.C., Vargas, F. H. and Parker, P. G. (2009). Plasmodium blood parasite found in endangered Galapagos penguins (Spheniscus mendiculus). Biological Conservation 142, 3191.
Levin, I. I., Valkiūnas, G., Santiago-Alarcon, D., Lee Cruz, L., Iezhova, T. A., O'Brien, S. L., Hailer, F., Dearborn, D., Schreiber, E. A., Fleischer, R. C., Ricklefs, R. E. and Parker, P. G. (2011). Hippoboscid-transmitted Haemoproteus parasites (Haemosporida) infect Galapagos Pelecaniform birds: evidence from molecular and morphological studies, with a description of Haemoproteus iwa . International Journal for Parasitology 41, 10191027.
Levin, I. I., Zwiers, P., Deem, S. L., Geest, E. A., Higashiguchi, J. M., Iezhova, T. A., Jiménez-Uzcátegui, G., Kim, D. H., Morton, J. P., Perlut, N. G., Renfrew, R. B., Sari, E. H. R., Valkiūnas, G. and Parker, P. G. (2013). Multiple lineages of avian malaria parasites (Plasmodium) in the Galápagos Islands and evidence for arrival via migratory birds. Conservation Biology 27, 13661377.
Lochmiller, R. L. and Deerenberg, C. (2000). Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88, 8798.
Marzal, A., De Lope, F., Navarro, C. and Møller, A. P. (2005). Malarial parasites decrease reproductive success: an experimental study in a passerin bird. Oecologia 142, 541545.
Marzal, A., Bensch, S., Reviriego, M., Balbontin, J. and De Lope, F. (2008). Effects of malaria double infection in birds: one plus one is not two. Journal of Evolutionary Biology 21, 979987.
Maxwell, M. H. (1993). Avian blood leucocyte responses to stress. Worlds Poultry Science J 49, 3443.
Merino, S. (2010). Immunocompetence and parasitism in nestlings from wild populations. The Open Ornithology Journal 3, 2732.
Merino, S. and Potti, J. (1995). High prevalence of hematozoa in nestlings of a passerine species, the pied flycatcher (Ficedula hypoleuca). Auk 112, 10411043.
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, 25072510.
Miller, G. D., Hofkin, B. V., Snell, H., Hahn, A. and Miller, R. D. (2001). Avian malaria and Marek's disease: potential threats to Galapagos Penguins Spheniscus mendiculus . Marine Ornithology 29, 4346.
Nelson, J. B. (1978). The Sulidae: Gannets and Boobies. Oxford University Press, Oxford, UK.
Norte, A. C., Araújo, P. M., Sampaio, H. L., Sousa, J. P. and Ramos, J. A. (2009). Haematozoa infections in a Great Tit Parus major population in Central Portugal: relationships with breeding effort and health. Ibis 151, 677688.
Ots, I. and Hõrak, P. (1998). Health impact of blood parasites in breeding great tits. Oecologia 116, 441448.
Padilla, L. R., Whiteman, N. K., Merkel, J., Huyvaert, K. P. and Parker, P. G. (2006). Health assessment of seabirds on Isla Genovesa, Galápagos Islands. Ornithological Monographs 60, 8697.
Palacios, D. M., Bograd, S. J., Foley, D. G. and Schwing, F. B. (2006). Oceanographic characteristics of biological hot spots in the North Pacific: a remote sensing perspective. Deep Sea Research Part II: Topical Studies in Oceanography 53, 250269.
Parejo, D., Silva, N. and Avilés, J. M. (2007). Within-brood size differences affect innate and acquired immunity in roller Coracias garrulus nestlings. Journal of Avian Biology 38, 717725.
Parker, P. G., Whiteman, N. K. and Miller, R. E. (2006). Conservation Medicine on the Galápagos Islands: partnerships among behavioral, population, and veterinary scientist. Auk 123, 625638.
R Development Core Team (2008). R: A Language, Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
Ricklefs, R. E. (1992). Embryonic development period and the prevalence of avian blood parasites. Proceedings of the National Academy of Sciences of the United States of America 89, 47224725.
Ricklefs, R. E., Duffy, D. C. and Coulter, M. (1984). Weight gain of blue-footed booby chicks: an indicator of marine resources. Ornis Scandinavica 15, 162.
Santiago-Alarcon, D., Outlaw, D. C., Ricklefs, R. E. and Parker, P. G. (2010). Phylogenetic relationships of haemosporidian parasites in New World Columbiformes, with emphasis on the endemic Galapagos dove. International Journal for Parasitology 40, 463470.
Sheldon, B. C. and Verhulst, S. V. (1996). Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology and Evolutionl 11, 317321.
Soler, J. J., Neve, L. D., Pérez Contreras, T., Soler, M. and Sorci, G. (2003). Trade-off between immunocompetence and growth in magpies: an experimental study. Proceedings of the Royal Society of Londond B: Biological Sciences 270, 241248.
Steadman, D. W. (2006). Extinction and Biogeography in Tropical Pacific Birds. University of Chicago Press, Chicago, Illinois, USA.
Štefka, J., Hoeck, P. E. A., Keller, L. F. and Smith, V. S. (2011). A hitchhikers guide to the Galápagos: co-phylogeography of Galápagos mockingbirds and their parasites. BMC Evolutionary Biology 11, 284.
Taylor, J. E., Hardner, J. and Stewart, M. (2009). Ecotourism and economic growth in the Galapagos: an island economy-wide analysis. Environment and Development Economics 14, 139162.
Taylor, S. A., Maclagan, L., Anderson, D. J. and Friesen, V. L. (2011). Could specialization to cold-water upwelling systems influence gene flow and population differentiation in marine organisms? A case study using the blue-footed booby, Sula nebouxii . Journal of Biogeography 38, 883893.
Tomás, G., Merino, S., Moreno, J., Morales, J. and Martínez-de la Puente, J. (2007). Impact of blood parasites on immunoglobulin level and parental effort: a medication field experiment on a wild passerine. Functional Ecology 21, 125133.
Valkiūnas, G. (2005). Avian Malaria Parasites and other Haemosporidia. CRC Press, Boca Raton, Florida, USA.
Valkiūnas, G., Bairlein, F., Iezhova, T. A. and Dolnik, O. V. (2004). Factors affecting the relapse of Haemoproteus belopolskyi infections and the parasitaemia of Trypanosoma spp. in a naturally infected European songbird, the blackcap, Sylvia atricapilla . Parasitology Research 93, 218222.
Valkiūnas, G., Santiago-Alarcon, D., Levin, I. I., Iezhova, T. A. and Parker, P. G. (2010). A new Haemoproteus species (Haemosporida: Haemoproteidae) from the endemic Galapagos dove Zenaida galapagoensis, with remarks on the parasite distribution, vectors, and molecular diagnostics. Journal of Parasitology 96, 783792.
Valkiūnas, G., Palinauskas, V., Ilgūnas, M., Bukauskaité, D., Dimitrov, D., Bernotiené, R., Zehtindjiev, P., Ilieva, M. and Iezhova, T. (2014). Molecular characterization of five widespread avian haemosporidian parasites (Haemosporida), with perspectives on the PCR-based detection of haemosporidians in wildlife. Parasitology Research 113, 22512263.
Vargas, H., Lougheed, C. and Snell, H. (2005). Population size and trends of the Galápagos Penguin (Spheniscus mendiculus). Ibis 147, 367374.
Velando, A. (2002). Experimental manipulation of maternal effort produces differential effects in sons and daughters: implications for adaptive sex ratios in the blue-footed booby. Behavioral Ecology 13, 443449.
Waldenström, J., Bensch, S., Hasselquist, D. and Östman, Ö. (2004). A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. Journal of Parasitology 90, 191194.
Wikelski, M., Foufopoulos, J., Vargas, H. and Snell, H. (2004). Galápagos birds and diseases: invasive pathogens as threats for island species. Ecology and Society 9 (issue 1, art. 5) www.ecologyandsociety.org/vol9/iss1/art5.
Zylberberg, M., Derryberry, E. P., Breuner, C. W., Macdougall-Shackleton, E. A. and Hahn, T. P. (2015). Haemoproteus infected birds have increased lifetime reproductive success. Parasitology 142, 10331043.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Parasitology Open
  • ISSN: -
  • EISSN: 2055-7094
  • URL: /core/journals/parasitology-open
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed