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Absence of haemosporidian parasite infections in the long-lived Cory’s shearwater: evidence from molecular analyses and review of the literature


The apparent scarcity or absence of blood parasites in some avian groups, such as seabirds, has been related to intrinsic and extrinsic factors including host immunological capacity, host-parasite assemblage, and ecological parameters, but also to reduced sensitivity of some methods to detect low parasite prevalence/intensities of infection. Here, we examined the haemosporidian parasite prevalence in a breeding population of Cory’s shearwater Calonectris diomedea borealis, a long-distance migrant seabird, nesting in the Macaronesian region, in the Eastern Atlantic. Previous studies on Calonectris diomedea complex were based on small sample sizes providing weak evidence for a lack of infections by haemoparasites. Here, we investigated the presence of both parasite infections in C. d. borealis and larvae of potential mosquito vectors on the area. By employing a PCR-based assay, we extensively examined the prevalence of blood parasites belonging to the genera Plasmodium, Haemoproteus, and Leucocytozoon in 286 individuals from different life stages (i.e., chicks, immatures, sabbatical, and breeding adults), facing their specific energetic trade-offs (immunological functions vs. life history activities). We sampled immatures and adult shearwaters, of different sexes, ages, and migratory origins, from two sub-colonies. None of the sampled individuals were infected by these parasites, supporting the hypothesis that there was no in situ or ex situ transmission of vector-borne parasites in marine habitats irrespective of host’s life stage and in spite of the presence of the potential Plasmodium vector Culiseta longiareolata breeding in the area. These results suggest that the lack of transmission of haemosporidian parasites on Selvagem Grande may be related to the lack of suitable dipteran vectors at the study sites, which may result from the geographic isolation of this area.

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  1. Bensch S, Hellgren O, Pérez-Tris J (2009) MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Mol Ecol Resour 9:1353–1358.

  2. Bensch S, Stjernman M, Hasselquist D, Ostman O, Hansson B, Westerdahl H, Pinheiro RT (2000) Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proc R Soc London Ser Biol Sci 267:1583–1589.

  3. Bernotienė R, Palinauskas V, Iezhova T, Murauskaitė D, Valkiūnas G (2016) Avian haemosporidian parasites (Haemosporida): a comparative analysis of different polymerase chain reaction assays in detection of mixed infections. Exp Parasitol 163:31–37.

  4. Campioni L, Granadeiro JP, Catry P (2016) Niche segregation between immature and adult seabirds: does progressive maturation play a role? Behav Ecol 27:426–433.

  5. Dias M, Granadeiro JP, Phillips RA, Alonso H, Catry P (2011) Breaking the routine: individual Cory’s shearwaters shift winter destinations between hemispheres and across ocean basins. Proc R Soc London Ser B Biol Sci 278:1786–1793.

  6. Feldman RA, Freed LA (1995) A PCR test for avian malaria in Hawaiian birds. Mol Ecol 4:663–673

  7. Ferraguti M, Martínez-de la Puente J, Muñoz J, Roiz D, Ruiz S, Soriguer R, Figuerola J (2013) Avian Plasmodium in Culex and Ochlerotatus mosquitoes from southern Spain: effects of season and host-feeding source on parasite dynamics. PLoS One 8(6):e66237.

  8. Forero M, González-Solis J, Igual JM, Hobson K, Ruíz X, Viscor G (2006) Ecological and physiological variance in T-cell mediated immune response in Cory’s shearwaters. Condor 108:865–876.;2

  9. Fredeen FJ, Mason PG (1991) Meteorological factors influencing host-seeking activity of female Simulium luggeri (Diptera: Simuliidae). J Med Entomol 28:831–840

  10. Figuerola J (1999) Effects of salinity on rates of infestation of waterbirds by haematozoa. Ecography 22:681–685.

  11. Gemmell NJ, Akiyama S (1996) An efficient method for the extraction of DNA from vertebrate tissues. Trends Genet 12(9):338.

  12. Gomez-Diaz E, Doherty PF Jr, Duneau D, McCoy KD (2010) Cryptic vector divergence masks vector-specific patterns of infection: an example from the marine cycle of Lyme borreliosis. Evol Appl 3:391–401.

  13. González-Solís J, Abella JC (1997) Negative record of haematozoan parasites on Cory’s shearwater Calonectris diomedea. Orn Fenn 74:153–155

  14. González-Solís J, Croxall J, Oro D, Ruiz X (2007) Trans-equatorial migration and mixing in the wintering areas of a pelagic seabird. Front Ecol Environ 5:297–301.;2

  15. Granadeiro JP (1991) The breeding biology of Cory’s shearwater Calonectris diomedea borealis on Berlenga Island, Portugal. Seabird 13:30–39

  16. Granadeiro JP, Dias MP, Rebelo R, Santos CD, Catry P (2006) Numbers and population trends of Cory's shearwaters Calonectris diomedea at Selvagem Grande, Northeast Atlantic. Waterbirds 29:56–60.;2

  17. Griffiths R, Double M, Orr K, Dawson R (1998) A simple DNA test to sex most birds. Mol Ecol 7:1071–1076.

  18. Gutiérrez-López R, Gangoso L, Martínez-de la Puente J, Fric J, López-López P, Mailleux M, Muñoz J, Touati L, Samraoui B, Figuerola J (2015) Low prevalence of blood parasites in a long-distance migratory raptor: the importance of host habitat. Parasit Vectors 8:189.

  19. Gutiérrez-López R, Martínez-de la Puente J, Gangoso L, Yan J, Soriguer RC, Figuerola J (2016) Do mosquitoes transmit the avian malaria-like parasite Haemoproteus? An experimental test of vector competence using mosquito saliva. Parasit Vectors 28:609.

  20. Hellgren O, Waldenström J, Bensch S (2004) A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. J Parasitol 90:797–802.

  21. Hervías S, Ramos JA, Nogales M, Ruiz de Ybáñez R (2013) Effect of exotic mammalian predators on parasites of Cory’s shearwater: ecological effect on population health and breeding success. Parasitol Res 112:2721–2730.

  22. Illera JC, Emerson BC, Richardson DS (2008) Genetic characterization, distribution and prevalence of avian pox and avian malaria in the Berthelot’s pipit (Anthus berthelotii) in Macaronesia. Parasitol Res 103:1435–1443.

  23. Jarvi SI, Schultz JJ, Atkinson CT (2002) PCR diagnostics underestimate the prevalence of avian malaria (Plasmodium relictum) in experimentally-infected passerines. J Parasitol 88:153–158.;2

  24. Jovani R, Tella JL (2006) Parasite prevalence and sample size: misconceptions and solutions. Trends Parasitol 22:214–218.

  25. Jovani R, Tella JL, Forero MG, Bertellotti M, Blanco G, Ceballos O, Donázar J (2001) Apparent absence of blood parasites in the Patagonian seabird community: is it related to the marine environment? Waterbirds 24:430–433

  26. Lobato E, Merino S, Morales J, Tomás G, Martínez-de la Puente J, Sánchez E, García-Fraile S, Moreno J (2008) Sex differences in circulating antibodies in nestling pied flycatchers Ficedula hypoleuca. Ibis 150:799–806.

  27. Martin FR, McCreadie JW, Colbo MH (1994) Effect of trap site, time of day, and meteorological factors on abundance of host-seeking mammalophilic black flies (Diptera: Simuliidae). Can Entomol 126:283–289.

  28. Martínez J, Martínez-de la Puente J, Herrero J, Del Cerro S, Lobato E, Rivero-de Aguilar J, Vásquez RA, 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.

  29. Martínez-Abrain A, Esparza B, Oro D (2004) Lack of blood parasites in bird species: does absence of blood parasite vectors explain it all? Ardeola 5:225–232

  30. Martínez-de la Puente J, Merino S, Lobato E, Rivero-de Aguilar J, Del Cerro S, Ruiz-de-Castañeda R, Moreno J (2009) Does weather affect biting fly abundance in avian nests? J Avian Biol 40:653–657.

  31. Martínez-de la Puente J, Merino S, Tomás G, Moreno J, Morales J, Lobato E, García-Fraile S, Belda EJ (2010) The blood parasite Haemoproteus reduces survival in a wild bird: a medication experiment. Biol Lett 6:663–665.

  32. Merino S, Moreno J, Sanz JJ, Arriero E (2000) Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus). Proc Roy Soc London Ser B Biol Sci 267:2507–2510.

  33. Merino S, Moreno J, Vásquez RA, Martínez J, Sánchez-Monsálvez I, Estades CF, Ippi S, Sabat P, Rozzi R, McGehee S (2008) Haematozoa in forest birds from southern Chile: latitudinal gradients in prevalence and parasite lineage richness. Austral Ecol 33:329–340.

  34. Mougin JL, Jouanin C, Roux F (2000) Démographie du puffin cendré Calonectris diomedea de Selvagem Grande. Rev Ecol Terre Vie 55:275–290

  35. Peirce MA (1981a) Distribution and host-parasite check-list of the haematozoa of birds in Western Europe. J Nat Hist 15:419–458.

  36. Peirce MA (1981b) Haematozoa of British birds. VI Redescription of Haemoproteus larae Yakunin from the lesser black-backed gull Larus fuscus. J Nat Hist 15:459–462.

  37. Perkins SL, Schall JJ (2002) A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. J Parasitol 88:978.;2

  38. Piersma T (1997) Do global patterns of habitat use and migration strategies co-evolve with relative investments in immunocompetence due to spatial variation in parasite pressure? Oikos 80:623–631.

  39. Quillfeldt P, Arriero E, Martínez J, Masello JF, Merino S (2011) Prevalence of blood parasites in seabirds—a review. Front Zool 8:26.

  40. Quillfeldt P, Martínez J, Bugoni L, Mancini PL, Merino S (2014) Blood parasites in noddies and boobies from Brazilian offshore islands—differences between species and influence of nesting habitat. Parasitology 141:399–410.

  41. Quillfeldt P, Martínez J, Hennicke J, Ludynia K, Gladbach A, Masello JF, Riou S, Merino S (2010) Hemosporidian blood parasites in seabirds—a comparative genetic study of species from Antarctic to tropical habitats. Naturwissenschaften 97:809–817.

  42. Ricklefs RE, Swanson BL, Fallon SM, Martinez-Abrain A, Scheuerlein A, Gray J, Latta SC (2005) Community relationships of avian malaria parasites in southern Missouri. Ecol Monogr 75:543–559.

  43. Ruiz X, Oro D, González-Solís J (1995) Incidence of a Haemoproteus lari parasitemia in a threatened Mediterranean gull: Larus audouinii. Orn Fenn 72:159–164

  44. Sangster G, Collinson JM, Crochet PA, Knox AG, Parkin DT, Votier SC (2012) Taxonomic recommendations for British birds: eighth report. Ibis 154:874–883.

  45. Santiago-Alarcon D, Havelka P, Schaefer HM, Segelbacher G (2012) Bloodmeal analysis reveals avian plasmodium infections and broad host preferences of Culicoides (Diptera: Ceratopogonidae) vectors. PLoS One 7(2):e31098.

  46. Scheuerlein A, Ricklefs RE (2004) Prevalence of blood parasites in European passeriform birds. Proc Roy Soc London Ser B Biol Sci 271:1363–1370.

  47. Sol D, Jovani R, Torres J (2000) Geographical variation in blood parasites in feral pigeons: the role of vectors. Ecography 23:307–314.

  48. Spurgin LG, Illera JC, Padilla DP, Richardson DS (2011) Biogeographical patterns and co-occurrence of pathogenic infection across island populations of Berthelot’s pipit (Anthus berthelotii). Oecologia 168:691–701.

  49. Super PE, van Riper IIIC (1995) A comparison of avian hematozoan epizootiology in two California coastal scrub communities. J Wildl Dis 31:447–461

  50. Valkiūnas G (2005) Avian malaria parasites and other haemosporidia. CRC Press, Boca Raton

  51. Valkiūnas G, Ilgūnas M, Bukauskaitė D, Iezhova TA (2016) Description of Haemoproteus ciconiae sp. nov. (Haemoproteidae, Haemosporida) from the white stork Ciconia ciconia, with remarks on insensitivity of established polymerase chain reaction assays to detect this infection. Parasitol Res 115:2609–2616.

  52. Wink M, Wink C, Ristow D (1979) Parasitenbefall juveniler und adulter Gelbschnabelsturmtaucher (Calonectris diomedea). Bonn Zool Beitr 30:217–219

  53. Zino PA, Zino F, Maul T, Biscoito JM (1987) The laying, incubation and fledging periods of Cory’s shearwater Calonectris diomedea borealis on Selvagem Grande in 1984. Ibis 129:393–398.

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Thanks to R. Furtado, C. Mateus, and B. Reis for their help in the fieldwork and to I. Martin and L. Gomez for their help in the laboratory. We are grateful to Bill Chobotar and one anonymous referee for their valuable suggestions which improved this manuscript. We are also grateful to Y. M. Gonçalves from Museu de História Natural do Funchal for the identification of the mosquito larvae. Instituto das Florestas e da Conservação da Natureza, particularly P. Oliveira, D. Menezes, and C.S. Jardim, made fieldwork on the Selvagens possible.


This study was supported by Fundação para a Ciência e a Tecnologia (FCT) through the grant awarded to L.C. (FCT-SFRH/BPD/89904/2012) and Grant CGL2015-65055-P from the Spanish Ministerio de Economia y Competitividad and European Regional Developments funds (FEDER) to JF. JMP was partially supported by a 2017 Leonardo Grant for Researchers and Cultural Creators, BBVA Foundation. The Foundation accepts no responsibility for the opinions, statements, and contents included in the project and/or the results thereof, which are entirely the responsibility of the authors. MCS was supported by the post-doctoral research fellowship FCT-SFRH/BPD/85700/2012. Moreover, Fundação para a Ciência e a Tecnologia (FCT Portugal) provided financial support through the strategic project UID/MAR/04292/2013 granted to MARE and the projects IF/00502/2013/CP1186/CT0003 and PTDC/BIA-ANM/3743/2014, UID/AMB/50017 to CESAM (with co-funding by FEDER, within the PT2020 Partnership Agreement and Compete 2020) and PTDC/MAR-PRO/0929/2014.

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Correspondence to Letizia Campioni.

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All work was approved by the relevant authorities: Instituto da Conservação da Natureza e da Biodiversidade and Serviço do Parque Natural da Madeira (annual research permit including animal manipulation and ringing: number 5/2014S).

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Campioni, L., Martínez-de la Puente, J., Figuerola, J. et al. Absence of haemosporidian parasite infections in the long-lived Cory’s shearwater: evidence from molecular analyses and review of the literature. Parasitol Res 117, 323–329 (2018).

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  • Avian malaria parasites
  • Insect vectors
  • Procellariiformes
  • Remote island
  • Seabirds