Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-23T03:21:34.979Z Has data issue: false hasContentIssue false
  • English
  • Français

Contrasting haemoparasite prevalence in larid species with divergent ecological niches and migration patterns

Published online by Cambridge University Press:  30 June 2022

Radosław Włodarczyk Open the ORCID record for Radosław Włodarczyk [Opens in a new window] ,
Sandra Bouwhuis ,
Coraline Bichet ,
Patrycja Podlaszczuk ,
Amelia Chyb ,
Piotr Indykiewicz ,
Beata Dulisz ,
Jacek Betleja ,
Tomasz Janiszewski  and
Piotr Minias
Radosław Włodarczyk*
Affiliation:
Department of Biodiversity Studies and Bioeducation, Faculty of Biology and Environmental Protection, University of Łódź, Banacha 1/3, 90-237 Łódź, Poland
Sandra Bouwhuis
Affiliation:
Institute of Avian Research, Wilhelmshaven, Germany
Coraline Bichet
Affiliation:
Centre d'Etudes Biologiques de Chizé, UMR 7372, CNRS-La Rochelle Université, Villiers-en-Bois, France
Patrycja Podlaszczuk
Affiliation:
Department of Biodiversity Studies and Bioeducation, Faculty of Biology and Environmental Protection, University of Łódź, Banacha 1/3, 90-237 Łódź, Poland
Amelia Chyb
Affiliation:
Department of Biodiversity Studies and Bioeducation, Faculty of Biology and Environmental Protection, University of Łódź, Banacha 1/3, 90-237 Łódź, Poland
Piotr Indykiewicz
Affiliation:
Department of Biology and Animal Environment, Faculty of Animal Breeding and Biology, Bydgoszcz University of Science and Technology, Mazowiecka 28, 85-084 Bydgoszcz, Poland
Beata Dulisz
Affiliation:
Department of Ecology and Environmental Protection, Faculty of Biology and Biotechnology, University of Warmia and Mazury in Olsztyn, Plac Łódzki 3, 10-727 Olsztyn, Poland
Jacek Betleja
Affiliation:
Department of Natural History, Upper Silesian Museum, Plac Jana III Sobieskiego 2, 41-902 Bytom, Poland
Tomasz Janiszewski
Affiliation:
Department of Biodiversity Studies and Bioeducation, Faculty of Biology and Environmental Protection, University of Łódź, Banacha 1/3, 90-237 Łódź, Poland
Piotr Minias
Affiliation:
Department of Biodiversity Studies and Bioeducation, Faculty of Biology and Environmental Protection, University of Łódź, Banacha 1/3, 90-237 Łódź, Poland
*
Author for correspondence: Radosław Włodarczyk, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Haemoparasites represent a diverse group of vector-borne parasites that infect a wide range of vertebrate hosts. In birds, haemoparasite infection rates may be associated with various ecological and life history traits, including habitat choice, colony size and migration distance. Here, we molecularly assessed the prevalence of 3 main haemoparasite genera (Plasmodium, Haemoproteus and Leucocytozoon) in 2 bird species with different habitat preferences and migratory behaviour: black-headed gulls (Chroicocephalus ridibundus) and common terns (Sterna hirundo). We found that gulls showed a much higher prevalence and diversity of Plasmodium or Haemoproteus (ca. 60% of individuals infected) than terns (zero prevalence). The prevalence of Leucocytozoon was low in both species (<3%). The differences in haemoparasite prevalences may be primarily driven by varying vector encounter rate resulting from different habitat preferences, as black-headed gulls mainly use vector-rich vegetated freshwater habitats, whereas common terns often use vector-poor coastal and brackish habitats. Since common terns migrate further than black-headed gulls, our results did not provide support for an association between haemoparasite prevalence and migratory distance. In gulls, we found a negative association between colony size and infection rates, suggestive of an ideal despotic distribution, and phylogenetic analyses of detected haemoparasite lineages provided evidence for higher host specificity in Haemoproteus than Plasmodium. Our results suggest that the preference for coastal areas and less vegetated habitats in terns may reduce haemoparasite infection rates compared to other larids, regardless of their migratory distance, emphasizing the role of ecological niches in parasite exposure.

Keywords

Avian malariabird migrationcomparative analyseshaemosporidiansLaridaemolecular diversity
Type
Research Article
Information
Parasitology , Volume 149 , Issue 11 , September 2022 , pp. 1479 - 1486
Check for updates
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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

Alerstam, T, Hedenström, A and Åkesson, S (2003) Long-distance migration: evolution and determinants. Oikos 103, 247–260.CrossRefGoogle Scholar
Apanius, V, Yorinks, N, Bermingham, E and Ricklefs, RE (2000) Island and taxon effects in parasitism and resistance of Lesser Antillean birds. Ecology 81, 1959–1969.CrossRefGoogle Scholar
Atkinson, CT and van Riper, C III (1991) Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. In Loye, J and Zuk, M (eds), Bird-Parasite Interactions. Oxford, UK: Oxford University Press, pp. 19–48.Google Scholar
Beadell, JS, Gering, E, Austin, J, Dumbacher, JP, Peirce, M, Pratt, TK, Atkinson, CT and Fleischer, RC (2004) Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region. Molecular Ecology 13, 3829–3844.CrossRefGoogle ScholarPubMed
Becker, PH, Voigt, CC, Arnold, JM and Nagel, R (2006) A non-invasive technique to bleed incubating birds without trapping: a blood-sucking bug in a hollow egg. Journal of Ornithology 147, 115–118.CrossRefGoogle Scholar
Bensch, S, Stjerman, M, Hasselquist, D, Östman, Ö, Hansson, B, Westerdahl, H and Pinheiro, RT (2000) Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proceedings of the Royal Society, London Series B: Biological Sciences 267, 1583–1589.CrossRefGoogle ScholarPubMed
Bensch, S, Hellgren, O and Pérez-Tris, J (2009) MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Molecular Ecology Resources 9, 1353–1358.CrossRefGoogle ScholarPubMed
BirdLife International (2021) IUCN Red List for birds. Available at http://www.birdlife.org (Accessed 25 October 2021).Google Scholar
Bosch, M, Figuerola, J, Cantos, FJ and Velarde, R (1997) Intracolonial differences in the infestation by Haemoproteus lari on yellow-legged gulls Larus cachinnans. Ornis Fennica 74, 105–112.Google Scholar
Brown, CR (2016) The ecology and evolution of colony-size variation. Behavioral Ecology and Sociobiology 70, 1613–1632.CrossRefGoogle Scholar
Christmas, SE, Christmas, TJ, Gosling, AP and Parr, AJ (1986) Feeding behaviour and geographical origins of black-headed gulls Larus ridibundus wintering in Central London. Ringing & Migration 7, 1–6.CrossRefGoogle Scholar
Coatney, GR (1938) Some blood parasites from birds of the Lake Okaboji region. American Midland Naturalist 20, 336–340.CrossRefGoogle Scholar
Cosgrove, CL, Wood, MJ, Day, KP and Sheldon, BC (2008) Seasonal variation in Plasmodium prevalence in a population of blue tits Cyanistes caeruleus. Journal of Animal Ecology 77, 540–548.CrossRefGoogle Scholar
Cramp, S and Simmons, KEL (1983) The Birds of the Western Palearctic, Vol. III. Waders to Gulls. Oxford, UK: Oxford University Press.Google Scholar
Dimitrov, D, Zehtindjiev, P and Bensch, S (2010) Genetic diversity of avian blood parasites in SE Europe: cytochrome b lineages of the genera Plasmodium and Haemoproteus (Haemosporida) from Bulgaria. Acta Parasitologica 55, 201–209.CrossRefGoogle Scholar
Drzewińska-Chańko, J, Włodarczyk, R, Gajewski, A, Rudnicka, K, Dunn, PO and Minias, P (2021) Immunocompetent birds choose larger breeding colonies. Journal of Animal Ecology 90, 2325–2335.CrossRefGoogle ScholarPubMed
Dunn, JC, Stockdale, JE, Bradford, EL, McCubbin, A, Morris, AJ, Grice, PV, Goodman, SJ and Hamer, KC (2017) High rates of infection by blood parasites during the nestling phase in UK Columbids with notes on ecological associations. Parasitology 144, 622–628.CrossRefGoogle ScholarPubMed
Fecchio, A, Clark, NJ, Bell, JA, Skeen, HR, Lutz, HL, De La Torre, GM, Vaughan, JA, Tkach, VV, Schunck, F, Ferreira, FC, Braga, ÉM, Lugarini, C, Wamiti, W, Dispoto, JH, Galen, SC, Kirchgatter, K, Sagario, MC, Cueto, VR, González-Acuña, D, Inumaru, M, Sato, Y, Schumm, YR, Quillfeldt, P, Pellegrino, I, Dharmarajan, G, Gupta, P, Robin, VV, Ciloglu, A, Yildirim, A, Huang, X, Chapa-Vargas, L, Álvarez-Mendizábal, P, Santiago-Alarcon, D, Drovetski, SV, Hellgren, O, Voelker, G, Ricklefs, RE, Hackett, SJ, Collins, MD, Weckstein, JD and Wells, K (2021) Global drivers of avian haemosporidian infections vary across zoogeographical regions. Global Ecology and Biogeography 30, 2393–2406.CrossRefGoogle Scholar
Fretwell, SD (1972) Populations in Seasonal Environments. Princeton, NJ: Princeton University Press.Google Scholar
Garcia-Longoria, L, Marzal, A, de Lope, F and Garamszegi, L (2019) Host-parasite interaction explains variation in the prevalence of avian haemosporidians at the community level. PLoS ONE 14, e0205624.CrossRefGoogle ScholarPubMed
Groff, TC, Lorenz, TJ, Iezhova, TA, Valkiūnas, G and Sehgal, RN (2022) Description and molecular characterization of novel Leucocytozoon parasite (Apicomplexa: Haemosporida: Leucocytozoidae), Leucocytozoon polynuclearis n. sp. found in North American woodpeckers. Systematic Parasitology 99, 103–114.CrossRefGoogle Scholar
Gutiérrez-López, R, Gangoso, L, Martínez-de la Puente, J, Fric, J, López-López, P, Mailleux, M, Muñoz, J, Touati, L, Samraoui, B and Figuerola, J (2015) Low prevalence of blood parasites in a long-distance migratory raptor: the importance of host habitat. Parasites & Vectors 8, 189.CrossRefGoogle Scholar
Hellgren, O, Waldenström, J and Bensch, S (2004) A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. Journal of Parasitology 90, 797–802.CrossRefGoogle ScholarPubMed
Huelsenbeck, JP and Ronquist, F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.CrossRefGoogle ScholarPubMed
Ilahiane, L, De Pascalis, F, Pisu, D, Pala, D, Ferrario, F, Cucco, M, Rubolini, D, Cecere, JG and Pellegrino, I (2022) No evidence of avian malaria in two Mediterranean endemic seabirds. Marine Ornithology 50, 13–17.Google Scholar
Indykiewicz, P, Podlaszczuk, P, Kamiński, M, Włodarczyk, R and Minias, P (2019) Central–periphery gradient of individual quality within a colony of black-headed gulls. Ibis 161, 744–758.CrossRefGoogle Scholar
Jelínek, M (2008) Common black-headed gull, Larus ridibundus. In Cepák, J, Klvaňa, P, Formánek, J, Horák, D, Jelínek, M, Schröpfer, L, Škopek, J and Zárybnický, J (eds), Czech and Slovak Bird Migration Atlas. Praha: Aventinum, pp. 217–221.Google Scholar
Jenkins, T, Gavin, H, Thomas, GH, Hellgren, O and Owens, IPF (2012) Migratory behaviour of birds affects their coevolutionary relationship with blood parasites. Evolution 66, 740–751.CrossRefGoogle ScholarPubMed
Jungwirth, A, Josi, D, Walker, J and Taborsky, M (2015) Benefits of coloniality: communal defence saves anti-predator effort in cooperative breeders. Functional Ecology 29, 1218–1224.CrossRefGoogle Scholar
Kairullaev, KK (1986) Blood parasites (Haemoproteus Kruse, 1890) in birds of Kazakh-SSR, USSR. Izvestiya Akademii Nauk Kazakhskoi SSR, Seriya Biologicheskikh Nauk, 39–42.Google Scholar
Knowles, SCL, Nakagawa, S and Sheldon, B (2009) Elevated reproductive effort increases blood parasitaemia and decreases immune function in birds: a meta-regression approach. Functional Ecology 23, 405–415.CrossRefGoogle Scholar
Knowles, SC, Palinauskas, V and Sheldon, BC (2010) Chronic malaria infections increase family inequalities and reduce parental fitness: experimental evidence from a wild bird population. Journal of Evolutionary Biology 23, 557–569.CrossRefGoogle ScholarPubMed
Kram, I, Kram, S, Suraka, V, Rattiste, K, Ābolins-Ābols, M, Krama, T, Rantala, MJ, Mierauskas, P, Cırule, D and Saks, L (2012) Comparative analysis reveals a possible immunity-related absence of blood parasites in common gulls (Larus canus) and black-headed gulls (Chroicocephalus ridibundus). Journal of Ornithology 153, 1245–1252.CrossRefGoogle Scholar
Krause, J and Ruxton, GD (2002) Living in Groups. Oxford, UK: Oxford University Press.Google Scholar
Kürten, N, Schmaljohann, H, Bichet, C, Haest, B, Vedder, O, González-Solís, J and Bouwhuis, S (2022) High individual repeatability of the migratory behaviour of a long-distance migratory seabird. Movement Ecology 10, 5.CrossRefGoogle ScholarPubMed
Levin, II, Valkiūnas, G, Iezhova, TA, O'Brien, SL and Parker, PG (2012) Novel Haemoproteus species (Haemosporida: Haemoproteidae) from the swallow-tailed gull (Lariidae), with remarks on the host range of hippoboscid-transmitted avian hemoproteids. Journal of Parasitology 98, 847–854.CrossRefGoogle ScholarPubMed
Lotta, AL, Pacheco, MA, Escalante, AA, Gonzalez, AD, Mantilla, JS, Moncada, LI, Adler, PH and Matta, NE (2016) Leucocytozoon diversity and possible vectors in the neotropical highlands of Colombia. Protist 167, 185–204.CrossRefGoogle ScholarPubMed
Loye, JE and Zuk, M (1991) Bird-Parasite Interactions: Ecology, Evolution and Behaviour. Oxford, NY: Oxford University Press, Ornithology Series 2.Google Scholar
Martinez-Abraín, A, Esparza, B and Oro, D (2004) Lack of blood parasites in bird species: does absence of blood parasite vectors explain it all? Ardeola 51, 225–232.Google Scholar
Marzal, A, de Lope, F, Navarro, C and Møller, AP (2005) Malarial parasites decrease reproductive success: an experimental study in a passerine bird. Oecologia 142, 541–545.CrossRefGoogle Scholar
Mendes, L, Piersma, T, Lecoq, M, Spaans, B and Ricklefs, RE (2005) Disease-limited distributions? Contrasts in the prevalence of avian malaria in shorebird species using marine and freshwater habitats. Oikos 109, 396–404.CrossRefGoogle Scholar
Merino, S, Hennicke, J, Martínez, J, Ludynia, K, Torres, R, Work, TM, Stroud, S, Masello, JF and Quillfeldt, P (2012) Infection by Haemoproteus parasites in four species of frigatebirds and the description of a new species of Haemoproteus (Haemosporida: Haemoproteidae). Journal of Parasitology 98, 388–397.CrossRefGoogle ScholarPubMed
Minias, P (2014) Evolution of within-colony distribution patterns of birds in response to habitat structure. Behavioral Ecology & Sociobiology 68, 851–859.CrossRefGoogle ScholarPubMed
Møller, AP, Garamszegi, LZ, Peralta-Sánchez, JM and Soler, JJ (2011) Migratory divides and their consequences for dispersal, population size and parasite–host interactions. Journal of Evolutionary Biology 24, 1744–1755.CrossRefGoogle ScholarPubMed
Murdock, CC, Foufopoulos, J and Simon, CP (2013) A transmission model for the ecology of an avian blood parasite in a temperate ecosystem. PLoS ONE 8, e76126.CrossRefGoogle Scholar
Oro, D (2008) Living in a ghetto within a local population: an empirical example of an ideal despotic distribution. Ecology 89, 838–846.CrossRefGoogle Scholar
Palinauskas, V, Kosarev, V, Shapoval, A, Bensch, S and Valkinas, G (2007) Comparison of mitochondrial cytochrome b lineages and morphospecies of two avian malaria parasites of the subgenera Haemamoeba and Giovannolaia (Haemosporida: Plasmodiidae). Zootaxa 1626, 39–50.CrossRefGoogle Scholar
Pérez-Tris, J and Bensch, S (2005) Dispersal increases local transmission of avian malarial parasites. Ecology Letters 8, 838–845.CrossRefGoogle Scholar
Quillfeldt, P, Arriero, E, Martínez, J, Masello, JF and Merino, S (2011) Prevalence of blood parasites in seabirds – a review. Frontiers in Zoology 8, 26.CrossRefGoogle ScholarPubMed
Ricklefs, RE and Fallon, SM (2002) Diversification and host switching in avian malaria parasites. Proceedings of the Royal Society, London Series B: Biological Sciences 269, 885–892.CrossRefGoogle ScholarPubMed
Ricklefs, RE, Fallon, SM and Bermingham, E (2004) Evolutionary relationships, cospeciation, and host switching in avian malaria parasites. Systematic Biology 53, 111–119.CrossRefGoogle ScholarPubMed
Ricklefs, RE, Fallon, SM, Latta, SC, Swansson, BL and Bermingham, E (2005) Migrants and their parasites: a bridge between two worlds. In Greenberg, R and Marrra, PP (eds), Birds of Two Worlds: The Ecology and Evolution of Migration. Baltimore and London: John Hopkins University Press, pp. 201–221.Google Scholar
Ricklefs, RE, Medeiros, M, Ellis, VA, Svensson-Coelho, M, Blake, JG, Loiselle, BA, Soares, L, Fecchio, A, Outlaw, D, Marra, PP, Latta, SC, Valkiūnas, G, Hellgren, O and Bensch, S (2016) Avian migration and the distribution of malaria parasites in New World passerine birds. Journal of Biogeography 44, 1113–1123.CrossRefGoogle Scholar
Rivero, A and Gandon, S (2018) Evolutionary ecology of avian malaria: past to present. Trends in Parasitology 34, 712–726.CrossRefGoogle ScholarPubMed
Ruiz, X, Oro, D and Gonzales-Solis, J (1995) Incidence of a Haemoproteus lari parasitemia in a threatened gull Larus audouinii. Ornis Fennica 72, 159–164.Google Scholar
Santiago-Alarcon, D, Palinauskas, V and Schaefer, HM (2012) Diptera vectors of avian haemosporidian parasites: untangling parasite life cycles and their taxonomy. Biological Reviews 87, 928–964.CrossRefGoogle ScholarPubMed
Santolíková, A, Brzonová, J, Čepička, I and Svobodová, M (2022) Avian louse flies and their trypanosomes: new vectors, new lineages and host–parasite associations. Microorganisms 2022, 584.CrossRefGoogle Scholar
Scheuerlein, A and Ricklefs, RE (2004) Prevalence of blood parasites in European passeriform birds. Proceedings of the Royal Society, London Series B: Biological Sciences 271, 1363–1370.CrossRefGoogle ScholarPubMed
Sehgal, RNM (2015) Manifold habitat effects on the prevalence and diversity of avian blood parasites. International Journal for Parasitology: Parasites and Wildlife 4, 421–430.Google ScholarPubMed
Snow, DW and Perrins, CM (1998) The Birds of the Western Palearctic, vol. 1. Oxford: Oxford University Press.Google Scholar
Sol, D, Jovani, R and Torres, J (2000) Geographical variation in blood parasites in feral pigeons: the role of vectors. Ecography 23, 307–314.CrossRefGoogle Scholar
Sorci, G and Møller, AP (1997) Comparative evidence for a positive correlation between haematozoan prevalence and mortality in waterfowl. Journal of Evolutionary Biology 10, 731–741.CrossRefGoogle Scholar
Valkiūnas, G (2005) Avian Malaria Parasites and Other Haemosporidia. Boca Raton: CRC Press.Google Scholar
Valkiūnas, G and Iezhova, TA (2018) Keys to the avian malaria parasites. Malaria Journal 17, 212.CrossRefGoogle Scholar
Valkiūnas, G, Ilgūnas, M, Bukauskaitė, D, Palinauskas, V, Bernotienė, R and Iezhova, TA (2017) Molecular characterization and distribution of Plasmodium matutinum, a common avian malaria parasite. Parasitology 144, 1726–1735.CrossRefGoogle ScholarPubMed
van Riper, C, van Riper, SG, Goff, ML and Laird, M (1986) The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecological Monographs 56, 327–344.CrossRefGoogle Scholar
Vedder, O, Moiron, M, Bichet, C, Bauch, CH, Verhulst, S, Becker, PH and Bouwhuis, S (2021) Telomere length is heritable and genetically correlated with lifespan in a wild bird. Molecular Ecology (online), 1–11. doi: 10.1111/mec.15807Google Scholar
Walther, E, Valkiūnas, G, Wommack, EA, Bowie, RC, Iezhova, TA and Sehgal, RN (2016) Description and molecular characterization of a new Leucocytozoon parasite (Haemosporida: Leucocytozoidae), Leucocytozoon californicus sp. nov., found in American kestrels (Falco sparverius sparverius). Parasitology Research 115, 1853–1862.CrossRefGoogle ScholarPubMed
Ward, P and Zahavi, A (1973) The importance of certain assemblages of birds as ‘information centres’ for food-finding. Ibis 115, 517–534.CrossRefGoogle Scholar
Wernham, C, Toms, M, Marchant, J, Clark, J, Siriwardena, G and Baillie, S (eds) (2002) The Migration Atlas: Movements of the Birds of Britain and Ireland. London: T. & A.D. Poyser.Google Scholar
Winkler, DW, Billerman, SM and Lovette, IJ (2015) Bird Families of the World: A Guide to the Spectacular Diversity of Birds. Ithaca, NY: Lynx Editions & Cornell Laboratory of Ornithology.Google Scholar
Zagalska-Neubauer, M and Bensch, M (2016) High prevalence of Leucocytozoon parasites in fresh water breeding gulls. Journal of Ornithology 157, 525–532.CrossRefGoogle Scholar
Zamora-Vilchis, I, Williams, SE and Johnson, CN (2012) Environmental temperature affects prevalence of blood parasites of birds on an elevation gradient: implications for disease in a warming climate. PLoS ONE 7, e39208.CrossRefGoogle Scholar