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Haemosporidian infections in skylarks (Alauda arvensis): a comparative PCR-based and microscopy study on the parasite diversity and prevalence in southern Italy and the Netherlands

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Abstract

Changes in agricultural management have been identified as the most probable cause for the decline of Skylark (Alauda arvensis) populations in Europe. However, parasitic infections have not been considered as a possible factor influencing this process. Four hundred and thirty-four Skylarks from the Southern Italy and the Netherlands were screened for haemosporidian parasites (Haemosporida) using the microscopy and polymerase chain reaction (PCR)-based methods. The overall prevalence of infection was 19.5%; it was 41.8% in Italian birds and 8.3% in Dutch birds. The prevalence of Plasmodium spp. was 34.1% and 6.5% in Skylarks from Italy and Netherlands, respectively. Approximately 15% of all recorded haemosporidian infections were simultaneous infections both in Italian and Dutch populations. Six different mitochondrial cytochrome b (cyt b) lineages of Plasmodium spp. and three lineages of Haemoproteus tartakovskyi were found. The lineage SGS1 of Plasmodium relictum was the most prevalent at both study sites; it was recorded in 24.7% of birds in Italy and 5.5% in the Netherlands. The lineages SYAT05 of Plasmodium vaughani and GRW11 of P. relictum were also identified with a prevalence of <2% at both study sites. Two Plasmodium spp. lineages (SW2 and DELURB4) and three H. tartakovskyi lineages have been found only in Skylarks from Italy. Mitochondrial cyt b lineages SYAT05 are suggested for molecular identification of P. vaughani, a cosmopolitan malaria parasite of birds. This study reports the greatest overall prevalence of malaria infection in Skylarks during the last 100 years and shows that both Plasmodium and Haemoproteus spp. haemosporidian infections are expanding in Skylarks so it might contribute to a decrease of these bird populations in Europe.

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References

  • Atkinson CT, van Riper IIIC (1991) Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. In: Loye JE, Zuk M (eds) ird-parasite interactions: Ecology, evolution, and behaviour. Oxford University Press, Oxford, U.K., pp 19–48

    Google Scholar 

  • Atkinson CT, Lease JK, Drake BM, Shema NP (2001) Pathogenicity, serological responses, and diagnosis of experimental and natural malarial infections in native Hawaiian thrushes. Condor 103:209–218

    Article  Google Scholar 

  • Bennett GF, Whiteway M, Woodworth-Lynas C (1982) A host-parasite catalogue of the avian haematozoa. Occas Pap Biol, Memorial University of Newfoundland 5:1–243

    Google Scholar 

  • Bensch S, Stjenman M, Hasselquist D, Östman Ö, Hansson B, Westerdahl H, Torres-Pinheiro R (2000) Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. P Roy Soc Lond B Bio 276:1583–1589. doi:10.1098/rspb.2000.1181

    Article  Google Scholar 

  • Bensch S, Hellgren O, Pérez-Tris J (2009) MalAvi: a public database of malaria parasites and related pigment-forming haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Mol Ecol Resour 9:1353–1358. doi:10.1111/j.1755-0998.2009.02692.x

    Article  PubMed  Google Scholar 

  • BirdLife International (2004) Birds in Europe: population estimates, trends and conservation status. Cambridge, UK: BirdLife International. (BirdLife conservation series No. 12)

  • Bishop MA, Bennett GF (1992) Host-parasite catalogue of the avian haematozoa: supplement 1, and bibliography of the avian blood-inhabiting haematozoa: supplement 2. Occas Pap Biol, Memorial University of Newfoundland 15:1–244

    Google Scholar 

  • Burtikashvili LP (1978) Blood parasites of wild birds in Georgia. Tbilisi, Metsniereba (in Russian)

    Google Scholar 

  • Chavatte JM, Gres V, Snounou G, Chabaud A, Landau I (2009) Plasmodium (Apicomplexa) of the skylark (Alauda arvensis). Zoosystema 31:369–383

    Article  Google Scholar 

  • Corradetti A, Scanga M (1973) The Plasmodium vaughani—complex. Exp Parasitol 34:344–349

    Article  PubMed  CAS  Google Scholar 

  • Cramp S (1988) The birds of the Western Palearctic, vol 5. Oxford University Press, Oxford

    Google Scholar 

  • Donald PF (2004) The skylark. T&AD Poyser, London

    Google Scholar 

  • Donald PF, Sanderson FJ, Burfield IJ, van Bommel FPJ (2006) Further evidence of continent-wide impacts of agriculture intensification on European farmland birds, 1990–2000. Agr Ecosyst Environ 116:189–196. doi:10.1016/j.agee.2006.02.007

    Article  Google Scholar 

  • Garnham PCC (1966) Malaria parasites and other Haemosporidia. Blackwell, Oxford

    Google Scholar 

  • Godfrey RD, Fedynich AM, Pence DB (1987) Quantification of hematozoa in blood smears. J Wildlife Dis 23:558–565

    Google Scholar 

  • Greiner EC, Bennett GF, White EM, Coombs RF (1975) Distribution of the avian hematozoa of North America. Can J Zool 53:1762–1787

    Article  PubMed  CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor v. 5.0.9. Nucl Acid S 41:95–98

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hellgren O, Waldenström J, Pérez-Tris J, Szöll ÖE, Hasselquist D, Križanauskienė A, Ottosson U, Bensch S (2007) Detecting shifts of transmission area in avian blood parasites—a phylogenetic approach. Mol Ecol 16:1281–1290. doi:10.1111/j.1365-294X.2007.03227.x

    Article  PubMed  Google Scholar 

  • Knowles SCL, Palinauskas V, Sheldon BC (2010) Chronic malaria infections increase family inequalities and reduce parental fitness: experimental evidence from a wild bird population. J Evol Biol 23:557–569

    Article  PubMed  CAS  Google Scholar 

  • Križanauskienė A, Hellgren O, Kosarev V, Sokolov LV, Bensch S, Valkiūnas G (2006) Variation in host specificity between species of avian haemosporidian parasites: evidence from parasite morphology and cytochrome b gene sequences. J Parasitol 92:1319–1324

    Article  PubMed  Google Scholar 

  • Križanauskienė A, Pérez-Tris J, Palinauskas V, Hellgren O, Bensch S, Valkiūnas G (2010) Molecular phylogenetic and morphological analysis of haemosporidian parasites (Haemosporida) in a naturally infected European songbird, the blackcap Sylvia atricapilla, with description of Haemoproteus pallidulus sp. nov. Parasitology 137:217–227

    Article  PubMed  Google Scholar 

  • Krone O, Waldenström J, Valkiūnas G, Lessow O, Muller K, Iezhova TA, Fickel J, Bensch S (2008) Haemosporidian blood parasites in European birds of prey and owls. J Parasitol 94:709–715. doi:10.1645/GE-1357.1

    PubMed  CAS  Google Scholar 

  • Levin II, Outlaw DC, Vargas FH, Parker PG (2009) Plasmodium blood parasite found in endangered galapagos penguins (Spheniscus mendiculus). Biol Conserv 142:3191–3195. doi:10.1016/j.biocon.2009.06.017

    Article  Google Scholar 

  • 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. Parasitol 136:713–722. doi:10.1017/S0031182009006118

    Article  Google Scholar 

  • Martinsen ES, Perkins SL, Schall JJ (2008) A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): evolution of life-history traits and host switches. Mol Phylogenet Evol 47:261–273. doi:10.1016/j.ympev.2007.11.012

    Article  PubMed  CAS  Google Scholar 

  • McClure HE, Poonswad P, Greiner EC, Laird M (1978) Haematozoa in the birds of Eastern and Southern Asia. Memorial University of Newfoundland, St. John’s, p 296

    Google Scholar 

  • Newton I (2004) The recent declines of farmland bird populations in Britain: an appraisal of causal factors and conservation actions. IBIS 146:579–600. doi:10.1111/j.1474-919X.2004.00375.x

    Article  Google Scholar 

  • Nylander JAA (2004) MrModeltest v2. Evolutionary Biology Centre, Uppsala, Program distributed by the author

    Google Scholar 

  • Olias P, Wegelin M, Freter S, Gruber AD, Klopfleischer R (2011) Avian malaria deaths in parrots, Europe. Emerg Infect Dis 17:950–952

    PubMed  Google Scholar 

  • Palinauskas V, Kosarev V, Shapoval A, Bensch S, Valkiūnas 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

    Google Scholar 

  • Palinauskas V, Valkiūnas G, Križanauskienė A, Bensch S, Bolshakov CV (2009) Plasmodium relictum (lineage P-SGS1): further observation of effects on experimentally infected passeriform birds, with remarks on the treatment with MalaroneTM. Exp Parasitol 123:134–139

    Article  PubMed  CAS  Google Scholar 

  • Parker PG, Whiteman NK, Miller E (2006) Conservation medicine on Galápagos Islands: partnership among behavioral, population, and veterinary scientists. Auk 123:625–638

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. doi:10.1093/bioinformatics/btg180

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Fritch FJ, Maniatis T (2002) Molecular cloning, a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NewYork

    Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599. doi:10.1093/molbev/msm092

    Article  PubMed  CAS  Google Scholar 

  • Valkiūnas G (1986) Haemoproteus tartakovskyi sp. n. (Haemosporidia, Haemoproteidae) from crossbill. Parasitologia 20:307–310, In Russian

    Google Scholar 

  • Valkiūnas G (2005) Avian malaria parasites and other haemosporidia. CRC Press, Boca Raton, 934 p

    Google Scholar 

  • Valkiūnas G (2011) Haemosporidian vector research: marriage of molecular and microscopical approaches is essential. Mol Ecol 20:3084–3086

    Article  PubMed  Google Scholar 

  • Valkiūnas G, Liutkevičius G (2002) Complete development of three species of Haemoproteus (Haemosporida, Haemoproteidae) in the biting midge Culicoides impunctatus (Diptera, Ceratopogonidae). J Parasitol 88:864–868. doi:10.1645/0022-3395(2002)088[0864:CDOTSO]2.0.CO;2

  • Valkiūnas G, Iezhova TA, Shapoval AP (2003) High prevalence of blood parasites in hawfinch Coccothraustes coccothraustes. J Nat Hist 37:2647–2652

    Article  Google Scholar 

  • Valkiūnas G, Bensch S, Iezhova TA, Križanauskienė A, Hellgren O, Bolshakov CV (2006) Nested cytochrome b PCR diagnostics underestimate mixed infections of avian blood hemosporidian parasites: microscopy is still essential. J Parasitol 92:418–422. doi:10.1645/GE-3547RN.1

    Article  PubMed  Google Scholar 

  • Valkiūnas G, Atkinson CT, Bensch S, Sehgal RNM, Ricklefs RE (2008a) Parasite misidentifications in GenBank: how to minimize their number? Tends Parasitol 24:247–248

    Article  Google Scholar 

  • Valkiūnas G, Iezhova TA, Križanauskienė A, Palinauskas V, Bensch S (2008b) A comparative analysis of microscopy and PCR-based detection methods for blood parasites. J Parasitol 94:1395–1401

    Article  PubMed  Google Scholar 

  • Waldenström J, Bensch S, Kiboi S, Hasselquist D, Ottosson U (2002) Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Mol Ecol 11:1545–1554. doi:10.1046/j.1365-294X.2002.01523.x

    Article  PubMed  Google Scholar 

  • Waldenström J, Hasselquist D, Bensch S, Östman Ö (2004) A new nested polymerase chain reaction method very efficient in detecting Haemoproteus and Plasmodium infections from avian blood. J Parasitol 90:191–194. doi:10.1645/GE-3221RN

    Article  PubMed  Google Scholar 

  • Yakunin MP, Zhazyltaev TA (1977) The blood parasite fauna of wild and domestic birds from Kazakhstan Trudi Instituta Zoooogii. Akademii Nauk Kazakskoi SSR 37:124–148 (in Russian)

    Google Scholar 

  • Zehtindjiev P, Ilieva M, Westerdahl H, Hansson B, Valkiūnas G, Bensch S (2008) Dynamics of parasitemia of malaria parasites in a naturally and experimentally infected migratory songbird, the great reed warbler Acrocephalus arundinaceus. Exp Parasitol 119:99–110. doi:10.1016/j.exppara.2007.12.018

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank A. Warren, the Natural History Museum, London, U.K. for providing the type and voucher material of P. vaughani. The authors are grateful to Vaidas Palinauskas for the help with images of parasites. Tatjana A. Iezhova is gratefully acknowledged for assistance during identification of parasites. Thanks are due to Najden Chukerov for participation during field studies. This study was partly funded by FP7 Capacities project WETLANET (PZ). The field work was supported by a grant from the Associazione dei Migratoristi Italiani per la Conservazione dell’Ambiente Naturale (ANUU). Laboratory work was supported by the Swedish Research Council (SB). The investigations described herein comply with the current laws of Italy and Netherlands.

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Authors and Affiliations

  1. Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, 2 Gagarin Street, 1113, Sofia, Bulgaria

    Pavel Zehtindjiev & Dimitar Dimitrov

  2. Nature Research Centre, Akademijos 2, Vilnius, 08412, Lithuania

    Asta Križanauskienė & Gediminas Valkiūnas

  3. Gruppo Inanellamento Limicoli, Traversa Napoli 58, 80078, Pozzuoli, Naples, Italy

    Sergio Scebba

  4. Animal Ecology Group, Centre for Ecological and Evolutionary Studies, University of Groningen, P.O. Box 14, 9750 AA, Haren, The Netherlands

    Arne Hegemann & B. Irene Tieleman

  5. Department of Ecology, Lund University, Ecology Building, 223 62, Lund, Sweden

    Staffan Bensch

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  1. Pavel Zehtindjiev
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Correspondence to Pavel Zehtindjiev.

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Communicated by C. Gortázar

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Zehtindjiev, P., Križanauskienė, A., Scebba, S. et al. Haemosporidian infections in skylarks (Alauda arvensis): a comparative PCR-based and microscopy study on the parasite diversity and prevalence in southern Italy and the Netherlands. Eur J Wildl Res 58, 335–344 (2012). https://doi.org/10.1007/s10344-011-0586-y

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  • DOI: https://doi.org/10.1007/s10344-011-0586-y

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