Haemoproteus syrnii in Strix aluco from France: morphology, stages of sporogony in a hippoboscid fly, molecular characterization and discussion on the identification of Haemoproteus species

Parasite

and Irène Landau⁴  Georges Snounou²  Jean-Marc Chavatte¹  Linda Duval⁴  Marie-Pierre Puech³  Grégory Karadjian⁴ 

[1] Malaria Reference Centre – National Public Health Laboratory, Ministry of Health, 9 Hospital Drive, Block C, #04-01, Sing Health Research Facilities,169612 Singapore;Université Pierre et Marie Curie-Paris 6, Faculté de Médecine Pitié-Salpêtrière, CHU Pitié-Salpêtrière,91 Bd de l’Hôpital,75013 Paris,France;Hôpital de la faune sauvage des Garrigues et Cévennes – Clinique vétérinaire,19 avenue du Vigan,34190 Ganges,France;UMR 7245 MCAM MNHN CNRS, Muséum National d’Histoire Naturelle,61 rue Buffon,CP 52,75231 Paris Cedex 05,France

关键词: Molecular identification;    Haemoproteus subgenera;    Pupiparous fly;    Volutin granules;    Strix aluco;    Haemoproteus syrnii;   

Others  :  808509
DOI  :  doi:10.1051/parasite/2013031

 received in 2013-06-27, accepted in 2013-08-30,  发布年份 2013

【 摘 要 】

In France, Haemoproteus syrnii is frequently found in the Tawny Owl, Strix aluco. Additional and complementary features of this species, and in particular the characteristics of volutin, are presented. The authors consider the volutin granules as constant in a given species, and discuss their taxonomic value. These cytoplasmic inclusions appear early during the first stages of development of the gametocytes as an initial granule which multiplies as the parasite develops. They were reported in some species of Haemoproteus but are seldom considered as a specific character and described with precision. Sporogony from ookinete to apparently mature sporozoites appears to take place in a pupiparous hippoboscid (Ornithomyia sp.). One specimen was crushed between two slides and stained with Giemsa. Gametocytes of H. syrnii, many ookinetes, an immature oocyst and mature sporozoites were observed spread all over the smear. This would allow classifying this species in the Haemoproteus subgenus. We provide associated molecular data derived from the cyt b and cox 1 gene from this parasite. We discuss the problems of multiple infections and the difficulties in identifying Haemoproteus species and in deriving conclusions from sequences deposited in databases.

【 授权许可】

   
© G. Karadjian et al., published by EDP Sciences, 2013

【 图 表 】

Figures 1–16.

Figures 17–31.

Figures 32–35.

Figure 36.

【 参考文献 】

• [1]Bennett GF, Garnham PCC, Fallis AM. 1965. On the status of the genera Leucocytozoon Ziemann, 1893 and Haemoproteus Kruse, 1890 (Haemosporidiida: Leucocytozoidae and Haemoproteidae). Canadian Journal of Zoology, 43(6), 927–932. [PubMed]
• [2]Bishop MA, Bennett GF. 1989. The haemoproteids of the avian order Strigiformes. Canadian Journal of Zoology, 67, 2676–2684.
• [3]Celli A, San Felice F. 1891. Ueber die Parasiten des rothen Blutkörperchens im Menschen und in Thieren. Fortschritte der Medizin, 9, 499–511, 541–552, 581–586.
• [4]Covaleda Ortega J, Gallego Berenguer J. 1950. Haemoproteus aviares. Revista Iberica de Parasitologia, 10, 141–185.
• [5]Duval L, Robert V, Csorba G, Hassanin A, Randrianarivelojosia M, Walston J, Nhim T, Goodman SM, Ariey F. 2007. Multiple host-switching of Haemosporidia parasites in bats. Malaria Journal, 6, 157. [PubMed]
• [6]Facoz L. 1926. Diptères pupipares – Faune de France. Fédération Française des Sociétés de Sciences Naturelles – Office Centrale de faunistique. Lachevalier P. (Ed.), Paris, 64 pp.
• [7]Garnham PCC. 1968. Malaria parasites and other Haemosporidia. Blackwell Scientific Publications, 1114 pp.
• [8]Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systems Biology, 59(3), 307–321.
• [9]Hellgren O, Waldenstrom J, Perez-Tris J, Szoll E, Si O, Hasselquist D, Krizanauskiene A, Ottosson U, Bensch S. 2007. Detecting shifts of transmission areas in avian blood parasites: a phylogenetic approach. Molecular Ecology, 16(6), 1281–1290. [PubMed]
• [10]Huff C. 1932. Studies on Haemoproteus of mourning doves. American Journal of Epidemiology, 16, 618–623.
• [11]Hutson AM. 1984. Keds, flat flies, and bat flies. Diptera, Hippoboscidae and Nycteribiidae. Handbook for the identification of British Insects, Vol. 10, Part 7. Royal Entomological Society of London, 40 pp.
• [12]Krizanauskiene A, Iezhova TA, Sehgal RNM, Carlson JS, Palinauskas V, Bensch S, Valkiūnas G. 2013. Molecular characterization of Haemoproteus sacharovi (Haemosporida, Haemoproteidae), a common parasite of columbiform birds, with remarks on classification of haemoproteids of doves and pigeons. Zootaxa, 3613(1), 85–94.
• [13]Krone O, Waldenstrom J, Valkiūnas G, Lessow O, Muller K, Iezhova TA, Fickel J, Bensch S. 2008. Haemosporidian blood parasites in European birds of prey and owls. Journal of Parasitology, 94(3), 709–715.
• [14]Kruse W. 1890. Ueber Blutparasiten. Archiv für pathologische Anatomie und Physiologie und für klinische Medizin, 121, 359–372, 453–485.
• [15]Levin II, Valkiūnas G, Santiago-Alarcon D, Cruz LL, Iezhova TA, O’Brien SL, Hailer F, Dearborn D, Schreiber EA, Fleischer RC, Ricklefs RE, Parker PG. 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(10), 1019–1027. [PubMed]
• [16]Luo S, Marchesini N, Moreno SN, Docampo R. 1999. A plant-like vacuolar H(+)-pyrophosphatase in Plasmodium falciparum. FEBS Letter, 460(2), 217–220.
• [17]Marchesini N, Luo S, Rodrigues CO, Moreno SN, Docampo R. 2000. Acidocalcisomes and a vacuolar H+-pyrophosphatase in malaria parasites. Biochemical Journal, 347 Pt 1, 243–253.
• [18]Martinsen ES, Paperna I, Schall JJ. 2006. Morphological versus molecular identification of avian Haemosporidia: an exploration of three species concepts. Parasitology, 133(Pt 3), 279–288. [PubMed]
• [19]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. Molecular Phylogenetics and Evolution, 47(1), 261–273. [PubMed]
• [20]Massonat E. 1909. Contribution à l’étude des pupipares. Annales de l’Université de Lyon. Nouvelle Série – I. Sciences, Médecine, Fascicule 24, 406 pp.
• [21]Mayer M. 1911. Über ein Halteridium und Leucocytozoon des Waldkauzes une deren Weiterentwicklung in Stechmücken. Archiv für Protistenkunde, 21, 232–254.
• [22]Mayer M. 1910. Über sein Entwicklung von Halteridium. Archiv für Schiffs und Tropenhygiene, 14, 197–202.
• [23]Merino S, Hennicke J, Martinez J, Ludynia K, Torres R, Work TM, Stroud S, Masello JF, 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(2), 388–397.
• [24]Novy F, MacNeal W. 1904. Trypanosomes and bird malaria. American Medicine, 8, 932–934.
• [25]Paperna I, Keong MSC, May CYA. 2008. Haemosporozoan parasites found in birds in Peninsular Malaysia, Singapore, Sarawak and Java. Raffles Bulletin of Zoology, 56(2), 211–243.
• [26]Rashdan NA. 1998. Role of Pseudolynchia canariensis in the transmission of Haemoproteus turtur from the migrant Streptopelia turtur to new bird hosts in Egypt. Journal of Egyptian Society for Parasitology, 28, 221–228.
• [27]Rodrigues CO, Scott DA, Bailey BN, De Souza W, Benchimol M, Moreno B, Urbina JA, Oldfield E, Moreno SN. 2000. Vacuolar proton pyrophosphatase activity and pyrophosphate (PPi) in Toxoplasma gondii as possible chemotherapeutic targets. Biochemical Journal, 349(Pt 3), 737–745.
• [28]Rodrigues CO, Scott DA, Docampo R. 1999. Presence of a vacuolar H+-pyrophosphatase in promastigotes of Leishmania donovani and its localization to a different compartment from the vacuolar H+-ATPase. Biochemical Journal, 340(Pt 3), 759–766.
• [29]Ruiz FA, Rodrigues CO, Docampo R. 2001. Rapid changes in polyphosphate content within acidocalcisomes in response to cell growth, differentiation, and environmental stress in Trypanosoma cruzi. Journal of Biological Chemistry, 276(28), 26114–26121.
• [30]Scott DA, Docampo R. 1998. Two types of H+-ATPase are involved in the acidification of internal compartments in Trypanosoma cruzi. Biochemical Journal, 331(Pt 2), 583–589.
• [31]Valkiūnas G. 2005. Avian malaria parasites and other Haemosporidia. CRC Press, Boca Raton, Florida, 946 pp.
• [32]Valkiūnas G, Atkinson CT, Bensch S, Sehgal RN, Ricklefs RE. 2008. Parasite misidentifications in GenBank: How to minimize their number? Trends in Parasitology, 24(6), 247–248. [PubMed]
• [33]Valkiūnas G, Iezhova TA, Evans E, Carlson JS, Martinez-Gomez JE, Sehgal RN. 2013. Two new Haemoproteus species (Haemosporida: Haemoproteidae) from columbiform birds. Journal of Parasitology, 99(3), 513–521.
• [34]Valkiūnas G, Kazlauskiene R, Bernotiene R, Palinauskas V, Iezhova TA. 2013. Abortive long-lasting sporogony of two Haemoproteus species (Haemosporida, Haemoproteidae) in the mosquito Ochlerotatus cantans, with perspectives on haemosporidian vector research. Parasitology Research, 112(6), 2159–2169. [PubMed]
• [35]Valkiūnas G, Santiago-Alarcon D, Levin II, Lezhova TA, Parker PG. 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(4), 783–792.
• [36]Work TM, Rameyer RA. 1996. Haemoproteus iwa n. sp. in great frigatebirds (Fregata minor) from Hawaii: parasite morphology and prevalence. Journal of Parasitology, 82(3), 489–491.