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An Experimental Study on Vertebrate Host Susceptibility to Avian Malaria Dimitar Dimitrov A,B,*, Vaidas Palinauskas A, Tatjana A

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An Experimental Study on Vertebrate Host Susceptibility to Avian Malaria Dimitar Dimitrov A,B,*, Vaidas Palinauskas A, Tatjana A Experimental Parasitology 148 (2015) 1–16 Contents lists available at ScienceDirect Experimental Parasitology journal homepage: www.elsevier.com/locate/yexpr Full length article Plasmodium spp.: An experimental study on vertebrate host susceptibility to avian malaria Dimitar Dimitrov a,b,*, Vaidas Palinauskas a, Tatjana A. Iezhova a, Rasa Bernotiene˙ a, Mikas Ilgu¯ nas a, Dovile Bukauskaite˙ a, Pavel Zehtindjiev b, Mihaela Ilieva b,c, Anatoly P. Shapoval d, Casimir V. Bolshakov d, Mikhail Yu Markovets d, Staffan Bensch c, Gediminas Valkiu¯ nas a a Institute of Ecology, Nature Research Centre, Akademijos 2, Vilnius 21, LT-08412, Lithuania b Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, 2 Gagarin Street, Sofia 1113, Bulgaria c Department of Biology, Lund University, Ecology Building, Lund S-22362, Sweden d Biological Station Rybachy of the Zoological Institute, Russian Academy of Sciences, Rybachy, Kaliningrad Region 238535, Russia HIGHLIGHTS GRAPHICAL ABSTRACT • Species of Haemamoeba and Giovannolaia have broad avian host range. • Species of Novyella and Huffia have restricted avian host range. • Specificity of different cyt b lineages of the same parasite species is variable. • Susceptibility of the same avian host to various Plasmodium isolates is variable. • Birds are more susceptible to co- infections, which are more virulent. ARTICLE INFO ABSTRACT Article history: The interest in experimental studies on avian malaria caused by Plasmodium species has increased re- Received 4 August 2014 cently due to the need of direct information about host–parasite interactions. Numerous important issues Received in revised form 20 October 2014 (host susceptibility, development of infection, the resistance and tolerance to avian malaria) can be an- Accepted 13 November 2014 swered using experimental infections. However, specificity of genetically different lineages of malaria Available online 18 November 2014 parasites and their isolates is largely unknown. This study reviews recent experimental studies and offers additional data about susceptibility of birds to several widespread cytochrome b (cyt b) lineages of Plas- Keywords: modium species belonging to four subgenera. We exposed two domesticated avian hosts (canaries Serinus Avian malaria Plasmodium canaria and ducklings Anas platyrhynchos) and also 16 species of common wild European birds to malaria Experimental infection infections by intramuscular injection of infected blood and then tested them by microscopic examina- Bird susceptibility tion and PCR-based methods. Our study confirms former field and experimental observations about low Parasite specificity specificity and wide host-range of Plasmodium relictum (lineages SGS1 and GRW11) and P. circumflexum * Corresponding author. Fax: +370 5 272 93 52. E-mail address: [email protected] (D. Dimitrov). http://dx.doi.org/10.1016/j.exppara.2014.11.005 0014-4894/© 2014 Elsevier Inc. All rights reserved. 2 D. Dimitrov et al./Experimental Parasitology 148 (2015) 1–16 (lineage TURDUS1) belonging to the subgenera Haemamoeba and Giovannolaia, respectively. However, the specificity of different lineages and isolates of the same parasite lineage differed between species of exposed hosts. Several tested Novyella lineages were species specific, with a few cases of successful development in experimentally exposed birds. The majority of reported cases of mortality and high parasitaemia were observed during parasite co-infections. Canaries were susceptible mainly for the species of Haemamoeba and Giovannolaia, but were refractory to the majority of Novyella isolates. Ducklings were susceptible to three malaria infections (SGS1, TURDUS1 and COLL4), but parasitaemia was light (<0.01%) and transient in all exposed birds. This study provides novel information about susceptibility of avian hosts to a wide array of malaria parasite lineages, outlining directions for future experimental research on various aspects of biology and epidemiology of avian malaria. © 2014 Elsevier Inc. All rights reserved. 1. Introduction ways and might be highly virulent and even lethal in some birds (Atkinson and LaPointe, 2009; Palinauskas et al., 2011). Important Blood parasites of the genus Plasmodium (Haemosporida, question about tolerance and resistance to avian malaria can be an- Plasmodiidae) are vector borne pathogens, which cause malaria and swered only using experimental infections (Atkinson et al., 2013). have complicated life cycles, involving female mosquitoes as de- Bird immunity play a key role in host–parasite interaction pro- finitive host and vertebrate animals including humans as cesses, and it is likely to have an effect on parasite evolution (Sorci, intermediate hosts. The vertebrate host serves as reservoir of the 2013). However, the existing knowledge about bird mortality during infection, with parasite development in the blood and other tissues. malaria infection is mainly due to observations of infections inci- A characteristic feature of Plasmodium spp. is the erythrocytic me- dentally reported in exotic birds that were moved from their natural rogony, which takes place in the peripheral blood. This feature allows distribution areas and kept in aviaries, zoos and private collec- initiation of controlled experimental infections without participa- tions (Cranfield et al., 1994; Ferrell et al., 2007; Fix et al., 1988). The tion of the vectors. This method of experimental research was challenges to identify emerging infection diseases in nature are developed in the end of the 19th century and has since been used mainly due the prevailing methods of sampling wild birds, i.e. dif- in studies of virulence, pathogenicity and other aspects of biology ferent methods for mist-netting and trapping. Such methods of avian malaria, and is still a frequently used method (Iezhova et al., preferably select actively moving healthy birds, but individuals suf- 2005; Larcombe et al., 2013; Palinauskas et al., 2007; Valkiu¯ nas, 2005; fering severe malaria, which leads to lowering of the locomotion Zehtindjiev et al., 2008). activity, remain underestimated (Valkiu¯ nas, 2005). For these reasons From the controlled experiments, huge knowledge about malaria the experimental studies constitute a powerful tool in determin- parasites’ pathogenicity, specificity and epidemiology have been re- ing the impact of malarial infections on bird individuals and vealed. Experiments with avian hosts as model organisms were populations (Larcombe et al., 2013; Palinauskas et al., 2008, 2011; particularly important in the beginning of human malaria re- Yorinks and Atkinson, 2000; Zehtindjiev et al., 2008). search; they contributed to the better understanding of Plasmodium Species identification of avian malaria and related haemospo- parasites’ biology and unravelling their complicated life cycles ridian parasites is currently based on microscopic examination of (Marzal, 2012). Currently, the experiments with bird malaria para- morphological features of the parasites, mainly during erythro- sites are performed for a variety of purposes aimed at better cytic stages; experimental data about specificity of the parasites to understanding of parasite diversity, host–parasites interactions, life- avian host and vectors are also considered (Garnham, 1966; history traits, interactions during co-infections, clarification of the Valkiu¯ nas, 2005). Application of molecular markers (DNA bar- genetic variation and the analysis of gene expression during primary codes) provides additional opportunities for parasite species infections (Garnham, 1966; Iezhova et al., 2005; Larcombe et al., identification. Initial molecular surveys revealed a much larger 2013; Palinauskas et al., 2008, 2009, 2011; Permin and Juhl, 2002; genetic diversity than existing morphospecies suggested by tradi- Valkiu¯ nas et al., 2013; Williams, 2005; Yorinks and Atkinson, 2000; tional taxonomy (Beadell et al., 2004, 2006; Bensch et al., 2000, 2004; Zehtindjiev et al., 2008). Hellgren et al., 2004; Martinsen et al., 2008; Perkins and Schall, 2002). Malaria parasites are widespread in birds, and the prevalence This information raises questions regarding validity of both the of infection often exceeds 20% in many bird populations. However, current systematic of haemosporidians and the established host rather low malaria infection prevalence (<10%) often is reported in specificity knowledge. For example, several mitochondrial cyto- some avian host species too, for example the birds belonging to the chrome b (cyt b) lineages (SGS1, GRW04, GRW11 and LZFUS01), families Hirundinidae, Icteridae, Prunellidae, Regulidae, Sittidae, which likely represent intraspecific genetic variation, have been de- Troglodytidae and some others (Valkiu¯ nas, 2005). Due to anthro- termined within the P. relictum morphospecies (Ilgu¯ nas et al., 2013; pogenic influence and the global climate and environmental changes, Palinauskas et al., 2007; Valkiu¯ nas et al., 2007, 2008). These and many widespread host-generalist malaria pathogens expand in new areas other cyt b lineages might have a different ability to infect differ- and bird populations. An example is P. relictum, a virulent invasive ent bird species, but this remains largely unknown. In addition, avian malaria parasite (Garamszegi, 2011; Loiseau et al., 2012a), variability of biological features of the same cyt b lineage isolated which is the most prevalent and widely distributed parasite among from different donor species (different isolates) might also affect the haemosporidians
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