Prevalence and Diversity of Avian Hematozoan Parasites in Asia: a Regional Study

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7-1-2007

Prevalence and Diversity of Avian Hematozoan Parasites in Asia: A Regional Study

Farah Ishtiaq Smithsonian Institution

Eben Gering Smithsonian Institution, [email protected]

Jon H. Rappole Conservation and Research Center

Asad R. Rahmani Bombay Natural History Society - Mumbai, India

Yadvendradev V. Jhala Wildlife Institute of India - Dehradun

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NSUWorks Citation Ishtiaq, Farah; Eben Gering; Jon H. Rappole; Asad R. Rahmani; Yadvendradev V. Jhala; Carla J. Dove; Christopher M. Milensky; Storrs L. Olson; Mike A. Peirce; and Robert C. Fleischer. 2007. "Prevalence and Diversity of Avian Hematozoan Parasites in Asia: A Regional Study." Journal of Wildlife Diseases 43, (3): 382-398. doi:10.7589/0090-3558-43.3.382.

This Article is brought to you for free and open access by the Department of Biological Sciences at NSUWorks. It has been accepted for inclusion in Biology Faculty Articles by an authorized administrator of NSUWorks. For more information, please contact [email protected]. Authors Farah Ishtiaq, Eben Gering, Jon H. Rappole, Asad R. Rahmani, Yadvendradev V. Jhala, Carla J. Dove, Christopher M. Milensky, Storrs L. Olson, Mike A. Peirce, and Robert C. Fleischer

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PREVALENCE AND DIVERSITY OF AVIAN HEMATOZOAN PARASITES IN ASIA: A REGIONAL SURVEY

Authors: Farah Ishtiaq, Eben Gering, Jon H. Rappole, Asad R. Rahmani, Yadvendradev V. Jhala, et. al. Source: Journal of Wildlife Diseases, 43(3) : 382-398 Published By: Wildlife Disease Association URL: https://doi.org/10.7589/0090-3558-43.3.382

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Downloaded From: https://bioone.org/journals/Journal-of-Wildlife-Diseases on 03 Oct 2019 Terms of Use: https://bioone.org/terms-of-use Journal of Wildlife Diseases, 43(3), 2007, pp. 382–398 # Wildlife Disease Association 2007

PREVALENCE AND DIVERSITY OF AVIAN HEMATOZOAN PARASITES IN ASIA: A REGIONAL SURVEY

Farah Ishtiaq,1,7,8 Eben Gering,1 Jon H. Rappole,2 Asad R. Rahmani,3 Yadvendradev V. Jhala,4 Carla J. Dove,5 Chris Milensky,5 Storrs L. Olson,5 Mike A. Peirce,6 and Robert C. Fleischer1 1 Genetics Program, National Zoological Park, National Museum of Natural History, Smithsonian Institution, 3001 Connecticut Ave. NW, Washington, D.C. 20008, USA. 2 Conservation and Research Center, Front Royal, Virginia 22630, USA 3 Bombay Natural History Society, Hornbill House, S. B. Singh Road, Mumbai 400023, India 4 Wildlife Institute of India, PO Box 18, Chandrabani, Dehra Dun 248001, Uttaranchal, India 5 Division of Birds, National Museum of Natural History, Smithsonian Institution, Room E 607, MRC 116, Washington, D.C. 20013-7012, USA 6 6 Normandale House, Normandale, Bexhill-on-Sea, East Sussex, TN39 3NZ, UK 7 Current address: Edward Grey Institute of Field Ornithology, Department of Zoology, University of Oxford, South Parks Road, Oxford, OX1 3PS, UK. 8 Corresponding author (email: [email protected])

ABSTRACT: Tissue samples from 699 birds from three regions of Asia (Myanmar, India, and South Korea) were screened for evidence of infection by avian parasites in the genera Plasmodium and Haemoproteus. Samples were collected from November 1994 to October 2004. We identified 241 infected birds (34.0%). Base-on-sequence data for the cytochrome b gene from 221 positive samples, 34 distinct lineages of Plasmodium, and 41 of Haemoproteus were detected. Parasite diversity was highest in Myanmar followed by India and South Korea. Parasite prevalence differed among regions but not among host families. There were four lineages of Plasmodium and one of Haemoproteus shared between Myanmar and India and only one lineage of Plasmodium shared between Myanmar and South Korea. No lineages were shared between India and South Korea, although an equal number of distinct lineages were recovered from each region. Migratory birds in South Korea and India originate from two different migratory flyways; therefore cross- transmission of parasite lineages may be less likely. India and Myanmar shared more host species and habitat types compared to South Korea. Comparison between low-elevation habitat in India and Myanmar showed a difference in prevalence of haematozoans. Key words: Avian malaria, hematozoan parasites, India, Myanmar, South Korea.

INTRODUCTION Molecular techniques also have been used to differentiate between native and in- The avian hematozoan parasites Plas- troduced parasite lineages in native and modium and Haemoproteus are two well- introduced populations of common myna studied and globally distributed genera of (Acridotheres tristis; Ishtiaq et al., 2006) blood parasites (Atkinson and Van Riper and to detect cross-species transmissions 1991). Recent molecular studies using between migratory and resident birds DNA sequencing to identify and charac- (Waldenstro¨m et al., 2002). terize parasite lineages (Bensch et al., Each year billions of migratory birds 2000; Ricklefs and Fallon, 2002; Fallon et migrate between tropical wintering areas al., 2003; Beadell et al., 2004) have to temperate summer breeding grounds revealed more detailed information than (McClure, 1974b). Although Asia is a win- was provided by morphology alone (Per- tering and staging ground for many migra- kins and Schall, 2002). Studies have been tory birds, and a major source of exotic conducted on the morphologic classifica- species that have been introduced into tion of these two parasite genera (Atkinson many other regions, it has remained the and Van Riper, 1991), host specificity least-explored region as far as the genetic (Bensch et al., 2000; Ricklefs and Fallon, diversity of avian blood parasites is con- 2002; Waldenstro¨m et al., 2002; Beadell et cerned. The global movements of diverse al., 2004), and geographical distribution avian species that may be infected with (Fallon et al., 2005; Durrant et al., 2006). blood parasites should be a cause of concern

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given the potential of migrants and in- monsoon during the dry season) that varied troduced species to spread novel diseases from dry deciduous forest to scrubland and marshland (Fig. 1A). Each bird captured was worldwide (McClure, 1974a; Rappole et al., banded for individual identification with rings 2000). This may be especially relevant to provided by the Bombay Natural History isolated regions where native species may Society (BNHS), sexed, aged, measured, have a reduced immune defense against weighed, and examined for flight or body such parasites (Van Riper et al., 1986). molt. Approximately 50–100 ml of whole blood was drawn by humeral venipuncture into Hawaii is an excellent example of a microvette with EDTA anticoagulant and biological invasion where the introduc- used for the preparation of blood smears and tions of avian malaria (Plasmodium relic- DNA analysis. In South Korea, 181 tissue tum) and avian pox into highly susceptible samples were collected in October 2004 from native populations led to the endanger- two airbases (Kunsan and Osan) (Fig. 1B). We examined 335 bird tissue samples (all blood ment and possible extinction of many impregnated) collected from four locations in native birds (Van Riper et al., 1986). Myanmar between November 1994 and About 125 bird species were introduced March 2001 (in winter–dry season). Myan- to the Hawaiian Islands in the late nine- mar’s climate and vegetation vary greatly from teenth and early twentieth centuries the temperate north and high-altitude zones to equatorial regions in the far south. The four (Caum, 1933; Berger, 1981; Pratt, 1994); sampling locations (Hkakabo Razi National the majority of these originated from India Park, Taungoo area, Alaungdaw Kathapa and Southeast Asia. As part of a global National Park, and Chatthin Wildlife Sanctu- survey to determine the origin of Plasmo- ary) varied from altitudes of 200 to 3,500 m dium relictum in Hawaii, India has been and habitats ranging from degraded forest to alpine forest (Fig. 1C). included as a region of interest as at least 12 avian species were introduced from Screening of blood smears by microscopy Hawaii from this source (Long, 1981). In Thin blood smear slides were obtained from this study, we examined the genetic di- each bird sampled in India. These were fixed versity of hematozoan parasites of India, with methanol, stained for 1 hr with 6% Myanmar, and South Korea. Although phosphate buffered Giemsa (pH 7.0) and McClure et al. (1978) conducted a large- scanned at 4003 for 10 min to diagnose scale microscopy-based survey of the malarial infections. Parasite species were identified using morphologic characteristics hematozoans in birds from eastern and (Garnham, 1966). A minimum of 50,000 southern Asia, molecular-based surveys erythrocytes were examined on each slide have not been previously conducted in (Atkinson et al., 1995). The level of parasite- Asia. Our goals were to 1) determine the mia was based upon results of these examina- prevalence of infection within and across tions. Blood smears were not available for birds sampled in Myanmar and South Korea. regions, and in families of host species shared between regions, 2) determine the Molecular analysis phylogenetic relationships of the hema- Host and parasite DNA was extracted from tozoan parasites found in these regions, 3) tissue and blood samples using Qiagen estimate the degree of lineage sharing DNeasy kits (Qiagen, Valencia, California between regions, and 4) determine para- USA) following manufacturer guidelines. To site diversity among regions. ensure the quality of DNA extractions, we amplified a small fragment (347 bp) of cyt b DNA of host using primers cytb-1 and cytb2 MATERIALS AND METHODS following the methods described in Kocher et Sampling al. (1989). These PCRs were successful in all cases. Two primers sets were used for parasite We collected blood samples from 183 birds screening of samples; these included primer in India from seven sites (three sites near set F2/R2 (91bp,cytochrome b gene [cyt b]) Pinjore, in Haryana, Meerut in Uttar Pradesh, and primer set 850F/1024R (167 bp; Beadell and three sites near Guwahati in Assam) et al., 2004; COIII gene). For positive samples, between May and June 2003 (before the we attempted to amplify a larger fragment

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FIGURE 1. Sampling sites in A) India, B) South Korea, and C) Myanmar.

(533 bp) of the cyt b sequence using primers TCT ACT GTA ATT GC-39; 313 bp) and FIFI 3760F/4292RW2 (Beadell et al., 2004). Be- (59-GGG TCA AAT GAG TTT CTGG-39) with cause it was not always possible to amplify the 4292RW2 (351 bp) were used. Details of the larger 533 bp fragments, we attempted to PCR protocols are reported in Beadell et al. amplify smaller fragments of either 256 bp (2004) and Ishtiaq et al. (2006). Negative and using primers 3760F with R1 (59-CTT TTT positive controls were included in all reactions. AAG GTT GGG TCA CTT-39) or 295 bp using Parasite DNA (P. relictum) from an infected primers F3 (59-CCA GGA CTT GTT TCA Hawaii Amakihi (Hemignathus virens)was TGG AT-39) with 4292RW2. When these used as a positive control. Samples from primer sets failed to amplify DNA, additional India were screened and amplified in reactions using F3 with R3 (59-GCA TAT CTA WII’s conservation genetics lab, and Myanmar

TABLE 1. Prevalence of Plasmodium and Haemoproteus based on polymerase chain reaction (PCR) detection for sampling sites in Myanmar and India.

Total Sampling sitea Date Altitude (m) Habitat samples Plasmodium Haemoproteus

Myanmar Hkakabo Razi NP February–March .3,500 Alpine 178 29 1 2001 Taungoo Area November 1994 200–500 Degraded 13 0 1 Alaungdaw Kathapa December 1994, 200–500 Lowland 23 4 1 NP 1997 deciduous Chatthin WLS November– 500–1,000 Lowland 121 35 8 December 1994 evergreen India Vulture (H) center May–June 2003 ,200 Dry deciduous 31 7 14 Pinjore (H) May–June 2003 ,200 City 16 3 4 Nagaon (A) May–June 2003 ,200 City 27 5 0 Meerut (UP) May–June 2003 ,200 Scrubland 64 18 11 Guwahati (A) May–June 2003 ,200 City 13 0 1 Deobali Jalah (A) May–June 2003 ,200 Marshland 17 4 0 Ambala (H) May–June 2003 ,200 City 15 8 3

a H 5 Haryana, A 5 Assam, UP 5 Uttar Pradesh.

and South Korea samples were analyzed at gamma shape parameter equaled 1.0639; for the genetics program at the Smithsonian Haemoproteus the invariable sites equaled Institution. 0.4514, and the gamma shape parameter All samples with positive amplification for equaled 0.4899. These settings were imple- larger fragments were purified using Qiaquick mented in a maximum likelihood analysis to kits (Qiagen) and sequenced bidirectionally on estimate the topology of the avian malaria an ABI 3100 Sequencer (Applied Biosystems, parasites. We used 100 replicates and the Inc., Foster City, California, USA). Sequences ‘‘fast’’ heuristic in PAUP* (Swofford, 1999) to were edited and aligned using the program estimate bootstrap support. SEQUENCHER version 4.1 and are available through Genbank (accession numbers Statistical analysis EF380111–EF380209). To assess differences in the prevalence of Plasmodium spp. and Haemoproteus spp. Phylogenetic analysis between different regions, we used contingen- Phylogenetic relationships were evaluated cy table analyses in SAS to compare frequency using samples for which we had at least 256 bp differences using x2 or Fisher exact tests. To of cyt b sequence. Based on the phylogeny in assess whether prevalence of parasites differed Perkins and Schall (2002), the phylogenetic across host families and regions, we performed trees were rooted using either lizard Plasmo- analysis of variance (ANOVA) on arcsine dium (Genbank accession numbers AY099061, square-root transformed prevalence rates at AY099060) or Haemoproteus (Genbank acces- the host species level (Scheuerlein and Rick- sion numbers AY099062, AY099057) se- lefs, 2004). We estimated generalized linear quences as outgroups. We used MODELT- models (SAS institute) with prevalence as the EST version 3.6 (Posada and Crandall, 1998) dependent variable and region and family as to determine the most appropriate evolution- independent variables. Avian families were ary model for our data. The hierarchical included in analyses only if they occurred in likelihood ratio test using Akaike Information two or more regions and included $5 Criterion (AIC) selected the general time- individuals per regions (Table 1). Individual reversible model (GTR+I+G) for both Plas- contribution of variables was summarized as F- modium and Haemoproteus phylogenies sepa- values and associated probabilities (type III rately. For Plasmodium, the proportion of sums of squares). Taxonomy follows the invariable sites equaled 0.6407, and the Handbook of the Birds of the World (http://

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www.hbw.com/ibc/phtml/familia.phtml). Esti- sites was detected (x2526.65, P50.0002, mateS version 7.0 (2004) was used to calculate df56). Shannon diversity (mean6s.d.) within regions for both parasite lineages and host species. Of the 181 samples of 46 bird species in South Korea, 76 individuals (42%) repre- RESULTS senting 34 species tested positive for Plasmodium spp. and Haemoproteus spp. Prevalence of parasites Of the positive samples, 56 (31%) were We screened a total of 699 birds from Plasmodium spp. and 20 (11%)were Myanmar, India, and South Korea. Of the Haemoproteus spp. infections. The posi- 335 samples tested in Myanmar, the tive samples included 10 Plasmodium and prevalence of infection was 122 (37.3%). five Haemoproteus lineages. Of these, 113 individuals were positive for There was no difference (x250.15, Haemoproteus spp. (45 [40%]) and Plas- P52.0, df51) in the parasite prevalence modium spp. (68 [60%]). Based on between host blood (India) and host tissue sequence data, nine individuals showed (Myanmar and South Korea) samples. double peaks indicating that these indi- There were significant differences for viduals were infected with two parasite Plasmodium spp. (x259.27, P50.009, lineages. Sequencing results identified 28 df52) and Haemoproteus spp. (x25 unique lineages for Plasmodium and 21 for 29.56, P50.001, df52) prevalence among Haemoproteus; these were detected in 42 the three regions, with India and South of 133 represented bird species. There Korea having the higher prevalence for was a significant difference in Plasmodium both lineages than Myanmar. Differences spp. (P50.012, Fisher’s exact test) but not in prevalence between Myanmar and in Haemoproteus spp. (P50.079, Fisher’s India at sites located between 200 and exact test) prevalence among populations 500 m elevation were not detected for at different study sites in Myanmar Plasmodium spp. (P50.48, Fisher’s exact (Table 1). Significant differences in prev- test) but were observed for Haemoproteus alence of Haemoproteus spp. (P50.232, spp. (P50.005, Fisher’s exact test). For Fisher’s exact Test) or Plasmodium spp. lower-sited elevations, prevalence differ- (P50.065, Fisher’s exact Test) between ences between South Korea and Myanmar the pooled low (500–3,500 m) and high and India (pooled together) also were not (200–500 m) elevation sites were not detected for Plasmodium spp. (P50.06, detected. Fisher’s exact test), but differences were In India, of the 183 samples represent- detected for Haemoproteus spp. (P50.04, ing 43 species, 84 individuals of 33 species Fisher’s exact test). tested positive for Plasmodium spp. and Of 52 avian families recorded, 17 were Haemoproteus spp. Of the positive sam- common to all three regions, but there was ples, 51 (28%) were Plasmodium spp. and no overlap at the species level between 33 (18%) were Haemoproteus spp. infec- regions (Table 2). Prevalence of Plasmo- tions. There were 11 individuals showing dium spp. (F51.16, df516, P50.310) and multiple infections; we were not able to Haemoproteus spp. (F51.08, df516, determine sequences for 23 positive sam- P50.383) did not differ among avian ples. Sequencing results indicated that families. Among regions, differences in positive samples represented 11 Plasmo- prevalence for the 17 families shared dium and 19 Haemoproteus lineages. between regions were detected for both There was no significant difference in Plasmodium spp. (F512.94, df52, P5 Plasmodium spp. (x2512.2, P50.056, 0.001) and Haemoproteus spp. (F512.89, df56) prevalence among populations in df52, P50.001). Regional grouping ex- India, but significant difference for the plained 35% and 27% of the total variance prevalence of Haemoproteus spp. between for Plasmodium spp. and Haemoproteus

TABLE 2. Prevalence of Plasmodium and Haemoproteus based on PCR detection for selected host families from three Asian regions (Myanmar, India, and South Korea).

Sample Plasmodium Haemoproteus Family Region Host species size positivee positivee Columbidaec Myanmar Spotted Dove Streptopelia chinensis 20 1 Red Turtle Dove Streptopelia tranque- 11 0 barica India Red Turtle Dove 1 0 1 Blue Rock Pigeon Columba livia 50 1 S. Korea Rufous Turtle Dove Streptopelia orientalis 41 0 Total 13 2 (15) 3 (23) Corvidaec Myanmar Collared Treepie Dendrocitta frontalis 20 0 India Rufous Treepie Dendrocitta vagabunda 50 3 S. Korea Black-billed Magpie Pica pica 31 1 Jay Garrulus glandarius 51 0 Total 15 2 (13)f 4 (26) Meropidaeb Myanmar Little Green Bee-eater Merops orientalis 52 0 India Little Green Bee-eater 1 0 0 Total 6 2 (33) 0 Motacillidaea Myanmar Black-backed Wagtail Motacilla lugens 10 0 S. Korea Olive-backed Pipit Anthus hodgsoni 32 0 Pipit Anthus sp. 2 0 0 Red-throated Pipit Anthus cervinus 31 0 White Wagtail Motacilla alba 11 0 Total 9 4 (44)f 0 Muscicapidaec Myanmar Grey-headed Flycatcher Culicicapa 10 0 ceylonensis Niltava 1 0 1 Large Niltava Niltava grandis 50 0 Little Forktail Enicurus scouleri 10 0 Oriental Magpie-Robin Cosychus saularis 76 0 White-rumped Shama Copsychus mala- 72 0 baricus Orange-flanked Bush Robin Tarsiger 21 0 cyanurus Plumbeous Water Redstart Rhyacornis 10 0 fuliginosus Daurian Redstart Phoenicurus auroreus 10 0 Red-breasted Flycatcher Ficedula parva 61 4 Rufous-bellied Niltava Niltava sundara 71 0 Rufous-gorgeted Flycatcher Ficedula 51 0 strophiata Slaty-backed Forktail Enicurus schistaceus 10 0 Small Nilatava Niltava macgregoriae 10 0 White-gorgeted Flycatcher Ficedula 80 0 monileger White-tailed Robin Cinclidium leucurum 11 0 Blue Flycatcher Cyornis sp. 1 0 0 India Oriental Magpie Robin 5 0 0 Indian Robin Saxicoloides fulicata 20 2 Brown Rock Chat Cercomela fusca 31 0 S. Korea Daurian Redstart Phoenicurus auroreus 41 0 Blue-and-white Flycatcher Cyanoptila 20 1 cyanomelana Common Stonechat Saxicola torquata 11 0 Mugimaki Flycatcher Ficedula mugi- 20 1 maki Total 75 16 (21)f 9 (12)f

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TABLE 2. Continued.

Sample Plasmodium Haemoproteus Family Region Host species size positivee positivee

Nectariniidaeb Myanmar Black-throated Sunbird Aethopyga 30 0 saturata Crimson Sunbird Aethopyga siparaja 20 0 Green-tailed Sunbird Aethopyga 10 0 nipalensis Little Spiderhunter Arachnothera 10 0 longirostra Streaked Spiderhunter Arachnothera 20 0 magna India Purple Sunbird Nectarinia sperata 40 2 Total 14 0 2 (15)f Paridaea Myanmar Great Tit Parus major 10 0 Green-backed Tit Parus monticolus 30 0 Sultan Tit Melanochlora sultanea 10 0 S. Korea Coal Tit Parus ater 21 0 Great Tit 16 12 1 Long-tailed Tit Aegithalos caudatus 40 0 Marsh Tit Parus palustris 21 0 Varied Tit Parus varius 74 0 Total 36 18 (50)f 1 (3) Passeridaed India House Sparrow Passer domesticus 21 4 2 Tree Sparrow Passer montanus 30 0 S. Korea Tree Sparrow 2 0 0 Total 26 4 (15) 2 (8) Phasianidaea Myanmar Himalayan Monal Lophophorus impeja- 10 0 nus Sclater Monal Lophophorus sclateri 10 0 Kalij Pheasant Lophura leucomelanos 10 0 S. Korea Japanese Quail Coturnix japonica 11 0 Ring-necked Pheasant Phasianus col- 41 0 chicus Total 8 2 (25) 0 Picidaea Myanmar Eurasian Wryneck Jynx torquilla 21 0 Greater Yellownape Woodpecker Picus 10 0 flavinucha Grey-headed Woodpecker Picus flavi- 12 0 0 nucha Yellow-crowned Woodpecker Dendro- 21 0 copos mahrattensis White-browed Piculet Sasia ochracea 30 0 Rufous Piculet Sasia abnormis 20 0 Common Goldenback Woodpecker Di- 10 0 nopium javanense S. Korea Grey-headed Woodpecker 2 1 0 Japanese Pygmy Woodpecker Picoides 20 0 kizuki Total 27 4 (15) 0 Psittacidaeb Myanmar Rose-ringed Parakeet Psittacula krameri 20 0 India Rose-ringed Parakeet Psittacula krameri 10 1 Alexandrine Parakeet Psittacula eupatria 21 0 Total 5 1 (20) 1 (20)

TABLE 2. Continued.

Sample Plasmodium Haemoproteus Family Region Host species size positivee positivee

Pycnonotidaeb Myanmar Black-crested Bulbul Pycnonotus mela- 30 1 nicterus Red-vented Bulbul Pycnonotus cafer 60 0 Grey-eyed Bulbul Iole propinqua 10 0 Alophoixus (Criniger auct.) spp. 4 0 0 India Red-vented Bulbul 10 3 2 Total 24 3 (12)f 3 (12) Paradoxorni- Myanmar Black-throated Parrotbill Paradoxornis 20 0 thidaea nipalensis Lesser Rufous-throated Parrotbill Para- 10 0 doxornis atrosuperciliaris S. Korea Vinous-throated Parrotbill Paradoxornis 91 0 webbianus Total 12 1 (8) 0 Sturnidaeb Myanmar Asian Pied Starling Sturnus contra 10 0 Black-collared Starling Sturnus nigri- 10 0 collis India Asian Pied Starling 4 0 1 Common Myna Acridotheres tristis 20 8 2 Bank Myna Acridotheres gingianianius 42 1 Jungle Myna Acridotheres fuscus 10 0 Total 31 10 (32) 4 (13) Sylviidaec Myanmar Common Tailorbird Orthotomus sutor- 51 0 ius Mountain Tailorbird Orthotomus cucu- 20 0 latus Thick-billed Warbler Acrocephalus ae- 11 0 don Rufous-faced Warbler Abroscopus albo- 10 0 gularis Blyth’s Leaf Warbler Phylloscopus reg- 20 0 uloides Yellow-browed Warbler Phylloscopus 30 1 inornatus Mountain Leaf Warbler Phylloscopus 20 0 trivirgatus Leaf Warbler Phylloscopus spp. 6 0 0 Grey-cheeked Warbler Seicercus polio- 61 0 genys Jungle Babbler Turdoides striatus 20 2 Black-chinned Babbler Stachyris pyr- 22 0 rhops Striated Grassbird Megalurus pryeri 22 0 Bush Warbler Cetti sp. 1 0 0 India Common Tailorbird 2 1 0 Yellow-eyed Babbler Chrysomma si- 42 1 nense S. Korea Yellow-browed Warbler 5 0 0 Arctic Warbler Phylloscopus borealis 10 1 Oriental Great Reed Warbler Acroce- 11 0 phalus orientalis Leaf Warbler 9 2 0 Total 57 13 (23)f 5 (9)

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TABLE 2. Continued.

Sample Plasmodium Haemoproteus Family Region Host species size positivee positivee

Timaliidaeb Myanmar Coral-billed Scimitar Babbler Pomator- 21 0 hinus ferrufinosus Eyebrowed Wren Babbler Napothera 10 0 epilepidotai Long-billed Wren Babbler Rimator ma- 21 0 laoptilus Golden Babbler Stachris chrysaea 31 0 Grey-cheeked Fulvetta Alcippe morri- 11 1 0 sonia Rufous-throated Fulvetta Alcippe rufo- 60 0 gularis Yellow-throated Fulvetta Alcippe cinerea 30 0 Rufous-winged Fulvetta Alcippe casta- 50 0 neceps Grey-throated Babbler Stachyris nigriceps 71 0 Spot-necked Babbler Stachyris striolata 21 0 Rufous-capped Babbler Stachyris ruficeps 40 0 Greater Necklaced Laughingthrush 32 0 Garrulax pectoralis Lesser Necklaced Laughingthrush Gar- 20 0 rulax monileger Scaly Laughingthrush Garrulax subunicolor 10 0 Striated Laughingthrush Garrulax 11 0 striatus White-crested Laughingthrush Garrulax 20 0 leucolophus Black-faced Laughingthrush Garrulax 10 0 affinis Chestnut-backed Laughingthrush Gar- 20 0 rulax nuchalis Chestnut-crowned Laughingthrush 40 0 Garrulax erythrocephalus Grey-sided Laughingthrush Garrulax 10 0 caerulatus Long-tailed Sibia Heterophasia pi- 51 0 caoides Puff-throated Babbler Pellorneum ruficeps 91 0 Pygmy Wren Babbler Pnoepyga pusilla 10 0 Red-faced Liocichla Liocichla phoenicea 10 0 Red-tailed Minla Minla ignotincta 10 0 Silver-eared Mesia Leiothrix argentauris 30 0 Streaked Wren Babbler Napothera 10 0 breavicaudata Wedge-billed Wren Babbler Sphenoci- 10 0 chla humei White-bellied Yuhina Yuhina zantholeuca 20 0 Black-chinned Yuhina Yuhina nigrimenta 10 0 White-naped Yuhina Yuhina bakeri 10 0 White-browed Scimitar Babbler Poma- 10 0 torhinus schisticeps White-throated Babbler Turdoides gularis 20 0 Yellow-bellied Warbler Abroscopus 10 0 superciliaris Yellow-eyed Babbler Chrysomma sinense 73 0 Total 35 14 (40) 0

TABLE 2. Continued.

Sample Plasmodium Haemoproteus Family Region Host species size positivee positivee Turdidaea Myanmar Long-tailed Thrush Zoothera dixoni 20 0 Lesser Shortwing Brachypteryx leu- 20 0 cophrys Blue Rock Thrush Monticola solitarius 10 0 Blue Whistling Thrush Myophonus 10 0 caeruleus S. Korea Grey Thrush Turdus cardis 10 1 Total 7 0 1 (14)

a Family shared between Myanmar and South Korea. b Family shared between Myanmar and India. c Family shared among Myanmar, India, and South Korea. d Family shared between India and South Korea. e n (% positive). f P # 0.001, Fisher’s exact test (among regions).

spp., respectively. Prevalence of parasites proteus were identified. Within the Plas- observed in families represented in a single modium tree (Fig. 2), there were four region was analyzed separately from fam- lineages (LIN 8, LIN 26, LIN 28, LIN 29) ilies shared among regions (Table 3). As shared between India and Myanmar, and found for shared families, the prevalence one lineage (LIN 15) shared between of Plasmodium spp. and Haemoproteus Myanmar and South Korea. In Haemo- spp. did not differ significantly among proteus (Fig. 3), a single lineage (LIN 1) these families. We tested the prevalence was shared between India and Myanmar. of parasites for families shared between The proportion of parasite lineages shar- two or more regions separately and found ing identical sequences in more than one significant differences in only a few cases host species occurs more frequently (Table 2). (x2515.1, P50.035) in the Plasmodium tree than in the Haemoproteus tree. This Microscopy and PCR detection may indicate higher rates of host-switching and reduced host-specificity in Plas- Of 183 blood smears collected in India, modium (see Figs. 2 and 3 for details on 61 individuals were positive for either host species). Plasmodium spp. or Haemoproteus spp. For 20 additional birds, short (91 bp) Of these, 22 (12%) Plasmodium and 39 sequences were obtained from primers F2/ (21.3%) Haemoproteus positive samples R2. These were used to identify parasite were detected by examination of blood genera but were not included in the smears. Results from blood smear exam- phylogenetic analysis. These results, how- ination and PCR where in agreement for ever, suggest the presence of the following only 98 (54%) of the 183 samples. Plasmodium lineages in host species in South Korea: LIN 7—great spotted wood- Phylogenetics pecker [Dendrocopos major], common We identified 241 infected birds and stonechat [Saxicola torquata], red throated obtained sequence for cyt b from 221 of pipit [Anthus cervinus]; LIN 10—bull- these. Within the 197 samples for which headed shrike [Lanius bucephalus], varied we had at least 256 bp of sequence, 34 tit [Parus varius], great tit [Parus major], lineages of Plasmodium and 41 of Haemo- coal tit [Parus ater], marsh tit [Parus

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TABLE 3. Prevalence of hematozoan parasites for avian families recorded within one region.

Plasmodium Haemoproteus Region Host family Species Sample size positive (n) positive (n) Myanmar Alcedidae Common Kingfisher Alcedo 61 0 atthis Strigidae Asian Barred Owlet Glauci- 41 0 dium cuculoides Oriental Scops Owl Otus sunia 20 0 Spotted Owlet Athene brama 11 0 Dicruridae Ashy Drongo Dicrurus leuco- 22 0 phaeus Bronzed Drongo Dicrurus ae- 10 0 neus Hair-crested Drongo Dicrurus 20 0 hottentottus Lesser Racket-tailed Drongo 20 0 Dicrurus remifer Common Green Magpie Cissa 20 0 chinensis Gold-billed Magpie Urocissa 10 0 flavirostus Aegithinidae Common Iora Aegithina tiphia 12 0 Prionopidae Common Woodshrike Te- 13 1 phrodornis pondicerianus Campephagidae Rosy Minivet Pericrocotus ro- 10 0 seus Scarlet Minivet Pericrocotus 30 0 flammeus Small Minivet Pericrocotus 31 0 cinnamomeus White-bellied Minivet Peri- 21 0 crocotus erythropygius Rhipiduridae White-browed Fantail Rhipi- 31 0 dura aureola White-throated Fantail Rhipi- 31 0 dura albicollis Sittidae Beautiful Nuthatch Sitta for- 20 0 mosa Chestnut-bellied Nuthatch 50 0 Sitta castanea India Cisticolidae Jungle Prinia Prinia sylvatica 10 0 Plain Prinia Prinia inornata 42 2 Ashy Prinia Prinia socialis 51 2 Grey-breasted Prinia Prinia 10 0 hodgsonii Prinia spp. 2 0 2 Streaked Fantail Warbler Cis- 20 0 ticola juncidis Zosteropidae Oriental White-eye Zosterops 72 1 palpebrosus Estrildidae Red Munia Estrilda amandava 31 11 0 Spotted Munia Lonchura 11 1 0 punculata White-throated Munia Lonch- 10 0 ura malabarica Black-headed Munia Lonch- 41 0 ura malaca atricapilla

TABLE 3. Continued.

Plasmodium Haemoproteus Region Host family Species Sample size positive (n) positive (n)

South Korea Emberizidae Black-faced Bunting Emberiza 94 0 spodocephala Chestnut Bunting Emberiza 71 3 rutila Rustic Bunting Emberiza rus- 20 0 tica Tristram’s Bunting Emberiza 21 1 tristrami Yellow-throated Bunting Em- 11 0 beriza elegans Laridae Black-tailed Gull Larus cras- 50 2 sirostris Laniidae Bull-headed Shrike Lanius 10 3 1 bucephalus Fringillidae Common Rosefinch Carpoda- 11 0 cus erythrinus Oriental Greenfinch Carduelis 71 1 sinica Scolopacidae Dunlin Calidris alpina 50 0 Red-necked Stint Calidris ru- 50 0 ficollis Anatidae Mallard Anas platyrhynchos 20 1 Spot-billed Duck Anas poeci- 50 0 lorhyncha

palustris], Daurian redstart [Phoenicurus DISCUSSION auroreus], leaf warbler [Phylloscopus sp.], black-billed magpie [Pica hudsonia]; LIN The overall prevalence (Haemoproteus 11—bull-headed shrike [Lanius bucepha- or Plasmodium) was higher in India lus], ring-necked pheasant [Phasianus col- (tropical zone); the highest number of chicus], yellow-browed warbler [Phyllosco- unique Haemoproteus lineages also was pus inornatus], great tit [Parus major]; LIN observed among birds sampled in India. 12—great tit; LIN 34—vinous-throated The lower parasite prevalence observed parrotbill [Paradoxornis webbianus]; LIN for Myanmar could be attributed to 35—great tit. Results suggested the pres- differences in habitat as most of the birds ence of one additional Haemoproteus from Myanmar were sampled from high lineage, LIN 41, from a black-billed altitudes where less exposure to vectors magpie (Pica hudsonia). may have occurred. On the other hand, the comparison between low-elevation Host and parasite diversity habitats of India and Myanmar (tropical The Shannon diversity indices indicate zone) and South Korea (temperate zone) that host diversity was higher in Myanmar showed no significant difference in prev- (5.8660.01) than in India (5.2060.03) or alence for either parasite. Our results are South Korea (5.2060.02); parasite diver- not entirely consistent with previous sity was lower in South Korea (3.9160.01) studies that have used PCR-based tech- as compared to Myanmar (4.3260.02) or niques. Durrant et al. (2006) found that India (4.3060.03). The host and parasite tropical zones had higher parasite preva- ratio was 82% in India followed by South lence than temperate zones, whereas Korea (75%) and Myanmar (73%). Ricklefs (1992) showed that temperate

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FIGURE 2. Relationships of Plasmodium lineages based on maximum likelihood using the model GTR+I+G. Each lineage represents host species and GenBank number.

birds had higher parasite prevalence. correspondence between PCR and mi- These differences may result from season- croscopy results for samples from India al differences in timing of sampling or was poor. This may have resulted from diagnostic techniques. In this study the a low-intensity peripheral parasitemia and

FIGURE 3. Relationships of Haemoproteus lineages based on maximum likelihood using the model GTR+I+G. Each lineage represents host species and GenBank number.

variation in diagnostic sensitivity and is blood and tissue samples; such differences consistent with results from the previous have not been apparent in our previous studies where blood smears were evaluat- studies (Ishtiaq et al., 2006; Pagenkopp, ed by both methods (Jarvi et al., 2002; 2006) using such samples. Richard et al., 2002). We are confident The prevalence of parasites differed at that the prevalence results from this study the regional level but not at host family are not biased by testing a combination of level. This finding is consistent with pre-

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vious studies (Hellgren, 2005; Durrant et The phylogenetic tree differentiates Hae- al., 2006). Temporal and spatial variation moproteus and Plasmodium lineages; a well- in parasite prevalence has been demon- supported topology is not necessary for our strated (Schall and Marghoob, 1995; analyses, but it clearly defines lineages Bensch and Akesson, 2003), and it is likely shared between different regions. There is that different parasite lineages are associ- some evidence of geographic structuring of ated with particular vector communities. parasite lineages in the Plasmodium tree as This factor may explain the differences in indicated in other studies (e.g., Beadell et the geographic distribution of parasite al., 2006). In our parasite phylogeny lineages at different sites. The Haemopro- (Fig. 2), more lineages of Plasmodium are teus tree shows regional clades, whereas shared between multiple host species than the Plasmodium clades are ‘‘scattered’’ are of Haemoproteus, which is indicative of between regions and host species. host switching (Bensch et al., 2000; Ricklefs Plasmodium and Haemoproteus are and Fallon, 2002; Waldenstro¨m et al., 2002; widely distributed blood parasites that Beadell et al., 2004) and supports Haemo- have been reported in many families of proteus as being relatively more host birds. Migrants can form a link for the specific than Plasmodium (Atkinson and transmission of parasites between tropical van Riper, 1991). and temperate resident birds, especially Variation in the abundance of dipteran among taxonomically similar hosts. Some vectors at a particular geographic location sharing of parasite lineages between is positively correlated with variation in resident and migratory songbirds has the prevalence of parasites in the avian been observed in Nigeria, indicating host community (Bennett and Cameron, parasite transmission between migrants 1974) and also may be related to variation and residents on the wintering grounds in the intensity of parasitic infection. Host (Waldenstro¨m et al., 2002). As a major habitat choice is known to influence wintering ground for hundreds of avian parasite load in host species as it can species, we would expect more shared affect the frequency of contact with flying parasite lineages between India and vectors of hematozoan parasites, which are Myanmar because migrants utilizing mainly associated with wet and closed these area originate from the same bio- habitats such as the forest canopy (Scott geographic region and share similar host and Edman, 1991). We did find a slight families. The Plasmodium phylogenetic difference in prevalence of Haemoproteus tree shows four shared lineages between inhigh-comparedwithlow-elevation these two regions (Fig. 1A). Birds mi- habitat in Myanmar and India but preva- grating to South Korea do not appear to lence of Plasmodium remained the same, use the same flyway as birds migrating to suggesting more exposure to ceratopogo- India and Myanmar, and this is reflected nids and hippoboscids at low elevations. by the few shared lineages between these Comparison between low-elevation habi- regions; only one Plasmodium lineage was tats in India and Myanmar may have been shared between Myanmar and South affected by the timing of sampling in two Korea (Fig. 1A). Although we found regions. Samples from India were collect- similar indices of parasite diversity in ed between May and June, which is the India and South Korea, the host-parasite peak breeding season for lowland resident ratio was higher in India, indicating more species, while winter (November–March) parasites infecting several host species was the sampling period in Myanmar and than in South Korea or Myanmar. India October in South Korea. Parasite load is had high parasite prevalence and highest known to increase in spring–summer number of unique parasite lineages as owing to the increased abundance of flying well. vectors at that time (Bennett and Ca-

meron, 1974; Atkinson and Van Riper, fected iiwi (Vestiaria coccinea). Parasitology 1991) and because higher levels of sexual 111: S59–S69. BEADELL, J. S., E. GERING,J.AUSTIN,J.P.DUMBA- steroid hormones are circulating in the CHER,M.A.PEIRCE,T.K.PRATT,C.T.ATKINSON, bird’s blood, which in general depresses AND R. C. FLEISCHER. 2004. Prevalence and the immune system and allows parasites to differential host-specificity of two avian blood survive (Wedekind and Følstad, 1994; parasite genera in the Australo-Papuan region. Saino et al., 1995). Molecular Ecology 13: 3829–3844. ———, F. ISHTIAQ,R.COVAS,M.MELO,B.H. The Asian region harbors a diverse WARREN,C.T.ATKINSON,S.BENSCH,G.R. community of avian hematozoan lineages GRAVES,Y.V.JHALA,M.A.PEIRCE, A.R.RAHMANI, that were distributed among 41% of the D. M. FONSECA, AND R. C. FLEISCHER. 2006. birds sampled in this study. Prevalence Global phylogeographic limits of Hawaii’s avian malaria. Proceeding of Royal Society London B. varied between regions but not at the host 273: 2935–2944. family level. An in-depth study on the BENNETT, G. F., AND M. CAMERON. 1974. Seasonal distribution of vector communities and prevalence of avian hematozoa in passeriform their relationship to hematozoa in these birds of Atlantic Canada. Canadian Journal of regions would be useful and may provide Zoology 52: 1259–1264. BENSCH, S., AND S. AKESSON. 2003. Temporal and some insight into the regional distribution spatial variation of Haematozoans in Scandina- of specific hematozoan lineages. vian willow warblers. Journal of Parasitology 89: 388–391. ACKNOWLEDGMENTS ———, M. STJERNMAN,D.HASSELQUIST,O.OSTMAN, B. HANSSON,H.WESTERDAHL, AND R. T. Part of this study was funded by a National PINHEIRO. 2000. Host specificity in avian blood Institutes of Health grant (1R01GM063258). parasites: A study of Plasmodium and Haemo- We would like to thank the Ministry of proteus mitochondrial DNA amplified from Environment and Forests, Government of birds. Proceedings of the Royal Society of India; Myanmar Forestry Ministry, Nature London B 267: 1583–1589. and Wildlife Conservation Division (Myanmar BERGER, A. J. 1981. Hawaiian birdlife. 2nd Edition. Collection and Export Permit 11853-55/ University Hawaii Press, Honolulu, Hawaii, 260 96, UYin-Office/TWMC/2303/2002, SI/4697/ pp. 2004) for permits to catch birds for blood and CAUM, E. L. 1933. The exotic birds of Hawaii. tissue samples. The Smithsonian expedition to Occasional Papers of the Bernice P. Bishop South Korea was supported by a grant from Museum, Honolulu, Hawaii 10: 1–55. the U.S. Department of Defense–Legacy Re- DURRANT, K. L., J. S. BEADELL,F.ISHTIAQ,G.R. source Management Program (DACA87-03- GRAVES,S.L.OLSON,E.GERING,M.PEIRCE,C. H-0006). We thank C. McIntosh, K. Durrant, ATKINSON,C.M.MILENSKY,B.K.SCHMIDT,C. and D. K. Sharma for facilitating laboratory GEBHARD, AND R. C. FLEISCHER. 2006. Avian analyses. We would also like to thank R. Jakati, malaria in South America: A comparison of A. Choudhury, R. Bharagava, H. Singha, K. temperate and tropical zones. Ornithological Lahkar, B. P. Lahkar, and S. Barua for help in Monographs 60: 98–111. organizing field camps in Assam, and Cho Sok FALLON, S. M., R. E. RICKLEFS,B.L.SWANSON, AND Hun, 51 Fighter Wing, Osan, Air Base for E. BERMINGHAM. 2003. Detecting avian malaria: organizing field work in South Korea. An improved PCR diagnostic. Journal of Para- sitology 89: 1044–1047. LITERATURE CITED ———, E. BERMINGHAM, AND R. E. RICKLEFS. 2005. Host specialization and geographic localization ATKINSON, C. T., AND C. VAN RIPER III. 1991. of avian malaria parasites: A regional analysis in Pathogenicity and epizootiology of avian haema- the Lesser Antilles. American Naturalist 165: tozoa: Plasmodium, Leucocytozoon, and Haemo- 466–480. proteus. In Bird-parasite interactions: Ecology, GARNHAM, P. C. C. 1966. Malaria parasites and other evolution and behaviour, J. E. Loye and M. Zuk haemosporidia. Blackwell Scientific, Oxford, (eds.), Oxford University Press, New York, UK, 1114 pp. pp. 19–48. HELLGREN, O. 2005. The occurrence of haemospor- ———, K. L. WOODS,R.J.DUSEK,L.S.SILEO, AND idian parasites in the Fennoscandian bluethroat W. M. IKO. 1995. Wildlife disease and conser- (Luscinia svecica) population. Journal of Orni- vation in Hawaii: Pathogenicity of avian malaria thology 146: 55–60. (Plasmodium relictum) in experimentally in- ISHTIAQ, F., J. S. BEADELL,A.J.BAKER,A.R.

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