Research Article Prevalence and Diversity of Avian ... · Research Article Prevalence and Diversity of Avian Haematozoan Parasites in Wetlands of Bangladesh RubayetElahi, 1,2 AusrafulIslam,

Research ArticlePrevalence and Diversity of Avian Haematozoan Parasites inWetlands of Bangladesh

Rubayet Elahi12 Ausraful Islam1 Mohammad Sharif Hossain1

Khaja Mohiuddin1 Andrea Mikolon1 Suman Kumer Paul1 Parviez Rana Hosseini3

Peter Daszak3 and Mohammad Shafiul Alam1

1 International Centre for Diarrhoeal Disease Research Bangladesh (icddrb) Dhaka 1212 Bangladesh2Department of Neurobiology and Developmental Sciences University of Arkansas for Medical Sciences (UAMS)Little Rock AR 72205 USA

3 EcoHealth Alliance New York NY 10001 USA

Correspondence should be addressed to Mohammad Shafiul Alam shafiulicddrborg

Received 30 June 2013 Revised 29 October 2013 Accepted 29 October 2013 Published 21 January 2014

Academic Editor D S Lindsay

Copyright copy 2014 Rubayet Elahi et al This is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

The parasites of genera Haemoproteus Plasmodium and Leucocytozoon are well-known avian haematozoa and can cause declinedproductivity and high mortality in wild birds The objective of the study was to record the prevalence of haematozoan parasites ina wide range of wetland birds in Bangladesh Six species of Haemoproteus seven species of Plasmodium one unidentified speciesof Leucocytozoon and one unidentified microfilaria of the genus Paronchocerca were found Data on the morphology size hostsprevalence and infection intensity of the parasites are provided The overall prevalence among the birds was 295 (95 out of 322birds) Of those 132 (42 of 319) of birds were infected withHaemoproteus spp 151 with Plasmodium spp (48 of 319) and 06with Leucocytozoon spp (2 of 319) Two birds were positive for both Haemoproteus sp and Plasmodium sp A single resident birdArdeola grayii was found positive for an unidentified microfilaria Prevalence of infection varied significantly among different birdfamilies Wild birds of Bangladesh carry several types of haematozoan parasites Further investigation with a larger sample sizeis necessary to estimate more accurately the prevalence of haematozoan parasites among wild birds as well as domestic ducks forbetter understanding of the disease ecology

1 Introduction

Haemoproteus Plasmodium and Leucocytozoon are well-known genera of avian haematozoa [1ndash3] Biting midgeslouse flies black flies and mosquitoes are the vectors thattransmit these parasites [3ndash5]Though the importance of birdhaematozoans remains undervalued declined productivity ofbirds and highmortality due to these parasitic infections havebeen reported [3] Most infections with parasites of genusHaemoproteus produce subclinical infections Liver spleenkidneys and gizzards become enlarged [6ndash8] Haemoproteuscan also parasitize in the lungs [9] In some birds anemiaanorexia and depression have also been reported [3] Par-asites of the Plasmodium genus cause avian malaria whichhas sublethal effects on host fitness The most significant

impact is long-term effect on the reproductive system ofthe host causing population decrease [10] Leucocytozoontypically causes anemia and enlargement of liver and spleen[3 7] Earlier research from South and Southeast Asia hasreported the prevalence and geographical distribution ofavian haematozoa [11ndash15] In 2005 five species ofPlasmodiumgenus one of Haemoproteus genus and two unidentifiedmicrofilariae of different birds were reported from Pakistan[16] Distributions of Haemoproteus spp and Plasmodiumspp in rock pigeons (Columba livia) from different areas ofIndia have been described with their prevalence and seasonalvariations [17]

Of 690 known bird species of Bangladesh 380 areresident and 310 are migratory (209 winter visitors 11summer visitors and 90 species vagrants) [18] To date

Hindawi Publishing CorporationJournal of Parasitology ResearchVolume 2014 Article ID 493754 12 pageshttpdxdoiorg1011552014493754

2 Journal of Parasitology Research

no information is available on haematozoan parasites inwild birds of Bangladesh although Leucocytozoon spp fromdomestic ducks [6] and Haemoproteus spp in domesticpigeons [7] have been reported recently As part of asurvey for influenza virus in wild birds this study wasconducted to identify the haematozoan parasites of var-ious wild birds from different areas of Bangladesh Theobjective of the study was to record the prevalence ofhaematozoan parasites in a wide range of wetland birdsMorphology of parasites and intensity of invasion were alsorecorded

2 Materials and Methods

A total of 322 wild birds were studied belonging to 48 species(15 families and four orders) from January 2011 to March2011 The birds were sampled from two wetland sites inBangladesh Hakaluki haor (N 21∘3310158401015840698 E 091∘5110158401015840682) inSylhet and Moulvibazar districts (212 birds) and Tanguarhaor (N 25∘087941015840 E 091∘040881015840) in Sunamganj district(110 birds) (Figure 1) Hakaluki haor and Tanguar haor areseasonal water bodies located in northern Bangladesh whichdry up during winter when they provide habitat for residentandmigratorywild birdsMist nets andnoose trapswere usedfor bird capicture Blood was drawn from jugular or tarsalvein of the bird Species identification and age determinationwere made using the description given by Grimmett et al[19] All of the birds were marked using metal rings withunique identification numbers at the tarsus and released aftersampling at the site of capture

From each bird typically three (but sometimes two) thinblood smears were prepared on clean grease-free slides Allslides were fixed in absolute methanol for one minute in thefield The fixed smears were then stained with 20 Giemsastain and were observed under 400x and 1000xmagnificationby skilled parasitologists Identification of the haematozoanswas performed using the taxonomic description of Valkiunas[3] and Bartlett [4] If any parasite was found within 100fields of microscopic observation the slide was consideredas positive otherwise it was considered as negative Allparasites in 100 microscope fields at 1000x magnificationwere counted to calculate the intensity of invasion of theparasites The nuclear displacement ratio (NDR) an index oflateral displacement of the erythrocyte nucleus by the parasite[20] was measured following the description of Valkiunas[3] Slides of each parasite identified up to species levelhave been deposited in the US National Parasite Collection(USNPC) Beltsville MD USA (accession numbers are in thesupplementary file 1 see Supplementary Material availableonline at httpdxdoiorg1011552014493754)

The birds were divided into 2 groups migratory andresident birds All measurements in the text and the tablesare presented in micrometers and given as mean plusmn stan-dard deviation Intensity of invasion was calculated per 100microscopic fields Statistical Package for the Social Sciences(SPSS) v 17 (SPSS Inc USA) was used to analyze the data Atwo-tailed Fisherrsquos exact test was used to find the correlationof prevalence within bird families and parasite genus To

indicate statistical significance a 119875 value less than 005 wasused

3 Results

31 Prevalence and Intensity of Infection The overall preva-lence of infection of the birds studied was 295 (95322birds) Among those 132 (42319) prevalence of infectionwas recorded for Haemoproteus spp 151 for Plasmodiumspp (48319) and 06 for Leucocytozoon spp (2319) Twobirds were positive for parasites of both Haemoproteus andPlasmodium genera A single slide was positive for unidenti-fiedmicrofilariae of genus Paronchocerca fromArdeola grayiia resident bird (Table 1)

The prevalence of infection for the three genera variedconsiderably amid different families of birds (Table 1) Amongthe families with sufficient sample size (119899 gt 20) thehighest prevalence was found in the family Laridae 441(15 of 44 birds) for genus Haemoproteus in the familyScolopacidae 208 (5 of 24) for Plasmodium genus in thefamily Dendrocygnidae 23 (1 of 43) for Leucocytozoongenus

The intensity of invasion varied across different parasitegenera For parasites of Haemoproteus genus it ranged from2 to 43 mostly being below 20 parasites per 100 microscopicfields The lowest intensity of invasion for parasites of Plas-modium genus was 2 while the highest was 18 parasites per100 microscopic fields mostly being less than 10 Parasites ofLeucocytozoon genus had 4-5 parasites per 100 microscopicfields while the only bird infected withmicrofilariae had only3 parasites per 100 microscopic fields

In the present study 724 (119899 = 233) of the birds studiedwere migrant and 276 (119899 = 89) were resident amongthese 335 (119899 = 78) of migrant birds and 191 (119899 = 17)of resident birds were positive for any of the parasites ofgenus Haemoproteus Plasmodium or Leucocytozoon Theseparasites weremore commonly found inmigratory birds (119875 lt005) 159 (119899 = 37) of migrant birds and 57 (119899 = 5) ofresident birds were positive for Haemoproteus genus while168 (119899 = 39) of migrant birds were positive for Plasmodiumgenus in contrast to 103 (119899 = 9) of resident birdsMigratory birds were significantly preferred by parasites ofHaemoproteus (119875 lt 005) but for parasites of Plasmodiumthere was no significant preference One migrant bird andone resident bird were found positive for parasites of genusLeucocytozoon spp One of each migrant and resident birdhad mixed infection by parasites of genera Haemoproteusand Plasmodium There was no significant difference in theinfection rates among the study sites

32 Description of Species Six species of Haemoproteus andseven species of Plasmodium were identified Haemopro-teus parasites from four birds belonging to two differentspecies were identified up to subgenus level subgenus Para-haemoproteus Plasmodium parasites from five birds of threespecies were identified only up to subgenus level subgenusHaemoamoeba and subgenus Giovannolaia All the Leucocy-tozoon (119899 = 2) parasites were identified up to genus level

Journal of Parasitology Research 3

N

00

30

6

12

Decimal degrees

Figure 1 Study sites

A single bird was found to be infected with unidentifiedmicrofilarae species of genus Paronchocerca

321 Genus Haemoproteus Kruse 1890

(1) Haemoproteus (Parahaemoproteus) pastoris Mello 1935

Morphology A single bird was infected with the macroga-metocyte of H pastoris The outline of the gametocytes wasamoeboid adhering to the erythrocyte nucleus and envelopefilling the erythrocyte up to their poles They displacedthe erythrocyte nucleus slightly The measurement of themacrogametocytes was 14575 plusmn 04 120583m times 412 plusmn 03 120583mThe nucleus of the macrogametocyte was compact and insubcentral position measuring 315 plusmn 002 120583m times 2575 plusmn01 120583m 9 to 17 small roundish pigment granules were seenrandomly scattered in the cytoplasm The NDR was 05 plusmn02 Invasion intensity was found to be 17 parasites per 100microscopic fields

Host Sturnus contra (Asian Pied Starling)

Locality Hakaluki haor (119899 = 1)

(2) Haemoproteus (Parahaemoproteus) scolopaci Galli-Valerio 1929

Morphology A single bird was found to be infected withthe macrogametocyte of H scolopaci The gametocyte wasoval with amoeboid outline and was slightly appressedwith the host erythrocyte envelope and nucleus completelyencircling the erythrocyte nucleus and occupying all availablecytoplasmic space in the erythrocytes The nucleus wasslightly displaced laterally and the host cell was hypertro-phied The NDR was 066 plusmn 003 The measurement ofthe gametocyte was 14575 plusmn 147 120583M times 3575 plusmn 0515 120583MParasite nucleus was centrally situated with the measurementof 309 plusmn 03 120583M times 257 plusmn 003 120583M The cytoplasm ofthe gametocyte was homogenous in appearance and con-tained small roundish pigment granules The intensity ofinvasion was found to be 13 parasites per 100 microscopicfields

Host Charadrius dubius (Little Ringed Plover)


(3) Haemoproteus (Parahaemoproteus) plataleaeMello 1935


Table1Num

bero

fthe

exam

ined

birdstheirm

igratio

nstatus

andbloo

dparasitep

revalence(in

)indifferent

bird

families

andspecies

Birdsfam

ilies

species

Migratio

nsta

tus

Num

bero

fexamined

birds

Genus

Haemoproteus

Genus

Plasmodium

Genus

Leucocytozoon

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Anatid

ae140

179

164

07

Anas

acuta

M32

94Hgreineri(2)

Hnettio

nis

188

P(G

)circum

flexum

(2)

P(H

)lutzi

P(H

)relictum

(2)

P(H

aemam

oeba)sp

Anas

clypeata

M3

667

P(H

)relictum

(2)

Anas

crecca

M4

250

Leucocytozoon

sp

Anas

falca

taM

1An

aspenelope

M2

500

P(H

)relictum

Anas

querquedula

M7

286

P(H

)relictum

P(H

aemam

oeba)sp

Anas

strepera

M12

83

Hgreineri

250

P(H

)lutzi

P(H

)relictum

P(H

aemam

oeba)sp

Aythya

ferina

M10

500

Hgreineri(2)

Mixed

Hgreineriand

Hnettio

nis(1)

Hnettio

nis(2)

100

P(G

)circum

flexum

Aythya

fuligula

M26

38

Hgreineri

154

P(G

)circum

flexum

(2)

P(H

)relictum

(2)

Aythya

nyroca

M14

429

Hgreineri(3)H

nettio

nis

(3)

71P(H

aemam

oeba)sp

Netta

rufin

aM

4750

Hgreineri(2)

H(Pa

rahaem

oproteus)sp

250

P(H

)relictum

Netta

puscorom

andelianu

sR

9111

P(G

)circum

flexum

Tadornafer

ruginea

M13

231

Hgreineri(3)

77P(H

)relictum

Tadornatadorna

M3

1000

Dendrocygnidae

4370

93

23

Dendrocygna

bicolor

R36

83

H(Pa

rahaem

oproteus)sp

(3)

83

P(G

)polarae

P(H

)relictum

(2)

28

Leucocytozoon

sp

Dendrocygna

javanica

R7

143

P(G

)circum

flexum

Accipitridae

1Circus

mela

noleu

cos

M1


Table1Con

tinued

Birdsfam

ilies

species

Migratio

nsta

tus

Num

bero

fexamined

birds

Genus

Haemoproteus

Genus

Plasmodium

Genus

Leucocytozoon

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Ardeidae

1520

0Ardeacin

erea

R1

Ardeolagrayii

R8

Bubu

lcusibis

R1

Egretta

garzetta

R1

Mesophoyx

interm

edia

R2

1000

P(G

)polarae

Nyctico

raxnyctico

rax

R2

500

P(H

)relictum

Charadriidae

8125

125

Charadriu

sdubius

R6

167

Hscolopaci

Vanellu

scinereus

M2

500

P(H

)relictum

Jacanidae

4Hydrophasians

chiru

rgus

R4

Larid

ae34

441

88

Chlid

oniash

ybrid

usM

1La

rusb

runn

icephalus

M7

286

P(H

)relictum

(2)

Larusridibun

dus

M26

577

Hplatalea

e(15)

39

P(G

)lophu

rae

Phalacrocoracidae

1Ph

alacrocoraxcarbo

M1

Podicipedidae

4250

Podiceps

cristatus

M2

500

P(G

iovann

olaia)

sp

Tachybaptusrufi

collis

R2

Rostr

atulidae

250

0Ro

stratulabenghalen

sisM

2500

P(H

)relictum

Scolop

acidae

2420

8Ca

lidris

alpina

M2

Calidris

minuta

M10

Calidris

temminckii

M1

Gallin

agoste

nura

M1


Table1Con

tinued

Birdsfam

ilies

species

Migratio

nsta

tus

Num

bero

fexamined

birds

Genus

Haemoproteus

Genus

Plasmodium

Genus

Leucocytozoon

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Limnodrom

oussem

ipalmatus

M1

Tringa

stagnatilis

M2

500

P(H

)relictum

Tringa

totanu

sM

7571

P(H

)relictum

(4)

Rallidae

38184

Fulicaatra

M32

156

P(H

)lutzi(3)

P(H

)relictum

(2)

Gallicrexcin

erea

R2

Gallin

urachloropu

sM

11000

P(H

)lutzi

Porphyrio

porphyrio

R3

333

P(H

)lutzi

Sturnidae

250

0Sturnu

scontra

R2

500

Hpastoris

Sylviid

ae2

Acrocephalus

stentoreus

M1

Megalurus

palustris

R1

Eurosto

podidae

1Eu

rosto

podu

smacrotis

R1

Total

319

132

151

06

Migratio

nsta

tusMm

igrantR

resident


(a) (b)

Figure 2 (a) Macrogametocyte of H plataleae (b) Macrogametocyte of H nettionis

Morphology Both macro- and microgametocytes of Hplataleaewere found in 17 birds of two speciesTwobirdswereinfected with both gametes Both the gametocytes markedlyencircled the erythrocyte nucleus and appressed closely withthe host cell envelope

The macrogametocytes were dumbbell-shaped with ameasurement of 155 plusmn 165 120583 M times 483 plusmn 088 120583 M (Fig-ure 2(a)) The nucleus of the parasite was in median positionwith the measurement of 437 plusmn 104 120583M times 346 plusmn 095 120583Mfrequently laid free in the cytoplasm The cytoplasm wascoarsely granular with 17 to 49 (34plusmn 906) small roundish pig-ment granules scattered randomly in the cytoplasm Infectederythrocytes were slightly hypertrophied Invasion intensityper 100 microscopic fields was 4 to 28 The NDR was 04 plusmn025

The microgametocytes were dumbbell-shaped withamoeboid outline and measured 1245 plusmn 250 120583M times 450 plusmn078120583M The nucleus of the parasite was in submedianposition and was also laid free in the cytoplasm likemacrogametocyte and measured 360 plusmn 073120583M times 283 plusmn07 120583M The cytoplasm contained more pigment granulesthan macrogametocytes 10 to 41 microgametocytes wereseen per 100 microscopic fields The NDR was 04 plusmn 001

Hosts Larus ridibundus (Black headed gull) and Ardeolagrayii (Indian pond heron)

Locality Hakaluki haor (119899 = 12) Tanguar haor (119899 = 5)

(4) Haemoproteus (Parahaemoproteus) greineri BennettTurner and Whiteway 1984

Morphology A total of 15 birds of seven species were foundto be infected with H greineri by both macro- and microga-metocytes Both gametocytes were dumbbell-shaped Thenucleus of the host erythrocytes was enclosed slightly by thegametocytes Some host cells were hypertrophied

The macrogametocytes were closely appressedwith both host erythrocyte nucleus and envelope

The macrogametocytes measured 1510 plusmn 102 120583M times 447 plusmn063 120583MThe nucleus was compact comparatively small andsubmedian in position measuring 474 plusmn 154 120583M times 314 plusmn092 120583M 18ndash32 (24 plusmn 54) small roundish pigment granuleswere randomly scattered throughout the parasite cytoplasmThe NDR was 066 plusmn 014 The invasion intensity rangedfrom 11 to 39 parasites per 100 microscopic fields

The microgametocytes were amoeboid in outline and1245 plusmn 258120583M times 374 plusmn 082 120583M in measurement and wereloosely appressedwith erythrocyte nucleus and envelopeThenucleus of themicrogametocyte was submedian ormedian inposition and measured 272 plusmn 063 120583M times 171 plusmn 038 120583M 16 to19 small (1785 plusmn 254 120583M) oval pigment granules were seenscattered randomly on the cytoplasm making it granular inappearance or sometimes were aggregated in dense clumpsat the end of the parasite The NDR was 07 plusmn 013 3 to 42parasites were seen per 100 microscopic fields

Hosts Aythya fuligula (Tufted Duck) Aythya nyroca (Ferrug-inous Pochard) Netta rufina (Red-Crested Pochard) Aythyaferina (CommonPochard)Anas strepera (Gadwall)Tadornaferruginea (Ruddy Shelduck) and Anas acuta (NorthernPintail)


(5) Haemoproteus (Parahaemoproteus) nettionis Johnstonand Cleland 1909

Morphology A total of seven birds belonging to three specieswere infected with both macro- and microgametocytes of Hnettionis The cytoplasm of both gametes was homogenousin form with occasionally some minute vacuoles The game-tocytes almost completely encircled the erythrocyte nucleusand markedly displaced laterally Host cell was hypertro-phied

The macrogametocyte was dumbbellshaped with mea-surement of 1575 plusmn 268 120583M times 485 plusmn 064 120583M (Figure 2(b))The macrogametocyte was closely appressed both to thenucleus and the envelope of erythrocytes The nucleus of


the parasite was compact and median in position withmeasurement of 45 plusmn128120583M times 333 plusmn 028 120583M Pigmentgranules were roundish and ranged from 13 to 28 (2025 plusmn618) The NDR was 038 plusmn 005 Invasion intensity rangedfrom 2 to 35 parasites per 100 microscopic fields

The microgametocytes were also dumbbell-shaped with12745 plusmn 48 120583M times 43 plusmn 026 120583M measurement The parasitenucleus was submedian in position with 27 plusmn 058120583M times 207plusmn 05 120583Mmeasurement The microgametocytes have 17 to 19(16 plusmn 1) small roundish pigment granules The NDR was 04plusmn 008 The invasion intensity was 4 to 16 parasites per 100microscopic fields

Hosts Aythya ferina (Common Pochard) Aythya nyroca(Ferruginous Pochard) and Anas acuta (Northern Pintail)


(6) Haemoproteus (Parahaemoproteus) sp

Morphology Parasites of genus Haemoproteus of four birdsof two species were identified up to subgenus level only Allof the parasites were macrogametocytes and were of ovalshapeThe gameteswere laid closelywith the host erythrocyteenvelope The dimension was 12785 plusmn 147 120583M times 3595 plusmn0515 120583MThe nucleus was oval and measured 463 plusmn 09 120583Mtimes 256 plusmn 05 120583M It was laid in the outer periphery of themacrogametocyte The cytoplasm was coarsely granular with25 to 29 roundish pigment granules Host erythrocyte cellwas slightly hypertrophied and the erythrocyte nucleus wasslightly displaced laterally The NDR was 09 plusmn 03 Theinvasion intensity was 3 to 9 per 100 microscopic fields

Hosts Dendrocygna bicolor (Fulvous Whistling Duck) andNetta rufina (Red Crested Pochard)


322 Genus Plasmodium Marchiafava and Celli 1885

(1) Plasmodium (Haemoamoeba) relictum Grassi and Feletti1891

Morphology A total of 25 birds belonging to 17 species wereinfected with P relictum One was found to be infected withthe microgamete and trophozoite of P relictum and otherswere infected with only trophozoites The microgamete waslobulated with oval pigment granules andmarkedly displacedthe erythrocyte nucleus The pigment granules were looselyclumped in the cytoplasm and the granules were 358 plusmn005120583M times 206 plusmn 003 120583M in measurement The invasionintensity was 5 parasites per 100 microscopic fields for themicrogamete

Some trophozoites were oval in shape and some werelobulated (Figure 3(a)) The trophozoites looked like solidbodies with relatively large nucleus Roundish pigmentgranules were randomly dispersed in the cytoplasm Themeasurements of the trophozoites were 354 plusmn 071120583M times

237 plusmn 07120583M Invasion intensity ranged from 2 to 19 per 100microscopic fields

Hosts Rostratula benghalensis (Greater Painted Snipes)Anas clypeata (Northern Shoveler) Anas penelope (EurasianWigeon) Aythya fuligula (Tufted Duck) Gallinura chloro-pus (Common Moorhen) Larus brunnicephalus (BrownHeaded Gull) Anas querquedula (Gargeney) Tringa stag-natilis (Marsh Sandpiper) Fulica atra (Common Coot)Tringa totanus (Common Redshank) Dendrocygna bicolor(Fulvous Whistling Duck) Anas acuta (Northern Pintail)Todorna ferruginea (Ruddy Shelduck) Nycticorax nycticorax(Black-Crowned Night Heron) Vanellus cinereus (Grey-headed Lapwing) Netta rufina (Red-Crested Pochard) andAnas strepera (Gadwall)

Locality Hakaluki Haor (119899 = 13) Tanguar Haor (119899 = 12)

(2) Plasmodium (Haemoamoeba) lutzi Lucena 1939

Morphology A total of nine birds belonging to seven specieswere found to be infected with P lutzi Trophozoites situatedin the subpolar or in polar position of the erythrocytewere somewhat oval in shape with measurements of 367plusmn 134 120583M times 25 plusmn 07 120583M (Figure 3(b)) The nucleus wascomparatively large Roundish to somewhat oval pigmentgranules were seen to be clumped near the margin of thetrophozoites When vacuoles were present they were fewin number measuring 103 plusmn 002 120583M Infected erythrocytewas deformed and the erythrocyte nuclei were displacedmarkedly Invasion intensity ranged from 2 to 12 parasites per100 microscopic fields

Hosts Fulica atra (Common Coot) Gallinura chloropus(CommonMoorhen)Anas strepera (Gadwall)Ardeola grayii(Indian PondHeron) Larus ridibundus (Black-HeadedGull)Porphyrio porphyrio (Purple swamp hen) and Anas acuta(Northern Pintail)


(3) Plasmodium (Giovannolaia) polare Manwell 1934

MorphologyThree birds belonging to two species were foundto be infected with P polarae In two birds somewhat ovalshaped trophozoites were observed with a measurementof 33 plusmn 034 120583M times 335 plusmn 11 120583M Several oval pigmentgranules were seen clumped in the cytoplasm Vacuoles inthe cytoplasm when present were plentifulThe trophozoiteswere in subpolar or polar position occupying less than halfof the erythrocyte Invasion intensity was 4 for one bird and7 parasites per 100 microscopic fields for the other bird

Both types of gametes were seen in one bird andwere lateral to the erythrocyte nucleus in position Ovalmacrogamete with coarse oval pigment granules was seenNo vacuoles were seen The macrogamete measured 3575 plusmn024 120583Mtimes 412plusmn 01 120583M Invasion intensitywas 6 parasites per100 microscopic fields Microgamete was elongated in shapeIt has oval pigment granules dispersed in the cytoplasm Themicrogamete measured 721 plusmn 004 120583M times 309 plusmn 023 120583M


(a) (b)

Figure 3 (a) Trophozoite of P relictum (b) Trophozoite of P lutzi

Hosts Mesophoyx intermedia (Intermediate Egret) and Den-drocygna bicolor (Fulvous Whistling Duck)


(4) Plasmodium (Giovannolaia) circumflexum Kikuth 1931

Morphology A total of seven birds of five species wereinfected with P circumflexum Trophozoites were oval inshape measuring 35 plusmn 163 120583M times 284 plusmn 08 120583M Pigmentgranules somewhat roundish to oval in shape were seenclumped at the edge of the trophozoites and sometimesdispersed in the cytoplasm Several vacuoles were seen withan average diameter of 103 plusmn 001 120583M Invasion intensityranged from 5 to 18 parasites per 100 microscopic fields

Hosts Nettapus coromandelianus (Cotton Pygmy Goose)Aythya fuligula (Tufted Duck) Aythya ferina (CommonPochard) Anas acuta (Northern Pintail) and Dendrocygnajavanica (Lesser Whistling Duck)


(5) Plasmodium (Giovannolaia) lophurae Manwell 1934

Morphology A single bird was found to be infected withP lophurae Trophozoites were highly amoeboid in outlinemeasuring 309 plusmn 002120583M times 206 plusmn 004 120583M Parasite nucleuswas large with plentiful cytoplasm Oval pigment granulesare clumped in the cytoplasm Several vacuoles were seenin trophozoites with average diameter of 103 plusmn 001 120583MIntensity of invasionwas 7 parasites per 100microscopic field

Host Larus ridibundus (Black-Headed Gull)


(6) Plasmodium (Haemoamoeba) sp Grassi and Feletti 1890

Morphology Four birds of four different species were infectedwith trophozoites of Plasmodium genus They were not

identified up to species level due to the small number of para-sites but they were identified up to subgenusHaemoamoebaIn general the trophozoites were elongatedwith oval pigmentgranules and dispersed in the cytoplasm measuring 33 plusmn08 120583M times 26 plusmn 02 120583MThey contained several vacuoles witha diameter of 103 plusmn 001 120583M

Hosts Anas acuta (Northern Pintail) Aythya nyroca (Fer-ruginous Pochard) Anas querquedula (Garganey) and Anasstrepera (Gadwall)


(7) Plasmodium (Giovannolaia) sp Corradetti Garnham andLaird 1963

Morphology A single bird was infected with trophozoites ofPlasmodium genus This was identified up to Subgenus Gio-vannolaia The merozoites were elongated with oval pigmentgranules measuring 515 plusmn 002 120583M times 2575 plusmn 02 120583M It didnot contain vacuoles

Host Podiceps cristatus (Great Crested Grebe)

Locality Tanguar haor (119899 = 1)

323 Genus Leucocytozoon sp Berestneff 1904

Morphology Only two birds of two species were positive forLeucocytozoon sp (Figure 4) They were very few in numberAll of them were macrogametocytes They measured 108 plusmn134 120583M times 87 plusmn 143 120583MThe dark blue cytoplasm with manysmall vacuoles appeared to be coarsely granulated Smallround organelles resembling the pigment granules were seenThe invasion intensitywas 4 to 5 parasites per 100microscopicfields

Hosts Anas crecca (Common Teal) and Dendrocygna bicolor(Fulvous Whistling Duck)



Figure 4 Macrogametocyte of Leucocytozoon sp

Figure 5 Microfilariae of genus Paronchocerca

324 Microfilariae One unidentified species of microfilariawas reported from the blood of Ardeola grayii (Indian PondHeron) It was caught fromHakaluki haorThemicrofilaria isof Paronchocerca genus (Figure 5)

The worm was sheathed long and cylindrical with lengthof 196 um and width of 35 120583mThe tail was bluntly roundedNuclei extend to posterior end of body are loosely arrangedIntensity of invasion was 3 microfilariae per 100 microscopicfields

4 Discussion

In this study six species of Haemoproteus seven speciesof Plasmodium an unidentified species of Leucocytozoonand an unidentified microfilarial species of genus Paron-chocerca were reported in wild birds from different sites ofBangladesh Although there are reports of Leucocytozoon spand Haemoproteus sp in domestic pigeons [7] and ducks[6] in Bangladesh but a comprehensive report on avianhaematozoans is lacking The findings of this study providea comprehensive report

According to the list of avian parasites prepared byBennett [1] and Valkiunas [3] one bird can be invadedby several congeneric species of parasites and parasites ofdifferent taxa In this study close to 45 of the examined birdspecies were infected with more than one congeneric speciesof parasite or parasites of different taxa

A lower prevalence ofHaemoproteus (131)Plasmodium(151) and Leucocytozoon (06) genera was observed herethan in studies in India and Myanmar which are neighbor-ing countries of Bangladesh In India 18 prevalence wasreported for Haemoproteus and 28 for Plasmodium in wildbirds and in Myanmar 40 for Haemoproteus and 60 forPlasmodium in wild birds [11] Their reported prevalence washigher likely because they used molecular methods to detectparasites which are known to be more sensitive Anotherreason for the low prevalence found in this study may bethat we sampled during winter (January to March) whichis not the breeding season of lowland resident birds [11] andthere are low levels of sexual steroid hormones circulating inthe birdsrsquo blood which are supposed to allow the parasite tosurvive [21 22]

The intensity of invasion for parasites varied remark-ably Most of the invasions for Haemoproteus were below20 parasites per 100 microscopic fields and invasions forPlasmodium were below 10 This verifies the proposition ofValkiunas [23] that it is difficult to capture heavily invadedbirds using themist netmethod as they are less active than theless heavily invaded birds [23] The intensity of invasion per100 microscopic fields was higher in Haemoproteus than inPlasmodium and Leucocytozoon Haemoproteus gametocytespersist in the peripheral blood for a long time [15] while somespecies of Leucocytozoon prefer visceral circulation [24]therefore Leucocytozoon may have escaped our attention Incontrast to Haemoproteus and Leucocytozoon for parasitesof Plasmodium genus though they prefer peripheral bloodcirculation the schizogonic cycle in the erythrocytes lasts foronly few days [3] As a result they may also have escaped ourattention

Variations in the prevalence of infection in different birdfamilies have been reported in this study a finding supportedby different studies around the globe [11 25ndash28]

The report of microfilarial infection in birds inBangladesh is perhaps the first The prevalence of microfila-riae in Bangladeshi birds appears to be low The intensity ofinfection was also low which may be an effect of the absenceof microfilariae in the peripheral blood stream in the daytimedue to their periodicity (sampling was done in the daytime)[29 30] It is assumed to be nonpathogenic to birds [31ndash33]It may have some histopathological impact but no cellularreaction [34] However microfilarial infection may lead toquestionable fitness of the host bird [35]

In our study more migratory birds were infected thanresident birdsThis finding is supported by someother studies[26 27] In different studies there are indistinct data onthis issue due to different host species composition [36] Asmigratory birds travel in the course of different terrain theyincrease their affinity for diverse parasite vectors which maylead to increased chance of infection in migratory birds [337 38]Migrants can play a vital role in transmitting parasites


among taxonomically similar birds from temperate regions totropical regions which has been observed in Nigeria [39]

5 Conclusion

Thepathogenic effects of these parasites can play a vital role indeclining wildlife population [40] Wild birds of Bangladeshcarry several types of hemoprotozoan parasites Furtherinvestigationwith a larger sample size is necessary to estimatemore accurately the prevalence of haematozoan parasitesamong wild birds and to understand the epidemiology ofthose parasites

Ethical Approval

Approval from the Research Review Committee (RRC) andthe Animal Experimentation Ethics Committee (AEEC) oficddrb was obtained for this study Birds were extracted fromthemist nets or noose traps as soon as possible after the catchto reduce stress on them All the samples were collected bytrained veterinarians Blood collected from each bird was lessthan 1 of the body weight

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Authorsrsquo Contribution

Ausraful Islam Andrea Mikolon and Mohammad ShafiulAlam conceptualized and designed the study Ausraful Islamand Suman Kumer Paul collected samples Rubayet ElahiKhaja Mohiuddin and Mohammad Shafiul Alam identifiedparasites Rubayet Elahi Ausraful Islam Mohammad SharifHossain and Mohammad Shafiul Alam analyzed the dataRubayet Elahi Ausraful Islam andMohammad Shafiul Alamdrafted the paper and made final revisions Suman KumerPaul Andrea Mikolon Parviez Rana Hosseini and PeterDaszak made critical revision of the manuscript All the au-thors read the final version of the manuscript and approvedit

Acknowledgments

This research study was partially funded by the NIHNSFEcology and Evolution of Infectious Diseases Award fromthe Fogarty International Center 3R01-TW005869 throughEcoHealth Alliance icddrb acknowledges with gratitude thecommitment of NIH to its research efforts The authorsacknowledge the efforts of M Asadur Rahman and M Shar-ifuzzaman during sample collectionThey are also grateful tothe Parasitology Laboratory of icddrb for the support in thestudy

References

[1] G F Bennett ldquoHematozoardquo in Companion Bird Medicine E WBurr Ed pp 120ndash128 The Iowa State University Press AmesIowa USA 1987

[2] M A Peirce ldquoThe significance of avian hematozoa in conserva-tion strategiesrdquo in Diseases and Threatened Birds J E CooperEd pp 69ndash76 ICBP Helmsley UK 1989

[3] G Valkiunas Avian Malaria Parasites and Other Haemo-sporidia CRC Press Boca Raton Fla USA 2005

[4] C M Bartlett ldquoFilaroid Nematodesrdquo in Parasitic Diseases ofWild Birds C T Atkinson N JThomas andD B Hunter Edspp 439ndash462 Wiley-Blackwell 2008

[5] E R Noble G A Noble G A Schad et al Parasitology theBiology of Animal Parasites Lea and Febiger Philadelphia PaUSA 1989

[6] A R Dey N Begum M A Khan et al ldquoHaemoprotozoaninfection in ducks prevalence and pathologyrdquo BangladeshJournal of Veterinary Medicine vol 6 no 1 pp 53ndash58 2008

[7] A RDeyN Begum S C Paul et al ldquoPrevalence and pathologyof blood ptotozoa in pigeons reared at Mymensingh districtBangladeshrdquo International Journal of BioResearch vol 2 no 12pp 25ndash29 2010

[8] E J SoulsbyArthropods and Protozoa of Domesticated AnimalsBailliere Tindall and Cassell 2nd edition 1982

[9] M Mubarak and G H Abed ldquoPathological changes of lungtissues of pigeons (Columba livia domestica) infected withHaemoproteus columbae (Haemosporina Haemoproteidae)rdquoJournal of Biological Sciences vol 5 no 5 pp 536ndash541 2005

[10] D A Lapointe C T Atkinson andM D Samuel ldquoEcology andconservation biology of avian malariardquo Annals of the New YorkAcademy of Sciences vol 1249 no 1 pp 211ndash226 2012

[11] F Ishtiaq E Gering J H Rappole et al ldquoPrevalence anddiversity of avian hematozoan parasites in Asia A regionalsurveyrdquo Journal of Wildlife Diseases vol 43 no 3 pp 382ndash3982007

[12] C Mathis and M Leger Recherches de Parasitologie et dePathologie Humaines et Animales au Tonkin (in French) Mas-son Paris France 1911

[13] H E McClure P Poonswad E C Greiner et al Hematozoa inthe Birds of Eastern and Southern Asia Memorial University ofNew Foundland St Johnrsquos Canada 1978

[14] I Paperna M C Soh C A Yap et al ldquoBlood parasiteprevalence and abundance in the bird communities of severalforested locations in Southeast Asia Blood parasite prevalenceand abundance in the bird communities of several forestedlocations in Southeast Asiardquo Ornothological Science vol 4 no2 pp 129ndash138 2005

[15] I PapernaM S C Keong andC Y AMay ldquoHaemosporozoanparasites found in birds in Peninsular Malaysia SingaporeSarawak and Javardquo Raffles Bulletin of Zoology vol 56 no 2 pp211ndash243 2008

[16] R Talat ldquoInfection of Haematozoan parasites found in birds ofNWFP (Pakistan)rdquo Pakistan Journal of Biological Sciences vol8 no 1 pp 1ndash5 2005

[17] D K Gupta N Jahan and N Gupta ldquoDistribution pattern ofapicomplexan parasites (Sporozoa Haemosporida) in Columbalivia Gmelinrdquo Journal of Parasitic Diseases vol 35 no 1 pp 18ndash22 2011

[18] M M H Khan Protected Areas of Bangladesh- A Guide toWildlife Nishorgo Program Bangladesh Forest Department2008

[19] R Grimmett C Inskipp and T Inskipp Pocket Guide to theBirds of the Indian Subcontinent Christopher Helm LondonUK 2001


[20] G F Bennett and A G Campbell ldquoAvian haemoproteidae IDescription of Haemoproteus fallisi n sp and a review of thehaemoproteids of the family Turdidaerdquo Canadian Journal ofZoology vol 50 no 10 pp 1269ndash1275 1972

[21] N Saino A P Moller and A M Bolzern ldquoTestosteroneeffects on the immune system and parasite infestations in thebarn swallow (Hirundo rustica) An experimental test of theimmunocompetence hypothesisrdquo Behavioral Ecology vol 6 no4 pp 397ndash404 1995

[22] CWedekind and I Folstad ldquoAdaptive or nonadaptive immuno-suppression by sex hormonesrdquo American Naturalist vol 143pp 936ndash938 1994

[23] G Valkiunas ldquoSampling bias in bird Haematozoa investiga-tions rdquo EMOP 8 Abstracts 160rdquo Acta Parasitologica vol 452000

[24] HGill and I Paperna ldquoLeucocytozoonosis in the Israeli sparrowPasser domesticus biblicus Hartert 1904rdquo Parasitology Researchvol 96 no 6 pp 373ndash377 2005

[25] P Jakunin ldquoBlood parasites of wild birds from South-easternKazakhstanrdquo Papers of Institute of Zoology AN Kazakhskoj SSRvol 33 pp 69ndash79 1972

[26] J Kucera ldquoBlood parasites of birds in Central Europe 3Plasmodium and Haemoproteusrdquo Folia Parasitologica vol 28no 4 pp 303ndash312 1981

[27] P Shurulinkov and V Golemansky ldquoHaemoproteids (Haemo-sporida Haemoproteidae) of wild birds in Bulgariardquo ActaProtozoologica vol 41 no 4 pp 359ndash374 2002

[28] G Valkiunas ldquoBlood parasites of birds fromBelomoro-baltijskystream of migration 2 Fauna and distribution of haemopro-teids (Sporozoa Haemosporida)rdquo Parazitologia vol 19 pp 55ndash63 1985

[29] R C AndersonNematode Parasites of Vertebrates Their Devel-opment and Transmission CABI Publishing 2nd edition 2000

[30] J Kucera ldquoBlood parasites of birds in Central Europe 4Trypanosoma ldquoAtoxoplasmardquo Microfilariae and other rarehaematozoardquo Folia Parasitologica vol 29 no 2 pp 107ndash1131982

[31] TW CampbellAvianHematology and CytologyThe Iowa StateUniversity Press Ames Iowa USA 2nd edition 1995

[32] G P Reppas W J Hartley and P A Gill ldquoMicrofilaraemia inAustralian native birdsrdquo Australian Veterinary Journal vol 72no 9 pp 356ndash357 1995

[33] BWRitchie G JHarrison andL RHarrisonAvianMedicinePrinciples and ApplicationWinger Publishing LakeWorth FlaUSA 1994

[34] S S Tsai K Hirai and C Itakura ldquoHistopathological surveyof protozoa helminths and acarids of imported and localpsittacine and passerine birds in Japanrdquo Japanese Journal ofVeterinary Research vol 40 no 4 pp 161ndash174 1992

[35] S Morand and R Poulin ldquoNematode parasite species richnessand the evolution of spleen size in birdsrdquo Canadian Journal ofZoology vol 78 no 8 pp 1356ndash1360 2000

[36] G Valkiunas ldquoBird Haemosporidardquo Acta Zoologica Lithuanicapp 3ndash5 1997

[37] A P Moslashller and J Erritzoslashe ldquoHost immune defence andmigration in birdsrdquo Evolutionary Ecology vol 12 no 8 pp 945ndash953 1998

[38] R B Smith E C Greiner and B O Wolf ldquoMigratory move-ments of sharp-shinned hawks (Accipiter striatus) captured inNewMexico in relation to prevalence intensity and biogeogra-phy of avian hematozoardquo The Auk vol 121 no 3 pp 837ndash8462004

[39] J Waldenstrom S Bensch S Kiboi D Hasselquist and UOttosson ldquoCross-species infection of blood parasites betweenresident and migratory songbirds in AfricardquoMolecular Ecologyvol 11 no 8 pp 1545ndash1554 2002

[40] P G Parker N K Whiteman and R E Miller ldquoConservationmedicine on the Galapagos Islands Partnerships among behav-ioral population and veterinary scientistsrdquo The Auk vol 123no 3 pp 625ndash638 2006

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of


Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology


Molecular Biology International

GenomicsInternational Journal of


The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014


BioinformaticsAdvances in

Marine BiologyJournal of



Signal TransductionJournal of


BioMed Research International

Evolutionary BiologyInternational Journal of



Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014


Genetics Research International


Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational



Enzyme Research



Microbiology


no information is available on haematozoan parasites inwild birds of Bangladesh although Leucocytozoon spp fromdomestic ducks [6] and Haemoproteus spp in domesticpigeons [7] have been reported recently As part of asurvey for influenza virus in wild birds this study wasconducted to identify the haematozoan parasites of var-ious wild birds from different areas of Bangladesh Theobjective of the study was to record the prevalence ofhaematozoan parasites in a wide range of wetland birdsMorphology of parasites and intensity of invasion were alsorecorded

2 Materials and Methods

A total of 322 wild birds were studied belonging to 48 species(15 families and four orders) from January 2011 to March2011 The birds were sampled from two wetland sites inBangladesh Hakaluki haor (N 21∘3310158401015840698 E 091∘5110158401015840682) inSylhet and Moulvibazar districts (212 birds) and Tanguarhaor (N 25∘087941015840 E 091∘040881015840) in Sunamganj district(110 birds) (Figure 1) Hakaluki haor and Tanguar haor areseasonal water bodies located in northern Bangladesh whichdry up during winter when they provide habitat for residentandmigratorywild birdsMist nets andnoose trapswere usedfor bird capicture Blood was drawn from jugular or tarsalvein of the bird Species identification and age determinationwere made using the description given by Grimmett et al[19] All of the birds were marked using metal rings withunique identification numbers at the tarsus and released aftersampling at the site of capture

From each bird typically three (but sometimes two) thinblood smears were prepared on clean grease-free slides Allslides were fixed in absolute methanol for one minute in thefield The fixed smears were then stained with 20 Giemsastain and were observed under 400x and 1000xmagnificationby skilled parasitologists Identification of the haematozoanswas performed using the taxonomic description of Valkiunas[3] and Bartlett [4] If any parasite was found within 100fields of microscopic observation the slide was consideredas positive otherwise it was considered as negative Allparasites in 100 microscope fields at 1000x magnificationwere counted to calculate the intensity of invasion of theparasites The nuclear displacement ratio (NDR) an index oflateral displacement of the erythrocyte nucleus by the parasite[20] was measured following the description of Valkiunas[3] Slides of each parasite identified up to species levelhave been deposited in the US National Parasite Collection(USNPC) Beltsville MD USA (accession numbers are in thesupplementary file 1 see Supplementary Material availableonline at httpdxdoiorg1011552014493754)

The birds were divided into 2 groups migratory andresident birds All measurements in the text and the tablesare presented in micrometers and given as mean plusmn stan-dard deviation Intensity of invasion was calculated per 100microscopic fields Statistical Package for the Social Sciences(SPSS) v 17 (SPSS Inc USA) was used to analyze the data Atwo-tailed Fisherrsquos exact test was used to find the correlationof prevalence within bird families and parasite genus To

indicate statistical significance a 119875 value less than 005 wasused

3 Results

31 Prevalence and Intensity of Infection The overall preva-lence of infection of the birds studied was 295 (95322birds) Among those 132 (42319) prevalence of infectionwas recorded for Haemoproteus spp 151 for Plasmodiumspp (48319) and 06 for Leucocytozoon spp (2319) Twobirds were positive for parasites of both Haemoproteus andPlasmodium genera A single slide was positive for unidenti-fiedmicrofilariae of genus Paronchocerca fromArdeola grayiia resident bird (Table 1)

The prevalence of infection for the three genera variedconsiderably amid different families of birds (Table 1) Amongthe families with sufficient sample size (119899 gt 20) thehighest prevalence was found in the family Laridae 441(15 of 44 birds) for genus Haemoproteus in the familyScolopacidae 208 (5 of 24) for Plasmodium genus in thefamily Dendrocygnidae 23 (1 of 43) for Leucocytozoongenus

The intensity of invasion varied across different parasitegenera For parasites of Haemoproteus genus it ranged from2 to 43 mostly being below 20 parasites per 100 microscopicfields The lowest intensity of invasion for parasites of Plas-modium genus was 2 while the highest was 18 parasites per100 microscopic fields mostly being less than 10 Parasites ofLeucocytozoon genus had 4-5 parasites per 100 microscopicfields while the only bird infected withmicrofilariae had only3 parasites per 100 microscopic fields

In the present study 724 (119899 = 233) of the birds studiedwere migrant and 276 (119899 = 89) were resident amongthese 335 (119899 = 78) of migrant birds and 191 (119899 = 17)of resident birds were positive for any of the parasites ofgenus Haemoproteus Plasmodium or Leucocytozoon Theseparasites weremore commonly found inmigratory birds (119875 lt005) 159 (119899 = 37) of migrant birds and 57 (119899 = 5) ofresident birds were positive for Haemoproteus genus while168 (119899 = 39) of migrant birds were positive for Plasmodiumgenus in contrast to 103 (119899 = 9) of resident birdsMigratory birds were significantly preferred by parasites ofHaemoproteus (119875 lt 005) but for parasites of Plasmodiumthere was no significant preference One migrant bird andone resident bird were found positive for parasites of genusLeucocytozoon spp One of each migrant and resident birdhad mixed infection by parasites of genera Haemoproteusand Plasmodium There was no significant difference in theinfection rates among the study sites

32 Description of Species Six species of Haemoproteus andseven species of Plasmodium were identified Haemopro-teus parasites from four birds belonging to two differentspecies were identified up to subgenus level subgenus Para-haemoproteus Plasmodium parasites from five birds of threespecies were identified only up to subgenus level subgenusHaemoamoeba and subgenus Giovannolaia All the Leucocy-tozoon (119899 = 2) parasites were identified up to genus level


N

00

30

6

12

Decimal degrees














Table1Num

bero

fthe

exam

ined

birdstheirm

igratio

nstatus

andbloo

dparasitep

revalence(in

)indifferent

bird

families

andspecies

Birdsfam

ilies

species

Migratio

nsta

tus

Num

bero

fexamined

birds

Genus

Haemoproteus

Genus

Plasmodium

Genus

Leucocytozoon

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Anatid

ae140

179

164

07

Anas

acuta

M32

94Hgreineri(2)

Hnettio

nis

188

P(G

)circum

flexum

(2)

P(H

)lutzi

P(H

)relictum

(2)

P(H

aemam

oeba)sp

Anas

clypeata

M3

667

P(H

)relictum

(2)

Anas

crecca

M4

250

Leucocytozoon

sp

Anas

falca

taM

1An

aspenelope

M2

500

P(H

)relictum

Anas

querquedula

M7

286

P(H

)relictum

P(H

aemam

oeba)sp

Anas

strepera

M12

83

Hgreineri

250

P(H

)lutzi

P(H

)relictum

P(H

aemam

oeba)sp

Aythya

ferina

M10

500

Hgreineri(2)

Mixed

Hgreineriand

Hnettio

nis(1)

Hnettio

nis(2)

100

P(G

)circum

flexum

Aythya

fuligula

M26

38

Hgreineri

154

P(G

)circum

flexum

(2)

P(H

)relictum

(2)

Aythya

nyroca

M14

429

Hgreineri(3)H

nettio

nis

(3)

71P(H

aemam

oeba)sp

Netta

rufin

aM

4750

Hgreineri(2)

H(Pa

rahaem

oproteus)sp

250

P(H

)relictum

Netta

puscorom

andelianu

sR

9111

P(G

)circum

flexum

Tadornafer

ruginea

M13

231

Hgreineri(3)

77P(H

)relictum

Tadornatadorna

M3

1000

Dendrocygnidae

4370

93

23

Dendrocygna

bicolor

R36

83

H(Pa

rahaem

oproteus)sp

(3)

83

P(G

)polarae

P(H

)relictum

(2)

28

Leucocytozoon

sp

Dendrocygna

javanica

R7

143

P(G

)circum

flexum

Accipitridae

1Circus

mela

noleu

cos

M1


Table1Con

tinued

Birdsfam

ilies

species

Migratio

nsta

tus

Num

bero

fexamined

birds

Genus

Haemoproteus

Genus

Plasmodium

Genus

Leucocytozoon

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Ardeidae

1520

0Ardeacin

erea

R1

Ardeolagrayii

R8

Bubu

lcusibis

R1

Egretta

garzetta

R1

Mesophoyx

interm

edia

R2

1000

P(G

)polarae

Nyctico

raxnyctico

rax

R2

500

P(H

)relictum

Charadriidae

8125

125

Charadriu

sdubius

R6

167

Hscolopaci

Vanellu

scinereus

M2

500

P(H

)relictum

Jacanidae

4Hydrophasians

chiru

rgus

R4

Larid

ae34

441

88

Chlid

oniash

ybrid

usM

1La

rusb

runn

icephalus

M7

286

P(H

)relictum

(2)

Larusridibun

dus

M26

577

Hplatalea

e(15)

39

P(G

)lophu

rae

Phalacrocoracidae

1Ph

alacrocoraxcarbo

M1

Podicipedidae

4250

Podiceps

cristatus

M2

500

P(G

iovann

olaia)

sp

Tachybaptusrufi

collis

R2

Rostr

atulidae

250

0Ro

stratulabenghalen

sisM

2500

P(H

)relictum

Scolop

acidae

2420

8Ca

lidris

alpina

M2

Calidris

minuta

M10

Calidris

temminckii

M1

Gallin

agoste

nura

M1


Table1Con

tinued

Birdsfam

ilies

species

Migratio

nsta

tus

Num

bero

fexamined

birds

Genus

Haemoproteus

Genus

Plasmodium

Genus

Leucocytozoon

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Limnodrom

oussem

ipalmatus

M1

Tringa

stagnatilis

M2

500

P(H

)relictum

Tringa

totanu

sM

7571

P(H

)relictum

(4)

Rallidae

38184

Fulicaatra

M32

156

P(H

)lutzi(3)

P(H

)relictum

(2)

Gallicrexcin

erea

R2

Gallin

urachloropu

sM

11000

P(H

)lutzi

Porphyrio

porphyrio

R3

333

P(H

)lutzi

Sturnidae

250

0Sturnu

scontra

R2

500

Hpastoris

Sylviid

ae2

Acrocephalus

stentoreus

M1

Megalurus

palustris

R1

Eurosto

podidae

1Eu

rosto

podu

smacrotis

R1

Total

319

132

151

06

Migratio

nsta

tusMm

igrantR

resident


(a) (b)









































(a) (b)






























4 Discussion










5 Conclusion


Ethical Approval






Acknowledgments


References

















































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


N

00

30

6

12

Decimal degrees














Table1Num

bero

fthe

exam

ined

birdstheirm

igratio

nstatus

andbloo

dparasitep

revalence(in

)indifferent

bird

families

andspecies

Birdsfam

ilies

species

Migratio

nsta

tus

Num

bero

fexamined

birds

Genus

Haemoproteus

Genus

Plasmodium

Genus

Leucocytozoon

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Anatid

ae140

179

164

07

Anas

acuta

M32

94Hgreineri(2)

Hnettio

nis

188

P(G

)circum

flexum

(2)

P(H

)lutzi

P(H

)relictum

(2)

P(H

aemam

oeba)sp

Anas

clypeata

M3

667

P(H

)relictum

(2)

Anas

crecca

M4

250

Leucocytozoon

sp

Anas

falca

taM

1An

aspenelope

M2

500

P(H

)relictum

Anas

querquedula

M7

286

P(H

)relictum

P(H

aemam

oeba)sp

Anas

strepera

M12

83

Hgreineri

250

P(H

)lutzi

P(H

)relictum

P(H

aemam

oeba)sp

Aythya

ferina

M10

500

Hgreineri(2)

Mixed

Hgreineriand

Hnettio

nis(1)

Hnettio

nis(2)

100

P(G

)circum

flexum

Aythya

fuligula

M26

38

Hgreineri

154

P(G

)circum

flexum

(2)

P(H

)relictum

(2)

Aythya

nyroca

M14

429

Hgreineri(3)H

nettio

nis

(3)

71P(H

aemam

oeba)sp

Netta

rufin

aM

4750

Hgreineri(2)

H(Pa

rahaem

oproteus)sp

250

P(H

)relictum

Netta

puscorom

andelianu

sR

9111

P(G

)circum

flexum

Tadornafer

ruginea

M13

231

Hgreineri(3)

77P(H

)relictum

Tadornatadorna

M3

1000

Dendrocygnidae

4370

93

23

Dendrocygna

bicolor

R36

83

H(Pa

rahaem

oproteus)sp

(3)

83

P(G

)polarae

P(H

)relictum

(2)

28

Leucocytozoon

sp

Dendrocygna

javanica

R7

143

P(G

)circum

flexum

Accipitridae

1Circus

mela

noleu

cos

M1


Table1Con

tinued

Birdsfam

ilies

species

Migratio

nsta

tus

Num

bero

fexamined

birds

Genus

Haemoproteus

Genus

Plasmodium

Genus

Leucocytozoon

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Ardeidae

1520

0Ardeacin

erea

R1

Ardeolagrayii

R8

Bubu

lcusibis

R1

Egretta

garzetta

R1

Mesophoyx

interm

edia

R2

1000

P(G

)polarae

Nyctico

raxnyctico

rax

R2

500

P(H

)relictum

Charadriidae

8125

125

Charadriu

sdubius

R6

167

Hscolopaci

Vanellu

scinereus

M2

500

P(H

)relictum

Jacanidae

4Hydrophasians

chiru

rgus

R4

Larid

ae34

441

88

Chlid

oniash

ybrid

usM

1La

rusb

runn

icephalus

M7

286

P(H

)relictum

(2)

Larusridibun

dus

M26

577

Hplatalea

e(15)

39

P(G

)lophu

rae

Phalacrocoracidae

1Ph

alacrocoraxcarbo

M1

Podicipedidae

4250

Podiceps

cristatus

M2

500

P(G

iovann

olaia)

sp

Tachybaptusrufi

collis

R2

Rostr

atulidae

250

0Ro

stratulabenghalen

sisM

2500

P(H

)relictum

Scolop

acidae

2420

8Ca

lidris

alpina

M2

Calidris

minuta

M10

Calidris

temminckii

M1

Gallin

agoste

nura

M1


Table1Con

tinued

Birdsfam

ilies

species

Migratio

nsta

tus

Num

bero

fexamined

birds

Genus

Haemoproteus

Genus

Plasmodium

Genus

Leucocytozoon

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Limnodrom

oussem

ipalmatus

M1

Tringa

stagnatilis

M2

500

P(H

)relictum

Tringa

totanu

sM

7571

P(H

)relictum

(4)

Rallidae

38184

Fulicaatra

M32

156

P(H

)lutzi(3)

P(H

)relictum

(2)

Gallicrexcin

erea

R2

Gallin

urachloropu

sM

11000

P(H

)lutzi

Porphyrio

porphyrio

R3

333

P(H

)lutzi

Sturnidae

250

0Sturnu

scontra

R2

500

Hpastoris

Sylviid

ae2

Acrocephalus

stentoreus

M1

Megalurus

palustris

R1

Eurosto

podidae

1Eu

rosto

podu

smacrotis

R1

Total

319

132

151

06

Migratio

nsta

tusMm

igrantR

resident


(a) (b)









































(a) (b)






























4 Discussion










5 Conclusion


Ethical Approval






Acknowledgments


References

















































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


Table1Num

bero

fthe

exam

ined

birdstheirm

igratio

nstatus

andbloo

dparasitep

revalence(in

)indifferent

bird

families

andspecies

Birdsfam

ilies

species

Migratio

nsta

tus

Num

bero

fexamined

birds

Genus

Haemoproteus

Genus

Plasmodium

Genus

Leucocytozoon

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Anatid

ae140

179

164

07

Anas

acuta

M32

94Hgreineri(2)

Hnettio

nis

188

P(G

)circum

flexum

(2)

P(H

)lutzi

P(H

)relictum

(2)

P(H

aemam

oeba)sp

Anas

clypeata

M3

667

P(H

)relictum

(2)

Anas

crecca

M4

250

Leucocytozoon

sp

Anas

falca

taM

1An

aspenelope

M2

500

P(H

)relictum

Anas

querquedula

M7

286

P(H

)relictum

P(H

aemam

oeba)sp

Anas

strepera

M12

83

Hgreineri

250

P(H

)lutzi

P(H

)relictum

P(H

aemam

oeba)sp

Aythya

ferina

M10

500

Hgreineri(2)

Mixed

Hgreineriand

Hnettio

nis(1)

Hnettio

nis(2)

100

P(G

)circum

flexum

Aythya

fuligula

M26

38

Hgreineri

154

P(G

)circum

flexum

(2)

P(H

)relictum

(2)

Aythya

nyroca

M14

429

Hgreineri(3)H

nettio

nis

(3)

71P(H

aemam

oeba)sp

Netta

rufin

aM

4750

Hgreineri(2)

H(Pa

rahaem

oproteus)sp

250

P(H

)relictum

Netta

puscorom

andelianu

sR

9111

P(G

)circum

flexum

Tadornafer

ruginea

M13

231

Hgreineri(3)

77P(H

)relictum

Tadornatadorna

M3

1000

Dendrocygnidae

4370

93

23

Dendrocygna

bicolor

R36

83

H(Pa

rahaem

oproteus)sp

(3)

83

P(G

)polarae

P(H

)relictum

(2)

28

Leucocytozoon

sp

Dendrocygna

javanica

R7

143

P(G

)circum

flexum

Accipitridae

1Circus

mela

noleu

cos

M1


Table1Con

tinued

Birdsfam

ilies

species

Migratio

nsta

tus

Num

bero

fexamined

birds

Genus

Haemoproteus

Genus

Plasmodium

Genus

Leucocytozoon

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Ardeidae

1520

0Ardeacin

erea

R1

Ardeolagrayii

R8

Bubu

lcusibis

R1

Egretta

garzetta

R1

Mesophoyx

interm

edia

R2

1000

P(G

)polarae

Nyctico

raxnyctico

rax

R2

500

P(H

)relictum

Charadriidae

8125

125

Charadriu

sdubius

R6

167

Hscolopaci

Vanellu

scinereus

M2

500

P(H

)relictum

Jacanidae

4Hydrophasians

chiru

rgus

R4

Larid

ae34

441

88

Chlid

oniash

ybrid

usM

1La

rusb

runn

icephalus

M7

286

P(H

)relictum

(2)

Larusridibun

dus

M26

577

Hplatalea

e(15)

39

P(G

)lophu

rae

Phalacrocoracidae

1Ph

alacrocoraxcarbo

M1

Podicipedidae

4250

Podiceps

cristatus

M2

500

P(G

iovann

olaia)

sp

Tachybaptusrufi

collis

R2

Rostr

atulidae

250

0Ro

stratulabenghalen

sisM

2500

P(H

)relictum

Scolop

acidae

2420

8Ca

lidris

alpina

M2

Calidris

minuta

M10

Calidris

temminckii

M1

Gallin

agoste

nura

M1


Table1Con

tinued

Birdsfam

ilies

species

Migratio

nsta

tus

Num

bero

fexamined

birds

Genus

Haemoproteus

Genus

Plasmodium

Genus

Leucocytozoon

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Limnodrom

oussem

ipalmatus

M1

Tringa

stagnatilis

M2

500

P(H

)relictum

Tringa

totanu

sM

7571

P(H

)relictum

(4)

Rallidae

38184

Fulicaatra

M32

156

P(H

)lutzi(3)

P(H

)relictum

(2)

Gallicrexcin

erea

R2

Gallin

urachloropu

sM

11000

P(H

)lutzi

Porphyrio

porphyrio

R3

333

P(H

)lutzi

Sturnidae

250

0Sturnu

scontra

R2

500

Hpastoris

Sylviid

ae2

Acrocephalus

stentoreus

M1

Megalurus

palustris

R1

Eurosto

podidae

1Eu

rosto

podu

smacrotis

R1

Total

319

132

151

06

Migratio

nsta

tusMm

igrantR

resident


(a) (b)









































(a) (b)






























4 Discussion










5 Conclusion


Ethical Approval






Acknowledgments


References

















































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


Table1Con

tinued

Birdsfam

ilies

species

Migratio

nsta

tus

Num

bero

fexamined

birds

Genus

Haemoproteus

Genus

Plasmodium

Genus

Leucocytozoon

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Ardeidae

1520

0Ardeacin

erea

R1

Ardeolagrayii

R8

Bubu

lcusibis

R1

Egretta

garzetta

R1

Mesophoyx

interm

edia

R2

1000

P(G

)polarae

Nyctico

raxnyctico

rax

R2

500

P(H

)relictum

Charadriidae

8125

125

Charadriu

sdubius

R6

167

Hscolopaci

Vanellu

scinereus

M2

500

P(H

)relictum

Jacanidae

4Hydrophasians

chiru

rgus

R4

Larid

ae34

441

88

Chlid

oniash

ybrid

usM

1La

rusb

runn

icephalus

M7

286

P(H

)relictum

(2)

Larusridibun

dus

M26

577

Hplatalea

e(15)

39

P(G

)lophu

rae

Phalacrocoracidae

1Ph

alacrocoraxcarbo

M1

Podicipedidae

4250

Podiceps

cristatus

M2

500

P(G

iovann

olaia)

sp

Tachybaptusrufi

collis

R2

Rostr

atulidae

250

0Ro

stratulabenghalen

sisM

2500

P(H

)relictum

Scolop

acidae

2420

8Ca

lidris

alpina

M2

Calidris

minuta

M10

Calidris

temminckii

M1

Gallin

agoste

nura

M1


Table1Con

tinued

Birdsfam

ilies

species

Migratio

nsta

tus

Num

bero

fexamined

birds

Genus

Haemoproteus

Genus

Plasmodium

Genus

Leucocytozoon

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Limnodrom

oussem

ipalmatus

M1

Tringa

stagnatilis

M2

500

P(H

)relictum

Tringa

totanu

sM

7571

P(H

)relictum

(4)

Rallidae

38184

Fulicaatra

M32

156

P(H

)lutzi(3)

P(H

)relictum

(2)

Gallicrexcin

erea

R2

Gallin

urachloropu

sM

11000

P(H

)lutzi

Porphyrio

porphyrio

R3

333

P(H

)lutzi

Sturnidae

250

0Sturnu

scontra

R2

500

Hpastoris

Sylviid

ae2

Acrocephalus

stentoreus

M1

Megalurus

palustris

R1

Eurosto

podidae

1Eu

rosto

podu

smacrotis

R1

Total

319

132

151

06

Migratio

nsta

tusMm

igrantR

resident


(a) (b)









































(a) (b)






























4 Discussion










5 Conclusion


Ethical Approval






Acknowledgments


References

















































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


Table1Con

tinued

Birdsfam

ilies

species

Migratio

nsta

tus

Num

bero

fexamined

birds

Genus

Haemoproteus

Genus

Plasmodium

Genus

Leucocytozoon

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Prevalence

()

Parasites

pecies

Limnodrom

oussem

ipalmatus

M1

Tringa

stagnatilis

M2

500

P(H

)relictum

Tringa

totanu

sM

7571

P(H

)relictum

(4)

Rallidae

38184

Fulicaatra

M32

156

P(H

)lutzi(3)

P(H

)relictum

(2)

Gallicrexcin

erea

R2

Gallin

urachloropu

sM

11000

P(H

)lutzi

Porphyrio

porphyrio

R3

333

P(H

)lutzi

Sturnidae

250

0Sturnu

scontra

R2

500

Hpastoris

Sylviid

ae2

Acrocephalus

stentoreus

M1

Megalurus

palustris

R1

Eurosto

podidae

1Eu

rosto

podu

smacrotis

R1

Total

319

132

151

06

Migratio

nsta

tusMm

igrantR

resident


(a) (b)









































(a) (b)






























4 Discussion










5 Conclusion


Ethical Approval






Acknowledgments


References

















































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


(a) (b)









































(a) (b)






























4 Discussion










5 Conclusion


Ethical Approval






Acknowledgments


References

















































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology

























(a) (b)






























4 Discussion










5 Conclusion


Ethical Approval






Acknowledgments


References

















































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


(a) (b)






























4 Discussion










5 Conclusion


Ethical Approval






Acknowledgments


References

















































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology






4 Discussion










5 Conclusion


Ethical Approval






Acknowledgments


References

















































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology



5 Conclusion


Ethical Approval






Acknowledgments


References

















































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology






























Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology








Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology

Documents

Research Article Prevalence and Diversity of Avian ... · Research Article Prevalence and Diversity of Avian Haematozoan Parasites in Wetlands of Bangladesh RubayetElahi, 1,2 AusrafulIslam,