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. 2020 Oct 19;148(1):1–30. doi: 10.1017/S0031182020001961

Epidemiologic significance of Toxoplasma gondii infections in turkeys, ducks, ratites and other wild birds: 2009–2020

J P Dubey 1,, F H A Murata 1, C K Cerqueira-Cézar 1, O C H Kwok 1, C Su 2
PMCID: PMC11010194  PMID: 33070787

Abstract

Toxoplasma gondii infections are common in humans and animals worldwide. Wild and domestic avian species are important in the epidemiology of T. gondii infections because felids prey on them and excrete millions of oocysts in the environment, disseminating the infection. Herbivorous birds are also excellent sentinels of environmental contamination with T. gondii oocysts because they feed on the ground. Toxoplasma gondii infections in birds of prey reflect infections in intermediate hosts. Humans can become infected by consuming undercooked avian tissues. Here, the authors reviewed prevalence, persistence of infection, clinical disease, epidemiology and genetic diversity of T. gondii strains isolated from turkeys, geese, ducks, ratites and avian species (excluding chickens) worldwide 2009–2020. Genetic diversity of 102 T. gondii DNA samples isolated worldwide is discussed. The role of migratory birds in dissemination of T. gondii infection is discussed.

Key words: Birds, clinical disease, epidemiology, genotype, oocyst, prevalence, Toxoplasma gondii

Introduction

Toxoplasma gondii infections are prevalent in humans and animals worldwide. The ingestion of undercooked infected meat or consumption of food and water contaminated with oocysts excreted in cat feces are the main sources of infection. Cats are everywhere and a single cat can excrete millions of oocysts that can remain viable in the environment for months under natural conditions (Dubey, 2010). Estimation of oocyst contamination of the environment is difficult because of low numbers present in soil or water (Lélu et al., 2012). Wild and domestic birds are excellent sentinels of environmental contamination with T. gondii oocysts because herbivorous birds feed on the ground, and birds of prey consume hundreds of rodents and other small mammals yearly that are important intermediate hosts of T. gondii (Dubey et al., 2020; Iemmi et al., 2020). Migratory birds (penguins, geese and others) can transport the parasite across seas (Sandström et al., 2013). Some species (turkeys, geese, ducks and ostriches) are part of food supply for humans. A study estimated that billions of birds are consumed by cats yearly (Loss et al., 2013). Thus, there is great potential for the spread of T. gondii oocysts in the environment.

We recently reviewed the biology of T. gondii infections in chickens (Gallus domesticus) (Dubey et al., 2020). Here, T. gondii infections in other avian species, including domestic turkeys, ducks, geese, ratites and other avian species, are reviewed.

Turkeys (Meleagris gallopavo)

Antibodies to T. gondii were detected from 11.0 to 89.8% of turkeys surveyed (Table 1). Using a kinetic recombinant antigen (GRA7 and GRA8) ELISA, T. gondii antibodies were detected in 387 (20.2%) of 1913 sera from 14 turkey farms in different areas of Germany (Koethe et al., 2011). Seroprevalence varied greatly among farms and within the individual farms, depending on fattening cycles and season which turkeys were slaughtered. Seroprevalences were higher in turkeys slaughtered in summer vs in fall or winter (Koethe et al., 2011).

Table 1.

Seroprevalence of Toxoplasma gondii in turkeys (Meleagris gallopavo)

Country Area Source No. tested No. positive % Positive Test Cut-off Remarks Reference
Brazil Pernambuco 28 Farms 204 21 11.0 MAT 1:25 et al. (2016)
Egypt Kafr El-Sheikh Farms 17 5 29.4 IHAa 1:80 Harfoush and Tahoon (2010)
Germany 5 States 14 Farms, abattoirs 1913 387 20.2 ELISA-in house 1:50 Sex, season association Koethe et al. (2011)
Iran Fars FR, abattoir 54 49 89.8 MAT 1:40 T. gondii DNA and isolation Sarkari et al. (2014)
Iran Shiraz Farms, abattoir 9 1 11.1 MAT 1:20 Asgari et al. (2013)
Iraq Ninevah Farms 107 82 76.6 LATb 1:20 Butty (2009)
Nigeria Ondo, Osun, Oyo Farms 320 13 4.1 MAT 1:20 Sex association Ayinmode et al. (2017)
USA Pennsylvania Hunted 20 6 30.0 MAT 1:5 T. gondii isolated Cerqueira-Cézar et al. (2019)

ELISA, enzyme-linked immunosorbent assay; FR, free-range; IHA, indirect haemagglutination assay; LAT, latex agglutination test; MAT, modified agglutination test (Dubey and Desmonts, 1987).

a

IHA (Toxo-IHA Fumouze, Diagnostics, France).

b

LAT (Toxo latex kit from Bio-kit-SA, Barcelona, Spain).

A very high rate of infection was reported in a study from Iran (Sarkari et al., 2014). Antibodies to T. gondii were found in 89.8% of turkeys (Table 1) and T. gondii DNA was detected in 61.6% of turkey tissues (Table 2). Viable T. gondii was isolated from the muscle of 5 wild hunted turkeys in the USA (Table 3).

Table 2.

Isolation of viable Toxoplasma gondii from wild bird by bioassay in mice and/or cats

Host Country Location No. tested Tissues No. isolated Strain designation PCR-RFLP genotype (Toxo DB) Notes Reference
Accipitriformes
Bald eagle (Haliaeetus leucocephalus) USA Alabama 1 B 1 TgBeAl 1 genotype: #5 (1, TgBeA1) Yu et al. (2013)
Bald eagle (Haliaeetus leucocephalus) USA California 5 H 1 TgHlUs1 1 genotype: #1, Type II (1, TgHlUs1) Dubey et al. (2011a), Shwab et al. (2014)
Common buzzard (Buteo buteo) Turkey Seferihisar, Manisa 25 B, H 9 TgBirdTr_Izmir4,6,7 TgBirdTr_Manisa1-3,5-7 Genotyped by microsatellites. 2 genotypes: Type II, ToxoDB #1 or #3 (6, TgBirdTr_Izmir4, TgBirdTr_Manisa2, TgBirdTr_Manisa3, TgBirdTr_Manisa6, TgBirdTr_Manisa7, TgBirdTr_Izmir7). Type III, ToxoDB #2 (1, TgBirdTr_Manisa1). Mixed types (2, TgBirdTr_Izmir6, TgBirdTr_Manisa5) Karakavuk et al. (2018)
Ferruginous hawk (Buteo regalis) USA Colorado 7 B, H 1 TgBrCoUs1 1 genotype: #1 (1, TgBrCoUs1) Dubey et al. (2010)
Red-shouldered hawk (Buteo lineatus) USA Alabama 1 B 1 TgRshAL 1 genotype: #10, Type I (1, TgRshAL) Yu et al. (2013)
Red-tailed hawk (Buteo jamaicensis) USA Colorado 25 B, H 1 TgBjCoUs1 1 genotype: #1 (1, TgBjCoUs1) Dubey et al. (2010)
Red-tailed hawk (Buteo jamaicensis) USA Wisconsin 1 H 1 TgBjUS1 1 genotype: #15 (1, TgBjUS1) Dubey et al. (2011a), Shwab et al. (2014)
Roadside hawk (Rupornis magnirostris) Brazil Minas Gerais 7 B, H 1 TgWildBrMG1 1 genotype: #108 (1, TgWildBrMG1) Rêgo et al. (2018)
Rough-legged hawk (Buteo lagopus) USA Colorado 4 B, H 1 TgBlCoUs1 1 genotype: #2, Type III (1, TgBlCoUs1) Dubey et al. (2010)
Swainson's hawk (Buteo swainsoni) USA Colorado 13 B, H 2 TgBsCoUs1,2 2 genotypes: #1, Type II (1, TgBsCoUs2), #167 (1, TgBsCoUs1) Dubey et al. (2010)
Anseriformes
Canada geese (Branta canadensis) USA Maryland Hunted H 9 TgGooseUS1-9 5 genotypes #1 (1, TgGooseUS9), #2 (4, TgGooseUS3,5,6,7), #4 (2, TgGooseUS2,8), #266 (1, TgGooseUS1), #267 (1, TgGooseUS4) One isolate by bioassay in cat Verma et al. (2016)
Domestic duck (unspecified) China Chongqing 12 B, H, K, Li, Lu, Sp 1 ND PCR (ITS-1) Zhao et al. (2015)
Domestic duck (unspecified) Malaysia Peninsular 23 B, H 4 DK1-4 PCR-RFLP-partial genotyping data Backyards of homes Puvanesuaran et al. (2013)
Mallard duck (Anas platyrhynchos) France Hunted 2 H 1 ND Microsatellite markers, 1 genotype: type II, ToxoDB, #1 or #3 (1, one isolate) Wild Aubert et al. (2010)
Mallard duck (Anas platyrhynchos) Malaysia 4 states 30 hunted B, H 4 NS ND T. gondii DNA was detected by PCR-RFLP in tissues of inoculated mice Puvanesuaran et al. (2013)
Mallard duck (Anas platyrhynchos) Senegal Saint-Louis 1 B, H 1 TgA117073 Genotyped by 15 microsatellite markers as Type II ToxoDB #1 or #3 (1, TgA117073) Galal et al. (2019)
Muskovy duck (Cairina moschata) Senegal Dakar, Kedougou, Saint-Louis 15 B, H 11 TgA117015, 117017, 117018, 117025, 117032, 117038, 117041, 117054, 117060, 117061, 117070. 12 strains genotyped with 15 microsatellites 4 genotypes: Type II, ToxoDB #1 or #3 (3, TgA117038, 117041, 117054), Type III, ToxoDB #2 (1, TgA117015), Africa 1, ToxoDB #6 (1, TgA117070), Africa 4, ToxoDB #20 (6, TgA117017, 177018, 177025, 177032, 177060, 117061). Galal et al. (2019)
Mute swan (Cygnus olor) USA Great lakes 14 H 3 TgSwanUs1-3 2 genotypes: #2 (2, TgSwanUs1,2), #216 (1, TgSwanUs3) Dubey et al. (2013)
Charadriiformes
Yellow-legged gull (Larus michahellis) Turkey Balçova 2 B, H 2 TgBirdTr_Izmir2,3 Genotyped by microsatellite. 2 genotypes: Type II, ToxoDB #1 or #3 (1, TgBirdTr_Izmir2). Type III, ToxoDB #2 (1, TgBirdTr_Izmir3) Karakavuk et al. (2018)
Columbiformes
Eared dove (Zenaida auriculata) Brazil Paraná 46 Several tissues 12 TgDoveBr1-12 Nine strains typed. 5 genotypes: #1 (4, TgDoveBr1,2,8,9), #6 (1, TgDoveBr7), #17 (1, TgDoveBr11), #65 (1, TgDoveBr12), #182 (2, TgDoveBr6,10) de Barros et al. (2014)
Rock pigeon (Columba livia) Mexico Durango 7 B, H 1 TgPigeonMx1 PCR-RFLP ToxoDB genotype # 9 (1, TgPigeonMx1) MAT 1:400 Alvarado-Esquivel et al. (2011), Shwab et al. (2014)
Rock pigeon (Columba livia) Portugal Lisbon 41 B 24 NS Genotyping by SAG2 (26 type II, two type III, one type I) and 5 microsatellites markers (12 type II, two type III, one type I and one recombinant) Waap et al. (2012), Vilares et al. (2014)
Rock pigeon (Columba livia) Serbia Belgrade 4 H 3 NS 529 bp, PCR-RFLP-incomplete Marković et al. (2014)
Falconiformes
American kestrel (Falco sparverius) USA Colorado 5 B, H 1 TgFsCoUs1 1 genotype: #157 (1, TgFsCoUs1) Dubey et al. (2010)
Southern caracara (Caracara plancus) Brazil Minas Gerais 7 B, H 2 TgWildBrMG4,6 2 genotypes: #13 (1, TgWildBrMG6) #290 (1, TgWildBrMG4) Rêgo et al. (2018)
Galliformes
Double-spurred spurfowl (Pternistis bicalcaratus) Senegal Kedougou 4 B, H 1 TgA117077 Genotyped with 15 microsatellites. 1 genotype: Africa 1, ToxoDB #6 (1, TgA117077) Galal et al. (2019)
Guinea fowl (Numida meleagris) Brazil Minas Gerais 2 B, H 1 TgNmBr1 1 genotype: # 1, type II (1, TgNmBr1) Dubey et al. (2011b)
Guinea fowl (Numida meleagris) Senegal Kedougou 1 B, H 1 TgA117058 Genotyped with 15 microsatellites. 1 genotype: Type Africa 1, ToxoDB genotype #6 (1, TgA117058) Galal et al. (2019)
Turkeys (Meleagris gallopavo) USA Pennsylvania 20 hunted H, Sk 5 TgturkeyPa1-5 (designated here) 2 genotypes: #5 (4, TgturkeyPa1-4), #216 (1, TgturkeyPa5) 18NC0055- (TgturkeyPa1) 18-WITU-0002 (TgturkeyPa2) 18-WITU-0012 (TgturkeyPa3) 18-WITU-0015 (TgturkeyPa4) 18-WITU-0019 (TgturkeyPa5) Cerqueira-Cézar et al. (2019)
Passeriformes
Hawaiian crow (Corvus hawaiiensis) USA Hawaii 2 B, Li, Sp, Lu 2 TgHcUS1, 2 1 genotype: #177 (2, TgHcUS1, 2) Work et al. (2000), Shwab et al. (2014)
Pelecaniformes
Striated heron (Butorides striata) Brazil Pernambuco 2 B, H, Sk 1 TgButstBrPE1 1 genotype: #13 (1, TgButstBrPE1) Silva et al. (2018b)
Piciformes
Campo flicker (Colaptes campestris) Brazil Minas Gerais 1 B, H 1 TgWildBrMG3 1 genotype: #11 (1, TgWildBrMG3) Rêgo et al. (2018)
Keel-billed toucan (Ramphastos sulfuratus) Costa Rica Zoo 1 Sk 1 TgRsCr1 1 genotype: #52 (1, TgRsCr1) Dubey et al. (2009), Shwab et al. (2014)
Toco toucan (Ramphastos toco) Brazil Minas Gerais 3 B, H 1 TgWildBrMG2 1 genotype: #290 (1, TgWildBrMG2) Rêgo et al. (2018)
Psittaciformes
Peach-Faced Lovebird (Agapornis roseicollis) Australia Sydney 1 pet B 1 AgapornisTg1 1 genotype: #3, Type II variant (1, AgapornisTg1) T. gondii genotyping in B of the bird Cooper et al. (2015)
Strigiformes
Barn owl (Tyto alba) Turkey Konak 2 B, H 2 TgBirdTr_Izmir1,5 Genotyped by microsatellites. 2 genotypes: Type II, ToxoDB #1 or #3 (1, TgBirdTr_Izmir5), Type III, ToxoDB #2 (1, TgBirdTr_Izmir1) Karakavuk et al. (2018)
Barn owl (Tyto alba) USA Colorado 1 B, H 1 TgTaCoUs1 PCR-RFLP ToxoDB genotype # 5 MAT<1:25 Dubey et al. (2010)
Barred owl (Strix varia) USA Alabama 1 B 1 TgSaUS1 1 genotype: #3, Type II variant (1, TgSaUS1) MAT 1:50 Love et al. (2016)
Eurasian eagle-owl (Bubo bubo) Turkey Salihli 2 B, H 1 TgBirdTr_Manisa4 Mixed types (1, TgBirdTr_Manisa4) Karakavuk et al. (2018)
Tropical screech owl (Megascops choliba) Brazil Minas Gerais 4 B, H 1 TgWildBrMG5 1 genotype: #8 (1, TgWildBrMG5) Rêgo et al. (2018)
Struthioniformes
Ostrich (Struthio camelus) Brazil São Paulo 38 B 14 TgOsBr1,2 2 genotypes: # 161 (1, TgOsBr2), #206 (1, TgOsBr1) Abattoirs da Silva and Langoni (2016)
Suliformes
Great cormorant (Phalacrocorax carbo) Turkey Çiğli 1 B, H 1 NS ND Karakavuk et al. (2018)

B, brain; H, heart; K, kidney; Li, liver; Lu, lung; Sk, skeletal muscle; Sp, spleen; NS, not stated; ND, no data; PCR, polymerase chain reaction; PCR-RFLP, Restriction fragment length polymorphism.

Table 3.

Toxoplasma gondii DNA from tissues of wild birds

Host Country Region No. tested Tissue No. positive % Positive Remarks and PCR (gene) Genotyping Reference
Accipitriformes
Black kite (Milvus migrans) Spain Several 3 B 1 33.3 N-PCR (529 bp – TOX9,11 primers) ND Darwich et al. (2012)
Common buzzard (Buteo buteo) Turkey Bergama, Bornova, Çiğli, Kemalpaşa, Konak, Manisa Salihli, Saruhanli, Seferihisar, Turgutlu 25 B, H 23 92.0 RT-PCR, (529 bp – TOX-SE,AS primers). Tg isolated 15 Microsatellite markers – ToxoDB #1 or #3 in 6, #2 in 1 and mixed in 2 Karakavuk et al. (2018)
Eurasian sparrow hawk (Accipiter nisus) Turkey Bornova, Çiğli, Karabağlar, Salihli, Saruhanlı 5 B, H 4 80.0 RT-PCR, (529 bp – TOX-SE,AS primers). Karakavuk et al. (2018)
Griffon vulture (Gyps fulvus) Spain Several 105 B 1 0.9 N-PCR (529 bp – TOX9,11 primers) ND Darwich et al. (2012)
Anseriformes
Canada geese (Branta canadensis) Snow geese (Chen caerulescens) Canada Nunavik 156 B, G, H, Li, Sk 14 9.0 RT-PCR (529 bp – TOX9,11 primers), highest concentration of parasite DNA (tachyzoite equivalent) in H = 744, B = 300, Sk = 104, Li = 33, G = 8 PCR-RFLP using GRA6 – type II Bachand et al. (2019)
Eurasian green-winged teal (Anas crecca) Italy NS 8 B, H 5 62.5 N-PCR (B1) ND Nardoni et al. (2019)
Eurasian teal (Anas crecca) Italy Tuscany 3 B 1 33.3 N-PCR (B1) 10 PCR-RFLP markers – genotype incomplete Mancianti et al. (2013)
Falcated teal (Falcated teal) China Jilin 8 H or Lu 1 12.5 N-PCR (B1) 10 PCR-RFLP markers – ToxoDB genotype incomplete Zhang et al. (2015)
Geese (unspecified) China Shandong 42 Sk 2 4.7 N-PCR (B1) Zou et al. (2017)
Hawaiian geese (Branta sandvicensis) USA Hawaii 4 Li, Lu 4 100.0 ND 10 PCR-RFLP markers – ToxoDB genotype #261 (21729-Li,21774-Lu, 25022-Li), #262 (21850-Li) (DNA from frozen tissues of IHC confirmed toxoplasmosis) Work et al. (2016)
Mallard (Anas platyrhynchos) China Jilin 25 H or Lu 5 20.0 N-PCR (B1) 10 PCR-RFLP markers – ToxoDB genotype incomplete Zhang et al. (2015)
Mallard (Anas platyrhynchos) China Shandong 115 Sk 9 7.8 N-PCR (B1) 10 PCR-RFLP markers – ToxoDB genotype #9 in a duck Zou et al. (2017)
Mallard (Anas platyrhynchos) Czech Republic Several 280 B, H, Sk 15 5.4 RT-PCR, (B1,529 bp), Tg genotyped 6 PCR-RFLP markers – 6 type II, 7 type III, 6 type II/III Skorpikova et al. (2018)
Mallard (Anas platyrhynchos) Italy Tuscany 2 B 1 50.0 N-PCR (B1) 10 PCR-RFLP markers – genotype incomplete Mancianti et al. (2013)
Northern shoveler (Anas clypeata) Italy Tuscany 2 B 1 50.0 N-PCR (B1) 10 PCR-RFLP markers – genotype incomplete Mancianti et al. (2013)
Bucerotiformes
Southern-Yellow-billed hornbill (Tockus leucomelas) South Africa Limpopo 4 B 1 25.0 PCR (B1 – Tg1,2 primers) Lukášová et al. (2018)
Charadriformes
Eurasian stone curlew (Burhinus oedicnemus) Turkey Çiğli 1 B, H 1 100.0 RT-PCR, (529 bp – TOX-SE,AS primers) Karakavuk et al. (2018)
Little tern (Sternula albifrons) Turkey Çiğli 1 B, H 0 0 RT-PCR, (529 bp – TOX-SE,AS primers) Karakavuk et al. (2018)
Woodcock (Scolopax rusticola) Greece Macedonia, Mesolonghi 86 B 4 4.7 PCR (529 bp – Tox -9upAu, Tox-11doAu primers) ND Moustakidis et al. (2017)
Yellow-legged gull (Larus michahellis) Turkey Balçova, Konak 2 B, H 2 100.0 RT-PCR, (529 bp – TOX-SE,AS primers). Tg isolated 15 Microsatellite markers – ToxoDB #1 or #3 in 1, #2 in 1 Karakavuk et al. (2018)
Ciconiiformes
Black stork (Ciconia nigra) Turkey NS 1 B, H 1 100.0 RT-PCR, (529 bp – TOX-SE,AS primers) Karakavuk et al. (2018)
White stork (Ciconia ciconia) Turkey Konak 1 B, H 1 100.0 RT-PCR, (529 bp – TOX-SE,AS primers) Karakavuk et al. (2018)
Columbiformes
Laughing dove (Streptopelia senegalensis) South Africa Limpopo 4 B 1 25.0 PCR (B1 – Tg1,2 primers) Lukášová et al. (2018)
Mourning dove (Zenaida macroura) USA Tennessee 186 B 2 1.0 PCR (529 bp, TOX4,5 primers) Ammar et al. (2020)
Red-eyed dove (Streptopelia semitorquata) South Africa Limpopo 5 B 1 20.0 PCR (B1 – Tg1,2 primers) 15 microsatellites markers – genotyping type II Lukášová et al. (2018)
Rock pigeon (Columba livia) Iran Khuzestan 43 B, H 3 6.9 PCR (B1 – TG1,2 primers) PCR-RFLP using GRA6, 1 type II and 2 type III Khademvatan et al. (2013)
Rock pigeon (Columba livia) Pakistan Punjab 54 H, Sk 19 35.1 PCR (B1 – TOX4,5 primers) ND Nazir et al. (2018)
Rock pigeon (Columba livia) Portugal Lisbon 41 B 28 68.2 PCR (B1) Genotyping by SAG2 (26 type II, 2 type III, 1 type I), and 5 microsatellites markers (12 type II, 2 type III, 1 type 1, 1 recombinant) Vilares et al. (2014)
Rock pigeon (Columba livia) Serbia Belgrade 7 H 5 71.4 RT-PCR (529 bp) 6 PCR-RFLP markers – 2 type II and 1 type III Marković et al. (2014)
Wood pigeon (Columba palumbus) Italy NS 1 B, H 1 100.0 N-PCR (B1) ND Nardoni et al. (2019)
Wood pigeon (Columba palumbus) Turkey Konak 1 B, H 1 100.0 RT-PCR, (529 bp – TOX-SE,AS primers) Karakavuk et al. (2018)
Falconiformes
Common kestrel (Falcus tinnunculus) Italy NS 3 B, H 2 66.6 N-PCR (B1) ND Nardoni et al. (2019)
Common kestrel (Falco tinnunculus) Poland Several 3 B, H, Li, Sk 1 33.3 PCR (B1) 5 PCR-RFLP markers – type II/III Sroka et al. (2019)
Common kestrel (Falco tinnunculus) Turkey Konak 1 B, H 0 0 RT-PCR, (529 bp – TOX-SE,AS primers) Karakavuk et al. (2018)
Eurasian jay (Garrulus glandarius) Slovakia Tatra National Park 2 Sk 1 50.0 PCR (TGR1E – TGR1E-1,2 primers) PCR-RFLP using SAG2 – type III Turčeková et al. (2014)
New Zealand falcon (Falco novaeseelandiae) New Zealand Palmerston 35 H, Li, Lu, Sp 2 5.7 N-PCR (Pppk-dhps) 7 PCR-RFLP markers – genotype incomplete Mirza et al. (2017)
Northern goshawk (Accipiter gentilis) Slovakia Tatra National Park 2 Sk 1 50.0 PCR (TGR1E – TGR1E-1,2 primers) PCR-RFLP using SAG2 – type II Turčeková et al. (2014)
Peregrine falcon (Falco peregrinus) Turkey Çiğli 1 B, H 1 100.0 RT-PCR, (529 bp – TOX-SE,AS primers) Karakavuk et al. (2018)
Galliformes
Quail (Coturnix coturnix) China Shandong 390 Sk 25 6.4 N-PCR (B1) 10 PCR-RFLP markers – ToxoDB genotype #9 in 5 Cong et al. (2017b)
Turkeys (Meleagris gallopavo) Iran Fars 54 B, Sk, T 33 66.0 N-PCR (B1). Samples from abattoirs ND Sarkari et al. (2014)
Gruiformes
Eurasian coot (Fulica atra) China Jilin 25 H or Lu 1 4.0 N-PCR (B1) 10 PCR-RFLP markers – ToxoDB genotype incomplete Zhang et al. (2015)
Passeriformes
Hooded crow (Corvus cornix) Iran Tehran 55 B 9 16.3 N-PCR (GRA6) PCR-RFLP using GRA6 – type III Abdoli et al. (2018)
Hooded crow (Corvus cornix) Israel Haifa 101 B 1 1.0 PCR (529 bp – TOX4,5 primers) 11 PCR-RFLP markers – type II Salant et al. (2013)
House sparrows (Passer domesticus) Brazil Bahia, Pernambuco 40 B 10 10.0 N-PCR (ITS1) ND Gondim et al. (2010)
House sparrows (Passer domesticus) Brazil Pernambuco 10 B 3 30.0 N-PCR (B1) Vilela et al. (2011)
House sparrows (Passer domesticus) China Lanzhou 39 B, H, Lu 11 28.2 N-PCR (B1) 9 PCR-RFLP markers – ToxoDB genotype #3 in 3 and a new type in 1 Cong et al. (2013)
House sparrows (Passer domesticus) China Several 22 Sk 1 4.5 N-PCR (B1) 10 PCR-RFLP markers – ToxoDB genotype #3 Huang et al. (2012)
House sparrows (Passer domesticus) Iran Khuzestan 64 B, H 17 26.5 PCR (B1 – TG1,2 primers) PCR-RFLP using GRA6, 1 type II and 16 type III Khademvatan et al. (2013)
House sparrows (Passer domesticus) Iran Tehran 200 B 17 8.5 LAMP, PCR (529 bp – B3,F3, TOX4,5 primers) ND Abdoli et al. (2016)
Magpie (Pica pica) Italy Tuscany 41 Bl, H 15 36.6 N-PCR (B1) 5 PCR-RFLP markers – 8 type II and 7 type III Mancianti et al. (2020)
Magpie (Pica pica) Slovakia Tatra National Park 3 Sk 1 33.3 PCR (TGR1E – TGR1E-1,2 primers) PCR-RFLP using SAG2 – type III Turčeková et al. (2014)
Magpie (Pica pica) Spain Several 33 B 5 12.8 N-PCR (529 bp – TOX9,11 primers) ND Darwich et al. (2012)
Olive-backed pipit (Anthus hodgsoni) China Hunan 44 B 1 2.2 N-PCR (B1) Liu et al. (2019)
Oriental skylark (Alauda gulgula) China Lanzhou, Tianshui 34 B 3 8.8 N-PCR (B1) 10 PCR-RFLP markers – type II variant in 2, ToxoDB genotype #3 Cong et al. (2014)
Starling (Sturnus vulgaris) Iran Khuzestan 39 B, H 5 12.8 PCR (B1 – TG1,2 primers) PCR-RFLP using GRA6, 2 type II and 3 type III Khademvatan et al. (2013)
Thrush nightingale (Luscinia luscinia) Turkey Konak 1 B, H 1 100.0 RT-PCR, (529 bp – TOX-SE,AS primers) Karakavuk et al. (2018)
Tree sparrows (Passer montanus) China Hunan 131 B 11 8.4 N-PCR (B1) 10 PCR-RFLP markers – ToxoDB genotype #10 in 3 sparrows Liu et al. (2019)
Tree sparrows (Passer montanus) China Several 35 Sk 1 2.8 N-PCR (B1) 10 PCR-RFLP markers – ToxoDB genotype #10 Huang et al. (2012)
Yellow-breasted bunting (Emberiza aureola) China Hunan 26 B 1 3.8 N-PCR (B1) Liu et al. (2019)
Phoenicopteriformes
Great flamingo (Phoenicopterus roseus) Turkey Konak 1 B, H 1 100.0 RT-PCR, (529 bp – TOX-SE,AS primers) Karakavuk et al. (2018)
Psittaformes
Black-headed gull (Chroicocephalus ridibundus) Italy NS 4 B, H 4 100.0 N-PCR (B1) ND Nardoni et al. (2019)
Black-headed gull (Chroicocephalus ridibundus) Poland Several 2 B, H, Li, Sk 1 50.0 PCR (B1) 5 PCR-RFLP markers type II/III Sroka et al. (2019)
Strigiformes
Barn owl (Tyto alba) Turkey Çiğli, Konak 2 B, H 2 100.0 RT-PCR, (529 bp – TOX-SE,AS primers). Tg isolated 15 Microsatellite markers – ToxoDB #1 or #3 in 1, #2 in 1 Karakavuk et al. (2018)
Eurasian eagle-owl (Bubo bubo) Turkey Kemalpaşa, Salihli 2 B, H 2 100.0 RT-PCR, (529 bp – TOX-SE,AS primers) 15 Microsatellite markers – mixed type in 1 Karakavuk et al. (2018)
Little owl (Athene noctua) Turkey Çiğli 1 B, H 1 100.0 RT-PCR, (529 bp – TOX-SE,AS primers) Karakavuk et al. (2018)
Morepork (Ninox novaeseelandiae) New Zealand Palmerston 36 H, Li, Lu, Sp 3 8.3 PCR (Pppk-dhps) 7 PCR-RFLP markers – genotype incomplete Mirza et al. (2017)
Struthioniformes
Ostrich (Struthio camelus) Brazil São Paulo 38 B 25 65.7 PCR (529 bp and 18S rRNA – TOX4,5 and Tg18s48F,359R primers). Tg isolated 10 PCR-RFLP markers – ToxoDB #161 and #206 in 2 da Silva and Langoni (2016)
Ostrich (Struthio camelus) Egypt Ismailia 120 Bl 9 7.5 N-PCR (B1) ND El-Madawy and Metawea (2013)
Suliformes
Australasian harrier (Circus approximans) New Zealand Palmerston 46 H, Li, Lu, Sp 4 8.7 PCR (Pppk-dhps) 7 PCR-RFLP markers – genotype incomplete Mirza et al. (2017)
Baikal teal (Anas formosa) China Jilin 50 H or Lu 11 22.0 N-PCR (B1) 10 PCR-RFLP markers – ToxoDB genotype #9 in 2 Zhang et al. (2015)
Common pheasants (Phasianus colchicus) China Several 98 Sk 2 2.0 N-PCR (B1) 10 PCR-RFLP markers – ToxoDB genotype #3 Huang et al. (2012)
Common pheasant (Phasianus colchicus) Czech Republic Several 350 B, H, Sk 12 3.4 RT-PCR, (B1,529 bp), Tg genotyped 6 PCR-RFLP markers – 1 type II, 4 type III, 4 type II/III Skorpikova et al. (2018)
Dalmatian pelican (Pelecanus crispus) Turkey Çiğli 1 B, H 1 100.0 RT-PCR, (529 bp – TOX-SE,AS primers) Karakavuk et al. (2018)
Eurasian jays (Garrulus glandarius) Spain Several 23 B 5 21.7 N-PCR (529 bp – TOX9,11 primers) ND Darwich et al. (2012)
Eurasian siskin (Carduelis spinus) China Lanzhou 41 B 5 12.2 N-PCR (B1) 10 PCR-RFLP markers – type II variant in 2, ToxoDB #3 Cong et al. (2014)
Great cormorant (Phalacrocorax carbo) Turkey Çiğli 1 B, H 1 100.0 RT-PCR, (529 bp – TOX-SE,AS primers). Tg isolated Karakavuk et al. (2018)

B, brain; Bl, blood; H, heart; G, gizzard; Li, liver; Lu, lung; Sk, muscle; Sp, spleen; Tg, Toxoplasma gondii; ND, not done; NS, not stated; PCR, polymerase chain reaction; N-PCR, nested PCR; RT-PCR, real-time PCR; PCR, polymerase chain reaction; PCR-RFLP, Restriction fragment length polymorphism.

Turkeys are considered resistant to clinical toxoplasmosis and there were no reports of clinical toxoplasmosis since 2009. Experimentally, turkeys inoculated intravenously with T. gondii tachyzoites or oocysts orally remained healthy, irrespective of the dose (Bangoura et al., 2013; Zöller et al., 2013; Hotop et al., 2014; Maksimov et al., 2018). A kinetic ELISA was developed based on a mixture of recombinant dense granule antigens GRA7 and GRA8 using sera from turkeys inoculated intravenously with Me49 tachyzoites; SAG1 antigen was not suitable in this ELISA using recombinant SAG1 (Koethe et al., 2011). In a subsequent study, information on a large panel of 101 synthetic peptides was obtained on sera from 18 turkeys intravenously inoculated with tachyzoites of 3 strains of T. gondii (RH-Type I, Me49-Type II and NED-Type III). The authors concluded that by using selected peptides, it was possible to serotype strains up to 9 weeks post-inoculation (p.i.) (Maksimov et al., 2018). Antibodies peaked at 5–7 weeks p.i., using the SAG1-ELISA, and the results varied with the T. gondii isolate. Similar results were obtained by the indirect fluorescent antibody assay (IFA) (Maksimov et al., 2018).

In turkeys orally inoculated with oocysts, the parasite was widely disseminated in turkey tissues (Bangoura et al., 2013). Inoculated turkeys were euthanized 6 or 12 weeks p.i. and parasite distribution was assessed by polymerase chain reaction (PCR); no difference was found with respect to 6 or 12 weeks p.i. Brain, heart and drumstick were most frequently infected tissues. The route of inoculation could affect the distribution of parasite DNA. In turkeys inoculated intravenously with tachyzoites, liver, pectoral muscle, heart and brain were affected in decreasing order (Zöller et al., 2013). Judging from the histopathological results, the number of T. gondii in turkey tissues was low. Tissue cysts were found in imprints of 1 liver, and 2 pectoral muscles of turkeys parenterally inoculated with tachyzoites (Zöller et al., 2013). By using magnetic-capture PCR and 100 g samples, most T. gondii were found in the brain and heart (Koethe et al., 2015). Parasite burden was higher in the drumstick vs pectoral muscles.

Ducks (Anas spp.) and geese

Ducks are important for the economy of some countries, especially China. Ducks are a good source of meat and eggs for human consumption. To our knowledge, there are no reports of clinical toxoplasmosis in domestic ducks or geese, but antibodies are common (Tables 4 and 5).

Table 4.

Seroprevalence of Toxoplasma gondii in domestic ducks

Country Area Source No. tested No. positive % Positive Test Cut-off Remarks Reference
China Chongqing NS 635 – FR 84 13.3 MAT 1:25 Tg isolated. Location, type of raising AS Zhao et al. (2015)
527 – caged 35 6.6
China Guangzhou Abattoirs 349 56 16.0 MAT 1:5 6 had MAT titers of 1:40 or higher Yan et al. (2009)
China Jilin Farms 268 29 0.8 LATa 1:64 Li et al. (2020)
China Lanzhou Abattoirs 111 – caged 7 6.3 MAT 1:5 Cong et al. (2012)
223 – FR 31 13.9
China Liaoning Farms 268 26 9.7 MAT 1:25 Wang et al. (2014)
China Shenyang Abattoirs 146 – caged 11 7.5 MAT 1:25 Yang et al. (2012)
122 – FR 15 12.3
Czech Republic Several Abattoirs 360 52 14.0 IFA 1:40 Bártová et al. (2009)
Egypt Behera Abattoirs 151 21 13.9 MAT 1:25 AbouLaila et al. (2011)
Egypt Kafr El-Sheikh Farms 58 32 55.0 IHAa 1:80 Harfoush and Tahoon (2010)
Egypt 5 regions Market 142 15 10.5 ELISA IHC 3 positive. Region AS Ibrahim et al. (2018)
Germany Lower Saxony 61 farms 2534 145 5.7 ELISA – SAG1 1:200 Protection AS to indoors kept animals Maksimov et al. (2011)
Iraq Al-Qadisiya Farms 50 28 56.0 LATa 1:2 Alkhaled et al. (2012)
Iran Mazandaran Market 87 40 46.0 MAT 1:20 Amouei et al. (2018)
Malaysia Johor, Kedah, Melaka, Perak Farms, FR 205 30 14.6 MAT 1:6 Tg DNA and genotyping Puvanesuaran et al. (2013)
Poland Lublin Farms 33 7 21.2 MATa 1:40 Sroka et al. (2010)
Senegal Dakar, Saint-Louis Households 306 16 5.2 MAT 1:20 Tg isolated Galal et al. (2019)

NS, not stated; ELISA, enzyme-linked immunosorbent assay; IFA, indirect fluorescent antibody test; IHAT, indirect haemagglutination test; LAT, latex agglutination test; MAT, modified agglutination test (Dubey and Desmonts, 1987); FR, free range; Tg, Toxoplasma gondii; AS, association; IHC, immunohistochemical.

a

IHA (Toxo-IHA Fumouze Diagnostics, France); LAT (PLASMATECH Co., UK); MAT (Toxo-Screen DA®, Biomerieux, Lyon, France). This is the same test as MAT.

Table 5.

Seroprevalence of Toxoplasma gondii in domestic goose

Country Area Source No. tested No. positive % Positive Test Cut-off Remarks Reference
China Guangdong Farms 274 41 14.9 MAT 1:5 Yan et al. (2011b)
China Guangdong Farms 520 9 1.7 MAT Age, management Wang et al. (2012)
China Hainan Farms 600 102 17.0 IHAa 1:64 Presence of cats, hygiene AS. Tg DNA and genotyping Rong et al. (2014)
China Jilin Farms 379 50 13.2 IHAa 1:64 Li et al. (2020)
China Liaoning Farms 128 9 7.0 MAT 1:25 Wang et al. (2014)
China Shenyang Abattoirs 83 – caged 5 6.0 MAT 1:25 Yang et al. (2012)
45 – FR 4 8.9
Czech Republic Bohemia, Olomouc Abattoirs 178 77 43.0 IFA 1:40 Bártová et al. (2009)
Germany Lower Saxony 13 farms 373 94 25.2 ELISA-SAG1 1:200 Protection AS to indoors kept animals Maksimov et al. (2011)
Iran Mazandaran Market 5 5 100.0 MAT 1:20 Amouei et al. (2018)
USA Maryland Hunted 169 12 7.1 MAT 1:25 Canada geese, Tg isolated Verma et al. (2016)

AS, association; FR, free-range; Tg, Toxoplasma gondii; ELISA, enzyme-linked immunosorbent assay; IFA, indirect fluorescent antibody test; IHA, indirect haemagglutination assay; MAT, modified agglutination test (Dubey and Desmonts, 1987).

a

IHA kit (Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, China).

Toxoplasma gondii DNA was found in 9 (7.8%) of 115 muscle samples from 115 ducks and 2 of 42 geese (4.7%) (Zou et al., 2017). Viable T. gondii was isolated from tissues of ducks in China, France and Malaysia (Table 3).

Ostriches (Struthio camelus) and other ratites

Ratite meat is lean and its human consumption is increasing. Serologic data are summarized in Table 6. Antibodies to T. gondii were detected up to 80.0% of sera (Table 6).

Table 6.

Seroprevalence of Toxoplasma gondii in ratites

Host Country Area Source No. tested No. positive % positive Test Cut-off Remarks Reference
Emus (Dromaius novaehollandiae) Brazil Goiás Farm 16 8 50.0 MAT 1:25 Gallo et al. (2019)
Ostriches (Struthio camelus) Brazil Mato Grosso, Rio Grande do Sul, São Paulo 3 Farms 46 8 17.4 MAT 1:16 Almeida et al. (2013)
Ostriches (Struthio camelus) Brazil Rio de Janeiro Abattoirs 20 16 80.0 MAT 1:25 Gallo et al. (2019)
Ostriches (Struthio camelus) Brazil São Paulo Farms 195 28 14.3 MAT 1:16 MAT titer 1:16384 in 2 ostriches Contente et al. (2009)
Ostriches (Struthio camelus) Brazil São Paulo Abattoir, 4 farms 344 38 11.0 MAT 1:8 Tg DNA and parasite isolation, Water source, presence of non-ostrich feces AS da Silva and Langoni (2016)
Ostriches (Struthio camelus) China Hebei, Henan Abattoirs 315 20 6.4 MAT 1:25 Tg DNA and parasite isolation Feng et al. (2017)
Ostriches (Struthio camelus) Egypt Ismailia Farm 120 15 12.5 MAT 1:25 Tg DNA. 5 (4.2%) IgM positive El-Madawy and Metawea (2013)
Rheas (Rhea americana) Brazil Espírito Santo, Goiás, São Paulo Farm 68 18 26.5 MAT 1:25 Gallo et al. (2019)
Rheas (Rhea americana) Brazil Rio Grande do Sul, Santa Catarina 2 Farms 20 10 50.0 MAT 1:25 Almeida et al. (2013)

MAT, modified agglutination test (Dubey and Desmonts, 1987); AS, association; Tg, Toxoplasma gondii.

Viable T. gondii was demonstrated in ostrich tissues. In a Brazilian report, T. gondii was detected in brains of ostriches and in soil samples from paddocks (da Silva and Langoni, 2016). Brain (25 g) samples of 38 seropositive and 20 seronegative ostriches were bioassayed in mice. Toxoplasma gondii was isolated from 14 seropositive but not from seronegative ostriches. All strains were apparently pathogenic for mice. Toxoplasma gondii DNA was found in peritoneal exudates of mice inoculated from tissues of 8 ostriches, and in brains of mice inoculated with 6 ostrich samples. Nothing was said concerning finding viable T. gondii. Of interest is the report of finding T. gondii-like oocysts microscopically in soil samples from 5 of 20 paddocks; all were confirmed by PCR. In repeat sampling, T. gondii-like oocysts were found microscopically in soil samples from 9 of 20 paddocks and results were confirmed by PCR. It should be noted that only a few oocysts are normally present in soil and their detection is a challenge (J.P.D. own observation).

In marked contrast to the Brazilian report, in a Chinese study, T. gondii DNA was not detected in any of the 293 hearts and 77 brains of ostriches (Feng et al., 2017).

A study in Egypt found T. gondii DNA in the blood of 9 of 120 ostriches (El-Madawy and Metawea, 2013). These authors also tested tissues of 5 ostriches that had died of toxoplasmosis-like illness; T. gondii DNA was found in the brains of 5, hearts of 3 and leg muscle of 1 (El-Madawy and Metawea, 2013) (Comment J.P.D. – tissues of these ostriches should be examined histologically for verification of molecular results).

Other wild avian species

Data on T. gondii seroprevalence, viable parasite and DNA characterization are arranged by scientific order of birds, by region and chronologically in Tables 2, 3 and 7.

Table 7.

Serologic prevalence of antibodies to Toxoplasma gondii in wild birds

Order, common name, (scientific name) Country Region No. tested No. positive % Positive Test Cut-off Notes Reference
Accipitriformes
Bald eagle (Haliaeetus leucocephalus) Czech Republic Zoos 1 1 100.0 LATa Bártová et al. (2018)
Bald eagle (Haliaeetus leucocephalus) USA Alabama 13 12 92.3 MAT 1:25 Love et al. (2016)
Bearded vulture (Gypaetus barbatus) Spain Several 15 6 42.8 MAT 1:25 Cabezón et al. (2011)
Black kite (Milvus migrans) Portugal Central, northern 1 1 100.0 MAT 1:20 Lopes et al. (2011)
Black kite (Milvus migrans) Senegal Dakar 2 2 100.0 MAT 1:20 Galal et al. (2019)
Black kite (Milvus migrans) Spain Several 17 5 29.4 MAT 1:25 Cabezón et al. (2011)
Bonelli's eagle (Aquila fasciata) Spain Several 9 1 11.1 MAT 1:25 Cabezón et al. (2011)
Booted eagle (Hieraaetus pennatus) Spain Southern 1 1 100.0 MAT 1:25 Cano-Terriza et al. (2015)
Broad-winged hawk (Buteo platypterus) USA Alabama 20 6 30.0 MAT 1:25 Love et al. (2016)
Cinereous vulture (Aegypius monachus) Czech Republic Zoos 11 7 64.0 LATa Bártová et al. (2018)
Cinereous vulture (Aegypius monachus) Spain Several 23 6 26.0 MAT 1:25 Cabezón et al. (2011)
Common buzzard (Buteo buteo) Portugal Central, northern 26 18 69.2 MAT 1:20 Lopes et al. (2011)
Cooper's hawk (Accipiter cooperii) USA Alabama 12 6 50.0 MAT 1:25 Love et al. (2016)
Crested goshawk (Accipiter trivirgatus) Taiwan Several 41 7 17.0 MATb 1:40 Chen et al. (2015)
Eagle (Aquila spp.) Mexico Durango 2 1 50.0 MAT 1:25 Location AS Alvarado-Esquivel et al. (2011)
Eurasian buzzard (Buteo buteo) Italy Northern 12 1 8.3 MATb 1:40 Gazzonis et al. (2018)
Eurasian buzzard (Buteo buteo) Spain Several 96 49 51.0 MAT 1:25 Cabezón et al. (2011)
Eurasian griffon (Gyps fulvus) Czech Republic Zoos 4 3 75.0 LATa Bártová et al. (2018)
Eurasian sparrow hawk (Accipiter nisus) Italy Northern 2 1 50.0 MATb 1:40 Gazzonis et al. (2018)
Golden eagle (Aquila chrysaetos) Spain Several 8 5 62.5 MAT 1:25 Cabezón et al. (2011)
Golden eagle (Aquila chrysaetos) USA Alabama 1 1 100.0 MAT 1:25 Love et al. (2016)
Griffon vulture (Gyps fulvus) Israel 4 Areas 101 40 39.6 MAT 1:25 Salant et al. (2013)
Griffon vulture (Gyps fulvus) Spain Several 175 31 17.7 MAT 1:25 Cabezón et al. (2011)
Montagu's harrier (Circus pygargus) Spain Several 7 1 14.3 MAT 1:25 Cabezón et al. (2011)
Northern goshawk (Accipiter gentilis) Portugal Central, northern 3 3 100.0 MAT 1:20 Lopes et al. (2011)
Northern goshawk (Accipiter gentilis) Spain Several 5 2 40.0 MAT 1:25 Cabezón et al. (2011)
Osprey (Pandion haliaetus) Spain Several 7 2 28.5 MAT 1:25 Cabezón et al. (2011)
Red kite (Milvus milvus) Spain Several 3 1 33.3 MAT 1:25 Cabezón et al. (2011)
Red-shouldered hawk (Buteo lineatus) USA Alabama 41 9 21.9 MAT 1:25 Love et al. (2016)
Red tailed hawk (Buteo jamaicensis) USA Alabama 71 22 30.9 MAT 1:25 Love et al. (2016)
Roadside hawk (Rupornis magnirostris) Brazil São Paulo 1 1 100.0 MAT 1:16 Gonçalves et al. (2013)
Serpent eagle (Spilornis cheela) Taiwan Several 43 20 46.5 MATb 1:40 Chen et al. (2015)
Short-toed Snake-eagle (Circaetus gallicus) Spain Several 10 5 50.0 MAT 1:25 Cabezón et al. (2011)
Spanish Imperial eagle (Aquila adalberti) Spain Several 146 25 17.0 MAT 1:25 Cabezón et al. (2011)
Tawny eagle (Aquilla rapax) Czech Republic Zoos 1 1 100.0 LATa Bártová et al. (2018)
Western marsh-harrier (Circus aeruginosus) Italy Northern 2 1 50.0 MATb 1:40 Gazzonis et al. (2018)
Western marsh-harrier (Circus aeruginosus) Spain Several 6 3 50.0 MAT 1:25 Cabezón et al. (2011)
Anseriformes
Bar-headed goose (Anser indicus) Spain Córdoba 11 1 9.1 MAT 1:25 Cano-Terriza et al. (2015)
Barnacle goose (Branta leucopsis) Europe Russia, Svalbard, The Netherlands 1087 98 9.0 MATb 1:40 See text Sandström et al. (2013)
Black swan (Cygnus atratus) Portugal Zoo 7 1 14.3 MATb 1:20 Tidy et al. (2017)
Canada goose (Branta canadensis) Canada Saskatoon 71 2 2.8 MATb 1:40 Al-Adhami et al. (2016)
Canada goose (Branta canadensis) Canada Nunavik 148 16 10.8 MATa 1:25 Bachand et al. (2019)
Canada goose (Branta canadensis) Europe The Netherlands 38 3 7.9 MATb 1:40 See text Sandström et al. (2013)
Common teal (Anas crecca) Italy Tuscany 41 3 7.3 MATb 1:10 PCR positive in 1 seropositive Mancianti et al. (2013)
Coscoroba swan (Coscoroba coscoroba) Czech Republic Zoos 2 1 50.0 LATa Bártová et al. (2018)
Domestic geese (Anser anser) Europe The Netherlands 161 13 8.1 MATb 1:40 See text Sandström et al. (2013)
Emperor goose (Chen canagica) Spain Southern 2 1 50.0 MAT 1:25 Cano-Terriza et al. (2015)
Eurasian green-winged teal (Anas crecca) Iran Mazandaran 20 12 60.0 MAT 1:20 Amouei et al. (2018)
Garganey (Spatula querquedula) Senegal Dakar 28 8 28.5 MAT 1:20 Galal et al. (2019)
Geese (Anser sp.) Brazil Paraná 149 27 18.1 IFA 1:25 Higher prevalence in animals from urban parks Konell et al. (2019)
Lesser snow geese (Chen caerulescens) Canada Karrak Lake Nunavut 121 43 36.0 IFA 1:20 Results higher than MATb at 1:40 dilution Elmore et al. (2014)
Lesser snow geese (Chen caerulescens) Canada Nunavut 233 66 28.3 ELISA Elmore et al. (2015)
Lesser snow geese (Chen caerulescens) Canada Nunavik 8 2 25.0 MATa 1:25 Bachand et al. (2019)
Ross's geese (Chen rossi) Canada Nunavut 234 76 32.4 ELISA Elmore et al. (2015)
Mallard duck (Anas brachyrhynchus) Europe Denmark, Svalbard 573 59 10.2 MATb 1:40 See text Sandström et al. (2013)
Mallard duck (Anas platyrhynchos) Mexico Durango 2 1 50.0 MAT 1:25 Location AS Alvarado-Esquivel et al. (2011)
Mallard duck (Anas platyrhynchos) Iran Mazandaran 20 9 45.0 MAT 1:20 Amouei et al. (2018)
Mallard duck (Anas platyrhynchos) Italy Tuscany 17 2 11.7 MATb 1:10 PCR positive in 1 seropositive Mancianti et al. (2013)
Mallard duck (Anas platyrhynchos) Portugal Zoo 4 3 75.0 MATb 1:20 Tidy et al. (2017)
Mallard duck (Anas platyrhynchos) Spain Several 6 2 33.3 MAT 1:25 Cabezón et al. (2011)
Mallard duck (Anas platyrhynchos) Spain Southern 4 1 25.0 MAT 1:25 Cano-Terriza et al. (2015)
Mallard duck (Anas platyrhynchos) Taiwan Several 1 1 100.0 MATb 1:40 Chen et al. (2015)
Mandarian duck (Aix galericulata) Portugal Zoo 6 3 50.0 MATb 1:20 Tidy et al. (2017)
Mexican duck (Anas diazi) Mexico Durango 2 1 50.0 MAT 1:25 Location AS Alvarado-Esquivel et al. (2011)
Mute swan (Cygnus olor) USA Northeastern 632 54 8.5 MAT 1:25 Tg isolated Dubey et al. (2013)
Northern pintail (Anas acuta) Spain Several 1 1 100.0 MAT 1:25 Cabezón et al. (2011)
Orinoco (Neochen jubata) Brazil Goiás 41 35 85.3 IFA 1:20 N. caninum in 12.1% André et al. (2019)
Paradise shelduck (Tadorna variegata) Czech Republic Zoos 1 1 100.0 LATa Bártová et al. (2018)
Ross's geese (Chen rossi) Canada Karrak Lake Nunavut 123 48 39.0 IFA 1:20 Results higher than MATb at 1:40 dilution Elmore et al. (2014)
Shoveller duck (Anas clypeata) Italy Tuscany 11 2 18.1 MATb 1:10 PCR positive in 1 seropositive Mancianti et al. (2013)
Sudanese duck (Anas platyrhynchos) Egypt Several 142 15 10.5 ELISA Region AS. IHC Ibrahim et al. (2018)
Swan goose (Anser cygnoides) Portugal Zoo 1 1 100.0 MATb 1:20 Tidy et al. (2017)
Tundra swan (Cygnus columbianus) China Jiangxi 9 2 22.2 IHAb 1:64 Luo et al. (2017)
Wood duck (Aix sponsa) Portugal Zoo 7 2 28.6 MATb 1:20 Tidy et al. (2017)
Bucerotiformes
Eurasian hoopoe (Upupa epops) Spain Several 1 1 100.0 MAT 1:25 Cabezón et al. (2011)
Cariamiformes
Crested seriema (Cariama cristata) Brazil Minas Gerais, São Paulo 1 1 100.0 MAT 1:5 Vitaliano et al. (2014)
Charadriformes
Audouin's gull (Larus audouinii) Spain Alboran Island 46 1 2.2 MAT 1:25 Age, food source, year AS Cabezón et al. (2016)
Caracara (Caracara plancus) Brazil Pernambuco 115 6 5.2 MAT 1:25 Silva et al. (2018a)
Common kestrel (Falco tinnunculus) Italy Northern 18 1 5.5 MATb 1:40 Gazzonis et al. (2018)
Common snipe (Gallinago gallinago) Italy Tuscany 8 2 25.0 MATb 1:10 Mancianti et al. (2013)
Common snipe (Gallinago gallinago) Pakistan Punjab 4 1 25.0 LATb 1:64 Age, health status AS Naveed et al. (2019)
Yellow-legged gull (Larus michahellis) Europe France, Spain, Tunisia 988 nests 233 23.6 ELISAb ELISA in 1122 egg yolk. Different prevalence between colonies AS Gamble et al. (2019)
Yellow-legged gull (Larus michahellis) Spain Iberian Peninsula 479 109 22.8 MAT 1:25 Age, food source, year AS Cabezón et al. (2016)
Ciconiiformes
Black stork (Ciconia nigra) Spain Several 1 0 0 MAT 1:25 Cabezón et al. (2011)
White stork (Ciconia ciconia) Spain Several 64 9 14.1 MAT 1:25 Cabezón et al. (2011)
Columbiformes
Dove (Spilopelia sp.) Senegal Dakar 1 1 100.0 MAT 1:20 Galal et al. (2019)
Eared dove (Zenaida auriculata) Brazil Paraná 206 46 22.3 MAT 1:16 Location AS. Tg isolated de Barros et al. (2014)
Eurasian collared dove (Streptopelai decaocto) Pakistan Punjab 10 2 20.0 LATb 1:64 Age, health status AS Naveed et al. (2019)
Feral pigeon (Columba livia var. domestica) Spain Southern 142 13 9.2 MAT 1:25 Cano-Terriza et al. (2015)
Gray-fronted dove (Leptotila rufaxilla) Brazil Paraíba 5 1 20.0 MAT 1:25 Andrade et al. (2016)
Oriental turtle dove (Streptopelia orientalis) Taiwan Several 16 4 25.0 MATb 1:40 Chen et al. (2015)
Picazuro pigeon (Patagioenas picazuro) Brazil Minas Gerais, São Paulo 3 1 33.3 MAT 1:5 Vitaliano et al. (2014)
Rock pigeon (Columba livia) Brazil São Paulo 126 0 0 MAT 1:5 Tg not isolated by bioassay of any of 126 pigeons de Godoi et al. (2010)
Rock pigeon (Columba livia) Brazil São Paulo 120 1 0.8 IFA 1:20 de Sousa et al. (2010)
Rock pigeon (Columba livia) Brazil São Paulo 238 12 5.0 MAT 1:8 Tg not isolated de Lima et al. (2011)
Rock pigeon (Columba livia) China Guangdong 275 24 8.7 MAT 1:5 Yan et al. (2011a)
Rock pigeon (Columba livia) China Several 963 104 10.8 IHAb 1:64 Age, gender AS Zhang et al. (2019)
Rock pigeon (Columba livia) Egypt Several 310 42 13.5 ELISA IHC Ibrahim et al. (2018)
Rock pigeon (Columba livia) Israel Several 495 20 4.0 MAT 1:5 Climate, population near to human settlement Salant et al. (2009)
Rock pigeon (Columba livia) Mexico Durango 521 7 1.9 MAT 1:25 Location AS. Tg isolated Alvarado-Esquivel et al. (2011)
Rock pigeon (Columba livia) Portugal Lisbon 1507 39 2.6 MATb 1:20 Tg isolated in cell cultures seeded with 13 of 20 seropositive pigeons Waap et al. (2012)
Rock pigeon (Columba livia) Russia Circus animals 28 10 35.7 ELISAa Sivkova and Neprimerova (2017)
Rock pigeon (Columba livia) Spain Córdoba 142 13 9.2 MAT 1:25 Cano-Terriza et al. (2015)
Rock pigeon (Columba livia) Taiwan Several 62 1 1.6 MATb 1:40 Chen et al. (2015)
Rock pigeon (Columba livia) Turkey Niğde 216 2 0.9 DT 1:16 Karatepe et al. (2011)
Rock pigeon (Columba livia) USA Colorado 129 5 3.9 MAT 1:25 Dubey et al. (2010)
Rock pigeon (Columba livia) USA Tennessee 1 1 100.0 MAT 1:32 Gerhold et al. (2017)
Spotted-necked dove (Streptopelia chinensis) Taiwan Several 17 5 29.4 MATb 1:40 Chen et al. (2015)
Cuculiformes
Coucal (Centropus sp.) Senegal Dakar 1 1 100.0 MAT 1:20 Galal et al. (2019)
Falconiformes
Common kestrel (Falco tinnunculus) Italy Parma 238 62 26.1 MATb 1:25 Age, year sampled, AS Iemmi et al. (2020)
Common kestrel (Falco tinnunculus) Spain Several 13 4 30.7 MAT 1:25 Cabezón et al. (2011)
Crested caracara (Caracara plancus) Brazil Minas Gerais, São Paulo 2 1 50.0 MAT 1:5 Vitaliano et al. (2014)
Eurasian hobby (Falco subbuteo) Italy Northern 3 1 33.3 MATb 1:40 Gazzonis et al. (2018)
Lesser kestrel (Falco naumanni) Spain Several 5 2 40.0 MAT 1:25 Cabezón et al. (2011)
Peregrine falcon (Falco peregrinus) Spain Several 4 1 25.0 MAT 1:25 Cabezón et al. (2011)
Yellow-headed caracara (Milvago chimachima) Brazil São Paulo 3 2 66.6 MAT 1:16 Gonçalves et al. (2013)
Galliformes
Common quail (Coturnix coturnix) China 3 Provinces 620 59 9.5 MAT 1:5 Cong et al. (2017b)
Common quail (Coturnix coturnix) Mexico Durango 7 1 14.2 MAT 1:25 Location AS Alvarado-Esquivel et al. (2011)
Common quail (Coturnix coturnix) Turkey Niğde 144 0 0 DT NS Kiliç et al. (2017)
Guinea fowl (Numida meleagris) Brazil Minas Gerais 10 2 20.0 MAT 1:10 Tg isolated Dubey et al. (2011a)
Guinea fowl (Numida meleagris) Brazil Rio de Janeiro 114 14 12.3 MAT 1:16 Ferreira et al. (2013)
Guinea fowl (Numida meleagris) Senegal Dakar 13 1 7.7 MAT 1:20 Tg isolated Galal et al. (2019)
Hawaiian goose (Branta sandvicensis) USA Hawaii 94 26 27.6 MAT 1:25 48% in Molokai, 23% in Maui, and 21% in Kauai Work et al. (2016)
Silver pheasant (Laphura nycthemera) Portugal Zoo 6 1 16.6 MATb 1:20 Tidy et al. (2017)
Rock ptarmigan (Lagopus muta) Canada Saskatoon 25 1 4.0 MATb 1:40 Al-Adhami et al. (2016)
Gruiformes
Common coot (Fulica atra) Spain Several 1 1 100.0 MAT 1:25 Cabezón et al. (2011)
Common moorhen (Gallinula chloropus) Pakistan Punjab 5 1 20.0 LATb 1:64 Age, health status AS Naveed et al. (2019)
Common moorhen (Gallinula chloropus) Spain Several 1 1 100.0 MAT 1:25 Cabezón et al. (2011)
Eurasian coot (Fulica atra) Iran Mazandaran 10 5 50.0 MAT 1:20 Amouei et al. (2018)
Grey crowned crane (Balearica regulorum) Portugal Zoo 4 0 0.0 MATb 1:20 Tidy et al. (2017)
Japanese crane (Grus japonensis) Portugal Zoo 2 1 50.0 MATb 1:20 Tidy et al. (2017)
Rail (Rallus sp.) Senegal Dakar 2 1 50.0 MAT 1:20 Galal et al. (2019)
Otidiformes
Great bustard (Otis tarda) Spain Several 7 1 14.2 MAT 1:25 Cabezón et al. (2011)
Passeriformes
Ashy-throated casiornis (Casiornis fuscus) Brazil Bahia 1 1 100.0 MAT 1:25 Andrade et al. (2016)
Black drongo (Dicrurus macrocercus) Pakistan Punjab 9 1 11.1 LATb 1:64 Age, health status AS. Naveed et al. (2019)
Buff-browed foliage-gleaner (Syndactyla rufosuperciliata) Brazil São Paulo 7 4 57.1 MAT 1:5 Gennari et al. (2014)
Common babbler (Turdoides caudatus) Pakistan Punjab 2 1 50.0 LATb 1:64 Age, health status AS. Naveed et al. (2019)
Common myna (Acridotheres tristis) Pakistan Punjab 11 2 18.1 LATb 1:64 Age, health status AS Naveed et al. (2019)
Common raven (Corvus corax) Spain Northeast 113 91 80.5 MAT 1:25 Year sampled AS Molina-López et al. (2012)
Creamy-bellied thrush (Turdus amaurochalinus) Brazil São Paulo 2 1 50.0 MAT 1:5 Gennari et al. (2014)
Curve-billed thrasher (Toxostoma curvirostre) Mexico Durango 2 1 50.0 MAT 1:25 Alvarado-Esquivel et al. (2011)
European goldfinch (Carduelis carduelis) Spain Several 1 1 100.0 MAT 1:25 Cabezón et al. (2011)
European starling (Sturnus vulgaris) USA Colorado 27 4 15.0 MAT 1:50 Dubey et al. (2010)
Formosan blue magpie (Urocissa caerulea) Taiwan Several 16 6 37.5 MATb 1:40 Chen et al. (2015)
Golden-crowned warbler (Basileuterus culicivorus) Brazil São Paulo 12 2 16.7 MAT 1:5 Gennari et al. (2014)
Great-tailed grackle (Quiscalus mexicanus) Mexico Durango 18 5 27.8 MAT 1:25 Location AS Alvarado-Esquivel et al. (2011)
Hooded crow (Corvus cornix) Israel 6 areas 101 48 47.5 MAT 1:25 Geographic location AS Salant et al. (2013)
Hooded crow (Corvus cornix) Italy Pisa 120 4 3.3 MATb 1.25 Mancianti et al. (2020)
House crow (Corvus splendens) Israel Eilat 16 2 12.5 MAT 1:25 Salant et al. (2013)
House crow (Corvus splendens) Pakistan Punjab 17 6 35.3 LATb 1:64 Age, health status AS Naveed et al. (2019)
House sparrow (Passer domesticus) Brazil Bahia, Pernambuco 293 3 1.0 IHA 1:32 Tg DNA Gondim et al. (2010)
House sparrow (Passer domesticus) Brazil Pernambuco 151 91 60.3 IHAa 1:16 Tg DNA Vilela et al. (2011)
House sparrow (Passer domesticus) China Lanzhou 313 39 12.4 MAT 1:5 Tg DNA in 11 tissues of 39 seropositive Cong et al. (2013)
House sparrow (Passer domesticus) Pakistan Punjab 9 1 11.1 LATb 1:64 Age, health status AS Naveed et al. (2019)
Indian silverbill (Lonchura malabarica) Pakistan Punjab 4 2 50.0 LATb 1:64 Age, health status AS Naveed et al. (2019)
Jackdaw crow (Corvus monedula) Israel Ganei Yavne 5 2 40.0 MAT 1:25 Salant et al. (2013)
Java sparrows (Lonchura oryzivora) China Beijing, Shangqiu 350 120 34.3 MAT 1:20 Gender, colour AS Huang et al. (2019)
Jungle babbler (Turdoides striatus) Pakistan Punjab 6 1 16.6 LATb 1:64 Age, health status AS Naveed et al. (2019)
Lesser woodcreeper (Xiphorhynchus fuscus) Brazil São Paulo 2 1 50.0 MAT 1:5 Gennari et al. (2014)
Magpie (Pica pica) Italy Pisa 651 41 6.2 MATb 1:40 Mancianti et al. (2020)
Magpie (Pica pica) Taiwan Several 22 10 45.5 MATb 1:40 Chen et al. (2015)
Pale-breasted thrush (Turdus leucomelas) Brazil São Paulo 1 1 100.0 MAT 1:5 Gennari et al. (2014)
Pied crow (Corvus albus) Senegal Dakar 2 2 100.0 MAT 1:20 Galal et al. (2019)
Plain antvireo (Dysithamnus mentalis) Brazil São Paulo 11 5 45.4 MAT 1:5 Gennari et al. (2014)
Red-crowned ant-tanager (Habia rubica) Brazil São Paulo 13 8 61.5 MAT 1:5 Gennari et al. (2014)
Red vented bulbul (Pycnonotus cafer) Pakistan Punjab 11 3 27.2 LATb 1:64 Age, health AS Naveed et al. (2019)
Ruby-crowned tanager (Tachyphonus coronatus) Brazil São Paulo 6 1 16.7 MAT 1:5 Gennari et al. (2014)
Rufous-bellied thrush (Turdus rufiventris) Brazil São Paulo 18 15 83.3 MAT 1:5 Gennari et al. (2014)
Rufous-breasted leaftosser (Sclerurus scansor) Brazil São Paulo 1 1 100.0 MAT 1:5 Gennari et al. (2014)
Rufous gnateater (Conopophaga lineata) Brazil São Paulo 15 6 40.0 MAT 1:5 Gennari et al. (2014)
Squamate antbird (Myrmeciza squamosa) Brazil São Paulo 4 3 75.0 MAT 1:5 Gennari et al. (2014)
White-browed warbler (Basileuterus leucoblepharus) Brazil São Paulo 5 1 20.0 MAT 1:5 Gennari et al. (2014)
White-eyed foliage-gleaner (Automolus leucophthalmus) Brazil São Paulo 14 3 21.4 MAT 1:5 Gennari et al. (2014)
White-lined tanager (Tachyphonus rufus) Brazil Bahia 16 1 6.2 MAT 1:25 Andrade et al. (2016)
White-necked thrush (Turdus albicollis) Brazil São Paulo 5 5 100.0 MAT 1:5 Gennari et al. (2014)
White-shouldered fire-eye (Pyriglena leucoptera) Brazil São Paulo 11 4 36.4 MAT 1:5 Gennari et al. (2014)
White-spotted woodpecker (Veniliornis spilogaster) Brazil São Paulo 1 1 100.0 MAT 1:5 Gennari et al. (2014)
White-throated woodcreeper (Xiphocolaptes albicollis) Brazil São Paulo 2 1 50.0 MAT 1:5 Gennari et al. (2014)
White-vented myna (Acridotheres javanicus) Taiwan Several 1 1 100.0 MATb 1:40 Chen et al. (2015)
White wagtail (Motacilla alba) Pakistan Punjab 11 1 9.0 LATb 1:64 Age, health AS Naveed et al. (2019)
Pelecaniformes
Black-crowned night heron (Nycticorax nycticorax) Taiwan Several 2 2 100.0 MATb 1:40 Chen et al. (2015)
Buff-necked ibis (Theristicus caudatus) Brazil Minas Gerais, São Paulo 2 2 100.0 MAT 1:5 Vitaliano et al. (2014)
Cattle egret (Bubulcus ibis) Brazil Fernando de Noronha 197 157 79.7 MAT 1:5 Costa et al. (2012)
Cattle egret (Bubulcus ibis) Taiwan Several 7 4 57.1 MATb 1:40 Chen et al. (2015)
Eurasian spoonbill (Platalea leucorodia) Spain Several 81 5 6.2 MAT 1:25 Cabezón et al. (2011)
Grey heron (Ardea cinerea) Spain Several 5 3 60.0 MAT 1:25 Cabezón et al. (2011)
Malay night heron (Gorsachius melanolophus) Taiwan Several 21 5 23.8 MATb 1:40 Chen et al. (2015)
Purple heron (Ardea purpurea) Spain Several 4 0 0 MAT 1:25 Cabezón et al. (2011)
Roseate spoonbill (Platalea ajaja) Czech Republic Zoos 6 1 16.6 LATa Bártová et al. (2018)
Phaethontiformes
Red-billed tropic bird (Phaeton aethereus) Brazil Abrolhos Archipelago 25 7 28.0 MAT 1:5 Gennari et al. (2016b)
Phoenicopteriformes
Lesser flamingo (Phoenicopterus minor) Portugal Zoo 3 1 33.0 MATb 1:20 Tidy et al. (2017)
Piciformes
Black vulture (Coragyps atratus) Brazil São Paulo 121 16 13.2 MAT 1:5 Gennari et al. (2017)
Black vulture (Coragyps atratus) USA Alabama 8 1 12.0 MAT 1:25 Love et al. (2016)
Crescent-chested puffbird (Malacoptila striata) Brazil São Paulo 3 2 66.7 MAT 1:5 Gennari et al. (2014)
Psittaformes
Alexandrine parakeets (Psittacula eupatria) China Beijing, Weifang 61 4 6.5 MAT 1:5 Season AS Zhang et al. (2014)
Black-goggled tanager (Lanio melanops) Brazil São Paulo 15 5 33.3 MAT 1:5 Gennari et al. (2014)
Black-headed gull (Chroicocephalus ridibundus) China Dianchi Lake 659 131 19.9 MAT 1:5 Miao et al. (2014)
Budgerigars (Melopsittacus undulatus) China Beijing, Weifang 202 18 8.9 MAT 1:5 Season AS Zhang et al. (2014)
Cockatiels (Nymphicus hollandicus) China Beijing, Weifang 22 3 13.6 MAT 1:5 Season AS Zhang et al. (2014)
Lovebirds (Agapornis sp.) China Beijing, Weifang 26 1 3.8 MAT 1:5 Season AS Zhang et al. (2014)
Rainbow lorikeet (Trichoglossus haematodus) Czech Republic Zoos 4 1 25.0 LATa Bártová et al. (2018)
Red-tailed Amazon parrot (Amazona brasiliensis) Brazil Paraná 51 0 0 IFA 1:16 Sato et al. (2020)
Turquoise-fronted Amazon (Amazona aestiva) Brazil São Paulo 71 7 10.0 MAT 1:16 Gonçalves et al. (2013)
Sphenisciformes
Galapagos penguin (Spheniscus mendiculus) Republic of Ecuador Galapagos 298 7 2.3 MAT 1:50 Region AS Deem et al. (2010)
Humboldt penguin (Spheniscus humboldti) Czech Republic Zoos 4 2 50.0 LATa Bártová et al. (2018)
Magellanic penguin (Spheniscus magellanicus) Brazil Bahia, Espírito Santo, Rio de Janeiro 145 18 12.4 MAT 1:20 Tg not isolated Acosta et al. (2018)
Magellanic penguin (Spheniscus magellanicus) Brazil Espírito Santo, Santa Catarina, São Paulo 100 28 28.0 MAT 1:20 Captive Gennari et al. (2016a, 2016b)
Magellanic penguin (Spheniscus magellanicus) Chile Magdalena Island 132 57 43.2 MAT 1:20 Acosta et al. (2019)
Struthioniformes
Greater rhea (Rhea americana) Portugal Zoo 1 1 100.0 MATb 1:20 Tidy et al. (2017)
Suliformes
Brown booby (Sula leucogaster) Brazil Abrolhos Archipelago 19 9 47.4 MAT 1:5 Gennari et al. (2016a, 2016b)
Masked booby (Sula dactylatra) Brazil Abrolhos Archipelago 23 8 34.8 MAT 1:5 Gennari et al. (2016a, 2016b)
Flightless cormorants (Phalacrocorax harrisi) Republic of Ecuador Galapagos 258 6 2.3 MAT 1:50 Tg isolated Deem et al. (2010)
Strigiformes
Barn owl (Tyto alba) Brazil São Paulo 4 2 50.0 MAT 1:16 Gonçalves et al. (2013)
Barn owl (Tyto alba) Spain Several 45 6 13.3 MAT 1:25 Cabezón et al. (2011)
Barred owl (Strix varia) USA Alabama 54 25 46.2 MAT 1:25 Tg isolated Love et al. (2016)
Burrowing owl (Athene cunicularia) Brazil Minas Gerais, São Paulo 5 1 20.0 MAT 1:5 Vitaliano et al. (2014)
Collard scops owl (Otus bakkamoena) Taiwan Several 74 20 27.0 MATb 1:40 Chen et al. (2015)
Common scops-owl (Otus scops) Spain Several 4 1 25.0 MAT 1:25 Cabezón et al. (2011)
Eastern screech owl (Megascops asio) USA Alabama 16 2 12.0 MAT 1:25 Love et al. (2016)
Eurasian eagle owl (Bubo bubo) Portugal Central, northern 3 1 33.3 MATb 1:20 Lopes et al. (2011)
Eurasian eagle owl (Bubo bubo) Spain Several 144 98 68.0 MAT 1:25 Cabezón et al. (2011)
Grass owl (Tyto capensis) Taiwan Several 20 3 15.0 MATb 1:40 Chen et al. (2015)
Great horned owl (Bubo virginianus) USA Alabama 28 13 46.4 MAT 1:25 Love et al. (2016)
Little owl (Athene noctua) Italy Northern 17 4 23.5 MATb 1:40 Gazzonis et al. (2018)
Little owl (Athene noctua) Spain Several 19 3 15.7 MAT 1:25 Cabezón et al. (2011)
Long-eared owl (Asio otus) Spain Several 9 1 11.1 MAT 1:25 Cabezón et al. (2011)
Long-eared owl (Asio otus) Taiwan Several 4 1 25.0 MATb 1:40 Chen et al. (2015)
Short-eared owl (Asio flammeus) Taiwan Several 11 1 9.0 MATb 1:40 Chen et al. (2015)
Spotted owlet (Athene brama) Pakistan Punjab 9 3 33.3 LATb 1:64 Age, health AS Naveed et al. (2019)
Tawny owl (Strix aluco) Italy Northern 12 1 8.3 MATb 1:40 Gazzonis et al. (2018)
Tawny owl (Strix aluco) Portugal Central, northern 5 1 20.0 MAT 1:20 Lopes et al. (2011)
Tawny owl (Strix aluco) Spain Several 38 5 13.6 MAT 1:25 Cabezón et al. (2011)

ELISA, enzyme-linked immunosorbent assay. Unless stated otherwise, ELISA=ELISA in-house; IFA, indirect fluorescent antibody test; IHA, indirect haemagglutination assay; LAT, latex agglutination test; MAT, modified agglutination test (Dubey and Desmonts, 1987); Tg, Toxoplasma gondii; AS, positive association; IHC, immunohistochemical.

a

ELISA Vekto-Toxo antibodies kits (Vektor-Best, Russian Federation); IHA (ImmunoHAI-Toxoplasmose, Wama Diagnostic, São Carlos, SP, Brazil); WAMA Diagnosis. Imuno-HAI; LAT Pastorex toxo, Bio-Rad Laboratories s.r.o., Prague, Czech Republic; MAT (New Life Diagnostic LLC, Carlsbad, CA, USA).

b

ELISA ID Screen Avian Toxoplasmosis Indirect (ID VET, France); IHA (Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, China); LAT Latex agglutination test (Antec Diagnostic Products, Bridport, Dorset, UK); MAT (Toxo-Screen DA®, Biomerieux, Lyon, France). This is the same test as MAT.

Carnivorous birds

Prevalence of T. gondii in carnivorous birds reflects the prevalence of the parasite in their prey. For example, owls consume hundreds of rodents yearly. In a recent survey of kestrels at an airport site in Italy, T. gondii antibodies were detected in 33.3% of kestrel trapped during 2016 and 14.3% of 91 kestrel during 2017; seroprevalence was lower in juveniles than in adults (Iemmi et al., 2020). Based on the remnants of animals in the feces of kestrels, rodents were a major component of the kestrel diet (Iemmi et al., 2020). In a large sample size of raptors in Spain, T. gondii antibodies were found in 51.0% of 96 common buzzard, 17.7% of 175 Griffon vulture and 17.0% of Spanish Imperial eagle (Cabezón et al., 2011). Among the raptors, vultures are considered resistant to clinical toxoplasmosis and other microbial infections in general. In 2 large surveys, T. gondii antibodies were found in 17.7% of 175 Gyps fulvus in Spain (Cabezón et al., 2011) but twice (39.6% of 101) more were infected in Israel (Salant et al., 2013); the results are comparable because modified agglutination test (MAT) at the serum dilution of 1:25 was used in both studies. Finding of T. gondii DNA in tissues of 43 of 48 (89.6%) wild birds (mostly carnivorous) in Turkey suggests a very high prevalence of the parasite in local rodents (Karakavuk et al., 2018). Of 281 raptors from a rehabilitation centre in the USA, 34.5% were seropositive with highest (46.0%) prevalence in Barred owl (Love et al., 2016)

Viable T. gondii was isolated (Table 2) and DNA demonstrated (Table 3) from several species of carnivorous birds. The highest prevalence of DNA was in Buteo buteo from Turkey; 23 (92.0%) of 25 were infected (Table 3).

Experimental infection of crested caracara with T. gondii

An experiment on caracara in Brazil provided useful information. Caracaras are raptors/scavengers with wide distribution. Eight caracaras that could not be released from a rehabilitation centre were used in this experiment. They were serologically negative to T. gondii by IFA (cut-off 1:40). Five caracaras were fed rodent (Calomys callosus) infected with Me49 strain of T. gondii. The birds were euthanized 68 days p.i. Blood was collected for serological examination weekly or more often. Seroconversion occurred between 5 and 14 days p.i. The serological response was erratic. In 1 bird (No.6), transient antibody was observed on day 14 and then at 45 days p.i. The highest antibody titer was 1:650. Antibodies became undetectable at 68 days p.i. in 2 birds. By immunohistochemistry, T. gondii was detected in the hearts and muscles of all 5 caracaras and demonstrated by bioassay in the hearts of 2 birds. Three control caracaras not inoculated with T. gondii remained serologically negative to T. gondii (Vitaliano et al., 2010).

Herbivorous/insectivorous birds

Seroprevalence varied depending on the geography, host and the habitat (Table 7). For example, in the ground feeding pigeon (Columba livia), seroprevalences varied from 1.6 to 35.7% (Table 7). In a large sample size of pigeons, a low prevalence (1.9% of 521) was reported; the pigeons were from Durango City, Mexico that has a dry climate (Alvarado-Esquivel et al., 2011). This low prevalence is likely related to the effect of climate on oocyst survival. In another survey from cold climate, only 3.9% of pigeons from Colorado, USA were seropositive (Dubey et al., 2010). Toxoplasma gondii antibodies were detected in 11.8% of 35 pigeons and 9.5% of 620 quails that were destined for human consumption in China (Cong et al., 2012, 2017a). Finding of T. gondii DNA in the muscles of 6.4% of 390 quails indicates that the parasite was present in these birds destined for human consumption (Cong et al., 2017b). Similarly, T. gondii DNA was detected in 5.4% of 280 wild ducks and 3.4% of 350 common pheasants hunted for human consumption in the Czech Republic (Skorpikova et al., 2018).

Toxoplasma gondii infection in sea gulls and other scavenging birds indicates contamination of marine/lake waters with oocysts. In one study, 22.8% of 479 yellow-legged gulls (Larus michahellis) were seropositive to T. gondii (Cabezón et al., 2016). In another investigation, T. gondii antibodies (assessed by ELISA) were detected in 233 of 1122 freshly laid L. michahellis eggs (Gamble et al., 2019). The freshness of eggs was verified by immersion in water; such eggs do not float in water (Gamble et al., 2019). The occurrence of T. gondii antibodies in 4 other species of sea birds (Sula spp. and Phaeton spp.) from Brazil (Gennari et al., 2016b) and in 19.9% of 659 black-headed gulls (Chroicocephalus ridibundus) in China (Miao et al., 2014) indicates that T. gondii infection is common in sea birds. Toxoplasma gondii oocysts from feline feces can be washed into sewage and freshwater run-off and contaminate marine waters. Antibodies to T. gondii were detected in 8.5% of 632 mute swans (Cygnus olor) from the USA and viable T. gondii was isolated from hearts of 3 (Dubey et al., 2013). Mute swan is an invasive species present in US waters; infection in these hosts is indicative of oocyst contamination.

Reports of viable T. gondii and parasite DNA from tissues of wild birds are summarized in Tables 2 and 3, respectively.

Experimental infection of pigeons with T. gondii

Little information is available concerning the efficacy of different diagnostic methods for the detection of T. gondii infection in wild birds. A diagnostically useful experimental study was conducted in pigeons in Brazil (de Godoi et al., 2010). Sixteen seronegative pigeons (C. livia) were inoculated orally with 50 oocysts of the T. gondii VEG strain and divided into 4 groups of 4 pigeons each and euthanized at 15, 30, 45 and 60 days p.i. One pigeon died of toxoplasmosis on day 23 p.i. and tissue cysts were found in its brain; other pigeons remained healthy. All pigeons were seronegative by the MAT (cut-off 1:5) and IFA (cut-off 1:4) before feeding oocysts and developed antibody titers of more than 1:4000 by both MAT and IFA. Tissues (brain, heart, muscle) were tested by bioassay in mice and by PCR. Viable T. gondii was isolated from 5 of 12 pigeons and DNA was detected by nested PCR in tissues of 7 of 12 pigeons. By serology and bioassay, none of the 160 naturally exposed pigeons were positive for T. gondii providing further evidence of the validity of serology (de Godoi et al., 2010).

Migratory birds

Toxoplasma gondii infections in migratory birds are of epidemiological significance because the parasite can be transported with the host and the introduction of T. gondii in new geographic locations can disturb the equilibrium (Gennari et al., 2014). For example, ToxoDB genotype #9 (Chinese 1) occurs mainly in China but has been occasionally found in other countries, including the USA and Mexico. Whether migratory birds could have transported the parasite is a possibility. Antibodies to T. gondii were detected in Magellanic penguins in Chile and these birds migrate throughout South American coastline (Acosta et al., 2018, 2019).

A study of migratory and non-migratory geese revealed interesting results (Sandström et al., 2013). A total of 2675 birds, both adults and juveniles, of 4 goose species (Anser anser, n = 266; A. brachyrhynchus, n = 787; Branta canadensis, n = 79; B. leucopsis, n = 1543) at Arctic brood-rearing areas in Russia and on Svalbard, and temperate wintering grounds in the Netherlands and Denmark (migratory populations) as well as temperate brood-rearing grounds (the Netherlands, non-migratory populations) were tested for T. gondii antibodies (MAT, 1:40). Only adult B. leucopsis were seropositive: T. gondii antibodies were found in 14.8% of 811 adults from Svalbard and 17.7% of 157 from Russia sampled during summer but not in any of the 456 juveniles sampled in summer (Arctic) and summer and winter in the Netherlands. Similar results were obtained with 3 other species of goose (Sandström et al., 2013). The authors concluded that geese become infected postnatally at wintering groups.

In a study of migratory birds and resident Nearctic brown lemmings (Lemmus trimucronatus) from Arctic Canada, T. gondii infections were detected only in migratory geese (Table 1) and not in resident lemmings (Elmore et al., 2015).

Clinical toxoplasmosis in wild birds

Little is known of clinical toxoplasmosis among wild birds in nature. Among all avian species, most severe toxoplasmosis has been reported in canaries (Serinus canaria), Hawaiian geese (Branta sandvicensis) and Hawaiian crows (Corvus hawaiiensis); reports between 1988 and 2009 were summarized previously (Dubey, 2010). In the past decade, few cases of fatal toxoplasmosis were documented in captive birds or those from National Parks (Table 8).

Table 8.

Clinical toxoplasmosis in wild birds

Host Country Observations Diagnostic method Remarks Reference
Bar-shouldered dove (Geopelia humeralis) France A 6-year-old dove born in the zoo was found dead. Pneumonia was the main lesion and only lungs were studied histologically. Numerous tachyzoites were seen in lesions. Diagnosis was confirmed ultrastructurally Histopathology and TEM Rigoulet et al. (2014)
Black-footed penguin (Spheniscus demersus) The Netherlands 3 captive penguins in a zoo died within a day after neurological signs were observed. All 3 had similar lesions. Liver, lungs, intestines, and brain had intralesional tachyzoites. Diagnosis confirmed by IHC and TEM Histopathology, IHC, TEM Ploeg et al. (2011)
Guinea fowl (Numida meleagris) Brazil Nine of 29 guinea fowl on a farm became ill and 6 died. Two guinea fowl were necropsied. Both birds had disseminated toxoplasmosis with intralesional T. gondii. One of the 2 sera tested had a MAT titer of 1:1280. Diagnosis was confirmed by IHC Serology, histopathology, IHC Vielmo et al. (2019)
Kereru (Hemiphaga novaeseelandiae) New Zealand 2 kererus were found dead in a wildlife park. Pneumonia was the main lesion in both birds. Tachyzoites and tissue cysts were associated with lesions Histopathology, IHC Limited genotyping revealed atypical Type II Howe et al. (2014)
Lovebird (Agapornis roseicollis) Australia A female pet bird developed ataxia 1 year after being caged. It had head tilt, tremors and was euthanized. The most important histologic findings were enlargement of spleen, encephalitis and cerebral haemorrhage IHC, PCR ToxoDB genotype #3 (Type II) DNA isolated from frozen brain sample Cooper et al. (2015)
North Island brown kiwi (Apteryx mantelli) New Zealand A juvenile hand raised kiwi was found dead. Most important lesion was hepatitis with tissue cysts. Lesions were seen in other organs, but protozoa were not identified Histopathology, IHC Limited genotyping revealed atypical Type II Howe et al. (2014)
North Island kaka (Nestor meridionalis) New Zealand 1 kaka was found dead in wild. Most important lesion was hepatitis with tissue cysts. Lesions were seen in other organs, but protozoa were not identified Histopathology, IHC Limited genotyping revealed atypical Type II Howe et al. (2014)
Valley quail (Callipepla californica) Brazil A captive raised quail recently acquired from another facility died suddenly with clinical signs of diarrhoea and dyspnoea. Disseminated toxoplasmosis involving most organs, many tachyzoites present IHC, PCR, T. gondii DNA in many tissues T. gondii DNA from kidney genotyped with 10 PCR-RFLP markers revealed ToxoDB genotype #87 Casagrande et al. (2015)

IHC, immunohistochemistry; PCR, polymerase chain reaction; TEM, transmission electron microscopy; PCR-RFLP, Restriction fragment length polymorphism.

Hawaiian crows (C. hawaiiensis) and Nene goose (B. sandvicensis) are endangered native species in Hawaii. Nene is the largest extant terrestrial bird in Hawaiian Island and the official state bird (Work et al., 2015). Of 300 Nene examined at necropsy, inflammatory conditions were found in 69 and 16.0% of these were thought to be toxoplasmosis (Work et al., 2015). Thus, 11 geese died of toxoplasmosis. The presence of cats in colonies near the native bird sites is thought to be a source of T. gondii oocysts for the birds (Lepczyk et al., 2020).

Two episodes of clinical toxoplasmosis were reported in guinea fowl in the USA and Brazil. An owner in Mississippi, USA lost 7 of 20 backyard guinea fowls. Birds were lethargic before death. Two dead birds were necropsied. Severe lesions of multifocal necrosis, fibrin exudation and inflammation of spleen, lung, heart and bone marrow were seen microscopically in 1 and mild lesions in the other guinea fowl. Toxoplasma gondii was identified histologically in tissues of both birds and the diagnosis was confirmed by PCR (Jones et al., 2012).

The Brazilian outbreak of clinical toxoplasmosis was reported in guinea fowl on a chicken farm; the farm had 47 chickens (G. domesticus) and 29 guinea fowl (Vielmo et al., 2019). Of these 76 birds, 22 (13 chickens and 9 guinea fowl) had clinical signs and 15 (9 chickens, 6 guinea fowl) died. Two guinea fowl were examined at necropsy and both had toxoplasmosis (Table 8).

Genetic diversity of T. gondii isolates

PCR-RFLP genetic data based on extraction of DNA from host tissue are summarized in Table 9 and from the live tachyzoites in Table 10. A total of 102 samples from birds were genotyped in this summary (Table 10), including 75 from viable T. gondii isolates (Table 2) and 27 from DNA extracted from tissues of birds (Table 10). Overall, genotype distribution follows the global patterns recognized previously (Shwab et al., 2014; Su and Dubey, 2020), with ToxoDB genotypes #1 and #3 (collectively known as Type II), and genotype #2 (known as Type III) being dominant in Africa and Europe. Most genotypes identified in the Americas were diverse and different from those in the Old World. Of interest is the predominance of ToxoDB genotype #9 (Chinese 1) in China and its rare occurrence in Mexico (Alvarado-Esquivel et al., 2011; Shwab et al., 2014). Type I isolates (ToxoDB genotype #10) are considered rare worldwide. It was detected in a hunted turkey in 4 tree sparrows in China (Table 3). As this genotype is highly virulent to mice and relatively easy to isolate by bioassay, future study to obtain isolates for genotyping is needed to confirm the findings. Also, of interest is the finding of ToxoDB genotypes #4 and #5, together known as Type 12, in North America but their rare frequency from the rest of the world.

Table 9.

Toxoplasma gondii genotypes based on DNA directly from host tissue

Country Host No. 10 PCR-RFLP markers ToxoDB genotype Reference
China Alauda gulgula 2 #3 Cong et al. (2014)
China Anas formosa 2 #9 Zhang et al. (2015)
China Anas sp. 1 #9 Zou et al. (2017)
China Carduelis spinus 2 #3 Cong et al. (2014)
China Coturnix coturnix 5 #9 Cong et al. (2017a, 2017b)
China Passer domesticus 1 #3 Huang et al. (2012)
China Passer domesticus 4 #3 in 3 and possible new type in 1 Cong et al. (2013)
China Phasianus colchicus 1 #3 Huang et al. (2012)
China Passer montanus 1 #10 Huang et al. (2012)
China Passer montanus 3 #10 Liu et al. (2019)
Israel Corvus cornix 1 #1 Salant et al. (2013)
South Africa Streptopelia semitorquata 1 #1 or #3 (15 microsatellites) Lukášová et al. (2018)
USA Branta sandvicensis 4 #261 in 3, #262 in 1 Work et al. (2016)

Table 10.

Distribution of PCR-RFLP (ToxoDB) Toxoplasma gondii genotypes from wild birds from different continents/countries

Continent/country Total typed I ToxoDB #10 Classic types III ToxoDB#2 #4 #5 #6 #9 #11 #20 Others
II ToxoDB #1 or #3
Africa
Senegal 15 5 1 3 6 Galal et al. (2019)
Asia
China (22)a 4 9 8 1 Possible new type See Table 9
Israel (1)a 1 Salant et al. (2013)
Oceania
Australia 1 1 Cooper et al. (2015)
Europe
France 1 1 Aubert et al. (2010)
Turkey 9 7 2 Karakavuk et al. (2018)
Central America
Costa Rica 1 1 (#52) Dubey et al. (2009), Shwab et al. (2014)
South America
Brazil 19 5 1 1 12 (#8-1, #13-2, #17-1, #65-1, #108-1, #161-1, #182-2, #206-1, #290-2) da Silva and Langoni (2016), de Barros et al. (2014), Dubey et al. (2011b), Rêgo et al. (2018), Silva et al. (2018a, 2018b)
North America
Mexico 1 1 Alvarado-Esquivel et al. (2011), Shwab et al. (2014)
USA 32(4)a 1 6 4 2 6 13 (#15-1, #157-1, #167-1, #177-2, #216-2, # 61-3, #262-1, #266-1, #267-1) Cerqueira-Cézar et al. (2019), Dubey et al. (2010), Dubey et al. (2011b), Dubey et al. (2013), Love et al. (2016), Shwab et al. (2014), Verma et al. (2016), Yu et al. (2013)
Grand total 102 5 35 7 2 6 4 9 1 6 27
a

DNA from tissues. Twenty-seven of the 102 samples were DNA from bird tissues.

Conclusions

Here, we summarized seroprevalence, clinical disease, epidemiology and genetic diversity of T. gondii strains isolated from wild birds worldwide for the past decade. It is obvious that T. gondii infection in raptors is common and they are excellent sentinels to monitor T. gondii in rodents and small other animals. Detection of T. gondii antibodies in eggs offers a non-invasive sampling method. In one investigation, T. gondii antibodies (assessed by ELISA) were detected in 233 of 1122 freshly laid yellow-legged gulls (L. michahellis) eggs (Gamble et al., 2019). Finding antibodies in sea gulls indicates contamination of fresh and marine waters with T. gondii oocysts. In general, T. gondii infection in herbivorous birds is a good measure of oocyst contamination in the environment. Genetic studies revealed low genetic diversity in Europe, Asia, Africa and the USA, but higher diversity of T. gondii in South America. A study of migratory and non-migratory geese at Arctic brood-rearing areas in Russia and on Svalbard, and temperate wintering grounds in the Netherlands and Denmark (migratory populations) revealed that geese become infected postnatally at wintering groups (Sandström et al., 2013).

Acknowledgements

This research was supported in part by an appointment of Camila K. Cerqueira-Cézar and Fernando H. A. Murata to the Agricultural Research Service (ARS) Research Participation administered by the Oak Ridge Institute for Science and Education (ORISE) through an interagency agreement between the US Department of Energy (DOE) and the US Department of Agriculture (USDA). ORISE was managed by ORAU under DOE contract number DE-SC 0014664. All opinions expressed in this paper were the authors' and did not necessarily reflect the policies and views of USDA, ARS, DOE or ORAU/ORISE. We thank Dr Yurong Yang for help with Chinese references.

Financial support

This research received no specific grant from any funding agency, commercial or not-for-profit sectors.

Ethical standards

Not applicable.

Conflict of interest

None.

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