Balantidium Coli

GASTROINTESTINAL PARASITES IN GREATER RHEAS (RHEA AMERICANA) 1

AND LESSER RHEAS (RHEA PENNATA) FROM ARGENTINA 2

3

Rafael A. Martnez-Daz1, Mnica Beatriz Martella

2, Joaqun Luis Navarro

2, Francisco 4

Ponce-Gordo3

5

6

1 Departamento de Medicina Preventiva, Salud Pblica y Microbiologa, Facultad de 7

Medicina, Universidad Autnoma de Madrid, Av. Arzobispo Morcillo s/n, 28029 8

Madrid, Spain. 9

2 Centro de Zoologa Aplicada, Facultad de Ciencias Exactas, Fsicas y Naturales, 10

Universidad Nacional de Crdoba, Rondeau 798, Crdoba 5000, Argentina. 11

3 Departamento de Parasitologa, Facultad de Farmacia, Universidad Complutense de 12

Madrid, Plaza Ramn y Cajal s/n, 28040 Madrid, Spain. 13

14

Author for correspondence: 15

Francisco Ponce Gordo 16

Tel: +34 91 3941817 17

Fax: +34 91 3941815 18

e-mail: [email protected] 19

20

21

*

http://ees.elsevier.com/vetpar/viewRCResults.aspx?pdf=1&docID=8119&rev=3&fileID=176348&msid={FD86C5EB-5ACA-43CE-AB17-520A0E3D3C2A}

ABSTRACT 22

23

Few data exist on the parasites of ratites, especially from regions within their natural 24

range. It is only recently that extensive studies on the parasites of ostriches (Struthio 25

camelus) have been published, mainly from European countries where commercial 26

farming has expanded. Two species of ratites are native in South America: the lesser 27

rhea also known as Darwin's rhea (Rhea pennata) and the greater rhea (Rhea 28

americana). Both species are considered near threatened by the IUCN and are included 29

in the CITES Apendices I and II, respectively. Parasitological studies have conservation 30

implications, as they allow us to assess the risk of transmission of pathogens from 31

farmed ratites to wild populations. In this study 92 faecal samples from greater rheas 32

and 55 faecal samples from lesser rheas from different localitities in Argentine were 33

analyzed to determine their gastrointestinal parasites. In greater rheas the protozoa 34

(Balantidium coli-like and Entamoeba spp.) and helminths (Fasciola hepatica and 35

Deletrocephalus spp.). The protozoa had not previously been cited as parasites of 36

greater rheas in South America. Cysts and/or trophozoites of Balantidium coli-like were 37

found in 16.3% of the samples, while the prevalence of the remaining parasites was 38

below 10%. Lesser rheas harboured the protozoa Balantidium coli-like, Entamoeba spp. 39

and Chilomastix spp. as well as F. hepatica and nematode eggs and larvae. Balantidium 40

coli-like cysts were found in 20.0% of the samples, while the prevalence of the other 41

parasites remained below 5%. Some of them had not been cited as infecting lesser rheas 42

yet. 43

44

Keywords: Rhea americana; Rhea pennata; Protozoa; Helminths; Argentina 45

46

1. Introduction 47

48

The geographic range of the greater rhea (Rhea americana) extends from Eastern Brazil 49

to the Ro Negro river in central Argentina, whereas the lesser rhea (Rhea pennata = 50

Pterocnemia pennata following SACC, 2012) inhabits the plains of the Patagonia 51

region in the south of Argentina and Chile, as well as the Andean regions of these two 52

countries and Bolivia and Peru (BirdLife International, 2012a,b). Both species are 53

considered near threatened in the red list of the IUCN (BirdLife International, 2012a,b) 54

and are included in the CITES Apendices I and II. 55

56

Parasitological studies have conservation implications for threatened and endangered 57

species (Pedersen et al., 2007). With regard to rheas, the Argentinean Rhea Project 58

(Martella and Navarro, 2006) considers the reintroduction of farmed animals in the 59

wild. Thus, the identification of parasites that might affect rheas would allow to assess 60

the risk of transmission of pathogens from farmed birds to wild populations. Few works 61

on the endoparasites of greater rheas have been published in the last 20 years. Several 62

protozoa have been described from rheas in Europe (Cryptosporidium sp., Eimeria sp., 63

Balantidium sp., Entamoeba sp., Endolimax sp., Trichomonas sp., Giardia sp. and 64

Pleuromonas sp.; Ponce-Gordo et al., 2002) and several helminths have been described 65

mostly from South American birds: the nematodes Deletrocephalus dimidiatus, D. 66

cesarpintoi, Paradeletrocephalus minor (Strongyloidea), Trichostrongylus 67

colubriformis (Trichostrongyloidea), Odontospirura (=Vaznema) zschokkei, Sicarius 68

uncinipenis, Torquatoides crotophaga (Habronematoidea), Dicheilonema rheae 69

(Diplotriaenoidea) and Capillaria venteli (Trichinelloidea), the cestodes Houttuynia 70

struthionis, Chapmania tauricolis (Davaineidae) and Monoecocestus sp. 71

(Anoplocephalidae) and the trematodes Philophthalamus aweerensis 72

(Philophthalmidae) and Fasciola hepatica (Fasciolidae) (Giossa et al., 2004; 73

Zettermann et al., 2005; Comolli et al., 2006; Schuster, 2011). References to parasitism 74

in lesser rheas are even more scant and only three nematodes (D. dimidiatus, 75

Trichostrongylus sp. and Capillaria sp.) and one protozoon (Eimeria sp.) have been 76

recorded (Ewing et al., 1995; Chang Reissig et al., 2001). The aim of the present study 77

was to contribute to the knowledge on parasites of ratites by describing the 78

gastrointestinal parasites of farmed and wild greater and lesser rheas in Argentina. 79

80

2. Materials and methods 81

82

Faecal samples of captive-bred and wild birds were collected during 2007-2009. 83

Captive birds were raised in farms or zoos whose typology varied depending on the 84

rearing scheme adopted (intensive or semi intensive). In general, the intensive model 85

(smaller paddocks with a greater density of birds and a controlled diet) is implemented 86

by most zoos and farms, and the semi intensive model (larger facilities where birds 87

graze freely in the pasture and receive a comparative smaller quantity of controlled 88

food) is implemented in few farms (Navarro and Martella, 2002). The wild greater rheas 89

were in areas with pastures and grasslands; cattle, horses, sheep and hares (Lepus sp.) 90

were also present in the area. Wild lesser rheas were located in areas of medium to low 91

shrub steppes; co-occurring with hares, sheep and guanacos (Lama guanicoe). The 92

location and characteristics of the sampling sites are given in Supplementary Files 1 and 93

2. 94

95

Fresh faeces (up to 12 h old) were randomly collected from the soil avoiding 96

contamination with soil debris. All birds within each farm/wild group appeared healthy 97

at the time the samples were collected, except in one farm raising lesser rheas 98

(Supplementary File 1, site code 24; faeces were greenish and two birds died the week 99

before the sampling). Samples were fixed in 70% ethanol and sent to Spain for further 100

processing. Faecal concentrates were made following the formaldehyde-ether 101

concentration technique (Levine and Estevez, 1983) and the sediments were examined 102

on temporary slides stained with Lugols iodine; when necessary, permanent slides 103

stained with trichromic stain were made. 104

105

3. Results and discussion 106

107

Protozoal and helminth parasites were present in both species of rheas; their 108

morphological characteristics and prevalences are given in Supplementary Files 3 -5. 109

110

3.1. Greater rhea 111

112

The most frequent parasite found was Balantidium, which had previously been cited in 113

greater rheas bred in Spain (Ponce-Gordo et al., 2002). The taxonomic status of 114

Balantidium from ratites is not clear and it is possible that the species B. struthionis 115

described in ostriches may be a synonym of B. coli (Ponce-Gordo et al., 2011). 116

Presently available data do not support considering the species from rheas as different 117

from that of ostriches. We therefore record it as B. coli-like (following Ponce-Gordo et 118

al., 2011) until further comparative analyses can be performed. 119

120

The morphology of the one nucleated cysts of Entamoeba spp. s compatible with that 121

of E. struthionis, described in ostriches and rheas raised in Europe (Ponce-Gordo et al., 122

2002) and also reported in pigs and humans (Martnez-Daz and Ponce-Gordo, 2010). 123

However they are also morphologically compatible with the cysts of other one nucleated 124

mature cyst-forming species of Entamoeba. For this reason, we prefer to identify the 125

organism as E. bovis-like, using the name of the one nucleated mature cyst-forming 126

Entamoeba group as proposed by Levine (1961), until further, more detailed studies 127

could determine the species. 128

129

The trematode eggs found resemble those of F. hepatica, which has previously been 130

reported from common rheas in Brazil (Soares et al., 2007). The morphology and size of 131

the strongylid-like eggs found are compatible with Deletrocephalus spp. (150-160 x 70 132

m; Vaz, 1936; Taylor et al., 2000); they are slightly smaller than the eggs of P. minor 133

(190-200 x 60-70 m; Acomolli et al., 2006) and larger than those of O. zschokkei, 134

Sicarius sp, T. crotophaga or Trichostrongylus sp., which were in all cases less than 135

100 m in length (Vaz, 1936; Freitas and Lent, 1947; Pence and Casto, 1976; Yong, 136

2012). The most frequent intestinal nematode in greater rheas is D. dimidiatus 137

(Zettermann et al., 2005), which is considered of veterinary relevance due to its blood-138

feeding habits. In heavy infections it is responsible for the onset of an anaemia 139

syndrome in rheas (Craig and Diamond, 1996). 140

141

3.2. Lesser rhea 142

143

The most prevalent parasite was Balantidium sp. The cysts and trophozoites are 144

indistinguishable from those in greater rheas and have been identified as B. coli-like 145

until further comparative analyses have been done. 146

147

Two different Entamoeba spp. cysts were found in this study. One of them corresponds 148

to a one nucleated cyst-forming species which has been tentatively identified as E. 149

bovis-like as in the greater rheas. The second species found corresponds to an eight 150

nucleated cyst-forming Entamoeba. Entamoeba gallinarum has been described from 151

poultry. Its cysts are slightly smaller than those found in lesser rheas (12-15 m vs. 14-152

22 m) (McDowell, 1953). However, the present cysts are similar in size to the eight 153

nucleated cysts of an Entamoeba sp. found in greater rheas in Spain (20 m; Ponce-154

Gordo et al., 2002). They also fall within the range described for E. coli and E. muris 155

(10-33 and 9-20 m, respectively; Levine, 1985). We have identified these cysts as E. 156

coli-like, using the name of the morphological group as proposed by Levine (1961) until 157

further analyses have been done. 158

159

The morphology of the Chilomastix cysts observed in two samples is in agreement with 160

that of C. gallinarum, the only species of this genus described in birds. However, the 161

cyst morphology is very similar among the species of this flagellate and we currently 162

prefer not to assign our specimens to a definitive species. All species of Chilomastix are 163

considered non-pathogenic (Kulda and Nohnkov, 1978; Levine, 1985). 164

165

The morphology of the trematode eggs found in a single sample clearly resembles that 166

of F. hepatica eggs. Flukes had not previously been described in lesser rheas and this is 167

the first report of this parasite in this host species. The positive sample was obtained 168

from the farm where two adult birds had died the week before the samplings. The owner 169

reported whitish lesions in the liver. Their association with a Fasciola infection could, 170

however, not be established because the carcasses were destroyed prior to our arrival. 171

172

Capillariinae eggs were present in one sample from the Crdoba zoo. This subfamily 173

includes several genera in birds that can, however, not be identified by egg morphology 174

(Yabsley, 2008). Capillaria parvumspinosa has been described from rheas in Europe 175

(Railliet and Henry, 1911) and Chang Reissig et al. (2001) reported Capillaria sp. eggs 176

from lesser rheas. 177

178

Two different types of nematode eggs and of larvae were found in farmed birds. In one 179

sample, the egg size and morphology found resemble that of Trichostrongylus spp. 180

previously reported from lesser rheas by Chang Reissig et al. (2001). The other sample 181

contained eggs resembling those of spirurids. Several spirurids have been recorded from 182

greater rheas (see above) but none from lesser rheas. The nematode larvae could not be 183

identified and it is possible that they are non-parasitic, belonging to free-living species. 184

185

Acknowledgements 186

187

We thank the owners of ranches and farms who are too numerous to mention here, for 188

allowing us to collect samples on their properties. A. Manero helped us and provided 189

logistical support from the Universidad de la Patagonia Austral (sede Ro Gallegos) 190

throughout the field sampling in Santa Cruz province. G. Giacone checked the English. 191

This work was funded by the Direccin General de Investigacin of the Ministerio de 192

Educacin y Ciencia de Espaa (Project CGL2006-04343). MBM and JLN are 193

researchers of the Consejo Nacional de Investigaciones Cientficas y Tcnicas de 194

Argentina. 195

196

References 197

198

Acomolli, J., Ocayo, D., Santa Cruz, A.C., Milano, F., Roux, J.P., 2006. Aspectos 199

morfolgicos de Paradeletrocephalus minor (Molin, 1861) Freitas & Lentz, 200

1947, en and (Rhea americana), por medio de microscopio de luz y 201

microscopio electrnico de barrido. Parasitol. Latinoam. 61, 183-187. 202

BirdLife International, 2012a. Rhea americana. In: IUCN 2012. IUCN Red List of 203

Threatened Species, Version 2012.1. Available on http://www.iucnredlist.org. 204

Last accessed: September 6, 2012. 205

BirdLife International, 2012b. Rhea pennata. In: IUCN 2012. IUCN Red List of 206

Threatened Species, Version 2012.1. Available on http://www.iucnredlist.org. 207

Last accessed: September 6, 2012. 208

Chang Reissig, E., Olaechea, F., Robles, C.A., 2001. Parasitological findings of lesser 209

rhea, Pterocnemia Pennata (D'orbigny) in faeces from northern Patagonia, 210

Argentina. Arch. Med. Vet. 33, 247-251. 211

http://www.iucnredlist.org/http://www.iucnredlist.org/

Comolli, J.A., Ocayo, D., Santa Cruz, A.C., Milano, F., Roux, J.P., 2006. Aspectos 212

morfolgicos de Paradeletrocephalus minor (Molin, 1861) Freitas & Lent, 213

1947, en andu (Rhea americana), por medio de miscroscopio de luz y 214

microscopio electrnico de barrido. Parasitol. Latinoam. 61, 183-187. 215

Craig, T.M., Diamond, P.L., 1996. Parasites of ratites. In: Tully, Jr., T.N., Shane, S.M., 216

(Eds.), Ratite Management Medicine and Surgery. Krieger Publishing Company, 217

Malabar, pp. 115-126. 218

Ewing, M.L., Yonzon, M.E., Page, R.K., Brown, T.P., Davidson, W.R., 1995. 219

Deletrocephalus dimidiatus infestation in an adult rhea (Pterocnemia pennata). 220

Avian Dis. 39, 441-443. 221

Freitas, J.F.T., Lent, H., 1947. Spiruroidea parasitos de Rheiformes (Nematoda). 222

Mem. Inst. Oswaldo Cruz 45, 743760. 223

Giossa, G., Trenchi, H., Castro Ramos, M., Morgades, D., de Souza, G., Castro, O., 224

Casas, L., Salazar, M., Perdomo, L., Venzal, J., 2004. Hallazgos Bacteriolgicos 225

y Parasitolgicos en una faena de and (Rhea americana). Veterinaria 226

(Montevideo) 39, 11-16. 227

Kulda, J., Nohnkov, E., 1978. Flagellates of the human intestine and of intestines of 228

other species. In: Kreier, J.P. (Ed.), Parasitic Protozoa, Volumen II. Academic 229

Press, New York, pp. 1-138. 230

Levine, N.D.,1961. Protozoan parasites of domestic animals and of man. Burgess 231

Publishing Co., Minneapolis, 412 pp. 232

Levine, N.D., 1985. Veterinary Protozoology. Iowa State University Press, Ames, IA, 233

414 pp. 234

Levine, J.A., Estevez, E.G., 1983. Method for concentration of parasites from small 235

amount of feces. J. Clin. Microbiol. 18, 786788. 236

Martella, M.B., Navarrro, J.L., 2006. Proyecto and. Manejo de Rhea americana y R. 237

pennata en la Argentina. In: Bolkovic, M. L., Ramadori, D. (Eds.), Manejo de 238

Fauna Silvestre en la Argentina. Programas de uso sustentable. Direccin de 239

Fauna Silvestre, Secretara de Ambiente y Desarrollo Sustentable, Buenos Aires, 240

pp. 39-50. 241

Martnez-Daz, R.A., Ponce-Gordo, F. 2010. Taxonoma y filogenia del gnero 242

Entamoeba. Una revisin histrica. Rev. Ibero-Latinoam. Parasitol. 69, 5-37. 243

McDowell, S., 1953. A morphological and taxonomic study of the caecal protozoa of 244

the common fowl, Gallus gallus L. J. Morphol. 92, 337-399. 245

Navarro, J.L., Martella, M.B., 2002. Reproductivity and raising of Greater Rhea (Rhea 246

americana) and Lesser Rhea (Pterocnemia pennata) a review. Arch. 247

Geflgelk. 66, 124-132. 248

Pedersen, A.B., Jones, K.E., Nunn, C.L., Altizer, S., 2007. Infectious diseases and 249

extinction risk in wild mammals. Conserv. Biol. 21, 12691279 250

Pence, D.B., Casto, S., 1976. Torquatoides crotophaga Williams (Nematoda: 251

Spiruridae: Habronematinae) from cuculiform birds in Texas. Proc. Helminth. 252

Soc. Wash. 43, 2428. 253

Ponce-Gordo, F., Castro, A.T., Herrera, S., Garca Durn, B., Martnez-Daz, R.A. 254

2002. Parasites from farmed ostriches (Struthio camelus) and rheas (Rhea 255

americana) in Europe. Vet. Parasitol. 107, 137-160. 256

Ponce-Gordo, F., Fonseca-Salamanca, F., Martnez-Daz, R.A., 2011. Genetic 257

heterogeneity in Internal Transcribed Spacer genes of Balantidium coli 258

(Litostomatea, Ciliophora). Protist 162, 774-794. 259

Railliet, A., Henry, A., 1911. Les helminths du nandou. Bull. Soc. Nat. Acclim. Paris 260

58: 538-541, 573-582. 261

SACC (South American Classification Committee), 2012. A classification of the bird 262

species of South America, Version 9 August 2012. Available on 263

http://www.museum.lsu.edu/~Remsen/SACCBaseline.html. Last accessed: 264

September 6, 2012. 265

Schuster, R.K., 2011. Philophthalmus aweerensis n. sp. (Trematoda: Philophthalmidae) 266

found in a rhea (Rhea americana) in the United Arab Emirates. Parasitol. Res. 267

109, 1029-1033. 268

Soares, M.P., da Silva, S.S., Nizoli, L.Q., Felix, S.R., Schild, A.L., 2007. Chronic 269

fascioliasis in farmed and wild greater rheas (Rhea americana). Vet. Parasitol. 270

145, 168-171. 271

Taylor, M.A., Hunt, K.R., Smith, G., Otter, A., 2000. Deletrocephalus dimidiatus in 272

greater rheas (Rhea americana) in the UK. Vet. Rec. 146, 19-20. 273

Vaz, Z., 1936. Estudos sobre nematoides parasitas da ema (Rhea americana). Arch. 274

Inst. Biol. Sao Paulo 7, 253-266. 275

Yabsley, M.J., 2008. Capillarid Nematodes. In: Atkinson, C.T., Thomas, N.J., Hunter, 276

D.B. (Eds.), Parasitic Diseases of Wild Birds. John Wiley & Sons, Inc., pp. 463-277

497. 278

Yong, T.-S., 2012. Trichostrongylus. In: Liu, D. (Ed.), Molecular detection of human 279

parasitic pathogens. CRC Press, Boca Raton, pp. 705-710. 280

http://www.museum.lsu.edu/~Remsen/SACCBaseline.html

Zettermann, C.D., Nascimento, A.A., Tebaldi, J.A., Szabo, M.J.P., 2005. Observations 281

on helminth infections of free-living and captive rheas (Rhea americana) in 282

Brazil. Vet. Parasitol. 129, 169-172. 283

284

Supplementary File 1. Geographical locations and characteristics of the farmed and wild

populations of Rhea americana and Rhea pennata sampled in this study. The codes for

each site location correspond to those showed in the map in the Supplementary File 2.

R.a. R. americana; R.p. R. pennata. Age groups: 12 months old, adults. The sex of birds was not recorded

because it could not be established in chicks and juveniles; adult males and females

were maintained in mixed groups and it was not possible in most of the samples to

individually identify the animal that generated it.

Site GPS coordinates Host Rearing conditions Number of

code species samples

1 232611S, 640635W R. a. farm; 300 adults in 5 Ha. 8

2 243809S, 652259W R. a. farm; 7 adults in a 50x30 m2 paddock 3

3 312534S, 641028W R. a. zoo; 5 chicks in one paddock 1

9 adults in one paddock 2

R. p. 8 adults in one paddock 2



6 320026S, 633031W R. a. farm; 68 chicks in a 20x20 m2 paddock 3

72 juveniles in a 40x20 m2 paddock 3

48 adults in a 40x20 m2 paddock 3

7 321708S, 631320W R. a. 46 adults in 4 Ha. 3

8 334854S, 634737W R. a. farm; 160 juveniles in two 4

30x30 m2 paddocks

20 adults in a 50x30 m2 paddock 2

9 330612S, 693928W R. a. farm; 50 juveniles in one paddock 2


10 332231S, 6459054W R. a. farm; 100 juveniles in 1 Ha. 2

250 adults in >3 Ha. 3

11 333245S, 595911W R. a. farm; 1 adult and 15 juveniles 2

in one paddock



12 340705S, 590801W R. a. farm; 600 birds (juvenile+adult) in 6

4 paddocks

13 342147S, 584759W R. a. zoo; 7 adults in one paddock 2

R. p. 5 adults in one paddock 2

14 345242S, 600143W R. a. farm; 120 juveniles in 0.1 Ha. 2

30 adults in 0.08 Ha. 2

114 adults in 0.04 Ha. 2

15 344241S, 653714W R. a. farm; undetermined number of adults 2

in several paddocks

16 352330S, 641722W R. a. farm; 160 subadults in one paddock 3


17 345106S, 581455W R. a. farm; ~1000 adults in 6 paddocks 7

18 372354S, 571051W R. a. wild; group of 10 birds 2

19 372150S, 585517W R. a. farm; 32 adults in 1.5 Ha. 4

20 374322S, 582255W R. a. farm; 20 adults in semi-captivity 3

21 374932S, 581244W R. a. farm; 80 adults in 4.5 Ha. 3

22 384841S, 680509W R. p. farm; 13 chicks in one paddock 2

45 juveniles in one paddock 2



23 385320S, 675650W R. p. farm; 16 adults in one paddock 2


6 adults in one paddock; another two 3

died the week before the sampling

25 403154S, 683809W R. p. farm; unknown number of birds in 3

semi-captivity

26 410723S, 711453W R. p. farm; ~30 adults in three paddocks 5


28 464659S, 683557W R. p. wild; unknown number of birds 1

29 490152S, 675152W R. p. farm; 18 chicks in 15x5 m2 paddocks 3

88 subadults in two paddocks 2

75 adults in five paddocks 5

wild; unknown number of birds 1


31 510332S, 701021W R. p. farm; 60 adults in 4 paddocks 4

wild; unknown number of birds 1



CHILE

URUGUAY

PARAGUAY

BRAZIL

BOLIVIA

1

2

34

56

7

8

9

10

11

12

14

15

1617

1819

2021

22

23

24

26

27

28

29

30

3132

33

25

13

300 km

200 mi

Supplementary File 2. Location of the sites where faecal samples of and were collected.

The site numbers correspond to those indicated in Supplementary File 1.

, farmed birds , farmed birds zoo animals

, wild birds , wild birds ( and )

Rhea americana Rhea pennata

R. americana R. pennata

R. americana R. pennata R. americana R. pennata

Supplementary File 3. Prevalence and morphological characteristics of the parasites found in this study in Rhea americana and Rhea pennata in Argentina.

Prevalence has been calculated only for farm samples; for those from other origins (zoo/wild birds), only the number of positive samples is shown to avoid bias

due to low sample size. SF Supplementary file.

Parasite (PROTOZOA) Host Origin Morphological characteristics Prevalence

Balantidium sp. R. americana 8 farms / 1 zoo Cyst (SF 4A): spheroidal, 40-55 m in diameter, with a thick wall; 15.3%; also in 2 samples

yellowish in unstained smears. from the Crdoba zoo

Trophozoite (SF 4B): ovoid, 45-68 x 32-47 m; cilia covering the

surface of the cell; cytostome subterminal. Usually with cytoplasmic

vacuoles.

R. pennata 4 farms / wild Cyst (SF 4C): spheroidal, 38-45 m in diameter, with a thick wall; 24.4%; also in 1 sample

yellowish in unstained smears. from wild birds.

Entamoeba sp. 1-N R. americana 1 farm Cyst (SF 4D,E): spheroidal, 5-11 m in diameter; one nucleus of 3.5%

1-3 m in diameter with a medium to large eccentric endosome.

R. pennata 1 farm Cyst (SF 4F): spheroidal, 6-11 m in diameter; one nucleus of 2.4%

1-3 m in diameter with a medium to large eccentric endosome.

Entamoeba sp. 8-N R. pennata 2 farms Cyst (SF 4G,H): spheroidal, 14-22 m in diameter; with eight 4.9%

nuclei of 2-4 m in diameter with a small eccentric endosome.

Chilomastix sp. R. pennata wild Cyst (SF 4I): ovoid, lemon-shaped, 7-11 x 6-7 m; with one 2 samples from wild

nucleus birds.

Parasite (HELMINTHS) Host Origin Morphological characteristics Prevalence

Fasciola hepatica R. americana 2 farms / wild Egg (SF 5A): ovoid, yellowish, operculated, 140-160 x 75-100 m. 2.4%; also in 1 sample

from wild birds.

R. pennata 1 farm Egg (SF 5B): ovoid, yellowish, operculated, 145-155 x 70-80 m. 2.4%

Deletrocephalus sp. R. americana 2 farms Egg (SF 5C): ovoid, elongated, with rounded ends, 5.9%

165-180 x 62-70 m, containing a morula.

Capillariinae R. pennata 1 zoo Egg (SF 5D): ovoid with a thick shell and two polar plugs, 1 sample from the

brownish, 80 x 30 m. Crdoba zoo.

Trichostrongylus sp. R. pennata 1 farm Egg (SF 5E,F): ovoid with slightly pointed ends, 65-75 x 35-42 m, 2.4%

containing a morula.

Spirurida R. pennata 1 farm Egg (SF 5G): ovoid with rounded ends, with a thick shell, 2.4%

60 x 30 m, containing a larva.

Strongylid-like larvae R. pennata 1 farm Larvae type I (SF 5H): 360 x 20 m; the length of the 2.4%

oesophagus is about 1/8 of the body length

1 farm Larvae type II (SF 5I): 360 x 15 m; the length of the 2.4%

oesophagus is about 1/3 of the body length

A B

50 m

50 m

C

50 m

10 m

D

10 m10 m

E F

10 m

G

10 m

H

10 m

I

Supplementary File 4. Protozoa found in faecal samples from and . All preparations

were stained with Lugol's iodine except (E) and (H) which were stained with trichromic stain. (A)

like cysts from . (B) like trophozoite from (C) like cyst from

(D)(E) -like cysts from . (F) -like cyst from (G)(H)

-like cysts from . (I) sp. from

Rhea americana Rhea pennata

Balantidium

coli- R. americana B. coli- R. americana. B. coli- R.

pennata. Entamoeba bovis R. americana E. bovis R. pennata. E.

coli R. pennata Chilomastix R. pennata.

100 m100 m

A B C100 m

50 m

D

50 m

E

100 m

H

G

50 m

100 m

I

50 m

F

Supplementary File 5. Helminth eggs and larvae found in faecal samples from and

All preparations were stained with Lugol's iodine. (A) egg from ; (B)

egg from (C) spp. egg from ; (D) Capillariinae egg from .

(E)(F) -like egg from ; (G) Spirurid-like egg from ; (H)(I) unidentified

nematode larvae from

Rhea americana Rhea pennata.

Fasciola hepatica R. americana F. hepatica

R. pennata. Deletrocephalus R. americana R. pennata

Trichostrongylus R. pennata R. pennata

R. pennata.

Balantidium Coli

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