First record of Paratanaisia bragai (Digenea: Eucotylidae) in blue and gold macaw (Ara ararauna)

Primeiro registro de Paratanaisia bragai (Digenea: Eucotylidae) em arara Canindé (Ara ararauna)

Tarcísio Macedo Silva Leonardo Fabrício Pavan Priscylla Tatiana Chalfum Guimarães-Okamoto Elisane Lenita Milbradt Raphael Lúcio Andreatti Filho Reinaldo José da Silva Adriano Sakai Okamoto About the authors

Abstract

The aim of this study was to provide the first report on a new host for the digenean Paratanaisia bragai in the caninde macaw Ara ararauna along with the pathological aspects of the infection in the new host. The microscopic findings revealed the presence of granulomatous interstitial nephritis. This study contributes towards knowledge of parasitism by P. bragai in A. ararauna, and emphasizes the need to use best practices in wildlife conservation parks.

Keywords:
Parasite; birds; histopathology; wildlife; macaw

Resumo

O objetivo deste estudo foi relatar, pela primeira vez, a arara canindéAra ararauna como um novo hospedeiro para o digenéticoParatanaisia bragai, bem como relatar aspectos patológicos relacionados à infecção no novo hospedeiro. Os achados microscópicos revelaram nefrite intersticial granulomatosa. Este estudo contribui para o conhecimento do parasitismo por P. bragai em A. ararauna e ainda faz um alerta para a adoção de boas práticas de criação em criatórios conservacionistas da fauna silvestre.

Palavras-chave:
Parasita; aves; histopatologia; fauna silvestre; arara

Ara ararauna, the caninde macaw is a large frugivorous bird belonging to the Psittacidae family that geographically is found in tropical regions of Central America, Bolivia, Paraguay and Brazil. It inhabits floodplains containing stands of moriche (buriti) palms, swamps, savannas and wetlands. Its population is classified as having near threatened status (IUCN, 2014International Union for Conservation of Nature and Natural Resources – IUCN. 2014 [cited 2014 Out 07]. Available from: http://www.iucnredlist.org
http://www.iucnredlist.org...
).

Digeneans belonging to the subfamily Eucotyloidea, family Eucolylidae, are classified into two genera: Tanaisia and Paratanaisia. Both of these affect the renal system of birds (TRAVASSOS et al., 1969Travassos L, Freitas JFT, Kohn A. Trematódeos do Brasil. Mem Inst Oswaldo Cruz 1969; 67(1): 1-886. PMid:5397756.). Parasitism due to Paratanaisia sp. has been reported in the following birds; pheasant, Phasianus colchicus (GOMES et al., 2005Gomes DC, Menezes RC, Tortelly R, Pinto RM. Pathology and first occurrence of the kidney trematode (Santos, 1934) Freitas, 1959 (Digenea: Eucotylidae) in L., 1758, from Brazil. Paratanaisia bragaiPhasianus colchicusMem Inst Oswaldo Cruz 2005; 100(3): 285-288. http://dx.doi.org/10.1590/S0074-02762005000300013. PMid:16113870.
http://dx.doi.org/10.1590/S0074-02762005...
); partridge, Rhynchotus rufescens (MAPELI et al., 2003Mapeli EB, Nascimento AA, Szabó MPJ, Tebaldi JH. Infecções naturais por helmintos em perdizes ( Temminck, 1815) de cativeiro, no Município de Jaboticabal, Estado de São Paulo. Rhynchotus rufescensArq Inst Biol (Sao Paulo) 2003; 70(4): 415-418.); turkey, Meleagris gallopavo (BRENER et al., 2006Brener B, Tortelly R, Menezes RC, Muniz-Pereira LC, Pinto RM. Prevalence and pathology of the nematode , the trematode and the protozoan Heterakis gallinarumParatanaisia bragai,Histomonas meleagridis in the turkey, Meleagris gallopavo.Mem Inst Oswaldo Cruz 2006; 101(6): 677-681. http://dx.doi.org/10.1590/S0074-02762006000600017. PMid:17072483.
http://dx.doi.org/10.1590/S0074-02762006...
); cattle egret, Heron Bubulcus ibis (ABDO & SULTAN, 2013Abdo W, Sultan K. Histopathological findings of the kidney Trematoda spp. (Digenea: Eucotylidae) in cattle egret (). ParatanaisiaBubulcus ibisRev Bras Parasitol Vet 2013; 22(2): 312-313. http://dx.doi.org/10.1590/S1984-29612013000200050. PMid:23856732.
http://dx.doi.org/10.1590/S1984-29612013...
); common waxbill,Estrilda astrild (TAVELA et al., 2014Tavela AO, Carretta Junior M, Oliveira AR, Carneiro FT, Silva VHD, Braga FR, et al. Parasitism by (Digenea, Eucotylidae) in commom waxbill (). Paratanaisia bragaiEstrilda astrildArq Bras Med Vet Zootec 2014; 66(4): 1276-1280. http://dx.doi.org/10.1590/1678-7136.
http://dx.doi.org/10.1590/1678-7136...
); blue-winged macaw, Propyrrhura maracana; parakeet,Pyrrhura leucotis (LUPPI et al., 2007Luppi MM, Melo AL, Motta ROC, Malta MCC, Gardiner CH, Santos RL. Granulomatous nephritis in psittacines associated with parasitism by the trematode Paratanaisia spp. Vet Parasitol 2007; 146(3-4): 363-366. http://dx.doi.org/10.1016/j.vetpar.2007.03.011. PMid:17418949.
http://dx.doi.org/10.1016/j.vetpar.2007....
); guinea-fowl, Numida meleagris (MENEZES et al., 2001Menezes RC, Mattos DG Jr, Tortelly R, Muniz-Pereira LC, Pinto RM, Gomes DC. Trematodes of free range reared guinea fowls ( Linnaeus, 1758) in the state of Rio de Janeiro, Brazil: morphology and pathology. Numida meleagrisAvian Pathol 2001; 30(3): 209-214. http://dx.doi.org/10.1080/03079450124448. PMid:19184902.
http://dx.doi.org/10.1080/03079450124448...
); spot-winged wood quail (uru),Odontophorus capueira; common toucan, Rhamphastos toco; tataupa tinamou, Crypturellus tataupa (TRAVASSOS et al., 1969Travassos L, Freitas JFT, Kohn A. Trematódeos do Brasil. Mem Inst Oswaldo Cruz 1969; 67(1): 1-886. PMid:5397756.); domestic hen,Gallus gallus domesticus (COSTA et al., 1975Costa JO, Guimarães MP, Grisi L, Barros GC. Helmintos parasitos de (L.) no litoral sul do Espírito Santo. Gallus gallus domesticusArq Esc Vet UFMG 1975; 27(1): 45-46.); red bird-of-paradise, Paradisaea rubra (UNWIN et al., 2013Unwin S, Chantrey J, Chatterton J, Aldhoun JA, Littlewood DTJ. Renal trematode infection due to in zoo housed Columbiformes and a red bird-of-paradise (. Paratanaisia bragaiParadisaea rubra)Int J Parasitol Parasites Wildl 2013; 2: 32-41. http://dx.doi.org/10.1016/j.ijppaw.2012.11.001. PMid:24533313.
http://dx.doi.org/10.1016/j.ijppaw.2012....
); and, especially, in Columbiformes: Columbina talpacoti, Columbia livia,Columba mayeri, Zenaida graysoni, Stigmatopelia senegalensis, Chalcophaps indica and Gallicolumba crinigera (BUNBURY et al., 2008Bunbury N, Stidworthy MF, Greenwood AG, Jones CG, Sawmy S, Cole RE, et al. Causes of mortality in free-living Mauritian pink pigeons , 2002–2006. Columba mayeriEndanger Species Res 2008; 9(3): 213-220. http://dx.doi.org/10.3354/esr00088.
http://dx.doi.org/10.3354/esr00088...
;UNWIN et al., 2013Unwin S, Chantrey J, Chatterton J, Aldhoun JA, Littlewood DTJ. Renal trematode infection due to in zoo housed Columbiformes and a red bird-of-paradise (. Paratanaisia bragaiParadisaea rubra)Int J Parasitol Parasites Wildl 2013; 2: 32-41. http://dx.doi.org/10.1016/j.ijppaw.2012.11.001. PMid:24533313.
http://dx.doi.org/10.1016/j.ijppaw.2012....
).

Yet Paratanaisia bragai has not been reported in blue-and-gold macaws;Ara ararauna, only P. robusta (LUPPI et al., 2007Luppi MM, Melo AL, Motta ROC, Malta MCC, Gardiner CH, Santos RL. Granulomatous nephritis in psittacines associated with parasitism by the trematode Paratanaisia spp. Vet Parasitol 2007; 146(3-4): 363-366. http://dx.doi.org/10.1016/j.vetpar.2007.03.011. PMid:17418949.
http://dx.doi.org/10.1016/j.vetpar.2007....
).

Although it has been reported that Paratanaisia affects the avian hosts, the degree of parasitism and the pathological impairment relating to infection are still a matter of debate. Little consensus has been reached regarding information about these aspects of the species that have been reported to be hosts for this genus (UNWIN et al., 2013Unwin S, Chantrey J, Chatterton J, Aldhoun JA, Littlewood DTJ. Renal trematode infection due to in zoo housed Columbiformes and a red bird-of-paradise (. Paratanaisia bragaiParadisaea rubra)Int J Parasitol Parasites Wildl 2013; 2: 32-41. http://dx.doi.org/10.1016/j.ijppaw.2012.11.001. PMid:24533313.
http://dx.doi.org/10.1016/j.ijppaw.2012....
). So far, it is known that this parasite is present in the renal system of some of the species involved, which leads to kidney volume increase, atrophy, asymmetry, cysts, changes to parenchymal coloration, distortion or dilatation, or even absence of changes (LUPPI et al., 2007Luppi MM, Melo AL, Motta ROC, Malta MCC, Gardiner CH, Santos RL. Granulomatous nephritis in psittacines associated with parasitism by the trematode Paratanaisia spp. Vet Parasitol 2007; 146(3-4): 363-366. http://dx.doi.org/10.1016/j.vetpar.2007.03.011. PMid:17418949.
http://dx.doi.org/10.1016/j.vetpar.2007....
). The microscopic alterations found in some hosts range from little inflammatory reaction (MAPELI et al., 2003Mapeli EB, Nascimento AA, Szabó MPJ, Tebaldi JH. Infecções naturais por helmintos em perdizes ( Temminck, 1815) de cativeiro, no Município de Jaboticabal, Estado de São Paulo. Rhynchotus rufescensArq Inst Biol (Sao Paulo) 2003; 70(4): 415-418.) to dilation of medullary collector ducts (PINTO et al., 2004Pinto RM, Menezes RC, Tortelly R. Systematic and pathologic study of Paratanaisia bragai (Santos, 1934) Freitas, 1959 (Digenea, Eucotylidae) infestation in ruddy ground dove Columbina talpacoti (Temminck, 1811). Arq Bras Med Vet Zootec 2004; 56(4): 472-479. http://dx.doi.org/10.1590/S0102-09352004000400008.
http://dx.doi.org/10.1590/S0102-09352004...
), necrosis, fibrosis, poor hyperplasia, mononuclear infiltration accentuated with intraluminal eosinophilic hyaline tubular degeneration, hemosiderin pigmentation within the tubular lining epithelium, hemorrhage, granulomatous nephritis and chronic granulomatous interstitial nephritis (ABDO & SULTAN, 2013Abdo W, Sultan K. Histopathological findings of the kidney Trematoda spp. (Digenea: Eucotylidae) in cattle egret (). ParatanaisiaBubulcus ibisRev Bras Parasitol Vet 2013; 22(2): 312-313. http://dx.doi.org/10.1590/S1984-29612013000200050. PMid:23856732.
http://dx.doi.org/10.1590/S1984-29612013...
; LUPPI et al., 2007Luppi MM, Melo AL, Motta ROC, Malta MCC, Gardiner CH, Santos RL. Granulomatous nephritis in psittacines associated with parasitism by the trematode Paratanaisia spp. Vet Parasitol 2007; 146(3-4): 363-366. http://dx.doi.org/10.1016/j.vetpar.2007.03.011. PMid:17418949.
http://dx.doi.org/10.1016/j.vetpar.2007....
; UNWIN et al., 2013Unwin S, Chantrey J, Chatterton J, Aldhoun JA, Littlewood DTJ. Renal trematode infection due to in zoo housed Columbiformes and a red bird-of-paradise (. Paratanaisia bragaiParadisaea rubra)Int J Parasitol Parasites Wildl 2013; 2: 32-41. http://dx.doi.org/10.1016/j.ijppaw.2012.11.001. PMid:24533313.
http://dx.doi.org/10.1016/j.ijppaw.2012....
).

In this first record of Paratanaisia bragai in caninde macaws (A. ararauna), we describe pathological data found in two cases of infection in this bird species.

Five specimens of A. ararauna from a conservation hatchery located in the rural municipality of Itatinga (23° 06’ 06” S, 48° 36’ 57” W), state of São Paulo, Brazil, were necropsied on March 13, 2014. During the necropsies, no macroscopic alterations were observed, except for paleness in the kidneys of two birds. Fragments from several organs were collected, fixed in 10% formalin, processed and embedded in paraffin. Histological sections of 4 μm thickness were cut and stained using hematoxylin and eosin. Among the samples from these five animals that were evaluated microscopically, the kidney fragment samples from the two birds that presented macroscopic alterations revealed the presence of flattened, elongated structures, wrapped in a refringent capsule that contained basophilic structures similar to those of digenean trematodes. These findings were similar to those illustrated by Fletcher et al. (2008)Fletcher OJ, Abdul-Aziz T, Barnes HJ. Urinary system. In: Fletcher O. Avian histopathology. 3rd ed. Jacksonville: American Association of Avian Pathologists; 2008. p. 238-259..

Subsequently, the digeneans were recovered from formalin and identified as P. bragai. The kidney samples that had previously been placed in formalin were gently sliced to search for parasites. Nearly 20 wax-embedded parasites, which were stained with acetic carmine and subsequently cleared and stained with creosote, were recovered. Morphological analysis on the features of the genusParatanaisia showed the following: elongated flattened body; tegument with spines; subterminal oral sucker; small acetabulum; intestinal caecum fused near the posterior end; post-bifurcal and pre-ovarian genital pore; pre-equatorial and post-ovarian testicles, largely intercaecal with lobed edge; pre-testes ovary of irregular outline; extracaecal vitellaria extending from bifurcal zone to the posterior region of the body; and intercaecal uterus, from the bifurcal zone to the posterior region. The species P. bragai was confirmed through morphometric analysis on the body (2.67 ± 0.8 by 0.52 ± 0.15), which differed this species fromParatanaisia robusta and Paratanaisia confusa(THATCHER, 1993Thatcher EV. Trematódeos neotropicais. Manaus: INPA; 1993.; VICENTE et al., 1995Vicente JJ, Rodrigues HO, Gomes DC, Pinto RM. Nematóides do Brasil. Parte IV: Nematóides de aves. Rev Bras Zool 1995; 12(S1): 1-273. http://dx.doi.org/10.1590/S0101-81751995000500001.
http://dx.doi.org/10.1590/S0101-81751995...
).

The histological aspects of the lesions were similar in the two birds parasitized byP. bragai and the following were seen: marked vascular congestion with hemorrhagic focus, numerous hemosiderin pigments, moderate vacuolar degeneration of renal tubules (Figure 1) and parasitic organization in the renal interstitium (Figure 2), thus resulting in a moderate mononuclear inflammatory cell infiltration, associated with deposition of fibrous tissue. The lesions worsen in a manner directly proportional to the size of the parasite (Figure 3). The diagnosis was established as “granulomatous interstitial nephritis” caused by P. bragai (Figure 4).

Figure 1
Histological section through kidney of Ara ararauna showing deposition of hemosiderin (A) and vacuolar tubular degeneration (B) (HE).
Figure 2
Histological section through kidney of Ara ararauna showing parasitic organization in the renal interstitium (HE).
Figure 3
Histological section through kidney of Ara ararauna showing deposition of fibrous tissue due to parasitism by P. bragai(HE).
Figure 4
Histological section through kidney of Ara ararauna showing chronic nephritis with mononuclear cell infiltrate associated with infection byP. bragai (HE).

Trematodiasis causing chronic granulomatous nephritis has been described only once byLuppi et al. (2007)Luppi MM, Melo AL, Motta ROC, Malta MCC, Gardiner CH, Santos RL. Granulomatous nephritis in psittacines associated with parasitism by the trematode Paratanaisia spp. Vet Parasitol 2007; 146(3-4): 363-366. http://dx.doi.org/10.1016/j.vetpar.2007.03.011. PMid:17418949.
http://dx.doi.org/10.1016/j.vetpar.2007....
. These were fatal infections, resulting in chronic kidney disease and mortality among birds of the family Psittacidae raised in captivity. In that study Luppi et al. (2007)Luppi MM, Melo AL, Motta ROC, Malta MCC, Gardiner CH, Santos RL. Granulomatous nephritis in psittacines associated with parasitism by the trematode Paratanaisia spp. Vet Parasitol 2007; 146(3-4): 363-366. http://dx.doi.org/10.1016/j.vetpar.2007.03.011. PMid:17418949.
http://dx.doi.org/10.1016/j.vetpar.2007....
reported infections due to the species Paratanaisia robusta in Ara ararauna and P. bragai inPropyrrhura maracana and Pyrrhura leucotis. However, we did not find any reports on parasitism by P. bragai inAra ararauna, and thus this present report provides the first record of parasitism in this bird species, along with the first report of chronic infection by P. bragai in this species.

Unwin et al. (2013)Unwin S, Chantrey J, Chatterton J, Aldhoun JA, Littlewood DTJ. Renal trematode infection due to in zoo housed Columbiformes and a red bird-of-paradise (. Paratanaisia bragaiParadisaea rubra)Int J Parasitol Parasites Wildl 2013; 2: 32-41. http://dx.doi.org/10.1016/j.ijppaw.2012.11.001. PMid:24533313.
http://dx.doi.org/10.1016/j.ijppaw.2012....
described new hosts forP. bragai, along with the molecular and microscopic aspects of parasitism, with occurrences of granulomatous inflammatory reactions. The microscopic results presented here are similar to those of Unwin et al. (2013)Unwin S, Chantrey J, Chatterton J, Aldhoun JA, Littlewood DTJ. Renal trematode infection due to in zoo housed Columbiformes and a red bird-of-paradise (. Paratanaisia bragaiParadisaea rubra)Int J Parasitol Parasites Wildl 2013; 2: 32-41. http://dx.doi.org/10.1016/j.ijppaw.2012.11.001. PMid:24533313.
http://dx.doi.org/10.1016/j.ijppaw.2012....
. Other data obtained by Abdo & Sultan (2013)Abdo W, Sultan K. Histopathological findings of the kidney Trematoda spp. (Digenea: Eucotylidae) in cattle egret (). ParatanaisiaBubulcus ibisRev Bras Parasitol Vet 2013; 22(2): 312-313. http://dx.doi.org/10.1590/S1984-29612013000200050. PMid:23856732.
http://dx.doi.org/10.1590/S1984-29612013...
from Bubulcus ibis showed that parasitism caused renal tubular hyperplasia. However, no such findings were observed in the bird species studied here.

The degree of severity of renal injury observed microscopically varied according to the size of the parasite, such that there was lower deposition of fibrous connective tissue in relation to the smaller specimens. This was in agreement with the injuries described by Gomes et al. (2005)Gomes DC, Menezes RC, Tortelly R, Pinto RM. Pathology and first occurrence of the kidney trematode (Santos, 1934) Freitas, 1959 (Digenea: Eucotylidae) in L., 1758, from Brazil. Paratanaisia bragaiPhasianus colchicusMem Inst Oswaldo Cruz 2005; 100(3): 285-288. http://dx.doi.org/10.1590/S0074-02762005000300013. PMid:16113870.
http://dx.doi.org/10.1590/S0074-02762005...
and Unwin et al. (2013)Unwin S, Chantrey J, Chatterton J, Aldhoun JA, Littlewood DTJ. Renal trematode infection due to in zoo housed Columbiformes and a red bird-of-paradise (. Paratanaisia bragaiParadisaea rubra)Int J Parasitol Parasites Wildl 2013; 2: 32-41. http://dx.doi.org/10.1016/j.ijppaw.2012.11.001. PMid:24533313.
http://dx.doi.org/10.1016/j.ijppaw.2012....
.

Systematic and pathological studies on mortality have an important role with regard to obtaining information on the behavior of new illnesses, especially among wild species that are threatened with or vulnerable to extinction (BUNBURY et al., 2008Bunbury N, Stidworthy MF, Greenwood AG, Jones CG, Sawmy S, Cole RE, et al. Causes of mortality in free-living Mauritian pink pigeons , 2002–2006. Columba mayeriEndanger Species Res 2008; 9(3): 213-220. http://dx.doi.org/10.3354/esr00088.
http://dx.doi.org/10.3354/esr00088...
). Information on this new host species for a parasite (P. bragai) that has been described as a chronic and fatal condition (LUPPI et al., 2007Luppi MM, Melo AL, Motta ROC, Malta MCC, Gardiner CH, Santos RL. Granulomatous nephritis in psittacines associated with parasitism by the trematode Paratanaisia spp. Vet Parasitol 2007; 146(3-4): 363-366. http://dx.doi.org/10.1016/j.vetpar.2007.03.011. PMid:17418949.
http://dx.doi.org/10.1016/j.vetpar.2007....
; UNWIN et al., 2013Unwin S, Chantrey J, Chatterton J, Aldhoun JA, Littlewood DTJ. Renal trematode infection due to in zoo housed Columbiformes and a red bird-of-paradise (. Paratanaisia bragaiParadisaea rubra)Int J Parasitol Parasites Wildl 2013; 2: 32-41. http://dx.doi.org/10.1016/j.ijppaw.2012.11.001. PMid:24533313.
http://dx.doi.org/10.1016/j.ijppaw.2012....
) for this species, which is experiencing population decline in natural settings (IUCN, 2014International Union for Conservation of Nature and Natural Resources – IUCN. 2014 [cited 2014 Out 07]. Available from: http://www.iucnredlist.org
http://www.iucnredlist.org...
), will play an important role in improving the management of breeding programs.

We suggest that best practices need to be sought in breeding programs, especially in wildlife conservation parks. Some molluscs have an important role in the production of metacercariae, in the cycle of avian infection due to P. bragai (BRANDOLINI & AMATO, 2006Brandolini SVPB, Amato SB. Desenvolvimento larval de (Santos) (Digenea, Eucotylidae) sob condições experimentais. Paratanaisia bragaiRev Bras Zool 2006; 23(4): 1097-1100. http://dx.doi.org/10.1590/S0101-81752006000400017.
http://dx.doi.org/10.1590/S0101-81752006...
). Therefore, gastropod eradication in the parks becomes important. Columbiformes are known to be the main hosts for P. bragai (PINTO et al., 2004Pinto RM, Menezes RC, Tortelly R. Systematic and pathologic study of Paratanaisia bragai (Santos, 1934) Freitas, 1959 (Digenea, Eucotylidae) infestation in ruddy ground dove Columbina talpacoti (Temminck, 1811). Arq Bras Med Vet Zootec 2004; 56(4): 472-479. http://dx.doi.org/10.1590/S0102-09352004000400008.
http://dx.doi.org/10.1590/S0102-09352004...
; UNWIN et al., 2013Unwin S, Chantrey J, Chatterton J, Aldhoun JA, Littlewood DTJ. Renal trematode infection due to in zoo housed Columbiformes and a red bird-of-paradise (. Paratanaisia bragaiParadisaea rubra)Int J Parasitol Parasites Wildl 2013; 2: 32-41. http://dx.doi.org/10.1016/j.ijppaw.2012.11.001. PMid:24533313.
http://dx.doi.org/10.1016/j.ijppaw.2012....
) because they are synanthropic and lead to important diseases (ROCHA-E-SILVA et al., 2014Rocha-e-Silva RC, Maciel WC, Teixeira RSC, Salles RPR. O pombo () como agente carreador de spp. e as implicações em saúde pública. Columba liviaSalmonellaArq Inst Biol 2014; 81(2): 189-194. http://dx.doi.org/10.1590/1808-1657000702012.
http://dx.doi.org/10.1590/1808-165700070...
). Special attention is needed in drawing up strategies for avoiding accidental risks relating to introduction of trematodes and diseases caused by them within wildlife parks, so as to keep hatcheries safe.

The pathological findings regarding the lesions, as observed in this study; demonstrate a situation of chronic impairment. These findings add to what has already been described a few times in other species. They also serve as a parameter and as a source of new information regarding new host infection, and provide a warning that best management practices for bird breeding programs within wildlife conservation parks need to be sought.

References

  • Abdo W, Sultan K. Histopathological findings of the kidney Trematoda spp. (Digenea: Eucotylidae) in cattle egret (). ParatanaisiaBubulcus ibisRev Bras Parasitol Vet 2013; 22(2): 312-313. http://dx.doi.org/10.1590/S1984-29612013000200050. PMid:23856732.
    » http://dx.doi.org/10.1590/S1984-29612013000200050
  • Brandolini SVPB, Amato SB. Desenvolvimento larval de (Santos) (Digenea, Eucotylidae) sob condições experimentais. Paratanaisia bragaiRev Bras Zool 2006; 23(4): 1097-1100. http://dx.doi.org/10.1590/S0101-81752006000400017.
    » http://dx.doi.org/10.1590/S0101-81752006000400017
  • Brener B, Tortelly R, Menezes RC, Muniz-Pereira LC, Pinto RM. Prevalence and pathology of the nematode , the trematode and the protozoan Heterakis gallinarumParatanaisia bragai,Histomonas meleagridis in the turkey, Meleagris gallopavo.Mem Inst Oswaldo Cruz 2006; 101(6): 677-681. http://dx.doi.org/10.1590/S0074-02762006000600017. PMid:17072483.
    » http://dx.doi.org/10.1590/S0074-02762006000600017
  • Bunbury N, Stidworthy MF, Greenwood AG, Jones CG, Sawmy S, Cole RE, et al. Causes of mortality in free-living Mauritian pink pigeons , 2002–2006. Columba mayeriEndanger Species Res 2008; 9(3): 213-220. http://dx.doi.org/10.3354/esr00088.
    » http://dx.doi.org/10.3354/esr00088
  • Costa JO, Guimarães MP, Grisi L, Barros GC. Helmintos parasitos de (L.) no litoral sul do Espírito Santo. Gallus gallus domesticusArq Esc Vet UFMG 1975; 27(1): 45-46.
  • Fletcher OJ, Abdul-Aziz T, Barnes HJ. Urinary system. In: Fletcher O. Avian histopathology. 3rd ed. Jacksonville: American Association of Avian Pathologists; 2008. p. 238-259.
  • Gomes DC, Menezes RC, Tortelly R, Pinto RM. Pathology and first occurrence of the kidney trematode (Santos, 1934) Freitas, 1959 (Digenea: Eucotylidae) in L., 1758, from Brazil. Paratanaisia bragaiPhasianus colchicusMem Inst Oswaldo Cruz 2005; 100(3): 285-288. http://dx.doi.org/10.1590/S0074-02762005000300013. PMid:16113870.
    » http://dx.doi.org/10.1590/S0074-02762005000300013
  • International Union for Conservation of Nature and Natural Resources – IUCN. 2014 [cited 2014 Out 07]. Available from: http://www.iucnredlist.org
    » http://www.iucnredlist.org
  • Luppi MM, Melo AL, Motta ROC, Malta MCC, Gardiner CH, Santos RL. Granulomatous nephritis in psittacines associated with parasitism by the trematode Paratanaisia spp. Vet Parasitol 2007; 146(3-4): 363-366. http://dx.doi.org/10.1016/j.vetpar.2007.03.011. PMid:17418949.
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Publication Dates

  • Publication in this collection
    11 Mar 2016
  • Date of issue
    Jan-Mar 2016

History

  • Received
    31 Mar 2015
  • Accepted
    20 Apr 2015
Colégio Brasileiro de Parasitologia Veterinária FCAV/UNESP - Departamento de Patologia Veterinária, Via de acesso Prof. Paulo Donato Castellane s/n, Zona Rural, , 14884-900 Jaboticabal - SP, Brasil, Fone: (16) 3209-7100 RAMAL 7934 - Jaboticabal - SP - Brazil
E-mail: cbpv_rbpv.fcav@unesp.br