Abstract
Protozoa of the Apicomplexa phylum are worldwide distributed with capacity to infect endothermic animals. The study of these protozoa in wild birds in Brazil is scarce. This study aimed to evaluate the occurrence of apicomplexan protozoa in wild birds in the Northeast of Brazil. From October to December 2019, brain tissue samples were collected from 71 captive birds from the Wild Animal Screening Center of the Pernambuco State (CETRAS-Tangara) and 25 free-living birds from the Caatinga biome in Rio Grande do Norte, totaling 96 animals (41 species). Brain fragments were subjected to molecular diagnosis by nested PCR for the 18s rDNA gene of Apicomplexa parasites, followed by DNA sequencing. This gene was detected in 25% (24/96) of the samples, and it was possible to perform DNA sequencing of 14 samples, confirming three genera: Isospora, Sarcocystis and Toxoplasma from eight bird species (Amazona aestiva, Coereba flaveola, Egretta thula, Paroaria dominicana, Sporophila nigricollis, Cariama cristata, Columbina talpacoti, Crypturellus parvirostris). The occurrence these coccidia in wild birds provides important epidemiological information for the adoption of preventive measures for its conservation. Future studies are needed to better understand the consequence of Apicomplexa infection in birds in Caatinga and Atlantic Forest biomes.
Keywords:
Toxoplasma gondii; Sarcocystis spp.; Isospora spp.; avifauna
Resumo
Protozoários do filo Apicomplexa são distribuídos mundialmente e com capacidade de infectar animais endotérmicos. O estudo destes protozoários, em aves silvestres do Brasil, é escasso. Objetivou-se avaliar a ocorrência de protozoários Apicomplexa em aves silvestres na região Nordeste do Brasil. De outubro a dezembro de 2019, foram coletadas amostras de encéfalo de 71 aves de cativeiro do Centro de Triagem e Reabilitação de Animais Silvestres de Pernambuco (CETRAS-Tangara). E 25 aves de vida livre do bioma Caatinga no Rio Grande do Norte, totalizando 96 animais (41 espécies). Os fragmentos de encéfalo foram submetidos ao diagnóstico molecular por nested PCR, para o gene 18s rDNA de protozoários Apicomplexa, seguido por sequenciamento do DNA. Este gene foi detectado em 25% (24/96) das amostras analisadas; foi possível realizar o sequenciamento de 14 amostras, confirmando-se três gêneros: Isospora, Sarcocystis e Toxoplasma em oito espécies de aves (Amazona aestiva, Coereba flaveola, Egretta thula, Paroaria dominicana, Sporophila nigricollis, Cariama cristata, Columbina talpacoti, Crypturellus parvirostris). A ocorrência destes coccídios nas aves silvestres fornece informações epidemiológicas importantes para a adoção de medidas preventivas tendo em vista sua conservação. Estudos futuros são necessários para melhor compreensão da consequência da infecção por Apicomplexa, em aves silvestres dos biomas Caatinga e Floresta Atlântica.
Palavras-chave:
Toxoplasma gondii; Sarcocystis spp.; Isospora spp.; avifauna
Introduction
Apicomplexa phylum comprise intracellular obligate protozoa that are widely distributed worldwide and can infect a wide range of endothermic animals, including humans (Dubey, 2010Dubey JP. Toxoplasmosis of animals and humans. 2nd ed. Boca Raton: CRC Press; 2010. https://doi.org/10.1201/9781420092370.
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). Members of this phylum have a complex biological cycle, with different infection stages, multiplying sexually and asexually (Besteiro, 2014Besteiro S. Autophagy in parasitic protists. In: Hayat MA, editor. Autophagy: cancer, other pathologies, inflammation, immunity, infection, and aging. Cambridge: Academic Press; 2014. Vol. 2, p. 185-195. http://dx.doi.org/10.1016/B978-0-12-405877-4.00012-3.
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). Among them, the genera Cystoisospora, Eimeria, Isospora, Neospora, Sarcocystis, and Toxoplasma are clinically and epidemiologically important for wild animals.
Toxoplasma gondii and Sarcocystis spp. are protozoa of the Sarcocystidae family most prevalent found in birds (Llano et al., 2022Llano HAB, Polato HZ, Keid LB, Oliveira TMFS, Zwarg T, Oliveira AS, et al. Molecular screening for Sarcocystidae in muscles of wild birds from Brazil suggests a plethora of intermediate hosts for Sarcocystis falcatula. Int J Parasitol Parasites Wildl 2022; 17: 230-238. http://dx.doi.org/10.1016/j.ijppaw.2022.03.002. PMid:35282411.
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). Carnivorous birds can become infected with Toxoplasma by ingesting tissue cysts present in infected intermediate hosts, such as small rodents (Karakavuk et al., 2018Karakavuk M, Aldemir D, Mercier A, Şahar EA, Can H, Murat JB, et al. Prevalence of toxoplasmosis and genetic characterization of Toxoplasma gondii strains isolated in wild birds of prey and their relation with previously isolated strains from Turkey. PLoS One 2018; 13(4): e0196159. http://dx.doi.org/10.1371/journal.pone.0196159. PMid:29668747.
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), as well as birds can become infected by ingesting oocysts present in contaminated water, food, or soil (Lindsay et al., 2003Lindsay DS, Collins MV, Mitchell SM, Cole RA, Flick GJ, Wetch CN, et al. Sporulation and survival of Toxoplasma gondii oocysts in seawater. J Eukaryot Microbiol 2003; 50(1): 687-688. http://dx.doi.org/10.1111/j.1550-7408.2003.tb00688.x. PMid:14736220.
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). Studies carried out in domestic birds (Gallus domesticus), which are generally asymptomatic hosts, have reported a high prevalence of infection by T. gondii (Dubey et al., 2010Dubey JP, Rajendran C, Costa DGC, Ferreira LR, Kwok OCH, Qu D, et al. New Toxoplasma gondii genotypes isolated from free-range chickens from the Fernando de Noronha, Brazil: unexpected findings. J Parasitol 2010; 96(4): 709-712. http://dx.doi.org/10.1645/GE-2425.1. PMid:20486738.
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; Magalhães et al., 2016Magalhães FJR, Ribeiro-Andrade M, Alcântara AM, Pinheiro JW Jr, Sena MJ, Porto WJN, et al. Risk factors for Toxoplasma gondii infection in sheep and cattle from Fernando de Noronha Island, Brazil. Braz J Vet Parasitol 2016; 25(4): 511-515. http://dx.doi.org/10.1590/s1984-29612016051. PMid:27580399.
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). However, cases of acute toxoplasmosis have been reported in wild birds. In canary (Serinus canaria), severe clinical signs of encephalitis and ocular toxoplasmosis, including blindness, have been reported in Uruguay, Australia, Italy, New Zealand, and the United Kingdom (Dubey, 2002Dubey JP. A review of toxoplasmosis in wild birds. Vet Parasitol 2002; 106(2): 121-153. http://dx.doi.org/10.1016/S0304-4017(02)00034-1. PMid:12031816.
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). These clinical signs are compatible with non-suppurative chorioretinitis in macrophages and tachyzoites of T. gondii in the subretinal space, in addition to tachyzoite aggregates in the retinal nerve fibers and cysts in the meninges and cerebellum (Williams et al., 2001Williams SM, Fulton RM, Render JA, Mansfield L, Bouldin M. Ocular and encephalic toxoplasmosis in canaries. Avian Dis 2001; 45(1): 262-267. http://dx.doi.org/10.2307/1593039. PMid:11332494.
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). Moreover, fatal toxoplasmosis has been described in a vinaceous amazon parrot (Amazona vinacea) from Brazil (Ferreira et al., 2012Ferreira FC Jr, Donatti RV, Marques MVR, Ecco R, Preis IS, Shivaprasad HL, et al. Fatal toxoplasmosis in a vinaceous Amazon parrot (Amazona vinacea). Avian Dis 2012; 56(4): 774-777. http://dx.doi.org/10.1637/10063-011912-Case.1. PMid:23397856.
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) and in 12 little penguins (Eudyptula minor) from Australia (Campbell et al., 2022Campbell K, Paparini A, Gomez AB, Cannell B, Stephens N. Fatal toxoplasmosis in little penguins (Eudyptula minor) from Penguin Island, Western Australia. Int J Parasitol Parasites Wildl 2022; 17: 211-217. http://dx.doi.org/10.1016/j.ijppaw.2022.02.006. PMid:35198375.
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).
Sarcocystis spp. are cyst-forming Apicomplexan parasites in which the definitive hosts are predatory carnivores that become infected by ingesting tissue cysts (mature sarcocysts) present in the muscles of intermediate hosts, which, in turn, become infected by ingestion of water or food contaminated with sporocysts shed in the feces of the definitive hosts (Prakas & Butkauskas, 2012Prakas P, Butkauskas D. Protozoan parasites from genus Sarcocystis and their investigations in Lithuania. Ekologija 2012; 58(1): 45-58. http://dx.doi.org/10.6001/ekologija.v58i1.2349.
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; Dubey et al., 2015Dubey JP, Calero-Bernal R, Rosenthal BM, Speer CA, Fayer R. Sarcocystosis of animals and humans. 2nd ed. Boca Raton: CRC Press; 2015. http://dx.doi.org/10.1201/b19184.
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). Birds can be definitive and/or intermediate hosts of several species of Sarcocystis, especially those that have potential pathogenicity. More than 25 Sarcocystis species, especially S. falcatula and S. calchasi are capable of forming cysts in the muscle tissue of birds, which can be highly pathogenic for Passeriformes, Psittaciformes, and Columbiformes (Kutkienė et al., 2012Kutkienė L, Prakas P, Butkauskas D, Sruoga A. Description of Sarcocystis turdusi sp. nov. from the common blackbird (Turdus merula). Parasitology 2012; 139(11): 1438-1443. http://dx.doi.org/10.1017/S0031182012000819. PMid:22814103.
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; Dubey et al., 2015Dubey JP, Calero-Bernal R, Rosenthal BM, Speer CA, Fayer R. Sarcocystosis of animals and humans. 2nd ed. Boca Raton: CRC Press; 2015. http://dx.doi.org/10.1201/b19184.
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).
Protozoa of the genus Isospora (Eimeriidae family) usually parasitize the enterocytes of birds and are responsible for enteric diseases. Furthermore, this protozoan may have an extra intestinal cycle and can be transported intracellularly through the blood stream to multiple organs, leading to the systemic manifestation of the disease (Sánchez-Cordón et al., 2007Sánchez-Cordón PJ, Gómez-Villamandos JC, Gutiérrez J, Sierra MA, Pedrera M, Bautista MJ. Atoxoplasma spp. infection in captive canaries (Serinus canaria). J Vet Med A Physiol Pathol Clin Med 2007; 54(1): 23-26. http://dx.doi.org/10.1111/j.1439-0442.2007.00909.x. PMid:17359450.
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; Cushing et al., 2011Cushing TL, Schat KA, States SL, Grodio JL, O’Connell PH, Buckles EL. Characterization of the host response in systemic isosporosis (atoxoplasmosis) in a colony of captive American goldfinches (Spinus tristis) and house sparrows (Passer domesticus). Vet Pathol 2011; 48(5): 985-992. http://dx.doi.org/10.1177/0300985810391114. PMid:21311069.
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), which is known as systemic isosporosis or atoxoplasmosis. Transmission often occurs via the fecal-oral route and is characterized by a direct life cycle. Clinical diseases are associated with stressful situations, immunosuppression, and young birds (Barbón et al., 2019Barbón AR, López J, Jamriška J, Thomasson A, Braun J, Stidworthy MF. Clinical and pathological aspects of systemic Isospora infection in blue-crowned laughing thrushes (Garrulax courtoisi) at Jersey Zoo. J Avian Med Surg 2019; 33(3): 265-277. http://dx.doi.org/10.1647/2018-377. PMid:31893622.
http://dx.doi.org/10.1647/2018-377...
). The parasite asexual reproduction occurs in intestinal and blood-circulating cells (lymphocytes and monocytes). The asexual stage of this parasite has been found in several somatic tissues, mainly liver, spleen, and intestine, and have been also detected in lungs, heart, pancreas, kidneys, proventriculus, gizzard, gonads, and brain (Sánchez-Cordón et al., 2007Sánchez-Cordón PJ, Gómez-Villamandos JC, Gutiérrez J, Sierra MA, Pedrera M, Bautista MJ. Atoxoplasma spp. infection in captive canaries (Serinus canaria). J Vet Med A Physiol Pathol Clin Med 2007; 54(1): 23-26. http://dx.doi.org/10.1111/j.1439-0442.2007.00909.x. PMid:17359450.
http://dx.doi.org/10.1111/j.1439-0442.20...
; Cushing et al., 2011Cushing TL, Schat KA, States SL, Grodio JL, O’Connell PH, Buckles EL. Characterization of the host response in systemic isosporosis (atoxoplasmosis) in a colony of captive American goldfinches (Spinus tristis) and house sparrows (Passer domesticus). Vet Pathol 2011; 48(5): 985-992. http://dx.doi.org/10.1177/0300985810391114. PMid:21311069.
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; Mohr et al., 2017Mohr F, Betson M, Quintard B. Investigation of the presence of Atoxoplasma spp. in blue-crowned laughingthrush (Dryonastes courtoisi) adults and neonates. J Zoo Wildl Med 2017; 48(1): 1-6. http://dx.doi.org/10.1638/2016-0044.1. PMid:28363058.
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; Oliveira et al., 2018Oliveira AR, Souza TD, Mol JPS, Flecher MC, Hiura E, Santos RL. Pathological and molecular characterization of systemic isosporosis (atoxoplasmosis) in captive green-winged saltator (Saltator similis). Vet Parasitol 2018; 255: 98-101. http://dx.doi.org/10.1016/j.vetpar.2018.04.007. PMid:29773145.
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). Pathogenesis of systemic isosporosis and its etiologic agent have not been well characterized (Oliveira et al., 2018Oliveira AR, Souza TD, Mol JPS, Flecher MC, Hiura E, Santos RL. Pathological and molecular characterization of systemic isosporosis (atoxoplasmosis) in captive green-winged saltator (Saltator similis). Vet Parasitol 2018; 255: 98-101. http://dx.doi.org/10.1016/j.vetpar.2018.04.007. PMid:29773145.
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), however, taxonomically Atoxoplasma is considered a junior objective synonym of Isospora causing systemic disease. According to Barta et al. (2005)Barta JR, Schrenzel MD, Carreno R, Rideout BA. The genus Atoxoplasma (Garnham 1950) as a junior objective synonym of the genus Isospora (Schneider 1881) species infecting birds and resurrection of Cystoisospora (Frenkel 1977) as the correct genus for Isospora species infecting mammals. J Parasitol 2005; 91(3): 726-727. http://dx.doi.org/10.1645/GE-3341.1. PMid:16108579.
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, the genus concept for Isospora Schneider, 1881 applies to all the species that belong to the large clade of isosporoid coccidia infecting passerines and this nomenclature should be used instead of Atoxoplasma (Barta et al., 2005Barta JR, Schrenzel MD, Carreno R, Rideout BA. The genus Atoxoplasma (Garnham 1950) as a junior objective synonym of the genus Isospora (Schneider 1881) species infecting birds and resurrection of Cystoisospora (Frenkel 1977) as the correct genus for Isospora species infecting mammals. J Parasitol 2005; 91(3): 726-727. http://dx.doi.org/10.1645/GE-3341.1. PMid:16108579.
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).
Studies on the occurrence of apicomplexan protozoa in wild birds in Northeast Brazil are important because of their impact on the imbalance of biomes in this region (Alves et al., 2013Alves RRN, Lima JRF, Araujo HFP. The live bird trade in Brazil and its conservation implications: an overview. Bird Conserv Int 2013; 23(1): 53-65. http://dx.doi.org/10.1017/S095927091200010X.
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), as infections may cause disease and even death, which is a threatened to endemic species. These biomes (Caatinga and Atlantic Forest) have more than 800 endemic species, of which ~45% of Atlantic Forest species are considered threatened and may become extinct, because of trafficking and deforestation, which, associated with disorderly urbanization, facilitate the establishment of new interactions between hosts and parasites (Ribon et al., 2003Ribon R, Simon JE, Mattos GT. Bird extinctions in Atlantic Forest fragments of the Viçosa region, Southeastern Brazil. Conserv Biol 2003; 17(6): 1827-1839. http://dx.doi.org/10.1111/j.1523-1739.2003.00377.x.
http://dx.doi.org/10.1111/j.1523-1739.20...
; Hasui et al., 2018Hasui É, Metzger JP, Pimentel RG, Silveira LF, Bovo AAA, Martensen AC, et al. Atlantic birds: a data set of bird species from the Brazilian Atlantic Forest. Ecology 2018; 99(2): 497. http://dx.doi.org/10.1002/ecy.2119. PMid:29266462.
http://dx.doi.org/10.1002/ecy.2119...
).
Given the scarcity of data on the occurrence of those protozoa in wild animals in the Northeast region of Brazil, the objective of this study was to identify Apicomplexa coccidia in wild birds from a screening center for wild animals and free-living birds.
Material and Methods
Sampling
Sampling was carried out between October and December 2019. Brain tissue samples from 71 wild birds of 27 species were collected from the Wild Animal Screening Center of the Pernambuco State (CETRAS-Tangara). These birds were found dead in the enclosures and submitted to necropsy to collect the brain fragments. This center houses hundreds of wild birds of different species, coming from voluntary delivery, seizure of trafficking, and open fairs by inspection agents. Additionally, 26 samples of wild free-ranging birds of 14 species were collected from the semi-arid region of the Caatinga biome in the state of Rio Grande do Norte. Information on the animals analyzed in this study is shown in Table 1.
Taxonomic order, common name, scientific name, number of samples, and origin (municipality and state) of the wild birds analyzed in this study.
DNA extraction and nested PCR
The brain fragments were macerated, weighed (25 mg), and subjected to DNA extraction using a commercial Wizard Genomic DNA Purification kit (Promega®). In order to evaluate contamination, a control sample (ultrapure water) was used in each round of DNA extraction. After extraction, the samples (including the controls of DNA extraction) were amplified by nested polymerase chain reaction (PCR) for the 18s gene of the ribosomal DNA (18S rDNA) of Apicomplexa protozoa, using 2µM of the external primers Tg18s48F (5'-CCATGCATGTCTAAGTATAAGC-3') and Tg18s359R (5'-GTTACCCGTCACTGCCAC-3'). Thermal profile consisted of an initial denaturation at 94 °C for 2 min, 30 cycles of denaturation at 94 °C for 30 s, annealing at 57 °C for 30 s, extension at 72 °C for 30 s, followed by a final extension at 72 °C for 1 min. It was followed by the nested PCR amplification using 2µM of the internal primers Tg18s58F (5'-CTAAGTATAAGCTTTTATACGGC-3') and Tg18s348R (5'-TGCCACGGTAGTCCAATAC-3'), according to the protocol described by Su et al. (2010)Su C, Shwab EK, Zhou P, Zhu XQ, Dubey JP. Moving towards an integrated approach to molecular detection and identification of Toxoplasma gondii. Parasitology 2010; 137(1): 1-11. http://dx.doi.org/10.1017/S0031182009991065. PMid:19765337.
http://dx.doi.org/10.1017/S0031182009991...
, and Melo et al. (2020)Melo RPB, Oliveira PRF, Albuquerque PPF, Barretto MLM, Moura GHF, Oliveira AAF, et al. Detection of Toxoplasma gondii DNA in heart tissue from a common marmoset (Callithrix jacchus) monitored for yellow fever and rabies in Pernambuco state, Northeastern of Brazil. Vet Parasitol Reg Stud Reports 2020; 21: 100447. http://dx.doi.org/10.1016/j.vprsr.2020.100447. PMid:32862888.
http://dx.doi.org/10.1016/j.vprsr.2020.1...
. The thermal profile was similar to the first PCR reaction, except for an increase to 35 cycles. Ultrapure water and the Toxoplasma gondii strain ME-49 were used as negative and positive control, respectively. Nested PCR products were visualized by electrophoresis in a 2% agarose gel stained with Blue Green (LGC®) and photodocumented.
Gel bands from the nested PCR products positively labeled for the 18S rDNA gene were purified using the QIAquick Gel Extraction Purification Kit (Qiagen), according to the manufacturer's protocol. The products were sequenced bidirectionally using the BigDye Terminator v3.1 Cycle Sequencing kit (Applied Biosystems). The oligonucleotides used for sequencing were the same as those for the second amplification step (Tg18s58F and Tg18s348R). Sequencing was performed by capillary electrophoretic separation on an ABI 3500 Genetic Analyzer sequencer (Applied Biosystems).
Sequencing data were collected using the Data Collection software (Applied Biosystems), and quality inspection was performed using Sequencing Analysis Software (Applied Biosystems). The sequences were analyzed by Staden Package 4.1.4 (Gene Codes Corporation, USA) and compared with the GenBank database using Basic Alignment Search Tools at the National Center for Biotechnology Information (www.ncbi.nlm.nih.gov) to identify genera or species.
Results
Protozoan DNA of the phylum Apicomplexa was detected in 26.7% (19/71) of the brain samples from the birds collected at CETRAS in Pernambuco. Regarding free-ranging birds, 23.75% (5/25) tested positive. Control samples of DNA extraction were all negative on PCR. It was not possible to obtain sufficient concentration of amplified DNA for sequencing for all the PCR-positive samples. Thus, 14 samples were sequenced: nine samples from CETRAS birds and five samples from free-living birds, from which three genera were identified: Isospora, Sarcocystis, and Toxoplasma (Table 2).
Identification of Apicomplexa phylum protozoan by nested Polymerase Chain Reaction (PCR) and DNA sequencing in brain fragment samples from 14 wild birds from Northeast Brazil.
Sequencing analysis of 12 positive samples indicated similarity of 100% with T. gondii sequences of the 18S rDNA gene (reference numbers from MT634248 to MT634250). One positive sample showed 99,6% similarity with Isospora sp. (reference numbers MW667591.1 and MW649139.1) and another positive sample was 100% similarity to Sarcocystis speeri, Sarcocystis neurona, and Sarcocystis felis (reference numbers KP681854.1, KT207459.1, AH009986.2, AY656815.1).
Toxoplasma gondii was the most frequently identified protozoan in the birds of CETRAS-Tangara, detected in two Red-cowled Cardinal (Paroaria dominicana), Yellow-bellied Seedeater (Sporophila nigricollis), two Turquoise-fronted Amazon (Amazona aestiva), and one Snowy Egret (Egretta thula). Isospora sp. was also identified in a cockerel and Sarcocystis sp. in a bananaquit, which is the first report of this genus in the species Coereba flaveola in Brazil.
Among free-ranging birds from the Caatinga biome in the state of Rio Grande do Norte, T. gondii was the only protozoan identified in a Ruddy Ground-dove (Columbina talpacoti), White-naped Jay (Cyanocorax cyanopogon), and three Red-legged Seriema (Cariama cristata).
Discussion
We detected Apicomplexa DNA in 25% (24/96) of the analyzed samples, and identified T. gondii (12.5%; 12/96), Sarcocystis spp. (1.04%; 1/96), and Isospora spp. (1.04%; 1/96) in the brain fragments of wild birds from the Northeast region of Brazil. Concentration and quality of the obtained amplified DNA limited the genetic sequencing of all positive samples, as they were directly collected from animal tissues where the parasites are heterogeneously distributed. Dubey (2010)Dubey JP. Toxoplasmosis of animals and humans. 2nd ed. Boca Raton: CRC Press; 2010. https://doi.org/10.1201/9781420092370.
https://doi.org/10.1201/9781420092370...
also reported that PCR was effective for diagnosis, but less so for genotyping, owing to the small amount of genetic material found in the tissues.
In Brazil, studies on the prevalence and distribution of protozoa of the Sarcocystidae family in wild animals by the detection of the 18S rDNA gene are limited. Melo et al. (2020)Melo RPB, Oliveira PRF, Albuquerque PPF, Barretto MLM, Moura GHF, Oliveira AAF, et al. Detection of Toxoplasma gondii DNA in heart tissue from a common marmoset (Callithrix jacchus) monitored for yellow fever and rabies in Pernambuco state, Northeastern of Brazil. Vet Parasitol Reg Stud Reports 2020; 21: 100447. http://dx.doi.org/10.1016/j.vprsr.2020.100447. PMid:32862888.
http://dx.doi.org/10.1016/j.vprsr.2020.1...
detected T. gondii in 17.9% (7/39) of heart samples from marmosets (Callithrix jacchus) in the state of Pernambuco. The genera Toxoplasma (22.7%, 10/44) and Sarcocystis (11.4%, 5/44) were reported in wild free-ranging birds rescued in the state of Minas Gerais (Rêgo et al., 2021Rêgo WMF, Costa JGL, Baraviera RCA, Pinto LV, Bessa GL, Lopes REN, et al. Sarcocystidae in wild birds of southeastern Brazil. Braz J Vet Parasitol 2021; 30(1): e028520. http://dx.doi.org/10.1590/s1984-296120201094. PMid:33605391.
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). Another study has shown 4.7% (91/1921) of bats with tissues positive for the 18S rDNA gene were detected, and eight genera of protozoa of the Sarcocystidae family (Besnoitia, Cystoisospora, Hammondia, Hyaloklossia, Neospora, Nephroisospora, Sarcocystis, and Toxoplasma) were identified in 50 samples of 16 bat species (belonging to the families Phyllostomidae, Molossidae, and Vespertilionidae) in the state of São Paulo (Cabral et al., 2021Cabral AD, Su C, Soares RM, Gennari SM, Sperança MA, Rosa AR, et al. Occurrence and diversity of Sarcocystidae protozoa in muscle and brain tissues of bats from São Paulo state, Brazil. Int J Parasitol Parasites Wildl 2021; 14: 91-96. http://dx.doi.org/10.1016/j.ijppaw.2021.01.003. PMid:33537206.
http://dx.doi.org/10.1016/j.ijppaw.2021....
). In addition, Ludwig et al. (2021)Ludwig A, Murer L, Santos HF, Ludwig A, Sangioni LA, Vogel FSF. Molecular detection of Apicomplexa protozoa in tissues from Alouatta guariba clamitans. Pesq Vet Bras 2021; 41: e06717. http://dx.doi.org/10.1590/1678-5150-pvb-6717.
http://dx.doi.org/10.1590/1678-5150-pvb-...
detected the 18S rDNA gene in brain and heart tissue from six brown howler monkey (Alouatta guariba clamitans) and identified the genus Sarcocystis (4/6) and Toxoplasma (2/6).
Silva et al. (2018)Silva MA, Pena HFJ, Soares HS, Aizawa J, Oliveira S, Alves BF, et al. Isolation and genetic characterization of Toxoplasma gondii from free-ranging and captive birds and mammals in Pernambuco State, Brazil. Braz J Vet Parasitol 2018; 27(4): 481-487. http://dx.doi.org/10.1590/s1984-296120180059. PMid:30184004.
http://dx.doi.org/10.1590/s1984-29612018...
isolated and genotypically characterized T. gondii from wild free-ranging or captive birds in the state of Pernambuco, Brazil, and described a non-virulent isolate of T. gondii in a free-living green-backed heron (Butorides striata). They also identified positive PCR samples for T. gondii in a spectacled owl (Pulsatrix perspicillata), an American kestrel (Falco sparverius), and a green-backed heron (B. striata), and warned of the risk of infection in endangered wild animals.
The identification of T. gondii in captive birds is a warning for wild animal conservation centers to take necessary measures, as severe clinical respiratory signs, blindness and encephalitis can occur in passerines with toxoplasmosis (Dubey, 2022Dubey JP. Clinical toxoplasmosis in zoo animals and its management. Emerg An Sp. 2022; 2: 100002. https://doi.org/10.1016/j.eas.2022.100002.
https://doi.org/10.1016/j.eas.2022.10000...
). Factors such as capture stress, environment and food changes, immunosuppression, inadequate enclosures, and the presence of individuals from different locations favor the spread of infectious agents (Andrade et al., 2016Andrade LHM, Lugarini C, Oliveira RA, Silva LT, Marvulo MFV, Garcia JE, et al. Occurrence of antibodies to Toxoplasma gondii in wild birds from three Federal Conservation Units of Paraíba and Bahia, Brazil. Pesq Vet Bras 2016; 36(2): 103-107. http://dx.doi.org/10.1590/S0100-736X2016000200007.
http://dx.doi.org/10.1590/S0100-736X2016...
; Silva et al., 2018Silva MA, Pena HFJ, Soares HS, Aizawa J, Oliveira S, Alves BF, et al. Isolation and genetic characterization of Toxoplasma gondii from free-ranging and captive birds and mammals in Pernambuco State, Brazil. Braz J Vet Parasitol 2018; 27(4): 481-487. http://dx.doi.org/10.1590/s1984-296120180059. PMid:30184004.
http://dx.doi.org/10.1590/s1984-29612018...
). CETRAS receives and shelters several species of birds from trafficking of wild animals from the Caatinga and Atlantic Forest, which are illegally captured and kept in unfavorable conditions, such as mistreatment, food stress, and overpopulation, making them susceptible to diseases.
In the present study, Psittaciformes and Passeriformes had the highest number (62/71) of analyzed individuals from CETRAS-Tangara, as these birds are trafficked the most in Brazil. P. dominicana is the most illegally traded species in Recife, Pernambuco (Pereira & Brito, 2005Pereira GA, Brito MT. Diversidade de aves silvestres brasileiras comercializadas nas feiras livres da Região Metropolitana do Recife, Pernambuco. Atual Ornitol 2005; 126: 14-20.), especially in the Northeast region of Brazil (Alves et al., 2013Alves RRN, Lima JRF, Araujo HFP. The live bird trade in Brazil and its conservation implications: an overview. Bird Conserv Int 2013; 23(1): 53-65. http://dx.doi.org/10.1017/S095927091200010X.
http://dx.doi.org/10.1017/S0959270912000...
), as the region has a high biodiversity, along with socioeconomic problems that drive the illegal capture and sale of animals, in addition to the cultural issues of hunting and domestic breeding. In this study, fragments of brain tissue from 13 specimens P. dominicana from Pernambuco state were analyzed and two samples were positive for T. gondii DNA and in one sample the DNA of Isospora was detected.
The free-living birds of the Caatinga biome that were found positive for T. gondii in our study have different feeding habits, such as the crow, which is omnivorous, and eats arthropods, insects and fruits, small rodents, small snakes, fish, and other smaller birds. The red-legged seriema eats insects to small vertebrates, such as rodents, reptiles, amphibians, and other bird species, whereas the Ruddy Ground-dove eats grains from the ground. It is not possible to state how the animals became infected. However, a possible source of infection for free-living birds is soil or water contaminated with T. gondii oocysts (Lindsay et al., 2003Lindsay DS, Collins MV, Mitchell SM, Cole RA, Flick GJ, Wetch CN, et al. Sporulation and survival of Toxoplasma gondii oocysts in seawater. J Eukaryot Microbiol 2003; 50(1): 687-688. http://dx.doi.org/10.1111/j.1550-7408.2003.tb00688.x. PMid:14736220.
http://dx.doi.org/10.1111/j.1550-7408.20...
), which is considered the most important form of T. gondii infection for animals (Dubey, 2010Dubey JP. Toxoplasmosis of animals and humans. 2nd ed. Boca Raton: CRC Press; 2010. https://doi.org/10.1201/9781420092370.
https://doi.org/10.1201/9781420092370...
). In addition, there are cataloged wild felids in this biome, such as the Northern Tiger Cat (Leopardus tigrinus), Ocelot (Leopardus pardalis), Jaguarundi (Herpailurus yagouaroundi), Puma (Puma concolor) (Marinho et al., 2018Marinho PH, Bezerra D, Antongiovanni M, Fonseca CR, Venticinque EM. Mamíferos de médio e grande porte da Caatinga do Rio Grande do Norte, nordeste do Brasil. Mastozool Neotrop 2018; 25(2): 345-362. http://dx.doi.org/10.31687/saremMN.18.25.2.0.15.
http://dx.doi.org/10.31687/saremMN.18.25...
) and Jaguar (Panthera onca) (Machado, 2020Machado L. A luta pela sobrevivência das onças da Caatinga [online]. São Paulo: BBC Brasil; 2020 [cited 2022 Mar 17]. Available from: https://www.bbc.com/portuguese/brasil-51289166
https://www.bbc.com/portuguese/brasil-51...
), which serve as definitive hosts of the parasite and may shed oocysts in feces contaminating the environment (Dubey, 2010Dubey JP. Toxoplasmosis of animals and humans. 2nd ed. Boca Raton: CRC Press; 2010. https://doi.org/10.1201/9781420092370.
https://doi.org/10.1201/9781420092370...
). Another possibility is the ingestion of tissue cysts from infected small mammals and birds. Wild birds, intermediate hosts of T. gondii, can be considered bioindicators of the presence of this coccidia, and the detection of seropositive birds suggests that they have ingested sporulated oocysts from the soil, water, or contaminated food (Gondim et al., 2010Gondim LSQ, Abe-Sandes K, Uzêda RS, Silva MSA, Santos SL, Mota RA, et al. Toxoplasma gondii and Neospora caninum in sparrows (Passer domesticus) in the Northeast of Brazil. Vet Parasitol 2010; 168(1-2): 121-124. http://dx.doi.org/10.1016/j.vetpar.2009.09.055. PMid:19879051.
http://dx.doi.org/10.1016/j.vetpar.2009....
), as well as the detection of protozoa DNA in animal tissues confirms the infection. Studies like ours can be performed without collecting blood to obtain sera and are a useful way to access environmental contamination with oocysts, since different avian populations feed directly on the ground (Dubey, 2002Dubey JP. A review of toxoplasmosis in wild birds. Vet Parasitol 2002; 106(2): 121-153. http://dx.doi.org/10.1016/S0304-4017(02)00034-1. PMid:12031816.
http://dx.doi.org/10.1016/S0304-4017(02)...
).
Caatinga is a unique Brazilian biome that is home to 182 species of endangered animals, of which 46 are endemic to this biome. This is mainly due to the expansion of agricultural activities that have already devastated >50% of the native vegetation. Thus, studying infectious agents, such as those of the Apicomplexa phylum, which have a negative impact on animal health, provides important data that help in the conservation of threatened species (Figueiredo, 2019Figueiredo P. Caatinga tem 182 animais ameaçados; no país, quase 10% dos monitorados estão sob risco de extinção [online]. Rio de Janeiro: G1; 2019 [cited 2022 Mar 28]. Available from: https://g1.globo.com/natureza/desafio-natureza/noticia/2019/02/20/caatinga-tem-182-animais-ameacados-no-pais-quase-10-dos-monitorados-estao-sob-risco-de-extincao.ghtml
https://g1.globo.com/natureza/desafio-na...
).
The detection of Isospora sp. in brain tissue of CETRAS animal poses health risks to wild birds. This parasite is considered as endemic in wild birds, and infection does not result in a significant mortality rate, however cases of fatal disease may occur under the influence of stress, concurrent infections, or immunosuppression, especially for young birds in captivity (Cushing et al., 2011Cushing TL, Schat KA, States SL, Grodio JL, O’Connell PH, Buckles EL. Characterization of the host response in systemic isosporosis (atoxoplasmosis) in a colony of captive American goldfinches (Spinus tristis) and house sparrows (Passer domesticus). Vet Pathol 2011; 48(5): 985-992. http://dx.doi.org/10.1177/0300985810391114. PMid:21311069.
http://dx.doi.org/10.1177/03009858103911...
). Isospora extraintestinal infection has been reported in a wide variety of birds, such as canaries (Quiroga et al., 2000Quiroga MI, Aleman N, Vázquez S, Nieto JM. Diagnosis of atoxoplasmosis in a canary (Serinus canarius) by histopathologic and ultrastructural examination. Avian Dis 2000; 44(2): 465-469. http://dx.doi.org/10.2307/1592564. PMid:10879930.
http://dx.doi.org/10.2307/1592564...
), blue-crowned laughingthrush (Jamriška et al., 2013Jamriška J, Barbón AR, Modrý D. A new species of Isospora Schneider, 1881 (Apicomplexa: Eimeriidae) from the blue-crowned laughingthrush Dryonastes courtoisi (Passeriformes: Timaliidae). Acta Protozool 2013; 52(2): 99-103. http://dx.doi.org/10.4467/16890027AP.13.0010.1089.
http://dx.doi.org/10.4467/16890027AP.13....
; Mohr et al., 2017Mohr F, Betson M, Quintard B. Investigation of the presence of Atoxoplasma spp. in blue-crowned laughingthrush (Dryonastes courtoisi) adults and neonates. J Zoo Wildl Med 2017; 48(1): 1-6. http://dx.doi.org/10.1638/2016-0044.1. PMid:28363058.
http://dx.doi.org/10.1638/2016-0044.1...
; Barbón et al., 2019Barbón AR, López J, Jamriška J, Thomasson A, Braun J, Stidworthy MF. Clinical and pathological aspects of systemic Isospora infection in blue-crowned laughing thrushes (Garrulax courtoisi) at Jersey Zoo. J Avian Med Surg 2019; 33(3): 265-277. http://dx.doi.org/10.1647/2018-377. PMid:31893622.
http://dx.doi.org/10.1647/2018-377...
), tanagers (Adkesson et al., 2005Adkesson MJ, Zdziarski JM, Little SE. Atoxoplasmosis in tanagers. J Zoo Wildl Med 2005; 36(2): 265-272. http://dx.doi.org/10.1638/03-091.1. PMid:17323568.
http://dx.doi.org/10.1638/03-091.1...
), green-winged saltator (Oliveira et al., 2018Oliveira AR, Souza TD, Mol JPS, Flecher MC, Hiura E, Santos RL. Pathological and molecular characterization of systemic isosporosis (atoxoplasmosis) in captive green-winged saltator (Saltator similis). Vet Parasitol 2018; 255: 98-101. http://dx.doi.org/10.1016/j.vetpar.2018.04.007. PMid:29773145.
http://dx.doi.org/10.1016/j.vetpar.2018....
), sparrows, finches, starlings, and thrushes (Cushing et al., 2011Cushing TL, Schat KA, States SL, Grodio JL, O’Connell PH, Buckles EL. Characterization of the host response in systemic isosporosis (atoxoplasmosis) in a colony of captive American goldfinches (Spinus tristis) and house sparrows (Passer domesticus). Vet Pathol 2011; 48(5): 985-992. http://dx.doi.org/10.1177/0300985810391114. PMid:21311069.
http://dx.doi.org/10.1177/03009858103911...
). Clinical signs of atoxoplasmosis (systemic isosporosis) in birds are nonspecific and may include anorexia, diarrhea, ruffled feathers, reduction of pectoral musculature, distended abdomen, retracted neck, and respiratory difficulties (Maslin & Latimer, 2009Maslin WR, Latimer KS. Atoxoplasmosis in canary fledglings: severe lymphocytic enteritis with preferential parasitism of B lymphocytes. Avian Dis 2009; 53(3): 473-476. http://dx.doi.org/10.1637/8557-121008-Case.1. PMid:19848092.
http://dx.doi.org/10.1637/8557-121008-Ca...
).
Furthermore, we identified Sarcocystis spp. in wild captive birds. This protozoan has already been described in wild free-ranging birds in Brazil (Rêgo et al., 2021Rêgo WMF, Costa JGL, Baraviera RCA, Pinto LV, Bessa GL, Lopes REN, et al. Sarcocystidae in wild birds of southeastern Brazil. Braz J Vet Parasitol 2021; 30(1): e028520. http://dx.doi.org/10.1590/s1984-296120201094. PMid:33605391.
http://dx.doi.org/10.1590/s1984-29612020...
), especially Sarcocystis falcatula, which has already been associated with the mortality of 38 parrots in Parque das Aves in Foz do Iguaçu, Paraná (Godoy et al., 2009Godoy SN, Paula CD, Cubas ZS, Matushima ER, Catão-Dias J. Occurrence of Sarcocystis falcatula in captive Psittacine birds in Brazil. J Avian Med Surg 2009; 23(1): 18-23. http://dx.doi.org/10.1647/2008-006R.1. PMid:19530402.
http://dx.doi.org/10.1647/2008-006R.1...
), with meningoencephalitis, and pulmonary alterations (Godoy et al., 2009Godoy SN, Paula CD, Cubas ZS, Matushima ER, Catão-Dias J. Occurrence of Sarcocystis falcatula in captive Psittacine birds in Brazil. J Avian Med Surg 2009; 23(1): 18-23. http://dx.doi.org/10.1647/2008-006R.1. PMid:19530402.
http://dx.doi.org/10.1647/2008-006R.1...
; Dubey, 2010Dubey JP. Toxoplasmosis of animals and humans. 2nd ed. Boca Raton: CRC Press; 2010. https://doi.org/10.1201/9781420092370.
https://doi.org/10.1201/9781420092370...
). Recently, Adão et al. (2021)Adão CE, Brisqueleal BGP, Daga CS, Piccoli R, Matos MR. Sarcocystis falcatula em papagaio-do-congo (Psittacus erithacus): relato de caso. Med Vet 2021; 15(3): 250-254. http://dx.doi.org/10.26605/medvet-v15n3-3549.
http://dx.doi.org/10.26605/medvet-v15n3-...
reported sudden illness and death in a gray parrot (Psittacus erithacus) that lived with its owner and had contact with other birds. At necropsy, macroscopic and microscopic features confirmed the diagnosis of S. falcatula.
Although Sarcocystis infection is usually asymptomatic, studies have warned about the presence of this pathogen in free-ranging and captive birds as an important epidemiological indicator of environmental imbalance, in addition to highlighting the risks for species of the orders Psittaciformes, Columbiformes, and Passeriformes, which are most prone to trafficking and extinction risks. Although studies on S. falcatula and S. calchasi in wild birds are scarce, S. falcatula infections generally show hyperacute symptoms with severe lung injury, whereas S. calchasi can lead to meningoencephalitis (Dubey et al., 2015Dubey JP, Calero-Bernal R, Rosenthal BM, Speer CA, Fayer R. Sarcocystosis of animals and humans. 2nd ed. Boca Raton: CRC Press; 2015. http://dx.doi.org/10.1201/b19184.
http://dx.doi.org/10.1201/b19184...
).
It is not possible to determine the moment at which the Apicomplexa infected the CETRAS birds, which may have occurred naturally or after the birds arrived at the enclosures. It is also not possible to comment on the infection sources, but it is known that the feeding habits of each species can influence the risk of infection. The species of birds that were positive for apicomplexan protozoans in this study had different feeding habits in nature.
The animals of the Psittacidae family, represented by the Turquoise-fronted Amazon (Amazona aestiva) and the Northern-red shouldered Macaw (Diopsittaca nobilis), feed on seeds and fruits, and foraging is done on tree branches. In restricted environments, these individuals remain in cages or nurseries and usually forage on the ground, which is the possible site of oocyst ingestion. The passerine diet consists of grains, seeds, fruits, and insects (Sick, 1997Sick H. Ornitologia brasileira. Rio de Janeiro: Nova Fronteira; 1997.). In nature, due to shrub/tree feeding, oocyst ingestion is minimized, whereas in nurseries, foraging is carried out in feeders and on the ground, which increases the risk of oocyst ingestion. The Snowy Egret (Egretta thula) is an aquatic bird that lives near lakes and rivers and feeds on fish; therefore, infection is associated with pollution and improper dumping of contaminants that carry oocysts (Gwynne et al., 2010Gwynne JA, Ridgely RS, Tudor G, Argel M. Wildlife conservation society birds of Brazil: the Pantanal and Cerrado of Central Brazil. Ithaca: Cornell University Press; 2010.). In captivity, their diet is usually similar to that in the wild, especially fish, and the risk of infection is related to the quality of food.
Conclusion
This is the most comprehensive study on the occurrence of Apicomplexa protozoa in wild birds from a rehabilitation center and in the wild in the Northeast region of Brazil. The results obtained confirms the infection of wild birds by apicomplexan coccidia (Toxoplasma gondii, Isospora sp. and Sarcocystis sp.) and provide important epidemiological information for the adoption of preventive measures for the conservation of wild birds in captivity and the environment.
Acknowledgements
This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brazil (CAPES) - Finance Code 001.
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How to cite: Moura GHF, Nascimento GS, Oliveira PRF, Santana VS, Shimabukuro A, Valença YM, et al. Occurrence of Apicomplexa protozoa in wild birds in the Northeast region of Brazil. Braz J Vet Parasitol 2023; 32(2): e014722. https://doi.org/10.1590/S1984-29612023020
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Publication Dates
-
Publication in this collection
17 Apr 2023 -
Date of issue
2023
History
-
Received
19 Oct 2022 -
Accepted
02 Mar 2023