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Revista Brasileira de Parasitologia Veterinária

Print version ISSN 0103-846XOn-line version ISSN 1984-2961

Rev. Bras. Parasitol. Vet. vol.28 no.4 Jaboticabal Oct./Dec. 2019  Epub July 29, 2019

https://doi.org/10.1590/s1984-29612019053 

Short communication

Parasitism of the nasal mite Sternostoma tracheacolum Lawrence, 1948 (Mesostigmata: Rhinonyssidae) in captive birds in Brazil

Parasitismo do ácaro nasal Sternostoma tracheacolum Lawrence, 1948 (Mesostigmata: Rhinonyssidae) em aves de cativeiro no Brasil

Ricardo Bassini-Silva1 
http://orcid.org/0000-0002-9568-4120

Fernando de Castro Jacinavicius1  2 
http://orcid.org/0000-0002-5503-3120

Josivania Soares Pereira3 
http://orcid.org/0000-0002-2407-9417

Karin Werther4 
http://orcid.org/0000-0002-8822-488X

Greg Sherwood Spicer5 
http://orcid.org/0000-0002-4923-4348

Darci Moraes Barros-Battesti1  4  * 
http://orcid.org/0000-0002-8541-2252

1Departamento de Medicina Veterinária Preventiva e Saúde Animal, Faculdade de Medicina Veterinária e Zootecnia – FMVZ, Universidade de São Paulo – USP, São Paulo, SP, Brasil

2Laboratório Especial de Coleções Zoológicas, Instituto Butantan, São Paulo, SP, Brasil

3Laboratório de Parasitologia Animal, Departamento de Biociências, Centro de Ciências Biológicas e da Saúde, Universidade Federal Rural do Semi-Árido – UFERSA, Mossoró, RN, Brasil

4Departamento de Patologia Veterinária, Faculdade de Ciências Agrárias e Veterinárias, Universidade Estadual Paulista – UNESP, Jaboticabal, SP, Brasil

5Department of Biology, San Francisco State University, San Francisco, CA, USA


Abstract

Nasal mites (Mesostigmata: Rhinonyssidae) are obligatory endoparasites of birds, and the resulting parasitism can be harmful to the host’s respiratory system. The nasal mite Sternostoma tracheacolum Lawrence has caused significant respiratory issues, including serious injuries that possibly cause death of the host. In this study, we report two cases of captive birds parasitized by S. tracheacolum. The first case is a histopathological description of S. tracheacolum parasitizing the Gouldian Finch (Chloebia gouldiae) in the southeast region of Brazil, that showed partially or totally absence of the characteristic respiratory epithelium in trachea lumen. The other describes, for the first time, the parasitism of this species in a canary (Serinus canaria) in the northeast region of the country.

Keywords:  Sternostoma tracheacolum; endoparasite; Chloebia gouldiae; Serinus canaria

Resumo

Os ácaros nasais (Mesostigmata: Rhinonyssidae) são endoparasitos obrigatórios das aves, e este parasitismo pode ser prejudicial ao sistema respiratório de seu hospedeiro. A espécie de ácaro nasal Sternostoma tracheacolum Lawrence tem causado importantes problemas respiratórios, incluindo lesões graves que possivelmente causam a morte do hospedeiro. Neste estudo, relatamos dois casos de aves em cativeiro parasitadas por S. tracheacolum. O primeiro caso é uma descrição histopatológica de S. tracheacolum parasitando um Diamante-de-gould (Chloebia gouldiae) na região sudeste do Brasil, mostrando parcial ou total ausência do epitélio respiratório característico do lúmen da traqueia. O outro descreve, pela primeira vez, o parasitismo desta espécie em um canário (Serinus canaria) na região nordeste do país.

Palavras-chave:  Sternostoma tracheacolum; endoparasita; Chloebia gouldiae; Serinus canaria

Introduction

Mites of the family Rhinonyssidae Trouessart, 1895, popularly known as nasal mites, are obligatory endoparasites of birds that specifically target the respiratory system (PENCE, 1975). This family is organized in eight genera, about 500 species, and has been described around the world (DOMROW, 1969; PENCE, 1975; BEAULIEU et al., 2011). Six genera have already been reported in Brazil, Larinyssus Strandtmann, 1948, Ptilonyssus Berlese & Trouessart, 1889, Rhinoecius Cooreman, 1946, Rhinonyssus Trouessart, 1894, Sternostoma Berlese & Trouessart, 1889 and Tinaminyssus Strandtmann & Wharton, 1958. Of these, Sternostoma has sixteen species recorded parasitizing birds of the order Apodiformes, Charadriiformes, Passeriformes, Psittaciformes and Strigiformes, across the Brazilian territory, except for the northeast region (CASTRO, 1948; FAIN & BASTIN, 1959; AMARAL, 1962; 1968; FAIN & AITKEN, 1968, 1969, 1971; AMARAL & REBOUÇAS, 1974a; MASCARENHAS et al., 2011; MENDES et al., 2014; BERNARDON et al., 2017; MASCARENHAS et al., 2018; SILVA et al., 2018; SANTOS et al., 2018).

Sternostoma tracheacolum Lawrence, 1948 is spread worldwide and has been recorded in both captive and wild birds. This species resides throughout the respiratory system, ranging from the trachea to the air sacs, and is known to cause complications (MURRAY, 1966; BELL, 1996). In general, the clinical signs on the hosts are dyspnea, coughing, sneezing, and in severe infestations the host may die from asphyxiation (BYGRAVE, 1980; DIMOV, 2011).

In Brazil, S. tracheacolum was found parasitizing captive birds, as Serinus canaria (Passeriformes: Fringillidae) in Rio Grande do Sul state (FAIN & HYLAND, 1962; GUIMARÃES et al., 2012), Rio de Janeiro state (TORRES et al., 1951; AMARAL, 1962) and São Paulo state (AMARAL, 1968; AMARAL & REBOUÇAS, 1974a), and Melopsittacus undulatus (Psittaciformes: Psittacidae) in Rio de Janeiro state (AMARAL, 1968). This mite species was also recorded parasitizing wild birds, as Cyanerpes cyaneus (Passeriformes: Thraupidae), without specific locality (FAIN & HYLAND, 1962), Molothrus bonariensis (Passeriformes: Icteridae) in Rio Grande do Sul state (AMARAL, 1968), Dendrocincla merula (Passeriformes: Furnariidae) and Rhynchocyclus olivaceus (Passeriformes: Tyrannidae) in Pará state (FAIN & AITKEN, 1971) and Passer domesticus (Passeriformes: Passeridae) in Rio Grande do Sul state (SANTOS et al., 2018).

The objectives of the present study are: to describe a parasitism and characterize the histopathological lesions of S. tracheacolum on a Gouldian Finch (Chloebia gouldiae) bird in the southeast region of Brazil; and to document parasitism of the same nasal mite on a canary (S. canaria), but in the northeast region of the country.

Materials and Methods

Morphological identification

Fifteen mite specimens were collected parasitizing the respiratory system of one C. gouldiae (Passeriformes: Estrildidae) found in the Ibitinga city, in the state of São Paulo, Brazil. Another ten specimens were collected parasitizing S. canaria, from the Mossoró city, in the state of Rio Grande do Norte, Brazil. Both birds were domestic. All the collected materials were initially preserved and stored in 100% alcohol. Later, selected materials were slide-mounted in Hoyer’s medium and prepared for scanning electron microscopy (SEM) for identification, both processes according to Walter & Krantz (2009). All the material was deposited in the Acari Collection of the Instituto Butantan (IBSP), São Paulo state, Brazil. The SEM micrographs were obtained using a Digital Scanning Microscope FEI, Quanta 250, located at the Laboratório de Biologia Celular, Instituto Butantan, São Paulo state, Brazil. The figures were prepared with Adobe Photoshop v. 13.0. The specimens were identified, up to genus and species, using the keys proposed by Pence (1975).

Histopathological analysis

The trachea and lungs of the C. gouldiae were collected during necropsy, and the tissues were fixed in 10% buffered formalin for 24 hours. The samples were through to routine processes of dehydration in growing alcohol battery, diaphanized in xylol and paraffinized. Soon after, the materials were embedded in paraffin, cut into portions measuring 4 micrometers each, and placed individually on slides. Then, the samples were deparaffinized in xylol, rehydrated in an alcohol battery, stained with hematoxylin and eosin, and mounted with coverslips (SLAOUI et al., 2017). No material was obtained for histological sections of the host S. canaria.

Results

The mites were identified as S. tracheacolum and the specimens were deposited in the IBSP collection. These nasal mites can be identified by the following characteristics: opisthosomal shield with six setae, stigma without peritremes, gnathosoma partially ventral, sternal shield with three setae, and anal shield terminal (Figure 1).

Figure 1 Morphological details of Sternostoma tracheacolum. (A) dorsal view of the podosoma; (B) anterior view of the podosoma shield; (C) ventral view of the idiosoma; (D) gnathosoma subcapitular; (E) sternal shield; (F) genital shield. Scales: A 100 µm; B, D-F 50 µm; C 200 µm. 

The parasitism of the S. tracheacolum was only found during necropsy in the trachea of C. gouldiae, since it had no clinical signs in the respiratory system. According to the owner of the Gouldian Finch, before death, the bird had brownish diarrhea and dirty feathers around the cloaca, but there was no breathing difficulty. A histopathological examination was carried out in the respiratory and digestive systems to know the actual cause of death of this bird. In the histopathological of the region of the trachea and lungs of C. gouldiae it is possible to observe the presence of the mites in the lumen. Also, we can observe partially or totally absence of the characteristic respiratory epithelium in trachea lumen. In the lumen of primary bronchi parasitized by S. tracheacolum the parenchyma presented congested blood vessels (Figure 2). No inflammatory cells were associated with the local of the parasites. However, the birds showed relevant alterations at intestines, pancreas and liver. According to the report of the bird, the intestine had loss of villi; inflammatory infiltrate in the submucosa, indicating enteritis, the pancreas already had signs of multifocal degeneration/necrosis with karyolysis, whereas the liver had a cytoplasmic degeneration with moderate vacuolization (steatosis), and limited hepatocyte delimitation indicating that the organ was degenerating. The most obvious change was enteritis (inflammation of the intestine) that would directly compromise the digestion and feeding of the animal, as seen by the droplets of fat in the faces, which may be responsible for the death, confirming what the bird owner reported. Differently from the canary’s case, since this bird, before death, already had shown signs of labored breathing, characterized by acute dyspnea. Possibly, it died as a consequence of the parasitism of these nasal mites, only detected after necropsy.

Figure 2 Histopathological images. (A) histopathological aspect of the lungs (L) of Chloebia gouldiae parasitized by Sternostoma tracheacolum. The nasal mite (P) are in the lumen of primary bronchi and the blood vessel (BV) are congest in the parenchyma; (B-D) histopathological aspect of the trachea of Chloebia gouldiae parasitized by Sternostoma tracheacolum. In the figures B, C and D, the red arrows show the partial absence of typical respiratory epithelium and in the figures B and C the “*” the presence of avian nucleated erythrocytes from the host; All images in HE stains. Scales: A 100 µm; B and C 50 µm; D 20 µm. 

Material examined. 15 ♀ (IBSP 13772), Ibitinga municipality, São Paulo state, V-2018, Chloebia gouldiae (Passeriformes: Estrildidae), Werther K. coll.; 10 ♀ (IBSP 13379), Mossoró municipality, Rio Grande do Norte state, Brazil, 03-VII-2017, Serinus canaria (Passeriformes: Fringillidae), Soares J. P. coll.

Discussion

In general, an infestation of the species S. tracheacolum in the host is diagnosed late, because of the difficulty of detecting the mites. This is only possible, after the death of the hosts, through necropsy (AMARAL & REBOUÇAS, 1974b), as well as, in this study with the species C. gouldiae, but this does not mean that the nasal mites were the direct cause of death of the bird.

Tidemann et al. (1992) observed areas of bronchial dilatation with detritus, macrophages and lymphocytes in the lumen. In fact, in the present study, these kinds of cells are not indicated but the mite infestation caused partial absence of typical respiratory epithelium of the C. gouldiae. On the other hand, although a histopathological examination was not performed, there were clinical signs in S. canaria that corroborated with that observed by Tidemann et al. (1992).

Some authors have quoted that wild birds better survive the infestation of S. tracheacolum than captive birds, so the wild birds are probably the natural hosts of this mite (FAIN & HYLAND, 1962; RIFFKIN & MCCAUSLAND, 1972). Besides that, the immune system of captive birds is affected by the captivity, thus causing a greater susceptibility to infestation in these birds (FAIN & HYLAND, 1962; GUIMARÃES et al., 2012). In fact, the competence of the bird immune system is also strongly influenced by inadequate nutrition for species, breeding health problems, high numbers of birds (overpopulation) and lack of quarantine and periodic examinations. As Dimov (2011) reported in his case report, in this study the S. canaria also presented labored respiration, characterized by acute dyspnea.

Also, Tidemann et al. (1992) demonstrated that this nasal mite may also influence in the development of Gouldian Finch populations in Australia, and Murray (1966) had already highlighted the susceptibility of this bird to the infestation by this mite. Thus, it is necessary to report the presence of this mite in captive birds, even if they do not present clinical signs of parasitism, since there are reports of the succession of these birds and possible injuries resulting from parasitism.

Besides that, there are several records of canaries being parasitized by S. tracheacolum in some states of Brazil, such as Pará, Rio de Janeiro, Rio Grande do Sul and São Paulo (AMARAL, 1962, 1968; AMARAL & REBOUÇAS, 1974a; GUIMARÃES et al., 2012). Except for the most recent study, the others are only taxonomic papers.

Here, we report the parasitism of S. tracheacolum in Gouldian Finch, for the first time in Brazil. We are also reporting this species parasitizing a canary in the northeast region of the country.

Acknowledgements

To Gabrielle Ribeiro de Andrade and Maria Cristina Ferreira do Rosário for technical contribution (CNPq no. 377343/2015-3 and 377342/2015-7, respectively). To Beatriz Mauricio of the Laboratory of Cellular Biology of the Butantan Institute for the images obtained through the Scanning Electron Microscopy. This work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq no. 454907/2014-1 and 440639/2015-8 to DMB-B, 377976/2014-8 to FCJ), Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP no. 2010/51875-9 to DMB-B and 2017/01416-7 to RB-S). This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001.

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Received: March 18, 2019; Accepted: June 05, 2019

*Corresponding author: Darci Moraes Barros-Battesti. Departamento de Patologia Veterinária, Faculdade de Ciências Agrárias e Veterinárias – UNESP, R. Castellane, s/n, Via de Acesso Professor Paulo Donato Castelane, Vila Industrial, CEP 14884-900, Jaboticabal, SP, Brasil. e-mail: barros.battesti@gmail.com

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