New reports of parasitism by Synhimantus (Dispharynx) nasuta (Rudolphi, 1819) (Nematoda: Acuariidae) in wild birds in Brazil

Novos relatos de parasitismo por Synhimantus (Dispharynx) nasuta (Rudolphi, 1819) (Nematoda: Acuariidae) em aves silvestres no Brasil

Abstract

The aim of this study was to register the first occurrence of Synhimantus (Dispharynx) nasuta (Nematoda: Acuariidae) in some species of wild birds in Brazil. In addition, the aim was to deepen the knowledge about the morphology of this species through analysis using scanning electron microscopy. Nematodes were collected in wild birds of the species Turdus leucomelas, T. rufiventris, Mimus saturninus, Pitangus sulphuratus, Megascops choliba, Tyto furcata, and Falco sparverius. The morphological and morphometric data observed in the nematodes prove that these parasites are S. (D.) nasuta. This study also provides morphological data from light microscopy and scanning electron microscopy (SEM), as well as the morphometry of this nematode in each host species. Therefore, the current study confirms the first record of this nematode in F. sparverius and T. furcata in South America and, at the same time, these findings expand the host range of this parasite species worldwide, through the first records in M. choliba, M. saturninus, T. leucomelas and T. rufiventris.

Keywords:
Nematoda; wild birds; morphology; Zona da Mata; new records

Resumo

O objetivo deste estudo foi registrar a primeira ocorrência de Synhimantus (Dispharynx) nasuta (Nematoda: Acuariidae) em algumas espécies de aves silvestres do Brasil. Além disso, pretendeu-se aprofundar o conhecimento sobre a morfologia desta espécie por meio de análises por microscopia eletrônica de varredura. Os nematoides foram coletados em aves silvestres das espécies Turdus leucomelas, T. rufiventris, Mimus saturninus, Pitangus sulphuratus, Megascops choliba, Tyto furcata e Falco sparverius. Os dados morfológicos e morfométricos observados nos nematoides comprovaram que esses parasitos são S. (D.) nasuta. Este estudo também fornece dados morfológicos de microscopia de luz e microscopia eletrônica de varredura (MEV), assim como a morfometria deste nematoide em cada espécie de hospedeiro. Portanto, o presente estudo confirma o primeiro registro desse nematoide em F. sparverius e T. furcata na América do Sul e, ao mesmo tempo, esses achados ampliam a gama de hospedeiros dessa espécie de parasito em todo o mundo, por meio dos primeiros registros em M. choliba, M. saturninus, T. leucomelas e T. rufiventris.

Palavras-chave:
Nematoda; aves silvestres; morfologia; Zona da Mata; novos registros

Introduction

Synhimantus (Dispharynx) nasuta (Rudolphi, 1819) (Spirurida: Acuariidae) is a nematode parasite that inhabits the gastrointestinal system of domestic and wild birds worldwide. It can be found in different organs such as the esophagus, gizzard, proventriculus and small intestine (Zhang et al., 2004; Carreno, 2008).

This nematode has a wide geographic distribution, with records of infection in North, Central and South America, Africa, Australia, Europe and Asia (Carreno, 2008). In Brazil, presence of S. (D.) nasuta has been reported in the domestic birds as Gallus gallus domesticus Linnaeus, 1758, Meleagris gallopavo Linnaeus, 1758, and Columba livia Gmelin, 1789 (Vicente et al., 1995), Pavo cristatus Linnaeus, 1758 (Duarte & Dórea, 1987), Passer domesticus Linnaeus, 1758 (Brasil & Amato, 1992); Phasianus colchicus Linnaeus, 1758 (Pinto et al., 2004). In wild birds from Brazil, this parasite was previously reported in Guira guira Gmelin, 1788, and Crotophaga ani Linnaeus, 1758 (Bartmann & Amato, 2009), Paroaria capitata Orbigny & Lafresnaye, 1837 (Mascarenhas et al., 2009), Pitangus sulphuratus Linnaeus, 1766 (Mendes, 2011), Molothrus bonariensis Gmelin, 1789 (Bernardon et al., 2016) and Vanellus chilensis Molina, 1782 (Silveira & Calegaro-Marques, 2016).

The aim of this study was to register the first occurrence of S. (D.) nasuta in some species of wild birds in Brazil. In addition, the aim was to deepen the knowledge about the morphology of this species through analysis using scanning electron microscopy analyses.

Material and Methods

Were necropsied a total of 69 wild birds of the species Turdus leucomelas Vieillot, 1818 (Passeriformes: Turdidae) (N=5), Turdus rufiventris Vieillot, 1818 (Passeriformes: Turdidae) (N=22), Mimus saturninus Lichtenstein, 1823 (Passeriformes: Mimidae) (N=2), Pitangus sulphuratus Linnaeus, 1766 (Passeriformes: Tyrannidae) (N=20), Megascops choliba Vieillot, 1817 (Strigiformes: Strigidae) (N=13), Tyto furcata Scopoli, 1769 (Strigiformes: Tytonidae) (N=3), and Falco sparverius Linnaeus, 1758 (Falconiformes: Falconidae) (N=4) over a period of time between 2013 and 2017. These birds were received at Wild Animal Screening Center (CETAS) of Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio), in the municipality of Juiz de Fora, after being collected in clandestine breeding and trafficking, abuse, and sales, in the Zona da Mata region in the state of Minas Gerais. The birds died in captivity were sent under freezing conditions for helminthological studies to the Laboratório de Taxonomia e Ecologia de Helmintos – Odile Bain (LATECH Odile Bain), of the Departamento de Zoologia of the Universidade Federal de Juiz de Fora (UFJF).

The parasites collected in these birds were fixed in 4% Formalin at room temperature (nematodes were dead at the time of collection) and kept in this fixative for 7 days and stored in 70ºGL ethanol (Vieira et al., 2015). For morphological and morphometric studies in the light microscope Olympus BX41 with drawing tube, the nematodes, after washing in current water, were clarified in Amann's lactophenol and mounted in temporary slides (Amato & Amato, 2010). The number of nematodes analyzed in light microscopy was selected according to the morphological condition of the parasites and the size of the infrapopulations in each host specimens. Photographs in light microscopy were taken under differential interference contrast microscopy (DIC) using an Olympus BX51 microscope coupled with an Olympus UC 30 digital camera. For scanning electron microscopy (SEM) a sample of these helminths was dehydrated in increasing series of ethanol, dried in 97% 1,1,1,3,3,3-Hexamethyldisilazane, mounted in stubs with carbon tape, gold coated, and analysed in a scanning electron microscope JEOL JSM 6390LV SEM (Vieira et al., 2015), in the Plataforma de Microscopia Eletrônica – Rudolf Barth, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro.

The identification to generic level of the nematodes collected in the proventriculus was made according to Chabaud (1975). For the specific identification, studies with morphological and morphometric data of Synhimantus (Dispharynx) were consulted (Zhang et al., 2004; Dewi et al., 2006; Bartmann & Amato, 2009; Oyarzún-Ruiz et al., 2016; Hernandez-Urraca et al., 2022). The morphometric data are provided in micrometers (µm), except when another unit is informed. The prevalence, mean intensity, and mean abundance of helminth were calculated according to Bush et al. (1997). Voucher specimens have been deposited in the Coleção Helmintológica Odile Bain (CHOB), Departamento de Zoologia, Universidade Federal de Juiz de Fora, in the state of Minas Gerais, Brazil.

Results

Description

Synhimantus (Dispharynx) nasuta (Rudolphi, 1819)

(Figures 1 and 2, Table 1)

Figure 1
Synhimantus (Dispharynx) nasuta from Pitangus sulphuratus, at light microscope. A, Male, cuticular projections in the cloacal region (white arrow); distal end of the right spicule (asterisk); B, Male, postcloacal papillae (black arrow); right spicule short (asterisk); left spicule long (white arrow); boundary between the shaft and the lamina of the left spicule (black setae); C, Male, right spicule short (asterisk); left spicule long (white arrow); D, Male. descending cephalic cordons (white arrow); ascending cephalic cordons (black arrow); cervical papillae (asterisk). Scale: A, 90μm; B 40μm; 60μm; C 40μm; D 60μm.

Figure 2
Synhimantus (Dispharynx) nasuta from Megascops choliba, at Scanning Electron Microscope (SEM). A, Male. Anterior region. Latero apical view. B, Male, deirid, lateral view. C, Male, anterior end. Apical view; D, Male. Posterior end. Latero ventral view; E. Male. Cloacal region, ventral view; F. Female. Latero ventral view (abbreviations: a – amphid, an – anus, cp - cephalic papapilla, d – deirid, db - descending branch of cord, pl – pseudo labia, post – post cloacal papilla, pre – pre cloacal papilla, rb - recurrent branch of cord, s - spicule).

Table 1
Morphometric data of males and females of Synhimantus (Dispharynx) nasuta in each host species, in the Microregion of Zona da Mata Mineira, Minas Gerais, Brazil.

Hosts species (Number of analyzed hosts)

Turdus rufiventris (N=22)

Turdus Leucomelas (N=5)

Pitangus sulphuratus (N=20)

Mimus Saturninus (N=2)

Tyto furcata (N=2)

Falco sparverius (N=4)

Megascops choliba (N=13)

Prevalence

22.7%

20%

65%

50%

33.3%

100%

69%

Male (n=10)

Femal (n=10)

Male (n=5)

Female (n=5)

Male -(n=10)

Female (n=10)

Male (n=2)

Female (n=2)

Male (n=2)

Female (n=2)

Male (n=10)

Female (n=10)

Male (n=5)

Female (n=5)

Total Body length (mm)

5.3–6

5–6.3

5.3–5.4

5.4–6

6.2–6.3

6.9–7.2

4.8–6

6–6.2

5.5–6.1

6–7.7

5.7–5.9

5.7–6.5

6.2–7.7

8.3–9.1

Body width

140–380

280–430

165–368

340–360

250–275

255–440

200–240

305–390

250–280

300–450

290–300

320–365

250–290

550–670

Descending branch of cordons length

335–450

345–595

380

420–505

375–385

530–590

350–370

410–470

390–420

410–530

360–400

375–590

530–400

570–760

Recurrent branch of cordons length

100–160

170–360

65–155

180–310

86–120

210–270

70–100

175–195

120–170

190–325

45–130

200–295

185–255

305–475

Deirids to anterior end

260–385

280–460

340–360

305–390

320–360

320–455

290–340

325–380

290–400

345–440

370–380

325–365

405–485

500–635

Buccal capsule length

118–130

90–170

80–120

90–115

100–140

110–165

100–115

100–145

100–130

125–150

75–120

120–135

100–130

120–170

Muscular esophagus length

400–540

570–660

440–450

510–635

270–410

670–680

350–400

545–570

360–510

490–680

405–550

415–600

440–690

460–650

Glandular esophagus length (mm)

1.1–1.5

1.3–1.6

1.3–1.4

0.8–1.3

1–1.7

1.6–2.2

1.3–2

1–1.7

1.5–1.6

1.8–1.9

1.5–1.7

1.3–1.7

1.35–1.73

1–2.1

Left spicule length

317–390

-

310–370

-

320–365

-

300–375

-

390–410

-

348–397

-

300–400

Right spicule length

160–180

-

170–180

-

180–185

-

180–190

-

190–200

-

185–205

-

120–190

Longitudinal striations length (mm)

1.6–1.9

-

1.65–1.8

-

1.7–2.1

-

1.6–1.7

-

1.8–2

-

1.95–2.4

-

1.79–2.6

Longitudinal striations extending to anterior end (mm)

3.3–3.8

-

3.2–3.5

-

3.4–4.1

-

2.8–3.3

-

3.2–4.7

-

4.2–4.8

-

5.1–5.8

Precloacal papillae

4

-

4

-

4

-

4

-

4

-

4

-

4

Postcloacal papillae

6

-

6

-

6

-

5

-

6

-

6

5

Vulva from posterior end (mm)

-

1.4–2

-

1–1.8

-

1.6–1.9

-

1.7–1.8

-

1.5–2

-

1.7–1.9

-

1.6–2

Tail length

230–325

160–205

240–310

150–195

390–450

185–210

340–345

195–200

360–430

220–355

320–375

255–270

270–340

150–210

General: White-colored nematodes. Robust, filiform body with transversally striated cuticle (Figure 2A, 2D, 2F). Sexual dimorphism present, with females larger than males. Two pseudolips small and conical (Figure 2C), with one small amphid in each (Figure 2C). Short buccal capsule striated transversely. Esophagus divided into short muscular and long glandular portions. Four distinct, unanastomosed, convoluted branch, beginning on the dorsal and ventral surface of the oral opening, extending to the posterior region of the muscular esophagus (Figure 2A, 2C). Nerve ring anterior to muscular esophagus. Excretory pore posterior to the nerve ring. Deirids bicuspid or tricuspid (Figure 2B), at level of excretory pore, located between recurrent branches of the cords (Figure 2A).

Males (n=10 from F. sparverius; n=10 from P. sulphuratus; n=10 from T. rufiventris; n=5 from T. leucomelas; n=2 from M. saturninus; n=2 from T. furcata; n=5 from M. choliba) (morphometric data of speciemens in each host are in the Table 1): Posterior region with one or two pairs of sessile papillae near the tail. Four pairs of pre-cloacal papillae and five or six post-cloacals papillae (Figure 1B). Irregular spicule (Figures 1B, 1C). Left spicule long and slender, right spicule short and thick (Figure 1B, 1C). Ventral surface of precloacal region with prominent longitudinal ridges (Figures 1B, 1C; Figures 2D, 2E). Tail bluntly rounded (Figure 1B; Figure 2D).

Females (n=10 from F. sparverius; n=10 from P. sulphuratus; n=10 from T. rufiventris; n=5 from T. leucomelas; n=2 from M. saturninus; n=2 from T. furcata; n=5 from M. choliba) (morphometric data of speciemens in each host are in the Table 1): Didelphic. Vulva located in the end of body. Tail short, conical, filiforme (Figure 2F). Eggs ellipsoid, thick shelled.

Taxonomic Summary

Hosts: T. leucomelas Vieillot, 1818, T. rufiventris Vieillot, 1818, M. saturninus Lichtenstein, 1823, P. sulphuratus Linnaeus, 1766, M. choliba Vieillot, 1817, T. furcata Scopoli, 1769, and F. sparverius Linnaeus, 1758.

Site of infection: Proventriculus, embedded in the mucosa or free.

Prevalences: 20% in T. leucomelas; 22.7% in T. rufiventris; 50% in M. saturninus; 65% in P. sulphuratus; 69% in M. choliba; 33.3% in T. furcata; and 100% in F. sparverius.

Intensity or mean intensity (range of infrapopulations): 33 specimens in Turdus leucomelas (one infected host); 10.2 (3-27) in 5 infected Turdus rufiventris; 5 specimens in Mimus saturninus (one infected host); 4.3 (1-19) in 13 infected Pitangus sulphuratus, 3.5 (2-13) in 9 infected Megascops choliba, 5 specimens in Tyto furcata (one infected host), and 37.5 (11-150) in 4infected Falco sparverius.

Localities: Zona da Mata Mineira (Juiz de Fora, Ubá and Cataguases, Minas Gerais, Brazil).

Voucher specimens: CHOB 130 (Host: T. leucomelas); CHOB 129 (Host: T. rufiventris); CHOB 132 (host: M. saturninus); CHOB 131 (host: P. sulphuratus); CHOB 054 (host: M. choliba); CHOB 133 (host: T. furcata); and CHOB 134 (host: F. sparverius).

Discussion

The morphological and morphometric data observed in the nematodes of the present study, such as the shape of the curved body in the males, striated cuticle of considerable thickness, the mouth has two conical pseudolabia close to where the cephalic attachment structures (cephalic cords) appear, are coincident with those described by previous authors (Cram, 1927; Macko et al., 1974; Zhang et al., 2004), and make it evident that the nematodes found in the present work belong to the species S. (Dispharynx) nasuta.

It can be observed measurement variation related to the host species (Table1). However, this values are within the limits of variation that have been reported for S. (D) nasuta in several descriptive studies (Zhang et al., 2004; Dewi et al., 2006; Bartmann & Amato, 2009; Oyarzún-Ruiz et al., 2016; Hernandez-Urraca et al., 2022).

Differential interference contrast (DIC) microscopy evaluations showed cuticular projections with rounded edges in the cloacal opening of males (Figure 1A): one just before the anterior edge of the cloacal opening and the other after the posterior edge (Figure 1A). These projections were not mentioned in the previous descriptions of S. (D.) nasuta available in the literature (Cram, 1927; Macko et al., 1974; Zhang et al., 2004; Dewi et al., 2006; Bartmann & Amato, 2009; Gómez-Puerta et al., 2009; Oyarzún-Ruiz et al., 2016; Hernandez-Urraca et al., 2022). However, in one of the figures published by Zhang et al. (2004), there are indications of the presence of these projections, although they were not highlighted by those authors. Findings like these emphasize the need for new taxonomic studies on some nematode species, especially those that have been referred to as having low specificity. Such studies should address morphology, light and scanning electron microscopy (SEM) and molecular biology.

In the present study, some morphological particularities are showing for the first time at SEM images, for example the two conical pseudolabia with a pair of labial papillae on each side and amphids (Figure 2C), and the two morphological types of deirids, i.e. bicuspid and tricuspid (Figure 2B). The images also revealed in detail the morphology of the descending and ascending cephalic cords (Figures 2A, 2C). These details at SEM were not provided by previous authors (Rodrigues et al., 2003; Dewi et al., 2006).

The SEM images also showed the rough area of the males, a region that assists in attachment for copulation (Figure 2E) and showed post-cloacal papillae (Figure 2D) and two papillae near the cloaca (Figures 2D, 2E). These had not been reported in any previous study with species description. In the study by Dewi et al. (2006), it was possible through SEM to observe in detail the pre and post cloacal papillae in males, similar to those observed in the nematodes collected in the present study. Scanning electron microscopy has become an important technical instrument for determining the taxonomy of this group since the species of the subgenus and genus have similarities with minimal morphoanatomical divergences.

In general, the prevalences recorded in the present study varied according to the host species, as observed by Zhang et al. (2004), Oyarzún-Ruiz et al. (2016), and in the review provided by Hernandez-Urraca et al. (2022), from several hosts in different localities.

Among the host species in which S. (D.) nasuta was found in the present study, there have been previous records of these nematodes in F. sparverius in the United States (Taft et al., 1993) and T. furcata in Italy (Santoro et al., 2012). Therefore, it can be said that the findings of the present study constitute the first record of S. (D.) nasuta in F. sparverius and T. furcata in South America and, at the same time, these findings expand the host range of this parasite species worldwide, through the first records in M. choliba, M. saturninus, T. leucomelas and T. rufiventris.

Acknowledgements

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) - Finance Code 001. Allan J.M. Severino was supported by a master’s fellowship from Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), state of Minas Gerais, Brazil. Alex J. Rocha was supported by a master’s fellowship from CAPES, Brazil. Fabiano M. Vieira was supported by a Research Fellowship from Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE), state of Pernambuco, Brazil (Process: BFP-0206-2.13/20).

• How to cite: Severino AJM, Rocha AJ, Vieira FM, Muniz-Pereira LC, Lima SS. New reports of parasitism by Synhimantus (Dispharynx) nasuta (Rudolphi, 1819) (Nematoda: Acuariidae) in wild birds in Brazil. Braz J Vet Parasitol 2023; 32(2): e002823. https://doi.org/10.1590/S1984-29612023033

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Publication Dates

• Publication in this collection
  23 June 2023
• Date of issue
  2023

History

• Received
  17 Feb 2023
• Accepted
  10 May 2023