First record of Dipetalonema graciliformis (Filarioidea: Onchocercidae) in Saguinus bicolor (Spix, 1823) in Brazil

Lignon, J.S.; Pinto, D.M.; Martins, N.S.; Santos, C.C.; Pappen, F.G.; Tonin, A.A.; Tochetto, C.; Monteiro, S.G.

doi:10.1590/1678-4162-13011

RESUMO

Saguinus bicolor é uma espécie de primata brasileiro, a qual se encontra criticamente em perigo de extinção. Os primatas são comumente parasitados por nematódeos filarídeos, transmitidos por insetos hematófagos, que parasitam vários tecidos e cavidades fora do trato gastrointestinal do hospedeiro. Portanto, o impacto dos helmintos parasitos em seus hospedeiros é um aspecto que não deve ser negligenciado como parte vital da conservação das espécies primatas. Com o presente estudo, objetivou-se descrever, pela primeira vez, o parasitismo por Dipetalonema graciliformis (Filarioidea: Onchocercidae) em Saguinus bicolor (Spix, 1823) no Brasil. Foram fornecidos dados morfológicos detalhados de espécimes fêmeas e, assim, expande-se o número de hospedeiros conhecidos parasitados por essa espécie de filarídeo no país.

Palavras-chave:
animais silvestres; filarias; nematódeo; primatas; sauim-de-coleira

Saguinus bicolor, popularly known as "sagui-de-duas-cores" or "sauim-de-coleira", is a species of Brazilian primate, with exclusive natural occurrence in the state of Amazonas (Gordo et al., 2019GORDO, M.; JERUSALINSKY, L.; MITTERMEIER, R.A. et al. Saguinus bicolor. The IUCN Red List of Threatened Species. 2019. Available in: http://dx.doi.org/10.2305/IUCN.UK.2019-3.RLTS.T40644A17931870.en. Accessed in: 12 fev. 2023.
http://dx.doi.org/10.2305/IUCN.UK.2019-3... ). The species is critically endangered (Gordo et al., 2019; Lista…, 2022) due to habitat loss and fragmentation, roadkill, in addition to hunting and illegal trade, since its area of occurrence is restricted and has been occupied by the disorderly growth of the metropolitan region of the Amazonian capital (Reis et al., 2011REIS, N.R.; PERACCHI, A.L.; PEDRO, W.A. et al. Mamíferos do Brasil. 2 ed. Brazil: Londrina: Nelio Reis, 2011. 439p.; Bezerra-Santos et al., 2021).

Neotropical primates are commonly parasitized by filarial nematodes of the genera Dipetalonema and Mansonella (Bain et al., 2015BAIN, O.; MUTAFCHIEV, Y.; JUNKER, K. et al. Review of the genus Mansonella Faust, 1929 sensu lato (Nematoda: Onchocercidae), with descriptions of a new subgenus and a new subspecies. Zootaxa, v.3918, p.151-193, 2015.; Laidoudi et al., 2020). Both differ morphologically, mainly by the presence of evident transverse striations and a pair of lateral conical processes near the tip of the tail in both sexes of Dipetalonema (Vicente et al., 1997VICENTE, J.J.; RODRIGUES, H.O.; GOMES, D.C. et al. Nematóides do Brasil. Parte 5: Nematóides de mamíferos. Rev. Bras. Zool., v.14, p.1-452, 1997.). These parasites are transmitted by hematophagous insects (especially keratopogonid and simuliid dipterans), live in various tissues and cavities outside the gastrointestinal tract of the host (Strait et al., 2012STRAIT, K.; ELSE, J.G.; EBERHARD, M.L. Nonhuman primates in biomedical research. 2.ed. Elsevier: Academic Press, 2012.), and may induce pathologies that involve pleuritis, fibrinopurulent peritonitis and fibrinous adhesion (Baker, 2018BAKER, D.G. Parasitic diseases. In: ROBERT, M.; LYNN, W.; SUZETTE, T.; KEITH, M.; JAMES, F. The common marmoset in captivity and biomedical research. Cambridge, Massachusetts, USA: Academic Press, 2018. p.289-303.). Thus, understanding the impact of parasitic helminths on their hosts is an aspect that should not be neglected as a vital part of the conservation of primate species.

Studies on primate parasitic nematodes are scarce, therefore, the present study aims to describe, for the first time, the parasitism by Dipetalonema graciliformis (Filarioidea: Onchocercidae) in Saguinus bicolor (Spix, 1823) in Brazil.

For this purpose, two specimens of adult female filarids were received at the Laboratory of Veterinary Parasitology of the University of Santa Maria for taxonomic identification. The parasites were found during the necropsies of two adult female primates of the species Saguinus bicolor, carried out by the veterinary team of a zoo in Manaus, Amazonas. The animals were free-ranging and were found lifeless by the Wild Animal Screening Center team, in forest fragments near the zoo.

The nematodes, found under the serous membrane of the intestine and liver, were fixed in 70º alcohol, clarified in Amann's Lactophenol, mounted on permanent slides with Canada balsam under slide and coverslip (Amato and Amato, 2010AMATO, J.F.R.; AMATO, S.B. Técnicas gerais para coleta e preparação de helmintos endoparasitos de aves. In: VON MATTER, S.; STRAUBE, F.C.; ACCORDI, I.A.; PIACENTINI, V.Q.; CÂNDIDO-JR, J.F. Ornitologia e conservação: ciência aplicada, técnicas de pesquisa e levantamento. Rio de Janeiro: Technical Books, 2010, p.369-393.) and taxonomically identified at the level of species according to the literature described by Freitas (1964FREITAS, J.F.T. Achegas helmintológicas. Rev. Ciênc. Biol., v.2, p.3-40, 1964.), Petit et al. (1985PETIT, G.; BAIN, O.; ROUSSILHON, C. Deux nouvelles filaires chez um singe. Saimiri Sciureus, au Guyana. Annales de Parasitologie Humaine et Comparee, v.60, p.65-81, 1985.), Bain et al. (1986BAIN, O.; PETIT. G.; ROSALES-LOESENER, L. Filaires de Singes sud-ame´ricains. Bull. Mus. Natl. Hist. Nat., v.8, p.513-542, 1986.) and Laidoudi et al. (2021LAIDOUDI, Y.; LIA, R.P.; MENDOZA-ROLDAN, J.A. et al. Dipetalonema graciliformis (Freitas, 1964) from the red-handed tamarins (Saguinus midas, Linnaeus, 1758) in French Guiana. Parasitology, v.148, p.1353-1359, 2021.). The specimens were identified and photographed with the aid of an Olympus optical microscope (CX22 series) and were deposited in the parasitological collection of the Laboratory of Veterinary Parasitology of the University of Santa Maria. The specimens were deposited in the parasitological collection of the Laboratory of Veterinary Parasitology at the Federal University of Santa Maria.

The two filarids were identified as Dipetalonema graciliformis (Fig. 1), which is the first record of the species in S. bicolor in Brazil. According to Côrrea et al. (2016), D. graciliformis had only been described in Saguinus midas, Saguinus mystax and Saguinus niger in the country, in the localities of Pará, Amazonas and Pará, respectively. The other species of Dipetalonema described in wild primates in Brazil are described in Table 1. In addition to D. graciliformis, D. caudispina and D. gracile are reported in the country, and these include records in S. bicolor.

The mean value, in μm (unless specified), of the measurements of D. graciliformis females found in this study are listed below: Body length (mm): 250 (240-260); Body width: 322.5 (310-335); Buccal capsule length: 10 (9-11); Nerve-ring from anterior extremity: 220.5 (219-222); Oesophagus length: 3400.5 (3315-3486); Muscular portion length: 408 (397-419); Glandular portion length: 2992.5 (2918-3067); Tail length: 249.5 (246-253); Caudal lappets length: 10.5 (10-11); Distance from the vulva to the anterior extremity: 766 (764-768) and vagina length: 205.5 (204-207). Comparative measurements of females of the other Dipetalonema species described in wild primates are detailed in Table 2.

The body of the filarids found is whitish with thin transverse cuticular striations. The anterior end is rounded, with a small buccal capsule, and the cuticle of the head in the cephalic region has a smooth quadrangular shape (Fig. 1 - A). A small oral opening with four labial papillae is arranged in a laterally elongated rectangle and four cephalic papillae are located around the oral opening. The oesophagus is divided into an anterior muscular part (short) and a posterior glandular part (long) and has a nerve ring located halfway along the muscular oesophagus, with an excretory pore visible behind the nerve ring. The vulva is at the level of the glandular oesophagus and the vagina has a sinuous duct (Fig. 1 - B). The ovaries are in the middle of the body. The posterior end is tapered, with the presence of the anal opening in this region (Fig. 1 - C). The females had an extremity with three well-developed petaloid appendages in a triangular shape (Fig. 1 - D).

Morphologically, D. graciliformis is similar to D. gracile, although females of D. graciliformis are longer and have a shorter oesophagus and tail (Bain et al., 1986BAIN, O.; PETIT. G.; ROSALES-LOESENER, L. Filaires de Singes sud-ame´ricains. Bull. Mus. Natl. Hist. Nat., v.8, p.513-542, 1986.). In size, D. graciliformis is similar to D. yatesi, D. freitasi, D. caudispina and D. digitatum. However, D. yatesi and D. caudispina have a simple vagina and a longer tail; D. freitasi and D. digitatum have a shorter oesophagus (Freitas, 1943FREITAS, J.F.T. Estudios sobre nematodeos filarideos Dipetalonema caudispina (Molin, 1858). Mem.. Inst Oswaldo Cruz, v.38, p.361-372, 1943.; Bain et al., 1986; Notarnicola et al., 2007NOTARNICOLA, J.; JIMÉNEZ, F.A.; GARDNER, S.L. A new species of Dipetalonema (Filarioidea: Onchocercidae) from Ateles chamek from the beni of Bolivia. J. Parasitol., v.93, p.661-667, 2007.).

In the current study, we provide detailed morphological data of female specimens of D. graciliformis isolated from S. bicolor in the Brazilian Amazon. And so, the number of known hosts parasitized by this species of filarid in the country expands.

Figure 1
Female Dipetalonema graciliformis. (A) Head end with small oral capsule (arrow). (B) Lateral view of the anterior region showing vulvar opening (arrow) and vagina with sinuous duct (arrowhead). (C) Posterior extremity with detail in the anal opening (arrow). (D) Posterior extremity with lapel details (arrows).

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Table 1
Dipetalonema species described in wild primates in Brazil

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Table 2
Measurements in μm, unless specified, of Dipetalonema species (adult females) described in wild primates worldwide

REFERENCES

AMATO, J.F.R.; AMATO, S.B. Técnicas gerais para coleta e preparação de helmintos endoparasitos de aves. In: VON MATTER, S.; STRAUBE, F.C.; ACCORDI, I.A.; PIACENTINI, V.Q.; CÂNDIDO-JR, J.F. Ornitologia e conservação: ciência aplicada, técnicas de pesquisa e levantamento. Rio de Janeiro: Technical Books, 2010, p.369-393.
BAIN, O.; MUTAFCHIEV, Y.; JUNKER, K. et al. Review of the genus Mansonella Faust, 1929 sensu lato (Nematoda: Onchocercidae), with descriptions of a new subgenus and a new subspecies. Zootaxa, v.3918, p.151-193, 2015.
BAIN, O.; PETIT. G.; ROSALES-LOESENER, L. Filaires de Singes sud-ame´ricains. Bull. Mus. Natl. Hist. Nat., v.8, p.513-542, 1986.
BAKER, D.G. Parasitic diseases. In: ROBERT, M.; LYNN, W.; SUZETTE, T.; KEITH, M.; JAMES, F. The common marmoset in captivity and biomedical research. Cambridge, Massachusetts, USA: Academic Press, 2018. p.289-303.
BEZERRA-SANTOS, M.A.; MENDOZA-ROLDAN, J.A.; THOMPSON, R.C.A. et al. Illegal wildlife trade: a gateway to zoonotic infectious diseases. Trends Parasitol., v.37, p.181-184, 2021.
CORREA, P.; BUENO, C.; SOARES, R. et al. Checklist of helminth parasites of wild primates from Brazil. Rev. Mex. Biodivers., v.87, p.908-918, 2016.
FREITAS, J.F.T. Achegas helmintológicas. Rev. Ciênc. Biol., v.2, p.3-40, 1964.
FREITAS, J.F.T. Estudios sobre nematodeos filarideos Dipetalonema caudispina (Molin, 1858). Mem.. Inst Oswaldo Cruz, v.38, p.361-372, 1943.
GORDO, M.; JERUSALINSKY, L.; MITTERMEIER, R.A. et al. Saguinus bicolor. The IUCN Red List of Threatened Species. 2019. Available in: http://dx.doi.org/10.2305/IUCN.UK.2019-3.RLTS.T40644A17931870.en Accessed in: 12 fev. 2023.
» http://dx.doi.org/10.2305/IUCN.UK.2019-3.RLTS.T40644A17931870.en
LAIDOUDI, Y.; LIA, R.P.; MENDOZA-ROLDAN, J.A. et al. Dipetalonema graciliformis (Freitas, 1964) from the red-handed tamarins (Saguinus midas, Linnaeus, 1758) in French Guiana. Parasitology, v.148, p.1353-1359, 2021.
LAIDOUDI, Y.; MEDKOUR, H.; LEVASSEUR, A. et al. New molecular data on filaria and its Wolbachia from red howler monkeys (Alouatta macconnelli) in French Guiana - a preliminary study. Pathogens, v.9, p.626, 1964.
LISTA de Primatas ameaçados de extinção. ICMBIO, 2022. Available in: https://www.icmbio.gov.br/cpb/index.php/primatas-brasileiros Accessed in: 27 abr. 2023.
» https://www.icmbio.gov.br/cpb/index.php/primatas-brasileiros
NOTARNICOLA, J.; JIMÉNEZ, F.A.; GARDNER, S.L. A new species of Dipetalonema (Filarioidea: Onchocercidae) from Ateles chamek from the beni of Bolivia. J. Parasitol., v.93, p.661-667, 2007.
PETIT, G.; BAIN, O.; ROUSSILHON, C. Deux nouvelles filaires chez um singe. Saimiri Sciureus, au Guyana. Annales de Parasitologie Humaine et Comparee, v.60, p.65-81, 1985.
PINTO, R.M.; KNOFF, M.; GOMES, D.C. et al. Nematodes from mammals in Brazil: an updating. Neotrop. Helminthol., v.5, p.139-183, 2011.
REIS, N.R.; PERACCHI, A.L.; PEDRO, W.A. et al. Mamíferos do Brasil. 2 ed. Brazil: Londrina: Nelio Reis, 2011. 439p.
STRAIT, K.; ELSE, J.G.; EBERHARD, M.L. Nonhuman primates in biomedical research. 2.ed. Elsevier: Academic Press, 2012.
VICENTE, J.J.; RODRIGUES, H.O.; GOMES, D.C. et al. Nematóides do Brasil. Parte 5: Nematóides de mamíferos. Rev. Bras. Zool., v.14, p.1-452, 1997.

Publication Dates

Publication in this collection
09 Feb 2024
Date of issue
Jan-Feb 2024

History

Received
01 Sept 2023
Accepted
27 July 2023

This is an open-access article distributed under the terms of the Creative Commons Attribution License

[1] AMATO, J.F.R.; AMATO, S.B. Técnicas gerais para coleta e preparação de helmintos endoparasitos de aves. In: VON MATTER, S.; STRAUBE, F.C.; ACCORDI, I.A.; PIACENTINI, V.Q.; CÂNDIDO-JR, J.F. Ornitologia e conservação: ciência aplicada, técnicas de pesquisa e levantamento. Rio de Janeiro: Technical Books, 2010, p.369-393.

[2] BAIN, O.; MUTAFCHIEV, Y.; JUNKER, K. et al. Review of the genus Mansonella Faust, 1929 sensu lato (Nematoda: Onchocercidae), with descriptions of a new subgenus and a new subspecies. Zootaxa, v.3918, p.151-193, 2015.

[3] BAIN, O.; PETIT. G.; ROSALES-LOESENER, L. Filaires de Singes sud-ame´ricains. Bull. Mus. Natl. Hist. Nat., v.8, p.513-542, 1986.

[4] BAKER, D.G. Parasitic diseases. In: ROBERT, M.; LYNN, W.; SUZETTE, T.; KEITH, M.; JAMES, F. The common marmoset in captivity and biomedical research. Cambridge, Massachusetts, USA: Academic Press, 2018. p.289-303.

[5] BEZERRA-SANTOS, M.A.; MENDOZA-ROLDAN, J.A.; THOMPSON, R.C.A. et al. Illegal wildlife trade: a gateway to zoonotic infectious diseases. Trends Parasitol., v.37, p.181-184, 2021.

[6] CORREA, P.; BUENO, C.; SOARES, R. et al. Checklist of helminth parasites of wild primates from Brazil. Rev. Mex. Biodivers., v.87, p.908-918, 2016.

[7] FREITAS, J.F.T. Achegas helmintológicas. Rev. Ciênc. Biol., v.2, p.3-40, 1964.

[8] FREITAS, J.F.T. Estudios sobre nematodeos filarideos Dipetalonema caudispina (Molin, 1858). Mem.. Inst Oswaldo Cruz, v.38, p.361-372, 1943.

[9] GORDO, M.; JERUSALINSKY, L.; MITTERMEIER, R.A. et al. Saguinus bicolor. The IUCN Red List of Threatened Species. 2019. Available in: http://dx.doi.org/10.2305/IUCN.UK.2019-3.RLTS.T40644A17931870.en Accessed in: 12 fev. 2023.
» http://dx.doi.org/10.2305/IUCN.UK.2019-3.RLTS.T40644A17931870.en

[10] LAIDOUDI, Y.; LIA, R.P.; MENDOZA-ROLDAN, J.A. et al. Dipetalonema graciliformis (Freitas, 1964) from the red-handed tamarins (Saguinus midas, Linnaeus, 1758) in French Guiana. Parasitology, v.148, p.1353-1359, 2021.

[11] LAIDOUDI, Y.; MEDKOUR, H.; LEVASSEUR, A. et al. New molecular data on filaria and its Wolbachia from red howler monkeys (Alouatta macconnelli) in French Guiana - a preliminary study. Pathogens, v.9, p.626, 1964.

[12] LISTA de Primatas ameaçados de extinção. ICMBIO, 2022. Available in: https://www.icmbio.gov.br/cpb/index.php/primatas-brasileiros Accessed in: 27 abr. 2023.
» https://www.icmbio.gov.br/cpb/index.php/primatas-brasileiros

[13] NOTARNICOLA, J.; JIMÉNEZ, F.A.; GARDNER, S.L. A new species of Dipetalonema (Filarioidea: Onchocercidae) from Ateles chamek from the beni of Bolivia. J. Parasitol., v.93, p.661-667, 2007.

[14] PETIT, G.; BAIN, O.; ROUSSILHON, C. Deux nouvelles filaires chez um singe. Saimiri Sciureus, au Guyana. Annales de Parasitologie Humaine et Comparee, v.60, p.65-81, 1985.

[15] PINTO, R.M.; KNOFF, M.; GOMES, D.C. et al. Nematodes from mammals in Brazil: an updating. Neotrop. Helminthol., v.5, p.139-183, 2011.

[16] REIS, N.R.; PERACCHI, A.L.; PEDRO, W.A. et al. Mamíferos do Brasil. 2 ed. Brazil: Londrina: Nelio Reis, 2011. 439p.

[17] STRAIT, K.; ELSE, J.G.; EBERHARD, M.L. Nonhuman primates in biomedical research. 2.ed. Elsevier: Academic Press, 2012.

[18] VICENTE, J.J.; RODRIGUES, H.O.; GOMES, D.C. et al. Nematóides do Brasil. Parte 5: Nematóides de mamíferos. Rev. Bras. Zool., v.14, p.1-452, 1997.

Dipetalonema species	Primate species	Geographic location	Reference
Dipetalonema caudispina	Alouatta guariba Ateles paniscus Brachyteles arachnoides Callicebus personatus Cebus apella Cebus capucinus Leontopithecus rosalia Leontopithecus chrysopygus Saguinus bicolor Saimiri sciureus	Amazonas, São Paulo Pará Rio de Janeiro, São Paulo Unspecified location Mato Grosso, Minas Gerais São Paulo Pará Unspecified location Unspecified location Amazonas
Dipetalonema graciliformis	Saguinus midas Saguinus mystax Saguinus niger	Pará Amazonas Pará	Pinto et al. (2011); Corrêa et al. (2016)
Dipetalonema gracile	Ateles paniscus Brachyteles arachnoides Callithrix jacchus Cebus apella Cebus capucinus Cebus cay Cebus libidinosus Lagothrix lagotricha Leontopithecus chrysopygus Leontopithecus rosalia Saginus bicolor Saimiris ciureus	Amazonas, Minas Gerais, Goiás, Pará, São Paulo Unspecified location Pará Mato Grosso do Sul, Pará Amazonas, Goiás, Mato Grosso, Mato Grosso do Sul, Minas Gerais, Pará, São Paulo Amazonas, Pará, Goiás, Minas Gerais, São Paulo Mato Grosso Amazonas, Goiás, Minas Gerais, Pará, São Paulo Unspecified location Unspecified location Unspecified location Amazonas, Goiás, Minas Gerais, Pará, Rio de Janeiro, São Paulo

Features	D. graciliformis (Freitas, 1964FREITAS, J.F.T. Achegas helmintológicas. Rev. Ciênc. Biol., v.2, p.3-40, 1964.)	D. yatesi (Notarnicola, Jimenez and Gardner, 2007NOTARNICOLA, J.; JIMÉNEZ, F.A.; GARDNER, S.L. A new species of Dipetalonema (Filarioidea: Onchocercidae) from Ateles chamek from the beni of Bolivia. J. Parasitol., v.93, p.661-667, 2007.)	D. robini (Petit Bain, and Roussilhon, 1985PETIT, G.; BAIN, O.; ROUSSILHON, C. Deux nouvelles filaires chez um singe. Saimiri Sciureus, au Guyana. Annales de Parasitologie Humaine et Comparee, v.60, p.65-81, 1985.)	D. freitasi (Bain Diagne and Muller, 1987)	D. caudispina (Molin,1858)	D. gracile (Rudolphi, 1819)	D. digitatum (Webber and Hawking, 1955)	D. obtusa (Esslinger, 1966)
Body length (mm)	255-330	239.6-254.2	130-152	210-230	295	167-210	170-260	23-46
Body width	340-350	339-575	250-430	450-460	220-250	400-450	380-550	57-77
Buccal capsule length	12	5-9	-	10-11	12	10	-	-
Buccal capsule width	-	17-21	-	-	-	-	-	35-43
Nerve-ring from anterior extremity	225	226-300	170-225	230	200	155	160	118-179
Oesophagus length	3360-3700	3175-4787	3920-4700	2000-2040	2720	3950-5500	1100-1300	417-882
Muscular portion length	430-550	350-750	700-1050	425-440	800	720	-	-
Glandular portion length	2930-3150	-	-	1575-1600	1980	-	-	-
Tail length	250-300	635-810	660	510-590	800	640-850	330-460	91-145
Caudal lappets length	12	10	8-11	9-10	10-12	7-12	-	-
Lateral lappets from tip of tail	8-14	-	-	6	8-10	5	-	-
Vulva from anterior extremity	760-850	588-1636	830-980	650-670	400-420	1150-1600	950-1200	324-510
Vagina length	280	269	200	380-390	350-460	300	-	-

Brasil