ABSTRACT

Keywords: Aonchotheca – bats – capillarids – mammals – Tenoranema

During a helminthological survey on bats from Minas Gerais state, Brazil, we found 3.13% of bats

parasitized with capillarids. Aonchotheca pulchra (Freitas, 1934), Tenoranema rivarolai (Lent et al.,

1946), and some specimens of capillarids non-identified were registered. This is the first report of A.

pulchra in Minas Gerais state and the second report of T. rivarolai in South America.

ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043

ORIGINAL ARTICLE / ARTÍCULO ORIGINAL

NEW RECORDS OF CAPILLARIIDAE SPECIES (NEMATODA, ENOPLIDA) PARASITING BATS

(MAMMALIA, CHIROPTERA) IN BRAZIL

NUEVOS REGISTROS DE ESPECIES DE CAPILLARIIDAE (NEMATODA, ENOPLIDA)

PARASITANDO MURCIÉLAGOS (MAMMALIA, CHIROPTERA) EN BRASIL

Neotropical Helminthology

353

Neotropical Helminthology, 2019, 13(2), jul-dic:353-358.

1,2 3

Érica Munhoz de Mello & Reinaldo José da Silva

1Universidade Federal de Minas Gerais (UFMG), Belo Horizonte, Minas Gerais, Brasil.

2Centro de Controle de Zoonoses, Belo Horizonte, Minas Gerais, Brasil.

3Universidade Estadual Paulista (UNESP), Instituto de Biociências, Botucatu, São Paulo, Brasil.

Correspondence to author/ Autor para correspondência: Érica Munhoz

Laboratório de Helmintologia Molecular, Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade

Federal de Minas Gerais, Avenida Antônio Carlos, 6627, Pampulha, CEP 31270-901. Belo Horizonte, MG, Brazil. Phone:

+55(31)3409-2851, Fax: +55(31)3409-2970.

*Corresponding author: ericabiologia@gmail.com

RESUMO

Palavras-chave: Aonchotheca – capillarides – mamíferos – murciélagos – Tenoranema

Durante un muestreo de helmintos de murciélagos realizado en el estado de Minas Gerais, Brasil, se

encontró 3,13% de murciélagos parasitados por capillaridos. Se registraron Aonchotheca pulchra

(Freitas, 1934), Tenoranema rivarolai (Lent et al., 1946) y algunos especímenes de capillaridos no

identificados. Este es el primer registro de A. pulchra en el estado de Minas Gerais y el segundo registro de

T. rivarolai en América del Sur.

ÓrganooficialdelaAsociaciónPeruanadeHelmintologíaeInvertebradosAfines(APHIA)

Lima-Perú

VersiónImpresa:ISSN2218-6425VersiónElectrónica:ISSN1995-1043

Volume13,Number2(jul-dec2019)

354

helminth found were conserved in 70% ethanol and

clarified with Amann's Lactophenol solution. The

parasites were photographed with a digital camera

(AxioCam ERc 5s, Carl Zeiss) coupled to the

microscope and the morphological measurements

performed through the photos by AxioVision 4.8

software (Carl Zeiss Vision). The measurements

are presented in micrometers (μm), except when

other measures are indicated. Drawings were made

on CorelDRAW X8 software using the photos as a

background for a more accurate drawing. The

helminths were deposited in the Helminthological

Collection of the Institute of Biosciences (CHIBB),

São Paulo State University (UNESP), municipality

of Botucatu, São Paulo State, Brazil. This study

was approved by the Ethics Committee in Animal

Experimentation (CEUA/UFMG) under the

protocol number 194/2015.

Out of 319 bats necropsied, 10 (3.13%) animals

were infected with capillarids: one host was

monoinfected with Aonchotheca pulchra (Freitas,

1934), one host was monoinfected with

Tenoranema rivarolai (Lent et al., 1946), four hosts

were co-infected with A. pulchra and T. rivarolai,

and four hosts were infected with capillarids no

identified (only females).

Aonchotheca pulchra

(Figure 1; Table 1)

Diagnosis

General: Long, thin, and smooth body. Very

narrow anterior, mouth opening reduced and

simple. Long esophagus with a single and

organized row of stichocytes. Nervous ring and

excretory pore not visualized.

Female: Muscular vulva, with or without external

appendage. Vulva opening slightly posterior to the

junction of the esophagus-intestine. Tail end

rounded, anus subterminal. Smooth and

bioperculated eggs.

Male: Complex posterior extremity, with small

membranes of aspect bursate and few and discrete

rays. Spicule and caudal papillae not visualized.

Surface of spicular sheath wrinkled and without

spines. Few specimens presented an exteriorized

Capillarids are cosmopolitan vertebrate nematodes

characterized by a filiform body, with a narrow

long anterior extremity, esophagus divided into a

short and muscular anterior region, and a long and

glandular posterior region with one to three

longitudinal rows of stichocyte, elongated and

bioperculated eggs, males smaller than females and

with an eversible spicule sheath (Moravec, 2001).

About 300 species are described and due to the

great difficulty of identification, for many years,

the capillarids were classified as belonging to a

single genus - Capillaria Zeder, 1800. However,

since the 1950s some authors have already

discussed the need for a reclassification of the

Capillariidae (Mas-Coma & Esteban, 1985).

Currently 22 genera are recognized in the family

and t he gen us id ent ific ati on ke ys us e

morphological characters mainly of the male

reproductive system, making it difficult to identify

samples that contain only females (Moravec,

2001).

In South America, 5 genera and 12 species of

capillarids have been found in bats, of which 4

genera and 9 species occur in Brazil (Santos &

Gibson, 2015). Few species have a well-elucidated

biological cycle, which may involve or not

intermediate hosts (Moravec, 2001). No cycle is

known of species bats´ capillarids in South

America. This study aims to report the occurrence

of capillarids infecting bats in Minas Gerais state,

Brazil.

A total of 319 adult bats of 33 species and four

families from 79 municipalities of Minas Gerais

State, Brazil, were received dead between 2013

January and 2016 March in the Urban Bats

Laboratory of the Zoonoses Control Center of the

municipality of Belo Horizonte, Minas Gerais

State, Brazil. The animals were previously

identified according to Vizotto & Taddei (1973)

and Gregorin & Taddei (2002) and after frozen at -

20ºC. For helminthological survey, the bats were

thawed at room temperature and necropsied. All

INTRODUCTION

Neotropical Helminthology, 2019, 13(2), jul-dic

MATERIAL AND METHODS

RESULTS

Munhoz de Mello

355

Nyctinomops macrotis (Gray, 1840) (São Paulo

state) (Cardia et al., 2014); Tadarida brasiliensis

(Geoffroy, 1824) (Rio de Janeiro state) (Freitas,

1934); Paraguay - Tadarida brasiliensis Geoffroy,

1824 (Lent et al., 1946).

Sites of infection: stomach and small intestine.

Specimens deposited: CHIBB 7921, CHIBB

7931*, CHIBB 7932* (*samples containing A.

pulchra and T. rivarolai).

spicular sheath, which resembles a hook shape.

Taxonomic summary

Synonyms: Capillaria pulchra Freitas, 1934;

Pterothominx pulchra (Freitas, 1934) Moravec,

1982.

Host: Nyctinomops laticaudatus (Geoffroy, 1805).

Host´s origin: Uberaba (19°45′1″S, 47°55′57″W)

and Uberlândia (18°54′41″S, 48°15′44″W).

Distribution and hosts: Brazil - N. laticaudatus and

Figure 1. Schematic representation of Aonchotheca pulchra. A - Anterior end; B – stichocytes detail; C – Vulva and egg; D -

Posterior end female; E – Posterior end male with inverted spinal sheath; F - Posterior end male with everted spinal sheath.

Neotropical Helminthology, 2019, 13(2), jul-dic New records of Capillariidae

356

Aonchotheca rivarolai (Lent et al., 1946) Moravec,

1982.

Host: Nyctinomops laticaudatus (Geoffroy, 1805).

Ho st ´s origin: Uberlândia (18°54′41″S,

48°15′44″W).

Distribution and hosts: Paraguay – N. laticaudatus

(Lent et al., 1946).

Site of infection: small intestine.

Specimens deposited: CHIBB 7923, CHIBB

7931*, CHIBB 7932* (*samples containing A.

pulchra and T. rivarolai).

Remarks

Lent et al. (1946) described the species as C.

rivarolai, being reclassified as A. rivarolai by

Moravec (1982), based on the presence of caudal

wings and spicules well-sclerotized. Mas-Coma

and Esteban (1985) erected the genus Tenoranema,

suggesting the reclassification of some

Aonchotheca species based on the complexity of

the rays in the terminal caudal bursa, besides

spicular features. These authors also discussed the

great similarity of A. rivarolai with the specimens

type of Tenoranema, and Santos and Gibson (2015)

considered this case as a synonymy. The present

work represents the second occurrence of this

species in bats.

Remarks

Freitas (1934) described the species as C. pulchra,

being reclassified as P. pulchra by Moravec (1982),

based on the presence of caudal wings and spines in

the spicular sheath, features mentioned in the

original description. However, the spines in the

spicular sheath were not verified by Lent et al.

(1946) and Cardia et al. (2014). Subsequently, the

species was again reclassified as A. pulchra by

Cardia et al. (2014) by the absence of well-

sclerotized spicule and spines in the spicular

sheath.

Tenoranema rivarolai

(Figure 2; Table 1)

Diagnosis

General: See A. pulchra.

Female: See A. pulchra.

Male: Posterior extremity with two caudal wings,

being the anterior larger than the posterior. Tail

ventrally curved. The posterior caudal wing with a

complex ray system. A single, large and well-

sclerotized spicule. Surface of spicular sheath

smooth and without spines.

Taxonomic summary

Synonym: Capillaria rivarolai Lent et al., 1946;

Figure 2. Schematic representation of Tenoranema rivarolai. Male. A – Single spicule; B – Caudal alae and rays of bursa.

Neotropical Helminthology, 2019, 13(2), jul-dic Munhoz de Mello

Table 1. Morphometrical data of Aonchotheca pulchra, Tenoranema rivarolai, and capillarids non-identied.

Species Aonchotheca pulchra Tenoranema rivarolai Capillariidae gen. sp.

Origin Uberaba e Uberlândia Uberlândia Belo Horizonte, Patos de Minas e

Uberaba

Host Nyctinomops laticaudatus Nyctinomops laticaudatus Nyctinomops laticaudatus and

Nyctinomops macrotis

Habitat Stomach and small intestine Small intestine Stomach and small intestine

Sex ♀ (n=1)

♂ (n=6) ♀ (n=1) ♂ (n=12) ♀ (n=3)

Body (mm) 18.46 12.26 (11.7-12.61) 13.24 9.85 (8.54-11.7) 14.68 (13.61-15.24)

Width junction

esophagus

88.54 74.25 (70.39-77.05) 86.49 53.28 (43.49-77.05) 98.44 (66.14-131.89)

Width body 212.61 88.21 (84.06-92.35) 125.11 63.31 (53.45-84.06) 138.1 (107.26-159.5)

Esophagus (mm) 6.55 4.53 (4.33-4.79) 3.28 4.4 (3.15-5.07) 5.92 (5.49-6.67)

Tail

16.53

35.68

14.73 (8.83-20.63)

Length sheath

3.85 (n=1)

Spicule

263.39 (209.20-

330.50)

Alae tail

90.63 (86.80-98.94)

Vulva-juntion

esophagus

76.15

20 (n=1)

Egg lenght

48 (44.97-

50.07) (n=10)

48.77 (45.01-

52.63) (n=10)

45.56 (43.99-48.79) (n=10)

Egg width 29.76 (28.4-

31.81) (n=10) -29.25 (28.22-

31.28) (n=10) - 29.75 (28-31.59) (n=10)

Neotropical Helminthology, 2019, 13(2), jul-dic New records of Capillariidae

357

358

Capillariidae gen. sp.

(Table 1)

Diagnosis

General: See A. pulchra.

Taxonomic summary

Hosts: Molossus rufus (Geoffroy, 1805),

Nyctinomops laticaudatus (Geoffroy, 1805) and

Nyctinomops macrotis (Gray, 1840).

Host´s origin: Belo Horizonte (19°48′57″S,

43°57′15″W), Governador Valadares (18°51′2″S,

41°56′53″W), Patos de Minas (18°34′46″S,

46°3 1′6 ″ W), and Ube raba (19° 45′1 ″S,

47°55′57″W).

Site of infection: stomach and small intestine.

Specimens deposited: CHIBB 7893, CHIBB 7926,

CHIBB 7927.

Remarks

The spe cim en s we re no t id en t if ied to

generic/species level because conspecific males

were absent. Besides, in samples co-infected with

A. pulchra and T. rivarolai, the females of both

species were indistinguishable morphometrically.

The species A. pulchra is more found in the host's

stomach than in the small intestine (Freitas, 1934;

Lent et al., 1946; Vicente et al., 1997; Cardia et al.,

2014). However, in the present study, specimens of

A. pulchra were found in the stomach only of the

host that presented monoinfection with the species.

The species A. pulchra and T. rivarolai, when

associated, were all found only in the small

intestine, especially in the jejunum. In the hosts that

were co-parasitized by both species, 13 females

could not be identified, since the females of A.

pulchra and T. rivarolai are morphometrically

indistinguishable.

DISCUSSION

Cardia, DFF, Hoppe, EGL, Tebaldi, JH, Fornazari,

F, Menozzi, BD, Langoni, H, Nascimento,

AA & Bresciani, KDS. 2014. Redescription

and taxonomical considerations about

Aonchotheca (Aonchotheca) pulchra n.

comb. (Enoplida: Trichuridae), a nematode

of Nyctinomops spp. Brazilian Journal of

Veterinary Parasitology, vol. 23, pp. 399-

402.

Freitas, JFT. 1934. Sobre as especies do gênero

Capillaria Zeder, 1800, parasitas de

morcegos. Memórias do Instituto Oswaldo

Cruz, vol. 28, pp. 239-261.

Gregorin, R & Taddei, V. 2002. Chave artificial

para a identificação de molossídeos

brasileiros (Mammalia, Chiroptera).

Mastozoología Neotropical, Journal of

Neotropical Mammalogy, vol. 9, pp. 13-32.

Lent, H, Freitas, JFT & Proença, MC. 1946.

Algunos nematodos de murcielagos

coleccionados en el Paraguay. Revista

Brasileira de Biologia, vol. 6, pp. 485-497.

Santos, CP & Gibson, DI. 2015. Checklist of the

helminth parasites of South American bats.

Zootaxa, vol. 3937, pp. 471-499.

Mas-Coma, S & Esteban, JG. 1985. Tenoranema

alcoveri g. n., sp. n. (Trichuridae:

Capillariinae), a nematode parasitizing

Eliomys quercinus (Rodentia: Gliridae).

Folia Parasitologica (Praha), vol. 32, pp. 35-

42.

Moravec, F. 1982. Proposal of a new systematic

arrangement of nematodes of the family

Capillariidae. Folia Parasitologica, vol. 29,

pp. 119-132.

Moravec, F. 2001. Trichinelloid nematodes

parasitic in coldblooded vertebrates.

Academia, Prague.

Vizotto, LD & Taddei, VA. 1973. Chave para

determinação de quirópteros brasileiros.

Boletim de Ciências Faculdade de Filosofia,

Ciências e Letras, vol. 1, pp. 1-72.

BIBLIOGRAPHIC REFERENCES

Received February 27, 2019.

Accepted December 31, 2019.

Neotropical Helminthology, 2019, 13(2), jul-dic Munhoz de Mello