235

Neotrop. Helminthol., 8(2), 2014

2014 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)

ISSN: 2218-6425 impreso / ISSN: 1995-1043 on line

ORIGINAL ARTICLE / ARTÍCULO ORIGINAL

A NEW SPECIES OF HASSALSTRONGYLUS (NEMATODA: HELIGMONELIDAE) FROM

EURYORYZOMYS RUSSATUS (RODENTIA: SIGMODONTINAE) IN THE ATLANTIC FOREST,

BRAZIL

UNA NUEVA ESPECIE DE HASSALSTRONGYLUS (NEMATODA: HELIGMONELIDAE) DE

EURYORYZOMYS RUSSATUS (RODENTIA: SIGMODONTINAE) EN LA MATA ATLÁNTICA,

BRASIL

Mariane Almeida Rodrigues Costa¹, Arnaldo Maldonado Júnior¹, Márcio Neves Bóia¹,Camila dos Santos Lucio¹ & Raquel de

Oliveira Simões

Abstract

Keywords: nematode - rodent - Rio de Janeiro - species.

Suggested citation Costa, MAR, Maldonado Jr, A, Bóia, MN, Lucio, CS & Simões, RO. 2014. a new species of Hassalstrongylus

(Nematoda: Heligmonelidae) from Euryoryzomys russatus (Rodentia: Sigmodontinae) in the Atlantic forest, Brazil. Neotropical

Helminthology, vol. 8, n°2, jul-dec, pp. 235-242.

¹Laboratório de Biologia e Parasitologia de Mamíferos Silvestres de Reservatórios. Instituto Oswaldo Cruz. Rio de janeiro – Brazil.

¹ Instituto Oswaldo Cruz, Av. Brasil, 4365, 21040 – 360 Rio de Janeiro, RJ, Brasil. Tel: 55 -21-2562-1644. *Correspondence to

author: raquel83vet@gmail.com

Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) research fellow

Hassalstrongylus luquei n. sp. is described from the small intestine of Euryoryzomys russatus

(Rodentia: Sigmodontinae) collected in the Atlantic Forest (Rio de Janeiro State, Angra dos Reis,

Brazil). The genus Hassalstrongylus includes 16 Neotropical species. The main characters of new

species are subsymmetrical caudal bursa with a type 2-2-1, rays 8 branching at midlength of dorsal

trunk, right lateral trunk larger than the left and the longest spicules in the genus. Only three

species of Hassalstrongylus have the rays 8 not emerging at the base trunk, these are: H. mazzai;

H. aduncus; and H. echalieri. However, the present species is distinguished from H. mazzai by

having the dorsal rays divided at fourth part of the trunk, H. bocqueti by having rays 5 bifurcating

at third part of trunk and H. echalieri by having a pattern of 2-2-1.

Resumen

Palabras clave: nematodo - especie - roedor - Rio de Janeiro.

Hassalstrongylus luquei n. sp. es descrito en el intestino delgado de Euryoryzomys russatus

(Rodentia: Sigmodontinae) colectado en la Mata Atlantica (Estado de Río de Janeiro, Angra dos

Reis, Brasil). El género Hassalstrongylus Durette-Desset de 1971 incluye 16 especies

neotropicales. Las características más importantes de la nueva especie son: la bursa caudal

subsimétrica con un tipo 2-2-1, rayos 8 ramificados en la mitad de la longitud del tronco dorsal, el

tronco lateral derecho es mayor que el izquierdo y las espículas son las más grandes del género.

Sólo tres especies de Hassalstrongylus tienen los rayos 8 no emergentes en la base del tronco,

éstas son: H. mazzai, H. aduncus y H. echalieri. Sin embargo, la presente especie se distingue de

H. mazzai por presentar los radios dorsales divididos en la cuarta parte del tronco, H. bocqueti por

tener los rayos 5 bifurcados en tercera parte del tronco y H. echalieri por tener un patrón de 2-2-1.

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Costa et al.

A new species of Hassalstrongylus

Animal Use (Permit Number: L – 0049/08). The

rodents were killed using a CO chamber and

necropsied.

The nematodes were collected from the small

intestine, washed twice in a 0.85% NaCl

solution and fixed in hot A.F.A. (2% acetic acid,

3% formaldehyde, and 95% ethanol) and further

clarified in lactophenol. Drawings were made

with the aid of a camera lucida attached to a

Zeiss standard microscope. Measurements are

given in micrometers (unless otherwise stated)

for Holotype specimen, followed by range for

paratypes in brackets and mean in parenthesis.

The synlophe was studied in 1 male from

following Durette-Desset (1985) and Durette-

Desset & Digiani (2005), and the terminology

related to the caudal bursa follows Durette-

Desset & Chabaud (1981). Females were not

found. The number of dorsal and ventral ridges

was counted with respect to the axis(es) of

orientation.

General: Small nematodes tightly coiled in

small intestine. Excretory pore below of

esophagus (Fig.1). Females were not found in

the small intestine in specimens of E. russatus.

Synlophe: Males with cuticle bearing

longitudinal, uninterrupted ridges appearing

posterior to cephalic vesicle and ending just

anterior to caudal bursa. Number of ridges: 22

(12 dorsal, 10 ventral) at level of esophagus-

intestinal junctions (Fig.2); 24 (13 dorsal, 11

ventral) at the midbody (Fig. 3); 19 (9 dorsal, 10

ventral) at the posterior end (Fig. 4). Double axis

of orientation of ridges directed from right

ventral quadrant to left dorsal quadrant. Right

axis inclined 62º to sagittal axis and left axis at

73º.

Male (holotype and 7 paratypes, except

otherwise stated): 4.07 [2.74 - 4.46 (3.35)] mm

long and 145 [127-190 (160)] wide at mid-body;

Cephalic vesicle 59 [36-59 (47)] long and 22

[18-31 (25)] wide (n=6). Nerve ring and

excretory pore situated at 81 [81-172(113)], 304

The genus Hassalstrongylus Durette-

D e s s e t , 1 9 7 1 ( T r i c h o s t r o n g y l i d a e :

Heligmosomoidea) includes 16 Neotropical

species, of which 13 are parasites of rodents

Sigmodontinae and 3 of Murinae rodents. This

genus is broadly distributed across the

Neotropical region (Digiani & Durette - Desset,

2007).

The rice rat, Euryoryzomys russatus (Wagner,

1848) (syn. Oryzomys russatus) (Cricetidae:

Sigmodontinae), is frequently found in

fragmented and continuous areas in the Atlantic

Forest in Brazil (Naxara et al., 2009; Umetsu &

Pardini, 2007; Passamani & Fernandez, 2011).

These rodents are terrestrial; feed on seeds,

fruits, and insects (Emmons & Feer, 1997).

The vegetation of Ilha Grande is a marine island

near the coast belonging Angra dos Reis. It`s

vegetation is characterized by a diverse set of

backgrounds: Rain Forest (montane and

lowland), Restinga, mangrove and rocky

outcrops. This variety of biological

environments attaches great importance to the

Island and ranks as an ecological sanctuary and

Biosphere Reserve of the Atlantic Rainforest

(Ribeiro et al., 2009).

Here we describe a new species of

Has s a lst ro n g ylu s (Trichostrongylina:

Nippostrongylinae), found parasitizing E.

russatus in the Atlantic Forest Coast, in Ilha

Grande, Angra dos Reis municipally of Rio de

Janeiro state.

Seven specimens of E. russatus were trapped in

the Atlantic Forest Coast, Angra dos Reis

municipally of Rio de Janeiro state, Brazil

(23°09'07.50'' S; 44°13'44.20'' W), using a

Sherman® trap (Model XLK; 7.6 x 9.5 x 30.5

cm). Collection permits for rodents were issued

by the State Environmental Institute (INEA,

Permit Number 019/2011) and by Oswaldo Cruz

Foundation (FIOCRUZ) Ethical Committee on

INTRODUCTION

MATERIAL AND METHODS

RESULTS

237

Neotrop. Helminthol., 8(2), 2014

Figures 1-5. Hassalstrongylus luquei n. sp. (1) Anterior extremity, lateral view. (2) Transverse section of body, at anterior

extremity. (3) Transverse section of body, at mid-body. Axes of orientation represented. Abbreviations: r: right side; v: ventral

side; SA: sagittal axis; FA: frontal axis passing through the lateral fields. (4) Transverse section of body, just anterior to caudal

bursa. (5) Caudal bursa, ventral view. Scale bar: 100 µm.

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Costa et al.

A new species of Hassalstrongylus

Taxonomic summary

Type host: Euryoryzomys russatus (Rodentia:

Sigmodontinae).

Site of infection: Small intestine.

Type locality: Ilha Grande (23°09'07.50'' S;

44°13'44.20'' W) municipality in Angra dos

Reis, Rio de Janeiro state, Brazil.

Prevalence and intensity of infection: 43% (3

rodents infected/ 7 rodents collected), 1-5 (3

mean intensity).

Specimens deposited: Holotype male (CHIOC

no. 35928a) and paratypes (CHIOC no. 35928b

- c) were deposited in the Helminthological

Collection of the Institute Oswaldo Cruz, Rio de

Janeiro, Brazil.

Etymology: New species is named in honor of

Dr. José Luis Fernando Luque Alejos for his

contribution to helminthology.

[304-681 (471)] from apex (n=5), respectively.

Oesophagus 345 [345-745 (480)] long (n=4).

Subssymetric caudal bursa, pattern of type 2-2-

1. Right lobe slightly more developed than left

lobe. Rays 2 and 3 bifurcating at the base trunk.

Rays 4 and 5 joined on third part of length,

diverging at extremities. Left ray 6 longer than

right one, both arising at about same level as rays

3 and separated from rays 5. Rays 8 branches at

midlength of dorsal trunk, reaching the margin

of the caudal bursa. Dorsal ray divided at third

fourth part into 2 branches, each branches

divided into 2 subequal subbranches (rays 9 and

10). Genital cone 31 [22-36 (27)] long and 22

[18-31 (22)] wide (n=6). Papilla 0 and 7 not

observed. Spicules filiformes, equal and short

640 [472-708 (629)] long. Gubernaculum 27

[22-31 (28)] long and 22 [18-27 (22)] wide

(n=6) at the base in ventral view (Fig. 5 and 6).

Figure 6. Light microscopy of Hassalstrongylus luquei n. sp., ventral view of caudal bursa. Scale bar: 100 µm.

239

Neotrop. Helminthol., 8(2), 2014

Table 1. Locality, host and main morphological features and measurements of Hassalstrongylus species.

H. dessetae H. epsilon

(=Longistriata epsilon)

H. chabaudi H.hoineffae

(=Longistriata

hoineffae)

H.puntanus H.echalieri H. argentina

(=longistriata

argentina)

H.aduncus

(=longistriata adunca;

longistriata norvegica)

Length

4,72 – 5,25 3,1 4,37 – 4,45

5,2 3,52 2,3 – 2,6 4,08 – 5,40

4 – 4,5

Width 50 – 70 100 140 – 150 150 150 80 – 100 184 – 208 45 – 50

Cephalic vesicle - 60 x 25 - 80 - 50 65x35 55x25 640x720 -

esophagus 280 – 320 230 322 420 340 250 420/440 275/300

excretory pore - 240 306 365 270 200 - 20/27

nerve ring 140 - 180 160 95 245 170 75 189 -

spicule 140/150 115 470 / 480 410 450 150/175 472/520 350/375

Caudal bursa 140 – 180 x 230 - - 220 - 500 - 250/247 - -

Dorsal ray 120 - - - - - - -

Gubernaculum - - 45 x 27 30 x 10 170/120 400/350 400-490 x 240-320 -

Gemital cone 210 x 360 - 50 x 40 50 x 42 450/400 40 – 35 - -

Synlophe 34 22 24 (13v 11d) 22 – 24 24 205 - -

Locality Porto Terezinha

– AP

Formosa – GO Exú – PE Exu – PE Argentina Guiana Francesa Salta – Argentina Louisiana – USA

Host Neacomys sp. Nectomys squamipes Wiedomys

pyrrhoinus

Calomys callosus

Oryzomys nigripes

Wiedomys

Holochilus

balnearum

Oryzomys sp. Holochilus balnearum Rattus sp.

Table 1. Continuation.

Costa et al.

A new species of Hassalstrongylus

H. mazzai

(=Heligmonoides

mazzai)

H. musculi

(=longistriata

musculi)

H.litchenfelsi H. schadi

(=longistriata

schadi)

H. beta

(=longistriata

beta)

H. dollfusi

(=longistriata

dollfusi)

H. forresteri H. bocqueti H. luquei n.sp.

2,81 – 3,60 3,25 – 4,5 2,1 2,6 2,2 – 2,6 3,53 2,7 4,7

105 - 131 95 – 100 65 80 130 – 170 140 110 110

- 65 – 75 40 – 22 - 560 – 630 65-70 x 33 – 35 - 87 - 43 59x22

328 - 381 320-450 x 30-40 240 250 350 – 390 310 – 25 270 420

210 - 240 - 170 180 - 250 155 350

121 - 162 - 115 120 - - 120 230

202 – 221

390 – 420

185

220

530 – 560

625 – 660

430-500x180-220

390

450

130 - - - - - 62 -

270x110 - - - - - - 17 27x22

- - 25 – 10 - - - - 50 – 30

- - - - - - - -

- - 23 20 - - 23 – 25 -

– Argentina Louisiana - USA Florida - USA

Rio Raposo - Colombia - Aragua - Venezuela Florida - USA Les Tuxtlas - México Ilha Grande - Brazil

Holochilus

balnearum

Mus musculus Oryzomys

palustris

Nectomys alfari Wild rat Mus musculus

Oryzomys palustris Oryzomys alfaroi Euryoryzomys russatus

4,07

145

345

304

Table 1. Continuation.

Salta

240

echalieri Diaw, 1976. However, H. luquei n. sp.

is distinguished from H. mazzai by presenting

the dorsal rays divided at fourth part of the trunk ,

H. bocqueti by having rays 5 bifurcating at third

part of trunk and H. echalieri by having a pattern

of 2-2-1.

Thus, the presence of specific characters of

caudal bursa allow us to consider the specimens

from E. russatus as a new species.

Seven E. russatus were collected in the study

area and only three were positive with a low

parasite burden which limited the study, being

found only male specimens. However, the male

morphological characteristics are crucial to

identify the species.

The genus Hassalstrongylus is characterized by

having non hypertrophied genital cone, caudal

bursa symmetric or subsymmetric, cuticular

ridges ranging 19 to 24 with different sizes and

parasiting rodents mainly from the family

Cricetidae (Durette-Desset, 1971) (Table 1).

The characteristics of the caudal bursa are

essential to identify and separate this genus from

Stilestrongylus Freitas, lent, and Almeida, 1937

because there is an overlap in the number of

ridges in both genera (Digiani and Durette-

Desset, 2007). By the number of ridges (24 at the

midbody) and the characteristics of the caudal

bursa (subsymmetric with non hypertrophied

genital cone), the studied specimens can be

included in the genus Hassalstrongylus.

The main characters of new species are

subsymmetrical caudal bursa with a type 2-2-1,

rays 8 branching at midlength of dorsal trunk,

right lateral trunk larger than the left and the

longest spicules in the genus. The new species

can be distinguished from H. dessetae

Magalhães Pinto, 1978; H. epsilon Durette –

Desset, 1971; H. chabaudi Diaw, 1976; H.

honiffae Durette – Desset, 1971; H. bocqueti

Denke, 1977; H. puntanus Digiani and Durette –

Desset, 2003; H. argentina Freitas, Lent, and

Almeida, 1937; H. lichtenfelsi Durette – Desset,

1974; H. forresteri Durette – Desset, 1974; H.

schadi Durette – Desset, 1970; H. beta and H.

dolfusi Diaz – Ungria, 1963; by having rays 8

emerging from the middle of the dorsal trunk. In

addition, H. luquei n. sp. is differed from H.

musculi Dikmans, 1935; by having the rays 2

and 3 bifurcating at the base trunk.

Only three species of Hassaltrongylus present

the rays 8 not emerging at the base trunk, these

are: H. mazzai Freitas, Lent and Almeida, 1937;

H. aduncus Durette – Desset, 1971; and H.

DISCUSSION

Neotrop. Helminthol., 8(2), 2014

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Accepted June 10, 2014.

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