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.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

de Oliveira Simões, Raquel

dos Santos Lucio, Camila

Maldonado Júnior, Arnaldo

Neves Bóia, Márcio

Rodrigues Costa, Mariane Almeida

Spanish

LAReferencia - Red Federada de Repositorios Institucionales de Publicaciones Científicas Latinoamericanas

235Neotrop. Helminthol., 8(2), 20142014 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)ISSN: 2218-6425 impreso / ISSN: 1995-1043 on lineORIGINAL ARTICLE / ARTÍCULO ORIGINALA NEW SPECIES OF HASSALSTRONGYLUS (NEMATODA: HELIGMONELIDAE) FROM EURYORYZOMYS RUSSATUS (RODENTIA: SIGMODONTINAE) IN THE ATLANTIC FOREST, BRAZILUNA NUEVA ESPECIE DE HASSALSTRONGYLUS (NEMATODA: HELIGMONELIDAE) DE EURYORYZOMYS RUSSATUS (RODENTIA: SIGMODONTINAE) EN LA MATA ATLÁNTICA, BRASILMariane Almeida Rodrigues Costa¹, Arnaldo Maldonado Júnior¹, Márcio Neves Bóia¹,Camila dos Santos Lucio¹ & Raquel de 1*Oliveira Simões   AbstractKeywords: 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.comConselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) research fellowHassalstrongylus 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.ResumenPalabras 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 2-2-1.236Costa et al.A new species of HassalstrongylusAnimal Use (Permit Number: L – 0049/08). The rodents were killed using a CO  chamber and 2necropsied.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 Hassals trongylus  (Tr ichost rongyl ina:  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 INTRODUCTIONMATERIAL AND METHODSRESULTS237Neotrop. Helminthol., 8(2), 2014Figures 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. 238Costa et al.A new species of HassalstrongylusTaxonomic summaryType 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. 239Neotrop. Helminthol., 8(2), 2014Table 1.  Locality, host and main morphological features and measurements of Hassalstrongylus species. H. dessetaeH. epsilon(=Longistriata epsilon)H. chabaudiH.hoineffae(=Longistriata hoineffae)H.puntanusH.echalieri     H. argentina(=longistriata argentina)H.aduncus(=longistriata adunca; longistriata norvegica)Length 4,72 – 5,253,14,37 – 4,45 5,23,522,3 – 2,64,08 – 5,40 4 – 4,5Width50 – 70100140 – 15015015080 – 100184 – 20845 – 50Cephalic vesicle-60 x 25-80 - 5065x3555x25640x720-esophagus280 – 320230322420340250420/440275/300excretory pore-240306365270200-20/27nerve ring140 - 1801609524517075189-spicule140/150115470 / 480410450150/175472/520350/375Caudal bursa140 – 180 x 230--220 - 500-250/247--Dorsal ray120-------Gubernaculum--45 x 2730 x 10170/120400/350400-490 x 240-320-Gemital cone210 x 360-50 x 4050 x 42450/40040 – 35--Synlophe342224 (13v 11d)22 – 2424205--LocalityPorto Terezinha – APFormosa – GOExú – PEExu – PEArgentinaGuiana FrancesaSalta – ArgentinaLouisiana – USAHostNeacomys sp.Nectomys squamipesWiedomys pyrrhoinusCalomys callosusOryzomys nigripesWiedomysHolochilus balnearumOryzomys sp.Holochilus balnearumRattus sp.Table 1. Continuation.Costa et al.A new species of HassalstrongylusH. mazzai(=Heligmonoides mazzai)H. musculi(=longistriata musculi)H.litchenfelsiH. schadi(=longistriata schadi)H. beta(=longistriata beta)H. dollfusi(=longistriata dollfusi)H. forresteriH. bocquetiH. luquei n.sp.2,81 – 3,603,25 – 4,52,12,62,2 – 2,63,532,74,7105 - 13195 – 1006580130 – 170140110110-65 – 7540 – 22-560 – 63065-70 x 33 – 35-87 - 4359x22328 - 381320-450 x 30-40240250350 – 390310 – 25270420210 - 240-170180-250155350121 - 162-115120--120230202 – 221- -390 – 420- -185 - -220 - -530 – 560- -625 – 660430-500x180-220-390 - -450 - -130-----62-270x110------1727x22--25 – 10----50 – 30----------2320--23 – 25-– Argentina Louisiana - USAFlorida- USA Rio Raposo - Colombia-Aragua - VenezuelaFlorida- USALes Tuxtlas - MéxicoIlha Grande - BrazilHolochilus balnearumMus musculusOryzomys palustrisNectomys alfariWild ratMus musculus Oryzomys palustrisOryzomys alfaroiEuryoryzomys russatus4,0714534530481 64 - - - - 24Table 1. Continuation.Salta  240echalieri 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. DISCUSSIONNeotrop. Helminthol., 8(2), 2014BIBLIOGRAPHIC REFERENCESDigiani, MC & Durette-Desset, MC. 2007. Trichostrongylina (Nematoda) parasitic in Phyllotis sp. (Rodentia:Sigmodontinae) from Argentina, with description of three new species. Parasitology International, vol. 56, pp. 9-18.Durette-Desset, MC. 1971. Essai de classification dês nematodes héligmosomes. Correlation avec la paléogeographie dês hôtes. Bulletin de Muséum National D'Histoire Naturalle, vol. 69, pp. 1-126.Durette-Desset, MC. 1985. Trichostrongyloid nematodes and their vertebrate hosts reconstruction of the phylogeny of a parasitic group. Advances in Parasitology, vol. 24, pp. 239-306.Durette-Desset, MC & Chabaud, AG. 1981. Novel essai de classification des nematodes t r i c h o s t ro n g y l o d e a .  A n n a l e s  d e  Parasitologie Humaine et Comparée, vol. 56, pp. 297-312.Durette-Desset, MC & Digiani, MC. 2005. The axis of orientation of the synlophe in the H e l i g m o s o m o i d e a  ( N e m a t o d a ,  Trichostrongylina): A new approach. Parasite,  vol. 12, pp.195-202.Emmons, L & Feer, F. 1997. Neotropical rainforest mammals: a field guide.  Chicago and London, The University of Chicago Press, 307p.Naxara, L, Pinotti, BT & Pardini, R. 2009. Seasonal microhabitat selection by terrestrial rodents in an old-growth Atlantic Forest. Journal of Mammalogy, vol. 90, pp. 404–415.Passamani, M & Fernandez, FAS. 2011. Abundance and richness of small mammals 241Costa et al.A new species of HassalstrongylusUmetsu, F & Pardini, R. 2007. Small mammals in a m o s a i c  o f  f o re s t  re m n a n t s  a n d  anthropogenic habitats — evaluating matrix quality in an Atlantic forest landscape. Landscape Ecology, vol. 22, pp. 517–530. in fragmented Atlantic Forest  of  southeastern Brazil. Journal of Natural History, vol. 45, pp. 553–565.Ribeiro, JR, Boggione, GA & Silva, MV. 2009. Diagnose da cobertura vegetal de Ilha Grande no município de Angra dos Reis – RJ, Pós Presídio, utilizando técnicas de Geoprocessamento. Anais XIV Simpósio Brasileiro de Sensoriamento Remoto, Natal, Brasil, INPE, pp. 1497 – 1504.Received April 8, 2014.Accepted June 10, 2014.242

UNA NUEVA ESPECIE DE HASSALSTRONGYLUS (NEMATODA: HELIGMONELIDAE) DE EURYORYZOMYS RUSSATUS (RODENTIA: SIGMODONTINAE) EN LA MATA ATLÁNTICA, BRASIL

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

Costa, Mariane Almeida Rodrigues

Maldonado Jr., Arnaldo

Bóia, Márcio Neves

Lucio, Camila dos Santos

Simões, Raquel de Oliveira

RCAAP - Repositório Científico de Acesso Aberto de Portugal

Una nueva especie de Hassalstrongylus (Nematoda: Heligmonelidae) de  Euryoryzomys russatus (Rodentia: Sigmodontinae) el la Mata Atlántica, Brasil

https://revistas.unfv.edu.pe/NH/article/download/916/806

UNA NUEVA ESPECIE DE HASSALSTRONGYLUS (NEMATODA: HELIGMONELIDAE) DE EURYORYZOMYS RUSSATUS (RODENTIA: SIGMODONTINAE) EN LA MATA ATLÁNTICA, BRASIL

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