A New Metastrongilid Species (Nematoda: Metastrongylidae): A Lungworm from Akodon montensis (Rodentia: Sigmodontinae) in Brazil Author(s): Joyce G. R. Souza , Raquel O. Simões , Silvana A. R. C. Thiengo , Walter S. Lima , Esther M. Mota , Rosangela Rodrigues-Silva , Reinalda M. Lanfredi , and Arnaldo Maldonado Jr Source: Journal of Parasitology, 95(6):1507-1511. 2009. Published By: American Society of Parasitologists DOI: http://dx.doi.org/10.1645/GE-2013.1 URL: http://www.bioone.org/doi/full/10.1645/GE-2013.1
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J. Parasitol., 95(6), 2009, pp. 1507–1511 F American Society of Parasitologists 2009
A NEW METASTRONGILID SPECIES (NEMATODA: METASTRONGYLIDAE): A LUNGWORM FROM AKODON MONTENSIS (RODENTIA: SIGMODONTINAE) IN BRAZIL Joyce G. R. Souza, Raquel O. Simo˜es, Silvana A. R. C. Thiengo*, Walter S. Lima, Esther M. Mota`, Rosangela Rodrigues-Silva§, Reinalda M. LanfrediI, and Arnaldo Maldonado, Jr.# Laborato´rio de Biologia e Parasitologia de Mamı´feros Silvestres Reservato´rio, Instituto Oswaldo Cruz—FIOCRUZ, Av. Brasil 4365, 21040-900, Rio de Janeiro, RJ, Brazil. e-mail:
[email protected] ABSTRACT:
Angiostrongylus lenzii n. sp. (Nematoda: Metastrongyloidea) is described and illustrated from the pulmonary artery of the wild rodent Akodon montensis Thomas, 1913, collected in the municipality of Teresopo´lis, Rio de Janeiro State, Brazil. It represents the 17th species of the genus and the 2nd in South America as parasites in rodents. This new species is the most similar morphologically to Angiostrongylus vasorum, Angiostrongylus gubernaculatus, Angiostrongylus schmidti, and Angiostrongylus morerai. It can be distinguished from them by the morphology of the caudal bursa, ventral rays 2 and 3 with conspicuous knobs, differences in width and length of lateral and dorsal rays, presence of rays 8, and length of spicules.
Species of Angiostrongylus Kamensky, 1905 (Metastrongyloidea) occur in domestic dogs and wild mammals (Anderson, 1978). Some species may accidentally infect humans, causing characteristic clinical symptoms of the disease (Graeff-Teixeira et al., 1991; Wang et al., 2008). Drozdz (1970) and Anderson (1978) divided Angiostrongylus into 2 subgenera, i.e., Angiostrongylus and Parastrongylus, based on the morphology of the lateral rays of the caudal bursa. Later, Ubelaker (1986) regarded these subgenera as a single genus based on specific host groups. However, this latter point of view has not been widely accepted (Robles et al., 2008). To date, 16 species of Angiostrongylus have been reported around the world. Three species have been described infecting carnivores, i.e., Angiostrongylus vasorum Baillet, 1866 (syn. Angyostrongylus raillieti Travassos, 1927); Angiostrongylus gubernaculatus Dougherty, 1946; and Angyostrongylus chabaudi Biocca, 1957. In rodents, 13 species have been described: Angiostrongylus taterone Baylis, 1928; Angiostrongylus cantonensis Chen, 1935; Angiostrongylus sciuri Merdevenci, 1964; Angiostrongylus mackerrasae Bhaibulaya, 1968; Angiostrongylus sandarsae Alicata, 1968; Angiostrongylus petrowi Tarjymanova and Tschertkova, 1969; Angiostrongylus dujardini Drozdz and Doby, 1970; Angiostrongylus schmidti Kinsella, 1971; Angiostrongylus costaricensis Morera and Ce´spedes, 1971; Angiostrongylus malaysiensis Bhaibulay and Cross, 1971; Angiostrongylus ryjikovi Jushkov, 1971; Angiostrongylus siamensis Ohbayashi, Kamiya, and Bhaibulaya, 1979; and Angiostrongylus morerai Robles, Navone, and Kinsella, 2008. Currently, there are 44 species of wild sigmodontine rodents (Akodon spp.) described in South America (Musser and Carleton, 2005). Akodon montensis Thomas, 1913 occurs from Rio de Janeiro to Rio Grande do Sul, Brazilian states, and is 1 of the most abundant Received 7 January 2009; revised 28 April 2009, revised 16 June 2009; accepted 26 June 2009. * Laborato´rio de Malacologia, Instituto Oswaldo Cruz-FIOCRUZ, 21040-900, RJ, Brasil. { Laborato´rio de Helmintologia Veterina´ria, Departamento de Parasitologia, Instituto de Cieˆncias Biolo´gicas, Universidade Federal de Minas Gerais, 31270-910, Belo Horizonte, Brasil. { Laborato´rio de Patologia, Instituto Oswaldo Cruz-FIOCRUZ, 21040900, Rio de Janeiro, RJ, Brasil. } Laborato´rio de Helmintos Parasitos de Vertebrados, Instituto Oswaldo Cruz-FIOCRUZ, 21040-900, Rio de Janeiro, RJ, Brasil. ILaborato´rio de Biologia de Helmintos OttoWucherer, Instituto de Biofı´sica Carlos Chagas Filho, CCS, bl. G. Universidade Federal do Rio de Janeiro, Ilha do Funda˜o, 21949-900 Rio de Janeiro, RJ, Brasil. # To whom correspondence should be addressed. DOI: 10.1645/GE-2013.1
sigmodontine species in the Neotropics (Bonvicino et al., 2008). Akodon spp. have deserved significant attention, because they can act as Hantavirus reservoirs (Suzuki et al., 2004) and as reservoir hosts for 2 human parasites, i.e., Schistosoma mansoni (RodriguesSilva et al., 1991) and Trypanosoma cruzi (Herrera et al., 2005). The purpose of the present article is to describe a new species of Angiostrongylus collected from the pulmonary artery of A. montensis. MATERIALS AND METHODS Fourteen Akodon montensis were captured in a fragment of the Atlantic ´ rga˜os, Tereso´polis, Rio de Janeiro State, Brazil in 2005, Forest Serra dos O with the use of Sherman and Tomahawk traps. Collection permits for rodents were issued by IBAMA (number 068/2005). Animals were killed with CO2 and dissected in the field. Nematodes were collected from the pulmonary artery, washed in physiologic solution, and fixed in hot AFA. Three male and 6 female specimens were cleared in lactophenol and examined with a Zeiss Standard 20 light microscope. Drawings were made with the aid of a camera lucida. Measurements are given in micrometers (unless otherwise stated) for holotype or allotype specimens, followed by range for paratypes in parentheses and mean in brackets. The nomenclature of the caudal bursa is in agreement with Anderson (1978) and the terminology of the host taxonomy follows Musser and Carleton (2005). The studied specimens of A. vasorum were isolated from Canis familiars in Minas Gerais state (Lima et al., 1985) and have been maintained by successive passages in Biomphalaria glabrata and domestic dogs under laboratory conditions. Symbiotype host was deposited in the Nacional Museum (MN), Rio de Janeiro State. Type specimens were deposited in the Helminth Collection of the Oswaldo Cruz Institute (Colec¸a˜o Helmintolo´gica do Instituto Oswaldo Cruz-CHIOC), Rio de Janeiro, Brazil.
DESCRIPTION Angiostrongylus lenzii n. sp (Figs. 1–3) General: Medium-size nematode with transparent transversally striated cuticle. Body of both sexes filiform and tapering at anterior end. Females larger and more robust than males. Cephalic vesicle absent. Anterior end dome shaped with mouth aperture surrounded by 4 pairs of cephalic papillae in apical view. Esophagus claviform. Excretory pore posterior to esophagus (Fig. 1). Caudal bursa showing pattern of type 2-3-1. Gubernaculum present; long spicules with ratio spicule length/ body length (Spl/Bl) 2.8% (Fig. 2). Male (based on 1 holotype and 2 paratypes): Body 14.1 (9.3–14.1 [11.7]) mm long (n 5 2) and 0.2 mm wide (n 5 1). Esophagus 232 from anterior end (n 5 1; Fig. 1). Caudal bursa slightly subsymmetrical, type 2-3-1 (Fig. 2). Ventral rays 2 and 3 with common origin, bifurcating at proximal half, each with an expansion (knob) ending narrower, not reaching bursal margins. Lateral trunks (rays 4–6) arise distally from ventral trunk, with common origin. Right ray 4, thicker and shorter than left, not extending to bursal margins, diverging from rays 5 and 6 at base. Rays 5 and 6 directed posteriad, bifurcating at distal third, extending bursal margins. Rays 9 short,
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FIGURES 1–3. Angiostrongylus lenzii n. sp. (1) Anterior extremity, right lateral view, male. Scale bar: 50 mm. (2) Male, caudal bursa, ventral view. Scale bar 5 100 mm. (3) Female, posterior extremity, lateral view. Scale bar 5 100 mm.
arising symmetrically from dorsal trunk that bifurcates distally into 2 short branches (Figs. 2, 4, 5). Spicules with strongly cuticularized sheath, thick, subequal length 390 (350–390 [370]; n 5 3), ending in sharp tips, representing 2.8% of body length. Gubernaculum present. Two adcloacal papillae present (Fig. 2). Female (based on 1 allotype and 5 paratypes): Body length 22.3 (22.1– 25.9 [23.64]) mm (n 5 4) and 0.4 (0.3–0.4 [0.4]) mm wide at midbody.
Esophagus 236 (200–240 [220]) long (n 5 4; Fig. 1). Excretory pore 365 (333–450 [391]; n 5 3), nerve ring 87 (81–106 [94]) from anterior end, respectively (Fig. 1). Monodelphic. Vulva situated anterior to anus with protuberant lips. Vulva and anus 345 (310–364 [334]); 77 (61–80 [69]), respectively, from caudal extremity (Fig. 3). Vagina and anus showed thick cuticularized walls. Uterine tubules spiral around blood-filled intestine and can be seen through transparent cuticle. Tail long and
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FIGURES 4–7. Light microscopy of Angiostrongylus spp. (4) Angiostrongylus lenzii n. sp., ventral view of caudal bursa showing knots (*) on ventral rays, difference on lengths of externolateral (R), posterodorsal rays (_) and dorsal trunk bifurcation (¢). Scale bar 5 50 mm. Detail of adcloacal papillae (p). Scale bar 5 25 mm. (5) Angiostrongylus lenzii n. sp., ventral view of caudal bursa showing a bifurcation of the dorsal trunk into 2 rays (R). Scale bar 5 50 mm. (6) Angiostrongylus vasorum, ventral view of caudal bursa. Scale bar: 50 mm. (7) Angiostrongylus vasorum, lateral view of caudal bursa. Scale bar 5 50 mm.
rounded without cuticle expansion and papillae, slightly ventrally curved (Fig. 3). Numerous uterine eggs 60 (50–100 [80]) long; 40 (30–50 [50]) wide (n 5 10). Taxonomic summary Types: Male holotype, CHIOC: 35621. Female allotype CHIOC: 35620. Paratypes, 4 females: CHIOC 35620a-d. Type host: Akodon montensis Thomas, 1913, grass rat (Cricetidae, Sigmodontinae), MN 72044. Site of infection: Pulmonary artery. ´ rga˜os, Tereso´polis, Rio de Janeiro, Brazil Type locality: Serra dos O (22u129440S, 042u489400W). Prevalence and intensity of infection: 14.2% of the hosts (2 of 14), mean infection 5.0, range 129 specimens. Etymology: The specific name is in honor of the renowned pathologist and parasitologist Dr. Henrique Leonel Lenzi from the Instituto Oswaldo Cruz–Fundac¸a˜o Oswaldo Cruz.
Remarks Based on Anderson’s (1978) classification key, Angiostrongylus is divided into 2 subgenera, i.e., Parastrongylus and Angiostrongylus, which are differentiated by the origin of the externolateral ray, which is joined in a common trunk in the former and separated from the other lateral rays in the latter. According to Robles et al. (2008), the diagnostic features that divide the genus Angiostrongylus deserve to be reviewed, because A. vasorum belongs to the subgenus Angiostrongylus, but have morphological characteristic of the subgenus Parastrongylus, i.e., the externolateral ray arise from a single trunk. Angiostrongylus lenzii n. sp was found in the pulmonary artery of the rodent A. montensis collected in the Atlantic Forest of Rio de Janeiro State. The reduced dorsal ray, cephalic extremity without elevation, external lateral rays well developed and arising from the common lateral trunk, ventral rays arising in a common trunk, presence of adcloacal papillae, and long spicules in males, and females with a rounded tail, collectively permitted identification of the specimens described herein as a new species of Angiostrongylus.
– – 310–364 61–80 – 50–89 3 38–49 30 3 30 187–209 – – – – – – – 75–90 205–250 – 45–50 – – – – – – – 175–345 57–99 – – – – 250–335 71–108 – – – – 220–315 61–100 – –
42–54 – – – – –
35–45 – – – – –
22.3–25.9 300–401 – 200–240 81–136 376 – 9.3–14.1 183 – 232 – – 350–390 22.0–24.0 350 – 335–350 – – – 18.0–19.5 300 – 300–355 – – 520–560 17.8–30.1 110–165 39–54 322–406 250 – – 29.0–30.0 – 285–335 388–395 – – –
Gubernaculum Width of bursa Vulva–tail Anus–tail Vulva–anus Eggs
Body length Width Width at the base of esophagus Esophagus Nerve ring Excretory pore Spicules
14.0–15.5 – – 220–275 80–92 310–350 400–480 450–500 40–55 – – – – –
15.0–20.5 – – 240–280 80–96 350–370 –
17.1–19.2 – 265–285 220–285 – – 400–465
9.5–14.9 – 32–43 290–350 225 – 215–279
R R R =
A. vasorum
R
A. morerai =
=
A. schmidti
R
=
A. gubernaculatus
=
A. lenzii n. sp.
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TABLE I. Comparative measurements of Angiostrongylus vasorum Baillet, 1866; Angiostrongylus morerai Robles, Navone, and Kinsella 2008; Angiostrongylus schmidti Kinsella, 1971; Angiostrongylus gubernaculatus Dougherty, 1946; and Angiostrongylus lenzii n. sp. Measurements are given in micrometers, except for body length, which is in millimeters.
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The morphologically similar species include A. vasorum, A. schmidti, A. gubernaculatus, and A. morerai. Angiostrongylus lenzii can be differentiated from A. schmidti by the size of spicules (350–390 vs. 215–279; Table I), as well as ventral rays 2–3 with knobs and a left external lateral ray 4 that is thinner and longer (both smaller than rays 5 and 6). In addition, it also differs from the other species in the genus by a bifurcation of the dorsal trunk into 2 rays, plus ray 9 being smaller than ray 10. Angiostrongylus lenzii is the first species to show knots at rays 2 and 3, both of equal length, whereas in A. vasorum rays 2 are smaller than rays 3. In A. gubernaculatus, rays 2 are shorter and thinner than rays 3, and in A. schmidti rays 2 and 3 are subequal and fused in the lower half. Rays 2 and 3 of A. morerai are similar in length to A. lenzii, but do not possess knobs. Moreover, A. lenzii is the first species in the genus to present asymmetrical length of rays 4 when compared to rays 5 and 6. The left ray 4 is thinner and longer than the right one, but does not reach the bursal margins and is shorter than rays 5–6, which almost reach the bursal margins, thus distinguishing it from A. vasorum, A. gubernaculatus, A. schmidti, and A. morerai. In addition, the closely related A. morerai presents an asymmetrical left lateral trunk (rays 4–6) when compared to the right trunk. Rays 4 also differs in width. The right ray 4 arises more proximally at the base of the trunk than the left one. Both rays 4 have lengths similar to rays 5, which are slightly shorter than rays 6, which differs from A. lenzii; i.e., rays 4 arise at the same level as the lateral main trunk, and rays 4 are slightly shorter than rays 5 and 6. In A. morerai, rays 8 are more proximal to the dorsal ray and thicker than rays 8 of A. lenzii. The dorsal ray of A. lenzii is longer than the dorsal ray of A. vasorum, A. gubernaculatus, and A. schmidti, but shorter than the dorsal ray of A. morerai, which presents a V-shaped bifurcation and a thinner distal region of the dorsal ray. Angiostrongylus lenzii males (9.3–14.1 mm) are shorter in length than A. gubernaculatus, and A. morerai, except for A. vasorum, in which males are longer and females are shorter (Table I). Rays 9 and adcloacal papillae are present only in A. lenzii. Differences were also observed in the length of the A. morerai female esophagus (388–395), which in this case were longer as well as in the shorter distance of the vulva from the tail (250–355). Finally, spicules of A. lenzii are smaller than those of A. gubernaculatus, A. morerai, A. vasorum, and longer than A. schmidti (Table I). There are 2 species of Angiostrongylus reported in South America as parasites in rodents, i.e., A. morerai and A. lenzii n. sp., which share some morphological similarities and occur in sigmodontine rodents. Despite their co-occurrence, they can be distinguished by morphological and morphometric characteristics.
DISCUSSION Drozdz (1970) separated species of Angiostrongylus into 2 subgroups based on morphological characters of the caudal bursa and assigned them in 2 subgenera. Angiostrongylus has the ventrolateral ray arising independent from mediolateral and posterolateral rays, which emerged as a single trunk. Moreover, species of Angistrongylus are parasites of the right heart and pulmonary artery of carnivores. In contrast, species of Parastrongylus, parasites of rodents, have lateral rays that arise in a common trunk and split at the same level. Species of a third subgroup are parasites of insectivores; they belong to Stefanskostrongylus, and include species with lateral rays similar to those of the subgenus Parastrongylus, except that the gubernaculum is absent. Anderson (1978) accepted these systematic criteria, but did not reference biological characters such as host specificity or site of infection. Morphologically, the closest species to A. lenzii are parasites of sigmodontine rodents, such as A. morerai and A. schmidti, or of carnivores, i.e., A. gubernaculatus and A. vasorum, indicating that the parasite host is somewhat problematic when used as a systematics character. Anderson (1978) considered A. vasorum as belonging to the subgenus Angiostrongylus. However, Robles et al. (2008) and Costa et al. (2003) asserted that the lateral rays in A. vasorum all arise from a single trunk. However, on studying A. vasorum
SOUZA ET AL.—NEW METASTRONGYLID FROM A. MONTENSIS
specimens collected from C. familiaris in Brazil, it was clearly shown that the right externolateral rays do not arise from a single trunk (Fig. 6), which is different from what was observed in the left side, where rays emerge from a single trunk (Figs. 6, 7). The insertion of the lateral rays as applied to the taxonomy of Angiostrongylus should be revised, because A. vasorum has morphological features found in both subgenera. Moreover, Guilhon and Cens (1973) illustrated A. vasorum as having the rays 4 emerging separated from rays 5, despite the micrographs showing distinct patterns for each side of the bursal rays. The intensity of infection by A. lenzii in A. montensis was low, with just 10 specimens recovered from 2 rodents of 14 potential hosts collected and necropsied. Likewise, Graeff-Teixeira et al. (1990) reported that only 2 specimens of A. costaricensis were observed in a natural infection of Oligoryzomys nigripes (syn. Oryzomys nigripes) and 2 specimens in Sooretamys angouya (syn. Oryzomys ratticeps) in Brazil. A low prevalence of A. schmidti was also observed by Kinsella (1971) in Oryzomys palustris in North America. Finally, Robles et al. (2008) reported A. azarae infected by only a few specimens of A. morerai in Argentina. According to Rodrı´guez et al. (2000), the pattern of infection of Sigmodon hispidus with A. cantonensis may be due to habitat variations, or feeding behaviors, or both. In fact, long-term studies on helminth parasitism in sigmodontine rodents have demonstrated substantive temporal variation in the pattern of infection (Maldonado et al., 2006). ACKNOWLEDGMENTS We thank Dr. Paulo Se´rgio D’Andrea for helping us capturing rodents and the anonymous referee for reviewing the manuscript. Brazilian financial support came from CNPq, PAPES IV, PIBIC, and CAPES-PROCAD.
LITERATURE CITED ANDERSON, R. C. 1978. Keys to genera of the superfamily Metastrongyloidea. In CIH Keys to the nematodes parasites of vertebrates, R. C. Anderson, A. G. Chabaud, and S. Willmott (eds.). Commonwealth Agricultural Bureaux, Farnham Royal, Bucks, U.K., p. 1–40. BONVICINO, C. R., J. A. OLIVEIRA, AND P. S. D’ANDREA. 2008. Guia dos roedores do Brasil, com chaves para geˆneros baseada em caracteres externos. Centro Pan-Americano de Febre Aftosa—OPAS/OMS, Rio de Janeiro, Brazil, 280 p. COSTA, J. O., H. M. DE ARAU´JO COSTA, AND M. P. GUIMARA˜ES. 2003. Redescription of Angiostrongylus vasorum (Baillet, 1866), and systematic revision of species assigned to the genera Angiostrongylus Kamensky, 1905 and Angiocaulus Schulz, 1951. Revue Me´dicine Ve´terinaire 154: 9–16. DROZDZ, J. 1970. Re´vision de le syste´matique du genre Angiostrongylus Kamensky, 1905 (Nematoda: Matastronguloidea). Annales de Parasitologie (Paris) 45: 597–603.
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