Pterygodermatites (Paucipectines) hymanae n. sp. (Rictulariidae) collected from the Incan shrew opossum, Lestoros inca, from Peru is described herein. These nematodes show a subapical, slightly dorsal oral opening and a laterally compressed buccal capsule with 2 conspicuous lateral walls and a dorsal wall. Each lateroventral wall possesses 4 relatively large denticles, and the dorsal wall has 6 denticles. Females are characterized by a conspicuously large postvulvar 37th spine, which may reach 1 mm. This is the first record of endoparasites in the Incan shrew opossum and the fifth species of Pterygodermatites recorded in New World marsupials

Jiménez, F Agustín

Patterson, Bruce D

English

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J. Parasitol., 98(3),2012, pp. 604-607@ American Society of Parasitologists 2012A NEW SPECIES OF PTERYGODERMATITES (NEMATODA: RICTULARIIDAE) FROM THEINCAN SHREW OPOSSUM, LESTOROS INCAF. Agustin Jimenez and Bruce D. Patterson*Department of Zoology, Southern Illinois University, Carbondale, Illinois 62901-6501. e-mail: agustinjz@zoology.siu.eduABSTRACT: Plerygodermalites (Paucipectines) hymanae n. sp. (Rictulariidae) collected from the [ncan shrew opossum, Lestoros inca,from Peru is described herein. These nematodes show a subapical, slightly dorsal oral opening and a laterally compressed buccalcapsule with 2 conspicuous lateral walls and a dorsal wall. Each lateroventral wall possesses 4 relatively large denticles, and the dorsalwall has 6 denticles. Females are characterized by a conspicuously large postvulvar 37th spine, which may reach I mm. This is the firstrecord of endoparasites in the [ncan shrew opossum and the fifth species of Pterygodermarites recorded in New World marsupials.Pterygodermatites Wedl, 1861, is a cosmopolitan genus ofspirurid nematodes that includes species with a prominent buccalcapsule and conspicuous spines along the surface of the cuticle.These nematodes occur in the digestive tract of mammals andshow a heteroxenous pattern of transmission (Quentin, 1969). InSouth America, there are II species of the genus included in 2subgenera, Pterygodermatites (Multipectines) or Pterygoderma-tites (Paucipectines) (Beldomenico et aI., 2005; Torres et aI., 2007;Hoppe et aI., 2010). Nine species of Pterygodermatites (Pauci-pectines) occur in South America, 4 in sigmodontine rodents(Quentin, 1967; Sutton, 1979, 1984); 1 in armadillos (Navone andLombardero, 1980; Navone, 1987); 1 in bats (Travassos, 1928);and I in microbiotherid and 3 in didelphid marsupials (Chabaudand Bain, 1981; Navone, 1989; Navone and Suriano, 1992;Ramallo and Claps, 2007; Torres et aI., 2007, 2009; Jimenez et aI.,2008). Pterygodermatites (Paucipectines) elegans (Travassos,1928) has been found in bats and didelphid marsupials. To ourknowledge, no other member of Pterygodermatites has beenreported in any of the 6 species of shrew opossums (Paucitu-berculata: Caenolestidae). The 3 genera of shrew opossums are allrestricted to Andean South America, i.e., Caenolestes at middle tohigh altitudes in the northern Andes, Lestoros on the easternVersant in southern Peru, and Rhyncholestes in the ValdivianForest of southern Chile and Argentina. All forage on the groundand feed on invertebrates and fungi (Patterson, 2007). We hereinpresent the first record for any helminth occurring in the Incanshrew opossum Lestoros inca (Thomas, 1917) and describe a newspecies of Pterygodermatites (Paucipectines).MATERIALS AND METHODS[ncan shrew opossums were collected at the locality of La Esperanza,Paucartambo, Cuzco, Peru (l3.17773°S, 71.60452°W, 2,880 m) from 25October to I November 2001. Shrew opossums were collected usingMuseum Special and Victor snap traps baited with peanut butter, oats,and fish oil, and killed by means of thoracic compression (Sikes andGannon, 2011). Specimens used in the present study were fixed in 4%buffered formaldehyde in the field and subsequently transferred to 70%ethanol for storage. Specimens are maintained in the fluid collection ofthe Division of Mammals, Field Museum of Natural History, Chicago,Illinois, accession numbers FMNH 174477, FMNH 174479, and FMNH174481. Viscera were extracted through an inguinal incision and wereexamined for helminths. Parasites found were separated from the organsand stored in 70% ethanol. Nematodes were cleared in temporary mountsof lactophenol. All measurements are given in micrometers, with theReceived 17 October 2011; revised 5 December 2011; accepted 22December 2011.* Department of Zoology, Field Museum of Natural History, Chicago,Illinois 60605-2496.DOl: lO.1645/GE-3014,1604exception of total length, esophagus, and distance to vulva; for eachcharacter, the range is given first, followed by mean, coefficient ofvariation (Sokal and Rohlf, 1995), and sample size. Drawings were madeusing an Olympus BX50 microscope equipped with a drawing tube.DESCRIPTIONPterygodermatites hymanae n. sp.(Figs. 1-9)General: Nematodes with thick cuticle, body uniformly cylindrical,slightly tapering at both ends (Figs. 1,2). Four pairs of papillae in anteriorend; 2 external pairs, subterminal, 2 internal pairs, both flanking stoma(Fig. 3). Oral opening subapical, slightly dorsal with 4 pseudolabia and Iventral groove (Fig. 3). Buccal capsule asymmetric, dorsally elongated(Fig. 4), laterally flattened (Fig. 5). Three strongly developed walls; 4denticles on margins of lateroventral walls (Figs. 3, 4), 6 minute denticlesin dorsal margin (Fig. 3), and 3 internal denticles in bottom of capsule, Idorsal and 2 lateroventral (Fig. 4). Two subventral rows of cuticularprojections run along the body. A single type of cuticular projectionpresent in males (Fig. I), 3 different types in females (Figs. 2, 6, 8).Esophagus filariform, with short muscular and long glandular portion(Figs. I, 2).Males (based on 2 specimens): Total length, 2.66--3.33 mm, maximumwidth at midbody 122-198. Dorsal wall of buccal capsule 18 (0.3%) long;ventral wall 23-24 (3.3%) long, 23-25 (7%) wide at base. Total length ofesophagus 1,057-1,224 (11.6%), length muscular portion 144-157 (5%),20-33 (31%) wide at level of nerve ring; glandular portion 913-1,057(12%) long, 36-59 (39%) wide. Nerve ring located 133-160 (14%) fromanterior end (Fig. I); excretory pore not observed. Forty-two pairs ofsubventral (n = I) and 3 precloacal ventral projections (Figs. I, 6). Eightpairs of caudal papillae. Spicules of different sizes, left 80-87 (6%) long, 9-10 (11%) wide at calomus; right 42-47 (9%) long, 5~6 (15%) wide atcalomus (Fig. 6). Tail 98-108 (8%) long (Fig. 6).Females (based on 8 gravid specimens): Total length, 16.22 by 26.37 mm(21.99, 17%), maximum width at midbody 448-881 (658, 24%). Dorsalwall of buccal capsule 69~123 (91, 24%) long; ventral wall 104-165 (127,19%) long, 89-151 (114,20%) wide at base. Total length of esophagus4.21-5.11 mm (4.64,7%), muscular portion 368-492 (426,12%, n = 6)long, 59-81 (73, 15%, n = 6) wide at nerve ring level; glandular portion3.72-4.51 mm (4.21,7%, n = 6) long, 133-223 (170, 22%) wide (Fig. 2).Nerve ring and deirids located 360-443 (399, 9%, n = 7) and 586 (n = I),respectively, from anterior end. Two subventral rows with 63 cuticularprocesses, 35 prevulvar (n = 6) (Fig. 2). Postvulvar processes 36-39 formhypertrophied spines (Fig. 2); processes 40 onward form smaller spines.Process 37 longer than rest, attached to body by 2 blunt roots, 561-901(769, 15%, n = 8) long, 133-188 (161, 12%, n = 8) wide at base (Fig. 7).Vulva 4.49-5.93 mm (5.32, 6%) from anterior end. Amphidelphicopisthodelphic, with ova 39-47 (42, 4.7%, n = 48) by 22-29 (26, 6.8%,n = 48) (Fig. 9). Tail 300-364 (329, 7%) (Fig. 8).Taxonomic summaryType host: [ncan shrew opossum, Lestoros inca (Thomas, 1917)(Paucituberculata: Caenolestidae). Symbiotype in FMNH 174481.Type locality: Peru, Cuzco, La Esperanza, 13.177733°S, 71.60451rW,2,880 m. Collected I November 2001.JIMt:NEZ AND PATIERSON-NEW SPECIES OF PTERYGOOERMATfTES 60553FIGURES1-6. Pterygodermatites (Paucipectilles) hymanae n. sp. (1) Male, whole body; scale bar = 100 11m.(2) Anterior end of female; anterior end islateral and body turns ventrally in the vulvar region where both rows of cuticular processes are parallel; scale bar = 200 11m.(3) En face view of a female,showing papillae, laterally compressed buccal capsule, and denticles in lateroventral and dorsal walls; scale bar = 50 11m.(4) Lateral view of anterior end,showing denticles in the bottom of buccal capsule; scale bar = 100 11m.(5) Dorsal view of anterior end; scale bar = 100 11m.(6) Tail of male, showingprecloacal formations, spicules, and tail; scale bar = 50 11m.Prevalence: Three of 3 shrew opossums (100%); mean intensity: 6.3;range: 2-9.Site of infection: Small intestine.Specimens deposited: Holotype in Museo de Historia Natural,Universidad Nacional Mayor de San Marcos, Lima [MUSM3057),allotype (FMNH-INVI4014), and paratypes (MUSM3058 and 3059 andFMNH-INVI4013,14015-14017).Etymology: The species is named after Dr. Libbie Henrietta Hyman,renowned invertebrate zoologist of the 20th century.RemarksPterygodennatites (Paucipectilles) hymallae is unique among all knownspecies of the subgenus from the Neotropics in having a laterally606 THE JOURNAL OF PARASITOLOGY, VOL. 98, NO.3, JUNE 2012FIGURES 7, 8. Pterygodermatites (Paucipectines) hymanae n. sp.Female. (7) Thirty-seventh cuticular process; scale bar = 200 Ilm. (8)Tail; scale bar = 300 Ilm.compressed buccal capsule, uniformly cylindrical body, and hypertrophiedpostvulvar spines. The body of the females of all other species in thesubgenus is divided into a thin anterior end and wide posterior half. Theposterior half contains the opisthodelphic uterus. The configuration of thebuccal capsule of P. (P.) hymanae is unique in that there are 4 relativelylarge denticles in the lateroventral walls of the capsule, and 6 minutedenticles in the dorsal wall. Relative to traits found in males, there are 3unpaired ventral cuticular processes in the tail, of which the most anterioris smaller. Among the 9 described species of the subgenus in SouthAmerica, only P. (P.) zygodontomys (Quentin, 1967) and P. (P.) eleganspossess 3 caudal processes. Pterygodermatites (Paucipectines) hymanae canbe distinguished from P. (P.) zygodontomys and P. (P.) elegans in the sizeFIGURE 9. Embryonated egg of Pterygodermatites (Paucipectines)hymanae n. sp.; scale bar = 20 Ilm.of the anterior ventral caudal process and shape of the body of females.Both P. (P.) hymanae and P. (P.) elegans show similar size and shape ofspicules. All remaining species in Pterygodermatites (Paucipectines) showspine-like subventral processes near the vulva; however, none of themshows spines as long as I mm.The configuration of the laterally compressed buccal capsule of P. (P.)hymanae is unique among all other species in the 5 subgenera. Thenematode herein described possesses a buccal capsule that appears to bean inverted triangle in face view, with 2 ventral walls and I dorsal wall.Each ventral wall bears 4 well-developed denticles, whereas the dorsal wallhas 6 smaller denticles. Known species of Pterygodennatites show anoblong buccal capsule in frontal view and bear a crown of minutedenticles. Examples of this configuration include species in Pterygoder-matites (Paucipectines) and Pterygodermatites (Neopaucipectines), whichpossess a similar number of homogeneous denticles. The latter subgenus isdiagnosed by the dorsally directed stoma, a trait that is common with thespecies herein described. However, the different numbers and sizes ofperi buccal denticles can be used to separate these taxa. In addition to thenumber of prevulvar cuticular processes, these structures are useful traitsto separate these 2 taxa from Pterygodermatites (Pterygodermatites), inwhich peri buccal denticles are notoriously irregular in size. Finally, theperibuccal structures in Pterygodermatites (Mesopectines) and Pterygo-dermatites (Multipectines) form apophyses in the ventral side.The configuration of the buccal capsule, the arrangement of the cephalicpapillae, and the sessile caudal papillae in P. (P.) hymanae make us suspectit could belong to a unique subgenus. The structures surrounding thestoma are of key relevance in the definition of subgenera in Ptery-godermatites. However, discrete and measurable characters used inthe differentiation of subgenera and species frequently overlap, makingspecies classification difficult (Tkach and Swiderski, 1996). More extensivesampling may reveal species showing similar traits. These could be used toreconstruct the phylogeny of the group, which may enable systematists toselect characters that can be used reliably in the definition of the genus andsubgenera.The 5 species of Pterygodermatites known to infect marsupials in theNew World include P. (Paucipectines) elegans in Marmosa sp. from Brazil,P. (P.) hymanae in Lestoros inca from Peru, Pterygodermatites (P.)jagerskioldi from Caluromys philander, Gracilinanus agilis, and Graci/ina-nus l1licrotarsus from Brazil, Pterygodermatites (P.) kozeki from Marl1losasp. from Colombia, and from Lestodelphys halli, Didelphis albiventris,Thylal1lis pusillus, and Thylal1lis pallidior from Argentina, and Pterygo-dermatites (P.) spinicaudatis in Drol1liciops gliroides from Argentina.ACKNOWLEDGMENTSThis work was funded by Faculty Seed grant 414095 of the SouthernIllinois University College of Sciences to F.A.J.; the specimens werecollected under National Science Foundation grant DEB-987019l toB.D.P.and colleagues. Thanks are due to Dr. Laura A. Campbell for herpatience and assistance in processing materials.LITERATURE CITEDBELDOMENICO,P. M., J. M. KINSELLA,M. M. UHART,G. L. GUTIERREZ,J.PEREIRA,H. D. FERREYRA,ANDC. A. MARULL. 2005. Helminths ofGeoffroy's cat, Oncifelis geofJroyi (Carnivora, Felidae) from theMonte Desert, central Argentina. Acta Parasitologica 50: 263-266.CHABAUD,A. G., AND O. BAIN. 1981. Quentius kozeki n. gen., n. sp.nematode rictularidae parasite de d'un marsupial americain. Anna1esde Parasitologie Humaine et Compare 56: 175-178.HOPPE,E. G. L., R. C. A. DELIMA, J. H. TEBALDI,ANDA. A. NASCIMENTO.2010. Pterygodermatites (Multipectines) pluripectinata n. sp. (Spiru-rida: Rictulariidae), a nematode parasite of the crab-eating foxCerdocyon thous (Linnaeus, 1766) from Caatinga shrubland, Brazil.Journal of Helminthology 84: 312-316.JIMENEZ,F. A., J. K. BRAUN,M. L. CAMPBELL,ANDS. L. GARDNER.2008.Endoparasites of fat-tailed opossums (Thylamys: Didelphidae) fromnorthwestern Argentina and southwestern Bolivia, with the descriptionof a new species of tapeworm. Journal of Parasitology 94: 1098-1102.NAVONE, G. T. 1987. Descripci6n del macho de Pterygodermatites(Paucipectines) chaetophracti (Navone y Lombardero, 1980) Sutton,1984 (Nematoda-Rictulariidae). Neotropica 33: 45-49.___ . 1989. Pterygodermatites (Paucipectines) kozeki (Chabaud et Bain,1981) n. comb., parasito de Lestodelphys halli Tate, 1934, Didelphisalbiventris L. y Thylamis pusilla (Desma rest) de la RepublicaArgentina. Anatomia y posici6n sistematica. Revista Iberica deParasitologia 49: 219-226.___ , ANDO. LOMBARDERO.1980. Estudios parasitol6gicos en edentadosArgentinos. I: Pterygodermatites (Pterygodermatites) chaetophractisp. nov. en Chaetophractus villosus y Dasypus hybridus (NematodaSpirurida). Neotropica 26: 65-70.___ , AND D. M. SURIANO. 1992. Pterigodermatites (Paucipectines)spinicaudatis n. sp. (Nematoda: Rictularidae) from Dromiciopsaustralis (Marsupialla: Microbiotheriidae) in Bariloche, Rio Negro,Argentina. Biogeographical distribution and host-parasite relation-ships. Memorias del Instituto Oswaldo Cruz 87: 533-538.JIM~NEZ AND PATIERSON-NEW SPECIES OF PTERYGOOERMATITES 607PATTERSON,B. D. 2008. Paucituberculata. In Mammals of South America,Volume 1. Marsupials, xenarthrans, shrews, and bats, A. L. Gardner(ed.). University of Chicago Press, Chicago, Illinois, p. 119-120.QUENTIN,J. C. 1967. Rictularia zygodontomys n. sp. nematode noveauparasite de rongeours du Bresil. Bulletin du Museum Nationald'Histoire Naturelle 39: 740-744.---. 1969. Essai de classification des nematodes rictulaires. Memoiresdu Museum National d'Histoire Naturelle 54: 55-115.RAMALLO,G., ANDL. E. CLAPS.2007. Nuevos hospedadores y registrosgeograficos de Pterygodermatites (Paucipectines) kozeki (Nematoda,Rictulariidae) en Argentina. Mastozoologia Neotropical 14: 93-96.SIKES, R. S., ANDW. L. GANNON. 2011. Guidelines of the AmericanSociety of Mammalogists for the use of wild mammals in research.Journal of Mammalogy 92: 235-253.SOKAL, R. R., AND F. J. ROHLF. 1995. Biometry: The principles andpractice of statistics in biological research, 3rd ed. W. H. Freeman,New York, New York, 887 p.SUTTON, c.' A. 1979. Contribuci6n al conocimiento de la faunaparasitol6gica Argentina. IV. Rictularia massoiai sp. n. y Enterobiusyagoi sp. n. (Nematoda). Acta Zoologica Lilloana 35: 29-37.___ . 1984. Contribuci6n al conocimiento de la fauna parasitol6gicaArgentina. XIII. Nuevos nematodes de la familia Rictulariidae.Neotropica 30: 141-152.TKACH,V. V., ANDZ. P. SWIDERSKI.1996. Scanning electron microscopy ofthe rare nematode species Pterygodermatites bovieri (Nematoda:Rictatuliriidae), a parasite of bats. Folia Parasitologica 43: 301-304.TORRES,E. L., A. MALDONADO,ANDR. M. LANFREDI.2007. Pterygoder-matites (Paucipectines) jagerskioldi (Nematoda: Rictulariidae) fromGracilinanus agilis and G. microtarsus (Marsupialia: Didelphidae) inBrazilian Pantanal and Atlantic forest by light and scanning electronmicroscopy. Journal of Parasitology 93: 274-279.___ , , AND ---. 2009. Spirurids from Gracilinanus agilis(Marsupialia: Didelphidae) in Brazilian Pantanal wetlands with a newspecies of Physaloptera (Nematoda: Spirurida). Veterinary Parasitol-ogy 163: 87-92.TRAVASSOS,L. 1928. Sobre uma especie do genera Rictularia Froelich(Nematoda). Boletim Biologico 62: 129-134.

A New Species of \u3ci\u3ePterygodermatites\u3c/i\u3e (Nematoda: Rictulariidae) from the Incan Shrew Opossum, \u3ci\u3eLestoros inca\u3c/i\u3e

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A New Species of \u3ci\u3ePterygodermatites\u3c/i\u3e (Nematoda: Rictulariidae) from the Incan Shrew Opossum, \u3ci\u3eLestoros inca\u3c/i\u3e

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