MORPHOLOGY, SYSTEMATICS, EVOLUTION
A New Species of Tunga (Siphonaptera: Tungidae) From Brazil With a Key to the Adult Species and Neosomes DANIEL M. DE AVELAR,1 ARI´CIO X. LINHARES,2
AND
PEDRO M. LINARDI1,3
J. Med. Entomol. 49(1): 23Ð28 (2012); DOI: http://dx.doi.org/10.1603/ME11111
ABSTRACT Tunga bossii new species of tungid sand ßea belonging to the caecata group is described with illustrations of the adult female, parasitizing the wild rodent Delomys dorsalis (Hensel) from Brazilian Atlantic Forest. Tunga bossii differs from the ten other known species of Tunginae by the size of the Þrst segment of the maxillary palp and the presence of two bristles at the base of the maxilla. Tunga bossii also can be differentiated from other species of the T. caecata group by the eye morphology. A key to the adult species and neosomes of the genus Tunga also is included.
Tunga Jarocki, 1838, is the most specialized genus of the order Siphonaptera because adult females penetrate into the skin of their hosts, causing serious ectoparasitosis and harmful infections (Hopkins and Rothschild 1953, Linardi and Guimara˜es 2000, Pampiglione et al. 2009). After mating, gravid females undergo hypertrophy, becoming a neosome 5Ð13 mm in size, deÞned as an entire organism of signiÞcant enlargement formed of new morphological structure, accompanied by growth of new tissue, during a single active stadium of an invertebrate (Audy et al. 1972, Rothschild 1992). Currently the genus includes 10 species of sand ßeas, parasitizing armadillos, anteaters, rodents, pigs, human and other domestic animals, distributed in the New World tropics, Sub-Saharan Africa, China, and Japan (Lewis 1998). According to Barnes and Radovsky (1969) the center of distribution of the genus Tunga is within the Neotropical region, considering that of the 10 described species, six are restricted to South America and another, Tunga penetrans (L., 1758), exhibits a wide Neotropical distribution, being now permanently established in much of tropical Africa (Lewis 1998). Based on morphology and host afÞnities, Smit (1962) divided Tunga into two species groups, penetrans and caecata. Currently, the penetrans group includes T. penetrans; T. trimamillata Pampiglione, Trentini, Fioravanti, Onore, and Rivasi, 2002 (Ecuador); and three Brazilian species: T. travassosi Pinto and Dreyfus, 1927, T. bondari Wagner, 1932 and T. terasma Jordan, 1937, all of them associated primarily with 1
Departamento de Parasitologia, Instituto de Cieˆ ncias Biolo´ gicas da Universidade Federal de Minas Gerais, Caixa Postal 486, Avenida Antoˆ nio Carlos, 6627, Campus UFMG, Minas Gerais, 31270-901, Brazil. 2 Departamento de Parasitologia, Instituto de Biologia, Universidade Estadual de Campinas. 3 Corresponding author, e-mail:
[email protected].
edentates. The caecata group, found exclusively on rodents, includes T. caecata (Enderlein 1901) (Brazil), T. caecigena Jordan and Rothschild, 1921 (China and Japan); T. callida Li & Chin, 1957 (China); T. libis Smit, 1962 (Ecuador); and T. monositus Barnes and Radovsky, 1969 (Mexico and United States). Another proposal that includes the two Chinese species in a distinct subgenus (Brevidigita) was presented by Wang (1976). However, in spite of morphological differences between the groups, some difÞculties are found when identifying species. The hypertrophial female is the most frequently observed form in hosts and after oviposition, the neosome involutes with the dead parasite being absorbed or sloughed from the host epidermis by tissue repair mechanisms (Lavoipierre et al. 1979, Eisele et al. 2003). More often the legs are missing after Þxation in the hosts (Rothschild 1992) and some characteristics cannot be seen in the most dissected specimens. With the exception of T. libis, all gravid females are known. However, only Þve species have known males: T. penetrans, T. terasma, T. libis, T. monositus, and T. trimamillata. The current study describes a new species of Tunga of the caecata group parasitizing the tail base of the striped rat Delomys dorsalis and collected during the course of the interrelationship ßea-host studies from Atlantic Forest areas in southeastern Brazil (Bossi 2003, de Moraes et al. 2003). A key for Tunga adult species and respective neosomes also is included. Materials and Methods Delomys dorsalis harboring specimen of Tunga was collected in one area of the Itatiaia National Park (Itatiaia, RJ 22⬚ 26.187⬘ S, 44⬚ 37.511⬘ W) and taken to the laboratory of the Department of Parasitology, State University of Campinas, where two
0022-2585/12/0023Ð0028$04.00/0 䉷 2012 Entomological Society of America
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KEY WORDS Siphonaptera, Tungidae, Tunga bossii sp. nov., sand ßea, neosome
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neosomes were removed from its tail base and Þxed in 70% ethanol. After identiÞcation the host specimen was released at the same trap site. The neosomes subsequently were sent to the Department of Parasitology of the Federal University of Minas Gerais, where they were measured and dissected. Only the head, thorax, spermatheca, and caudal disk of one of the neosomes was recovered (in the second neosome these structures already were deteriorated by dying of the ßea), diaphanized in 10% cold potash, dehydrated in an ethanol series, clariÞed in creosote, and mounted on slides in Canada balsam (Linardi and Guimara˜ es 2000). Morphometric parameters were measured using an Olympus binocular microscope (Japan) Þtted with ocular and stages micrometers. Except for the neosome, all measurements are in micrometers, including the units cited in parentheses. Morphologic comparisons were performed with species deposited in collections from the Zoology Museum of the University of Sa˜ o Paulo and the Department of Parasitology of the Federal University of Minas Gerais, Brazil. A female holotype was deposited in the Collection of Ectoparasites of the Department of Parasitology of the Federal University of Minas Gerais, Brazil.
Results Tunga bossii, sp. nov. (Figs. 1Ð 4) Hypertrophied Female. Globular neosome (9-mm length, 8-mm width, and 7-mm height) without lobes, located at the base of the tail of the host (Fig. 1A). Head and thorax completely invaginated within the abdomen. Caudal disk forming a circular opening of 2 mm (Fig. 1B). Anterior extremity of the neosome with a small, medially localized opening in the same position of the head (Fig. 1C). Head (Fig. 2): rounded dorsal margin with a slightly pronounced frontal tubercle and six small bristles in a slight depression, posterior to the frontal tubercle. Pre and postantennal regions with 10 bristles each not organized in welldeÞned rows. Preoral internal sclerotization similar to that of T. monositus, with the posterior arm (41.8 m) nearly two times longer than the anterior arm (22.1 m). Rounded ventral and dorsal genal lobes extending to the antennal fossa covering more than half of the segment II but not reaching the antennal segment III. Eye without black pigment and recess into its internal margin with the greatest diameter (36.9 m) exceeding half of its distance to the dorsal margin of the head (60 m). Antennal segment II with a single long bristle
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Fig. 1. T. bossii sp. nov., neosomes. A. Two neosomes located on the base of the tail of a specimen of D. dorsalis collected from Serra do Itatiaia, Rio de Janeiro, Brazil. Bar: 10 mm. B. Dorsal view of the neosome. Bar: 5 mm. C.) Ventral view of the neosome, where it is possible to visualize a small, medially located opening. Bar: 2 mm.
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AVELAR ET AL.: T. bossii NEW SPECIES
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posterodorsally. Antennal clava with six antennomeres on its posterior margin (Fig. 3A). Laciniae strong, heavily serrated, and slightly exceeding the distal part of the anterior trochanter and exhibiting a total length of 233.7 m. Maxillary palps reaching the base of anterior trochanter and increasing in length in the following order: I ⬍ II ⬍ III ⬍ IV (Fig. 3B). Segment I is very small (9.8 by 12.3 m) when compared with the rest of the segments, which have the following length and width measurements: II: 49.2 by 17.2 m; III: 61.5 by 22.1 m; IV: 71.3 by 22.1 m. A complete division between the segments III and IV of maxillary palp was not observed in the specimen studied. Base of the maxilla anteriorly with two bristles. Thorax: Pronotum and mesonotum not completely fused dorsally, each with two bristles on their ventral halves. Proepimeron with a small and rounded posterodorsal lobe (Fig. 2). Legs: Mesocoxa with a complete oblique external break. Metacoxa with an anterodistal angle projecting down like a wide tooth (Fig. 2) and exhibiting on its median surface, two irregular rows with 15 bristles in total near to the anterior margin. Other two apical bristles, four submarginals, and three tiny submarginals located posteroproximally. As is often the case in gravid females of Tunga, the other segments of the legs are not found. Spermatheca (Fig. 4A): Bulga approximately globular measuring 61.5 m long and 66.4 m wide. Hilla with length of 41.8 m and width
of 12.3 m. Caudal disk (Fig. 4B): Tergite VIII divided into two halves, each having one functional spiracle located dorsally in the spiracular fossa. Bristles only in the ventral region, being four each laterally on the internal surface. Segment X with eight trichobothria on each side and a plate projecting around the sensilium, exhibiting three robust bristles and two microbristles on the sides and two medium-length bristles. Another plate below with a row of four bristles. Type Material. HOLOTYPE: one female, BRAZIL: Serra do Itatiaia, RJ (22⬚ 26.187⬘ S, 44⬚ 37.511⬘ W), 17-XII-2000, on Delomys dorsalis, Leandro B. de Moraes. Etymology. The new species is named in honor of the late David Eduardo Paolinetti Bossi, a Brazilian entomologist. Discussion The pronotum of Tunga bossii is not completely fused with the mesonotum, which is a characteristic of the caecata group (Smit 1962). Tunga bossii can be differentiated from all other known species of Tunga by the size of the segment I of the maxillary palps, which is greatly reduced compared with other species (segment IV is at least seven times longer than segment I). In other Tunga species, the segment III is always the smallest segment. In addition, it is the
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Fig. 2. T. bossii sp. nov., female holotype. Bar: 120 m.
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only species that possesses two bristles at the base of the maxilla. Still, it differs from the other species of the “caecata” group by its eye morphology (the eyes are large and nonpigmented, whereas those of T. libis are pigmented, those of T. caecata and T. monositus are small, and T. caecigena and T. callida have no eyes) (Pinto and Dreyfus 1927, Wagner 1932, Jordan 1937, Hopkins and Rothschild 1953, Johnson 1957, Smit 1962, Linardi and Guimara˜ es 2000, Pampiglione et al. 2002). The majority of species belonging to the caecata group are parasites of the auricular region of rodents (except T. libis, which is not known to form a neosome and T. callida, parasitizing the rear end of the body) (Li and Chin 1957, Smit 1962, Barnes and Radovsky 1969). This is the Þrst time that a Tunga specimen has been found to parasitize the base of the tail of a sigmodontine rodent. This site of infestation in rodents also represents the Þrst record in the New World, up until now restricted to the external base of the ear pinna. Key for Adult Species and Neosomes of the Genus Tunga 1. Pronotum and mesonotum not completely fused dorsally (caecata group) . . . . . . . . . . . . . Pronotum and mesonotum fused dorsally (penetrans group) . . . . . . . . . . . . . . . . . . . . 2. Eye absent . . . . . . . . . . . . . . . . . . . . . . Eye present . . . . . . . . . . . . . . . . . . . . . 3. Occipital region with 8 Ð10 bristles. Preoral internal sclerotization with anterior arm extend-
2 7 3 4
ing to half the distance between frontal tubercle and base of maxillary palp. Lacinia as long as maxillary palp. Elliptical neosome, with dorsal and ventral portions of similar dilatation, measuring: 7Ð10-mm length, 5-mm width, and 6-mm height . . . . . . . . . . . . . . . . . . . . . . . . . T. caecigena Jordan and Rothschild, 1921 Occipital region with 3Ð5 bristles. Preoral internal sclerotization with anterior arm extending near to the base of maxillary palp. Lacinia longer than maxillary palp. Spherical neosome, with the dorsal portion more swelled than the ventral portion, measuring: 4.5-mm length, 4.5-mm width, and 4.5-mm height. . . . . . . . . . . . . . . . . . . . . T. callida Li & Chin, 1957 4. Eye pigmented. Gravid female unknown. . . . . . . . . . . . . . . . . . . . . . . . . libis Smit, 1962 Eye without black pigment. Gravid female with diverse forms . . . . . . . . . . . . . . . . . . . . 5 5. Posterodorsal lobe of proepimeron large, strongly projecting. Base of maxilla with no bristles. Lacinia as long as maxillary palp. Gravid female with eight lobes, arranged as four large outer lobes and four small inner lobes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . T. monositus Barnes & Radovsky, 1969 Posterodorsal lobe of proepimeron small, rounded. Base of maxilla with one or two bristles. Lacinia longer than maxillary palp. Gravid female globular . . . . . . . . . . . . . . . . . . . 6 6. Preoral internal sclerotization with posterior arm more than eight times the length of anterior arm. Segment III is the smallest among the four
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Fig. 3. T. bossii sp. nov., female holotype. A. Maxillary palp. Bar: 72 m. B. Antenna. Bar: 25 m. C. Posterodorsal lobe of proepimeron. Bar: 50 m.
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Downloaded from http://jme.oxfordjournals.org/ by guest on January 16, 2017 Fig. 4. T. bossii sp. nov., female holotype. A. Spermatheca. Bar: 32 m. B) Neosome: central region of the caudal disk. Bar: 190 m.
segments of maxillary palp. Segment IV of the maxillary palp about twice length of segment I. Spermatheca with the bulga longer than wide and hilla two times longer than wide. Neosome with length, width, and height measuring 7 ⫻ 6 ⫻ 6 mm . . . . . . . . . . . . . . . . . . . . . . . . . . . T. caecata (Enderlein, 1901) Preoral internal sclerotization with posterior arm less than four times the length of anterior arm. Segment I is the smallest among the four segments of maxillary palp. Segment IV of the maxillary palp as long as segment III. Spermatheca with the bulga wider than long and
hilla about four times longer than wide. Neosome with length, width, and height measuring 9 ⫻ 8 ⫻ 7 mm . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . T. bossii sp. nov. 7. Eye without black pigment. Base of maxilla with only a micro-bristle. Neosome with head invaginated within abdomen, measuring: 12Ð13-mm length, 8-mm width, and 10-mm height . . . . . . . . . . . . . . . . . . . . . . . . . . T. travassosi Pinto and Dreyfus, 1927 Eye pigmented. Base of maxilla with two or more bristles. Neosome with head not invaginated within abdomen or laterally visible . . . . . . 8
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Acknowledgments The research forms part of the Ph.D. thesis of D.M.A. produced under the auspices of the Programa de Po´ s-graduac¸ a˜o em Parasitologia, Instituto de Cieˆ ncias Biolo´ gicas, Universidade Federal de Minas Gerais (UFMG), Brasil. We thank the Conselho Nacional de Desenvolvimento Cientõ´Þco e Tecnolo´ gico (CNPq) for research fellowships to P.M.L. and A.X.L.
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ciated with arthropod symbioses. J. Med. Entomol. 6: 487Ð 494. Barnes, A. M., and F. J. Radovsky. 1969. A new Tunga (Siphonaptera) from the Neartic region with description of all stages. J. Med. Entomol. 6: 19 Ð36. Bossi, D.E.P. 2003. Associac¸ o˜ es entre artro´ podes e pequenos mamõ´feros silvestres de treˆ s a´reas serranas do sudeste brasileiro. Tese de doutoramento, Universidade Estadual de Campinas, Campinas, Brasil. de Moraes, L. B., D.E.P. Bossi, and A. X. Linhares. 2003. Siphonaptera parasites of wild rodents and marsupials trapped in three mountain ranges of the Atlantic Forest in Southeastern Brazil. Mem. Inst. Oswaldo Cruz 98: 1071Ð1076. Eisele, M., J. Heukelbach, E. Van Marck, H. Melhorn, O. Meckes, S. Franck, and H. Feldmeier. 2003. Investigations on the biology, epidemiology, pathology and control of Tunga penetrans in Brazil. I. Natural history of tungiasis in man. Parasitol. Res. 90: 87Ð99. Hopkins, G.H.E., and M. Rothschild. 1953. An illustrated catalogue of the Rothschild collection of ßeas (Siphonaptera) in the British Museum (Natural History). vol. 1. British Museum (Natural History), London, United Kingdom. Johnson, P. T. 1957. A classiÞcation of Siphonaptera of South America with descriptions of new species. Mem. Entomol. Soc. Wash. 5: 1Ð298. Jordan, K. 1937. Two new ßeas from South America (Siphonaptera). Novit. Zool. 39: 305Ð310. Lavoipierre, M.M.J., F. J. Radovsky, and P. D. Budwiser. 1979. The feeding process of a tungid ßea, Tunga monositus (Siphonaptera: Tungidae), and its relationship to the host inßammatory and repair response. J. Med. Entomol. 15: 187Ð217. Lewis, R. E. 1998. Re´ sume´ of the Siphonaptera (Insecta) of the World. J. Med. Entomol. 35: 377Ð389. Li, K.-C., and T.-H. Chin. 1957. Tunga callida sp. nov., a new species of sandßea from Yunnan. Acta Entomol. Sin. 7: 113Ð120. Linardi, P. M., and L. R. Guimara˜ es. 2000. Sifona´pteros do Brasil. Museu de Zoologia USP/Fapesp, Sa˜o Paulo, Brasil. Pampiglione, S., M. Trentini, M. L. Fioravanti, G. Onore, and F. Rivasi. 2002. A new species of Tunga (Insecta, Siphonaptera) in Ecuador. Parassitologia 44: 127. Pampiglione, S., M. L. Fioravanti, A. Gustinelli, G. Onore, B. Mantovani, A. Luchetti, and M. Trentini. 2009. Sand ßea (Tunga spp.) infections in humans and domestic animals: state of the art. Med. Vet. Entomol. 23: 172Ð186. Pinto, C., and A. Dreyfus. 1927 Tunga travassosi n. sp., parasite de Tatusia novemcinctus do Brasil. Bol. Biol. 9: 174 Ð 178. Rothschild, M. 1992. Neosomy in ßeas, and the sessile lifestyle. J. Zool. Lond. 226: 613Ð 629. Smit, F.G.A.M. 1962. A new sand-ßea from Ecuador. Entomologist 95: 89 Ð93. Wagner, J. 1932. Tunga bondari, eine neue art der sandßo¨ he. Novit. Zool. 38: 248 Ð249. Wang, D.-C. 1976. The Chinese Tunga (Siphonaptera: Tungidae). Acta Entomol. Sin. 19: 117Ð118. Received 27 May 2011; accepted 12 October 2011.
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8. Eye small, its greatest diameter only slightly exceeding half the distance from eye to dorsal margin of head. Dorsal genal lobe covering part of antennal segment III. Spermatheca with bulga wider than long. Neosome measuring: 6-mm length, 6-mm width, and 5-mm height . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . T. bondari Wagner, 1932 Eye large, its greatest diameter nearly equal to the distance from eye to dorsal margin of head. Dorsal genal lobe not covering the antennal segment III. Spermatheca with bulga longer than wide . . . . . . . . . . . . . . . . . . . . . . . 9 9. Antennal segment II with only two bristles. Maxillary palp with few bristles. Hypertrophied female not globular and containing four prominent subcylindrical lobes, measuring: 10-mm length, 9-mm width, and 13-mm height . . . . . . . . . . . . . . . . . . . T. terasma Jordan, 1937 Antennal segment II with more than two bristles. Maxillary palp with numerous bristles. Hypertrophied female globular without lobes or exhibiting three anterior lobes . . . . . . . . . . 10 10. Anteromedial surface of posterior tibia with row of 9 Ð12 bristles. Anterior base of maxilla with 6 Ð7 bristles. Segment I of maxillary palp longer than segment II. Spermatheca with hilla 2.5 times longer than wide. Bulga nearly Þve times longer than hilla. Hypertrophied female with three lobes located anteriorly, measuring: 12-mm length, 5-mm width, and 5-mm height . . . . . . . . . . . . . . . . . . . . . . . . . T. trimamillata Pampiglione, Trentini, Fioravanti, Onore, and Rivasi, 2002 Anteromedial surface of posterior tibia without bristles. Anterior base of maxilla with three thick bristles. Segment II of maxillary palp longer than segment I. Spermatheca with hilla as long as wide. Bulga ⬇3.5 times longer than hilla. Globular hypertrophied female without projections or lobes, measuring: 6-mm length, 5-mm width, and 5-mm height. . . . . . . . . . . . . . . . T. penetrans (L., 1758)
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