Parasitol Res (2013) 112:3239–3242 DOI 10.1007/s00436-013-3501-5
ORIGINAL PAPER
Establishment of Tunga trimamillata (Siphonaptera: Tungidae) in Brazil Pedro Marcos Linardi & Daniel Moreira De Avelar & Elias Jorge Facury Filho
Received: 22 April 2013 / Accepted: 12 June 2013 / Published online: 25 June 2013 # Springer-Verlag Berlin Heidelberg 2013
Abstract Tunga trimamillata is a species of sand flea occurring in Ecuador and Peru parasitizing cattle, goat, sheep, swine, and man. This is the first report of this species in Brazil, having been found on the hooves of cows in Barretos, São Paulo State, and Felixlândia, Minas Gerais State, and previously misidentified as Tunga penetrans. A previous report concerning Hydrochoerus hydrochaeris from Rio Novo, Minas Gerais State, may also be attributed to that species of sand flea, a possible the primary host. Given the large geographical distribution of T. trimamillata, the vast cattle population in Brazil, and the high number of individuals subject to the risk of tungiasis, the number of cases attributed to this sand flea will most likely increase over time.
Introduction Currently, the genus Tunga Jarocki, 1838 encompasses 13 species of sand fleas (De Avelar et al. 2013), of which Tunga penetrans (L., 1758) is the most reported species and has been found parasitizing 27 different genera of wild and domestic hosts (De Avelar 2010) in the Neotropical region and subSaharan Africa (Lewis 1998). Another ten species have been associated primarily with wild mammals, including rodents in the New World tropics, China, and Japan (Beaucournu et al. P. M. Linardi (*) : D. M. De Avelar Departamento de Parasitologia, Instituto de Ciências Biológicas da Universidade Federal de Minas Gerais, Caixa Postal 486, Avenida Antônio Carlos, 6627, Campus UFMG, Belo Horizonte, Minas Gerais 31270-901, Brazil e-mail:
[email protected] D. M. De Avelar Laboratório de Pesquisas Clínicas, Centro de Pesquisas René Rachou, Fundação Oswaldo Cruz, Belo Horizonte, Minas Gerais, Brazil E. J. Facury Filho Escola de Veterinária, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil
2012; De Avelar et al. 2013; Lewis 1998) and edentates in Brazil (Hopkins and Rothschild 1953; Lima and Hathaway 1946; Linardi and Guimarães 2000). Other two species, Tunga trimamillata, Pampiglione, Trentini, Fioravanti, Onore and Rivasi, 2002 and Tunga hexalobulata, have been exclusively detected on domestic animals. Although T. hexalobulata was described infesting a Brahman cow from a farm in the municipality of Funilândia, Minas Gerais State, Brazil, T. trimamillata has been recorded in Ecuador and Peru (Fioravanti et al. 2006) parasitizing cattle, goat, sheep, swine, and man. The neosome is the most marked characteristic of the genus Tunga and also the most frequently observed form in hosts, causing serious ectoparasitosis and harmful infections. It is an enlarged structure of 5–13 mm in size, formed as a result of the hypertrophy of gravid females and the growth of new tissue, following the penetration and mating of adult females into the skin of their hosts (Audy et al. 1972; Rothschild 1992). Of the 13 species of the genus Tunga, only one species has not known neosome: Tunga libis Smit, 1962. On other hand, four species, respectively, Tunga travassosi (Pinto and Dreyfus, 1927); Tunga bondari Wagner, 1932; Tunga bossi De Avelar, Linhares and Linardi, 2012; and T. hexalobulata De Avelar et al. 2013 are known only by neosomes. After oviposition, the neosome involutes with the death of the parasite (Lavoipierre et al. 1979) being absorbed or sloughed from the host epidermis by tissue repair mechanisms (Eisele et al. 2003; Lavoipierre et al. 1979), making the specific identification more difficult because some characteristics cannot be seen in the most dissected specimens. However, in spite of the morphological difficulties for differentiation of sand fleas, De Avelar et al. (2012) recently presented a key for identification of adult species and neosomes. Although the potential for vast numbers of hosts exists, with new records on wild animals in Brazil (Frank et al. 2012; Widmer and Azevedo 2012), the pig has been considered the most important animal reservoir for T. penetrans (Pampiglione et al. 1998; Ugbomoiko et al. 2008). To date, T. penetrans and T. trimamillata are the only species of sand fleas known to
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Table 1 Some differential characteristics between females of T. penetrans and T. trimamillata Characteristics
T. penetrans
T. trimamillata
Neosome: shape
Globular without humps 6×5×5
Conical with three anterior humps 12×5×5
II > I > IV > III
I > II > IV > III
217.5×62.5
295.2×59.0
142.5×32.5
201.7×22.1
Neosome: size length/ width/height (mm) Maxillary palps: decreasing order of segments Spermathecae: length bulga/hilla (μm) Spermathecae: width bulga/hilla (μm)
infest humans (Pampiglione et al. 2004, 2009). According to Fioravanti et al. (2006), the inhabitants of the Andean region are able to differentiate the clinical types of tungiasis that affect humans: one is less bothersome and is caused by small sand fleas found on swine (T. penetrans, “niguas de cerro”), whereas the other is more painful and is attributed to the larger sand fleas that infest cattle (T. trimamillata, “niguas de cerro”). Because these species parasitize both domestic animals and man, previous misidentifications may have occurred prior to the description of T. trimamillata and because this identification is not always performed by experts and is based on the sole criterion of penetrating fleas. In fact, some occurrences of T. penetrans on certain hosts, such as bats and birds, are likely incorrect records and may instead be attributed to Hectopsylla Frauenfeld, 1860. Thus, given the epidemiological and economic importance of these fleas, accurate species identification is indispensable.
Materials and methods Data and illustrations previously considered representative of T. penetrans (Vaz and Rocha 1946; Ribeiro et al. 2007) or Tunga
Fig. 1 Spermathecae: a T. penetrans; b T. trimamillata
Fig. 2 Gravid female (neosome) of T. trimamillata being withdrawn from the hoof of a cow
sp. (Rodrigues and Daemon unpublished work) were reexamined and morphologically compared to those of T. trimamillata.
Results These two species could be distinguished according to the shape and size of the neosomes, the length of the maxillary palps and segments, and the shape and size of the spermathecae after dissection (Table 1, Fig. 1). As seen in Figs. 2 and 3, the neosomes on the hooves of one F1 Holstein-Zebu cow document the presence of T. trimamillata, which had been previously attributed to T. penetrans, in the municipality of Felixlândia, Minas Gerais State, Brazil, in July 2004. Specimens collected from the hooves of cattle from Barretos, São Paulo State, Brazil, showed that the first segment of the maxillary palps was longer than the others. Although Vaz and Rocha (1946) considered these specimens to be T. penetrans, they were in fact identified as T. trimamillata. Similarly, the specimens obtained by Rodrigues and Daemon (unpublished work) from the capybara Hydrochoerus hydrochaeris in the municipally of Rio Novo, Minas Gerais
Fig. 3 Shape and size of the neosome of T. trimamillata
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State, were also shown to be T. trimamillata. This reclassification was based on the presence of three prominent lobes in the neosomes. However, because the laciniae were two times longer than the maxillary palps, this identification could not be confirmed.
Discussion The present report confirms the establishment of T. trimamillata in Brazil because this sand flea was collected in localities separated up to 580 km in different states. Furthermore, one of these records was made approximately 60 years ago, prior to the description of this species. In addition to the misidentifications of T. penetrans, molecular biological studies have revealed a high level of variation in the hypervariable section of 16S rDNA among isolates of this species, collected from man, dogs, cats, rats, and pigs in Northeast Brazil (Vobis et al. 2005). Consequently, T. penetrans would probably be a complex with closely related species. Nagy et al. (2007) also observed a slight morphological variation among samples of T. penetrans collected from different hosts in Fortaleza, Brazil, indicating the existence of different strains or races or the beginning of such a formation. Barnes and Radovsky (1969) stressed that the center of the distribution of the genus Tunga was within the Neotropical region. Indeed, tungiasis caused by T. penetrans is probably one of the oldest plagues of the American continent (Feldmeier et al. 2004). Although T. penetrans has originated in South America, it is now also endemic of sub-Saharan Africa due to a recent accidental introduction. Using mitochondrial marker, Luchetti et al. (2007) observed that the haplotype distribution was in agreement with a recent colonization of Africa and with a rapid spreading across this continent. Also, isolates from Africa and South America indicated a recent separation of both populations when studying by nucleotide sequence differences (Gamerschlag et al. 2008). Notably, the Neotropical region contains a diversity of biomes and at least 40 dispersion centers, 13 of which are located in Brazil (Müller 1972). Furthermore, Brazil is considered a hotspot of global biodiversity (Mittermeier et al. 1998; Myers et al. 2000) and occupies a vast area. Among the 13 species of Tunga, eight occur in Brazil, and six of these demonstrate endemicity. In addition, although initially described in Ecuador, T. trimamillata likely originated in Brazil. Based on morphology and host affinities, Smit (1962) divided Tunga into two species groups: penetrans and caecata. Both T. penetrans and T. trimamillata are included in the penetrans group, but T. penetrans is associated primarily with edentates, in spite of its preference by domestic animals and man. For this reason, it is possible that H. hydrochaeris be a primary, rather than a secondary host for T. trimamillata.
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Finally, given the vast cattle population in Brazil, with more than 212 million heads (IBGE 2011), the number of cases attributed to this tungiasis by T. trimamillata will most likely increase over time. Being T. penetrans and T. trimamillata the species of sand fleas that present the largest geographical extension and number of hosts, it is important to stress that the dispersion must be guaranteed thanks to the man or domestic animals, since that they live in stables and stock farms, as well in soil and dust close to farms. According to Pampiglione et al. (2009), T. trimamillata has been found on pigs less frequently than on ruminants and always as a co-infestation with T. penetrans. Moreover, regarding cases of human infestation, it remains to be determined whether diagnoses of T. penetrans may represent an underestimation of the true level of T. trimamillata infestation, considering that in Brazil more than 106 individuals are at risk for severe tungiasis (Heukelbach et al. 2001). Acknowledgments The authors wish to thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico for the research fellowship granted to P.M.L. The research forms part of the PhD thesis of D.M.A. in Parasitology/Post-graduate program in Parasitology/Instituto de Ciências Biológicas/Universidade Federal de Minas Gerais/UFMG.
References Audy JR, Radovsky FJ, Vercammen-Grandjean PH (1972) Neosomy: radical intrastadial metamorphosis associated with arthropod symbioses. J Med Entomol 6:487–494 Barnes AM, Radovsky FJ (1969) A new Tunga (Siphonaptera) from the Neartic region with description of all stages. J Med Entomol 6:19– 36 Beaucournu JC, Mergey T, Muñoz-Leal S, González-Acuña D (2012) Description de Tunga bonneti n. sp. du Chili (Siphonaptera– Tungidae) et notes sur su spécificité, as chorologie, son dermecos et as phénologie. Parasite 19:207–216 De Avelar DM (2010) Sistemática e análise cladística das espécies neotropicais do gênero Tunga Jarocki, 1838 (Siphonaptera: Tungidae). PH thesis, Federal University of Minas Gerais, Belo Horizonte, Brasil De Avelar DM, Facury Filho EJ, Linardi PM (2013) A new species of Tunga (Siphonaptera: Tungidae) parasitizing cattle from Brazil. J Med Entomol. (in press) De Avelar DM, Linhares AX, Linardi PM (2012) A new species of Tunga (Siphonaptera: Tungidae) from Brazil with a key to the adult species and neosomes Eisele M, Heukelbach J, Van Marck E, Mehlhorn H, Meckes O, Franck S, Feldmeier H (2003) Investigations on the biology, epidemiology, pathology and control of Tunga penetrans in Brazil. 1. Natural history of tungiasis in man. Parasitol Res 90:87–99 Feldmeier H, Eisele M, Van Marck E, Mehlhorn H, Ribeiro R, Heukelbach J (2004) Investigations on the biology, epidemiology, pathology and control of Tunga penetrans in Brazil: IV. Clinical and histopathology. Parasitol Res 94:275–282 Fioravanti ML, Gustinelli A, Onore G, Pampiglione S, Trentini M (2006) Presence of Tunga trimamillata (Insecta, Siphonaptera) in Peru. Parasite 13:85–86 Frank R, Melaun C, Martins MM, Santos ALQ, Heukelbach J, Klimpel S (2012) Tunga penetrans and further parasites in the giant
3242 anteater (Myrmecophaga tridactyla) from Minas Gerais, Brazil. Parasitol Res 11:1907–1912 Gamerschlag S, Mehlhorn H, Heukelbach J, Feldmeier H, D’Haese J (2008) Repetitive sequences in the ITS1 region of the ribosomal DNA of Tunga penetrans and other flea species (Insecta, Siphonaptera). Parasitol Res 102:193–199 Heukelbach J, Oliveira FAS, Hesse G, Feldmeier H (2001) Tungiasis: a neglected health problem of poor communities. Trop Med Int Health 6:267–272 Hopkins GHE, Rothschild M (1953) An illustrated catalogue of the Rothschild collection of fleas (Siphonaptera) in the British Museum (Natural History), vol 1. British Museum (Natural History), London IBGE, Instituto Brasileiro de Geografia e Estatística (2011) Produção da Pecuária Municipal 39:1–63 http://www.ibge.gov.br/home/estatistica/ economia/ppm/2011/default.shtm. Accessed 20 April 2013 Lavoipierre MMJ, Radovsky FJ, Budwiser PD (1979) The feeding process of a tungid flea, Tunga monositus (Siphonaptera: Tungidae), and its relationship to the host inflammatory and repair response. J Med Entomol 15:187–217 Lewis RE (1998) Résumé of the Siphonaptera (Insecta) of the world. J Med Entomol 35:377–389 Lima AC, Hathaway CR (1946) Pulgas. Bibliografia, catálogo e hospedadores. Instituto Oswaldo Cruz, Rio de Janeiro, Brasil Linardi PM, Guimarães LR (2000) Sifonápteros do Brasil. Museu de Zoologia USP/FAPESP, São Paulo, Brasil Luchetti A, Trentini M, Pampiglione S, Fioravanti ML, Mantovani B (2007) Genetic variability of Tunga penetrans (Siphonaptera, Tungidae) sand fleas across South America and Africa. Parasitol Res 100:593–598 Mittermeier RA, Myers N, Thomsen JB, Da Fonseca GAB, Olivieri S (1998) Biodiversity hotspots and major tropical wilderness areas: approaches to setting conservation priorities. Conserv Biol 12:516–520 Müller P (1972) Centres of dispersal and evolution in the Neotropical region. Stud Neotrop Fauna Environ 7:173–185 Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858
Parasitol Res (2013) 112:3239–3242 Nagy N, Abari E, D’Haese J, Calheiros C, Heukelbach J, Mencke N, Feldmeier H, Mehlhorn H (2007) Investigations on the life cycle and morphology of Tunga penetrans in Brazil. Parasitol Res 101(Suppl 2):S233–S242 Pampiglione S, Trentini M, Mattei Gentili F, Mendes JLX, Pampiglione C, Rivasi F (1998) Tunga penetrans (Insecta: Siphonaptera) in pigs in São Tomé (Equatorial Africa): epidemiological, clinical, morphological and histopathological aspects. Rev Elev Med Vet Pays Trop 51:201–205 Pampiglione S, Trentini M, Fioravanti ML, Gustinelli A (2004) Differential diagnosis between Tunga penetrans (L., 1758) and T. trimamillata Pampiglione et al., 2002 (Insecta, Siphonaptera), the two species of the genus Tunga parasitic in man. Parasite 11:51–57 Pampiglione S, Fioravanti ML, Gustinelli A, Onore G, Mantovani B, Luchetti A, Trentini M (2009) Sand flea (Tunga spp.) infections in humans and domestic animals: state of the art. Med Vet Entomol 23:172–186 Ribeiro JCVC, Coelho SC, Ruas JRM, Lana AMQ, Carvalho AU, Facury Filho EJ, Saturnino HM, Reis RB (2007) Infestação de Tunga penetrans Siphonaptera: Tungidae em cascos de vacas leiteiras F1 Holandês-Zebu. Arq Bras Med Vet Zootec 59:520–522 Rothschild M (1992) Neosomy in fleas, and the sessile life-style. J Zool (Lond) 226:613–629 Smit FGAM (1962) A new sand-flea from Ecuador. Entomologist 95:89–93 Ugbomoiko S, Ariza L, Heukelbach J (2008) Pigs are the most important animal reservoir for Tunga penetrans (jigger flea) in rural Nigeria. Trop Doct 38:226–227 Vaz Z, Rocha UF (1946) Tunga penetrans (L., 1758), “bicho de pé” em gado bovino. Livro de homenagem a R.F. Almeida, 40:327–332 Vobis M, D’Haese J, Mehlhorn H, Heukelbach J, Mencke N, Feldmeier H (2005) Molecular biological investigations of Brazilian Tunga sp. isolates from man, dogs, cats, pigs and rats. Parasitol Res 96:107–112 Widmer CE, Azevedo FCC (2012) Tungiasis in a free-ranging jaguar (Panthera onca) population in Brazil. Parasitol Res 110:1311–1314
