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Metacercariae of Eumegacetes medioximus (Digenea: Eumegacetidae) in larvae of Odonata from Brazil

Metacercárias de Eumegacetes medioximus (Digenea: Eumegacetidae) em larvas de Odonata no Brasil

Abstracts

During studies on the participation of larval Odonata in the life cycle of trematodes carried out at the Pampulha reservoir, Belo Horizonte, State of Minas Gerais, Brazil, between May and September 2011, dragonfly larvae, Orthemis discolor (Burmeister, 1839) and Perithemis mooma Kirby, 1889, were found harboring metacercariae identified as Eumegacetes medioximusBraun, 1901BRAUN, M.V. 1901. Zur Kenntnis der Trematoden der Saugethiere. Zool. Jb. Abt. Syst. 14:311-348.. This is the first report and morphological description of metacercariae of E. medioximus in the Neotropical region.

trematodes; insects; dragonfly; parasites


Durante estudos sobre a participação de larvas de Odonata no ciclo biológico de trematódeos realizados na represa da Pampulha, Belo Horizonte, Minas Gerais, Brasil, entre maio e setembro de 2011, larvas de libélulas, Orthemis discolor (Burmeister, 1839) e Perithemis mooma Kirby, 1889, foram encontradas apresentando metacercárias identificadas como Eumegacetes medioximusBraun, 1901BRAUN, M.V. 1901. Zur Kenntnis der Trematoden der Saugethiere. Zool. Jb. Abt. Syst. 14:311-348.. Este é o primeiro relato e caracterização morfológica de metacercárias de E. medioximus para a região neotropical.

trematódeos; insetos; libélula; parasitos


Introduction

The involvement of insects belonging to the order Odonata Fabricius, 1793 in the life cycle of digeneans has been known since the beginning of the twentieth century (Sinitsin 1905SINITSIN, D.T. 1905. Data on the natural history of trematodes. Distomes of fishes and frogs in the vicinity of Warsaw. Warsaw University, Warsaw.). Several digenean that parasitize birds and amphibians, such as the species of Eumegacetes Looss, 1900 (Eumegacetidae), Gorgoderina Looss, 1902 (Gorgoderidae), Haematoloechus Looss, 1899 (Plagiorchiidae), Halipegus Looss, 1899 (Derogenidae), and Prosthogonimus Lühe, 1899 (Prosthogonimidae), have been reported parasitizing dragonfly larvae as second intermediate or paratenic hosts in North America, Europe and Asia (Stafford 1931STAFFORD, E.W. 1931. Platyhelmia in aquatic insects and Crustacea. J. Parasitol. 18:131., Boddeke 1960BODDEKE, R. 1960. The life history of Prosthogonimus ovatus. II. The intermediate hosts. Trop. Geogr. Med. 12(4):363-377., Hall 1960HALL, J.E. 1960. Some lecithodendriid metacercariae from Indiana and Michigan. J. Parasitol. 46(3):309-314. http://dx.doi.org/10.2307/3275492
http://dx.doi.org/10.2307/3275492...
, Snyder & Janovy Jr 1994SNYDER, S.D. & JANOVY JR, J. 1994. Second intermediate host-specificity of Haematoloechus complexus and Haematoloechus medioplexus (Digenea: Haematoloechidae). J. Parasitol. 80(6):1052-1055. http://dx.doi.org/10.2307/3283461
http://dx.doi.org/10.2307/3283461...
, Kumari & Madhavi 1994KUMARI, V.G.M.S. & MADHAVI, R. 1994. The life cycle of Eumegacetes artamii Mehra, 1935 (Trematoda, Eumegacetidae). Acta Parasitol. 39(1):9-12., Zelmer & Esch 1998ZELMER, D.A. & ESCH, G.W. 1998. Bridging the gap: the odonate naiad as a paratenic host for Halipegus occidualis (Trematoda: Hemiuridae). J. Parasitol 84(1):94-96. http://dx.doi.org/10.2307/3284536
http://dx.doi.org/10.2307/3284536...
, Bolek & Janovy Jr 2007BOLEK, M.G. & JANOVY JR, J. 2007. Evolutionary avenues for, and constraints on, the transmission of frog lung flukes (Haematoloechus spp.) in dragonfly second intermediate hosts. J. Parasitol. 93(3):593-607. PMid:17626352. http://dx.doi.org/10.1645/GE-1011R.1
http://dx.doi.org/10.1645/GE-1011R.1...
, Bolek et al. 2010BOLEK, M.G., TRACY, H.R. & JANOVY JR, J. 2010. The role of damselflies (Odonata: Zygoptera) as paratenic hosts in the transmission of Halipegus eccentricus (Digenea: Hemiuridae) to anurans. J. Parasitol. 96(4):724-735. PMid:20738199. http://dx.doi.org/10.1645/GE-2365.1
http://dx.doi.org/10.1645/GE-2365.1...
). Although several species of these helminths have been recorded as adult parasites in vertebrate hosts from Brazil (Travassos et al. 1969TRAVASSOS, L., FREITAS J.F.T. & KOHN, A. 1969. Trematódeos do Brasil. Mem. Inst. Oswaldo Cruz 67:1-886. PMid:5397756.), there are no reports of natural infection of larval dragonflies by digeneans in this country.

In the present study the natural infection of larval dragonflies with metacercariae identified as Eumegacetes medioximusBraun, 1901BRAUN, M.V. 1901. Zur Kenntnis der Trematoden der Saugethiere. Zool. Jb. Abt. Syst. 14:311-348. is reported for the first time in the Neotropical region.

Material and Methods

During malacological surveys conducted at the Pampulha reservoir (43° 59′ 35″ W and 19° 50′ 50″ S), Belo Horizonte, Minas Gerais, Brazil, between May and September 2011, naiads of Odonata belonging to the suborder Anisoptera were collected using a hand net and transported alive to the laboratory.

After morphological identification in accordance with Santos (1973)SANTOS, N.D. 1973. Contribuição ao conhecimento da fauna do Estado da Guanabara e arredores. 84 - Descrição da ninfa de Perithemis mooma Kirby, 1889 (Odonata: Libellulidae). Atas Soc. Biol. Rio de Janeiro 16:71-72., Costa et al. (2004)COSTA, J.M., SOUZA, L.O.I. & OLDRINI, B.B. 2004. Chave de identificação das famílias e gêneros das larvas conhecidas de Odonata do Brasil: comentários e registros bibliográficos (Insecta, Odonata). Pub. Avul. Mus. Nac. 99:1-44. and Costa & Santos (2009)COSTA, J.M. & SANTOS, T.C. 2009. Description of the larva of Orthemis schmidti (Odonata, Libellulidae). Iheringia, Sér. Zool. 99(2):129-131., the odonate naiads were teased apart using dissecting needles and examined for parasites under a stereomicroscope. The cysts recovered were initially studied in temporary mounts using light microscope. The metacercariae were mechanically excysted using metal needles, slightly pressed between glass slides, fixed in formalin at 70 °C, stained with alum acetocarmine, dehydrated in an ascending series of alcohol, cleared in beechwood creosote and mounted in Canada balsam.

Photographs were obtained using a Leica ICC50 HD digital camera attached to a light microscope and measurements were obtained by analyzing the captured images using the Leica Application Suite (LAZ EZ) software, version 2.0. A drawing was made with aid of a camera lucida. The parasite was identified based on taxonomic keys and descriptions according Travassos et al. (1969)TRAVASSOS, L., FREITAS J.F.T. & KOHN, A. 1969. Trematódeos do Brasil. Mem. Inst. Oswaldo Cruz 67:1-886. PMid:5397756. and Lotz & Font (2008)LOTZ, J.M. & FONT, W.F. 2008. Family Eumegacetidae Travassos, 1922. In Keys to the Trematoda, Volume 3. (R.A Bray, D.I. Gibson & A. Jones, eds.). CAB International and Natural History Museum, London, p.501-504.. Measurements are presented in micrometers. Specimens studied were deposited in the collection of the Invertebrate Taxonomy and Biology Laboratory (DPIC), Instituto de Ciências Biológicas, UFMG, Brazil.

Results and Discussion

Odonate naiads, identified as Orthemis discolor (Burmeister) and Perithemis mooma Kirby (Anisoptera: Libellulidae), had metacercariae in the abdominal cavity. Six similar cysts were found in the content of the proventriculus of a specimen of Striated Heron, Butorides striata (Linnaeus), found dead in the same locality. After morphological analysis and morphometry, the parasite was identified as belonging to the family Eumegacetidae Travassos, 1922 and the species characterized below.

Eumegacetes medioximusBraun, 1901BRAUN, M.V. 1901. Zur Kenntnis der Trematoden der Saugethiere. Zool. Jb. Abt. Syst. 14:311-348. (Figure 1 and 2)

Figure 1.
Metacercaria of Eumegacetes medioximus found in naiads of Odonata collected at the Pampulha reservoir, Belo Horizonte, Minas Gerais, Brazil. (a) Encysted. (b) Excysted. Unstained wet mount.

Figure 2.
Line drawing of excysted metacercaria of Eumegacetes medioximus found in naiads of Odonata collected at the Pampulha reservoir, Belo Horizonte, Minas Gerais, Brazil.

Synonyms: Eumegacetes perodiosus Travassos, 1922.

Stage: Metacercaria.

Hosts: Orthemis discolor (Burmeister, 1839) and Perithemis mooma Kirby, 1889.

Site of infection: Hemocoel.

Locality: Pampulha reservoir, Belo Horizonte, State of Minas Gerais, Brazil.

Description: Cysts oval to spherical 1254 (1117-1375) in length by 1080 (840-1375) in width. Cystic membrane transparent measuring 45 (34-60) in thickness. Excysted metacercariae oval 1953 (1812-2137) in length by 1224 (937-1428) in width. Oral sucker subterminal, 529 (363-643) in length by 530 (362-643) in width. Ventral sucker equatorial, 353 (286-432) in length by 407 (296-590) in width. Oral sucker width to ventral sucker width ratio 1.52 (1.27-2.11). Prepharynx short. Pharynx muscular, 203 (142-226) in length by 242 (157-302) in width. Esophagus short. Intestinal caeca extending to the posterior portion of the body. Two testes spherical, opposite, pre-acetabular, intercaecal. Right testis 263 (154-326) in length by 237 (142-314) in width. Left testis 234 (142-307) in length by 233 (135-289) in width. Ovary round, post-acetabular, median, 176 (111-227) in length by 172 (110-204) in width. Vitellaria follicular, extracaecal, in two fields lateral, extending from posterior margin of testes to posterior extremity of body. Uterine primordium inconspicuous, seen only in the anterior region of ovary. Cirrus pouch oval to elongated, median, located in the anterior portion of body, 152 (144-177) in length by 84 (75-95) in width. Genital pore median, bifurcal. Excretory vesicle V- shaped, with arms reaching the level of the anterior region of body, presenting lateral diverticula and filled with dark granules. Excretory pore terminal.

Specimens deposited: DPIC 6220-6222

Remarks: Eumegacetes medioximus was described by Braun (1901)BRAUN, M.V. 1901. Zur Kenntnis der Trematoden der Saugethiere. Zool. Jb. Abt. Syst. 14:311-348. from material collected by Johann Natterer from the Great Jacamar, Galbula grandis Latham (Galbulidae), in Brazil in the mid-nineteenth century. It was subsequently recorded in several species of birds in the States of Mato Grosso do Sul and Rio de Janeiro in Brazil (Travassos 1928TRAVASSOS, L. 1928. Fauna helmintológica do Mato Grosso (Trematódeos - 1ª parte). Mem. Inst. Oswaldo Cruz 21(2):309-341. http://dx.doi.org/10.1590/S0074-02761928000200002
http://dx.doi.org/10.1590/S0074-02761928...
, Travassos & Freitas 1940TRAVASSOS, L. & FREITAS, J.F.T. 1940. Relatório da excursão científica realizada na zona da Estrada de Ferro Noroeste do Brasil em julho de 1939. Mem. Inst. Oswaldo Cruz 35(3):525-556. http://dx.doi.org/10.1590/S0074-02761940000300004
http://dx.doi.org/10.1590/S0074-02761940...
, Travassos et al. 1969TRAVASSOS, L., FREITAS J.F.T. & KOHN, A. 1969. Trematódeos do Brasil. Mem. Inst. Oswaldo Cruz 67:1-886. PMid:5397756., Brasil & Amato 1992), and in Venezuela (Lutz 1928LUTZ, A. 1928. Estudios sobre trematodes observados en Venezuela. In Estúdios de Zoologia y Parasitologia Venezolanas (A. Lutz). Rio de Janeiro, p.101-125., Caballero & Díaz-Ungría 1958CABALLERO, E.C. & DÍAZ-UNGRÍA, C. 1958. Intento de un catálogo de los tremátodos digéneos registrados en territorio venezolano. Mem. Soc. Cien. Nat. La Salle 18:19-36.). Except for the absence of eggs in the uterus, other morphological traits of the metacercariae studied in the present study are in accordance with reported by these authors. Recently, Eumegacetes sp. was found in sparrows, Passer domesticus (Linnaeus) (Passeridae), in the State of Rio Grande do Sul (Calegaro-Marques & Amato 2010CALEGARO-MARQUES, C. & AMATO, S.B. 2010. Helminths of introduced house sparrows (Passer domesticus) in Brazil: does population age affect parasite richness? Iheringia, Ser. Zool. 100(1):73-78. http://dx.doi.org/10.1590/S0073-47212010000100010
http://dx.doi.org/10.1590/S0073-47212010...
). Other developmental stages of E. medioximus were not previously known.

Members of Eumegacetidae are intestinal parasites of birds with worldwide distribution (Lotz & Font 2008LOTZ, J.M. & FONT, W.F. 2008. Family Eumegacetidae Travassos, 1922. In Keys to the Trematoda, Volume 3. (R.A Bray, D.I. Gibson & A. Jones, eds.). CAB International and Natural History Museum, London, p.501-504.). The life cycle is known for Eumegacetes artammi Mehra, 1935, and Orthetrotrema monostomum Macy and Basch, 1972, and includes a prosobranch mollusc, Melanoides tuberculata (Müller) (Thiaridae), as intermediate host; xiphidiocercariae belonging to the microcotylous group emerge from infected molluscs and penetrate odonate larvae, to form metacercariae, in the case of E artammi, or progenetic adults in O. monostomum (Kumari & Madhavi 1994KUMARI, V.G.M.S. & MADHAVI, R. 1994. The life cycle of Eumegacetes artamii Mehra, 1935 (Trematoda, Eumegacetidae). Acta Parasitol. 39(1):9-12., Madhavi & Swarnakumari 1995MADHAVI, R. & SWARNAKUMARI, V.G.M. 1995. The morphology, life-cycle and systematic position of Orthetrotrema monostomum Macy & Basch, 1972, a progenetic trematode. Syst. Parasitol. 32(3):225-232. http://dx.doi.org/10.1007/BF00008831
http://dx.doi.org/10.1007/BF00008831...
). Different species of dragonfly larvae have been reported harboring metacercariae of Eumegacetes in the United States of America (Stafford 1931STAFFORD, E.W. 1931. Platyhelmia in aquatic insects and Crustacea. J. Parasitol. 18:131., Hall 1960HALL, J.E. 1960. Some lecithodendriid metacercariae from Indiana and Michigan. J. Parasitol. 46(3):309-314. http://dx.doi.org/10.2307/3275492
http://dx.doi.org/10.2307/3275492...
) and India (Rao & Madhavi 1961RAO, K.H. & MADHAVI, R. 1961. Metacercaria of Eumegacetes sp. (Trematoda: Lecithodendriidae) in dragon-fly naiads from a stream at Waltair. Curr. Sci. 30(8):303-304., Singh & Pande 1968SINGH, P. & PANDE, B.P. 1968. Adult of Eumegacetes artamii from white leghorn pullets infected with the metacercariae from two dragonflies. Curr. Sci. 37(19):563-564., Prakash & Pande 1970PRAKASH, R. & PANDE, B.P. 1970. Libellulid dragonflies as second intermediate hosts of flukes. Indian J. Helminthol. 21(2):150-160., Kumari & Madhavi 1994KUMARI, V.G.M.S. & MADHAVI, R. 1994. The life cycle of Eumegacetes artamii Mehra, 1935 (Trematoda, Eumegacetidae). Acta Parasitol. 39(1):9-12.). The present study is the first report of metacercariae of Eumegacetes in larvae of Odonata in the Neotropics.

The first intermediate hosts of E. medioximus remain unknown. Recently, a small xiphidiocercariae with morphological characteristics consistent with cercariae of Eumegacetidae known have been found in Pomacea lineata (Spix) (Ampullariidae) at the Pampulha reservoir (HAP, unpublished data), however experimental or molecular evidences are still necessary to confirm that these cercariae are conspecific with E. medioximus. Although M. tuberculata is the only intermediate host of Eumegacetes known so far, larvae of these parasites have not yet been reported in this thiarids in the Neotropical region (Pinto & Melo 2011PINTO, H.A. & MELO, A.L. 2011. A checklist of trematodes (Platyhelminthes) transmitted by Melanoides tuberculata (Mollusca: Thiaridae). Zootaxa 2799:15-28.). Experimental infection studies are needed in order to elucidate the participation of these prosobranch molluscs in the transmission of E. medioximus.

Few studies have evaluated the involvement of aquatic insects in the biological cycle of digeneans in South America. Larvae of Odonata and Coleoptera have been found harboring metacercariae of Gorgoderina sp. and Rauschiella repandum (Rudolphi, 1819), respectively, in Venezuela (Lutz 1926LUTZ, A. 1926. Société de Biologie de Rio de Janeiro: Session de 15 de Septembre de 1926. Mem. Inst. Oswaldo Cruz 19(2):237-238. http://dx.doi.org/10.1590/S0074-02761926000200005
http://dx.doi.org/10.1590/S0074-02761926...
, 1928LUTZ, A. 1928. Estudios sobre trematodes observados en Venezuela. In Estúdios de Zoologia y Parasitologia Venezolanas (A. Lutz). Rio de Janeiro, p.101-125.). Natural infection with metacercariae of Stomylotrema vicariumBraun, 1901BRAUN, M.V. 1901. Zur Kenntnis der Trematoden der Saugethiere. Zool. Jb. Abt. Syst. 14:311-348. (Stomylotrematidae), in aquatic Coleoptera, Megadytes glauca Brullé (Dityscidae), and Heteroptera, Belostoma spp. (Belostomatidae), have been reported in Argentina and Brazil (Ostrowski de Núñez 1978OSTROWSKI DE NÚÑEZ, M. 1978. Zum Entwicklungszyklus von Stomylotrema vicarium. Angew. Parasitol. 19:208-213. PMid:736315., Digiani 2002DIGIANI, M.C. 2002. Belostomatidae (Insecta: Heteroptera) as intermediate hosts of digenetic trematodes. Comp. Parasitol. 69(1):89-92. http://dx.doi.org/10.1654/1525-2647(2002)069[0089:BIHAIH]2.0.CO;2
http://dx.doi.org/10.1654/1525-2647(2002...
, Amato & Amato 2006AMATO, S.B. & AMATO, J.F.R. 2006. Belostoma dilatatum (Dufour) (Hemiptera, Belostomatidae) hospedando metacercárias de Stomylotrema vicarium Braun (Digenea, Stomylotrematidae) na região Sul do Brasil. Rev. Bras. Zool. 23(1):307-310. http://dx.doi.org/10.1590/S0101-81752006000100028
http://dx.doi.org/10.1590/S0101-81752006...
).

Over the last decade, studying the biological interactions between insects and trematodes has become important, since metacercariae found in aquatic insects, including Odonata, have been found infected by Neorickettsia risticii (Holland et al. 1985) (Anaplasmataceae), the etiological agent for Potomac Horse Fever (Chae et al. 2000CHAE, J.S., PUSTERLA, N., JOHNSON, E., DEROCK, E., LAWLER, S.P. & MADIGAN, J.E. 2000. Infection of aquatic insects with trematode metacercariae carrying Ehrlichia risticii, the cause of Potomac horse fever. J. Med. Entomol. 37(4):619-625. PMid:10916305. http://dx.doi.org/10.1603/0022-2585-37.4.619
http://dx.doi.org/10.1603/0022-2585-37.4...
, Madigan et al. 2000MADIGAN, J.E., PUSTERLA, N., JOHNSON, E., CHAE, J.S., PUSTERLA, J.B., DEROCK, E. & LAWLER, S.P. 2000. Transmission of Ehrlichia risticii, the agent of Potomac horse fever, using naturally infected aquatic insects and helminth vectors: preliminary report. Equine Vet. J. 32(4):275-279. PMid:10952374. http://dx.doi.org/10.2746/042516400777032219
http://dx.doi.org/10.2746/04251640077703...
, Mott et al. 2002MOTT, J., MURAMATSU, Y., SEATON, E., MARTIN, C., REED, S. & RIKIHISA, Y. 2002. Molecular analysis of Neorickettsia risticii in adult aquatic insects in Pennsylvania, in horses infected by ingestion of insects, and isolated in cell culture. J. Clin. Microbiol. 40(2):690-693. PMid:11825999 PMCid:153368. http://dx.doi.org/10.1128/JCM.40.2.690-693.2002
http://dx.doi.org/10.1128/JCM.40.2.690-6...
, Gibson & Rikihisa 2008GIBSON, K.E. & RIKIHISA, Y. 2008. Molecular link of different stages of the trematode host of Neorickettsia risticii to Acanthatrium oregonense. Environ. Microbiol. 10(8):2064-2073. PMid:18422641. http://dx.doi.org/10.1111/j.1462-2920.2008.01625.x
http://dx.doi.org/10.1111/j.1462-2920.20...
).

Despite the diversity of species of trematodes found in Brazil, studies involving the possible role of insects in the transmission of these parasites are still needed.

References

  • AMATO, S.B. & AMATO, J.F.R. 2006. Belostoma dilatatum (Dufour) (Hemiptera, Belostomatidae) hospedando metacercárias de Stomylotrema vicarium Braun (Digenea, Stomylotrematidae) na região Sul do Brasil. Rev. Bras. Zool. 23(1):307-310. http://dx.doi.org/10.1590/S0101-81752006000100028
    » http://dx.doi.org/10.1590/S0101-81752006000100028
  • BRASIL, M.C. & AMATO S.B. 1992. Faunistic analysis of helminths of sparrows (Passer domesticus L., 1758) captured in Campo Grande, Rio de Janeiro, RJ. Mem. Inst. Oswaldo Cruz 87 (Suppl. I):43-48. http://dx.doi.org/10.1590/S0074-02761992000500009
    » http://dx.doi.org/10.1590/S0074-02761992000500009
  • BODDEKE, R. 1960. The life history of Prosthogonimus ovatus. II. The intermediate hosts. Trop. Geogr. Med. 12(4):363-377.
  • BOLEK, M.G. & JANOVY JR, J. 2007. Evolutionary avenues for, and constraints on, the transmission of frog lung flukes (Haematoloechus spp.) in dragonfly second intermediate hosts. J. Parasitol. 93(3):593-607. PMid:17626352. http://dx.doi.org/10.1645/GE-1011R.1
    » http://dx.doi.org/10.1645/GE-1011R.1
  • BOLEK, M.G., TRACY, H.R. & JANOVY JR, J. 2010. The role of damselflies (Odonata: Zygoptera) as paratenic hosts in the transmission of Halipegus eccentricus (Digenea: Hemiuridae) to anurans. J. Parasitol. 96(4):724-735. PMid:20738199. http://dx.doi.org/10.1645/GE-2365.1
    » http://dx.doi.org/10.1645/GE-2365.1
  • BRAUN, M.V. 1901. Zur Kenntnis der Trematoden der Saugethiere. Zool. Jb. Abt. Syst. 14:311-348.
  • CABALLERO, E.C. & DÍAZ-UNGRÍA, C. 1958. Intento de un catálogo de los tremátodos digéneos registrados en territorio venezolano. Mem. Soc. Cien. Nat. La Salle 18:19-36.
  • CALEGARO-MARQUES, C. & AMATO, S.B. 2010. Helminths of introduced house sparrows (Passer domesticus) in Brazil: does population age affect parasite richness? Iheringia, Ser. Zool. 100(1):73-78. http://dx.doi.org/10.1590/S0073-47212010000100010
    » http://dx.doi.org/10.1590/S0073-47212010000100010
  • CHAE, J.S., PUSTERLA, N., JOHNSON, E., DEROCK, E., LAWLER, S.P. & MADIGAN, J.E. 2000. Infection of aquatic insects with trematode metacercariae carrying Ehrlichia risticii, the cause of Potomac horse fever. J. Med. Entomol. 37(4):619-625. PMid:10916305. http://dx.doi.org/10.1603/0022-2585-37.4.619
    » http://dx.doi.org/10.1603/0022-2585-37.4.619
  • COSTA, J.M. & SANTOS, T.C. 2009. Description of the larva of Orthemis schmidti (Odonata, Libellulidae). Iheringia, Sér. Zool. 99(2):129-131.
  • COSTA, J.M., SOUZA, L.O.I. & OLDRINI, B.B. 2004. Chave de identificação das famílias e gêneros das larvas conhecidas de Odonata do Brasil: comentários e registros bibliográficos (Insecta, Odonata). Pub. Avul. Mus. Nac. 99:1-44.
  • DIGIANI, M.C. 2002. Belostomatidae (Insecta: Heteroptera) as intermediate hosts of digenetic trematodes. Comp. Parasitol. 69(1):89-92. http://dx.doi.org/10.1654/1525-2647(2002)069[0089:BIHAIH]2.0.CO;2
    » http://dx.doi.org/10.1654/1525-2647(2002)069[0089:BIHAIH]2.0.CO;2
  • GIBSON, K.E. & RIKIHISA, Y. 2008. Molecular link of different stages of the trematode host of Neorickettsia risticii to Acanthatrium oregonense. Environ. Microbiol. 10(8):2064-2073. PMid:18422641. http://dx.doi.org/10.1111/j.1462-2920.2008.01625.x
    » http://dx.doi.org/10.1111/j.1462-2920.2008.01625.x
  • HALL, J.E. 1960. Some lecithodendriid metacercariae from Indiana and Michigan. J. Parasitol. 46(3):309-314. http://dx.doi.org/10.2307/3275492
    » http://dx.doi.org/10.2307/3275492
  • KUMARI, V.G.M.S. & MADHAVI, R. 1994. The life cycle of Eumegacetes artamii Mehra, 1935 (Trematoda, Eumegacetidae). Acta Parasitol. 39(1):9-12.
  • LOTZ, J.M. & FONT, W.F. 2008. Family Eumegacetidae Travassos, 1922. In Keys to the Trematoda, Volume 3. (R.A Bray, D.I. Gibson & A. Jones, eds.). CAB International and Natural History Museum, London, p.501-504.
  • LUTZ, A. 1926. Société de Biologie de Rio de Janeiro: Session de 15 de Septembre de 1926. Mem. Inst. Oswaldo Cruz 19(2):237-238. http://dx.doi.org/10.1590/S0074-02761926000200005
    » http://dx.doi.org/10.1590/S0074-02761926000200005
  • LUTZ, A. 1928. Estudios sobre trematodes observados en Venezuela. In Estúdios de Zoologia y Parasitologia Venezolanas (A. Lutz). Rio de Janeiro, p.101-125.
  • MADHAVI, R. & SWARNAKUMARI, V.G.M. 1995. The morphology, life-cycle and systematic position of Orthetrotrema monostomum Macy & Basch, 1972, a progenetic trematode. Syst. Parasitol. 32(3):225-232. http://dx.doi.org/10.1007/BF00008831
    » http://dx.doi.org/10.1007/BF00008831
  • MADIGAN, J.E., PUSTERLA, N., JOHNSON, E., CHAE, J.S., PUSTERLA, J.B., DEROCK, E. & LAWLER, S.P. 2000. Transmission of Ehrlichia risticii, the agent of Potomac horse fever, using naturally infected aquatic insects and helminth vectors: preliminary report. Equine Vet. J. 32(4):275-279. PMid:10952374. http://dx.doi.org/10.2746/042516400777032219
    » http://dx.doi.org/10.2746/042516400777032219
  • MOTT, J., MURAMATSU, Y., SEATON, E., MARTIN, C., REED, S. & RIKIHISA, Y. 2002. Molecular analysis of Neorickettsia risticii in adult aquatic insects in Pennsylvania, in horses infected by ingestion of insects, and isolated in cell culture. J. Clin. Microbiol. 40(2):690-693. PMid:11825999 PMCid:153368. http://dx.doi.org/10.1128/JCM.40.2.690-693.2002
    » http://dx.doi.org/10.1128/JCM.40.2.690-693.2002
  • OSTROWSKI DE NÚÑEZ, M. 1978. Zum Entwicklungszyklus von Stomylotrema vicarium. Angew. Parasitol. 19:208-213. PMid:736315.
  • PINTO, H.A. & MELO, A.L. 2011. A checklist of trematodes (Platyhelminthes) transmitted by Melanoides tuberculata (Mollusca: Thiaridae). Zootaxa 2799:15-28.
  • PRAKASH, R. & PANDE, B.P. 1970. Libellulid dragonflies as second intermediate hosts of flukes. Indian J. Helminthol. 21(2):150-160.
  • RAO, K.H. & MADHAVI, R. 1961. Metacercaria of Eumegacetes sp. (Trematoda: Lecithodendriidae) in dragon-fly naiads from a stream at Waltair. Curr. Sci. 30(8):303-304.
  • SANTOS, N.D. 1973. Contribuição ao conhecimento da fauna do Estado da Guanabara e arredores. 84 - Descrição da ninfa de Perithemis mooma Kirby, 1889 (Odonata: Libellulidae). Atas Soc. Biol. Rio de Janeiro 16:71-72.
  • SINGH, P. & PANDE, B.P. 1968. Adult of Eumegacetes artamii from white leghorn pullets infected with the metacercariae from two dragonflies. Curr. Sci. 37(19):563-564.
  • SINITSIN, D.T. 1905. Data on the natural history of trematodes. Distomes of fishes and frogs in the vicinity of Warsaw. Warsaw University, Warsaw.
  • SNYDER, S.D. & JANOVY JR, J. 1994. Second intermediate host-specificity of Haematoloechus complexus and Haematoloechus medioplexus (Digenea: Haematoloechidae). J. Parasitol. 80(6):1052-1055. http://dx.doi.org/10.2307/3283461
    » http://dx.doi.org/10.2307/3283461
  • STAFFORD, E.W. 1931. Platyhelmia in aquatic insects and Crustacea. J. Parasitol. 18:131.
  • TRAVASSOS, L. 1928. Fauna helmintológica do Mato Grosso (Trematódeos - 1ª parte). Mem. Inst. Oswaldo Cruz 21(2):309-341. http://dx.doi.org/10.1590/S0074-02761928000200002
    » http://dx.doi.org/10.1590/S0074-02761928000200002
  • TRAVASSOS, L. & FREITAS, J.F.T. 1940. Relatório da excursão científica realizada na zona da Estrada de Ferro Noroeste do Brasil em julho de 1939. Mem. Inst. Oswaldo Cruz 35(3):525-556. http://dx.doi.org/10.1590/S0074-02761940000300004
    » http://dx.doi.org/10.1590/S0074-02761940000300004
  • TRAVASSOS, L., FREITAS J.F.T. & KOHN, A. 1969. Trematódeos do Brasil. Mem. Inst. Oswaldo Cruz 67:1-886. PMid:5397756.
  • ZELMER, D.A. & ESCH, G.W. 1998. Bridging the gap: the odonate naiad as a paratenic host for Halipegus occidualis (Trematoda: Hemiuridae). J. Parasitol 84(1):94-96. http://dx.doi.org/10.2307/3284536
    » http://dx.doi.org/10.2307/3284536

Publication Dates

  • Publication in this collection
    Apr-Jun 2013

History

  • Received
    6 Feb 2013
  • Reviewed
    9 Apr 2013
  • Accepted
    26 June 2013
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