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Home , Adelea, Adelina (Apicomplexa), Rio de Janeiro Metro, Thoropa lutzi, Thoropa miliaris

ISSN 2318-9673 r1.ufrrj.br/lcc/

Adelina sp. (: Adeleidae) , a pseudoparasite of miliaris Spix (Amphibia: ) in Southeastern

Bruno do Bomfim Lopes | Caroline Spitz dos Santos | Hermes Ribeiro Luz | Bruno Pereira Berto | Carlos Wilson Gomes Lopes

Submitted in 01.12.2013 Accepted in 11.12.2013

Abstract Lopes B doB, Santos CS, Luz HR, polysporocystic, . Berto BP, Lopes CWG. 2013. sp. (Apicomplexa: Adeleidae), a pseudopara- Resumo O hábito insetívoro de alguns verte- site of Thoropa miliaris Spix (Amphibia: brados é essencial para alguns coccídios de Cycloramphidae) in Southeastern Brazil. invertebrados, pois estes dependem dos hábi- [Adelina sp. (Apicomplexa: Adeleidae), um tos alimentares de vertebrados que predam pseudoparasita de Thoropa miliaris Spix invertebrados para garantir que serão disper- (Amphibia: Cycloramphidae) no Sudeste do sos. Este estudo relata a presença de oocistos Brasil] Coccidia 1, 26-31. Departamento de polisporocísticos de um adelídeo nas fezes de Biologia , Instituto de Biologia, Uni- Thoropa miliaris Spix na Ilha da Marambaia, versidade Federal Rural do . Estado do Rio de Janeiro, Brasil. Esta espécie BR-465 km 7, 23897-970 Seropédica, RJ, pertence ao gênero Adelina, a qual estava Brasil. E-mail: [email protected] parasitando um invertebrado ingerido por T. The insectivorous habit of some verte- miliaris. Os oocistos foram elipsoidais, 37,6 × brates is essential for the life cycle of some 31,4 µm, com parede lisa e dupla. Micrópila, coccidia of invertebrates because they depend resíduo e grânulo polar estavam ausentes. O of the feeding habits of vertebrates which número de esporocistos por oocisto variou de ingest invertebrate hosts to ensure that the adeleid oocysts will be dispersed. This study BB Lopes reports adeleid polysporocystic oocysts from Programa de Pós-Graduação em Ciência, Tecno- feces of the Thoropa miliaris Spix in logia e Inovação em Agropecuária, Universidade Marambaia Island, State of Rio de Janeiro, Federal Rural do Rio de Janeiro (UFRRJ). BR-465 Brazil. This sporulated oocysts belong to the km 7, 23897-970 Seropédica, RJ, Brasil. E-mail: [email protected] genus Adelina, which was parasitizing an invertebrate ingested by T. miliaris. The oo- CS Santos | HR Luz cysts were ellipsoidal, 37.6 × 31.4 µm, with a Curso de Pós-Graduação em Ciências Veteriná- smooth, bilayered wall. Micropyle, oocyst rias, UFRRJ. BR-465 km 7, 23897-970 Seropédi- residuum and polar granule were absent. The ca, RJ, Brasil. E-mail: [email protected] number of sporocysts per oocyst varied from [email protected] 14 to 21. The sporocysts were subspherical, 9.1 × 8.5 µm. Stieda and substieda bodies BP Berto  absent. Sporocyst residuum composed of scat- Departamento de Biologia Animal, Instituto de tered granules. Sporozoites present sub- Biologia, UFRRJ. BR-465 km 7, 23897-970 Sero- pédica, RJ, Brasil. spherical refractile bodies at both ends. This is E-mail: [email protected] the first report of a pseudoparasite in am- phibians. Comparative morphology of 29 CWG Lopes Adelina spp. is presented in tabulated data. Departamento de Parasitologia Animal, Instituto de Veterinária, UFRRJ. BR-465 km 7, 23897-970 Seropédica, RJ, Brasil. CNPq fellowship. Keywords pseudoparasite, predaction, inver- E-mail: [email protected] tebrate, habit, coccidia, morphology, oocysts,

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14 a 21. Os esporocistos foram subesféricos, Materials and methods 9,1 × 8,5 µm. Corpos de Stieda e substieda ausentes. Resíduo do esporocisto formado por Three specimens of T. miliaris were col- grânulos dispersos. Esporozoítos com corpos lected at Marambaia Island (23° 04’ S, 43° refráteis sub-esféricos em ambas as extremi- 53’ W) in the State of Rio de Janeiro. They dades. Este é o primeiro relato desse pseudo- were kept in individual vials, and feces were parasita em anfíbios. A morfologia compara- collected immediately after defecation. Fecal tiva de 29 Adelina spp. é apresentada em da- samples were placed in plastic vials contain- dos tabelados. ing 2.5% potassium dichromate solution (K2Cr2O7) 1:6 (v/v). Samples were carried to Palavras-chave pseudoparasita, predação, the Laboratório de Coccídios e Coccidioses, invertebrados, hábito, coccidia, morfologia, Universidade Federal do Rio de Janeiro. Sam- oocistos, polisporocístico, Adeleorina ples were placed in a thin layer (c.5 mm) of K2Cr2O7 2.5% solution in Petri plates and Introduction incubated at 23-28°C for 10 days or until 70% of the oocysts were sporulated. Oocysts were The of the genus Thoropa are recovered by flotation in Sheather’s sugar endemic to Eastern and Southeastern Brazil. solution (S.G. 1.20) and examined micro- Five species are grouped in this genus, includ- scopically using the technique described by ing Thoropa lutzi Cochran and Thoropa Duszynski & Wilber (1997). Morphological petropolitana Wandolleck, which are listed observations, photomicrographs and meas- respectively as Endangered and Vulnerable by urements, given in micrometers, were made the IUCN (International Union for Conserva- using a Olympus BX binocular microscope tion of Nature and Natural Resources). In coupled to a digital camera Eurocam 5.0. Size contrast, Thoropa miliaris Spix is not threat- ranges are in parentheses following the ened. This species from southern and eastern means. Brazil ranges from the southern part of the State of Rio de Janeiro, north to the State of Results and discussion Bahia, inland to the eastern part of the State of Minas Gerais. It is found in rocky areas in Three specimens of T. miliaris were exam- forest, above forest, or near forest, living on ined; being that one was positive for wet rock walls near streams or waterfalls. The sporulated polysporocystic oocysts of coc- species feeds mostly on invertebrates, espe- cidia. This species belong to the genus Ade- cially ants, , grasshoppers, caterpillars, lina, which was parasitizing an invertebrate and spiders (Feio et al. 2006, Siqueira et al. ingested by T. miliaris. 2006, Silva et al. 2008, Frost 2013, IUCN The identified oocysts (Figure 1) were el- 2013). lipsoidal, 37.6 (33-41) × 31.4 (29-34) µm, The insectivorous habit of some verte- with shape-index of 1.2 (1.1-1.2). Oocyst wall brates, as amphibians, is essential for some bi-layered and smooth, 1.2 μm thick. Micro- coccidia of invertebrates because they depend pyle, oocyst residuum and polar granule were of the feeding habits of vertebrates, which absent. The number of sporocysts per oocyst ingest its invertebrate hosts to ensure that will varied from 14 to 21. Sporocysts predomi- be dispersed. In other words, the vertebrate nantly subspherical, 9.1 (8-9) × 8.5 (8-9) µm, that ingests an invertebrate parasitized by a with shape-index of 1.1 (1.0-1.1). Stieda and coccidium should shed its oocysts encoun- substieda bodies absent. Sporocyst residuum tered in coelomic cavity of invertebrates, after composed of scattered granules. Sporozoites be digested (Berto et al. 2010). present sub-spherical refractile bodies at both The aim of this study was to report oocysts ends. of an invertebrate coccidium Adelina sp. from The oocysts recovered from T. miliaris feces of T. miliaris at Marambaia Island in the were identified as Adelina sp., because they State of Rio de Janeiro, Brazil. have polysporocystic oocysts with dizoic

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cystid oocysts in the feces of vertebrates. Finally, in the current study, a Adelina sp. is reported from feces of T. miliaris in Brazil, becoming the first description of this pseu- doparasite in amphibians.

Acknowledgements

We thank Dr. Hélio Ricardo da Silva (De- partamento de Biologia Animal, Instituto de Biologia, Universidade Federal Rural do Rio de Janeiro) for the identification of the am- phibians. We also thank the Brazilian Navy, in special to the command of CADIM (Centro de Adestramento da Ilha da Marambaia) that allowed us to access the Marambaia Island, located in Rio de Janeiro State, Brazil, and use some of the facilities of CADIM during the field work.

References

Berto BP, Lopes B doB, Flausino W, Teixei- ra-Filho WL, Lopes CWG. Contribution on the study of hemidactyli Cari- ni, 1936 and a report of an adeleid pseudo- parasite of the house gecko Hemidactylus mabouia, from the Rio de Janeiro - politan region, Brazil. Revista Brasileira de Parasitologia Veterinária, 17, 150-154, 2008. Berto BP, Lopes B doB, Teixeira-Filho WL, Flausino W, Lopes CWG. Coccídios de in- Fig. 1. Sporulated oocysts of Adelina sp., a pseu- vertebrados associados ao hábito alimentar doparasite recovered from feces of the frog Tho- de vertebrados: uma breve revisão dos gê- ropa miliaris. Scale-bar: 10 µm. neros , Adelina e Barroussia. Revis- ta Brasileira de Medicina Veterinária, 32, sporocysts. The genus Adelea also has these 33-41, 2010. characteristic features; however, this genus Duszynski DW, Wilber PG. A guideline for have discoidal sporocysts, rather than sub- the preparation of species descriptions in spherical sporocysts as in the current work the Eimeridae. Journal of Parasitology, 83, (Wenyon 1926, Ghosh 2000). Table 1 com- 333-336, 1997. pares the morphology and morphometry of the Feio RN, Napoli MF, Caramaschi U. Consid- oocysts of the current work with the main derações taxonômicas sobre Thoropa mila- reports of Adelina spp. in the world. ris (Spix, 1824), com revalidação e redes- Importantly, the finding of adeleid oocysts crição de Thoropa tapophora (Miranda- in the feces vertebrates, which feeding habit is Ribeiro, 1923) (Amphibia, Anura, Lepto- the ingestion of larvae or adults of inverte- dactylidae). Arquivos do Museu Nacional, brates, indicates that these are not its para- 64, 41-60, 2006. sites. Berto et al. (2010) emphasize some Frost DR. Thoropa. Species of the studies describing new genera and species, World: an Online Reference. American which were subsequently invalidated because Museum of Natural History, New York. they were carried out from adeleid polysporo- 2013. http://research.amnh.org/vz/herpeto

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Table 1. Comparative morphology of Adelina spp. reported from true and false hosts. Oocysts Sporocysts

Number Species Hosts References Diameter Diameter Shape per o- (µm) µm ocyst

Adelina sim- Gyrinus sp. (Insecta: Malone & Dhana plex Schnei- - 25-40 8-16 - Gyrinidae) (1988) der, 1875

Adelina tipu- Tipula sp. (Insecta: Malone & Dhana lae Schneider, - 35-40 4-10 - Tipulidae) (1988) 1875

Wenyon (1926), Adelina dimi- Scolopendra spp. Purrini (1984), diata Schnei- (Chilopoda: Scolo- - - 13-17 15 Malone & Dhana der, 1885 pendridae) (1988)

Tineola biseliella Purrini (1984), Adelina mesni- Hummel (Insecta: Malone & Dhana - - 6-8 15 li Pérez, 1899 Tineidae) (1988) Adelina aki- Olocrates abbreviatus Wenyon (1926), dum Leger, Reitter (Insecta: Te- Malone & Dhana - 30-40 12-20 10 1900 nebrionidae) (1988) Wenyon (1926), Haploembia solieri Adelina transi- Purrini (1984), Rambur (Insecta: - 30-40 6-20 10-11 ta Leger, 1904 Malone & Dhana Oligotomidae) (1988) Wenyon (1926), Blaps mortisaga L. Adelina zonula Purrini (1984), (Insecta: Tenebrioni- - - 8 - Moroff, 1906 Malone & Dhana dae) (1988) Adelina octos- Slavina appendiculata pora Hesse, d'Udekem (Oligocha- Purrini (1984) - 19-20 8 8 × 5-9 1911 eta: Naididae) Purrini (1984), Adelina tene- Tenebrio molitor L. Malone & Dhana brionis Sautet, (Insecta: Tenebrioni- - 20-35 2-12 10-12 (1988), Ghosh et 1930 dae) al. (2000) Adelina cryp- Cryptocercus punctu- Purrini (1984), tocerci Yar- latus Scudder (Insec- Malone & Dhana - 24-51 5-21 10-12 wood, 1937 ta: Cryptocercidae) (1988) Purrini (1984), Tribolium spp. Fabri- Adelina tribol- Malone & Dhana subspherical 26-50 × cius (Insecta: Tene- 2-14 - li Bhatia, 1937 (1988), Ẑizka or ovoidal 22.5-36.5 brionidae) (1969)

Adelina schel- Cormocephalus den- lacki Ray, 30-35 × 20- tipes Pocock (Chilo- Purrini (1984) - 8 15-18 Dasgupta, 25 poda: Scolopendridae) 1940

Adelina dero- Dero limosa Leidy nis Hauschka, (: Naidi- Purrini (1984) - - - -

Penny, 1942 dae)

Adelina seri- Sericesthis pruinosa Purrini (1984), cesthis Weiser, Dalman (Insecta: Malone & Dhana - - 4-8 -

Beard, 1959 Scarabaeidae) (1988)

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Kharazi-Pakdel & Adelina melolon- Melolontha melolon- Amargier (1973), thae Tuzet, Vago, tha L. (Insecta: Scara- Purrini (1984), - 30-35 6-14 11 Ormieres, Robert, baeidae) Malone & Dhana 1965 (1988)

Phlebotomus ariasi Adelina riouxi Malone & Dhana Tonnoir (Insecta: - 30-40 8-18 7-10 Levine, 1977 (1988) Psychodidae) Rhysida longipes Adelina rayi Nara- Narasimhamurti 20.0-22.0 × 12.0-14.0 Newport (Chilopoda: - 8 simhamurti, 1977 (1977) 18.0-20.0 × 2.0-2.5 Scolopendridae) Nothrus silvestris Adelina acarinae Nicolet (Arachnida: Purrini (1984) - 15-25 8-12 7-7.5 Purrini, 1984 Nothridae)

Neanura muscorum Adelina collembo- Templeton (Entogna- Purrini (1984) - 40 24 7.5-8 lae Purrini, 1984 tha: Neanuridae

Gryllus bimaculatus Adelina grylli de Sokolova (1999) subspherical 36.3 4-10 13.3 Butaeva, 1996 Geer (Insecta: Grylli- dae) Adelina castana Tribollium castaneum

Ghosh, Choudhur, Herbst (Insecta: Tene- Ghosh et al. (2000) ovoidal 29.3 × 25.4 4-12 8.2 Misra, 2000 brionidae)

Adelina picei Alphitobius piceus Ghosh, Choudhur, Olivier (Insecta: Te- Ghosh et al. (2000) subspherical 33.9 × 29.9 8-18 8.5 Misra, 2000 nebrionidae) Adelina palori Palorus ratzeburgi Ghosh, Choudhur, Wissmann (Insecta: Ghosh et al. (2000) ovoidal 30.3 × 24.6 4-12 8 Misra, 2000 Tenebrionidae) Anolis trinitatis Rei- 30.5-39.2 Adelina sp.a nhardt, Lütking (Rep- Daszak & Ball 30.5-39.2 × 7-16 subspherical ×26.5-31.7 tilia: Dactyloidae) (1998) 26.5-31.7

Anurogryllus muticus Lange & Wittenste- Adelina sp. de Geer (Insecta: subspherical 24 3-12 - in (2001) Gryllidae) Didelphis aurita Wied-Neuwied Teixeira et al. 11.0 × Adelina sp.a, b subspherical 34.7 × 31.6 6-12 (Mammalia: Didel- (2003) 10.7 phidae) Nasua nasua L. Adelina sp.a, b (Mammalia: Procyo- Lopes et al. (2006) subspherical 23.9 × 21.5 8-12 10.3 × 8.6 nidae) Hemidactylus ma- bouia Moreau de 12.4 × Adelina sp.a, b Berto et al. (2008) ellipsoidal 36.3 × 30.9 8- 15 Jonnès (Reptilia: 11.2 Gekkonidae) Thoropa miliaris Spix a, b Adelina sp. (Amphibia: Cyclo- current study ellipsoidal 37.6 × 31.4 14-21 9.1 × 8.5 ramphidae) aPseudoparasites; b Reported in Brazil.

logy/amphibia/?action=references&id=92 dia. Acta Protozoologica, 39, 233-240, 70 [19-11-2013] 2000. Ghosh C, Choudhur Y, Misra KK. Life histo- IUCN. International Union for Conservation ries of three new coccidian parasites from of Nature and Natural Resources. 2013. three coleopteran stored-grain pests of In- http://www.iucnredlist.org [19-11-2013]

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Kharazi-Pakdel A, Amargier A. La kunde, 128, 99-107, 1984. pathogénèse des infections simultanées a Silva HR, Carvalho ALGD, Bittencourt-Silva Adelina melolonthae et a Nosema melolon- GB. of Marambaia: a naturally iso- thae chez Melolontha melolontha. Ento- lated Restinga and Atlantic Forest remnant mophaga, 18, 229-235, 1973. of southeastern Brazil. Biota Neotropica, 8, Lange CE, Wittenstein E. An Adelina sp. 167-174, 2008 (Apicomplexa: Coccidia) found in Anuro- Siqueira CC, Van Sluys M, Ariani CV, Rocha gullus muticus (De Geer) (: CFD. Feeding ecology of Thoropa miliaris Gryllidae). Journal of Invertebrate Pathol- (Anura, Cycloramphidae) in four areas of ogy, 77, 83-84, 2001. Atlantic rain forest, southeastern Brazil. Lopes B doB, Souza JD, Lopes CWG. Coccí- Journal of Herpetology, 40, 520-525, dios pseudoparasitos do quati do focinho 2006. preto (Nasua nasua). Revista Universidade Sokolova YY. Light and electron microscopic Rural: Ciência e Vida, 26, 53-54, 2006. observation on life cycle stages of Adelina Malone LA, Dhana S. Life cycle and ultras- grylli Butaeva 1996 (Sporozoa, Adeleidae) tructure of Adelina tenebrionis (Sporozoea: from the fat body of the cricket Gryllus Adeleidae) from Heteronychus arator (Co- bimaculatus. Protistology, 1, 34-42, 1999. leoptera: Scarabaeidae). Parasitology Re- Teixeira M, Albuquerque GR, Lopes CWG, search, 74, 201-207, 1988. Florentino MVN. An adeleid coccidia, a Narasimhamurti CC. Observations on the pseudoparasite of Didelphis aurita (Mar- morphology and sporogony of a coccidian supialia: Didelphoidea). Revista Brasileira Adelina rayi n. sp. from the gut of the cen- de Parasitologia Veterinária, 12, 33-35, tipede, Rhysida longipes. Proceedings of 2003. the Indian Academy of Sciences, 86, 239- Wenyon CM. Protozoology. New York: Wil- 244, 1977. liam, Wood and Company, 1926. Purrini K. Two New Coccidian Parasites of Ẑizka Z. The fine structure of the macrogame- the Genus Adelina (Adeleidae, Coccidia) tocytes of Adelina tribolii Bhatia, 1937 Parasitizing Oribatid Mite Nothrus Silve- (Eucoccidia, Telosporea) from the fat body stris (Oribatei, Acarina) and of the Tribolium castaneum Hbst. Neanura Muscorum (Collembola, Aptery- Journal of Protozoology, 16, 111-120, gota) in Forest Soils. Archiv für Protisten- 1969.

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