(Didelphimorphia: Didelphidae), in Costa Rica Author(S): Idalia Valerio-Campos, Misael Chinchilla-Carmona, and Donald W

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Eimeria marmosopos (Coccidia: Eimeriidae) from the Opossum Didelphis marsupialis L., 1758 (Didelphimorphia: Didelphidae), in Costa Rica Author(s): Idalia Valerio-Campos, Misael Chinchilla-Carmona, and Donald W. Duszynski Source: Comparative Parasitology, 82(1):148-150. Published By: The Helminthological Society of Washington DOI: http://dx.doi.org/10.1654/4693.1 URL: http://www.bioone.org/doi/full/10.1654/4693.1

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Research Note Eimeria marmosopos (Coccidia: Eimeriidae) from the Opossum Didelphis marsupialis L., 1758 (Didelphimorphia: Didelphidae), in Costa Rica

1 1,3 2 IDALIA VALERIO-CAMPOS, MISAEL CHINCHILLA-CARMONA, AND DONALD W. DUSZYNSKI 1 Research Department, Medical Parasitology, Faculty of Medicine, Universidad de Ciencias Me´dicas (UCIMED), San Jose´, Costa Rica, Central America, 10108 (e-mail: [email protected]; [email protected]) and 2 Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131, U.S.A. (e-mail: [email protected])

ABSTRACT: Oocysts of a coccidium found in the small philanderi Lainson and Shaw, 1989, is the only intestine of a road-killed opossum, Didelphis marsupialis known eimerian, and from members of the Marmo- (Didelphimorphia: Didelphidae), are described and identi- sops, only Eimeria marmosopos Heckscher, Wickes- fied as Eimeria marmosopos. Sporulated oocysts (n 5 57) berg, Duszynski, and Gardner 1999 is known. were subspherical to spherical and measured 21.9 3 22.1 Members of the genera Philander and Didelphis are (20–25 3 20–25); oocyst wall rough and striated, yellowish known to share similar environments, and Marmo- and bilayered; micropyle, polar body, and oocyst residuum all absent, but some oocysts have a polar granule. sops dorothea apparently also is present in Costa Sporocysts were ovoidal, 9.8 3 8.7 (8–13 3 7–12), with Rica (Mora, 2000). The relative paucity of published both a conspicuous Stieda body and sub-Stieda body, but reports of coccidian parasites from D. marsupialis,1 para-Stieda body was absent. The sporocyst residuum was of the 63 species belonging to the family Didelphidae composed of 2–5 globules (1–4 wide) and several smaller in Costa Rica (Gardner, 1993; Mora, 2000), is the ones. Sporozoites (n 5 10) were comma-shaped, ,7 3 2.7 reason of the report herein. and had 1 refractile body at their wider end and a centrally Feces from a road-killed opossum were examined located nucleus. These morphological characters were for coccidian oocysts after suspension in a 0.85% compared with other Eimeria species found in related saline solution followed by placement in 2.5% genera of New World marsupials; based on oocyst aqueous (w/v) potassium dichromate (K2Cr2O7) morphology, we identified this species as Eimeria marmo- solution in petri dishes at room temperature. sopos Heckscher, Wickesberg, Duszynski, and Gardner Conventional methods for concentration, preserva- 1999. This finding constitutes both a new host genus and new geographical record for this species. tion, and description of oocysts were used (Bandoni and Duszynski, 1988; Duszynski and Wilber, 1997). KEY WORDS: Coccidia, Eimeriidae, Eimeria marmosopos, Marsupialia, Didelphimorphia, Didelphidae Didelphis mar- After sporulation, the oocysts were examined with an supialis, Atenas, Alajuela, Costa Rica, sporulated oocysts. Olympus BX41 microscope and photographed with an Olympus C-60 camera. All measurements are To our knowledge, eimerians parasitizing opos- given in micrometers (mm), with means followed by sum, Didelphis marsupialis, have not been recorded ranges in parenthesis. Morphological features were in Costa Rica or in Central America to date. The then compared with those eimerian species previous- reports of coccidia from the American opossum ly reported from members of the genera Didelphis, are rare (Carini, 1936, 1937, 1938; Joseph, 1974; Philander, and Marmosops (family Didelphidae; Lainson and Shaw, 1989; Heckscher et al., 1999; Table 1). We use the standardized abbreviations of Teixeira et al., 2007). These authors described 12 Wilber et al. (1998): length (L) and width (W) and Eimeria and Isospora species. Within the family their ratio (L/W); micropyle (M); oocyst residuum Didelphidae 7 eimerians are described from 3 genera (OR); polar granule (PG); sporocyst L and W and (Table 1). Within the genus Didelphis, oocysts of their L/W ratio; Stieda body (SB) sub-Stieda body Eimeria didelphydis Carini, 1938; Eimeria gambai (SSB), para-Stieda body (PSB); sporocyst residuum Carini, 1936; Eimeria indianensis, Joseph, 1974; and (SR); sporozoite (SZ); refractile body (RB), and Eimeria auritanensis Teixeira, Rauta, Albuquerque, nucleus (N). A 2-tailed test for the 95% confidence and Lopes 2007 have been studied morphologically. interval on the difference between the means was Within members of the genus Philander, Eimeria done for statistical purposes. Fecal samples contained sufficient numbers of sporulated oocysts to allow morphological character- 3 Corresponding author. ization.

148 RESEARCH NOTES 149

Table 1. Comparison of morphologic characteristics of Eimeria species infecting hosts of the genera Didelphis, Marmosops, and Philander (family Didelphidae).

Oocyst and sporocyst features* Eimeria sp. Hosts Mean L 3 W(m) OR PG Mean L 3 W(m) SB SSB SR

E. philanderi P. opposum 23.5 3 22.4 2 + 11.4 3 8.1 + 2 + E. auritanensis D. aurita 31.6 3 29.6 2 + 13.2 3 10.4 + 2 + E. indianensis D. virginiana 17.6 3 16.4 2 + 9.1 3 6.2 + 2 + E. didelphydis D. aurita 16.0 3 16.0 + 2 10.0 3 6.0 + 2 + E. gambai D. aurita 26.5 3 24.8 2 + 12.5 3 10.0 + 22 E. marmosopos M. dorothea 22.2 3 19.9 2 + 11.1 3 6.8 +++ E. marmosopos D. marsupialis 21.9 3 22.1 2 + 9.8 3 8.7 +++

* L, length; W, width; OR, oocyst residuum; PG, polar granule; SB, Stieda body; SSB, sub–Stieda body; SR, sporocyst residuum.

Eimeria marmosopos Description of sporocyst and sporozoites: Sporo- (Figs. 1, 2) cyst shape: elongate–ovoidal; L 3 W(n 5 79): 9.8 3 8.7 Type host: Marmosops dorothea Thomas, 1911, (8.0–13.0 3 7.0–12.0); L/W: 1.2; SB: present (2 3 1.5) mouse opossum. as a knob-like extension of the sporocyst wall; SSB: present, L 3 W about the same width as SB; PSB: absent; Type locality: SOUTH AMERICA: Bolivia, Santa SR present; SR characteristics: 2–5 round globules Cruz. (,1.5–4 wide) and several smaller ones; SZ: elongated, Other hosts: Didelphis marsupialis Linnaeus, smooth or finely granular; L 3 W(n 5 10) 7 3 2.7. 1758, opossum. Sporulation: Exogenous, 6–7 days at 21 6 3uC. CENTRAL AMERICA: Costa Other locality: Prepatent period: Unknown. Rica, Alajuela, Atenas, 9u589510N; 84u249230E; elevation 550 m, average temperature 21uC, relative Site of infection: Unknown humidity 82%, rainfall 1,500–2,500 mm/yr. Endogenous stages: Unknown. Geographic distribution: South America: Bolivia; Cross-transmission: None to date. Central America: Costa Rica. Pathology: Unknown. Description of sporulated oocyst: Oocyst shape: spherical or subspherical; number of walls: 2; outer, Material deposited: Photosyntypes of sporulated ,1 thick, yellowish, rough and striated; inner is beige oocysts, IB-1-D-1,2 are in the Department of with a dotted appearance in optical cross section; L 3 Parasitology Research, Universidad de Ciencias W(n 5 57): 21.9 3 22.1 (20.0–25.0 3 20.0–25.0); Me´dicas, San Jose´ Costa Rica, Central America. L/W: 1; M, OR: both absent; PG: slightly elongated, Host skin and skeleton in the Museo Nacional ,3 3 2. (MNCR-432), San Jose´ Costa Rica.

Figures 1, 2. Sporulated oocyst of Eimeria marmosopos from Didelphis marsupialis from Costa Rica. 1. Photomicrograph. 2. Line drawing from the feces of D. marsupialis. 150 COMPARATIVE PARASITOLOGY, 82(1), JANUARY 2015

Remarks: We compared all known Eimeria species This work was partially supported by the Universidad from 3 genera of marsupials that have overlapping de Ciencias Me´dicas (UCIMED), Ministerio de Ciencia ranges in Costa Rica, including Didelphis, Marmo- y Tecnologıá (MICIT), and Consejo Nacional de sops, and Philander (Table 1). Our conclusion is that Ciencia y Tecnologıá (CONICIT). We thank Juan the mensural and qualitative characters found for the Carlos Vanegas for statistical comparative analysis. species reported here correspond with those already described for E. marmosopos (Heckscher et al., 1999). LITERATURE CITED Comparative statistical analysis of our measurements Bandoni, S., and D. W. Duszynski. 1988. A plea for to those of E. marmosopos showed that there are not improved presentation of type material for coccidia. significant differences (P 5 0.0734) between them. Journal of Parasitology 74:519–523. Heckscher et al. (1999) reported on how little we Carini, A. 1936. Eimeria didelphydis n. sp. dell’intestino de know about Eimeria species in various genera and Didelphis aurita. Archivo Italiano di Scienze Mediche Tropical e di Parassitologia 17:332–335. species of the family Didelphidae, and little has Carini, A. 1937. Sur une noveulle Eimeria, parasite de changed since then. There are 4 eimerians known l’intestin du Caluromys philander. Annales of Parasi- from D. marsupialis, but none in D. marsupialis tology 15:453–455. throughout Central and South America from Mexico Carini, A. 1938. Mais uma Eimeria, parasita do intestino do Didelphys aurita. Arquives of Biology S Paulo 22:61–62. to Brazil, Bolivia, and Peru according to Gardner Castro, A., M. Chinchilla, O. M. Guerrero, and R. (1993) and Mora (2000). We believe that E. Gonza´lez. 1998. Especies de Eimeria (Eucoccidia: marmosopos, previously described and reported only Eimeriidae) en la rata de milpa Sigmodon hispidus de in M. dorothea from Bolivia, to be the coccidium that Costa Rica. Revista de Biologıá Tropical 46:339–340. ´ ´ we found infecting D. marsupialis in Costa Rica. The Chinchilla, M., I. Valerio, R. Sanchez, A. Gonzalez, L. Martıńez, and D. W. Duszynski. 2013. Two new fact that little is known about what coccidians are Eimeria spp. (Apicomplexa: Eimeriidae) from the found in the marsupials of the Americas, not to dusky rice rat, Melanomys caliginosus, Tome 1860, mention their relationships with their natural host in Costa Rica. Journal of Parasitology 99:82–84 species, led Heckscher et al. (1999) to conclude that it Duszynski, D. W., and P. G. Wilber. 1997. A guideline for the preparation of species descriptions in the Eimeri- is unclear whether Eimeria species from Bolivian idae. Journal of Parasitology 83:333–336. marsupials were either generalists or specialists. One Gardner, A. L. 1993. Order Didelphimorphia. Pages 15–23 eimerian Heckscher et al. (loc. cit.) studied, Eimeria in D. E. Wilson and D. M. Reeder, eds. Mammal Species cochabambensis, was found in hosts from 3 genera of the World. A Taxonomic and Geographic Reference. Smithsonian Institution, Washington, DC 2000 pp. (Monodelphis, Thylamys, and Marmosops); they Heckscher, S. K., B. A. Wickesberg, D. W. Duszynski, argued that the structural and mensural differences and S. L. Gardner. 1999. Three new species of of oocysts from the 3 were not enough to distinguish Eimeria from Bolivian marsupials. International Jour- each as a separate species, leading them to call all of nal of Parasitology 29:275–284. Joseph, T. 1974. Eimeria indianensis n sp. and Isospora sp. them E. cochabambensis until molecular and cross- from the opossum Didelphis virginiana (Kerr). Journal transmission studies could be used to determine of Protozoology 21:12–15. definitively whether their oocysts represented 1 or Lainson, R., and J. Shaw. 1989. Two new species of more species from the different host genera. Thus, we Eimeria and three new species of Isospora (Apicom- plexa, Eimeriidae) from Brazilian mammals and birds. will consider them the same species until molecular Bulletin Museum National History Natural 11:349–365. or cross-transmission or both studies can confirm or Mora, J. M. 2000. Mamı´feros silvestres de Costa Rica. 1 refute our decision. ed. EUNED, San Jose´, Costa Rica. This report adds one more species to the coccidia Rodrı´guez, B., R. Gonza´lez, and M. Chinchilla. 1999. Fauna Parasitolo´gica de la rata de milpa Sigmodon already known from Costa Rica: Eimeria sigmodon- hispidus,enuna´rea urbana-industrial de Alajuela, tis, Eimeria tuskegeensis, Eimeria roperi, and Costa Rica. Parasitologia al Dıá 23:95–99. Eimeria webbae from Sigmodon hispidus (Castro et Teixeira, M., P. D. Rauta, G. R. Albuquerque, and C. W. al., 1998; Rodriguez et al., 1999), as well as Eimeria G. Lopes. 2007. Eimeria auritanensis n. sp. and E. gambai Carini, 1938 (Apicomplexa:Eimeriidae) from melanomytis and Eimeria rebambensis from Mela- the opossum Didelphis aurita Wied-Neweid, 1826 nomys caliginosus (Chinchilla et al., 2013) and (Marsupiala: Didelphidae) from southeastern Brazil. represents another contribution to the knowledge of Revista Brasilenã de Parasitologıá Veternaria 16:83–86. parasites infecting the diverse assemblage of animals Wilber, P. G., D. W. Duszynski, S. J. Upton, R. S. Seville, from Costa Rica. Significantly, this report also and J. O. Corliss. 1998. A revision of the taxonomy and nomenclature of the Eimeria (Apicomplexa: represents a new geographic record for E. marmoso- Eimeriidae) from rodents in the Tribe Marmotini pos and adds a new host genus for this species. (Sciuridae). Systematic Parasitology 39:113–135.