Helminths of Molothrus bonariensis ( Gmelin , 1789 ) ( Passeriformes : Icteridae ) from southernmost Brazil Helmintos of Molothrus bonariensis ( Gmelin , 1789 ) ( Passeriformes : Icteridae ) do extremo sul do Brasil

Information about helminths of Molothrus bonariensis (Gmelin, 1789) (Passeriformes: Icteridae) are scarce; in this sense the objective of this paper was to contribute to its knowledge. Five hosts of southern Brazil were examined and the helminths Prosthogonimus ovatus, Tanaisia valida (Digenea), Diplotriaena bargusinica and Synhimantus (Dispharynx) nasuta (Nematoda) were identified. The species T. valida, P. ovatus and S. (D.) nasuta are for the first time registered for the bird in Brazil. Prosthogonimus ovatus, T. valida, D. bargusinica e S. (D.) nasuta are first recorded in M. bonariensis in the southern Brazilian state Rio Grande do Sul.

Parasites are among the most common organisms in the world (HOBERG & KUTZ, 2013).They are extremely diversified and play a key role in ecological and evolutionary processes (GOMÉZ & NICHOLS, 2013).Parasitism is one of the most successful ways of living presented by living organisms (POULIN & MORAND, 2000).
Birds are commonly parasitized by trematodes, nematodes, cestodes and acanthocephalans, as well as other groups (AMATO & AMATO, 2010).Taking into account the fact that Brazil presents one of the richest avifaunas in the world, much remains to be explored regarding this subject.
Molothrus bonariensis (Gmelin, 1789) (Passeriformes: Icteridae), known as the shiny cowbird, occurs in South America, islands of Central America, United States and Canada (The IUCN Red List of Threatened Species, 2015).In the state of Rio Grande do Sul, Brazil, they inhabit the entire state, where enormous flocks often gather in cereal crops, especially rice, during and after harvesting (BELTON, 1994).The male is black-feathered with bluish reflexes, and the female is brown.They feed on seeds and insects, and occasionally on fruits, and often can be seen near to cattle, turning over excrement to look for undigested seeds (EFE et al., 2001).
Information regarding the shiny cowbird is mainly focused on the fact that this species lays its eggs in other birds' nests.In Brazil, approximately 60 species belonging to nine families of Passeriformes are affected by the action of the shiny cowbird.This species is entirely dependent on other bird species for its reproduction, because it has not only lost the ability to build its own nests but also the instinct of taking care of its offspring (BLANCO, 1995;SICK, 1997;EFE et al., 2001;MERMOZ & REBOREDA, 2003;ASTIÉ & REBOREDA, 2006).
Five hosts were examined (one male and four females), originating from the municipality of Rio Grande, Rio Grande do Sul,Brazil (32º 14'.37.24" S;52°29'38.71" W) two birds in the summer and three in the winter.They were accidentally sampled in a trap that had been set to catch Chrysomus ruficapillus (Vieillot, 1819) (Passeriformes: Icteridae), in accordance with a license granted by the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio No. 41095-3) and approval granted by the Comitê de Ética e Experimentação Animal from the Universidade Federal de Pelotas (CEEA/UFPel No. 147), covering the period of 2013-2015.
These specimes of Molothrus bonariensis were euthanasied, individually placed in identified plastic bags, and were transported to the Laboratório de Parasitologia de Animais Silvestres (LAPASIL/UFPel) and frozen until processing.To collect helminths, were necropsied and their organs (mouth, esophagus, proventriculus, gizzard, cecum, small and large intestines, trachea, lungs, heart, liver, gall bladder, pancreas, reproductive system, kidneys, cloaca and air sacs) were separated from each other, opened and rinsed with running water under a sieve of mesh size 150 µm.
The helminths were fixed in AFA for 24 hours and were stored in accordance with the protocol proposed by Amato & Amato, 2010.Trematodes were stained with Langeron's carmine and nematodes were clarified with Aman's lactophenol.They were mounted on permanent and semi-permanent slides and photographed through a microscope (Olympus ® BX 41) with a coupled camera system.Morphological and morphometric identification were performed in accordance with Freitas (1951), Kohn & Fernandes (1972), Gibson et al. (2002), Bray et al. (2008), Lunaschi et al. (2015) for Digenea, and with Vicente et al. (1983), Zhang et al. (2004) and Anderson et al. (2009), for Nematoda.The parameters calculated were prevalence (P), mean abundance (MA) and mean intensity of infection (MI), in accordance with Bush et al. (1997).The voucher specimens were deposited in the "Coleção de Helmintos do Laboratório de Parasitologia de Animais Silvestres" from Instituto de Biologia, Universidade Federal de Pelotas (CHLAPASIL/UFPel) (No. 612 to 616).
The morphological identification of each species was carried out according to the characteristics described by the previously mentioned authors.We present below the relevant aspects of each helminth.P. ovatus (Figure 1) is characterized by having the piriformis body, subterminal oral sucker, muscular pharynx present (Figure 2), simple intestinal cecum, few meandering surpassing the testicles.Acetabulum pre-equatorial, terminal genital pore located next to the oral sucker.Cirrus sac extending from the genital pore to the level of esophageal bifurcation, well-developed testicles, post-acetabular, post-ovarian, equatorial (Figure 3).Ovary pretesticular lobed, Mehlis gland situated below the ovary, uterus occupies half of the body and the excretory portion is terminal.
Tanaisia valida has elongated body, flattened, in tegument with thorns, vitelline glands begging in post-ovarian region to the back of the body (Figure 4), oral sucker subterminal, non visible acetabulum, muscular pharynx (Figure 5), intestinal cecum is positioned dorsally in relation to the gonads fused near to end of the body.Lobate testis with diagonal layout, pre-equatorial, post-ovarian (Figure 6).Lobate ovary, uterus with a large number of eggs, these yellow-brownish color with a smooth shell.
In the anterior region of D. bargusinica has a trident well developed (Figure 7), trident with tapered apex (Figure 8), females has a genital opening near to the anterior region (Figure 9), eggs with size range of 0.044 × 0.029mm (Figure 10), females with posterior rounded region (Figure 11), males with uneven spicules with small number of papillae (Figure 12).Synhimantus (D.) nasuta (Figure 13) has a filiform body, cuticle striated crosswise, small and conic lips, four cords recurrent non anastomosing beginning on surface dorsal and ventral of the oral opening extending to the posterior portion of the muscle esophagus and bifurcated cervical papillae (Figure 14) Females presented well-developed uterine, vulvar opening near the posterior end of the body (Figure 15).Males presented curved caudal end, nine pairs of caudal papillae, four pairs pre-cloacal and five post-cloacal (Figure 16), unequal and dissimilar spicules (Figure 17).
The trematodes Prosthogonimidae (Lühe, 1909) have worldwide distribution.They are parasites of the bursa of Fabricius, oviduct, cloaca or nictitating membrane of birds, in mammals are found in the intestine, liver and body cavity (BRAY et al., 2008).
Tanaisia Skrjabin, 1924, parasitizes the renal tubules and kidneys of birds.In Brazil, it has mainly been reported in Passeriformes, although there have been records of occurrences in Cuculiformes, Charadriiformes, Gruiformes and Strigiformes.The Eucotylidae taxonomy is a complex one due to morphological structures that characterize the genera and species (integument, position and shape of the testis and ovaries, etc.).Lunaschi et al. (2015) redescribed Tanaisia dubia Freitas, in 1951, had created a key to the Neotropical species Tanaisia and a key to the Tanaisiinae genres that gives support in species About the life cycle of T. valida does not exist information, however considering the life cycle of Tanaisiinae, the birds become infected by ingesting (Mollusca: Gastropoda) containing metacercariae (LUNASCHI et al. 2015).
In Brazil D. bargusinica was reported by Vicente et al. (1983) parasitizing some Passeriformes in different areas of the country: Cacicus cela (Linnaeus, 1758), Cacicus haemorrhous (Linnaeus, 1766), The biological cycle of S. (D.) nasuta is heteroxenous, using terrestrial isopods, orthopterans, beetles or millipedes (GOBLE & KUTZ, 1945).The larvae develop in non-specific tissues of isopods, in which they become encapsulated and are later on ingested by birds (ANDERSON, 2000).The effects on the definitive host are related to the parasitic load, usually comprising inflammations, granulomas and lesions in the proventriculus.In wild birds, these macroscopic and histopathological alterations were described by Bartmann & Amato (2009).
In general, the parasitological indexes of M. bonariensis are similar to those found by those previously mentioned authors, considering that the previous studies had sample sizes close to the one of the present study future research is needed to complement existing information in order to contribute to the understanding of the biology and ecology of these organisms.
In Brazil, for the first time the species T. valida, P. ovatus e S. (D.) nasuta are recorded parasitizing M. bonariensis.Prosthogonimus ovatus, T. valida, D. bargusinica e S. (D.) nasuta characterize first record in M. bonariensis in Rio Grande do Sul.Whereas the helminthological information for the specie are scarce, this work expands the knowledge to Icteridae and Molothrus bonariensis.