First records of parasites from the Long-tailed Meadowlark Sturnella loyca (Passeriformes: Icteridae) from the Biobío Region, Chile
Primer registro de parásitos de la loica Sturnella loyca (Passeriformes: Icteridae) de la región del Biobío, Chile
Marta Soto1, Lucila Moreno2, María S. Sepúlveda3, J. Mike Kinsella4, Sergei Mironov5 and Daniel González-Acuña1*
1 Facultad de Ciencias Veterinarias, Universidad de Concepción, Casilla 537, Chillán, Chile. *danigonz@udec.cl
]]> 2 Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Casilla 160C, Concepción, Chile.3 Department of Forestry and Natural Resources, Purdue University, West Lafayette, IN 47907, USA.
4 Helm West Lab, 2108 Hilda Avenue, Missoula, MT 59801, USA.
5 Zoological Institute, Russian Academy of Sciences, Universitetskaya Embankment 1, Saint Petersburg 199034, Russia.
Recibido: 22 octubre 2012
Aceptado: 19 junio 2013
Abstract
A total of 27 Long-tailed Meadowlarks Sturnella loyca (Molina, 1782) from the Biobío Region were examined between January 2005 and December 2008. Birds were infected with chewing lice (Phthiraptera), feather mites (Acari), and helminths (Platyhelminthes, Acanthocephala). Three species of chewing lice were found: Brueelia boae Cicchino and Castro, 1996 (26% prevalence), Menacanthus leistidis Cicchino, 1984 (7.4%), and Menacanthus sturnellae Price, 1977 (7.4%). Mites included 4 taxa: Amerodectes sp. (Mironov, 2008) (14.8%), Harphyrhynchoides sp. (Fain, 1972) (7.4%), Mesalgoides sp. (Fain, 1972) (3.7%), and Proctophyllodes sp. (Robin, Mégnin, 1877) (3.7%). Gastrointestinal helminths included the cestode Anonchotaenia longiovata (Fuhrmann, 1901) (18%) and the acanthocephalan Mediorhynchus robustus (Van Cleave, 1916) (3.7%). With the exception of B. boae and M. leistidis, all parasites represent new records for this passerine bird species.
]]> Key words: helminths, gastrointestinal, ectoparasites, mites, lices, Chile.
Resumen
Se analizaron 27 loicas Sturnella loyca (Molina, 1782) procedentes de la región del Biobío entre enero de 2005 y diciembre de 2008. Se recolectaron piojos (Phthiraptera), ácaros de plumas (Acari) y helmintos (Platyhelminthes, Acanthocephala). Se identificaron 3 especies de piojos: Brueelia boae Cicchino y Castro, 1996 (26% prevalencia), Menacanthus leistidis Cicchino, 1984 (7.4%) y Menacanthus sturnellae Price, 1977 (7.4%). Los ácaros incluyeron 4 taxa: Amerodectes sp. (Mironov, 2008) (14.8%), Harphyrhynchoides sp. (Fain, 1972) (7.4%), Mesalgoides sp. (Fain, 1972) (3.7%) y Proctophyllodes sp. (Robin, Mégnin, 1877) (3.7%). Los helmintos gastrointestinales encontrados fueron: el céstodo Anonchotaenia longiovata (Fuhrmann, 1901) (18%) y el acantocéfalo Mediorhynchus robustus (Van Cleave, 1916) (3.7%). Con excepción de B. boae y M. leistidis, todos los parásitos representan nuevos registros para esta especie.
Palabras clave: helmintos, gastrointestinal, ectoparásitos, ácaros, piojos, Chile.
The Long-tailed Meadowlark, Sturnella loyca (Molina, 1782) (Passeriformes: Icteridae) inhabits the cold temperate region of South America. In Chile, it can be found from Copiapo (Atacama Region, 27°22'02" S, 70°20'04" W) to Tierra del Fuego (Magallanes Region, 54°01'54" S, 68°31'13" W) (Araya and Millie, 2000) and from the coast and continental islands to an altitude of 2 500 m (Goodall et al., 1957). Its preferred habitats include areas with moist terrain and shrubs (Couve and Vidal, 2003), close to pastures (De la Peña and Rumbol, 1998), as well as coastal ravines and open grass areas (Couve and Vidal, 2003). Long-tailed Meadowlarks are also commonly observed in urban areas (Estades, 1995; Urquiza and Mella, 2002). In addition, it is considered a beneficial species for the maintenance of healthy ecosystems (SAG, 2007).
Although it is well known that wild birds harbor a large variety of parasites (Figueiroa et al., 2002), only a handful of studies have been published on this subject from Chilean bird species (Hinojosa and González-Acuña, 2005). Further, the present study constitutes the first report on the parasitic fauna of Long-tailed Meadowlarks in Chile.
Between January 2005 and December 2008, a total of 27 Long-tailed Meadowlarks were retrieved from different locations within the Biobío Region. Carcasses (resulting from roadkills, poaching, dog kills, etc.) were taken to the Faculty of Veterinary Sciences, Universidad de Concepción, Chillán for parasite examination. Ectoparasites were collected manually with fine forceps after exhaustive examination and preserved in 70% ethanol. They were then cleaned in 20% potassium hydroxide, dehydrated in a series of ethanol solutions (40, 80, and 100%), cleared for 24 h in clover oil, and finally mounted in Canadian balsam (Palma, 1978). Techniques used for the collection, fixation, and staining of endoparasites followed those described in Kinsella and Forrester (1972) and Pritchard and Kruse (1982). Ectoparasites were identified using keys from Price (1977), Cicchino (1984), and Cicchino and Castro (1996) for Phthiraptera and from Park and Atyeo (1971), Mironov and Fain (2003), Valim and Hernandes (2006), Mironov (2008), Mironov et al. (2008), Atyeo and Braasch (1966), and Gaud and Atyeo (1996) for Acari. Endoparasites were identified to species using keys by Rausch and Morgan (1947) and Schmidt and Kuntz (1977). Mean intensity, range, and abundance for each parasite species were calculated as described in Bush et al. (1997). All specimens have been deposited in the Department of Zoology, Universidad de Concepción, Chile.
Table 1 summarizes the parasites found from the 27 Long-tailed Meadowlarks examined. In total, 8 taxa were recovered, 3 species of chewing lice (overall prevalence of 26.6%), 4 species of feather mites (22.2%), 1 cestode, and 1 acanthocephalan (22.2%).
]]> Overall, there was a large variation in the number of ectoparasites recovered from the birds examined, which could be due to the fact that birds were collected after their death. This variation in abundance could also be due to annual and seasonal differences in host and parasite numbers. For some species, it was possible to calculate sex and developmental ratios. For instance, a total of 33 Brueelia boae Cicchino and Castro, 1996 were collected, of which 7 were males, 17 were females, and 9 were nymphs (female:male ratio of 2.2 and nymph:adult ratio of 0.37). In Pterodectes, a larger number of females (31) than males (20) were collected (ratio of 1.55). In this species, the nymph:adult ratio was 0.1. Finally, in Harpyrhynchoides, the sex and developmental stage ratios were 0.83 and 0.5, respectively.Phthiraptera. The genus Brueelia Keler, 1936 (Ischnocera, Philopteridae) includes approximately 276 species (Cicchino and Castro, 1998b) parasitizing a large number of bird orders including Passeriformes, Piciformes, Coraciiformes, and Trogoniformes (Cicchino and Castro, 1998a). Despite Brueelia's broad host distribution, members of this genus are highly species-specific, with ~ 90% of them infecting only 1 host species (Johnson et al., 2002). Before this study, B. boae had only been described from S. loyca loyca from Argentina (Santa Rosa, Provincia de La Pampa) (Cicchino and Castro, 1996) and from Chile in individuals sampled from Huilmo (Pumitaqui, Coquimbo, 30°52'59" S, 71°09'05" W) and Llanquihue (41°15'28" S, 73°00'29" W) (González-Acuña et al., 2006). The larger number of female B. boae detected in the present study could be due to a potential larger loss of males to predation from the host due to their smaller size and thus higher activity and/or to adverse climatic conditions (Marshall, 1981).
The genus Menacanthus Neumann, 1912 (Amblycera: Menoponidae) includes close to 50 species reported from Passeriformes, Piciformes, Apodiformes, Coraciiformes, Tinamiformes, and Galliformes (Cicchino and Castro, 1998b). Menacanthus leistidis Cicchino, 1984 was described from Argentina in Sturnella militaris superciliaris Bonaparte, 1850 (Cicchino, 1984) and Sturnella defilipi (Cicchino and Castro, 1998b). In Chile, this same species had already been described in S. loyca from a more northern location (Las Cabras, 34°17'23" S, 71°18'05" W) (González-Acuña et al., 2006). Menacanthus sturnellae was originally described by Price (1977) from S. magna sampled from different localities in the United States. The present study constitutes the first report of M. sturnellae in S. loyca and in South America.
Acarina. None of the feather mites found in this study could be identified to species. It is likely they represent undescribed species, but more studies are needed, because material collected was insufficient for identification to species level.
Proctophyllodes sp. (Analgoidea: Proctophyllodidae) inhabit primary and secondary wing and tail feathers and are highly adapted to these microhabitats by having enlarged and flattened bodies with well-developed dorsal plates (Mironov et al, 2008). The genus Proctophyllodes Robin, 1877 is the most species-rich genus among feather mites and currently includes more than 160 species infecting over 20 Passeriform families world-wide (Atyeo and Braasch, 1966; Kanegae et al., 2008). Although mites of this genus have been reported from birds belonging to the Icteridae family (Černý, 1974), this study gives the first record from S. loyca.
As the previous mite, Amerodectes sp. (Analgoidea: Proctophyllodidae) inhabits primary and secondary wing and tail feathers. Currently, the genus Amerodectes Mironov, 2008 includes 22 described species that infect birds from 9 New World Passeriform families: Cardinalidae, Emberizidae, Furnariidae, Icteridae, Parulidae, Thraupid ae,Troglodytidae, Turdidae, and Tyrannidae (Valim and Hernades, 2010; Mironov and González-Acuña, 2011). Because of the high host specificity of these parasites, it is likely that the individuals found in this study belong to a different, yet undescribed species.
Mesalgoides sp. (Analgoidea: Psoroptoididae) inhabits the lower portion of down feathers. A total of 13 Mesalgoides Gaud and Atyeo, 1967 species have been described from Passeriform birds belonging to the families Emberizidae, Fringillidae, Furnariidae, Icteridae, Mimidae, Pipridae, Thraupidae, Turdidae, and Tyrannidae worldwide (Gaud and Atyeo, 1996; Mironov, 2004; Kanegae et al., 2008). Only 2 species of the genus Mesalgoides have been reported previously from icterids of the genus Ageilais by Černý (1974).
Mites of the genus Harpyrhynchoides Fain, 1972 (Cheyletoidea: Harpyrhynchidae) inhabit the skin of birds and some snakes (Colubridae) and feed on lymph. Thirty-three species infecting 12 orders of birds are known (Fain, 1994; Fain et al., 1999; Bochkov, 2000; Bochkov et al., 2000; Bochkov and Galloway, 2004). This is the first report of this mite in S. loyca.
Helminths. The acanthocephalan genus Mediorhynchus Van Cleave, 1916 (Gigantorhynchida: Giganthorhynchidae) comprises about 50 species, which are relatively common in Passeriformes world-wide (Schmidt and Kuntz, 1977; Golvan, 1994; Smales, 2002; Smales, 2011). Moya et al. (2011) described M. peruensis from Turdus chiguanco in Peru and compared it to 4 other species reported from South America. However, the species collected here more closely resembles M. robustus Van Cleave, 1916 in total number of hooks and spines, number of rows of hooks and spines, and length of the largest hooks (38 microns). This species was originally described from the intestines of Icteria virens in Washington, United States (Van Cleave, 1947). This constitutes the first record of M. robustus in Chile and in S. loyca.
Similarly to what was found in the present study, the abundance of Mediorhynchus is usually very low, with only 1 parasite per host (Van Cleave, 1947). The intermediate hosts for this acanthocephalan are unknown, but cystacanths of M. robustus have been reported in Japan from Nyctereutes procyonoides (Carnivora: Canidae), which probably represents a dead end host since all known final hosts for this acanthocephalan are Passeriformes (Sato et al., 2006).
]]> Anonchotaenia Cohn, 1900 (Cyclophyllidea: Paruterinidae) is a cosmopolitan genus of cestodes primarily parasitizing birds of the Order Passeriformes. Schmidt (1986) listed 20 species in the genus and 2 additional species have subsequently been described from India. Species are primarily differentiated by the number and distribution of testes. The species collected here with 8 testes distributed in a continuous group most closely resembles A. longiovata (Fuhrmann, 1901), which has previously been reported from the Chilean blackbird, Curaeus curaeus (Icteridae) according to Rausch and Morgan (1947). This is the first record of this helminth in S. loyca.
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