Gastrointestinal and external parasites of the white-crested elaenia Elaenia albiceps chilensis ( Aves , Tyrannidae ) in Chile Parasitas gastrointestinais e externos de guaracava de crista branca Elaenia albiceps chilensis ( Aves , Tyrannidae ) de Chile

The objective of this study is to evaluate the ectoparasites and helminths of the white-crested elaenia, Elaenia albiceps chilensis. Feather mites Anisophyllodes elaeniae, Trouessartia elaeniae, and Analges sp. were detected in 51% of birds (n=106), whereas 24% were infected with lice (Tyranniphilopterus delicatulus, Menacanthus cfr. distinctus, and Ricinus cfr. invadens). Helminths Viguiera sp. and Capillaria sp. were found in five of the birds that were necropsied (n=20). With the exception of A. elaeniae, T. elaeniae, and T. delicatulus, all parasites represented new records found for the white-crested elaenia, and therefore for the Chilean repertoire of biodiversity.


Introduction
The knowledge of parasite-host associations provides vital information regarding the hosts, which should be taken into account in biodiversity and conservation initiatives (PÉREZ-PONCE DE LEON & GARCIA, 2001).The winter range of the whitecrested elaenia Elaenia albiceps d'Orbigny and Lafresnaye, 1837 (Passeriformes: Tyrannidae) spans from southeastern Colombia to the Peruvian and Brazilian Amazonian regions, and is mainly represented by the subspecies E. albiceps chilensis Hellmayr, 1927(ARAYA & MILLIE, 2000;COUVE & VIDAL, 2003).In Chile, this bird is present from spring to fall, where it is known to reproduce throughout its entire geographic range (MARTÍNEZ & GONZÁLEZ, 2004;JARAMILLO, 2005).The subspecies E. albiceps modesta Tschudi, 1844 has been recorded near Arica (MARTÍNEZ & GONZÁLEZ, 2004), in the valleys and oases of the Tarapacá Region, Chile northern (ARAYA & MILLIE, 2000).
Currently, only three studies have examined parasites in E. albiceps.Kellogg & Mann (1912) described a louse Physostomum fasciatus var.arcuatus from Tyrannus vociferous collected from Cerros Island in Baja California, which later transferred to Ricinus De Geer, 1778 by Hopkins and Clay (1952:324).Price et al. (2003) reported this species on E. albiceps, although no geographic location was reported.More recently, Mey (2004) described a new Ischnoceran louse, Tyranniphilopterus delicatulus, on E. albiceps modesta collected in Santa Cruz, central Chile.The identification of this host subspecies was likely made in error since the geographic distribution of E. albiceps modesta is restricted to northern Chile in Tarapacá (MARTÍNEZ & GONZÁLEZ, 2004).Thus, T. delicatulus was likely collected from E. albiceps chilensis, as it is a subspecies that inhabits central and southern Chile.Lastly, González-Acuña et al. (2005) reported immature stages of the tick Ixodes auritulus Newmann, 1904 on E. albiceps from Ñuble, Chile.Mironov and González-Acuña describes the species Anisophyllodes elaeniae and Trouessartia elaeniae from E. albiceps, in 2009 and 2013, respectively.Due to the scant amount of information on the parasitic fauna of the white-crested elaenia, the main goal of the present work was to conduct a study on the ecto-and endoparasitic fauna of this species during its spring and fall migratory periods in Chile.
Birds were necropsied using protocols described by Kinsella & Forrester (1972).Helminths were preserved in 70% ethanol.Nematodes were cleared in temporary mounts of lactophenol and were identified using different keys including those by Chabaud (1975), Moravec (1982), and Gibbons (2010), and the samples later were fixed in glycerin.The terminology that was used follows the work of Bush et al. (1997).All parasites have been deposited into the collection of the Zoology Laboratory, Faculty of Veterinary Science, University of Concepción, Chile.

Ectoparasites
Ectoparasites were found in 51% (n = 54) of the birds examined.A total of 227 mites were collected from 37 birds (34.9%), with 116 belonging to Trouessartia elaeniae (15.1%) -a recently described species by Mironov & González-Acuña (2013) (Acarina, Trouessartiidae) (Figures 2 and 3).The overall male to female ratio was 1.5 and the adult to juvenile ratio was 5.8.The mites were collected in Chillán, Santa Elena Lagoon, Huemules del Niblinto National Reserve, Los Peucos, Santa Juana, Santa Bárbara, La Mina, Altos de Lircay National Reserve, Parque Inglés, La Campana National Park, and El Yali National Reserve.One hundred and one specimens were identified as Anisophyllodes elaeniae Mironov and González-Acuña, 2009 (Acarina, Proctophyllodidae) (21.4%) (Figures 4 and 5), The overall male to female ratio was 0.33 and the adult to juvenile ratio was 10.2, they were collected in Bosques Fray Jorge National Park, Chillán, Santa Elena Lagoon, Huemules del Niblinto National Reserve, Los Peucos, Santa Juana, Santa Bárbara, La Mina, Altos de Lircay National Reserve, Parque Inglés, La Campana National Park, and Lago Peñuelas National Reserve.The remaining ten specimens belonged to the genus Analges Nitzsch, 1818 (3.3%), and they possibly represented a new species.These mites were found in the breast and rump of three birds collected in Santa Elena Lagoon, La Mina, and La Campana National Park.
Mites of the family Trouessartiidae are known to parasitize birds belonging to the orders Caprimulgiformes, Coraciiformes, Cuculiformes, Piciformes and Passeriformes (PROCTOR, 2003;HERNANDES, 2014).The genus Trouessartia Canestrini, 1899 is the most species-rich one in the family, and there are currently over 100 species that have been counted, which have been collected from bird species belonging to 28 families of Passeriformes (GAUD & ATYEO, 1996; MIRONOV & GONZÁLEZ-ACUÑA, 2013).Five species, including T. elaeniae, have been recorded so far from birds of the family Tyrannidae (SANTANA, 1976;HERNANDES, 2014).
The family Proctophyllodidae includes mites that predominately parasitize Passeriformes and hummingbirds, with a few species  The feather mites of the genus Analges, as is the case for all representatives of the family Analgidae, live exclusively on passerines and are mainly located in the hosts' downy and body covert feathers.Given their location in the plumage of hosts, analgids are a quite difficult group of feather mites to collect from live birds, and even from museum skins.The genus Analges is also the most abundant genus of the family, and it currently includes over 50 species, most of which are known from passerines of the Old World.To date, only one species, Analges tyranni Tyrrell, 1882, was recorded on a tyrannid host, Tyrannus tyrannus Linnaeus, 1758 in Canada.
Lice of the genus Tyranniphilopterus Mey, 2004 are represented by 14 species, half of which are known as parasites of birds belonging to the family Tyrannidae (CICCHINO, 2007).These lice inhabit and lay their eggs in the plumage of the head of their passeriform hosts, which belong to the families Pipridae, Cotingidae, Tyrannidae, and Platysteiridae (MEY, 2004).
The genus Ricinus De Geer, 1778 is composed of 72 species that are characterized by a relatively large size (3.1-5.3 mm), and which feed on blood, although some of them may complement their diet with feathers.They infest avian hosts belonging to at least 30 Passeriforme families (CICCHINO & CASTRO, 1998).The two heavily pigmented Ricinus female specimens collected from E. albiceps chilensis belong to the invadens species group sensu Nelson, 1972, but details of their pigmentation, cephalic chaetotaxy, and dimensions do not fit well with those typical of the only species included in this group, Ricinus invadens Kellogg, 1899(NELSON, 1972).This species, primarily described as a member of the family Pipridae, has been collected from birds of at least three genera in this family, and also from one member of the family Tyrannidae, Anairetes parulus (Kittlitz, 1830) (PRICE et al.,  1912), which is widely distributed on several tyrannid hosts, has also been recorded on this same host (PRICE et al., 2003).A larger number of specimens, including males, is required for the proper identification of the taxa recorded here.

Endoparasites
Of the 20 E. albiceps chilensis necropsied, five harbored a total of 14 nematodes.Thirteen of these (93%) were identified as Viguiera sp.Seurat, 1913 (Nematoda: Habronematidae) and were found in the small intestine of the white-crested elaenia from Chillán.The specimens were not identified due to the lack of sufficient material.All individuals were adults (eight males, five females), with a male to female ratio of 1.6.No females were gravid, which could indicate that E. albiceps chilensis may not be the true definitive host for this nematode.The genus Viguiera includes 20 species (NANDI, 2005), some of which parasitize Passeriformes of the families Cuculidae (Cuculiformes) and Paridae (Passeriformes) in the United States (PENCE, 1973).Viguiera buckleyi (Chabaud, 1957) has been reported on Nectarinia pulchella incidipectus (Passeriformes: Nectariniidae) in Africa (CANARIS & GARDNER, 2002).In addition, nine Viguiera species have been described from India (NANDI, 2005).In South America, Viguiera osmanhilli Yeh, 1955 has been reported from Cyanerpes cyaneus Linnaeus, 1766 (Passeriformes: Thraupidae) in Brazil (Yeh, 1954).
A single male of the nematode genus Capillaria sens.lat.Zeder, 1800 (Nematoda, Trichuridae) was also recovered from the small intestine of the white-crested elaenia from Chillán.This genus, which is characterized by the absence of caudal alae and a spiny spicule sheath in the male, is known to infect the gastrointestinal tract of all vertebrate groups (MORAVEC, 1982).Identification at the species level could not be made on the basis of the single specimen found.
Infection and infestation parameters of parasites of E. albiceps chilensis are shown in Table 1.
With the exception of A. elaeniae, T. elaeniae, and T. delicatulus, all of the parasites reported here represent new parasitological records for E. albiceps chilensis and for the Chilean repertoire of biodiversity.

Figure 1 .
Figure 1.Map of Chile showing the sampling locations.