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Revista Brasileira de Parasitologia Veterinária

Print version ISSN 0103-846XOn-line version ISSN 1984-2961

Rev. Bras. Parasitol. Vet. vol.24 no.3 Jaboticabal July/Sept. 2015

https://doi.org/10.1590/S1984-29612015053 

Original Article

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

Danny Fuentes 1  

Jaime Reyes 1  

María Soledad Sepúlveda 2  

Mike Kinsella 3  

Sergey Mironov 4  

Armando Cicchino 5  

Lucila Moreno 6  

Carlos Landaeta-Aqueveque 1  

Ignacio Troncoso 7  

Daniel González-Acuña 1   *  

1Facultad de Ciencias Veterinarias, Universidad de Concepción – UDEC, Chillán, Chile

2Department of Forestry and Natural Resources, Purdue University, West Lafayette, IN, USA

3Helm West Lab, Missoula, MT, USA

4Zoological Institute, Russian Academy of Sciences – RAS, Universitetskaya Embankment 1, Saint Petersburg, Russia

5Universidad Nacional de Mar del Plata – UNMDP, Mar del Plata, Argentina

6Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción – UDEC, Concepción, Chile

7Escuela de Medicina Veterinaria, Universidad Santo Tomás – USTA, Concepción, Chile


ABSTRACT

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.

Key words: Birds; Elaenia albiceps chilensis ; feather mites; Acarina; Phthiraptera; Nematoda

RESUMO

O objetivo deste estudo foi avaliar a fauna de ectoparasitas e helmintos do guaracava de crista branca Elaenia albiceps chilensis. Em 51% das aves (n=106), foram detectados os ácaros de pena Anisophyllodes elaeniae, Trouessartia elaeniae e Analges sp. enquanto 24% foram infectadas por piolhos (Tyranniphilopterus delicatulus, Menacanthus cfr. distinctus e Ricinus cfr. invadens. Em contrapartida, em cinco aves necropsiadas foram encontrados os helmintos Viguiera sp. e Capillaria sp. Com exceção de A. elaeniae, T. elaeniae e T. delicatulus, todos os parasitas representam novos registros para a guaracava de crista branca e, portanto, para a diversidade da fauna parasitária do Chile.

Palavras-Chave: Pássaros; Elaenia albiceps chilensis ; ácaros de penas; Acarina; Phthiraptera; Nematoda

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 white-crested 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 chilensisHellmayr, 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.

Materials and Methods

Over more than a decade (2001–2012), a total of 20 white-crested elaenias was collected from different Chilean localities ranging from the northern (Arica and Parinacota), central (Valparaíso), and southern (Biobío and Los Lagos) regions. All birds were found dead on roads after being struck by cars or by unknown causes.

Immediately after collection, the birds were frozen in sealed plastic bags until laboratory examination. Ectoparasites were preserved in 70% ethanol. Lice were mounted in Canada balsam following protocols described by Palma (1978) and Price et al. (2003). Mites were cleared in Nesbitt’s solution (40 g of chloral hydrate, 25 mL of distilled water, and 2.5 mL of hydrochloric acid) for 72 h and were later mounted in Berlese solution (KRANTZ, 1978). Phthiraptera were identified using papers by Kellogg & Mann (1912), Nelson (1972), and Mey (2004). Acarina were identified from keys published by Santana (1976), Gaud & Atyeo (1996) and Mironov & González-Acuña (2009).

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.

In addition, 106 specimens of E. albiceps chilensis were captured using mist nests (Permit number: 6082 23/11/2006; Servicio Agrícola y Ganadero). Captures occurred between 2006 and 2014 from the following locations: Huemules del Niblinto National Reserve (36°43’ S; 71°33’ W); Pemuco (36°36’ S; 72°06’ W), Los Peucos, Ñuble National Reserve (37°06’ S; 71°38’ W); Chillán Campus, University of Concepción (36°34’ S; 72°05’ W); highway El Itata (36°39’ S; 72°15’ W); El Carmen (36°54’ S; 72°01’ W); Santa Elena Lagoon (36°48’ S; 72°23’ W); Santa Bárbara (37°40’ S; 72°01’ W); Santa Juana (37°10’ S; 72°56’ W); Bosques Fray Jorge National Park (30°30’ S; 71°35’ W); Valle de Azapa (18°31’ S; 70°11’ W); Río Clarillo National Reserve (33°45’ S; 70°25’ W); La Mina (35°49’ S; 70°47’ W); Altos de Lircay National Reserve (36°36’ S; 71°03’ W); Siete Tazas National Park (35°27’ S; 71°01’ W); Parque Inglés (35°28’ S; 70°59’ W); Termas del Flaco (34°57’ S; 70°26’ W); Sierras de Bellavista (34°48’ S; 70°45’ W); La Patagua (34°42’ S; 71°21’ W); Til Til (33°04’ S; 70°56’ W); Ocoa, La Campana National Park (32°58’ S; 71°02’ W); Lago Peñuelas National Reserve (33°11’ S; 7°29’ W); and El Yali National Reserve (33°44’ S; 71°42’ W) (Figure 1). Once captured, the birds were measured, weighed, and exhaustively examined for the presence of ectoparasites. Only birds captured alive were considered for analysis of ectoparasites. All birds were ringed with a unique leg number and immediately released.

Figure 1 Map of Chile showing the sampling locations. 

Results and Discussion

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.

Figure 2 Trouessartia elaeniae: Male (A). Dorsal view.  

Figure 3 Trouessartia elaeniae: Female. Dorsal view.  

Figure 4 Anisophyllodes elaeniae: Female.  

Figure 5 Anisophyllodes elaeniae: Male.  

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 recorded from birds of the orders Gruiformes, Charadriiformes, and Psittaciformes (GAUD & ATYEO, 1996; PROCTOR, 2003). Relatively little is known regarding the diversity of proctophyllodid mites found on South American Passeriformes (HERNANDES et al., 2007; VALIM & HERNANDES, 2010; MIRONOV & GONZÁLEZ-ACUÑA, 2011). Three other known species of the genus Anisophyllodes Atyeo, 1967 are also associated with birds of the family Tyrannidae: A. pipromorphae has been reported from Mionectes oleagineus (Tyrannidae); A. intermedius on Elaenia martinica Linnaeus, 1766 and Elaenia flavogaster (Tyrannidae) (ČERNÝ & LUKOSCHUS, 1975); A. candango on Elaenia chiriquensis Lawrence, 1865 from Brazil (HERNANDES et al., 2007) and Anisophyllodes sp. on Elaenia chiriquensisand Mionectes rufiventris Cabanis, 1846 (Tyrannidae) (KANEGAE et al., 2008).

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 tyranniTyrrell, 1882, was recorded on a tyrannid host, Tyrannus tyrannus Linnaeus, 1758 in Canada.

Three species of lice totaling 78 specimens were found on 25 birds (24%). These included 65 specimens of Tyranniphilopterus delicatulus Mey, 2004 (Ischnocera: Philopteridae) (Figure 6), which were commonly found on the head and upper neck of 15 birds in Chillán, Altos de Lircay National Reserve, Parque Inglés, and La Campana National Park. Moreover, seven specimens (all nymphs) of Menacanthus cfr. distinctus Neumann, 1912 (Amblycera: Menoponidae) (Figure 7) were found on five white-crested elaenia birds from Chillán, Santa Bárbara, Sierras de Bellavista, and Altos de Lircay National Reserve. Finally, four specimens of Ricinus sp. (Figure 8) were found on three birds collected in Chillán and Valle de Azapa.

Figure 6 Tyranniphilopterus delicatulus: Male. Drawing by Armando Cicchino. 

Figure 7 Menacanthus distinctus: second nymphal instar (N II) male. Magnification 100×. 

Figure 8 Ricinus cfr. invadens: Female. Magnification 100×. 

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).

Menacanthus Neumann, 1912 is a cosmopolitan genus, which is known to parasitize birds in the orders Passeriformes, Galliformes, Piciformes, Tinamiformes, Coraciiformes, and Cuculiformes (PRICE et al., 2003). Menacanthus distinctus has been described as parasitizing the following species of Tyrannidae: Myiarchus tyrannulus Müller, 1776; M. cinerascensLawrence, 1851; M. ferox Gmelin, 1789; M. tuberculifer d'Orbigny and Lafresnaye, 1837; Rhytipterna simplex Lichtenstein, 1823; Contopus borealisSwainson, 1832; and Lathrotriccus euleri Cabanis, 1868 (PRICE et al., 2003). The specimens obtained were nymphs of the first (N I) and second instars (N II), and they were tentatively attributed to this species (here noted as M. cfr. distinctus) by direct comparison with the N II available from numerous males, females, and nymphs of M. distinctus from L. euleri collected in Buenos Aires Province, Argentina.

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., 2003). Another well-pigmented species belonging to another very different species group, Ricinus arcuatus (KELLOGG & MANN, 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.

Table 1 Infection and infestation parameters of endoparasites from 20 Elaenia albiceps chilensis, and ectoparasites from 126 same hosts, during 2001-2012. 

Parasite species Location in host Positive birds Mean intensity Range Abundance
(Prevalence) Mean Total
Endoparasites (n=20)
Nematoda
Viguiera sp. SI* 5 (25.0%) 2.6 0–5 0.65 13
Capillaria sp. SI* 1 (5.0%) 1 0–1 0.05 1
Ectoparasites (n=126)
Acari
Trouessartia elaeniae WT 19 (15.1%) 6.1 0–16 0.92 116
Anisophyllodes elaeniae WT 27 (21.4%) 3.7 0–22 0.80 101
Analges sp. AR 3 (2.4%) 3.3 0–5 0.08 10
Phthiraptera
Tyranniphilopterus delicatulus HN 15 (4.3%) 4.3 0–11 0.52 65
Menacanthus cfr. distinctus BD 5 (1.4%) 1.4 0–2 0.06 7
Ricinus cfr. invadens. BD 3 (1.3%) 1.3 0–2 0.03 4

*SI= small intestine, WT= wing and tail feathers, AR= abdomen and rump, HN= head and upper neck, BD= breast and dorsus.

With the exception of A. elaeniae, T. elaeniae, and T. delicatulus, all of the parasites reported here represent new parasitological records for E. albiceps chilensisand for the Chilean repertoire of biodiversity.

Acknowledgements

The authors wish to thank the Corporación Nacional Forestal for graciously providing its facilities in the various protected areas in Chile that we visited. In addition, we owe special thanks to Pablo Olmedo, Pedro Álvarez, Sebastián Muñoz, Braulio Muñoz, Iván Torres, Nicolás Fernández, Daniela Doussang, Gonzalo Torres, Cecilia Figueroa, Consuelo Manosalva, Carolina Silva, Nicolás Martín, Francisco González, Sofía González, and Karen Ardiles, for their valuable assistance during field work. This study was funded by the FONDECYT project number 1130948.

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Received: January 14, 2015; Accepted: May 26, 2015

*Corresponding author: Daniel González-Acuña. Universidad de Concepción – UDEC, Avenida Vicente Méndez, 595, Casilla 537, Chillán, Chile. e-mail: danigonz@udec.cl

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