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Revista Brasileira de Parasitologia Veterinária

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

Rev. Bras. Parasitol. Vet. vol.28 no.3 Jaboticabal July/Sept. 2019  Epub Sep 16, 2019

http://dx.doi.org/10.1590/s1984-29612019067 

Original Article

External and intestinal parasites of the Austral thrush Turdus falcklandii (Aves, Turdidae) in central Chile

Parasitas externos e intestinais do tordo-austral Turdus falcklandii (Aves, Podicipedidae) no Chile

Sebastián Llanos-Soto1  2 

Mabel Córdoba1 

Lucila Moreno3 

John Mike Kinsella4 

Sergey Mironov5 

Armando Cicchino6 

Carlos Barrientos7 

Julio San Martín-Ordenes1 

Daniel González-Acuña1  * 
http://orcid.org/0000-0002-2397-2991

1Laboratorio de Parásitos y Enfermedades de Fauna Silvestre, Departamento de Ciencia Animal, Facultad de Ciencias Veterinarias, Universidad de Concepción, Chillán, Chile

2Laboratorio de Vida Silvestre, Departamento de Ciencia Animal, Facultad de Ciencias Veterinarias, Universidad de Concepción, Chillán, Chile

3Laboratorio de Ecología Parasitaria, Departamento de Zoología, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Concepción, Chile

4HelmWest Lab, Missoula, Montana USA

5Zoological Institute, Russian Academy of Sciences, Universitetskaya Embankment 1, Saint Petersburg, Russia

6Universidad Nacional de Mar del Plata, Mar del Plata, Argentina

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

Abstract

A total of thirty Austral thrushes Turdus falcklandii Quoy & Gaimard, 1824 (Turdidae) carcasses were brought to the Departamento de Ciencia Animal, Facultad de Ciencias Veterinarias, Universidad de Concepción, to be examined for ecto- and endoparasites. Ectoparasites were found on 20% (6/30) of the thrushes and belonged to species Brueelia magellanica Cichino, 1986 (Phthiraptera), Menacanthus eurysternus Burmeister, 1838 (Phthiraptera) and Tyrannidectes falcklandicus Mironov & González-Acuña, 2011 (Acari). Endoparasites were isolated from 26.6% (8/30) of the birds and identified as Lueheia inscripta Westrumb, 1821 (Acanthocephala), Plagiorhynchus cylindraceus Goeze, 1782 (Acanthocephala), Wardium sp. sensu Mayhew, 1925 (Cestoda), Dilepis undula (Cestoda) Schrank, 1788, and Zonorchis sp. (sensu Travassos, 1944) (Trematoda). To our knowledge, all endoparasites collected in this study are new records in T. falcklandii and expand their distributional range to Chile.

Keywords:  Acanthocephala; Acari; Cestoda; Phthiraptera; Trematoda; Turdidae

Resumo

Um total de trinta carcaças do tordo-austral Turdus falcklandii Quoy & Gaimard, 1824 (Turdidae) foi encaminhado ao Departamento de Ciência Animal, Facultad de Ciencias Veterinarias, Universidad de Concepción, para ser examinado quanto a presença de parasitas externos e internos. Parasitas externos foram encontrados em 20% (6/30) dos tordos inspecionados e identificados como Brueelia magellanica Cichino, 1986 (Phthiraptera), Menacanthus eurysternus Burmeister, 1838 (Phthiraptera), e Tyrannidectes falcklandicus Mironov & González-Acuña, 2011 (Acari). Parasitas internos foram identificados em 26,6% (8/30) dos espécimes examinados como Lueheia inscripta Westrumb, 1821 (Acanthocephala), Plagiorhynchus cylindraceus Goeze, 1782 (Acanthocephala), Wardium sp. sensu Mayhew, 1925 (Cestoda), Dilepis undula sensu Schrank, 1788 (Cestoda) e Zonorchis sp. (sensu Travassos, 1944) (Trematoda). Tanto quanto é do nosso conhecimento, todos os parasitas internos coletados neste estudo pertencem a novos registros em T. falcklandii e com expansão de sua distribuição para o Chile.

Palavras-chave:  Acanthocephala; Acari; Cestoda; Phthiraptera; Trematoda; Turdidae

Introduction

The family Turdidae is composed of more than 300 species distributed on most continents. Only five thrush species have been recorded in Chile: The veery Catharus fuscescens Stephens, 1817; the wood thrush Hylocichla mustelina Gmelin, 1789; the Chiguanco thrush Turdus chiguanco Lafresnaye & d’Orbigny, 1837; the creamy-bellied thrush T. amaurochalinus Cabanis, 1851; and the Austral thrush T. falcklandii Quoy & Gaimard, 1824, with only T. chiguanco and T. falcklandii being residents (MARTÍNEZ & GONZÁLEZ, 2004). Turdus falcklandii is an abundant bird of urban and rural areas of Chile, including city gardens and orchards (CHESTER, 2008) and Nothofagus forests of the central and south areas of the country (JARAMILLO, 2005; CHESTER, 2008). It is an omnivorous species, spending most of its time feeding from fruits on trees or preying on invertebrates on the ground (ROZZI et al., 1996). It is distributed from Antofagasta (23°37’ S, 70°23’ W) to Cape Horn (55°59’ S, 67°15 W), with subspecies T. f. magellanicus (King 1831) ranging from Chañaral (26°20 S, 70°37 W) to Cape Horn and T. f. mochae (Chapman, 1934) found only in the Isla Mocha National Reserve (38°22’ S, 73°54’ W) (CHESTER, 2008).

Currently, T. falcklandii does not face any conservation issues with a stable population size and large distributional range. However, there is a lack of information about parasites carried by this species. To this date, the only descriptions of ectoparasites are Dasypsyllus stejnegeri Smit, 1976 (Siphonaptera: Ceratophyllidae) in the Falkland/Malvinas Islands (HASTRITER & SCHLATTER, 2006), Tyrannidectes falcklandicusMironov & González-Acuña 2011 (Acari: Proctophyllolidae) in central Chile (MIRONOV & GONZÁLEZ-ACUÑA, 2011), Ixodes auritulus Neumann, 1904 (Acari: Ixodidae) in southern Chile (GONZÁLEZ-ACUÑA et al., 2005), Brueelia magellanica Cicchino, 1986 (Phthiraptera: Philoptheridae) in central Chile (CICCHINO, 1986; GONZÁLEZ-ACUÑA et al., 2006), and Menacanthus eurysternus Burmeister, 1838 (Mallophaga: Menoponidae) in central and southern Chile (GONZÁLEZ-ACUÑA et al., 2006). Regarding endoparasites, Hymenolepis fernandensis Nybelin, 1929 (Cestoda: Hymenolepididae) was described on Robinson Crusoe Island (Chile), the only internal parasite documented for this thrush (NYBELIN, 1929). The main purpose of this study is to identify ecto- and endoparasites of the Austral thrush T. falcklandii in Chile.

Materials and Methods

Thirty thrush carcasses were collected in different localities of the Biobío region, Chile, in the period 2004–2010. Carcasses were brought to the Departamento de Ciencia Animal, Facultad de Ciencias Veterinarias, Universidad de Concepción, Chillán, and stored at -20°C until examination. Thrushes examined in this study died of anthropogenic causes common to birds living in the countryside, such as poisoning, dog attacks, and illegal hunting.

External inspection of carcasses included a rigorous examination of their feathers in search of ectoparasites. Specimens found were preserved in ethanol (70%) for future identification. Lice (Phthiraptera) collected were processed using KOH (20%) and dehydrated in a series of alcohols (40, 80 and 100%) and then mounted using Canada balsam as described in Price et al. (2003). Mites (Acari) were cleared using Nesbitt’s solution (40g 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). Ectoparasites species and sex were identified using keys indicated in Burmeister (1838) and Cicchino (1986, 1987). To evaluate the presence of endoparasites, thrushes were necropsied following procedures described in Kinsella & Forrester (1972). Acanthocephala were cleared in temporary mounts of 80% phenol, identified, and then returned to the preservative. Cestodes and trematodes were and stained in Semichon’s carmine stain and mounted in Canada balsam (PRITCHARD & KRUSE, 1982). Helminths were identified following descriptions in Yamaguti (1958, 1959, 1963) and Khalil et al. (1994).

Basic population parameters of prevalence, mean intensity, range, and mean abundance were calculated for ectoparasites and endoparasites collected. Prevalence was defined as the percentage of hosts infested by a particular parasite species. Mean intensity is represented by the mean number of parasites found in infected hosts. Range is the difference in the number of parasites collected in the most and least infested/infected hosts. Mean abundance is the number of individuals of a particular parasite from single host. Calculations were performed according to Bush et al. (1997). Additionally, ecto- and endoparasites collected were digitally measured using KS100 Imaging system 3.0 (Carl Zeiss Vision GmbH, Hallbergmoos, Germany).

Results and Discussion

Ectoparasites

Ectoparasites were present on 20% (6/30) of the thrushes examined. Lice were identified on 20% (6/30) with a total of 672 individuals collected. Mites were found on 3.3% (1/30) of the birds examined with only a single specie of mite collected. Population parameters for ectoparasites are indicated in Table 1.

Table 1 Range, mean intensity, mean abundance and prevalence of ectoparasites collected from the Austral thrush (Turdus falcklandii), Chile. 

Species N° of birds examined Positive birds N° of parasites collected Range Mean intensity Mean abundance Prevalence (%)
Phthiraptera
Brueelia magellanica 30 3 29 2-25 9.7±13.3 0.97±4.6 10.0
Menacanthus eurysternus 30 5 643 2-266 128.6±136.0 21.43±70.2 16.7
Acariformes
Tyrannidectes falcklandicus 30 1 30 1-30 30±5.5 0.1 3.3

Phthiraptera

Brueelia magellanica

Brueelia is a diverse genus composed of approximately 276 species (CICCHINO & CASTRO, 1998; PRICE et al., 2003). In South America, 37 representatives of the genus have been documented to parasitize birds of the families Icteridae, Emberizidae, Mimidae, Thraupidae, Turdidae, and Picidae (CARRIKER, 1963; CICCHINO, 1979, 1982, 1983, 1986, 1990, 2004; CASTRO & CICCHINO, 1996; CICCHINO & CASTRO, 1996; GONZÁLEZ-ACUÑA et al., 2006; VALIM & PALMA, 2006; CICCHINO & GONZÁLEZ-ACUÑA, 2008, 2009; CUNHA et al., 2013; GOMEZ-PUERTA & CRIBILLERO, 2015; VALIM & CICCHINO, 2015). In this study, the presence of B. magellanica was found in T. falcklandii (Figure 1). A total of 10 males, 13 females (23 adults), and 6 nymphs were identified with a female/male ratio of 1.3 and a nymph/adult ratio of 0.2. Body measures for B. magellanica are indicated in Table 2. Brueelia magellanica has been previously recorded for T. falcklandii in Argentina and south-central Chile (CICCHINO, 1986; CICCHINO & CASTRO, 1996; GONZÁLEZ-ACUÑA et al., 2006). González-Acuña et al. (2006) suggest that B. magellanica has a broader distribution in Chile and parasitizes more Turdidae. They also indicate that many other Brueelia species are probably present on Chilean birds.

Figure 1 Female (A) and male (B) adult Brueelia magellanica (100x magnification). 

Table 2 Mean body measures (μm) of Brueelia magellanica and Menacanthus eurysternus collected from the Austral thrush (Turdus falcklandii), Chile. 

Brueelia magellanica Menacantus eurysternus
Sex Male (n=10) Female (n=13) Male (n=128) Female (n=343)
Body structure Length Width Length Width Length Width Length Width
Head 396 396.2 416.25 412.87 456.99 466.98 273.67 508.09
Thorax 118.4 260.2 155.75 385.38 166.53 354.30 178.86 388.80
Pterothorax 98.2 345.9 150.12 351.45 106.26 340.41 115.17 342.62
Abdomen 990.6 559 1176.3 616.62 967.86 545.99 1169.92 640.07
Genitalia 195 375.75

Menacanthus eurysternus

The genus Menacanthus Neumann, 1912 is composed of 94 parasite species hosted by birds from the orders Pelecaniformes, Passeriformes, Piciformes, Tinamiformes, and Galliformes (PRICE et al., 2003; PRICE, 1975; PRICE & EMERSON, 1975; PRICE et al., 2003). In South America, a total of 34 genus have been reported parasitizing birds from the families Cracidae, Tinamidae, Ramphastidae, Odontophocidae, Picidae, Galbulidae, Tyrannidae, Thraupidae, Pipridae, Turdidae, Grallariidae, Capitonidae, Mimidae, Cardinalidae, Icteridae, and Troglodytidae (PRICE, 1975; PRICE & EMERSON, 1975; PRICE et al., 2003; KUABARA & VALIM, 2017). The presence of M. eurysternus was accounted in the thrushes examined with 343 males, 128 females (471 adults), and 172 nymphs identified and a female/male ratio and nymph/adult ratio of 2.67 and 0.4, respectively (Figure 2). Body measurements for both B. magellanica and M. eurysternus are indicated in Table 2. González-Acuña et al. (2006) previously recorded M. eurysternus on T. falcklandii in Chile. The louse M. eurysternus is a cosmopolitan and generalist parasite of 176 bird species from 20 families around the world (PRICE et al., 2003). In America, it has been found on Sturnus vulgaris (Sturnidae), Colaptes auratus (Picidae), Cyanocitta cristata (Corvidae), Pica hudsonia (Corvidae), Turdus migratorius (Turdidae), Passer domesticus (Passeridae), Acanthis flammea (Fringillidae), Quiscalus quiscula (Icteridae), and Icterus galbula (Icteridae) in Canada (PRICE, 1975; FAIRN et al., 2014; GALLOWAY et al., 2014); Peucaea carpalis (Emberizidae), Aphelocoma coerulescens (Corvidae), C. cristata, C. stelleri, Cyanocorax yncas (Corvidae), Pica pica (Corvidae), Cardinalis cardinalis (Cardinalidae), Pheucticus ludovicianus (Cardinalidae), P. domesticus, S. vulgaris, Junco hyemails (Passerellidae), Pipilo chlorurus (Passerallidae), Seiurus aurocapilla (Parulidae), Setophaga ruticilla (Parulidae), Toxostoma bendirei (Mimidae), Tx. redivivum, Tx. rufum, Mimus polyglottos (Mimidae), Molothrus aeneus (Icteridae), M. ater, I. galbula, Q. quiscula, Agelaius phoeniceus (Icteridae), Dryobates pubescens (Icteridae), H. mustelina, T. migratorius, Sialia mexicana (Turdidae), Zonotrichia leucophrys (Passerellidae), and Z. querula in the United States (PRICE, 1975; NELDER & REEVES, 2005); Chlorospingus flavopectus (Passerellidae), Arremon brunneinucha (Passerellidae), Mitrospingus cassinii (Thraupidae), Tangara dowii (Thraupidae), Turdus assimilis (Turdidae), T. grayi, and T. nigrescens in Costa Rica (PRICE, 1975; LINDELL et al., 2002; SYCHRA et al., 2007; MARTINŮ et al., 2015), Thraupis bonariensis bonariensis (Thraupidae), T. amaurochalinus and Manacus manacus (Pipridae) in Argentina (CASTRO & CICCHINO, 1978, 1996; CICCHINO, 2007); Manacus manacus, Turdus leucomelas, T. amaurochalinus, and T. rufiventris in Brazil (ENOUT et al., 2009; CUNHA et al., 2013; MARTINŮ et al., 2015); Grallaria ruficapilla (Grallaridae) and Eubucco richardsoni (Capitonidae) in Peru (PRICE, 1975; CLAYTON et al., 1992); Chiroxiphia lanceolata (Pipridae), Grallaria quitensis (Grallaridae), Mimus gilvus (Mimidae), and Pelecanus occidentalis (Pelecanidae) in Colombia (PRICE, 1975; PARRA-HENAO et al., 2011); M. gilvus in Venezuela (PRICE, 1975), M. polyglottos in Cuba (PRICE, 1975); and T. amaurochalinus in Bolivia (PRICE, 1975).

Figure 2 Female (A) and male (B) adult Menacanthus eurysternus (100x magnification). 

Acari

Tyrannidectes falcklandicus

The genus Tyrannidectes Mironov, 2008 (Analgoidea: Proctophyllolidae) appears to be restricted to passerine birds of the New World, with eleven species distributed along the American continent (VALIM & HERNANDES, 2010; MIRONOV & GONZÁLEZ-ACUÑA, 2011). Previous reports detail the presence of Tyrannidectes crassus Trouessart, 1885; Tyrannidectes pteroptochi Mironov & González-Acuña, 2015; Tyrannidectes anairetes Mironov & González-Acuña, 2011; Tyrannidectes cinclodes Mironov & González-Acuña, 2011; Tyrannidectes berlai Mironov, 2008; Tyrannidectes fissuratus Hernandes & Valim, 2005; Tyrannidectes synallaxis Hernandez et al., 2016; Tyrannidectes amaurochalinus Hernandes & Valim, 2006; and Tyrannidectes reticulatus Černý, 1974 in South America (TROUESSART, 1885; MIRONOV et al., 2008; VALIM & HERNANDES, 2008; VALIM & HERNANDES, 2010; BARRETO et al., 2012; ENOUT et al., 2012; MIRONOV & GONZÁLEZ-ACUÑA, 2015; HERNANDES et al., 2016); T. berlai in Central America (SARI et al., 2013); and T. banksi in Sayornis phoebe (Tyrannidae) in North America (VALIM & HERNANDES, 2010; GALLOWAY et al., 2014).

Tyrannidectes falcklandicus Mironov & González-Acuña, 2011 was the only mite species identified on T. falcklandii in this study (Figure 3). Mironov & González-Acuña (2011) have previously recorded T. falcklandicus on Turdus falcklandii in Chile.

Figure 3 Male (A) and female (B) adult Tyrannidectes falcklandicus (400x magnification). 

Endoparasites

Of the birds examined, 26.6% (8/30) were host to at least one kind of endoparasite. Two Acanthocephala, two Cestoda, and a single Trematoda were identified. Population parameters for endoparasites are indicated in Table 3.

Table 3 Range, mean intensity, mean abundance and prevalence of endoparasites collected from the Austral thrush (Turdus falckandii), Chile. 

Species N° of birds examined Positive birds N° of parasites collected Range Mean intensity Mean abundance Prevalence (%)
Acantocephala
Lueheia inscripta 30 2 34 1-22 17±14.8 1.13±4.0 6.7
Plagiorhynchus cilindraceus 30 2 7 3-4 3.5±0.7 0.23±0.9 6.7
Cestoda
Wardium sp. 30 6 27 1-11 4.5±1.4 0.9±2.7 20
Trematoda
Zonorchis sp. 30 1 1 1-1 1 0.03 3.3

Acanthocephala

Lueheia inscripta

The genus Luehia Travassos, 1920 (Acanthocephala: Plagiorhynchidae) is composed of only four species present in the American continent, L. adlueheia Werby, 1938 in North America; L. cajabambensis Machado & Ibañez, 1967 and L. lueheia Travassos, 1919 in South America; and L. inscripta Westrumb, 1821 reported in North, Central and South America (GOLVAN, 1994; SALGADO-MALDONADO & CASPETA-MANDUJANO, 2010). Lueheia inscripta (Figure 4) was found in 6.7% (2/30) of the thrushes. This acanthocephalan parasitizes birds mainly from the Turdidae family but also infects lizards and anurans as paratenic hosts (TRAVASSOS, 1926; WHITTAKER et al., 1970; ACHOLONU, 1976). Information about the life cycle of L. inscripta and its possible intermediary hosts is still limited; however, it is known that transmission of this acanthocephalan occurs through ingestion of infected cockroaches (ACHOLONU, 1976). Lueheia inscripta has been described in Platycichla flavipes (Turdidae), Turdus rufiventris, T. albicollis, T. leucomelas, T. amaurochalinus, and T. fumigatus in Brazil (TRAVASSOS, 1926; CALEGARO-MARQUES & AMATO, 2010), T. grayi in Nicaragua (SCHMIDT & NEILAND, 1966), Quiscalus niger (Icteridae) and Anolis cristatellus (Squamata) in Puerto Rico (WHITTAKER et al., 1970; ACHOLONU, 1976), and Leptodactylus fragilis (Anura) and Bufo marinus (Anura) in Mexico (SALGADO-MALDONADO & CASPETA-MANDUJANO, 2010). This is the novel report of L. inscripta in Turdus falcklandii expanding its distributional range to Chile.

Figure 4 Proboscis morphology of Lueheia inscripta (100X magnification). 

Plagiorhynchus cylindraceus

The subgenus Plagiorhynchus Lühe, 1911 (Acanthocephala: Plagiorhynchidae) is composed of 12 validated species, amongst them P. (P.) crassicollis Villot, 1875; P. (P.) odhneri Lundström, 1942; P. (P.) charadrii Yamaguti, 1939; P. (P.) charadriicola Dollfus, 1953; P. (P.) allisonae Skuballa et al. 2010; P. (P.) menurae Johnston, 1912; P. (P.) cylindraceus Goeze, 1782; P. (P.) lemnisalis Belopol'skaia, 1959; P. (P.) linearis Westrumb, 1891; P. (P.) paulus, P. (P.) spiralis and, P. (P.) totani (LISITSYNA, 1992; GOLVAN, 1994; SMALES, 2002; DIMITROVA, 2009). In this study, Plagiorhynchus cylindraceus Goeze, 1782 (Figure 5) was found in 6.7% (2/30) of the birds examined. It is a cosmopolitan internal parasite of birds, mostly passerines, but also infects mammals as paratenic hosts (SMALES, 2002). The life cycle of P. cylindraceus has been detailed in SCHMIDT & OLSEN (1964). The infected definitive host releases fully embryonated eggs through its feces, which are ingested by isopod intermediate hosts. The parasite increases its size and develops its organs in the intermediate host until it become infective. When the isopod is ingested by a bird, the parasite attaches itself to its gut wall. It was apparently introduced from Europe to North America, South America, Australia, New Zealand, Asia, and Africa (JONES, 1928; SCHMIDT & KUNTZ, 1966; AMIN et al., 1999; SMALES, 2002; SKUBALLA et al., 2010; VALENTE et al., 2014).

Figure 5 Proboscis morphology of Plagiorhynchus cilyndraceus (100X magnification). 

Plagiorhyinchus cylindraceus has been found in bird and mammal of various families: Sturnidae in Argentina (VALENTE et al., 2014), Scolopacidae in South Africa (AMIN et al., 1999), Procyonidae and Scolopacidae in Canada (CHING et al., 2000; DIDYK et al., 2007), Picidae, Mimidae, Turdidae, Emberizidae, Passerellidae, Anatidae, Phasianidae, Corvidae, Sturnidae, Icteridae, Didelphidae, and Soricidae in the United States (VAN CLEAVE, 1918; JONES, 1928; CUVILLIER, 1934; VAN CLEAVE, 1942; CHANDLER & RAUSCH, 1949; HUNTER & QUAY, 1953; SCHMIDT & OLSEN, 1964; ELTZROTH et al., 1980; MCDONALD, 1988; COADY & NICKOL, 2000; CARLETON et al., 2012; RICHARDSON, 2013), Strigiformes in Spain (FERRER et al., 2004), Erinaceidae in Czech Republic (PFÄFFLE et al., 2014), Turdidae and Sturnidae in Bulgaria (DIMITROVA et al., 2000), Sturnidae in Ukraine (LISITSYNA, 2010), Erinaceidae in United Kingdom and Germany (SKUBALLA et al., 2010), Turdidae in Poland (RZĄD et al., 2014), Charadriidae, Rallidae, Turdidae, Sturnidae, Corvidae, Monarchidae, Artamidae, Threskiornithidae, Peramelidae, Muridae, Canidae, Macropodidae, Dasyuridae, and Potoroidae in Australia (EDMONDS, 1989; SMALES, 2002), Erinaceidae in New Zealand (SKUBALLA et al., 2010), and Leiothrichidae, Turdidae, and Muscicapidae in Taiwan (SCHMIDT & KUNTZ, 1966). Infections in small mammals such as shrews are apparently dead ends since the parasites do not mature and passerines such as thrushes are unlikely to ingest these mammals. This is the first time that P. cylindraceus is reported in a native species of South America (T. falcklandii) and expands its range to Chile.

Cestoda

Wardium sp.

Wardium sp. sensu Mayhew, 1925 (Cestoda: Hymenolepididae) (Figure 6 and 7) was identified in 20% (6/30) of the birds examined. Wardium is a cosmopolitan genus of cestodes found mostly in shorebirds (Charadriiformes) but also in birds from the orders Podicipediformes Lariformes, Anseriformes, and Passeriformes (MCDONALD, 1969; BONDARENKO & KONTRIMAVICHUS, 1978; BONDARENKO, 1997). In South America, few species have been described: Wardium fernandensis in Turdus rufiventris from Brazil (CALEGARO-MARQUES & AMATO, 2010), W. neotropicale in Himantopus melanurus (Charadriidae) from Paraguay (DEBLOCK & VAUCHER, 1997), W. paucispinosum in Larus maculipennis (Laridae), and W. semiductilis in L. maculipennis and Larus dominicanus from Argentina (LABRIOLA & SURIANO, 2000). This is the first time that the genus Wardium is recorded in T. falckandii and Chile.

Figure 6 Wardium sp. Specimen (200X magnification). 

Figure 7 Scolex morphology of Wardium sp. (400X magnification). 

Dilepis undula

The genus Dilepis Weinland, 1858 is composed of only two species, D. brachyarthra and D. undula (JAMES & LLEWELLYN, 1967). Dilepis undula Schrank, 1788 (Cyclophyllidea: Dilepididae) (Figure 8) was observed in a single thrush (1/30) examined. Dilepis undula) is a cosmopolitan cestode that parasitizes the small intestine of passerine birds and mammals (HAUKISALMI, 2015). Its life cycle includes earthworms as intermediate hosts (RYSAVÝ, 1973). Dilepis undula parasitizes different species of the genus Turdus, T. rufiventris in Brazil (CALEGARO-MARQUES & AMATO, 2010), T. pilaris in Ukraine, Finland, Germany, and United Kingdom (GÄSSLEIN, 1954; JENNINGS & SOULSBY, 1957; METTRICK, 1958; RAITIS, 1968; ŚWIDERSKI et al., 2000), T. merula in Ukraine, Czech Republic, United Kingdom, Poland, Israel, Spain, United States, Bulgaria, Russia, and New Zealand (DAVIES, 1938; GÄSSLEIN, 1954; PASPALEV & PASPALEVA, 1965; TARAZONA, 1974; WEEKES, 1982; SCHMIDT et al., 1986; ŚWIDERSKI et al., 2004; PETKEVIČIŪTĖ et al., 2006; OKULEWICZ & SITKO, 2012; RZĄD et al., 2014), T. iliacus in Finland (RAITIS, 1968), T. philomelos in Finland, Spain, United Kingdom, Germany, and New Zealand (DAVIES, 1938; GÄSSLEIN, 1954; TARAZONA, 1974; WEEKES, 1982; HAUKISALMI, 2015), T. viscivorus in Finland and the United Kingdom (METTRICK, 1958; PASPALEV & PASPALEVA, 1965; TARAZONA, 1974; HAUKISALMI, 2015), T. migratorius in the United States and Canada (SLATER, 1967; CHING, 1993), and T. grayi in Nicaragua (SCHMIDT & NEILAND, 1971). This is the first record of D. undula in T. falcklandii expanding its range to Chile. Sitko & Zaleśny (2014) indicated that D. undula is a dominant parasite species of T. merula in urban settings but is less prevalent in the individuals living in forests. This could also be the case for T. falcklandii, which possesses urban and natural populations in Chile.

Figure 8 Rostellum of Dilepis undula (200X magnification). 

Trematoda

Only a single Zonorchis sp. sensu Travassos, 1944 (Trematoda: Dicrocoeliidae) was collected from the thrushes examined. Zonorchis species are usually found in the gall bladder and bile ducts of birds and mammals all over the world, but predominantly in tropical countries of Central and South America (TRAVASSOS, 1945; THATCHER & PORTER, 1968). Zonorchis goliath has been found in Didelphis marsupialis (Didelphidae) and Saguinus geoffroyi (Callitrichidae); Z. confusus in Procnias nudicollis (Cotingidae) and Zonorchis spp. in Didelphis albiventris (Didelphidae) from Brazil (TRAVASSOS, 1945; TRAVASSOS et al., 1969; MELO, 2009; RAMOS et al., 2016); Z. microrchis in Psophia viridis (Gruiformes), Z. costaricensis in Gymnostinops montezuma (Icteridae) and Z. macroovarus in Pteroglossus torquatus (Ramphastidae) from Costa Rica (BRENES & JIMÉNEZ-QUIRÓS, 1959; JIMÉNEZ-QUIRÓS & ARROYO, 1960); Z. allentoshi in Caluromys derbianus (Didelphidae) and Z. goliath in S. geoffroyi and Aotus trivirgatus (Aotidae) from Panamá (THATCHER & PORTER, 1968; LAMOTHE-ARGUMEDO et al., 1997); Z. delectans in Gymnopithys leucaspis (Thamnophilidae), Myrmeciza hyperythra (Thamnophilidae), Schistocichla leucostigma (Thamnophilidae), Cymbilaimus lineatus (Thamnophilidae), Hypocnemis cantator (Thamnophilidae), Myrmoborus myotherinus (Thamnophilidae), M. axillaris (Thamnophilidae), M. hauxwelli, M. ornate, M. schisticolor, Phlegopsis erythroptera (Thamnophilidae), P. nigromaculata, Thamnomanes ardesiacus (Thamnophilidae) and Th. caesius, and Z. meyeri in Laterallus jamaicensis (Rallidae) in Ecuador (VERCAMMEN-GRANDJEAN, 1966; TALLMAN & TALLMAN, 1994). The only record of Zonorchis in the Turdus genus is Zonorchis petiolatus in the Czech Republic (SITKO & ZALEŚNY, 2014). This is the first time that a member of the Zonorchis genus is reported in a free-ranging species in Chile.

Acknowledgements

The authors would like to thank Catalina Ramírez and María Ignacia Bueno for their assistance during sample collection. Thank to Project FONDECYT 1170972.

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Received: March 22, 2019; Accepted: July 05, 2019

*Corresponding author: Daniel González-Acuña. Laboratorio de Parásitos y Enfermedades de Fauna Silvestre, Facultad de Ciencias Veterinarias, Universidad de Concepción, Casilla 537, 3812120, Chillán, Chile. e-mail: danigonz@udec.cl

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