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Introduction
The rufous-collared sparrow, Zonotrichia capensis Müller, 1776 (Emberizidae), inhabits almost all environments of the New World spanning from southern Mexico to Tierra del Fuego (Chile), excluding any areas covered with dense forests (CHESTER, 2008). This bird species can be found in cities and any other areas where forests have been cleared due to human activity; it also occurs at high altitudes, such as in the Altiplano (MILLER & MILLER, 1968). The bird’s feeding behavior is mostly frugivorous, but it also preys insects with some seasonal variations in its diet throughout the year (NOVOA et al., 1996). In Chile, Z. capensis is distributed from Arica (18°28'30”S, 70°18'52”W) to Tierra del Fuego (53°36'00”S, 69°23'00”W). Five subspecies of Z. capensis are endemic in Chile: Z. c. chilensis from Arica to Aysén; Z. c. antofagastae from Arica to Antofagasta; Z. c. australis in the Andes from Santiago to Aysén; Z. c. peruviensis in Arica; and Z. c. sanborni from Atacama to Valparaíso (CHESTER, 2008).
Currently, Z. capensis does not face any conservation issues due to its ability to exploit different environments. However, at present, there is limited information regarding the parasite fauna of South-American birds, and Z. capensis is no exception (HINOJOSA-SÁEZ & GONZÁLEZ-ACUÑA, 2005). Previous studies of ectoparasites associated with Z. capensis recorded a number of arthropods and helminths from this bird in South America: the louse fly Ornithoctona fusciventris Wiedemann, 1830 (Diptera: Hippoboscidae) in Brazil (GRACIOLLI & CARVALHO, 2003); mites Acarus batatas Linnaeus 1758 (Acari: Astigmata) in Guatemala (BRENNAN & DALMAT, 1960), Amerodectes zonotrichiae Mironov and González-Acuña, 2014 (Analgoidea: Proctophyllodidae) in Chile (MIRONOV & GONZÁLEZ-ACUÑA, 2014), Analges sp. (Analgoidea: Analgidae) and Pterodectes sp. (Analgoidea: Proctophyllodidae) (KANEGAE et al., 2008) in Brazil, Ornithonyssus bursa (Berlese, 1888) (Mesostigmata: Macronyssidae) in Argentina (SANTILLÁN et al., 2015), Mesalgoides sp. (Analgoidea: Psoroptoididae) in Brazil and Colombia (KANEGAE et al., 2008; BARRETO et al., 2012), and Trouessartia capensis Berla, 1959 (Analgoidea: Trouessartiidae) in Colombia, Argentina, Paraguay, and Brazil (SANTANA, 1976; KANEGAE et al., 2008; BARRETO et al., 2012); the lice Menopon laticorpus Carriker, 1903 (Phthiraptera: Menoponidae) in Costa Rica and Venezuela (PRICE et al., 2002) and Menacanthus bonariensis Burmeister, 1838 (Phthiraptera: Menoponidae) in Argentina (CICCHINO, 2003); and ticks Ixodes auritulus Neumann, 1904 (Acari: Ixodidea) in Chile (GONZÁLEZ-ACUÑA et al., 2005), Amblyomma aureolatum Pallas, 1772 (Acari: Ixodidae) in Brazil (GUGLIELMONE et al., 2003a), and A. triste Koch, 1844 in Argentina (NAVA et al., 2011). Endoparasites have rarely been reported in Z. capensis with records of Anonchotaenia zonotrichicola Dollfus, 1959 (Cestoda: Paruterinidae) in Peru (DOLLFUS, 1959); A. globata von Linstow, 1879 in an unspecified location of South America (RAUSCH & MORGAN, 1947); and Lubens lubens Braun, 1901 (Digenea: Dicrocoeliidae) in Brazil (TRAVASSOS et al., 1969).
The main purpose of this study is to document new records of the ecto- and endoparasites of the rufous-collared sparrow, Z. capensis, in Chile.
Materials and Methods
This study was performed in seven locations throughout northern and central Chile: Llanos del Challe National Park (28°10’S, 71°00’W); Las Chinchillas National Reserve (31°28’S, 71°03’W); Bosques de Fray Jorge National Park (30°39’S, 71°41’W); Lago Peñuelas National Reserve (33°10’S, 71°29’W); La Campana National Park (32°58’S, 71°05’W); Tiltil (33°05’S, 70°55’W); and Termas del Flaco (34°57’S, 70°25’W) (Figure 1).
Between April 2010 and August 2014, a total of 277 Z. capensis were caught using three mist nets in each locality (two 12 × 2.8 m nets and one 18 × 2.8 m net). The hosts were externally inspected with the naked eye and a magnifier in searching for ectoparasites. Feathers on the wings, tail, head, neck, flanks, back and abdomen were closely examined for ectoparasites. The birds were banded and released in the same place where they were captured. All capture and handling procedures were authorized by the Agricultural and Livestock Services (SAG; Resolution Nº2012).
Following collection, the ectoparasites were preserved in 70% ethanol. Lice were cleared using 20% KOH and ascending concentrations of ethanol solutions (40%, 70%, and 96%); they were subsequently mounted using Canada balsam, as indicated in Palma (1978) and Price et al. (2003). Lice were identified using the keys and descriptions of Price et al. (2003); moreover, the body measurements of these lice were taken. Mites were cleared using Nesbitt’s solution (40 g of chloral hydrate, 25 mL of distilled water, and 2.5 mL of hydrochloric acid) for 72 h, and then they were mounted in Berlese solution (KRANTZ, 1978). Mite identification was performed using keys constructed by Flechtman (1975) and Gaud & Atyeo (1996).
In addition to the birds examined in the field, seven carcasses of the rufous-collared sparrows from the Biobío region were necropsied for endoparasites using the protocols detailed in Kinsella & Forrester (1972). Acanthocephalans were cleared and studied in temporary mounts of 80% phenol and then returned to the preservative. These sparrows died for different reasons (i.e., they were either road killed, or they died as a result of predator attacks, poisoning, or illegal hunting), and they were subsequently brought to the Facultad de Ciencias Veterinarias of Universidad de Concepción, Chillán. Endoparasites were identified following the keys of Schmidt & Kuntz (1977) and Amin & Dailey (1998). Specimens collected were stored in the parasite collection from the Department of Animal Sciences, Universidad de Concepción, with access numbers CDCA-UDEC 132, CDCA-UDEC 133, CDCA-UDEC 134, CDCA-UDEC 135, CDCA-UDEC 136, and CDCA-UDEC 137.
The terminology used to describe parasitic assemblages (prevalence, mean intensity, and mean abundance) follows that of Bush et al. (1997). ‘Range’ displays the minimum and maximum number of individuals of a particular parasite species collected from the least and most infested hosts. The prevalence, mean intensity, mean abundance, and range were calculated for lice. In the case of mites, prevalence was the only estimated parameter, as it is extremely difficult to calculate accurately the abundance, range, and intensity of mites on live birds with the methods applied in this study. Population parameters were not obtained for ticks and endoparasites, because only a few individuals were collected for both groups of parasites. Ectoparasites collected from the seven rufous-collared sparrow carcasses were not considered for the numeric analysis, as in most cases, the parasites tended to abandon their former hosts after the host’s death.
Results and Discussion
Ectoparasites were found in 35.8% (99/277) of the rufous-collared sparrows examined in this study. The following groups of ectoparasites were recorded: three feather mite species from the suborder Astigmata; one chewing louse; and two ixodid tick species. In the case of endoparasites, a single specimen of Acanthocephala was recorded in two of seven necropsied sparrows.
Ectoparasites
Astigmata
Three feather mite species of the superfamily Analgoidea were found in 27.1% (75/277) of the sparrows examined. These mites were identified as Amerodectes zonotrichiae Mironov and González-Acuña, 2014 (Figure 2), Proctophyllodes polyxenus Atyeo and Braasch, 1966 (Analgoidea: Proctophyllodidae) (Figure 3) and Trouessartia capensis Berla, 1959 (Analgoidea: Trouessartiidae) (Figure 4).
Representatives of A. zonotrichiae were found on 1,44% (4/277) of bird specimens. These mites were found on vanes of the wing feathers of the sparrows (mainly primaries, secondaries, tertialis and rectrices), where they were located in corridors formed by barbs. These locations are the most common for feather mites of the family Proctophyllodidae (MIRONOV & GONZÁLEZ-ACUÑA, 2011). Specimens were collected from birds captured in Llanos del Challe National Park, Las Chinchillas National Reserve, Bosques de Fray Jorge National Park, Lago Peñuelas National Reserve, La Campana National Park and Tiltil. Of pterodectine genera restricted to passerines of the New World, the genus Amerodectes Valim and Hernandes, 2010 is the most speciose and currently includes 28 species parasitizing a wide spectrum of passerines belonging to 11 families: Cardinalidae, Emberizidae, Furnariidae, Icteridae, Mimidae, Parulidae, Thraupidae, Turdidae, Troglodytidae, Tyrannidae and Veronidae (MIRONOV et al., 2008; VALIM & HERNANDES, 2010; MIRONOV & GONZÁLEZ-ACUÑA, 2011, 2014; MIRONOV & OCONNOR, 2014; MIRONOV & OVERSTREET, 2015; HERNANDES et al., 2016). Mites of this genus has been recorded on passerines from Galapagos Islands (Ecuador) (VALIM & HERNANDES, 2010; VILLA et al., 2013); the United States (VALIM & HERNANDES, 2010; HRIBAR, 2013, 2014; MIRONOV & OCONNOR, 2014; MIRONOV & OVERSTREET, 2015); Guatemala (VALIM & HERNANDES, 2010); Surinam (ČERNÝ, 1974; VALIM & HERNANDES, 2010); Argentina (VALIM & HERNANDES, 2010); Colombia (BARRETO et al., 2012); Brazil (BERLA, 1958; VALIM & HERNANDES, 2006, 2010; BARRETO et al., 2012; MENDES et al., 2012; ENOUT et al., 2012; SILVA et al., 2015; HERNANDES et al., 2016) and Cuba (MIRONOV & GONZÁLEZ-ACUÑA, 2011; MIRONOV & GONZÁLEZ-ACUÑA, 2014). In Chile, A. zonotrichiae was originally found on Z. capensis in Atacama Region (MIRONOV & GONZÁLEZ-ACUÑA, 2014). Other Amerodectes species were recorded in this country on Sturnella loyca (Icteridae) and Phrygilus patagonicus (Emberizidae) in Los Lagos Region, and on Sicalis luteola (Emberizidae) in Biobío Region (SOTO et al., 2013; MIRONOV & GONZÁLEZ-ACUÑA, 2011).
Representatives of P. polyxenus were found in 1.4% (4/277) of the examined bird individuals. As the previous feather mite, this species is a typical inhabitant of the flight feathers of the wings and tail feathers having large and firm vanes. However, these mite, as for most proctophyllodines, usually occupy vane areas which are closer to the rachis than pterodectines (MIRONOV, 2009). Specimens of this mite were collected from sparrows captured in Bosques de Fray Jorge National Park and Tiltil. Proctophyllodes polyxenus is a feather mite uncommonly widely distributed among passerine hosts; it has been recorded so far from 37 passerine species of the families Calcariidae, Cardinalidae, Emberizidae, Motacillidae, Parulidae, Passerellidae, Thraupidae, and Turdidae in the New World. All records of this mite were made from hosts captured in the USA, Mexico, and in a minor part in Canada (Newfoundland) (ATYEO & BRAASCH, 1966). It is necessary to note that the authors of this species admitted that this so widely distributed mite could represent in fact a complex of very closely related or cryptic species. However, this question has never been specifically examined by statistic or molecular-based methods. Among numerous passerine hosts, P. polyxenus was previously recorded on three sparrow species of the genus Zonotrichia, – Z. albicollis (Gmelin), Z. leucophrys (Forster) and Z. querula (Nuttall) in the United States (ATYEO & BRAASCH, 1966). The present study reports Z. capensis as a new host of P. polyxenus and expands its geographical range of this mite to Chile.
The genus Proctophyllodes Robin, 1868 is the species-richest in the family Proctophyllodidae and among all families of feather mites currently including about 170 species (ATYEO & BRAASCH, 1966; MIRONOV, 2012, 2017; WANG et al., 2014). Representatives of this genus are distributed worldwide, predominately parasitize oscine passerines and have been recorded from 35 families of this grouping (as classified by THE CORNELL LAB OF ORNITHOLOGY, 2016). Additionally, three Proctophyllodes species are found on suboscine passerines of the families Furnariidae, Pittidae, and Tyrannidae, and a single species is known from each of the following non-passerine orders, Apodiformes (Trochilidae), Charadriiformes and Piciformes (ATYEO & BRAASCH, 1966). The world revision of the genus Proctophyllodes was carried out by Atyeo & Braasch (1966) and this monograph is still the main taxonomic work of this genus and the only key for identification of its species. The fauna of the genus Proctophyllodes on passerines of the New World currently includes about 70 species (ATYEO & BRAASCH, 1966; OCONNOR et al., 2005; GALLOWAY et al., 2014; MIRONOV & OCONNOR, 2014).
Trouessartia capensis was collected from 7.2% (20/277) of the sparrows examined. This mite was found on these birds in Las Chinchillas National Reserve, Bosques de Fray Jorge National Park, Lago Peñuelas National Reserve, La Campana National Park, and Tiltil.
Trouessartia capensis was originally described from Z. capensis subtorquata in Brazil (BERLA, 1959); it was later recorded on Z. capensis from Brazil and Colombia (KANEGAE et al., 2008; BARRETO et al., 2012), Z. capensis mellea from Argentina, Z. capensis subtorquata from Paraguay, and Z. capensis insularis from Curaçao Island (SANTANA, 1976). Our study indicates, for the first time, the presence of T. capensis on rufous-collared sparrows in Chile. Additionally, this mite species was previously reported from various passerines of the New World: Ammodramus savannarum floridanus (Emberizidae) from the United States (FORRESTER & SPALDING, 2003); and Hylocryptus rectirostris (Furnariidae), Leptopogon amaurocephalus (Tyrannidae), Elaenia chiriquensis, E. cristata (Tyrannidae), Trichothraupis melanops, and Eucometis penicillata (Thraupidae) from Brazil (KANEGAE et al., 2008). However, the records of T. capensis from birds other than those from the family Emberizidae are quite questionable, and they may possibly represent misidentifications.
Phthiraptera
A total of 170 individuals belonging to the genus Philopterus Nitzsch, 1818 (Phthiraptera: Ischnocera) were identified from 10.83% (30/277) of the rufous-collared sparrows examined (Figure 5). The genders of 82 individuals were identified, including 58.54% (n=48) of nymphs and 41.46% (n=34) of adults. The Philopterus sp. was collected from this bird species across all of the sites that were visited during this study. The population parameters for Philopterus sp. are indicated in Table 1.
Table 1 Population parameters of Philopterus sp. collected from rufous-collared sparrows (Zonotrichia capensis).
| Lice | Nº of captured birds | Positive birds | Prevalence % | Mean intensity | Mean abundance | Range |
|---|---|---|---|---|---|---|
| Philopterus sp. | 277 | 30 | 10.83 | 5.66 | 0.61 | 1-40 |
Lice of the genus Philopterus primarily parasitize passerine birds; it is one of the most speciose genera of the ischnoceran family Philopteridae, with more than 210 species and subspecies (PRICE & HELLENTHAL, 1998). This is the first record of lice of the genus Philopterus on Z. capensis. The body measurements of the collected lice are indicated in Table 2. Louse specimens collected in this study probably represent a new species, particularly since they differ in terms of certain morphological features when compared to other known species of the same genus (PRICE & HELLENTHAL, 1998).
Table 2 Mean body measurementss (μm) of Philopterus sp. collected from rufous-collared sparrows (Zonotrichia capensis).
| Body structure | Male | Female | ||
|---|---|---|---|---|
| Length | Width | Length | Width | |
| Head | 450.14 | 407.39 | 490.17 | 459.51 |
| Prothorax | 116.02 | 244.98 | 129.38 | 266.07 |
| Pterothorax | 128.39 | 360.54 | 161.85 | 403.95 |
| Abdomen | 661.52 | 528.10 | 869.13 | 608.79 |
Ticks
Only three tick larvae were collected from the sparrows. Two ticks were identified as Amblyomma tigrinum Koch, 1844 (Figure 6) and one as Ixodes auritulus Neumann, 1904 (Acari: Ixodidae) (Figure 7). Amblyomma tigrinum and I. auritulus were collected in the Bosques de Fray Jorge National Park and Termas del Flaco, respectively.
Amblyomma tigrinum, commonly referred to as ‘the white-ribbed dog tick’, parasitizes carnivores and birds in South America. Adult ticks primarily feed on domestic and wild carnivores, as well as on other members of the family Canidae; they occasionally feed on humans (GUGLIELMONE et al., 2000). During its larval and nymph stages, this tick can be found on wild birds and rodents (NAVA et al., 2006). Amblyomma tigrinum adapts to hosts living in different habitats that are found in the lowlands of Central Chile, or in high-altitude areas in the Peruvian Andes (MENDOZA & CHÁVEZ-CHOROCCO, 2004; GONZÁLEZ-ACUÑA & GUGLIELMONE, 2005) It has also been reported in Bolivia, Argentina, French Guiana, Paraguay, Uruguay, Venezuela, and Brazil (JONES et al., 1972; GONZÁLEZ-ACUÑA et al., 2004). In Chile, it has been described to parasitize such bird species as Nothoprocta perdicaria (Tinamidae), Callipepla californica (Odontophoridae), and Zenaida auriculata (Columbidae) (GONZÁLEZ-ACUÑA et al., 2004). It is likely that populations of Z. capensis and other possible host species, such as Lycalopex culpaeus, are assisting in the maintenance of the endemic status of A. tigrinum in Bosques de Fray Jorge National Park. This is the first record of A. tigrinum on Z. capensis.
Ixodes auritulus is commonly recorded as a parasite of land birds in South America, primarily from the Turdidae and Furnariidae families (GONZÁLEZ-ACUÑA et al., 2005). It inhabits areas with low temperatures, such as mountainous environments, or in lowlands featuring cold or temperate climates (BERMÚDEZ et al., 2015). This species has been reported from different hosts in Guatemala, Panamá, Venezuela, Costa Rica, Ecuador, Peru, Brazil, Uruguay, Argentina, and Chile, but it is also distributed in the Ethiopian, Nearctic, and Australian regions (GUGLIELMONE et al., 2003b; BERMÚDEZ et al., 2015). Its subspecies I. a. zealandicus was found on seabirds from the New Zealand sub-region (HEATH et al., 2011). In Chile, I. auritulus has been previously recorded on Z. capensis, Cinclodes fuscus (Furnariidae), C. antarcticus, Aphrastura spinicauda (Furnariidae), Elaenia albiceps (Tyrannidae), Pygarrhichas albogularis (Furnariidae), Troglodytes sp. (Troglodytidae), Curaeus curaeus (Icteridae), and Turdus falcklandii (Turdidae) (GONZÁLEZ-ACUÑA et al., 2005).
Endoparasites
Two endoparasite specimens were isolated from two of the seven birds carcasses examined. Both were identified as Mediorhynchus papillosus Van Cleave, 1916 (Gigantorhynchida: Gigantorhynchidae).
The genus Mediorhynchus includes 35 species parasitizing the small intestine of wild birds all over the world (SCHMIDT & KUNTZ, 1977). Detailed information about the life cycle of this genus is unknown for most species. Studies of M. centurorum indicated that this parasite infects cockroaches as intermediary hosts during its larval stage before being transmitted to birds through ingestion (JACKSON & NICKOL, 1979).
Mediorhynchus papillosus has been previously recorded in a wide range of bird families, primarily in North America, with fewer reports in Eurasia. This acanthocephalan has been reported in Tringa erythropus (Scolopacidae) in Bulgaria (DIMITROVA & GENOV, 1992); Calliope calliope (Muscicapidae) in Russia; Alauda gulgula wattersi (Alaudidae) and Dicrurus macrocercus (Dicruridae) in Taiwan; Alauda arvensis pescadores in the Pescadores Islands (SCHMIDT & KUNTZ, 1977); Passer domesticus (Passeridae) in Brazil (BRASIL & AMATO, 1992); and Charadrius vociferus (Charadriidae), Colinus virginianus (Odontophoridae), Contopus virens (Tyrannidae), Sayornis phoebe (Tyrannidae), Pooecetes gramineus (Emberizidae), Melospiza melodia (Emberizidae), Ammospiza maritima (Passerellidae), Agelaius phoeniceus (Icteridae), Oreoscoptes montanus (Mimidae), Petrochelidon pyrrhonota (Hirundidae), Tachycineta bicolor (Hirundidae), Porzana carolina (Rallidae), Tympanuchus cupido (Phasianidae), and Numenius americanus (Scolopacidae) in the United States (VAN CLEAVE, 1947; WEBSTER, 1948; HUNTER & QUAY, 1953; ECKMAN, 1968; KAYTON & SCHMIDT, 1975; BUTLER & PFAFFENBERGER, 1981; SHERWIN & SCHMIDT, 1988; WALLACE & OLSEN, 1996; AMIN & DAILEY, 1998; BRUNO et al., 2015).
This is the first record of M. papillosus from Z. capensis and the first record of this acanthocephalan in Chile. It is possible that M. papillosus infects a much wider range of bird species in Chile and South America due to its generalist behavior and cosmopolitan distribution. Additional information about its intermediary and definitive hosts is required to better understand the ecology of this parasite in South America.
This scientific work contributes to the knowledge about the prevalence and diversity of parasites occurring in Z. capensis, as three feather mites, A. zonotrichiae, P. polyxenus and T. capensis; a louse, Philopterus sp.; two ixodid ticks, A. tigrinum and A. auritulus; and an acanthocephalan, M. papillosus, were recorded. For the first time, this study reports the occurrence of Philopterus sp., A. tigrinum, and M. papillosus on Z. capensis, and it expands the distributional range of T. capensis to Chile.
