Gastrointestinal and external parasites of Enicognathus ferrugineus and Enicognathus leptorhynchus (Aves, Psittacidae) in Chile

Parasite species are important components of biodiversity, as they provide valuable information about host health, evolutionary relationships, population structures, trophic interactions, the existence of environmental stresses, and climatic conditions. With the aim of describing the parasites associated with parrots of the genus Enicognathus Gray 1840 from central Chile, thirteen austral parakeets, Enicognathus ferrugineus , and five slender-billed parakeets, E. leptorhynchus , were examined between September 2007 and March 2014. The prevalence of ectoparasites and endoparasites was 88.9% and 22.2%, respectively. On eleven of the E. ferrugineus (84.6%) analyzed, and on all of the E. leptorhynchus analyzed (100%), five feather mite species ( Pararalichus hastifolia , Genoprotolichus major , Protonyssus sp., Fainalges sp., and Eurydiscalges sp.) were collected. On ten E. ferrugineus (76.9%) and two E. leptorhynchus (40%), the chewing lice Heteromenopon macrurum , Psittacobrossus patagoni , and Paragoniocotes enicognathidis were collected. The nematode Capillaria plagiaticia was collected from three E. ferrugineus (23.1%), and the nematode Ascaridia hermaphrodita was found in one E. leptorhynchus (20%). The presence of C. plagiaticia , Protonyssus sp., Fainalges sp., and Eurydiscalges sp. from the two Enicognathus spp. are new records for Chile and represent new parasite-host associations.

These birds are of special concern for conservation given their recent population declines during the last century (COLLAR, 1997;DÍAZ, 2012;GOODALL et al., 1957). This situation renders these birds a priority, especially with regards to acquiring knowledge about their biology -including their parasites; nevertheless, scientific literature on this topic is scarce (CARNEIRO et al., 2012). In addition, because of their low population sizes, only those birds that have died by natural or accidental deaths can be examined for endoparasites. Previous investigations into the parasitic fauna associated with parrots of the genus Enicognathus revealed three major groupings of parasites: two roundworm species (Nematoda: Ascaridiidae); three chewing lice (Insecta: Phthiraptera); and two feather mites (Arachnida: Acarina: Astigmata). The nematode Ascaridia hermaphrodita Froelich, 1789, was found in slender-billed parakeets in Chile (GONZÁLEZ-ACUÑA et al., 2007) and A. platyceri Hartwich and Tscherner, 1979 in austral parakeets in Germany (HARTWICH & TSCHERNER, 1979). Both were found in birds kept in captivity. The chewing lice species Heteromenopon macrurum Eichler, 1952 was recorded on austral parakeets in Argentina and Chile (EICHLER, 1952), and on slender-billed parakeets in Chile (CICCHINO & GONZÁLEZ-ACUÑA, 2009 & TROUESSART, 1904), first described as Protolichus, was found on austral parakeets, both of which were in Chile.
The objective of the present study is to document new records of gastrointestinal and external parasites for both Enicognathus species from central Chile.

Materials and Methods
Between September 2007 and March 2014, thirteen austral parakeets and five slender-billed parakeets from central Chile were received by the School of Veterinary Science of the University of Concepción (Concepción, Chile). Their causes of death were vehicle collisions and poaching. The birds were stored individually at -12 °C until their analysis. The date of reception, provenance, coordinates, and date of analysis for each individual bird are found in Table 1. Lice and mites were collected by visual inspection of feathers. Ectoparasites were preserved in 70% ethanol, and lice were cleared and mounted in Canada balsam (PALMA, 1978;PRICE et al., 2003). Mites were cleared in Nesbitt's solution for 72 hours at sub-boiling temperature, and they were finally mounted in Berlese's medium (KRANTZ & WALTER, 2009). To identify lice, the keys and descriptions of Eichler (1952), Price & Beer (1967, 1968, Castro & Cicchino (1996), and Cicchino & González-Acuña (2009) were used. Mites were identified using the keys proposed by Atyeo (1989a, b), Gaud & Atyeo (1996a, b), and Krantz & Walter (2009). For endoparasites, the dissection of birds, as well as the collection and preservation of helminthes, followed the methods of Kinsella & Forrester (1972). The identification of the endoparasites followed the keys of Freitas & Mendonça (1959), Yamaguti (1961), and Kajerová et al. (2004). The terms for prevalence, range, and mean intensity follow Margolis et al. (1982) and Bush et al. (1997).
All of the collected parasite specimens are stored in the collection of the Zoology Laboratory of the School of Veterinary Science of the University of Concepción, Chillán campus.

Results
Endoparasites were found in 22.2% (4/18) (two species of nematodes) and ectoparasites were found on 88.9% (16/18) of the examined birds (there were three species of chewing lice and six species of mites). Tables 2 and 3 summarize the data on the parasites found on the austral and slender-billed parakeets. Two nematode species were found: A. hermaphrodita (Figure 1) was found in slender-billed parakeets, and Capillaria plagiaticia Freitas and Mendonça, 1959 (Figures 2 and 3) in austral parakeets.

Nematoda
Seven species of the genus Ascaridia Dujardin, 1845 (Nematoda: Ascaridiidae) have been reported from the order Psittaciformes. Among these, A. hermaphrodita is one of the most frequently reported in these birds (HODOVÁ et al., 2008). Previously, heavy infections of A. hermaphrodita were found in two female slender-billed parakeets that died at the Chilean National Zoo in Santiago (GONZÁLEZ-ACUÑA et al., 2007). This parasite is considered one of the most common parasites found among                 Parasites of Enicognathus in Chile wild in Chile has not been confirmed. The high intensity of this parasite in dead birds highlights the need to perform additional studies to determine the importance of this parasite in the ecology of these two types of parakeets. The nematode C. plagiaticia (Nematoda: Trichuridae) was originally described by Freitas & Mendonça (1959) on the basis of samples collected from cactus parakeets, Aratinga (Eupsittula) cactorum caixana Spix, 1824, in Brazil. Capillaria plagiaticia is considered to be specific to psittacids (KAJEROVÁ & BARUS, 2005). The present finding in this study is the first record of this nematode in the austral parakeet, and it also represents its first record in Chile.
The genus Psittacobrossus Carriker, 1954 (Amblycera: Monoponidae) contains 20 species, all of which are parasites of New World parrots. The description of P. patagoni was based on samples obtained from a burrowing parrot, Cyanoliseus patagonus bloxami Olson, 1995 from Angol, Chile (PRICE & BEER, 1968). This parasite has also been found on C. p. patagonus in Argentina, and on the austral parakeet in Chile and Argentina (ARAMBURÚ, 2012; CICCHINO & GONZÁLEZ-ACUÑA, 2009). Thus, our finding is the first record of P. patagoni on the slender-billed parakeet.
Paragoniocotes enicognathidis was recently described by Cicchino & González-Acuña (2009) on austral and slender-billed parakeets from Argentina and Chile. Thus, P. enicognathidis has only been recorded on parrots of the genus Enicognathus.

Acari
The mite Pararalichus hastifolia (L Pterolichoidea: Pterolichidae) is considered specific to parrots of the genus Enicognathus (ATYEO, 1989b). This species was originally described by Mégnin & Trouessart (1884) on the austral parakeet and it was named Pterolichus (Pterolichus) hastifolia. Atyeo (1989a) redescribed this species and assigned it to the genus Aralichus Gaud, 1966; in addition, he found it on the slender-billed parakeet from Chiloé, Chile. Later, Atyeo (1989b) created the genus Pararalichus, and included this species within this category. This genus is associated with various parrots from the New World. Pararalichus hastifolia, as well as all pterolichids, are specialized to inhabit the ventral surface of feathers with large vanes -i.e., the flight and covert feathers of the wing, as well as the tail feathers (MIRONOV & DABERT, 2007).
Mites of the genus Genoprotolichus Gaud and Atyeo, 1996 (Pterolichoidea: Pterolichidae) live on the longest wing feathers of psittacid birds (GAUD & ATYEO, 1996a, b) and they are comprised in four species. Genoprotolichus major was described by Favette & Trouessart (1904) from austral parakeets from Patagonia and Tierra del Fuego, Chile; it was further recorded in this country on the subspecies Enicognathus ferrugineus minor Chapman, 1919 in Mafil, Valdivia, andMelinka, Chiloé (CUERVO &PÉREZ, 2009). The present study represents the first record of G. major on the slender-billed parakeet.
The feather mite genera Protonyssus Trouessart, 1916, andFainalges Gaud andBerla, 1964 (Analgoidea: Xolalgidae) belong to the subfamily Ingrassiinae, and they represent two of three ingrassiine genera known to infest birds of the order Psittaciformes (GAUD & ATYEO, 1981). Fainalges and Protonyssus are exclusively associated with parrots, while species of the third genus, Dubininia Vassilev, 1958, live on parrots of the Old World and also on birds of the orders Falconiformes and Cuculiformes.
The genus Fainalges currently includes thirteen species of New World parrots from the genera Aratinga Spix, 1824;Deroptyus Wagler, 1832;andConuropsis Salvadori, 1891 (MIRONOV et al., 2005;PEREZ, 1995). The genus Fainalges is considered to be restricted to parrots from this part of the world.
The finding of two supposedly new ingrassine species, Protonyssus sp. and Fainalges sp., on the austral and slender-billed parakeets represents new host-parasite associations, both for these birds and in Chile.
Some feather mite specimens represented by junior preimaginal instars (larvae and protonymphs) were identified only at the family level (Table 2; Pterolichidae gen. sp.). Given the present state of systematics for most feather mite families, the identification of preimaginal instars up to the species and genera level is quite difficult because they are understudied.

Conclusion
The list of ecto-and endoparasites reported from the austral and slender-billed parakeets in Chile includes the following species: Pararalichus hastifolia; G. major; Protonyssus sp.; Fainalges sp.; Eurydiscalges sp.; H. macrurum; Psittacobrosus patagoni; and Paragoniocotes enicognathidis. Additionally, the nematodes C. plagiaticia and Ascaridia platyceri were found in the austral parakeet, while A. hermaphrodita was recorded in the slender-billed parakeet.