Gastrointestinal and ectoparasites of plumbeous rail, Pardirallus sanguinolentus (Aves: Rallidae) in Central Chile

With the aim to identify the parasite fauna of plumbeous rail, Pardirallus sanguinolentus (Aves: Rallidae) in Chile, 26 carcasses were parasitologically necropsied. The present study revealed the presence of 14 species of parasites (inverse Simpson index = 4.64; evenness = 0.332), including ectoparasites: feather mites: Analloptes megnini, Grallobia sp., Grallolichus sp., Megniniella sp., and Metanalges sp.; the feather lice Pseudomenopon meinertzhageni, Rallicola andinus, and Fulicoffula sp.; and six species of gastrointestinal helminths: Heterakis psophiae, Porrocaecum ardeae, Tetrameres sp., Capillaria sp., Diorchis sp., and Plagiorhynchus sp. The relatively high parasite richness that was found could be attributed to the highly favorable conditions of wetlands for parasite development. All parasites found, except feather lice, are new records for plumbeous rail. A checklist of parasites for plumbeous rail is presented.


Introduction
Parasite-host associations reveal valuable information about the host that should always be considered for studies of biodiversity and conservation (PÉREZ-PONCE DE LEÓN & GARCÍA-PRIETO,
freshwaters, which offer ideal conditions for the high presentation of parasitism (KAMIYA et al., 2014;LEUNG & KOPRIVNIKAR, 2016).The previous records of parasites for plumbeous rail include both gastrointestinal and ectoparasites (see Table 1); however, these reports have been strongly biased toward taxonomic descriptions that either focus on specific parasite groups or species (e.g.CICCHINO, 2011;SKORACKI et al., 2014).The aim of this study was to identify the ecto and gastrointestinal parasites of plumbeous rail in Chile.

Materials and Methods
Between June 2001 and March 2015, the anatomic organs of 26 adult birds from the Ñuble Province, Biobío Region (36°37'S; 71°57'W), were analyzed.The organs corresponded to museum skins of three birds (which were part of the Ornithological Collection of Avian Carcasses of the Zoology Laboratory of the Faculty of Veterinary Sciences, University of Concepción), ten carcasses whose deaths were attributed to road kills and poaching (retrieved by the Wildlife Rehabilitation Center, University of Concepción), and 13 gastrointestinal tracts.Ectoparasites were collected through plumage inspection (15 minutes per bird), followed by immediate preservation in 70% ethanol.Feather lice were mounted using Canada balsam following the techniques described by Palma (1978) and Price et al. (2003).Feather mites were cleared in Nesbitt solution (40 g of chloral hydrate, 25 mL of distilled water, and 2.5 mL of hydrochloric acid) for 72 hours and were later mounted in Berlese solution (KRANTZ & WALTER, 2009).For the endoparasites, the dissection of birds and the collection and preservation of helminths followed the methods of Kinsella & Forrester (1972).The keys used for taxonomic identification adopted the approach of Carriker (1949), Emerson (1955), Price (1974), andCicchino (2011) for feather lice; Trouessart (1885), Gaud (1958), andGaud &Mouchet (1963) for feather mites; and Yamaguti (1961Yamaguti ( , 1963) ) and Khalil et al. (1994) for helminths.
To quantify the parasite community, we determined the inverse Simpson diversity index, as follows: where p is the proportional biomass of species i, species richness (S), and evenness (D/S) (WILSEY et al., 2005).All parasite specimens were deposited in the Collection of Parasites of Chile, Zoology Laboratory, Faculty of Veterinary Science, University of Concepción, Chile, under the codes CDCA 132 to 136 for mites, UdeCPhsa 147 to 168 for lice and CDCA 180 to 182 for helminths.

Results and Discussion
Ectoparasites Acari: All inspected birds were parasitized with at least one mite species (Table 2): Analloptes megnini Trouessart (1885), Grallobia sp., Grallolichus sp., Megniniella sp., or Metanalges sp.A male individual of A. megnini (Astigmata: Xolalgidae) (Figure 1) was found on one bird.Despite the small number of individuals analyzed, low prevalence rates were frequently found among the Analloptes Trouessart, 1885 species.Miller et al. (1997) commented that this will likely underestimate the presence of this genus, as it generally occurs in small quantities.Furthermore, these mites inhabit downy and covert feathers, which may hinder the collection of this genus.The genus Analloptes includes 11 species that parasitize phylogenetically distant hosts, including Coraciiformes, Gruiformes, Pelecaniformes, Accipitriformes, and Passeriformes (GAUD, 1968;MIRONOV & HERNANDES, 2014).
Porrocaecum ardeae (Ascaridida) (Figure 10) was found in three birds (13%).One bird presented this parasite underneath the parietal peritoneum and mesentery of its body cavity (coelom), as well as in the lumen of the small intestine, which was perforated.This does not seem to be an isolated incident given that Fanke et al. (2011) reported the death of three common crane, Grus grus Linnaeus (1758), due to intestinal perforation caused by severe infestation with this parasite.Species of the genus Porrocaecum Railliet & Henry, 1912 are cosmopolitan and present indirect life cycles; invertebrates serve as an intermediate host (ATKINSON et al., 2008;DZIEKONSKA-RYNKO et al., 2015).There are several records of P. ardeae regularly affecting birds of the families Gruidae and Ardeidae in Europe and Central America (SCHMIDT & NEILAND, 1973;HARTWICH, 1979;FANKE et al., 2011;     -RYNKO et al., 2015;SITKO & HENEBERG, 2015).

DZIEKONSKA
In one bird (4.3%), seven individuals from the genus Capillaria Zeder, 1800 (Capillariidae) were found (Figure 11).The parasites were in the final portion of the small intestine and a few were identified in the caecum.These parasites have a worldwide distribution and there are several records of its existence in Chile (e.g., HINOJOSA-SÁEZ & GONZÁLEZ-ACUÑA, 2005; GONZÁLEZ-ACUÑA et al., 2010;VALDEBENITO et al., 2015).Among all members of this genus, Capillaria fulicae Pavlov & Borgarenko (1959) is often found in rallid birds from North America (KINSELLA, 1973;KINSELLA et al., 1973).In addition to its distinctive morphological features, there are no Capillaria species described for South American rallids; therefore, this parasite is a good fit as a possible new species.Further studies need to be conducted to verify whether this does, in fact, represent a new species.
Five females from the genus Tetrameres Creplin, 1846 (Tetrameridae) were found in one bird (4.3%).These nematodes are widely distributed and can affect captive and wild birds.Female Tetrameres are typically attached to the proventriculus of the definitive host, while males tend to move more freely and are more likely to be found on the mucosa or lumen (ANDERSON, 2000).On certain occasions, Tetrameres species were recorded to affect terrestrial birds (e.g., Passeriformes and Galliformes); however, their main hosts are aquatic birds like Anseriformes, Pelecaniformes, Charadriiformes, and Gruiformes (MOLLHAGEN, 1976;ATKINSON et al., 2008), where T. fissispina Diesing, 1861, T. globosa Linstow (1879), and Tetrameres sp. were found to affect several species around the world (KINSELLA et al., 1973;MOLLHAGEN, 1976;AL-AWADI et al., 2010;BIRMANI et al., 2011).
Acanthocephala: In one bird (4.3%), one individual from the genus Plagiorhynchus Lühe (1911) (Plagiorhynchidae) was found.These parasites have a global distribution and were recorded in several bird orders (YAMAGUTI, 1963), including rallids (YOSHINO et al., 2009;ONUMA et al., 2011).All members of this phylum present an indirect life cycle, and invertebrates serve as intermediate host and occur exclusively in the small intestine of the definitive host (ATKINSON et al., 2008).
The overall parasite diversity and evenness was 4.64 and 0.332, respectively.Both ectoparasites and helminths had a similar species diversity index (inverse Simpson index: ectoparasites, 2.91; helminths, 2.92), whereas evenness was higher in helminths (0.487) when compared to ectoparasites (0.364).High parasite diversity is generally attributed to numerous factors including, for example, high latitude, large body size, and various habitat characteristics (KAMIYA et al., 2014).For plumbeous rail, habitat seems to be the primary contributing factor for the relatively high degree of diversity found.Wetlands have been shown to be advantageous for parasite communities, as there is a greater opportunity for contact with the various stages of parasite infection and/or the consumption of infected hosts (LEUNG & KOPRIVNIKAR, 2016).These ecosystems also serve as stopover point for many  Although Skoracki et al. (2014) did not report information on the prevalence of Rafapicobia melzeri (Table 1), we speculate that this absence was due to the relatively small numbers of birds examined.Cicchino (2011) found the louse Rallicola pratti on birds from Buenos Aires Province, Argentina (Table 1), which were located close to the area where the hosts blackish rail P. nigricans Vieillot, 1819 and plumbeous rail overlap in terms of their distribution.Therefore, this louse could likely only occur on plumbeous rail in areas where there is a close relationship between these two rallids.On the other hand, the absence of the trematodes Microphallus szidati and Echinostoma parcespinosum (Table 1) recorded in Argentina (MARTORELLI, 1986;MARTORELLI, 1987) were likely due to the absence of their intermediate hosts, which are needed to complete their life cycle.However, must be noted that the snail Pomacea canaliculata Lamarck (1828), an intermediate host of E. parcespinosum, was recently introduced to Chile and first reported by Jackson & Jackson (2009) in the Coquimbo Region.Additionally, E. parcespinosum can abbreviate its life cycle in this snail by using it as a primary and secondary intermediate host (MARTORELLI, 1987), enabling the possibility of future presentation of this parasite in Chile.
The present study contributes to the understanding of parasite communities by supporting the current findings on the associations between habitat type and parasite richness and diversity (LEUNG & KOPRIVNIKAR, 2016;GUTIÉRREZ et al., 2017).Plumbeous rail presented a high degree of parasite diversity, 14 species, including ecto and gastrointestinal parasites; these species featured 11 species that were not previously recorded in this host and nine not previously reported in Chile.

Figure 1 .
Figure 1.Light microscopy of ventral view of male Analloptes megnini.

Figure 2 .
Figure 2. Light microscopy of ventral view of female (A) and male (B) Grallobia sp.

Figure 3 .
Figure 3.Light microscopy of ventral view of male (A) and female with egg (B) Grallolichus sp.

Figure 5 .
Figure 5.Light microscopy of Metanalges sp.showing ventral view of male (A) and female (B).

Figure 4 .
Figure 4. Light microscopy of ventral view of male (A) and female (B) Megniniella sp.

Figure 6 .
Figure 6.Light microscopy of Pseudomenopon meinertzhageni showing ventral view of female.

Figure 7 .
Figure 7.Light microscopy of Rallicola andinus showing ventral view of male.

Figure 9 .
Figure 9.Light microscopy of Heterakis psophiae showing posterior end of male.

Figure 10 .
Figure 10.Light microscopy of Porrocaecum ardeae showing anterior end of female (A) and posterior end of male (B).

Figure 11 .
Figure 11.Light microscopy of Capillaria sp.showing posterior end of male.

Parasite Prevalence (%) Range Mean intensity Number of parasitized birds Total of parasites Acari: Pterolichidae
*New record for plumbeous rail and Chile; §New record for plumbeous rail.