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

Gastrointestinais e ectoparasitas do saracura-do-banhado, Pardirallus sanguinolentus (Aves: Rallidae) do Chile central

José Osvaldo Valdebenito Lucila Moreno Carlos Barrientos Sergey Mironov John Mike Kinsella Armando Cicchino Mabel Mena Alexandra Grandón-Ojeda Daniel González-Acuña About the authors

Abstract

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.

Keywords:
Parasites; helminths; diversity; wetlands; rallids

Resumo

Com o objetivo de identificar a fauna parasitária do saracura-do-banhado, Pardirallus sanguinolentus (Aves: Rallidae) no Chile, 26 carcaças foram necropsiadas. O presente estudo revelou a presença de 14 espécies de parasitos (índice Simpson inverso = 4,64; equitatividade = 0,332), incluindo os ácaros de penas: Analloptes megnini, Grallobia sp., Grallolichus sp., Megniniella sp. e Metanalges sp.; os piolhos de penas Pseudomenopon meinertzhageni, Rallicola andinus e Fulicoffula sp.; e seis espécies de helmintos gastrointestinais: Heterakis psophiae, Porrocaecum ardeae, Tetrameres sp., Capillaria sp., Diorchis sp. e Plagiorhynchus sp. A riqueza parasitária relativa encontrada pode ser devido às condições altamente favoráveis das zonas úmidas para o desenvolvimento do parasita. Todos os parasitos encontrados, com exceção dos piolhos de pena, são novos registros para o saracura-do-banhado. Um checklist dos parasitos do saracura-do-banhado é apresentado.

Palavras-chave:
Parasitos; helmintos; diversidade; zona úmida; ralídeos

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, 2001 Pérez-Ponce de León G, García-Prieto L. Los parásitos en el contexto de la biodiversidad y la conservación. Biodiversitas 2001; 34: 11-15. ), particularly since parasites have been linked to important variations in biodiversity, population declines, and even species extinction (e.g., JOHNSON et al., 1999 Johnson PTJ, Lunde KB, Ritchie EG, Launer AE. The effect of trematode infection on amphibian limb development and survivorship. Science 1999; 284(5415): 802-804. http://dx.doi.org/10.1126/science.284.5415.802. PMid:10221912.
http://dx.doi.org/10.1126/science.284.5...
; CUNNINGHAM & DASZAK, 1998 Cunningham AA, Daszak P. Extinction of a species of land snail due to infection with a Microsporidian parasite. Conserv Biol 1998; 12(5): 1139-1141. http://dx.doi.org/10.1046/j.1523-1739.1998.97485.x.
http://dx.doi.org/10.1046/j.1523-1739.1...
). The plumbeous rail, Pardirallus sanguinolentus (SWAINSON, 1838), is one of three members of the genus Pardirallus Bonaparte, 1856, in South America. Six subspecies are recognized, three of which are partially distributed in Chile. This bird inhabits all types of wetlands, including brackish and freshwaters, which offer ideal conditions for the high presentation of parasitism ( KAMIYA et al., 2014 Kamiya T, O’Dwyer K, Nakagawa S, Poulin R. What determines species richness of parasitic organisms? A meta-analysis across animal, plant and fungal hosts. Biol Rev Camb Philos Soc 2014; 89(1): 123-134. http://dx.doi.org/10.1111/brv.12046. PMid:23782597.
http://dx.doi.org/10.1111/brv.12046 ...
; LEUNG & KOPRIVNIKAR, 2016 Leung TL, Koprivnikar J. Nematode parasite diversity in birds: the role of host ecology, life history and migration. J Anim Ecol 2016; 85(6): 1471-1480. http://dx.doi.org/10.1111/1365-2656.12581. PMid:27496635.
http://dx.doi.org/10.1111/1365-2656.125...
). 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 Cicchino AC. Piojos (Insecta: Psocodea: Phthiraptera) parásitos de Gruiformes y Podicipediformes (Aves) en la Argentina: una aproximación sistemática, bioecológica y evolutiva [thesis]. Mar del Plata: Universidad Nacional de Mar del Plata; 2011. ; SKORACKI et al., 2014 Skoracki M, Unsoeld M, Skorupski M, Kavetska K. Syringophilid mites (Acari: Syringophilidae) associated with the rails (Aves: Rallidae) and a key to the species of the genus Rafapicobia Skoracki, 2011. Syst Parasitol 2014; 88(3): 227-232. http://dx.doi.org/10.1007/s11230-014-9502-7. PMid:24935125.
http://dx.doi.org/10.1007/s11230-014-95...
). The aim of this study was to identify the ecto and gastrointestinal parasites of plumbeous rail in Chile.

Table 1
Checklist of parasites found in plumbeous rail, Pardirallus sanguinolentus , to date.

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) Palma RL. Slide-mounting of lice: a detailed description of the Canada balsam technique. NZ Entomol 1978; 6(4): 432-436. http://dx.doi.org/10.1080/00779962.1978.9722313.
http://dx.doi.org/10.1080/00779962.1978...
and Price et al. (2003) Price RD, Hellenthal RA, Palma RL, Johnson KP, Clayton DH. The chewing lice: world checklist and biological overview. Champaign: Illinois Natural History Survey; 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 Krantz GW, Walter DE. A manual of acarology. 3rd ed. Lubbock: Texas Tech; 2009. ). For the endoparasites, the dissection of birds and the collection and preservation of helminths followed the methods of Kinsella & Forrester (1972) Kinsella JM, Forrester DJ. Helminths of the Florida duck, Anas platyrhynchos fulvigula. Proc Helminthol Soc Wash 1972; 39(2): 173-176. . The keys used for taxonomic identification adopted the approach of Carriker (1949) Carriker MA. Neotropical Mallophaga miscellany. V. New genera and species. Rev Bras Biol 1949; 9(3): 297-313. , Emerson (1955) Emerson KC. A review of the genus Rallicola (Philopteridae, Mallophaga) found on Aramidae, Psophiidae and Rallidae. Ann Entomol Soc Am 1955; 48(4): 284-299. http://dx.doi.org/10.1093/aesa/48.4.284.
http://dx.doi.org/10.1093/aesa/48.4.284...
, Price (1974) Price RD. A Review of the genus Pseudomenopon (Mallophaga: Menoponidae). Ann Entomol Soc Am 1974; 67(1): 73-84. http://dx.doi.org/10.1093/aesa/67.1.73.
http://dx.doi.org/10.1093/aesa/67.1.73 ...
, and Cicchino (2011) Cicchino AC. Piojos (Insecta: Psocodea: Phthiraptera) parásitos de Gruiformes y Podicipediformes (Aves) en la Argentina: una aproximación sistemática, bioecológica y evolutiva [thesis]. Mar del Plata: Universidad Nacional de Mar del Plata; 2011. for feather lice; Trouessart (1885) Trouessart EL. Note sur le classification des Analgésiens et diagnoses d’espèces et de genres nouveaux. Bulletin de la Société d’Études Scientifiques d’Angers 1885; 14: 46-89. , Gaud (1958) Gaud J. Acariens plumicoles (Analgesoidea) parasites des oiseaux du Maroc. Bull Soc Sci Nat Phys Maroc 1958; 38: 27-49. , and Gaud & Mouchet (1963) Gaud J, Mouchet J. Révision des genres Grallobia Hull et Grallolichus Gaud (Pterolichidae, Sarcoptiformes). Acarologia 1963; 5(4): 628-643. for feather mites; and Yamaguti (1961 Yamaguti S. Systema Helminthum: the nematodes of vertebrates. New York: Interscience Publisher; 1961. (vol. 3). , 1963 Yamaguti S. Systema Helminthum: Acanthocephala. New York: Interscience Publisher; 1963. (vol. 5). ) and Khalil et al. (1994) Khalil LF, Jones A, Bray RA. Keys to the cestode parasites of vertebrates . Wallingfrord: CAB International; 1994. for helminths.

To quantify the parasite community, we determined the inverse Simpson diversity index, as follows:

D = 1 / ( p i 2 ) (1)

where p is the proportional biomass of species i , species richness (S), and evenness (D/S ) ( WILSEY et al., 2005 Wilsey BJ, Chalcraft DR, Bowles CM, Willig MR. Relationships among indices suggest that richness is an incomplete surrogate for grassland biodiversity. Ecology 2005; 86(5): 1178-1184. http://dx.doi.org/10.1890/04-0394.
http://dx.doi.org/10.1890/04-0394 ...
).

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 megniniTrouessart (1885 Trouessart EL. Note sur le classification des Analgésiens et diagnoses d’espèces et de genres nouveaux. Bulletin de la Société d’Études Scientifiques d’Angers 1885; 14: 46-89. ), Grallobia sp., Grallolichus sp., Megniniella sp., or Metanalges sp.

Table 2
Ecto and gastrointestinal parasites found in 26 plumbeous rails, Pardirallus sanguinolentus, between 2001-2015 in Central Chile.

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) Miller MJ, Ewins PJ, Galloway TD. Records of ectoparasites collected on ospreys from Ontario. J Wildl Dis 1997; 33(2): 373-376. http://dx.doi.org/10.7589/0090-3558-33.2.373. PMid:9131582.
http://dx.doi.org/10.7589/0090-3558-33....
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 Gaud J. Acariens sarcoptiformes plumicoles (Analgoidea) parasites sur les oiseaux Ralliformes et Gruiformes d’Afrique. Belgique: Musée Royal de l'Afrique Centrale; 1968. 101 p. (Sciences Zoologiques; vol. 164). ; MIRONOV & HERNANDES, 2014 Mironov S, Hernandes FA. Two new species of the feather mite genus Analloptes (Trouessart, 1885) (Acariformes: Astigmata: Xolalgidae) from passerines (Aves: Passeriformes) in Brazil. Zootaxa 2014; 3889(4): 589-600. http://dx.doi.org/10.11646/zootaxa.3889.4.6. PMid:25544285.
http://dx.doi.org/10.11646/zootaxa.3889...
).

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

Grallobia sp. (Astigmata: Pterolichidae) ( Figure 2 ) presented with the highest prevalence rates in this study (80%). A similar result was found in american coot Fulica americana Gmelin, 1789, which was affected by G. fulicae Trouessart, 1885, with a prevalence of 82.4% ( ROUAG-ZIANE et al., 2007 Rouag-Ziane N, Boulahbal A, Gauthier-Clerc M, Thomas F, Chabi Y. Inventaire et quantification des ectoparasites de la Foulque macroule Fulica atra (Gruiformes: Rallidés) dans Le Nord-Est De L’Algérie. Parasite 2007; 14(3): 253-256. http://dx.doi.org/10.1051/parasite/2007143253. PMid:17933305.
http://dx.doi.org/10.1051/parasite/2007...
). Conversely, Grallolichus sp. ( Figure 3 ) had a prevalence of 10% and a mean intensity of 13.0. These mites were morphologically similar to the species G. minutus Gaud & Mouchet, 1963. Both genera, as well as all mites from the family Pterolichidae, inhabit the surface of feathers with large vanes, such as flight and covert feathers of the wings and tail ( MIRONOV & DABERT, 2007 Mironov SV, Dabert J. Three new feather mite genera of the Protolichus generic group (Astigmata, Pterolichidae) from parrots (Aves, Psittaciformes) of the Old World. Acta Parasitol 2007; 52(4): 386-402. http://dx.doi.org/10.2478/s11686-007-0042-z.
http://dx.doi.org/10.2478/s11686-007-00...
). These mites affect a rather homogeneous group of birds; Grallobia Hull, 1932 is only associated with the avian family Rallidae, whereas Grallolichus Gaud, 1960 is associated with Rallidae, Jacanidae, and Heliornithidae ( GAUD, 1968 Gaud J. Acariens sarcoptiformes plumicoles (Analgoidea) parasites sur les oiseaux Ralliformes et Gruiformes d’Afrique. Belgique: Musée Royal de l'Afrique Centrale; 1968. 101 p. (Sciences Zoologiques; vol. 164). ; GAUD & MOUCHET, 1963 Gaud J, Mouchet J. Révision des genres Grallobia Hull et Grallolichus Gaud (Pterolichidae, Sarcoptiformes). Acarologia 1963; 5(4): 628-643. ).

Figure 2
Light microscopy of ventral view of female (A) and male (B) Grallobia sp.
Figure 3
Light microscopy of ventral view of male (A) and female with egg (B) Grallolichus sp.

Both Megniniella sp. and Metanalges sp. (Astigmata: Analgidae) ( Figures 4 and 5 ) were found in three (30%) and eight (80%) birds, respectively. Unlike most other genera from the subfamily Megniniinae, Megniniella Gaud & Mouchet, 1959 and Metanalges Truessart, 1919 occur almost exclusively on birds of the family Rallidae ( GAUD, 1968 Gaud J. Acariens sarcoptiformes plumicoles (Analgoidea) parasites sur les oiseaux Ralliformes et Gruiformes d’Afrique. Belgique: Musée Royal de l'Afrique Centrale; 1968. 101 p. (Sciences Zoologiques; vol. 164). ; GAUD & ATYEO, 1982 Gaud J, Atyeo WT. The subfamilies of the Analgidae and Psoroptoididae (Acari: Analgoidea). J Med Entomol 1982; 19(3): 299-305. http://dx.doi.org/10.1093/jmedent/19.3.299.
http://dx.doi.org/10.1093/jmedent/19.3....
), and they are often found in downy and covert feathers. The genus Megniniella has seven species, six of which are described from New and Old World rallids ( MIRONOV & GALLOWAY, 2002 Mironov SV, Galloway TD. Four new species of feather mites (Acari: Analgoidea). Can Entomol 2002; 134(5): 605-618. http://dx.doi.org/10.4039/Ent134605-5.
http://dx.doi.org/10.4039/Ent134605-5 ...
). Conversely, 11 species make up the genus Metanalges, which are allocated to the subgenera Metanalges and Agrialges Gaud & Mouchet, 1959, both of which are exclusive to rallids ( GAUD & MOUCHET, 1959 Gaud J, Mouchet J. Acariens plumicoles (Analgesoidea) parasites des oiseaux du Cameroun 11. Analgesidae. Ann Parasitol Hum Comp 1959; 34(1-2): 149-208. http://dx.doi.org/10.1051/parasite/1959341149.
http://dx.doi.org/10.1051/parasite/1959...
; MIRONOV & GALLOWAY, 2002 Mironov SV, Galloway TD. Four new species of feather mites (Acari: Analgoidea). Can Entomol 2002; 134(5): 605-618. http://dx.doi.org/10.4039/Ent134605-5.
http://dx.doi.org/10.4039/Ent134605-5 ...
). The individuals collected here could not be taxonomically identified beyond genus; nevertheless, they shared several similarities with Megniniella gallinulae Buchholz (1869), Metanalges crexi Mironov, 1985, and M. rallorumTrouessart (1885 Trouessart EL. Note sur le classification des Analgésiens et diagnoses d’espèces et de genres nouveaux. Bulletin de la Société d’Études Scientifiques d’Angers 1885; 14: 46-89. ), respectively.

Figure 4
Light microscopy of ventral view of male (A) and female (B) Megniniella sp.
Figure 5
Light microscopy of Metanalges sp. showing ventral view of male (A) and female (B).

Lice: All birds were parasitized with at least one species of the feather lice Pseudomenopon meinertzhageni Price, 1974, Rallicola andinus Carriker, 1949, and Fulicoffula sp. ( Table 2 ).

Pseudomenopon meinertzhageni (Phthiraptera: Amblycera) ( Figure 6 ) was found in eight birds (61.5%). Lice from this genus can be found in the hosts Gruiformes, Podicipediformes, and Charadriiformes, and they essentially feed on contour feather barbs and are occasionally recorded with hematophagous behavior ( CICCHINO, 2011 Cicchino AC. Piojos (Insecta: Psocodea: Phthiraptera) parásitos de Gruiformes y Podicipediformes (Aves) en la Argentina: una aproximación sistemática, bioecológica y evolutiva [thesis]. Mar del Plata: Universidad Nacional de Mar del Plata; 2011. ). According to Lakshminarayana (1977) Lakshminarayana KV. Notes on the genus Pseudomenopon with remarks on host relationships. Angew Parasitol 1977; 18(3): 152-162. PMid:920994. , lice from this genus are widely distributed in birds from the family Rallidae. Pseudomenopon meinertzhageni was exclusively recorded in plumbeous rail in Brazil, Chile, and Argentina ( PRICE, 1974 Price RD. A Review of the genus Pseudomenopon (Mallophaga: Menoponidae). Ann Entomol Soc Am 1974; 67(1): 73-84. http://dx.doi.org/10.1093/aesa/67.1.73.
http://dx.doi.org/10.1093/aesa/67.1.73 ...
; CICCHINO & CASTRO, 1998a Cicchino A, Castro DC. Amblycera. In: Morrone JJ, Coscarón S, editors. Biodiversidad de artrópodos Argentinos: una perspectiva biotaxonómica. Buenos Aires: Ediciones Sur; 1998a. p. 84-103. ; CICCHINO, 2011 Cicchino AC. Piojos (Insecta: Psocodea: Phthiraptera) parásitos de Gruiformes y Podicipediformes (Aves) en la Argentina: una aproximación sistemática, bioecológica y evolutiva [thesis]. Mar del Plata: Universidad Nacional de Mar del Plata; 2011. ).

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

Rallicola andinus (Phthiraptera: Ischnocera) ( Figure 7 ) was found in all analyzed birds. Rallicola Johnston & Harrison, 1911 is composed of 55 species, all of which are parasites of Guiformes and Chardriiformes birds ( CICCHINO & CASTRO, 1998b Cicchino A, Castro DC. Ischnocera. In: Morrone JJ, Coscarón S, editors. Biodiversidad de artrópodos Argentinos: una perspectiva biotaxonómica . Buenos Aires: Ediciones Sur; 1998b. p. 104-124. ). Since the first description of Rallicola andinus in plumbeous rail in Peru ( CARRIKER, 1949 Carriker MA. Neotropical Mallophaga miscellany. V. New genera and species. Rev Bras Biol 1949; 9(3): 297-313. ), this parasite has been recorded in Brazil, Argentina, and Chile ( EMERSON, 1955 Emerson KC. A review of the genus Rallicola (Philopteridae, Mallophaga) found on Aramidae, Psophiidae and Rallidae. Ann Entomol Soc Am 1955; 48(4): 284-299. http://dx.doi.org/10.1093/aesa/48.4.284.
http://dx.doi.org/10.1093/aesa/48.4.284...
; CICCHINO & EMERSON, 1983 Cicchino AC, Emerson CK. Contribución al conocimiento de los malófagos Argentinos. XIV. Algunos Philopteridae (Mallophaga, Ischnocera) nuevos o poco conocidos parásitos de Rallidae (Aves, Gruiformes). Neotropica 1983; 29(82): 151-172. ; CICCHINO, 2011 Cicchino AC. Piojos (Insecta: Psocodea: Phthiraptera) parásitos de Gruiformes y Podicipediformes (Aves) en la Argentina: una aproximación sistemática, bioecológica y evolutiva [thesis]. Mar del Plata: Universidad Nacional de Mar del Plata; 2011. ).

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

Two birds (15.4%) presented with Fulicoffula sp. (Phthiraptera: Ischnocera) ( Figure 8 ). This genus was originally erected to allocate all Ischnocera Kellogg, 1896 species with an elongated shape found on rallid birds ( EMERSON & PRICE, 1967 Emerson KC, Price RD. A new species of Fulicoffula (Mallophaga: Philopteridae) from Thailand. Entomol News 1967; 78(6): 163-166. ). The specimens found shared similarities with F. americana Emerson, 1960, but with notable differences in size. Equally, Cicchino (2011) Cicchino AC. Piojos (Insecta: Psocodea: Phthiraptera) parásitos de Gruiformes y Podicipediformes (Aves) en la Argentina: una aproximación sistemática, bioecológica y evolutiva [thesis]. Mar del Plata: Universidad Nacional de Mar del Plata; 2011. recently found a similar Fulicofulla Clay & Meinertzhagen, 1938 species on plumbeous rail that likely corresponded to a new species.

Figure 8
Light microscopy of Fulicoffula sp. showing head (A) and geniatalia (B) of male.

Gastrointestinal parasites

In 23 birds, six helminth species were found ( Table 2 ) to be distributed in the phylum Nematoda: Heterakis psophiae Travassos, 1913, Porrocaecum ardeae Frölich (1812), Tetrameres sp., and Capillaria sp.; Platyhelminthes: Diorchis sp.; and Acanthocephala: Plagiorhynchus sp.

Nematoda: Heterakis psophiae (Ascaridida) ( Figure 9 ) was a helminth with a higher prevalence rate (52.2%) and mean intensity (2.9). This parasite was found in the cecal lumen of 12 birds, as usually reported for members of this genus ( ATKINSON et al., 2008 Atkinson CT, Thomas NJ, Hunter DB. Parasitic diseases of wild birds. Ames: Wiley-Blackwell; 2008. http://dx.doi.org/10.1002/9780813804620.
http://dx.doi.org/10.1002/9780813804620...
). These parasites present a direct life cycle and worldwide distribution ( ATKINSON et al., 2008 Atkinson CT, Thomas NJ, Hunter DB. Parasitic diseases of wild birds. Ames: Wiley-Blackwell; 2008. http://dx.doi.org/10.1002/9780813804620.
http://dx.doi.org/10.1002/9780813804620...
), and they have been recorded on two previous occasions in Chile: H. gallinarum (Shrank, 1788) in eared dove Zenaida auriculata (Des Murs, 1847) in Ñuble, as well as H. dispar (Shrank, 1790) in upland goose Chloephaga picta (Gmelin, 1789) in the Magallanes region ( GONZÁLEZ et al., 2004 González D, Daugschies A, Rubilar L, Pohlmeyer K, Skewes O, Mey E. Fauna parasitaria de la tórtola común (Zenaida auriculata, de Murs 1847) (Columbiformes: Columbidae) en Ñuble, Chile. Parasitol Latinoam 2004; 59(1-2): 37-41. http://dx.doi.org/10.4067/S0717-77122004000100007.
http://dx.doi.org/10.4067/S0717-7712200...
; GONZÁLEZ et al., 2005 González D, Skewes O, Candia C, Palma R, Moreno L. Estudio del parasitismo gastrointestinal y externo en caiquén Chloephaga picta Gmelin, 1789 (Aves, Anatidae) en la Región de Magallanes, Chile. Parasitol Latinoam 2005; 60(1-2): 86-89. http://dx.doi.org/10.4067/S0717-77122005000100016.
http://dx.doi.org/10.4067/S0717-7712200...
). Heterakis psophiae was described by Travassos (1913) Travassos L. Sobre as especies brazileiras da subfamília Heterakinae Railliet & Henry. Mem Inst Oswaldo Cruz 1913; 5(3): 271-318. http://dx.doi.org/10.1590/S0074-02761913000300005.
http://dx.doi.org/10.1590/S0074-0276191...
from green-winged trumpeter Psophia viridis Spix, 1825 in Brazil; thus far, this parasite corresponds to the only known Heterakis species from South American Gruiformes.

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

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) Fanke J, Wibbelt G, Krone O. Mortality factors and diseases in free-ranging Eurasian Cranes (Grus grus) in Germany. J Wildl Dis 2011; 47(3): 627-637. http://dx.doi.org/10.7589/0090-3558-47.3.627. PMid:21719827.
http://dx.doi.org/10.7589/0090-3558-47....
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 Atkinson CT, Thomas NJ, Hunter DB. Parasitic diseases of wild birds. Ames: Wiley-Blackwell; 2008. http://dx.doi.org/10.1002/9780813804620.
http://dx.doi.org/10.1002/9780813804620...
; DZIEKONSKA-RYNKO et al., 2015 Dziekonska-Rynko J, Mierzejewska K, Hliwa P. Parasitic helminths in grey heron ( Ardea cinerea) chicks. Biologia 2015; 70(2): 279-282. http://dx.doi.org/10.1515/biolog-2015-0022.
http://dx.doi.org/10.1515/biolog-2015-0...
). There are several records of P. ardeae regularly affecting birds of the families Gruidae and Ardeidae in Europe and Central America ( SCHMIDT & NEILAND, 1973 Schmidt GD, Neiland KA. Helminth fauna of Nicaragua. V. Cardiofilaria stepheni sp. n. (Onchocercidae) and other nematodes of birds. Proc Helminthol Soc Wash 1973; 40(2): 285-288. ; HARTWICH, 1979 Hartwich G. Ascariden (Nematoda, Ascaridoidea) aus Vögeln von Ungarn. Parasit Hung 1979; 12: 79-85. ; FANKE et al., 2011 Fanke J, Wibbelt G, Krone O. Mortality factors and diseases in free-ranging Eurasian Cranes (Grus grus) in Germany. J Wildl Dis 2011; 47(3): 627-637. http://dx.doi.org/10.7589/0090-3558-47.3.627. PMid:21719827.
http://dx.doi.org/10.7589/0090-3558-47....
; DZIEKONSKA-RYNKO et al., 2015 Dziekonska-Rynko J, Mierzejewska K, Hliwa P. Parasitic helminths in grey heron ( Ardea cinerea) chicks. Biologia 2015; 70(2): 279-282. http://dx.doi.org/10.1515/biolog-2015-0022.
http://dx.doi.org/10.1515/biolog-2015-0...
; SITKO & HENEBERG, 2015 Sitko J, Heneberg P. Composition, structure and pattern of helminth assemblages associated with central European herons (Ardeidae). Parasitol Int 2015; 64(1): 100-112. http://dx.doi.org/10.1016/j.parint.2014.10.009. PMid:25449288.
http://dx.doi.org/10.1016/j.parint.2014...
).

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

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 Hinojosa-Sáez A, González-Acuña D. Estado actual del conocimiento de helmintos en aves silvestres de Chile. Gayana 2005; 69(2): 241-253. ; GONZÁLEZ-ACUÑA et al., 2010 González-Acuña D, Moreno L, Cicchino A, Mironov S, Kinsella JM. Checklist of the parasites of the black-necked swan, Cygnus melanocoryphus (Aves: Anatidae), with new records from Chile. Zootaxa 2010; 2637(1): 55-68. http://dx.doi.org/10.11646/zootaxa.2637.1.3.
http://dx.doi.org/10.11646/zootaxa.2637...
; VALDEBENITO et al., 2015 Valdebenito JO, Moreno L, Landaeta-Aqueveque C, Kinsella JM, Mironov S, Cicchino A, et al. Gastrointestinal and external parasites of Enicognathus ferrugineus and Enicognathus leptorhynchus (Aves, Psittacidae) in Chile. Rev Bras Parasitol Vet 2015; 24(4): 422-431. http://dx.doi.org/10.1590/S1984-29612015074. PMid:26648008.
http://dx.doi.org/10.1590/S1984-2961201...
). Among all members of this genus, Capillaria fulicae (Pavlov & Borgarenko (1959) is often found in rallid birds from North America ( KINSELLA, 1973 Kinsella JM. Helminth parasites of the American Coot, Fulica americana americana , on its winter range in Florida. Proc Helminthol Soc Wash 1973; 40(2): 240-242. ; KINSELLA et al., 1973 Kinsella JM, Hon LT, Reed PB. A comparison of the helminth parasites of the Common Gallinule (Gallinula chloropus cachinnans) and the Purple Gallinule ( Porphyrula martinica) in Florida. Am Midl Nat 1973; 89(2): 467-473. http://dx.doi.org/10.2307/2424053.
http://dx.doi.org/10.2307/2424053 ...
). 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.

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

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 Anderson RC. Nematode parasites of vertebrates: their development and transmission . 2nd ed. Wallingford: CABI Publishing; 2000. http://dx.doi.org/10.1079/9780851994215.0000.
http://dx.doi.org/10.1079/9780851994215...
). 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 Mollhagen TR. A study of the systematics and hosts of the parasitic nematode genus Tetrameres (Habronematoidea: Tetrameridae) [dissertation]. Lubbock: Texas Tech University; 1976. ; ATKINSON et al., 2008 Atkinson CT, Thomas NJ, Hunter DB. Parasitic diseases of wild birds. Ames: Wiley-Blackwell; 2008. http://dx.doi.org/10.1002/9780813804620.
http://dx.doi.org/10.1002/9780813804620...
), 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 Kinsella JM, Hon LT, Reed PB. A comparison of the helminth parasites of the Common Gallinule (Gallinula chloropus cachinnans) and the Purple Gallinule ( Porphyrula martinica) in Florida. Am Midl Nat 1973; 89(2): 467-473. http://dx.doi.org/10.2307/2424053.
http://dx.doi.org/10.2307/2424053 ...
; MOLLHAGEN, 1976 Mollhagen TR. A study of the systematics and hosts of the parasitic nematode genus Tetrameres (Habronematoidea: Tetrameridae) [dissertation]. Lubbock: Texas Tech University; 1976. ; AL-AWADI et al., 2010 Al-Awadi H, Mhaisen F, Al-Joborae F. Helminth parasitic fauna of aquatic birds in Bahr Al-Najaf Depression, Mid Iraq. Bull Iraq Nat Hist Mus 2010; 11(2): 7-15. ; BIRMANI et al., 2011 Birmani NA, Dharejo AM, Khan MM. First record of the genus Tetrameres Creplin, 1846 (Nematoda: Tetrameridae) in Pakistan. Pak J Nematol 2011; 29(2): 213-218. ).

Platyhelminthes: In the lumen of the small intestine of three birds (13%), nine parasites were found in poor condition; however, given their rostellum ( Figure 12 ) with 8 hooks 80 µm in length, they were placed in the genus Diorchis Clerc, 1903 (Cestoda: Hymenolepididae). This genus appears to commonly affect the avian families Anatidae, Rallidae and, occasionally, Charadriiformes ( MARINOVA et al., 2015 Marinova MH, Georgiev BB, Vasileva GP. Description of Diorchis thracica n. sp. (Cestoda, Hymenolepididae) from the Ruddy shelduck Tadorna ferruginea (Pallas) (Anseriformes, Anatidae) in Bulgaria. Syst Parasitol 2015; 91(3): 261-271. http://dx.doi.org/10.1007/s11230-015-9569-9. PMid:26063303.
http://dx.doi.org/10.1007/s11230-015-95...
). While several Diorchis species have been collected from Fulica Linnaeus, 1758 birds (e.g., MCLAUGHLIN, 1986 McLaughlin JD. Helminths of the Red-knobbed Coot (Fulica cristata) from Barberspan, Republic of South Africa. J Wildl Dis 1986; 22(4): 577-579. http://dx.doi.org/10.7589/0090-3558-22.4.577. PMid:3503147.
http://dx.doi.org/10.7589/0090-3558-22....
; GUILLÉN & MORALES, 2003 Guillén G, Morales E. First record of helminth parasites in Fulica ardesiaca (Aves: Rallidae) from Peru: Pantanos de Villa - Lima. Rev Peru Biol 2003; 10(2): 203-208. ; LUNASCHI et al., 2012 Lunaschi L, Merlo H, Damborenea C. Type material housed in the Helminthological Collection of the Museo de La Plata, Buenos Aires, Argentina. Zootaxa 2012; 3199: 1-59. ), only D. ralli Jones, 1944 was found in rallids, affecting king rail, Rallus elegans Audubon, 1834, in North America ( JONES, 1944 Jones AW. Diorchis ralli n. sp., a Hymenolepidid Cestode from the King Rail. Trans Am Microsc Soc 1944; 63(1): 50-53. http://dx.doi.org/10.2307/3223337.
http://dx.doi.org/10.2307/3223337 ...
).

Figure 12
Light microscopy of Diorchis sp. showing hooks of rostellum.

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 Yamaguti S. Systema Helminthum: Acanthocephala. New York: Interscience Publisher; 1963. (vol. 5). ), including rallids ( YOSHINO et al., 2009 Yoshino T, Nakamura S, Endoh D, Onuma M, Osa Y, Teraoka H, et al. A helminthological survey of four families of waterfowl (Ardeidae, Rallidae, Scolopacidae and Phalaropodidae) from Hokkaido, Japan. J Yamashina Inst Ornithol 2009; 41(1): 42-54. http://dx.doi.org/10.3312/jyio.41.42.
http://dx.doi.org/10.3312/jyio.41.42 ...
; ONUMA et al., 2011 Onuma M, Yoshino T, Zhao C, Nagamine T, Asakawa M. Parasitic helminths obtained from Okinawa Rails Gallirallus okinawae. J Yamashina Inst Ornithol 2011; 43(1): 74-81. http://dx.doi.org/10.3312/jyio.43.74.
http://dx.doi.org/10.3312/jyio.43.74 ...
). 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 Atkinson CT, Thomas NJ, Hunter DB. Parasitic diseases of wild birds. Ames: Wiley-Blackwell; 2008. http://dx.doi.org/10.1002/9780813804620.
http://dx.doi.org/10.1002/9780813804620...
).

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 Kamiya T, O’Dwyer K, Nakagawa S, Poulin R. What determines species richness of parasitic organisms? A meta-analysis across animal, plant and fungal hosts. Biol Rev Camb Philos Soc 2014; 89(1): 123-134. http://dx.doi.org/10.1111/brv.12046. PMid:23782597.
http://dx.doi.org/10.1111/brv.12046 ...
). 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 Leung TL, Koprivnikar J. Nematode parasite diversity in birds: the role of host ecology, life history and migration. J Anim Ecol 2016; 85(6): 1471-1480. http://dx.doi.org/10.1111/1365-2656.12581. PMid:27496635.
http://dx.doi.org/10.1111/1365-2656.125...
). These ecosystems also serve as stopover point for many migrant bird species usually presenting elevated parasite diversity ( LEUNG & KOPRIVNIKAR, 2016 Leung TL, Koprivnikar J. Nematode parasite diversity in birds: the role of host ecology, life history and migration. J Anim Ecol 2016; 85(6): 1471-1480. http://dx.doi.org/10.1111/1365-2656.12581. PMid:27496635.
http://dx.doi.org/10.1111/1365-2656.125...
). Additionally, studies on sympatric species, including various birds from the family Ardeidae ( NAVARRO et al., 2005 Navarro P, Lluch J, Font E. The component helminth community in six sympatric species of Ardeidae. J Parasitol 2005; 91(4): 775-779. http://dx.doi.org/10.1645/GE-3342.1. PMid:17089743.
http://dx.doi.org/10.1645/GE-3342.1 ...
) and F. americana ( CANARIS & WALDMANN, 2017 Canaris AG, Waldmann ME. Metazoan parasites of the American Coot, Fulica americana , from the Rio Grande Valley in Colorado and Southwest, Texas, U.S.A., with a checklist of parasites for North America and West Indies. Comp Parasitol 2017; 84(2): 102-110. http://dx.doi.org/10.1654/1525-2647-84.2.102.
http://dx.doi.org/10.1654/1525-2647-84....
), have shown similar species richness and diversity.

Although Skoracki et al. (2014) Skoracki M, Unsoeld M, Skorupski M, Kavetska K. Syringophilid mites (Acari: Syringophilidae) associated with the rails (Aves: Rallidae) and a key to the species of the genus Rafapicobia Skoracki, 2011. Syst Parasitol 2014; 88(3): 227-232. http://dx.doi.org/10.1007/s11230-014-9502-7. PMid:24935125.
http://dx.doi.org/10.1007/s11230-014-95...
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) Cicchino AC. Piojos (Insecta: Psocodea: Phthiraptera) parásitos de Gruiformes y Podicipediformes (Aves) en la Argentina: una aproximación sistemática, bioecológica y evolutiva [thesis]. Mar del Plata: Universidad Nacional de Mar del Plata; 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 SR. Estudio sistemático y biológico de un digeneo perteneciente a la familia Microphallidae Travassos, 1920. I: Microphallus szidati sp. nov. parásito intestinal de Rallus sanguinolentus sanguinolentus (Aves, Rallidae) e Himantopus melanurus (Aves, Recurvirrostridae). Rev Iber Parasitol 1986; 46(4): 373-378. ; MARTORELLI, 1987 Martorelli SR. Estudios parasitológicos en biotopos lenticos de la republica argentina. IV. El ciclo biológico de Echinostoma parcespinosum Lutz, 1924 (Digenea) parásito de Rallus maculatus maculatus y Rallus sanguinolentus sanguinolentus (Aves: Rallidae). Rev Mus La Plata 1987; 14(153): 47-62. ) 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) Jackson D, Jackson D. Record of Pomacea canaliculata (Lamarck, 1822) (Ampullariidae), exotic mollusk for to North Chile. Gayana 2009; 73(1): 40-44. 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 Martorelli SR. Estudios parasitológicos en biotopos lenticos de la republica argentina. IV. El ciclo biológico de Echinostoma parcespinosum Lutz, 1924 (Digenea) parásito de Rallus maculatus maculatus y Rallus sanguinolentus sanguinolentus (Aves: Rallidae). Rev Mus La Plata 1987; 14(153): 47-62. ), 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 Leung TL, Koprivnikar J. Nematode parasite diversity in birds: the role of host ecology, life history and migration. J Anim Ecol 2016; 85(6): 1471-1480. http://dx.doi.org/10.1111/1365-2656.12581. PMid:27496635.
http://dx.doi.org/10.1111/1365-2656.125...
; GUTIÉRREZ et al., 2017 Gutiérrez JS, Rakhimberdiev E, Piersma T, Thieltges DW. Migration and parasitism: habitat use, not migration distance, influences helminth species richness in Charadriiform birds. J Biogeogr 2017; 44(5): 1137-1147. http://dx.doi.org/10.1111/jbi.12956.
http://dx.doi.org/10.1111/jbi.12956 ...
). 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.

Acknowledgements

The authors thank Carolina Silva de la Fuente, Gonzalo Torres, Pedro Pablo Álvarez, Karen Ardiles and Sofia González Ardiles for their support and help processing the samples, and Sebastián Muñoz-Leal for providing the abstract in Portuguese. This research work was founded by the Fondo Nacional de Desarrollo Científico y Tecnológico (FONDECYT) 1130948, 1170972. JOV was funded by the Comisión Nacional de Investigación Científica y Tecnológica (CONICYT), Becas Chile 72170569.

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Publication Dates

  • Publication in this collection
    06 Sept 2018
  • Date of issue
    Jul-Sep 2018

History

  • Received
    22 Feb 2018
  • Accepted
    03 May 2018
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