First record of helminths parasitizing Vanellus chilensis (Aves, Charadriiformes) in Acre state, southwestern Brazilian Amazon

Primeiro registro de helmintos parasitando Vanellus chilensis (Aves, Charadriiformes) no estado do Acre, sudoeste da Amazônia brasileira

ABSTRACT

The southern lapwing, Vanellus chilensis, is a bird frequently seen in most of Brazil. Although it is widely distributed in other Brazilian biomes, including some parts of the Brazilian Amazon, it has only been recorded in the western Amazonian state of Acre since 2000. We report the presence of intestinal parasites in individuals of V. chilensis from the Cazumbá-Iracema Extractive Reserve in Acre through a coproparasitological analysis. Seven of the nine sampled individuals were parasitized. We observed larvae of Strongyloides sp. (28.5% of the samples), and eggs of Ascaridia sp. (28.5%), Ancylostoma sp. (14.2%), and Choanotaenia sp. (42.8%). These parasites are reported for the first time parasitizing V. chilensis in Brazil. The parasitized birds may act as reservoirs and were recorded in a peridomicile area, which may facilitate their contact with domestic birds.

KEYWORDS:
endoparasites; wild birds; Nematoda; Cestoda; coproparasitology

RESUMO

O quero-quero, Vanellus chilensis é uma ave vista com frequência no Brasil. Apesar de ser uma espécie amplamente distribuída em todos os biomas brasileiros, incluindo algumas partes da Amazônia bresileira, somente a partir de 2000 começou a ser observado no Estado do Acre. Neste trabalho relatamos a presença de parasitas intestinais em indivíduos de V. chilensis capturados na Reserva Extrativista Cazumbá-Iracema, no Acre, por meio de análise coproparasitológica. Dos nove indivíduos com amostras coletadas, sete estavam parasitados. Foram encontradas larvas de Strongyloides sp. (28,5%), ovos de Ascaridia sp. (28,5%), ovos de Ancylostoma sp. (14,2%) e ovos de Choanotaenia sp. (42,8%). Estes parasitos são registrados pela primeira vez parasitando V. chilensis no Brasil. As aves parasitadas podem atuar como reservatórios e foram registradas em área de peridomicílio, o que pode facilitar o contato com aves domésticas.

PALAVRAS-CHAVE:
endoparasitos; aves silvestres; Nematoda; Cestoda; coproparasitologia

The genus Vanellus Brisson, 1760 has 24 species, which are found on all continents (Wiersma and Kirwan 2020), but only two species occur in Brazil, the pied lapwing, Vanellus cayanus (Latham, 1790) and the southern lapwing, Vanellus chilensis (Molina, 1782) (Piacentini et al. 2015). Vanelus chilensis is found primarily in the vicinity of water bodies, including rivers, lakes, wetlands, and beaches, but also inhabits open fields, pastures, and even urban environments (Sick 2001; Wiersma and Kirwan 2020). These birds may live in groups of more than 100 individuals, within which individuals defend territories and engage in anti-predator vigilance (Maruyama et al. 2009).

As V. chilensis does not undertake any major post-reproductive migration, it is considered to be a sedentary species, although it may travel short distances to avoid flooding and other changes in the local environment (Guimarães et al. 2016). It is a typical bird from South America, but its distribution has already expanded to Central and North America (Wiersma and Kirwan 2020). It has also extended to the Amazon biome (Guilherme and Czaban 2015; Guimarães et al. 2016), where it has colonized areas that have been deforested for cattle ranching, with rivers and roads providing dispersal corridors that have allowed the species to reach the interior of the biome (Guilherme and Czaban 2015; Borges et al. 2017). Vanelus chilensis is considered to be an invasive species in the Brazilian state of Acre, where it can now be found on river margins during the dry season, as well as in cattle pastures and urban environments (Guilherme and Czaban 2015; Guilherme 2016).

The helminth fauna of V. chilensis is little known. The existing studies are restricted to some regions of Brazil and Argentina, with records of individuals parasitized by Platyhelminthes Gegenbaur, 1859, Acanthocephala Rudolphi, 1808 and Nematoda Rudolphi, 1808 (Travassos and Freitas 1940; Rêgo 1968; Pinto and Noronha 1972; Vicente et al. 1995; Avancini 2009; Silveira 2016). Here we report the first record of the presence of intestinal parasites in V. chilensis in the Amazon biome based on coproparasitological tests.

Birds were captured in the Extractivist Reserve Cazumbá-Iracema (Resex do Cazumbá-Iracema), a federal environmental protection area that covers a total of 750,794.70 ha in the municipality of Sena Madureira, Acre state, Brazil. Captures occurred in May and June 2018 in the community of Cuidado (9°08’47.2”S, 69°01’05.3”W), in the northwestern extreme of the reserve (Figure 1). The area has a considerable diversity of fauna and flora typical of the Western Amazon Corridor, one of seven major ecological corridors proposed for Brazil (ICMBio 2007).

Figure 1
Location of the state of Acre in Brazil, and of the site at which Vanellus chilensis was captured (red dot) within the Cazumbá-Iracema Extractivist Reserve in the municipality of Sena Madureira. This figure is in color in the electronic version.

Individuals of V. chilensis were first observed in a group of approximately 16 birds in an area of pasture near local residences (Figure 2). These individuals were captured using five mist nets. The nets were set at 5:00 am and closed at 5:30 pm, three times per week during the study period. Each individual captured in the nets was placed in a cloth bag containing absorbent paper for 20 min, before being released at the capture site. The feces deposited by the birds in the bags were collected in sterile containers containing a Merthiolate-Iodine-Formaldehyde (MIF) solution for preservation until the parasitological analysis. The capture and handling of individuals and the collection of feces was authorized by the Ethics Committee on the Use of Animals of Universidade Federal do Acre (CEUA/UFAC nr. 2107.009788/2016-01) and Instituto Chico Mendes de Conservação da Biodiversidade - ICMBio (SISBIO license nr. 54692-2).

Figure 2
Individuals of southern lapwing, Vanellus chilensis in a pasture in the study area in Sena Madureira, Acre, Brazil. Credit: Edson Guilherme. This figure is in color in the electronic version.

The samples were sent for coproparasitological analysis to the Laboratory of Biology and Parasitology of Wild Mammal Reservoirs of Instituto Oswaldo Cruz (LABPMR/IOC), Rio de Janeiro, Brazil. The diagnosis was based on three complementary techniques: (i) direct examination of the fresh feces, stained with Lugol’s solution; (ii) spontaneous sedimentation; and (iii) centrifugal flotation with saturated sucrose solution under optical microscopy. All the parasite specimens observed during these analyses were photographed and measured using 10x and 40x magnification (Axio Scope A1). The parasites were identified based on the diagnostic characteristics described by Foret (2005) and Zajac and Conboy (2011). Testimony material was deposited in the Helminthological Collection of the Instituto Oswaldo Cruz (CHIOC 38988 -38991).

Eleven lapwings were captured in the mist nets, of which, nine (82%) provided fecal samples. The analysis of these samples revealed the presence of parasites in 77.8% (n = 7) of the cases. Four helminth taxa were identified, three nematodes and one cestode (Figure 3). Eggs of the cestode Choanotaenia sp. were the most common, present in three (42.8%) of the seven samples. Larvae of Strongyloides sp. were observed in two (28.5%), eggs of Ascaridia sp. in two (28.5%) and eggs of Ancylostoma sp. in one (14.2%) of the samples. Overall, 58 helminth eggs or larvae were found, of which almost half (48%, n = 28) were Choanotaenia sp. eggs, 24% (n = 14) were Ascaridia sp. eggs, 17% (n = 10) were Ancylostoma sp. eggs, and 10% (n = 6) were larvae of Strongyloides sp. (Figure 3).

Figure 3
Endoparasites found in the feces of southern lapwings, Vanellus chilensis captured in the Cazumbá-Iracema Extractive Reserve in Sena Madureira, Acre, Brazil. A - egg of Choanotaenia sp. (amplified 40x); B - egg of Ancylostoma sp. (20x); C - egg of Ascaridia sp. (20x); D - larva of Strongyloides sp. (20x). This figure is in color in the electronic version.

Helminths have already been recorded parasitizing V. chilensis in a number of Brazilian states (Table 1), based on necropsy and the analysis of internal organs. Overall, six species of Nematoda, four species of Digenea, four species of Cestoda, and four of Acanthocephala were recorded. Travassos and Freitas (1940) reported the infection of two southern lapwings by cestodes during a scientific survey of a railroad in Mato Grosso do Sul, Brazil, but did not identify the taxon.

Table 1
Helminths observed parasitizing Vanellus chilensis in Brazil.

Parasite	Stage	Organ infected	Brazilian state	Reference
Nematodes
Ancylostoma sp.	Eggs	Feces	Acre	Present study
Ancyracanthopsis coronata	Adult	Gizzard	Not reported	Vicente et al. 1995
Ascaridia sp.	Eggs	Feces	Acre	Present study
Brevithominx asperodorsus	Adult	Gizzard	Rio Grande do Sul	Avancini 2009
Capillariidae	Adult	Gizzard, esophagus, trachea	Paraná	Silveira 2016
Dispharynx nasuta*	Adult	Gizzard, proventricle	Rio Grande do Sul	Avancini 2009
Heterakis psophiae*	Adult	Cecum, proventricle, duodenum, large intestine	Rio Grande do Sul	Avancini 2009
Oxyspirura matogrosensis	Adult	Eyes	Not reported	Vicente et al. 1995
Strongyloides sp.	Larvae	Feces	Acre	Present study
Digenetics
Echinostoma aphylactum	Adult	Small intestine, large intestine	Rio Grande do Sul	Avancini 2009
Leucochloridium parcum	Adult	Cloaca	Paraná	Silveira 2016
Neivaia cymbium	Adult	Bill, trachea	Rio Grande do Sul	Avancini 2009
Stomylotrema vicarium	Adult	Large intestine, cecum	Rio Grande do Sul	Avancini 2009
Cestodes
Choanotaenia sp.	Eggs	Feces	Acre	Present study
Gyrocoelia crassa	Adult /strobe	Small intestine	Pará, Mato Grosso	Rêgo 1968
			Minas Gerais	Pinto and Noronha 1972
Gyrocoelia perversa	Adult	Small intestine	Rio Grande do Sul	Avancini 2009
Infula macrophallus	Adult	Jejunum, anterior ileum	Paraná	Silveira 2016
Parachoanotaenia macracantha	Adult	Small intestine	Pará, Mato Grosso	Rêgo 1968
Cestoda	Not reported	Not reported	Mato Grosso do Sul	Travassos and Freitas 1940
Acanthocephala
Centrorhynchus sp.	Adult	Jejunum, posterior ileum	Paraná	Silveira 2009
Gigantorhynchida	Adult	Jejunum, posterior ileum	Paraná	Silveira 2009
Mediorhynchus sp.	Adult	Jejunum, posterior ileum	Paraná	Silveira 2009
Plagiorhynchus sp.	Adult	Jejunum, posterior ileum	Paraná	Silveira 2009

We observed V. chilensis in peridomicile areas in very close proximity to human residences, which may facilitate their contact with domestic birds. Ascaridia galli, Strongyloides sp., and Choanotaenia sp. are all known to parasitize domestic birds (Olivares et al. 2006; Siqueira and Marques 2016; Marques et al. 2019; Neto et al. 2020) and, in the same region in Acre where the individuals of V. chilensis were captured, we have recorded parasites of three taxa (Strongyloides sp., Ascaridia sp., and Strongylida) in other bird species (Souza et al. 2020), which indicates possible transmission between local birds that share the same environment.

Wild animals are considered to be potential hosts and reservoirs of parasitic diseases, and wild birds, whether free-ranging or in captivity, may act as reservoirs of diseases that may be transmitted to humans (Souza et al. 2018). This emphasizes the importance of further research to catalogue the parasitological fauna of wild birds in the study region, together with molecular analyses to verify the possible presence of parasites with zoonotic potential that may infect the local human population.

ACKNOWLEDGMENTS

We would like to thank Mrs. Maria Marilene Rufino, the adminsitrator of the Cazumbá-Iracema Extractive Reserve, for her support during fieldwork, with special thanks to the residents of the Cazumbá Reserve for their help with the bird captures, in particular, Mr. José Acácio and Mrs. Francisca da Rocha.

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• CITE AS:

  Souza, L.S.; Souza, L.S.; Guilherme, E.; Santos, F.G.A. 2021. First record of helminths parasitizing Vanellus chilensis (Aves, Charadriiformes) in Acre state, southwestern Brazilian Amazon. Acta Amazonica 51: 255-259.

Edited by

ASSOCIATE EDITOR:

Sérgio H. Borges

Publication Dates

• Publication in this collection
  20 Sept 2021
• Date of issue
  Jul-Sep 2021

History

• Received
  22 Mar 2021
• Accepted
  09 Apr 2021