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Journal of Parasitic Diseases: Official Organ of the Indian Society for Parasitology logoLink to Journal of Parasitic Diseases: Official Organ of the Indian Society for Parasitology
. 2021 Jun 15;45(4):1114–1122. doi: 10.1007/s12639-021-01403-z

Diversity of endohelminths parasitizing bred Muscovy ducks Cairina moschata domestica (Anseriformes: Anatidae) from the eastern Brazilian Amazon

Elaine Lopes de Carvalho 1,2, Ricardo Luís Sousa Santana 1,2, Raimundo Nonato Moraes Benigno 3, Raul Henrique da Silva Pinheiro 2,4, Marcos Tavares-Dias 5,✉, Elane Guerreiro Giese 1,2,✉
PMCID: PMC8556447  PMID: 34789997

Abstract

Raising of Muscovy ducks Cairina moschata domestica for subsistence of human populations is common in northern Brazil, although their helminth infections have been poorly investigated, despite the possible presence of helminths with zoonotic potential. The aim of this study was to investigate the diversity of parasite endohelminths in C. moschata domestica raised in the Marajó Island region, state of Pará, Brazilian Amazon region. Of 33 specimens examined, 90.9% were parasitized by one or more parasite species, for a total of 926 parasites recorded. The species mean richness of endohelminths varied from 0 to 6, and there was a predominance of hosts with 1 to 2 species of parasite endohelminths and low prevalence and low abundance of parasites. This was the first report of larvae of Anisakis sp., Contracaecum sp., Hysterotylacium sp., Raphidascaris sp., Eustrongylides sp., Syngamus sp., Ascocotyle sp. and Athesmia heterolecithodes for C. moschata domestica. The parasitic community of C. moschata domestica was composed of 11 species, with a high species richness for nematode species and a small number of digeneans.

Keywords: Avian, Diversity, Helminths, Infection, Parasites

Introduction

Muscovy ducks Cairina moschata domestica (Linnaeus, 1758) are birds adapted to varied climatic conditions and have been widely bred due to their ease in handling (Béjcek & Stastný 2008). They have adapted to the captive breeding system, especially when that involves cool places with good availability of water and space (Geromel 2012). In Brazil, ducks for subsistence of human populations are common, but the hygienic and sanitary conditions of raising have been little investigated (Souza-Almeida et al. 2016). Although ducks have great physical resistance, they are susceptible to disease because they are particularly prone to infections caused by parasitic helminths (Gower 1939; Mattos-Junior et al. 2008). However, the helminth infections of the Muskovy ducks C. moschata domestica have been poorly studied (Carvalho et al. 2019), despite possible losses in terms of reduced body growth and mortality in breeding, as well as the presence of helminths with zoonotic potential. Carvalho et al. (2020) described the first report of Anisakis sp. parasitizing Muscovy duck in Marajó Island, State of Pará (Brazil). In addition, Gnathostoma sp. has been reported in tetraodontiform Colomesus Psittacus (Bloch & Schneider 1801) from Marajó Island (Pinheiro et al. 2017).

Infection by nematodes, cestodes and trematodes has been reported for C. moschata domestica (Table 1), although only a few studies have been carried out with domestic animals (Muhairwa et al. 2007; Mattos-Junior et al. 2008; Carvalho et al. 2019, 2020). Muscovy ducks are one of the food items for human populations in the northern region of Brazil, including Marajó Island, state of Pará, in the Brazilian Amazon. Eggs of nematodes, trematodes and cestodes were reported from Cyanoloxia rothschildii, Paroaria gularis and Tangara episcopus kept in captivity in the city of Belém, State of Pará (Magalhães-Matos et al. 2016). As there are few studies about helminths in C. moschata domestica, the knowledge related to diversity of these parasites is consequently limited, and the community structure of endohelminths is unknown so far.

Table 1.

Endohelminths in Cairina moschata domestica from different localities

Parasite species Taxon Locality References
Eucoleus cairinae Lopez-Neyra, 1947 Nematoda Brazil Vicente et al. (1995)
Eucoleus contortus Gagarin, 1951 Nematoda Brazil Carvalho et al. (2019)
Eucoleus contortus Creplin, 1839 Nematoda Tanzania Muhairwa et al. (2007)
Heterakis gallinarum Schrank, 1788 Nematoda Brazil Vicente et al. (1995)
Heterakis gallinarum Schrank, 1788 Nematoda Brazil Machado et al. (2006)
Heterakis gallinarum Schrank, 1788 Nematoda Tanzania Muhairwa et al. (2007)
Heterakis neglecta Chabaud, 1975 Nematoda Brazil Vicente et al. (1995)
Heterakis neglecta Chabaud, 1975 Nematoda Brazil Machado et al. (2006)
Tetrameres fissispina Travassos, 1914 Nematoda Brazil Vicente et al. (1995)
Hadjelia neglecta Chabaud, 1975 Nematoda Brazil Mattos-Junior et al. (2008)
Capillaria phasianina Kotlán, 1914 Nematoda Brazil Mattos-Junior et al. (2008)
Tetrameres fissispina Travassos, 1914 Nematoda Brazil Mattos-Junior et al. (2008)
Eucoleus cairinae Lopez & Neyra, 1947 Nematoda Brazil Mattos-Junior et al. (2008)
Ascaridia columbae Gmelin, 1790 Nematoda Tanzania Muhairwa et al. (2007)
Ascaridia dissimilis Pérez-Vigueras, 1931 Nematoda Tanzania Muhairwa et al. (2007)
Ascaridia galli Schrank, 1788 Nematoda Tanzania Muhairwa et al. (2007)
Capillaria anatis Schrank, 1790 Nematoda Tanzania Muhairwa et al. (2007)
Capillaria annulata Molin, 1858 Nematoda Tanzania Muhairwa et al. (2007)
Heterakis dispar Schrank, 1790 Nematoda Tanzania Muhairwa et al. (2007)
Heterakis isolanche Linstow, 1906 Nematoda Tanzania Muhairwa et al. (2007)
Subulura strongylina Rudolphi, 1819 Nematoda Tanzania Muhairwa et al. (2007)
Subulura brumpti Cram, 1927 Nematoda Tanzania Muhairwa et al. (2007)
Subulura sucturia Molin, 1860 Nematoda Tanzania Muhairwa et al. (2007)
Tetrameres sp. Nematoda Brazil Vicente et al. (1995)
Tetrameres sp. Nematoda Brazil Machado et al. (2006)
Heterakis sp. Nematoda Brazil Vicente et al. (1995)
Heterakis sp. Nematoda Brazil Machado et al. (2006)
Subulura sp. Nematoda Brazil Vicente et al. (1995)
Subulura sp. Nematoda Brazil Machado et al. (2006)
Capillaria sp. Nematoda Brazil Vicente et al. (1995)
Capillaria sp. Nematoda Brazil Mattos-Junior et al. (2008)
Anisakis sp. Nematoda Brazil Carvalho et al. (2020)
Raillietina echinobothrida Mégnin, 1880 Cestoda Tanzania Muhairwa et al. (2007)
Raillietina tetragona Molin, 1858 Cestoda Tanzania Muhairwa et al. (2007)
Fimbriaria fasciolaris Frolich, 1802 Cestoda Brazil Mattos-Junior et al. (2008)
Lateriporus sp. Cestoda Brazil Mattos-Junior et al. (2008)
Prosthogonimus sp. Trematoda Brazil Machado et al. (2006)
Echinostoma revolutum Frolich, 1802 Trematoda Brazil Mattos-Junior et al. (2008)
Echinostoma mendax Dietz, 1909 Trematoda Brazil Machado et al. (2006)
Echinostoma revolutum Froelich, 1802 Trematoda Brazil Machado et al. (2006)
Ophthalmophagus magalhãesi Travassos, 1921 Trematoda Brazil Machado et al. (2006)
Zigocotyle lunatum Diesing, 1836 Trematoda Brazil Machado et al. (2006)
Typhlocoelum cucumerinum Rudolphi, 1809 Trematoda Brazil Machado et al. (2006)
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Several patterns associated with parasitic communities of different animal host populations can be detected through quantitative descriptors as diversity index and species richness (Magurran 2004). Such studies provide relevant information about avian host populations and expand the knowledge of parasite-host-environment interactions (Bush et al. 1997; Sanmartín et al. 2004; Carvalho et al. 2020). Since several studies in bird hosts (Gower 1939; Alexander & Mclaughlin 1997; Sanmartín et al. 2004; Junker et al. 2008), have focused on the determinant factors structuring the species richness of the communities of parasitic helminths, a diverse and interactive community can be expected, based on their complex habitats and feeding practices (Alexander & Mclaughlin 1997; Navarro et al. 2005). The local populations of potential definitive and intermediate hosts also have an important influence on helminth community patterns in avian species because of the set of helminths they support (Alexander & Mclaughlin 1997; Navarro et al. 2005; Carvalho et al. 2020). Thus, the aim of this study was to investigate the diversity of parasite endohelminths in C. moschata domestica, raised in the region of Marajó Island, state of Pará (Brazil).

Materials and methods

Ducks and collection

Collection was performed from June 2018 to August 2019 in accordance with the Ethics Committee for Animal Use (CEUA-UFRA) under protocol No 030/2018. Thirty-three C. moschata domestica ducks (21 females and 12 males, aged 4–8 months) were acquired from rural properties of the municipality of Soure (00° 43′ 00″ S; 48° 31′ 24″ W), on Marajó Island. The ducks were components of small extensively raised herds with free access to the environment, used to provide food for families or for sale in local markets. The ducks were slaughtered by stunning with a club, cutting the blood vessels of the neck and exsanguination on the farm and only the organs of the digestive tract were transported to the Laboratório de Histologia e Embriologia Animal/UFRA, Campus Belém (PA, Brazil) for parasitological analyses. The organs are placed in airtight bags, identified and transported in an isothermal box containing ice. In the laboratory, all the duck parts were weighed in a balance (Ramuzatron 15 BAT, Brazil), and organs were separated, individualized, and placed in Petri dishes with NaCl 0.9% solution and examined in less than 24 h, using a stereomicroscope (LEICA-ES2) using ampliation from 5 x (Carvalho et al. 2019). The contents of the lumen and wall were individualized in Petri dish and analyzed separately using a stereomicroscope (LEICA-ES2) using ampliation from 5 x. We do not use sieves because the content was analyzed separately with the aid of a stereomicroscope (LEICA-ES2), being only removed from the analysis of corn grain and plant fragments. The lining of the gizzard was removed to search for parasites. The recovered nematodes were fixed in a solution of AFA (93 parts of 70% ethanol, 5 parts of formaldehyde, and 2 parts of glacial acetic acid) and processed using light microscopy and scanning electron microscopy according to the method described by Pinheiro et al. (2018). Amman's lactophenol (crystallized phenol 20 g, lactic acid 20 mL, glycerin 40 mL and distilled water 20 mL) was used to observe the internal structures of nematodes for taxonomic identification. Nematodes were clarified with Amman´s lactophenol solution, placed on a microscope slide under a coverslip as a temporary mount, observed using a light microscope, and photographed using a photomicroscope (LEICA DM2500) with an imaging capture system. The trematodes specimens were compressed and fixed in AFA, stained with alcoholic carmine, dehydrated in an alcohol series, clarified in methyl salicylate and mounted on permanent slides for light microscopy analysis. Taxonomic classification of nematodes was according to Moravec (1982); Vicente et al. (1995) and Gibbons (2010), and for trematodes was based in the works of Travassos (1969); Jones et al. (2002); Jones et al. (2005) and Bray et al. (2008).

Parasite collection and analysis

Ecological terms (prevalence, mean intensity and mean abundance) were used following Bush et al. (1997). We used Diversity software (Pisces Conservation Ltd., UK) to calculate the following descriptors for the parasite community: for species richness of parasites, the Brillouin diversity index (HB), evenness (E) in association with the diversity index, and the dominance frequency (percentage of the infrapopulation in which a parasite species is numerically dominant) (Rohde et al. 1995; Magurran 2004). In order to detect the distribution pattern of the parasite infrapopulation (Rózsa et al. 2000), the index of dispersion (ID) and the Poulin discrepancy index (D) were calculated using Quantitative Parasitology 3.0 software for species with prevalence > 10%. The ID significance for each infrapopulation was tested using d-statistics (Ludwig & Reynolds 1988).

The Shapiro–Wilk test was applied to determine whether the parasite abundance data followed a normal distribution, and Barlett test to homocedasticity. The G-test was used for determining the sex effect of host sex in the prevalence of parasites, and the Mann–Whitney test (U), was employed to compare the abundance of species of parasites between male and female hosts. The Spearman correlation coefficient (rs) was used for evaluating possible correlation of abundance and prevalence of helminths with the weight of hosts, as well as with the Brillouin index (Zar 2010).

Results

Of 33 specimens of C. moschata domestica examined, 90.9% were parasitized by one or more parasite species, and a total of 926 parasites were collected from different organs. A predominance of nematode larvae such as Anisakis sp., Contracaecum sp., Hysterotylacium sp., Raphidascaris sp., Eustrongylides sp., Syngamus sp., Capillaria sp. and Subulura sp. was found. Among these parasites, Anisakis sp. and Eucoleus contortus Creplin, 1839 were the dominant species (Table 2). Infection by Anisakis sp. presented a random dispersion, while Capillaria sp. and E. contortus presented an aggregated dispersion (Table 3).

Table 2.

Parasitological indices of endohelminths in Cairina moschata domestica (N = 33) from the eastern Amazon (Brazil)

SI Parameters Eucoleus contortus Anisakis sp. Contracaecum sp. Hysterotylacium sp. Raphidascaris sp. Eustrongylides sp. Syngamus sp. Capillaria sp. Subulura sp. Athesmia heterolecithodes Ascocotyle sp.
Esophagus P (%) 75.8 9.1 3.0 6.1 3.0 0 0 0 0 0 0
MI 11.2 95.7 3.0 2.0 1.0 0 0 0 0 0 0
MA 85 8.7 0.1 0.1 0.03 0 0 0 0 0 0
NTP 281 287 3 4 1 0 0 0 0 0 0
FD (%) 30.3 31.0 0.3 0.4 0.1 0 0 0 0 0 0
Gizzard P (%) 9.1 9.1 0 0 0 0 0 0 0 0 0
MI 10.7 0.3 0 0 0 0 0 0 0 0 0
MA 1 0.03 0 0 0 0 0 0 0 0 0
NTP 32 1 0 0 0 0 0 0 0 0 0
FD (%) 3.5 0.1 0 0 0 0 0 0 0 0 0
Proventriculus P (%) 12.1 0 6.1 0 0 0 0 0 0 0 0
MI 17.3 0 3.5 0 0 0 0 0 0 0 0
MA 2.1 0 0.2 0 0 0 0 0 0 0 0
NTP 69 0 7 0 0 0 0 0 0 0 0
FD (%) 7.5 0 0.8 0 0 0 0 0 0 0 0
Ventriculus P (%) 0 0 12.1 0 0 0 0 0 0 0 0
MI 0 0 2.3 0 0 0 0 0 0 0 0
MA 0 0 0.3 0 0 0 0 0 0 0 0
NTP 0 0 9 0 0 0 0 0 0 0 0
FD (%) 0 0 1.0 0 0 0 0 0 0 0 0
Cecum P (%) 0 0 0 0 0 0 0 54.5 3.3 0 0
MI 0 0 0 0 0 0 0 10.5 2.0 0 0
MA 0 0 0 0 0 0 0 5.7 0.2 0 0
NTP 0 0 0 0 0 0 0 189 2 0 0
FD (%) 0 0 0 0 0 0 0 20.4 0.2 0 0
Colon P (%) 0 0 0 0 0 3.0 0 0 0 0 0
MI 0 0 0 0 0 1.0 0 0 0 0 0
MA 0 0 0 0 0 0.03 0 0 0 0 0
NTP 0 0 0 0 0 1 0 0 0 0 0
FD (%) 0 0 0 0 0 0.1 0 0 0 0 0
Intestine P (%) 0 3.0 3.0 0 0 0 0 3.0 3.3 0 3.0
MI 0 1.0 2.0 0 0 0 0 8.0 2.0 0 1.0
MA 0 0.03 0.1 0 0 0 0 0.2 0.2 0 0.03
NTP 0 1 2 0 0 0 0 8 2 0 1
FD (%) 0 0.1 0.2 0 0 0 0 0.9 0.2 0 0.1
Trachea P (%) 0 0 0 0 0 0 9.1 0 0 0 0
MI 0 0 0 0 0 0 3.7 0 0 0 0
MA 0 0 0 0 0 0 0.3 0 0 0 0
NTP 0 0 0 0 0 0 11 0 0 0 0
FD (%) 0 0 0 0 0 0 1.2 0 0 0 0
Gallbladder, hepatic ducts P (%) 0 0 0 0 0 0 0 0 0 12.1 0
MI 0 0 0 0 0 0 0 0 0 3.8 0
MA 0 0 0 0 0 0 0 0 0 0.5 0
NTP 0 0 0 0 0 0 0 0 0 15 0
FD (%) 0 0 0 0 0 0 0 0 0 1.6 0
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P Prevalence, MI Mean intensity, MA Mean abundance, SD Standard deviation, TNP Total number of parasites, FD Frequency of dominance

Table 3.

Dispersion index (ID), statistic-d (d) and discrepancy index (D) for the parasite infracommunities in Cairina moschata domestica from the eastern Amazon (Brazil)

Species of parasites ID d D Type of dispersion
Anisakis sp. 1.52 1.81 0.54 Random
Eucoleus contortus 2.46 4.61 0.47 Aggregated
Capillaria sp. 2.70 5.20 0.62 Aggregated
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No difference (G = 1.25, p = 0.26) in prevalence (P) of endohelminth parasites between females (P = 95.2%, n = 21) and males (P = 83.3%, n = 12) was found, as well as (U = 84.00, p = 0.09) between the mean abundance of parasites (MA) in females (MA = 38.5 ± 74.9) and males (MA = 11.9 ± 14.7). No correlation (rs =—0.270, p = 0.128) of endohelminth abundance with the weight of hosts and with the Brillouin index (rs =−0.234, p = 0.188) was found. No correlation (rs = 0.279, p = 0.124) of endohelminth prevalence with the weight of hosts) was found.

The species mean richness of endohelminths varied from 0 to 6, Brillouin diversity index from 0 to 1.2 and evenness from 0 to 0.5 (Table 4).

Table 4.

Body and diversity parameters for the endohelminth parasite in Cairina moschata domestica from the eastern Amazon (Brazil)

Parameters Mean ± SD Range
Weight (kg) 2.6 ± 0.9 1.2–4.5
Species richness of parasites 1.9 ± 1.3 0–6
Brillouin diversity index (HB) 0.4 ± 0.4 0–1.2
Evenness (E) 0.2 ± 0.2 0–0.5
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Discussion

The fauna of endohelminths in C. moschata domestica was composed of 9 species of Nematoda and two species of Trematoda found in different organs, and was characterized by a predominance of nematode larvae, low diversity, low species richness and low evenness. Mattos-Junior et al. (2008) reported seven species of endohelminths for domestic C. moschata domesticus in Rio Janeiro State (Brazil), five species of Nematoda, one Cestoda and one Trematoda. For free range C. moschata in Tanzania, the endohelminth fauna was constituted by 12 species of Nematoda and two species of Cestoda (Muhairwa et al. 2007) (Table 1). Although these studies did not provide information on the stomach contents of this avian host, they are known to ingest a certain range of prey in their habitats, thus exposing themselves to potential intermediate hosts, which accounts for this distinctly differentiated fauna of parasitic helminths. Thus, in addition to dietary differences being a significant factor in defining the helminth fauna in these host populations, spatial factors may also have played an important role in these hosts.

Among wild avian species, it is suggested that such hosts harbor a richer diversity of helminths (Santoro et al. 2012) than domestic birds, because the fauna and species richness of parasite helminths are influenced by specific factors such as particular habitat, geographic range, a broad host diet and selective feeding by the host on prey that serve as intermediate hosts (Alexander & Mclaughlin 1997; Sanmartín et al. 2004; Junker et al. 2008; Santoro et al. 2012). Therefore, the specimens of C. moschata domestica examined in our study had fed selectively on prey species that are intermediate hosts of endohelminths, because they acquired a richer diversity of nematode larvae species than trematoides.

In avian species, factors governing the dynamics of spatial distribution of endohelminth species are varied and complex. The most dispersion common pattern of parasites is the aggregated distribution (Sanmartín et al. 2004; Junker et al. 2008), which indicates that the parasite species has achieved a certain degree of stability. This pattern of dispersion can be due to the wide dimensions of the hosts’ ecological niches, the genetic heterogeneity and the heterogeneity of exposure and susceptibility of the host population (Dobson 1990; Poulin, 2013). In contrast, the random dispersion pattern is characteristic of parasite populations in the early stages of colonization of a new environment or in decline, which thus show low population densities (Sanmartín et al. 2004). Therefore, an aggregated dispersion pattern depends on factors such as genetic heterogeneity, exposure and susceptibility of the host population, feeding preferences and species-specific host behavior and environmental factors (Sanmartín et al. 2004; Junker et al. 2008). In C. moschata domestica, we found that larvae of Anisakis sp., a moderately abundant endohelminth, had a random dispersion, while E. contortus and larvae of Capillaria sp. had aggregated dispersion. Those parasite species have different niches within the host and are thus not in direct competition. In parasite species that are not in direct competition, aggregated dispersion could allow the coexistence of parasites that would otherwise be excluded; and hence, more parasite species can coexist in a same host population (Salgado-Maldonado et al. 2019). In addition, Lester & McVinish (2016) reported that most parasites that are able to remain at one trophic level are less aggregated than those that pass through the food web.

Infection parameters (sensu Bush et al. 1997) traditionally used to quantify parasite populations or the severity of parasitic infections, are subject to variations (Poulin 2006), because such parameters can vary for a single avian species, influenced by factors such as the host diet and selective feeding on prey that are intermediate hosts in the environment, among other factors (Alexander & Mclaughlin 1997; Sanmartín et al. 2004; Junker et al. 2008; Santoro et al. 2012). Our results for C. moschata domestica indicated low infection levels by nematodes and trematodes, except for E. contortus and Capillaria sp., but no difference was found between males and females, because males and females had a similar diet and lifestyle. In addition, we found a higher overall prevalence of helminths (90.9%) than that reported by Mattos-Junior et al. 2008 for this same duck (56.5%) raised in Rio Janeiro State (Brazil), although these authors found that females presented a higher prevalence of endohelminths than males. We attribute this high prevalence and intensity of E. contortus and Capillaria sp. to the humid environment characteristic of the Amazon. This high prevalence and intensity of nematodes in C. moschata domestica can be related to the interactions of this avian with the soil, which is essential for the maintenance of the life cycle of many parasites such as E. contortus, where this avian ingests the intermediate hosts, possibly earthworms, besides the viable eggs in the environment (Carvalho et al. 2019).

We observe that in 36.3% of C. moschata domestica there was an occurrence of double parasite infection, generally with E. contortus or Capillaria sp., which may lead to body weight loss. This high prevalence of helminths can be a problem for duck raising by affecting their total protein content and, consequently, the full economic benefits of their production (Carvalho et al. 2019). Additionally, we found no correlation between endohelminth abundance and the body weight of C. moschata domestica, indicating that possibly the amount of foods consumed containing infective stages was not a factor responsible for such infection levels.

Free-range and extensively raised ducks are in constant contact with soil and aquatic habitats, which serve as an important reservoir and transmission for larval stages of parasite endohelminths species. Hence, terrestrial and aquatic invertebrates can become vectors for these parasites (Alexander & Mclaughlin 1997; Muhairwa et al. 2007; Junker et al. 2008; Carvalho et al. 2019). Wild fish species are infected by larvae of Anisakis sp., Contracaecum sp., Hysterotylacium sp., Raphidascaris sp., Eustrongylides sp., Capillaria sp. and Ascocotyle sp. because they are secondary intermediate or paratenic hosts for such helminths, while fish-eating avian are definite hosts (Moravec 1998; Barson & Marshall 2004; Knoff et al. 2013; Pinheiro et al. 2019).

Fish-eating birds are abundant in freshwater habitats in the eastern Amazon, as they are in most regions of the Amazon. However, we also found Anisakis sp., Contracaecum sp., Hysterotylacium sp., Raphidascaris sp., Eustrongylides sp., Capillaria sp., E. contortus, Athesmia heterolecithodes (Braun, 1899) Looss, 1899 and Ascocotyle sp. in C. moschata domestica raised in the Brazilian Amazon, where they are dead-end hosts (i.e., accidental hosts) for these endohelminths. Thus, it is possible that this duck also feeds on fish, which are intermediate hosts for these nematode species in the environment. Athesmia heterolecithodes is a ubiquitous, nearly cosmopolitan digenean species with a wide diversity of hosts that includes avian species from the Gruiformes, Charadriiformes, Cuculiformes, Falconiformes, Strigiformes, Ciconiiformes and Passeriformes from the Old World, Nearctic and Neotropical regions, as well as mammal species from the Marsupialia, Chiroptera, Carnivora and Rodentia (Digiani 2000). In general, infrapopulation of nematodes and digeneans in C. moschata domestica had few individuals, suggesting that the same diet variation that produces the low diversity in the endohelminths community limits both the probability and frequency of encounters with parasites at the individual level. Since this host does not specialize on any prey species, this fact further limits exposure to helminth larvae. This is reflected in the generally low prevalence and intensity seen for most helminth species.

In C. rothschildii, P. gularis and T. episcopus of captivity in the city of Belém, State of Pará (Brazil) was reported eggs of nematode Trichostrongyloidea (4.6%), Ascaridoidea (0.6%) and Trichuroidea (0.6%); eggs of cestodes in 2.9% of examined birds and trematode eggs in 2.3% of samples. As species of Anisakis, Contracaecum, Hysterotylacium, Raphidascaris, Eustrongylides and Capillaria are widely distributed in other parts of world (Gower 1939; Alexander & Mclaughlin 1997; Moravec 1998; Barson & Marshall 2004; Sanmartín et al. 2004; Navarro et al. 2005; Muhairwa et al. 2007; Santoro et al. 2012), it is also important to investigate the occurrence of these helminths in the Amazon region. In addition, Anisakis sp., Contracaecum sp., Eustrongylides sp. and Ascocotyle sp. have zoonotic potential for humans (Knoff et al. 2013) due to the risk of contamination by larvae in the food of Amazon populations. This means that studies of infections by such parasites should not be neglected.

Conclusions

This study was characterized by a high richness of nematode species and a small number of digeneans with low abundance, low diversity, and low evenness, with a predominance of E. contortus and Capillaria sp. There was a predominance of single or double parasitic infection, generally with E. contortus and/or Capillaria sp. Our studies of these ducks raised in the Brazilian Amazon region revealed that they are accidental hosts for most of the larvae species, and definitive hosts for few of the species found. Furthermore, results suggest that C. moschata domestica is an omnivorous species that uses several aquatic and terrestrial habitats that contain a rich nematode fauna related to these two habitats, but mainly prefers aquatic habitats where there is greater opportunity for contact and consumption of invertebrates and fish infected with infectious stages of parasites. This was the first report of Contracaecum sp., Hysterotylacium sp., Raphidascaris sp., Eustrongylides sp., Syngamus sp., Ascocotyle sp. and A. heterolecithodes for C. moschata domestica. Because this duck is an important source of food for several human populations in northern Brazil, knowledge regarding contamination by helminths found to have zoonotic potential is particularly important.

Acknowledgements

Marcos Tavares-Dias was supported by a researcher fellowship of the Conselho Nacional de Pesquisa e Desenvolvimento Tecnologico (CNPq, Brazil) (# 303013/2015-0).

Author contributions

All authors have participated in conception and design, or analysis and interpretation of the data; drafting the article or revising it critically for important intellectual content; and approval of the final version.

Declaration

Conflict of interest

Authors declare that there is no conflict of interest regarding the publication of this paper.

Footnotes

Publisher's Note

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Contributor Information

Marcos Tavares-Dias, Email: marcos.tavares@embrapa.br.

Elane Guerreiro Giese, Email: marcos.tavares@embrapa.br.

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