Introduction
Some authors consider birds as the vertebrate group with the highest parasite richness due to their varied diet, high vagility and gastrointestinal tract complexity (Poulin, Reference Poulin1995; Leung & Koprivnikar, Reference Leung and Koprivnikar2016). Moreover, waterfowl host a wide diversity of helminth parasites that may affect their body condition, behaviour, reproduction and survival (Wobeser, Reference Wobeser1997; Souchay et al., Reference Souchay, Gauthier and Pradel2013). Most of the helminths of waterfowl require water bodies to complete their life cycles. Anatids are mainly aquatic feeders and are particularly subject to infection from helminths; in areas where waterfowl congregate during nesting and rearing seasons, the opportunities of infection increase. During the winter, Mexican wetlands receive approximately 84% of the total waterfowl migration from northern areas of North America, particularly anatids (Barragán et al., Reference Barragán, López-López and Babb2002; SEMARNAT, 2009). Migratory birds can spread parasites in warmer climates, like the ones found in their breeding grounds in Mexico. The main factors that influence the large abundance of parasite infection in waterfowl were probably first mentioned by Gower (Reference Gower1939). This author reported 260 species of helminths of waterfowl recorded in the literature, particularly ducks; moreover, he argued that ducks may act as reservoir host and vectors in the spread of some parasites of domestic poultry.
Studies of anatid parasites worldwide are extensive, probably because they are easily available to parasitologists for examination; parasite records include protozoans, helminths and arthropods infecting swans, geese and ducks all over the world (Gower, Reference Gower1939; Lapage, Reference Lapage1961; McDonald, Reference McDonald1969a). Fifty years ago, McDonald (Reference McDonald1969a) published a catalogue of waterfowl helminth parasites (Anatidae), listing 465 helminth species and presenting data on their life cycle, hosts, distribution, habitat and potential importance. Another key publication by the same author reported the world literature on helminths of waterfowl from 1890 to 1969, presenting the number of birds examined, country and described species from each host species (McDonald, Reference McDonald1969b). Similarly, in Africa, Alexander & McLaughlin (Reference Alexander and McLaughlin1997) published a checklist of the helminths of the respiratory and gastrointestinal tract of members of Anatidae. Still, many studies on the helminth parasite fauna of waterfowl are focused on a particular host species or in a small geographical area (e.g. Broderson et al., Reference Broderson, Canaris and Bristol1977; Wilkinson et al., Reference Wilkinson, Canaris and Broderson1977; Shaw & Kocan, Reference Shaw and Kocan1980; Canaris et al., Reference Canaris, Mena and Bristol1981). In Mexico, information on the waterfowl helminth parasites is scattered in the literature, and no attempt has been made until the present study to compile all the data available up to the present time. Helminth parasites of birds have been documented for more than 90 years, and some papers have recently summarized the information, but this is usually reported by parasite group (e.g. Pérez-Ponce de León et al., Reference Pérez-Ponce de León, García-Prieto and Mendoza-Garfias2007; García-Prieto et al., Reference Garcia-Prieto, Garcia-Varela, Mendoza-Garfias and Pérez-Ponce de León2010; García-Prieto et al., Reference García-Prieto, García-Varela and Mendoza-Garfias2014), and no comprehensive checklist of the helminth parasites of birds in Mexico is currently available, not even for commercially important birds such as waterfowl; this is surprising because anatids are an economically important resource, either for hunting activities or for maintaining population in captivity. In either case, they represent a significant income to people managing these resources (SEMARNAT, 2009).
Considering the lack of information about the health status of members of the family Anatidae in Mexico, the aim of this study was, first, to report the helminth fauna composition of anatids occurring in three localities of Mexico, and, second, to generate an updated checklist by gathering the extant published data on the helminth parasites of this important group of birds in Mexico, which holds many sites where large populations of migratory birds arrive every year to their wintering grounds.
Material and methods
Collection of parasites
Parasites were collected from the viscera of birds donated by hunters with legal authorizations, according to hunting federal regulations. New parasite records in this study were obtained from the analysis of the gastrointestinal tract of 59 individuals from nine species – namely, Spatula discors (Linnaeus, 1766), Spatula cyanoptera (Vieillot, 1816), Spatula clypeata (Linnaeus, 1758), Mareca strepera (Linnaeus, 1758), Anas crecca Linnaeus, 1758, Anas acuta Linnaeus, 1758, Anas diazi Ridgway, 1886, Dendrocygna bicolor (Vieillot, 1816) and Aythya collaris (Donovan, 1809). Birds were sampled between November 2017 and February 2018 in three localities of Mexico: ‘La Venta’, Villahermosa, Tabasco (n = 4); UMA Patolajara, Jalisco (n = 23); and Metztitlán lagoon, Barranca de Metztitlán, Hidalgo (n = 32) (table 1). Once obtained, birds were placed in plastic bags and kept under refrigeration until further examination in the Laboratory of Diagnostic Parasitology, Faculty of Veterinary Medicine of the National Autonomous University of Mexico (UNAM).
Table 1. Species of helminths collected from the gastrointestinal tract of nine species of waterfowl (Anatidae) in Mexico.
For the helminth examination, gastrointestinal tracts were placed in Petri dishes containing saline solution (0.85%) and observed under a stereoscope. Collected parasites were processed following helminthological routine techniques (Lamothe, Reference Lamothe1997). Briefly, helminths were observed and measured microscopically and thereafter identified emphasizing characteristic structures to determine the taxonomic classification. Specialized literature and identification keys were consulted (Yamaguti, Reference Yamaguti1940; McDonald, Reference McDonald1981, Reference McDonald1988; Khalil et al., Reference Khalil, Jones and Bray1994; Gibson et al., Reference Gibson, Jones and Bray2002; Anderson et al., Reference Anderson, Chabaud and Willmott2009). Reference material was deposited in the National Helminth Collection (Colección Nacional de Helmintos (CNHE)) at the Biology Institute of UNAM (table 1). Bird names (as well as authority and publication year) follow the Handbook of the Birds of the World and BirdLife International digital checklist of the birds of the world (BirdLife International, 2017).
Dataset construction
The dataset was built with data obtained in published records in specialized literature. The latter was performed after an exhaustive search in the ISI Web of Science®. A search was carried out for each bird species using combinations of terms – for example, ‘parasites’ and Anas crecca. Only the records of helminths were retrieved to be incorporated in the database. We also searched the database of the CNHE – the main depository of specimens and information on helminth parasites in the country. Helminth records reported in unpublished bachelor theses were also included. Each record was checked individually, and we only considered those whose specimens were deposited (and verified) in a scientific collection to standardize the quality of the records. We also acknowledge that taxonomic identification in most of the studies that were searched was accomplished using morphology, and some studies used molecular techniques to achieve or corroborate the identification of acanthocephalans belonging to the family Polymorphidae, and trematodes of the family Strigeidae (e.g. Hernández-Mena, Reference Hernández-Mena2010; García-Varela et al., Reference García-Varela, Pinacho-Pinacho, Uribe and Mendoza-Garfías2013). Records of domestic or caged birds (zoos, experimental, pet) were discarded. We only considered the records related with the helminth parasite diversity of anatids, as avian hosts belonging to other families were not included in this work.
A database was created in Microsoft® Excel® (2016) (https://www.microsoft.com/es-mx/)and the geographic coordinates for each locality were included in the spreadsheet. To check for duplicate records, Microsoft® Access® (2010) (https://www.microsoft.com/es-mx/) was used. For each reference, the following information was included: (1) anatid species; (2) reported helminth taxa; (3) location and state where the parasite was found; (4) publication year of the reference; and (5) number and acronym of the scientific collection in which the helminth was deposited.
Finally, the database was exported to a geographic information system software (ArcGis 10.4.1) (https://www.arcgis.com) to create the maps of the current distribution of helminth parasites of Anatidae in Mexico. The information is presented in two lists: a host–parasite list, in which the information is presented in alphabetical order of the subfamily and tribe of the corresponding anatid (Clements, Reference Clements2007; Berlanga et al., Reference Berlanga, Gómez de Silva, Vargas-Canales, Rodríguez-Contreras, Sánchez-González, Ortega-Álvarez and Calderón-Parra2017); and a parasite–host list, where the information is alphabetically ordered and organized by phyla – Platyhelminthes (trematodes and cestodes), Nematoda and Acanthocephala, presented as supplementary material because of the large number of records.
Results
Helminths of anatids in localities of central and south-eastern Mexico
Of the 59 gastrointestinal tracts examined, 89.6% (52) were positive to the infection by at least one helminth species. One of the species of host, the northern pintail, A. acuta, was free of infection by helminths. After the helminthological examination, 26 taxa were identified: eight trematodes, five cestodes, 12 nematodes and one acanthocephalan (table 1; Supplementary table S1). All helminths conform with the diagnosis of previous taxonomic descriptions or redescriptions of the species we report herein (Caballero & Larios, Reference Caballero and Larios1940; Caballero, Reference Caballero1942; Larios, Reference Larios1944; Bravo & Caballero, Reference Bravo and Caballero1973; Woodyard & Bolen, Reference Woodyard and Bolen1984; Farias & Canaris, Reference Farias and Canaris1986; Canaris & Ching, Reference Canaris and Ching1989; Orozco-Flores, Reference Orozco-Flores2000; Soto-Méndez, Reference Soto-Méndez2006; Pérez-Ponce de León et al., Reference Pérez-Ponce de León, García-Prieto and Mendoza-Garfias2007; Mercado-Reyes et al., Reference Mercado-Reyes, Angulo-Castillo, Clemente-Sánchez, Hernández-Llamas, Gonzáles-Rojas, López-Torres and Tavizón-García2010; García-Varela et al., Reference García-Varela, Henández-Orts and Pinacho-Pinacho2017). The common gadwall, Mareca strepara, was the species of host with the highest helminth species diversity, with 18 of the 25 species of helminths collected in our samples (table 1). Instead, in the ring-necked duck, A. collaris, and in the fulvous whistling duck, D. bicolor, only one and three species of helminth were found, respectively. Two species of nematodes, Epomidiostomum uncinatum and Tetrameres sp., were found in six of the nine species of analysed waterfowl in the three localities. In this study, 30 new host, and 62 new locality records are reported. The trematodes Zygocotyle lunata in A. collaris and Echinoparyphium sp. in D. bicolor, as well as the nematodes Amidistomum sp. and Tetrameres sp. in D. bicolor, are reported in Mexico for the first time.
Database built from literature search
Records from the first published finding in Mexico from 1943 to 2019 were used to build the database. The number of studies has intensified in the last two decades; 76% of the total records were published between 2003 and 2019 (fig. 1). In total, 563 records of helminth parasites of Anatidae in Mexico were retrieved from the literature, including those obtained in the present study. Moreover, 651 specimens from different wetlands have been examined, with A. diazi and S. discors as the species more intensively studied, with 170 and 105 specimens, respectively (table 2). Ninety-five parasite taxa have been reported, including 38 trematodes (one identified to family rank, three to genus and 34 to species level), 24 cestodes (six identified to genus, 18 to species level), 23 nematodes (ten identified to genus, 13 to species level) and ten acanthocephalans (three identified to genus and seven to species level) (Supplementary table S1). Helminths were collected from 17 species of anatids (A. crecca, Anas platyrhynchos Linnaeus, 1758, A. diazi, A. acuta, Mareca americana (Gmelin, 1789), M. strepera, Oxyura jamaicensis (Gmelin, 1789), S. cyanoptera, S. discors, S. clypeata, Bucephala albeola (Linnaeus, 1758), Cairina moschata (Linnaeus, 1758), D. bicolor, Aythya affinis (Eyton, 1838), Aythya americana (Eyton, 1838), Aythya valisineria (Wilson, 1814) and A. collaris). The georeferenced records were reported in 55 localities corresponding to 20 states of Mexico. Trematodes were the helminths that accounted for the highest number of records as well as the highest number of reported taxa (table 2).
Fig. 1. Number of records of helminth parasites of waterfowl (Anatidae) in Mexico from 1943 (first record) to 2019. Data presented as five-year intervals.
Table 2. Number of taxa per helminth group according to data gathered from the bibliographical search for each species of anatid studied in Mexican wetlands.
*Number of taxa/identified species up to species level. T, trematodes; C, cestodes; N, nematodes; A, acanthocephalans.
Host species with the highest number of records were as follows: A. diazi (183), followed by S. clypeata (54), S. discors (52) and A. crecca (50) (table 3). The remaining hosts accounted for less than 50 records each. The anatid that hosted the highest helminth species richness is the Mexican duck, A. diazi, with 52 species reported along its distribution range in Mexico, including 16 trematode species, 15 cestodes, 17 nematodes and four acanthocephalans (table 3); the blue-winged teal, S. discors, harbours 37 helminth species (20 trematodes, four cestodes, nine nematodes and four acanthocephalans) (table 3). This is related to the fact that the largest number of reports have been published for these two species, where at least 170 individuals of the Mexican duck, and 105 of the blue-winged teal have been studied for helminths. Regarding geographical distribution, the states with the highest number of records are located in central and northern Mexico, particularly in wetlands of the Estado de México (312 records), Chihuahua (75), Tlaxcala (68) and Durango (48) (fig. 2); these records accounted for 89% of all records of helminths in waterfowl, although this result might be biased because in these states some wetlands are established as registered waterfowl hunting areas, and, concomitantly, hosts are available for parasitological examination. The locality where more species of anatids have been sampled, and where more helminth species have been reported thus far is the Lerma Swamp (Ciénega de Lerma) in Estado de México. In this locality, eight species of anatids have been studied, and, from them, 15 species of helminths were reported.
Fig. 2. Distribution of records of helminths infecting waterfowl (Anatidae) in Mexico by parasite group.
Table 3. Host-parasite checklist of the helminth parasites of waterfowl (Anatidae) in Mexico
Discussion
About 150 waterfowl species of the family Anatidae have been described in the world. Thirty-three species (23%) have been reported in Mexico; most of the species migrate from their nesting sites in northern regions of North America and occupy wintering grounds in wetlands in Mexico; five species are permanent residents (Howell & Webb, Reference Howell and Webb1995; Edwards & Butler, Reference Edwards and Butler1998). One of them, the Mexican duck, A. diazi (considered in the past as a subspecies of the mallard, A. platyrhynchos), is a dabbling duck which breeds in Mexico and the southern USA, and is the only duck distributed throughout the year in the internal wetlands of Mexican Highlands (Colón-Quezada, Reference Colón-Quezada2009; SEMARNAT, 2009). This species is classified as threatened under official regulations (SEMARNAT, 2010). By far, A. diazi is the most studied anatid in Mexico, and, hence, shows the highest number of parasite records and the highest helminth species richness (Supplementary table S1). Another resident species, the Royal duck (C. moschata), is only distributed in the coastal wetlands of the Mexican Pacific and Gulf of Mexico (SEMARNAT, 2009); this species is also classified as an endangered species, and can only be sampled for conservation and research studies. This explains why only one study dating from 1984 was found during the literature search, in which 22 individuals were examined, reporting 14 helminth species (Woodyard & Bolen, Reference Woodyard and Bolen1984).
Overall, 17 of the 33 species of anatids occurring in Mexico (52%) have been studied for helminths. The helminth parasites reported in these 17 species of anatids are common parasites of waterfowl in North America as a result of their migrating patterns during the winter season (McDonald, Reference McDonald1969a; Broderson et al., Reference Broderson, Canaris and Bristol1977; Wilkinson et al., Reference Wilkinson, Canaris and Broderson1977; Shaw & Kocan, Reference Shaw and Kocan1980; Canaris et al., Reference Canaris, Mena and Bristol1981; Farias & Canaris, Reference Farias and Canaris1986; Gladden & Canaris, Reference Gladden and Canaris2009). It is well known that migratory birds may disperse parasites across broad geographic areas depending on suitable environmental conditions and the presence of intermediate hosts (Hoberg et al., Reference Hoberg, Polley, Jenkins, Kutz, Veitch and Elkin2008; Koprivnikar & Leung, Reference Koprivnikar and Leung2015). The data gathered from the literature search corroborated the decrease of the helminth parasite abundance and the loss of species as they migrate from their nesting sites during the winter; this pattern was previously described by Wallace & Pence (Reference Wallace and Pence1986) when these authors compared the helminth species of the blue-winged teal, S. discors, between breeding and wintering grounds. However, in studies with particular waterfowl species, such a decrease is not evident. For instance, Gladden & Canaris (Reference Gladden and Canaris2009) studied the helminth communities of the bufflehead duck, B. albeola, in their nesting and breeding sites in Canada, USA and northern Mexico to test the hypothesis that the change in food was the cause of the parasite loss during migration. Their results showed low similarity values of the helminth communities of B. albeola between Manitoba, Canada and the Chihuahua Desert in Mexico, which may reflect the loss of parasites during migration, although these authors detected recruitment of parasites by their feeding habits, making the loss difficult to detect. In another study, Garvon et al. (Reference Garvon, Fedynich, Peterson and Pence2011) also studied the helminth communities of the blue-winged teal, S. discors, from two migratory corridors to evaluate the degree of similarity in helminth community structure in terms of species richness, prevalence and abundance of infections. One of the main findings of that study was the similarity in species composition and less similarity when the abundance of these species was incorporated in the analysis (not included by Wallace & Pence, Reference Wallace and Pence1986). Garvon et al. (Reference Garvon, Fedynich, Peterson and Pence2011) reported 40 species of helminths (20 trematodes, nine cestodes, one acanthocephalan and ten nematodes). In our study, a very similar species composition was found in populations of S. discors in their breeding sites in Mexico; 36 helminth species have been reported, with trematodes accounting for 56% of the parasite community (table 3; Supplementary table S1). Unfortunately, no data are available to incorporate prevalence and abundance of infection as few studies on helminth parasites of waterfowl in Mexico report these data.
The waterfowl species more intensively studied, and those displaying the highest number of records and helminth species richness, were the ones belonging to the tribe Anatini. This is correlated with the abundance of these ducks, as they are very common in the wetlands of Mexico during the breeding season. The feeding behaviour of these waterfowl explains their high helminth species richness. These species are considered dabbling ducks – that is, shallow-water ducks that feed primarily along the surface of the water by tipping headfirst into the water, and grazing on the surface of the waterbody (Baldassarre & Bolen, Reference Baldassarre and Bolen1994; Johnsgard, Reference Johnsgard2010). Their diet includes a wide variety of seeds, roots and tubers, and some invertebrates like annelids, crustaceans (copepods, water fleas and ostracods), snails and insects (beetles, flies, butterflies and dragonflies), and even small frogs (Swanson et al., Reference Swanson, Meyer and Adomaitis1985; Combs & Fredrickson, Reference Combs and Fredrickson1996; Johnsgard, Reference Johnsgard2010). The invertebrates may act as intermediate hosts to most of their helminths (Wobeser, Reference Wobeser1997; Cordero del Campillo, Reference Cordero del Campillo1999; Atkinson et al., Reference Atkinson, Thomas and Bruce2008; Saijuntha et al., Reference Saijuntha, Duenngai and Tantrawatpan2013). Instead, species of waterfowl in the tribes Mergini and Oxyurini, which are known as ‘diving’ ducks, have been scarcely studied for helminths in Mexico. Interestingly, species such as the bufflehead duck, B. albeola, and the ruddy duck, O. jamaicensis, harbour 18 and 23 species of helminths, respectively (table 3; Supplementary table S1), which is a comparatively high species richness. The main food items of these two species of diving ducks are molluscs, amphipods and ostracods, which are also intermediate hosts to several helminth species (Wobeser, Reference Wobeser1997; Cordero del Campillo, Reference Cordero del Campillo1999). Their distributional range in Mexico is more restricted since it is limited to wetlands of the northern and central highlands of Mexico (SEMARNAT, 2009). In contrast, anatids belonging to the tribe Aythyini showed very few helminth records, with only one to five species per duck (table 3; Supplementary table S1). The four species of Aythya studied thus far are also diving ducks, and their food items include the same invertebrates acting as intermediate hosts (Baldassarre & Bolen, Reference Baldassarre and Bolen1994; Johnsgard, Reference Johnsgard2010). In a previous study, Noseworthy & Threlfall (Reference Noseworthy and Threlfall1978) reported 17 species of helminths in the ring-necked duck, A. collaris, in their nesting sites in Canada, with trematodes accounting for 47% of the species. However, that species of diving duck has not been studied for helminths in Mexico. In this study, we only present the record of the trematode Z. lunata as a parasite of the same host species from a hunting area in Jalisco, western Mexico. Likewise, 14 of the 17 species of helminths reported by Noseworthy & Threlfall (Reference Noseworthy and Threlfall1978) in A. collaris are found in other species of anatids in Mexico. Most of the helminths of these migratory birds find the necessary conditions and intermediate hosts available to complete their life cycles – either molluscs for trematodes (Cordero del Campillo, Reference Cordero del Campillo1999; Fried et al., Reference Fried, Huffman, Keeler and Peoples2009; Ostrowski et al., Reference Ostrowski de Núñez, Davies and Spatz2011), copepods, water fleas and ostracods for cestodes (Haukos & Neaville, Reference Haukos and Neaville2003; Green et al., Reference Green, Georgiev, Brochet, Gauthier-Clerc, Fritz and Guillemain2011; Saijuntha et al., Reference Saijuntha, Duenngai and Tantrawatpan2013) or amphipods for acanthocephalans (Keithly, Reference Keithly1968; Podesta & Holmes, Reference Podesta and Holmes1970; Aznar et al., Reference Aznar, Pérez-Ponce de León and Raga2006; Atkinson et al., Reference Atkinson, Thomas and Bruce2008). All these invertebrates act as intermediate hosts, are common in wetlands and are part of the diet of dabbling and diving ducks (Atkinson et al., Reference Atkinson, Thomas and Bruce2008). Most of the nematodes in waterfowl have direct cycles (Leiby & Olsen, Reference Leiby and Olsen1965; Atkinson et al., Reference Atkinson, Thomas and Bruce2008; Saijuntha et al., Reference Saijuntha, Duenngai and Tantrawatpan2013), except for Tetrameres, which also infect crustaceans (Atkinson et al., Reference Atkinson, Thomas and Bruce2008).
In the present study, only one potentially zoonotic parasite was identified – Echinostoma revolutum – with 23 records in seven anatid species; this trematode is broadly distributed in localities of eight states of Mexico, exhibiting different types of climate spanning from very dry to warm sub-humid. Anatids are the definitive hosts of E. revolutum, whereas snails, mainly Lymnaea spp., are the intermediate hosts. Humans might become infected by ingesting the intermediate host, as it has been previously reported (Yousuf et al., Reference Yousuf, Das, Anisuzzaman and Banowary2009; Chai et al., Reference Chai, Sohn, Na and Nguyen2011; Sohn et al., Reference Sohn, Chai, Yong, Eom, Yoon, Sinuon, Socheat and Lee2011; Saijuntha et al., Reference Saijuntha, Duenngai and Tantrawatpan2013). Nonetheless, at the present time, there are no reports of naturally acquired infections in Mexico. The only report of a human case in Mexico was through a volunteer experimental infection (Larios, Reference Larios1940).
In conclusion, waterfowl represent a group of birds with economic importance because they are used for legal hunting activities either for recreation or for food, representing a significant income to people managing these resources. On the one hand, migratory waterfowl spend some of their lives in wintering grounds in Mexican wetlands. It is important to have a comprehensive list of the parasites that may affect these hosts and understand the dynamic of the parasite communities during migration. This information will be useful for conservation planning of these species and the habitats where they occur; in Mexico, problems associated with pollution and habitat loss of wetlands where migratory birds spend the breeding season can be monitored through the study of their parasites, since they are good indicators of environmental health (Pérez-Ponce de León, Reference Pérez-Ponce de León, González Zuarth, Vallarino, Pérez Jiménez and Low Pfeng2014). On the other hand, since birds transport their parasites during migration, a comprehensive list of their parasites is important because even though implications for the hosts are usually unknown, several species have been associated with morbidity and mortality in captive and wild waterfowl (Ballweber, Reference Ballweber2004). Still, not all the species of waterfowl have been studied for helminths; only 17 of the 33 species have been analysed. Almost 50% of the species that annually migrate to Mexican wetlands have not been studied for parasites, although the conservation status and current laws restrict sampling specimens for any parasitological study that would require killing individuals. Still, the checklist we present in this paper is useful because all the scattered information is concentrated in one source that can be easily accessed by veterinarians interested in describing the epidemiological aspects of wildlife bird parasites, and by conservation biologists interested in ecological programs aiming to guarantee the health and conservation of migratory birds from North America. Parasite ecologists would be also interested in the data for studies aimed at understanding the effect of bird migration in the composition of the helminth parasite communities, as well as freshwater biologists interested in the understanding of freshwater ecosystem health, because the lack of parasites of waterfowl in wetlands might be a direct indicator of the effect of pollution on the invertebrates that act as intermediate hosts in the life cycles of the helminths in waterfowl.
Supplementary material
To view supplementary material for this article, please visit https://doi.org/10.1017/S0022149X20000577
Acknowledgements
Special thanks to Jorge Alfonso Toledo and Ana Belem Isaak Delgado for all their support during collecting and processing at the Laboratory of Parasitic Diagnosis in the Faculty of Veterinary Medicine, UNAM, and special thanks to the hunters who donated the ducks to obtain the samples – without their help, this study would not have been possible. We thank Luis García for access to the records of the database of the CNHE. We sincerely thank two anonymous reviewers whose comments were very important in improving the quality of the manuscript.
Financial support
This work was supported by the Dirección General de Asuntos del Personal Académico of Universidad Nacional Autónoma de México (grant number PAPIIT IN218720).
Conflicts of interest
None.
Ethical standards
The study complied with federal regulations and permissions regarding the cynegetic activities of the hunters who donated animal organs. Collection of organs was approved by the Institutional Animal Care and Use Subcommittee of the Graduate Program of Veterinary Medicine of UNAM (Subcomité Institucional para el Cuidado y Uso de Animales Experimentales-Pogrado CPSA UNAM).
