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ISSN 1519-6984 (Print)

ISSN 1678-4375 (Online)

THE INTERNATIONAL JOURNAL ON NEOTROPICAL BIOLOGY


THE INTERNATIONAL JOURNAL ON GLOBAL BIODIVERSITY AND ENVIRONMENT

Original Article

Gastrointestinal parasites in captive and free-living wild birds


in Goiania Zoo
Parasitas gastrointestinais em aves silvestres em cativeiro e de vida livre no Zoológico
de Goiânia

Y. J. O. Meloa , H. T. Ferrazb , K. C. Saturninoc , T. D. P. Silvad , I. A. Bragac,e , A. V. C. Amaralc ,


R. B. Meirelles-Bartolic  and D. G. S. Ramosc* 
a
Universidade Federal de Goiás, Regional Jataí – UFG, Jataí, GO, Brasil
b
Universidade Federal de Jataí – UFJ, Laboratório de Anatomia Veterinária, Unidade Acadêmica de Ciências Agrárias, Jataí, GO, Brasil
c
Universidade Federal de Jataí – UFJ, Programa de Pós-graduação em Biociência Animal, Unidade Acadêmica Especial de Ciências Agrárias, GO, Brasil
d
Parque Zoológico de Goiânia, Goiânia, GO, Brasil
e
Centro Universitário de Mineiros, Unidade Básica de Biociências, Mineiros, GO, Brasil

Abstract
Helminths are endoparasites that infect a variety of bird species. Endoparasite infections can cause severe diseases,
including kill captive avian hosts and represents a problem to maintenance and conservation. The eggs and larval
forms of these parasites are usually eliminated in the host feces. The main interest of this study is to report
the occurrence of eggs and oocysts in feces from captive wild birds in Goiânia Zoo and free-living birds in its
surroundings. The fecal samples were subjected to parasitological examination to identify the presence of helminths
and to classify their eggs based on morphological characteristics. Eggs of nematode parasites (Positive/N) were
identified as Ascaridia spp. in Brotogeris chiriri (2/2), Dromaius novaehollandiae (1/1) and Rhea americana (2/2);
Ascarididae in Pavo cristatus nigripensis (1/1); Capillaria spp. in Ara chloropterus (1/1) and Penelope jacucaca (1/1);
Capillaria plagiaticia in Anodorhynchus hyacinthinus (1/2) and Ara spp. (2/2); Capillaria venusta in Rhamphastus
tucanus (1/2); and unidentified nematode eggs from Amazona amazonica (2/2). Eimeria spp. oocyst was founded in
feces from A. hyacinthinus (1/2). Considering free-living birds, Diphyllobothrium spp. eggs were founded in Ardea alba
(2/2) and Nycticorax nycticorax (2/3). Co-infection of Eustrongylides spp. was founded in A. alba (1/2). This is the
first occurrence of: Ascaridia spp. parasitizing B. chiriri; and C. venusta parasitizing R. tucanus. In conclusion, the
helminth eggs found in the abovementioned host bird species are consistent with those reported in the literature,
and treatment and control protocols were based on their identification.
Keywords: coprology, infection, parasitology, preservation.

Resumo
Helmintos são endoparasitas que infectam uma variedade de espécies de aves. As infecções por endoparasitas
podem causar doenças graves, podendo matar aves em cativeiro e representam um problema de manutenção e
conservação. Os ovos e as formas larvais desses parasitas são geralmente eliminados nas fezes do hospedeiro.
O principal objetivo deste estudo é relatar a ocorrência de ovos e oocistos em fezes de aves silvestres em cativeiro
no Zoológico de Goiânia e em aves de vida livre em seu entorno. As amostras fecais foram submetidas a exame
parasitológico para identificação da presença de helmintos e classificação dos ovos com base nas características
morfológicas. Ovos de nematóides (Positivo/N) foram identificados como Ascaridia spp. em Brotogeris chiriri
(2/2), Dromaius novaehollandiae (1/1) e Rhea americana (2/2); Ascarididae em Pavo cristatus nigripensis (1/1);
Capillaria spp. em Ara chloropterus (1/1) e Penelope jacucaca (1/1); Capillaria plagiaticia em Anodorhynchus
hyacinthinus (1/2) e Ara spp. (2/2); Capillaria venusta em Rhamphastus tucanus (1/2); e ovos de nematóide não
identificado de Amazona amazonica (2/2). Oocistos de Eimeria spp. foram encontrados nas fezes de A. hyacinthinus
(1/2). Considerando pássaros de vida livre, ovos de Diphyllobothrium spp. foram encontrados em Ardea alba
(2/2) e Nycticorax nycticorax (2/3). Coinfecção de Eustrongylides spp. foi encontradada em A. alba (1/2). Esta é a
primeira ocorrência de: Ascaridia spp. parasitando B. chiriri; e C. venusta parasitando R. tucanus. Em conclusão,
os ovos de helmintos encontrados nas espécies de aves hospedeiras acima mencionadas são consistentes com
os relatados na literatura, e os protocolos de tratamento e controle foram baseados em sua identificação.
Palavras-chave: coprologia, infecção, parasitologia, preservação.

*e-mail: [email protected]
Received: July 1, 2020 – Accepted: October 28, 2020

This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use,
distribution, and reproduction in any medium, provided the original work is properly cited.

Brazilian Journal of Biology, 2022, vol. 82, e240386 | https://doi.org/10.1590/1519-6984.240386 1/8


Melo, Y.J.O. et al.

1. Introduction The infected birds (captive or free-living) were treated


orally with a combination of fenbendazole, pyrantel
Parasitic diseases are one of the most frequent
pamoate and praziquantel (Cubas et al., 2014), which was
and important health problems that affect wild birds
repeated after 14 days (Atkinson et al. 2008), except the
(Freitas et al., 2002). According Borgsteede (1996), parasites
white-throated toucan (Ramphastos tucanus, Linnaeus
affects wild animals in feeding, reproduction or killing
1758), which was treated subcutaneously with the dosage
also. In this sense, free-living and captive wild birds can
recommended by Carpenter (2010), and the hyacinth
be parasitized by many helminth species, whose effects
macaw (Anodorhynchus hyacinthinus, Latham 1790),
range from asymptomatic infections up to the host’s death
which was treated with a combination of sulfadiazine and
(Carneiro et al., 2011).
trimethoprim (Carpenter, 2010; Tully et al., 2010). Fire was
The detection and identification of helminths is based on
used as a control and prevention measure to disinfect the
the parasitological examination of feces, which consists in
enclosures (Cubas et al., 2014).
identifying eggs and other parasitic forms eliminated in the
feces of host birds (Snak et al., 2014). Diagnostic procedures
involve direct microscopic examination of fecal samples and
3. Results
flotation and sedimentation methods (Snak et al., 2014).
Parasites eggs differ in terms of size, eggshell thickness, Of the 31 fecal samples from captive birds, 12 (38.71%)
shape and other morphological characteristics that were positive for helminth eggs, while six (54.54%) of the
serve to identify them as well as the host bird species 11 fecal samples from free-living birds contained eggs of
(Carneiro et al, 2011; Cubas et al., 2014). Thus, their these parasites. Eggs of nematode parasites recovered from
identification serves to guide treatment and control captive birds were identified (Positive/N - %) as Ascaridia
strategies against parasitic infections (Cubas et al., 2014). spp. Dujardin, 1845 in Brotogeris chiriri Vieillot, 1818 (2/2),
The impact of helminth infections on the maintenance Dromaius novaehollandiae Latham, 1790 (1/1) and Rhea
and conservation of captive birds, as well as on the americana Linnaeus, 1758 (2/2); Ascarididae Baird, 1853
survival of wildlife populations and their ecosystems, in Pavo cristatus nigripensis Linnaeus, 1758 (1/1); Capillaria
underscore the importance of knowledge about the parasitic spp. Zeder, 1800 in Ara chloropterus Gray, 1859 (1/1) and
diseases of wild birds (Cubas et al., 2014), and the scarce Penelope jacucaca Spix, 1825 (1/1); Capillaria plagiaticia
knowledge about the parasitic diseases of wild birds Freitas & Mendonça, 1959 in Anodorhynchus hyacinthinus
(Carneiro et al., 2011), explains the reason for this study. (1/2) and Ara spp. Lacepede, 1799 (2/2); Capillaria venusta
This study aims to identify helminth eggs in fecal Freitas & Mendonça, 1958 in Rhamphastus tucanus (1/2);
samples from captive and free-living wild birds belonged and unidentified nematode eggs from Amazona amazonica
to Goiânia Zoo reporting its occurrence and importance Linnaeus, 1766 (2/2). Eimeria spp. Schneider, 1875 oocyst
for conservation of these species. was founded in feces from A. hyacinthinus (1/2). This is
the first occurrence of: Ascaridia spp. parasitizing B. chiriri;
and C. venusta parasitizing R. tucanus. A. chloropterus and
2. Material and Methods R. tucanus with capillariasis presented clinical signs of
prostration, finicky appetite, weight loss and dehydration.
Fresh fecal samples (n=42) were collected between
Considering free-living birds, Diphyllobothrium spp.
August 20, 2018 and January 26, 2019. The fecal samples
Cobbold, 1858 eggs were founded in Ardea alba Linnaeus,
were collected from the floor of aviaries of captive wild
1758 (2/2 – 100%) and Nycticorax nycticorax Linnaeus,
birds (n=31) in Goiânia Zoo, and from free-living wild birds
1758 (2/3 – 33,33%). Co-infection of Eustrongylides spp.
(n=11) in the surrounding area of the zoo. The samples of
Jägerskiöld, 1909 was founded in A. alba (1/2 – 50%)
captive birds were from birds in isolation (one bird per All results are shown in Tables 1 and 2. Table 1 lists
cage) or in enclosures with birds of the same species. the free-living (FL) and captive © bird species from which
Some enclosures at the zoo are not fully enclosed or fecal samples were collected. Table 2 describes positive
covered, where free-living birds come to feed. Samples of birds and the helminth eggs identified in the feces. Some
these free-living birds were collected when they were helminth eggs found in this study are shown in Figure 1.
injured for some reason and taken to the zoo’s veterinary
care. After, were stored in 40 mL flasks and subjected to
flotation testing in sucrose solution (Sheather, 1923) and
4. Discussion
spontaneous sedimentation (Lutz, 1919). In addition, on
the day they were collected, fresh samples were subjected According to Cubas et al. (2014), the genus Ascaridia
to direct microscopic examination. All the samples were is among the two most common ascarids that infect
examined under 10x and 40x objective lenses as described Psittaciformes birds. Kajerova et al. (2004) stated that
by Zajac and Conboy (2012), and Taylor et al. (2016). seven species of this parasite genus have already been
The identification of eggs was based on morphological identified in Psittaciformes birds, and the two most
analysis compared with descriptions in studies and specific common species are Ascaridia hermaphrodita Froelich,
descriptions (Vicente et al., 1995; Freitas et al., 2002; 1789 and Ascaridia platyceri Hartwich & Tscherner, 1979.
Kajerova et al., 2004; Cunha, 2007; Cubas et al., 2014; Atkinson et al. (2008) stated that the genus Ascaridia
Atkinson et al., 2008; Hofstatter and Guaraldo, 2015; is widely distributed around the world, and reported
Santos et al., 2015). the occurrence of Ascaridia sergiomeirai Pereira, 1933

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Gastrointestinal parasites in wild birds from Goiania Zoo

Table 1. List of free-living (FL) and captive © wild birds in Goiânia Zoo subjected to parasitology fecal tests between 20 August 2018
and 26 January 2019.

Birds species First Description Common name Condition N° of Birds

Alopochen aegyptiaca Linnaeus, 1766 Egyptian goose FL 1

Amazona aestiva Linnaeus, 1758 Turquoise-fronted amazon C 2

Amazona amazonica Linnaeus, 1766 Orange-winged amazon C 2

Amazona farinosa Boddaert, 1783 Southern mealy amazon C 1

Amazona ochrocephala Gmelin, 1788 Yellow-crowned amazon C 1

Anodorhynchus hyacinthinus Latham, 1790 Hyacinth macaw C 2

Ara ararauna Linnaeus, 1758 Blue-and-yellow macaw C 2

Ara ararauna Linnaeus, 1758 Blue-and-yellow macaw FL 1

Ara chloropterus Gray, 1859 Red-and-green macaw C 1

Ara macao Linnaeus, 1758 Scarlet macaw C 1

Ara spp. Lacépede, 1799 Hybrid macaw C 2

Aratinga jandaya Gmelin, 1788 Jandaya parakeet C 2

Ardea alba Linnaeus, 1758 Great egret FL 2

Brotogeris chiriri Vieillot, 1818 Yellow-chevroned parakeet C 1

Brotogeris chiriri Vieillot, 1818 Yellow-chevroned parakeet FL 2

Deroptyus accipitrinus Linnaeus, 1758 Red-fan parrot C 1

Dromaius novaehollandiae Latham, 1790 Emu C 1

Gnorimopsar chopi Vieillot, 1819 Chopi blackbird FL 1

Guaruba guarouba Gmelin, 1758 Golden parakeet C 2

Nycticorax nycticorax Linnaeus,1758 Black-crowned night heron FL 3

Orthopsittaca manilata Boddaert, 1783 Red-bellied macaw C 1

Pavo cristatus nigripennis Linnaeus, 1758 Black-shouldered peafowl C 1

Penelope jacucaca Spix, 1825 White-browed guan C 1

Pionus menstruus Linnaeus, 1766 Blue-headed parrot C 2

Pitangus sulphuratus Linnaeus, 1758 Great kiskadee FL 1

Pyrrhura melanura Spix, 1824 Maroon-tailed parakeet C 1

Ramphastos tucanus Linnaeus, 1758 White-throated toucan C 2

Rhea americana Linnaeus, 1758 Greater rhea C 2

in golden-winged parakeet (Brotogeris chrysoptera infection in ratites, although the genus Baylisascaris
Linnaeus, 1766) from Brazil, a bird of the same genus Sprent, 1968 has been reported with greater relevance
as the yellow-chevroned parakeet (B. chiriri) of this in this group of hosts.
report, wich is the first occurrence of Ascaridia spp. Parasites of genus Ascaridia are monoxenic
parasitizing B. chiriri. (Taylor et al., 2016). Monoxenic parasites easily infect wild
Rosa (2003) stated that eggs from parasites of the birds and mammals, with direct cycle and environmental
superfamily Ascaridoidea Baird, 1853 are among the resistance (Santos et al., 2015). According to Ritchie et al.
ones most frequently found by the flotation method (1994) ascariasis was an occurrent gastrointestinal parasitic
in ratite birds. The author reported the occurrence of infections in Psittaciformes, causing weight loss, anorexia,
Ascaridia spp. in emus (D. novaehollandiae) in Rio de and death. The most common injury in these parasitic
Janeiro. In a study by Mattos et al. (2011), Ascaridia spp. infections was associated to intestinal obstruction (González-
eggs presented the second highest prevalence in ostrich Acuña et al., 2007; Hodová et al., 2008; Melo et al., 2013).
fecal samples analyzed in Rio Grande do Sul. Vicente et al. Considering the monoxenic cycle, in addition to the
(1995) reported the presence of Ascaridia orthocerca treatment of parasitized birds, sanitary measures and
Tossich, 1902 in greater rhea (R. americana) in Brazil. cleaning of the environment must be adopted, and control
Gallo et al. (2020) reported the importance of ascarid of the population density of birds (Taylor et al., 2016).

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Melo, Y.J.O. et al.

Table 2. Helminth eggs and protozoan oocyst identified in fecal samples from captive © and free-living (FL) birds in Goiania Zoo collected
between 20 Aug 2018 and 26 Jan 2019.

Host Specie Condition N1 Positive Parasite Specie Life Cycle Type First Description

Amazona amazonica C 2 2 Unidentified nematode - -

Anodorhynchus Capillaria plagiaticia Monoxenic Freitas & Mendonça, 1959


C 2 1
hyacinthinus Eimeria spp. Monoxecic Schneider, 1875

Ara chloropterus C 1 1 Capillaria spp. * Zeder, 1800

Ara spp. C 2 2 Capillaria plagiaticia Monoxenic Freitas & Mendonça, 1959

2 2 Diphyllobothrium spp. Heteroxenic Cobbold, 1858


Ardea alba2 FL
1 Eustrongylides spp. Heteroxenic Jägerskiöld, 1909

Brotogeris chiriri FL 2 2 Ascaridia spp. Monoxenic Dujardin, 1845

Dromaius
C 1 1 Ascaridia spp. Monoxenic Dujardin, 1845
novaehollandiae

Nycticorax
FL 3 2 Diphyllobothrium spp. Heteroxenic Cobbold, 1858
nycticorax

Pavo cristatus
C 1 1 Ascarididae * Baird, 1853
nigripennis

Penelope jacucaca C 1 1 Capillaria spp. * Zeder, 1800

Ramphastos tucanus C 2 1 Capillaria venusta Monoxenic Freitas & Mendonça, 1958

Rhea americana C 2 2 Ascaridia spp. Monoxenic Dujardin, 1845


1
N is the number of individuals per species present in the zoo. All individuals of each species were analyzed. Co-infection was observed. *The
2

type of biological cycle can be different at the species level.

The egg identified in P. cristatus nigripennis (black- (Cubas et al., 2014). Santos et al. (2015) identified Capillaria
shouldered peacock) belongs to the Ascarididae family. spp. in 44.2% of fecal samples from Psittaciformes birds from
Within this family, the parasites most commonly the Wild Animal Screening Center of Pernambuco, including
found in Galliformes Temminck, 1820 birds belong two specimens of A. chloropterus (Red-and-green macaw).
to the genera Ascaridia and Heterakis Schrank, 1790 Hofstatter and Guaraldo (2015) identified Capillaria spp.
(Atkinson et al., 2008; Taylor et al., 2016). In line with in A. chloropterus specimens from Itatiba Zoo, and also
this, Cubas et al. (2014) stated that parasites from these confirmed the presence of this genus in all the zoos of
genera are common in Galliformes birds, particularly their study. This nematode was also identified in birds of
those kept in captivity. The nematodes Ascaridia galli the genus Penelope Merrem, 1786 at Dois Irmãos zoo in
Schrank, 1788, Ascaridia columbae Gmelin, 1790 and Recife (Cunha, 2007). The occurrence of Capillaria spp. in
Ascaridia perspicillum Rudolphi, 1803 have already A. chloropterus and P. jacucaca is a common problem in
been identified in P. cristatus (Atkinson et al., 2008). zoo and captive animals and can become a bigger problem
Titilincu et al. (2009) reported that eggs of Ascaridia spp. if the population density of birds is not regulated (Godoy,
and Heterakis spp. parasites were present in 59.9% of the 2007). Godoy (2007) reports that despite some species
P. cristatus samples they analyzed. Costa et al. (2018) of Capillaria spp. present annelids as intermediate hosts,
reported the presence of H. gallinarum Schrank, 1788 in most have a monoxenic cycle with high distribution and
the cecal lumen of necropsied P. cristatus on a farm in occurrence in environments with inadequate hygiene
the state of Rio Grande do Sul, Brazil. The birds presented conditions, which is an important aspect in the control
clinical signs suggestive of Histomonas meleagridis Smith, of parasitosis.
1895 infection, which is a parasitic protozoan that uses Prathipa et al. (2013) also reported that C. plagiaticia
H. gallinarum nematodes as intermediate hosts. specifically infects Psittaciformes. In a study by Snak et al.
Most ascaridids have a monoxenic cycle (Taylor et al., 2016), (2014), 43.3% of the fecal samples testing positive for
however Sprent (1954) described that certain species of the parasites in birds at Danilo Galafassi Municipal Zoo in
group utilize intermediate or paratenic hosts in life cycle. Cascavel, state of Paraná, were mixed infections, that
Thus, discussing control strategies becomes a difficult included six samples from Ara ararauna Linnaeus, 1758,
process without more specific identification. The treatment of and contained oocysts of Eimeria spp. Schneider, 1875.
parasitized birds is recommended, as infections by ascaridids The occurrence of C. plagiaticia has been previously
can lead peacocks to death (Ramos et al., 2018). reported in A. hyacinthinus and Ara spp. by Hofstatter (2011),
Nematodes of the genus Capillaria are among the which describes C. plagiaticia parasitizing 11 species of
main parasites of Psittaciformes birds, including macaws Psittaciformes. This parasite was considered to be specific

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Gastrointestinal parasites in wild birds from Goiania Zoo

to psittacids (Kajerová and Baruš, 2005), being reported were the main species infecting Ramphastidae, a family
from different countries and continents (Weekes, 1982; of birds that includes toucans. These authors also reported
Valdebenito et al., 2015). that capillariosis is the main parasitic disease that affects
Cubas et al. (2014) reported that Capillaria columbae these birds in captivity in Brazil and that it can be fatal
Rudolphi, 1819 and Capillaria obsignata Madsen, 1945 to toucans. However, the Capillaria species found in the

Figure 1. Helminth eggs found in the feces of captive and free-living birds at Goiania Zoo. (a) unidentified nematode in a fecal sample from
Amazona amazonica, Bar = 20μm; (b) Ascarididae family egg found in Pavo cristatus nigripennis fecal samples, Bar = 20μm; (c) Capillaria
sp. egg identified in Ara chloropterus fecal sample, Bar = 20μm; (d) Capillaria venusta eggs identified in Ramphastos tucanus fecal sample,
Bar = 20μm; (e) Capillaria spp. egg identified in Penelope jacucaca fecal sample, Bar = 20μm; Eustrongylides spp. (f) and Diphyllobothrium
spp. (g) eggs found in Ardea alba fecal sample, Bar = 20μm; Ascaridia spp. eggs found in Brotogeris chiriri (h), Bar = 20μm, Rhea americana
(i) and Dromaius novaehollandiae (j) fecal samples, Bar = 20μm; (k) Diphyllobothrium sp. egg found in Nycticorax nycticorax; Capillaria
plagiaticia egg (l) and Eimeria sp. oocyst (m) found in Anodorhynchus hyacinthinus fecal sample, Bar = 10 μm; and (n) Capillaria plagiaticia
egg found in Ara sp. fecal sample, Bar = 20μm.

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Melo, Y.J.O. et al.

white-tailed toucan (R. tucanus) specimen in this report being controlled with hygiene measures similar to those
was Capillaria venusta, the fist host record to this parasite. already mentioned for other parasites, and administration
In addition, Atkinson et al. (2008) described the presence of anticoccidial drugs (Taylor et al., 2016).
of C. venusta in toco toucan (Ramphastos toco Muller, Like this study, Fithri (2017) reported the occurrence
1776) and the green-billed toucan (Ramphastos dicolorus Diphyllobothrium spp. eggs in N. nycticorax (black-crowned
Linnaeus, 1766). night heron). The N. nycticorax and A. alba (great egret)
Two captive birds with capillariasis (A. chloropterus specimens of this report were free-living birds and the
and R. tucanus), presented clinical signs of prostration, infection may have resulted from their habit of feeding
finicky appetite, weight loss and dehydration. Snak et al. on infected fish, since the genus needs intermediate hosts
(2014) reported that parasitic diseases are more frequent that are mainly fish and have wide distribution in nature
among captive wild animals than in free-living animals, (Taylor et al., 2016).
due to predisposing factors such as stress and inadequate Atkinson et al. (2008) reported that parasites of the
sanitary management. Furthermore, these authors genus Eustrongylides widely distributed throughout
stated that restricted areas enable parasites to complete the world, including tropical regions, and the species
their cycles within the enclosure (Snak et al., 2014). Eustrongylides ignotus Jägerskiöld, 1909 have been
Captive birds with inapparent infections reinforce the identified in most reports from Central and South
need to perform periodic parasitological evaluations. America. According to Cubas et al. (2014), Ciconiiformes
According to Cubas et al. (2014), such evaluations Bonaparte, 1854 and Pelecaniformes Sharpe, 1891
should be done at 3 or 4-month intervals to ensure birds become infected with this parasite by eating fish
the early diagnosis of parasitic infections. Considering containing larvae of the parasite. Vicente et al. (1995)
the monoxenic cycle of C. plagiaticia and C. venusta, reported that E. ignotus and Eustrongylides perpapillatus
control of the dispersion of eggs in the environment is Jägerskiöld, 1909 occurred in Brazil, and the latter
necessary, and can be performed with periodic removal has already been identified in A. alba. The species E.
of the surface layers of the substrate and feces from the ignotus has also been found in A. alba by Spalding and
cages, hygiene and disinfection and measures of sanitary Forrester (1993).
vacuum (Godoy, 2007), in addition to the quarantine of Zoos located in urban centers often attract free-living
newly introduced birds (Dislich, 2007). animals such as rats, herons, vultures and pigeons.
The R. tucanus specimen had a history of recurrent This facilitates contact between free-living and captive
infections by Capillaria spp., and due to its physical animals and is a major contributing factor to the infection
limitations, the bird spent more time on the floor of of animals living in captivity (Snak et al., 2014). This
its enclosure, possibly facilitating reinfection. The floor situation may have occurred in Goiânia Zoo, given the
and walls of its enclosure were disinfected with fire in proximity of free-living animals in the proximities (or at
order to control intermediate hosts and prevent further least their excreta) and even inside the zoo enclosures in
reinfections. With regard to control and treatment search of food.
measures, Cubas et al. (2014) stated that using fire in These parasites can generate clinically worrisome
animal enclosures does not ensure the destruction of conditions, such as those observed in some of the
Capillaria eggs, and that boiling water is more effective. captive species of this report. The presence of helminth
Drug therapies are more effective when they are based on eggs in the zoo’s captive birds indicates the need for
the diagnosis of a coproparasitological analysis (Bowman, targeted treatments, efficient sanitary management to
2014; Cubas et al. 2014). According to Tully et al. (2010), control intermediate hosts, and proper disinfection of
after concluding a treatment the co-parasitological analysis the enclosures. Moreover, it should be kept in mind that
should be repeated to ascertain its efficacy. The birds contact between free-living and captive birds may play
that presented persistent infections after treatment were an important role in triggering infections among the zoo’s
treated again using different bases. Cubas et al. (2014) birds. The main route of infection of free-living birds may
describes difficulty in controlling capillariasis in toucans have been the ingestion of intermediate hosts and, so far,
due to resistance to anthelmintic drugs by Capillaria few reports are available about the clinical significance of
spp. species, also associated with the rapid intestinal parasites in these individuals.
transit of toucans causing low absorption of the drug,
increases the importance of environmental strategies of
parasitosis control. Acknowledgements
Eimeria spp. is coccidian parasites, that causes
a recurrent infection in many species of birds To Goiania Zoo for all support provided.
(Taylor et al., 2016), and has been reported parasitizing
Psittaciformes Wagler, 1830 (Farr, 1960; Todd et al., 1977;
Upton and Wright, 1994; Hofstatter and Kawazoe, References
2011). The infection involves a direct cycle, which leads ATKINSON, C.T., THOMAS, N.J. and HUNTER, D.B., 2008. Parasitic
to the occurrence of the disease with destruction of diseases of wild birds. Ames: Blackwell, 595 p. http://dx.doi.
the host’s intestinal epithelial cells (Long, 1987). Like org/10.1002/9780813804620.
most parasites mentioned in this study, the factors that BORGSTEEDE, F.H.M., 1996. The effect of parasites on wildlife.
predispose the occurrence of parasitosis are related to The Veterinary Quarterly, vol. 18, suppl. 3, pp. 138-140. http://
population density and are common in captive birds, dx.doi.org/10.1080/01652176.1996.9694717. PMid:8933697.

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Gastrointestinal parasites in wild birds from Goiania Zoo

BOWMAN, D.D., 2014. Georgis’ parasitology for veterinarians. 10th HOFSTATTER, P.G., 2011. Contribuições ao perfil parasitológico de
ed. Saint Louis: Elsevier Health Sciences, 499 p. Psittacidae e descrição de uma nova espécie de Eimeria. Campinas:
CARNEIRO, M.B., CALAIS-JÚNIOR, A. and MARTINS, I.V.F., 2011. Instituto de Biologia, Universidade Estadual de Campinas, 52
Avaliação coproparasitológica e clínica de aves silvestres e p. Dissertação de mestrado em Parasitologia.
exóticas mantidas em criatórios particulares no município de KAJEROVÁ, V. and BARUŠ, V., 2005. Psittacine birds (Aves:
Alegre-ES. Ciência Animal Brasileira, vol. 12, no. 3, pp. 525-529. Psittaciformes) as new hosts of Baruscapillaria obsignata
http://dx.doi.org/10.5216/cab.v12i3.6821. (Nematoda: Capillariidae). Acta Veterinaria Brno, vol. 74, no.
CARPENTER, J.W., 2010. Exotic animal formulary. 3rd ed. Philadelphia: 4, pp. 571-574. http://dx.doi.org/10.2754/avb200574040571.
W.B. Saunders, 423 p. KAJEROVA, V., BARUS, V. and LITERAK, I., 2004. Nematodes from
COSTA, R. A., PEREIRA, A. P. M., SILVEIRA, C. S. and ANJOS, B. L., the genus Ascaridia parasitizing psittaciform birds: a review
2018. Infecção natural por Histomonas meleagridis em pavões- and determination key. Veterinarni Medicina, vol. 49, no. 6, pp.
indianos (Pavo cristatus). Acta Scientiae Veterinariae, vol. 46, 217-223. http://dx.doi.org/10.17221/5698-VETMED.
suppl. 1, e333. https://doi.org/10.22456/1679-9216.88166. LONG, P.L., 1987. Coccidiosis in poultry. CRC Critical Review, vol
CUBAS, Z.S., SILVA, J.C.R. and CATÃO-DIAS, J.L., 2014. Tratado de . 1, pp. 25-50.
animais selvagens. 2nd ed. São Paulo: Roca. 2512 p. LUTZ, A.O., 1919. Schistosomum mansoni e a Schistosomatose segundo
CUNHA, A.L.B., 2007. Prevalência de endo e ectoparasitas em cracídeos observações, feitas no Brazil. Memorias do Instituto Oswaldo
criados em cativeiro no Parque Dois Irmãos, Recife-PE. Recife: Cruz, vol. 11, no. 1, pp. 121-155. http://dx.doi.org/10.1590/
Universidade Federal Rural de Pernambuco, 42 p. Dissertação S0074-02761919000100006.
de Mestrado em Ciência Animal.
MATTOS, M.J.T., RIBEIRO, V.S. and MARQUES, S.M.T., 2011. Parasitismo
DISLICH, M., 2007. Tinamiformes (Macuco, Inhambu, Perdiz. In: gastrintestinal e aspectos do manejo de avestruzes (Struthio
Z.S. CUBAS, J.C.R. SILVA and J.L. CATÃO-DIAS. Tratado de Animais camelus) de pequenas propriedades do Rio Grande do Sul, Brasil.
Selvagens. São Paulo: Roca, pp. 158-168. Veterinária em Foco, vol. 8, no. 2, pp. 143-151.
FARR, M.M., 1960. Eimeria dunsingi n.sp. (Protozoa: Eimeriidae) from MELO, C.M.F., OLIVEIRA, J.B., FEITOSA, T.F., VILELA, V.L.R., ATHAYDE,
the intestine of a parakeet, Melopsittacus undulates (SHAW). A.C.R., DANTAS, A.F.M., WAGNER, P.G.C. and FEBRÔNIO, A.B., 2013.
Ciudad de México: Editorial Politécnica, pp. 31-35. Libro Parasites of Psittaciformes and Accipitriformes in Paraíba state,
Homenaje als Dr. Eduardo Caballero y Caballero. northeastern Brazil. Revista Brasileira de Medicina Veterinária,
FITHRI, K., 2017. Identification of worm in black crowned night heron vol. 22, no. 2, pp. 314-317. http://dx.doi.org/10.1590/S1984-
(Nycticorax nycticorax) in Ujung Pangkah Gresik. Indonésia: 29612013000200051. PMid:23856738.
Perpustakaan Universitas Airlangga. Doctoral Thesis in PRATHIPA, G., JAYATHANGARAJ, M.G., SANKARALINGAM, G. and
Veterinary Medicine. THANGAYELU, A., 2013. Prevalence of endoparasites in captive
FREITAS, M.F.L., OLIVEIRA, J.B., CAVALCANTI, M.D.B., LEITE, A.S.L., psittacine birds belonging to pet shops and private residences in
MAGALHÃES, V.S., OLIVEIRA, R.A. and SOBRINO, A.E., 2002. Parásitos and around Chennai. International Journal of Veterinary Science,
gastrointestinales de aves silvestres em cautiverio em el estado de vol. 2, no. 2, pp. 58-60.
Pernambuco, Brasil. Parasitología Latinoamericana, vol. 57, pp. 50-54.
RAMOS, D.G.S., SILVA, A.P.J., ABREU, R.R., WESSEL, A.C.R., SILVA, N.G.,
GALLO, S.S.M., TEIXEIRA, C.S., EDERLI, N.B. and OLIVEIRA, F.C.R., 2020. OLIVEIRA, I.B., NUNES, L.F.B., FREITAS, M.R. and SATURNINO,
Gastrointestinal parasites of a population of emus (Dromaius K.C., 2018. Ocorrência e lesões causadas por ascarídeos em Pavo
novaehollandiae) in Brazil. Brazilian Journal of Biology = Revista cristatus (Phasianidae) de criatório não comercial em Jataí,
Brasileira de Biologia, vol. 80, no. 1, pp. 66-72. http://dx.doi. Goiás. Brazilian Journal of Animal and Environmental Research,
org/10.1590/1519-6984.189922. PMid:31116295. vol. 1, no. 2, pp. 268-275.
GODOY, S.N., 2007. Psitaciformes (Arara, Papagaio, Periquito). In: RITCHIE, B.W., HARRISON, G.J. and HARRISON, L.R., 1994. Parasites.
Z.S. CUBAS, J.C.R. SILVA and J.L. CATÃO-DIAS. Tratado de animais In: E.C. GREINER and B.W. RITCHIE. Avian medicine: principles and
selvagens. São Paulo: Roca. pp. 222-251. application. Flórida: Wingers Publishing; 1994. p. 1007-1009.
GONZÁLEZ-ACUÑA, D., FABRY, M., NASCIMENTO, A.A. and ROSA, F.G.D.I., 2003. Apostila de criação de avestruzes. São Paulo:
TEBALDI, J.H., 2007. Death of two slender-billed parakeet (King) Struthio Consult, 159 p.
(Enicognathus leptorhynchus) (Aves, Psittacidae) by Ascaridia
hermaphrodita (Froelich, 1789, Railliet & Henry, 1914) at the SANTOS, P.M.S., SILVA, S.G.N., FONSECA, C.F. and OLIVEIRA, J.B.,
National Zoo of Santiago, Chile. Arquivo Brasileiro de Medicina 2015. Parasitos de aves e mamíferos silvestres em cativeiro
Veterinária e Zootecnia, vol. 59, no. 2, pp. 539-540. http://dx.doi. no estado de Pernambuco. Pesquisa Veterinária Brasileira,
org/10.1590/S0102-09352007000200044. vol. 35, no. 9, pp. 788-794. http://dx.doi.org/10.1590/S0100-
736X2015000900004.
HODOVÁ, I., BARUS, V. and TUKAC, V., 2008. Note on morphology
of two nematode species Ascaridia hermaphrodita and Ascaridia SHEATHER, A.L., 1923. The detection of intestinal protozoa and
platyceri (Nematoda): scanning electron microscope study. mange parasites by a flotation technique. The Journal of
Helminthologia, vol. 45, no. 3, pp. 109-113. http://dx.doi. Comparative Pathology and Therapeutics, vol. 36, pp. 266-275.
org/10.2478/s11687-008-0021-4. http://dx.doi.org/10.1016/S0368-1742(23)80052-2.

HOFSTATTER, P.G. and GUARALDO, A.M.A., 2015. Parasitological SNAK, A., LENZI, P.F., AGOSTINI, K.M., DELGADO, L.E., MONTANUCCI,
survey on birds at some selected brazilian zoos. Revista Brasileira C.C. and ZABOTT, M.V., 2014. Análises coproparasitológicas de
de Parasitologia Veterinária, vol. 24, no. 1, pp. 87-91. http:// aves silvestres cativas. Ciência Animal Brasileira, vol. 15, no. 4,
dx.doi.org/10.1590/S1984-29612015005. PMid:25909259. pp. 502-507. http://dx.doi.org/10.1590/1089-6891v15i425797.
HOFSTATTER, P.G. and KAWAZOE, U., 2011. Two new Eimeria SPALDING, M.G. and FORRESTER, D.J., 1993. Pathogenesis of
species (Apicomplexa: Eimeriidae) from the Yellow-Crowned Eustrongylides ignotus (Nematoda: Dioctophymatoidea) in
Amazon, Amazona ochrocephala (aves: Psittacidae). The Journal Ciconiiformes. Journal of Wildlife Diseases, vol. 29, no. 2, pp.
of Parasitology, vol. 97, no. 3, pp. 503-505. http://dx.doi. 250-260. http://dx.doi.org/10.7589/0090-3558-29.2.250.
org/10.1645/GE-2681.1. PMid:21506846. PMid:8487374.

Brazilian Journal of Biology, 2022, vol. 82, e240386 7/8


Melo, Y.J.O. et al.

SPRENT, J.F., 1954. The life cycles of nematodes in the family VALDEBENITO, J.O., MORENO, L., LANDAETA-AQUEVEQUE, C.,
Ascarididae Blanchard 1896. The Journal of Parasitology, vol. KINSELLA, J.M., MIRONOV, S., CICCHINO, A., TRONCOSO,
40, no. 5, pt 1, pp. 608-617. http://dx.doi.org/10.2307/3274028. I. and GONZÁLEZ-ACUÑA, D., 2015. Gastrointestinal
PMid:13202021. and external parasites of Enicognathus ferrugineus and
TAYLOR, M.A., COOP, R.L. and WALL, R.L., 2016. Veterinary Enicognathus leptorhynchus (Aves, Psittacidae) in Chile.
parasitology. 4th ed. Hoboken: Wiley Blackwell, 1006 p. Revista Brasileira de Parasitologia Veterinária, vol. 24, no. 4,
pp. 422-431. http://dx.doi.org/10.1590/S1984-29612015074.
TITILINCU, A., MIRCEAN, V., BEJAN, A., IOVU, A., UNGUREANU, R.
and COZMA, V., 2009. Prevalence of Endoparasites in Peacocks PMid:26648008.
(Pavo cristatus). Scientica Parasitologica, vol. 1, no. 2, pp. 101-105. VICENTE, J.J., RODRIGUES, H.O., GOMES, D.C. and PINTO, R.M., 1995.
TODD, K.S., GALLINA, A.M. and SCHMIDT, J.M., 1977. Eimeria dunsingi Farr Nematóides do Brasil. Parte IV: nematoides de aves. Revista
1960: A coccidium of parakeet, Melopsittacus undulatus. Proceedings Brasileira de Zoologia, vol. 12, suppl. 1, pp. 1-273. http://dx.doi.
of the Helminthological Society of Washington, vol. 44, pp. 188-190. org/10.1590/S0101-81751995000500001.

TULLY, T.N., DORRESTEIN, G.M. and JONES, A.K., 2010. Clínica de WEEKES, P.J., 1982. Checklist of helminth parasites of birds in
aves. 2nd ed. Rio de Janeiro: Elsevier, 344 p. New Zealand. New Zealand Journal of Zoology, vol. 9, no. 4, pp.
451-460. http://dx.doi.org/10.1080/03014223.1982.10423876.
UPTON, S.J. and WRIGHT, T.F., 1994. A new species of Eimeria
(Apicomplexa) from the orange-fronted conure, Aratinga canicularis ZAJAC, A.M. and CONBOY, G.A., 2012. Veterinary clinical parasitology.
(Psittaciformes), in Costa Rica. Acta Protozoologica, vol. 33, pp. 117-119. 8th ed. Hoboken: Wiley-Blackwell, 354 p.

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