Coproparasitological research in birds housed at the Sargento Prata Zoo, Fortaleza - Ceará, Brazil

Pesquisa coproparasitológica em aves alojadas no Zoológico Sargento Prata, Fortaleza - Ceará, Brasil

Abstract

Birds kept in captivity are subject to various diseases that affect their well-being, with parasites being among the most common. The aim of this study was to report the occurrence of endoparasites in the feces of birds kept in captivity at Fortaleza Zoo, using the Willis Mollay and Hoffman techniques. Of the samples analyzed, 50.98% were positive for endoparasites, including the suborder Coccidia, the genera Capillaria spp., Strongyloides spp., Ascaridia spp., Libyostrongylus spp., cysts of a specific parasite of Ostriches, Balantidium spp., the Strongyloidea superfamily and cestodes. In conclusion, the wild birds in the zoo investigated had a diversity of endoparasites and a considerable infection rate.

Keywords:
endoparasites; birds; zoo; Coccidia; Capillaria

Resumo

As aves mantidas em cativeiro estão sujeitas a diversas enfermidades que afetam seu bem-estar, estando as parasitoses entre as mais frequentes. Este trabalho teve como objetivo relatar a ocorrência de endoparasitas em fezes de aves alojadas em cativeiro no zoológico de Fortaleza, utilizando as técnicas de Willis Mollay e de Hoffman. Das amostras analisadas, 50,98% foram positivas para endoparasitas, incluindo os da subordem Coccidia., os gêneros Capillaria spp., Strongyloides spp., Ascaridia spp., Libyostrongylus spp. (parasita específico de Avestruzes), cisto de Balantidium spp., superfamília Strongyloidea e cestódeos. Conclui-se que as aves silvestres do zoológico investigado apresentaram, além de uma diversidade de endoparasitas, uma considerável taxa de infecção.

Palavras-chave:
endoparasitas; aves; zoológico; Coccidia; Capillaria

1. Introduction

Keeping wild birds in zoos is a fundamental tool for their preservation, especially endangered species or victims of wildlife trafficking. In addition, they are important as a form of environmental education and in the development of scientific studies (Conde, 2013; Morezzi et al., 2021).

Wild and exotic animals kept in captivity are subject to various health problems that can affect their survival and reproduction. Parasitic infections represent one of the most relevant diseases in captive birds (Snak et al., 2014), due to the high environmental contamination that results from keeping animals in confinement, combined with the stress caused by captivity, which can compromise the birds' immune system, making them susceptible to various infections (Fagiolini et al., 2010; Oliveira et al., 2011; Reed et al., 2012).

Early detection and identification of parasites is essential for treatment, reducing the occurrence of clinical complications and deaths (Cringoli et al., 2010; Capasso et al., 2019; Lozano et al., 2021), as well as favoring the development and implementation of effective control measures (Brito et al., 2017). Coproparasitological diagnosis is based on the examination of fecal samples to identify eggs or other parasitic forms that are eliminated in the feces of the host bird (Snak et al., 2014).

Therefore, considering the importance of this subject, the aim of this work was to carry out an investigation into the main endoparasites found in birds kept at the Sargento Prata Zoo, located in the city of Fortaleza-Ceará, in order to discuss the main findings and the impact of parasites on the health of these animals.

2. Material and Methods

This project was authorized by IBAMA, upon request and approval of SISBIO project number: 82857-1. It was also submitted to and approved by the Ethics Committee for the Use of Animals of the State University of Ceará (CEUA-UECE) under the following protocol number: 04595739/2019. From November 2022 to May 2023, 51 samples were collected from enclosures containing wild birds at the Sargento Prata Municipal Zoo, located in the city of Fortaleza, Ceará, Brazil.

The water provided to the zoo animals was regularly tested for sanitary quality. Another practice adopted to minimize health risks was periodic antiparasitic treatment. Samples were collected from all the enclosures available at the zoo, resulting in 41 samples from enclosures with a single individual and 10 samples from collective enclosures with multiple birds, respecting veterinary guidelines on the arrangement of birds and ensuring that the zoo's dynamics were maintained. Most of the enclosures from which the droppings were collected had cement floors, which were cleaned properly and daily with soap and hypochlorite. In the enclosures with a sand substrate, this was changed regularly and previously treated with lime. In both cases, fire brooms were used for disinfection when necessary. The droppings were collected from the ground in the morning to ensure that fresh samples were obtained. Those without apparent dirt and from the highest part of the pile were selected to minimize environmental contamination. The samples were collected using glass rods, stored in sanitized plastic containers and sent to the Laboratory of Ornithological Studies (LABEO) and the Laboratory of Veterinary Clinical Pathology - Parasitology Sector, located at the State University of Ceará (UECE). Table 1 shows the orders and number of specimens (N) used in this study.

Table 1
Relative and absolute frequency of parasites found in birds at the Sargento Prata Zoo, Fortaleza-Ceará, Brazil.

Filo	Order	Parasite	Absolute/Relative Frequency
Apicomplexa	Eucoccidiorida	Coccidia	10/51 (19.60%)
Ciliophora	Vestibuliferida	Ballantidium spp.	1/51 (1.96%)
Nematoda	Trichocephalida	Capillaria spp.	8/51 (15.68%)
	Rhabditida	Strongyloides spp.	7/51 (13.72%)
	Ascaridida	Ascaridia spp.	2/51 (3.92%)
	Strongylida	Libyostrongylus spp.	1/51 (1.96%)
		Strongyloidea	1/51 (1.96%)
Platyhelminthes	Cyclophyllidea	Cestodo	2/51 (3.92%)
Total positive samples			26/51 (50.98%)*

• ^*
  Represents the total number of samples containing one or more parasites. Note: Mixed infections were observed in 12 samples (23.52%), where more than one parasite was detected per sample.

Two techniques were used to process the samples: the Willis Mollay method, which consists of floating light eggs in a saturated sugar solution, which allows the visualization of nematode eggs and larvae and protozoan oocysts, and the Hoffman method, based on the spontaneous sedimentation, by the action of gravity, of parasite eggs, cysts, oocysts and larvae in distilled water. In both techniques, the slides were read in duplicate under 10X and 40X objectives (Willis, 1921; Hoffman, 1987). Descriptive statistical analysis was used to find absolute and relative frequencies.

3. Results

The material collected for parasitological investigation came from birds that did not show any apparent clinical signs of illness, with the exception of an emu (Rhea Americana) which had blood in its feces and a cactus parakeet (Eupsittula cactorum) with a chronic neurological condition. Out of a total of 51 feces investigated, 26 (50.98%) were positive for endoparasites (Figure 1). The most prevalent parasite was Coccidia (19.60%) followed by Capillaria sp. (15.68%) and Strongyloides sp. (15.68%). Mixed infections, i.e. cases in which two or more types of parasites occurred, were observed in 12 samples (23.52%) (Table 1).

Figure 1
Helminth eggs found in the feces of birds from the Sargento Prata Zoo, Fortaleza – Ceará. (a) Coccidian egg (Apicomplexa, Eucoccidiorida) identified in the feces of Patagioenas picazuro; (b) Balantidium sp. cyst (Ciliophora, Vestibuliferida) identified in the feces of Rhea americana; (c) Capillaria sp. egg (Nematoda, Trichocephalida) identified in the feces of Amazona aestiva; (d) Strongyloides sp. egg (Nematoda, Rhabditida) identified in the feces of Spatula querquedula; (e) Ascaridia sp. egg (Nematoda, Ascaridida) identified in the feces of Sarcoramphus papa; (f) Libyostrongylus sp. egg (Nematoda, Strongylida) identified in the feces of Struthio camelus; (g) Strongyloidea egg (Nematoda, Strongylida) identified in the feces of Ara ararauna; (h) Cestode egg (Platyhelminthes, Cyclophyllidea) identified in the feces of Eupsittula cactorum.

Parasite eggs from the Coccidia subclass were found in birds from seven of the orders analyzed (Rheiformes, Psittaciformes, Strigiformes, Falconiformes, Cathartiformes, Columbiformes and Galliformes). Among the species of the orders Galliformes (Crax fasciolata) and Falconiformes (Falco femoralis and Caracara plancus), Coccidia was the only parasite detected. Eggs of the genus Strongyloides sp. were identified in five orders: Psittaciformes, Strigiformes, Piciformes, Anseriformes and Columbiformes. Parasites from the Cestoda class were found on two occasions: one in a sample of a bird from the Strigiformes order (Megascops choliba) and another from the Psittaciformes order (Eupsitulla cactorum). The same occurred with Ascaris sp. eggs, recorded in one sample of a bird from the order Anseriformes (Spatula querquedula) and another from the order Cathartiformes (Sarcoramphus pa pa). Forms of the genus Libyostrongylus sp. and Balantidium sp., as well as the superfamily Strongyloidea sp., were detected only once in samples from birds of the orders Struthioniformes (Struthio camelus), Rheiformes (Rhea americana) and Psittaciformes (Ara ararauna), respectively. Eggs of the genus Capillaria sp. were also identified in a single order (Psittaciformes), but in three different samples, involving at least three different species (Eupsittula cactorum, Amazona aestiva, Ara chloropterus and Aratinga jandaya + Psittacara leucophtalmus) (Table 2).

Table 2
Bird species used, distribution of individuals by enclosure, number of samples collected, absolute frequency of positive samples, and endoparasites identified in feces at Sargento Prata Zoo, Fortaleza, Ceará, Brazil (november 2022 to may 2023).

Order	Species of birds		Number of birds	Number of Birds in Individual Environments	Collective Environments (Total Birds Distributed in Enclosures)	Number of samples collected	Number of Positive Samples	Identification of eggs/oocyst
Rheiformes		Rhea americana †	1	1	-	1	1	Coccidia (1), Balantidium sp.(1)
Struthioniformes		Struthio camelus	1	1	-	1	1	Libyostrongylus spp.(1)
Psittaciformes		Ara ararauna	5	5	-	5	1	Strongyloidea (1), Coccidia (1)
		Eupsittula cactorum ‡	11	2	2 (9)	4	3	Capillaria spp. (2), Cestodo (1)
		Amazona aestiva	10	10	-	10	4	Capillaria (4), Strongyloides spp. (1)
		Ara chloropterus	2	2	-	2	1	Capillaria spp.(1)
		Amazona farinosa	2	2	-	2	1	Strongyloides spp.(1)
		Guaruba guarouba	1	1	-	1	-	-
		Ara macao + Ara ararauna *	4*	-	1 (4)*	1*	1*	Coccidia (1)
		Ara ararauna + Ara chloropterus*	2*	-	1 (2)*	1*	1*	Coccidia (1)
		Aratinga jandaya + Psittacara leucophtalmus*	2*	-	1 (2)*	1*	1*	Capillaria spp.(1)
		Diopsittaca nobilis + Primolius maracana*	5*	-	1 (5)*	1*	-	-
Strigiformes		Megascops choliba	2	2	-	2	-	-
		Glaucidium brasilianum	2	2	-	2	2	Strongyloides spp.(1), Cestodo (1)
		Athene cunicularia	1	1	-	1	-	-
		Pulsatrix perspicillata	1	1	-	1	-	-
		Tyto furcata	1	1	-	1	1	Coccidia (1)
Piciformes		Ramphastos toco	7	1	1 (6)	2	-	-
		Ramphastos vitellinus	2	2	-	2	1	Strongyloides spp.(1)
Falconiformes		Falco femoralis	1	1	-	1	1	Coccidia (1)
		Caracara plancus	2	2	-	2	1	Coccidia (1)
Accipitriformes		Heterospizias meridionalis	1	1	-	1	-	-
		Rupornis magnirostris	1	1	-	1	-	-
Anseriformes		Dendrocygna viduata	4	-	1 (4)	1	-	-
		Spatula querquedula	2	-	1 (2)	2	2	Strongyloides spp.(2), Ascaridia spp.(1)
Cathartiformes		Sarcoramphus papa	1	1	-	1	1	Ascaridia spp.(1),Coccidia (1)
Columbiformes		Patagioenas picazuro	-	-	1	1	1	Strongyloides spp.(1), Coccidia (1)
Galliformes		Crax fasciolata	1	1	-	1	1	Coccidia (1)
Total		-	74	41	10	51	26/51	-

• ^*
  Birds of different species in collective enclosures;
• ^†
  Bird with blood in feces;
• ^‡
  Bird with chronic neurological condition.

4. Discussion

Among the parasites identified in this study, the genus Capillaria spp. was one of the most commonly found, with all the positive birds belonging to the psittaciformes order. The species belonging to this genus are among the main endoparasites found in psittaciform birds (Cubas et al., 2014). Hofstatter and Guaraldo (2015) reported that nematodes of the genus Capillaria spp. is the most relevant parasites in psittaciformes bred in captivity, more specifically, in parrots. In their study, carried out in zoos in the states of São Paulo and Paraná, the genus Capillaria spp. was present in all the zoos collected, mainly in fecal samples of psittaciformes. In Valle Del Cauca, Colombia, Burbano et al. (2003) reported the prevalence of Capillaria spp. in birds belonging to the Psittacidae family resident at the Cali Zoological Foundation, the eggs of this parasite were present in 58.0% of the samples analyzed, especially in birds of the Ara and Amazona genera, in agreement with the present study.

The rate of occurrence of nematodes of the genus Capillaria spp. observed may be related to the adoption of insufficient hygiene measures (Godoy, 2007), since these parasites have eggs that are very resistant to both physical and chemical agents, which makes it difficult to effectively disinfect enclosures, allowing re-infection. In addition, factors such as high population density, stress and adaptation to new environments or prolonged periods of confinement are aggravating factors for the emergence of these infections, and birds kept in zoos are often subjected to these conditions (Papini et al., 2012).

Although parasites of the genus Ascaridia spp. have been reported in psittacines kept in zoos (Hofstatter and Guaraldo, 2015; Neiva and Martins, 2021; Melo et al., 2021), we did not observe any cases in birds belonging to this order. Cases involving this endoparasite were observed in two individuals, one from the order Anseriformes and the other from the order Cathartiformes. It is a parasite that can easily contaminate birds and wild mammals, as well as being highly resistant to the environment, and can remain viable in the environment for months (Santos et al., 2015; Brito et al., 2021). The main clinical signs of ascariasis are weight loss, anorexia, malabsorption of nutrients, diarrhea and in cases of high parasite load, intestinal obstruction and intussusception can occur (Cubas and Godoy, 2004; Melo et al., 2013).

In the present study, ten samples (19.60%) tested positive for protozoa of the suborder Coccidia. In captive birds, these coccidia lead to persistent disease and are among the most commonly isolated endoparasites in domestic and wild birds (Marietto et al., 2009). In the study by Santos et al. (2022), a high presence of oocysts was also observed (86.1%), and infection by coccidia was probably attributed to contact with paratenic hosts or contaminated fomites carried by keepers, on shoes, on objects used in cleaning and handling. In addition, they are parasites that survive for long periods in the environment, remaining in cages or enclosures and, consequently, leading to the contamination of other birds. In addition to sanitary control, it is necessary to administer coccidiostatic drugs to prevent parasitosis (Dingle and Shanawany, 1999).

Another relevant finding in this research was related to one individual of the Ema species (Rhea americana) with blood-stained feces, who tested positive for the protozoan of the genus Balantidium spp. which is considered a zoonotic parasite with uncertain pathogenicity in birds (Marietto et al., 2009). Similar to what was found in this study, Martínez-Díaz et al. (2013) reported the presence of Balantidium spp. cysts in 16.3% of the samples in their study of Emus from different locations in Argentina. Infection with this protozoan can lead to weight loss, anorexia and diarrhea in ratite birds (Taylor et al., 2016). With regard to human infections, the pathogen is acquired by ingesting water and food contaminated by feces from infected animals or humans (CDC, 2020), the parasite inhabits the host's intestinal tract and can be pathogenic or not, causing intestinal disorders that can be fatal (Ponce-Gordo and García-Rodríguez, 2021). This highlights the importance of monitoring captive birds to control and prevent zoonotic risks, protecting human and animal health. Snak et al. (2014) in their study of birds kept in captivity obtained a prevalence of 59.84% of Strongyloides spp. and 26.77% of the Strongyloidea superfamily. In the present study, the prevalence of Strongyloides spp. eggs was 15.68% in relation to the positive samples and eggs from the Strongyloidea superfamily were detected in only one bird, the Blue-and-yellow Macaw (Ara ararauna). These helminths have serious consequences, especially in young birds. In infections caused by Strongyloides spp. the most common clinical signs in high infestations are weakness, emaciation and bloody, viscous diarrhea, and adult worms in the cecum can cause inflammation with edema and erosion of the epithelium (Taylor et al., 2016).

One specimen of the common ostrich species (Struthio camelus) asymptomatic, tested positive for the nematode of the genus Libyostrongylus spp. One research realized on Colombia identified Libyostrongylus spp. in adult ostriches without symptons of parasitc diseases, suggesting that these parasites may exist in birds in a subclinical state (Paz Campuzano et al., 2019). It's a kind of parasite a specific and most relevant parasite of ostriches, due to its high pathogenicity, which leads to anemia, weight loss, anorexia, proventriculitis and high mortality in young individuals. In a study carried out in the state of Rio Grande do Sul in five commercial farms, L. douglassii and L. dentatus were identified in 82.35% and 79.41% of the ostriches, respectively, and were found simultaneously in all but one of the samples (Pesenti et al., 2015). The eggs and first-stage larvae of this helminth are highly resistant to desiccation and can survive up to 30 months in the environment in hot climates, making it essential to adopt control measures and disinfect the environment (Taylor et al., 2016).

The detection rate of cestodes in the birds analyzed was one of the lowest, similar to that observed in some previous studies carried out in Brazil. In a parasitological survey conducted in zoos in the states of São Paulo and Paraná, Brazil, various groups of birds were examined, with a predominance of Psittacidae, and no cestodes were detected in the fecal samples analyzed (Hofstatter and Guaraldo, 2015). In a study of Psittaciformes and Accipitriformes submitted for necropsy at a Rehabilitation Center in the state of Paraíba, Brazil, only 2.4% (1/41) of the birds examined were positive for cestodes (Melo et al., 2013). Similarly, Ilić et al. (2018) did not detect this parasite in birds kept in a zoo in Serbia, suggesting that birds raised in captivity are less likely to be infected with cestodes when kept in controlled conditions, where the consumption of intermediate hosts is minimized. However, it is possible to find cases in the literature involving higher percentages of cestode detection. Tomás et al. (2017) found that 13.6% of the samples investigated from wild birds in a rehabilitation center in Portugal were positive for this parasite.

Although the total endoparasite infection rate was 50.8%, other studies involving wild birds have reported even higher frequencies. In a study carried out by Marietto et al. (2009), analyzing fecal samples from, free-living wild birds and captive wild birds, wild birds kept in captivity showed a higher rate of parasitism, with 87.8% of positive samples. Santos et al. (2015) detected a 70.3% positivity rate in fecal samples from wild birds sent to a rehabilitation center in Pernambuco, Brazil. In both studies, the presence of parasites was associated with poor sanitary conditions.

In a study carried out by Papini et al. (2012) with wild birds kept in a zoo in Italy, a slightly lower infection rate was detected than that observed in our study (42.2%). Most of the infected birds also showed no clinical signs, probably due to the low parasite load. The authors point out that the presence of parasites is common in birds kept in zoos, which is why they emphasize the importance of continuous monitoring, accurate diagnosis and treatment of infections, especially in those that manifest symptoms. However, even in cases where there are no clinical manifestations, these infections should be considered relevant, since many of the parasites identified in our research are considered opportunistic (Santos et al., 2015).

The conditions promoted by captivity, such as inadequate hygiene, high population density and stress, are important factors in triggering parasitosis, even a parasite with low pathogenicity can cause serious clinical manifestations when associated with conditions such as immune suppression, stress or other diseases (Santos et al., 2015; Brito et al., 2021). Despite adequate sanitary care, such as water quality analysis and periodic cleaning of the enclosures at Fortaleza Zoo, and the fact that the birds are not subjected to stressful conditions, the infection rate detected can be explained by factors commonly associated with this problem in other captive facilities. These factors include transmission by soil, food and water contaminated with parasite eggs, or even by free-living birds accessing the enclosures (Papini et al., 2012; Carrera-Játiva et al., 2020).

5. Conclusion

This study reveals a considerable rate of endoparasites detected in wild birds kept in captivity in a zoo located in Fortaleza, Ceará, Brazil. A diversity of endoparasites was also observed, with coccids, Capillaria sp. and Strongyloides sp. being the most prevalent. In general, the parasitized birds had no clinical manifestations. However, parasite control is of the utmost importance, through regular deworming of the birds, proper enclosure hygiene, maintaining population density and diagnosis for appropriate therapeutic treatment, in order to avoid transmission to susceptible animals, high parasitical loads and the consequential development of serious illnesses.

Acknowledgements

We would like to thank the National Council for Scientific and Technological Development (CNPq) for promoting this study. Furthermore, we would also like to thank the Laboratory of Ornithological Studies (LABEO) and the Laboratory of Veterinary Clinical Pathology (LPCV) for providing the space to carry out the research and, finally, the team at the Sargento Prata Zoo, in the city of Fortaleza.

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Publication Dates

• Publication in this collection
  21 Oct 2024
• Date of issue
  2024

History

• Received
  30 Apr 2024
• Accepted
  02 Sept 2024